Reserch rticles Differences in heptitis B infection rte between ethnic groups in ntentl women in Birminghm, United Kingdom, My 2004 to December 2008 M Cley (Michel.cley@wrwickshire.nhs.uk) 1, T Fowler 2, S Gretrex 3, A Wood 4 1. NHS Wrwickshire, Wrwick, United Kingdom 2. UK Deprtment of Helth, United Kingdom 3. Hert of Birminghm PCT, United Kingdom 4. University of Birminghm, United Kingdom Cittion style for this rticle: Cley M, Fowler T, Gretrex S, Wood A. Differences in heptitis B infection rte between ethnic groups in ntentl women in Birminghm, United Kingdom, My 2004 to December 2008. Euro Surveill. 2012;17(30):pii=20228. Avilble online: http://www.eurosurveillnce.org/viewarticle.spx?articleid=20228 Article submitted on 11 November 2011 / published on 26 July 2012 Heptitis B virus (HBV) is mjor cuse of morbidity nd mortlity worldwide. Although the United Kingdom (UK) prevlence of HBV is low, it is incresing. There is some evidence tht the rte of infection is much higher in some popultions living in Britin of non-white ethnicity or who were not born in Britin, compred with the British-born white popultion. We exmined the prevlence of HBV infection in pregnnt women through heptitis B surfce ntigen (HBsAg) or e-ntigen (HBeAg) in Birminghm UK between My 2004 nd December 2008 nd the effect of ethnicity on the reltive risk of infection. There ws significnt increse in the number of ntentl HBV infections detected over the study period from 106 cses in 2005 to 161 cses in 2008 (p=0.037). Women who define themselves s of blck Africn, non-british white nd Pkistni ethnicity hd mrkedly elevted rte of HBV infection (reltive risk (RR): 11.25, 5.87 nd 2.33 respectively) compred to the Englnd verge. Helth orgnistions tht serve popultions with high or incresing proportion of women originting from intermedite nd high HBV prevlence res of the world such s Afric, some prts of Europe nd Asi, should nticipte need for perintl nd postntl prophylxis to children born to HBV infected mothers. Introduction Heptitis B virus (HBV) is mjor cuse of morbidity nd mortlity worldwide. It is estimted to hve ffected two billion people, 350 million of which hve chronic infection [1]. The overll United Kingdom (UK) prevlence of chronic infection is low (<1%) prticulrly in pregnnt women, however the nnul number of heptitis B notifictions in Englnd nd Wles is incresing [1,2]. Although dt on the prevlence of heptitis B in the UK nd the impct of migrtion ptterns re limited, there is some evidence tht the rte of infection is much higher in people not born in Britin or of non-white ethnicity compred with the British-born white popultion reflecting the higher HBV prevlence in their countries of birth or fmily origin [3,4]. All pregnnt women in the UK re offered HBV testing s prt of the ntionl ntentl screening progrmme for infectious diseses. Women re offered HBV testing t their first ntentl ppointment, usully t 8 12 weeks of pregnncy. In the UK, pregnnt women with HBV infection re treted bsed upon the severity of disese, nd benefits of reducing virl ctivity blnced ginst potentil side effects nd the unknown tertogenicity of ntivirl tretment [5]. These judgements re mde by specilist physicins on cse-by-cse bsis. Verticl trnsmission of HBV infection occurs in 90% of pregnncies where the mother is heptitis B e-ntigen (HBeAg) positive nd in bout 10% of pregnncies where the mother is heptitis B surfce ntigen (HBsAg) positive, e-ntigen negtive. More thn 90% of infected infnts become chronic crriers [6]. In the UK, bbies born to HBV infected mothers should ll receive course of HBV immunistion strting with first dose of vccine t birth nd three further doses t one, two nd twelve months of ge. Bbies born to highly infectious mothers, this includes those who re positive for HBeAg, lso receive heptitis B immunoglobulin t birth. This regime reduces verticl trnsmission by 90% [1]. A booster vccine t round five yers of ge is lso recommended for those t ongoing risk. The Englnd verge rte of HBV infection in ntentl blood specimens is 350 per 100,000 specimens [7]. Fctors tht influence prevlence include geogrphicl loction of residence nd country of birth, with both people residing in urbn res nd people born in countries of high prevlence hving higher rtes of infection [1,7]. www.eurosurveillnce.org 1
