11
Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden N Danchenko 1* , JA Satia 2 and MS Anthony 3 1 6 Canal Park, Suite 708, Cambridge, Massachusetts, USA; 2 Departments of Epidemiology and Nutrition, University of North Carolina at Chapel Hill, USA; and 3 Amgen, Inc., Thousand Oaks, California, USA Systemic lupus erythematosus (SLE) is a disease of multifactorial etiology. Quantifying the burden of SLE across different countries can clarify the role of genetic, environmental and other causative factors in the natural history of the disease, and to understand its clinical and societal consequences. The aim of this study is to summarize data on SLE incidence and prevalence in the USA, Europe, Asia, and Australia. An extensive review of electronic resources (PubMed and MedLine) and medical journals was conducted to identify published studies on SLE incidence and prevalence over the period of 1950–early 2006. Researchers in the countries of interest provided additional information on the epidemiology of SLE. The incidence and prevalence of SLE varies considerably across the countries. The burden of the disease is considerably elevated among non-white racial groups. There is a trend towards higher incidence and prevalence of SLE in Europe and Australia compared to the USA. In Europe, the highest prevalence was reported in Sweden, Iceland and Spain. There are marked disparities in SLE rates worldwide. This variability may reflect true differences across populations, or result from methodological differences of studies. The true geographic, racial, and temporal differences in SLE incidence and prevalence may yield important clues to the etiology of disease. Lupus (2006) 15, 308–318. Key words: epidemiology; incidence; lupus; prevalence Lupus (2006) 15, 308–318 www.lupus-journal.com © 2006 Edward Arnold (Publishers) Ltd 10.1191/0961203306lu2305xx LUPUS AROUND THE WORLD Introduction Systemic lupus erythematosus (SLE) is a multisystem autoimmune disorder with variable manifestations, with etiology that has not yet been fully described but believed to be multifactorial. Epidemiological studies on SLE show marked gender, age, racial, temporal and regional variations, indicating hormonal, genetic and environmental disease triggers. There are striking gender disparities in SLE burden, with higher disease prevalence in women compared to men. Based on clinical experiences alone, it was esta- blished that the disease generally affected females in 80–90% of the cases. 1 In a more recent review, the female-to-male ratio in the childbearing years was reported to be about 12 : 1. 2 These observations suggest that hormonal factors play important role in SLE pathogenesis. Age distribution of SLE cases is usually broad, ranging from children as young as two years old to adults 80 years of age and older. However, in females, incidence of the disease is usually highest at 15–44 years of age, while its prevalence maximal at 45–64 years. 1 Females’ highest risk for SLE during childbear- ing age also suggests a key role of hormones in SLE etiology. Studies of racial tendencies showed that SLE more frequently affected non-Caucasian individuals. For instance, in the USA, SLE is more frequent in African- Americans, Hispanics and Asians than in Caucasians. SLE occurrence is three to four times higher among African-American women compared to Caucasian women. 2 This suggests an importance of genetic pre- disposition to SLE, although differences in exposure to environmental factors may also explain excess morbi- dity from SLE in non-Caucasians. 3 Temporal increase in SLE burden has been reported by a number of researchers. For instance, only for a period from 1955 to 1974, the incidence of SLE in the USA increased from 1.0 to 7.6. 4,5 Temporal increase in SLE burden may be associated with changes in environmental factors, although increased recognition of the disease and improved diagnostic methods may cause artifactual changes in SLE frequency. * Correspondence: Natalya Danchenko, 6 Canal Park, Suite 708, Cambridge, Massachusetts, 02141, USA. E-mail: [email protected] Received 26 July 2005; accepted 16 February 2006

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Page 1: SLE Epidemiology Danchenko 2006(1)

Epidemiology of systemic lupus erythematosusa comparison of worldwide disease burden

N Danchenko1 JA Satia2 and MS Anthony3

16 Canal Park Suite 708 Cambridge Massachusetts USA 2Departments of Epidemiology and NutritionUniversity of North Carolina at Chapel Hill USA and 3Amgen Inc Thousand Oaks California USA

Systemic lupus erythematosus (SLE) is a disease of multifactorial etiology Quantifying the burdenof SLE across different countries can clarify the role of genetic environmental and other causativefactors in the natural history of the disease and to understand its clinical and societal consequencesThe aim of this study is to summarize data on SLE incidence and prevalence in the USA EuropeAsia and Australia An extensive review of electronic resources (PubMed and MedLine) and medicaljournals was conducted to identify published studies on SLE incidence and prevalence over the periodof 1950ndashearly 2006 Researchers in the countries of interest provided additional information on theepidemiology of SLE The incidence and prevalence of SLE varies considerably across the countriesThe burden of the disease is considerably elevated among non-white racial groups There is a trendtowards higher incidence and prevalence of SLE in Europe and Australia compared to the USAIn Europe the highest prevalence was reported in Sweden Iceland and Spain There are markeddisparities in SLE rates worldwide This variability may reflect true differences acrosspopulations or result from methodological differences of studies The true geographic racial andtemporal differences in SLE incidence and prevalence may yield important clues to the etiology ofdisease Lupus (2006) 15 308ndash318

Key words epidemiology incidence lupus prevalence

Lupus (2006) 15 308ndash318wwwlupus-journalcom

copy 2006 Edward Arnold (Publishers) Ltd 1011910961203306lu2305xx

LUPUS AROUND THE WORLD

Introduction

Systemic lupus erythematosus (SLE) is a multisystemautoimmune disorder with variable manifestationswith etiology that has not yet been fully described butbelieved to be multifactorial Epidemiological studieson SLE show marked gender age racial temporal andregional variations indicating hormonal genetic andenvironmental disease triggers

There are striking gender disparities in SLE burdenwith higher disease prevalence in women compared tomen Based on clinical experiences alone it was esta-blished that the disease generally affected females in80ndash90 of the cases1 In a more recent review thefemale-to-male ratio in the childbearing years wasreported to be about 12 12 These observations suggestthat hormonal factors play important role in SLEpathogenesis

Age distribution of SLE cases is usually broadranging from children as young as two years old to

adults 80 years of age and older However in femalesincidence of the disease is usually highest at 15ndash44years of age while its prevalence maximal at 45ndash64years1 Femalesrsquo highest risk for SLE during childbear-ing age also suggests a key role of hormones in SLEetiology

Studies of racial tendencies showed that SLE morefrequently affected non-Caucasian individuals Forinstance in the USA SLE is more frequent in African-Americans Hispanics and Asians than in CaucasiansSLE occurrence is three to four times higher amongAfrican-American women compared to Caucasianwomen2 This suggests an importance of genetic pre-disposition to SLE although differences in exposure toenvironmental factors may also explain excess morbi-dity from SLE in non-Caucasians3

Temporal increase in SLE burden has been reportedby a number of researchers For instance only for aperiod from 1955 to 1974 the incidence of SLE in theUSA increased from 10 to 7645 Temporal increasein SLE burden may be associated with changes inenvironmental factors although increased recognitionof the disease and improved diagnostic methods maycause artifactual changes in SLE frequency

Correspondence Natalya Danchenko 6 Canal Park Suite 708 CambridgeMassachusetts 02141 USA E-mail Natalya_danchenkoyahoocomReceived 26 July 2005 accepted 16 February 2006

Regional variations and in particular differences inSLE incidence and prevalence in similar racial groupsliving in different parts of the world could further shedthe light on role of genetic environmental and othercausative factors in etiology and natural history of thedisease However the differences in SLE burdenacross the countries and continents are not fullydescribed Although some published studies includedfindings on various countries the available data con-cerning the incidence and prevalence of SLE are limi-ted and conflicting partially due to differences in studymethodology In addition the full worldwide review ofthe available data has not been performed The presentstudy was undertaken to summarize the available dataon SLE incidence and prevalence in the USA Canadaseveral European countries (UK France GermanyItaly Spain Sweden and Iceland) Australia Japanand Martinique to give an estimation of diseaseburden in these countries

Methods

To identify relevant studies the computerized biblio-graphic database of the National Library of Medicine(Medline 1966 to January 2006) was searched usingOvid and PubMed The references from all retrievedarticles and selected review papers and books werealso reviewed to ensure that all potentially eligible arti-cles were identified for evaluation From the articlesidentified we selected all those that reported data onincidence andor prevalence of systemic lupus in thecountries of interest with or without stratification byrace and gender

From each article we abstracted information onauthor(s) journal year of publication countrygeo-graphical area studied case source(s) (eg hospitalrecords physians interviews or population surveys)timeframe over which incidence andor prevalence ofSLE were assessed actual number of cases identifiedand incidence andor prevalence estimates reported Itwas also recorded whether capturendashrecapture tech-nique was used for more accurate estimation of inci-dence and prevalence by formally calculatingascertainment-corrected rates6

We reported incidence as a number of new cases per100 000 of the population per year and prevalence as across-sectional estimate of the number of cases per100 000 of the population per year as per figures pre-sented in the Results We summarized incidence andorprevalence by race andor gender whenever the datawere available If only gender-specific estimates wereprovided the overall number was calculated as anaverage between male and female estimates adjustingfor a male to female ratio in a population of interest

assessed from country-specific census data We alsorecorded whether the estimates were adjusted by age

SLE researchers in the countries of interest wereasked to provide any additional available reports onepidemiology of SLE or to confirm unavailability ofsuch information

Results were arrayed by outcome (incidence andprevalence) countries of interest and date of publica-tion The results across studies for a same outcomecountry and racial group were pooled to report amedian estimate and a range (presented in the figures)No statistical testing of differences in SLE burdenacross the countries has been performed

We identified approximately 60 studies that men-tioned incidence andor prevalence of systemic lupuserythematosus in the countries of interest The presentreview is focused on 32 studies reported quantitativeassessment of SLE burden in adults aged 16 years orolder other reports were excluded either due to focuson children aged 16 years or due to lack of cleardefinition of the target population or methods used forcase identification Of the 32 selected studies eightreported the information on the USA one on Canada16 on Europe three on Australia three on Japan andone on Martinique

Results

SLE incidence

USA and Canada The data for the USA and Canada aresummarized in Table 1 Siegel et al147 conductedstudies in New York and Alabama states Over theperiod of 1956ndash1965 in New York overall age-adjusted incidence for both genders was reported to be14 among whites 46 among black and 23 amongPuerto Rican The incidence in Jefferson County ALwas at least twice as low as those reported in NewYork NY 08 in whites and 17 in black4 Michetet al8 found an overall age-adjusted incidence of 18for all races combined in the Rochester area MN norace-specific estimates were reported in this study Asurvey conducted by Hochberg et al9 in BaltimoreMD showed the age-adjusted incidence of 22 and 72in whites and black respectively McCarty et al10

assessed SLE incidence in the Allegheny CountyPennsylvania6 using capture-recapture technique andreported the crude incidence of 20 in whites and 53 inblack The most recent study of Naleway et al11

showed the age-adjusted incidence of 51 for all racescombined in rural Wisconsin areaThe data on incidence of SLE in adult population ofCanada are scarce In a population-based study ofPeschken et al12 crude annual incidence rates ranged

Epidemiology of SLEN Danchenko et al

309

Lupus

Epidemiology of SLEN Danchenko et al

310

Lupus

Tabl

e 1

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

the

USA

and

Can

ada

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Sieg

el e

tal

(19

62)

USA

W

hite

1951

ndash195

942

I1

20

140

7aN

DN

DN

DY

esN

oN

ew Y

ork

NY

Bla

ck13

I3

90

82

4aN

DN

DN

DSi

egel

et

al(

1973

)U

SA

Whi

te19

56ndash1

965

552

50

31

4a16

82

99

9aY

esN

oN

ew Y

ork

NY

Bla

ck16

79

11

46a

558

33

296

a

Puer

to R

ican

254

10

32

3a33

62

318

0a

Sieg

el e

tal

(19

70)

