The health benefits of HIV antiretroviral therapy (ART) are well documented [1,2]. However, the socioeconomic benefits of ART are still being established . Abundant studies have illustrated the negative effect of HIV on individual and household economic well-being via decreased physical and mental health [4,5]. Food insecurity can deepen as income, productivity, and assets decrease due to HIV . Several recent studies in Uganda have documented food insecurity as a serious problem for HIV-affected households [7–9].
Food insecurity is the limited or uncertain availability of adequate food, or inability to acquire food in socially acceptable ways . Food insecurity is associated with lower CD4 cell count [11,12], incomplete viral suppression [13,14], increased morbidity and mortality [15,16], and poor ART adherence and treatment retention in resource-poor settings [17–19].
Less is known about how ART affects food insecurity. Food security, by definition, is closely related to the ability to conduct economic activities. A growing number of studies conducted mainly in sub-Saharan Africa suggest that improved physical and mental health due to ART can lead to improved economic well-being via increased labor productivity and ability to conduct daily activities required for basic needs .
We use data from a prospective cohort study in Uganda to examine how the food insecurity of a treatment-naive population changes over the first year of HIV care. We then investigate the effect of ART on food insecurity by comparing patients on ART with patients not yet on ART, and explore the potential pathways through which ART may affect food insecurity. We hypothesize that ART will influence food security via improved mental health, improved physical health, and improved ability to work.
Study design and sample
The Joint Clinical Research Center (JCRC)/RAND prospective cohort study (January 2008 to November 2009) was designed to determine the effect of ART on physical and mental health, as well as socioeconomic outcomes. New patients at two clinics in Uganda were consecutively recruited into the study using the following inclusion criteria: adults over 18 years of age; assessed for ART eligibility; and CD4 cell count less than 400 cells/μl. Patients previously receiving HIV care were excluded. Predetermined ART and non-ART groups were assigned based on ART eligibility: CD4 cell count of 250 cells/μl or less or WHO stage 3 or 4 HIV disease, as well as self-disclosure of HIV status to a patient-identified ‘treatment supporter’. The two clinics were both operated by JCRC, one in the capital city Kampala and one in Kakira, a rural town about 100 km away. Importantly, HIV care and treatment at the JCRC clinics did not include food supplementation.
Participants were interviewed at baseline, 6, and 12 months and paid 5000 Ugandan Shillings (US$2.50) for each assessment. Written informed consent was obtained from all participants. The interview protocol was approved by the Institutional Review Board at RAND and JCRC in Uganda.
All questionnaire-based measures in the protocol were collected in face-to-face interviews administered in Luganda, the native language of the participants. Clinical data were abstracted from clinical charts using standardized forms.
Food insecurity was assessed using a five-item scale adapted by the study team from the US Household Food Security Survey Module 6-Item Short Form . The adapted scale assessed individual food sufficiency and affordability in the context of household resources, and categorized food security as ‘very low’, ‘low’, or ‘marginal or better’. Cronbach's α for the adapted scale at baseline was 0.92, indicating high internal consistency. For analysis, we constructed a binary variable for severe food insecurity representing participants with ‘very low’ food security.
Depression was assessed using the nine-item Patient Health Questionnaire (PHQ-9), whose items correspond to symptoms of major depression from the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. The range of possible scores was 0–27, with higher scores indicating higher depression. The PHQ-9 has been used successfully with HIV clients in other parts of sub-Saharan Africa .
Physical health was assessed using the two-item subscale for role functioning of the Medical Outcomes Study HIV Health Survey (MOS-HIV) , specifically adapted for Uganda . The role functioning subscale assessed whether health has limited the participant from working at a job or around the house. Raw scores ranged from 0 to 2.
Current work status was a binary variable defined as having worked (other than housework) in the last 7 days based on self-report as measured by the World Bank Living Standard Measurement Surveys .
Financial or asset wealth has been associated with food insecurity and HIV-related health . We used the method of principal components  to create an asset index based on relatively liquid forms of wealth (cell phone, television, radio, motorized vehicle, and livestock) that might be expected to change with current economic circumstances .
Recent studies among people with HIV have identified material support as important for both food security and health . Our material support measure represented whether the participant had received food or financial support from any source in the last month.
