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PLOS ONE  2014 

Food Insecurity Is Associated with Increased Risk of Non-Adherence to Antiretroviral Therapy among HIV-Infected Adults in the Democratic Republic of Congo: A Cross-Sectional Study

DOI: 10.1371/journal.pone.0085327

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Background Food insecurity is increasingly reported as an important barrier of patient adherence to antiretroviral therapy (ART) in both resource-poor and rich settings. However, unlike in resource rich-settings, very few quantitative studies to date have investigated the association of food insecurity with patient adherence to ART in Sub-Saharan Africa. The current study examines the association between food insecurity and adherence to ART among HIV-infected adults in the Democratic Republic of Congo (DRC). Methods and Findings This is a cross-sectional quantitative study of patients receiving ART at three private and one public health facilities in Kinshasa, DRC. Participants were consecutively recruited into the study between April and November 2012. Adherence was measured using a combined method coupling pharmacy refill and self-reported adherence. Food insecurity was the primary predictor, and was assessed using the Household Food Insecurity Access Scale (HFIAS). Of the 898 participants recruited into the study, 512 (57%) were food insecure, and 188 (20.9%) were not adherent to ART. Food insecurity was significantly associated with non-adherence to ART (AOR, 2.06; CI, 1.38–3.09). We also found that perceived harmfulness of ART and psychological distress were associated respectively with increased (AOR, 1.95; CI, 1.15–3.32) and decreased (AOR, 0.31; CI, 0.11–0.83) odds of non-adherence to ART. Conclusion Food insecurity is prevalent and a significant risk factor for non-adherence to ART among HIV-infected individuals in the DRC. Our findings highlight the urgent need for strategies to improve food access among HIV-infected on ART in order to ensure patient adherence to ART and ultimately the long-term success of HIV treatment in Sub-Saharan Africa.


[1]  Joint United Nations Programme on HIV/AIDS (2012) Global Report: UNAIDS Report on the Global AIDS Epidemic 2012 Available: 2013 Apr 25.
[2]  Mills EJ, Bakanda C, Birungi J, Chan K, Ford N, et al. (2011) Life expectancy of persons receiving combination antiretroviral therapy in low-income countries: a cohort analysis from Uganda. Ann Intern Med. 155: 209–216.
[3]  Brinkhof MW, Boulle A, Weigel R, Messou E, Mathers C, et al. (2009) Mortality of HIV-infected patients starting antiretroviral therapy in sub-Saharan Africa: comparison with HIV-unrelated mortality. PLoS Med 6: e1000066 doi:10.1371/journal.pmed.1000066.
[4]  Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, et al. (2011) Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 365: 493–505.
[5]  Baeten JM, Donnell D, Ndase P, Mugo NR, Campbell JD, et al. (2012) Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Engl J Med 365: 399–410.
[6]  Tanser F, Barnighausen T, Grapsa E, Zaidi J, Newell ML (2013) High coverage of ART associated with decline in risk of HIV acquisition in rural KwaZulu-Natal, South Africa. Science 339: 966–971.
[7]  Sethi AK, Celentano DD, Gange SJ, Moore RD, Gallant JE (2003) Association between adherence to antiretroviral therapy and human immunodeficiency virus drug resistance. Clin Infect Dis. 37: 1112–1118.
[8]  Paterson DL, Swindells S, Mohr J, Brester M, Vergis EN, et al. (2000) Adherence to protease inhibitor therapy and outcomes in patients with HIV infection. Ann Intern Med 133: 21–30.
[9]  Lima VD, Harrigan R, Bangsberg DR, Hogg RS, Gross R, et al. (2009) The combined effect of modern highly active antiretroviral therapy regimens and adherence on mortality over time. J Acquir Immune Defic Syndr 50: 529–536.
[10]  Balcha TT, Jeppsson A, Bekele A (2011) Barriers to antiretroviral treatment in Ethiopia: a qualitative study. J Int Assoc Physicians AIDS Care 10: 119–125.
[11]  Curioso W, Kepka D, Cabello R, Segura P, Kurth A (2010) Understanding the facilitators and barriers of antiretroviral adherence in Peru: a qualitative study. BMC Public Health 10: 13.
[12]  Sanjobo N, Frich JC, Fretheim A (2008) Barriers and facilitators to patients’ adherence to antiretroviral treatment in Zambia: a qualitative study. SAHARA J 5: 136–143.
[13]  Tuller DM, Bangsberg DR, Senkungu J, Ware NC, Emenyonu N, et al. (2009) Transportation costs impede sustained adherence and access to HAART in a clinic population in southwestern Uganda: a qualitative study. AIDS Behav 14: 778–784.