USA

Jef

fers

on

Whi

te19

56ndash1

965

181

10

40

8a7

71

84

8aY

esN

oC

ount

yA

LB

lack

193

00

31

7a18

50

93a

Mic

het e

tal

(19

85)

USA

A

ll ra

ces

1950

ndash197

925

I2

50

91

853

819

040

0Y

esN

oR

oche

ster

MN

Hoc

hber

g et

al(

1985

)U

SA

Whi

te19

70ndash1

977

79I

39

04

22a

ND

ND

ND

Yes

No

Bal

timor

eM

DB

lack

223I

114

25

72a

McC

arty

et

al(

1995

)U

SA

Whi

te19

85ndash1

990

141I

35

04

20

ND

ND

ND

Noc

Yes

Pitts

burg

hPA

Bla

ck48

I9

20

75

3W

ard

etal

(20

04)

USA

A

ll ra

ces

1988

ndash199

440

ND

ND

ND

100

03

453

6N

oN

oN

atio

nwid

eN

alew

ay e

tal

(20

05)

USA

rur

al

All

race

s19

91ndash2

001

117

82

19

51

131

524

878

5Y

esN

oW

isco

nsin

are

aPe

schk

en e

tal

(20

00)

Can

ada

Nor

th A

mer

ican

19

80ndash1

996

49N

DN

D2

0ndash7

4bN

DN

D42

3Y

esN

oPr

ovin

ce o

f In

dian

s W

hite

208

ND

ND

09ndash

23b

ND

ND

206

Man

itoba

Pre

vale

nt c

ases

if n

ot o

ther

wis

e in

dica

ted

ldquoIrdquo

supe

rscr

ipt

inci

dent

est

imat

ea C

alcu

late

d as

an

aver

age

betw

een

mal

e an

d fe

mal

e es

timat

esa

djus

ting

for

a m

ale

to f

emal

e ra

tio in

ove

rall

popu

latio

nb R

epor

ted

estim

ates

are

not

age

-adj

uste

dc O

nly

crud

e ov

eral

l est

imat

es r

epor

ted

(alth

ough

age

-spe

cific

rat

es w

ere

also

est

imat

ed)

Cou

ntry

ge

ogra

phic

al

area

Num

ber

of

pati

ents

A

gead

just

men

t

Cap

ture

ndashre

capt

ure

tech

niqu

e

20ndash74 for North American Indians and 09ndash23 forthe remaining population between 1980 and 1996(Table 1)

European countries The incidence of SLE in FranceIceland Spain Sweden and the UK are summarized inTable 2

In France in 1982 Amor et al13 conducted anationwide survey among rheumatologists belongingto the French Rheumatology Society and reported theoverall crude incidence of 10 per 1 000 000 Based onthe recent National Public Insurance survey Pietteet al reported the overall nationwide incidence of5014

In Iceland a nationwide retrospective study byGudmundsson et al15 found that the overall age-adjusted incidence was 33

In Spain Lopez et al16 conducted a hospital-basedstudy in the Caucasian population of from the North ofthe country and reported the overall crude incidenceof 22

In Sweden Nived et al17 conducted a hospital-based study in Southern part of the country during1981 and 1982 and reported the overall incidence of48 Jonsson et al18 conducted a study within the samegeographical area during 1981ndash1986 and foundthe overall incidence of 40 Stahl-Hallengren et al19

studied incidence of SLE in the same region during1987ndash1991 and reported overall age-adjusted inci-dence of 48 and 45 in 1986 and 1991 respectively

In the UK a hospital- and clinic-based study ofHopkinson et al20 showed that the overall age-adjusted incidence in Nottingham was 40 Using pop-ulation estimates from 1991 National Census theylater reported race-specific incidence rates of 319 inAfro-Caribbean 41 in Asian and 34 in Caucasian21

Johnson et al22 conducted a study in BirminghamUK and reported the age-adjusted incidence of 119 inAfro-Caribbean 152 in Asian and 25 in CaucasianThe most recent nationwide study of Nightingaleet al23 based on the population of the General PracticeResearch Database (GPRD) showed the overall crudeincidence of 30

Other countries The summary of incidence data insome selected countries is given in Table 2

In Australia a hospital-based study of Australianaborigines24 showed the overall crude incidence of110 In Japan Iseki et al25 conducted a hospital- andclinic-based study on the population of Okinawa andreported that over the period from 1972 to 1991 theoverall crude incidence increased from 09 to 29Deligny et al26 conducted an extensive population-based study in Martinique and reported the overallincidence of 47

SLE incidence in the countries of interest is summa-rized in Figure 1 The figure reflects remarkably higherSLE incidence among non-whites compared to whitesThe lowest overall incidence estimates were reportedin Iceland and Japan and highest in the USA andFrance

SLE prevalence

USA and Canada The prevalence data for the USAare summarized in Table 1 In New York NY Siegelet al147 reported the age-adjusted prevalence of 99 inwhites 296 in black and 180 in Puerto Rican1 InJefferson County Alabama they found the prevalenceat least two-fold lower that in the New York area of 48in whites and 93 in black4 Michet et al8 reported theoverall age-adjusted prevalence of 400 in theRochester area MN In the nationwide study of Wardet al27 the overall crude prevalence was 536Naleway et al11 recently found that over 1991ndash2001the overall age-adjusted prevalence in rural Wisconsinarea was 785

In Canada Peschken et al12 showed a two-foldhigher prevalence of SLE in North American Indians(423) compared to non-Indians (206)

European countries The prevalence of SLE in FinlandFrance Germany Iceland Italy Northern IrelandSpain Sweden and the UK are summarized in Table 2

In Finland Helve et al28 conducted a nationwidestudy based on hospital discharge records and cause ofdeath statistics of 1976ndash1978 and reported the overallcrude prevalence of 280 In France Piette et al14

reported the nationwide overall prevalence of 400based on the National Public Insurance survey InGermany Zink et al29 described the case mix of theGerman rheumatologic database in 1998 They found1211 prevalent cases of SLE but have not reported theformal prevalence estimate In Iceland a nationwideretrospective study by Gudmundsson et al15 showedthe overall age-adjusted prevalence of 359 In ItalyBenucci et al30 recently studied prevalence of SLE inthe population of Scandicci-Le Signe area of Florenceusing the Lupus Screening Questionnaire (LQS) Theyreported the overall crude prevalence of 710 InNorthern Ireland6 Gourley et al31 found that the over-all crude prevalence of SLE was 254 In Spain theEPISER nationwide survey32 conducted by rheumato-logists on randomly selected residents showed the over-all prevalence of SLE of 910 In the hospital-basedstudy of Lopez et al16 conducted in the Caucasianpopulation of from the north of the country the overallcrude prevalence was 341 In Sweden in the hospital-based study of Nived et al the overall prevalence inthe Southern region of the country was found to

Epidemiology of SLEN Danchenko et al

311

Lupus

Epidemiology of SLEN Danchenko et al

312

Lupus

Tabl

e 2

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

oth

er c

ount

ries

Inci

denc

eP

reva

lenc

e

Aut

hor

Peri

od

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Hel

ve e

tal

(19

85)

Finl

and

All

race

sH

ospi

tal

1976

ndash197

814

27N

DN

DN

DN

DN

D28

0N

oN

ore

cord

s an

d ca

use

of d

eath

re

gist

ers

Am

or e

tal

(19

83)

Fran

ceA

ll ra

ces

Phys

icia

ns

1982

64N

DN

D1

per

ND

ND

ND

No

No

surv

ey1

000

000

Piet

te e

tal

(20

04)

Fran

ceA

ll ra

ces

Nat

iona

l 20

04N

SN

DN

D5

0N

DN

D40

0N

SN

opu

blic

in

sura

nce

surv

eyZ

ink

(200

1)G

erm

any

All

race

sC

linic

al

1993

ndash199

812

11N

DN

DN

DN

DN

D12

11

NS

No

hosp

ital

case

sre

cord

sG

udm

unds

son

Icel

and

All

race

sC

linic

al

1975

ndash198

476

58

08

33

620

72

359

Yes

No

etal

(19

90)

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Ben

ucci

et

al(

2003

)It

aly

All

race

sC

linic

al

2002

23N

DN

DN

DN

DN

D71

0N

oN

oFl

oren

cere

cord

spa

tient

s ev

alua

tion

Gou

rley

et

al(

1997

)N

orth

ern

All

race

sC

linic

al

1992

ndash199

341

5N

DN

DN

D46

54

325

4N

obY

esIr

elan

dre

cord

s

phys

ians

pa

tient

s su

rvey

pa

tient

s E

PISE

R s

tudy

(20

01)

Spai

n A

ll ra

ces

Popu

latio

n 19

98ndash1

999

9N

DN

DN

D13

00

520

910

NS

No

incl

udin

g su

rvey

is

land

spa

tient

s ev

alua

tion

Lop

ez e

tal

(20

03)

Spai

nW

hite

Clin

ical

19

92ndash2

002

367

36

05

22

579

83

341

No

No

Nor

thho

spita

l re

cord

sN

ived

et

al(

1985

)Sw

eden

A

ll ra

ces

Clin

ical

19

81ndash1

982

657

62

04

864

811

738

9N

SN

oSo

uth

hosp

ital

reco

rds

Jons

son

Swed

en

All

race

sC

linic

al

1981

ndash198

639

I5

41

04

0N

DN

DN

DN

SN

oet

al(

1990

)So

uth

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

cont

inue

d

Cap

ture

ndashre

capt

ure

tech

niqu

e

Epidemiology of SLEN Danchenko et al

313

Lupus

Tabl

e 2

cont

inue

d

Stah

l-H

alle

ngre

n Sw

eden

A

ll ra

ces

Clin

ical

19

8612

1N

DN

D4

8N

DN

D42

0Y

esN

oet

al(

2000

)So

uth

hosp

ital

1991

379

ND

ND

45

ND

ND

680

reco

rds

patie

nts

eval

uatio

nH

opki

nson

U

K

All

race

sC

linic

al

1989

ndash199

014

76

51

54

045

43

724

6Y

esN

oet

al(

1993

)N

ottin

gham

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Hop

kins

on

UK

A

fro-

Clin

ical

19

89ndash1

990

21N

DN

D31

9N

DN

D20

70

Yes

No

etal

(19

94)

Not

tingh

amC

arib

bean

hosp

ital

Asi

anre

cord

s

7N

DN

D4

1N

DN

D48

8C

hine

seph

ysic

ians

2

ND

ND

ND

ND

ND

929

Whi

tesu

rvey

11

7N

DN

D3

4N

DN

D20

3po

pula

tion

estim

ates

N

atio

nal

Cen

sus

1991

John

son

UK

A

fro-

Clin

ical

19

9150

228

05

119

197

26

411

18

Yes

Yes

etal

(19

95)

Bir

min

gham

Car

ibbe

anho

spita

l A

sian

reco

rds

36

292

152

965

43

467

Whi

teph

ysic

ians

15

54

52

536

33

420

7A

ll ra

ces

surv

ey24

16

8i2a

38i

496

a3

6a27

7a

Nig

htin

gale

U

K

All

race

sC

linic

al

1992

ndash199

839

0I5

30

73

0N

DN

DN

DN

obN

oet

al(

2006

)N

atio

nwid

eho

spita

lpr

escr

iptio

n re

cord

sA

nste

y et

al

Aus

tral

ia

Abo

rigi

nes

Clin

ical

19

9322

ND

ND

110

100

05

252

6N

oN

o(1

993)

