Reconsidering the impact of conflict on HIV infection among women in the era of antiretroviral treatment scale-up in sub-Saharan Africa: a gender lens

As increasing international and local efforts focus on scaling up access to antiretroviral treatment (ART) in sub-Saharan Africa [1], the United Nations High Commissioner for Refugees (UNHCR), Médecins Sans Frontières (MSF), and the Joint United Nations Program on HIV/AIDS (UNAIDS) have increasingly advocated that the lack of essential medicines in conflict settings, including ART, is a violation of human rights [2–5]. HIV infection and armed conflict are disproportionately represented in sub-Saharan Africa, with women and children experiencing the largest burden of harms and adverse health outcomes due to both HIV infection risk and impact of conflict [5,6]. Given emerging disparities in access to ART among HIV-positive women in conflict zones, there is an urgent need to reconsider the impact of conflict on HIV infection. Importantly, recent evidence suggests that there may be a protective effect of armed conflict on HIV prevalence as a result of reduced mobility and urbanization, disruption of sexual networks, and decreased casual consensual sex [6–9]. At the same time, substantial evidence suggests an increased vulnerability to HIV in conflict settings among women and children due to widespread human rights violations, rape as a weapon of war, forced occupational exposure, the need for women to turn to sex work to support themselves and their families (i.e., survival sex), and reduced access to HIV prevention and reproductive health services [7,10–12]. Regardless, inequitable access to ART scale up in conflict zones suggests a need to re-examine the complex relationship between conflict and HIV infection. The current scale-up of ART in Uganda illustrates the importance of reconsidering the impact of armed conflict on HIV transmission. During the past two decades over 1.5 million have been displaced due to warfare and insurgency by the Lord's Resistance Army (LRA) in Northern Uganda [13]. Although initial evidence suggested an increase in HIV transmission risk due to conflict and warfare, subsequent evidence revealed a lower HIV prevalence among pregnant women inside internally displaced persons' (IDP) camps in Northern Uganda [6.3% in camps vs. 11.6% outside IDP camps, adjusted odds ratio = 1.55, 95% confidence interval (CI): 1.15–2.08] [14]. Although HIV prevalence peaked in Uganda in the 1990s, the large majority of HIV-positive individuals did not have access to ART until the late 1990s/early 2000s [5,13]. This time period coincided with the mass influx of IDPs into camps in the Acholi region of northern Uganda, with the largest influxes seen in 1996–1997 and 2002–2004 due to increased rebel activities [15]. As of February 2005, it was estimated that there were 1 million IDPs living across 96 protected camps in the Acholi region. A survey conducted in the same year by the World Health Organization (WHO) and the Ugandan Ministry of Health showed that crude all-cause mortality rates in the IDP camps of Kitgum and Pader Districts were three to four times higher than outside the camps, with AIDS as the second most common cause of death (after malaria), particularly affecting women and children [15]. Further recent Service Availability Mapping (SAM) by WHO and the Ugandan Ministry of Health in Gulu, Kitgum, and Pader Districts showed most ART, voluntary counseling and testing (VCT) and prevention of mother-to-child transmission (PMTCT) services clustered in urban centers outside the camps, leaving limited access inside camps and in rural areas [16]. Accordingly, the reported lower HIV prevalence among IDPs from antenatal care (ANC) surveillance data in 2005 in the Gulu, Kitgum, and Pader Districts of the Acholi region [14] may actually be due to higher rates of AIDS-related deaths in the absence of access to effective ART in the IDP camps, compared with outside the camps. This is of particular concern given reports of high levels of gender-based violence, survival and transactional sex, maternal malnutrition, over-crowding, and a lack of preventive health services (including HIV testing) available within the IDP camps in Northern Uganda [8,15]; all factors shown to drive HIV transmission risk in conflict settings [7,10]. Importantly, though relatively understated to date, the vast majority of epidemiological data on HIV prevalence in conflict settings relies on ANC sentinel surveillance data [7]. Surprisingly, little attention has been paid to how the relationship between conflict and HIV prevalence may be impacted by inequitable access to reproductive health and ART services among HIV-positive women. Relying exclusively on ANC surveillance data assumes similar access and utilization of reproductive health and ART services among sexually active women