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Published by Oxford University Press on behalf of the International Epidemiological Association ß The Author 2009; all rights reserved. Advance Access publication 6 May 2009 International Journal of Epidemiology 2009;38:757–765 doi:10.1093/ije/dyp194 Community transmission of hepatitis B virus in Egypt: results from a case–control study in Greater Cairo Adela Paez Jimenez,1 Noha Sharaf El-Din,2 Mostafa El-Hoseiny,2 Mai El-Daly,3,4 Mohamed Abdel-Hamid,3,5 Saeed El Aidi,6 Yehia Sultan,7 Nasr El-Sayed,8 Mostafa Kamal Mohamed2 and Arnaud Fontanet1* Accepted 7 October 2008 Background To identify current risk factors for hepatitis B virus (HBV) transmission in Greater Cairo. Methods A 1:1 matched case–control study was conducted in two ‘fever’ hospitals in Cairo. Acute hepatitis B cases were patients with acute hepatitis, positive HBs antigen, and high anti-HBc IgM titres. Control subjects were acute hepatitis A patients (positive anti-HAV IgM) or relatives of patients diagnosed with acute hepatitis C, identified at the same hospitals, with no past HBV infection (negative anti-HBc) and matched to cases on the same age and sex. Conditional logistic regression was used to identify factors associated with acute hepatitis B. Results Between April 2002 and June 2006, 233 cases and 233 controls were recruited to the study. In multivariate analysis, factors associated with an increased HBV risk in males were illiteracy [odds ratio (OR) ¼ 6.1, 95% confidence interval (CI) ¼ 2.8–13.1], shaving at barbers (OR ¼ 2.1, 95% CI ¼ 1.1–3.9) and injecting drug use (IDU) (OR ¼ 3.4, 95% CI ¼ 1.0–11.4). In females, factors associated with an increased HBV risk were illiteracy (OR ¼ 2.2, 95% CI ¼ 1.0–5.0), recent (<1 year) marriage (OR ¼ 42.0, 95% CI ¼ 3.8–463.9 compared with single women) and giving birth (OR ¼ 3.7, 95% CI ¼ 1.0–13.9). Conclusion In this study, HBV transmission took place primarily in the community, whether as a result of recent marriage (presumably first sexual intercourse), shaving at barbershops or IDU, and was more common among illiterates. Health promotion campaigns should be carried out to increase awareness about community transmission of HBV. In addition to routine immunization for infants and other populations, premarital screening might be useful to identify at-risk spouses in order to propose targeted immunization. Keywords Acute hepatitis, risk factors, hepatitis B infection, epidemiology, Egypt 5 1 2 3 4 Emerging Disease Epidemiology Unit, Institut Pasteur, Paris, France. Department of Community, Environmental and Occupational Medicine, Faculty of Medicine, Ain Shams University, Cairo, Egypt. Viral Hepatitis Research Laboratory, National Hepatology & Tropical Medicine Research Institute, Cairo, Egypt. National Liver Institute, Menoufia University, Shibin El Kom, Egypt. Department of Microbiology, Faculty of Medicine, Minia University, Minia, Egypt. 6 Hepatitis Section, Imbaba Fever Hospital, Cairo, Egypt. 7 Hepatitis Section, Abassaia Fever Hospital, Cairo, Egypt. 8 Department of Preventive Affairs, Ministry of Health and Population, Cairo, Egypt. * Corresponding author. Unité d’Epidémiologie des Maladies Emergentes, Institut Pasteur, 25–28, rue du Docteur Roux, Bâtiment Laveran 3ème étage, 75724 Paris cedex 15, France. E-mail: [email protected] 757 758 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY Introduction Hepatitis B vaccination is the most effective measure to prevent hepatitis B virus (HBV) infection and its consequences, including cirrhosis of the liver, liver cancer, liver failure and death.1 Persons infected as infants or young children are less likely to develop acute hepatitis but more likely to develop chronic infection, and are the main reservoir for continued HBV transmission.2,3 Mass immunization lowers transmission rates and hence, pushes back the average age of infection.4 This phenomenon has been well documented in Italy.5 In the USA, following implementation of universal vaccination of infants beginning at birth in the early 1990s, as well as routine vaccination of previously unvaccinated children and adolescents plus vaccination of adults at risk in 1995, incidence of