Dar

win

ho

spita

l K

athe

rine

re

cord

s

and

Eas

t ph

ysic

ians

A

rnhe

msu

rvey

Gre

nnan

et

al(

1995

)A

ustr

alia

A

bori

gine

sC

linic

al

1993

ndash199

420

ND

ND

ND

ND

ND

893

No

No

Nor

ther

n ho

spita

l Q

ueen

slan

d re

cord

s

phys

icia

ns

surv

eyA

ustr

alia

A

bori

gine

s3

ND

ND

ND

ND

ND

134

Sydn

eySe

gaso

thy

Aus

tral

ia

Abo

rigi

nes

Hos

pita

l Ju

lyndashD

ec 1

999

14N

DN

DN

D12

25

245

735

No

No

etal

(20

01)

Cen

tral

reco

rds

ph

ysic

ians

su

rvey

Whi

te6

ND

ND

ND

322

64

193

Fuka

se

Japa

nA

ll ra

ces

Clin

ical

19

7211

77N

DN

DN

D9

10

85

0N

oN

oet

al(

1980

)ex

cept

ho

spita

l O

kina

wa

surv

eyN

akae

Ja

pan

All

race

sC

linic

al

1984

2285

6N

DN

DN

D36

83

619

1N

oN

Set

al(

1984

)ho

spita

l su

rvey

cont

inue

d

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 2: SLE Epidemiology Danchenko 2006(1)

Regional variations and in particular differences inSLE incidence and prevalence in similar racial groupsliving in different parts of the world could further shedthe light on role of genetic environmental and othercausative factors in etiology and natural history of thedisease However the differences in SLE burdenacross the countries and continents are not fullydescribed Although some published studies includedfindings on various countries the available data con-cerning the incidence and prevalence of SLE are limi-ted and conflicting partially due to differences in studymethodology In addition the full worldwide review ofthe available data has not been performed The presentstudy was undertaken to summarize the available dataon SLE incidence and prevalence in the USA Canadaseveral European countries (UK France GermanyItaly Spain Sweden and Iceland) Australia Japanand Martinique to give an estimation of diseaseburden in these countries

Methods

To identify relevant studies the computerized biblio-graphic database of the National Library of Medicine(Medline 1966 to January 2006) was searched usingOvid and PubMed The references from all retrievedarticles and selected review papers and books werealso reviewed to ensure that all potentially eligible arti-cles were identified for evaluation From the articlesidentified we selected all those that reported data onincidence andor prevalence of systemic lupus in thecountries of interest with or without stratification byrace and gender

From each article we abstracted information onauthor(s) journal year of publication countrygeo-graphical area studied case source(s) (eg hospitalrecords physians interviews or population surveys)timeframe over which incidence andor prevalence ofSLE were assessed actual number of cases identifiedand incidence andor prevalence estimates reported Itwas also recorded whether capturendashrecapture tech-nique was used for more accurate estimation of inci-dence and prevalence by formally calculatingascertainment-corrected rates6

We reported incidence as a number of new cases per100 000 of the population per year and prevalence as across-sectional estimate of the number of cases per100 000 of the population per year as per figures pre-sented in the Results We summarized incidence andorprevalence by race andor gender whenever the datawere available If only gender-specific estimates wereprovided the overall number was calculated as anaverage between male and female estimates adjustingfor a male to female ratio in a population of interest

assessed from country-specific census data We alsorecorded whether the estimates were adjusted by age

SLE researchers in the countries of interest wereasked to provide any additional available reports onepidemiology of SLE or to confirm unavailability ofsuch information

Results were arrayed by outcome (incidence andprevalence) countries of interest and date of publica-tion The results across studies for a same outcomecountry and racial group were pooled to report amedian estimate and a range (presented in the figures)No statistical testing of differences in SLE burdenacross the countries has been performed

We identified approximately 60 studies that men-tioned incidence andor prevalence of systemic lupuserythematosus in the countries of interest The presentreview is focused on 32 studies reported quantitativeassessment of SLE burden in adults aged 16 years orolder other reports were excluded either due to focuson children aged 16 years or due to lack of cleardefinition of the target population or methods used forcase identification Of the 32 selected studies eightreported the information on the USA one on Canada16 on Europe three on Australia three on Japan andone on Martinique

Results

SLE incidence

USA and Canada The data for the USA and Canada aresummarized in Table 1 Siegel et al147 conductedstudies in New York and Alabama states Over theperiod of 1956ndash1965 in New York overall age-adjusted incidence for both genders was reported to be14 among whites 46 among black and 23 amongPuerto Rican The incidence in Jefferson County ALwas at least twice as low as those reported in NewYork NY 08 in whites and 17 in black4 Michetet al8 found an overall age-adjusted incidence of 18for all races combined in the Rochester area MN norace-specific estimates were reported in this study Asurvey conducted by Hochberg et al9 in BaltimoreMD showed the age-adjusted incidence of 22 and 72in whites and black respectively McCarty et al10

assessed SLE incidence in the Allegheny CountyPennsylvania6 using capture-recapture technique andreported the crude incidence of 20 in whites and 53 inblack The most recent study of Naleway et al11

showed the age-adjusted incidence of 51 for all racescombined in rural Wisconsin areaThe data on incidence of SLE in adult population ofCanada are scarce In a population-based study ofPeschken et al12 crude annual incidence rates ranged

Epidemiology of SLEN Danchenko et al

309

Lupus

Epidemiology of SLEN Danchenko et al

310

Lupus

Tabl

e 1

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

the

USA

and

Can

ada

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Sieg

el e

tal

(19

62)

USA

W

hite

1951

ndash195

942

I1

20

140

7aN

DN

DN

DY

esN

oN

ew Y

ork

NY

Bla

ck13

I3

90

82

4aN

DN

DN

DSi

egel

et

al(

1973

)U

SA

Whi

te19

56ndash1

965

552

50

31

4a16

82

99

9aY

esN

oN

ew Y

ork

NY

Bla

ck16

79

11

46a

558

33

296

a

Puer

to R

ican

254

10

32

3a33

62

318

0a

Sieg

el e

tal

(19

70)

USA

Jef

fers

on

Whi

te19

56ndash1

965

181

10

40

8a7

71

84

8aY

esN

oC

ount

yA

LB

lack

193

00

31

7a18

50

93a

Mic

het e

tal

(19

85)

USA

A

ll ra

ces

1950

ndash197

925

I2

50

91

853

819

040

0Y

esN

oR

oche

ster

MN

Hoc

hber

g et

al(

1985

)U

SA

Whi

te19

70ndash1

977

79I

39

04

22a

ND

ND

ND

Yes

No

Bal

timor

eM

DB

lack

223I

114

25

72a

McC

arty

et

al(

1995

)U

SA

Whi

te19

85ndash1

990

141I

35

04

20

ND

ND

ND

Noc

Yes

Pitts

burg

hPA

Bla

ck48

I9

20

75

3W

ard

etal

(20

04)

USA

A

ll ra

ces

1988

ndash199

440

ND

ND

ND

100

03

453

6N

oN

oN

atio

nwid

eN

alew

ay e

tal

(20

05)

USA

rur

al

All

race

s19

91ndash2

001

117

82

19

51

131

524

878

5Y

esN

oW

isco

nsin

are

aPe

schk

en e

tal

(20

00)

Can

ada

Nor

th A

mer

ican

19

80ndash1

996

49N

DN

D2

0ndash7

4bN

DN

D42

3Y

esN

oPr

ovin

ce o

f In

dian

s W

hite

208

ND

ND

09ndash

23b

ND

ND

206

Man

itoba

Pre

vale

nt c

ases

if n

ot o

ther

wis

e in

dica

ted

ldquoIrdquo

supe

rscr

ipt

inci

dent

est

imat

ea C

alcu

late

d as

an

aver

age

betw

een

mal

e an

d fe

mal

e es

timat

esa

djus

ting

for

a m

ale

to f

emal

e ra

tio in

ove

rall

popu

latio

nb R

epor

ted

estim

ates

are

not

age

-adj

uste

dc O

nly

crud

e ov

eral

l est

imat

es r

epor

ted

(alth

ough

age

-spe

cific

rat

es w

ere

also

est

imat

ed)

Cou

ntry

ge

ogra

phic

al

area

Num

ber

of

pati

ents

A

gead

just

men

t

Cap

ture

ndashre

capt

ure

tech

niqu

e

20ndash74 for North American Indians and 09ndash23 forthe remaining population between 1980 and 1996(Table 1)

European countries The incidence of SLE in FranceIceland Spain Sweden and the UK are summarized inTable 2

In France in 1982 Amor et al13 conducted anationwide survey among rheumatologists belongingto the French Rheumatology Society and reported theoverall crude incidence of 10 per 1 000 000 Based onthe recent National Public Insurance survey Pietteet al reported the overall nationwide incidence of5014

In Iceland a nationwide retrospective study byGudmundsson et al15 found that the overall age-adjusted incidence was 33

In Spain Lopez et al16 conducted a hospital-basedstudy in the Caucasian population of from the North ofthe country and reported the overall crude incidenceof 22

In Sweden Nived et al17 conducted a hospital-based study in Southern part of the country during1981 and 1982 and reported the overall incidence of48 Jonsson et al18 conducted a study within the samegeographical area during 1981ndash1986 and foundthe overall incidence of 40 Stahl-Hallengren et al19

studied incidence of SLE in the same region during1987ndash1991 and reported overall age-adjusted inci-dence of 48 and 45 in 1986 and 1991 respectively

In the UK a hospital- and clinic-based study ofHopkinson et al20 showed that the overall age-adjusted incidence in Nottingham was 40 Using pop-ulation estimates from 1991 National Census theylater reported race-specific incidence rates of 319 inAfro-Caribbean 41 in Asian and 34 in Caucasian21

Johnson et al22 conducted a study in BirminghamUK and reported the age-adjusted incidence of 119 inAfro-Caribbean 152 in Asian and 25 in CaucasianThe most recent nationwide study of Nightingaleet al23 based on the population of the General PracticeResearch Database (GPRD) showed the overall crudeincidence of 30

Other countries The summary of incidence data insome selected countries is given in Table 2

In Australia a hospital-based study of Australianaborigines24 showed the overall crude incidence of110 In Japan Iseki et al25 conducted a hospital- andclinic-based study on the population of Okinawa andreported that over the period from 1972 to 1991 theoverall crude incidence increased from 09 to 29Deligny et al26 conducted an extensive population-based study in Martinique and reported the overallincidence of 47

SLE incidence in the countries of interest is summa-rized in Figure 1 The figure reflects remarkably higherSLE incidence among non-whites compared to whitesThe lowest overall incidence estimates were reportedin Iceland and Japan and highest in the USA andFrance

SLE prevalence

USA and Canada The prevalence data for the USAare summarized in Table 1 In New York NY Siegelet al147 reported the age-adjusted prevalence of 99 inwhites 296 in black and 180 in Puerto Rican1 InJefferson County Alabama they found the prevalenceat least two-fold lower that in the New York area of 48in whites and 93 in black4 Michet et al8 reported theoverall age-adjusted prevalence of 400 in theRochester area MN In the nationwide study of Wardet al27 the overall crude prevalence was 536Naleway et al11 recently found that over 1991ndash2001the overall age-adjusted prevalence in rural Wisconsinarea was 785

In Canada Peschken et al12 showed a two-foldhigher prevalence of SLE in North American Indians(423) compared to non-Indians (206)

