Prevalence of hepatitis C virus infection among pregnant women in a rural district in Egypt

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1 Article Prevalence of hepatitis C virus infection among pregnant women in a rural district in Egypt Tropical Doctor 2016, Vol. 46(1) 21 27! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalspermissions.nav DOI: / tdo.sagepub.com Hossam Hassan Khamis 1, Azza Galal Farghaly 2, Hanan Zakaria Shatat 3 and Engy Mohamed El-Ghitany 4 Abstract Background: Egypt has the highest prevalence of hepatitis C virus (HCV) infection in the world. Screening of HCV during pregnancy is not as routinely done in Egypt compared with many other countries, although pregnancy is an important period where screening of HCV infection is important owing to low immunity, the possibility of vertical transmission and possible horizontal transmission to the baby or other household contacts at a later stage. Aim: To determine the seroprevalence of HCV antibodies (HCV-Ab) and risk factors associated with infection among pregnant women in Egypt. Patients and Method: A total of 360 pregnant women visiting the healthcare units for routine antenatal care were tested using third generation ELISA test for detection of HCV-Ab. Polymerase chain reaction (PCR) was done for seropositive cases. Results: A total of 6.1% (22/360) of pregnant women were HCV seropositive; of them only 45% (9/20) had viraemia. Risk factors were their age, the age of their husband and the presence of chronic liver disease in the husband. Conclusion: The prevalence of HCV infection in pregnant women in Egypt appears to be lower than previously reported. The detected risk factors are old age of the pregnant women and their husbands, and chronic liver disease in the husbands. None of the other known risk factors was found to be significantly associated with HCV infection in pregnant women. Keywords HCV, pregnant women, prevalence, rural, Egypt, risk factors Introduction It is estimated that million people or approximately 3% of the world s population are living with chronic hepatitis C virus (HCV) infection. 1 In Egypt, the incidence was estimated to be about 7/1,000 with 14.7% prevalence. One in every 10 Egyptians is a carrier of HCV infection. This means that there are at least 4.5 million persons infected with HCV who are infectious to others. More than 500,000 new HCV infections occur in Egypt every year, likely signalling an epidemic in a country of more than 85 million people. 2 With a 75 85% rate of chronicity, cirrhosis develops in around 10% of chronic cases in 20 years and the percentage increases to 20% in 30 years. The annual rate of mortality in cirrhotic patients is approximately 1 5% per year and that of hepatocellular carcinoma is 12.8% per year. 3 The rate of HCC development among HCV-infected persons is in the range of 1 3% after 30 years. 4 HCV increases HCC risk by promoting fibrosis and eventually cirrhosis. Once HCV-related cirrhosis is established, HCC develops at an annual rate of 1 4%, although rates of up to 7% have been reported in Japan. 5 The prevalence of HCV infection in pregnant women varies widely among studies, in the range of % worldwide, but in Egypt it was estimated to be about 15.8%. 6 The presence of HCV infection does 1 Resident Physician, Alexandria fever hospital, Alexandria, Egypt 2 Professor, Tropical Health Department, Tropical Health High Institute of Public Health, University of Alexandria, Alexandria, Egypt 3 Professor, Tropical Health Department of Tropical Health, High Institute of Public Health, University of Alexandria, Alexandria, Egypt 4 Assistant Professor, Tropical Health Department, Tropical Health High Institute of Public Health, University of Alexandria, Alexandria, Egypt Corresponding author: Hossam Hassan Khamis, Tropical Health Department, High Institute of Public Health, University of Alexandria, Alexandria, Egypt. hossam.khamis84@gmail.com

