Seroprevalence of hepatitis B, hepatitis C, and HIV in pregnant women from Eastern Turkey.
Hepatitis B virus (HBV) may cause chronic viral hepatitis, liver cirrhosis, and even hepatocellular carcinoma (HCC) in the long term. HBV is responsible for approximately one million deaths per year. It is estimated that 257 million people are chronically infected with HBV. In 2015, 887,000 people died due to complications of HBV infection, cirrhosis, and liver cancer, which could be prevented by vaccination. The World Health Organization has declared HBV as the second important carcinogen after tobacco and has recommended routine newborn vaccinations (1,2). HBV can be transmitted parenterally (percutaneous contact with infected blood or body fluids), horizontally (close contact without intercourse), sexually, and perinatally or vertically (from mother to child). In highly endemic areas, perinatal transmission is one of the most significant ways of HBV spread. Intrauterine infection of the fetus is of low possibility due to the placental barrier. The transmission of HBV usually occurs during or after labor through the contact of the epithelia and mucosal surfaces with infected maternal fluids, swallowing of maternal blood while passing through the vaginal channel, contact with the mother's blood during cesarean section, or via a damaged placenta (3). When the mother is acutely infected, the infection risk for the infant is 10% in the first 2 trimesters and 80-90% during the last trimester and the prenatal period (4). About 50% of pregnant women with chronic HBV infection infect their infants in the perinatal period. Maternal HBeAg positivity and HBV DNA levels are important in perinatal transmission. The risk of HBV transmission from an HBeAg-positive mother is 70-90%, where-as this rate is around 10-40% for the HBeAg-negative mother. As the viral load increases, the transmission rate of HBV also increases (5,6).
Chronic HBV infection risk is inversely proportional to maternal age. The rate of chronic HBV infection is higher than 90% in newborns, 20-30% in children exposed to HBV at the age of 1-5, and less than 5% in adults (7). Accordingly, it was reported that before the standardization of vaccination and hepatitis B immune globulin (HBIG) application, 70-90% of infants of mothers with chronic HBV infection would become chronically infected in the following 6 months. In pregnant women infected with HBV, the superiority of vaginal birth over cesarean section or vice versa has not been demonstrated. Since it does not prevent intrauterine transmission, cesarean section should be preferred only in the presence of obstetric indications.
A protection rate of 90% is possible via immunization (8). Some infants may be affected (8-30%) despite the administration of vaccination with HBIG. High levels of maternal viremia, HBV infection during intrauterine period, and inactivity of HBIG due to the mutation of the gene coding HBsAg have been suggested as reasons (3). HBIG and HBV vaccines should be administered to infants of mothers infected by HBV in the first 12 hours after labor; the vaccination should be applied in three doses within the first year (at birth, fourth week, and at 6 months). In one study, maternal HBIG application to HBsAg and HBeAg positive pregnant women in the third trimester was shown to be advantageous and effective in preventing intrauterine fetal HBV infection and contributed to the enhancement of immune responses of the infants (3,9). Although routine vaccination is not suggested during pregnancy, there is no negative impact of HBV vaccine on the mother or the fetus (10). The Turkish Ministry of Health applies HBV vaccination routinely to all newborns since 1998.
Hepatitis C virus (HCV) is another important hepatitis agent that may cause chronic viral hepatitis, liver cirrhosis, and HCC (5,6). It is estimated that there are 170 million HCV-positive people in the world, and the HCV prevalence rates are between 1-8% among pregnant women (6). Although at a lower rate compared to HBV and HIV, HCV infection can also be transmitted perinatally. Perinatal transmission is the major source of pediatric HCV infection. Thus, nearly 7000 new HCV cases are born from infected mothers each year (11). Perinatal transmission rates are reported as 4-7%, and transmission occurs if HCV-RNA is positive in maternal blood during labor (5,6). The transmission risk is closely related to the viral load. In cases where the viral load is higher than [10.sup.6] copies/mL, the risk increases up to 36% (12). Other factors increasing transmission risk are the presence of HIV co-infection, intravenous drug use, prolonged membrane rupture, elongated labor action, exposure of the fetus to maternal blood or secretions, and invasive internal fetal monitoring (5,6). Cesarean section and breastfeeding do not increase the risk of transmission if the mother is only HCV positive but increase the risk for HIV co-infected women (5).
