As the distance between clinic and household increased by 1 km, the odds for combination antiretroviral regimen uptake decreased in bivariable (OR: 0.89, 95% CI: 0.82 to 0.97) and multivariable (adjusted OR: 0.88, 95% CI: 0.80 to 0.97) models. Each 1-km increase in distance was associated with a 12% decreased odds for combination antiretroviral regimen uptake. Findings were consistent in sensitivity analyses limited to communities with high ascertainment of GPS information (adjusted OR: 0.87, 95% CI: 0.78 to 0.96). Our model suggested that older women were more likely to uptake a combination antiretroviral regimen, while those who initiated antenatal care later in pregnancy were less likely (Table 2). The probability of initiating a combination antiretroviral regimen declined gradually as distance increased. The probability of initiating a combination antiretroviral regimen was the highest among participants living within 1.9 km of the facility and steadily declined with increased distance (Fig. 2B). Overall, 65 of 145 (45%) who lived within 1.9 km of the facility initiated PMTCT compared with 37 of 109 (34%) who lived farther away.
We observed reduced uptake of PMTCT services, including maternal combination antiretroviral regimens, as the distance between home and clinic increased. Uptake of PMTCT was the highest within 1.9 km of a clinic and steadily declined as distance increased. This finding is consistent with previous work in the field of HIV treatment, where long distance and travel costs are recognized barriers to care and treatment in resource-constrained settings.10,12,1510,12,1510,12,15 However, it contrasts past studies of antenatal care in which distance did not appear to influence the timing or frequency of antenatal visits.19,2019,20 We expected this contrast due to potential fear of stigma associated with PMTCT uptake.14 Because PMTCT bridges these two health services, dedicated studies such as this, focused on PMTCT utilization at the population level, provide important supporting evidence for the design of future programs.
We used precise GPS household location information, which allowed us to calculate distance from home to clinic and examine geospatial patterns of uptake. However, we were unable to measure path distance, or to estimate travel time, to clinic because of limited data on the rural road network in our study area. Instead, we used Euclidean distance, which has been found to be highly correlated with path distance in other rural settings.18,2718,27 In addition, we did not have the necessary data to weight distance measures by costs associated with travel (e.g., car, bus, bicycle, foot). This analysis thus assumes that potential modes of transportation have no influence on PMTCT uptake, which may not be realistic because cost would likely increase with distance.28
More than one-third of the GPS coordinates were missing from participating households. This is a potential limitation of this analysis; if these missing data were not at random, it could unduly bias the study results. To address this issue, we compared individuals with and without recorded GPS coordinates and found that there were few differences between these populations, including by uptake of PMTCT services. Missing data appeared to be concentrated in the Kafue Estates community, due to technical difficulties with the instruments themselves that were discovered only after the survey had finished. When we excluded this single site in a sensitivity analysis, we were reassured to find that the results were consistent. Although not definitive, these supporting analyses do provide a degree of reassurance about our primary findings.
Negative perceptions about clinical care and fear of stigma could have adversely affected service uptake in the antenatal setting.14,2914,29 It is also possible that the use of self-reported PMTCT uptake measures influenced our primary outcome. These factors may explain the overall low uptake of services with fewer than 50% of participants receiving combination antiretroviral regimens, and more than 30% never initiating PMTCT at all. However, we were unable to examine potential cultural or social factors that may influence a mother's decision to start a PMTCT regimen. Mixed methods approaches may be of particular promise for future work, as program managers and researchers seek to identify and understand the host of potential obstacles for PMTCT service utilization. Such formative work is critical to the design of interventions and implementation strategies appropriate to the local context.
Long distance and travel costs have been linked to poor program outcomes among HIV-infected adults in several settings and are recognized barriers to HIV testing, timely antiretroviral therapy initiation, and consistent drug adherence.30–3330–3330–3330–33 The impact of distance in this PMTCT context is particularly important because PMTCT and general HIV treatment become increasingly aligned through innovative strategies such as Option B+. Interestingly, our distance threshold of 1.9 km, after which the uptake of PMTCT services steadily declined, is similar to those observed in other settings. In South Africa, for example, ART uptake was the highest among individuals living within 1 km of a health facility, after which a decline in uptake was observed.34 In Kenya, clients living within 1 km of the main road (correlated with hospital distance) were less likely to be lost to the follow-up after registering for HIV care compared with individuals living 1–5 km and >5 km from the main road.35 This distance threshold is important to consider in planning for health care availability as it appears to apply across diverse settings in sub-Saharan Africa.
