Skip to main content
BMC Nutrition logoLink to BMC Nutrition
. 2017 Aug 3;3:58. doi: 10.1186/s40795-017-0180-0

High magnitude of under nutrition among HIV infected adults who have not started ART in Tanzania--a call to include nutrition care and treatment in the test and treat model

Bruno F Sunguya 1,, Nzovu K Ulenga 2, Hellen Siril 2, Sarah Puryear 4, Eric Aris 2, Expeditho Mtisi 3, Edith Tarimo 1, David P Urassa 1, Wafaie Fawzi 5, Ferdnand Mugusi 1
PMCID: PMC7050693  PMID: 32153838

Abstract

Background

Undernutrition among people living with HIV (PLWHIV) can be ameliorated if nutrition specific and sensitive interventions are integrated into their HIV care and treatment centers (CTC). Integrated care is lacking despite expansion of antiretroviral therapy (ART) coverage, representing a substantial missed opportunity. This research aims to examine nutritional status and associated risk factors among HIV-positive adults prior to ART initiation in Tanzania in order to characterize existing gaps and inform early integration of nutrition care into CTC.

Methods

We analyzed data from 3993 pre-ART adults living with HIV enrolled in CTCs within the Trial of Vitamin (TOV3) and progression of HIV/AIDS study in Dar es salaam, Tanzania. The primary outcome for this analysis was undernutrition, measured as body mass index (BMI) below 18.5 kg/m2. We conducted descriptive analyses of baseline characteristics and utilized multiple logistic regression to determine independent factors associated with pre-ART undernutrition.

Results

Undernutrition was prevalent in about 27.7% of pre-ART adults, with a significantly higher magnitude among males compared to females (30% vs. 26.6%, p < 0.025). Severe undernutrition (BMI < 16.0 kg/m2) was prevalent in one in four persons, with a trend toward higher magnitudes among females (26.2% vs. 21.1% p = 0.123). Undernutrition was also more prevalent among younger adults (p < 0.001), those with lower wealth quintiles (p = 0.003), and those with advanced HIV clinical stage (p < 0.001). Pre-ART adults presented with poor feeding practices, hallmarked by low dietary diversity scores and infrequent consumption of proteins, vegetables, and fruits. After adjusting for confounders and important co-variates, pre-ART undernutrition was associated with younger age, low wealth indices, advanced clinical stage, and low dietary diversity.

Conclusions

One in every four pre-ART PLWHIV presented with undernutrition in Dar es salaam, Tanzania. Risk factors for undernourishment included younger age, lower household income, advanced HIV clinical stage, and lower dietary diversity score. Knowledge of the prevalence and prevailing risk factors for undernutrition among pre-ART PLWHIV should guide targeted, early integration of nutrition interventions into routine HIV care and treatment in high-prevalence, low-income settings such as Tanzania.

Keywords: Undernutrition, Antiretroviral therapy, Nutrition care, And integrated care

Background

Massive gains have been achieved in the fight against HIV/AIDS owing to the global efforts in rolling out effective interventions [1]. These include treatment with potent antiretroviral drugs, strategies to prevent mother to child transmission, advocacy, and other behavior modification interventions. Such interventions have led to a significant decline in HIV prevalence in the most affected countries in sub Saharan Africa—Tanzania is no exception [2]. For example, the prevalence of HIV among adults aged 15–49 in Tanzania has declined from 7.0% in 2004 [3] to 5.3% in 2012 [4], and 4.7% in 2015. Moreover, the incidence of the disease has also declined to below 1% of the general population [5].

The decline in HIV prevalence in Tanzania is partially attributable to increased ART coverage. The cumulative number of people on ART in Tanzania increased by 50% in only 1 year between 2011 to 2012 [4]. By 2015, about 47.6% of people living with HIV (PLWHIV) were on ART [5]. However, even with such efforts, HIV case fatality rate has remained high. A total of 47,860 people died of disease in 2015 alone [5]. Such poor treatment outcomes have been attributed to poor viral suppression, continued immune suppression, poor nutritional status, opportunistic infections, and non-communicable diseases owing to chronic HIV/AIDS [6]. Tailor-made interventions are therefore needed to address modifiable factors and should be integrated into their routine HIV care and treatment.

Improving nutritional status may be an entry point in addressing many other risk factors among PLWHIV. Evidence has shown that food insecurity results in poor outcomes among PLWHIV [7]. The most commonly demonstrated negative outcomes have been nutritional status, adherence to medication, and psychological wellbeing [8]. In Tanzania, poor feeding practices are widespread and have been associated with undernutrition [9, 10]. Despite this evidence, nutrition integrated HIV care is lacking in Tanzania, representing a substantial missed opportunity. Beginning in 2016, the country adopted the test and treat strategy for HIV, which will result in more people on ART and longer durations of treatment. For this strategy to attain its desired effects, HIV-positive adults should also be provided with nutrition care and treatment that is integrated into their routine HIV care and treatment.

To design tailor made interventions for adults living with HIV, it is essential to understand the magnitudes and factors associated with undernutrition in Tanzania. Such evidence has not been published. The aim of the current study was therefore, first, to examine magnitudes and severity of undernutrition among adults enrolled for ART services. The second aim was to examine determinants of undernutrition in such population. Results from this study aimed to inform the HIV/AIDS program on the needs to integrate other important but left out services to improve treatment outcomes among adults attending care and treatment services in Tanzania and countries with similar HIV/AIDS landscape.

