Brote Sar Hamburgo Eurosurv 2012 Art20194

7/30/2019 Brote Sar Hamburgo Eurosurv 2012 Art20194

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1www.eurosurveillance.org

Surveillance and outbreak reports

Description o measles D4-Hamburg outbreak inHamburg, Germany, December 2008 to June 2009,which disproportionally afected a local Roma

communityG Hy ([email protected].)1, K Kz2, M H3, A Mz4, S Bm5, A W6, G F1

1. Centre or Inectious Disease Epidemiology, Institute or Hygiene and Environment, Hamburg, Germany2. Public Health Department o Hamburg-Mitte, Hamburg, Germany3. Public Health Department o Hamburg-Harburg, Hamburg, Germany4. National Reerence Centre Measles, Mumps, Rubella, Robert Koch-Institute, Berlin, Germany5. Department o Microbiological Consumer Protection, Institute or Hygiene and Environment, Hamburg, Germany6. Department o Medical Microbiology, Institute or Hygiene and Environment, Hamburg, Germany

C y f h :Hegasy G, Ktzner K, Helle M, Mankertz A, Baumgarte S, Wille A, Fell G. Description o measles D4-Hamburg outbreak in Hamburg, Germany, December 2008 toJune 2009, which disproportionally afected a local Roma community. Euro Surveill. 2012;17(24):pii=20194. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20194

Article submitted on 27 October 2011 / published on 14 June 2012

From December 2008 to June 2009 a measles outbreakoccurred in the Federal State of Hamburg, Germany.The outbreak affected 216 persons and was caused bya new measles strain termed D4-Hamburg which led toconsecutive outbreaks between 2009 and 2011 in atleast 12 European countries. Here, we describe epide-miological characteristics of the outbreak and evalu-ate the control measures taken in Hamburg. In one of

the seven boroughs of Hamburg a local Roma commu-nity comprised more than 50% of the notified cases.We compared in a stratified analysis the age distribu-tion of these cases with cases of fellow citizens whodid not belong to the Roma community. The age groupof infants (0-11 months) comprised 33% among thenon-Roma measles cases, while in the Roma commu-nity only 4% belonged to this stratum. In the stratumof 5-17 year-olds only 8% were affected among thenon-Roma cases, whereas in the Roma community50% belonged to this age group. We discuss the influ-encing factors that might have led to this difference inage distribution between the two groups.

BackgroundIn December 2008 a measles outbreak started in thecity o Hamburg, reached its peak during Februaryand March 2009 and ended in June 2009 [1]. As dem-onstrated later by molecular typing, this outbreak wasthe origin o European-wide spread o a measles strainclosely related to D4-Enield, but later classiied asa separate strain on the basis o sequence analysis.Consequently this strain was named D4 Hamburg. Thespread o this D4-Hamburg virus continued in Europein the ollowing three years and led to consecutive out-

breaks in Bulgaria, Poland, Ireland, Northern Ireland,Austria, Greece, Romania, Turkey, Macedonia, Serbia,Switzerland and Belgium with over 25,000 personsinected [2].

The ollowing surveillance data on the D4-Hamburgoutbreak concerning age, vaccination status and hos-pitalisation rate o cases have been published earlier[1,2] and are only briely summarised here: The agerange o cases was 1 day to 54 years; the mean agewas 14.6 years and the median age was 13.5 years. Avaccination card was available or 196 o 216 cases(91%). O these, 157 cases had no record o immunisa-

tion with measles-containing vaccine (MCV), including28 cases below the recommended vaccination age o11 months. O 39 cases with a record o MCV immuni-sation, one dose was documented or 33 cases, twodoses or three cases, and or three cases the recordwas ambiguous. O the 33 cases with one documenteddose, 26 were contacts who had received a combinedmeasles-mumps-rubella vaccine (MMR) as post-expo-sure prophylaxis, but still developed the disease. Nocase ulilled the criteria or application o passive pro-tection using antiserum according to guidelines o theGerman Standing Committee on Vaccination (StndigeImpkommission, STIKO) [3]. The hospitalisation ratewas 40%, with pneumonia and otitis media as the mostrequent complications. No atality was reported in thisoutbreak.

