*Corresponding Author:

Dr. LC Ikeako
Department of Obstetrics and Gynecology, Anambra State University Teaching Hospital, Amaku, Awka, Nigeria.
E-mail: ikeakolawrence@yahoo.com

Abstract

Background: Sexually transmitted infections and human immunodeficiency virus (HIV)/AIDS are a major public health concern owing to both their prevalence and propensity to affect offspring through vertical transmission. Aim: The aim was to determine the seroprevalence of HIV, hepatitis B virus (HBV), hepatitis C virus (HCV), syphilis, and co‑infections among antenatal women in Enugu, South‑East Nigeria. Materials and Methods: A retrospective study of antenatal women at the University of Nigeria Teaching Hospital, Enugu, South‑East Nigeria from May 1, 2006 to April 30, 2008. A pretested data extraction form was used to obtain data on sociodemographic variables and screening test results from the antenatal records. The analysis was carried out with SPSS version 17 (Chicago, IL, USA). Results: A total of 1239 antenatal records was used for the study. The seroprevalence of HIV, HBV, HCV, and syphilis among the antenatal women were 12.4%(154/1239(, 3.4%(42/1239), 2.6%(32/1239), and 0.08%(1/1239), respectively. The HIV/HBV and HIV/HCV co‑infection prevalence rates were 0.24%(3/1239) and 0.14%(2/1239), respectively. There was no HBC and HCV co‑infection among both HIV positive and negative antenatal women. There was no statistically significant difference in HBV and HCV infection between the HIV positive and negative antenatal women. The only woman that was seropositive for syphilis was also positive to HIV. Conclusion: The seroprevalence of HIV, HBV, HCV, and syphilis is still a challenge in Enugu. Community health education is necessary to reduce the prevalence of this infection among the most productive and economically viable age bracket.

Keywords

Antenatal women, Coinfection, Human immunodeficiency virus, Hepatitis C virus, Hepatitis B virus, Seroprevalence, Syphilis

Introduction

The largest epidemic facing mankind today is human immunodeficiency virus (HIV) infection.[1] Sub-Saharan Africa, the hardest hit region, is home to more than two-thirds (69%) of people living with HIV, but only about 12% of the world’s population.[2] Nigeria still has the largest HIV prevalence among pregnant women, ranging from as low as 1.6% in the west, to 8% in the South-South, 6.5% in the South-East, and 10% in the North-Central.[3]

Nigeria is also endemic for hepatitis B virus (HBV) infection, a virus that shares similar transmission routes with HIV.[4] Over 2 billion of the world’s population have been exposed to HBV and an estimated 387 million of these are now chronically infected with a rate of 10 million new carriers each year.[5] Approximately, 13% of the carriers will die from the consequences of the HBV infection with an overall annual mortality of about 1 million.[6] HBV is believed to be the main etiological factor in over 75% of chronic liver disease.[6]

Hepatitis C virus (HCV) is a single stranded ribonucleic acid virus in the Flaviviridae family and also a major cause of liver disease in the world.[7] The overall prevalence of HCV in sub-Saharan Africa is 3%.[7] There are several routes of transmission of HCV but direct percutaneous inoculation is the most efficient.[8] In South-Western Nigeria, a higher percentage of those with HCV infection had additional risk factors, especially scarification marks.[9]

Syphilis is also a systemic disease caused by Treponema pallidium, which can be spread by sexual contact, blood transfusion, and through vertical transmission.[10] Syphilis can seriously complicate pregnancy and result in spontaneous abortion, prematurity, low birth weight, still birth as well serious sequelae in live born infected children.[11]

Due to the similarity in the routes of transmission, many individuals have been exposed to HIV, HBV, HCV, and syphilis infection in various combinations. A study on blood donors showed that seroprevalence of HIV, HBV, HCV, and syphilis was 3.8%, 4.7%, 0.7%, and 1.3%, respectively.[12] Among those with co-infections, the most common combinations were HIV-syphilis 38% and HIV-HBV 34%.[12] These co-infections have been associated with reduced survival, drug related hepatotoxicity, drug resistance, cross-resistance, and sub-optimal response.[13,14]

There are worldwide variations in seroprevalence of these infections depending on geographic area, risk groups, and the type of exposure involved.[4]

This study aimed at estimating the seroprevalence of HIV, HBV, HCV, syphilis, and co-infections among antenatal women in Enugu, South-East Nigeria. The outcome will help in formulating intervention policies aimed at curtailing the spread of these infections.

