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JAIDS Journal of Acquired Immune Deficiency Syndromes:
doi: 10.1097/QAI.0b013e3182797363
Epidemiology and Prevention

Poor Diet Quality Is Associated With Low CD4 Count and Anemia and Predicts Mortality Among Antiretroviral Therapy–Naive HIV-Positive Adults in Uganda

Rawat, Rahul PhD*; McCoy, Sandra I. MPH, PhD; Kadiyala, Suneetha PhD

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Author Information

*Poverty, Health, and Nutrition Division, International Food Policy Research Institute, Washington, DC

Division of Epidemiology, School of Public Health, University of California, Berkeley, CA

Poverty, Health, and Nutrition Division, International Food Policy Research Institute, New Delhi, India.

Correspondence to: Sandra I. McCoy, MPH, PhD, Division of Epidemiology, School of Public Health, University of California, 1918 University Avenue, Suite 3B, Berkeley, CA 94704 (e-mail: smccoy@berkeley.edu).

Supported by the Regional Network on AIDS, Livelihoods and Food Security (RENEWAL), facilitated by the International Food Policy Research Institute (IFPRI), the International Initiative for Impact Evaluation (3ie), and through an IFPRI Concern Worldwide research partnership funded by the Kerry Group. RENEWAL is grateful for support from the International Initiative for Impact Evaluation (3ie), Irish Aid, and the Swedish International Development Cooperation Agency. Dr S. I. McCoy is supported by Award Number K01MH094246 from the National Institute of Mental Health.

The authors have no conflicts of interest to disclose.

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health.

Received July 09, 2012

Accepted October 12, 2012

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Abstract

Background: We assessed the association between dietary diversity and CD4 count, moderate anemia, and mortality among 876 antiretroviral therapy–naive people living with HIV/AIDS infection (PLHIV) in Uganda.

Methods: Participants were interviewed and followed for an average of 21.6 months. Dietary diversity was measured using the Individual Dietary Diversity Score (IDDS) (range, 0–12) and summarized into an overall measure and disaggregated into nutrient-rich food groups (range, 0–7), cereals, roots, and tubers (range, 0\x{2013} 2); and oils, fats, sugars, and condiments (range, 0\x{2013} 3). We determined the cross-sectional associations between dietary diversity and (1) immunosuppression (CD4 count ≤ 350 cells/μL) and (2) moderate anemia (hemoglobin < 10 g/dL) at baseline with logistic regression. We assessed the association between IDDS and mortality using Cox proportional hazards regression.

Results: The mean IDDS score was 6.3 (SD 1.7) food groups per day, with a mean of 2.7 (SD 1.1) nutrient-rich food groups per day. Each additional nutrient-rich food group consumed was associated with a 16% reduction in the likelihood of having a CD4 count ≤350 cells/μL [adjusted odds ratio, 0.84; 95% confidence interval (CI): 0.72 to 0.97] at baseline. Among those with >350 CD4 cells per microliter, but not those with CD4 count ≤350 cells per microliter, consumption of nutrient-rich food groups was associated with a lower odds of moderate anemia (adjusted odds ratio, 0.57; 95% CI: 0.34 to 0.96). During follow-up, 48 participants (5.6%) died (mortality rate of 3.1 per 100 person-years). IDDS was inversely associated with mortality [adjusted hazard ratio, 0.76; 95% CI: 0.63 to 0.91].

Conclusion: These results suggest that diet quality is an important determinant of HIV disease severity and mortality in antiretroviral therapy–naive PLHIV.

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INTRODUCTION

It is increasingly recognized that food insecurity both heightens vulnerability to HIV infection and exacerbates poor clinical outcomes among people living with HIV/AIDS (PLHIV).1–5 Food security exists when people have adequate physical, social, and economic access to sufficient, safe, and nutritious food that meets their dietary needs and food preferences for an active and healthy life.6 Among PLHIV, food insecurity is associated with incomplete HIV RNA suppression,7,8 CD4 decline over time,9 increased opportunistic infections and hospitalizations,10 and HIV-related mortality.3 However, most of the research in this area has focused on one element of food insecurity, food access, which refers to having adequate resources (eg, income) to obtain food for a nutritious diet.11 There has been little focus on how nutrient-rich foods and diet quality in general might be related to HIV disease progression and severity.