Several aspects of our pilot program may have influenced PMTCT uptake. We incorporated CD4 screening and triage as mandated by the Zambian national guidelines.23 CD4 evaluation significantly delays antiretroviral therapy initiation during pregnancy in many settings.36 Guided by national guidelines23 to initiate ZDV at 28-week gestation, we waited until at least 28-week gestation to start combination antiretroviral regimens for those women who did not immediately qualify for antiretroviral therapy based on maternal health. Thus, those who presented early in pregnancy and learned their HIV status were required to return later in pregnancy to start combination prophylaxis. The need for a second visit may have negatively influenced uptake. Although newer PMTCT policies for Option B/B+ largely address these bottlenecks (e.g., antiretroviral therapy initiation from 14 weeks onward, elimination of CD4 triage), and thus should improve uptake of services, distances between home and clinic will continue to have an important and ongoing role in drug adherence and clinical care engagement.
Our pilot program integrated HIV treatment within the framework of maternal–child health services, a strategy that has been shown to increase the timely initiation of antiretroviral therapy among pregnant women.36,3736,37 However, decentralization to primary care settings alone may not be enough to maximize coverage of services. In rural settings, new models may be needed to extend the existing health system. Mobile clinics, for example, have been shown to be effective for ongoing monitoring and drug distribution.38 Community health workers and other outreach personnel can also reliably increase service uptake, enhance adherence (through counseling and drug delivery), and improve program retention over time.39,4039,40
In summary, we observed an important association between home-to-clinic distance and uptake of PMTCT services. These results are consistent with other studies in the HIV treatment literature and highlight the need for greater investments in health infrastructure beyond primary health care facilities and into communities. As national programs seek to further reduce the number of new pediatric HIV infections, the enhancement of existing PMTCT services must be accompanied by new strategies to decentralize care and maximize coverage across rural and remote settings.
2. Kesho Bora Study Group. Triple antiretroviral compared with zidovudine and single-dose nevirapine prophylaxis during pregnancy and breastfeeding for prevention of mother-to-child transmission of HIV
-1 (Kesho Bora study): a randomised controlled trial. Lancet Infect Dis. 2011;11:171–180.
3. Thomas TK, Masaba R, Borkowf CB, et al.. Triple-antiretroviral prophylaxis to prevent mother-to-child HIV transmission through breastfeeding—the Kisumu Breastfeeding Study, Kenya: a clinical trial. PLoS Med. 2011;8:e1001015.
4. Shapiro R, Hughes M, Ogwu A, et al.. Antiretroviral regimens in pregnancy and breast-feeding in Botswana. N Engl J Med. 2010;362:2282–2294.
5. Chasela CS, Hudgens MG, Jamieson DJ, et al.. Maternal or infant antiretroviral drugs to reduce HIV-1 transmission. N Engl J Med. 2010;362:2271–2281.
6. World Health Organization. Antiretroviral Therapy for Treating Pregnant Women and Preventing HIV Infection in Infants; Recommendations for a Public Health Approach—2010 Revision. Geneva, Switzerland: WHO Press; 2010.
7. World Health Organization. Consolidated Guidelines on the use of Antiretroviral Drugs for and Preventing HIV Infection: Recommendations for a Public Health Approach. Geneva, Switzerland: WHO Press; 2013.
8. Schouten EJ, Jahn A, Midiani D, et al.. Prevention of mother-to-child transmission of HIV
and the health-related millennium development goals: time for a public health approach. Lancet. 2011;378:282–284.
9. Gourlay A, Birdthistle I, Mburu G, et al.. Barriers and facilitating factors to the uptake of antiretroviral drugs for prevention of mother-to-child transmission of HIV
in sub-Saharan Africa: a systematic review. J Int AIDS Soc. 2013;16:18588.
10. Zachariah R, Harries AD, Manzi M, et al.. Acceptance of anti-retroviral therapy among patients infected with HIV and tuberculosis in rural Malawi is low and associated with cost of transport. PLoS One. 2006;1:e121.
11. Chinkonde JR, Sundby J, Martinson F. The prevention of mother-to-child HIV transmission programme in Lilongwe, Malawi: why do so many women drop out. Reprod Health Matters. 2009;17:143–151.
12. Tuller DM, Bangsberg DR, Senkungu J, et al.. Transportation costs impede sustained adherence and access to HAART in a clinic population in southwestern Uganda: a qualitative study. AIDS Behav. 2010;14:778–784.
13. O'Gorman DA, Nyirenda LJ, Theobald SJ. Prevention of mother-to-child transmission of HIV
infection: views and perceptions about swallowing nevirapine in rural Lilongwe, Malawi. BMC Public Health. 2010;10:354.
14. Duff P, Kipp W, Wild TC, et al.. Barriers to accessing highly active antiretroviral therapy by HIV-positive women attending an antenatal clinic in a regional hospital in western Uganda. J Int AIDS Soc. 2010;13:37.
15. Skinner D, Mfecane S, Gumede T, et al.. Barriers to accessing PMTCT services in a rural area of South Africa. Afr J AIDS Res. 2005;4:115–123.
16. Cook RE, Ciampa PJ, Sidat M, et al.. Predictors of successful early infant diagnosis of HIV in a rural district hospital in Zambezia, Mozambique. J Acquir Immune Defic Syndr. 2011;56:e104–e109.