Methods

Study design

This cross-sectional study analyzed secondary data of the baseline phase of a randomized double-blind controlled trial on the efficacy of multivitamins on disease progression among HIV-positive adults in Dar es salaam, Tanzania—the TOV3 trial. We used this data to study ART-naïve adults so as to inform of the needs for integrated nutrition care on ART services. The trial aimed at recruiting a total of 4000 randomized into two intervention arms. Data were collected before ART initiation and the participants were followed for 5 years.

Study settings

Participants were recruited from seven HIV care and treatment clinics (CTCs). At the time of study preparation, Highly Active Antiretroviral Therapy (HAART) was provided under the Tanzania National AIDS Control Program with the support of the President’s Emergency Plan for AIDS Relief program and in collaboration with the Harvard School of Public Health, Muhimbili University of Health and Allied Sciences, and the City of Dar es Salaam Regional Office of Health in only seven CTCs. Those CTCs were Infectious Disease Center (IDC), Buguruni, Mwananyamala, Temeke, Mbagala-Rangitatu, Amana, and Sinza CTCs. A CTC is the primary health facility for care and treatment of PLWHIV. Therefore, all CTCs were included as study sites for the TOV3 study. HIV-positive individuals are referred to the CTCs after testing positive in the community, voluntary care and treatment facilities, or any other health facility.

Population and sampling

The TOV3 study included all confirmed HIV-positive patients who had not started ART and consented to participate. Participant eligibility was determined at the first CTC visit. HIV status was confirmed using two licensed HIV-1 Enzyme-linked immunosorbent assay (ELISA) or two rapid tests, and discordant results were verified via Western Blot. Exclusion criteria included individuals aged below 18 years, and those who would be on transit. For the current paper, we selected adult participants with no missing outcome variables of interest.

Measurements

The outcome variable of interest in the current study was undernutrition measured through BMI in kg/m2. BMIs were calculated based on height and weight at the first study visit. Undernutrition was defined as BMI of less than 18.5 kg/m2. Severity of undernutrition was further classified into severe (BMI < 16 kg/m2), moderate (BMI 16 to <17 kg/m2) and mild (BMI 17 to <18.5 kg/m2).

Independent variables included socio-demographic characteristics, feeding practices variables, psychosocial variables, and HIV clinical stage. For demographic characteristics, variables included age (in years), sex, the highest attained level of education, and socio economic status. Dietary characteristics included dietary diversity score. Psychosocial variables included emotional distress score and depression score. We used the World Health Organization’s HIV clinical classification to assess the disease progression at the time of recruitment.

Education level was categorized into primary school incomplete, primary school complete, secondary school attended, and advanced education attended. Age in years was divided into quintiles to distribute the age groups evenly. Economic status was assessed using weighted wealth index. It incorporated household assets ownership, housing characteristics, fuel for lighting and cooking, type of toilet, source of water, and feeding characteristics. Dichotomous variables were constructed and factor analysis using principle component analysis (PCA) was used to reduce 31 items to 14 in component one to three. These were the most important components before the hinge of the scree plot. Factor loadings were used as item weights totaled to yield the wealth index for each household. It was then divided into quintiles designating lowest (−1.56–1.40), low (1.41–2.19), middle (2.20–2.71), high (2.72–3.50) and highest (3.51–4.85) quintiles of the economic status.

Dietary diversity scores were calculated by summing the number of food groups consumed in the day that preceded the enrolment. It was used as a continuous variable and a categorical variable. For the categorical variable, dietary diversity score below three was considered low. Food groups assigned were starch or carbohydrate, any protein, animal protein, plant protein, green vegetables, and fruits. Categorical variables were made for each food groups as none, once, 2–3, and 4 and above times a day.

We measured emotional distress using the Hopkins Symptom Checklist (HSCL), which assigns scores for depression (15 items) and anxiety (10 items). In the current study, the 15-item depression scale had a Cronbach’s alpha of 0.9168. The Cronbach’s alpha for the 10-item anxiety scale was 0.8871. The 25-item HCL checklist had a Cronbach’s alpha of 0.9333. Finally, we used the WHO clinical HIV classification to stage the disease progress among the enrollees. Stage one and two are the early stages whereas three and four signify advanced disease.

Data analysis

Descriptive and regression analyses were used. Chi-square test was used to compare the characteristics of participants by gender and nutritional status for categorical variables. T-test was used for continuous variables. We conducted bivariate logistic regression to examine the associations between each independent variable and undernutrition. Statistical associations with p-values below or equal to 0.2 were entered into a multiple logistic regression model to find factors associated with undernutrition after adjusting for confounders and important covariates. Social support and emotional distress were not entered into the model because of their high correlations with depression score. Statistical significance was set at the p-value < 0.05. Missing variables were excluded as cases during regression analyses when the variables introduced into the modules were being analyzed. Analyses were conducted using Stata version 13.