Measles virus inection has been a notiiable diseasein Germany since 2001 according to the CommunicableDisease Law Reorm Act (Inektionsschutzgesetz,ISG). Vaccination guidelines are provided by theSTIKO, which is ailiated to the Robert Koch Institute(RKI) representing the ederal institution or diseaseprevention and control in Germany. According to STIKOguidelines, a irst dose o MCV should be given at the

age o 11 to 14 months and a second dose at the age o15 to 23 months, preerably using combined MMR vac-cine [3]. For individuals missed in the regular sched-ule, catch-up vaccination is recommended. Since 2010,


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the STIKO has additionally recommended a single doseo MCV to be given to any person born ater 1970 whohas not received two doses o MCV or does not havea medical record o a subsided measles inection [4].This decision to extend MCV immunisation to adultswas taken as a result o continuing measles outbreaksin Germany, including the outbreak described here [5].

To meet the WHO European Region measles eliminationtarget by 2015, a vaccination coverage o 95% or twodoses o MCV is necessary [6]. According to assess-ment at school entry, adequate vaccination status hasincreased in Germany over the last 10 years, but cov-erage is still below this threshold (Germany 90.2%,Hamburg 90.5%) [7]. Furthermore, underserved minori-ties have repeatedly been involved in large outbreaks inGermany [8,9]. Here, we describe the measles outbreakin the Federal State o Hamburg in 2008-09, which dis-proportionally aected a local Roma community.

MethodsFor the D4-Hamburg outbreak description, data romthe electronical surveillance system were re-evaluatedaccording to ISG using SurvNet sotware o RKI. Thesenotiication data include case inormation on age, sex,onset and duration o disease, clinical symptoms, lab-oratory conirmation, epidemiological links betweencases and vaccination status i available. In addition,semi-structured records on contact tracing and out-break containment measures o the seven public healthdepartments o Hamburg were evaluated.

Cases were deined as persons with a) a generalisedmaculopapular rash or more than three days ANDever AND at least one o the ollowing symptoms:cough, coryza, conjunctivitis or Koplik spots, OR b) ageneralised maculopapular rash or more than threedays AND/OR ever, AND laboratory diagnosis o mea-sles inection. Persons with laboratory diagnosis o ameasles vaccine strain were excluded.

Measles virus RNA in nasopharyngeal swabs or oralluid was detected by real-time RT-PCR perormed atthe municipal Institute or Hygiene and Environmentas described earlier [10]. Genotyping was perormedat the National Reerence Centre (NRC) or Measles,Mumps, and Rubella as described earlier [11].

Analysis o the cases areas o residence by post-code and cartography was perormed employingthe Geographical Inormation System sotware ESRIArcGIS.

Outbreak description

Epidemic curve and geographical distributionThe outbreak started in 2008 with a case in week 49

and a second case in week 52. It continued in 2009rom week 2 to week 25 with 214 cases (Figure 1). Thecase in week 52 o 2008 was initially termed as theindex case or Hamburg, although the patient alling ill

Figure 1

Epidemic curve of measles D4-Hamburg outbreak,Hamburg, 1 December 200817 June 2009 (n=216)

Cases were assigned to the corresponding week according toappearance o irst measles symptoms.

0

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48 49 50 51 52 1 2 3 4 5 6 7 8 9 10 1 1 12 1 3 14 1 5 16 1 7 18 19 20 21 2 223 24 25 26

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2009

Numberofcases

Week

Schleswig-

Holstein

Hamburg

Lower

Saxony

Figure 2

Outbreak location in the Federal State of Hamburg,Germany, bordering Lower Saxony and Schleswig-Holstein, 1 December 200817 June 2009 (n=216)


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in week 49 o 2008 was retrospectively counted in asbelonging to the outbreak as well. The outbreak lastedor 29 weeks with highest case numbers between week6 and week 10 o 2009 (Figure 1).

