Between 1986 and 2006, Northern Uganda suffered from civil conflict between the Lord's Resistance Army and the Government of Uganda. The conflict displaced an estimated 2 million people who were forced to live in internally displaced people (IDP) camps.1 Although there has been no official end to the conflict, the Juba peace talks created relative peace2 and allowed people to move back to their villages starting in 2006.
HIV and AIDS in Uganda
Although the Uganda 2011 AIDS Indicator Survey showed a national HIV prevalence rate of 7.3% in the general population and 6.5% among pregnant women attending antenatal care (ANC) clinics, the prevalence in northern Uganda was 8.3%.3 In the same year, the national fertility rate was 6.2 children per woman and 6.3 per woman in the Acholi subregion while Uganda's general fertility rate was 212/1000 and the crude birth rate 42.1/1000, among the highest in the world.4
Prevention of Mother-to-child HIV Transmission in Uganda
Based on the results of the PETRA study,5 the Uganda Ministry of Health (MoH) started in 2000 a pilot prevention of mother-to-child HIV transmission (PMTCT) program in 5 referral hospitals in 3 Ugandan districts. Since then, the number of PMTCT service delivery sites was expanded nationally. Currently, all hospitals (131), all health centers (HC) IV (178), 90% of HC III (1000/1114) and 11% (339/3018) of HC II provide PMTCT services.6 The increase in the number of health facilities providing routine HIV testing and counseling (HTC) for pregnant women and antiretroviral (ARV) prophylaxis for those infected with HIV has resulted in an 82% uptake of HTC among women attending ANC clinics nationally in 2011. The proportion of HIV-positive pregnant women receiving ARV for PMTCT increased from 12% in 2005 to 53% in 2009. MoH data show that vertical transmission rates in children whose mothers received PMTCT prophylaxis reduced from 19% in 2007 to 10% in 2009.4,6
The MoH recommendations for PMTCT ARV prophylaxis have continuously evolved over the years, closely reflecting guidance from the World Health Organization (WHO) based on results of international trials on PMTCT prophylaxis efficacy7−14 subsequent to the PETRA study. The MoH 2010–2015 Scale Up Plan for PMTCT15 aims to achieve an HIV-free generation of Ugandans by 2015 through the virtual elimination of MTCT of HIV.
AVSI Foundation is an international not-for-profit nongovernmental organization active in Uganda since 1984, supporting private not-for-profit (PNFP) and public health facilities. AVSI has supported Uganda MoH's HIV/AIDS care programs since 1984 and the provision of PMTCT services since 2002 in 4 remote rural districts of the Acholi subregion in Northern Uganda: Kitgum (estimated population 222,737), Lamwo (164,754), Pader (237,100), and Agago (285,300) districts (Fig. 1). This article presents data covering 10 years of MoH/AVSI PMTCT program activities in these districts.
From January 2002 till December 2011, 24 MoH health facilities providing PMTCT services were supported by AVSI in Kitgum, Lamwo, Pader, and Agago districts. In 2011, the facilities included 21 health centers II, III, and IV (1 PNFP and 20 public), and 3 hospitals (2 PNFP and 1 public) (see Figure S1, Supplemental Digital Content,http://links.lww.com/QAI/A385).
AVSI support has consisted of community sensitization, distribution of information and education materials, radio programs, provision of drugs and medical supplies, technical, logistic, administrative, and financial support to health facility and district health and social staff, home-based care and follow-up of PMTCT mothers and babies, nutrition education and promotion of locally available foods, economic empowerment, and male involvement strategies. In the MoH/AVSI PMTCT sites, counselors follow the national counseling guidelines for HIV/AIDS, which provide information on MTCT of HIV, interventions to reduce the risk of HIV transmission, and the importance of delivery and receiving postnatal care in health facilities. Men have been involved through peer counseling (men experienced in the PMTCT program counseling other men), as well as couple HIV counseling and testing, and participation in Family Support Groups (FSG), a structure promoted by the MoH in which HIV serodiscordant and concordant couples and their infants are supported at community level. FSG discuss and implement health education, social support, and income-generating activities in collaboration with health facility, district, and AVSI staff. Health system strengthening such as technical capacity building for timely reporting and supply chain management has also been provided. All AVSI's support activities have been implemented through MoH and PNFP health facilities in collaboration with the district government and local nongovernmental and community-based organizations.