Ethical consideration

The current study utilized data from the Trial of Vitamin study (TOV3) that observed all ethical guidelines. The parent study was approved by the Institutional Review Board of the National Medical Research Institute (NIMR), Muhimbili University of Health and Allied Sciences (MUHAS), and the Harvard School of Public Health. Participants were assured of confidentiality and anonymity throughout the process and for all reports and publications generated. A written consent was obtained after the participants were explained about the study and agree to voluntarily participate. Participation was voluntary and there were no implications for care at the CTC upon refusal to participate.

Results

Data of 3993 HIV-positive adults were available for analyses. Of them, 1268 (31.8) were male. The mean age at enrolment to the TOV3 study was 38.0 years, sd. 8.6.

General characteristics

Male participants had a higher mean age in years compared to their female counterparts (40.9 vs. 36.7, p < 0.001). Table 1 shows participants’ characteristics. A higher proportion of male participants had higher weighted wealth index compared to female. For example, only 15.2% of males were in the lowest wealth quintile compared to 22.1% of female participants (P < 0.001). Highest attained level of education was also different across the gender profiles. There was no difference in the proportion of participants with the primary level of education (p = 0.949). However, a higher proportion of male participants had attended any secondary school class compared to females (51.8% vs. 40.2%, p = 0.001) and a similar trend was found for advanced schooling (29.6% vs. 17.7%, p < 0.001).

Table 1.

General characteristics of TOV study participants

Variable Male Female Total p
N (x̅) % (SD) N (x̅) %(SD) N %
Socio-demographic characteristics
 Wealth index
  Lowest 151 15.2 498 22.1 649 20.0 <0.001
  Low 177 17.82 480 21.3 657 20.2
  Middle 242 24.4 492 21.8 734 22.6
  High 215 21.7 413 18.3 628 19.4
  Highest 208 20.9 370 16.5 578 17.8
 Primary school
  Completed 743 86.5 1659 86.4 2402 86.4 0.949
  Not completed 116 13.5 261 13.6 377 13.6
 Secondary education
  Any class 170 51.8 254 40.2 424 44.2 0.001
  None 158 48.2 378 59.8 536 55.8
 Advanced schooling
  Any level 73 29.6 89 17.7 162 21.6 <0.001
  None 174 70.4 415 82.3 589 78.4
Nutritional status (BMI)
 Nutritional status
  Underweight 380 30.0 724 26.6 1104 27.7 <0.001
  Normal 769 60.7 1506 55.3 2275 57.0
  Overweight 119 9.3 495 18.1 614 15.3
 Severity of undernutrition
  Severe 80 21.1 190 26.2 270 24.4 0.123
  Moderate 81 21.3 157 21.7 238 21.6
  Mild 219 57.6 377 52.1 596 54.0
Feeding practices
 Dietary diversity
  Mean (2.94) (0.05) (2.94) (0.03) 0.424
  DDS < 3 459 46.2 985 46.1 1444 46.1 0.945
  DDS > =3 534 53.8 1152 53.9 1686 53.9
 Any starchy
  None 93 9.5 182 8.5 275 8.8
  Once 833 83.9 1782 83.4 2615 83.6 0.294
  2–3 56 5.6 155 7.2 211 6.7
  4 and above 11 1.0 18 0.9 29 0.9
 Any protein
  None 299 30.1 677 31.7 976 31.2
  Once 647 65.2 1355 63.4 2002 64.0 0.367
  2–3 35 3.5 89 4.1 124 3.9
  4 and above 12 1.2 16 0.8 28 0.9
 Any Animal protein
  None 313 31.5 711 33.3 1024 32.7
  Once 634 63.9 1332 62.3 1966 62.8 0.180
  2–3 34 3.4 82 3.8 116 3.7
  4 and above 12 1.2 12 0.6 24 0.8
 Any other protein
  None 870 87.6 1884 88.2 2754 88.0
  Once 119 12.0 228 10.7 347 11.1 0.144
  2–3 3 0.3 20 0.9 23 0.7
  4 and above 1 0.1 5 0.2 6 0.2
 Any green vegetables
  None 605 60.9 1265 59.2 1870 59.8
  Once 350 35.3 778 36.4 1128 36.0 0.673
  2–3 31 3.1 81 3.8 112 3.6
  4 and above 7 0.7 13 0.6 20 0.6
 Any fruits
  None 456 47.9 999 46.8 1455 46.5
  Once 470 47.3 979 45.8 1449 46.3 0.348
  2–3 51 5.2 135 6.3 186 5.9
  4 and above 16 1.6 24 1.1 40 1.3

A total of 1104 (27.7%) had a BMI score below 18.5 kg/m2. A higher proportion of them were male compared to female participants (30.0% vs. 26.6%, p < 0.001. Of those with undernutrition, 24.4% were severe while 21.6% were moderate and 54.0% were mild.

The mean dietary diversity score was 2.94 for both sexes. About 46.1% of all patients consumed less than 3 different types of foods in the day that preceded the interview. As high as 91.2% of recruited clients consumed starchy foods at least once in the previous day, while only 68% consumed any type of food with protein at least once during the same period. Animal sources of protein were consumed by about 67% of those interviewed; only 12% reported consuming plant related protein-contained foods. About 60% did not consume any green vegetables and 46.5% did not consume any type of fruit.

