Longitudinal assessment of associations between food insecurity, antiretroviral adherence and HIV treatment outcomes in rural Uganda

Sheri D Weiser, Kartika Palar, Edward A Frongillo, Alexander C Tsai, Elias Kumbakumba, Saskia Depee, Peter W Hunt, Kathleen Ragland, Jeffrey Martin, David R Bangsberg, Sheri D Weiser, Kartika Palar, Edward A Frongillo, Alexander C Tsai, Elias Kumbakumba, Saskia Depee, Peter W Hunt, Kathleen Ragland, Jeffrey Martin, David R Bangsberg

Abstract

Introduction: Food insecurity is a potentially important barrier to the success of antiretroviral therapy (ART) programs in resource-limited settings. We undertook a longitudinal study in rural Uganda to estimate the associations between food insecurity and HIV treatment outcomes.

Design: Longitudinal cohort study.

Methods: Participants were from the Uganda AIDS Rural Treatment Outcomes study and were followed quarterly for blood draws and structured interviews. We measured food insecurity with the validated Household Food Insecurity Access Scale. Our primary outcomes were: ART nonadherence (adherence <90%) measured by visual analog scale; incomplete viral load suppression (>400 copies/ml); and low CD4 T-cell count (<350 cells/μl). We used generalized estimating equations to estimate the associations, adjusting for socio-demographic and clinical variables.

Results: We followed 438 participants for a median of 33 months; 78.5% were food insecure at baseline. In adjusted analyses, food insecurity was associated with higher odds of ART nonadherence [adjusted odds ratio (AOR) 1.56, 95% confidence interval (CI) 1.10-2.20, P < 0.05], incomplete viral suppression (AOR 1.52, 95% CI 1.18-1.96, P < 0.01), and CD4 T-cell count less than 350 (AOR 1.47, 95% CI 1.24-1.74, P < 0.01). Adding adherence as a covariate to the latter two models removed the association between food insecurity and viral suppression, but not between food insecurity and CD4 T-cell count.

Conclusions: Food insecurity is longitudinally associated with poor HIV outcomes in rural Uganda. Intervention research is needed to determine the extent to which improved food security is causally related to improved HIV outcomes and to identify the most effective policies and programs to improve food security and health.