Although the evidence is mixed about the effects of micronutrient supplementation on progression of HIV infection,12–15 the World Health Organization recommends that access to and intake of a diet that provides the full range of essential micronutrients is a critical component of health for PLHIV.16 They further recommend that in areas where micronutrient deficiencies are endemic, efforts should be made to ensure that micronutrient needs are met by increasing access to a diversified diet, fortified foods, and micronutrient supplements as appropriate.16 Nevertheless, among rural poor populations in much of sub-Saharan Africa, consumption of a diverse diet is often a challenge and can be a critical constraint to meeting nutritional needs. Thus, we assessed the association between diet quality and HIV disease severity, moderate anemia, and mortality among HIV-infected individuals living in a resource-limited setting in Uganda.

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METHODS

We conducted an analysis of survey data from adults 18 years and older participating in the evaluation of a World Food Programme (WFP)–supported food assistance program for PLHIV in Uganda. The study has been previously described.17 In brief, 2 districts participated in the evaluation, with one receiving the food assistance intervention (Gulu) and the other serving as the matched comparison (Soroti). The data for the current analysis are from the baseline survey of the parent WFP evaluation and mortality data from medical records. We conducted a cross-sectional analysis to determine the association, at baseline, between dietary diversity and (1) CD4 count and (2) moderate anemia. In addition, using a prospective cohort, we examined the association between baseline dietary diversity and mortality.

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Study Population

Between July 2008 and October 2009, 450 PLHIV registered with The AIDS Support Organization (TASO) were recruited from each district. TASO is the largest indigenous nongovernmental organization in Uganda with more than 200,000 registered clients receiving HIV prevention, care, and treatment services. All TASO clients receive the TASO standard of care, including counseling on positive living and risk reduction, prophylaxis for opportunistic infections, and antiretroviral therapy (ART) (when eligible). Study participants met the following inclusion criteria: (1) qualified to receive a WFP monthly household food basket based on WFP’s poverty assessment criteria, (2) no receipt of food assistance in the past 12 months, (3) CD4 cell count between 200 and 450 cells per microliter, (4) not currently on ART (97% of participants were ART naive), and (5) not pregnant. WFP’s poverty assessment tool was administered by TASO personnel and includes the following domains: household composition, employment status, income, housing characteristics, basic food sources and consumption, household expenditures, and access to services.

At study enrollment, participants were interviewed and provided blood specimens for assessment of CD4 and hemoglobin (Hb) levels. The CD4 cell count range (200–450 cells/μL) was purposefully selected to include ART ineligible individuals with some level of immunosuppression who could therefore benefit from the intervention (at the time of the study, the threshold for ART initiation was ≤200 cells/μL for asymptomatic PLHIV18). For the current analysis, we restricted the study to participants who were ART naive at enrollment.

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Outcome Assessment

The outcomes of interest were baseline CD4 count, moderate anemia at baseline, and mortality. CD4 count was examined both as a continuous variable ranging from 200 to 450 cells per microliter and a binary variable indicating ≤350 cells per microliter = 1 or >350 cells per microliter = 0, using the current threshold for ART initiation.18 Similarly, Hb was dichotomized into <10 g/dL = 1, the upper threshold for moderate anemia or ≥10 g/dL = 0 (too few participants met the criteria for severe anemia to use the <8 g/dL cutoff, and we therefore used the next most conservative cutoff).19 Hb was only available for a subset of participants due to interviewer error. Thus, we also created a 3-level categorical variable for anemia (used in the survival analysis) that included a level for unknown anemia status (no anemia = 0, moderate anemia = 1, and unknown anemia = 2). Mortality was recorded by TASO clinics and was collected on an ongoing basis until October 2011 for all patients and linked to baseline interview data for the current analysis. The maximum follow-up time was 3.3 years.