Descriptive characteristics according to nutritional status

Table 2 displays the results of descriptive analyses stratified by undernutrition. Younger age was associated with undernutrition. Mean age among individuals with undernutrition was lower compared to those with normal or higher BMI (37.14 sd. 8.59 vs. 38.61 sd. 8.61, p < 0.001). The trend of undernutrition was such that, young ages had higher magnitudes of undernutrition compared to higher age groups, p = 0.003. Women had a lower magnitude of undernutrition compared to their male counterparts (30.0% vs. 26.6%, p = 0.025). As expected, wealth index was associated with undernutrition. The lower weighted wealth index quintiles had higher magnitudes of undernutrition, while as the weighted wealth index increased, the BMI tended to increase, p < 0.001.

Table 2.

Descriptive analyses, BMI as outcome variable

Variable BMI < 18.5 BMI > =18.5 Total p
N (x̅) % (SD) N (x̅) %(SD) N %
Age (mean years) (37.14) (8.59) (38.32) (8.61) 3999 <0.001
Age (years)
 18.47–30.65 249 22.6 551 19.0 800 20.0 0.003
 30.66–34.96 234 21.2 566 19.6 800 20.0
 34.97–39.07 231 20.9 569 19.7 800 20.0
 39.08–44.80 204 18.5 596 20.6 800 20.0
 44.80–83.35 186 16.8 613 20.1 799 20.0
Sex
 Male 380 30.0 888 70.0 1268 31.8 0.025
 Female 724 26.6 2001 73.4 2725 68.2
Wealth index
 Lowest 217 26.6 434 17.8 651 20.0 <0.001
 Low 196 24.0 462 19.0 658 20.2
 Middle 175 21.5 560 23.0 735 22.6
 High 123 15.1 506 20.8 629 19.4
 Highest 105 12.8 473 19.4 578 17.8
Emotional distress (1.29) (0.43) (1.25) (0.39) 3055 0.019
Depression score (1.35) (0.52) (1.30) (0.48) 0.010
Depression
 Yes 779 70.4 1849 63.6 2628 65.5 <0.001
 No 327 29.6 1057 36.4 1384 34.5
Social support (25.37) (8.00) (25.07) (8.39) 3154 0.381
Alcohol dependency
 Yes 4 1.4 17 2.1 21 1.9 0.005
 No 290 98.6 797 97.9 1091 98.1
HIV clinical stage
 Stage 1 12 1.2 181 6.8 193 5.3 <0.001
 Stage 2 112 11.1 522 19.5 634 17.2
 Stage 3 599 59.4 1701 63.8 2300 62.6
 Stage 4 285 28.3 264 9.9 549 14.9
Dietary diversity
 Mean (2.90) (1.56) (2.97) (1.61) 3137 0.280
 DDS < 3 399 48.7 1050 45.3 1449 46.2 0.099
 DDS > =3 421 51.3 1267 54.7 1688 53.8

There were significant differences in psychosocial variables among those with low compared to those with normal or higher BMI. For example, mean emotional distress was higher among individuals with undernutrition compared with their counterparts (1.29 sd. 0.43 vs. 1.25 sd. 0.39, p = 0.019). Mean score in the depression scale was also higher among individuals with undernutrition compared to their counterparts (1.35 sd. 0.52 vs. 1.30 sd. 0.48, p = 0.010). Magnitude of depression was high in this population. For example, about 65.5% of the enrolled HIV-positive individuals had depression symptoms. A higher proportion was among individuals with undernutrition compared to their counterparts (70.4% vs 63.6%, p < 0.001). There was no difference in social support indicators between individuals with or without undernutrition (p = 0.381). A total of 4 (1.4%) individuals with alcohol dependency had undernutrition compared to 17(2.1%) who had normal nutritional status (p = 0.005).

HIV clinical stage was also associated with undernutrition. For example, only 1.2% of individuals with stage 1 were underweight status compared to 59.4% of those with stage 3 and 28.3% of those with stage 4 disease. There was no statistically significant difference in dietary diversity among those with undernutrition and their counterparts, however, a lower proportion of those with undernutrition (89.6%) had not consumed any of the starchy foods.

Factors associated with undernutrition

Table 3 shows results of bivariate and multiple logistic regression analyses. At bivariate logistic regression analyses, association between age, sex, wealth index, depression, HIV clinical stage, and emotional distress with nutritional status reached a statistically significant level. Social support and alcohol dependency were not statistically significant in bivariate analyses. The multiple regression analysis model included all statistically significant variables, with the exception of emotional distress, which was excluded due to the high correlation with depression.

Table 3.

