Chapter 3 Use of screening for cervical cancer - IARC · Chapter 3 Use of screening for cervical cancer ... Organized screening programme 117-162 24/01/05 11:07 Page 117. 118

117

Chapter 3

Use of screening for cervical cancer

Cervical cancer screening startedwith the introduction of the Papani-colaou test into clinical practice. Inmany countries, this occurred as partof family-planning services, so thatthe target group was younger women.Because such services are frequentlynot well integrated with secondary lev-els of care, it was not always possibleto ensure adequate diagnosis andtreatment of women with a positivetest result. It has now become clearthat organized screening programmeshave a greater impact than oppor-tunistic screening because they havethe potential to achieve greater partic-ipation and this can improve equity ofaccess and the likelihood of reachingwomen at higher risk.

Cervical cancer screening com-prises various types of care or ser-vices, ranging from provision of thescreening test to diagnosis and treat-ment, as shown in Figure 46.

Implementation of a national pro-gramme requires that there be anational policy that defines the screen-ing age and interval and what methodof screening will be used, as well assufficient political and financial invest-ment. The major issues that have to beconsidered are:• The budget to run the programme• Training of health-care providers in:

the logic of the screening policy;

carrying out the screening test;patient counselling; and collectionand interpretation of monitoring data(participation and follow-up rates)

• Setting up equipment supply sys-tems for the clinic or health centre

• Ensuring that high-quality labora-tory services are available

• Establishing a referral pathway fortreatment of patients (which mayinvolve training of people at local leveland referral for more advanced casesneeding specialized treatment)

• Developing the capacity to offertreatment (for in situ disease, defin-itive treatment and palliative care)

• Setting up national monitoring sys-tems

• Education of the population toensure participation in the screen-ing programme

Overall, a screening programmeshould be an integrated system inwhich, as seamlessly as possible,women are recruited, screened,receive and understand the results, arereferred for treatment as required,return for repeat screening as deter-mined by the policy and become advo-cates for others to participate. Thismeans that all staff must know, under-stand and give the same message topatients, that services be accessible,equipped and welcoming, and thattransport and communications mecha-nisms with institutions for reading ofresults and treatment are functional. Inother words, a functional health systemmust operate with sufficient coverage,so that all women in the target grouphave satisfactory access to services.

The organization and financing ofthe overall health-care system of a

Delivery and uptake ofscreening

• an explicit policy with specified age categories, method and interval forscreening;

• a defined target population;

• a management team responsible for implementation;

• a health-care team for decisions and care;

• a quality assurance structure; and

• a method for identifying cancer occurrence in the target population

Organized screening programme

117-162 24/01/05 11:07 Page 117

118

IARC Handbooks of Cancer Prevention Volume 10: Cervix cancer screening

Ris

k as

sess

men

t

Age

Fam

ily

hist

ory

Exp

osur

ehi

stor

y

Life

styl

e

Scr

eeni

nghi

stor

y

Failu

re to

iden

tify

need

tosc

reen

or

coun

sel

Failu

re to

scre

enFa

ilure

durin

g fo

llow

-up

of a

bnor

-m

al r

esul

t

PO

TE

NT

IAL

FAIL

UR

ES

DU

RIN

G T

HE

PR

OC

ES

SE

S O

F C

AR

E

Failu

re d

urin

g fo

llow

-up

ofdi

agno

stic

or

trea

tmen

tpl

an

Failu

re to

follo

w-u

psu

rvei

l-la

nce

plan

Failu

re to

acce

ssca

re

Failu

re in

acce

ss to

care

Prim

ary

prev

en-

tion

failu

re

Failu

re in

dete

ctio

nFa

ilure

durin

gdi

agno

stic

evlu

atio

n

Failu

re o

ftre

atm

ent

Failu

re in

surv

eil-

lanc

e

Failu

re in

care

Prim

ary

prev

entio

n

Life

styl

e

Cou

nsel

ling

Che

mo-

prev

entio

n

Det

ectio

n

Scr

eeni

ng(a

sym

pto-

mat

ic)

App

ropr

iate

test

ing

(sym

pto-

mat

ic)

Dia

gnos

is

Imag

ing

Bio

psy

Rep

eat

exam

s

Labo

rato

ryte

sts

Oth

erap

prop

riate

proc

edur

es

Can

cer

orpr

ecur

sor

trea

tmen

t

Exc

isio

n

Sur

gery

Rad

iatio

n

Adj

uvan

tch

emo-

palli

atio

n

Rec

urre

nce

surv

eilla

nce

Test

ing

Fol

low

-up

care

Pal

liatio

n

Sur

vivo

r-sh

ipca

re

End

of

life

care

Pal

liativ

eca

re

Adv

ance

dca

re

Pla

nnin

g

Ber

eave

-m

ent

supp

ort

Ris

k st

atus

Clin

ical

stat

us

Fun

ctio

nal

stat

us

Qua

lity

oflif

e

Sat

isfa

ctio

n

Mor

talit

y

Qua

lity

ofde

ath

TY

PE

S O

F C

AR

EO

UT

CO

ME

S

Fig

ure

46

The

cer

vica

l can

cer

scre

enin

g pr

oces

sFr

om Z

apka

et

al.(

2003

)

117-162 24/01/05 11:07 Page 118

creo

119

country affects the potential effective-ness of a cervical screening pro-gramme, in particular if only part of theservice is free of charge or covered byinsurance (state or other). Furtherinfluences on programme effective-ness include the accessibility of ser-vices in poorly developed health-caresystems and the way that informationabout the programme is conveyed tothe target population.

EuropeAmong 38 European countries, 25 aremember states of the European Union,which includes all western Europeancountries except Iceland, Norway andSwitzerland, and (as of 2004) also sev-eral eastern European countries. TheEuropean Union includes 450 millioninhabitants. Most data on the use ofcervical cancer screening are availablefrom western European countries.Despite its relatively good level ofresources, Europe has rather fewnational well organized and docu-mented programmes. In mostEuropean countries, cervical cancerscreening started as an opportunisticactivity, performed on the initiative ofwomen or doctors. This opportunisticscreening activity is still predominant inmost European countries.

The European Union has recom-mended cervical cancer screeningsince the start of the Europe againstCancer programme in 1987. Europeanguidelines for quality assurance in cer-vical cancer screening were issued in1993 (Coleman et al., 1993). A Councilrecommendation in 2003 stressed theneed for the adoption of organizedscreening programmes with personalinvitations and quality assurance(Boyle et al., 2003; European Com-mission, 2003).

Table 46 lists European countriesthat have organized screening pro-grammes. Nationwide programmeswith personal invitation started in the1960s and 1970s in Iceland, Finland,

Sweden, Denmark and Latvia.However, participation in the Latvianprogramme decreased after 1987. Inthe United Kingdom, a computerizedcall/recall system was established in1988. This is a system that inviteswomen who are registered with a GP,keeps track of any follow-up investiga-tion and, if all is well, recalls thewoman for screening in three or fiveyears time. National coordination andquality assurance was adopted in1995. In the Netherlands, local pro-grammes existed from the 1970s and anational organized programme was setup in 1996. A national programmestarted in Norway in 1995. A pro-gramme for the Flemish Region ofBelgium including about 60% of thenational population started in 1994. InItaly, a few local programmes started inthe late 1980s or early 1990s, andnational guidelines recommendedorganized programmes on a regionalbasis in 1996. In 2002, 12 regions outof 20 had programmes targeting intotal about half of Italian women.Nationwide programmes were veryrecently started in Hungary andSlovenia. In the other countries listed,organized programmes are mainly pilotprogrammes and cover a small per-centage of the national population. InGermany, a committee is currentlyconsidering the possibilities for estab-lishing organized screening.

Screening testCytological (Pap smear) testing is generally used. A combination Ayre’sspatula and brush or an extended-tipspatula is commonly used for sam-pling, although in Germany mostsmears are reported to be taken with acotton-swab (Schenk & von Karsa,2000). In Germany, a gynaecologicalexamination is also a mandatory partof screening, while colposcopy is left tothe discretion of the physician (Schenk& von Karsa, 2000). Colposcopy,although not recommended, is still

quite common in opportunistic screen-ing in Italy (Segnan et al., 2000).

Most smears are fixed on glass bythe smear-taker. However, in theUnited Kingdom (National Institute forClinical Excellence, 2003) andDenmark (Hoelund, 2003; Patolo-giafdelingen, Hvidovre Hospital, 2003),the screening programmes are chang-ing to liquid-based cytology. Thesmears are read by cytotechnicians. InFinland, a trial of the use of neural-net-work-assisted screening (Papnet) is inprogress (Nieminen et al., 2003). Since1999, the largest screening pro-gramme in Denmark has used auto-mated reading (Focal Point; Patolo-giafdelingen, Hvidovre Hospital, 2003).In Denmark, national guidelines havebeen issued on the use of HPV testingin assessment of women with atypicalcytological results (Kjær et al., 2002a).Trials on the use of HPV testing for pri-mary screening are under way inFinland (Nieminen et al., 2003), Italy(Ronco et al., 2004), the Netherlands(Bulkmans et al., 2004), Sweden(Dillner, 2000) and the United Kingdom(Cuzick et al., 2003).

Screening interval and ageEuropean guidelines (EuropeanCommission, 2003) recommend three-to five-year screening intervals,depending on the resources available,but there is wide variation in actual rec-ommendations at the national levelacross Europe. The most commonlyrecommended interval between nor-mal cytological tests is three years(Table 47). Five-year intervals are rec-ommended in Finland, Ireland and theNetherlands. A three- to five-year inter-val used to be recommended in theUnited Kingdom, but recently a three-year interval was recommended forwomen aged 25–49 and five years forwomen 50–64 years old.These recom-mendations were based on an audit ofscreening histories (Sasieni et al.,2003). The recommended interval is


117-162 24/01/05 11:07 Page 119

120


g

Country Population included in organized cervical Start Referencesscreening

Austria Regional programme in Vorarlberg (120 000 1970 Breitenecker et al. (2000)women, 4% of Austrian women 20+)

Belgium Flemish Region (about 60% of Belgian population) 1994 Arbyn & Van Oyen (2000)

Denmark Regional programmes 1962 first pilot. 1969 local pro- Lynge (1984); Lynge etNationwide grammes and opportunistic smears. al. (1996)

1996 nationwide programmes

Estonia Pilot programme (Tallinn, Tartu, Narva), invitation 2003 T. Aareleid (2003)only via media (personal communication)

Finland National programme 1961 first pilot. Kauraniemi (1969), 1970 nationwide. Timonen & Pyörälä (1977)

France Pilot programmes in 4 departments: Bas-Rhin, 1990 (Isère) Schaffer et al. (2000)Isère and Doubs (500 000 women) and Martinique 1991 (Martinique)

1993–94 (Bas-Rhin and Doubs)

Greece Pilot programmes in Ormylia (< 20 000 women) Linos & Riza (2000)and Ilia and Messinia Region

Hungary Nationwide 2003 Döbrössy & Bodo (per-sonal communication)

Iceland National programme 1964 Reykjavik Johannesson et al. (1982)1969 nationwide (1982)

Ireland Pilot programme in Mid Western Health Board 2000 O’Neill (2000)Region (67 000 women)

Italy Regional programmes in 12 of 20 regions Most after 1996 (where 13% of Segnan et al. (2000);targeting 52% of women aged 25–64 population targeted). Ronco et al. (2003a)

Latvia National programme 1972. After 1987 the programme V. Grjunberg (personalgradually disappeared due to communication)economic and political factors

Netherlands Regional programmesNationwide with national co-ordination and 1970 local programmes and Van Ballegooijen &policy opportunistic screening Hermens (2000)

1996 national programme

Norway National programme 1959 first pilot Messelt & Höeg (1967);National coordination and policy 1980s - 1990s many opportunistic Nygård et al. (2002)

smears1995 national programme

Portugal Regional programme in central Portugal (300 000 1990 Real et al. (2000)women)

Table 46. Organized programmes in Europe

117-162 24/01/05 11:07 Page 120

creo

121


one year in Germany, Austria andLuxembourg.

The European guidelines recom-mend screening for cervical abnormal-ities "starting at the latest by the age of30 and definitely not before the age of20" (European Commission, 2003). Inthe updated European Code againstCancer, this has been phrased as"Women from 25 years of age shouldparticipate in cervical cancer screen-ing" (Boyle et al., 2003). However, widevariation is also seen here in what isrecommended at the national level.Most European countries recommendscreening from age 25 up to age 64 or65. The organized programmes inFinland and the Netherlands targetwomen aged 30 to 60 years. InGermany and Austria, women aged 20or older are eligible for annual cytology,and in Luxembourg those aged 15 orolder are eligible.

The combination of differences inthe recommended age group and inscreening interval results in dramaticdifferences in the number of recom-mended lifetime smears, from 6–8 inFinland, Ireland and the Netherlands,12–18 in most European countries, up

to 50 or more in Austria, Germany andLuxembourg.

InvitationsA call/recall system based on personalinvitations is considered to be a keyelement of an organized programme inEurope. For this purpose, an accuratelist of the target population with namesand addresses is needed. Sources ofsuch lists vary between countries andinclude population registries, healthservice registers, general practitioners’(GPs) medical files, electoral registersand others.

Usually, only women who are notregistered as having had a cytologicaltest within the recommended intervalare invited. This ‘integrated’ approachis applied with the intention of savingresources by avoiding re-screening ofrecently tested women (Coleman etal., 1993). It requires comprehensiveregistration of cytological testing,including opportunistic tests, at thepopulation level. In some Italian pro-grammes, all women are invited inde-pendently of their screening history(Ronco et al., 1998). This approachmay be used if cytology registration is

incomplete or if it is hoped to modifythe spontaneous frequency of screen-ing. In Finland, the organized pro-gramme invites all women (Nieminenet al., 1999); until the 1990s, all smearsfrom the organized programme wereanalysed in laboratories run by theCancer Society of Finland (Nieminenet al., 2002).

The nature of the invitation mayvary from a suggestion to contact asmear-taker to a pre-assignment of amodifiable place and date. In random-ized trials (Wilson & Leeming, 1987;Pierce et al., 1989; Segnan et al.,1998), compliance rates were signifi-cantly higher with letters offering pre-allocated appointments than withopen-ended invitations.

Outside organized programmes,no systematic active personal invita-tion is sent. In Germany until 1995,statutory insurers used to issue yearlyvouchers for reimbursement to all eligi-ble women, which also served as areminder.

Information campaigns via massmedia are implemented both in areascovered by invitational programmesand in areas not covered.

Country Population included in organized cervical Start Referencesscreening

Romania Regional Cluji county (200 000 women, 3% of 2002 Suteu et al. (2003)Romanian women 25–64)

Slovenia Nationwide 2003 Primic Zakelj (personal communication)

Spain Regional programme in Castilla y Leon 1986 Fernandez Calvo et al.(2000)

Sweden Regional programmes 1964 first country Ahlgren et al. (1969),Nationwide 1965 national plan Pettersson et al. (1986)

1973 nationwide (except one city)

United Regional programmes 1988 computerized call/recal Patnick (2000)Kingdom Nationwide with national co-ordination and policy 1995 national co-ordination and

quality assurance

Table 46 (contd)

117-162 24/01/05 11:07 Page 121

creo

122


Country Age group Interval between normal Lifetime number of Referencestests (years) recommended smears

Austria 20+ 1 50 (to age 70) Breitenecker et al. (2000)

Belgium 25–64 3 14 Arbyn & Van Oyen (2000)

Denmark 23–59 3 13 Sundhedsstyrelsen (1986)

Finland 30–60 5 6 Anttila & Nieminen (2000)

France 25–65 3 14 Schaffer et al. (2000)

Germany 20+ 1 50 (to age 70) Schenk & von Karsa (2000)

Greece 25–64 (in pilot) 3 after 2 negative smears 15 (Omylia) Riza et al. (2000)(Omylia), 2 (Ilia/Messinia) 21 (Ilia/Messinia)

Hungary 25–65 (previously 18+) 3 after 2 negative smears 15 Döbrössy & Bodo, (from 2003, before 1) (personal communication)

Iceland 25–59 (1964–69) 2–3 18–26 Sigurdsson (1999)25–69 (1970–87)20–69 (1988–)

Ireland 25–60 (in pilot) 5 8 O´Neill (2000)

Italy 25–64 3 14 Segnan et al. (2000)

Luxembourg 15+ 1 55 (to age 70) Scheiden et al. (2000)

Netherlands 30–60 5 (3 until 1996) 6 Van Ballegooijen &(35–53 until 1996) Hermens (2000)

Norway 25–69 3 15 Nygård et al. (2002)

Portugal 20–64 3 after 2 negative smears 17 Real et al. (2000)

Romania 25–65 3 14 Suteu et al. (2003)

Slovenia 20–64 3 after 2 negative smears 17 Primic Zakelj (personal(formerly 20+) (from 2003, before 1) communication)

Spain 35–64, below 35 if 5 after 2 negative smears, but 14 (age 25–65, 3 year) Ascunze Elizaga et al.with risk factors. Most 3 in organized programme (1993); AETS (2002);regions women aged Fernandez Calvo et al.25–65 (2000)

Sweden 30–49 (1965–85) 4–5 (1965–85) 14 Mählck et al. (1994), 20–59 (1985–) 3 (1985–) Dillner (2000)

United Kingdom 20 (or 25 from 2004) 3 for age 25–49 12 Patnick (2000)–64 5 for age 50–64 NHS (2003a)

(From 2004, before 3–5)

Table 47. National recommendations in Europe on age group and screening interval

117-162 24/01/05 11:07 Page 122

creo

GPs frequently act as advisers both inthe presence and in the absence of per-sonal invitations. Attendance followinginvitation was higher with letters signedby the GP than with letters signed byprogramme staff (Segnan et al., 1998;Palm et al., 1993). In the UnitedKingdom, GPs are paid for screeningbased on the coverage among theirpatients.This was introduced to increasecoverage (Rudiman et al., 1995).

The facilities for testing and the pro-fessionals involved vary widelybetween countries and between orga-nized and opportunistic activity (Table48). In the Netherlands and the UnitedKingdom, smears are most commonlytaken by GPs or their assistants, whilegynaecologists play a major role inmost other countries, especially inopportunistic screening. In the Finnishorganized programme, the smearswere taken at maternity and childhealth centres invariably by publichealth nurses and midwives. In theItalian organized programmes, smearsare most often taken by midwives infamily-planning clinics, and midwivesalso participate in Finland and Sweden.

Coverage and participationTable 49 shows published estimates ofparticipation by cervical screening atthe national level. This measure hasbeen provided at a national level onlyin Finland, Iceland, Norway, Englandand the Netherlands. For France, anestimate has been made on the basisof individual linkage on a sample ofwomen, using insurance data. For anumber of other countries, estimatesare based on interviews, with the pos-sibility of recall bias, although somekind of validation was frequently per-formed. Comparability of the findings isalso limited by differences in the agegroups considered, and by the fact thathysterectomized women were exclu-ded in some case (e.g., England) butnot in others (frequently not men-tioned).

Participation over 80% is seen inEngland and Iceland and in rural areasof Sweden and Denmark. Participationof 70–80% is found in the Flemish partof Belgium, Finland, the Netherlands,Norway and Copenhagen, Denmark.Participation is around or below 60% inAustria, France, Italy and Spain. InGermany, where women are eligiblefor yearly screening, the number oftests in 1996 was about 50% of thenumber of women (Schenck & vonKarsa, 2000). A three-year participa-tion of 65% was estimated for theEuropean Union (women aged 25–54years) on the basis of an interview sur-vey in 1991 (Coleman et al., 1993).

Participation also varies betweenareas within countries. This variationwas quite low in England, with partici-pation ranging from 76% in London to85% in the East Midlands in 2002–03(NHS, 2003a). However, in Spain, thereported participation (women 40–70years) ranged from 25% in Castilla-LaMancha to 61% in Madrid (AETS,2002). In Italy, there was a strong gra-dient in participation from northern-central (53–61%) to southern Italy(26%) (Ronco et al., 2003a; Mancini etal., 2004). In France, the annual num-ber of tests ranged from 17 to 39 per100 women, with a north–south andwest–east increasing trend (Rousseauet al., 2002).

There is also a difference in activityby age, with a common pattern oflower activity at the highest ages. InEngland in 2002–03, participation wasover 80% among women aged 30–59years, 74% among those aged 25–29,and 77% among those aged 60–64(NHS, 2003a). In Spain, participationdecreased from 61% in the 40–45-yearage group to 31% in the 61–65-yearage group (AETS, 2002). In Flanders(Belgium), participation remained highup to 40 years of age, and decreasedthereafter (Arbyn et al., 1997). In Italy,it was 27% at age 25–34, over 50% atage 35–44, and 43% at age 55–64

(Mancini et al., 2004). In France, therate of activity increased slightly up toage 50–54, and then decreasedrapidly (Rousseau et al., 2002).