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Exposure Assessment

Diet quality was assessed at baseline using the Individual Dietary Diversity Score (IDDS), a proxy measure for the nutritional quality of an individual’s diet.20 The IDDS ranges from 0 to 12 and is the number of different food groups consumed in the 24 hours preceding the interview, out of the following 12 groups: (1) cereals; (2) roots and tubers; (3) pulses, legumes, and nuts; (4) vegetables; (5) fruits; (6) meat and poultry; (7) eggs; (8) fish and seafood; (9) milk and milk products; (10) oils and fats; (11) sugar and sweets; and (12) condiments and miscellaneous.

In addition to computing the overall IDDS score, we grouped the 12 food categories into 3 subgroups and computed a summary score for each: (1) nutrient-rich foods (range, 0–7); (2) cereals, roots, and tubers (range, 0–2); and (3) oils, fats, sugars, and condiments (range, 0–3). Given the pattern of dietary diversity in Uganda, with an overreliance on starchy staple foods, a relatively high consumption of energy-dense sugars, fats, and oil and a very low consumption of foods rich in protein and micronutrients, we refer to nutrient-rich foods as those foods rich in protein and micronutrients. Therefore, nutrient-rich foods included pulses, legumes, and nuts; vegetables; fruits; meat and poultry; eggs; fish and seafood; and milk and milk products. We evaluated the number of nutrient-rich food groups consumed as a continuous variable and a binary indicator for low (0–3 groups) and high (4–7 groups) consumption of nutrient-rich food groups.

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Covariates

Covariates included individual, household, and community characteristics measured at baseline that may confound the association between dietary diversity and the outcomes of interest. In all adjusted models, we included age (continuous), sex, underweight at baseline (body mass index < 18.5 kg/m2), education (below primary school=1, 0=completed primary school or more), whether the participant was married or cohabitating with a partner (yes/no), whether the participant was the head of household or spouse of the head of household, whether the participant lives in an internal displacement camp (yes/no), household size, and per capita total monthly household expenditures in tertiles. We also included distances (in kilometers) to market and government health clinic as measures of connectedness to basic services. In addition, we included time (in minutes) to the TASO clinic, which accounts for both distance and mode of transportation and could affect retention in care. We included month and year of the interview and a district indicator variable (Gulu = 1; Soroti = 0) to control for district-level unobservable characteristics and receipt of WFP food assistance. Food insecurity was measured using the Household Food Insecurity Access Scale.21 Given that all participants in the study met the minimum threshold for food insecurity, we included a binary indicator for severe food insecurity (Household Food Insecurity Access category = 4) in all models.

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Statistical Analysis

We first compared participant characteristics stratified by consumption of nutrient-rich foods (low or high). To determine the association between dietary diversity and CD4 count, we used multivariate ordinary least squares (OLS) linear regression. We also used logistic regression with the binary outcome variable CD4 ≤350 versus >350 cells per microliter. When moderate anemia was the outcome, we used logistic regression with a binary outcome variable for moderate anemia. In this model, an interaction between dietary diversity and baseline CD4 cell count (cells/μL) was specified a priori given the likelihood that anemia in immunosuppressed PLHIV may be more strongly associated with opportunistic infections and HIV infection itself, rather than iron deficiency, which may be more strongly associated with moderate anemia in PLHIV with higher CD4 counts.22 We present parameter estimates and SEs for OLS models and unadjusted and adjusted odds ratios (ORas) and 95% confidence intervals (CIs) for the logistic regression models.