European countries The prevalence of SLE in FinlandFrance Germany Iceland Italy Northern IrelandSpain Sweden and the UK are summarized in Table 2

In Finland Helve et al28 conducted a nationwidestudy based on hospital discharge records and cause ofdeath statistics of 1976ndash1978 and reported the overallcrude prevalence of 280 In France Piette et al14

reported the nationwide overall prevalence of 400based on the National Public Insurance survey InGermany Zink et al29 described the case mix of theGerman rheumatologic database in 1998 They found1211 prevalent cases of SLE but have not reported theformal prevalence estimate In Iceland a nationwideretrospective study by Gudmundsson et al15 showedthe overall age-adjusted prevalence of 359 In ItalyBenucci et al30 recently studied prevalence of SLE inthe population of Scandicci-Le Signe area of Florenceusing the Lupus Screening Questionnaire (LQS) Theyreported the overall crude prevalence of 710 InNorthern Ireland6 Gourley et al31 found that the over-all crude prevalence of SLE was 254 In Spain theEPISER nationwide survey32 conducted by rheumato-logists on randomly selected residents showed the over-all prevalence of SLE of 910 In the hospital-basedstudy of Lopez et al16 conducted in the Caucasianpopulation of from the north of the country the overallcrude prevalence was 341 In Sweden in the hospital-based study of Nived et al the overall prevalence inthe Southern region of the country was found to

Epidemiology of SLEN Danchenko et al

311

Lupus

Epidemiology of SLEN Danchenko et al

312

Lupus

Tabl

e 2

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

oth

er c

ount

ries

Inci

denc

eP

reva

lenc

e

Aut

hor

Peri

od

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Hel

ve e

tal

(19

85)

Finl

and

All

race

sH

ospi

tal

1976

ndash197

814

27N

DN

DN

DN

DN

D28

0N

oN

ore

cord

s an

d ca

use

of d

eath

re

gist

ers

Am

or e

tal

(19

83)

Fran

ceA

ll ra

ces

Phys

icia

ns

1982

64N

DN

D1

per

ND

ND

ND

No

No

surv

ey1

000

000

Piet

te e

tal

(20

04)

Fran

ceA

ll ra

ces

Nat

iona

l 20

04N

SN

DN

D5

0N

DN

D40

0N

SN

opu

blic

in

sura

nce

surv

eyZ

ink

(200

1)G

erm

any

All

race

sC

linic

al

1993

ndash199

812

11N

DN

DN

DN

DN

D12

11

NS

No

hosp

ital

case

sre

cord

sG

udm

unds

son

Icel

and

All

race

sC

linic

al

1975

ndash198

476

58

08

33

620

72

359

Yes

No

etal

(19

90)

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Ben

ucci

et

al(

2003

)It

aly

All

race

sC

linic

al

2002

23N

DN

DN

DN

DN

D71

0N

oN

oFl

oren

cere

cord

spa

tient

s ev

alua

tion

Gou

rley

et

al(

1997

)N

orth

ern

All

race

sC

linic

al

1992

ndash199

341

5N

DN

DN

D46

54

325

4N

obY

esIr

elan

dre

cord

s

phys

ians

pa

tient

s su

rvey

pa

tient

s E

PISE

R s

tudy

(20

01)

Spai

n A

ll ra

ces

Popu

latio

n 19

98ndash1

999

9N

DN

DN

D13

00

520

910

NS

No

incl

udin

g su

rvey

is

land

spa

tient

s ev

alua

tion

Lop

ez e

tal

(20

03)

Spai

nW

hite

Clin

ical

19

92ndash2

002

367

36

05

22

579

83

341

No

No

Nor

thho

spita

l re

cord

sN

ived

et

al(

1985

)Sw

eden

A

ll ra

ces

Clin

ical

19

81ndash1

982

657

62

04

864

811

738

9N

SN

oSo

uth

hosp

ital

reco

rds

Jons

son

Swed

en

All

race

sC

linic

al

1981

ndash198

639

I5

41

04

0N

DN

DN

DN

SN

oet

al(

1990

)So

uth

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

cont

inue

d

Cap

ture

ndashre

capt

ure

tech

niqu

e

Epidemiology of SLEN Danchenko et al

313

Lupus

Tabl

e 2

cont

inue

d

Stah

l-H

alle

ngre

n Sw

eden

A

ll ra

ces

Clin

ical

19

8612

1N

DN

D4

8N

DN

D42

0Y

esN

oet

al(

2000

)So

uth

hosp

ital

1991

379

ND

ND

45

ND

ND

680

reco

rds

patie

nts

eval

uatio

nH

opki

nson

U

K

All

race

sC

linic

al

1989

ndash199

014

76

51

54

045

43

724

6Y

esN

oet

al(

1993

)N

ottin

gham

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Hop

kins

on

UK

A

fro-

Clin

ical

19

89ndash1

990

21N

DN

D31

9N

DN

D20

70

Yes

No

etal

(19

94)

Not

tingh

amC

arib

bean

hosp

ital

Asi

anre

cord

s

7N

DN

D4

1N

DN

D48

8C

hine

seph

ysic

ians

2

ND

ND

ND

ND

ND

929

Whi

tesu

rvey

11

7N

DN

D3

4N

DN

D20

3po

pula

tion

estim

ates

N

atio

nal

Cen

sus

1991

John

son

UK

A

fro-

Clin

ical

19

9150

228

05

119

197

26

411

18

Yes

Yes

etal

(19

95)

Bir

min

gham

Car

ibbe

anho

spita

l A

sian

reco

rds

36

292

152

965

43

467

Whi

teph

ysic

ians

15

54

52

536

33

420

7A

ll ra

ces

surv

ey24

16

8i2a

38i

496

a3

6a27

7a

Nig

htin

gale

U

K

All

race

sC

linic

al

1992

ndash199

839

0I5

30

73

0N

DN

DN

DN

obN

oet

al(

2006

)N

atio

nwid

eho

spita

lpr

escr

iptio

n re

cord

sA

nste

y et

al

Aus

tral

ia

Abo

rigi

nes

Clin

ical

19

9322

ND

ND

110

100

05

252

6N

oN

o(1

993)

Dar

win

ho

spita

l K

athe

rine

re

cord

s

and

Eas

t ph

ysic

ians

A

rnhe

msu

rvey

Gre

nnan

et

al(

1995

)A

ustr

alia

A

bori

gine

sC

linic

al

1993

ndash199

420

ND

ND

ND

ND

ND

893

No

No

Nor

ther

n ho

spita

l Q

ueen

slan

d re

cord

s

phys

icia

ns

surv

eyA

ustr

alia

A

bori

gine

s3

ND

ND

ND

ND

ND

134

Sydn

eySe

gaso

thy

Aus

tral

ia

Abo

rigi

nes

Hos

pita

l Ju

lyndashD

ec 1

999

14N

DN

DN

D12

25

245

735

No

No

etal

(20

01)

Cen

tral

reco

rds

ph

ysic

ians

su

rvey

Whi

te6

ND

ND

ND

322

64

193

Fuka

se

Japa

nA

ll ra

ces

Clin

ical

19

7211

77N

DN

DN

D9

10

85

0N

oN

oet

al(

1980

)ex

cept

ho

spita

l O

kina

wa

surv

eyN

akae

Ja

pan

All

race

sC

linic

al

1984

2285

6N

DN

DN

D36

83

619

1N

oN

Set

al(

1984

)ho

spita

l su

rvey

cont

inue

d

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 3: SLE Epidemiology Danchenko 2006(1)

Epidemiology of SLEN Danchenko et al

310

Lupus

Tabl

e 1

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

the

USA

and

Can

ada

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Sieg

el e

tal

(19

62)

USA

W

hite

1951

ndash195

942

I1

20

140

7aN

DN

DN

DY

esN

oN

ew Y

ork

NY

Bla

ck13

I3

90

82

4aN

DN

DN

DSi

egel

et

al(

1973

)U

SA

Whi

te19

56ndash1

965

552

50

31

4a16

82

99

9aY

esN

oN

ew Y

ork

NY

Bla

ck16

79

11

46a

558

33

296

a

Puer

to R

ican

254

10

32

3a33

62

318

0a

Sieg

el e

tal

(19

70)

USA

Jef

fers

on

Whi

te19

56ndash1

965

181

10

40

8a7

71

84

8aY

esN

oC

ount

yA

LB

lack

193

00

31

7a18

50

93a

Mic

het e

tal

(19

85)

USA

A

ll ra

ces

1950

ndash197

925

I2

50

91

853

819

040

0Y

esN

oR

oche

ster

MN

Hoc

hber

g et

al(

1985

)U

SA

Whi

te19

70ndash1

977

79I

39

04

22a

ND

ND

ND

Yes

No

Bal

timor

eM

DB

lack

223I

114

25

72a

McC

arty

et

al(

1995

)U

SA

Whi

te19

85ndash1

990

141I

35

04

20

ND

ND

ND

Noc

Yes

Pitts

burg

hPA

Bla

ck48

I9

20

75

3W

ard

etal

(20

04)

USA

A

ll ra

ces

1988

ndash199

440

ND

ND

ND

100

03

453

6N

oN

oN

atio

nwid

eN

alew

ay e

tal

(20

05)

USA

rur

al

All

race

s19

91ndash2

001

117

82

19

51

131

524

878

5Y

esN

oW

isco

nsin

are

aPe

schk

en e

tal

(20

00)

Can

ada

Nor

th A

mer

ican

19

80ndash1

996

49N

DN

D2

0ndash7

4bN

DN

D42

3Y

esN

oPr

ovin

ce o

f In

dian

s W

hite

208

ND

ND

09ndash

23b

ND

ND

206

Man

itoba

Pre

vale

nt c

ases

if n

ot o

ther

wis

e in

dica

ted

ldquoIrdquo

supe

rscr

ipt

inci

dent

est

imat

ea C

alcu

late

d as

an

aver

age

betw

een

mal

e an

d fe

mal

e es

timat

esa

djus

ting

for

a m

ale

to f

emal

e ra

tio in

ove

rall

popu

latio

nb R

epor

ted

estim

ates

are

not

age

-adj

uste

dc O

nly

crud

e ov

eral

l est

imat

es r

epor

ted

(alth

ough

age

-spe

cific

rat

es w

ere

also

est

imat

ed)

Cou

ntry

ge

ogra

phic

al

area

Num

ber

of

pati

ents

A

gead

just

men

t

Cap

ture

ndashre

capt

ure

tech

niqu

e

20ndash74 for North American Indians and 09ndash23 forthe remaining population between 1980 and 1996(Table 1)

European countries The incidence of SLE in FranceIceland Spain Sweden and the UK are summarized inTable 2

In France in 1982 Amor et al13 conducted anationwide survey among rheumatologists belongingto the French Rheumatology Society and reported theoverall crude incidence of 10 per 1 000 000 Based onthe recent National Public Insurance survey Pietteet al reported the overall nationwide incidence of5014

In Iceland a nationwide retrospective study byGudmundsson et al15 found that the overall age-adjusted incidence was 33

In Spain Lopez et al16 conducted a hospital-basedstudy in the Caucasian population of from the North ofthe country and reported the overall crude incidenceof 22

In Sweden Nived et al17 conducted a hospital-based study in Southern part of the country during1981 and 1982 and reported the overall incidence of48 Jonsson et al18 conducted a study within the samegeographical area during 1981ndash1986 and foundthe overall incidence of 40 Stahl-Hallengren et al19

studied incidence of SLE in the same region during1987ndash1991 and reported overall age-adjusted inci-dence of 48 and 45 in 1986 and 1991 respectively