acute hepatitis B declined by 75%, with the greatest decrease (96%) occurring among children and adolescents. At present, adults account for 95% of new infections in the USA. In these low-endemicity countries [0.1–2% HBs antigen (HBsAg) prevalence], ongoing HBV transmission occurs primarily among unvaccinated adults through sexual transmission and injecting drug use (IDU).6 A similar decrease in HBV incidence is expected among children in intermediate-endemicity countries (3–5% HBsAg prevalence), such as Saudi Arabia7 or Egypt,8 where 90% immunization coverage has been achieved.9 In Egypt, HBV vaccination was included in 1992 in the Expanded Program of Immunization (EPI) with injections at 2, 4 and 6 months of age using recombinant vaccine.10 To identify current risk factors for HBV transmission among older adolescents and adults in Greater Cairo, we have conducted a case–control study, the results of which are presented in this article. Methods A matched case–control study was conducted enrolling incident acute symptomatic hepatitis B patients identified through a surveillance system for acute hepatitis in two public ‘fever’ hospitals in Cairo (description of the surveillance system published elsewhere11). Patients with recent (<3 weeks) symptoms suggestive of hepatitis (fever and/or jaundice) were invited to participate in the study. After providing informed consent (from parents if <18 years of age), they answered orally administered standardized questionnaires covering socio-demographic characteristics, present and past health conditions, and exposure to potential risk factors for viral hepatitis during the 6 months preceding the onset of symptoms. Exposures were categorized as iatrogenic and community related. Iatrogenic exposures included history of invasive medical procedures (e.g. surgery, intravenous catheter, endoscope, blood transfusion, drip infusions, injections), obstetrical procedures (women only) and dental treatment. Community exposures included history of circumcision, shaving at barbershops, sharing razors or nail trimmers with family members, getting manicures or pedicures at beauty salons, and tattooing and ear-piercing. Questions on high-risk behaviour such as multiple sexual partners or drug use (e.g., pills, sniffing or injecting) were only asked to men, due to their sensitive nature. Serum samples were collected and tested according to the manufacturer’s instructions for the following hepatitis markers: anti-HAV IgM (HAVABÕ , M EIA, Abbott Laboratories, Diagnostics Division, IL, USA), anti-HBc IgM (CORZYMEÕ , M rDNA, Abbott Laboratories, Diagnostics Division, IL, USA), HBs antigen (AUSZYME MONOCLONALÕ , third generation EIA, Abbott Laboratories, Diagnostics Division, IL, USA), anti-HCV antibody (INNOTESTÕ HCV Ab IV, Innogenetics, Ghent, Belgium). For patients whose anti-HAV and anti-HBc IgM were negative, HCV RNA was detected by direct nested reverse transcriptase polymerase chain reaction (in-house array using 50 -untranslated region primers).12 Standard liver functions were also tested, including alanine aminotransferase (ALT), aspartate aminotransferase (AST), bilirubin and alkaline phosphatase. An acute hepatitis B case was defined as a patient with acute hepatitis symptoms lasting for <3 weeks, ALT three times or higher the upper limit of normal (ULN), no haemolysis and no obstructive cause of jaundice, positive HBs antigen and anti-HBc IgM readings at least twice the optical density cut-off chosen to be positive according to the manufacturer’s instructions (to rule out moderate elevations of antiHBc IgM in chronic hepatitis B).13 Controls were recruited among hepatitis A patients (anti-HAV IgM positive) or among the relatives of the hepatitis C patients identified in the same fever hospitals (note: a case–control study on factors associated with acute hepatitis C is on going; this is the original purpose for controls among relatives of acute hepatitis C cases). All were anti-HBc antibody negative (i.e. had not been infected by HBV in the past). Controls were matched 1:1 to cases on the same age and sex. No case was <11 years old, whereas only seven hepatitis A controls were 440 years old. Therefore, for matching purposes, only 