We assessed the association between baseline dietary diversity and mortality using Cox proportional hazards regression. Participants were censored when they initiated ART or at last record review (October 2011), whichever was earlier. For each covariate, we assessed confounding and the covariate\x{2019}s effect on mortality. We also tested the proportional hazards assumption for that covariate. The fully adjusted model includes all covariates and an interaction between CD4 count (≤350 versus >350 cells/μL) and continuous time to relax the proportional hazards assumption. Moderate anemia had a strong independent effect on mortality but was only available for a subset of participants. We therefore ran adjusted mortality models with and without adjustment for the 3-level anemia variable; both models are presented. We present unadjusted and adjusted hazard ratios (HRas) and 95% CIs with robust standard errors. The analysis was conducted with STATA statistical software (v.12; College Station, TX).

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RESULTS

Descriptive Characteristics

Overall, 876 ART-naive participants completed the baseline survey and were included in the study. Most participants were female (71%), many had not completed primary school (79%), and severe food insecurity was common (66%, Table 1). The mean age was 39 (SD 9.6) years. The mean CD4 count was 338 (SD: 64) cells per microliter; 495 participants (57%) had a CD4 count ≤350 cells per microliter. Baseline Hb was available for 716 participants (82%); individuals who had Hb available did not differ meaningfully from those who were missing Hb data on most characteristics, although those who were missing Hb were more likely to be male (37% versus 27%), to live in an internally displaced camp (14% versus 8%), to live farther from the nearest market and hospital, and have a lower mean CD4 cell count (322 versus 342 cells/μL). The mean Hb among women and men was 12.2 (SD 1.5) and 13.4 (SD 2.0) g/dL, respectively. Overall, 55 participants (7.7%) met the definition for moderate anemia (Hb < 10 g/dL).

Table 1
Table 1
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The mean IDDS was 6.3 (SD 1.7) food groups per day, with a mean of 2.7 (SD 1.1) nutrient-rich food groups per day, a mean of 1.5 (SD 0.5) cereals, roots, and tubers groups per day, and a mean of 2.1 (SD 0.8) oils, fats, sugars, and condiment groups per day. Overall, 197 participants (22%) consumed a high level of nutrient-rich foods (4–7 groups/d) at baseline. Participants who reported high consumption levels of nutrient-rich foods were more often from Soroti and were more likely to be married, be better educated, be more food secure, have higher per capita expenditures, and have higher CD4 cell counts (Table 1).

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Relationship Between Dietary Diversity and Baseline CD4 Count

In OLS and logistic models, IDDS was not associated with CD4 count (either continuous or CD4 count ≤ 350, Table 2). However, when disaggregated into the 3 subcategories of food groups, we found a strong association between consumption of nutrient-rich food groups and CD4 count in both unadjusted and adjusted models. Every additional nutrient-rich food group consumed was associated with a 6 CD4 cell per microliter increase (model 2, β = 6.43, SE = 2.25). In the adjusted logistic model (model 4), each additional nutrient-rich food group consumed was associated with a 16% reduction in the likelihood of having a CD4 count ≤350 cells per microliter (ORa, 0.84; 95% CI: 0.72 to 0.97). Individuals who consumed high levels of nutrient-rich food groups had, on average, 18 CD4 cells per microliter higher than those with low consumption levels of nutrient-rich food groups (adjusted predicted mean, 352 versus 334 cells/μL; P < 0.01; Fig. 1). Consumption of cereals or oils and fats was not associated with baseline CD4 count in adjusted models.

Table 2
Table 2
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Figure 1
Figure 1
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Relationship Between Dietary Diversity and Moderate Anemia

IDDS was not associated with moderate anemia in bivariable or multivariable models among individuals with CD4 count >350 or ≤350 cells per microliter (Table 3). When disaggregated, we found a strong association between consumption of nutrient-rich food groups and moderate anemia among individuals with CD4 count >350 cells per microliter but not among individuals with ≤350 cells per microliter. In the higher CD4 category, consumption of nutrient-rich food groups was associated with a lower odds of moderate anemia (ORa, 0.57; 95% CI: 0.34 to 0.96) and consumption of oils and fats was associated with a higher odds of moderate anemia (ORa, 2.04; 95% CI: 1.08 to 3.86). Consumption of cereals was not associated with moderate anemia (ORa, 2.12; 95% CI: 0.76 to 5.90).