In the UK a hospital- and clinic-based study ofHopkinson et al20 showed that the overall age-adjusted incidence in Nottingham was 40 Using pop-ulation estimates from 1991 National Census theylater reported race-specific incidence rates of 319 inAfro-Caribbean 41 in Asian and 34 in Caucasian21

Johnson et al22 conducted a study in BirminghamUK and reported the age-adjusted incidence of 119 inAfro-Caribbean 152 in Asian and 25 in CaucasianThe most recent nationwide study of Nightingaleet al23 based on the population of the General PracticeResearch Database (GPRD) showed the overall crudeincidence of 30

Other countries The summary of incidence data insome selected countries is given in Table 2

In Australia a hospital-based study of Australianaborigines24 showed the overall crude incidence of110 In Japan Iseki et al25 conducted a hospital- andclinic-based study on the population of Okinawa andreported that over the period from 1972 to 1991 theoverall crude incidence increased from 09 to 29Deligny et al26 conducted an extensive population-based study in Martinique and reported the overallincidence of 47

SLE incidence in the countries of interest is summa-rized in Figure 1 The figure reflects remarkably higherSLE incidence among non-whites compared to whitesThe lowest overall incidence estimates were reportedin Iceland and Japan and highest in the USA andFrance

SLE prevalence

USA and Canada The prevalence data for the USAare summarized in Table 1 In New York NY Siegelet al147 reported the age-adjusted prevalence of 99 inwhites 296 in black and 180 in Puerto Rican1 InJefferson County Alabama they found the prevalenceat least two-fold lower that in the New York area of 48in whites and 93 in black4 Michet et al8 reported theoverall age-adjusted prevalence of 400 in theRochester area MN In the nationwide study of Wardet al27 the overall crude prevalence was 536Naleway et al11 recently found that over 1991ndash2001the overall age-adjusted prevalence in rural Wisconsinarea was 785

In Canada Peschken et al12 showed a two-foldhigher prevalence of SLE in North American Indians(423) compared to non-Indians (206)

European countries The prevalence of SLE in FinlandFrance Germany Iceland Italy Northern IrelandSpain Sweden and the UK are summarized in Table 2

In Finland Helve et al28 conducted a nationwidestudy based on hospital discharge records and cause ofdeath statistics of 1976ndash1978 and reported the overallcrude prevalence of 280 In France Piette et al14

reported the nationwide overall prevalence of 400based on the National Public Insurance survey InGermany Zink et al29 described the case mix of theGerman rheumatologic database in 1998 They found1211 prevalent cases of SLE but have not reported theformal prevalence estimate In Iceland a nationwideretrospective study by Gudmundsson et al15 showedthe overall age-adjusted prevalence of 359 In ItalyBenucci et al30 recently studied prevalence of SLE inthe population of Scandicci-Le Signe area of Florenceusing the Lupus Screening Questionnaire (LQS) Theyreported the overall crude prevalence of 710 InNorthern Ireland6 Gourley et al31 found that the over-all crude prevalence of SLE was 254 In Spain theEPISER nationwide survey32 conducted by rheumato-logists on randomly selected residents showed the over-all prevalence of SLE of 910 In the hospital-basedstudy of Lopez et al16 conducted in the Caucasianpopulation of from the north of the country the overallcrude prevalence was 341 In Sweden in the hospital-based study of Nived et al the overall prevalence inthe Southern region of the country was found to

Epidemiology of SLEN Danchenko et al

311

Lupus

Epidemiology of SLEN Danchenko et al

312

Lupus

Tabl

e 2

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

oth

er c

ount

ries

Inci

denc

eP

reva

lenc

e

Aut

hor

Peri

od

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Hel

ve e

tal

(19

85)

Finl

and

All

race

sH

ospi

tal

1976

ndash197

814

27N

DN

DN

DN

DN

D28

0N

oN

ore

cord

s an

d ca

use

of d

eath

re

gist

ers

Am

or e

tal

(19

83)

Fran

ceA

ll ra

ces

Phys

icia

ns

1982

64N

DN

D1

per

ND

ND

ND

No

No

surv

ey1

000

000

Piet

te e

tal

(20

04)

Fran

ceA

ll ra

ces

Nat

iona

l 20

04N

SN

DN

D5

0N

DN

D40

0N

SN

opu

blic

in

sura

nce

surv

eyZ

ink

(200

1)G

erm

any

All

race

sC

linic

al

1993

ndash199

812

11N

DN

DN

DN

DN

D12

11

NS

No

hosp

ital

case

sre

cord

sG

udm

unds

son

Icel

and

All

race

sC

linic

al

1975

ndash198

476

58

08

33

620

72

359

Yes

No

etal

(19

90)

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Ben

ucci

et

al(

2003

)It

aly

All

race

sC

linic

al

2002

23N

DN

DN

DN

DN

D71

0N

oN

oFl

oren

cere

cord

spa

tient

s ev

alua

tion

Gou

rley

et

al(

1997

)N

orth

ern

All

race

sC

linic

al

1992

ndash199

341

5N

DN

DN

D46

54

325

4N

obY

esIr

elan

dre

cord

s

phys

ians

pa

tient

s su

rvey

pa

tient

s E

PISE

R s

tudy

(20

01)

Spai

n A

ll ra

ces

Popu

latio

n 19

98ndash1

999

9N

DN

DN

D13

00

520

910

NS

No

incl

udin

g su

rvey

is

land

spa

tient

s ev

alua

tion

Lop

ez e

tal

(20

03)

Spai

nW

hite

Clin

ical

19

92ndash2

002

367

36

05

22

579

83

341

No

No

Nor

thho

spita

l re

cord

sN

ived

et

al(

1985

)Sw

eden

A

ll ra

ces

Clin

ical

19

81ndash1

982

657

62

04

864

811

738

9N

SN

oSo

uth

hosp

ital

reco

rds

Jons

son

Swed

en

All

race

sC

linic

al

1981

ndash198

639

I5

41

04

0N

DN

DN

DN

SN

oet

al(

1990

)So

uth

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

cont

inue

d

Cap

ture

ndashre

capt

ure

tech

niqu

e

Epidemiology of SLEN Danchenko et al

313

Lupus

Tabl

e 2

cont

inue

d

Stah

l-H

alle

ngre

n Sw

eden

A

ll ra

ces

Clin

ical

19

8612

1N

DN

D4

8N

DN

D42

0Y

esN

oet

al(

2000

)So

uth

hosp

ital

1991

379

ND

ND

45

ND

ND

680

reco

rds

patie

nts

eval

uatio

nH

opki

nson

U

K

All

race

sC

linic

al

1989

ndash199

014

76

51

54

045

43

724

6Y

esN

oet

al(

1993

)N

ottin

gham

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Hop

kins

on

UK

A

fro-

Clin

ical

19

89ndash1

990

21N

DN

D31

9N

DN

D20

70

Yes

No

etal

(19

94)

Not

tingh

amC

arib

bean

hosp

ital

Asi

anre

cord

s

7N

DN

D4

1N

DN

D48

8C

hine

seph

ysic

ians

2

ND

ND

ND

ND

ND

929

Whi

tesu

rvey

11

7N

DN

D3

4N

DN

D20

3po

pula

tion

estim

ates

N

atio

nal

Cen

sus

1991

John

son

UK

A

fro-

Clin

ical

19

9150

228

05

119

197

26

411

18

Yes

Yes

etal

(19

95)

Bir

min

gham

Car

ibbe

anho

spita

l A

sian

reco

rds

36

292

152

965

43

467

Whi

teph

ysic

ians

15

54

52

536

33

420

7A

ll ra

ces

surv

ey24

16

8i2a

38i

496

a3

6a27

7a

Nig

htin

gale

U

K

All

race

sC

linic

al

1992

ndash199

839

0I5

30

73

0N

DN

DN

DN

obN

oet

al(

2006

)N

atio

nwid

eho

spita

lpr

escr

iptio

n re

cord

sA

nste

y et

al

Aus

tral

ia

Abo

rigi

nes

Clin

ical

19

9322

ND

ND

110

100

05

252

6N

oN

o(1

993)

Dar

win

ho

spita

l K

athe

rine

re

cord

s

and

Eas

t ph

ysic

ians

A

rnhe

msu

rvey

Gre

nnan

et

al(

1995

)A

ustr

alia

A

bori

gine

sC

linic

al

1993

ndash199

420

ND

ND

ND

ND

ND

893

No

No

Nor

ther

n ho

spita

l Q

ueen

slan

d re

cord

s

phys

icia

ns

surv

eyA

ustr

alia

A

bori

gine

s3

ND

ND

ND

ND

ND

134

Sydn

eySe

gaso

thy

Aus

tral

ia

Abo

rigi

nes

Hos

pita

l Ju

lyndashD

ec 1

999

14N

DN

DN

D12

25

245

735

No

No

etal

(20

01)

Cen

tral

reco

rds

ph

ysic

ians

su

rvey

Whi

te6

ND

ND

ND

322

64

193

Fuka

se

Japa

nA

ll ra

ces

Clin

ical

19

7211

77N

DN

DN

D9

10

85

0N

oN

oet

al(

1980

)ex

cept

ho

spita

l O

kina

wa

surv

eyN

akae

Ja

pan

All

race

sC

linic

al

1984

2285

6N

DN

DN

D36

83

619

1N

oN

Set

al(

1984

)ho

spita

l su

rvey

cont

inue

d

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 4: SLE Epidemiology Danchenko 2006(1)

20ndash74 for North American Indians and 09ndash23 forthe remaining population between 1980 and 1996(Table 1)

European countries The incidence of SLE in FranceIceland Spain Sweden and the UK are summarized inTable 2

In France in 1982 Amor et al13 conducted anationwide survey among rheumatologists belongingto the French Rheumatology Society and reported theoverall crude incidence of 10 per 1 000 000 Based onthe recent National Public Insurance survey Pietteet al reported the overall nationwide incidence of5014

In Iceland a nationwide retrospective study byGudmundsson et al15 found that the overall age-adjusted incidence was 33

In Spain Lopez et al16 conducted a hospital-basedstudy in the Caucasian population of from the North ofthe country and reported the overall crude incidenceof 22

In Sweden Nived et al17 conducted a hospital-based study in Southern part of the country during1981 and 1982 and reported the overall incidence of48 Jonsson et al18 conducted a study within the samegeographical area during 1981ndash1986 and foundthe overall incidence of 40 Stahl-Hallengren et al19

studied incidence of SLE in the same region during1987ndash1991 and reported overall age-adjusted inci-dence of 48 and 45 in 1986 and 1991 respectively

In the UK a hospital- and clinic-based study ofHopkinson et al20 showed that the overall age-adjusted incidence in Nottingham was 40 Using pop-ulation estimates from 1991 National Census theylater reported race-specific incidence rates of 319 inAfro-Caribbean 41 in Asian and 34 in Caucasian21

Johnson et al22 conducted a study in BirminghamUK and reported the age-adjusted incidence of 119 inAfro-Caribbean 152 in Asian and 25 in CaucasianThe most recent nationwide study of Nightingaleet al23 based on the population of the General PracticeResearch Database (GPRD) showed the overall crudeincidence of 30

Other countries The summary of incidence data insome selected countries is given in Table 2

In Australia a hospital-based study of Australianaborigines24 showed the overall crude incidence of110 In Japan Iseki et al25 conducted a hospital- andclinic-based study on the population of Okinawa andreported that over the period from 1972 to 1991 theoverall crude incidence increased from 09 to 29Deligny et al26 conducted an extensive population-based study in Martinique and reported the overallincidence of 47