of reproductive age inside and outside IDP camps, including ART postexposure prophylaxis and PMTCT, and similar incidence and distributions of pregnancy between HIV positive and negative women inside and outside IDP camps [17,18]. If disparities exist in access to reproductive health and ART between conflict and nonconflict zones, the interpretation of a protective effect of conflict on HIV transmission risk may be masking larger reproductive health disparities and AIDS-related mortality among HIV-positive women. There are several pathways through which differential access to HIV treatment could impact HIV-positive women's utilization of ANC services. First, poorer access to ART within conflict zones would lead to higher mortality and morbidity rates among HIV-positive women within the camps, resulting in reduced numbers of HIV-positive women accessing ANC services. Secondly, poorer access to HIV care and treatment in IDP camps [15] may lead to fewer HIV-positive women who require ANC services due to morbidity-related reductions in fecundity and incidence of pregnancy. For instance, at the population level, substantial evidence indicates that, in the absence of treatment, HIV-infected women have between 25 and 40% lower fertility rates than noninfected women [17,18], whereas HIV-positive women accessing ART may not see the same reduction in fertility rates [19]. Although the mechanism for this relationship is uncertain, differential access to ART inside and outside camps could lead to differences in both reproductive biology and behaviors, which may impact the incidence of pregnancy among HIV-positive women in the camps. In addition to poorer access to ART, existing evidence indicates that access to PMTCT and VCT services is also lower in conflict settings, which may lead to an increase in adverse pregnancy outcomes (including increased rates of spontaneous abortion [20]) among HIV-infected women not accessing ART [21], thereby further reducing the numbers of HIV-positive women accessing ANC services in IDP camps. In early 2007, the UNHCR called on governments and nongovernment organizations (NGOs) in sub-Saharan Africa to ensure that national strategies to roll-out ART supported similar access to essential medicines in conflict and refugee settings, highlighting the public health imperative of equitable access to ART in conflict zones [3]. Although challenges in infrastructure, human capacity, and clinical and laboratory monitoring due to instability have generally been cited as major obstacles to ART roll-out in conflict settings, the relative stability of mid/long-term refugee and IDP camps may in fact offer more support for ART provision than some postconflict settings outside the camps [3,4]. Of note, given lower stability of conflict areas outside the camps, recently published evaluation data of the first comprehensive HIV treatment program in a chronic conflict-affected area demonstrates the feasibility and effectiveness of the provision of ART in conflict zones, with similar health outcomes as in nonconflict settings [22]. The findings, conducted as part of MSF's 3-year roll-out of HIV treatment and care in Bukavu, Democratic Republic of the Congo (DRC), suggest that a managed treatment interruption contingency plan can minimize the risk of destabilizing ART programs, including treatment interruption and development of drug resistance, due to conflict and insecurity. With over 14 million HIV-positive women in sub-Saharan Africa alone and at least 24 African states affected by conflict, the disparities in access in ART among HIV- positive women in conflict settings is an urgent public health concern. Furthermore, the current reliance on generalizing estimates of HIV prevalence among sexually active women of reproductive age in conflict settings to the larger population of men, children, and nonpregnant women needs to be re-considered within the emerging disparities in access to reproductive health and ART among HIV-positive women. The launch of NGO and United Nations-led maternal health initiatives under the Global Campaign for the Health Millennium Development Goals appears to have opened a crucial policy window challenging reproductive health inequities [23]. However, by failing to consider the impact of conflict on HIV transmission through a gender lens, we risk minimizing its catastrophic effect on rights violations, including lack of access to essential medicines, among some of the world's most vulnerable women. Acknowledgement The authors have no conflicts of interest. The authors have no funding sources to declare. K.S., A.K., B.R. and E.L.S. conceptualized the paper. K.S. drafted the initial version and G.G. and S.A.S. provided critical feedback on revised versions. All authors read and approved the final version for submission.

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