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  EMHJ  • Vol. 16 No.11 • 2010 Eastern Mediterranean Health JournalLa Revue de Santé de la Méditerranée orientale 1128 Viral hepatitis E outbreak in Al-Sadr city, Baghdad, Iraq K.K. Al-Nasrawi, 1  J.K. Al- Diwan, 1  T.S. Al-Hadithi 1 and A.M. Saleh  2   ABSTRACT Hepatitis E virus (HEV) is a major cause of acute hepatitis in many developing countries. This study describes an outbreak of HEV infection in Al-Sadr city, Baghdad. Blood samples obtained from patients with  jaundice attending 19 primary health care centres in Al-Sadr city during a 6-month period in 2005 were tested for HEV. HEV (IgM) antibodies were detected in 38.1% of 268 patients. The association of HEV infection with unacceptable residual chlorine concentrations and/or bacteriologically unsafe water samples was significant. High rates of HEV infection, low chlorine concentrations and unsafe water were reported in June. Gross disruption of sanitation and water supplies was the most likely contributing factor. 1 Department of Community Medicine, College of Medicine, University of Baghdad, Baghdad, Iraq (Correspondence to T.S. Al-Hadithi: talhadithi@ yahoo.com).  2 Department of Community Medicine, College of Medicine, Hawler Medical University, Erbil, Iraq. Received: 13/01/09; accepted: 08/04/09 قرعل   ،دغب   ،دصل   ةندم  » ئ « سويل   دكل   اهتل   م   ةشاف ا   د   رب   وب   ،د    س   اط   ،ود   ظاك   وج   ،صن   ظاك   اشا      ًشا   ةسد   ذ   ت  . ةان   د      يك   ف   د   اه   اس      ًئ   ًس   E  » ئ « د   اه   دَُ  : ةـ    رـت   م   ،اقياب   با   ر      د      انع   ع   اه   وحا   ح   ،دب   ،د   ةند   ف  » ئ « د   اه   يب   ىد   اس      اخ   اهع   رج   ، 2005   اع   ف   ةسد   س      ة   رهش   خ   د   ةند   ف   ة   ة   ةاعر   ًزكر   19   ع   اهاب   ىد   ب   ُرـ   اك   دق  . ًضر   268         % 38 . 1   ة   ىد   IgM   ن     » ئ « ي   د   اه   د   دجو   ،ىد   دَُ   ًُرـت   ،ةوثر    ة   ت         ال   انّع   ف   و   ُث     –   ْَدجُ   إ  –   ةول   يغ   زكرـ   ب  » ئ « ي   د   رهش   ف   ةوأل   يغ   ال   و   او   ا     » ئ « ي   د   اهاب   ىد   ةتر   د   وحا   س   دق  . ًئاحإ   ب .    ف   ا   اع         ص   ال   دإ   ف   ي   ر   و        . وو / رزح Flambée d’hépatite virale E à Al-Sadr city, Bagdad, Iraq RÉSUMÉ Le virus de l’hépatite E (VHE) est une cause majeure d’hépatite aiguë dans de nombreux pays en développement. Cette étude décrit une flambée d’infection à VHE à Al-Sadr city, Bagdad. Des échantillons de sang prélevés sur des patients souffrant de jaunisse et consultant dans 19 centres de soins de santé primaires à Al-Sadr city sur une période de 6 mois en 2005 ont été soumis à un test de dépistage du VHE. Des anticorps anti-VHE (IgM) ont été détectés chez 38,1 % des 268 patients. L’infection par le VHE était fortement associée à des concentrations de chlore résiduel inacceptables et/ou des échantillons d’eau de mauvaise qualité bactériologique. Des taux élevés d’infection à VHE, de faibles concentrations de chlore et une eau de mauvaise qualité ont été signalés en juin. Une interruption massive de l’assainissement et de l’approvisionnement en eau était la cause la plus probable.  سول      ة   ةلع   ا   دلع   ا    د 1129 Introduction Hepatitis E virus (HEV) is endemic in the subcontinent of India, South-East  Asia, China, parts of the Middle East,  Africa and Mexico [1,2] and is a major cause of acute hepatitis in many devel-oping countries [3]. HEV is transmied principally by the faecal–oral route, and  waterborne epidemics are character-istics of outbreaks of HEV infection [1,3]. HEV infection has been reported in haemodialysis patients [4] and a zoonotic route has been suggested [3]. Iraq used to have one of the best health services in the region [5]. How-ever, during the last 3 decades the health system has suered from a serious de-terioration in the provision of health services. is decline has arisen from the massive and swi degradation of the country’s infrastructure as a result of the Iraqi–Iranian war in the 1980s, the Gulf  war of 1991 and the prolonged period of economic sanctions [6]. is situa-tion was further aggravated by the 2003 invasion of Allied forces and subsequent civil strife which led to further disrup-tion of the infrastructure necessary for proper sanitation and safe water supply and consequently to a dramatic up-surge of infectious diseases [7–9]. HEV outbreaks are increasingly reported, in Basra (1986), Erbil (1989), Diyala (2001) and Baghdad (2001) [10,11]. ese circumstances provided the impetus to carry out an epidemiological study of HEV outbreaks in Al-Sadr city, Baghdad. e objectives of the study  were to describe the distribution of cases according to the primary health care (PHC) centre catchment areas  where they presented and to nd out the risk factors for infection including unsafe water supply and lack of eective chlorination. Methods  A total of 268 patients with jaundice diagnosed by physicians at 19 PHC centres in Al-Sadr city were included in this study during the period 1 January to 30 June 2005. Jaundice was diagnosed clinically and conrmed by laboratory tests (high serum bilirubin and positive urine bile pigments).  