Between week 3 and week 18 o 2009 the outbreakexpanded to Lower Saxony, a bordering ederal state

south o Hamburg (Figure 2). Here, 53 cases were noti-ied. Within the city limits o Hamburg the outbreakwas mainly localised in the boroughs south o the riverElbe with a ocus on the boroughs o Hamburg-Mitteand Harburg (Figure 3). To analyse the spatial distribu-tion o the outbreak in more detail, postcodes o thecases place o residence were mapped using geoinor-mation sotware at the Centre or Inectious DiseaseEpidemiology. As demonstrated by this approach, eighto 21 postcode areas were aected in this borough. Thehighest incidences were restricted to the two postcodeareas in the district o Wilhelmsburg (Figure 4).

Clinical and laboratory-confirmed casesFor 207 o the 216 cases the diagnosis was based onthe clinical presentation and 190 o the 216 cases werelinked to another case epidemiologically. For 149 o the216 cases a laboratory conirmation was notiied rep-resenting 69%. For 100 o them laboratory diagnosiswas based on PCR, o which 78 were conirmed by PCRalone, 20 by PCR in conjunction with IgM detection,and one each by PCR in combination with rising IgGtitre or virus isolation. A urther 44 o the 149 labora-tory-conirmed diagnoses were based on IgM detectionalone, while our cases were based solely on rising IgG

titre. One case was conirmed by virus isolation in con-junction with IgM detection.

In addition to patients who received laboratory con-irmation o measles inection by their amily doctor,physicians o the public health departments oeredimmediate laboratory diagnostics during contact trac-ing to potentially inected individuals. To this endnasopharyngeal swabs or oral luid were taken andanalysed or measles virus RNA by real-time RT PCR.Laboratory analyses were oered ree o charge to thepublic health departments o Hamburg by the munici-pal Institute or Hygiene and Environment. O 174 per-sons rom whom nasopharyngeal swabs or oral luidwere taken during contact tracing, 100 were ound pos-itive. This represents 67% o all laboratory-conirmedcases o the outbreak. For sequencing and geneticstrain analysis, 23 swabs were sent to the NRC. Twelveo them were identiied as the virus strain later termedD4-Hamburg [2]. Ten samples that were ound positivein diagnostic PCR could not be sequenced successully.For one sample sequencing revealed an inection withthe vaccine virus, and consequently this patient wasnot counted as a case.

Index caseOn 27 and 28 December 2008, a patient in their 20spresented to the outpatient department (OPD) o a

hospital in Hamburg. The patient had suered rom asore throat since 24 December 2008 and had devel-oped a rash ater taking acetylsalicylic acid. Underthe assumption o streptococcal pharyngitis and drugeruption ambulatory treatment with amoxicillin, par-acetamol and an anti-histamine was given. Because

the patients condition deteriorated, they presentedon 29 December 2008 to the OPD o a second hospi-tal where inection with measles virus was suspectedand the patient was hospitalised. As any case o

Figure 3

Measles cases in the seven boroughs of Hamburg, 1December 200817 June 2009 (n=216)

Wandsbek19(4.1)Nord

11(3.8)

Eims-bttel

5(1.9)

Altona12

(4.8)RiverElbe

Bergedorf6

(5.0)

Mitte107(43.7)Harburg

56(29.6)

Number of Cases

0

1 - 5

6 - 20

21 - 100> 100

Incidence per 100,000 is given in parentheses.

3 (0.13)

3(n.d.)

1 (n.d.)

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0

00 0 0

00

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2(0.08)1 (0.06)

6 (0.45)

16(0.60)

75(3.05)

Number of Cases

0

1 - 5

6 - 20

21 - 100

> 100

Figure 4

Measles cases in the borough of Hamburg-Mitte bypostcode areas of residence, 1 December 200825 May2009 (n=107)

Incidence per 100,000 is given in parentheses. For two postcodeareas extending outside the borough borders o Hamburg-Mitte,the incidence was not determined (n.d.).