10–40-yearsold subjects were included in the final analysis. Statistical analysis Categorical and continuous variables were compared across groups using Chi-square and Mann–Whitney U-test, respectively. All putative exposures were tested for association with acute hepatitis B in univariate analysis and those with P < 0.20 were then entered into a conditional logistic regression model to examine their independent effect. Since sex was found to be an effect modifier on socio-demographic COMMUNITY TRANSMISSION OF HBV IN EGYPT characteristics (marriage status and illiteracy, defined as the lack of ability to read and write), since many potential risk factors were sex specific (e.g. pregnancy, ear-piercing, barber shaving), and since questions regarding high-risk behaviours were only asked to men (alcohol consumption, drug use and sexual promiscuity), we present data separately for men and women. The final models were obtained through stepwise deletion of variables until all variables left in the model had P < 0.05. Two-tailed P-values were reported. We also tested whether the results would differ according of the series of controls used. Therefore, for each pair of observations (i.e. a case and its matched control), we allocated the value 1 if the control was a hepatitis A patient, or 0 if the control was a relative of hepatitis C patient. We then tested in each of the two final models (males and females) whether there was any effect modification by this newly created variable for each of the exposures associated with acute hepatitis B. All statistical analyses were performed using STATA 9.0 software (Stata Corporation, College Station, TX, USA). The study was conducted with the approval of the Institutional Review Board at the Egyptian Ministry of Population and Health (MOPH), and with 759 clearance from the ethics committee of the National Hepatology and Tropical Medicine Research Institute in Cairo, Egypt. Results Between April 2002 and June 2006, 233 cases and as many controls matched on the same age and sex were identified in the two study hospitals. Among the 233 controls, 124 (53%) were relatives of patients diagnosed with acute hepatitis C and 109 were acute hepatitis A patients. Clinical description of cases Among the 233 HBV cases retained for the analysis, 64% (149) were men with a median interquartile range (IQR) age of 22 (19–26) years and 36% (84) were women with a median (IQR) age of 23 (20– 27) years (Table 1). All 233 cases were symptomatic and 76.4% had an insidious onset. Median ALT was 765 IU/l (close to 20 times the ULN, 40 IU/l), and no difference was observed between men and women. There was no age effect on the duration of illness, but an effect of sex, with a longer mean (SD) duration of symptoms at the time of examination for Table 1 Recruitment and clinical among male and female acute hepatitis B cases, Greater Cairo, 2002–06 All patients (N ¼ 233) Males (N ¼ 149) Females (N ¼ 84) P-value 2002 47 (20.2%) 33 (22.2%) 14 (16.7%) 0.633 2003 65 (27.9%) 41 (27.5%) 24 (28.6%) 2004 64 (27.5%) 37 (24.8%) 27 (32.1%) 2005 53 (22.8%) 36 (24.2%) 17 (20.2%) 2006 4 (1.7%) 2 (1.3%) 2 (2.4%) 9.4 ( 4.6) 9.9 ( 4.8) 8.5 ( 4.3) 0.03 Time trend in case identification Symptoms Mean (þSD) duration (days)a Fever 112 (48.1%) 65 (43.6%) 47 (55.9%) 0.07 Jaundice 231 (99.1%) 148 (99.3%) 83 (98.8%) 0.68 Light clay stools 192 (82.4%) 123 (82.5%) 69 (82.1%) 0.9 Dark urine 228 (97.8%) 146 (97.9%) 82 (97.6%) 0.7 Abdominal pain 176 (75.5%) 103 (69.1%) 73 (86.9%) 0.002 Vomiting 135 (57.9%) 84 (56.4%) 49 (58.3%) 0.58 765 (570–1301) 765 (570–1176) 785 (550–1554) 0.75 575 (365–902) 550 (368–854) 600 (365–1007) 0.24 8.8 (6.4–12.6) 8.7 (6.0–12.2) 9.4 (7.3–12.9) 0.13 156 (107–236) 163 (115–241) 146 (100–216) 0.20 Liver functions: median (IQR) Alanine aminotransferase (IU/l)b Aspartate aminotransferase (IU/l) Total bilirubin (mg/dl)a Alkaline phosphatase (IU/l) Data missing: a Three males. b Two males. c Six males and three females. c b 760 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY males compared with females [9.9 (4.8) vs 8.5 (4.3) days, respectively, P ¼ 0.03]. Socio-demographic characteristics associated with acute hepatitis B The proportion of illiterates was