2 22 Tropical Doctor 46(1) not appear to result in a high-risk pregnancy or a higher incidence of poor obstetric outcome. 7 The rate of vertical transmission of HCV has also been estimated with widely varying results, approximately 5% of pregnant women with chronic HCV infection will transmit the virus to their infants and about 25% of infected infants will clear the virus spontaneously. The other 75% generally have only mild hepatitis throughout childhood, but they require follow-up because a small percentage will develop progressive liver disease and are at risk for hepatocellular carcinoma. 8 Pregnancy, however, seems be an opportune time to screen for HCV infection. Many women will already have reached their peak likelihood of becoming infected by the time they become pregnant, making the yield of testing near its maximum. Screening at this point in a woman s life may lead to an early diagnosis, with the chance of treatment that may offset the future burden of HCV on the healthcare system as well as providing care to pillars of family life in the Egyptian context. Furthermore, testing for HCV during pregnancy may help to identify infected newborns, allowing for appropriate follow-up and increasing awareness of control measures to be applied to house hold contacts. Patients and Methods There are 14 villages affiliated to Al-nobareya town. Most of residents of these villages had moved recently from different rural governorates to live and work. The total population size is 60,588 persons according to Albeheira Governorate (personal communication). We randomly selected nine villages, namely: Belal; Aboelyosr; Elishaa; Soliman; Adam; Abd Elwahab; Abd Alrakeeb; Alemam Malek; and Yousef. Each of the selected villages is designed to be 1 km 2 and their population sizes are 6,120, 4,209, 6,125, 4,143, 6,360, 4,550, 5,540, 6,790 and 5,370, respectively, representing about half the total population of Al-nobareya town. Each of the selected villages has one antenatal healthcare unit. This study was carried out among pregnant women visiting the antenatal healthcare units in the selected villages for regular follow-up. In this cross-sectional study, no age restriction was made but pregnant women known to be HCV-infected or have a history of chronic liver disease were excluded. Using a power of 80%, an alpha error of 0.05 and a precision of 2%, the minimal required sample size to estimate the prevalence of HCV infection among pregnant women was found to be 360 cases. The sample size was calculated using STATA software and depending on a prevalence of 10.8%. 6 For nearly 18 weeks, one of the participating antenatal healthcare units was visited each week and sometimes the researcher had to visit the same unit more than once. The purpose was to include all eligible pregnant women visiting these units. During each visit about 20 women were included. The study protocol strictly followed the declaration of Helsinki and was approved by the High Institute of Public Health Ethics Committee. The participating women gave an informed consent before enrolment in the study. A pre-designed questionnaire was completed. It contained data regarding sociodemographic detail and contacts, and information regarding possible risk factors including history of operations, dental procedure, blood transfusion, tattooing, circumcision, intravenous drugs, invasive procedures, HCV-positive husband, family history, contact with jaundiced patient, contact with a diagnosed HBV or HCV patient and so on. A 5 ml blood sample was withdrawn using universal sterile precautions. The sera were separated and preserved at 20 C. All samples were tested for HCV-Ab using a third generation ELISA test (WKEA, Zhejiang, China). All study participants were informed about their results. Only those who were positive for HCV-Ab were invited to provide blood samples for the following tests: 1. PCR test (real-time cobas amplipred cobas Taqman); 2. ELISA (Dialab, Austria, Vienna) for hepatitis B virus surface antigen (HBs-Ag) and core antibodies (anti-hbc). Results During the 4-month recruitment period, 360 women consented to participate in the present study. Of them, only 22 were found to be HCV-Ab positive indicating a sample prevalence of 6.1% (95% confidence interval [CI], ). The prevalence in different villages is shown in Table 1. About 77.3% (17/22) of the HCV-Ab positive women were found in four of the total nine villages, namely Abo-elyosr, Adam, Malek and Belal. No statistical difference was noted between villages in which the prevalence was in the range of %. The age of participants was in the range of years ( x ¼ years). The mean age for HCV- Ab positive women was years which was significantly higher (P ¼ 0.023) than HCV-Ab negative women ( x ¼ years). As shown in Table 2, the highest prevalence was found among pregnant women who were aged above 35 years (13.2%) while the least prevalence was found in those who were aged years (2.3%). Although pregnant women who