[14]  Mills EJ, Nachega JB, Bangsberg DR, Singh S, Rachlis B, et al. (2006) Adherence to HAART: a systematic review of developed and developing nation patient-reported barriers and facilitators. PLoS Med 3(11): e438 doi:10.1371/journal.pmed.0030438.
[15]  Tsai AC, Bangsberg DR (2011) The importance of social ties in sustaining medication adherence in resource-limited settings. J Gen Intern Med 26: 1391–1393.
[16]  Ware NC, Idoko J, Kaaya S, Biraro IA, Wyatt MA, et al. (2009) Explaining adherence success in sub-Saharan Africa: an ethnographic study. PLoS Med 6(1): e1000011 doi:10.1371/journal.pmed.1000011.
[17]  Wanyama J, Castelnuovo B, Wandera B, Mwebaze P, Kambugu A, et al. (2007) Belief in divine healing can be a barrier to antiretroviral therapy adherence in Uganda. AIDS 21: 1486–1487.
[18]  Weiser SD, Fernandes KA, Anema A, Brandson EK, Lima VD, et al.. (2009) Food insecurity as a barrier to antiretroviral adherence among HIV-infected individuals in British Columbia. Presented at: 5th International AIDS Society (IAS) conference on HIV pathogenesis, treatment and prevention. Cape Town, South Africa. Available: Accessed 2011 Jun 20.
[19]  Weiser S, Frongillo E, Ragland K, Hogg R, Riley E, et al. (2009) Food insecurity is associated with incomplete HIV RNA suppression among homeless and marginally housed HIV-infected individuals in San Francisco. J Gen intern Med 24: 14–20.
[20]  Kalichman S, Cherry C, Amaral C, White D, Kalichman M, et al. (2010) Health and treatment implications of food insufficiency among people living with HIV/AIDS, Atlanta, Georgia. J Urban Health 87: 631–641.
[21]  Kalichman S, Pellowski J, Kalichman M, Cherry C, Detorio M, et al. (2011) Food insufficiency and medication adherence among people living with HIV/AIDS in urban and peri-urban settings. Prevention Science 12: 324–332.
[22]  Peretti-Watel P, Spire B, Schiltz MA, Bouhnik AD, Heard I, et al. (2006) Vulnerability, unsafe sex and non-adherence to HAART: evidence from a large sample of French HIV/AIDS outpatients. Soc Sci Med 62: 2420–2433.
[23]  Musumari PM, Feldman MD, Techasrivichien T, Wouters E, Ono-Kihara M, et al.. (2013) “If I have nothing to eat, I get angry and push the pills bottle away from me”: A qualitative study of patient determinants of adherence to antiretroviral therapy in the Democratic Republic of Congo. AIDS Care
[24]  Weiser SD, Tuller DM, Frongillo EA, Senkungu J, Mukiibi N, et al. (2010) Food insecurity as a barrier to sustained antiretroviral therapy adherence in Uganda. PLoS One 5(4): e10340 doi:10.1371/journal.pone.0010340.
[25]  Hardon AP, Akurut D, Comoro C, Ekezie C, Irunde HF, et al. (2007) Hunger, waiting time and transport costs: time to confront challenges to ART adherence in Africa. AIDS Care 19: 658–665.
[26]  Weiser SD, Palar K, Frongillo EA, Tsai AC, Kumbakumba E, et al. (2013) Longitudinal assessment of associations between food insecurity, antiretroviral adherence and HIV treatment outcomes in rural Uganda. AIDS 27: 000–000.
[27]  Wang E, McGinnis K, Fiellin D, Goulet J, Bryant K, et al. (2011) Food insecurity is associated with poor virologic response among HIV-infected patients receiving antiretroviral medications. J Gen intern Med 26: 1012–1018.
[28]  Weiser SD, Fernandes KA, Brandson EK, Lima VD, Anema A, et al. (2009) The association between food insecurity and mortality among HIV-infected individuals on HAART. J Acquir Immune Defic Syndr 52: 342–349.
[29]  World Bank and UNAIDS (2009) The Global Economic Crisis and HIV Prevention and Treatment Programmes: Vulnerabilities and Impact. Available: Accessed 2013 Feb 17.
[30]  Food and Agriculture Organization of the United Nations (2012) The state of food insecurity in the world: Economic growth is necessary but not sufficient to accelerate reduction of hunger and malnutrition. Available: Accessed 2013 Jan 25.
[31]  Institut National de la Statistique et Fonds des Nations Unies pour l’Enfance (National Institut of Statistics and United Nations Children’s Fund) (2011) Enquête par Grappes à Indicateurs Multiples en République Démocratique du Congo 2010: Rapport Final (Democratic Republic of Congo Multiple Indicators Cluster Survey 2010: Final Report) Available: 2012 Nov 20.