Materials and Methods

Study design

This was a retrospective study, which covered the antenatal cases in the hospital between May 1, 2006 and April 30, 2008. A total of 2500 pregnant women attended the antenatal clinic within the study period. All the antenatal records with complete sociodemographic variables, HIV, HBV, HCV, and syphilis screening results were used for the study. All antenatal women whose mothers were HBV or HIV carriers were excluded. This study was approved by the Ethics Committee of the University of Nigeria Teaching Hospital (UNTH), Enugu. All the antenatal records were thoroughly reviewed and 1239 of them met the inclusion criteria while 1261 of them did not. A pretested data extraction form was used to obtain information on the sociodemographic status, parity, screening for HIV, hepatitis B surface antigen (HBsAg), syphilis and HCV from the antenatal records. The data were extracted by two trained assistants.

Hepatitis B surface antigen and antibodies to HCV were determined using Clinotech diagnostic enzyme linked immunosorbent assay (ELISA) test kits (Clinotech Laboratories, USA; batch/lot no. for HBsAg screening kit is F0416J2 and F0106J2 for HCV). The test sensitivity is 100% and specificity 99.7% for both HbsAg and HCV test kits. Syphilis was screened with Veneral Disease Research Laboratory (Clinotech Biotech Inc., California; batch/lot no. F0731J4, sensitivity 100% and specificity 99.7%). Antibodies to T. pallidium were confirmed with T. pallidium hemagglutination test. Antibodies to HIV 1 and 2 were screened with Abott Determine and Immunocomb (Alere Medical Company, Limited, Japan; batch/ lot no. 54921U100, sensitivity 100% and specificity 99.5%). All reactive samples were confirmed using ELISA.

Statistical analysis was achieved using SPSS version 17 (Chicago, IL, USA). Chi-square analysis was used for discrete variables and P < 0.05 were considered as statistically significant. The results were presented in tables and simple percentages.

Results

Of 1239 antenatal women, 154 were HIV positive giving a seroprevalence rate of 12.4%(154/1239), 42 were HBV positive resulting in an HBV seroprevalence of 3.4%(42/1239), and 32 of them were positive to HCV antibodies with a seroprevalent rate of 2.6%(32/1239) [Table 1]. One of the pregnant women was treponema palladium hemoagglutination assay positive with seroprevalence rate of 0.08%(1/1239).

Table 1: Screening pattern of the antenatal women

Three out of 1239 women were both HIV and HBV positive with co-prevalent rate of 0.24% [Table 2]. As was shown by the Chi-square values in Table 2, there was no statistically significant difference in HBV infection between the HIV positive and negative antenatal women. Two women were both HIV and HCV positive with a seroprevalent rate of 0.16%(2/1239). Similarly in Table 2, there was no statistically significant difference in HCV infection between the HIV positive and negative women (he only patient that was T. pallidium hemoagglutination test positive was also HIV positive. There was no HBV, HCV, and syphilis co-infection in both HIV positive and negative antenatal women in Enugu.

Table 2: HIV, HBV and HCV co-infection

The most predominant age group of the women was 21-30 years 53.9% (669/1239). The mean (SD) for age was 30.1 (2.1) years [Table 3]. Four hundred and ninety-three 39.8%(493/1239) of the women were public/civil servants followed by the unemployed group 28.7% (356/1239). Table 3 also shows that most of the antenatal women 38.7% (479/1239) were multiparous.

Table 3: Sociodemographic variables among the antenatal women

Table 4 revealed that the unemployed group of the antenatal women and the Artisans constitute the bulk of the women that were seropositive to HIV, HBV, and HCV anti-bodies.