A questionnaire was lled for each patient. e data requested included demographic characteristics and resi-dency (by sector of Al-Sadr city). Blood samples were obtained from each patient and sera were tested for HEV (IgM) antibodies using an enzyme-linked immunosorbent assay (ELISA) at the public health laboratory of the Ministry of Health.e results of bacteriological exami-nation of drinking water were obtained from the Ministry of Environment’s Baghdad environment laboratory, ac-cording to the sector of Al-Sadr city.  Water samples were cultured for detec-tion of  Escherichia coli  , total coliform  bacteria and total plate counts. e Baghdad environment administration’s criteria for unsafe water were: zero levels of  E. coli  , total coliforms < 10/100 mL and total plate counts < 50/1 mL in any  water sample. e water samples are  judged unsafe for drinking if any one of the tests exceeds the normal limits.Residual free chlorine of the piped drinking water supply was measured directly at the PHC centres. Residual free chlorine concentration < 0.5 mg per L of drinking water was considered unacceptable. Visits to catchment areas of PHC centres were carried out to ob-serve leaking or ooding in the sewage system.e chi-squared test was used to assess the association of HEV with the independent variables (demographic characteristics, residual chlorine and unsafe water supply). A  P  value ≤ 0.05  was considered statistically signicant. Results Of the 268 patients, 102 (38.1%) were positive for HEV (IgM) antibody. e highest rate of HEV infection was observed in the oldest age group ≥ 40  years (45.5%). e lowest rate (12.9%) of HEV infection was among those   < 10 years of age. ese variations  were statistically signicant (χ  2  = 11.96,    P  = 0.017).   No signicant statistical dif-ference was observed in HEV infection  between males and females (39.5% and 35.6% respectively) (Table 1). High rates of HEV infection were reported from the PHC catchment ar-eas of El-Kemalia (75.0%), Fourteenth Tamouz (71.4%), Eighth (60.0%), Fih (54.2%) and Eked (50.0%). e catchment areas of PHC centres with high rates of unacceptable residual Table 1  Age and sex distribution of patients with hepatitis E virus (HEV) infection among patients presenting with jaundice at primary health care centres in Al-Sadr city VariableTotal patients testedHEV positiveNo.No.%  Age group (years)  < 1031412.910–191074643.020–29823643.930–39371129.7≥ 4011545.5  Sex  Male1013635.6Female1676639.5 Total  26810238.1  EMHJ  • Vol. 16 No.11 • 2010 Eastern Mediterranean Health JournalLa Revue de Santé de la Méditerranée orientale 1130 chlorine concentrations and/or bac-teriologically unsafe water samples mostly reported high rates of HEV infection. No HEV cases were reported from the catchment areas of the First, Seventh, El-Umaliah and El-Fdeliah PHC centres, despite high rates of unacceptable residual chlorine con-centrations and/or bacteriologically unsafe water supply. ese variations in HEV infection with the geographical location of PHC centres were statisti-cally signicant (χ  2  = 126.7,  P  = 0.02). e association of HEV infection  with unacceptable residual chlorine and/or bacteriologically unsafe water samples was statistically signicant   (χ  2 = 946,  P  < 0.001) (Table 2).e highest rates of HEV infection, unacceptable residual chlorine and  bacteriologically unsafe water samples  were reported in the month of June (53.1%, 52.0% and 50.0% respective-ly). Lower rates were reported in the period January to May. ese varia-tions were not statistically signicant (Figure 1). Sewage system leaking or ooding  was observed in the catchment areas of ird, Fourth, Fih and Sixth, Eighth, El-Kemaliah, Eked, Hay El-Nasr, El-Gayareh and El-Fdeiliah PHC centres;  between them they reported 91% of HEV infections. Discussion e prevalence of HEV infection re- vealed by this study (38.1%) is higher than that previously reported in 2001 in Al-Sadr city (24.2%) [10]. However, this rate is similar to that reported from Diyala governorate in 2002 (40.9%) [11]. Widely varying rates of HEV infec-tion have been reported worldwide; for example from Morocco (77.3%) [12], India (47.3%–53.0%) [13,14], Somalia (83.7%) [15], Japan (13%) [16] and Egypt (6%) [17]. Variations in the prevalence of HEV infection could be related to the degree of water pollution,  variation in the distribution of types of  viral hepatitis in the community and the level of immunity in the community. e signicant association of HEV infection with age revealed in this study is consistent with