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clinically suspected measles has to be notiied accord-ing to the ISG, the responsible public health depart-ment received a report on this case on 31 December2008. Laboratory diagnosis later conirmed the inec-tion by demonstrating positive IgM titre against mea-sles virus and increasing IgG titres.

First and following generations of casesThe OPD visited irst by the index patient was highlyrequented between Christmas and New Year. The wait-ing area was overcrowded and patients had to wait orseveral hours. Potentially inectious patients were notseparated. Between 8 and 11 January 2009, ive per-sons that had been present in this OPD on 27 or 28December 2008 ell ill with measles. These comprisedtwo patients present in the waiting area or accidentand emergency consultation, our persons accompany-ing patients to the OPD or medical advice in internalmedicine or accident and emergency, and one hospitalsta. All ive cases were notiied by their physicians

according to the ISG. Further spread rom these ivecases to household contacts was traced by the pub-lic health departments. In the entire outbreak, one ormore, transmission chains were identiied at each othe aected publicly accessible sites such as kinder-gartens, primary and secondary schools, shoppingcentres, and waiting areas o medical practices. Exactnumbers cannot be given because not all records ontransmission sites were accessible or retrospectiveevaluation.

Spread in a Roma community

On 26 January 2009, the public health department oHamburg-Mitte received a report on a measles casein a woman in her 20s who was in her 16th week opregnancy when she was diagnosed with measles on16 January 2009. As part o the contact tracing activi-ties, a home visit was paid to this patient. She declaredunquestioned that she belonged to a settled Romacommunity that traditionally lives in this borougho Hamburg. She urther stated that all contact per-sons named by her also belonged to that community.Consequently, she was regarded as the index case orthe Roma community. In the ollowing nine weeks, 60persons who indicated that they belonged to the samecommunity ell ill with measles. O those, 56 caseslived in Hamburg-Mitte which represents 52% o the107 cases reported in this borough. The last case othe community ell ill on 19 March 2009. Additionally,in Lower Saxony seven cases stated that they belongedto the ethnic group o Roma.

On subsequent home visits paid to the community, twomore cases were identiied who had occurred earlierthan the case regarded initially as the Roma commu-nity index: On 2 December 2008, an adolescent romthe community was diagnosed with measles. The

patient had been visited by relatives rom London inthe month o November 2008. This case was notiied,but notiication reached the responsible public healthdepartment with a delay o several weeks. Although no

link could be ound to the patient who later presentedto the OPD, this adolescent was most likely the trueindex case o the measles D4-Hamburg outbreak. On17 December 2008 the patients older sibling ell illwith measles. No notiication o this case was receivedalthough the patient had been seen by a physician. Theolder sibling was acquainted with the pregnant woman

ormerly regarded as the Roma community index case,but stated no personal contact to her. Even assuming amaximal length o inectious and incubation period (9and 21 days, respectively), disease onset in the oldersibling occurred at least ive days too early to allowa direct virus transmission rom them to the preg-nant woman. Thus, it is highly probable that at leastone more connecting case occurred in the communitythat was not seen by a physician, misdiagnosed or notnotiied.

Control measuresIn all boroughs o Hamburg control measures were

taken, but actions were ocused on those boroughssouth o the river Elbe where most cases were reported.Visits were paid to 34 community acilities such as kin-dergartens, primary schools and secondary schools.A community acility was selected or a visit i a casehad occurred there, i a contact o a case attended thatacility, or i it was located in a district highly aectedby the outbreak. On these occasions, 364 doses oMCV were given on site to children as well as teach-ers and sta. Another 497 children who could not pro-duce parental consent to vaccination were advised toreceive MCV rom their amily doctor. A total o 701

persons attending or working at the community acili-ties could not provide proo o MCV immunisation or amedical record o a subsided measles inection, andwere, based on ISG, suspended or two weeks romtheir last potential contact to an inectious person.

In the context o enhanced measles surveillance,the requency o case notiications rom local healthdepartments to RKI was increased rom weekly to daily.In parallel, surveillance data were evaluated and com-piled by the Centre or Inectious Disease Epidemiologyor brieings o the State Health Department o Hamburgand or press releases targeting either the general pub-lic or speciically local physicians.