[32]  Programme National Multisectoriel de lutte contre le VIH/SIDA (National Multi-sectoral Programme on HIV/AIDS) (2012) Rapport d’activité sur la riposte au VIH/SIDA en République Démocratique du Congo (Country Progress Report on HIV/AIDS Response). Available:[1].pdf. Accessed 2012 Dec 12.
[33]  Young S, Wheeler AC, McCoy SL, Weiser SD (2013) A review of the role of food insecurity in adherence to care and treatment among adult and pediatric populations living with HIV and AIDS. AIDS Behav doi:10.1007/s10461-013-0547-4.
[34]  Godin G, Gagne C, Naccache H (2003) Validation of a self-reported questionnaire assessing adherence to antiretroviral medication. AIDS Patient Care STDS 17: 325–332.
[35]  Coates J, Swindale A, Bilinsky P (2007) Household Food Insecurity Access scale (HFIAS) for Measurement of Food Access: Indicator guide. Washington, DC: Food and Nutrition Technical Assistance Project, Academy for Educational Development.
[36]  Kalichman SC, Simbayi LC, Cloete A, Mthembu PP, Mkhonta RN, et al. (2009) Measuring AIDS stigmas in people living with HIV/AIDS: the internalized AIDS-related stigma scale. AIDS Care 21: 87–93.
[37]  Kessler RC, Green JG, Gruber MJ, Sampson NA, Bromet E, et al.. (2010) Screening for serious mental illness in the general population with the K6 screening scale: results from the WHO World Mental Health (WMH) survey initiative. Int J Methods Psychiatr Res (Suppl 19): 4–22.
[38]  Wouters E, Heunis C, van Rensburg D, Meulemans H (2008) Patient satisfaction with antiretroviral services at primary health-care facilities in the Free State, South Africa - a two-year study using four waves of cross-sectional data. BMC Health Serv Res 8: 210.
[39]  McMahon JH, Jordan MR, Kelley K, Bertagnolio S, Hong SY, et al. (2011) Pharmacy adherence measures to assess adherence to antiretroviral therapy: review of the literature and implications for treatment monitoring. Clin Infect Dis 52: 493–506.
[40]  Chi BH, Cantrell RA, Zulu I, Mulenga LB, Levy JW, et al. (2009) Adherence to first-line antiretroviral therapy affects non-virologic outcomes among patients on treatment for more than 12 months in Lusaka, Zambia. Int J Epidemiology 38: 746–756.
[41]  Bisson GP, Gross R, Bellamy S, Chittams J, Hislop M, et al. (2008) Pharmacy refill adherence compared with CD4 count changes for monitoring HIV-infected adults on antiretroviral therapy. PLoS Med 5(5): e109 doi:10.1371/journal.pmed.0050109.
[42]  Weidle PJ, Wamai N, Solberg P, Liechty C, Sendagala S, et al. (2006) Adherence to antiretroviral therapy in a home-based AIDS care programme in rural Uganda. Lancet 368: 1587–1594.
[43]  Nguyen H, Zyl GV, Geboers D, Gross R, Mills EJ, et al.. (2011) Pharmacy refill data combined with self-report adherence questions improves prediction of boosted protease inhibitor regimen failure. Presented at: 6th International Conference on HIV Treatment and Prevention Adherence. Miami, USA.
[44]  Goldman JD, Cantrell RA, Mulenga LB, Tambatamba BC, Reid SE, et al. (2008) Simple adherence assessments to predict virologic failure among HIV-infected adults with discordant immunologic and clinical responses to antiretroviral therapy. AIDS Res Hum Retroviruses 24: 1031–1035.
[45]  Peltzer K, Ramlagan S (2011) Perceived stigma among patients receiving antiretroviral therapy: a prospective study in KwaZulu-Natal, South Africa. AIDS Care 23: 60–68.
[46]  Filmer D, Pritchett LH (2001) Estimating wealth effects without expenditure data–or tears: an application to educational enrollments in states of India. Demography 38(1): 115–132.
[47]  Heaney CA, Israel BA (2008) Social networks and social support. In: Glanz K, Rimer BK, Viswanath K. Health Behavior and Health Education. San Francisco, CA: John Wiley & Sons. 189–210.
[48]  Weiser SD, Tsai AC, Gupta R, Frongillo EA, Kawuma A, et al. (2012) Food insecurity is associated with morbidity and patterns of healthcare utilization among HIV-infected individuals in a resource-poor setting. AIDS 26: 67–75.