In England, the introduction of thecomputerized call/recall system in1988 and the target payments for GPsin 1990 increased the five-year partici-pation for women aged 25–64 yearsfrom 40% in 1988 (Havelock et al.,1988; Shroff et al., 1988; Robertson etal., 1989b) to persistently over 80%between 1992 and 2003 (NHS,2003b). In Norway, opportunisticscreening has been very common, butwhen organized screening with per-sonal invitations was introduced in1995 the participation increased from65% to 71% (Nygård et al. 2002). InFrance, a three-year participation of69% was found in the organized pro-gramme of Bas-Rhin after four years ofactivity (Fender et al., 2000), com-pared with the national estimate of54% (Rousseau et al., 2002). InCastilla y Leon, a region of Spain withan organized programme, the esti-mated three-year participation of 41%was similar to the 44% for Spain(AETS, 2002). In Italy, national partici-pation data for 1999–2000 were onlymarginally influenced by the recentlystarted organized programmes,although in one of the latter, the three-year participation was estimated to be74%, compared with 43% before(Ronco et al., 1997). A strong reduc-tion in variability by age, education andmarital status was also observed.

Excess use of Pap testingPap testing is unevenly distributedamong women in many countries, withmany women not screened at all or notscreened within the recommendedinterval, and other women screenedmore frequently than recommended.

In general, over-testing is assumedto be high in opportunistic screening.The level of testing is high in Germany,where women are eligible for yearly

123


117-162 27/01/05 15:49 Page 123

124


Country Smear-taker Communication of cytology results

Normal Suspicious

Austria Gynaecologists Mail or phone to the smear taker Mail or phone to the smear taker

Belgium Gynaecologists/GPs Report to the smear taker Report to the smear taker

Denmark GPs Mostly: woman asked to call GP As for normal or GP contact woman

England GPs or general practice nurses Report to the smear taker Report to the smear taker

Finland Midwives or public health nurses Letter to woman Phone and always byletter with fixed appointment

France Gynaecologists/GPs Not specified Not specified

Germany Office-based gynaecologists (90%) By the smear taker Mail or phone by the smear and GPs (10%) taker

Greece Organized: Gynaecologists (Ormylia) Organized: letter directly to the women Organized: phone or gynaecologists, trained rural doctors personal meeting withand midwives (Ilia/Messinia) screening physician or Opportunistic: gynaecologists (Riza house callet al., 2000)

Iceland Gynaecologists/GPs (Sigurdsson et al., Not specified Not specified1991)

Ireland GPs, family planning and community Letter to woman Advised to contact smear clinics, hospitals taker

Italy Organized: mainly midwives in family Organized: mostly Organized: letter or phoneplanning clinics letter directly to the woman call to womanOpportunistic: mainly gynaecologists

Luxembourg GPs and/or gynaecologists Not specified Not specified

Netherlands GPs and their practice assistants Via the GP Via the GP

Norway Primary physicians Not specified Not specified(Krogh & Malterud, 1995)

Portugal GPs (organized) Organized: letter via the GP Organized: letter via the GP

Spain Organized: family doctors Organized: letter via the primary Organized: by the primaryOpportunistic: mainly gynaecologists care physician care physican(>80%) and family clinics of primary care centres (about 20%) (AETS, 2000)

Sweden Nurse-midwives (Sarkadi et al., 2004) Letter to woman Referral to gynaecological out-patient clinic for test result

Modified from Linos & Riza (2000)

Table 48. Staff involved in taking smears and methods of communicating results in European countries

117-162 27/01/05 15:52 Page 124

creo

screening; the number of smears in1996 was about 50% of the number ofwomen in the target population. In Italy,52% of screened women reported hav-ing a test every year (Mancini et al.,2004).

Over-testing in countries andregions with organized screening pro-grammes depends on the organizationof the programme. The total level is

often high in countries where the orga-nized programme runs independentlyof opportunistic activity. In Finland, 200 000 smears are taken annuallywithin the organized programme and400 000 smears are taken outside(Finnish Cancer Registry, 2003). In anItalian programme in which all womenare invited independently of previoustesting, 20–25% of those who joined

the programme also had tests outsidethe protocol (Ronco et al., 1997).Sweden, where there were regional dif-ferences in the organizational set-up,over-testing was heavy in 1994, with292 000 smears taken in the organizedprogramme and 656 000 taken outside.Opportunistic testing was free,whereas a small fee had to be paid forthe organized screening (Dillner,

125


Country Estimated coveragea Source Reference

Austria Lifetime: Interviews with sample of women Vutuc et al. (1999)60% 2+ smears (reported in Breitenecker10% 1 smear et al., 2000)30% never

Belgium 74% in 3 years, Flemish region, National health interview survey Arbyn & Van Oyen (2000)64% in 3 years, Walloon region

Denmark 85% County of Funen Register linkage Hoelund (2003);73% Copenhagen Patologiafdelingen,

Hvidovre Hospital (2003)

England 81% in 5 years, 71% in 3 years, 2003 Register linkage NHS (2003b)

Finland 70% (organized screening) Register-based national health Finnish Cancer Registry 93% (all smears) interview survey (2003)

France 54% in 3 years, 1998–2000 Registration of smears in two health Rousseau et al. (2002)insurance systems and linkage for sample of 9374 women

Germany 42–47% in 1997 for women aged Personal interviews Kahl et al. (1999)25–54

Iceland 83% in 1990–92 Register linkage Sigurdsson (1999)

Italy 50% reporting usual frequency of National periodic survey on health Mancini et al. (2004)3 years, 1999–2000 (44 433 women)

Netherlands About 80% in 2 years, 1996–97 Register linkage Van Ballegooijen & Hermens(2000)

Norway 71% in 1998–2000 Register linkage Nygård et al. (2002)

Spain 44% reporting one or more tests in 3 Personal interview. random sample AETS (2002)years for preventive reasons (2409 women)

Sweden >80% northern Sweden, Register linkage Dillner (2000)20–30% Malmö,50–70% most common

a Proportion of the target population having had at least one test in the defined interval

Table 49. Participation estimates at the national level in European countries

117-162 24/01/05 11:07 Page 125

creo

2000). Since a government reportexamined this issue (Socialstyrelsen,1998), all counties have changed tothe ‘integrated approach’ (see above)for invitations.

There can be a lower level of over-testing in integrated programmes,although this is not always the case. InEngland, GPs are paid based on cov-erage of their patients and not on thenumber of smears taken. Data on over-testing are not published, but the levelseems to be small. In 2002–03, a totalof 4.1 million smears were taken.There were 13.8 million women in thetarget 25–64-year age group, of whom66.1% were screened within the lastthree years, giving 3.0 million annualsmears used for screening. An addi-tional 1.0 million women were recalledmore often than every third year forsurveillance etc. This leaves very fewsmears corresponding to possible‘over-use’ (NHS, 2003b). In Norway,the average number of smears perwoman aged 25–69 in a three-yearperiod decreased from 1.68 to 1.52when an integrated programme wasintroduced, at the same time increas-ing participation (Nygård et al., 2002).Denmark runs integrated programmes,and the level of over-testing was 28%in Copenhagen in 1999–2001(Patologiafdelingen, Hvidovre Hospital,2003), but only 4% in Fyn in 1999(Hoelund, 2003). In the Netherlands,out of about one million smears takenin 1996, 450 000 were in the organizedprogramme, 300 000 were other ‘pri-mary’ smears, and 250 000 ‘secondary’(follow-up or repeat) smears (vanBallegooijen & Hermens, 2000). InBas-Rhin, France, 63% of women hada second test before the recom-mended interval (Fender et al., 2000).

The difficulties in limiting over-test-ing are illustrated by the fact that27–29% of female primary physiciansin Norway in 1995 recommendedscreening more often that the threeyears stated in the national guidelines

(Krohg & Malterud 1995). In Stockholm,a common practice among privategynaecologists seems to be to have anannual appointment with private patientsand a Pap test is often part of the con-sultation (Sarkadi et al., 2004).

Cytological interpretation and man-agement of abnormal resultsThere is no unique European systemof classification. National classificationsystems are applied in theNetherlands and in the UnitedKingdom. In Germany (where stan-dardized national reporting formsexist) and in Austria, the Munich clas-sification is used (Schenk & von Karsa,2000; Breitenecker et al., 2000). InItaly, the Bethesda system is widelyapplied, although with many localadaptations (Ronco et al., 1998). Astandard reporting protocol, related tothe Bethesda system, is applied in theFlemish Region of Belgium (Arbyn &Van Oyen, 2000). Tables of ‘equivalentterminology’ between different classifi-cations have been published in theEuropean Guidelines (Coleman et al.,1993). Data on comparability of the cri-teria actually used in different coun-tries are limited. In a study of agree-ment in cytological interpretation con-ducted in six Italian laboratories andone Danish using the Bethesda 1991classification, agreement between theDanish and the Italian results was sim-ilar to that within Italians (Ronco et al.,2003b).

Table 48 summarizes the methodsof communication of test results to thewoman. In some cases the report issent directly to the woman (e.g., Italianorganized programmes), while morefrequently the laboratory reports to thesmear-taker. The practice of sendingnegative test results directly to thewomen was abandoned in one Danishcounty after a survey showed thatwomen preferred to have the resultsreported via their GP (Andreasen etal., 1998). In most countries, the deci-

sion on the action to be taken followinga non-negative smear is left to thesmear-taker (Belgium, Germany),while in others (England) the recom-mendation is given by the laboratoryand it is the responsibility of the smear-taker to ensure that the womanreceives the result.

Criteria for management of womenbased on cytology results vary widely,also depending on the cost and avail-ability of colposcopy facilities. Nationalguidelines with implementation poli-cies are applied in England and theNetherlands. National guidelines forthe management of abnormal smearsexist in France (ANAES, 1998), Austria(stated in Breitenecker et al., 2000)and Germany (Bundesärtzekammer,1994; Schenk & von Karsa, 2000). InItaly the national guidelines recom-mend development of detailed localprotocols for the management ofabnormal results (Ronco et al., 1998).Recommendations have also beenprepared in the Flemish programme(Arbyn & Van Oyen, 2000).

In the United Kingdom, womenwith moderate and severe dyskaryosis(equivalent to HSIL in the Bethesdasystem) are referred for colposcopy,while those with mild dyskaryosis(Bethesda: LSIL) and borderline cytol-ogy (Bethesda: ASCUS) are advisedto repeat testing and referred for col-poscopy only in case of persistence,although some of these cases are infact directly referred for colposcopy.The same policy is applied in Belgiumand the Netherlands. In France, achoice between colposcopy andrepeat cytology is left for borderlineand low-grade lesions. In Portugal,women with ASCUS are advised toundergo repeat testing, while thosewith LSIL or worse are referred for col-poscopy. In Italy, most organized pro-grammes refer all women with ASCUSor more severe cytology for col-poscopy, although some programmesperform a repeat cytology in the case

126


117-162 27/01/05 15:53 Page 126

of ASCUS (but not LSIL). Referral of allASCUS-positive women for col-poscopy is also the usual practice inopportunistic activity in Italy. In Finland,treatment is given to women with low-grade dysplasia, whereas in Norway amore conservative stance is taken andtreatment is given only after threerepeated low-grade abnormal results(Nygård et al. 2002). In Denmark, fol-low-up of women with atypia variesfrom direct referral to colposcopy to arepeat test within 6–12 months(Bigaard et al., 2000).

An issue relevant to screeningeffectiveness is that all women need-ing further action (repeat or col-poscopy) should actually have it. Fail-safe methods are implemented in mostorganized programmes. Monitoring offollow-up is applied in French orga-nized programmes (Schaffer et al.,2000). In the Netherlands, it is theresponsibility of the GP to inform thewoman of the results and to ensurecompletion of follow-up. It has beenplanned that laboratories should pro-vide GPs with lists of women withincomplete follow-up (van Ballegooijen& Hermens, 2000). A similar system isimplemented in Denmark (Patologi-afdelingen, Hvidovre Hospital, 2003).In Finland and in most Italian orga-nized programmes, women needingcolposcopy receive a pre-arrangedappointment to a reference centre andare reminded in case of default.

Quality assuranceSeveral factors contribute to the impactof cervical screening, including cover-age of the targeted population, theactual participation, the quality ofsmear-taking and interpretation, the fol-low-up of women with abnormalresults, the quality of diagnostic proce-dures and initial treatment. Several ini-tiatives have been taken to develop andpromote quality assurance systems,and guidelines have been publishedboth at European and national levels.

Quality assurance addresses thefollowing issues: rules concerningstructural requirements (e.g., numberof smears interpreted, qualification andtraining of staff), procedures to be fol-lowed (e.g., methods of smear prepa-ration, re-interpretation of smears,including guidelines for the manage-ment of women); and monitoring ofperformance for taking action inresponse to such information.

National guidelines concerningcytological interpretation exist inAustria (reported in Breitenecker et al.,2000), England (Johnson & Patnick,2000), France (Marsan & Cochand-Priollet, 1993), Germany (Bundesärz-tekammer, 1994; reported in Schenk &von Karsa, 2000) and the Netherlands(van Ballegooijen & Hermens, 2000).Guidelines for quality assurance in col-poscopy were published for England(Luesley,1996) and the Netherlands(Helmerhorst & Wijnen, 1998). Poorcompliance with guidelines in Austriahas been reported (Breitenecker et al.,2000).

Rules or guidelines concerning thenumber of smears to be read exist inmany countries both as a maximumnumber per cytologist (Austria,England, Germany, the Netherlands)and as a minimum (Denmark,England, Italy). Laboratories varygreatly in size and in some countriesmany are small. In the Flemish Regionof Belgium, a total of 620 000 smearswere processed in 1993 in over 100 lab-oratories (Arbyn & van Oyen, 2000). InAustria, the annual number of smearsper laboratory varied from 3000 to 150 000, with an average of 25 000(Breitenecker et al., 2000). In Germany,an annual total of 17 000 000 smearsare interpreted by some 2000 laborato-ries (Schenk & von Karsa, 2000). In theNetherlands, the annual number variesfrom 5000 to over 50 000 per laboratory(van Ballegoijen & Hermens, 2000).Among Italian laboratories involved in organized programmes in 1997, the

workload varied from 3000 to over 50 000 smears per year (Ronco et al.,1998).

Proficiency testing for cytologicalinterpretation is compulsory for all lab-oratory staff in the United Kingdom,and for cytopathologists (but not forcytotechnicians) in Germany. In manyother countries, proficiency testing isencouraged but not compulsory.

Re-screening of a sample of nega-tive smears, which is mandatory in theUSA, is not compulsory in mostEuropean countries. A rapid review(Faraker & Boxer, 1996) of all negativesmears is mandatory in England(NHSCSP, 2000) and this policy is sup-ported by a meta-analysis (Arbyn &Schenk, 2000). Suspicious smears areusually reviewed by a supervisor. InItaly, where quality assurance pro-grammes are decided on a regionalbasis, circulation and discussion ofsets of smears is becoming widelyapplied on both a local and nationalbasis in order to improve consistencybetween laboratories (Branca et al.,1998; Ronco et al., 2003b).

Data registrationMonitoring of screening performancerequires comprehensive registration ofall events related to screening and therecovery and linkage of the data at anindividual level in order to allow recon-struction of the screening histories andtheir results. European guidelines(Coleman et al., 1993) recommendcomprehensive registration of all cyto-logical and histological findings.

Registration of events related toscreening, particularly cytologicalresults, exists in the organized pro-grammes listed in Table 46 and in otherareas. Individual linkage of data takesplace in Denmark, Finland, Iceland,the Netherlands, Norway, Sweden, theUnited Kingdom, and in the organizedprogrammes in Italy. In Germany, individual linkage is prohibited due toregulations on privacy.

127


117-162 24/01/05 11:07 Page 127

Where results are registered, thelevel of comprehensiveness varies.Comprehensive computerized registra-tion of all tests is performed in theNetherlands through a national data-base covering all pathology units (thePALGA system). In the United Kingdom,registration of cytology is comprehen-sive (data are registered locally and for-warded periodically for central analysis)and highly complete, leaving out only asmall percentage of privately per-formed tests.

Screening registers with compre-hensive registration of cytology havealso been set up in the French orga-nized programmes through agree-ments with the involved parties (labo-ratories, GPs, gynaecologists) and inthe Flemish Region in Belgium. In thelatter case, personal identificationcodes are encrypted. In other areas,however, complete registration only ofcytology and histology taken within theorganized programme is possible,while registration of opportunistic testresults and of histology performed outside the reference centres is incom-plete or absent. This is the case forsome Italian programmes, where com-pleteness also depends on the numberof laboratories in the area and on theamount of private activity.

In France, outside organized pro-grammes, computerized registration ofcytological testing is performed at thenational level by the social securitysystem, although mainly for adminis-trative purposes. Individual linkage hasbeen performed experimentally on asample of women in order to estimateparticipation (Rousseau et al., 2002).In Germany, cytology reports are registered on paper, transmitted toregional insurance billing offices, andfinally registered on a central comput-erized database. Only results of initiallyabnormal test results and of a randomsample of normal ones are registered.Follow-up and histology data after aninitially abnormal result are reported

on the same sheet. However, problemsof quality and completeness have beenreported. No special registration of col-poscopies or biopsies exists (Schenk &von Karsa, 2000). Colposcopies per-formed in referral centres are recordedby most Italian programmes and par-tially in England.

Performance indicatorsThe European Guidelines proposed anumber of standard tabulations andparameters (coverage, interval toreporting, proportion of unsatisfactorysmears, treatment compliance, sensi-tivity and specificity, distribution ofinvasive cancers, interval cancers) for‘short-term monitoring’ of pro-grammes (Coleman et al., 1993). InEngland, a national system of mea-surements and of reference stan-dards for them, each related to anobjective, was adopted (NHSCSP,1996). Annual reports, produced inboth a synthetic (NHS, 2003b) anddetailed (NHS, 2003a) format, areavailable on the NHS screening website(http://www.cancerscreening.nhs.uk). In Italy, a system of process indi-cators (partly with reference stan-dards) has been published (Ronco etal., 1999) and included in officialguidelines. Annual surveys of theactivity of organized screening pro-grammes have been conducted from1998 and a report published annuallyfrom 2002 (Ronco et al., 2002). In theNetherlands, regular reports are pro-duced on the outcome of the orga-nized programme. Regular reportshave been published from theIcelandic (Sigurdsson, 1995),Norwegian (Nygård et al., 2002) andFinnish (Finnish Cancer Registry,2003) programmes. Process mea-sures have been published for French organized programmes (Fender et al.,2000; Schaffer et al., 2000) and thedistribution of cytology results for theFlemish Region has been reported(Arbyn & van Oyen, 2000).

Participation is a key indicator andhas been described in a previous sec-tion. Another important indicator is theproportion of unsatisfactory cytologicaltests. The proportion is high inEngland, at 9.4% of smears (NHS,2003b), plausibly as a result of strictcriteria for adequacy. In Norway, 4.7%of smears were considered unsatisfac-tory in 1998–2000 (Nygård et al.,2002). The Netherlands has 1% (vanBallegooijen & Hermens, 2000),Finland 0.004% (Finnish CancerRegistry, 2003), Flemish programmes0.6–1.0% (Arbyn & van Oyen, 2000),the French programmes 0.12–2%(Schaffer et al., 2000) and the Italianorganized programmes 3.8% (Roncoet al., 2003a). In Copenhagen in1999–2001, 2.5% of smears wereunsatisfactory, but 8.5% were normalwithout endocervical cells. In the lattercase, the GP decides whether testingshould be repeated (Patologiafdelingen,Hvidovre Hospital, 2003). In Funen in1999, 7.5% of smears were unsatisfac-tory, including smears without endo-cervical cells. This percentagedecreased to 2.5% after introduction ofliquid-based cytology (Hoelund, 2003).In many organized programmes,reports on unsatisfactory smears aresent to smear-takers.

A measure of the proportion ofwomen referred for further action(repeat cytology or colposcopy) is obvi-ously useful as an indication of thehuman and economic cost of screen-ing. More frequently, the proportion ofabnormal cytological results (or ofscreened women with abnormalresults) is reported. However, this doesnot translate immediately to referral orrepeat action, both because guidelinesleave choice for some diagnoses (e.g.,LSIL/ASCUS in France) and becauseof referral for clinical reasons. Cyto-his-tological correlation data are frequentlyreported, sometimes in terms of positive predictive value. However,comparison is difficult because of the

128


117-162 24/01/05 11:07 Page 128

variability of criteria for inclusion, bothin relation to the cytological diagnosesconsidered (frequently only certaincytological categories among those ofreferred women are included) and tothe presence of histology (in somecases but not others, women exam-ined colposcopically but without histol-ogy are included, assuming that nobiopsy was done because no suspectarea was identified at colposcopy). It isnevertheless clear that the proportionof screened women immediatelyreferred for colposcopy varies betweencountries from 0.8% in Finland(Finnish Cancer Registry, 2003) to2.9% in Italian organized programmes(Ronco et al., 2003a).

Some measure of completeness offollow-up is also reported or can becomputed from available data,although sometimes the data relate tocolposcopy only (Italy) and sometimesto either colposcopy or repeat testing(France). Statistics on the timebetween referral and attendance forcolposcopy are computed in England.