higher among HBV cases (35.0%) compared with controls (12.8%) (P < 0.001) (Table 2). This increase in HVB risk due to illiteracy was true for both sexes but the risk was of a higher magnitude for men [odds ratio (OR) ¼ 6.6, 95% confidence interval (CI) ¼ 3.1–14.0] compared with women (OR ¼ 2.5, 95% CI ¼ 1.3–5.1) (P-value for the interaction term ¼ 0.07). The same effect modification by sex was found with marriage, with a higher magnitude of the associated risk for women (OR ¼ 8.0, 95% CI ¼ 3.1–20.7) compared with men (OR ¼ 1.2, 95% CI ¼ 0.6–2.5) (P-value for the interaction term ¼ 0.007). After splitting marriage into categories by duration of marriage, the increased risk of acute hepatitis B was particularly elevated for women married for <1 year (OR ¼ 49.4, 95% CI ¼ 4.3–562.0), compared with singles. Iatrogenic exposures Iatrogenic exposures in the past 6 months were quite common in the control series, as shown by the percentage who received injections (15.4 and 38.1% for males and females, respectively), dental treatment (10.7 and 17.9%, respectively) or stitches (4.0 and 7.1%, respectively) (Table 3). In general, females experienced more frequent invasive medical procedures than males. However, none of the procedures was associated with an increase in HBV risk except for giving birth (OR ¼ 3.3, 95% CI ¼ 1.1–9.8). Episiotomy, forceps and Caesarean section were not individually associated with an increase in HBV risk, but numbers were low for each procedure (data not shown). Dental and gum treatments have been previously described as risk factors for HBV transmission.14,15 In our data, none of the dental procedures (gingival treatment, tooth filling, tooth extraction and dental anaesthesia) was associated with an increase in HBV risk. Community exposures Acupuncture and tattooing were not common practices among study participants. There was no difference among cases and controls regarding ear-piercing or getting manicures or pedicures in beauty salons (Table 4). Noteworthy is the finding that shaving at barbershops was at increased risk of HBV transmission (OR ¼ 2.4, 95% CI ¼ 1.3–4.4) since this is a very common practice among Egyptian men (64.4% of controls). Only men were asked about high-risk behaviour, such as drinking alcohol, sexual promiscuity or drug use. The frequency of alcohol consumption (17% of controls) and drug use (13% of controls) was higher than expected. Alcohol use (OR ¼ 2.7, 95% CI ¼ 1.5– 4.8) and IDU (OR ¼ 4.2, 95% CI ¼ 1.4–13.9) were associated with acute hepatitis B. Multivariate analysis In multivariate analysis, we found the same risk factors related to HBV transmission as in the univariate analysis (Table 5). Among men, illiteracy, shaving at barbershops and IDU all remain associated with a substantial increase in risk. Among women, illiteracy was again associated with increased risk, as well as recent marriage and giving birth. For each of these Table 2 Distribution of socio-demographic risk factors among male and female acute hepatitis B cases and controls, Greater Cairo, 2002–06 Males (N ¼ 298) Cases (%) Controls (%) (N ¼ 149) (N ¼ 149) ORa (95% CI) Females (N ¼ 168) Cases (%) Controls (%) (N ¼ 84) (N ¼ 84) ORa (95% CI) Education Illiterate Some education 46 (30.9) 10 (6.7) 6.6 (3.1–14.0) 36 (42.9) 20 (23.8) 2.5 (1.3–5.1) 103 (69.1) 139 (93.3) 1 48 (57.1) 64 (76.2) 1 113 (75.8) 116 (77.9) 1 14 (16.7) 38 (45.2) 1 36 (24.2) 33 (22.2) 1.2 (0.6–2.5) 70 (83.3) 46 (54.8) 8.0 (3.1–20.7) Marital status Single Married Marriage duration (years) 113 (75.8) 116 (77.9) 1 14 (16.7) 38 (45.2) 1 <1 4 (2.7) 1 (0.7) 5.0 (0.5–51.6) 8 (9.5) 1 (1.2) 49.4 (4.3–562.0) 1–5 Single a 18 (12.4) 19 (12.8) 0.9 (0.4–2.1) 25 (29.7) 16 (19.0) 7.7 (2.5–23.5) 6–10 6 (4.2) 11 (7.4) 0.6 (0.1–2.2) 16 (19.0) 13 (15.5) 12.9 (2.9–55.9) 410 4 (2.7) 2 (1.3) 1.9 (0.3–13.9) 12 (14.3) 12 (14.3) 10.3 (1.4–75.5) Estimated using conditional logistic regression. Statistically significant ORs are shown in bold. COMMUNITY TRANSMISSION OF HBV IN EGYPT 761 Table 3 Health care-related risk factors among male and female acute hepatitis B cases and controls, Greater Cairo, 2002–06 Males (N ¼ 298) Cases (%) Controls (%) (N ¼ 149) (N ¼ 149) Invasive medical procedures Hospitalization