Logistic regression analyses on the factors associated with low BMI among the clients enrolled into the study

Variable Logistic regression Multiple logistic regression
OR 95% CI P-value AOR 95% CI P-value
Age (quintiles)
 18.47–30.65 1.00 1.00
 30.66–34.96 0.91 0.74–1.13 0.414 0.84 0.63–1.12 0.241
 34.97–39.07 0.90 0.73–1.11 0.326 0.84 0.63–1.13 0.259
 39.08–44.80 0.76 0.61–0.94 0.013 0.66 0.49–0.88 0.005
 44.80–83.35 0.67 0.54–0.84 <0.001 0.63 0.46–0.85 0.002
Sex
 Male 1.00 1.00
 Female 0.85 0.73–0.98 0.025 0.87 0.70–1.07 0.179
Wealth index
 Lowest 1.00 1.00
 Low 0.85 0.67–1.07 0.168 0.80 0.60–1.06 0.114
 Middle 0.63 0.49–0.79 <0.001 0.67 0.50–0.88 0.004
 High 0.49 0.38–0.63 <0.001 0.49 0.37–0.67 <0.001
 Highest 0.44 0.34–0.58 <0.001 0.46 0.34–0.63 <0.001
Depression 1.23 1.05–1.44 0.010 1.15 0.96–1.38 0.138
HIV clinical stage
 Stage 1 1.00 1.00
 Stage 2 3.24 1.74–6.01 <0.001 5.05 1.99–12.83 0.001
 Stage 3 5.31 2.94–9.58 <0.001 8.77 3.55–21.65 <0.001
 Stage 4 16.28 8.87–29.90 <0.001 22.90 9.08–57.75 <0.001
Dietary diversity
 DDS < 3 1.00 1.00
 DDS > =3 0.87 0.75–1.03 0.099 0.79 0.66–0.96 0.016
Alcohol dependency 0.63 0.21–1.90 0.414
Emotional distress 1.26 1.04–1.53 0.019
Social support 1.00 0.99–1.01 0.300

Compared to the first age quintile (below 30.6 years), those at the fourth quintile (39.1–44.8 years) were 34% less likely to have undernutrition (p = 0.005) after adjusted for other important confounders and covariates. Moreover, those at fifth age quintile (>44.8 years) were 37% less likely to have undernutrition compared to their counterparts in the first quintile of age (below 30.6 years), p = 0.002. Compared to HIV-positive males, females were 13% less likely to be underweight, but this association did not reach a statistically significant level (p = 0.179). Higher wealth index was also associated with better nutritional status. For example, after adjusting for confounders, individuals at middle wealth index were 33% less likely to have undernutrition compared with those at the lowest weighted wealth index (p = 0.004). Similarly, those at higher and highest wealth quintiles were 51% and 54% less likely to exhibit undernutrition compared with their counterparts at the lowest wealth index (p < 0.001).

The association between depression and undernutrition did not reach a statistical significant level. An increase in the HIV clinical stage was associated with higher magnitudes of undernutrition. For example, patients with HIV clinical stage two were five times more likely to have undernutrition compared to those with clinical stage 1 (p = 0.001). Those with HIV clinical stage 3 were 8.77 times more likely to be underweight compared to those with HIV clinical stage 1 (p < 0.001). Likewise, those at stage 4 were 22.90 times more likely to have undernutrition compared to those with stage 1 of the disease (p < 0.001). HIV-positive individuals who had a dietary diversity score of three or above were 21% less likely to be undernourished (p = 0.016).

Discussion

This study examined magnitudes of undernutrition among pre-ART HIV-positive adults in Dar es salaam, Tanzania. The study found that, more than one in every four of pre-ART adults had undernutrition measured as BMI below 18.5 kg/m2. Of them, one in four had a severe form of undernutrition reflected by a BMI below 16.0 kg/m2. Those with undernutrition were more likely to be of the younger age, low wealth index, advanced HIV clinical stage, and low dietary diversity score.

More than one in four pre-ART HIV-positive adults in Dar es salaam presented with undernutrition. Such unprecedented magnitude of undernutrition is not uncommon in this [9, 11] and other areas with similar context [12]. A syndemic theory can help explain such high magnitude of undernutrition in this context. First, the disease itself can exacerbate nutritional debilitation through high-energy expenditure, loss through fever, recurrence of opportunistic infections, including diarrheas that lead to emaciation of lean tissues. Secondly, HIV as a disease can subject the affected people to socio-economic disadvantages including food insecurity, poverty, and other challenges associated with undernutrition [13]. People living with HIV are therefore at a higher risk of undernutrition compared to their counterparts in the general population.

Despite such burden, to a large extent, nutrition care and treatment has not been integrated into most HIV care and treatment facilities [14]. Tanzania is no exception. With such magnitudes of undernutrition, HIV-positive individuals are likely to succumb to treatment failure, higher risk of opportunistic infections [15, 16], and even mortality [11, 12, 17]. Addressing undernutrition among adults is of paramount importance to attain treatment goals, especially in the new era of test and treat for all HIV-positive individuals.

In this study, undernutrition was associated with a number of modifiable factors. Like in other studies conducted in similar settings among HIV-positive children [9, 10], adults were more likely to succumb to undernutrition when they had poor feeding practices such as consuming foods with low dietary diversity. Moreover, only a small proportion consumed protein-rich foods, fruits, or vegetables in their routine meals, similar to other studies [1820]. Such low diversity diets predispose patients not only to macronutrient undernutrition but also to micronutrient deficits [8]. Poor feeding practices could also be associated with other social demographic disadvantages [21, 22]. Studies have revealed a link between poor feeding practices with food insecurity, poverty, and other social demographic characteristics [8]. However, in the context of Tanzania, even in areas with high yields of agricultural products, HIV-positive individuals succumb to selective food insecurity and therefore undernutrition [10]. Nutrition specific and sensitive interventions should be integrated within ART services to complement care for these populations [23]. Nutrition specific interventions include improving feeding practices such as frequency, diversity, and quantity. It also includes prevention and treatment of opportunistic infections leading to nutritional challenges such as diarrhea. Nutrition sensitive interventions include improving food insecurity, access to health care, poverty alleviation and education pertinent to food and nutrition.