ndings reported from India [14], Hong Kong [18] and Indo-nesia [19]. e nding of no signicant sex variation in HEV infection is similar to that previously reported in Iraq [10] and Brazil [20]. However, Corwin et al. in Indonesia reported a signicantly higher HEV infection among males than females [19]. Table 2 Rates of hepatitis E virus (HEV) infection in patients presenting with jaundice at primary health care (PHC) centres, and rates of bacteriologically unsafe water samples and unacceptable residual chlorine concentrations in water supplies in PHC catchment areas of Al-Sadr city PHC catchment areaHEV testingBacteriological testingResidual chlorine levelTotal patients testedHEV positiveTotal water samples testedUnsafe water samplesTotal water samples testedUnacceptable residual chlorineNo.No.%No.No.%No.No.% First000.09333.311911395.0Second3133.316425.0000.0Third491938.812866.72727100.0Fourth12433.312216.711500.0Fifth593254.26350.08911.1Sixth622133.92150.0963536.5Seventh000.055100.01082523.1Eighth5360.015426.7843545.2El-Habibiah10110.014214.38400.0El-Belediat000.0000.05411.9El-Umaliah000.010770.04848.3El-Meshtel6116.6400.09900.0El-Ameen1417.120420.09033.3Fourteenth Tamuz7571.4231356.5593762.7El-Kemaliah4375.0241041.7714056.3Eked8450.0191263.215714089.2Hay El-Naser8112.510220.0802835.1El-Gayareh16637.56466.7252496.0El-Fdeiliah500.07342.9947781.9Total26810238.12148740.7149959039.4  سول      ة   ةلع   ا   دلع   ا    د 1131 In this study, detection of  E. coli   and total coliforms was used as an in-dicator for faecal contamination of  water samples, as has been used in other studies [21]. Our nding of a signicant association between HEV infection and unsafe water supply (unacceptable residual chlorine con-centrations and/or bacteriologically unsafe water sample) is suggestive of gross faecal contamination of piped drinking-water supplies in most of the geographical areas of Al-Sadr city, in addition to unacceptably low chlorina-tion levels. e lack of cases reported from catchment areas with a high pro-portion of unsafe water samples and unacceptable chlorination could be aributed to the continuing displace-ment of the residents from one sector of the city to another or the improper registration of cases as a result of the civil strife and violence.Faecal contamination could be at-tributed to the leaking and ooding of sewage observed at PHC centres in this study. e intermient short-ages and even interruption of drinking- water supplies forces the residents to use electric pumps for the water which further aggravate water contamination through recession of ood water into  broken or leaking water pipes. Accord-ing to surveys conducted in June and September 2003 by the Ministry of Health, low levels of chlorination were demonstrated in 73% of Baghdad dis-tricts where piped chlorinated water  was available. In other governorates, low chlorination was found in 94% of surveyed districts [5]. e needs assess-ment report of the United Nations and the World Bank in 2003 indicated that the sewage collection and treatment systems were serving mainly the city of Baghdad and reaching approximately 80% of the population [22]. Contami-nated water is closely associated with HEV outbreaks [1–3]. HEV has been detected in sewage and wastewater plants in other studies, in both Egypt and Norway [23,24]. Figure 1 Monthly variation in 2005 of hepatitis E virus (HEV) infection in patients presenting with jaundice (A), unacceptable residual chlorine levels in water samples (B) and bacteriologically unsafe water samples (C) in Al-Sadr city, Iraq Much of the drinking-water and  wastewater systems in Baghdad are cur-rently out of order or working at low capacity. Treatment plants function at a fraction of their former capacities and  water distribution suers from reduced ow and limited chlorination. Sewage collection systems are also only partially operational due to an array of problems caused by the shut-down of li stations following the Gulf war [25,26] and the Allied invasion. ere are a great number of constraints facing the recon-struction and restoration of essential services in Iraq and rehabilitation of the water distribution and sewage col-lection network and treatment plants remains an enormous health challenge [7–9]. is study described an outbreak of HEV infection in Al-Sadr city as an example of a man-made disaster. Gross disruption of sanitation and water sup-plies aer extensive damage to the in-frastructure seems to be the most likely contributing factor.  EMHJ  • Vol. 16 No.11 • 2010 Eastern Mediterranean Health JournalLa Revue de Santé de la Méditerranée orientale 1132 References Krawczynski K, Aggarwal R, Kamili S. Hepatitis E. 1. Infectious Dis-eases Clinics of North America , 2000, 14(3):669–667.Zuckerman JN. Hepatitis E and the traveler. 2. 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