The World Helth Orgniztion (WHO) hs ctegorised countries bsed upon the prevlence of HBsAg into high (more thn 8%), intermedite (2 to 8%) nd low (less thn 2%) prevlence countries [1]. The highest rtes of HBV infection in low prevlence countries re often in people who immigrte from high prevlence countries [8,9]. However those groups t highest risk often hve lower uptke of preventtive helth services due to lnguge brriers nd lck of wreness [10,11]. In immigrnts from high prevlence to low prevlence countries, difficulties in mstering the lnguge of the host country hs lso been found to correlte with poor levels of ntentl cre [12]. It is therefore importnt tht ntentl services meet the need of pregnnt women infected with HBV nd tht services dpt s the demogrphics of the popultion they serve chnges. This pper describes the differences in epidemiology of HBV infection in pregnnt women in lrge multiethnic city in Englnd. Methods Birminghm is the second lrgest city in the UK with popultion of pproximtely 1.1 million. Bsed on 2001 UK census dt, where ethnicity is self reported, nd other fctors ffecting popultion chnge, it is estimted tht 65% of the popultion re white British, 20% re of South Asin ethnicity nd bout 5% re from blck ethnic groups. Solihull is neighbouring metropolitn borough tht is continuous with Birminghm nd hs popultion of bout 220,000. The Birminghm nd Solihull Helth Protection Unit receives ll notifictions of women testing positive for HBsAg or HBeAg s prt of ntentl screening, who live within the boundry of the Birminghm nd Solihull re. All pregnnt women between My 2004 nd December 2008 who tested positive for HBsAg or HBeAg were identified s cses in this study. All cses were tested for HBsAg. In the vst mjority of ptients, HBeAg ws tested, lthough smll number filed to hve this test completed. Demogrphic detils were recorded for ll cses. Women who were identified s testing positive for HBV by ntentl screening in the time of this study, but who were previously known to hve been dignosed with HBV, were lso included in the study. Where women were identified in two or more seprte pregnncies during the study period, ll pregnncies were included to estimte the level of demnd for prevention nd tretment services. Repet pregnncies were excluded from ethnic group rte of infection nd reltive risk of infection clcultions, in order to void counting the sme cses more thn once. Duplicte cses were removed mnully. Regression nlysis ws used to exmine the chnges over time of the totl number of cses per qurter. Differences between the rte of HBV infection in different ethnic groups were lso exmined using chi-squred test. Ethnicity ws self reported by cses, choosing from predefined list of ethnicity ctegories. This is the recommended method for identifying ethnicity by the Office for Ntionl Sttistics (ONS) [13]. Ethnic ctegories were bsed on the 2001 census ctegories [13], but number of ctegories were combined to llow meningful comprisons. Membership of n ethnic ctegory is not defined by plce of birth, though this my be determining fctor in peoples choice of group, but rther the ethnic group person feels they belong to. Thus person defining themselves s of blck Africn ethnicity could be born in Afric or born in Britin but be member of the blck Africn community. The ethnicity ctegories comprised: (i) white British, denoting person of white ethnicity who considers their ethnic bckground to be predominntly of British origin, (ii) white other, person of white ethnicity who considers their ethnic origin from country other thn Britin, including the ctegory white Irish, (iii) blck Africn, (iv) blck Cribben, (v) blck other, person of blck ethnicity who considers their ethnic