References

    1. Radimer KL, Olson CM, Greene JC, Campbell CC, Habicht JP. Understanding hunger and developing indicators to assess it in women and children. Journal of Nutrition Education. 1992;24:36S–44S.
    1. Bukusuba J, Kikafunda J, Whitehead R. Food security status in households of people living with HIV/AIDS (PLWHA) in a Ugandan urban setting. British Journal of Nutrition. 2007;98:211–217.
    1. Tsai AC, Bangsberg DR, Emenyonu N, Senkungu JK, Martin JN, Weiser SD. The social context of food insecurity among persons living with HIV/AIDS in rural Uganda. Social Science & Medicine. 2011;73:1717–1724.
    1. Weiser S, Tsai AC, Gupta R, Frongillo EA, Kawuma A, Senkugu J, et al. Food insecurity is associated with morbidity and patterns of healthcare utilization among HIV-infected individuals in rural Uganda. AIDS. 2012;26:67–75.
    1. Tsai AC, Bangsberg DR, Frongillo EA, Hunt PW, Muzoora C, Martin JN, et al. Food insecurity, depression and the modifying role of social support among people living with HIV/AIDS in rural Uganda. Social Science & Medicine. 2012;74:2012–2019.
    1. Vogenthaler NS, Hadley C, Rodriguez AE, Valverde EE, del Rio C, Metsch LR. Depressive symptoms and food insufficiency among HIV-infected crack users in Atlanta and Miami. AIDS and Behavior. 2011;15:1520–1526.
    1. Weiser SD, Hatcher A, Frongillo EA, Guzman D, Riley ED, Bangsberg DR, et al. Food Insecurity Is Associated with Greater Acute Care Utilization among HIV-Infected Homeless and Marginally Housed Individuals in San Francisco. Journal of General Internal Medicine. 2012;28:67–75.
    1. Weiser SD, Frongillo EA, Ragland K, Hogg RS, Riley ED, Bangsberg DR. Food insecurity is associated with incomplete HIV RNA suppression among homeless and marginally housed HIV-infected individuals in San Francisco. J Gen Intern Med. 2009;24:14–20.
    1. Weiser SD, Tuller DM, Frongillo EA, Senkungu J, Mukiibi N, Bangsberg DR. Food insecurity as a barrier to sustained antiretroviral therapy adherence in Uganda. PLoS One. 2010;5:e10340.
    1. Thompson MA, Mugavero MJ, Amico KR, Cargill VA, Chang LW, Gross R, et al. Guidelines for Improving Entry Into and Retention in Care and Antiretroviral Adherence for Persons With HIV: Evidence-Based Recommendations From an International Association of Physicians in AIDS Care Panel. Annals of Internal Medicine. 2012;156:817–833.
    1. Bärnighausen T, Chaiyachati K, Chimbindi N, Peoples A, Haberer J, Newell ML. Interventions to increase antiretroviral adherence in sub-Saharan Africa: a systematic review of evaluation studies. The Lancet Infectious Diseases. 2011;11:942–951.
    1. ACC/SCN. Nutrition and HIV/AIDS. Statement by the Administrative Committee on Coordination, Sub-Committee on Nutrition at its 28th Session. Nairobe, Kenya: United Nations Administrative Committee on Coordination, Sub-Committee on Nutrition (ACC/SCN); 2001. [Accessed 16 June 2013]. Available from: .
    1. PEPFAR. Report on Food and Nutrition for People Living with HIV/AIDS (Report to Congress mandated by House Report 109–265, accompanying H.R. 3057) Washington DC: Department of State. Office of the United States Global AIDS Coordinator; 2006. [Accessed 16 June 2013]. Available from: .
    1. UNAIDS. Political Declaration on HIV/AIDS. [Accessed 16 June 2013];Joint United Nations Programme on HIV/AIDSs. 2006 Available from .
    1. World Food Programme. HIV, AIDS, TB and Nutrition. [Accessed 13 June 2013];World Food Programme. 2012 Available from: .
    1. Weiser SD, Young SL, Cohen CR, Kushel MB, Tsai AC, Tien PC, et al. Conceptual framework for understanding the bidirectional links between food insecurity and HIV/AIDS. The American journal of clinical nutrition. 2011;94:1729S–1739S.
    1. Coates J, Swindale A, Bilinsky P. Household Food Insecurity Access Scale (HFIAS) for measurement of food access: indicator guide. Washington, D.C: Food and Nutrition Technical Assistance Project, Academy for Educational Development; 2006.
    1. Frongillo EA, Nanama S. Development and Validation of an Experience-Based Measure of Household Food Insecurity within and across Seasons in Northern Burkina Faso. J Nutr. 2006;136:1409S–1419S.
    1. Swindale A, Bilinsky P. Development of a universally applicable household food insecurity measurement tool: process, current status, and outstanding issues. J Nutr. 2006;136:1449S–1452S.
    1. Giordano TP, Guzman D, Clark R, Charlebois ED, Bangsberg DR. Measuring adherence to antiretroviral therapy in a diverse population using a visual analogue scale. HIV Clin Trials. 2004;5:74–79.
    1. Oyugi JH, Byakika-Tusiime J, Charlebois ED, Kityo C, Mugerwa R, Mugyenyi P, et al. Multiple validated measures of adherence indicate high levels of adherence to generic HIV antiretroviral therapy in a resource-limited setting. J Acquir Immune Defic Syndr. 2004;36:1100–1102.
    1. Simoni JM, Kurth AE, Pearson CR, Pantalone DW, Merrill JO, Frick PA. Self-report measures of antiretroviral therapy adherence: A review with recommendations for HIV research and clinical management. AIDS and Behavior. 2006;10:227–245.