Some studies have reported perinatal complications in anti-HCV positive pregnant women, such as early membrane rupture, preterm delivery, placental abruption, low birth weight, low Apgar score, congenital malformation, neonatal jaundice, and perinatal mortality; however, these were not confirmed by other studies (5,6,13-15).
Human immunodeficiency virus (HIV) is another important virus that may be vertically, perinatally, and postnatally transmitted from the mother to the fetus at a total rate of 35-40% (16).
Vertical transmission of HBV, HCV, and HIV infections are important public health problems. Many studies have been conducted on the seroprevalence of these infections in pregnancy (Table 1) (1,7,17-26). The aim of this study was to evaluate HBV, HCV, and HIV seroprevalence in pregnant women and to compare the results with previous data from Turkey.
MATERIALS AND METHODS
This retrospective study was conducted between January 2013 and December 2016 on pregnant women who presented to a regional maternity hospital in Eastern Anatolia for antenatal follow-up or delivery. Ethical approval was obtained from the Ethics committee of the Erzurum Regional Training and Research Hospital in 2013. Data were collected from the hospital electronic health records and patient files. Blood samples were tested at the microbiology laboratory of the hospital. HBsAg, anti-HBs, anti-HCV, anti-HIV levels were determined using the chemiluminescence enzyme immunoassay method (Architect, Abbott Laboratories, USA). Qualitative anti-HCV and anti-HIV results that were examined during this period were also included in the study. The results were evaluated in terms of the number of cases and percentages. Due to the retrospective nature of the study, informed consent forms could not be obtained.
Statistical analysis was performed using the Statistical Package for Social Sciences version 17.0 (SPSS Inc.; Chicago, IL, USA) software. Results of the analyses were described in the form of frequencies and percentages.
A total of 35,295 pregnant women were included in this study. The mean age of the patients was 25.35[+ or -]5.18 years. The HBsAg, anti-HBs, anti-HIV, and anti-HCV results were evaluated separately for each year (Table 2, Figure 1). HBsAg and anti-HBs levels were determined as 1.2% (425/35295) and 27.7% (9583/34.483), respectively. From 2013 to 2016, the rate of HBsAg decreased from 1.4% to 0.87%, and anti-HBs levels increased from 25.4% to 30.2%.
Anti-HCV was detected in 6 of the 9,709 patients tested (0.06%). All the 7,113 women tested for HIV showed negative results, and none had co-infections. HCV and HIV tests were not screened in all patients because seroprevalences of HCV and HIV are very low among people living in Turkey. Occasionally, kits were not available in the hospital laboratory. Another important cause was the different test-ordering behaviors of doctors.
Turkey is considered an intermediate country according to the HBV prevalence classification (7). In Turkey, 4-10% of the population (3-5 million) is considered HBV carriers. The mean HBsAg and anti-HBs seropositivity rates among pregnant women in Turkey were reported as 4.4% (range: 1.2-12.3%) and 23% (range: 3.7-41.1%), respectively (7,17).
In previous studies in Eastern Turkey, Parlak et al. (20) and Kadanali et al. (21) reported HBsAg positivity rates in pregnant women as 2.3% and 6.3%, respectively. In our study, among 35,265 pregnant women, the total HBsAg and anti-HBs positivity rates were 1.2% and 27.7%, respectively. From 2013 to 2016, the HBsAg positivity rate decreased from 1.4% to 0.87% and that of anti-HBs increased from 25.4% to 30.2%. In other regions of Turkey, HBsAg positivity rates in pregnant women were reported between 1.5-5.1% (18,19,23-26). In a nationwide study conducted on 20,472 persons between 1987 and 1998, the HBsAg and antiHBs positivity were reported as 4.4% and 23%, respectively. In another nationwide study performed between 1998 and 2012, HBsAg was positive in 4.3% of the 41,107 persons tested (17).
When compared with the results from other studies, the antibody values were higher and antigen levels were lower than the national and previous regional values. This situation shows the success of HBV vaccination in this region. When the results of our study were compared with the general population in this region, it was noted that the HBV carrier rate in pregnancy is lower and antibody levels are higher. Furuncuoglu et al. (26) reported a similar increase in the rate of anti-HBs and decrease in the rate of HBsAg in their study conducted on pregnant women over a 20-year period. Similarly, Guclu et al. (28) reported a decrease in the HBsAg positivity after the introduction of the national HBV vaccination program.