SLE incidence in the countries of interest is summa-rized in Figure 1 The figure reflects remarkably higherSLE incidence among non-whites compared to whitesThe lowest overall incidence estimates were reportedin Iceland and Japan and highest in the USA andFrance

SLE prevalence

USA and Canada The prevalence data for the USAare summarized in Table 1 In New York NY Siegelet al147 reported the age-adjusted prevalence of 99 inwhites 296 in black and 180 in Puerto Rican1 InJefferson County Alabama they found the prevalenceat least two-fold lower that in the New York area of 48in whites and 93 in black4 Michet et al8 reported theoverall age-adjusted prevalence of 400 in theRochester area MN In the nationwide study of Wardet al27 the overall crude prevalence was 536Naleway et al11 recently found that over 1991ndash2001the overall age-adjusted prevalence in rural Wisconsinarea was 785

In Canada Peschken et al12 showed a two-foldhigher prevalence of SLE in North American Indians(423) compared to non-Indians (206)

European countries The prevalence of SLE in FinlandFrance Germany Iceland Italy Northern IrelandSpain Sweden and the UK are summarized in Table 2

In Finland Helve et al28 conducted a nationwidestudy based on hospital discharge records and cause ofdeath statistics of 1976ndash1978 and reported the overallcrude prevalence of 280 In France Piette et al14

reported the nationwide overall prevalence of 400based on the National Public Insurance survey InGermany Zink et al29 described the case mix of theGerman rheumatologic database in 1998 They found1211 prevalent cases of SLE but have not reported theformal prevalence estimate In Iceland a nationwideretrospective study by Gudmundsson et al15 showedthe overall age-adjusted prevalence of 359 In ItalyBenucci et al30 recently studied prevalence of SLE inthe population of Scandicci-Le Signe area of Florenceusing the Lupus Screening Questionnaire (LQS) Theyreported the overall crude prevalence of 710 InNorthern Ireland6 Gourley et al31 found that the over-all crude prevalence of SLE was 254 In Spain theEPISER nationwide survey32 conducted by rheumato-logists on randomly selected residents showed the over-all prevalence of SLE of 910 In the hospital-basedstudy of Lopez et al16 conducted in the Caucasianpopulation of from the north of the country the overallcrude prevalence was 341 In Sweden in the hospital-based study of Nived et al the overall prevalence inthe Southern region of the country was found to

Epidemiology of SLEN Danchenko et al

311

Lupus

Epidemiology of SLEN Danchenko et al

312

Lupus

Tabl

e 2

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

oth

er c

ount

ries

Inci

denc

eP

reva

lenc

e

Aut

hor

Peri

od

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Hel

ve e

tal

(19

85)

Finl

and

All

race

sH

ospi

tal

1976

ndash197

814

27N

DN

DN

DN

DN

D28

0N

oN

ore

cord

s an

d ca

use

of d

eath

re

gist

ers

Am

or e

tal

(19

83)

Fran

ceA

ll ra

ces

Phys

icia

ns

1982

64N

DN

D1

per

ND

ND

ND

No

No

surv

ey1

000

000

Piet

te e

tal

(20

04)

Fran

ceA

ll ra

ces

Nat

iona

l 20

04N

SN

DN

D5

0N

DN

D40

0N

SN

opu

blic

in

sura

nce

surv

eyZ

ink

(200

1)G

erm

any

All

race

sC

linic

al

1993

ndash199

812

11N

DN

DN

DN

DN

D12

11

NS

No

hosp

ital

case

sre

cord

sG

udm

unds

son

Icel

and

All

race

sC

linic

al

1975

ndash198

476

58

08

33

620

72

359

Yes

No

etal

(19

90)

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Ben

ucci

et

al(

2003

)It

aly

All

race

sC

linic

al

2002

23N

DN

DN

DN

DN

D71

0N

oN

oFl

oren

cere

cord

spa

tient

s ev

alua

tion

Gou

rley

et

al(

1997

)N

orth

ern

All

race

sC

linic

al

1992

ndash199

341

5N

DN

DN

D46

54

325

4N

obY

esIr

elan

dre

cord

s

phys

ians

pa

tient

s su

rvey

pa

tient

s E

PISE

R s

tudy

(20

01)

Spai

n A

ll ra

ces

Popu

latio

n 19

98ndash1

999

9N

DN

DN

D13

00

520

910

NS

No

incl

udin

g su

rvey

is

land

spa

tient

s ev

alua

tion

Lop

ez e

tal

(20

03)

Spai

nW

hite

Clin

ical

19

92ndash2

002

367

36

05

22

579

83

341

No

No

Nor

thho

spita

l re

cord

sN

ived

et

al(

1985

)Sw

eden

A

ll ra

ces

Clin

ical

19

81ndash1

982

657

62

04

864

811

738

9N

SN

oSo

uth

hosp

ital

reco

rds

Jons

son

Swed

en

All

race

sC

linic

al

1981

ndash198

639

I5

41

04

0N

DN

DN

DN

SN

oet

al(

1990

)So

uth

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

cont

inue

d

Cap

ture

ndashre

capt

ure

tech

niqu

e

Epidemiology of SLEN Danchenko et al

313

Lupus

Tabl

e 2

cont

inue

d

Stah

l-H

alle

ngre

n Sw

eden

A

ll ra

ces

Clin

ical

19

8612

1N

DN

D4

8N

DN

D42

0Y

esN

oet

al(

2000

)So

uth

hosp

ital

1991

379

ND

ND

45

ND

ND

680

reco

rds

patie

nts

eval

uatio

nH

opki

nson

U

K

All

race

sC

linic

al

1989

ndash199

014

76

51

54

045

43

724

6Y

esN

oet

al(

1993

)N

ottin

gham

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Hop

kins

on

UK

A

fro-

Clin

ical

19

89ndash1

990

21N

DN

D31

9N

DN

D20

70

Yes

No

etal

(19

94)

Not

tingh

amC

arib

bean

hosp

ital

Asi

anre

cord

s

7N

DN

D4

1N

DN

D48

8C

hine

seph

ysic

ians

2

ND

ND

ND

ND

ND

929

Whi

tesu

rvey

11

7N

DN

D3

4N

DN

D20

3po

pula

tion

estim

ates

N

atio

nal

Cen

sus

1991

John

son

UK

A

fro-

Clin

ical

19

9150

228

05

119

197

26

411

18

Yes

Yes

etal

(19

95)

Bir

min

gham

Car

ibbe

anho

spita

l A

sian

reco

rds

36

292

152

965

43

467

Whi

teph

ysic

ians

15

54

52

536

33

420

7A

ll ra

ces

surv

ey24

16

8i2a

38i

496

a3

6a27

7a

Nig

htin

gale

U

K

All

race

sC

linic

al

1992

ndash199

839

0I5

30

73

0N

DN

DN

DN

obN

oet

al(

2006

)N

atio

nwid

eho

spita

lpr

escr

iptio

n re

cord

sA

nste

y et

al

Aus

tral

ia

Abo

rigi

nes

Clin

ical

19

9322

ND

ND

110

100

05

252

6N

oN

o(1

993)

Dar

win

ho

spita

l K

athe

rine

re

cord

s

and

Eas

t ph

ysic

ians

A

rnhe

msu

rvey

Gre

nnan

et

al(

1995

)A

ustr

alia

A

bori

gine

sC

linic

al

1993

ndash199

420

ND

ND

ND

ND

ND

893

No

No

Nor

ther

n ho

spita

l Q

ueen

slan

d re

cord

s

phys

icia

ns

surv

eyA

ustr

alia

A

bori

gine

s3

ND

ND

ND

ND

ND

134

Sydn

eySe

gaso

thy

Aus

tral

ia

Abo

rigi

nes

Hos

pita

l Ju

lyndashD

ec 1

999

14N

DN

DN

D12

25

245

735

No

No

etal

(20

01)

Cen

tral

reco

rds

ph

ysic

ians

su

rvey

Whi

te6

ND

ND

ND

322

64

193

Fuka

se

Japa

nA

ll ra

ces

Clin

ical

19

7211

77N

DN

DN

D9

10

85

0N

oN

oet

al(

1980

)ex

cept

ho

spita

l O

kina

wa

surv

eyN

akae

Ja

pan

All

race

sC

linic

al

1984

2285

6N

DN

DN

D36

83

619

1N

oN

Set

al(

1984

)ho

spita

l su

rvey

cont

inue

d

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 5: SLE Epidemiology Danchenko 2006(1)

Epidemiology of SLEN Danchenko et al

312

Lupus

Tabl

e 2

Stud

ies

on in

cide

nce

and

prev

alen

ce o

f SL

E in

oth

er c

ount

ries

Inci

denc

eP

reva

lenc

e

Aut

hor

Peri

od

Fem

ales

Mal

esO

vera

llFe

mal

esM

ales

Ove

rall

Hel

ve e

tal

(19

85)

Finl

and

All

race

sH

ospi

tal

1976

ndash197

814

27N

DN

DN

DN

DN

D28

0N

oN

ore

cord

s an

d ca

use

of d

eath

re

gist

ers

Am

or e

tal

(19

83)

Fran

ceA

ll ra

ces

Phys

icia

ns

1982

64N

DN

D1

per

ND

ND

ND

No

No

surv

ey1

000

000

Piet

te e

tal

(20

04)

Fran

ceA

ll ra

ces

Nat

iona

l 20

04N

SN

DN

D5

0N

DN

D40

0N

SN

opu

blic

in

sura

nce

surv

eyZ

ink

(200

1)G

erm

any

All

race

sC

linic

al

1993

ndash199

812

11N

DN

DN

DN

DN

D12

11

NS

No

hosp

ital

case

sre

cord

sG

udm

unds

son

Icel

and

All

race

sC

linic

al

1975

ndash198

476

58

08

33

620

72

359

Yes

No

etal

(19

90)

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Ben

ucci

et

al(

2003

)It

aly

All

race

sC

linic

al

2002

23N

DN

DN

DN

DN

D71

0N

oN

oFl

oren

cere

cord

spa

tient

s ev

alua

tion

Gou

rley

et

al(

1997

)N

orth

ern

All

race

sC

linic

al

1992

ndash199

341

5N

DN

DN

D46

54

325

4N

obY

esIr

elan

dre

cord

s

phys

ians

pa

tient

s su

rvey

pa

tient

s E

PISE

R s

tudy

(20

01)

Spai

n A

ll ra

ces

Popu

latio

n 19

98ndash1

999

9N

DN

DN

D13

00

520

910

NS

No

incl

udin

g su

rvey

is

land

spa

tient

s ev

alua

tion

Lop

ez e

tal

(20

03)

Spai

nW

hite

Clin

ical

19

92ndash2

002

367

36

05

22

579

83

341

No

No

Nor

thho

spita

l re

cord

sN

ived

et

al(

1985

)Sw

eden

A

ll ra

ces

Clin

ical

19

81ndash1

982

657

62

04

864

811

738

9N

SN

oSo

uth

hosp

ital

reco

rds

Jons

son

Swed

en

All

race

sC

linic

al

1981

ndash198

639

I5

41

04

0N

DN

DN

DN

SN

oet

al(

1990

)So

uth

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

cont

inue

d

Cap

ture

ndashre

capt

ure

tech

niqu

e

Epidemiology of SLEN Danchenko et al

313

Lupus

Tabl

e 2

cont

inue

d

Stah

l-H

alle

ngre

n Sw

eden

A

ll ra

ces

Clin

ical

19

8612

1N

DN

D4

8N

DN

D42

0Y

esN

oet

al(

2000

)So

uth

hosp

ital

1991

379

ND

ND

45

ND

ND

680

reco

rds

patie

nts

eval

uatio

nH

opki

nson

U

K

All

race

sC

linic

al

1989

ndash199

014

76

51

54

045

43

724

6Y

esN

oet

al(

1993

)N

ottin

gham

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Hop

kins

on

UK

A

fro-

Clin

ical

19

89ndash1

990

21N

DN

D31

9N

DN

D20

70

Yes

No

etal

(19

94)