The Ugandan MoH recommendations for ARV prophylaxis for PMTCT have closely followed WHO guidelines. For pregnant women with a CD4 count >200 cells/mm3, prophylaxis from 2002 to 2006 consisted of single-dose Nevirapine (sd-NVP) tablet for the mother and 7-day NVP syrup for the baby while breastfeeding was recommended for 3–6 months.16,17 Between 2006 and 2009, prophylaxis included azidothymidine (AZT) from 28 weeks of gestation complemented by an sd-NVP tablet during labor, or AZT/3 TC as of 32 weeks of gestation plus sd-NVP at labor, followed by AZT/3 TC for 7 days in either case.18 As of 2010, after the 2010 WHO-updated PMTCT guidelines,19 2 options were recommended: option A including AZT prophylaxis for the mother from 14 weeks of gestation complemented by an sd-NVP tablet in labor and a 7-day course of AZT/3 TC postpartum to minimize the occurrence of resistance to NVP, plus daily NVP for the baby until the end of breastfeeding, or option B consisting of triple ARV therapy (ART) for the mother as of 14 weeks of gestation until the end of breastfeeding and daily NVP for the baby for 6 weeks. The MoH/AVSI sites implemented option A and started implementing option B when supplies became available in June 2010. From 2006 to 2009, HIV-infected pregnant women with a CD4 count ≤200 cells/mm3 were eligible to receive triple ART for their own health. First-line ART consisted of AZT; lamivudine (3 TC) and efavirenz (EFV) or NVP; or stavudine (d4T), 3 TC, and NVP. In 2008, new guidelines were released recommending only AZT, 3 TC, and NVP or EFV, but no longer d4T/3 TC/NVP as the preferred first-line ART. Since 2010, TDF, 3 TC, and EFV are the preferred first-line ART for infected women with CD4 cell counts ≤350 cells/mm3.
Infant HIV Testing
In the MoH/AVSI sites, from 2004 to 2006, children born to HIV-infected women were tested at 18 months using rapid HIV antibody tests. From 2007 to 2009, HIV-exposed children were to be tested at 3, 6, and 12 months by HIV DNA polymerase chain reaction (PCR) assay followed by an 18-month rapid HIV antibody test as per national protocol. PCR samples were sent to the Joint Clinical Research Center laboratory in Gulu. Dry blood spots were used for PCR sample collection as of 2009. Since June 2010, early infant HIV diagnosis (EID) at 6 weeks of age and repeat testing at 12 months have been implemented, with dry blood spots samples sent to the Uganda Virus Research Institute, followed by an 18-month rapid HIV antibody confirmation test on site. Only children who presented at health facilities at the specified age were tested.
Throughout the 10-year period, program data were collected by AVSI staff in collaboration with MoH staff on a monthly basis using the MoH PMTCT registers. The registers included figures for new ANC attendance, HIV test acceptance (until 2009 when opt-out provider-initiated HTC was established), partner HIV testing, mothers accessing ARV prophylaxis or ART, and babies accessing ARV prophylaxis and HIV PCR testing. Data checks were carried out by program staff through spot checks at health center level and by crosschecking hand-filled data forms against existing databases.
Data from registers were entered into a computer database by the AVSI program data clerk and supervised by the AVSI PMTCT program manager. In case of errors, data were verified at the health facility level. In case obvious entry errors were made on the original data forms, the data in question were removed from analysis. Annual totals were compiled, and trends were analyzed using Predictive Analytics SoftWare (PASW) Statistics 18. Trends were analyzed by testing for significant different slopes using linear regression of the indicators against the reference years. T-statistics and P values were calculated for the coefficients for the “year” variable.
In total,140,658 women newly attended ANC services from 2002 to 2011 in the 24 MoH/AVSI health facilities (Table 1). Of these, 94.4% (132,783/140,658) were tested for HIV (range, 86.8%–99%). Attendance of the male partners of pregnant women increased significantly from 5.9% (296/5186) in 2002 to 75.8% (14,564/20,032) in 2011 (t = 4.892, P = 0.001); partner acceptance for testing was 99.5% (44,783/45,028) over the 10-year period, with 100% of acceptance in 2010 and 2011 (Table 1 and Fig. 2).