Females (N ¼ 168) Cases (%) Controls (%) (N ¼ 84) (N ¼ 84) ORa (95% CI) ORa (95% CI) 9 (6.0) 8 (5.4) 1.1 (0.4–3.1) 15 (17.9) 11 (13.1) 1.4 (0.6–3.2) 0 1 (0.7) – 1 (1.2) 0 – Intensive care unit Surgery 6 (4.0) 0 – 3 (3.6) 4 (4.8) 0.7 (0.2–3.4) Stitches 12 (8.0) 6 (4.0) 2.1 (0.8–5.7) 8 (9.5) 6 (7.1) 1.3 (0.5–3.9) Injections 19 (12.8) 23 (15.4) 0.8 (0.4–1.5) 30 (35.7) 32 (38.1) 0.9 (0.5–1.7) IV infusion 6 (4.0) 5 (3.4) 1.2 (0.4–4.0) 14 (16.7) 13 (15.5) 1.1 (0.5–2.5) Catheter 3 (2.0) 1 (0.7) 3.2 (0.3–32.1) 3 (3.6) 1 (1.2) 3.0 (0.3–28.8) Abscess 6 (4.0) 0 – 1 (1.2) 3 (3.6) 0.3 (0.03–3.2) Endoscopy Transfusion 0 0 – 0 1 (1.2) – 1 (0.7) 0 – 4 (4.8) 1 (1.2) 4.7 (0.5–46.2) Obstetrical history (females only) Pregnancy NA NA 22 (26.2) 9 (10.7) 1.7 (0.7–4.5) Delivery NA NA 14 (16.7) 5 (6.0) 3.3 (1.1–9.8) 18 (12.1) 16 (10.7) 1.2 (0.5–2.4) 13 (15.5) 15 (17.9) 0.8 (0.4–1.9) 14 (9.4) 10 (6.7) 0.8 (0.1–7.0) 11 (13.1) 12 (14.3) 3.6 (0.3–38.7) Dental treatment Any Gingival treatment Tooth filling Tooth extraction Anesthesia a Estimated using conditional logistic regression. Statistically significant ORs are shown in bold. NA ¼ not applicable. Table 4 Community exposures among male and female acute hepatitis B cases and controls, Greater Cairo, 2002–06 Males (N ¼ 298) Cases (%) Controls (%) (N ¼ 149) (N ¼ 149) ORa (95% CI) Females (N ¼ 168) Cases (%) Controls (%) (N ¼ 84) (N ¼ 84) ORa (95% CI) Community exposures Circumcision 0 0 – 0 0 116 (77.8) 96 (64.4) 2.4 (1.3–4.4) NA NA 17 (11.4) 20 (13.4) 0.8 (0.4–1.6) NA NA 4 (2.7) 1 (0.7) 4.1 (0.5–37) 9 (10.7) 3 (3.6) 85 (57.0) 102 (68.5) 0.8 (0.4–1.3) 58 (69.1) 55 (65.5) 1.6 (0.8–3.6) NA NA 4 (4.8) 2 (2.4) 2.1 (0.4–11.8) 3 (2.0) 1 (0.7) 3.1 (0.3–29.6) 0 0 – 49 (32.9) 25 (16.8) 2.7 (1.5–4.8) 9 (6.0) 11 (7.4) 1.0 (0.4–2.8) Drug use 39 (26.2) 20 (13.4) 2.4 (1.3–4.4) IDU 15 (10.1) 4 (2.7) 4.2 (1.4–13.9) Shaving at barber Sharing razor blades Manicure Sharing nail cutter Ear-piercing Tattooing High-risk habits (males only) Drinking alcohol Sexual promiscuity a Estimated using conditional logistic regression. Statistically significant ORs are shown in bold. NA ¼ not applicable. – 3.6 (0.9–14.5) 762 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY Table 5 Multivariate analysis showing factors independently associated with acute hepatitis B by sex, Greater Cairo, 2002–06 Males (N ¼ 292) adjusted OR (95% CI)a 6.1 (2.8–13.1) Illiteracy Barber shaving Intravenous drug use Females (N ¼ 155) adjusted OR (95% CI)b 2.2 (1.0–5.0) 2.1 (1.1–3.9) NA 3.4 (1.0–11.4) NA Marriage duration (years) Single 1 <1 42.0 (3.8–463.9) 1–5 Not in the final model 4.5 (1.4–4.8) 6–10 7.1 (1.6–32.5) 410 3.5 (0.4–308) Giving birth in the past 6 months a Estimated using conditional the variables included in the Estimated using conditional the variables included in the NA ¼ not applicable. b NA 3.7 (1.0–13.9) logistic regression. Only 292 participants out of 298 were included due to missing data for any of regression. logistic regression. Only 155 participants out of 168 were included due to missing data for any of regression. models (males and females), the magnitude of risk associated with each exposure was no different according to the series of controls used (hepatitis A patients or relatives of hepatitis C patients) (test for interaction not significant). Discussion This is the first study of risk factors for HBV transmission among older adolescents and adults in an intermediate-endemicity country that has recently implemented a national immunization plan for infants. The main finding of this study is that of continuing HBV transmission as a result of community, rather than iatrogenic, exposure (except for obstetrical procedures in women). This study has several strengths: (i) it recruited incident cases, who as such had a well-defined 6-month exposure period preceding the onset of symptoms (the length of HBV’s incubation period), allowing for the use of detailed questionnaires; (ii) the use of incident cases also allowed for the identification of current sources of exposure to HBV in Greater Cairo, making our findings particularly relevant for on-going prevention programs; and (iii) analyses had 80% power to detect associations characterized by OR as being