Like in other contexts, undernutrition among pre-ART individuals was associated with low wealth index [10, 24]. Previous models have established associations between poverty and undernutrition, especially among PLWHIV [8]. For this specific population in Tanzania, such an association calls for establishment of a mechanism to identify those from poor households and to develop an innovative approach to alleviate the effects of poverty. In so doing, we can improve their undernutrition and, in turn, improve their HIV treatment outcomes [10]. Such poverty-alleviating interventions include conditional cash transfer [25, 26], small productivity groups, microfinancing of economic activities, and other livelihood programs [27, 28].

Advanced HIV clinical stage was also associated with undernutrition [12]. This should also be taken into consideration when patients are enrolled into care as they are more prone to mortality [12]. Early, integrated and innovative nutrition interventions can improve their outcomes and should be targeted at this vulnerable population.

To achieve better treatment outcomes, the results of this study emphasize the integration of nutrition care and treatment into HIV care and treatment [29, 30]. This should be done from the moment these individuals are enrolled into care and sustained throughout treatment to attain optimal results [31]. Individuals with depression were more likely to be undernourished in this study although not at the multivariate regression analyses. The high magnitude of depression also emphasizes the needs for integrated services to ameliorate HIV-positive individuals with psychological stress and depressive symptoms to further improve their quality of lives and treatment outcomes. Currently, HIV care and treatment centers do not possess such services in Tanzania.

Results of this study should be interpreted carefully owing to the following limitations. First, this was a secondary analysis of data originally collected for a trial of vitamins. It might therefore have failed to include all confounders that should have been controlled for, especially in regression analyses. Second, results of this study may not be generalizable to the entire country. However, they may be useful in areas with similar context as in Dar es Salaam. Third, we used atypical dietary diversity score. This could have introduced validity challenges of assessment of dietary diversity score of participants.

Conclusion

The fact that more than one in four pre-HAART HIV-positive adults in Dar es salaam, Tanzania presented with undernutrition in various severity implies nutrition care is needed hand in hand with scaling up of the test and treat strategy. Such unprecedented magnitude of undernutrition was associated with young age, advanced clinical stage, low wealth index, and low dietary diversity. To ameliorate undernutrition and improve treatment outcomes with ART, integration of nutrition and treatment into HIV care and treatment is of paramount importance in Dar es salaam, and areas with similar context.

Acknowledgements

Analysis and manuscript preparation for the current project was made possible by Afya Bora Consortium Fellowship, which is supported by the President’s Emergency Plan for AIDS Relief (PEPFAR) and the Office of AIDS Research (OAR) of the U.S. National Institutes of Health through funding to the University of Washington under Cooperative Agreement U91 HA06801 from the US Department of Health and Human Services, Health Resources and Services Administration (HRSA) Global HIV/AIDS Bureau.

Funding

Authors did not receive any grant for this particular analysis. However, the parent trial (TOV3) was sponsored by the National Institute of Health (NIH). The National Institute of Health had no role in the design, analysis or writing of this article. The first author was an Afya Bora Consortium (ABC) fellow under the Department of Global Health, University of Washington.

Availability of data and materials

The dataset used during and/or analyzed during the current study is not publicly available because it is still being used for other analyses in a research group. However, the dataset will be available from the corresponding author on reasonable request.

Abbreviations

ABC

Afya Bora Consortium

AIDS

Acquired immunodeficiency syndrome

ART

Antiretroviral therapy

BMI

Body Mass Index

CTC

Care and treatment center

ELISA

Enzyme-linked immunosorbent assay

HAART

Highly active antiretroviral therapy

HIV

Human Immunodeficiency Virus

MUHAS

Muhimbili University of Health and Allied Sciences

NIH

National Institute of Health

NIMR

National Institute of Medical Research

PLWHIV

People living with Human Immuno-deficiency Virus

Sd.

Standard deviation

TOV3

Trial of Vitamin 3

Authors’ contributions

BFS conceived the research questions, analyzed the data, and prepared the first manuscript. SP was involved in drafting the first manuscript. NKU was involved in conception and design of the study, and acquisition of data to be used. HS and EA were involved in drafting the first manuscript. EM was involved in data analysis. DPU and EAMT were involved in drafting the manuscript. WF and FM approved the use of the database, involved in analyses, and revised the manuscript. All authors read and approved the final version of the manuscript.

Ethics approval and consent to participate

The current study utilized data from the Trial of Vitamin study (TOV3) that observed all ethical guidelines. The parent study was approved by the Institutional Review Board of the National Medical Research Institute (NIMR), Muhimbili University of Health and Allied Sciences (MUHAS), and the Harvard School of Public Health. Participants were assured of confidentiality and anonymity throughout the process and for all reports and publications generated. A written consent was obtained after the participants were explained about the study and agree to voluntarily participate. TOV3 study was registered under ClinicalTrial.org with registration number: NCT00383669.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Bruno F. Sunguya, Phone: +255 685 217 272, Email: sunguya@gmail.com

Nzovu K. Ulenga, Email: nulenga@mdh-tz.org

Hellen Siril, Email: neemasiril@gmail.com.