origin not to be in Afric or Cribben, (vi) Pkistni, (vii) Chinese, (viii) Bngldeshi, (ix) Indin, (x) Asin other, person of Asin ethnicity who considers their ethnic origin to be from tht of country other thn the countries listed bove. Ethnicity dt ws collected using the primry ethnicity identified by the cse. There ws no cpcity to cpture dul ethnicity ctegoristion, nd country of birth ws not collected. Denomintor dt on the ethnicity of ll pregnnt women ws only vilble for the yers 2007 nd 2008. The ctegoristion of ethnicity differed slightly between the HBV infected cses nd the denomintor dt becuse this informtion ws collected by different orgnistions. Cse dt ws collected by questionnire on epidemiology, which provided more detiled brekdown of ethnicity, whilst denomintor dt ws collected routinely by mternity services using broder ctegories s prt of usul cre. Therefore to clculte the rte of infection in different ethnic groups, it ws necessry to merge some ethnicity ctegories with others. For these purpose the cses with ethnicity ctegories Chinese, blck other, Asin other nd not stted were merged into the other ctegory. Where denomintor dt ws not required to clculte results, we used the entire dtset (My 2004 December 2008). Where denomintor ws required, for exmple to clculte the rte of infection in different ethnic groups, the dtset is restricted to cses in 2007 nd 2008 only. Confidence intervls were clculted using stndrd methods [14]. Results Between My 2004 nd December 2008, testing for ntentl screening for HbsAg nd HbeAg reveled 595 cses with HBV infection. Of these cses 130/595 (22%) were previously known to be infected prior to their pregnncy. Of the 130 known cses, 108 hd been dignosed in previous pregnncy within the study period. The mjority, 347/595 (58%), of cses were in the 25 34 yers-old ge groups (Tble 1). A totl of 407 2 www.eurosurveillnce.org
tble 1 Number of Birminghm residents dignosed with heptitis B on ntentl screening by ge group, United Kingdom, My 2004 December 2008 (n=595) Age group in yers Number of heptitis B cses <20 14 20 24 105 25 29 181 30 34 166 35 39 100 40 44 27 45 49 1 >50 1 Totl 595 tble 2 Cses of heptitis B dignosed on ntentl screening, by ethnic group, Birminghm, United Kingdom, My 2004 December 2008 (n=595) Ethnic group Number of cses Percentge (%) of cses (95% confidence intervls) Blck Africn 194 32.6 (28.8 36.4) Pkistni 146 24.5 (21.1 28.0) Chinese 67 11.3 (8.7 13.8) Other 51 8.6 (6.3 10.8) White other b 31 5.2 (3.4 7.0) Blck other c 25 4.2 (2.6 5.8) Bngldeshi 23 3.9 (2.3 5.4) Blck Crriben 17 2.9 (1.5 4.2) Indin 16 2.7 (1.4 4.0) Asin other d 13 2.2 (1.0 3.4) Not stted 8 1.3 (0.4 2.3) Not recorded 3 0.5 (0.0 1.1) White British 1 0.2 (0.0 0.5) Other ethnic group thn listed in the tble. b White other thn white British. c Blck other thn blck Africn nd blck Cribben. d Asin other thn Bngldeshi, Indin, Chinese nd Pkistni. of 595 cses (68%) were in blck Africn, Pkistni nd Chinese ethnic groups (Tble 2). Regression nlysis showed tht there ws significnt increse in the number of cses of heptitis B being identified though ntentl screening from 106 cses in 2005 to 161 cses in 2008 (p=0.037) (Tble 3). This represents 52% increse in cses in 2008 compred to 2005 with n verge increse of 13.7 cses per yer. The effect of ethnicity ws lso exmined nd lthough the number of cses in different ethnic groups ws significntly different (p<0.001) the rte of chnge in the number of cses over time between ethnic groups ws not. HBeAg sttus ws vilble on 585 of 595 cses. Ptients with positive HBeAg test hve the highest infectivity nd re most likely to trnsmit the virus to their child. A totl of 67 of 585 (11%) of cses were positive for HBeAg. Of HBeAg positive cses, 42 of 67 (63%) were in women of Chinese nd Pkistni ethnicity (Tble 4). Women with HBV infection of Chinese nd Pkistni ethnicity were significntly more likely thn other ethnicities to be HBeAg positive (chi-squred test p vlue<0.001 nd 0.025 respectively). Rtes nd reltive risks of