3 Khamis et al. 23 Table 1. Prevalence of HCVAbs in different villages. Village name HCV Abs ve (n ¼ 388) þ ve (n ¼ 22) Belal Solyman Abo-elyosr Abd elwahab Abd elrakeeb Malek Elishaa Yousef Adam MC p Table 2. Pervalence of the pregnant women in different age groups. Age group HCV Ab Positive No. (n ¼ 360) No (n ¼ 22) % Test of sig MC p ¼ * þ Mean SD t ¼ * MC p: p value for Monte Carlo test. t: Student t-test. *Statistically significant at p p ¼ were aged above 30 years constituted about one-quarter of the studied population, they contributed to more than half of those proved to be HCV-Ab positive. About one-third of the participants were illiterate and another one-third had secondary school education. This made no significant difference between seronegative and seropositive women (P value ¼ 0.567). Most of the surveyed women (96.4%) were housewives and only 3.6% were working. There was no significant difference between seropositive and seronegative women regarding to the nature of their work (P ¼ 0.567). Surprisingly, none of potential HCV risk behaviour individually or combined appeared to have a relation with the presence of HCV-Ab in the study participants. Blood transfusion and dental manouvres but did not reach significance (P values ¼ and 0.879, respectively). None of the factors related to previous gestational history was significantly associated with HCV-Ab presence. These factors included: number of previous pregnancies; history of bleeding during pregnancy; type of previous labour; and medical history related to pregnancy. The sociodemographic data of the husbands are shown in Table 3. Their ages were in the range of years ( x ¼ years). About half of them (52.8%) were aged years. The mean husbands age for HCV-Ab positive women husbands was significantly higher (P ¼ 0.013) than that of HCV-Ab negative women. More than one-quarter of the husbands were illiterate. Those who reached a secondary education constituted 37.5%. Only 8.6% had a university degree. The educational levels were distributed normally between both groups except for those who could only read and write (50% in each group; P ¼ 0.007). However, the type of work of the husbands did not differ significantly between both groups. The percentage of HCV-positive women whose husbands had dental manoeuvres was higher than those who denied such a history, but did not reach a statistically significant level (P ¼ 0.067). A history of tattooing, intravenous medications and surgical operation of husbands were not significantly associated with HCV infection in their wives. A history of chronic liver disease in the husbands was significantly associated with seropositive HCV-Ab in their pregnant women. About one-third of those who reported chronic liver disease were among the husbands of HCV-Ab positive group (P ¼ 0.018). Regarding the presence of HCV viraemia as detected by real time PCR, only 20 out of the 22 HCV positive pregnant women consented to have this test. Less than half of them (9/20; 45%) had viraemia. The viraemia ranged from to with a mean SD of ( ). Only one (4.5%) had a detectable HBsAg and four (18.2%) had evidence of exposure to HBV as indicated by detection of (anti-hbc). None of the factors listed in Table 5 was associated with persistence of HCV infection indicated by positive results of PCR. Seven women (77.8%) of the PCR-positive women were aged over 30 years and none of the six seropositive women aged years had viraemia. Moreover, neither husband s age nor his history of chronic liver disease were associated with presence of viraemia (P ¼ and 1.000, respectively). Discussion The prevalence rate of HCV infection in pregnant women in this study (6.1%) is lower than that reported before in other similar studies. It was reported to be 15.8%, 11.7% and 8.6% in 2006, 6, and ,

4 24 Tropical Doctor 46(1) Table 3. Distribution of the studied sample according to Sociodemographic characteristics of the husband. HCV Ab Sociodemographic characteristics of the husband Negative (n ¼ 338) Positive (n ¼ 22) Test of significance ge in years þ Mean SD (Median) (30.0) (30.0) (35.0) Education Illiterate Read and Write Primary Middle Secondary University Work Farmer Clerk Manual Professional Others X 2 ¼ * p ¼ t ¼ 2.71 p ¼ MCP ¼ MCP¼ 0.89 Table 4. Distribution of the studied sample according to risk factors of HCV in the husband. HCV Ab Negative (n ¼ 338) Positive (n ¼ 22) Risk factors for HCV Test of significance Dental manouvers No Yes Tattoing No Yes Intravenous drug use No Yes Surgical operation No Yes Chronic liver disease No Yes X 2 ¼ 3.36 p ¼ FETp ¼ FETp ¼ X 2 ¼ 0.05 p ¼ FETp ¼ 0.018

5 Khamis et al. 25 Table 5. Relationship between PCR results and different parameters of pregnant women. PCR ve (n ¼ 11) þ ve (n ¼ 9) Test of sig. Age MCp ¼ þ Mean SD p ¼ Education Illiterate Read and write Primary MCp ¼ Middle Secondary Undergone surgery No Minor MCp ¼ Mojor Had blood or blood production transfusion No Yes (After 1992) FEp ¼ Undergone dental manipulation No Infrequent MCp ¼ Frequent Sharing razors, tooth brush, or any item that could carry infected blood No Yes FEp ¼ Number of pervious pregnancies p ¼ MCp ¼ History of bleeding during pregnancy No Yes FEp ¼ Medical history related to pregnancy None HTN MCp ¼ Bleeding

