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Acceptability of Outpatient Ready-To-Use Food-Based Protocols in HIV-Infected Senegalese Children and Adolescents

Cecile Cames, PhD1, Marie Varloteaux, MSc1,
Ndeye Ngone Have2, Alhadji Bassine Diom3,
Philippe Msellati, MD, PhD1, Ngagne Mbaye, MD3,
Helene Mbodj, MD2, Haby Sy Signate, MD, PhD2,
and Aminata Diack, MD2; for the ANRS 12279 MAGGSEN Cohort Study Group

Abstract
Objectives: To assess the acceptability of ready-to-use food (RUF)-based outpatient protocols in HIV-infected children and adolescents with severe acute malnutrition (SAM) and moderate acute malnutrition (MAM).
Methods: Plumpy Nut and Plumpy Sup were supplied every 2 weeks and prescribed by weight to SAM and MAM children, respectively. Forty-three children, 24 MAM and 19 SAM, were enrolled. Orga- noleptic appreciation, feeding modalities, and perceptions surrounding RUF were recorded at week 2. Sachets were counted to measure adherence throughout the study.
Results: Median age was 12.2 years (interquartile range: 9.3-14.8), and 91% were on antiretroviral treatment. Overall, 80%, 76%, 68%, and 68% of children initially rated RUF color, taste, smell, and mouth feeling as good. However, feelings of disgust, refusal to eat, fragmentation of intake, self-stigma, and sharing within the household were commonly reported. Eighteen MAM and 7 SAM experienced weight recovery. Recovery duration was 54 days (31-90) in MAM versus 114 days (69-151) in SAM children (P 1⁄4 .02). Their rate of RUF consumption compared to amount prescribed was approximately 50% from week 2 to week 10. Nine failed to gain weight or consume RUF and were discontinued for clinical management, and 9 dropped out due to distance to the clinic.
Conclusion: Initial RUF acceptability was satisfactory. More than half the children had successful weight recovery, although adherence to RUF prescription was suboptimal. However, further research is needed to propose therapeutic foods with improved palatability, alternative and simpler intervention design, and procedures for continuous and tailored psychosocial support in this vulnerable population. Trial registration: NCT01771562 (Current Controlled Trials).

Introduction

Scaling up of antiretroviral treatment (ART) has dramatically reduced the mortality of HIV- infected children worldwide and thus allowed HIV infection to become, to some extent, a

1

qualities were rated as good in another quantita- tive study from Vietnam carried out in HIV-

12

dren and adolescents are unavailable.
The ANRS 12279 MAGGSEN Pediatric

Cohort Study aims to investigate the growth and metabolic disorders among HIV-infected Sene- galese children. Recently, we reported a high prevalence of acute malnutrition in children aged 5 to 16 years, after a median duration of

chronic disease.
potential to induce growth failure in children or to increase the severity of preexisting undernutri- tion. Consequently, severe acute malnutrition (SAM) and moderate acute malnutrition (MAM) remain common in HIV-infected children and adolescents, even when on ART,2,3 and are

However, HIV infection has the

strongly associated with death.
Since 2007, the United Nations has recom-

mended ready-to-use therapeutic food (RUTF) for the outpatient nutritional rehabilitation of children with uncomplicated SAM,5 and most African countries adopted national guidelines for RUTF-based nutritional rehabilitation of children <5 years, including those with HIV. In the management of MAM, ready-to-use sup- plementary food (RUSF) is recommended as an option as well as other fortified foods and
enhanced family diet. Provision of RUTF and

RUSF, although originally developed for

pediatric use, has become a widely used strat-

egy among HIV-infected adults through food-

by-prescription programs in low-income

ished outpatients are sparse and mixed. Qualita- tive studies conducted in Southern Africa among HIV-infected adults9,10 reported poor overall acceptability of RUTF. The RUTF was mostly found unacceptable by pregnant and lactating Bangladeshi women,11 whereas its organoleptic

intervention within the cohort for outpatient nutritional rehabilitation using imported RUTF (Plumpy Nut; Nutriset, Malaunay, France) and RUSF (Plumpy Sup; Nutriset). Both ready-to- use foods (RUFs) are energy-dense lipid pastes made from peanut butter, oil, sugar, and a high vitamin and mineral supplement (RUTF also contains milk powder, while RUSF contains soy proteins) packed in 92 g individual sachets pro-