Not

tingh

amC

arib

bean

hosp

ital

Asi

anre

cord

s

7N

DN

D4

1N

DN

D48

8C

hine

seph

ysic

ians

2

ND

ND

ND

ND

ND

929

Whi

tesu

rvey

11

7N

DN

D3

4N

DN

D20

3po

pula

tion

estim

ates

N

atio

nal

Cen

sus

1991

John

son

UK

A

fro-

Clin

ical

19

9150

228

05

119

197

26

411

18

Yes

Yes

etal

(19

95)

Bir

min

gham

Car

ibbe

anho

spita

l A

sian

reco

rds

36

292

152

965

43

467

Whi

teph

ysic

ians

15

54

52

536

33

420

7A

ll ra

ces

surv

ey24

16

8i2a

38i

496

a3

6a27

7a

Nig

htin

gale

U

K

All

race

sC

linic

al

1992

ndash199

839

0I5

30

73

0N

DN

DN

DN

obN

oet

al(

2006

)N

atio

nwid

eho

spita

lpr

escr

iptio

n re

cord

sA

nste

y et

al

Aus

tral

ia

Abo

rigi

nes

Clin

ical

19

9322

ND

ND

110

100

05

252

6N

oN

o(1

993)

Dar

win

ho

spita

l K

athe

rine

re

cord

s

and

Eas

t ph

ysic

ians

A

rnhe

msu

rvey

Gre

nnan

et

al(

1995

)A

ustr

alia

A

bori

gine

sC

linic

al

1993

ndash199

420

ND

ND

ND

ND

ND

893

No

No

Nor

ther

n ho

spita

l Q

ueen

slan

d re

cord

s

phys

icia

ns

surv

eyA

ustr

alia

A

bori

gine

s3

ND

ND

ND

ND

ND

134

Sydn

eySe

gaso

thy

Aus

tral

ia

Abo

rigi

nes

Hos

pita

l Ju

lyndashD

ec 1

999

14N

DN

DN

D12

25

245

735

No

No

etal

(20

01)

Cen

tral

reco

rds

ph

ysic

ians

su

rvey

Whi

te6

ND

ND

ND

322

64

193

Fuka

se

Japa

nA

ll ra

ces

Clin

ical

19

7211

77N

DN

DN

D9

10

85

0N

oN

oet

al(

1980

)ex

cept

ho

spita

l O

kina

wa

surv

eyN

akae

Ja

pan

All

race

sC

linic

al

1984

2285

6N

DN

DN

D36

83

619

1N

oN

Set

al(

1984

)ho

spita

l su

rvey

cont

inue

d

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 6: SLE Epidemiology Danchenko 2006(1)

Epidemiology of SLEN Danchenko et al

313

Lupus

Tabl

e 2

cont

inue

d

Stah

l-H

alle

ngre

n Sw

eden

A

ll ra

ces

Clin

ical

19

8612

1N

DN

D4

8N

DN

D42

0Y

esN

oet

al(

2000

)So

uth

hosp

ital

1991

379

ND

ND

45

ND

ND

680

reco

rds

patie

nts

eval

uatio

nH

opki

nson

U

K

All

race

sC

linic

al

1989

ndash199

014

76

51

54

045

43

724

6Y

esN

oet

al(

1993

)N

ottin

gham

hosp

ital

reco

rds

ph

ysic

ians

su

rvey

Hop

kins

on

UK

A

fro-

Clin

ical

19

89ndash1

990

21N

DN

D31

9N

DN

D20

70

Yes

No

etal

(19

94)

Not

tingh

amC

arib

bean

hosp

ital

Asi

anre

cord

s

7N

DN

D4

1N

DN

D48

8C

hine

seph

ysic

ians

2

ND

ND

ND

ND

ND

929

Whi

tesu

rvey

11

7N

DN

D3

4N

DN

D20

3po

pula

tion

estim

ates

N

atio

nal

Cen

sus

1991

John

son

UK

A

fro-

Clin

ical

19

9150

228

05

119

197

26

411

18

Yes

Yes

etal

(19

95)

Bir

min

gham

Car

ibbe

anho

spita

l A

sian

reco

rds

36

292

152

965

43

467

Whi

teph

ysic

ians

15

54

52

536

33

420

7A

ll ra

ces

surv

ey24

16

8i2a

38i

496

a3

6a27

7a

Nig

htin

gale

U

K

All

race

sC

linic

al

1992

ndash199

839

0I5

30

73

0N

DN

DN

DN

obN

oet

al(

2006

)N

atio

nwid

eho

spita

lpr

escr

iptio

n re

cord

sA

nste

y et

al

Aus

tral

ia

Abo

rigi

nes

Clin

ical

19

9322

ND

ND

110

100

05

252

6N

oN

o(1

993)

Dar

win

ho

spita

l K

athe

rine

re

cord

s

and

Eas

t ph

ysic

ians

A

rnhe

msu

rvey

Gre

nnan

et

al(

1995

)A

ustr

alia

A

bori

gine

sC

linic

al

1993

ndash199

420

ND

ND

ND

ND

ND

893

No

No

Nor

ther

n ho

spita

l Q

ueen

slan

d re

cord

s

phys

icia

ns

surv

eyA

ustr

alia

A

bori

gine

s3

ND

ND

ND

ND

ND

134

Sydn

eySe

gaso

thy

Aus

tral

ia

Abo

rigi

nes

Hos

pita

l Ju

lyndashD

ec 1

999

14N

DN

DN

D12

25

245

735

No

No

etal

(20

01)

Cen

tral

reco

rds

ph

ysic

ians

su

rvey

Whi

te6

ND

ND

ND

322

64

193

Fuka

se

Japa

nA

ll ra

ces

Clin

ical

19

7211

77N

DN

DN

D9

10

85

0N

oN

oet

al(

1980

)ex

cept

ho

spita

l O

kina

wa

surv

eyN

akae

Ja

pan

All

race

sC

linic

al

1984

2285

6N

DN

DN

D36

83

619

1N

oN

Set

al(

1984

)ho

spita

l su

rvey

cont

inue

d

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 7: SLE Epidemiology Danchenko 2006(1)

Epidemiology of SLEN Danchenko et al

314

Lupus

Isek

i et

al(

1994

)Ja

pan

All

race

sC

linic

al

1972

566

16

04

09

66

08

37

No

No

Oki

naw

aho

spita

l re

cord

s19

914

70

82

968

47

037

7D

elig

ny

Mar

tiniq

ueA

ll ra

ces

Hos

pita

l 19

90ndash1

999

286

85

07

47

115

92

642

NS

No

etal

(20

02)

reco

rds

phys

icia

ns

surv

ey

deat

h re

gist

ry

NS

no

t spe

cifie

dP

reva

lent

cas

es if

not

oth

erw

ise

indi

cate

d I

sup

ersc

ript

in

cide

nt e

stim

ate

a Est

imat

es r

epor

ted

are

not a

ge-a

djus

ted

b Onl

y cr

ude

over

all i

ncid

ence

est

imat

es w

ere

repo

rted

(al

thou

gh a

ge-s

peci

fic in

cide

nce

rate

s w

ere

also

rep

orte

d)

be 389 In the study of Stahl-Hallengren et al19

conducted within the same geographical area theoverall age-adjusted prevalence was 420 in 1986 and680 in 1991

In the UK Hopkinson et al20 reported the overallage-adjusted prevalence of 246 in the Nottinghamarea Racial breakdown based on 1991 NationalCensus further showed the prevalence of 2070in Afro-Caribbean 488 in Asian 929 in Chinese and203 in Caucasian respectively21 Johnson et alreported the age-adjusted prevalence of 1118 467and 207 in Afro-Caribbean Asian and Caucasianrespectively in the population of Birmingham UK22

Other countries The summary of prevalence data insome other countries of the world are presented inTable 2 In the study of Australian aborigines24 in thedefined geographical area of Darwin Katherine andEast Arnhem the overall crude prevalence reported tobe 526 Grennan et al33 reported the crude SLE preva-lence of 893 in Australian Aborigines located inNorthern Queensland in the Cape York Peninsula and134 in metropolitan Sydney Segasothy et al34 com-pared the prevalence of SLE among Aborigines andCaucasians in Central Australia and reported the crudeprevalence of 735 in Aborigines and 193 inCaucasians

In Japan an early nationwide study by Fukaseet al35 showed the overall crude prevalence of 50The authors mention that only 50 of patientsdiagnosed at hospitals met preliminary ARA criteria(1971) Nakae et al36 conducted a nationwideepidemiological survey and found that the overallcrude prevalence was 191 However the researchersnote that the response rate from objected medical insti-tutions was only 433 The hospital- and clinic-basedstudy in Okinawa Iseki et al25 reported an increase inprevalence from 1972 to 1991 from approximately 37to 377

In Martinique Deligny et al26 estimated the overallprevalence of 642

The summary of SLE prevalence across the coun-tries is presented in Figure 2 It shows remarkablyhigher SLE prevalence in non-white racial groupscompared to whites The lowest overall prevalence wasfound in Ireland the UK and Finland and highest inItaly Spain and Martinique

Discussion

The report represents a review of the published data inincidence and prevalence of SLE in the USA CanadaWestern Europe Australia Japan and Martinique itprovides the most recent summary of SLE burdenTa

ble

2co

ntin

ued

Inci

denc

eP

reva

lenc

e

Aut

hor

Rac

ePe

riod

Fe

mal

esM

ales

Ove

rall

Fem

ales

Mal

esO

vera

ll

Cou

ntry

ge

ogra

phic

al

area

Cas

eso

urce

(s)

Num

ber

of

pati

ents

A

ge

adju

stm

ent

Cap

ture

ndashre

capt

ure

tech

niqu

e

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 8: SLE Epidemiology Danchenko 2006(1)

worldwide We found remarkable disparities in SLEburden across the countries Historically the rates ofSLE in Europe have been lower than in the USA22 butrecent data from the USA1027 makes this tendency lessobvious The lowest overall incidence was found inIceland and Japan and highest in the USA and FranceThe overall prevalence was the lowest in NorthernIreland the UK and Finland and the highest inItaly Spain and Martinique The burden of SLE wasconsistently increased in non-white population of theUSA Europe Canada and Australia The gender dif-ferences are well recognized1ndash337 and the presentreview did not intend to emphasize them

The findings summarized in the present review pro-vide no sufficient evidence to conclude that SLE is lesscommon in some countries compared to others The

variability in incidence and prevalence estimates canbe attributable to true disparities across the countriesor result from the methodological differences amongthe studies

Racial composition and its stability (the level ofimmigrationemigration) in a population have beenrecognized as one of the important determinants oftrue disparities in SLE burden Higher diseaseprevalence was reported in non-white racialgroups149102434 Unstable racial composition of apopulation due to transitory nature of certain groups(eg European population in Australia) makes it chal-lenging to accurately assess SLE burden On the con-trary countries with homogeneic and racially stablepopulation (eg Iceland) are considered well suited forepidemiological studies

Epidemiology of SLEN Danchenko et al

315

Lupus

Figure 1 SLE incidence in the countries of interest

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 9: SLE Epidemiology Danchenko 2006(1)