Lowering the rate of HBsAg to 1.2% in the last 20 years is a remarkable success in terms of controlling HBV infection. The low carrier rate encountered in Turkey is a pleasant consequence of the vaccinations conducted by the Ministry of Health, improvement of public hygiene, and awareness raised by organizations, such as the Viral Hepatitis Control Society and the Turkish Liver Research Society.
We contemplate that, the low level of HBV carriage among pregnant women in the present study region is a milestone for the prevention of the infection occurrence in the next generations. Besides, our results indicate the progress in the control of HBV infection. Since it includes the most recent data and due to the large sample size, our study reflects the latest condition. This seems promising, but in terms of immunization, there is still a way to go.
Hepatitis B virus seroprevalences in pregnancy similar to our results have been reported from other countries. The HBsAg seropositivity was found 1.9% in Bali, 1% in northern Italy, 1.7% in Panama, 4.6% in Niger, and 2.8% in Greece (29-33).
In Turkey, the anti-HCV positivity rate was reported as 0.3% (range 0-1.5%) among blood donors and the general population and as 0-2.04% among pregnant women (27).
Erol et al. (34) detected an anti-HCV positivity of 1.12% in 26,577 blood donors. In the current study, only 6 HCV positive results were found out of 9,709 (0.06%) pregnant women, and this value is low when compared to previous regional and national data.
The prevention of HIV transmission from the mother to the newborn is possible with screening and antiviral treatment of the mother during pregnancy and prophylaxis administered to the newborn after delivery. Particularly, pregnant women in risk groups should be screened in HIV-endemic areas (16). In this study, all 7,113 patients examined for anti-HIV showed negative results. Studies investigating HIV antibody among pregnant women in Turkey generally did not find any positive cases, and the positivity detected in a few patients was determined to be false positive after subsequent tests. As in our study, also Ozlu et al. (18) and Dundar et al. (29) could not detect any HIV positivity using the enzymelinked immunosorbent assay (ELISA) test, and the only studies that have reported positivity were those by Madendag et al. (18) with 0.0004% positivity rate in 60,562 pregnant women and Tekay et al. (22) with 0.1% seropositivity in 2,548 pregnant women. In summary, the absence of HIV positive patients in our sample was consistent with literature.
In this study, HCV and HIV positive results were extremely low. The results of the study showed that HBV carriage is decreasing, and immunity is increasing in the study region.
Limitations of the study
We could not document the age groups of the mothers and the perinatal complications in this study. Besides, not all the samples could be tested for antiHCV and HIV.
In conclusion, hepatitis B virus carriers among pregnant women in Eastern Turkey are gradually decreasing, and immunity is increasing. HCV seroprevalence is low, and HIV positivity is not encountered in the study region. To prevent perinatal infections and protect the newborn from the long-term effects, all pregnant women should be screened for HBV, HCV, and HIV in addition to risk group screening.
Ethics Committee Approval: Ethics committee approval was received for this study from Ethics Committee of the Erzurum Regional Training and Research Hospital.
Informed Consent: N/A.
Peer-review: Externally peer-reviewed.
Author Contributions: Concept - E.C.T., Z.O.; Design - Z.K., O.K., Supervision - Z.O.; Materials - E.C.T., O.K., B.G.K.; Data Collection and/or Processing - H.A., E.C.T., B.G.K.; Analysis and/or Interpretation - E.C.T., Z.O., O.C.; Literature Search - Z.K., H.A., B.G.K.; Writing Manuscript - E.C.T., Z.O., O.K.; Critical Review - Z.O.
Conflict of Interest: The authors have no conflict of interest to declare.
Financial Disclosure: The authors declared that this study has received no financial support.
(1.) World Health Organization, Global Hepatitis Report 2017. (http://www.who.int/hepatitis/publications/global-hepatitis-report2017/en/) accessed 06/02/2018.
