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Childhood malnutrition is associated with increased mortality and morbidity irrespective of HIV status. Up to 30% of deaths in children aged under 5 years are attributable to undernutrition defined as a weight-for-age z-score (WAZ) <−1 (Black et al. 2008). The prevalence of stunting and undernutrition increases inversely with household socio-economic status (SES), whilst stunting is synonymous with chronic undernutrition and an indicator of social deprivation (WHO 1986).
Up to 50% of children initiated on antiretroviral treatment (ART) in African HIV treatment programmes are reported to be undernourished (Bolton-Moore et al. 2007), and severe malnutrition at initiation of ART is a recognised risk factor for mortality in HIV-infected children (Sutcliffe et al. 2008), especially when co-infected with HIV and TB (Hesseling et al. 2005).
Both antiretroviral treatment (ART) and good nutrition are important for the management of HIV-infected, malnourished children. Improvements in anthropometric measurements have been demonstrated in undernourished HIV-infected children following the initiation of ART irrespective of baseline nutritional status or the provision of nutritional supplements (Davies et al. 2009; Sutcliffe et al. 2011). Those who are severely malnourished demonstrate similar improvements in anthropometric measurements following the initiation of ART and nutritional therapy as HIV-uninfected children with SAM but have a higher initial mortality rate (Fergusson et al. 2009). In a recent study from Malawi, prompt initiation of ART within 3 weeks of starting therapeutic feeding was associated with better nutritional outcomes compared with those who started ART after this time (Kim et al. 2012).
The WHO published ‘Guidelines for an Integrated Approach to the Nutritional Care of HIV-Infected Children (the ‘Guidelines’) (WHO 2009). The Guidelines provide a structured ten-step plan for the nutritional management of HIV-infected children aged 6 months to 14 years and can be applied to both inpatient and outpatient settings. Three ‘Nutritional Care Plans’ (NCP-A, NCP-B and NCP-C) are recommended depending on the child's weight status (based on anthropometric measurements) and presence of comorbidities (see Box 1). For each NCP, the specific additional daily calorific intake for a child in that category is given (Box 1).
Box 1. WHO Nutritional Care Plans
- NCP-A for children who are growing appropriately as determined using WHO Child Growth Standards (The WHO Child Growth Standards, 2006).
- Children require an additional 10% of energy based on their actual weight, usually provided as part of the diet and not nutritional supplements
- NCP-B for children with poor weight gain or increased nutritional needs including reported weight loss, very low weight (WAZ <−3), underweight (WAZ <−2), confirmed weight loss (>5%) since the last visit, or growth curve flattening.
- Morbidities with increased nutritional requirements include chronic lung disease, TB, persistent diarrhoea, or other chronic opportunistic infection or malignancy (this will include most children who have stage 3 or 4 disease).
- These children require an additional 20–30% energy per day based on their age.
- NCP-C for children with severe malnutrition including signs of severe visible wasting, oedema present in both feet, WHZ <−3, or MUAC <115 mm for children aged 6–60 months, 129 mm in children 5–9 years or 160 mm in children 10–14 years.
- These children require an additional 50–100% energy per day in the form of therapeutic feeds with total daily energy calculated on their weight and age.
Whilst the development of these Guidelines is a significant advance in the nutritional management of HIV-infected children, the financial cost of supplying these additional calories with macronutrient supplements in rural HIV programmes needs to be explored. We investigate the proportion of children in a rural South African HIV programme who would be eligible for supplementation at the time of ART initiation, the proportion within each category of NCP and the costs of purchasing the appropriate NCP with locally available nutritional supplements.
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In 2010, 251 children aged 6 months to 14 years initiated ART in the Programme. Of these, 113 (45%) would have been eligible for nutritional supplementation according to the Guidelines of whom 88 (78%) would have required 6-month NCP-B (40 with prevalent TB, 41 with moderate malnutrition and 7 with a condition with increased nutritional needs); 25 (22%) with SAM (4 of whom also had prevalent tuberculosis) would have required NCP-C for 10 weeks followed by NCP-B for 16 weeks (Figure 1). In total, 44 of 251 (17.5%) children had prevalent TB at initiation and an additional 24 had a previous history of TB. Thus, 69 of 251 (27.5%) children initiating ART had a history of TB disease.