17. Iroha E, Esezobor CI, Ezeaka C, et al.. Adherence to antiretroviral therapy among HIV-infected children attending a donor-funded clinic at a tertiary hospital in Nigeria. Afr J AIDS Res. 2010;9:25–30.
18. Siedner MJ, Lankowski A, Tsai AC, et al.. GPS-measured distance to clinic, but not self-reported transportation factors, are associated with missed HIV clinic visits in rural Uganda. AIDS. 2013;27:1503–1508.
19. Prudhomme O'Meara W, Platt A, Naanyu V, et al.. Spatial autocorrelation in uptake of antenatal care and relationship to individual, household and village-level factors: results from a community-based survey of pregnant women in six districts in western Kenya. Int J Health Geogr. 2013;12:55.
20. Kyei NN, Campbell OM, Gabrysch S. The influence of distance and level of service provision on antenatal care use in rural Zambia
. PLoS One. 2012;7:e46475.
21. Chi BH, Stringer JS, Moodley D. Antiretroviral drug regimens to prevent mother-to-child transmission of HIV: a review of scientific, program, and policy advances for sub-Saharan Africa. Curr HIV/AIDS
22. Gartland MG, Chintu NT, Li MS, et al.. Field effectiveness of combination antiretroviral prophylaxis for the prevention of mother-to-child HIV transmission in rural Zambia
. AIDS. 2013;27:1253–1262.
24. Chi BH, Musonda P, Lembalemba MK, et al.. Universal combination antiretroviral regimens to prevent mother-to-child transmission of HIV in rural Zambia
: a two-round cross-sectional study. Bull World Health Organ. 2014;92:582–592.
25. Silverman BW. Density Estimation for Statistics and Data Analysis. New York, NY: Chapman and Hall; 1986.
26. Filmer D, Pritchett LH. Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography. 2001;38:115–132.
27. Perez-Heydrich C, Furgurson JM, Giebultowicz S, et al.. Social and spatial processes associated with childhood diarrheal disease in Matlab, Bangladesh. Health Place. 2013;19:45–52.
28. Stout BD, Leon MP, Niccolai LM. Nonadherence to antiretroviral therapy in HIV-positive patients in Costa Rica. AIDS Patient Care STDS. 2004;18:297–304.
29. Van Eijk AM, Bles HM, Odhiambo F, et al.. Use of antenatal services and delivery care among women in rural western Kenya: a community based survey. Reprod Health. 2006;3:2.
30. Ramadhani HO, Thielman NM, Landman KZ, et al.. Predictors of incomplete adherence, virologic failure, and antiviral drug resistance among HIV-infected adults receiving antiretroviral therapy in Tanzania. Clin Infect Dis. 2007;45:1492–1498.
31. Sowah L, Turrene F, Delva G, et al.. B112 an evaluation of distance and its impact on long-term follow up outcomes in a rural HIV clinic in Northern Haiti. J Acquir Immune Defic Syndr. 2013;62:40.
32. Lankowski A, Siedner M, Bangsberg D, et al.. Impact of Geographic and transportation-related barriers on HIV outcomes in sub-Saharan Africa: a systematic review. AIDS Behav. 2014;18:1199–1223.
33. Govindasamy D, Ford N, Kranzer K. Risk factors, barriers and facilitators for linkage to antiretroviral therapy care: a systematic review. AIDS. 2012;26:2059–2067.
34. Cooke GS, Tanser FC, Barnighausen TW, et al.. Population uptake of antiretroviral treatment through primary care in rural South Africa. BMC Public Health. 2010;10:585.
35. Hassan AS, Fielding KL, Thuo NM, et al.. Early loss to follow‐up of recently diagnosed HIV‐infected adults from routine pre‐ART care in a rural district hospital in Kenya: a cohort study. Trop Med Int Health. 2012;17:82–93.
36. Killam WP, FAU TB, Chintu NF, et al.. Antiretroviral therapy in antenatal care to increase treatment initiation in HIV-infected pregnant women: a stepped-wedge evaluation. AIDS. 2010;24:85–91.
37. Chi BH, Bolton-Moore C, Holmes CB. Prevention of mother-to-child HIV transmission within the continuum of maternal, newborn, and child health services. Curr Opin HIV AIDS. 2013;8:498–503.
38. Moon TD, Jequicene T, Blevins M, José E, Lankford JR, Wester CW, Fuchs MC, Vermund SH. Mobile clinics for antiretroviral therapy in rural Mozambique. Bull World Health Organ. 2014;92(9):680–684.
39. Chang LW, Alamo S, Guma S, et al.. Two-year virologic outcomes of an alternative AIDS care model: evaluation of a peer health worker and nurse-staffed community-based program in Uganda. J Acquir Immune Defic Syndr. 2009;50:276–282.
40. Jaffar S, Amuron B, Foster S, et al.. Rates of virological failure in patients treated in a home-based versus a facility-based HIV-care model in Jinja, southeast Uganda: a cluster-randomised equivalence trial. Lancet. 2010;374:2080–2089.