United States and CanadaThe type of organization of cervicalcancer screening services in the USAand Canada covers the range fromopportunistic screening, with accessbased on availability of individual orthird-party financial resources, to orga-nized screening at the local, regionaland national level funded by work-based groups or government agencies.

Organization and financingUnited StatesIn the USA, cervical cancer screeningis provided in various settings: privatepractices, public health clinics, com-munity health centres, sexually trans-mitted disease clinics, family planningclinics and prenatal clinics. Thisscreening is offered on an entirelyopportunistic basis. Financing for cervical cancer screening and other

preventive services depends on awoman’s personal resources and/orhealth insurance coverage. Most insur-ance plans cover cervical cancerscreening services, but if follow-uptesting is necessary, there may becover only for part of the expenses.

In the Government-sponsoredMedicare and Medicaid, the propor-tions paid by individuals, if any, are lim-ited by law and are often related toincome levels. Medicare provides reim-bursement for screening services ofindividuals aged 65 years or more andsome younger disabled individuals.Medicaid, administered by states, pro-vides reimbursement for very low-income families with highly limitedresources. Persons covered by sometype of insurance, public or private,represent a median of 84% of the statepopulations (Mansley et al., 2002) andthere is some geographical variation inthe availability of insurance. For exam-ple, the State of Wisconsin has cover-age for 91% of its constituentswhereas the State of Texas has cover-age for only 76% of its residents(Mansley et al., 2002). Populationswith lower socioeconomic status aremore likely to have no or insufficientinsurance coverage (Henson et al.,1996).

Special programmes like theNational Breast and Cervical CancerEarly Detection Program (NBCCEDP),administered by the Centers forDisease Control and Prevention(CDC), make cancer screening ser-vices available to uninsured or under-insured women who meet certainincome and family size criteria but arenot eligible for other government reim-bursement programmes. Funding isavailable to provide screening and cer-tain follow-up services for only 6% ofwomen eligible for this programme,aged 18–64 years. In the absence of astructured national health care regis-tration system, women are informedabout and recruited into the NBC-

CEDP by a variety of means includingthe media, community- and religion-based organizational health fairs andpublic health announcements.However, the first contact with the pro-gramme is initiated voluntarily by thewoman when she applies for eligibility.Since 2001, many professional organi-zations and government agencies(CDC, the Institute of Medicine–USPreventive Services Task Force (USP-STF) and the National Institutes ofHealth (NIH)) have deliberated on thefeatures of cervical cancer screeningin the USA (see Table 50). After exten-sive review of published evidence andconsensus building among the variousgroups, updated recommendationshave been published for cytologicaltesting and follow-up of women withabnormal results. New screening rec-ommendations include changes in theage to begin screening (previously 18years, now 21), frequency of repeatscreening if results are negative (previ-ously annual, now up to every threeyears if over age 30), and the age toconsider ending screening (previouslyno recommendation, now age 70 ifrecent screening results are negative)(Saslow et al., 2002; American Collegeof Obstetricians and Gynecologists,2003; US Preventive Services TaskForce, 2003).

CanadaIn Canada, organization and provisionof health care is the responsibility ofthe provincial and territorial govern-ments. The universal coverageincludes cancer screening and follow-up activities. Furthermore, mostprovinces have cancer agencies thatare usually responsible for planning,coordinating and monitoring cancerscreening programmes.

Since the introduction of cytologicaltesting in Canada, opportunistic cervi-cal cancer screening has been themost frequently used method to screenwomen. In recognition of the fact that

129


117-162 24/01/05 11:07 Page 129

effective organization not only reducesthe cost of screening programmes butimproves their effectiveness, recom-mendations have been made on sev-eral occasions over the years for thedevelopment of organized screeningprogrammes that incorporate a com-puterized information system, popula-tion-based recruitment and effectivequality management.

Summarized below are highlightsof the recommendations from the 1989National Workshop on Cervical CancerScreening (Miller et al., 1991). Theserecommendations have been variablyaccepted and updated by provincialagencies responsible for screening.

• Cytological screening should startat age 18 years or at initiation ofsexual activity.

• A second test should, in general,be performed after one year, espe-cially for women who begin screen-ing after age 20.

• If the first two tests are satisfactoryand show no significant epithelialabnormality, women should, ingeneral, be advised to be re-screened every three years up toage 69.

• Screening should occur at this fre-quency in areas where a popula-tion-based information systemexists for identifying women andallowing notification and recall. Inthe absence of such a system, it isadvisable to repeat tests annually.

• Women over the age of 69 whohave had at least two satisfactorytests and no significant epithelialabnormality in the last nine years

and who have never had biopsy-confirmed severe dysplasia or car-cinoma in situ can leave the cervi-cal cytology screening programme.

• If mild dysplasia is found, a cyto-logical test is to be repeated everysix months for two years.

• If the lesion persists or progressesto moderate or severe dysplasia,the patient must be referred for col-poscopy.

• More frequent testing may be con-sidered for women at high risk (firstintercourse at less than 18 years ofage, multiple sexual partners, part-ner who has had multiple sexualpartners, smoking, low socioeco-nomic status).

• Women do not need to bescreened if they have never hadsexual intercourse or have had a

130


Organization American Cancer Society (ACS), American College of Obstetricians US Preventive Task ForceNov./Dec. 2002 and Gynecologists (ACOG), Aug. 2003 (USPSTF), Jan. 2003(Saslow et al., 2002) (American College of Obstetricians (US Preventive Services

and Gynecologists, 2003) Task Force, 2003)

When to start Age 21 or within 3 y of start of sexual Age 21 or within 3 y of start of sexual Age 21 or within 3 y ofcervical screening activity activity start of sexual activity

Interval Annually with conventional or every Every year for women < 30 or every2 y using liquid-based cytology; age 2–3 y for women > 30 (except women> 30, women with 3 negative may be with HIV, immunosuppressed or DESscreened every 2–3 y exposure)HPV-negative, Pap-negative: HPV-negative, Pap-negative: everyevery 3 y 3 y

Thin Prep Recommend Option Insufficient evidence

HPV testing with Option Insufficient evidenceASCUS

HPV testing > 30 Guidelines not out before FDA Option Insufficient evidenceapproval; preliminary recommend

Post-hysterectomy Discontinue if for benign reasons Discontinue except in special Discontinuecircumstances

When to stop Age 70 or 3 or more negative No upper limit > 65cervical screening tests within 10-year period

Table 50. Recommendations for cervical cancer screening, United States, 2003

117-162 24/01/05 11:07 Page 130

creo

hysterectomy for a benign condi-tion with adequate pathologicaldocumentation that the cervicalepithelium has been totallyremoved and previous screeningtests have been normal.

Two Canadian provinces, BritishColumbia and Nova Scotia, have wellestablished, organized programmesfor cervical cancer screening and inrecent years other provinces such asAlberta, Manitoba, Ontario and PrinceEdward Island have launched new pro-grammes. These programmes targetall women in the provincial populationin a specified age range (usually18–69 years), but no province yet haspopulation-based recruitment. Variationbetween provinces in the implementa-tion of screening programme compo-nents reflects the maturity of their pro-gramme development (Table 51)(Health Canada, 2002).

Most women who develop cervicalcancer have either not been screenedor have been screened too infre-quently (Quality Management WorkingGroup, 1998). About 60% of cervicalcancers occur in women who have notbeen screened in the previous threeyears. Lack of organization has con-tributed to this failure, including aninability to reach high-risk women,inadequate quality control, or ineffec-tive follow-up procedures.

The cost of cervical cancer screen-ing and follow-up of abnormal findingsis covered through universal provincialhealth funding.

Extent of use and accessUnited StatesThe extent of screening in the USA isaffected by the proportion of womenwith some reimbursement for primarycare and preventive health, andapproximately 50 million cytologicaltests are performed annually (Kurmanet al., 1994). The NBCCEDP providesapproximately 250 000 of those tests.

About 7% of all tests are reported toreveal an abnormality requiring furthertesting (Jones & Davey, 2000).

The Behavioral Risk FactorSurveillance System (BRFSS) and theNational Health Interview Survey(NHIS), both administered by the CDC,show that more than 85% of women inthe USA have had a previous cervicalcancer screening test, and that approx-imately 80% have had one in the pasttwo years (Blackman et al., 1999).

Overall, screening tends to occurmore frequently among youngerwomen (every 1–2 years under age40) than among older women (40years or older), who present them-selves for screening services lessoften as they have less need for repro-ductive health services. According tothe NHIS 2000 data, over 82% womenaged at least 25 years reported havinga test within the last three years; thenumbers are slightly different fromthose from the BRFSS because of thetime interval included. The groups withthe lowest proportions of women whohad had a test within the previousthree years were women without ausual source of health care (58.3%;95% CI 55.3–61.3), women withouthealth insurance (62.4%; 95% CI58.1–66.8) and women who immi-grated to the USA within the last 10years (61.0%, 95% CI 55.2–66.8).Women with lower levels of education,women with limited income andwomen with chronic disabilities hadlower levels of screening comparedwith other groups (Swan et al., 2003).

The burden of cervical cancerremains highest among women who arerarely or never screened, who accountfor an estimated 60% of newly diag-nosed invasive cancers (Sung, 2001).

CanadaIn Canada, access to cervical cancerscreening is available to all womenwho meet the criteria for screeningeither through national or provincial

programmes. Table 52 shows the fre-quency of self-reported cytologicaltests in Canada by province and agegroup for the period 1998–99.

More recently, the CanadaCommunity Health Survey (CCHS), anational, biennial, cross-sectional sur-vey, provided information on cervicalcancer screening (Statistics Canada,2002). From the survey cycle of2000/2001, an estimated 89% ofCanadian women aged 20–69 yearsanswered "Yes" to the question "Haveyou ever had a Pap test?", with thehighest percentage in the AtlanticProvinces (95%) and the lowest inQuebec (83%). Nationally, 53% and73% of women aged 18–69 yearsreported having had a test within thelast year and last three years, respec-tively, with the highest percentages inNova Scotia (60% for one year; 80%for three years) and the lowest inQuebec (50% for one year and 67% forthree years).

Methods of assuring qualityUnited StatesIn the 1980s, intensive media cover-age of poor cytology laboratory prac-tices and charges of lax enforcementof federal regulations contributed to thepassage of the Clinical LaboratoryImprovement Amendments (CLIA) in1988 and the regulations that nowdefine standards of cytology laboratorypractice in the USA. CLIA and therelated regulations serve as a baseline,through biennial inspections and certifi-cation, for assessing the quality of lab-oratory work including cervical cytology(Lawson et al., 1997). The regulationsallow for enforcement of CLIA stan-dards and for corrective measureswhen laboratories fail to meet thesestandards. The Centers for Medicareand Medicaid Services (CMS) in theUS Department of Health and HumanServices and the CDC are responsiblefor establishing and implementing theCLIA regulations. CMS is responsible

131


117-162 24/01/05 11:07 Page 131

for enforcing the regulations, and CDCprovides technical and scientific sup-port to CMS. The CMS central office inBaltimore, Maryland, establishes CLIAprogramme policies and oversees andcoordinates the work of 10 CMSregional offices. The regional offices areresponsible for enforcing the CLIA regu-

lations among the cytology laboratoriesin their jurisdictions. These regulationswere amended in 1991 and have beenfurther streamlined over the last decade.Some issues still exist regarding inter-pretation and review of screenings andreview for false negative tests, but someimprovements in cervical cancer

screening technology such as thin-layercytology, liquid-based preparations andHPV DNA testing may increase thesensitivity and specificity of testing.

To ensure the reliability of cytologi-cal tests, the following steps must beperformed and monitored correctly andadequately (Lawson et al., 1997):

132


Province Programme Year of Computerized Target age Screening frequencyinception information systema group

Newfoundland No – 18+ Annual

Nova Scotia Yes 1991 18+ Annual

Prince Edward Island Yes 2001 20–69 After three normal annual tests, screening should be continued at least every 2 y

New Brunswick No – – – –

Quebec No – – 18–69 Annual

Ontario Yes 2000 20–69 After three normal annual tests, screening should be continued every 2 y

Manitoba Yes 1999 18–69 After three normal annual tests, screening should be continued every 2 y

Saskatchewan No – – – –

Alberta Yes 2000 Under development 18–69 Annual (to be reviewed when all components of programme in place

British Columbia Yes 1960 18–69 After three normal annual tests, screening should be continued every 2 y.If high risk, continue annually

Northwest Territories No – – 18+ After three normal annual tests, screening should be continued every 2 y

Yukon No – – 18+ After three normal annual tests, screening should be continued every 2 y

Nunavut No – – 18+ After three normal annual tests, screening should be continued every 2 yIf high risk, continue annually

a Has a provincial computerized information system for cytology, which may have been implemented before inception of full programme.

From Health Canada (2002)

Table 51. Organized screening programmes in Canadian provinces

117-162 24/01/05 11:07 Page 132

creo

• Patients must be properly exam-ined and cervical cells from thetransformation zone must be sam-pled.

• Specimens must be properly col-lected and labelled.

• Laboratory requisition forms mustbe complete and contain sufficientinformation.

• Cytological tests must be evaluatedin a CLIA-certified laboratory.

• Laboratory reports must bereviewed to identify patients whorequire follow-up.

• Health-care providers and theirpatients must be notified of thescreening results and any follow-upindicated.

• Appropriate follow-up must betaken.

• Any substantive discrepancybetween clinical, cytological andhistological findings must beresolved by the referring clinicianand an anatomic pathologist.

In 1988, the first Bethesda SystemConference was organized to stream-line and update the use of cervicalcancer screening terminology. Thisconference established the BethesdaSystem, to simplify and improve com-munication of findings between

cytopathologists, clinicians andpatients (see Chapter 2).The Bethesdasystem, with refinements made in1991 and 2001, is widely accepted inthe USA and Canada (Solomon et al.,2002).

CanadaCervical cancer screening programmeshave adopted a system closely resem-bling the 2001 Bethesda System toclassify cytological specimens on thebasis of their perceived adequacy forinterpretation: satisfactory for interpre-tation or unsatisfactory. The "unsatis-factory" category is used when thesmear quality is inadequate for inter-pretation (Health Canada, 2002).

Three provinces reported on spec-imen adequacy for smears taken in1998, before the changes resultingfrom the 2001 Bethesda System con-ference. The percentage of unsatisfac-tory smears varied from 0.3% to 3.8%(Health Canada, 2002).

Performance indicatorsUnited StatesWhile estimates of screening participa-tion in the USA are readily available,they come primarily from self-reporteddata collected in the BRFSS and NHISnational surveillance programmes.

These figures are not validated andmay represent either over- or under-estimates. Few if any measures of ade-quacy of interpretation other thanthose required by CLIA exist to monitoraccuracy. Little information is availableat the national level on such perfor-mance indicators as proportion ofunsatisfactory tests, proportion ofwomen not receiving indicated follow-up and the proportion of women diag-nosed with cancer who were never orrarely screened. Information that is notpopulation-based has come primarilyfrom case series and from the qualitycontrol experience of cytology refer-ence laboratories (Sung, 2001; Krieger& Naryshkin, 1994; Tabbara & Sidawy,1996).

In the NBCCEDP, performanceindicators measure adequacy andtimeliness of screening and follow-up,the proportion of unsatisfactory testsand the proportion of women never orrarely screened who enter the pro-gramme each year. A target has beenset of 20% of women screened annu-ally who have rarely or never beenscreened. In addition, to monitor over-utilization of screening, a target of 75%has been established as the proportionof women who are moved to a triennialtest interval if they have had three suc-

133


Age Canada BC ALTA SASK MAN ON QUE NB NS PEI NFLDgroup % % % % % % % % % % %

20–29 80 76 80 91 86 77 81 84 92 84 9220–39 86 83 85 85 88 87 82 96 92 89 9140–49 82 79 89 82 83 80 83 80 90 83 8550–59 77 79 70 74 90 77 78 73 69 77 6760–69 60 58 72 64 73 60 56 54 59 68 53

Total 79 77 81 80 85 78 78 80 83 82 80(20–69)

Source: National Population Health Survey, 1998/99From Health Canada, 2002ALTA, Alberta, BC, British Columbia; MAN, Manitoba; NB, New Brunswick; NFLD, Newfoundland; NS, Nova Scotia; ON, Ontario; PEI, PrinceEdward Island; QUE, Quebec, SASK, Saskatchewan

Table 52. Self-reported screening within the previous three years by age group and province, Canada, 1998–99

117-162 24/01/05 11:07 Page 133

creo

cessive confirmed negative pro-gramme tests over a five-year period.

CanadaObjective information on cervical can-cer screening in Canada is not readilyavailable in most provinces on a rou-tine basis. Furthermore, administrativedatabases at the provincial level, suchas physician billing data, cannot beused for the most part as they may notinclude separate billing codes for Paptests and, even if they do, will not allowdistinction between tests done specifi-cally for screening in asymptomaticwomen and those done for follow-up.Self-reports from women in nationaland provincial health surveys andsmall-area studies are thus the onlysources of information.

The only cervical cytology perfor-mance indicators currently availablerelate directly to cytology laboratories.The indicators collected are:

• Cyto-histological correlation ratesfor each grade of squamousintraepithelial lesion and for carci-nomas measured against follow-upsurgical material or clinical out-come.

• False-negative rates.The false-nega-tive rate of the laboratory and of indi-vidual cytotechnologists should beseparately measured. A false-nega-tive result is defined as a screeningmiss, in a satisfactory smear, of anabnormality graded as ASCUS orworse, or an equivalent if an alterna-tive terminology is in use (CanadianSociety of Cytology, 1996).

• The rate of satisfactory and unsat-isfactory specimens at the labora-tory and slide-taker levels.

• The total number and rates ofabnormal gynaecological diag-noses and specific diagnostic cate-gories for the laboratory.

• Turnaround time. Clinicians andlaboratories should establish amutually agreed turnaround time

from the date the specimen isreceived in the laboratory to thedate of the final report; an optimaltime could be approximately onemonth.

Latin America and theCaribbeanThis region includes 28 countries,ranging from the small island states inthe Caribbean to Brazil.

OrganizationHealth services in Latin America andthe Caribbean began offering screen-ing services with cervical cytology inthe early 1960s, through family-plan-ning services and later within primaryhealth care. Table 53 provides informa-tion about the current status of cervicalcancer screening programmes in theregion. There is considerable variationwith regard to the age range of the tar-get population, but most of the guide-lines recommend screening everythree years. To what extent theseguidelines are followed by health-careproviders is unknown.

Several countries have attemptedto set up organized screening pro-grammes, often achieving partial orga-nization. Chile and Colombia have hada national organized programme for atleast 15 years, with documentedimprovements in quality and coverage,as well as decreased mortality inSantiago, Chile and decreased inci-dence in Cali, Colombia.

In Chile, the programme was reor-ganized in 1987, focusing on improvingfollow-up of women screened positiveand involving all public laboratoriesthat served the programme in a qualityassurance system. No data are avail-able on rates of follow-up, but thecountry has a large health infrastruc-ture, a public subsidy for health insur-ance for 70% of the population, with30% paying for private insurance. Inboth these systems, services for treat-ment of pre-malignant lesions are

widely offered and access to cancertreatment is guaranteed. In 1990, 40%of women aged 25–64 years had beenscreened in the past three years,according to a national survey, andparticipation increased to 66% in 1997,remaining at a similar level in 2000(68%). The programme is centrallysupervised by the Ministry of Health,but managed by each health region. Amanagement agreement for budgetallocation is signed between regionsand the Ministry of Health, in whichspecific services and outcomes areagreed upon.

In Colombia, organization of anational programme started in 1989and guidelines were approved in 1990.These guidelines placed emphasis ondiagnosis and treatment for womenwith a positive screening result. Healthsector reform in the 1990s privatizedand decentralized the delivery ofhealth care, but special legislationensured preventive care including cer-vical cancer screening.

Extent of useIn the absence of country-wide popula-tion registries, participation in cytologi-cal screening has been assessedthrough surveys. One source of infor-mation is a series of Health andFertility Surveys sponsored by the USAgency for International Development(USAID) in countries in which theyhave a reproductive health pro-gramme. A probabilistic sample ofwomen aged 15–49 years are inter-viewed in their homes to investigatevarious aspects of reproductive health.Several countries collect data onscreening for cervical lesions by ask-ing women if they had a Pap test in thelast 12 months. Table 54 shows partic-ipation in cytological screening incountries for which data are available.The lowest participations are observedin Jamaica (15.3%) and Nicaragua(20.5%). Ecuador and Costa Ricareport high participation (72.2% and

134


117-162 24/01/05 11:07 Page 134

135


Country State of cervical cancer screening programme Screening Lifetime no.policy of smears

Mexico In 1996, a national guideline was approved by consensus with the participation of all Age 25+ of all 13+major health-care providers. Various studies have shown deficiencies in quality services, Every 3 yincluding cytology.