To provide inormation on measles to residents oaected districts and to oer low-threshold accessto vaccination, a promotional bus was borrowed romthe German Organisation or the Protection o Children(Deutscher Kinderschutzbund Hamburg, DKSB) andallocated or medical advice on measles prevention.Sta included two physicians, two assistants, and atleast two interpreters. Interpreters were health media-tors o the programme With Migrants or Migrants (MitMigranten r Migranten, MiMi) which is described in

detail elsewhere [12]. The promotional bus was openedon six occasions or our hours at central public placesin the borough o Hamburg-Mitte. On these occasions


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964 consultations were requested and 18 MMR vacci-nations were given.

To speciically reach the Roma community, 10 homevisits were paid by the Public Health Departmento Hamburg-Mitte to Roma patients and their con-tacts between 19 January and 5 February 2009. Sta

included a physician and at least one assistant. Onthese occasions, vaccination cards were controlled andMMR immunisation was oered as well as laboratorydiagnostics by nasopharyngeal swabs or oral luid. Nodata were recorded separately or the Roma communityconcerning the number o persons seen, contact per-sons traced or vaccinations given, but on these occa-sions 19 PCR-positive measles cases were identiied inthe community.

Age distribution of cases in Hamburg-MitteO 107 cases notiied in the borough o Hamburg-Mitte,56 belonged to the Roma community. We considered

these surveillance data as suitable or urther analy-sis with respect to the aected Roma and non-Romacommunity in Hamburg-Mitte. No signiicant dier-ence in sex distribution o inected individuals wasseen between both groups (non-Roma: 28 male and23 emale, Roma: 29 male and 27 emale, chi-squaredtest, two-tailed p value: 0.747). As shown in Figure5A the mean age o the cases was 10.1 years or theRoma group and 11.8 years or the non Roma group,while their median age was one year or the non-Romaand nine years or the Roma group. As the dierencebetween mean and median in the non-Roma group

pointed to a non-Gaussian distribution, we wanted tostudy the age distribution in both groups in more detailand thereore deined ive age groups or a stratiiedanalysis. Stratiication was chosen as ollows accord-ing to the standard vaccination schedule as recom-mended by STIKO guidelines [3]: (i) inants under theage or receiving MCV (11 months), (ii) age range orscheduled administration o two doses o MCV (1223months), (iii) age range without scheduled vaccina-tions (24 years), (iv) age range or urther scheduledand catch-up vaccinations (517 years), (v) adults (18years). As shown in Figure 5B, the age distribution inthe strata (i) and (iv) diered between the groups.

DiscussionFor outbreak surveillance to be suicient, 80% o clini-cally diagnosed measles cases should according to theWorld Health Organizations guidelines, be laboratory-conirmed [6]. In the outbreak described here, 149 o216 cases (69%) were conirmed by laboratory analy-ses. O these 100 were identiied by PCR rom naso-pharyngeal swabs or oral luid, representing 67% othe tests. These PCR diagnostics were oered duringcontact tracing and home visits by the public healthdepartments and perormed at the municipal Institute

or Hygiene and Environment. In contrast to serologicalanalyses as a standard tool or laboratory diagnosiso measles inection, taking o nasopharyngeal swabsor oral luid or PCR is non-invasive and was easily

A

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Non-Roma community(n=51)

Roma community

Non-Roma community Roma community

(n=56)

B

9(18%)

17(33%)

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7(12%)

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28(50%)

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70%

80%

90%

100%

18 y

5-17 y

2-4 y

12-23 m

0-11 m

Age(years)

(n=51) (n=56)

Figure 5

Age distribution of affected Roma and non-Roma inthe borough of Hamburg-Mitte measles D4-Hamburgoutbreak, 1 December 200825 May 2009 (n=216)

A. Boxplot showing mean, median and quartiles o disease onsetage o aected Roma and non-Roma community. Figures aregiven in table below.