Table 3
Table 3
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Relationship Between Dietary Diversity and Mortality

Of the 876 participants completing the baseline survey, 852 (97.3%) were included in the mortality analysis [we excluded 19 participants (2.1%) who were lost to follow-up and 5 participants (0.5%) who initiated ART during follow-up but who had unknown ART start dates]. These 852 participants contributed 1534 person-years of follow-up with a mean follow-up period of 21.6 months (range, 0.33–39.3 months).

Forty-eight participants (5.6%) died during follow-up for a mortality rate of 3.1 per 100 person-years. Only 6 deaths (13%) occurred among participants who consumed high levels of nutrient-rich foods (4–7 groups/d). Thus, we examined the effect of the overall baseline IDDS score on mortality rather than disaggregated by subgroup. IDDS was associated with mortality in both unadjusted (HR, 0.80; 95% CI: 0.69 to 0.93) and adjusted models with the 3-level anemia status (HRa, 0.76; 95% CI: 0.63 to 0.91). The effect estimate was similar when anemia status was excluded (HRa, 0.79; 95% CI: 0.65 to 0.94).

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DISCUSSION

In this study of 876 ART-naive PLHIV in Uganda, our baseline cross-sectional analysis revealed that consumption of nutrient-rich food groups was positively associated with higher CD4 cell counts and, among those with CD4 counts between 350 and 450 cells per microliter, inversely associated with moderate anemia. We also found that baseline dietary diversity was protective against mortality during the 22-month follow-up period. Taken together, these data suggest that consumption of a nutrient-rich diet may be an important determinant of HIV disease severity and progression before ART initiation.

The role of nutrition in health and disease is well established.23 Poor nutrient status among PLHIV, especially micronutrient deficiencies, leads to immunosuppression, oxidative stress, and the subsequent acceleration of HIV replication and CD4 T-cell depletion.24 Furthermore, although the causes of anemia are multifactorial, including iron deficiency, infections, and blood disorders, it is widely recognized that anemia is a major consequence of HIV infection and is strongly associated with disease progression and mortality.25 Although we were unable to characterize the cause of anemia in our study, the differential association we observed between dietary diversity and moderate anemia by level of immunosuppression is likely related to the nature of anemia in PLHIV. Nutritional deficiencies possibly comprise a larger attributable fraction for anemia in individuals with less advanced HIV disease (defined as CD4 counts > 350 cells per microliter in this study), when anemia is less affected by HIV infection. When immunosuppression is more severe, HIV infection may play a larger role in the development of anemia than nutritional deficiencies, even though nutritional deficiencies remain common.

The HIV/AIDS epidemic has had a devastating impact on health in sub-Saharan Africa and has also had harmful effects on food security and diet quality among households affected by HIV/AIDS. Competing demands for essential goods heightens the risk of food insecurity, as PLHIV must make difficult choices between essential goods like food and medications.10,26 In addition, the consequences of HIV infection itself, including anemia and iron deficiency, may reduce the capacity for physical labor, further increasing the risk of food insecurity.27 For example, in rural areas, the HIV epidemic compromises food security through debilitation of the agricultural labor force, reduced crop variety, and reduced cultivated land area.28–30 Reducing dietary diversity is one coping strategy in response to these stresses,31 consistent with the predictable patterns of loss management that households use to alleviate the deleterious effects of shocks.32 For example, when facing a real or potential shock, households typically stabilize their consumption of staples (grains or tubers) and reduce consumption of more nutrient-dense foods like eggs, vegetables, meat, and diary.33,34 In rural Uganda, dietary diversity is poor with an overreliance on starchy staple foods; relatively high consumption of energy-dense sugars, oils, and fats; and a very low, almost negligible, consumption of nutrient-rich animal source foods.35 The results from this study underscore the importance of ensuring high-quality diets for PLHIV, especially in resource-limited settings where the vicious cycle of HIV/AIDS and food insecurity is the most acute.