Guatemala No organized cervical cancer screening programme exists in these countries. Although cytology 30–45, 15El Salvador is performed through family-planning programmes, no follow-up of women screened positive is annual 30–59, 15Honduras ensured. Initial attempts to pilot and evaluate visual inspection have been carried out in Nicaragua every 2 yNicaragua and El Salvador. Health-care systems in these countries are fragmented and coverage for women 25–59, every y 34Dominican is restricted to maternal health.Republic

Costa Rica Several attempts have been made to organize a cervical cancer screening programme.They have 20–59, every 17been able to centralize the cytology laboratory and maintain good quality standards. Nearly 90% 2 yof the population is covered by insurance and high coverage of cervical cytology has been reported, but no significant reduction in incidence or mortality from cervical cancer.

Panama Screening has been available, but no organized screening programme is in place 15+, every 3 y 17+

Cuba A programme is in place; coverage has been estimated at 70% using records reported from 25–59, every 11provincial health departments. No reduction in mortality has been observed. 3 y

Colombia Has had a cervical cancer screening programme since 1989. With health-sector reform in which 25–64, every 13multiple health-care providers emerged, major efforts were made to maintain the programme and 3 yimprove coverage. Decreased incidence has been observed in data from the Cali cancer registry.

Venezuela Efforts were made at the state level to improve follow-up of women screened positive by 25–64, every 13promoting out-patient care and use of colposcopy and LEEP. 3 y

Ecuador In the city of Quito, a cytology quality assurance programme was implemented through a large 30–59, every 7NGO in charge of cancer care (SOLCA); more recently coverage has been extended and efforts 5 ydirected to screen women aged 35–59 years every five years.

Peru National guidelines were issued in 2000.Cervical cytology is available.A large project in the province of 25–59, every 17San Martin has improved capacity and is leading the way for other provinces to improve their programmes. 2 y

Bolivia The Ministry of Health has recognized the importance of the problem, but cervical cancer screening, diagnosis and treatment were recently excluded from the maternal insurance package.

Paraguay A recent needs assessment was conducted, but no cervical cancer screening programme has been organized

Uruguay Presents among the lowest cervical cancer mortality rates in Latin America; opportunistic screeningis offered in health care services

Brazil A large cervical cancer screening programme was initiated in 1996 through the National Cancer 25–60 every 11Institute. In 1998 a large campaign to reach women who had never been screened was launched. 3 yEfforts are now being made to incorporate the screening programme into the primary care family health programme.

Argentina Cervical cytology is widely offered throughout the country. Cervical cytology programmes have been 35–64, every 10organized at the provincial level. No quality assurance programme is in place. 3 y

Chile A cervical cancer programme was reoriented in 1987, with clear attention to improving quality of 25–64, every 13cytology and follow-up of women screened positive before increasing coverage. Mortality from 3 ycervical cancer has begun to decrease, particularly in Santiago where the programme started.

Haiti No programme

Dutch/ No organized programme exists in any of the 14 countries, although over the past 15 years several English- attempts have been made. In 2003, the Ministers responsible for health of the Caribbean Community speaking (CARICOM) placed cervical cancer high on their agenda and 10 countries have assigned new Caribbean resources to this area.

Table 53. Cervical cancer screening programmes in Latin American countries, 2004

117-162 24/01/05 11:07 Page 135

creo

66.9%, respectively), largely due tofamily-planning programmes in theirprimary health-care infrastructure.

In other Latin American countriesnot covered by Health and FertilitySurveys, various studies haveassessed screening participation inthe population. The proportions ofwomen ever screened by cytologywere reported as 68.9% amongwomen aged 15–69 years in SãoPaulo, Brazil (Nascimento et al., 1996);65% among women aged 20–69 yearsin Pelotas, Brazil (Dias-Da-Costa et al.,1998); 63.3% among women aged15–49 years in Morelos, Mexico

(Lazcano-Ponce et al., 1996); 81.6% inGuadalajara, Mexico (Jiménez-Pérez& Thomas, 1999) and 45% in MexicoCity (Aguilar-Pérez et al., 2003).Consistent with the 1993 fertility sur-vey, in a sample of women aged 18years and older in Guanacasteprovince, Costa Rica, 87.8% reportedhaving had a cytological test in theirlifetime (Herrero et al., 1997); and in2000–03, 44.3% of women aged25–59 years in the province of SanMartin, Peru, declared having had atest in the last three years (Ferreccio etal., 2004), consistent with the figurereported in the 1996 survey. The pro-

gramme in Chile, using a periodichousehold survey to ask women aged25–64 whether they had a test in thelast three years, reported participationof 68% in the year 2000. Other coun-tries collect similar data from periodicsurveys, but these are seldom pub-lished. The quality of such informationis difficult to assess. In Latin America,higher participations have been foundin women who are aware of the bene-fits of screening (Lazcano-Ponce et al.,1999b; Aguilar-Pérez et al., 2003),have high socioeconomic status, asmeasured by schooling or housingconditions (Torres-Mejia et al., 2002;

136


Country (year) Age Percentage N Source

Within the last twelve monthsCosta Rica (1993) 15–49 66.9 3618 H&F Surveys a

Ecuador (1994) 15–49 72.2 13 582 H&F Surveys a

Honduras (1996) 15–49 55.4 7505 H&F Surveys a

Jamaica (1997) 15–49 15.3 6384 H&F Surveys a

Nicaragua (1998) 15–49 20.5 7150 H&F Surveys a

Paraguay (1996) 15–49 49.1 6465 H&F Surveys a

Peru (1996) 15–49 42.9 H&F Surveys a

Dominican Republic (1996) 15–49 44.8 H&F Surveys a

Ever screenedBrazil

São Paulo (1987) 15–69 68.9 Nascimento et al. (1996)Pelotas (1992) 20–69 65.0 Dias-Da-Costa et al. (1998)Pelotas (2000) 20–69 72.0 Dias-Da-Costa et al. (2003)

MexicoMorelos (1996/97) 15–49 63.3 Lazcano-Ponce et al. (1996)Guadalajara (1997) 15–49 81.6 Jiménez-Pérez & Thomas (1999)Mexico City (1997/98) 14–54 45.0 Aguilar-Pérez et al. (2003)

Costa RicaGuanacaste (1995/96) 18+ 87.8 Herrero et al. (1997)

In the past three yearsChile (2000) 25–64 68.3 CASEN Surveyb

PeruSan Martin (2000/03) 25–59 40.3 Ferreccio et al. (2004)

a Unpublished data from USAID/CDC Health and Fertility Surveys, for countries that receive assistance for a reproductive health programme.b Unpublished data from Employment Household Interview SurveySource: www.cdc.gov/reproductivehealth/logistics/global_rhs.htm [accessed 25 April 2004]

Table 54. Proportion of women reporting having had a test in selected countries of Latin America and theCaribbean

117-162 24/01/05 11:07 Page 136

creo

Dias-da-Costa et al., 2003) and whoreport satisfaction with previous care(Alvarez, 1996; Brenna et al., 2001).

Quality of cytologySeveral cytology laboratories in LatinAmerica and the Caribbean performquality assurance procedures, bystudying reproducibility, performanceevaluation or cyto-histological correla-tion. In Mexico, two studies on repro-ducibility of cytological testing, as mea-sured by weighted kappa, concludedthat intra-class agreement was low fordysplasia and carcinoma in situ buthigher for invasive carcinoma (Alonsode Ruíz et al., 1996; Lazcano-Ponce etal., 1997a). Kappa coefficients rangedfrom –0.02 to 0.17 for moderate andsevere dysplasia between the twostudies and were 0.29 and 0.36 forinvasive carcinoma. One study(Lazcano-Ponce et al., 1997a) alsoassessed reproducibility for histologyof cervical lesions among 30 patholo-gists; kappa coefficients were 0.07 forsevere dysplasia, 0.23 for moderatedysplasia and to 0.64 for invasive car-cinoma. Following these studies, amajor initiative was undertaken toimprove cytology in the country.

An initial evaluation of all cytologylaboratories of the Mexican Ministry ofHealth found that only 70% of micro-scopes were in satisfactory condition;deficiencies in the supply of reagentsand in laboratory facilities werereported. An evaluation of the perfor-mance of cytotechnicians was con-ducted by reviewing sets of slides pre-viously diagnosed by an expert panel.In this exercise only 16% of cytotechni-cians achieved a good or excellentscore, which meant at least 70% ofsimple agreement (Flisser et al.,2002). A quality assurance programmewas initiated which included improvingphysical infrastructure, training ofcytotechnicians and establishing a per-formance evaluation programme. Inpre-course tests, 21% of the cytotech-

nicians achieved a good or excellentscore; the percentage increased to69% after the course. At a thirdassessment six months to one yearlater, the proportion with good or excel-lent scores decreased to 56%, stillmuch better than the situation found atbaseline.

Seven countries in Latin Americaparticipate in a joint quality assuranceprogramme (RedPAC). The pro-gramme includes on-site evaluationand technical support, as well as peri-odic performance evaluation, mea-sured as agreement between thecytotechnicians and an expert panel.Improvements were observed in CostaRica, Ecuador and Mexico, where inthree consecutive years (1999–2001)weighted kappas rose from 0.43 to0.65, from 0.44 to 0.63 and 0.52 to0.63 respectively (Luciani et al., 2003).The improvement was attributedmostly to the reduction in the propor-tion of slides that were undercalled.Other areas of concern have also beenaddressed, such as the proportion ofinadequate slides, which was reducedafter training programmes from 3.71%to 1.98% in Ecuador and from 4.47%to 2.0% in Mexico. In three other par-ticipating countries (Bolivia, Peru andVenezuela), no significant change hasbeen observed and agreements(weighted kappas) were under 0.40.The only data from Brazil are for thecity of São Paulo, where an analysis ofcytology and the corresponding histol-ogy in a sample of 157 cases from amajor laboratory found agreement in75.8% of the cases; cytology underes-timated 17.2% of the lesions (Di Loretoet al., 1997).

Performance indicatorsMajor efforts and investments toincrease participation have been madein many Latin American countries, butother aspects of the programme havenot received equal attention. In Mexico,the cytology-based cervical cancer

screening programme has been ableto avert only 13% of potentially pre-ventable deaths, as estimated byLazcano-Ponce et al. (1996). This situ-ation has been attributed to low accu-racy of the test or quality of cytology inthese settings (Alonso de Ruíz et al.,1996). A basic element of a screeningprogramme is to provide diagnostic andtreatment services for those screenedpositive, but this has been neglected inmany countries. In a study in Peru, only25% of women who were screenedpositive received appropriate follow-up(Gage et al., 2003); a similar situationwas found in El Salvador (Robles,2004). In a municipality of São Paulo,Brazil, 78.3% of women with a positivecytological result received adequatetreatment in primary care services; butwhen they were referred to secondarycare, only 37.4% had adequate follow-up (Santiago & Andrade, 2003).

Overall, cytological testing hasbeen offered throughout Latin Americaand the Caribbean, but most countrieshave failed to organize screening pro-grammes. Research is under way toassess the potential effectiveness oflow-cost technology such as visualinspection methods and of HPV DNAtesting in various populations of LatinAmerica and the Caribbean.

AfricaScreening is difficult to achieve inAfrica partly because of significantcompeting, urgent health-care needs,in particular the HIV epidemic, andpartly because of poorly functioninghealth-care delivery systems.

A review on the functioning ofhealth-care systems undertaken by theWorld Health Organization (2000)rated and ranked these systems world-wide, revealing that among the 191WHO Member States, most of theleast functional health-care deliverysystems are in Africa.

To make an impact on the epidemi-ology of cervical cancer, as with any

137


117-162 24/01/05 11:07 Page 137

screening programme, national orga-nized programmes that achieve highparticipation are required. Research inAfrican settings confirms that integra-tion of screening services into theexisting health-care systems is theonly way that high participation ratescould be achieved (JHPIEGO, 1997).Other research is attempting to findtechnological solutions (screeningmethods that are cheaper, that do notrequire laboratory back-up, or thatallow immediate treatment, with low-technology and low-cost treatmentoptions) to address some of the healthsystem inadequacies that are preva-lent in Africa and some research islooking at other treatment options(Adewole et al., 1998; Darwish &Gadallah, 1998). In addition, suchefforts may provide pilot sites fromwhich national programmes canevolve.

OrganizationOnly South Africa has an officialnational cervical screening policy,which recommends three cytologicaltests for women over the age of 30years at ten-year intervals. However,the need for national policy has beenarticulated in many countries in Africa(Adanu, 2002). Absence of policy hasresulted in lack of action and in screen-ing of women at inappropriate ages(Ngwalle et al., 2001; Konje et al.,1991); in addition, facilities for treat-ment of precancerous lesions are ofteninadequate (for example, Tanzania:Ngwalle et al., 2001).

There are indications, however,that even in the absence of formal pol-icy, many countries have plans toimplement programmes. In Malawi, aprogramme for cervical cancer screen-ing and early treatment, as a partner-ship between the Ministry of Healthand Population and an internationalnon-governmental organization, hasbeen initiated and a nationwide cam-paign is planned which will start in the

southern part of country (Anonymous,2002). In Zimbabwe, screening basedon visual inspection with acetic acid(VIA) has been under consideration(Chirenje et al., 2000), but it is not clearif this is a national programme andwhether this is a priority for Zimbabwe(Rutgers & Verkuyl, 2000). The currentstate of the Zimbabwe health servicesuggests that rapid implementation ishighly unlikely. Cameroon has had anoperational cervical screening pro-gramme since 1992, but services areprovided only in two major cities andthe cost is such that most women donot have access to the service (Robyret al., 2002).

It is clear that access to screeningis poor for most women in Africa(Kenya and Sierra Leone; BurkinaFaso, Senegal, Ghana, Nigeria: Brown& Morgan, 1998) and this results inlate presentation of women at treat-ment centres (Gharoro et al., 1999;Were & Buziba, 2001).

Although policy frameworks areuseful and their absence can lead toirrational programmes and confusion(Moyo et al., 1997), they are not suffi-cient to ensure implementation;processes to ensure that policy isunderstood are essential (Anonymous,2001). In South Africa, there is now anational initiative to implement anational cervical screening policy,which is probably the best developedin the region and might provide anexample for other countries to follow.South Africa is, however, different frommany other countries in the region inhaving a relatively well developed lab-oratory-based capacity to providecytology services.

South AfricaThe South African National CancerControl Programme was adopted asofficial government policy in 1997.Policy development is a national func-tion, but implementation and delivery isa provincial (and more recently a local

government) function. While policyindicates what is required, it often doesnot explain how services should bedeveloped. This leads to unrealisticexpectations at the policy level andfrustration for implementers. After vari-ous attempts to implement screeningby promoting the policy, a nationalstrategy spearheaded by the nationalDepartment of Health was initiated.The main objectives of this strategyare to strengthen the existing health-management systems to implement,monitor and sustain the cervical can-cer screening programme; to ensuremaximum coverage of the target popu-lation; to ensure provision of facilitiesfor screening and treatment of precan-cerous lesions and develop referrallinks between screening and treatmentservices; to increase awareness of cer-vical cancer and its prevention; and toensure monitoring and evaluation ofthe programme.

Despite this policy framework,progress in cervical cancer screeninghas been slow and hard to achieve.The nine provinces in South Africa areat different levels of development andthere are resulting differences in imple-mentation. Two provinces (Limpopoand Eastern Cape) are predominantlyrural in nature and poor, with health-care delivery systems that functionpoorly. Others (Gauteng and WesternCape) are urban and have goodresources. The other provinces arelocated between these two extremes.

Study of the South African situationshows that where policy does exist, itis more likely that resources will bededicated to cervical screening ser-vices. Thus in the Western Capeprovince, cervical screening has beenidentified as a priority service anddevelopment of services has beenincluded in the key performance indi-cators or in performance agreementsof health-system managers. Similarlyin KwaZuluNatal, cervical screening isa performance target for districts.

138


117-162 24/01/05 11:07 Page 138

These two provinces have the greatestaccess to screening services. In threeprovinces budgetary allocation for cer-vical screening exists. While inprovinces such as Limpopo andMpumalanga, poor transport systemsare considered a barrier to implemen-tation, as this hampers the delivery ofslides to laboratories. However, otherpossibly poorer provinces have foundcreative ways of overcoming this prob-lem, for example by linking cervicalscreening with the tuberculosis pro-gramme and using the same labora-tory transport system. This illustratesthe value of integrating cervicalscreening into existing health-care ser-vices. In another case, private taxistransport the slides as part of their rou-tine runs. While in all provinces thereare colposcopes at the district level,there may be no trained staff availableto use them. In one rural province apartnership with a non-governmentalorganization has been set up toimprove access to screening servicesand three of the five districts compris-ing the province report offering ser-vices. Nonetheless, in some instanceswomen in the wrong age group arebeing screened. However, it is becom-ing increasingly clear what kinds ofintervention are required in order toassist provinces to implement a pro-gramme. Pilot programmes have beenset up and manuals for managers havebeen developed.

The South African experience hasshown the need to provide health ser-vice managers with tools to assistthem with practical aspects of imple-mentation. For example, one tool indicates how to work out the targetpopulation and thus the number ofsmears to be taken in a year and theworkload and equipment needs ateach service site. Another tool indi-cates what clinic-based data to collectand how to estimate the participationrate and the follow-up in each servicedelivery area.

The rest of the regionNo data on cervical cancer screeningare available from northern Africa.

In a review of cervical cancer diag-nosis and treatment in countries of east,central and southern Africa, a lack ofpolicy guidelines, infrequent supply ofbasic materials and absence of suitablyqualified staff were the common rea-sons reported for the low percentage ofwomen actually screened. The reviewfound that 95% of the facilities at primarycare level had the basic infrastructure tooffer cervical screening (Chirenje et al.,2001). However, once slides were taken,there was no way to send them for read-ing and limited access to referral path-ways to treat patients. In Botswana, forexample, cervical screening is limitedbecause few facilities have easy accessto laboratories to read cervical smears(Baakile et al., 1996).

Given the competing demands onhealth-care services, the only way inwhich cervical screening programmeswill gain the required political supportis if they are developed in such a wayas to benefit the overall functioning ofthe health-care system. The imperativeof high coverage requires that servicesbe decentralized, thus integrating cer-vical screening into the existing health-care services offers the best approachto reducing cervical cancer mortality.However, such integration is not sim-ple, as much of the organization ofhealth services in Africa is donor-dri-ven, often resulting in single-servicefacilities such as family-planning ser-vices. In a study in Kenya, integrationof cervical screening into family plan-ning clinics was reported to be feasibleand acceptable to both providers andpatients, and would benefit thepatients screened. However, only asmall percentage of women utilizethese services and in the Kenyanstudy, 43.5% of women were less than30 years of age, so that the potentialreduction in cervical cancer mortality islimited (Claeys et al., 2003).

It has been suggested that manyAfrican countries are not able to imple-ment screening and that cervical can-cer is not a priority (McCoy & Barron,1996; Rutgers & Verkuyl, 2000) or thatit is important but impossible toachieve (Wilkinson, 1997). However,the benefits that accrue from setting upa cervical screening service can beextended to other services, so thatreferral pathways, laboratory services,equipment supply systems and moni-toring systems, once operational forcervical screening, can be extended toother health-care needs or be devel-oped in tandem with and complementexisting systems (Fonn, 1997).

There are neither the resources northe human capacity in Africa to developvertical programmes (single-serviceprogrammes with staff working only inthat programme, frequently with uniqueconditions of service and unlinked inde-pendent supply and monitoring sys-tems, unrelated to other health-careservices often provided in adjacentsites). Yet existing resources can bemarshalled and applied to cervicalscreening. An approach that recog-nizes and builds health-systems capac-ity to deliver cervical cancer screeningcan improve the overall functioning ofhealth services in general.

AsiaData on cervical cancer screening fromwestern and south-central Asian coun-tries were available to the WorkingGroup only from Israel and India. Dataare also available for a number of south-eastern and far eastern Asian countries.

IsraelAs the incidence rate of cervical can-cer in Israel is very low, the official pol-icy is not to screen average-riskwomen. However, the NationalInsurance Plan reimburses cytologicaltesting for women aged 35–54 yearsonce every three years. In practice,many women are screened, usually at

139


117-162 24/01/05 11:07 Page 139

shorter intervals than recommended,with generally low-quality cytology. Inaddition, most women attendingscreening are of high socioeconomicstatus and probably are not the womenat highest risk. About 150 000 tests areperformed every year.

IndiaIndia has a National Cancer ControlProgramme that supports the principleof early diagnosis and treatment ofcancer of the cervix. Although cytolog-ical testing is available to a limited pop-ulation of mainly urban women, thereare no screening programmes(Dinshaw & Shastri, 2001; Shanta,2001; Varghese et al., 1999). India is ahigh-risk country for cervical cancer(Shanta et al., 2000; Sen et al., 2002).Women at highest risk of cervical can-cer are those over the age of 35 years,in low socioeconomic strata and withlittle or no education. Given that over80% of the population lives in ruralareas, screening programmes need towork within this sector (Dinshaw &Shastri, 2001; Sankaranarayaranan etal., 2001; Shanta, 2004). Cytology-based screening is not regarded aspractical or achievable in India(Dinshaw & Shastri, 2001).