The 10-year HIV prevalence rate in the AVSI-supported sites was 6.2% (8283/132,783) for women and 6.8% (3045/44,783) for partners, and did not vary significantly over the period (Table 1). Of the 8283 women who tested HIV-positive over the 10-year period, 69.4% (5749/8283) were started on ARV prophylaxis for PTMCT, whereas 9.6% (792/8283) were started on triple ART. These percentages increased significantly over the years; although 47.2% (126/267) of all HIV-infected women were started on ARV prophylaxis and none of them were on triple ART in 2002, these proportions increased to 67.1% (707/1053) and 0.2% (2/1053), respectively, by 2006, and to 78.5% (919/1171) and 32.0% (375/1171), respectively, by 2011 (t = 3.693, P = 0.006 for prophylaxis and t = 4.232, P = 0.003 for ART) (Fig. 3 and Table 1—see explanation for overlapping data in 2010 and 2011 in legend of Table 1).
During the 10-year period, 49% (68,928/140,658) of ANC women delivered in a health facility (Table 1). Of these, 6.9% (4783/68,928) were HIV-positive. This proportion remained stable throughout the period. Although the rate of health facility delivery increased for both HIV-negative women (51%–57%) and HIV-positive women (56%–81%) between 2004 and 2011, only the increase among HIV-positive women reached statistical significance (t = 2.823, P = 0.033 for HIV-positive women versus t = 0.057, P = 0.956 for HIV-negative women) (see Table S1 and Figure S2, Supplemental Digital Content,http://links.lww.com/QAI/A385). In comparison, the national proportion of women who delivered in health facilities was 49.4% in 2006 but data were not available for other years or for HIV-positive women.4
By 2011, a total of 4436 children born to HIV-infected mothers had been tested between the ages of 6 weeks and 18 months; 6.1% (269) of them tested were HIV-positive (Table 1). Figure 4 shows the trend in the number and proportion of HIV-exposed children tested between the ages of 6 weeks and 18 months by HIV DNA PCR and the HIV prevalence in these children between 2004 and 2011. In this period, the prevalence declined significantly from 10.3% to 5.0% (t = −3.669, P = 0.01). Data on infant test results at specific ages were not available.
Our data show that the MoH/AVSI PMTCT program in Northern Uganda achieved increasingly improving results from January 2002 through December 2011, despite the conflict-related insecurity and the precarious work conditions that prevailed in the area until 2006. In short, in the 10-year period, nearly 95% of the women who attended ANC services in the 24 program sites were tested for HIV while testing of their male partners increased significantly from 5.9% in 2002 to 75.8% in 2011. The overall HIV prevalence in the sites was 6.2% for women and 6.8% for partners. Over the 10-year period, 69.4% of the women who tested HIV-positive were started on ARV prophylaxis for PMTCT, whereas 9.6% started on ART; by 2011, these figures had risen to 78.5% and 32%, respectively. Although nearly half of all women (49%) delivered in health facilities over the period, more than 80% of HIV-infected women did so as of 2010. Lastly, the number of infants tested between 6 weeks and 18 months of age steadily increased since the EID program was initiated in 2004, whereas the proportion of HIV-infected infants decreased to 4.7% and 5% in the last 2 years of the program.
The increase in ANC attendance in the early years of the program paralleled increased access to, and sustained, sensitization about the availability of PMTCT services. The decline in attendance after 2006 coincided with the return of the displaced population to their villages of origin, often far from existing health facilities.
The uptake of HIV testing nationally in women attending antenatal clinics in Uganda was 60% in 2006/7, 82% in 2007/8, 82% in 2008/9, 91.8% in 2009/10, and 94% in 2011.6 According to the Uganda DHS 2011, only 76.1% of the women in the northern region were counseled and tested for HIV, and received their results.4 The MoH/AVSI PTMCT sites in northern Uganda thus consistently achieved higher HTC rates among pregnant women attending ANC, exceeding 90% in all but 2 years (2005 and 2006) of the 10-year period.