Table 4: Occupational distribution of the women HIV, HBsAg and HCV infection

Discussion

The overall seroprevalence of HIV, 12.4% among antenatal women in Enugu recorded in this study is higher than the national HIV prevalence of 4.6% among pregnant women.[15] It is also higher when compared with the 7.8% reported in Minna and 8.6% in Anambra state, Nigeria.[16,17]

In North-West Ethiopia, a seroprevalence of 9.6% for HIV-1 was observed among pregnant women receiving antenatal services at the University of Gondar Teaching Hospital.[14] The seroprevalence in this study is lower than the 26% seroprevalence reported in Swaziland.[18] The seroprevalence of HIV, 12.4% in this study could be due to increased level of awareness among antenatal women in Enugu and environs on the Prevention of Mother to Child Transmission (PMTCT) of HIV/AIDS as well as the functional PMTCT program in UNTH, Enugu thereby attracting more HIV-positive pregnant women to book at UNTH.

The seroprevalence of HBV 3.4%, among the women is lower than previous reports from Nigeria; 8.2% in Yola,[19] and 5% in Niger Delta.[20] It is similar to 3.7% reported in Jimma, Ethiopia.[21] Higher prevalence was recorded among pregnant Sudanese 5%,[22] and India women 3.07%.[23]

However, cross-study comparisons may be misleading because of the kits used for the assay of HBsAg. In our study, HBsAg was assayed by ELISA technique. The use of polymerase chain reaction (PCR) and antibodies sensitive to the hepatitis B core antigen have been shown to be more sensitive than the serological methods used in our study and PCR could detect about 10% of occult HBV infection.[24] In addition, the differences in the sociodemographic characteristics of the women should be taken into consideration in such comparisons.

The HCV antibody prevalence among the women in the study was 2.6%. This is in agreement with the overall seroprevalence of HCV in sub-Saharan Africa 3%.[7] It is however, higher than the result from Niger Delta, Nigeria 0.5%,[20] Iran 0.98%,[25] and Sudan <1%.[22] These variations may be related to the differences in the modes of transmission, which is influenced by socio-cultural practices and environmental factors.[20] In a tertiary medical center in South-West Nigeria where over 90.8% of the women had scarification marks, a seroprevalence of 9.2% was reported.[9] The differences have also been attributed to the choice of serological tests to determine HCV prevalence especially in developing countries where intercurrent infections contribute to false-positive enzyme immunoassay results.[26]

From this study, the seroprevalence of syphilis among antenatal attendees in Enugu is 0.08%. The seroprevalence is lower than 0.13% recorded by Ozumba et al.[27] in the same hospital two decades ago. It is lower than the national average for syphilis in pregnant Nigeria women, 0.3%.[28] However, a higher prevalence of 10% was reported among pregnant women in Osogbo, south western Nigeria.[29] Among antenatal women in Gondar, Ethiopia, the seroprevalence was 1%.[10] The variation is seroprevalence could be attributed to the differences in sexual practices and behavior. The seroprevalence of syphilis in Enugu is low and has declined over the past two decades. Similar observation was made in Ethiopia.[10] Early seeking of effective medical treatment for sexually transmitted infections among the largely literate urban antenatal women may explain the decline. The low prevalence has also been attributed to over-the-counter use of antibiotics for minor complaints and easy access to the drugs.[10]

The HIV and HBV co-infection prevalent rate was 0.24%. This is <0.7% reported in Anambra state.[17] In this study, 0.14% of the antenatal women were positive for HIV and HCV. The only woman that was positive for syphilis was also HIV positive and whether syphilis predisposed her to HIV and vice versa could not be ascertained. There was no HBV and HCV co-infection in both HIV positive and negative women and this supported the study in Rwanda and Uganda,[30] but varied with the results from Malekan City, Iran.[25] The difference in HBV and HCV infection in both HIV-positive and negative antenatal women in Enugu was not statistically significant. On the contrary a study conducted in Addis Ababa, Ethiopia showed that higher prevalence of HCV antibodies was seen among HIV positive compared to HIV negative antenatal attendees (2.9% vs. 0.87%, respectively).[31] The absence of HCV and HBV infections in both HIV negative and positive women may be due to the absence of such risk factors as injection drug use commonly seen in the West and scarification marks that are not common in our area of study.