as low as 1.8 for exposures present among 50% of controls or 2.2 for exposures present among 10% of controls (although the power decreased with subsequent sex stratification, the initial analysis for iatrogenic exposures was performed with combined male and female datasets without identifying any risk factors associated with acute hepatitis B). The study has, however, some limitations: by focusing on symptomatic cases, it selects for an age distribution which does not reflect that of all acute infections, since symptomatic forms of acute infections are associated with older age. Indeed, while the absence of children in our sample may be related to vaccine efficacy, it may also reflect the rarity of symptomatic forms among children. Still, it is unlikely that recruiting only symptomatic forms of infection would select for specific exposures or routes of transmission unless these are related to age. Another limitation concerns the avoidance of certain sensitive questions about behaviours (mainly alcohol use, drug use and sexual promiscuity) with women. As a result, we were not able to identify these factors as risk factors for HBV transmission in women. Had we identified these factors, some associations documented in this paper such as with educational level might have been weakened. However, we believe that these behaviours are rare in the female population for cultural reasons and thus would have limited confounding ability in this context. Interestingly, community transmission, rather than iatrogenic transmission, was responsible for most cases documented in this study. Among males, shaving at barbershops was associated with a 2 fold increase in risk of infection, a rather worrisome figure considering that a majority of males (64% of controls in this study) continue to get shaves at barbershops. This is a well-known risk factor not only for HBV16 but also for HCV,17,18 calling for targeted education programmes. Barbers are usually unaware of the concept of blood-borne transmission, and razors and scissors are used repeatedly for different COMMUNITY TRANSMISSION OF HBV IN EGYPT customers without intervening sterilization.19,20 An additional risk that needs to be further explored is the ‘hijama’, or wet cupping, where blood is drawn by vacuum from a small skin incision for therapeutic purposes. Since the location is first shaved to ensure a tight seal with the cup, it is frequently performed by barbers. It is worth noting that in many countries, laws have been passed to enforce sterilization of equipment in barbershops. Among males, another important contribution to HBV transmission was intravenous drug use. The substantial proportion of controls (13%) who acknowledged drug use, with almost 3% admitting intravenous drug use, was a surprise to us. The low socio-economic status of study participants consulting at ‘Fever hospitals’ may explain this high proportion. As recommended by the Centers for Diseases Control and Prevention (Atlanta, USA),6 HBV immunization should be offered to drug users. In addition, given the magnitude of the HCV pandemic in Egypt and the growing concern regarding HIV transmission, needle exchange programmes, accompanied by awareness activities, should be urgently considered. In females, marriage emerged as a risk factor for acute HBV infection. The increase in risk was independent of pregnancy and delivery in multivariate analysis and much higher for women being married <1 year (i.e. recently married women). In a country where premarital sex is rare, and notwithstanding household transmission through the multiple exposures shared by married couples (e.g. sharing of personal hygiene items), this suggests a significant rate of HBV transmission through first sexual contact with infected spouses. Sexual transmission within married couples has already been speculated as a possible explanation for the high prevalence of HBV infection in a closed population of Saudi Arabia.21 It may be wise to consider premarital screening for HBV infection22 in order to propose immunization to nonimmune spouses marrying a chronically infected individual. Furthermore, considering the high fertility rate among recently married women, and the risk of transmission