Sarah Puryear, Email: sarah.puryear@gmail.com.

Eric Aris, Email: aeric@mdh-tz.org.

Expeditho Mtisi, Email: emtisi@gmail.com.

Edith Tarimo, Email: etarimo54@yahoo.co.uk.

David P. Urassa, Email: durassa2@yahoo.co.uk

Wafaie Fawzi, Email: mina@hsph.harvard.edu.

Ferdnand Mugusi, Email: fm.mugusi@gmail.com.

References

  • 1.UNAIDS. 90–90-90 An ambitious treatment target to help end the AIDS epidemic. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS); 2014.
  • 2.UNAIDS . UNAIDS Global Report 2013. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS); 2013. [Google Scholar]
  • 3.TACAIDS, ZAC, NBS, OCGS, ICF. Tanzania HIV/AIDS and Malaria Indicator Survey 2003–2004. Dar es salaam, Tanzania: TACAIDS, ZAC, NBS, OCGS, ICF International. Dar es salaam: Tanzania Commission for AIDS (TACAIDS), Zanzibar AIDS Commission (ZAC), national Bureau of Statistics (NBS), Office of the Chief Government Statistician (OCGS), ICF International; 2004.
  • 4.TACAIDS, ZAC, NBS, OCGS, ICF. Tanzania HIV/AIDS and Malaria Indicator Survey 2011–12. Dar es Salaam, Tanzania. Dar es Salaam: Tanzania Commission for AIDS (TACAIDS), Zanzibar AIDS Commission (ZAC), National Bureau of Statistics (NBS), Office of the Chief Government Statistician (OCGS), and ICF International; 2013.
  • 5.Wang H, Wolock TAC. Estimates of global, regional, and national incidence, prevalence, and mortality of HIV, 1980–2015: the Global Burden of Disease Study 2015. Lancet HIV. 2016;16(S2352–3018):30083–9. [DOI] [PMC free article] [PubMed]
  • 6.Anema A, Vogenthaler N, Frongillo EA, Kadiyala S, Weiser SD. Food insecurity and HIV/AIDS: current knowledge, gaps, and research priorities. Curr HIV/AIDS Rep. 2009;6(4):224–231. doi: 10.1007/s11904-009-0030-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Weiser SD, Fernandes KA, Brandson EK, Lima VD, Anema A, Bangsberg DR, Montaner JS, Hogg RS. The association between food insecurity and mortality among HIV-infected individuals on HAART. J Acquir Immune Defic Syndr. 2009;52(3):342–349. doi: 10.1097/QAI.0b013e3181b627c2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Weiser SD, Young SL, Cohen CR, Kushel MB, Tsai AC, Tien PC, Hatcher AM, Frongillo EA, Bangsberg DR. Conceptual framework for understanding the bidirectional links between food insecurity and HIV/AIDS. Am J Clin Nutr. 2011;94(6):1729S–1739S. doi: 10.3945/ajcn.111.012070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Sunguya BF, Poudel KC, Otsuka K, Yasuoka J, Mlunde LB, Urassa DP, Mkopi NP, Jimba M. Undernutrition among HIV-positive children in Dar es salaam, Tanzania: antiretroviral therapy alone is not enough. BMC Public Health. 2011;11:869. doi: 10.1186/1471-2458-11-869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Sunguya BF, Poudel KC, Mlunde LB, Urassa DP, Yasuoka J, Jimba M. Poor nutrition status and associated feeding practices among HIV-positive children in a food secure region in Tanzania: a call for tailored nutrition training. PLoS One. 2014;9(5):e98308. doi: 10.1371/journal.pone.0098308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Woodd SL, Kelly P, Koethe JR, Praygod G, Rehman AM, Chisenga M, Siame J, Heimburger DC, Friis H, Filteau S. Risk factors for mortality among malnourished HIV-infected adults eligible for antiretroviral therapy. BMC Infect Dis. 2016;16(1):562. doi: 10.1186/s12879-016-1894-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Tesfamariam K, Baraki N, Kedir H. Pre-ART nutritional status and its association with mortality in adult patients enrolled on ART at fiche Hospital in North Shoa, Oromia region, Ethiopia: a retrospective cohort study. BMC Res Notes. 2016;9(1):512. doi: 10.1186/s13104-016-2313-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Himmelgreen DA, Romero-Daza N, Turkon D, Watson S, Okello-Uma I, Sellen D. Addressing the HIV/AIDS-food insecurity syndemic in sub-Saharan Africa. Afr J AIDS Res. 2009;8(4):401–412. doi: 10.2989/AJAR.2009.8.4.4.1041. [DOI] [PubMed] [Google Scholar]
  • 14.Sint TT, Lovich R, Hammond W, Kim M, Melillo S, Lu L, Ching P, Marcy J, Rollins N, Koumans EH, et al. Challenges in infant and young child nutrition in the context of HIV. AIDS. 2013;27(Suppl 2):S169–S177. doi: 10.1097/QAD.0000000000000089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Weiser SD, Hatcher A, Frongillo EA, Guzman D, Riley ED, Bangsberg DR, Kushel MB. Food insecurity is associated with greater acute care utilization among HIV-infected homeless and marginally housed individuals in San Francisco. J Gen Intern Med. 2013;28(1):91-8. [DOI] [PMC free article] [PubMed]