Figure 1. Number of children initiating ART by nutritional care plan. *Twenty-one children were unassigned because of missing data.
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For 21 (8%) children, it was not possible to classify which NCP was required from the data available (because of lack of clinical data regarding WHO staging and presence of co-existent disease such as TB), and they were classified as ‘unassigned’.
The cost of supplying each additional kcal with nutritional supplements equated to 0.021 ZAR/kcal for Sibusiso and 0.009 ZAR/kcal for Future Life Porridge. Costs of providing 26-week NCP-B (Future Life Porridge) equated to ZAR516 per child and ZAR 45,414 ($5858) for all 88 children requiring NCP-B (Table 2) and ZAR1,636 per child or ZAR40,910 ($5277) for all 25 children with SAM who were provided with 10-weeks NCP-C (Sibusiso) and 16-weeks NCP-B (Future Life Porridge) (Table 3). Thus, the cost of 26-weeks supplementation for the entire group of 113 children requiring supplementation was ZAR86,324 ($11 135).
Of the 21 children with missing clinical staging or evidence of TB at initiation, 20 had a WAZ >−2 (thus unlikely to have SAM unless markedly oedematous), a further child did not have any weight or clinical details recorded. If we assume that all these children had a stage 3 or 4 disease requiring supplementation with NCP-B, then the additional cost of supplementing these children determined by their age would be ZAR12,449 ($1606). This estimation provides an upper limit of ZAR98,773 ($12 742) for purchasing supplements for all children initiated during the year period.
The mean weight of all children aged ≤3 years initiating ART was 9.8 kg (92 children) and for children >3 years was 21.6 kg (159 children). The total estimated cost of supplying first-line ART for 26 weeks to all 251 children was ZAR745,637 ($96 187). The cost of nutritional supplements ($11 136) represents an estimated additional 11.6% to the cost of the drugs for these children (Table 4).
Table 4. Estimated cost of supplying first-line ART by mean weight for age for 26 weeks
|Age group (years)|| ||Estimated cost of 26-weeks ART per child|| |
|Mean weight (kg)||Number of children (251)||ABC||3TC||LPV/r||EFV||Estimated total cost for age group (ZAR)|
|Estimated total cost for cohort|| || || || || || ||ZAR 745,637|
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This study investigates the financial costs of providing nutritional supplementation to a rural cohort of HIV-infected children in a public health HIV treatment programme using standardised international guidelines, with costs based on the nutritional supplements available and used in the country. Applying these guidelines, we found that almost half the children initiated on ART in 2010 would have been eligible for nutritional supplementation, reflecting the levels of poverty and comorbid TB in the area (Houlihan et al. 2010b). Whilst the proportion of children found to be undernourished at initiation of ART in this study is similar to that found in previous studies (Bolton-Moore et al. 2007), further generalisability of our results may be limited by a lack of similar nutritional supplements and differences in programmatic costs in other settings which were not accounted for in this study.
In our programme, the estimated annual cost of purchasing the recommended quantities of nutritional supplementation for 26 weeks for all eligible children initiated during the study period was approximately $11 136. This represents 11.6% of the cost of procuring ART for 26 weeks for all children initiating ART during 2010. Nutritional supplements are provided until exit criteria are achieved with a 26-week time frame used in this study (see above). Thereafter, with appropriate supplementation, follow-up and the initiation of ART, children should remain adequately nourished and only require an additional 10% daily energy requirement (NCP-A), which is provided at the household level. Thus, supplementation should only be required once for a maximum period of 26 weeks during a 52-week (1-year) period, whereas ART is required for the entire period. The proportional costs of supplementation in this ART programme for a 1-year period equates to 5.8% of ART costs.
The estimation of costs for purchasing nutritional supplementation will be affected by a number of factors. The proportion of children who would have been eligible for supplements is likely to have been underestimated for three reasons. First, our inability to assign a NCP to 21 children because of missing documentation of clinical staging or prevalent TB may have led to an underestimation of the number of children requiring supplementation. Second, as heights or MUACs were not recorded at initiation for the majority of children, we depended on WAZ to estimate undernutrition, which may have resulted in misclassification of some children. Finally, accurate documentation of comorbidities and clinical signs indicative of SAM may have been missing in the case files resulting in an underestimation of the extent of undernutrition and inaccurate assignment of children to a NCP.