Food insecurity is associated with measures of HIV-related health [12,28]. Continuous CD4 cell count (cells per microliter) and binary WHO HIV disease stage 3 or 4 were abstracted manually from patients’ clinical charts.
Sex, age, education, head of household, and household size are associated with both food insecurity and HIV outcomes  and were assessed in our study based on modules of the World Bank Living Standard Measurement Surveys .
Analyses were based on comparisons of food insecurity across the ART and non-ART groups at baseline and over time. We first used bivariate statistics (χ 2-test and two-sample t-test) to compare baseline characteristics across the ART and non-ART groups, and across food insecurity groups. To examine change over time, we explored trends in the outcome and pathway variables and tested for statistically significant differences over the three assessments by ART status (paired t-test, McNemar's test).
Our primary analysis was an intention-to-treat (ITT) approach that included all participants. We conducted multivariate longitudinal logistic regression to investigate the effect of ART on food insecurity over the three assessments, with severe food insecurity as the outcome. The main independent variables were ART status at baseline, an ordinal variable for time representing the three assessments, and an interaction term of ART status by time. We then used a staged regression approach to explore the potential explanatory role of the pathway variables identified in our conceptual framework. In the first step, we analyzed the regression model for food insecurity using the main independent variables listed above. In subsequent steps, we reexamined the models while consecutively adding in change in depression, work status, and role functioning from 0 to 12 months as potential pathway variables. Change in depression was modeled as an inverse change so that an increase would indicate improvement. We implemented the regression using generalized estimating equations for analysis of correlated repeated measurements , using semirobust standard errors and assuming a binomial distribution for the binary food insecurity outcome.
All regressions controlled for the following ‘baseline’ characteristics: female, Kampala, CD4 cell count, food security score, work status, role functioning score, depression score, asset index score, and receipt of material support, as well as month-of-interview indicators to account for seasonal food insecurity. We excluded age, household size, and head of household status from the regressions, as they neither differentiated the ART groups or food security groups in bivariate analysis (Table 1).
All analyses included attrition weights to account for drop out from the study, which were derived via logistic regression using completion status as the outcome and baseline measures associated with ART and completion status as the independent variables. All statistical analyses were conducted in STATA/IC 11.1 (StataCorp, College Station, Texas, USA).
We addressed the issue of comparability between the ART and non-ART groups by restricting the non-ART group to those patients with CD4 cell count (<250 μl) or WHO HIV stage 3 or 4, who would normally qualify for ART but were deferred for medical or psychosocial reasons. In addition, we changed our ITT analysis to an ‘as treated analysis’ by excluding 50 patients assigned to the non-ART group at baseline, who started ART during the course of the study. Finally, we re-ran our original models with alternate measures of physical health status from the MOS-HIV to explore whether choice of measure affected our results.
The sample consisted of 602 participants, including 300 ART and 302 non-ART patients, distributed evenly between Kampala and Kakira. Retention in the study was high: 92% of the ART group and 94% of the non-ART group completed the 12-month assessment. At baseline, the ART group had lower CD4 cell count, lower education, lower asset wealth, lower health functioning, lower work status, and higher depression compared with the non-ART group (Table 1).
At baseline, 50% of all participants had severe food insecurity. In bivariate analysis, the ART group had a higher prevalence of severe food insecurity (54%) compared with the non-ART group (46%; P < 0.05) (Table 1).
The prevalence of severe food insecurity decreased for both the ART and non-ART group over the first 12 months of treatment, although this trend was more pronounced for the ART group (Fig. 1). In the ART group, food insecurity decreased significantly from baseline (53%) to month 6 (37%; P < 0.001), and again from months 6 to 12 (13%; P < 0.001). The non-ART group experienced a similar reduction from baseline (46%) to month 6 (33%; P < 0.001), and again from months 6 to 12 (18%; P < 0.001).
In the multivariate regression model of food insecurity over 12 months, the significant odds ratios (ORs) on both ‘time’ (OR 0.352; P < 0.001) and the interaction of ‘ART×time’ (OR 0.642; P < 0.01) indicate that both time and ART were significant predictors of decreased of food insecurity after controlling for baseline differences (Table 2, column 1). The OR on ‘ART×time’ means that the ART group had almost 36% lower odds of food insecurity at each assessment above and beyond the non-ART group.