In theory, food-related interventions for PLHIV have the potential to interrupt the pathways through which food insecurity and poor diet quality undermine the health of HIV-infected individuals.36 However, the appropriate intervention to help PLHIV achieve more diverse diets depends on the level of vulnerability and whether the need is for the short or long term. For example, assistance in the form of food, food vouchers, or cash is an important short-term response to tackle undernutrition and improve ART response. Several studies have found positive effects of food supplementation on ART adherence and HIV clinical outcomes,37–40 and WFP currently provides food and nutrition support to more than 1.4 million food insecure and malnourished people living with and affected by HIV.41 Although the immediate goal of such programs is to manage malnutrition, a secondary goal is to facilitate labor force participation and future food security. More research is needed to understand which assistance modalities improve clinical and economic outcomes and under what conditions. In Ecuador, for example, a recent impact evaluation of 3 different modalities of WFP transfers—food, cash, and vouchers—given to Columbian refugees found that voucher transfers led to the greatest increases in household dietary diversity.42 However, no equivalent data exist on the comparative effectiveness of different transfer types among HIV-infected populations.

However, although short-term aid in the form of food, vouchers, or cash provides critical short-term support, livelihood interventions and social protection schemes (including long-term cash transfers) aim to sustainably enhance food security and improve diet quality. These programs may have a greater chance of achieving long-term improvements by addressing the numerous upstream pathways through which food insecurity and poor diet quality negatively impacts health.43 Livelihood strategies integrate HIV care with income-generating programs, typically supporting clients in small enterprise activities, agricultural production, or animal husbandry.44 A prime target for such livelihood programs is the support of smallholder agriculture, which is inextricably linked to poverty and food security in the developing world.45–48 The goal of all such programs is to mitigate the effects of chronic food insecurity and increase access to nutrient-dense foods, whether through agriculture or increased income to purchase food.

As with all observational studies, this study is subject to important limitations. This study uses baseline data of a WFP evaluation and was not designed to determine the effect of dietary diversity on HIV disease severity or mortality. Furthermore, the analyses of dietary diversity and CD4 cell count and anemia were cross-sectional and we cannot make inferences about the direction of effect (ie, temporality) or causation. In all of our models, there may be unmeasured confounders and endogeneity of dietary diversity that would bias our estimates of effect; this must be considered when interpreting the results. In addition, although it would have been useful to disaggregate nutrient-rich food by plant and animal sources, we could not do so due to the limited range in the diversity score of animal source foods. Baseline anemia data were only available for a subset of participants; however, participants with missing Hb data only differed from those with Hb data on a few characteristics that were adjusted for in all models. Finally, only 6 deaths occurred among participants with higher consumption levels of nutrient-rich foods, so we could only examine the association of dietary diversity (overall) with mortality rather than with disaggregated subgroups of food types.

Our study also has significant strengths, including a large sample size, the use of a validated measure of dietary diversity, and prospective data on mortality. Furthermore, although food security has previously been shown to influence HIV disease severity, to our knowledge, this represents the first study to demonstrate an association between nutrient-rich food consumption and HIV disease severity and mortality. Our findings demonstrate the importance of diet quality to the health of PLHIV, an important contribution considering that WFP, World Health Organization, the Joint United Nations Programme on HIV/AIDS, and the United States President's Emergency Plan for AIDS Relief have recommended integration of interventions to improve nutrition security into AIDS care and treatment programs.1,2,49 Our data may help to guide the types of food assistance provided and essential elements of nutrition education and counseling that increase the likelihood of improving dietary diversity. In addition, our findings highlight the need for future research to determine the most cost-effective approaches to improve diet quality in both the short and long terms.

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Keywords:

HIV infection; dietary diversity; CD4; mortality; Uganda

© 2013 Lippincott Williams & Wilkins, Inc.

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