(2.) Dinsmoor MJ. Hepatitis in the obstetric patients. Infect Dis Clin North Am 1997; 11: 77-91. [CrossRef]
(3.) Aktug Demir N, Asan A, Ayaz C, et al. Management of Chronic Hepatitis B in Pregnancy: A Consensus Report of the Study Group for Viral Hepatitis of the Turkish Society of Clinical Microbiology and Infectious Diseases. Klimik Journal 2013; 26(Suppl 1): 12-9. [CrossRef]
(4.) Cunningham GF, Gant NF, Leveno KJ, et al. Gastrointestinal Disorders. In: Williams Obstetrics, 21st ed. New York: McGraw-Hill, 2001; pp: 1273-1306.
(5.) Tosone G, Maraolo AE, Mascolo S, et al. Vertical hepatitis C virus transmission: Main questions and answers. World J Hepatol 2014; 6: 538-48. [CrossRef]
(6.) Yeung CY, Lee HC, Chan WT, et al. Vertical transmission of hepatitis C virus: Current knowledge and perspectives. World J Hepatol 2014; 6: 643-51. [CrossRef]
(7.) Mistik R, Balik I. Epidemiological analysis of viral hepatitis in Turkey. In: Kilicturgay K, Badur S editors. Viral Hepatitis. Istanbul: Medikal Saglik ve Yayincilik, 2001; p:10-55.
(8.) Wasmuth JC. HepatitisB-epidemiology, transmission and natural history. In: Mauss S, Berg T, Rockstroh J, Sarrazin C, Wedemeyer H, editors. Hepatology. Dusseldorf: Flying Publisher; 2009, p: 25-36.
(9.) Xiao XM, Li AZ, Chen X, et al. Prevention of vertical hepatitis B transmission by hepatitis B immunoglobulin in the third trimester of pregnancy. Int J Gynaecol Obstet 2007; 96:167-70. [CrossRef]
(10.) Grosheide PM, Wladimiroff JW, Heijtink RA, et al. Proposal for routine antenatal screening at 14 weeks for hepatitis B surface antigen. Br Med J 1995; 311:1197. [CrossRef]
(11.) Bal A, Petrova A. Single Clinical Practice's Report of Testing Initiation, Antibody Clearance, and Transmission of Hepatitis C Virus
(HCV) in Infants of Chronically HCV Infected Mothers. Open Forum Infect Dis 2016; 3: of w021.
(12.) Thomas, SL, Newell ML, Peckham CS, et al. A review of hepatitis C virus (HCV) vertical transmission: risks of transmission to infants born to mothers with and without HCV viraemia or human immunodeficiency virus infection. Int J Epidemiol 1998; 27:108-20. [CrossRef]
(13.) Reddick KL, Jhaveri R, Gandhi M, et al. Pregnancy outcomes associated with viral hepatitis. J Viral Hepat 2011; 18: e394-8. [CrossRef]
(14.) Pergam SA, Wang CC, Gardella CM, et al. Pregnancy complications associated with hepatitis C: data from a 2003-2005 Washington state birth cohort. Am J Obstet Gynecol 2008; 199: 38.e1-9. [CrossRef]
(15.) Buresi MC, Lee J, Gill S, et al. The prevalence of gestational diabetes mellitus and glucose abnormalities in pregnant women with hepatitis C virus infection in British Columbia. J Obstet Gynaecol Can 2010; 32: 935-41. [CrossRef]
(16.) Rimawi BH, Haddad L, Badell ML, et al. Management of HIV Infection during Pregnancy in the United States: Updated Evidence-Based Recommendations and Future Potential Practices. Infect Dis Obstet Gynecol 2016; 2016: 7594306. [CrossRef]
(17.) Tosun S. Turkiye'de viral hepatit B epidemiyolojisi yayinlarin metaanalizi. In: Tabak F, Tosun S editors. Viral Hepatit 2013, 1. Baski, Istanbul: Medikal Saglik ve Yayincilik, 2013; p 25-80. (in Turkish).
(18.) Madendag Y, Madendag Ic: Celen S, Unlu S, Danisman N. Seroprevalence of Hepatitis B, Hepatitis C And HIV at whole obstetric and gynecologic patients who applied our hospital. J Gynecol Obst 2007; 17:442-6. (in Turkish).
(19.) Ozlu T, Tas T, Mengeloglu FZ, et al. Frequency of HBsAg, anti-HCV, and anti-HIV in pregnant women and/or patients with gynecologic diseases in a tertiary hospital. J Clin Exp Invest 2013; 4: 166-70. [CrossRef]
(20.) Parlak M, Selimoglu M, Energin M, et al. Prevalance of Hepatitis B in pregnant women and perinatal transmission. Turkiye Klinikleri Journal of Gastroenterohepatology 1994; 5:270-2. (in Turkish).
