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Background: The prevalence of HIV/AIDS has exacerbated the impact of childhood undernutrition in many developing countries, including Tanzania. Even with the provision of antiretroviral therapy, undernutrition among HIV-positive children remains a serious problem. Most studies to examine risk factors for undernutrition have been limited to the general population and ART-naive HIV-positive children, making it difficult to generalize findings to ART-treated HIV-positive children. The objectives of this study were thus to compare the proportions of undernutrition among ART-treated HIV-positive and HIV-negative children and to examine factors associated with undernutrition among ART-treated HIV-positive children in Dar es Salaam, Tanzania. Methods. From September to October 2010, we conducted a cross-sectional survey among 213 ART-treated HIV-positive and 202 HIV-negative children in Dar es Salaam, Tanzania. We measured the children’s anthropometrics, socio-demographic factors, food security, dietary habits, diarrhea episodes, economic status, and HIV clinical stage. Data were analyzed using both univariate and multivariate methods. Results: ART-treated HIV-positive children had higher rates of undernutrition than their HIV-negative counterparts. Among the ART-treated HIV-positive children, 78 (36.6%) were stunted, 47 (22.1%) were underweight, and 29 (13.6%) were wasted. Households of ART-treated HIV-positive children exhibited lower economic status, lower levels of education, and higher percentages of unmarried caregivers with higher unemployment rates. Food insecurity was prevalent in over half of ART-treated HIV-positive children’s households. Furthermore, ART-treated HIV-positive children were more likely to be orphaned, to be fed less frequently, and to have lower body weight at birth compared to HIV-negative children. In the multivariate analysis, child’s HIV-positive status was associated with being underweight (AOR = 4.61, 95% CI 1.38-15.36 P = 0.013) and wasting (AOR = 9.62, 95% CI 1.72-54.02, P = 0.010) but not with stunting (AOR = 0.68, 95% CI 0.26-1.77, P = 0.428). Important factors associated with underweight status among ART-treated HIV-positive children included hunger (AOR = 9.90, P = 0.022), feeding frequency (AOR = 0.02, p < 0.001), and low birth weight (AOR = 5.13, P = 0.039). Factors associated with wasting among ART-treated HIV-positive children were diarrhea (AOR = 22.49, P = 0.001) and feeding frequency (AOR = 0.03, p < 0.001). Conclusion: HIV/AIDS is associated with an increased burden of child underweight status and wasting, even among ART-treated children, in Dar es Salaam, Tanzania. In addition to increasing coverage of ART among HIV-positive children, interventions to ameliorate poor nutrition status may be necessary in this and similar settings. Such interventions should aim at promoting adequate feeding patterns, as well as preventing and treating diarrhea. © 2011 Sunguya et al; licensee BioMed Central Ltd.
This cross-sectional study was conducted among HIV-negative and ART-treated HIV-positive children in Dar es Salaam, Tanzania. Nutritional status among ART-treated HIV-positive children was compared with that of HIV-negative children. In 2010, Dar es Salaam reported that about 18.8% of children in the general population were stunted, 11.8% were underweight, and 6.8% were wasted [22].The HIV prevalence in the city was 8.9% in 2009, which was higher than the national average [20]. While approximately 7,000 HIV-positive children in Dar es Salaam were attending Care and Treatment Centers (CTCs); only about 4,000 children were under ART [20]. Dar es Salaam has 44 health facilities with ART programs, the majority of which are run by the government and collaborating partners [24]. According to the national guidelines for HIV care and treatment in Tanzania, which were in use during this survey, ART treatment initiation depends on disease progression [24]. Since disease progression differs among children, the guidelines also demand individualization at initiation of treatment based on biological and social factors. Pertinent biological factors include age, HIV-related diseases, immunosupression, and viral load. Social factors include disclosure status, caregiver's commitment, and family support. All HIV-positive children under 12 months of age are supposed to start ARV, while for HIV-positive children older than 12 months, both clinical and immunological threshold were used as indicators. Such criteria include WHO clinical stages 1 and 2 with CD4 <25% or WHO clinical stage 3 or 4, irrespective of CD4%. [24]. ART-treated, HIV-positive children in Tanzania are typically treated by combination therapy incorporating three ARVs. The recommended fixed combination of ART is either two Nucleoside Reverse Transcriptase Inhibitors (NRTI) and a Non-Nucleoside Reverse Transcriptase Inhibitors (NNRTI) or two NRTI and Boosted Protease inhibitor (PIr). The appropriate combination also varies with age, where, for children younger than 36 months of age, a combination therapy includes Zidovudine, Lamivudine and Niverapine. Children older than 36 months receive a combination of Zidovudine, Lamivudine and Efavirenz. In the event of Nevirapine exposure such as during pregnancy for PMTCT, Nevirapine is usually substituted with Lopinavir boosted with Ritonavir. When a child presents with anemia, Zidovudine is exchanged for Stavudine. A monthly visit for ARV refills ensures adherence, monitoring of side effects, and early detection of treatment failure [24]. We