Difficulties in the accurate recording and interpretation of anthropometric measures by field staff in resource-poor settings have been found to range from a lack of confidence in calculating accurate age from birth dates (Hamer et al. 2004), difficulties in plotting growth charts appropriately (resulting in inaccurate WAZ and WHZ) (Qayad 2005), and limited access to, and training in, the use of reference growth charts and equipment such as scales and stadiometers (Duggan 2010). These issues are likely to have been present within the Hlabisa HIV Programme and to have affected the accurate detection of children who were undernourished and required supplementation during the study period.
It is also possible that an overestimation of costs per child may have occurred when using the 26-weeks time frame for the supply of supplementation. In practice, the actual time taken to nutritional recovery defined by the exit criteria is often <26 weeks (except for those with concurrent TB who require supplementation until the completion of their TB treatment). Clinically, we found that children with moderate malnutrition often achieved exit criteria, and moved to NCP-A, by approximately 12 weeks and those with SAM by 12–16 weeks. Assessing each child carefully and exiting them from additional supplementation appropriately would reduce supply costs to a total of ZAR57,079 ($7363) (ZAR20,960 for the management of children requiring 12-week NCP-B only, and ZAR36,119 for those requiring NCP-C initially (10-weeks Sibusiso and 6-weeks Future Life Porridge)). This reduces the proportional costs further to 7.6% of ART costs for 26 weeks and approximately 3.8% over the course of 52 weeks.
Alternatively, if we assume that the 48 children eligible for NCP-B who did not have prevalent TB at diagnosis required only 13-weeks NCP-B instead of 26 weeks (and continued to provide 26-week NCP-B to those with prevalent TB), the cost of supplying NCP-B would be reduced to ZAR34,072 ($4395). Furthermore, if we assume that children with SAM recover more quickly than the 10 weeks allowed for here and require only 6 weeks of NCP-C followed by 20-week NCP-B, the costs of supplying nutritional supplements to this groups is reduced to ZAR29,528 ($3809). Combining these two estimations would reduce the overall cost of supplementation for all children to ZAR63,600 ($8204), which would represent 4.2% of the cost of 52-weeks ART to the same group.
This analysis is limited to the costs of purchasing supplements and compares these to purchase costs of ART. It does not account for the costs of staff training, transport, distribution and wastage of goods, inpatient care, outpatient review, and opportunity costs for carers to attend clinics. Further analyses are required to estimate these additional costs, which may impact on the feasibility of adopting the Guidelines.
The provision of nutritional supplements by the Programme during, and prior to, 2010 was relatively unstructured and relied on physicians or nurses identifying undernourished children. Studies in HIV-uninfected children have found improvements in anthropometric status and clinical outcomes, including greater rates of weight gain and reduced nutritional relapse and mortality, following the implementation of formalised nutritional supplementation with RTUF (Weisstaub & Araya 2008) even when compared with traditional milk and flour supplementation (Ciliberto et al. 2005; Bhutta et al. 2008). It is possible that, in the absence of Guidelines, undernourished children or those with comorbidities would not receive supplementation in the correct amounts for a prescribed period of time.
Good nutritional management is essential for the improvement of nutritional outcomes and anthropometric measures in HIV-infected children (Kim et al. 2012), but especially important for those who are undernourished or have additional comorbidities (including tuberculosis) to reduce their higher burden of morbidity and mortality (Hesseling et al. 2005). Assuming the level of undernutrition is representative of other paediatric populations initiating ART in resource-poor regions, this additional cost should be budgeted for in programmes.
Undernourished children and those with comorbidities represent an extremely vulnerable group of HIV-infected children. This study illustrates the low proportional cost of procuring nutritional supplements for HIV-infected children in resource-poor areas. The provision of nutritional supplements should be considered for the optimal management of these children to improve their poor outcomes. We recommend that programmes explore the integration of nutritional care for HIV-infected children along with the provision of ART either by providing supplements themselves or through partnership with organisations that have the resources to provide these.