dance for the nutritional rehabilitation of HIV- infected children 􏰁5 years, the intervention protocol was designed in compliance with Sene- galese recommendations15 and adapted from the World Health Organization (WHO) framework for the nutritional care of HIV-infected children

settings.
Data on the acceptability of RUTF in malnour-

Data on acceptability outcomes of RUTF or RUSF thera- pies in undernourished HIV-infected older chil-

infected children <5 years and adults.
4 years on ART. We implemented a pilot

viding 500 kcal.
In the absence of specific and practical gui-

aged 6 months to 14 years.
present analysis are to assess the acceptability of this intervention in HIV-infected children and adolescents through their description of organo- leptic appreciation of RUF and compliance with the protocol modalities.

The objectives of the

Cames et al

Methods

Study Setting

The study was carried out in Dakar from April to December 2014 within the ANRS 12279 MAGG- SEN Pediatric Cohort Study. Full details of the rationale for the MAGGSEN Study and methods

RUF was limited to 2000 kcal/d (ie, 4 sachets),

and children were advised to spread the RUF

intake throughout the day, preferably outside

mealtimes. Children were discharged from the

nutritional intervention when they reached their

target weight, derived from BMIZ/WHZ

Population and Data Collection

The study included HIV-infected children aged 􏰁6 months to <18 years, enrolled in the MAGG- SEN Study or attending the study clinics, present- ing at their follow-up visit with MAM or SAM without medical complications, and who suc- ceeded at the appetite test. This was a conveni- ence sample as children were enrolled during a 6- month period (April to September 2014) up to the financial and human resource limits for the cohort.

At enrollment, a clinical assessment was per- formed, and patients’ socioeconomic and thera- peutic data were recorded from the patients’ files. The Household Food Insecurity Access Scale—a list of 9 specific questions about the availability and accessibility of foods and related worry for the household during the previous month—was are provided elsewhere.
SEN Study included HIV-1–infected children aged 2 to <16 years under active follow-up in 2 HIV clinics, Albert Royer National Hospital and Roi Baudoin Hospital. Children were seen every 3 months for a complete clinical assessment and every 6 months for laboratory monitoring. The study protocol was approved by the Ethics and Regulatory Committees in Senegal and the Ethics Committee of the Institute of Research for Devel- opment. All parents or legal guardians provided written consent.

Study Protocol

According to the WHO guidelines,17 MAM was defined as weight-for-height z score (WHZ) in children <5 years or body mass index-for-age z score (BMIZ) in children 􏰁5 years of <􏰂2 and 􏰁􏰂3, respectively, and SAM as WHZ or BMIZ <􏰂3. Within the week preceding enrollment, all eligible children were prescribed anthelmintics

and given an appetite test,

15

which assesses the

used to assess food insecurity.
generates a 4-class variable of food insecurity— none, mild, moderate, and severe. In this study, we used a binary indicator—food-secure (none) versus food-insecure household (mild to severe). At each follow-up visit, the unused RUF sachets from the previous provision were collected and registered for consumption monitoring. Children were weighed in their underwear to the nearest 100 g with an electronic scale. At enrollment and at target weight visit, height was measured twice to the nearest millimeter with a roll-up measuring rod, and the mean was used in the analyses. Anthropometrics were measured using Seca devices (Hamburg, Germany). At week 2, a struc- tured questionnaire covering the organoleptic perception of RUF, the mode of consumption, the associated stigma, and potential sharing within the family was administered to children 􏰁5 years and/or to the caregiver.

child’s ability to consume a quantity of RUTF or

RUSF per his/her weight. As an example, a child

weighing 10 to 15 kg should be able to eat at least

half a sachet during the test. Subsequent study

visits took place every 2 weeks and were con-

ducted by a nurse and a social worker, under the

supervision of a physician. At each visit, RUSF or

RUTF was dispensed—RUSF was provided to

children with MAM following a prescription of

75 kcal/kg of body weight/d and RUTF to chil-

dren with SAM following a prescription of 200

kcal/kg/d. Prescription by weight involves a high

daily dose in older HIV-infected children and

adolescents. In particular, RUTF is expected to

provide the child with SAM a complete diet in

replacement of the habitual household diet16 and

also cover the extra energy needs due to HIV

18
diet, the maximum energy intake provided by

infection.