  • 16.Ford N, Shubber Z, Meintjes G, Grinsztejn B, Eholie S, Mills EJ, Davies MA, Vitoria M, Penazzato M, Nsanzimana S, et al. Causes of hospital admission among people living with HIV worldwide: a systematic review and meta-analysis. Lancet HIV. 2015;2(10):e438–e444. doi: 10.1016/S2352-3018(15)00137-X. [DOI] [PubMed] [Google Scholar]
  • 17.Hussen S, Belachew T, Hussien N. Nutritional status and its effect on treatment outcome among HIV infected clients receiving HAART in Ethiopia: a cohort study. AIDS Res Ther. 2016;13:32. doi: 10.1186/s12981-016-0116-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Mpontshane N, Van den Broeck J, Chhagan M, Luabeya KK, Johnson A, Bennish ML. HIV infection is associated with decreased dietary diversity in south African children. J Nutr. 2008;138(9):1705–1711. doi: 10.1093/jn/138.9.1705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Kadiyala S, Rawat R. Food access and diet quality independently predict nutritional status among people living with HIV in Uganda. Public Health Nutr. 2012:1–7. [DOI] [PMC free article] [PubMed]
  • 20.Rawat R, McCoy S, Kadiyala S. Poor diet quality is associated with low CD4 count and anemia and predicts mortality among antiretroviral therapy-naive HIV-positive adults in Uganda. J Acquir Immune Defic Syndr. 2012;62(2):246–253. doi: 10.1097/QAI.0b013e3182797363. [DOI] [PubMed] [Google Scholar]
  • 21.Miller CL, Bangsberg DR, Tuller DM, Senkungu J, Kawuma A, Frongillo EA, Weiser SD. Food insecurity and sexual risk in an HIV endemic community in Uganda. AIDS Behav. 2011;15(7):1512–1519. doi: 10.1007/s10461-010-9693-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.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. 2012;24(6):728–736. doi: 10.1080/09540121.2011.630358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Gillespie S, Haddad L, Mannar V, Menon P, Nisbett N, Group MaCNS The politics of reducing malnutrition: building commitment and accelerating progress. Lancet. 2013;382(9891):552–569. doi: 10.1016/S0140-6736(13)60842-9. [DOI] [PubMed] [Google Scholar]
  • 24.Oldewage-Theron WH, Dicks EG, Napier CE. Poverty, household food insecurity and nutrition: coping strategies in an informal settlement in the Vaal triangle, South Africa. Public Health. 2006;120(9):795–804. doi: 10.1016/j.puhe.2006.02.009. [DOI] [PubMed] [Google Scholar]
  • 25.Adato M, Bassett L. Social protection to support vulnerable children and families: the potential of cash transfers to protect education, health and nutrition. AIDS Care. 2009;21(Suppl 1):60–75. doi: 10.1080/09540120903112351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.McCoy SI, Njau PF, Czaicki NL, Kadiyala S, Jewell NP, Dow WH, Padian NS. Rationale and design of a randomized study of short-term food and cash assistance to improve adherence to antiretroviral therapy among food insecure HIV-infected adults in Tanzania. BMC Infect Dis. 2015;15:490. doi: 10.1186/s12879-015-1186-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Rawat R, Faust E, Maluccio JA, Kadiyala S. The impact of a food assistance program on nutritional status, disease progression, and food security among people living with HIV in Uganda. J Acquir Immune Defic Syndr. 2014;66(1):e15–e22. doi: 10.1097/QAI.0000000000000079. [DOI] [PubMed] [Google Scholar]
  • 28.Yager JE, Kadiyala S, Weiser SD. HIV/AIDS, food supplementation and livelihood programs in Uganda: a way forward? PLoS One. 2011;6(10):e26117. doi: 10.1371/journal.pone.0026117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Byron E, Gillespie S, Nangami M. Integrating nutrition security with treatment of people living with HIV: lessons from Kenya. Food Nutr Bull. 2008;29(2):87–97. doi: 10.1177/156482650802900202. [DOI] [PubMed] [Google Scholar]
  • 30.Lindegren ML, Kennedy CE, Bain-Brickley D, Azman H, Creanga AA, Butler LM, Spaulding AB, Horvath T, Kennedy GE. Integration of HIV/AIDS services with maternal, neonatal and child health, nutrition, and family planning services. Cochrane Database Syst Rev. 2012(9):CD010119. [DOI] [PubMed]
  • 31.Scarcella P, Buonomo E, Zimba I, Doro Altan AM, Germano P, Palombi L, Marazzi MC. The impact of integrating food supplementation, nutritional education and HAART (highly active antiretroviral therapy) on the nutritional status of patients living with HIV/AIDS in Mozambique: results from the DREAM Programme. Ig Sanita Pubbl. 2011;67(1):41–52. [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The dataset used during and/or analyzed during the current study is not publicly available because it is still being used for other analyses in a research group. However, the dataset will be available from the corresponding author on reasonable request.


Articles from BMC nutrition are provided here courtesy of BMC

RESOURCES