(21.) Kadanali A, Celebi S, Aydos, SK, et al. Perinatal transmission of Hepatit B virus in Erzurum. AUTD 1997; 29: 450-42. (in Turkish).
(22.)Tekay F, Ozbek E. Hepatitis B, Hepatitis C and Human Immunodeficiency Virus seropositivities in women admitted to Sanliurfa Gynecology And Obstetrics Hospital. Mikrobiyol Bult 2006; 40:369-72.
(23.) Dundar O, Celik S, Tutuncu L, et al. The prevalence of Hepatitis B, Hepatitis C, HIV, toxoplasmosis and rubella among pregnant women delivered in our clinic between 2000 and 2005. Zeynep Kamil Tip Bulteni 2009; 40: 1-9.
(24.) Cicek CA, Duygu F ve Inakci IH. Hepatitis B and Hepatitis C Seropositivities in Women Admitted To Gynecology and Obstetrics Hospital in Sanliurfa City: A 3- Year Evaluation. Viral Hepat J 2012; 18: 15-8.
(25.) Kolgelier S, Demir LS, Demir NA, et al. Seropositivity of HBsAg and anti-HCV in Pregnant Women in Adiyaman. Viral Hepat J 2012; 18: 98-101.
(26.) Furuncuoglu Y, Bolukbas FF, Bolukbas C, et al. Changes in the prevalence of HBV infection in pregnant women in Turkey between 1995 and 2015: a 20-year evaluation. Postgrad Med J 2016; 92:5 [10.sup.3]. [CrossRef]
(27.) Mistik R. The epidemiology of hepatitis C virus infection. In: Tabak F, Tosun S editors. Viral Hepatit 2013, 1. Baski, Istanbul: Medikal Saglik ve Yayincilik, p. 2013: 83-112.
(28.) Guclu E, Ogutlu A, Karabay O. A Study on the Age-Related Changes in Hepatitis B and C Virus Serology. Eurasian J Med 2016; 48:37-41. [CrossRef]
(29.) Surya GP, Kornia K, Suwardewa TGA. Serological markers of hepatitis B, C, E viruses and HIV type-1 infections in pregnant women in Bali, Indonesia. J Med Virol 2005; 75:499-503. [CrossRef]
(30.) Baldo V, Fleroani A, Menegon T, et al. Hepatitis C virus, hepatitis Bvirus infection in pregnant Women in Nort-East Italy: a seroepide-miological study. Eur J Epidemiol 2000; 1: 87-91. [CrossRef]
(31.) Bertolini DA, Pinho JRR, Saraceni CP. Prevalence of serological markers of hepatitis B virus in pregnant women from Parana State, Brazil. Braz J Med Biol Res 2006; 39:1083-90. [CrossRef]
(32.) Obi SN, Onah HE, Ezugwu FO. Risk factors for hepatitis B infection during pregnancy in a Nigerian obstetric population. J Obstet Gynaecol 2006; 26: 770-2. [CrossRef]
(33.) Papaevangelou V, Hadjichristodoulou C, Cassimos D. Adherence to the screening program for HBV infection in pregnant women delivering in Greece. BMC Infect Dis 2006; 6: 84. [CrossRef]
(34.) Erol S, Sahin UA, Ozkurt Z, et al. Seroprevalence of HBsAg, anti-HCV, anti-HIV and Non-treponemal syphilis antibody in blood donor at Erzurum region. J Turk Microbiol Soc 2001; 31: 245-9.