B. Stratiied age analysis. Cases were assigned to groups asindicated based on age at disease onset.

Mean MedianM Q1 Q3 Max

Non-Roma community 11,8 1 0 0 24 44

Roma community 10,1 9 0 3,8 15 31


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perormed by medical assistants. Ater arrival o thematerial at the Institute or Hygiene and Environment,PCR results were available within our to 24 hours andthus proved to be a ast and useul tool or laboratoryconirmation o suspected cases ound during contacttracing. The Institute or Hygiene and Environmentoered PCR analyses ree o charge to the public

health departments in Hamburg which do not have abudget or laboratory analyses. Furthermore, availabil-ity o nasopharyngeal or oral luid swab material wasa prerequisite or genetic comparison o the strainsby the NRC and identiication o the epidemiologicallinks o the D4-Hamburg virus in Europe [2]. In sum-mary, ree-o-charge PCR analyses provided a useultool or rapid case identiication, laboratory conirma-tion and genetic analysis o the measles strain in theD4-Hamburg outbreak.

Healthcare acilities can play an important role inmeasles outbreaks [13,14]. This was also true or the

outbreak in Hamburg, where an early ocus o virustransmission was a waiting area in a hospital, and atleast one urther transmission site was the waitingarea at a doctors practice. Among the irst generationo notiied cases a member o hospital sta was identi-ied. Later, a second case o measles in a nurse wasnotiied. Both cases had never received a dose o MCVaccording to their vaccination cards. The STIKO hassince 2007 recommended a single dose o MCV to begiven to non-immune healthcare sta, preerably as acombined MMR vaccination [15]. Still there is no obliga-tion to comply with this recommendation and control

o adequate vaccination status o their employees isthe responsibility o the healthcare acility. Suboptimalimmunisation coverage o healthcare proession-als in Germany has been described beore [16]. TheD4-Hamburg outbreak demonstrates again that pre-vention o disease transmission in healthcare acilitiesneeds to be addressed.

One o the measures to contain the outbreak was apromotional bus positioned in public places on sixoccasions, providing inormation and vaccinations.Counselling was requested by 964 visitors who, accord-ing to the physicians present, were almost exclusivelyadults on their way to the nearby shopping centres.Only 18 persons (less than 2% o visitors) acceptedon-site MMR vaccination. No data were recorded onage, sex or immunisation status, but it is likely thatmore visitors with inadequate measles protection didnot want to receive a vaccination on this occasion. Weconclude that the promotional bus as used in this out-break was appropriate or providing inormation onmeasles to the local public, but it was not eicient inpromptly raising vaccination numbers. We would there-ore recommend this approach in an outbreak situationwhere the main intent is increasing public awareness.

Furthermore, any outbreak containment measureshould record all accessible data in order to allow alater evaluation o the measures eiciency.

To speciically reach the Roma community, home vis-its were paid to Roma patients and their householdcontacts. This approach was chosen because otherattempts to establish contact with cases in the com-munity were unsuccessul. As reported by the outbreakinvestigation teams, initial visits to a household werereceived with apprehension. On subsequent visits,

members o the community stated that this may havebeen caused by an uncertainty to which public author-ity the team belonged and what their actual intentionwas. When a team member identiied themselves asa physician they were met with more trust on urthervisits, and contact tracing and outbreak investiga-tions became possible. During the home visits PCRdiagnostics could be oered without delay, whichallowed identiication o a total o 19 cases that oth-erwise might not have been notiied. Based on inor-mation gained during the visits the likely index patiento the outbreak was identiied retrospectively andthe initial transmission chain in the Roma community

could be partially reconstructed. Furthermore, pres-ence o a physician allowed on-site vaccinations in theRoma community. It is a shortcoming that no data wererecorded on the number o vaccinations given on thesevisits, but this measure might have contributed to theact that virus transmission stopped nine weeks ear-lier in the Roma community than in the non Roma com-munity o Hamburg-Mitte. In our experience, repeatedhome visits by a physician are an advisable approachto establish contact to this minority and to take imme-diate outbreak containment measures.