recruited 435 pairs of children aged 6-60 months, along with their caregivers. For the HIV-positive group, only those under ART were selected. ART-treated, HIV-positive children were selected from HIV care and treatment centers (CTCs) where they undergo treatment. Upon their enrollment or referral to CTCs, several diagnostic tests are conducted to confirm their sero-status. For children under 18 months of age, DNA-PCR test is done to avoid false-positive results due to persistent maternal antibodies. A PCR machine is housed within the specialized laboratory of Muhimbili National Hospital. The collected Dried Blood Samples (DBS) are sent to this laboratory for diagnosis. The algorithm for HIV/AIDS diagnosis among children older than 18 months is through three rapid antibody tests which are Determine® (Abbot, Wiesbaden, Germany), SD Bioline HIV-1/2® (Standard Diagnostics, Kyonggi-do, South Korea) and Uni-gold® (Trinity Biotech, Bray, Ireland) in the CTC. Enzyme-linked Immunosorbent Assay (ELISA) may also be used under special circumstances where rapid antibody tests could not facilitate definitive diagnosis. However, a specialized laboratory and technicians are required for such diagnostic [24]. We excluded children with missing ART information and those whose caregivers did not consent to participate. For the comparison group, we recruited HIV-negative children and their caregivers from general pediatric clinics in Dar es Salaam. General pediatric clinics are part of Reproductive and Child Health (RCH) clinics, which under-five children with or without ailments attend for growth monitoring and vaccination. Children who presented at the clinic with minor ailments, such as fever, diarrhea, or upper respiratory infections, were excluded from this study. To group these children as an HIV-negative group, we relied on self-reported information from the caregiver, medical files and child follow-up cards, child's past medical history, reported HIV/AIDS results from mother during antenatal care, and physical examination of the child. From this group, we excluded children with known HIV-positive status and those whose parents were known to have HIV/AIDS or to have died of HIV/AIDS-related illnesses. HIV-positive participants were recruited from health facilities providing free ART services to over 100 children. In total, 12 out of a total of 44 facilities with ART programmes in the region fit the selection criteria. Three health centers were dropped due to their peripheral location. Muhimbili was also dropped because it is the city's referral hospital. Five centers that provide nutrition supplements to children with severe undernutrition were also excluded. The final three health facilities selected for the study were thus Buguruni, AKC, and Sinza CTCs. To recruit children for the control group, we selected reproductive and child health clinics from a list of health facilities with ART programmes by convenience sampling. In this study, we selected AKC and Sinza RCH clinics for recruitment of HIV-negative children. The selected health facilities consisted of both CTCs and RCHs serving the three Dar es Salaam municipalities – Ilala, Kinondoni, and Temeke. With respect to access, a client from any municipality may attend any of the facilities inside the municipality or other areas. We selected HIV-positive participants from each respective CTC health facility by systematic random sampling using a prepared register of eligible children. We chose one participant after every other eligible one in the prepared roster for participation in the study. When the participant refused to participate after being chosen, we proceeded on to the next individual on the list. For the HIV-negative group, we used random sampling based on daily attendance, with a minimum of 15 children recruited for one day. The recruited participants from both CTCs and RCHs represented the three municipalities, i.e. Ilala (HIV-positive-79, HIV-negative-70), Kinondoni (HIV-positive-101, HIV-negative-106) and Temeke (HIV-positive-33, HIV-negative-26). About the participants per clinic, we recruited: 84 HIV-positive participants from AKC CTC and 99 HIV-negative participants from its RCH clinic; 76 HIV-positive participants from Sinza CTC and 103 HIV-negative participants from its RCH clinic; and 53 HIV-positive participants were recruited from Buguruni CTC. All the selected facilities are run by the government and have similar standard operating procedures. We used Power and Precision version 4 (Biostat, Englewood, NJ, USA) software to calculate the minimum sample size that would detect the difference in the proportion of undernutrition between HIV-positive and HIV-negative children at a power of 80, with 95% CI and a standard deviation of 17. As information on the prevalence of undernutrition among ART treated HIV-positive children in Tanzania or Sub-Saharan Africa was not available, we used data from a study conducted in Dar es Salaam [7] among HIV-positive and HIV-negative children. In this study, the proportion of stunting among HIV-positive and HIV-negative children was 35.6% and 29.6%, respectively. Relevant proportions for underweight and wasting among the two groups could not be found. Therefore, the estimated minimum sample size for each group was calculated to be 183. In this study, we recruited a total of 435 children, among whom 233 were HIV-positive and 202 HIV-negative. The data for 20 ART-treated HIV-positive children were excluded due to missing data regarding ART and errors in anthropometric information. The children's weights were measured