6 26 Tropical Doctor 46(1) respectively. This may reflect a better control strategy with decreasing frequency overtime. Although the prevalence of HCV in Egypt appears to have decreased, it is still higher than in other developing countries such as Pakistan (3.44%), 11 India (1.03%) 12 and Nigeria (0.4%). 13 In Canada, Collen et al. found that the prevalence was 0.5% among pregnant women. 14 In Central Brazil, out of 28,561 pregnant women the prevalence of HCV infection was 0.15% (95% CI, %). 15 Our study showed that the most important risk factors for HCV infection among pregnant women were older age of the pregnant woman, older age of the husband and chronic liver disease of the husband. In agreement with our results, Abdulqawi et al. 10 and Costa et al. 15 found an association between HCV infection and older age of the pregnant women. In contrast to our results, however, Zahran et al. reported that there were no significant differences in mean age of the HCV seropositive and seronegative pregnant women. 9 The higher rate of infection among the older age group can be explained by a cohort phenomenon and the cumulative effect of exposure to HCV due to the long period of viral exposure over one s lifetime, as well as exposure to other potential HCV risk factors. Surprisingly, none of the potential HCV risk behaviours of the pregnant women had a relation with the presence of HCV-Ab in the study participants. But we found a significant association between seropositivity and husband s age and being a chronic liver disease patient. This suggests a degree of caution regarding the sexual route of transmission. According to this study, blood transfusion had a respectable association with HCV infection as 13.6% of the seropositive women had previous blood transfusion (3/22) but it did not reach a significant value as pregnant women who previously received blood transfusion and have HCV-Ab were only 0.83% of all screened women, while those who received blood but did not have HCV-Ab were 3.33% of all screened women. These findings closely coincide with that of Ashok Kumar et al. (4.8% of HCV-Ab had blood transfusion versus 3.1% among HCV-Ab negative). 12 In contrast, Zahran et al. reported a history of blood transfusion in 6.6% of HCV-Ab positive versus 2.2% in those who were negative. 9 AbdulQawi et al. also found blood transfusion as a risk factor for infection (15% of HCV-Ab positive women had transfusion versus 3.9% among HCV-Ab negative women). 10 Conclusion The prevalence of HCV infection in pregnant women in Egypt appears to be lower than previously reported. The detected risk factors are: age of the pregnant women; age of their husbands; and chronic liver disease of the husbands. None of the other known risk factors was found to be significantly associated with the HCV infection. Declaration of conflicting interests None declared. Funding This case report received no specific grants from any funding agency in the public, commercial or not-for-profit sectors. References 1. Houghton M. The long and winding road leading to the identification of the hepatitis C virus. J Hepatol 2009; 51: Mohamoud YA, Mumtaz GR, Riome S, Miller D and Abu-Raddad LJ. The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis. BMC Infect Dis 2013; 13: World Health Organization. Cancer. Fact sheet number 297. Geneva: WHO, Goodgame B, Shaheen NJ, Galanko J and El-Serag HB. The risk of end stage liver disease and hepatocellular carcinoma among persons infected with hepatitis C virus: publication bias? Am J Gastroenterol 2003; 98: El-Serag HB. Hepatocellular carcinoma and hepatitis C in the United States. Hepatology 2002; 36(5 Suppl 1): S Stoszek SK, Abdel-Hamid M, Narooz SH, El Daly M, Saleh DA, Mikhail N, et al. Prevalence of and risk factors for hepatitis C in rural pregnant Egyptian women. Trans R Soc Trop Med Hyg 2006; 100: Newell ML and Pembrey L. Mother-to-child transmission of hepatitis C virus infection. Drugs Today (Barc) 2002; 38: Robinson JL. Vertical transmission of Hepatitis C virus: current knowledge and issues. Paediatr Child Health 2008; 13: Zahran KM, Badary MS, Agban MN and Abdel Aziz NH. Pattern of hepatitis virus infection among pregnant women and their newborns at the Women s Health Center of Assiut University, Upper Egypt. Int J Gynaecol Obstet 2010; 11: AbdulQawi K, Youssef A, Metwally A, Ragih I, AbdulHamid M and Shaheen A. Prospective study of prevalence and risk factors of hepatitis C in pregnant Egyptian women and its transmission to their infants. Croat Med J 2010; 51: Shaikh F, Naqvi SQ, Jilani K and Memon RA. Prevalence and risk factors of hepatitis C virus during pregnancy in Pakistan. Gomal J Med 2009; 7: Kumar A, Sharma KA, Gupta RK, Kar P and Chakravarti A. Prevalence and risk factors for hepatitis C virus among pregnant women. Indian J M Ed Res 2007; 126: Clement MI, Andy EI, Eni LO and Jewell PA. Prevalence, sociodemographic characterestics and risk

7 Khamis et al. 27 factors for hepatitis C infection among pregnant women in Calabar municipality, Nigeria. Hepat Mon 2010; 10: McDermott CD, Moravac CC and Yudin MH. The effectiveness of screening of Hepatitis C virus in pregnancy. JOGC 2010; 32: Costa ZB, Machado GC, Avelino MM, Gomes Filho C, Macedo Filho JV, Minuzzi AL, et al. Prevalence and risk factors for Hepatitis C and HIV-1 infections among women in Central Brazil. BMC Infect Dis 2009; 9: 116.