Epidemiology of SLEN Danchenko et al

316

Lupus

Environmental triggers such as infections andultraviolet light constitute another important groupof factors determining the burden of SLE Infectiousagents may initiate SLE onset by disturbingimmunoregulation causing damage to tissue whichleads to the release of antigens2 High prevalence ofmajor bacterial infections in certain regions ofAustralia is thought to be involved in SLE patho-genesis in local Aborigines populations3334 UV radi-ation may induce keratinocyte apoptosis with therelease of nuclear antigens that may drive an autoim-mune response3839 Varying levels of sunlight expo-sure in different parts of the world may thereforecontribute to disparities in SLE burden across thecountries partially explaining elevated prevalence of

the disease in the north of Australia and in the southof Europe

Estrogens account for the higher immune reactivityin females and can also act as a trigger of autoimmunediseases such as SLE240 Varying physiological thera-peutic and pathological conditions (eg menstrualcycle chronic stress inflammatory cytokines use ofcorticosteroids oral contraceptives and steroid hor-monal replacement) may change serum estrogen leveltherefore contributing to true variations in exposure toSLE in different population groups41

Country-specific health care issues can alsocontribute to true discrepancies in SLE burden Theseinclude accessibility and affordability of health caredetermined by health care system of a particular

Figure 2 SLE prevalence in the countries of interest

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 10: SLE Epidemiology Danchenko 2006(1)

country and dependent on a geographical area (urbanversus rural) Availability of sensitive diagnostic testsinfluences the number of identified SLE patients buthas a two-fold effect facilitating detection of mildercases and increasing the number of false positive diag-noses Physician knowledge and recognition of diseasevarying over time and across countries and regions canalso explain temporal and geographical dissimilaritiesin the number of diagnosed SLE cases Finally betterhealth care is associated with lower mortality ratesexplaining discrepancies in SLE prevalence across thecountries22

Methodological differences among studies causingadditional artifactual variability in SLE burden acrossthe countries are mostly related either to disparities incase identification and data sources or to analyticalissues The former include differences in diagnosticcriteria chosen by authors with American College ofRheumatology (ACR) criteria used most widely andother options available such as Lupus ScreeningQuestionnaire (LQS) Different sources of cases (eghospital records review physicians surveys majorpopulation surveys use of population-based databasesand registries) have different strengths and weak-nesses and may contribute to variability in studyresults Hospital records interpretation may varydepending on the diagnostic criteria applied andpatients treated without hospitalization are not esti-mated Physicians surveys rely on physiciansrsquo recallwhich introduces bias Major population surveys allowavoiding many potential biases however such studiesmay not be efficient for the evaluation of the raredisease such as SLE Population-based databases areunique source of information on large well-definedpopulations but their use limits the generalizability ofstudy results and the ability to compare results fromanalyses of different databases Analytical issuesinclude adjustment for major demographic characteris-tics (eg age) and application of capture-recapturemethods whenever multiple case ascertainmentsources are used6

Therefore the variability in incidence and preva-lence across the countries can be attributed to a widevariety of true differences among geographical regionsand populations as well as to variations in studydesigns including (but not limited to) methodology ofcase identification and analytical issues

Conclusion

There are marked disparities in SLE incidence andprevalence worldwide However rigorously conductedepidemiologic studies with similar study methodolo-gies and taking into account all potential sources of

variation are needed to permit comparisons of SLEburden across the countries

Acknowledgements

I would like to thank Drs Mary Anthony and JessieSatia Department of Global Epidemiology AmgenInc for providing helpful insights and support on thisproject I would also like to thank Dr Debra ZackAssoc Medical Director Clinical Research AmgenInc for valuable advices

I am very thankful to Dr Susan Manzi University ofPittsburgh Pittsburgh Pennsylvania for the knowl-edge of epidemiology of systemic lupus erythematosusI was gaining under her guidance and support duringfive years of my PhD programme

I would also like to thank Dr Piette and otherresearchers in Europe for their help in summarizing theavailable data Their cooperation was invaluable to thisproject

References

1 Siegel M Lee SL The epidemiology of systemic lupus erythematosusSemin Arthritis Rheum 1973 3 1ndash54

2 Ramsey-Goldman R Manzi S Systemic lupus erythematosis Womenand Health Academic Press 2000 704

3 Hochberg MC The epidemiology of systemic lupus erythematosus InWallace D Hahn B eds Duboisrsquo Lupus Erythematosus Fifth editionWilliam amp Wilkins 1997 49ndash69

4 Siegel M Holley HL Lee SL Epidemiologic studies on systemic lupuserythematosus Comparative data for New York City and JeffersonCounty Alabama 1956ndash1965 Arthritis Rheum 1970 13 802ndash811

5 Fessel WJ Systemic lupus erythematosus in the community Incidenceprevalence outcome and first symptoms the high prevalence in blackwomen Arch Intern Med 1974 134 1027ndash1035

6 McCarty DJ Tull ES Moy CS Kwoh CK LaPorte RE Ascertainmentcorrected rates applications of capture-recapture methods Int JEpidemiol 1993 22 559ndash565

7 Siegel M Lee SL Widelock D et al The epidemiology of systemiclupus erythematosus preliminary results in New York City J ChronicDis 1962 15 131ndash140

8 Michet CJ Jr McKenna CH Elveback LR Kaslow RA Kurland LTEpidemiology of systemic lupus erythematosus and other connectivetissue diseases in Rochester Minnesota 1950 through 1979 Mayo ClinProc 1985 60 105ndash113

9 Hochberg MC The incidence of systemic lupus erythematosus inBaltimore Maryland 1970ndash1977 Arthritis Rheum 1985 28 80ndash86

10 McCarty DJ Manzi S Medsger TA Jr Ramsey-Goldman R LaPorteRE Kwoh CK Incidence of systemic lupus erythematosus Race andgender differences Arthritis Rheum 1995 38 1260ndash70

11 Naleway AL Davis ME Greenlee RT Wilson DA McCarty DJEpidemiology of systemic lupus erythematosus in rural WisconsinLupus 2005 14 862ndash866

12 Peschken CA Esdaile JM Systemic lupus erythematosus in NorthAmerican Indians a population based study J Rheumatol 2000 271884ndash1891

13 Amor B Bouchet H Delrieu F [National survey on reactive arthritis bythe French Society of Rheumatology] Rev Rhum Mal Osteoartic 198350 733ndash743

14 Piette J Papo T Amoura Z Godeau P Lupus erythemateux systemiqueTraite de Medecine Fourth edition Paris 2004

Epidemiology of SLEN Danchenko et al

317

Lupus

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638

Page 11: SLE Epidemiology Danchenko 2006(1)

Epidemiology of SLEN Danchenko et al

318

Lupus

15 Gudmundsson S Steinsson K Systemic lupus erythematosus in Iceland1975 through 1984 A nationwide epidemiological study in anunselected population J Rheumatol 1990 17 1162ndash1167

16 Lopez P Mozo L Gutierrez C Suarez A Epidemiology of systemiclupus erythematosus in a northern Spanish population gender and ageinfluence on immunological features Lupus 2003 12 860ndash865

17 Nived O Sturfelt G Wollheim F Systemic lupus erythematosus in anadult population in southern Sweden incidence prevalence and validityof ARA revised classification criteria Br J Rheumatol 1985 24147ndash154

18 Jonsson H Nived O Sturfelt G Silman A Estimating the incidence ofsystemic lupus erythematosus in a defined population using multiplesources of retrieval Br J Rheumatol 1990 29 185ndash188

19 Stahl-Hallengren C Jonsen A Nived O Sturfelt G Incidence studies ofsystemic lupus erythematosus in Southern Sweden increasing agedecreasing frequency of renal manifestations and good prognosis J Rheumatol 2000 27 685ndash691

20 Hopkinson ND Doherty M Powell RJ The prevalence and incidenceof systemic lupus erythematosus in Nottingham UK 1989ndash1990 Br J Rheumatol 1993 32 110ndash115

21 Hopkinson ND Doherty M Powell RJ Clinical features and race-specific incidenceprevalence rates of systemic lupus erythematosus in ageographically complete cohort of patients Ann Rheum Dis 1994 53675ndash680

22 Johnson AE Gordon C Palmer RG Bacon PA The prevalence andincidence of systemic lupus erythematosus in Birmingham EnglandRelationship to ethnicity and country of birth Arthritis Rheum 199538 551ndash558

23 Nightingale AL Farmer RD de Vries CS Incidence of clinicallydiagnosed systemic lupus erythematosus 1992ndash1998 using the UKGeneral Practice Research Database Pharmacoepidemiol Drug Saf2006 Epub ahead of print

24 Anstey NM Bastian I Dunckley H Currie BJ Systemic lupus erythe-matosus in Australian aborigines high prevalence morbidity andmortality Aust N Z J Med 1993 23 646ndash651

25 Iseki K Miyasato F Oura T Uehara H Nishime K Fukiyama K Anepidemiologic analysis of end-stage lupus nephritis Am J Kidney Dis1994 23 547ndash554

26 Deligny C Thomas L Dubreuil F et al [Systemic lupus erythematosus inMartinique an epidemiologic study] Rev Med Interne 2002 23 21ndash29

27 Ward MM Prevalence of physician-diagnosed systemic lupus erythemato-sus in the United States results from the third national health and nutritionexamination survey J Womens Health (Larchmt) 2004 13 713ndash718

28 Helve T Prevalence and mortality rates of systemic lupus erythematosusand causes of death in SLE patients in Finland Scand J Rheumatol1985 14 43ndash46

29 Zink A Listing J Klindworth C Zeidler H The national database of theGerman Collaborative Arthritis Centres I Structure aims and patientsAnn Rheum Dis 2001 60 199ndash206

30 Benucci M Del Rosso A Li Gobbi F Manfredi M Cerinic MMSalvarani C Systemic lupus erythematosus (SLE) in Italy anItalian prevalence study based on a two-step strategy in an area ofFlorence (Scandicci-Le Signe) Med Sci Monit 2005 11 CR420ndashCR425

31 Gourley IS Patterson CC Bell AL The prevalence of systemic lupuserythematosus in Northern Ireland Lupus 1997 6 399ndash403

32 EPISER Study The prevalence and impact of rheumatologic diseaseson the adult Spanish population Project of the Spanish Societyof Rheumatology From httpwwwseresproyectosindexhtml 2001

33 Grennan DM Bossingham D Systemic lupus erythematosus (SLE)different prevalences in different populations of Australian aboriginalsAust N Z J Med 1995 25 182ndash183

34 Segasothy M Phillips PA Systemic lupus erythematosus in Aboriginesand Caucasians in central Australia a comparative study Lupus 200110 439ndash444

35 Fukase M The epidemiology of systemic lupus erythematosus in JapanUniversity Park Press 1980

36 Nakae K A nationwide epidemiological survey on diffuse collagendiseases estimation of prevalence rate in Japan Elsevier 1987

37 Manzi S Epidemiology of systemic lupus erythematosus Am J ManagCare 2001 (16 Suppl) S474ndashS479

38 Mongey A-B Hess E The role of the environment in systemic lupuserythematosus and associated disorders In Wallace D Hahn B edsDuboisrsquo Lupus Erythematosus Williams amp Wilkins 1997 31ndash48

39 DrsquoCruz D Autoimmune diseases associated with drugs chemicals andenvironmental factors Toxicol Lett 2000 112ndash113 421ndash432

40 Walker S The importance of sex hormones in lupus In Wallace D HahnB eds DuboisrsquoLupus Erythematosus Williams amp Wilkins 1997 311ndash322

41 Cutolo M Sulli A Capellino S et al Sex hormones influence on theimmune system basic and clinical aspects in autoimmunity Lupus2004 13 635ndash638


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