[49]  Cantrell RA, Sinkala M, Megazinni K, Lawson-Marriott S, Washington S, et al. (2008) A pilot study of food supplementation to improve adherence to antiretroviral therapy among food-insecure adults in Lusaka, Zambia. J Acquir immune Defic Syndr 49: 190–195.
[50]  Tirivayi N, Koethe JR, Groot W (2012) Clinic-based food assistance is associated with increased medication adherence among HIV-infected adults on long-term antiretroviral in Zambia. J AIDS Clin Res 3(7): 171.
[51]  Tsai AC, Bangsberg DR, Emenyonu N, Senkungu JK, Martin JN, et al. (2011) The social context of food insecurity among persons living with HIV/AIDS in rural Uganda. Soc Sci Med 73: 1717–1724.
[52]  Tiyou A, Belachew T, Alemseged F, Biadgilign S (2012) Food insecurity and associated factors among HIV-infected individuals receiving highly active antiretroviral therapy in Jimma zone Southwest Ethiopia. Nutrition Journal 11: 51.
[53]  Weiser SD, Hatcher A, Frongillo EA, Guzman D, Riley ED, et al. (2013) Food Insecurity Is Associated with Greater Acute Care Utilization among HIV-Infected Homeless and Marginally Housed Individuals in San Francisco. J Gen Intern Med 28: 91–98.
[54]  Anema A, Weiser SD, Fernandes KA, Ding E, Brandson EK, et al. (2011) High prevalence of food insecurity among HIV-infected individuals receiving HAART in a resource-rich setting. AIDS Care 23: 221–230.
[55]  World Food Programme (2003) Programming in the Era of AIDS: WFP’s Response to HIV/AIDS. Available:’s%20Response%20to%20HIV:AIDS.pdf. Accessed 2012 Nov 11.
[56]  United Nations. Nutrition and HIV/AIDS. Statement by the Administrative Committee on Coordination, Sub-Committee on Nutrition as its 28th Session. Nairobi, Kenya: United Nations Administrative Committee on Coordination, Sub-Committee on Nutrition; 2001. Available: Accessed 2012 Dec 3.
[57]  Johnston BE, Ahmad K, Smith C, Rose DN (1998) Adherence to highly active antiretroviral therapy among-HIV-infected patients of the inner city. Presented at: 12th World AIDS Conference. Geneva, Switzerland.
[58]  Horne R, Weinman J (1999) Patients’ beliefs about prescribed medicines and their role in adherence to treatment in chronic physical illness. Journal of Psychosom Res 47(6): 555–567.
[59]  Wasti SP, Simkhada P, Randall J, Freeman JV, van Teijlingen E (2012) Factors Influencing Adherence to Antiretroviral Treatment in Nepal: A Mixed-Methods Study. PLoS One 7: e35547.
[60]  Jacquet A, Ekouevi DK, Bashi J, Aboubakrine M, Messou E, et al.. (2009) Alcohol use and adherence to antiretroviral therapy in HIV-infected patients in West Africa. Presented at: 5th International AIDS Society (IAS) conference on HIV pathogenesis, treatment and prevention. Cape Town, South Africa. Available: Accessed 2012 Jan 12.
[61]  Nemes MI, Carvalho HcB, Souza MF (2004) Antiretroviral therapy adherence in Brazil. AIDS 18: S15–S20.
[62]  Godin G, Cote J, Naccache H, Lambert LD, Trottier S (2005) Prediction of adherence to antiretroviral therapy: a one year longitudinal study. AIDS Care 17: 493–504.
[63]  Nel A, Kagee A (2013) The relationship between depression, anxiety and medication adherence among patients receiving antiretroviral treatment in South Africa. AIDS Care 8: 948–955.
[64]  Campos L, Guimaraes M, Remien R (2008) Anxiety and Depression Symptoms as risk factors for non-adherence to antiretroviral therapy in Brazil. AIDS Behav 14: 289–299.
[65]  Molassiotis A, Nahas-Lopez V, Chung WYR, Lam SWC, Li CKP, et al. (2002) Factors associated with adherence to antiretroviral medication in HIV-infected patients. Int J STD AIDS 13: 301–310.
[66]  Furukawa TA, Kessler RC, Slade T, Andrews G (2003) The performance of the K6 and K10 screening scales for psychological distress in the Australian National Survey of Mental Health and Well-Being. Psychol Med 33: 357–362.
[67]  Andersen LS, Grimsrud A, Myer L, Williams DR, Stein DJ, et al. (2011) The psychometric properties of the K10 and K6 scales in screening for mood and anxiety disorders in the South African Stress and Health study. Int J Methods Res 20: 215–223.
[68]  Joint United Nations Programme on HIV/AIDS & World Health Organization (2009) AIDS Epidemic update. Available: Accessed 2012 Mar 23.


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