Visual inspection-based approachesto cervical cancer screening such asVIA have been extensively investigatedin India, although their long-term effi-cacy in reducing the burden of cervicalcancer has not yet been demonstrated(Sankaranarayaranan et al., 2001; Basuet al., 2003). Visual inspection is nowregarded as the best option for pro-posed cancer control programmes, withtraining curricula and courses devel-oped by international organizationssuch as IARC and JHPIEGO (Shanta,2001). The Bill and Melinda GatesFoundation funds the Alliance forCervical Cancer Prevention which sup-ports projects in India, including throughIARC (http://www.alliance-cxca.org/index.html).

The advantages of visual inspec-tion methods are the lower costs thancytology and the short training periodrequired for health workers, includingthe ability to train nursing and non-medical workers (Basu et al., 2003;Sankaranarayaranan et al., 2003).Some 457 000 women (0.25% of alleligible women at risk) have partici-pated in screening studies of visualinspection methods (Shanta, 2004).The results indicate that the womenaccepted screening by visual inspec-tion with acetic acid or magnificationafter application of acetic acid (and col-poscopy and cryotherapy) by nurses,that a moderate level of compliancewith screening and treatment wasreached, and that these methods havehigher sensitivity and lower specificitythan cytology in the Indian setting(Basu et al., 2003). The low specificity,however, that causes high rates ofreferral and treatment, was a majorlimitation. Nevertheless, visual inspec-tion has been recommended as theimmediate option for cervical cancercontrol initiatives in 54 districts of India(Shanta, 2001; Sankaranarayanan etal., 2001).

Viet NamViet Nam does not have a nationalscreening programme. Research activ-ity relates mainly to HPV prevalence. Asubstantial difference in the prevalenceof cervical cancer and of HPV infectionbetween the north and south of thecountry are regarded as due to thegreater isolation of north during thedecades of war and socialist economy(Pham et al., 2003). A survey carriedout in 1997, within the framework of anIARC multicentre study, found thatHPV infection was rare in Hanoi andfive-fold higher in Ho Chi Min City(Pham et al., 2003).

In November 1998, the WesternPacific Regional Office of WHO collab-orated in strengthening cervicalscreening programmes with a series of

training sessions on cytologicalscreening, and pilot projects wereestablished in Hanoi and Ho Chi MinhCity. In co-operation with theViet/American Cervical CancerPrevention Project, the feasibility ofcytological screening in Viet Nam wasestablished by a formal cost-effective-ness analysis, and population-basedcytological screening services wereestablished in 1999 in Ho Chi MinhCity (Suba et al., 2001; Le Van et al.,2004). Pilot-scale screening is continu-ing to assess whether cervical cancerconstitutes a public health problem ofsufficient magnitude in northern VietNam to warrant the initiation of popula-tion-based screening.

ThailandThailand has attempted to establish acervical cancer prevention programmefor 30 years, with activity in selecteddistricts through maternal and childhealth or family-planning services(Gaffikin et al., 2003). In 1997, anational policy for cervical cancer pro-posed that screening be offered towomen aged 35–54 years with a Paptest every five years and, in the north-east of Thailand, using visual inspec-tion methods. However, surveys havefound that few women know about thePap test and few have ever beenscreened (Kritpetcharat et al., 2003;Tinker, 2004). National annual partici-pation is estimated to be no more than5% (Gaffikin et al., 2003). A mobile unitprogramme offering cytological testingwas established in 1993 (Swaddiwu-dhipong et al., 1999) and a demonstra-tion programme of visual inspectionmethods in 2000 (Gaffikin et al., 2003).The latter programme concluded that asingle-visit approach with VIA andcryotherapy by nurses was safe,acceptable and feasible and could beconsidered in areas where setting upcytological screening is unlikely(Gaffikin et al., 2003). Concerns havebeen raised, however, about potential

140


117-162 24/01/05 11:07 Page 140

overtreatment due to the low specificityof VIA (Walraven, 2003). Other imped-iments to the use of VIA in a popula-tion-based programme include theneed for standardized initial trainingand continuing education, and that nostudy has shown that VIA screeningreduces cervical cancer incidence ormortality (Walraven, 2003).

PhilippinesCervical cancer is the second mostcommon cancer in women in thePhilippines. The Department of Healthin the Philippines has proposed anorganized cervical cancer screeningprogramme, with recommendations forregular cytological tests every threeyears, although a recent policy shifthas recommended visual inspectionmethods (Ngelangel & Wang, 2002;Ngelangel et al., 2003). Changes inpublic health policy, including aspectsrelated to education of screening personnel, strategies for ensuringcompliance with screening and healthinsurance coverage for preventive services, have been mentioned as barriers to the development and implementation of a screening pro-gramme (Ngelangel et al., 2003). Thelack of a skilled workforce is also anissue. The Philippines Cancer Societyis involved in cytological testing,although this is not widely available(http://www.kanser.com.ph).

Republic of KoreaIn Korea, a national screening pro-gramme for cervical cancer started in1999. Cytological screening is recom-mended every two years for women 30years or older, of whom 33% had a testin 1999–2000. The provision of ser-vices is insurance-based, administeredby the Ministry of Health and Welfare.This insurance covers the costs to indi-vidual women of screening for cervicalcancer selectively for lower-incomewomen. Discussion and planning arecontinuing in order to define the

screening interval, upper age limit, thetest and quality control procedures.

ChinaOccurrence of cervical cancer islargely unrecorded in China, but isknown to be higher in rural areas; mor-tality from cervical cancer is aroundthe level in the USA (Belinson et al.,1999). Mortality has decreased overthe past 25 years, maybe as a result ofthe major social changes and thehealth programme set up by theChinese government after the foundingof the People’s Republic in 1949, inparticular, the outlawing of prostitutionand closure of brothels, and establish-ment of health facilities in factories andother work units, and specific publichealth programmes to screen for andtreat sexually transmitted diseases (Liet al., 2000). Cervical canceraccounted for only 1% of cancers inwomen in 1995 (Wang, 2001).Cancer prevention is not a high priorityand lacks government funding. Thereis no national screening programmeand cytology-based services arepatient- or employer-initiated. Womenwho have insurance can attend a hos-pital for screening. While governmentagencies cover employees for insur-ance, private employees may or maynot be covered. Screening is now lesscommon than 10 years ago and isbecoming more of a personal activity,organized at the level of individualcompanies or groups and subject tomarket forces. This change has led tofewer individuals being screened(Wang, 2001).

Small centres offer a screening ser-vice, mainly associated with universitiesor small studies. In the past, the workunit was the sole channel through whichscreening could be offered and wasresponsible for organizing any screen-ing that took place. Health professionalshope that the new medical insurancesystem will cover cancer screening andprevention (Wang, 2001).

In Shandong Province, a cytologicalscreening programme started in1970–72 and covered 1.5% of thefemale population, before governmentfunding was withdrawn; screening thencontinued in only a few areas (Li et al.,2000).

More recently, a pilot study in ahigh-risk province (Shanxi province)conducted a trial of cytological testingand HPV direct and self-testing in1997 among women aged 35–45years (Belinson et al., 2003).

Three national demonstration cen-tres will be set up for screening, orga-nized through field stations in women’sand children’s health centres or villageclinics.

Hong KongCytological screening has been offeredfor 10 years in Hong Kong by theDepartment of Health through 34gynaecological clinics and health cen-tres, including maternal and childhealth centres, social hygiene clinicsand others such as family planning, forwhich the service statistics indicatearound 100 000 tests per year in1997–2001 (http://www.famplan.org.hk/fpahk/en/template1.asp?style=tem-plate1.asp&content=info/statistics.asp&type=3). It has been estimated thatthe Department of Health and FamilyPlanning was responsible for 24% ofPap tests, the Hospital Authority for15% and private hospitals and medicalpractitioners for 37% in 2003 (AsianHPV Summit, 2003). The existing cyto-logical testing has not been part of anorganized programme and has no tar-get population, no screening registerand no formal quality-control process.

Several surveys conducted in HongKong showed that around half of allwomen were not receiving cervicalscreening (Yeung & Cheung, 2003).The Shatin Community Clinic for thePrevention of Cervical Cancer was setup in 1995 to reduce the incidence ofcervical cancer. It provides a free

141


117-162 27/01/05 15:54 Page 141

service to women who have neverbeen tested, without age restriction,and tested 20 000 women in 1995–99.In 1998, it received funding from theHong Kong Cancer Society for anautomated screening instrument, andhas accreditation from the Australianlaboratory accreditation authority. Theclinic provides training in diagnosticcytology to the Chinese PLA GeneralHospital in Beijing.

A population-based cervicalscreening programme was to belaunched by the Department of Healthin collaboration with other health ser-vices providers in late 2003 or early2004 (Yeung & Cheung, 2003), target-ing women aged 25–64 years withthree-yearly screening, recruitmentbeing through invitation letters, public-ity campaigns and community out-reach. The programme will providetraining for smear-takers, have a cen-tral register and establish qualityassurance indicators.

TaiwanIn 1993, an estimated 40% of womenin Taiwan had never been screened(Wang & Lin, 1996) and a programmeof free mass screening was estab-lished as part of the national healthinsurance in 1995 (Chen et al., 2002).An educational and cervical screeningprogramme at 12 public health centresin Taipei was extended (Pair & Ruey,1996), using outreach clinics in areaswith inadequate medical facilities andoffering training courses (Chen et al.,2002). The goal of the programme is toachieve a screening rate of 40% inwomen 30 years or older, who areoffered free three-yearly screening.TheCentral Department of Health monitorsand evaluates the programme, which isdelivered by the City and CountyHealth Bureau and local health stationswith follow-up of HSIL grades by localpublic health nurses. The programmehas a central registry and a process forlaboratory quality control.

SingaporeThe 1998 National Health Surveyreported that about two thirds ofSingapore women had ever had acytological test (Yian, 2000). Screeningof sexually active women aged 20–69years is carried out at 16 polyclinics,1900 private medical clinics and hospi-tals and the Singapore Cancer Society,although no annual figures are avail-able (Thamboo et al., 2003). Womenpay for the test but older age groupsare offered a subsidy. In January 1999,the Ministry of Health launched aCervical Cancer Education Program,with a recommendation for an annualtest in the first two years and three-yearly tests thereafter (http://www.hpb.gov.sg/hpb/haz/haz01123.asp).

A coordinated national programmehas been set up to start in 2004 (AsianHPV Summit, 2003, Dr Quek), withtraining programmes for smear-takers,a smear reporting system as inAustralia, a system of audit and man-agement guidelines for abnormalresults. The full programme isexpected to commence after a one-year pilot programme at selected pri-mary health care clinics.

JapanOrganization and financingCytological screening for cervical can-cer was introduced in selected regionsof Japan in 1961. These early pro-grammes were established and orga-nized voluntarily by gynaecology prac-titioners in cooperation with local gov-ernment officials. National governmentfunding, initiated in 1967, led to imple-mentation of screening programmes ata nationwide level. In 1983, the Healthand Medical Service Law for the Agedwas passed, which established cervi-cal cancer screening as one aspect ofcancer screening programmes to beimplemented nationwide at each city,town or prefecture. Although nationalgovernment funding for cancer screen-ing was phased out in 1998 and the

Health and Medical Service Law forthe Aged was virtually inactivated,leaving implementation to be decidedby each regional government, the con-tinuation of cancer screening pro-grammes has been strongly advocatedby the national government. Cervicalcancer screening is now funded byeach regional government. Womenhave to make an out-of-pocket pay-ment of 10–30% of the total cost of thetest, the proportion differing betweenregions.

In addition to the mass-screeningoffered by the regional governments,many women have the opportunity toparticipate in company-based cancerscreening, often offered by employersas part of a health insurance and ben-efits package, or personal healthexaminations, usually including cervi-cal cancer screening, at private clinicsand institutions. Cervical cancerscreening offered by these pro-grammes is implemented under almostthe same criteria as programmessponsored by regional governments. Ina questionnaire survey, from 216 com-pleted questionnaires, 147 companies(68%) stated that they offered cervicalcancer screening as part of theiremployee health check-up (Nagai etal., 1998). Thus, a variety of screeningprogrammes are available to mostwomen.

Extent of use and method of screeningSince the passage in 1983 of theHealth and Medical Service Law forthe Aged, the screening protocol rec-ommended by the national govern-ment has been offered to residents ofall prefectures. The target populationincludes all women aged 30 years orabove, with a screening interval of oneyear. Women are individually invited to participate. The test is performed by obstetricians/gynaecologists under-speculum examination using a cottonswab, spatula, scraper or brush for

142


117-162 24/01/05 11:07 Page 142

sampling. Interpretation of cytologicalspecimens is carried out by certifiedcytotechnologists and cytopathologists;their certification is carried out under theauspices of the Japanese Society ofClinical Cytology. All cytotechnologistsand cytopathologists are members ofthis society and in order to assure thequality of cytology screening, the soci-ety offers regular training and educationcourses in addition to renewal of certifi-cations every four years, based uponstipulated conditions.

The results of screening arereported in a five-tier evaluation desig-nated as Classes I to V, based upon amodified Papanicolaou classification.Although the tiered evaluation systemwas not incorporated in the BethesdaSystem of 2001, the use of only a writ-ten evaluation report is still not widelyaccepted among clinical practitionersin Japan and the five-tier cytology clas-sification is still used to avoid misun-derstanding and to facilitate reportingof the screening results. The five-tierevaluation consists of Class I as normal, Class II as inflammatorychange, Class III as dysplasia, ClassIV as carcinoma in situ, and Class V asinvasive carcinoma, as deduced fromcytological features. All Class III resultsand above are interpreted as screen-positive and a repeat cytological exam-ination as well as a colposcopicallyguided cervical biopsy are recom-mended as secondary testing.

The accuracy of cervical cancerscreening carried out in Miyagi prefec-ture as part of the nationwide pro-gramme showed sensitivity of 94.7%,specificity of 98.9% and a false nega-tive rate of 5.3% by linkage analysis,when all women screened were com-pared with patients having invasivecervical cancer or carcinoma in situwho were registered in a regional can-cer registry (Table 55; Yoshida et al.,2001). False negative cases weredefined as those diagnosed as havingcancer, including carcinoma in situ,

within one year after the negativescreening result.

Quality assurance control for cervi-cal screening programmes is adminis-tered by Management ControlCommittees for Lifestyle-relatedDisease established in each prefec-ture. These committees monitor infor-mation regarding the total number ofparticipants, participation rate, sec-ondary screening rate and individualparticipation history for cervical cancerscreening programmes in each city ortown in all prefectures (Ministry ofHealth, Labor, and Welfare, 1998).

The only data on total participationnumbers and rates, as well as screen-ing results for the programmes pro-vided by regional governments, areintegrated at a nationwide level andpublished annually in a Report onElderly Health Care by the Statisticsand Information Department, Minister’sSecretariat of the Ministry of Health,Labor, and Welfare. A participation rateof about 14–15% is reported. No simi-lar comprehensive analysis is availablefor non-government-sponsored cervi-cal cancer screening programmes,although the estimated overall partici-pation, combining both governmentand non-government-sponsored pro-grammes, has been estimated to be24%. Few quality assurance controlsexist for non-government-sponsoredcervical cancer screening pro-grammes.

Future perspectivesThe low participation of the cervicalcancer screening programmes hasbeen a matter of concern. In 2000, thenational government presented a‘National Health Promotion Movementin the 21st Century (Healthy Japan21)’, which included the goal ofincreasing the number of participantsby more than 50%.

Another concern is to broaden thetarget population, taking into accountan observed increase in the incidence

of carcinoma in situ and invasive can-cer in younger women (ResearchGroup for Population-based CancerRegistration in Japan, 2003). In April2004, the Ministry of Health, Labor,and Welfare recommended thatscreening should be initiated at 20years of age with an interval of twoyears.

OceaniaAustraliaCytological screening was readilyavailable to Australian women from the1960s but largely on an opportunisticbasis. In 1988, however, the AustralianHealth Ministers' Advisory Council setup the Cervical Cancer ScreeningEvaluation Steering Committee, whichrecommended an organized pro-gramme that was established in 1991and renamed the National CervicalScreening Program in 1995. The orga-nized programme is a joint initiative ofthe commonwealth, state and territorygovernments to provide cervicalscreening by coordinating the localprogrammes in individual states andterritories, each of which has adoptedor endorsed the goals and priorities ofthe national programme and uses thesame performance indicators and tar-gets. States and territories are respon-sible for regional coordination anddelivery of screening.

Cervical screening is available toall sexually active women between 18and 69 years of age, with a two-yearscreening interval. Women are askedto give their consent to their detailsbeing entered in the local cervicalcytology register, from which areminder is sent two years after theirlast screen. If the test result is abnor-mal, the register sends a letter to thewoman and her medical practitioner tohelp ensure that appropriate follow-upaction is taken. Coordination and programme administration are fundedjointly through a national and stategovernment agreement that covers

143


117-162 24/01/05 11:07 Page 143

several health areas and outlinesresponsibilities for delivery of thenational screening programme.

Extent of use and accessThe screening programme offers a testevery two years to all sexually activewomen from around age 18–20, oryounger if appropriate, and up to age69 at which time screening may ceaseafter two normal test results within fiveyears. Women 70 years and older whohave never had a test, or who requestone, are eligible for screening. Womenwho have an intact uterus and have nosymptoms or history suggestive of cer-vical pathology are eligible. There areseparate national guidelines for man-agement outside of the screening pro-gramme for women with a history ofhigh-grade cervical lesions or who arebeing followed up for a previous abnor-mal test result.

Education campaigns encourageeligible women and under-screenedgroups to attend. General medicalpractitioners take most Pap smears(80%); gynaecologists, women’shealth nurses, Indigenous healthgroups and sexual health and otherclinics are other providers. The scarcityof medical practitioners, particularlywomen practitioners, in remote andrural parts of Australia limits access toscreening test services, althoughwomen’s health nurses may be avail-

able. Accredited cervical cytology labora-tories read the slides and send theresults to the state or territory screeningregister and also to the health-careprovider who took the smear and to thewoman.

The costs of a visit to a medicalpractitioner and the laboratory costsfor reading the slide are reimbursed byMedicare, the national health insur-ance scheme funded by the Common-wealth government. The same is truefor treatment. The woman’s contribu-tion varies, since some medical practi-tioners charge more than the Medicarereimbursement and the women them-selves must fund the difference in thefee. For women who are eligible, thereis no charge for visits to providersfunded through Health ProgramGrants or by state governments.

In 1991, the year before thenational programme began, 52% ofwomen nationally had a screening test.In the programme in 2000–01, 61.8%of women had a test. Participation var-ied by state: 58% in Queensland,60–63% in New South Wales, WesternAustralia, the Northern Territory, andthe Australian Capital Territory, and66–67% in South Australia andTasmania (Australian Institute of Healthand Welfare, 2003a). Nationally, 32% ofwomen registered with the programmewere re-screened within less than therecommended two-year interval in

1999–2000 and 2000–01 (AustralianInstitute of Health and Welfare, 2003b).Women known to be under-screenedare those of low socioeconomic statusor with indigenous or other culturallyand linguistically diverse backgrounds,and women 60 years and older or fromrural and remote areas (Department ofHealth and Aged Care, 2000). No iden-tifier by indigenous status is availablein screening registers. Published four-yearly mortality rates, however, showthat death rates from cervical cancerare much higher in indigenous (11.4per 100 000 in 1998–2001) than non-indigenous (2.5 per 100 000) women(Australian Institute of Health andWelfare, 2003b).

The computerized cytology registersset up in each Australian state and terri-tory in 1989–99 record contact details ofconsenting women and the smear-takersforwarded by health-care practitioners;results of tests and identification of thereporting laboratory are sent directly bylaboratories. All information is confiden-tial. Around 1–3% of women choose notto be registered by name and de-identi-fied demographic details and smearresults only are recorded for them.All reg-isters have a protocol to ensure thatwomen with test abnormalities haveappropriate follow-up.

Registry data are collated nation-ally at the Australian Institute of Healthand Welfare, which has produced fiveannual reports on the performanceindicators endorsed by the nationalscreening programme, beginning withdata for 1996–97 and continuing up to2000–2001. Data standards in placeensure consistent and reliable data forperformance indicators.

Government expenditure onscreening with cervical cytology in1994–95 was mainly (61%) throughMedicare reimbursement for privatemedical services and some pathology,23% was a direct national governmentcontribution to the screening pro-gramme and 16% came from the local

144


Cervical cancer

Screening result (+)a (–) Total

Positive b 54 2099 2153Negative 3 184 005 184 008

Total 57 186 104 186 161

a Including carcinoma in situb Class III+ and non-assessable cases

Table 55. Accuracy of cervical cancer screening in Miyagi prefecture,Japan (Yoshida et al., 2001)

117-162 24/01/05 11:07 Page 144

creo

resources of the states and territories(AusAID, 1999). In 1999–2000,Medicare expenditure on cytologicaltests and pathology was $84.2 million,while national recruiting activities wereallocated $4.8 million over the threeyears. Funding to increase participa-tion was introduced in November 2001and offers incentives to medical practi-tioners for increasing participation bywomen who were not tested in the lastfour years.