Esra Cinar Tanriverdi (1) [iD], Zulal Ozkurt (2), Berrin Goktug Kadioglu (3) [iD], Handan Alay (4) [iD], Oksan Calikoglu (5) [iD], Ozlem Koca (6) [iD], Zeynep Kamalak (7)
(1) Department of Medical Education, Gynecology and Obstetrics, Ataturk University School of Medicine, Erzurum, Turkey
(2) Department of Infectious Diseases, Ataturk University School of Medicine, Erzurum, Turkey
(3) Department of Gynecology and Obstetrics, Nenehatun Maternity Hospital, Erzurum, Turkey
(4) Department of Infectious Diseases, Nenehatun Maternity Hospital, Erzurum, Turkey
(5) Department of Public Health, Ataturk University School of Medicine, Erzurum, Turkey
(6) Department of Microbiology, Ataturk Regional Hospital, Antalya, Turkey
(7) Department of Gynecology and Obstetrics, Buhara Hospital, Erzurum, Turkey
Cite this article as: Qinar Tanriverdi E, Ozkurt Z, Goktug Kadioglu B, et al. Seroprevalence of hepatitis B, hepatitis C, and HIV in pregnant women from Eastern Turkey. Turk J Gastroenterol 2019; 30(3): 260-5.
Corresponding Author: Zulal Ozkurt; email@example.com
Received: October 11, 2018 Accepted: July 16, 2018 Available online date: December 7, 2018
Table 1. Previous studies on HBV, HCV, and HIV seroprevalences among pregnant women in Turkey (*) Study and Year Region HBsAg n (%) Anti-HBs (%) 1987-1998 (17) Nationwide 20 472 (4.4) 23% 1998-2012 (17) Nationwide 41 107 (4.3) - Parlak et al. 1994 (20) Erzurum 171 (2.3) 31.5% Kadanali et al. 1997 (21) Erzurum 282 (6.3) - Tekay et al. 2006 (22) Sanliurfa 2335 (5.1) - Madendag et al. 2007 (18) Ankara 90 351 (2.1) - Dundar et al. 2009 (23) Istanbul 3503 (2.2) - Cicek et al. 2012 (24) Sanliurfa 56 275 (3.5) 25% Ozlu et al. 2012 (19) Bolu 1653 (1.8) - Kolgelier et al. 2012 (25) Adiyaman 9420 (4.7) 38.4% Furuncuoglu et al. 2015 (26) Istanbul 7605 (1.5) 11.5% Tanriverdi EC, 2016 Erzurum 35 265 (1.2) 9583/34 489(27.7) Study and Year Anti-HCV n (%) Anti-HIV n (%) 1987-1998 (17) - - 1998-2012 (17) - - Parlak et al. 1994 (20) - - Kadanali et al. 1997 (21) - - Tekay et al. 2006 (22) 2066 (0.9) 2548 (0.1) Madendag et al. 2007 (18) 60 729 (0.2) 6056(0.004) Dundar et al. 2009 (23) 3496 (0.1) 3496 (0) Cicek et al. 2012 (24) 13719 (0.8) - Ozlu et al. 2012 (19) 653 (0.5) 653 (0) Kolgelier et al. 2012 (25) 0.2% - Furuncuoglu et al. 2015 (26) - - Tanriverdi EC, 2016 6/9709 (0.06) 0/7113 (0) (*) Adapted from reference number 17 Table 2. HBsAg, anti-HBs, anti-HCV, and anti-HIV positivities of pregnant women Year HBsAg n (%) Anti-HBs n (%) Anti-HCV n (%) 2013 128/9191 (1.4%) 2150/8465 (25.4%) 1/3412 (0.03%) 2014 114/8692 (1.3%) 2281/8641 (26.4%) 1/3163 (0.03%) 2015 106/8696 (1.2%) 2519/8667 (29.0%) 3/1516 (0.19%) 2016 76/8716 (0.87%) 2633/8716 (30.2%) 1/1618 (0.06%) Total 425/35.295 (1.2%) 9583/34.489 (27.7%) 6/9709 (0.06%) Year Anti-HIV n (%) 2013 0/1389 (0) 2014 0/2802 (0) 2015 0/1401 (0) 2016 0/1521 (0) Total 0/7113 (0)
|Printer friendly Cite/link Email Feedback|
|Title Annotation:||ORIGINAL ARTICLE|
|Author:||Tanriverdi, Esra Cinar; Ozkurt, Zulal; Kadioglu, Berrin Goktug; Alay, Handan; Calikoglu, Oksan; Koca|
|Publication:||The Turkish Journal of Gastroenterology|
|Date:||Mar 1, 2019|
|Previous Article:||Adverse factors responsible for below-normal platelet count after laparoscopic splenectomy and azygoportal disconnection.|
|Next Article:||Screening for hepatic fibrosis and steatosis in Turkish patients with type 2 diabetes mellitus: A transient elastography study.|