Seroprevalence and correlates of HIV, syphilis, and hepatitis B and C virus among intrapartum patients in Kabul, Afghanistan

Testing for human immunodeficiency virus (HIV), syphilis, and hepatitis B surface antigen (HBsAg) in pregnancy and labor is medically indicated to prevent vertical transmission. Prevalence of these infections among the antenatal population may be a reliable indicator of general population prevalence and determinant of vaccination policy [1–3]. The intrapartum period may be the only clinical access point for the antenatal population in limited resource settings. Successful interventions to prevent vertical transmission linked to intrapartum rapid testing have been demonstrated in a variety of limited resource settings [4, 5]. One such intervention is birth dose hepatitis B vaccine. Recommendations for birth dose vaccination are determined by antenatal prevalence of hepatitis B e antigen (HBeAg) and to some degree by HBsAg in settings where HBeAg prevalence is unknown [6]. Risk of vertical transmission should not be underestimated in settings where HBeAg is relatively low or assumed to be low; Chauvin et al. indicate that even in settings where HBeAg prevalence among mothers is relatively low (< 20%), the number of chronic carriers resulting from lack of birth dose vaccination exceeds 500/100,000, the threshold for instituting other neonatal immunization programs, such as poliomyelitis [7]. In many settings, resources do not exist to assess HBeAg prevalence so vaccination policy may be made on HBsAg prevalence alone.

Afghanistan has an evolving health infrastructure and many barriers remain to accessible care, including ongoing conflict and a shortage of trained providers. Blood donor data is the sole published source of population-based prevalence data. From March through December 2006, the Central Blood Banks in Afghanistan reported prevalence of transfusion-associated infections based on single screening test protocol [8]. For Kabul province, low prevalence of HIV antibody (0.0006%), syphilis-suggestive reaction (VDRL 1.1%), HBsAg (3.9%), and hepatitis C antibody (anti-HCV) (1.9%) was reported, with HBsAg prevalence suggesting intermediate prevalence [[8]; see additional file 1]. For the last three years in Afghanistan, monovalent hepatitis B vaccine has been administered simultaneously with diphtheria-pertussis-tetanus (DPT) vaccine at two, four, and six months of life. In 2005, the DPT completion rate for the Kabul urban area was estimated to be 28.6% [9].

Hepatitis B virus (HBV) prevalence has also been reported among Afghan refugee populations outside of Afghanistan, with higher prevalence noted than that reported among Afghan blood donors [10, 11]. Since 2002, the return of 4.8 million refugees, largely from neighboring countries with higher prevalence of HBV and hepatitis C virus (HCV) (e.g. Iran, Pakistan), raises concern that prevalence of hepatitis and other blood-borne infections within the country may increase [11]. Reliable general population prevalence is also needed to inform evolving vaccination and sexually transmitted infection (STI) prevention programs. The purposes of this study were to determine the prevalence and correlates of HIV, syphilis, and hepatitis B and C infection and to model the impact of various vaccination strategies at measured HBsAg prevalence among intrapartum patients in Kabul, Afghanistan.

Enrollment comprised 4,452 participants, with 1,179 women ineligible and 153 declining participation. Reasons for ineligibility included imminent delivery (62.9%), emergent operative intervention (22.5%), hemorrhage (7.2%), non-reassuring fetal status (6.7%), or other reasons (e.g. eclampsia, 0.7%). Participants were younger (mean 25.74 vs. 27.70, p < 0.001) and had lower parity (mean 2.09 vs. 3.41, p < 0.001) than those ineligible. Women declining enrollment were of greater parity (mean = 3.06, p < 0.001), but did not differ significantly by age.

No participants tested positive for either syphilis or HIV. Prevalence of HBsAg was 1.53% (95% CI: 1.18 – 1.94) and anti-HCV was 0.31% (95% CI: 0.17 – 0.53). There were two false positive HBsAg Determine^® rapid tests; the second serum-based rapid test was negative (PPV = 97.1%). There were no participants testing positive for both HBsAg and anti-HCV. The absence or low prevalence of HIV, syphilis, and anti-HCV precluded subsequent analysis of correlates.