Methods for assuring qualityThe National Advisory Committee tothe National Cervical ScreeningProgram (Advisory Committee onCancer Prevention, 2000) has fiveworking groups with members from allprogrammes, health professionals(pathology, general practice, healtheconomics, epidemiology, gynaecol-ogy), and a consumer and indigenousrepresentative. A working groupresponsible for quality assurance mon-itors specified programme outcomesand identifies areas for improvement inlaboratory adherence to performancestandards and methods to improvequality of Pap smears.

Australia has required formalaccreditation of all pathology laborato-ries since 1987 with three-yearlyinspections to ascertain compliancewith national standards set by industryand professional authorities (NationalPathology Accreditation AdvisoryCouncil (NPAAC), 2003). In addition,the screening programme, in consulta-tion with pathology accreditationauthorities, has formulated perfor-mance standards for technical compe-tence in gynaecological cytology inlaboratories; these were voluntary from1996 and mandatory since 1999. Theformal accreditation process requireslaboratories to submit standard data,which are compiled in a national reportdistributed to all laboratories with theirown performance data. No individuallaboratory is identified in the national

report.The information in these reportsis verified against data supplied by thecervical cytology registers. Laboratoryperformance is self-assessed using in-house quality systems, which set upcorrective measures as necessary andreport on the process to the assess-ment authorities. Reimbursementthrough the national health-care sys-tem is unavailable for services in unac-credited laboratories.

The pathology performance stan-dards for Australian laboratoriesreporting cervical cytology werereviewed in 2003 by NPAAC.Performance measures include theproportion of unsatisfactory and satis-factory specimens, the positive predic-tive value of a cytology report of ahigh-grade intraepithelial lesion, thefalse negative rate among women withhistologically confirmed carcinoma insitu, and the turnaround time in pro-cessing slides. All states have a feed-back loop whereby the register sup-plies laboratories with a performancereport on test reporting and laborato-ries feed information back to the regis-ter to allow monitoring of data integrity.Performance indicators, endorsed bythe national advisory committee, arereported annually for screening pro-grammes: these include the proportionof women participating by age, the per-centage of women with re-screening inthe 21 months following a negativescreen, the ratio of low- to high-gradeabnormalities verified on histology forwomen aged 20–69 years, the incidenceof micro-invasive and all invasive cervicalcancers, and mortality. Incidence andmortality by location and mortality inindigenous women is reported every fouryears (Australian Institute of Health andWelfare, 2003a, b).

New ZealandA national screening programme cameinto operation in 1990–91 followingrecommendations in 1985 for routinecervical screening and the Cartwright

Inquiry that recommended a nation-wide population-based programmewith central coordination (Skegg et al.1985; Ministry of Health, 1997;National Cervical Screening Pro-gramme (NCSP), 2002).

In 1993, enrolment in the pro-gramme increased after a legislativechange from registration only of thosewomen who consent (‘opt-on’) to non-registration only of those who specifi-cally refuse (‘opt-off’), and histologyreporting became compulsory. Maoriwomen’s data was protected in 1995under the Kaitiaki regulations and in1997, the Ministry of Health estab-lished a data management group forPacific women. Statistical reports wereproduced in 1993, 1995 and 1998. In1996–97, a national cervical cytologyscreening register was centralized inWellington and in 1998, responsibilityfor national coordination of the screen-ing programme passed from theMinistry of Health to the HealthFunding Authority. Following a review,an additional $1.4 million was injectedinto the NCSP during the 1999/2000year to improve quality standards, setup new independent monitoringprocesses, improve coordinationbetween providers and improve infor-mation for women and training forhealth educators. The NationalScreening Team transferred to theMinistry of Health as a separate unit,the National Screening Unit (NSU),within the Public Health Directorate inJanuary 2001.

The NSU funds the screening pro-gramme by contracting four indepen-dent service providers to providehealth promotion to Maori, Pacific andother women in their regions and 12laboratories (2 public and 10 private) toprovide cervical cytology services.Regional screening services are con-tracted through 13 District HealthBoards that provide health promotionand cytology to priority-group womenand regional coordination; eight of the

145


117-162 24/01/05 11:07 Page 145

regional services are responsible forlocal management and data entry oflaboratory results to the screening reg-ister. In addition, the NSU also fundssome low-cost or free cytological andcolposcopic services and treatmentprovided by District Health Boards.

An inquiry into the apparent under-reporting of abnormal results in theGisborne region found that during the1990s the NCSP lacked the necessaryorganization, coordination and some ofthe constituent parts required for safeand effective screening programmes. Akey finding of the inquiry was the needfor the Health Act 1956 to be amendedto enhance the capacity to monitor,audit and evaluate the NCSP.Appropriate legislation is now beforeParliament.

The NCSP Operational Policy andQuality Standards were introducedfrom November 2000 across the pro-gramme. These set standards for labo-ratory and publicly funded colposcopyservices. Since mid 2003, 758 585women have had one or more screen-ing tests in the NCSP in accordancewith the new standards. The nationalprogramme sets minimum standardsfor health services; providers con-tracted by the Ministry of Health aremonitored against these standards. Acomplete copy of the standards isavailable on the National ScreeningProgramme website (http://www.healthywomen.org.nz).

The screening programme targetsall women aged 20–69 who have everhad intercourse for a three-yearly cyto-logical test. In particular, the pro-gramme targets women who havenever been tested or whose previoustest was more than five years ago;these women have a second test afterone year. Women who have had a hys-terectomy for a benign condition, withcomplete removal of histologically nor-mal cervical epithelium and a normalcytological history, do not require fur-ther screening. Women aged over 40

years and Maori and Pacific womenare priority groups in the NCSP.

Pap smears are taken by generalmedical practitioners (70%), special-ists (5%), nurse smear-takers (25%),and two lay smear-takers without aprofessional background. Cytologyreading is funded by the government in10 community-based and two publichospital-based laboratories. The costto the woman is only the normal con-sultation fee, except when the screen-ing unit is directly funding the service,and an additional fee when a liquid-based cytology specimen is used, andprivate colposcopy services.

Test results are forwarded to theregister unless the woman has optedoff and does not want the result sent tothe programme; results are also sent tothe smear-taker. The register sendsthe woman a reminder when a test isoverdue and also supplies thewomen’s cervical screening historiesto smear-takers and laboratory cytolo-gists to assist in management deci-sions. The register also makes surethat the woman is informed of anabnormal result. It holds the name,address, date of birth, smear-taker andtheir details, cytological and histologi-cal history and a record of letters sentto the woman.

Extent of use and accessThe programme aims to cover 85%(adjusted for hysterectomy) of all20–69-year-old women recorded onthe screening register in the previous36 months. In 1998, 76% of eligiblewomen (84% after adjustment for hys-terectomy) were tested (IndependentMonitoring Group of the NationalCervical Screening Programme,2003). By May 2003, 99.14% of the eli-gible population (1 084 592 women)were enrolled on the Register(http://www.csi.org.nz/other_reports/NCSPQuestionsnAnswers.htm). Extentof use and access are currently esti-mated using census data, as the lack

of a population register precludesready identification of women for tar-geted recruitment.

The rate of cervical cancer forMaori women in 1997 was nearly threetimes that of non-Maori (Ministry ofHealth, 1997). An important function ofthe screening programme, therefore, isto address the disparities in health out-comes for Maori women. The issue ofchoice of service provider is importantto Maori women. A Maori Women’sCytology Working Group was estab-lished and funded. Although Maorismear-takers are not available in allareas, Maori community health initia-tives are offered in most areas and aNational Kaitiaki Group was formed toact as guardian of registry data(Ministry of Health, 1997).

Performance indicatorsNational indicators for quantitativemonitoring have been developed aspart of the process of improving overallquality assurance in the NCSP(National Screening Team, 2000).

An independent monitoring groupat the University of Otago is contractedto evaluate the programme againstnational indicators and targets(Independent Monitoring Group of theNational Cervical Screening Pro-gramme, 2003). Performance indica-tors are reported quarterly, six-monthlyor annually. The indicators reportedquarterly are short-interval re-screen-ing, delayed re-screening for womenwith a high-grade abnormality, follow-up of women with HSIL cytology, labo-ratory test reporting, including cytologyand histology turnaround time, satis-factory but limited and unsatisfactorysmears by laboratory and smear-taker,and the positive predictive value ofcytological reports of HSIL.

Annual reporting is required for thenumbers of women enrolled, participa-tion, coverage of women having ascreening test recorded on the registryin the 36 months preceding the end of

146


117-162 24/01/05 11:07 Page 146

the reporting period, non-participation,re-participation, incidence of cervicalcancer and incidence by stage, cervi-cal cancer mortality, rates of cervicalabnormality and histology abnormalityreporting on the register, interval can-cers, programme sensitivity, the opt-offrate, the accuracy of negative cytologyreports and residual high-grade dis-ease after treatment (IndependentMonitoring Group of the NationalCervical Screening Programme,2003).

Success in delivering a screening pro-gramme requires a good understand-ing of, and attention to, behaviouralfactors. These factors include commu-nication about cervical cancer and thescreening process, the psychologicalconsequences of participating inscreening and issues that affect partic-ipation. Most research in this area hasfocused on predictors of attendance atscreening and the evaluation of strate-gies designed to increase participa-tion.

Information and understandingThe cancer screening process canhave substantial negative conse-quences for an individual in terms ofanxiety and, if screening results arepositive, additional tests and treat-ment. The psychological conse-quences of cervical screening are dis-cussed further in Chapter 5.

The fact that screening usually tar-gets individuals who do not have symp-toms enhances the significance ofpotential negative consequences.Women should receive accurate, evi-dence-based information about both thehazards and the benefits of a screeningprogramme, so that they can makeinformed decisions about whether totake part (see, for example, General

Medical Council, 1998). While researchhas identified barriers and deficienciesin information provision, little is knownabout effective ways of enabling womento make informed decisions (Cockburnet al., 1995; Raffle, 1997; Coulter, 1998;Anderson & Nottingham, 1999). It canbe difficult to reconcile the aim of pro-moting effective forms of health carewith that of promoting patient choice andthe rights of women who may decide notto be screened (Austoker, 1999).

Knowledge and understanding ofcervical cancerWhen making a decision about partici-pation in screening, women shouldideally take into account their ownunderstanding of cervical cancer andperception of their risk of it, in additionto their understanding of the risks andbenefits of screening.

Survey data about knowledge ofrisk factors for cervical cancer indiverse groups of women has shown alow prevalence of information. HPVtesting is increasingly being incorpo-rated in some cervical screening pro-grammes. Knowledge about HPV is, ingeneral, poor. In a survey of femaleuniversity staff, 70% of respondents(280/400) reported that they had neverheard of HPV infection (Pitts & Clarke,2002). A survey of university students(of whom only 18% had undergonescreening due to the age distribution)reported a very similar percentage of69% (Philips et al., 2003). Amongthese students, 51% thought that HPVmight increase the risk of cervical can-cer. In a series of groups of low-incomeand minority women in the USA, justover half of the participants had heardof HPV, but they greatly overestimatedthe risk of developing cancer if infectedwith the virus (Anhang et al., 2004).Implementation of HPV testing in pri-mary screening for cervical cancerwould result in a large proportion ofwomen having to be told that they har-bour a sexually transmitted viral infec-

tion that can ultimately cause cancer(see Chapter 2). The potential negativeimpact of imparting this information tothe screening public has not been wellassessed from a psychological stand-point.

Among Vietnamese migrants to theUSA, 52% identified many sexual part-ners as a risk factor, 49% identifiedsexual intercourse at an early age and59%, incorrectly, thought that cervicalcancer was familial (Schulmeister &Lifsey, 1999). Another survey reportedthat 35% of mainly black South Africanwomen, all cancer patients andapproximately 90% of medical stu-dents and student nurses from thesame catchment area had some basicknowledge about cervical cancer(Wellensiek et al., 2002). Similar lowproportions of women with limited orno knowledge of cervical cancer andrisk factors have been reported inGhana (Adanu, 2002), Botswana(McFarland, 2003), Kenya (Gichangi etal., 2003) and Nigeria (Ayinde &Omigbodun, 2003).

Knowledge and understanding ofcervical screeningWhile some earlier surveys reportedpoor general knowledge of cervicalscreening, (Kennedy, 1989; Schwartzet al., 1989; Nicoll et al., 1991; Nugent& Tamlyn-Leaman, 1992; McKie,1993a, b; Greimel et al., 1997), morerecent research indicates an improve-ment (Eiser & Cole, 2000; Slater, 2000;Eaker et al., 2001a; Marteau et al.,2001; Ideström et al., 2002; Pitts &Clarke, 2002; Philips et al., 2003).Additional explanations may help com-munication: the proportion of UKwomen who understood the implica-tions of a normal result increased from52% to 70% after an explanation that‘normal’ meant that risk was low andnot that there was no risk of cancer(Marteau et al., 2001). In a high-resource country (Sweden) wherescreening is well established, 92% of

147


Behavioural considerationsin screening

117-162 24/01/05 11:07 Page 147

survey respondents were aware thatcytological testing detects abnormali-ties in asymptomatic women (Eaker etal., 2001a) and 95% of respondentsknew the purpose of screening,although fewer (62%) knew the type ofcancer detected by the screening test(Ideström et al., 2002).

Knowledge of the implications of anabnormal test result and the reasonswhy colposcopy is needed are also notwell understood (Nugent & Tamlyn-Leaman, 1992; Onyeka & MartinHirsch, 2003). As may be expected,understanding was greater amongwomen who had received an abnormalresult in the past than among womenwho had not undergone colposcopy(Pitts & Clarke, 2002); once an abnor-mality was detected, the perception ofpersonal risk increased (Kavanagh &Broom, 1998).

Bankhead et al. (2003) reviewed 49studies on beliefs and behaviourrelated to cervical cancer screening,all observational, and found thatadherence to follow-up recommenda-tion after a positive test result rangedfrom 53 to 75%. Several interventionstudies have looked at the provision ofinformation to try to reduce anxiety,with the assumption that lower anxietywould result in better adherence to fol-low-up recommendations, but havefound that provision of informationincreased knowledge without reducinganxiety or increasing attendance at fol-low-up.

Informed choice about whether ornot to attend for cancer screening wasexplicitly introduced in England in2001. New mandatory leaflets explain-ing the benefits and limitations ofscreening were to accompany everyinvitation (http://www.cancerscreening.nhs.uk/news/001.html). Since this pol-icy and new leaflet were introduced,despite concerns in some areas, nochange has been observed in accep-tance of screening (Department ofHealth, Statistical Bulletins for 2001/2,

2002/3, 2003/4, available on http://www.cancerscreening.nhs.uk/news/001.html).

Bankhead et al. (2003) commentedon the relatively poor quality of studiesinto health behaviour, attitudes andbeliefs with regard to cervical cancerscreening, although the trend in mostobservational studies is towards a ben-eficial effect.

Predictors of attendance forscreeningObtaining the high levels of attendancefor screening that are essential toreduce the incidence of cervical can-cer has been a major problem in manycountries with and without organizedscreening programmes (Ponten et al.,1995, Lazcano-Ponce et al., 1999a).Besides a high screening coverage ofthe population at risk, a comprehen-sive cervical screening programmemust also assure maximum returnrates among women with abnormalscreening results and ensure appropri-ate care for women requiring follow-uptreatment.

Establishing the main determinantsof participation is essential to deviseeffective strategies to increase atten-dance. These include factors such asthe health-care system organization,the socioeconomic level of the popula-tion, the costs involved, women’s per-ceptions of vulnerability, anxiety andfear about cervical cancer, beliefsabout the relevance of the test, con-current family difficulties, and the prior-ity accorded to cervical screening(Austoker, 1994). The relative impor-tance of each of these factors willdepend on the specific setting.

Studies of predictors of participa-tion published in the last 10 years arepresented in Table 56. Studies carriedout among specific social or ethnicgroups and qualitative studies were notincluded. Most studies were carried outin developed countries, with only fivefrom developing countries, and mostanalysed predictors of participation in

cytology-based screening; oneanalysed determinants of participationin visual inspection-based screening(Sankaranarayan et al., 2003).

Only one of the studies included inTable 56 analysed perceived barriersto screening (Eaker et al., 2001a); itfound that time-consuming barriersand economic barriers were associ-ated with non-attendance. The associ-ation of emotional barriers was foundto be non-significant.

Socio-demographic factorsAgeMost studies have found that youngerwomen are more likely to attend forscreening than older women (Calle etal., 1993; Perez-Stable et al., 1995;Mandelblatt et al., 1999a; Hsia et al.,2000; Chan et al., 2002a; Sankaran-arayan et al., 2003).

Socioeconomic statusParticipation in cervical cancer screen-ing was associated with higher incomeand educational level in many studies(Calle et al., 1993; Katz & Hofer, 1994;Perez-Stable et al., 1995; Nascimentoet al., 1996; Lazcano-Ponce et al.,1997b, 2002; Borras et al., 1999; Hsiaet al., 2000; Maxwell et al., 2001; Chanet al., 2002a; Hewitt et al., 2002;O’Malley et al., 2002, Siahpush &Singh, 2002; Selvin & Brett, 2003). Forexample, Calle et al. (1993) found that19% of women under the poverty linehad never had a screening test com-pared with only 5.8% of women whoseincomes were at least 300% of thepoverty level.

Although socioeconomic level maybe an important determinant of theability to pay for preventive services,Katz & Hofer (1994) found that womenwith higher income and education inthe USA and Canada were more likelyto have been tested, and that therewas no difference between countries,despite Canada’s universal health coverage. The authors suggested that

148


117-162 24/01/05 11:07 Page 148

149


Table 56. Predictors of attending for cervical cancer screening

Ever having had a test associated with:Demographic: having been married; white/black back-ground; younger than 65; education > 12 years;income above the poverty line. No difference according to rural residence.

Having had a test associated with:Health care: having a female physician.

Ever having had a test associated with:Demographic: college degree, higher income, no differences between countries. Disparities persistedwhen the effect of health insurance was controlled.

Having had a test associated with:Demographic: percentage of the practice population under 5 years of age. Overcrowding, age 35–44, and change of address negatively associated with atten-dance.Health care: female partner. Size of practice and com-puterization not significant predictors of screening uptake

Attendance increased with:Demographic: older age, lower education levelHealth care: having had a test more than three years ago. Receiving an invitation with a pre-fixed appoint-ment.

Cognitive: Anxiety

Attendance associated with:Demographic: Younger age, Health care: oral contraception, and receiving a GP letter.Cognitive: perceive screening as necessary

Test in the last three years associated with:Demographic: age 35–49; education level > 12 yearsEthnicity was not a significant predictor for use of screening in the previous three years

Having a test in the last three years associated with:Demographic: being marriedHealth care: having health insurance, having a regularphysician, having seen a health practitioner in the pastyear, and having a physician make a recent recommen-dation for a test

The association with income and education was non-significant. Having a hysterectomy and perceiving screen-ing tests to involve physical discomfort were negativelyassociated.

Calle et al.(1993)

Lurie et al.(1993)

Katz & Hofer(1994)

Majeed etal. (1994)

Ronco et al.(1994)

Bowman etal. (1995)

Perez-Stableet al. (1995)

Lantz et al.(1997)

Population-basedcross-sectional study;reported screening

Cross-sectional.Women enrolled in alarge Mid-westernhealth plan

Population-basedcross-sectional survey

Cross-sectional/-correlation study.General practice

Survey of attendersand non-attenders to apilot programme inTurin (invitation byGPs)

Prospective studyafter invitation


Population-based tele-phone survey

.

USA

USA

USA/Canada

England

Italy

Australia

USA

USA

12 252 women aged 18and older who participatedin the National HealthInterview Survey in 1987

24 713 women aged 18 to75 years old

23 521 and 23 932 womenaged 18 and older partici-pating in the 1990 OntarioHealth Survey and in the1990 US National HealthInterview Survey respec-tively

174 724 women aged 25to 64

374 (372 analysed) com-pliers and 513 (398analysed) non-compliersaged 25–64 years

504 women aged 18–70from intervention groups

1242 Latino and Anglowomen aged 35–74 years

1168 rural Wisconsinwomen aged 40 years andolder

Reference Study type Country Study population Key findings

117-162 27/01/05 15:56 Page 149

creo

150


Health care: Ever and recent screening associated withusual site of care

Screening in the past three years was associated with:Health care: having health insurance.

Higher attendance when age 45–54, married, receiving aninvitation from GP, higher education level

Ever having a test associated with:Demographic: younger age, higher educational levelHealth care: enrolled in voluntary health insurance

Ever and recent test associated with:Demographic: younger age, higher educationHealth care: regular source of care, health insuranceCognitive: positive cancer attitudes

Test in the last three years associated with:Demographic: younger age, higher education; higher income, married status, ethnic backgroundHealth care: usual care provider, medical visit in the past year; health insuranceHealth status: Presence of some chronic medical conditions, smoking.