infection were only clculted for cses in 2007 nd 2008. In the two ltter yers, excluding cses occurring more thn once due to repeted pregnncies resulted in totl of 268 cses of HBV infection. Women of blck Africn, Pkistni, white other nd other ethnicities ll hd significntly higher rte of infection when compred to the Englnd verge rte of 350 per 100,000 ntentl tests (Tble 5). Women of blck Africn nd white other ethnicity hd mrkedly elevted risks (reltive risk (RR): 11.25 nd 5.87 respectively) compred to the Englnd verge. Women of white British ethnicity hd significntly lower reltive risks of infection (RR: 0.01) but this represents single cse nd this result should be interpreted with cution. tble 3 Totl number of heptitis B cses identified by ntentl screening per yer nd percentge of totl nnul cses by ethnic group, Birminghm, United Kingdom, My 2004 December 2008 (n=595) Yer Cses Blck Africn Pkistni Chinese Other White Other Percentge (%) of totl nnul ntentl heptitis B cses Other Blck Bngldeshi Blck Cribben Indin Asin Other Not stted Not Recorded 2004 69 23 30 12 7 0 9 6 4 3 1 4 0 0 2005 106 36 31 5 5 5 5 5 4 3 2 1 0 0 2006 131 32 21 14 8 8 7 2 2 2 2 1 0 1 2007 128 38 27 9 9 7 3 3 2 3 0 0 0 0 2008 161 31 19 16 12 4 1 4 2 2 4 2 2 0 The yer 2004 does not represent dt for complete yer, s dt were only collected from My to December 2004. White British www.eurosurveillnce.org 3
tble 4 Cses of heptitis B virus infection, by heptitis B e-ntigen sttus nd ethnic group, Birminghm, United Kingdom, My 2004 December 2008 (n=595) HBeAg negtive HBeAg positive Not recorded Totl HBeAg positivity rte (%) Chinese 48 17 2 67 25 Blck Cribben 13 4 0 17 24 Pkistni 117 25 4 146 17 Other 43 8 0 51 16 Asin other b 11 2 0 13 15 Blck other c 22 3 0 25 12 White other d 29 2 0 31 6 Bngldeshi 21 1 1 23 4 Blck Africn 186 5 3 194 3 Indin 16 0 0 16 0 Not stted 8 0 0 8 0 Not recorded 3 0 0 3 0 White British 1 0 0 1 0 Totl 518 67 10 595 11 HBeAg: heptitis B e-ntigen. Significntly higher positivity thn verge, chi-squred p<0.05. b Asin other thn Bngldeshi, Indin, Chinese nd Pkistni. c Blck other thn blck Africn nd blck Cribben. d White other thn white British. Discussion The number of cses of heptitis B dignosed through ntentl screening in Birminghm nd Solihull incresed over the period 2004 2008. However, s limited historicl denomintor informtion is vilble it is impossible to distinguish whether this increse is due to incresed numbers of women ttending ntentl screening from high risk groups or whether this represents n ctul increse in the prevlence of infection. The gretest burden of HBV infection in pregnnt women cred for in Birminghm nd Solihull is in women of blck Africn, white other nd Pkistni ethnicity. Of these ethnicity ctegories, the rte of infection is gretest in blck Africn women t 3,938 per 100,000 or pproximtely 4%. This is similr figure compred to estimtes of HBV prevlence in intermedite prevlence countries [15]. It is lso reltively consistent with study in Liverpool, Englnd tht found the prevlence of HBsAg in people ged 20 44 yers-old nd born in Somli to be 9.4% [16]. Hving considered wht is known bout migrtion ptterns in Birminghm, we hypothesise tht the high rte of infection in women of white other t 2,054 per 100,000, pproximtely 2%, reflects infection in recent immigrnts from Estern Europe where HBV prevlence is of the order of 2 7% [15]. However, more ccurte informtion bout ntionlity or country of birth is required to confirm this hypothesis. In the other ethnicity ctegory, which ccounted for rte of infection of 671 per 100,000, 48% were of Chinese ethnicity. We hypothesise tht the HBV infection rte in Chinese women my be substntilly higher thn estimted, due to the reltively smll Chinese popultion in Birminghm nd Solihull. However, the lck of denomintor dt for this ethnicity ctegory limited our bility to nlyse this directly. The higher burden of HBeAg positivity in Chinese nd Pkistni women suggests tht clinicins should be prticulrly wre of the higher risks of verticl trnsmission