In a retrospective analysis we compared the age distri-bution o cases in the Roma community and the non-Roma community in the borough o Hamburg-Mitte.We considered the outbreak parameters as suitable orthis comparison or two reasons: (i) number o casesand sex distribution were similar in both groups, (ii)both groups were citizens o the same borough, with85% living in the same district as demonstrated bypostcode analysis. No reliable igures exist on the sizeo this settled Roma community in Wilhelmsburg, butas an estimate, the community may comprise severalhundred persons. It is a shortcoming o our analysisthat no statistical reerence igures are available tocompare age-related incidences in the two subpopula-tions. Thus, our data only describe case numbers asthey were recorded.

The most prominent dierences occurred in the stratao 011 month- and 517 year-olds. In the non-Romacommunity, 33% o 011 month-olds were inected withmeasles, compared with only 4% o the Roma com-munity. This age group consists o inants too youngor MCV immunisation according to STIKO guidelines.Their immune protection correlates with the level andpersistence o transerred maternal antibodies and

may depend on whether the mothers immunity wasacquired by natural inection or by vaccination [17].Other actors modiy this passive immunity, e.g. expo-sure to wildtype measles virus as a natural booster or


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age o the mother during pregnancy [18]. It is temptingto speculate that early protection in the Roma commu-nity described here may have been higher because themothers were exposed to wildtype measles inection,but this hypothesis could only be veriied i data ontheir measles immune status were available.

Only 8% o 517 year-olds were aected among thenon-Roma citizens, compared with 50% in the Romacommunity. For this age group standard and catch-upvaccinations including MCV are recommended accord-ing to STIKO guidelines. There are two mandatorycheckpoints in Hamburg or control o a childs vac-cination status by a physician, the irst on entry tokindergarten, the second on entry to school. The irstcheckpoint is unlikely to reach children o a Roma com-munity as they are usually parented by communitymembers. At school entry the main ocus is on control-ling the vaccination record, and in case o undervac-cination the parents are usually reerred to their amily

doctor. This reerral might be ineective with memberso a Roma community as they tend to make less useo standard healthcare and preventive services [19-21]. Thus, it is conceivable that the current approachto ensure adequate immunisation status o children inHamburg is more eective in the non-Roma than theRoma population, in which undervaccinated childrenand adolescents may accumulate.

In other measles outbreaks in Europe involvingRoma communities, the age distribution o cases di-ered between Roma and non-Roma citizens [22,23],

although the results o these analyses are divergent.This might be explained by dierences in the subpopu-lation analysed (e.g. Roma or Sinti), the living condi-tions o the subpopulation (e.g. settled or travelling),diversity in national vaccination schemes, and dier-ent approaches to implement vaccination programmesor underserved minorities.

The group o Roma has suered extensively rom thisoutbreak in Hamburg and in other European countries[24]. The D4-Hamburg outbreak demonstrates againthat strategies to raise measles vaccination coverageshould be speciically devised to target underservedpopulations. Furthermore, innovative outbreak con-tainment measures and vaccination programmes areneeded. In a review o the literature concerning theinteraction between Roma communities and healthservice providers, Hajio and McKee came to theconclusion that published research is sparse [25]. Wesuggest that studies are needed to better understandthe view o Roma community members towards thehealthcare sector in order to be able to create vaccina-tion programmes that are acceptable to this neglectedminority.

Acknowledgments

We would like to thank Jrg Thyro, Sabine Richtberg,Veronika Hellmund, Susanne Steinberg rom the PublicHealth Department Hamburg-Mitte and Katharina Traudt,Joachim Kanschik rom the Public Health DepartmentHamburg-Harburg or outbreak investigations. Furthermorewe would like to thank Markus Kirchner rom the NLGA,Hannover, or inormation on measles outbreak in LowerSaxony. Finally, we would like to thank Klaus Baumgardt

rom the Division or Environmental Monitoring, Hamburg,or instruction on geographic inormation system sotware.Cartography was based on standard maps rom the StateOice Geoinormation and Geodetic Survey, Hamburg.


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