Attendance associated with (5 years for women 30–59and 3 years for 25–29 years):

Cognitive: perceived satisfactory benefits.Access: time-consuming barriers and economic barriersassociated with non-attendance

Association between perceived severity of cancer, socialsupport and anxiety non-significant

Attendance associated with (5 years for women 30–59and 3 years for 25–29 years):

Demographic: living in urban areas. Socioeconomic status was not determinant of participationHealth care: oral contraception, visits to a physician 1–5times/year or less than once a year; seeing the same gynaecologist; having a test on their own initiativeCognitive: Knowing the recommended screening interval

Screening associated with:Demographic: being non-migrant, ever married, higher education, spoken language: English, younger ageHealth behaviour: having a recent blood pressure checkand frequent physical activityHealth care: regular physician

O’Malley etal. (1997)

Potosky etal. (1998)

Segnan etal. (1998)

Borras et al.(1999)

Mandelblattet al.(1999a)

Hsia et al.(2000)

Eaker et al.(2001a)

Eaker et al.(2001b)

Maxwell etal. (2001)


Population-basedcross-sectional survey.Reported screening

Prospective studyafter intervention

Population-basedcross-sectional survey,reported screening

Population-based tele-phone survey; report-ed screening

Cross-sectional study;reported screening

Population-based tele-phone survey; validat-ed reported screening

Population-based tele-phone survey; validat-ed reported screening


.

USA

USA

Italy

Spain

USA

USA

Sweden

Sweden

Canada

1420 women aged 18years and older from fourHispanic groups and threeblack groups

9455 women 18 years andolder participating in theNational Health InterviewSurvey in 1992

8385 women aged 25–64years

5865 women aged 20years and older participat-ing in the Catalan HealthSurvey in 1994

1420 women aged 18–74from four Hispanic groupsand three black groups inNew York city

55 278 women aged50–79 participating in theWomen’s Health InitiativeObservational Study in1994–97

430 non-attenders and514 attenders aged 25–59years.

430 non-attenders and514 attenders aged 25–59years

23 287 women aged25–64 years participatingin the National PopulationHealth Survey 1996–1997

Table 56 (contd)


117-162 24/01/05 11:07 Page 150

creo

151


Having had a test in the last three years associated with:Demographic: higher education, higher income, increased level of urbanization, fewer than three persons in the household, being currently married and White/Hispanic/black background. Women aged 30–39 years were more likely to have had a recent test.Health care: health insurance coverage.Health status: having seen a physician in the past year,good or excellent health status, non-smoking and no alcohol consumption.

Having had a test in the last year associated with:Demographic: family incomes at or above 300% of the poverty level, at least a college degree; not having a non-Hispanic black background.Health care: health insurance.Cervical cancer risk: Having at least one of five risk factors for cervical cancer

Reported receipt of the last two screening tests within therecommended intervals for age:

Demographic: higher incomeHealth care: Women under 65: continuity of care, primary care more comprehensive, counselling, patient–physician relationship, trustOlder than 64: knowledge about cervical cancer, evermarried, continuity of care, counselling, patient–physician relationship

Ever having a test associated with:Demographic: age 30–49, being married, being born inAustralia or New Zealand and high education level.Socio-economic level was not a predictor of participation.

Test within three years before interview associated with:Demographic: Income above or at 200% of poverty level (except for black women), bachelor’s degree or higherHealth care: Having a usual source of care; private health insuranceHealth behaviour: non-smoking except for non-Hispanicblack

Residential status, self-reported health and marital statusnot significant predictors of attendance

Ever having had a test associated with:Demographic: older than 24, higher education, higherincome, ever marriedHealth care: consulted a physician in the year precedingthe survey, oral contraceptive use, and performed breast self-examination

Ever having had a test associated with:Demographic: higher education level; higher socioeconomic level; living in urban areasHealth care: access to social security health careCognitive: knowledge of what the Pap test is used for

Coughlin etal. (2002)

Hewitt et al.(2002)

O’Malley etal. (2002)

Siahpush &Singh (2002)

Selvin &Brett (2003)

Nascimentoet al. (1996)

Lazcano-Ponce et al.(1997)



Population-based tele-phone survey; report-ed screening

Population-basedcross-sectional study


Population-basedcross-sectional survey;reported screening

Population-basedcross-sectional survey;reported screening

.

USA

USA

USA

Australia

USA

Brazil

Mexico

131 813 women aged 18years and older who par-ticipated in the BehavioralRisk Factor SurveillanceSystem in 1998–99

10 847 women aged15–44 years who partici-pated in the NationalSurvey of Family Growthin 1995

1205 women 40 years and older


5509 women aged 40–64years who participated inthe 1998 National HealthInterview Survey


4208 women aged 15–49years from Mexico City orin selected rural areas ofthe state of Oaxaca

Table 56 (contd)


Developing countries

117-162 24/01/05 11:07 Page 151

creo

152


Test in the previous 12 months associated with:Demographic: Younger age, education level higher thanprimary level.Health care: receiving hormone treatment; breast self-examination performedHealth status: premenopausal status; chronic disease

Increased screening associated with:Demographic: higher educational level of the head of the familyHealth care: history of using two or more family planning methodsCognitive: knowing why the screening test is employed;good experience of screening quality

VIA-based screening associated with:Demographic: Younger age, higher educational level, being married, multiparous status and low-income levelHealth care: having had tubal sterilization for birth control

Chan et al.(2002)

Lazcano-Ponce etal. (2002)

Sankarana-rayanan etal. (2003b)

Population-basedcross-sectional sur-vey; reported screen-ing


Prospective study ofwomen invited forscreening; objectivemeasure of screening

HongKong

Mexico

India(rural)


2094 women aged 15–49years with a CCSP(National Cervical CancerScreening Programme)Pap test history

48 225 women aged30–59 years

Table 56 (contd)


factors linked to recruitment and ser-vice delivery should also be taken intoaccount in explaining socioeconomicdifferences. For example, in rural India,women with higher income levels wereless likely to participate in the visual-inspection-based screening (Sankara-narayan et al., 2003). The authors con-sidered that the fact that the screeningclinics were organized in public institu-tions such as health centres or schoolsmight have deterred high-incomewomen from attending.

Marital statusMarried, divorced and widowedwomen were more likely than singlewomen to attend for screening (Calleet al., 1993; Nascimento et al., 1996;Lantz et al., 1997; Segnan et al., 1998;Hsia et al., 2000; Maxwell et al., 2001;Siahpush & Singh, 2002).

Rural residenceMost research suggests that womenliving in urban areas are more likely toattend for screening (Eaker et al.,2001b; Coughlin et al., 2002).

However, in some European countries,higher participation is seen in ruralareas than in large urban centres.

EthnicityThe evidence on the influence of ethnic-ity in screening attendance is not con-clusive. In the USA, for example, Calle etal. (1993) found that women with whiteor black ethnic background were morelikely to be screened and Coughlin et al.(2002) found that Hispanic women wereas likely as white women to bescreened. Perez-Stable et al. (1995), intheir study comparing Latino and ‘Anglo’(non-Latino white) women found no sig-nificant effect of ethnicity and Hsia et al.(2000) found that only Asian/Pacificislander women were less likely to par-ticipate. It is important to note that eth-nicity is often a proxy of socioeconomicstatus, particularly in the USA.

Health statusSome studies have shown that atten-dance was higher among women withgood or excellent health status(Coughlin et al., 2002), while others

have found that women with chronicdiseases were more likely to bescreened (Chan et al., 2002a). In theUSA, Mandelblatt et al. (1999a) foundthat both younger women in poorhealth and elderly women in goodhealth were more likely to have everhad or to recently have had a test.

Interactions with the health systemMost studies have shown that contactswith the health-care system increasethe likelihood of a woman beingscreened (Lantz et al., 1997; O’Malleyet al., 1997; Mandelblatt et al., 1999a;Eaker et al., 2001b; Hsia et al., 2000;Maxwell et al., 2001; Coughlin et al.,2002; Lazcano-Ponce et al., 2002;O’Malley et al., 2002). For example,Maxwell et al. (2001) reported that, inCanada, having had a medical consul-tation in the past year and having a lastblood pressure check less than twoyears ago were important predictors ofcervical cancer screening. A contactwith the health-care system seems tobe one of the main determinants ofattendance also in developing

117-162 27/01/05 15:59 Page 152

creo

countries (Nascimento et al., 1996;Sankaranarayanan et al., 2003b). Forexample, in India, both a greater num-ber of children and use of family plan-ning methods were associated withhigher participation (Sankaranarayananet al., 2003b). A previous contact withgynaecological and maternal servicesmay increase awareness about gynae-cological procedures and encouragefurther contacts with health-care ser-vices, making women more responsiveto screening. Having a regular sourceof care was also linked to higher atten-dance in many studies (Lantz et al.,1997; Mandelblatt et al., 1999a; Eakeret al., 2001b; Maxwell et al., 2001;O’Malley et al., 2002). Indeed, Lantz etal. (1997) found that having a regularsource of care was a main predictor ofscreening, even after controlling forother health-care access factors suchhealth insurance.

Aspects related to the patient–physician relationship and contact withthe health-care system appear to beimportant determinants of attendance.The probability of attending screeningwas higher in women who reportedgood experiences with the health sys-tem. For example, O’Malley et al.(2002) reported that women who eval-uated primary care as more compre-hensive, and their relation with theirphysician based on trust, were alsomore likely to be screened. In Mexico,women with good previous screeningexperiences were four times morelikely to be re-screened (Lazcano-Ponce et al., 2002). In El Salvador, apilot study that implemented a quality-improvement process resulted inscreening 25% of women aged 30–59years who had never been screened.Another qualitative study summarizingthe experiences of research projects inBolivia, Peru, Kenya, South Africa, andMexico carried out by the Alliance forCervical Cancer Prevention (ACCP)reported that women expressed theneed for confidentiality and privacy.

Women commonly report feelingashamed, especially when privacy islacking or when male providers per-form the examination (Bingham et al.,2003).

The effect of the gender of thephysician was examined in two studiesand in both it appeared that womenhaving a female physician were morelikely to be screened (Lurie et al. 1993;Majeed et al., 1994). A recommenda-tion by a doctor to attend screeningalso appeared to have an importantinfluence on women’s decision to bescreened (Bowman et al., 1995; Lantzet al., 1997; Segnan et al., 1998). Forexample, in the USA, women whoreceived a physician’s recommenda-tion for screening were 2.3 times morelikely to be screened (Lantz et al.,1997). Ronco et al. (1994) reported thatif the recommendation included a fixedappointment, women were more likelyto attend than if the invitation did not.

Among the factors related toaccess to health care, health insur-ance appears to be one of the mostimportant predictors of screening, asmost studies have found that havinghealth insurance increased the likeli-hood of participation (Katz & Hofer,1994; Lantz et al., 1997; Potosky et al.,1998; Borras et al., 1999; Lazcano-Ponce et al., 1997b; Hsia et al., 2000;Selvin & Brett, 2003; Hewitt et al.,2002). There is limited evidencerelated to other access factors such asdistance to a health-care centre andcost of transport. The introduction ofmobile clinics in rural Thailandincreased participation in a cytology-based screening from 21 to 57%(Swaddiwudhipong et al., 1995, 1999).

Knowledge and attitudes as predic-tors of attendanceKnowledge of screeningAll of the studies included in Table 56that analysed the effect of knowledge(Bowman et al., 1995; Mandelblatt etal., 1999a; Eaker et al. 2001b;

Lazcano-Ponce et al., 1997b, 2002;O’Malley et al., 2002) found that knowl-edge about the screening testincreased the probability of screening.For example, in Mexico, women whoknew why the test was given werethree times more likely to be screened(Lazcano-Ponce et al., 2002). InSweden, knowing the recommendedscreening interval increased the prob-ability of attendance (Eaker et al.,2001b). Also, women are more likely toattend screening if they perceivescreening as necessary or beneficial(Bowman et al., 1995; Eaker et al.,2001a). There is no evidence thatawareness of risk influences women’sdecisions on whether to be screened.

Fear/anxietyIn most studies, increased anxiety wasassociated with lower probability ofwomen attending for screening. In Italy,Ronco et al. (1994) found that anxietycaused by periodic controls was animportant negative determinant ofcompliance. In the USA, positive atti-tudes to cancer (less anxiety andhopelessness and a lower level ofdenial) were key determinants of participation (Mandelblatt et al.,1999a). Extensive qualitative researchon reasons for non-attendance indi-cates that both fear of cancer and anxiety and knowledge of screeningare key barriers to screening. A recentin-depth qualitative analysis in fiveLatin American countries indicated‘fear of cancer’ as an underlying rea-son for women not to seek screeningservices (Agurto et al., 2004). Theauthors suggest that this aspect isarticulated by women in differentforms, such as poor knowledge andunderstanding or not having time,depending on the questions of the sur-vey; but when women are prompted toexplain further they consistentlyalluded to ‘fear of cancer’.

153


117-162 24/01/05 11:07 Page 153

154


Strategies to encourage partici-pation in cervical cancerscreening programmesMany approaches to increase participa-tion in screening have been analysed(Table 57). Studies differ in the popula-tions addressed, the settings where theywere implemented and the methodsused to test the approach. Even whentwo studies test the same strategy, forexample, an invitation by letter, it is notpossible to control for all the variablesthat may have an influence on women’sparticipation, such as the style and toneof the letter, the actual service beingoffered, who signs the letter and so on.In general, limited information is avail-able about these methodological differ-ences, but it is clear that apparently sim-ilar approaches can differ in variousaspects that might affect participation.

The effectiveness of a strategy willdepend on how the health system isorganized; thus, an invitation letter maybe effective if the service is provided freeof charge, but may not be in certain set-tings if women have to pay for the test.

The types of intervention that havebeen investigated include strategiestargeting individual women, health-care providers and communities.

Strategies targeting individualwomenInvitation lettersOf the 29 studies presented in Table57, 15 evaluated the effectiveness ofinvitation letters compared with a con-trol group with no intervention(McDowell et al., 1989; Pierce et al.,1989; Clementz et al., 1990; Ornsteinet al., 1991; Lancaster & Elton, 1992;Bowman et al., 1995; Lantz et al.,1995; Pritchard et al., 1995; Binstocket al., 1997; Buehler & Parsons, 1997;Somkin et al., 1997; Burack et al.,1998; Del Mar et al., 1998;Torres Mejiaet al., 2000; Vogt et al., 2003).Invitation letters significantly increasedscreening uptake in 10 of these stud-ies. Two studies found a non-signifi-

cantly better participation in the controlgroup (Clementz et al., 1990; Del Maret al., 1998). In the one by Clementz etal. (1990), subjects were offered up toseven other screening tests in thesame letter (including faecal occultblood test, digital rectal examination,sigmoidoscopy, pelvic bimanual exam-ination, breast examination and mam-mography), so it is difficult to draw con-clusions related only to cervical cancerscreening, as the reasons for lowattendance may be related to howpatients react when invited for severalscreening tests. Additional evidencefrom programme evaluations (notincluded in Table 57) confirms theimportance of the invitation letter. Forexample, a screening programme inDenmark issued personal invitations totarget women over a period of 15years. The participation among womenaged 30–50 was 91% (Lynge et al.,1992). After that, personal invitationswere stopped and participation in thesame age group dropped to 66%.

The context of the trial and thecharacteristics of the letter variedacross the studies in Table 57. Forexample, in two studies (Burack et al.,1998; Vogt et al., 2003), the letterswere accompanied by educationalbrochures. In six studies, letters werefollowed by mailed or phone reminders(McDowell et al., 1989; Ornstein et al.,1991; Lantz et al., 1995; Buelher &Parsons, 1997; Torres Mejia et al.,2000; Vogt et al.; 2003). In the study byVogt et al. (2003), the increase inattendance was significant only whenthe letter was followed by a phonereminder; a letter followed by a mailedreminder led to no significant increase.

The two studies that analysed theeffect of sending a letter to minoritygroup women found no effect of theintervention (Del Mar et al., 1998; Huntet al., 1998). However, in one of these(Del Mar et al., 1998), the letter fol-lowed a media campaign introducedtwo months before in the whole region,

so an effect of contamination betweenthe intervention and control groupscannot be eliminated.

The only study conducted in adeveloping country found significantlyhigher participation among womenwho received an invitation letter(Torres Mejia et al., 2000). The projectwas carried out in the context of theMexican Social Security Institute,which provides medical services fornearly 60% of the Mexican population.In the total group of women invited, theeffectiveness of the intervention was20.1% versus 3.3% in the controlgroup. However, it may be difficult toadopt this strategy in other developingcountries due to the lack of mailinglists, ineffective or inexistent postalsystems and women’s difficulties inreading or understanding letters.

Two studies used invitation letterssigned by different authority sources.Significantly better participation wasobserved in the intervention groupsreceiving letters signed by GPs versus let-ters signed by female nurse practitioners(Bowman et al., 1995) or by programmecoordinators (Segnan et al., 1998).

Three studies explored the effect ofincluding a fixed appointment in the let-ter versus an open invitation to makean appointment (Wilson & Leeming.1987; Pritchard et al., 1995, Segnan etal., 1998); all found a favourable effectof a fixed appointment. For example, inItaly, the overall compliance withscreening was 36.1% when the lettersigned by the GP included a fixedappointment, but 22.7% when it onlyincluded a prompting to contact thescreening centre to make an appoint-ment (Segnan et al., 1998).

In three studies, invitation letterswere compared with phone invitations.Binstock et al. (1997) found that tele-phone invitations were more effective,whereas in the study by Mc Dowell etal. (1989) invitation letters were moreeffective. However, the latter studyincluded a reminder 21 days later if the

117-162 24/01/05 11:07 Page 154

155


a. 32%b. 47%Significant differences

a. 25.9%b. 16.1%c. 20%d. 13.7%Significant increase only for the GP letter

a. 32%*b. 27%*c. 15%*p <0.01Differences between intervention groups NS

a. 76%b. 49%p <0.001

a. 20.6%b. 30.3%NS differences

a. 30%*b. 26%*c. 11%#d. 5%*Difference with control group significant#Difference with control group NS

Slight decline in intervention group.

Wilson &Leeming(1987), UK

McDowell etal. (1989),USA

Pierce et al.(1989), UK

Robson etal. (1989),UK

Clementz etal. (1990),USA

McAvoy &Raza(1991), UK

Ornstein etal. (1991),USA

Screeninguptake

Test duringstudy year

Test duringstudy year

Test within pre-ceding threeyears

Test up to fourmonths afterthe intervention

Test within fourmonths afterthe intervention

Screeninguptake

.

NationalScreeningProgramme;women aged45–65 yearswith no recordof having a pre-vious smear

Hospital; no testin past year

General prac-tice; women reg-istered with ageneral practiceeligible for a test

General practice

Female patientsattending ambu-latory clinic;aged 50–69years

National screen-ing programme;Asian womenresident inLeicester, aged18–52 yearswith no recordof having had atest

Family medicineclinic; womenaged 18 yearsand over; notscreened in pre-vious 2 years;active patient ofthe family medi-cine centre (i.e.had visited clinicin previous 2years)

a. Letter of invitation to make anappointment + two reminders, N = 125 (122 analysed)b. Letter with an appointment date+ two reminders. N = 125 (118analysed)

a. GP letter and reminder letterafter 21 days. N = 367b. Physician reminder. N = 332c. Telephone call. N = 377d. Control group. N = 330

a. Letter asking women to have asmear. N = 140b. Physician reminder. N = 142c. Control group. N = 134

a. Patients had open access tohealth promotion nurse and hadtheir risk factors assessed and fol-lowed up by both their GP and thenurse. N = 799b. Control, usual care (i.e. man-aged by GP alone). N = 806

a. Personalized GP’s letter, onemonth before due date of testswith an educational component.N = 102b. Control group received usualcare (not described). N = 76

a. Home visit and a multilingualvideo. N = 263b. Home visit, multilingual leafletand fact sheet. N = 219c. Posted multilingual leaflet andfact sheet. N = 131d. Control group received no inter-vention. N = 124

a. Physicians received computer-ized reminders. N = 1988 partici-pants; 14 physiciansb. Participants were sent and invita-tion to attend followed by anotherpersonalized reminder letter (6months later). N = 1925 partici-pants, 12 physiciansc. Both physicians and participantreminders. N = 1908 participants,13 physiciansd. Control group, no intervention. N= 1576 participants, 10 physicians

Table 57. Studies evaluating interventions to increase cervical cancer screening attendance


117-162 27/01/05 16:03 Page 155

creo

156


a. 55%b. 67%NS differences.

a. 28% b. 13%p<0.001

a. 36.9%b. 22.6%c. 25.9%d. 24.5%Letter from the general practitioner signifi-cantly increased pap smear uptake.Differences between other groups andcontrol group NS.

a. 19%b. 6%[values recalculated from original data]Significant difference

a. 21.2%*b. 25.7%#c. 30.4%#d. 16.8%*NS difference with the control group# Difference with the control group statisti-cally significant.

a. 19.4%b. 13.7 %p <0.05.

