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Objective To assess the associations between maternal HIV infection and growth outcomes of HIV-exposed but uninfected infants and to identify other predictors for poor growth among this population. Design Within a trial of de-worming during pregnancy, the cohort of offspring was followed from birth. HIV status of the mothers and their children was investigated and growth data for children were obtained at age 1 year. Length-for-age, weight-for-age and weight-for-length Z-scores were calculated for each child; Z-scores <-2 were defined as stunting, underweight and wasting, respectively. Setting The study was conducted in Entebbe municipality and Katabi sub-county, Uganda. Subjects The sample consisted of 1502 children aged 1 year: HIV-unexposed (n 1380) and HIV-exposed not infected (n 122). Results Prevalence of stunting, underweight and wasting was 14·2 %, 8·0 % and 3·9 %, respectively. There was evidence for an association between maternal HIV infection and odds of being underweight (adjusted OR = 2·32; 95 % CI 1·32, 4·09; P = 0·006) but no evidence for an association with stunting or with wasting. Young maternal age, low maternal education, low birth weight, early weaning and experiencing a higher number of episodes of malaria during infancy were independent predictors for stunting and underweight. A higher number of living children in the family was associated with wasting. Conclusions Maternal HIV infection was associated with being underweight in HIV-exposed uninfected infants. The success of programmes for prevention of mother-to-child HIV transmission means that an increasing number of infants will be born to HIV-infected women without acquiring HIV. Therefore, viable nutritional interventions need to be identified for this population. Copyright © The Authors 2013. The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence . The written permission of Cambridge University Press must be obtained for commercial re-use. The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence . The written permission of Cambridge University Press must be obtained for commercial re-use..
The study was conducted in Entebbe municipality and Katabi sub-county as previously described( 16 ). It was a randomized, double-blind, placebo-controlled trial of anthelminthics in pregnancy, using albendazole v. placebo and praziquantel v. placebo in a 2 × 2 factorial design. The study was originally designed to examine effects of anthelminthic treatment during pregnancy on infant responses to immunization and infectious disease incidence. Results of the trial have been reported elsewhere and no effect of the trial intervention on growth parameters was observed( 17 , 18 ). The study results reported herein represent a retrospective observational analysis of differences in growth at 1 year of age between HIV-exposed but uninfected infants and infants born to women who were HIV-negative. Socio-economic, maternal and infant characteristics were also evaluated for associations with growth outcomes at 1 year of age. Women were recruited at the antenatal clinic at Entebbe Hospital between April 2003 and November 2005. They were eligible if they were well, resident in the study area, planning to deliver their baby at the hospital, willing to participate and willing to know their HIV status; and excluded if they had Hb <8 g/dl, clinically apparent severe liver disease, diarrhoea with blood in the stool, abnormal pregnancy, history of adverse reaction to anthelminthic drugs or had participated in the study during an earlier pregnancy. Following delivery, children were followed up according to the study protocol. Morbidity data were collected prospectively at the research clinic. Malaria was diagnosed as fever (≥37·5°C) with Plasmodium falciparum parasitaemia. Data on asymptomatic parasitaemia were collected annually. Study nurses were trained on how to take and record the anthropometric measurements. Weight measurements for 1-year-olds were taken using CMS Weighing Equipment, model MP25 (Chasmors Ltd, London, UK). The children were lightly dressed wearing undergarments only, and wore a measuring trouser which was then suspended on a weighing scale. Measurement of recumbent length at age 1 year was done using an adjustable child-length measuring board (Seca; Vogel & Halke, Hamburg, Germany). In 2002, prior to the start of the study, the research team in collaboration with Entebbe Hospital established a programme for prevention of mother-to-child HIV transmission at the hospital. In accordance with guidelines current at the time( 19 ), women identified as HIV-positive were offered a single dose of nevirapine for themselves and their infants, to be taken during labour and after delivery, respectively. HIV-positive women were provided with cotrimoxazole daily for prophylaxis of opportunistic infections; HIV-exposed infants were provided with cotrimoxazole syrup from age 6 weeks until their HIV status was assessed at age 18 months; at this time, cotrimoxazole was discontinued for HIV-negative children. HIV-positive infants were referred for care at nearby specialist centres. Highly active antiretroviral therapy (HAART) for treatment was not widely available in Uganda at the time when women were recruited to the study; however, five HIV-positive women were recorded as taking HAART during pregnancy. Mothers’ HIV status was assessed by a rapid test algorithm before delivery as previously described( 20 ). Vertical HIV transmission was diagnosed by RNA and DNA PCR at age 6 weeks as previously described( 18 ) and by rapid test at age 18 months. Infants were regarded as being HIV-positive if the 6-week sample had a positive DNA PCR for any of the viral regions examined and a viral load of 1000 copies per millilitre or more, or if the rapid test at 18 months of age was positive. Blood samples were obtained from HIV-infected pregnant women. CD4 cell counts were ordered as part of the baseline measurement and done using a BD FACScount™ flow cytometer (Becton Dickinson, San Jose, CA, USA). Maternal immunological status was dichotomized based upon results of CD4 testing performed at enrolment, with women having a CD4 count of ≤350 cells/mm3 being categorized as having poor immunological status. The outcome variables for the present study were the three continuous anthropometric measures, length-for-age Z-score (LAZ), weight-for-age Z-score (WAZ) and weight-for-length Z-score (WLZ), derived by importing growth parameters into WHO Anthro software version 3 (April 2009). The continuous value of each of the three anthropometric measures was also used to derive three binary variables reflecting the presence or absence of a Z-score <−2, i.e. stunting (LAZ <−2), underweight (WAZ <−2) and wasting (WLZ <−2), which were then also used as dependent variables for the study objectives. Data management was done using the Microsoft® Access database designed for the anthelminthic trial. Statistical analyses were performed using the STATA statistical software package version 10. The second( 17 ) or third infant( 1 ) in a twin or triplet pregnancy was excluded from the analysis but five women on HAART were retained. In order to evaluate the associations between HIV exposure, other factors and growth outcomes, we used as response variables the continuous Z-scores and the binary variables for stunting, underweight and wasting defined above. Univariable analysis was first performed. For the continuous outcomes linear regression was used to investigate whether HIV exposure and other risk factors were associated with the mean Z-score; mean differences in Z-score and 95 % confidence intervals were used to quantify the association between each risk factor and growth. For the binary outcomes, logistic regression was used to investigate whether HIV exposure and other risk factors were associated with the prevalence of stunting, underweight and wasting; odds ratios were used to quantify the association between each risk factor and poor growth. Multivariable analyses were then conducted investigating factors considered likely to be potential confounders, including maternal age, maternal education, maternal income, household socio-economic status (a score based on building materials, number of rooms and items owned) and episodes of malaria during infancy; variables assumed to be potential confounders and variables that presented a P value of <0·05 in the univariable analysis were included in multivariable regression models. Significance levels in the final model were determined using likelihood ratio tests. A similar approach was used to investigate other risk factors for stunting, underweight and wasting in this population. The following factors were considered: sex of the child, low birth weight, low maternal CD4 cell count, number of living children in the family and early weaning (defined as introducing cow's milk at or before the age of 6 weeks).
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