The age group of 21-40 years had the predominant HIV, HBV, and HCV prevalence and this supported the studies in North-West Ethiopia.[10] This calls for concerted efforts aimed at preventive measures to reduce risky lifestyle practices among the most productive and economically viable age bracket.[13]

The unemployed group and artisans similarly had the highest seroprevalence of HIV, HBV and HCV. A similar observation in Anambra State, Nigeria[17] showed that the occupation of the antenatal women influenced the infection of the women. Low socioeconomic factor initiates multiple sexual partnership, unprotected sex, and predisposes to sexually transmitted infections.[32]

This study has a number of limitations. This is an institutional study conducted in an urban area and consisted of only pregnant women who were able to access hospital; for this reason, the seroprevalence reported here maybe a lower estimate of the true prevalence among pregnant women in Enugu. The rate might be higher in individuals who had a lower socioeconomic status such that they could not even reach a hospital from the rural area. No data is available for such risk factors as residence and place of birth. The size of the population is small, and it will not be possible to generalize the outcome of the study.

Conclusion

Human immunodeficiency virus, HBV, and HCV infection is a major global health problem necessitating a high priority in their prevention and control. There is a need for effective health education on behavioral change as well as the inclusion of HBV immunization for women of reproductive age to reduce the risk of spread to neonates through mother to child transmission. The low seroprevalence of syphilis observed in this study should not engender complacency in view of the deleterious effect of untreated maternal infection on pregnancy outcome and spread of HIV.