Ward et al.(1991),Australia

Lancaster &Elton(1992), UK

Bowman etal. (1995),Australia

Lantz et al.(1995), USA

Pritchard etal. (1995),Australia

Yancey et al.(1995), USA

Test up to onemonth after theinitial consulta-tion

Test during asix week period

Screeninguptake at sixmonths afterthe intervention

Screeninguptake 6months afterthe intervention

Test within 12months ofentry into thestudy

Test within 5months afterthe intervention

General prac-tice; womenaged 20–65years; providedconsent

General prac-tice; womenaged 50–64years; residentin study area

Community andgeneral practice.Women aged18–70 yearswho reportedever having sex-ual intercourseand who had nothad a test in theprevious threeyears if a com-plete set of infor-mation wasavailable

Communityhealth centre;women aged40–79 years,enrolled in bene-fit scheme’ noclaim for Pap testin past 3 years

General practice;women aged36–69 years at auniversity generalpractice in asocio-economi-cally disadvan-taged area ofPerth

Health clinic;women attendingone of the twostudy clinics.

a. Minimal intervention: GP advised eligi-ble women of need for test and offered toperform it immediately. Those not con-senting advised to make appointment fortest within a week. N = 99b. Maximal intervention: GP advisedwomen of need for test and offered toperform it immediately; GP attempted topersuade those not consenting duringthat consultation by exploring barriers andreasons for self-exclusions. If still did notconsent, GP advised making an appoint-ment for test within a week. N = 103

a. Cervical screening invitation sent withbreast screening invitation. N = 474b. Breast screening invitation only sent(control). N = 483

a. GP reminder letter. N = 220 (178analysed)b. Women’s health clinic invitation forscreening by a female nurse practitioner.N = 220 (164 analysed)c. Mailed educational pamphlet personallyaddressed to women. N = 219 (162analysed)d. Control group (not stated) N = 219 (155analysed).Note: analysis carried out on women whoresponded to the follow-up survey

a. Reminder letter from primary-carephysician for test(s) required. Follow-upphone call/letter from a health educator(nurse or social work intern) 7–10 dayslater, to offer barrier counselling and/orassistance with appointment making.N = 337b. Control group received ‘usual care’ (notdescribed). N = 322

a. Physician reminder (tagged notes).N = 198b. Letter with invitation to make anappointment. N = 206c. Letter with fixed appointment. N = 168d. Control group (usual care). N = 185

a. Culturally sensitive health educationvideos dealing with breast and cervicalcancer played in waiting room. N = 868b. Control, no intervention. N = 876

Table 57 (contd)


117-162 24/01/05 11:07 Page 156

creo

157


a. 35.1%b. 26.4%c. 25.5%d. 23.9%e. 16.3%Differences with control group significantfor all groups. p < 0.001No significant differences between b, cand d

a. 10.7%b. 6.3%NS differences

a. 19.4%*b. 22.8%*c. 9.1%Difference with control group significant.p < 0.01

No significant increase

a. 29%b. 29%c. 32%d. 28%Differences with control group NS

a. 63.2%b.50.3 %p <0.002

.

Binstock etal. (1997),USA

Buehler &Parsons(1997),Canada

Somkin etal. (1997),USA

Sung et al.(1997)

Burack etal. (1998),USA

Margolis etal. (1998),USA

Screeninguptake at 12months afterintervention

Screeninguptake at 6months afterintervention

Test in the sixmonths follow-ing the inter-vention

Test up to sixmonths aftercompletion ofthe intervention

Screeninguptake duringthe study year

Screeninguptake 1 yearafter the inter-vention

Health maintenanceorganization.Women aged 25–49years, enrolled forthree years at theKaiser PermanenteHealth Plan whowere likely to seekout-patient care atone of the threemedical centres

Family medicineclinic. Patients of theclinics aged 18–69years who had nothad a test in theprevious three years

Health maintenanceorganization (HMO);women aged 20–64years, no test inprevious 36 months;residents of studyarea; continuouslyenrolled as a mem-ber of HMO for theprevious 36 months

Community; AfricanAmerican women;aged 18 years andolder

Health maintenanceorganization (HMO)Age 18–40 years;HMO member; visit-ed one of the prima-ry care study sites inthe previous years;had not had a test inthe previous year.

Community healthcentre; women aged40 years and overattending appoint-ments in the clinics;had not had a testin the previous year.

a. Telephone call. N = 1526b. Letter. N = 1526c. Memo to woman’s primaryprovider. N = 1526d. Chart reminder affixed to outside ofwoman’s medical record. N = 1526e. No intervention (control group).N = 1526

a. Personal letter and reminder letter4 weeks later (letter head of theprovincial cytology registry signed byco-investigators). N = 178b. Control group not received letter.N = 208

a. Letter signed by a physician invitingwomen to make an appointment.N = 1188b. . Letter signed by a physician invit-ing women to make an appointmentand chart. Providers encouraged bypresentations by researchers andmemoranda describing the project.N = 1188c. Usual care (required a referral froma physician). N = 1188.

a. Lay health workers visited womenthree times to provide a culturallysensitive educational programmeemphasizing need for screeningthrough printed material and video.N = 163b. Control group received educationalinformation on completion of follow-up

a. Patient reminder (invitation lettersigned by the HMO director) +National Cancer Institute educationalbrochure. N = 964b. Reminder for physician. N = 960c. Reminders for both physician andparticipants. N = 960d. Control (no reminder). N = 964

a. Lay health workers assessedscreening status and offered womenscreening with a female nurse practi-tioner. N = 566 (470 analysed)b. Usual care group. N = 536 (437analysed)

Table 57 (contd)


117-162 27/01/05 16:06 Page 157

creo

158


a. 36.1%b. 22.7%*c. 30.9%*d. 36.7%Personal invitation letters signed by theGP with prefixed appointments induced asignificant increase in compliance withscreening. p value not provided* Significant difference with group (a)

a. 56%b. 52%c. 64%Provider prompting, tailored educationalprint communications and tailored tele-phone counselling induced increasedcompliance, p = 0.05

a. 89.9%b. 87.7%Significant difference

\

a. 22%*b. 54%#c. 50%#d. 17%#p <0.0001*p = 0.16Interventions were more effective thanusual care except for the letter/letter onlyintervention. Letter with phone was aseffective as phone/phone outreach

a. 10%b. 12% NS differences

Segnan etal. (1998),Italy

Rimer et al.(1999),USA

Allen et al.(2001),USA

Vogt et al.(2003),USA

Del Mar etal. (1998),Australia

Screeninguptake at 12months afterthe initial invita-tion


Screeninguptakewithin pastthree years

Test within 12weeks after theintervention

Screeninguptake oneyear after theintervention

General practice innational screeningprogramme; womenaged 25–64 years;resident of Turin

Community healthcentre, women aged18 years or over;client of medicalcentre who had vis-ited centre in previ-ous 18 months(care for black, lowincome, low educa-tion population), hadnot had a test in thelast year

Worksite; women 40years and older whowere employed formore than 15 hoursper week on a per-manent basis

Health-care organi-zation; women aged18–70 who had atleast 3 years of con-tinuous membershipbefore the studywho had notreceived a test dur-ing the same 3-yearperiod

Community; womenaged 18–67 years;Vietnamese

a. Personal letter signed by GP withprefixed appointment (control). N =2100b. Personal letter, signed GP withopen-ended appointment. N = 2093c. Personal letter signed by pro-gramme coordinator with prefixedappointment. N = 2094d. Personal letter with extended textsigned by GP with prefixed appoint-ment. N = 2098

a. Provider prompting interventiononly. N = 202b. Provider prompting and tailorededucational print communications(Healthy Birthday cards) N = 204c. Provider prompting, tailored educa-tional print communications and tai-lored telephone counselling. N = 213

a. Intervention sites: Voluntary adviso-ry boards with worker participation;peer health advisors (PHA); groupsessions led by PHAs; one-to oneoutreach activities, worksite-widehealth education; other events. N =1489b. Control sites: no specific activities.N = 1308

a. Letter from the programme andbrochure followed by a second letterto women who had not had an exami-nation six weeks later after the firstcontact. N = 206b. Letter as in the first group followedby a phone call to all those notscreened in the first six weeks. N =113c. Phone call followed by a secondphone call to all those not screenedin the first six weeks. N = 88d. Usual care. N = 280

a. Personal letter in Vietnameseinforming them about screening andits benefits. N = 359b. Control group did not receive a let-ter. N = 330

Table 57 (contd)


117-162 24/01/05 11:07 Page 158

creo

Developing countries

159


a. 65.3%b. 61.1%NS differencesDifferences in increase between the control and the intervention NS

a. 6.7%b. 2.4%c. 0NS differences.

a. 39%b. 25%c. 15%a versus c, p <0.001b versus c, p = 0.03a versus b, p = 0.02

a. 61%b. 62%NS differences

a. 20.1%b. 3.3%Significant differences

Navarro etal. (1998),USA

Hunt et al.(1998),Australia

Taylor et al.(2002a),USA

Taylor et al.(2002),USA


Screeninguptake threemonths afterthe intervention

Screeninguptake

Screeninguptake in thelast twelvemonths.

Latino community,18 years and older

Community healthcentre; aboriginalwomen seen morethan twice in thepast three yearsand had no recordof hysterectomy,had not had a testin the last 3 years

Community;Chinese women20–69 years of age;spoke Cantonese,Mandarin orEnglish, had no his-tory of invasive cer-vical cancer andwere under-utilizersof screening

Community;Cambodianrefugees in Seattle;women aged 18 andolder

Mexican SocialSecurity Clinics(Morelos). Women20–64 years whohad not had a testin the previous 12months

a. Por La Vida (PLV) programme withcommunity workers (consejeras) tak-ing 12 weekly educational sessionswith the groups of women. N = 274;analysed 199b. Control, no PLV programme; insteadconsejeras participated in a communi-ty living skills programme. N = 238;analysed 162

a. Personal approach. Womenapproached by aboriginal health work-ers and invited for screening. N = 119b. Letter. Designed by aboriginal work-ers stating individual overdue for testand inviting them to attend. N = 125c. Control. Usual care with remindertags for clinic staff attached to medicalrecords. N = 122

a. Culturally appropriate outreachworker intervention. Health education,video, motivational pamphlet, educa-tional brochure and a fact sheet. Homevisits, tailored counselling by outreachworkers. N = 161; analysed = 129b. Direct mail with a cover letter, theeducation video, motivational pam-phlet, educational brochure and factsheet. N = 161; analysed = 139

c. Control: usual care. N = 160;analysed = 134a. Introductory mailing, home visitincluding educational video and tai-lored counselling; group meetings. N= 144b. Control: usual care. N = 145

a. Intervention: Letter of invitation andreminder. N = 2119b. Control group not received letter. N= 2100

Table 57 (contd)


Minority groups

TorresMejia et al.(2000),Mexico

Screeninguptake upto 8.5weeks afterthe inter-vention

117-162 24/01/05 11:07 Page 159

creo

women did not respond to the first let-ter, whereas in the former no reminderwas sent after the phone call. When aphone call was followed by a secondphone call to all women not screenedin the first six weeks, it was more effec-tive than a letter followed by a mailedreminder (Vogt et al., 2003). Thesethree studies also compared an invita-tion phone call and no intervention. Inall three studies, the uptake of screen-ing was higher in the phone call group,but not significantly in the study byBinstock et al. (1997). In the study byVogt et al. (2003) the phone–phoneapproach was as effective as a let-ter–phone approach. However, the let-ter followed by a phone call was themost cost-effective approach. It wasestimated that the phone–phoneapproach produced one additionalscreening for $305 versus $185 withthe letter–phone approach.

Personal approachThe efficacy of a personal contact wasevaluated in six studies (McAvoy &Raza, 1991; Sung et al., 1997; Hunt etal., 1998; Margolis et al., 1998; Tayloret al., 2002a, b). The face-to-faceapproach significantly increasedscreening uptake in three of them(McAvoy & Raza, 1991; Margolis et al.,1998; Taylor et al., 2002a). However,the conditions under which the per-sonal contact took place varied enor-mously from study to study. In thestudy by Margolis et al. (1998), layhealth workers approached womenattending a community health centreand offered screening with a femalenurse practitioner. The effectiveness ofthis approach was evaluated in relationto usual care; 63.2% of the invitedwomen complied with screening versus 50.3% in the control group.However, 36% of randomized womencancelled or missed appointments, sothey were not contacted at all and werenot included in the final analysis. Witha strategy based on approaching

women attending a health centre, non-users will never be reached. Tayloret al. (2002a) evaluated home visitsthat included delivering educationalmaterial (a health education video, amotivational pamphlet, an educationalbrochure and fact sheet) and providingtailored counselling, in comparisonwith only mailing the educational mate-rial and with a control group receivingusual care. The first approach was themost effective in increasing participa-tion rates. However, no data on costswere provided; as up to ten attemptswere made to contact each woman inthe first group, it would presumablyhave been the most expensive.

Educational interventionsTen studies evaluated different types ofeducational intervention includingprinted material (Rimer et al., 1999;Bowman et al., 1995), video/slide pre-sentations (Yancey et al., 1995), face-to-face contacts (Navarro et al., 1998;Allen et al., 2001) or combinations ofvarious educational approaches (Tayloret al., 2002a, b; McAvoy & Raza, 1991;Sung et al., 1997). Mailed printed mate-rials do not appear to increase uptakeof screening. For example, in Australia,Bowman et al. (1995) found that mailededucational pamphlets personallyaddressed to women did not increaseuptake compared with a letter from theGP without the educational pamphletor a control group (no intervention).Educational video tapes were found tobe effective compared with no interven-tion, both when mailed (Taylor et al.,2002a) and when played in a health-care setting. For example, video pre-sentations played in the waiting roomof health clinics increased uptake ofscreening among women attending theclinics in the USA by around 30%(Yancey et al., 1995).The effectivenessof face-to-face educational interven-tions seems to be low, as no (Navarroet al., 1998) or modest (Allen et al.,2001) effect was found in the two stud-

ies included. However, the face-to-faceapproaches differed greatly. Navarro etal. (1998) compared the effect of 12educational sessions on cervical cancerscreening with the effect of 12 educa-tional sessions about living in the com-munity. Allen et al. (2001) invited womento a group meeting carried out in theirworkplace. Multi-component interven-tions seemed to be the most effectiveapproach (Allen et al., 2001;Taylor et al.,2002a). For example, Allen et al. (2001)found that health education provided inworkplaces together with worker partici-pation, group sessions and one-to-oneoutreach activities significantlyincreased the uptake of screening.

Counselling, with exploration ofpossible barriers to screening and rea-sons for self-exclusion, to persuadethe woman to have screening wasanalysed in three studies. In the USA,Rimer et al. (1999) found that comple-menting the physician’s reminder andmailed tailored educational print commu-nication with tailored telephone coun-selling increased participation. Atten-dance was increased in a general prac-tice setting in the United Kingdom ifpatients had access to a health promo-tion nurse and had their risk factorsassessed and followed up by both theGP and the nurse (Robson et al., 1989).In contrast, Ward et al. (1991) found nosignificant difference in Australiabetween a minimal intervention by whichGPs advised eligible women to bescreened and a maximal interventionduring which they also attempted to pro-vide counselling. However, since theaverage time spent on counselling wasonly 91 seconds (range 6 seconds to 3minutes and 44 seconds), it is impossibleto determine whether counselling wasreally ineffective or if insufficient time wasallocated to perform it effectively.

Strategies targeting health-careprovidersDespite the recognized influential roleof doctors in promoting screening,

160


117-162 24/01/05 11:07 Page 160

161


many women still report that their doc-tor failed to recommend screening.Seven of the studies included in Table57 evaluated the effect of several typesof physician reminder (including a flagreminder affixed to the woman’s medical record) versus a control groupwith no intervention (Binstock et al.1997; Burack et al., 1998; McDowell etal., 1989; Ornstein et al., 1991;Pritchard et al., 1995; Pierce et al.,1989; Somkin et al., 1997). Only two ofthese studies found a significantincrease in screening uptake com-pared with no intervention (Binstock etal., 1997; Pierce et al., 1989). However,no differences were found between thephysician reminders and other types ofintervention measured in these two stud-ies (i.e., telephone or mailed invitationssent to women).

In the United Kingdom, target pay-ments for GPs have been linked to thelevel of coverage achieved, with thepayment for coverage of 80% or overbeing almost four times that for 50% to79%. Introduction of such paymentsled to a dramatic improvement in cov-erage, from less than 40% to over 80%(Patnick, 2000; NHS 2003a, b).

Community strategiesMass media campaignsThe impact of mass media campaigns inincreasing attendance in cervical cancerscreening was summarized in a reviewof different strategies by Black et al.(2002). Studies included in this reviewshowed that mass media campaignscombined with other strategies wereeffective at increasing either screeningrates or early cancer detection. Of thefour studies reviewed that used massmedia campaigns alone (Suarez et al.,1993a, b; Mitchell et al., 1997; Suarez etal., 1997), only one was effective, in aspecific subpopulation targeted with lan-guage-specific materiel (Mitchell et al.,1997). Shelley et al., (1991) reported anincreased attendance in New SouthWales, Australia, after a mass media

campaign including television and radiocommercials, advertisements in twowomen’s magazines and posters andpamphlets distributed to GPs.

Involving family and communitymembersFor many women, particularly those ofethnic or minority groups in developedcountries and women in developingcountries, their decision about cervicalcancer screening will be greatly influ-enced by the husband or other key fam-ily and community members (Lazcano-Ponce et al., 2002). Involving family andcommunity members has been pro-posed as an important strategy toincrease attendance in screening pro-grammes. However, there is limited evi-dence on the effectiveness of thisapproach. In a randomized controlled trialcarried out in rural India to evaluate theeffectiveness of VIA (Sankaranarayananet al., 2003b), the main components of theproject included health education activi-ties, personal invitations, mobile clinicsand involving key members and leadersof the community. Attendance reached63.4%, which represents a reasonablelevel considering that no women had everbeen tested previously in the region.

Strategies to improve follow-upafter an abnormal test resultObtaining good levels of attendance forscreening is a necessary but insufficientcondition for effectiveness of a cervicalcancer screening programme. Screenedwomen with abnormal tests must alsoreceive follow-up and appropriate treat-ment. Rates of incomplete follow-upvary enormously across settings andpopulations; between 7 and 49% ofwomen with abnormal test results fail toreceive adequate follow-up (Yabroff etal., 2000) and a study in the Amazonianregion of Peru found that only 25% ofwomen with abnormal cytology receivedappropriate follow-up care (Gage et al.,2003). Despite the importance of assur-ing good levels of compliance with fol-

low-up, most efforts have focused onincreasing attendance in screening pro-grammes. For example, in a CochraneReview of strategies to increase atten-dance at cervical cancer screening(Forbes et al., 2004), only three of theselected 35 studies were about compli-ance with follow-up.

A notification letter including someeducational material was evaluated intwo studies (Paskett et al., 1990;Marcus et al., 1992). Adding educa-tional materials to the notification letterdid not have a significant impact on theuptake of follow-up visits in any of thesestudies except in the group that alsoreceived an educational slide-tape pro-gramme (Marcus et al., 1992). In thisstudy, providing transportation incen-tives increased the odds of follow-upcompared with women receiving usualcare, but the effect was lower than thatobtained with the letter plus slide-tapeprogramme. A combination of computer-ized tracking of follow-up, transportationand financial incentives yielded only alimited increase in the intervention groupin relation to the control group (Kaplan etal., 2000). An invitation to consult anurse who presented educational infor-mation about abnormal tests did notresult in a significant difference betweenthe groups (Peters et al., 1999).

Although educational interventionshave been shown to improve women’sknowledge about the meaning of anabnormal test result, whether thisimproved knowledge correlates withlower anxiety or improved adherencefor follow-up is unclear (Zeisler et al.,1997; Fylan, 1998).

Studies using alternativescreening approachesAlternative methods are being evalu-ated to provide simple and low-costscreening in developing countrieswhere organizing a cytology-basedprogramme is not feasible (Sankaran-arayanan et al., 2001). Combining testing with an immediate offer of treat-

117-162 24/01/05 11:07 Page 161

ment for screen-positive women hasbeen shown to be a feasible option inlow-resource settings (Gaffikin et al.,2003). One advantage of the "see-and-treat" or "screen-and-treat" approachesis that they reduce the need for follow-up visits and thus decrease the proba-

bility of loss to follow-up. Severalrecent studies have evaluated compli-ance with treatment using thisapproach. For example, in a VIA-baseddemonstration project in rural Thailand,nearly 93% of screen-positive womenreceived cryotherapy in a "screen-and-

treat" scheme (Gaffikin et al., 2003). InIndia, compliance with treatment forhigh-grade lesions was 74%; in thisstudy, cryotherapy was offered on a"see-and-treat" basis and LEEP wasprovided through referral to a hospital(Sankaranarayanan et al., 2003b).

162


117-162 27/01/05 16:07 Page 162

Documents

Chapter 3 Use of screening for cervical cancer - IARC · Chapter 3 Use of screening for cervical cancer ... Organized screening programme 117-162 24/01/05 11:07 Page 117. 118