Our sensitivity analyses, including the ‘as treated’ analysis and the comparison of the sickest of the non-ART group to the ART group yielded similar multivariate regression results (data not shown, available from authors upon request).
Role of pathway variables
Work status improved significantly for the ART group from baseline (49%) to month 6 (72%; P < 0.01) and again from months 6 to 12 (81%; P < 0.01), whereas the non-ART group experienced a smaller increase from baseline (69%) to month 6 (75%; P < 0.01) and again from months 6 to 12 (80%; P < 0.01) (see Fig. 2a).
When change in work status was added to the regression model for food insecurity, improved work status was a significant predictor of decreased odds of food insecurity (OR 0.438; P < 0.001) (Table 2, column 4), whereas the OR on ‘ART×time’ weakened in magnitude and significance (OR 0.689; P < 0.05).
In the ART group, depression decreased significantly from baseline (mean 5.9) to month 6 (mean 2.4; P < 0.01) and again from months 6 to 12 (mean 1.4; P < 0.01). In the non-ART group, depression decreased from baseline (mean 4.2) to month 6 (mean = 2.4), but did not change further from months 6 to 12 (see Fig. 2b).
When change in depression was added to the regression model for food insecurity, one unit of decreased depression was a significant predictor of decreased odds of food insecurity (OR 0.902; P < 0.001) (Table 2, column 3), whereas the OR on ‘ART×time’ weakened in magnitude and significance (OR 0.684; P < 0.05).
Role functioning improved for both the ART and non-ART groups over time (Fig. 2c) but was not a significant predictor of food insecurity in multivariate analysis. When alternate measures of physical health were used in sensitivity analysis, physical health was still not a significant predictor of food insecurity.
Although food security improved over time for patients entering care and treatment regardless of ART status, ART was a significant predictor of improved food security above and beyond HIV care without ART. This study contributes to growing evidence that ART benefits people with HIV beyond improving their health, and extends the range of socioeconomic benefits of ART to include improved food security. To our knowledge, no published studies have explicitly examined changes in food insecurity as an outcome of HIV treatment and care. We provide some of the first robust evidence that ART helps alleviate the food insecurity of adults with HIV, even in the absence of treatment-related food assistance.
Our results suggest that greater ability to work and reduced symptoms of depression may be the primary pathways through which ART improves food insecurity. These results are consistent with growing evidence that ART improves employment status and productivity for people with HIV [31,32], and that mental health may play a key role [33,34]. Identifying improved work and mental health as possible pathways between ART and reduced food insecurity reinforces the growing recognition of the importance of mental health support and livelihoods programs as part of comprehensive treatment and care for people with HIV.
Our findings on the effect of ART on food insecurity, taken together with evidence that reducing food insecurity may improve ART outcomes, provide empirical support for the bidirectional relationship between ART and food insecurity. However, although ART may improve food security, we find that the magnitude of this benefit is modest and that ART alone will not resolve food insecurity for people with HIV. Rather, a bidirectional relationship implies food security and ART may work in a positive feedback cycle that could be leveraged by ART programs to improve well-being by promoting mental health support, livelihoods interventions, such as income generation projects, and food assistance as part of HIV treatment.
In addition, improved food security in the non-ART group suggests that entering HIV care could have a positive effect on food security, even prior to ART. Controlling for seasonality in our regressions strengthens the proposition that food security may improve due to HIV care rather than to secular trends in the community. Furthermore, significant improvement in depression and work status in the non-ART group suggests that entering HIV care may improve food security via similar pathways as ART. However, without a control group of people not receiving any HIV treatment and care, we cannot formally test this hypothesis.
The primary limitation of this study is that ART could not be randomly assigned for ethical reasons, given the widespread access to ART in Uganda at the time of study enrollment. Therefore, we constructed our sample to be as comparable as possible by restricting the control group to those who were almost, though not yet, eligible for ART and then included key group differences as covariates in our regression models. Our results were robust to sensitivity analysis that limited the non-ART group to its sickest members to be comparable with the ART group. Nevertheless, as an observational study, it is possible that some important confounding variables were not measured.