References

1. UNAIDS. Core Slides; Global Summary of the AIDS Epidemics; 2012. Available from: http://www.slideshare. net/UNAIDS/unaids-global-report-2012-epidemiology-slides-15262667. [Last assessed on 2013 Oct 01].
2. Population Reference Bureau. World Population Data Sheet, 2011. Available from: http://www.prb.org//publications/ datasheets/2011/world-population-data-Sheet.aspx. [Last assessed on 2013 Sep 02].
3. Osotimehin B. Director General, National Action Committee for the Control of AIDS (NACA), Federal Ministry of Health, Nigeria. NACA Bulletin; July 2008.
4. Puoti M, Manno D, Nasta P, Carosi G. Hepatitis B virus and HIV coinfection in low-income countries: Unmet needs. Clin Infect Dis 2008;46:367-9.
5. Drosten C, Nippraschk T, Manegold C, Meisel H, Brixner V, Roth WK, et al. Prevalence of hepatitis B virus DNA in anti-HBc-positive/HBsAg-negative sera correlates with HCV but not HIV serostatus. J Clin Virol 2004;29:59-68.
6. Awang EW, Cheung R. Global epidemiology of hepatitis B virus (HBV) infection. N Am J Med Sci 2011;4:7-13.
7. Madhava V, Burgess C, Drucker E. Epidemiology of chronic hepatitis C virus infection in sub-Saharan Africa. Lancet Infect Dis 2002;2:293-302.
8. Hou J, Liu Z, Gu F. Epidemiology and prevention of hepatitis B virus infection. Int J Med Sci 2005;2:50-7.
9. Ogunro PS, Adekanle DA, Fadero FF, Ogungbamigbe TO, Oninla SO. Prevalence of anti-hepatitis C virus antibodies in pregnant women and their offspring in a tertiary hospital in Southwestern Nigeria. J Infect Dev Ctries 2007 1;1:333-6.
10. Mulu A, Kassu A, Tessema B, Yismaw G, Tiruneh M, Moges F, et al. Seroprevalence of syphilis and HIV-1 during pregnancyin a teaching hospital in northwest Ethiopia. Jpn J Infect Dis 2007;60:193-5.
11. Chakraborty R, Luck S. Syphilis is on the increase: The implications for child health. Arch Dis Child 2008;93:105-9.
12. Tessema B, Yismaw G, Kassu A, Amsalu A, Mulu A, Emmrich F, et al. Seroprevalence of HIV, HBV, HCV and syphilis infections among blood donors at Gondar University Teaching Hospital, Northwest Ethiopia: Declining trends over a period of five years. BMC Infect Dis 2010;10:111.
13. Otegbayo JA, Taiwo BO, Akingbola TS, Odaibo GN, Adedapo KS, Penugonda S, et al. Prevalence of hepatitis B and C seropositivity in a Nigerian cohort of HIV-infected patients. Ann Hepatol 2008;7:152-6.
14. PinedaJA, Romero-Gómez M, Díaz-García F, Girón-González JA, Montero JL, Torre-Cisneros J, et al. HIV coinfection shortens the survival of patients with hepatitis C virus-related decompensated cirrhosis. Hepatology 2005;41:779-89.
15. United Nations Children’s Fund State of the World’s Children. New York; 2009.
16. Ndams IS, Joshua IA, Luka SA, Sadiq HO, Ayodele SB. Human immunodeficiency virus seroprevalence among pregnant women in Minna, Nigeria. Ann Niger Med 2010;4:14-7.
17. Ezegbudo CN, Agbonlahor DE, Nwobu GO, Igwe CU, Agba MI, Okpala HO, et al. The seroprevalence of hepatitis B surface antigen and human immunodeficiency virus among pregnant women in Anambra state, Nigeria. Shiraz E-Med J 2004;5:1-9.
18. UNAIDS. 2008 Report on Global AIDS Epidemic. Geneva, Switzerland: UNAIDS; 2008.
19. Olokoba AB, Salawu FK, Danburam A, Olokoba LB, Midala JK, Badung LH, et al. Hepatitis B virus infection amongst pregnant women in North-eastern Nigeria-A call for action. Niger J Clin Pract 2011;14:10-3.
20. Buseri F, Seiyaboh E, Jeremiah Z. Surveying infections among pregnant women in the Niger Delta, Nigeria. J Glob Infect Dis 2010;2:203-11.
21. Awole M, Gebre-Selassie S. Sero prevalence of HBsAg and its risk factors among pregnant women in Jimma, South west Ethiopia. Ethiop J Health Dev 2005;19:45-50.
22. Elsheikh RM, Daak AA, Elsheikh MA, Karsany MS, Adam I. Hepatitis B virus and hepatitis C virus in pregnant Sudanese women. Virol J 2007;4:104.
23. Khakhkhar VM, Bhura PJ, Bhuva SP, Patel CP,Cholera MS. Sero prevalence of hepatitis B amongst pregnant women attending the antenatal clinic of a tertiary care hospital, Jamnagar (Gujarat). Natl J Med Res 2012;2:362-5.
24. Gonçales FL Jr, Pereira JS, Da Silva C, Thomaz GR, Pavan MH, Fais VC, et al. Hepatitis B virus DNA in sera of blood donors and of patients infected with hepatitis C virus and human immunodeficiency virus. Clin Diagn Lab Immunol 2003;10:718-20.
25. Bahaf F, Tanom A, Montazam H, Sany AA. Seroprevalence of hepatitis C, hepatitis B and HIV and co-infections among pregnant women: A retrospective study in 2006 Malekan City, Iran. Res J Med Sci 2007;1:138-41.
26. Raghuraman S, Subramaniam T, Daniel D, Sridharan G, Abraham P. Occurrence of false positives during testing for antibodies to hepatitis C virus among volunteer blood donors in India. J Clin Microbiol 2003;41:1788-90.
27. Ozumba UC, Oshi DC, Nwokeji CM, Anya SE. Trends in seroreactivity for syphilis among pregnant Nigerian women. Sex Transm Infect 1999;75:120.
28. Federal Ministry of Health, Nigeria (FMOH). Technical Report on 2003 National HIV/Syphilis Sentinel Survey among Women Attending Antenatal Clinics in Nigeria. Abuja: Nigeria Federal Ministry of Health; 2004.
29. Ojo DA, Oyetunji IA. Sero prevalence of syphilis among pregnant women in Osogbo in Southwestern Nigeria. Asset Ser B 2007;6:61-5.
30. Pirillo MF, Bassani L, Germinario EA, Mancini MG, Vyankandondera J, Okong P, et al. Seroprevalence of hepatitis B and C viruses among HIV-infected pregnant women in Uganda and Rwanda. J Med Virol 2007;79:1797-801.
31. Ayele W, Nokes DJ, Abebe A, Messele T, Dejene A, Enquselassie F, et al. Higher prevalence of anti-HCV antibodies among HIV-positive compared to HIV-negative inhabitants of Addis Ababa, Ethiopia. J Med Virol 2002;68:12-7.
32. Kebede E, Chamiso B. Prevalence of syphilis in pregnancy in Addis Ababa. East Afr Med J 2000;77:212-6.