in these groups nd the greter likelihood of the need for neontl immunoglobulin tretment. Currently, screening for heptitis B infection only occurs s prt of ntentl infectious disese screening in order to reduce the mother to child trnsmission of HBV infection. Helth services in res with lrge blck Africn, white other nd Pkistni popultions my wish to consider introducing trgeted testing/cse finding for HBV in people from these ethnic groups, for exmple s prt of new ptient ssessments t generl prctices. Wider testing of these high risk groups is importnt s ntentl screening misses the lrger proportion of the popultion mde up of non-pregnnt women nd men. Current guidelines for pre-exposure HBV vccintion do not include recommendtions for vccintion bsed on ethnicity or being born in country with high HBV prevlence [1]. It is recommended, however, tht some people trvelling to high 4 www.eurosurveillnce.org
tble 5 Ethnic group rte nd reltive risk, compred to the Englnd verge, of ntentl heptitis B virus infection, United Kingdom, Jnury 2007 December 2008 (n=268) Ethnic group Rte of heptitis B virus infections per 100,000 pregnnt women (95% confidence intervl) Reltive risk (95% confidence intervl) Reference 350 Reference White British 3.9 (0.1 195.3) b 0.01 (0.00 0.56) b White other c 2,054.2 (966.1 4,368.0) b 5.87 (2.76 12.48) b Indin 411.1 (144.2 1,172.1) 1.17 (0.42 3.35) Pkistni 815.1 (562.8 1,180.5) b 2.33 (1.61 3.37) b Bngldeshi 641.0 (253.5 1,614.9) 1.83 (0.73 4.61) Blck Cribben 557.9 (202.8 1,535.1) 1.59 (0.58 4.39) Blck Africn 3,938.4 (2,888.9 5,369.2) b 11.25 (8.25 15.34) b Other 676.3 (363.9 1,256.9) b 1.93 (1.04 3.59) b Englnd verge [7]. b Significntly different t 0.05 level from the Englnd verge. c White other thn white British. recording to ensure tht it is complete, ccurte nd consistent using ntionlly greed ctegoristion. Further reserch to corroborte these findings nd quntify the burden of HBV infection in pregnnt women of Chinese ethnicity is required s is reserch to exmine the effect of country of birth on the rte of infection. Orgnistions tht serve popultions with high or incresing proportion of women originting from res of the world with high prevlence of HBV infection should nticipte n incresing need for perintl nd postntl prophylxis to children born to infected mothers. This will be in ddition to the incresing need for hrm reduction mesures nd the tretment of ptients with HBV infection nd its sequele. Helthcre providers should be prticulrly wre of the finncil nd humn resource implictions of n incresing rte of HBV infection in pregnnt women which is likely to reflect the trend in the popultion s whole. prevlence countries should receive vccintion prior to trvel. The high prevlence rtes mongst blck Africn, white other nd Pkistni pregnnt women found in this study provide strong rgument to reconsider trgeted testing nd immunistion for high risk ethnic groups. There is lso evidence to show tht selective vccintion of high risk groups with similr prevlence rtes to groups identified in this study such s genitourinry medicine (GUM) clinic ttendees, prisoners nd dilysis ptients is cost effective [17,18]. The most importnt limittion to this study is the lck of historicl nd linked ethnicity dt for pregnnt women. This prevented us from ssessing trends over time to estimte the rte of increse in different ethnic groups. The ethnicity ctegories lso differed slightly between the cse dt nd the denomintor dt mening tht some ethnicity ctegories, notbly Chinese, were merged with other ctegories in the finl prt of the nlysis. We lso did not hve informtion on the country of birth for cses. This is likely to be significnt fctor in determining the likelihood of HBV infection s the rte of infection for women of lter genertion immigrnts is likely to pproch tht of the white British popultion, s is seen for mny other infectious diseses, s opposed to recent immigrnts who re more likely to crry the risk of the country they hve moved from. Despite these limittions, this study shows tht the routine collection of ethnicity dt cn identify ltent helth inequlities tht were previously unnoticed or only supported by necdotl evidence. Helthcre orgnistions should continue to improve ethnicity www.eurosurveillnce.org 5