This study is among the first to assess prevalence of HIV, syphilis, HBV, and HCV in an obstetric population in modern Afghanistan. HIV was not detected, corroborating low prevalence noted in other Afghan populations [[8] – see additional file 1;[23]]. Prevalence of both HBsAg and HCV were lower than those detected through the Central Blood Bank for Kabul province or among Afghan populations in refugee camps in Balochistan (i.e., the Northwest Frontier province of Pakistan) or in southwest Iran [[8] – see additional file 1; [10, 11]]. The associations between HBsAg and therapeutic injections or markers of low socioeconomic status noted in among Afghan refugees and in other settings were not detected in the study population, perhaps because reported therapeutic injections in the last year were fairly uncommon or because low prevalence may have diminished the power to detect some associations [10, 24, 25]. Given the large number of Afghans repatriating from areas of higher hepatitis prevalence in the last five years, similar assessments should be considered in border areas where former refugee camp denizens often initially reside upon repatriation.

It is unclear why the highest spousal educational level was associated with hepatitis B. This relationship may reflect husbands educated in countries with greater hepatitis B prevalence who, following cessation of civil conflict, returned to Afghanistan, married, and transmitted the infection to their spouse. This relationship is similar to that between HIV and higher educational level in rural populations in Africa, where migration for education and possibly infection occurred [26]. In the Afghan context, adult hepatitis B transmission is likely to be iatrogenic or sexual and may predominantly affect the male population. A study assessing HBsAg seroprevalence among blood donors in Pakistan noted males were more likely to be infected than females; both this study and a study exclusively looking at first-time male blood donors noted that hepatitis B transmission likely occurred through unclean medical or shaving supplies [27, 28]. We did not interview or test the spouses, but such an assessment may be indicated.

Screening for HIV and syphilis has been posited as optional in some low prevalence settings as resources expended on screening are not justified by the low number of infections detected [29]. However, analyses indicate that screening for HIV and syphilis is cost effective even in very low prevalence settings [30, 31]. We did not detect any cases of HIV or syphilis among participants delivering in government hospitals, suggesting that scarce resources should not be diverted to screening at this time. However, generalization of our findings is limited as only women accessing care in government hospitals were assessed.

In the case of hepatitis B, it is reasonable to consider peripartum testing with birth dose vaccine and parental counseling to ensure completion of the vaccine series, as reported rates of likely vaccination series completion are sub-optimal [9]. Based on international recommendations on birth dose hepatitis B vaccination, modeling did not suggest a significant advantage in changing the current strategy [5, 6, 32]. However, due to the shifting population dynamics in Afghanistan, routine surveillance should be conducted as birth dose vaccination will be recommended if antenatal prevalence of HBsAg reaches 2% [5, 33].

This study has a number of important limitations. First, the population consists only of those women able to access care, likely those of higher socioeconomic status. Because hepatitis has been associated with lower socioeconomic status, the prevalence reported here may underestimate the true prevalence among reproductive-aged women in Kabul. Second, there may have been under-reporting of risky behaviors or other socially-desirable responses in this interviewer-administered survey. Further, as the questionnaire was administered during labor, there may have been response truncation due to discomfort. We attempted to minimize this by conducting all interviews in a private setting with a female interviewer. However, interviewer administration was the only feasible means of data collection, due to low literacy and the prohibitive cost of audio computer-assisted self-interview (ACASI) in this setting. Questionnaires were administered only with the participant's assent; if discomfort was preventing response, the participant was offered the option of resuming the questionnaire following delivery.

The findings of this study indicate that HIV and syphilis were not present among intrapartum patients tested and that HBsAg prevalence was lower than for other general population groups assessed. A general screening program for HIV and syphilis does not appear cost-effective when the limited available resources are considered. However, HBsAg prevalence indicates hepatitis B is a pertinent public health issue and that routine surveillance among antepartum populations should be considered, particularly should HBeAg prevalence be assessed and found to be high. Future programming should include viral hepatitis in public health service announcements and awareness raising activities, potentially improving vaccination series completion. Intrapartum screening with rapid testing is feasible, acceptable, and suited for periodic surveillance activities as population shifts may introduce measurable changes in viral hepatitis prevalence, resulting in potential change in vaccination policy and practice. However, other models to disseminate testing, vaccine, and health information should also be developed to reach populations that do not access care centers and may be at greater risk for these infections.