The potential for ART to improve the food security of people living with HIV strengthens both the policy and public health case for sustaining and scaling-up treatment for all those in need of it, with a special imperative to improve access and uptake in areas where ART is available. This is more important than ever as the WHO now recommends ART initiation at earlier CD4 thresholds, effectively increasing the demand for ART . A nuanced understanding of the bidirectional relationship between ART and food security, in which employment and mental health play key roles, should inform decision-makers as they consider the development of interventions to halt the ‘vicious cycle’ of HIV and poor social and economic outcomes, including food insecurity. Well integrated and implemented interventions in the context of comprehensive care have the potential to produce an ‘upward spiral’ in which food security and ART can mutually reinforce each other for the benefit of all those in treatment.
K.P. planned and conducted the analysis, conducted the data interpretation, drafted the manuscript, and made final edits to the manuscript. G.W. designed the study, supervised the collection and management of the data, supported the analysis, contributed to data interpretation, and provided significant feedback on the manuscript. B.G.-D. supported the analysis, contributed to data interpretation, and provided feedback on the manuscript. P.M. oversaw the data collection and contributed to the data interpretation. All authors have read and approved the final manuscript.
The authors would like to thank the study coordinators (Tonny Kizza, Joseph Bebe, and Mark Magina), the clinic directors (William Tamale and Grace Namayanja), nurse Erina Turya, and counselors (Hellen Nakyambadde, Rose Byaruhanga, and Grace Barungi) who helped to identify and refer participants, and the client participants who gave so generously of their time and their personal information. The authors also thank Homero Martinez at RAND for early contributions to the analysis and feedback on the manuscript, and Sheri Weiser at University of California San Francisco for detailed feedback and comments on the manuscript.
This research is supported by a grant from the Rockefeller Foundation (HE 007; principal investigator G.W.). K.P. receives support from grant number T32HS00046 from the Agency for Healthcare Research and Quality. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Agency for Healthcare Research and Quality.
Conflicts of interest
There are no conflicts of interest.
1. Bartlett JA, DeMasi R, Quinn J, Moxham C, Rousseau F. Overview of the effectiveness of triple combination therapy in antiretroviral-naive HIV-1 infected adults
2. Murphy EL, Collier AC, Kalish LA, Assmann SF, Para MF, Flanigan TP, et al. Highly active antiretroviral therapy decreases mortality and morbidity in patients with advanced HIV disease
. Ann Inter Med
3. Beard J, Feeley F, Rosen S. Economic and quality of life outcomes of antiretroviral therapy for HIV/AIDS in developing countries: a systematic literature review
. AIDS Care
4. Russell S. The economic burden of illness for households in developing countries: a review of studies focusing on malaria, tuberculosis, and human immunodeficiency virus/acquired immunodeficiency syndrome
. Am J Trop Med Hyg
5. McIntyre D, Thiede M, Dahlgren G, Whitehead M. What are the economic consequences for households of illness and of paying for healthcare in low-and middle-income country contexts?
. Soc Sci Med
6. Crush J, Drimie S, Frayne B, Caesar M. The HIV and urban food security nexus in Africa
. Food Secur
7. Bukusuba J, Kikafunda J, Whitehead R. Food security status in households of people living with HIV/AIDS (PLWHA) in a Ugandan urban setting
. Br J Nutr
8. 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
. Soc Sci Med
9. Weiser S, Tuller D, Frongillo E, Senkungu J, Mukiibi N, Bangsberg D, et al. Food Insecurity as a barrier to sustained antiretroviral therapy adherence in Uganda
. PLoS One
10. Radimer KL, Olson CM, Greene JC, Campbell CC, Habicht JP. Understanding hunger and developing indicators to assess it in women and children
. J Nutr Educ