The National PMTCT Plan and the 2010–2015 National HIV Strategic Plan aimed at increasing the proportion of male partners of pregnant and lactating women undergoing HTC and receiving results to 25% by 2010 and to 50% by 2015. In the MoH/AVSI PMTCT sites, this proportion increased dramatically and continuously as of 2007, reaching nearly 76% in 2011. National male testing in PMTCT settings had reached only 12.3% by 2009/10.6 The multisectorial collaboration of AVSI with the district health office and health facilities strived to make the interventions tailored, culturally appropriate and timely for the Acholi population in the areas of implementation. Thus, we believe targeted interventions such as FSG, sensitization of men by peers, creation of male-friendly spaces in ANC clinics, and offering couple HTC as part of the standard of care largely contributed to this outcome. We also believe staff mentoring at health facility level and peer education and FSG support greatly facilitated the involvement of men.
The observed HIV prevalence in pregnant women remained stable over the years, confirming earlier published data showing that albeit conflict is often believed to accelerate the spread of HIV locally, prevalence in conflict-affected regions is similar to other unaffected regions and PMTCT performance indicators can be comparable or even better than those in non–conflict-affected areas in the western and central parts of the country.20,21 In 2004, HIV prevalence was 6.9% in the North-Central and North-Eastern regions compared with 6.7% in Western and Central Uganda.20 Our previously presented data covering the 2002–2004 period also showed that, compared with non-IDP centers, IDP camps had higher rates of pretest counseling, 89% versus 81%; HIV testing, 91% versus 85%; and posttest counseling, 99% versus 93% in the period.20,21
The number of women started on ARV prophylaxis and ART increased significantly over the years and exceeded the 2011 national proportions of women started on ARV prophylaxis (67.1% versus 34% nationally) and ART (78.5% versus 60.9% nationally).6 Although ART became freely available in Uganda in 2004, drug supply in remote conflict areas such as Northern Uganda was not reliable until 2006. From then on, ART uptake by eligible pregnant women in the MoH/AVSI sites increased continuously, averaging nearly 27% for 2010 and 2011. This result exceeded the national proportion of 19% of HIV-positive pregnant women receiving ART in the same period.6
The overall rate of health facility deliveries remained well above the national average of 58% in 20114 and the MoH 2010 target of 60% throughout the period of AVSI support. The decrease observed in 2006–2007 coincided and may be attributed to the return of IDP to their villages of origin often at greater distance from health facilities following improved levels of security. This trend reversed as AVSI and the MoH supported the expansion of PMTCT services to lower level health units as of 2008. The proportion of HIV-positive women delivering in health facilities increased significantly over the years and parallels the sustained counseling and activities by the FSG through which PMTCT mothers are empowered to make informed decisions about the importance and need for safe delivery at health facilities.
The number of HIV-exposed children tested for HIV between 6 weeks and 18 months of age in the MoH/AVSI-supported facilities has increased continuously since the start of the EID program in 2005 and equaled or exceeded the number of HIV-infected women since 2009. Although these 2 numbers are not directly comparable due to the time lag between the testing of the women and the testing of their babies, they can, when aggregated over a long period of time, give a reasonable estimate of coverage. Paralleling this increase, HIV prevalence among the infants tested steadily decreased over the years to 4.7% in 2010 and 5% in 2011. This outcome sets a promising mark for reaching by the government's target to achieve virtual elimination of MTCT by 2015.