    1. Walsh JC, Mandalia S, Gazzard BG. Responses to a 1 month self-report on adherence to antiretroviral therapy are consistent with electronic data and virological treatment outcome. AIDS. 2002;16:269–277.
    1. Garcia de Olalla P, Knobel H, Carmona A, Guelar A, Lopez-Colomes JL, Cayla JA. Impact of adherence and highly active antiretroviral therapy on survival in HIV-infected patients. J Acquir Immune Defic Syndr. 2002;30:105–110.
    1. Bangsberg DR, Perry S, Charlebois ED, Clark RA, Roberston M, Zolopa AR, et al. Non-adherence to highly active antiretroviral therapy predicts progression to AIDS. AIDS. 2001;15:1181–1183.
    1. World Health Organization. Antiretroviral therapy for HIV infection in adults and adolescents: recommendations for a public health approach. 2010 revision. Geneva: World Health Organization; 2010. [Accessed 20 September 2012]. pp. 1–359. Available from . 2011.
    1. Kitahata MM, Gange SJ, Abraham AG, Merriman B, Saag MS, Justice AC, et al. Effect of early versus deferred antiretroviral therapy for HIV on survival. N Engl J Med. 2009;360:1815–1826.
    1. 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.
    1. Bush K, Kivlahan DR, McDonell MB, Fihn SD, Bradley KA. The AUDIT alcohol consumption questions (AUDIT-C): an effective brief screening test for problem drinking. Ambulatory Care Quality Improvement Project (ACQUIP). Alcohol Use Disorders Identification Test. Arch Intern Med. 1998;158:1789–1795.
    1. Au JT, Kayitenkore K, Shutes E, Karita E, Peters PJ, Tichacek A, et al. Access to adequate nutrition is a major potential obstacle to antiretroviral adherence among HIV-infected individuals in Rwanda. AIDS. 2006;20:2116–2118.
    1. Kalofonos IA. All I Eat Is ARVs. Medical Anthropology Quarterly. 2010;24:363–380.
    1. Nagata JM, Magerenge RO, Young SL, Oguta JO, Weiser SD, Cohen CR. Social determinants, lived experiences, and consequences of household food insecurity among persons living with HIV/AIDS on the shore of Lake Victoria, Kenya. AIDS Care. 2011;24:728–736.
    1. Hardon A, Akurut D, Comoro C, Ekezie C, Irunde H, Gerrits T, et al. Hunger, waiting time and transport costs: time to confront challenges to ART adherence in Africa. AIDS Care. 2007;19:658–665.
    1. Drain PK, Losina E, Parker G, Giddy J, Ross D, Katz JN, et al. Risk Factors for Late-Stage HIV Disease Presentation at Initial HIV Diagnosis in Durban, South Africa. PloS one. 2013;8:e55305.
    1. World Food Programme. Policy Issues. World Food Programme; 2010. WFP HIV AND AIDS POLICY. Executive Board Second Regular Session: Rome, 8–11 November 2010.
    1. Cantrell RA, Sinkala M, Megazinni K, Lawson-Marriott S, Washington S, Chi BH, et al. A pilot study of food supplementation to improve adherence to antiretroviral therapy among food-insecure adults in Lusaka, Zambia. J Acquir Immune Defic Syndr. 2008;49:190–195.
    1. Serrano C, Laporte R, Ide M, Nouhou Y, de Truchis P, Rouveix E, et al. Family nutritional support improves survival, immune restoration and adherence in HIV patients receiving ART in developing country. Asia Pacific Journal of Clinical Nutrition. 2010;19:68–75.
    1. Ivers LC, Chang Y, Gregory Jerome J, Freedberg KA. Food assistance is associated with improved body mass index, food security and attendance at clinic in an HIV program in central Haiti: a prospective observational cohort study. AIDS Res Ther. 2010;7:33.
    1. Koh HK, Oppenheimer SC, Massin-Short SB, Emmons KM, Geller AC, Viswanath K. Translating research evidence into practice to reduce health disparities: a social determinants approach. Am J Public Health. 2010;100(Suppl 1):S72–80.
    1. UNAIDS. UNAIDS Expanded Business Case: Enhancing Social Protection. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS); 2010.
    1. World Bank. HIV/AIDS, nutrition, and food security: what we can do: A Synthesis of international guidance. Washington, DC: World Bank; 2007.
    1. American Diatetic Association. Position of the American Diatetic Association: Food insecurity in the United States. Journal of the American Dietetic Association. 2010;110:1368–1376.
    1. IFAD. Rural Poverty Report 2011. Rome: International Fund for Agricultural Development (IFAD); 2010. [Accessed 19 June 2013]. Available from .
    1. Yager JE, Kadiyala S, Weiser SD. HIV/AIDS, food supplementation and livelihood programs in Uganda: a way forward? PloS One. 2011;6:e26117.
    1. Frega R, Duffy F, Rawat R, Grede N. Food insecurity in the context of HIV/AIDS: A framework for a new era of programming. Food & Nutrition Bulletin. 2010;31:292S–312S.
    1. Pandit J, Sirotin N, Tittle R, Onjolo E, Bukusi E, Cohen C. Shamba Maisha: A pilot study assessing impacts of a micro-irrigation intervention on the health and economic wellbeing of HIV patients. BMC Public Health. 2010;10:245.
    1. McMahon JH, Wanke CA, Elliott JH, Skinner S, Tang AM. Repeated assessments of food security predict CD4 change in the setting of antiretroviral therapy. Journal of Acquired Immune Deficiency Syndromes. 2011;58:60–63.

Source: PubMed

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