11. Kalichman S, Cherry C, Amaral C, White D, Kalichman M, Pope H, et al. Health and treatment implications of food insufficiency among people living with HIV/AIDS, Atlanta, Georgia. J Urban Health
12. Weiser S, Bangsberg D, Kegeles S, Ragland K, Kushel M, Frongillo E. Food insecurity among homeless and marginally housed individuals living with HIV/AIDS in San Francisco
. AIDS Behav
13. Wang EA, McGinnis KA, Fiellin DA, Goulet JL, Bryant K, Gibert CL, et al. Food insecurity is associated with poor virologic response among HIV-infected patients receiving antiretroviral medications
. J Gen Intern Med
14. Weiser S, 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
15. Weiser S, Fernandes K, Brandson E, Lima V, Anema A, Bangsberg D, et al. The association between food insecurity and mortality among HIV-infected individuals on HAART
. J Acquir Immune Defic Syndr
16. 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
17. Deribe K, Hailekiros F, Biadgilign S, Amberbir A, Beyene B. Defaulters from antiretroviral treatment in Jimma University Specialized Hospital, southwest Ethiopia
. Trop Med Int Health
18. Franke M, Murray M, Muñoz M, Hernández-Díaz S, Sebastián J, Atwood S, et al. Food insufficiency is a risk factor for suboptimal antiretroviral therapy adherence among HIV-infected adults in urban Peru
. AIDS Behav
19. Marcellin F, Boyer S, Protopopescu C, Dia A, Ongolo-Zogo P, Koulla-Shiro S, et al. Determinants of unplanned antiretroviral treatment interruptions among people living with HIV in Yaoundé, Cameroon (EVAL survey, ANRS 12-116)
. Trop Med Int Health
20. Bickel G, Nord M, Price C, Hamilton W, Cook J. Guide to measuring household food security, revised 2000
. Alexandria, Virginia: Food and Nutrition Service, US Department of Agriculture; 2000.
21. Monahan PO, Shacham E, Reece M, Kroenke K, Ong’or WO, Omollo O, et al. Validity/reliability of PHQ-9 and PHQ-2 depression scales among adults living with HIV/AIDS in western Kenya
. J Gen Intern Med
22. Wu A, Revicki D, Jacobson D, Malitz F. Evidence for reliability, validity and usefulness of the Medical Outcomes Study HIV Health Survey (MOS-HIV)
. Qual Life Res
23. Mast T, Kigozi G, Wabwire-Mangen F, Black R, Sewankambo N, Serwadda D, et al. Measuring quality of life among HIV-infected women using a culturally adapted questionnaire in Rakai district, Uganda
. AIDS Care
24. Grosh ME, Glewwe P. Designing household survey questionnaires for developing countries: lessons from 15 years of the living standards measurement study
. Washington, District of Columbia: World Bank; 2000.
25. Rose D. Economic determinants and dietary consequences of food insecurity in the United States
. J Nutr
26. Filmer D, Pritchett LH. Estimating wealth effects without expenditure data – or tears: an application to educational enrollments in states of India
27. Linnemayr S, Stearns Lawson B, Glick P, Wagner G. Economic status and coping mechanisms of individuals seeking HIV care in Uganda. J Afr Economies
28. Normen L, Chan K, Braitstein P, Anema A, Bondy G, Montaner JS, et al. Food insecurity and hunger are prevalent among HIV-positive individuals in British Columbia, Canada
. J Nutr
29. Anema A, Vogenthaler N, Frongillo E, Kadiyala S, Weiser S. Food insecurity and HIV/AIDS: current knowledge, gaps, and research priorities
. Curr HIV/AIDS Rep
30. Zeger SL, Liang KY, Albert PS. Models for longitudinal data: a generalized estimating equation approach. Biometrics
31. Rosen S, Larson B, Brennan A, Long L, Fox M, Mongwenyana C, et al. Economic outcomes of patients receiving antiretroviral therapy for HIV/AIDS in South Africa are sustained through three years on treatment
. PLoS One
32. Thirumurthy H, Zivin JG, Goldsten M. The economic impact of AIDS treatment: labor supply in western Kenya
. J Hum Resources
33. Collins PY, Holman AR, Freeman MC, Patel V. What is the relevance of mental health to HIV/AIDS care and treatment programs in developing countries? A systematic review
34. Wagner GJ, Holloway I, Ghosh-Dastidar B, Kityo C, Mugyenyi P. Understanding the influence of depression on self-efficacy, work status, and condom use among HIV clients in Uganda. J Psychosom Res
35. Konde-Lule J, Makumbi F, Pakker N, Muyinda A, Mubiru M, Cobelens F. Effect of changing antiretroviral treatment eligibility criteria on patient load in Kampala, Uganda
. AIDS Care