Our findings of high coverage of PMTCT services are in line with findings from Kenya where 92% of the women attending ANC tested and 90% received prophylaxis.22 High acceptance for testing among both women and men has also been found earlier in Kenya,23 Zambia,24 Eastern Uganda,25 and more recently in Tanzania.26 Increased PMTCT coverage in the region has been attributed to policy changes in integrating HIV testing in ANC and shifting from opt-in to opt-out testing. For example, in Malawi, HIV testing integrated with ANC and free maternity services led to a greater number of HIV-positive women delivering in hospitals and higher usage of PMTCT prophylaxis.27 In Ethiopia, HIV counseling and testing uptake increased after shifting to opt-out testing and reached 84.5% of testing in 2009.28
The results presented in this article are aggregated health facility program data, collected as part of the MoH Health Management Information Systems. They do not include individual or longitudinal information on women, couples, or mother–baby pairs through the cascade of PMTCT events. For this reason, proportions of women and babies retained in care could not be assessed and the rates of facility delivery and infant testing could only be approximated using the concurrent number of women tested HIV-positive in ANC as the denominator. Moreover, the infant data did not include deaths and losses to follow-up and could not be linked to their mothers' data in the analyses. Also data on provision of infant cotrimoxazole and NVP were unavailable, as well as overall and HIV-free infant survival data, and maternal mortality. Although we believe male partner attendance and couple HTC increased through active involvement of men in FSG and through peer sensitization and role models, there is no direct evidence to invoke a causal association between these events. Further research is needed to enable documentation of best practices for male involvement in mother, newborn, and child health and PMTCT and effectively assess their effect in diverse settings. Qualitative studies are also needed to establish if the unique social situation of IDP contributed to the higher than usual male partner attendance and if male gender norms in northern Uganda communities had a bearing on the relative success of this PMTCT program. Lastly, while the MoH/AVSI PMTCT program registered a systematic decrease in HIV prevalence in infants tested between 6 weeks and 18 months of age through EID, further follow-up is needed to understand the program's long-term PMTCT impact and to document the HIV prevalence in infants no longer breastfeeding.
Notwithstanding these limitations, our data show that PMTCT programs can be implemented successfully in a remote conflict-affected setting and underline how much overall health system challenges affect the implementation and ultimate success of the programs. Lack of human resources, limited knowledge, ineffective referral and follow-up systems, shortages of medical supplies, and inadequate infrastructure all hamper implementation of quality mother, newborn, and child health services including PMTCT, both in Uganda29–31 and other settings in sub-Saharan Africa. In Kenya, Kinuthia et al22 reported that “health systems factors rather than stigma were barriers to utilization of PMTCT services.” Similarly in Botswana, fear or stigma were not reasons to refuse an HIV test, yet knowledge of a partner being tested, knowledge of PMTCT, and living in urban dwellings were factors associated with acceptance of HIV testing and uptake of PMTCT services.32
AVSI has played and continues to play a key role in filling gaps in staff recruitment, training, and retention. Currently in the northern region, only 53% staff positions are filled in health centers, 79.3% in hospitals, and absenteeism is high at more than 25%.33 Coupled with the frequently changing PMTCT guidelines, this high turnover makes investing in continuous staff education and training a priority. Training on supply chain management is equally required to avoid delays in distribution, delivery, and stock out of PMTCT drugs. Community, health, and interdepartmental linkages from ANC/PMTCT and EID to ART clinics can improve and enhance health service seeking–behaviors and follow-up. To achieve all this, continuous collaboration and lobbying with government and other stakeholders is required. For these reasons, AVSI has combined its PMTCT activities with health system strengthening activities. Technical advisors with knowledge about health systems and service delivery, together with PMTCT and nutrition specialists, are placed at district health offices to build capacity in human resource and supply chain management, community linkages, and on job mentoring at health facilities.
This article shows how a comprehensive PMTCT program emphasizing social and community engagement alongside provision of and access to essential medical care and support services can be successful in a conflict and post-conflict setting such as Northern Uganda. Together with primary HIV prevention for women of reproductive age, and treatment of persons living with HIV/AIDS, PMTCT is a proven prevention strategy to stop the spread of HIV and reach UNAIDS and Uganda MoH goal of achieving an HIV-free generation.
The authors are indebted to the numerous patients who have put their trust in the services offered by our program. The authors thank all hospital, health center and AVSI staff, and Ministry of Health and District Health Officers, District HIV & AIDS Focal Persons, District PMTCT Focal Persons, and other NGOs and community-based organizations who have over the years contributed to the MoH/AVSI's PMTCT program. The authors also wish to acknowledge the generosity of the donors who have funded the AVSI Uganda PMTCT program over the years, including the European Union, USAID/PEPFAR, UNICEF, the Dutch Government, the Elizabeth Glaser Pediatric AIDS Foundation, and other private foundations.
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