to newborns, HBsAg screening of pregnant women should be considered where feasible. If the mother is found to be chronically infected, newborns may benefit from HBV immunization at birth, as well as administration of hepatitis B immunoglobulin.23 While HBV is transmissible through contact with infected blood, no iatrogenic factor other than past birth delivery was found associated with HBV transmission in this study. We were not able to identify which of the procedures related to delivery might have explained this association. This will unfortunately limit the type of recommendations that can be made, excepting the standard precautions against blood-borne infections in medical settings. Whether the low relative contribution of iatrogenic transmission to new HBV infections reflects an improvement 763 in infection control in hospital facilities in Egypt24 needs to be confirmed through other studies. Of note, we are currently gathering data for a similar analysis comparing acute hepatitis C cases and controls from the same hospitals, and will assess whether iatrogenic factors emerge as risk factors for another blood-borne infection for which community transmission is probably much more limited. More difficult to interpret is this study’s finding that illiteracy is a risk factor for HBV infection, especially since controls came from the same socio-economic background. Low educational attainment has previously been associated with higher prevalence of hepatitis B in both developed and developing countries.25–27 But illiteracy is not in itself a specific mechanism for HBV transmission and could stand in for other risk factors, such as community exposures or high-risk habits, which may not have been adequately identified in our questionnaire. This is particularly true for women for whom questions about risk habits were avoided. It may also reflect the fact that prevention messages do not reach the most vulnerable groups. In conclusion, this study has confirmed the ongoing transmission of HBV in Greater Cairo during a transition period following the introduction of childhood immunization. While efforts related to bloodborne infection control in medical settings should be continued, this study suggests that the majority of HBV transmission occurs within the community. Based on the results of this study, health promotion campaigns and prevention programs should be targeted to specific groups, such as intravenous drugs users and barbershops clients and owners. Premarital screening for HBV infection should be proposed. Finally, control of HBV transmission should be viewed in the larger context of blood-borne infection control, in a country where HCV infection rates are among the world’s highest. Funding Agence Nationale de Recherche sur le SIDA et les hépatites virales – France (ANRS 1203 & 12122). Acknowledgements The authors are indebted to the ‘Fever Hospital’ Abassaia and Imbaba and to the Department of Community Medicine of Aim Shams University for the scientific and logistical support in the recruitment and diagnosis of the study participants, as well as to the participants themselves for their assistance in providing this information. The National Hepatology and Tropical Medicine Research Institute carried out the laboratory analysis for this project. Conflict of interest: None declared. 764 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY KEY MESSAGES A case–control study was performed in Greater Cairo (Egypt) to identify current risk factors for HBV transmission. In this setting, HBV transmission took place primarily in the community, whether as a result of recent marriage (presumably first sexual intercourse), shaving at barbershops or IDU, and was more common among illiterates. Health promotion campaigns and prevention programmes should be targeted to specific groups, such as IDUs and barbershop tenants and clients. In addition to routine immunization for infants and other populations, premarital screening might be useful to identify at-risk spouses in order to propose targeted immunization. References 1 2 3 4 5 6 7 8 9 10 11 Margolis HS, Coleman PJ, Brown RE, Mast EE, Sheingold SH, Arevalo JA. 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