using a standardized hanging Salter scale® (UK) calibrated to 0.1 kg for children who could not stand and a standardized Seka® digital scale (Brooklyn, USA) for children who could stand. We measured height using a Seka® measuring rod calibrated to 0.5 cm. Weight and height were converted to weight-for-age z-score (WAZ), weight-for-height z-score (WHZ) and height-for-age z-score (HAZ) using Epi-Info/ENA version 3.5.1, 2008 (CDC, Atlanta, Georgia, USA) software, according to WHO reference values [25]. Based on the recommendations of the WHO Global Database on Child Growth and Malnutrition, z-scores <-2SD and <-3SD defined moderate and severe undernutrition, respectively. Socio-demographic variables pertaining to children and their caregivers were adopted from the Tanzania Demographic and Health Survey (TDHS), women and household questionnaires [21,22]. A caregiver was defined as the child's caretaker, parent, or a guardian that accompanied the child to the clinic. Information collected included education level, orphanhood, religion, and marital status. A child was considered an orphan if he/she had lost one or both parents. Food security was assessed using the short-form HFSS [26], a 6-item scale developed in the United States (US) from the original 18-item scale [27] and used in various settings including the US [28], Bolivia, Burkina Faso, the Philippines [29], and the Caribbean [30]. This scale is used to measure household food security by 12-month recall. Characterization is based on the sum of affirmative responses; two or more affirmatives indicates 'food insecurity', while 5 or more affirmatives indicates 'hunger'. In the present study, Cronbach's alpha for the HFSS was 0.72, with corrected item-total correlation ranging from 0.09 to 0.74. A total dietary diversity score was calculated from a recalled list of food items consumed over the previous day. Based on a set list of 12 food items, a score lower than 6 was classified as low dietary diversity [31]. Listed food items were adopted from the TDHS, child questionnaire [21,22]. Frequency of feeding was assessed by a 24-hour feeding recall; feeding frequency of less than 4 (median) was considered low. Economic status was assessed by using a Weighted Wealth Index incorporating household assets ownership, housing characteristics, fuel for lighting and cooking, type of toilet, source of water, and feeding characteristics [21,22]. Dichotomous variables were constructed and factor analysis using principle component analysis (PCA) used to reduce 42 items to 22 (loaded as factor 1). Factor loadings were used as item weights, which were totaled to yield the wealth index for each household [32-34]. The total Weighted Wealth Index score was then equally divided into terciles designating high, middle, and low economic status. Children registering a WHO clinical HIV stage above two were regarded as advanced cases [35]. In this study, we extracted the highest reached WHO clinical HIV stage from the medical file of each child. Such information is routinely updated on every CTC visit. Eight nurse counselors were hired and trained for one day on interviewing technique and questionnaire content. They thereafter pre-tested the questionnaire under supervision of the first author. Data were collected by face-to-face interview and relevant medical data were retrieved from medical files in September and October 2010. We analyzed data from 213 ART-treated HIV-positive children and 202 HIV-negative children. Descriptive analysis was conducted by Chi-square and independent sample T-tests. Both bivariate and multiple logistic regression analyses were used to examine associations of various factors with wasting, underweight, and stunting. Multiple logistic regression analyses were used to examine the associations between children's HIV status and underweight, wasting, and stunting, respectively. In these models, we controlled for child's age, sex, birth weight, dietary diversity score, ever breastfed status, caregiver's age and education level, employment status, food security, and wealth index score. We also used multiple logistic regression to examine the factors associated with nutritional status (underweight, wasting, and stunting) among ART-treated HIV-positive children alone. Variables included in these multivariate analyses models were as follows: age, sex, birthweight, diarrhea episodes in the past six months, caregiver's age, caregiver's education level, feeding frequency, HIV stage, household food security, household wealth index, dietary diversity score, and ART duration. From the regression models, we excluded 'malaria episodes' and 'hospitalization in the past six months' variables because they showed high correlations with diarrhea (R = 0.5 and R = 0.6, respectively). 'Orphanhood' and 'total months breastfed' variables were also excluded due to missing values. Multicollinearity in both models was checked by examining the standard errors for regression coefficients. Statistical significance was set at P-value<0.05. Analysis was conducted using PASW 18 (SPSS Inc., Chicago, Illinois, USA). This study was approved by the Institutional Review Boards of The University of Tokyo and the Muhimbili University of Health and Allied Sciences, Dar es Salaam. Permission to conduct the research was granted by the relevant municipality health departments and by the managing medical officer in the health facilities. Participation was voluntary, confidentiality ensured, and informed consent secured before the start of each interview.
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