References 1. Slisbury D, Rmsy M, Nokes K, editors. Immunistion Aginst Infectious Disese. London: The Sttionry Office. 2006. 2. Helth Protection Agency (HPA). Heptitis B. Notifictions for Englnd nd Wles 1990-2003. London: HPA. [Accessed 22 Jun 2012]. Avilble from: http://www.hp.org.uk/ Topics/InfectiousDiseses/InfectionsAZ/HeptitisB/ EpidemiologiclDt/hepbNotAge/ 3. Gilson RJ, De Ruiter A, Wite J, Ross E, Lovedy C, Howell DR et l. Heptitis B virus infection in ptients ttending genitourinry medicine clinic: Risk fctors nd vccine coverge. Sexully Trnsmitted Infect. 1998;74(2): 110-5. 4. Uddin G, Shoeb D, Solimn S, Mrley R, Gore C, Rmsy M, et l. Prevlence of chronic virl heptitis in people of south Asin ethnicity living in Englnd: the prevlence cnnot necessrily be predicted from the prevlence in the country of origin. J Virl Hept. 2010;17(5):327-35. 5. British Assocition of Sexul Helth nd HIV (BASHH). United Kingdom Ntionl Guideline on the Mngement of the Virl Heptitides A, B & C 2008. London: BASHH. 2008. [Accessed 22 Jun 2012]. Avilble from: http://www.bshh.org/ documents/1927 6. Helth Protection Agency. Surveillnce of mrkers of infection detected in ntentl smples tested by NHS Blood nd Trnsplnt (NHSBT): Englnd, 2008. Helth Protection Report. 2009;3(12):16-21. 7. Boxll E, Skidmore S, Evns C, Nightingle S. The prevlence of heptitis B nd C in ntentl popultions of vrious ethnic origins. Epidemiol Infect. 1994;113(3):523-8. 8. Elefsiniotis IS, Glynou I, Zorou I, Mgziotou I, Broklki H, Apostolopoulou E et l. Surveillnce for heptitis B virus infection in pregnnt women in Greece shows high rtes of chronic infection mong immigrnts nd low vccintioninduced protection rtes: Preliminry results of single centre study. Euro Surveill. 2009;14(9): pii=19132. Avilble from: http://www.eurosurveillnce.org/viewarticle. spx?articleid=19132 9. Bonur F, Sorgi M, Pern AM, Puccio G, Trmuto F, Cjozzo C et l. Pregnnt women s sentinel popultion to trget nd implement heptitis B (HBV) vccine coverge: three-yer survey in Plermo, Sicily. Vccine. 2005;23(25):3243-6. 10. Tng KY, Chn T, Fenton KA, Gilson RJ. Heptitis B in the Chinese community in Britin. BMJ. 1996;312(7029):507. 11. Twk HM, Vickery K, Bisset L, Selby W, Cossrt YE; Infection in Endoscopy Study Group. The impct of heptitis B vccintion in Western country: recll of vccintion nd serologicl sttus in Austrlin dults. Vccine. 2006;24(8):1095-106. 12. Stengel B, Surel-Cubizolles MJ, Kminski M. Pregnnt immigrnt women: occuptionl ctivity, ntentl cre nd outcome. Int J Epidemiol. 1986;15(4):533-9. 13. Office for Ntionl Sttisics (ONS). Guidnce nd methodology; Ethnic group. [Accessed 22 Jun 2012]. Avilble from: http:// www.ons.gov.uk/ons/guide-method/mesuring-equlity/ equlity/ethnic-nt-identity-religion/ethnic-group/index.html 14. Pencheon D, Guest C, Melzer D, Gry JAM, editors. Oxford Hndbook of Public Helth Prctice 2nd edition. Oxford: Oxford University Press. 2006. 15. Centers for Disese Control nd Prevention. CDC Helth Informtion for Interntionl Trvel 2012. New York: Oxford University Press; 2012. [Accessed 22 Jun 2012]. Avilble from: http://wwwnc.cdc.gov/trvel/yellowbook/2012/chpter-3- infectious-diseses-relted-to-trvel/heptitis-b.htm 16. Aweis D, Brbin BJ, Beeching NJ, Bunn JE, Cooper C, Grdner K et l. Heptitis B prevlence nd risk fctors for HBsAg crrige mongst Somli households in Liverpool. Commun Dis Public Helth. 2001;4(4):247-52. 17. Mngtni P, Hll AJ, Normnd CE. Heptitis B vccintion: the cost effectiveness of lterntive strtegies in Englnd nd Wles. J Epidemiol Community Helth. 1995;49(3):238-44 18. Willims JR, Nokes DJ, Anderson RM. Trgeted heptitis B vccintion cost effective immunistion strtegy for the UK? J Epidemiol Community Helth. 1996;50(6):667-73. 6 www.eurosurveillnce.org