In this study and to preserve habitual

Briefly, the MAGG-

Throughout the study, the social worker provided incentives, advice, and explanations to children and caregivers whenever needed.

>􏰂1.5.

This access scale

Food and Nutrition Bulletin 38(1)

Data Management and Analysis

Children who reached their target weight are

referred to as ‘‘recovery.’’ Those who experienced

medical complications after their enrollment, failed

to gain weight during 6 consecutive weeks, or

refused to consume the RUF were discontinued

from the study for clinical management and are

referred to as ‘‘failure.’’ Those who discontinued

their participation in the study are referred to as

‘‘default.’’ Height and weight were converted into

WHZ, BMIZ, and height-for-age z score using

20,21

Consumption of RUF was assessed at each follow-up visit by subtracting the number of unused sachets from the number prescribed. Acceptability data were compared, using the Fisher exact test, by malnutrition status, by age as a categorical variable (<12 years, 􏰁12 years), and by outcome in the study.

Continuous variables are expressed as median with interquartile range. Differences were consid- ered statistically significant at P < .05. All statis- tical analyses were performed using SAS version 9.3 (Cary, North Carolina).

Results

Size and Characteristics of the Study Population

During the inclusion period, 43 children, perina- tally HIV infected, presented at the study clinics with MAM (n 1⁄4 24) or SAM without complica- tions (n 1⁄4 19) and were enrolled in the interven- tion; 39 were on ART (􏰁3 drugs; Table 1). All passed the appetite test at the first attempt, except 1 who succeeded at the third. Most (38 of 43) were enrolled in the MAGGSEN Study. Median age was 12.2 years (9.3-14.8), and only 2 of the children were <5 years. In most cases, the mother was the caregiver; however, 7 of 24 MAM chil- dren and 9 of 19 SAM children were permanently placed with a grandmother (n 1⁄4 8), aunt (n 1⁄4 6), cousin (n 1⁄4 1), or neighbor (n 1⁄4 1). Of the 43

enrolled children, 25 (58%) recovered their weight; 9 failed to gain weight and/or to consume RUF and were discontinued from the study to be initiated on the first- (n 1⁄4 1) or second-line ART (n 1⁄4 8), of the latter, 2 also initiated an HIV status disclosure process; and 9 defaulted to follow-up due to distance from the clinic (Table 2). Children with MAM (n 1⁄4 18 of 24) were more likely to recover their weight than their SAM counterparts (n 1⁄4 7 of 19; P 1⁄4 .01). Their nutritional rehabi- litation was also faster, 54 days (31-90) in MAM children versus 114 days (69-151) in SAM children (P 1⁄4 .02), but their daily weight gains were similar, 1.4 g/kg (1.0-1.9) versus 1.3 g/kg (1.1-2.8), in MAM and SAM children, respectively.

Acceptability Outcomes

Overall acceptability was assessed by questionnaire in 41 child–caregiver pairs at the 2-week visit.

Organoleptic appreciation. Overall, 80%, 76%, 68%, and 68% of children initially rated the RUF color, taste, smell, and mouth feeling as good, respectively (Table 3). However, 12 of the 41 children reported that they felt disgusted by RUF, and there had been occasions when they simply refused to eat it.

Intake modalities. In most cases, the caregiver was responsible for supervising RUF intake, and the child needed encouragement to eat (Table 4). Half of the children ate the RUF in place of break- fast. The main mode for eating the RUF was directly from the sachet; however, some children/ caregivers used other feeding strategies like dilut- ing the sachet into water to make a gruel or spread- ing it over a piece of bread.

Perceptions and behaviors surrounding RUF. Most children (n 1⁄4 34) had understood that they were prescribed RUF due to their malnutrition status, 3 because they were sick, and 4 did not know the reason; 38 of the 41 perceived RUF as a drug. At least 15 of the 41 children stated they used to hide from others when eating RUF. Reasons given to explain this embarrassment were the fear of jealous reactions (n 1⁄4 5), teasing (n 1⁄4 2), or arousing pity (n 1⁄4 1), and 7 did not wish to respond to the question.

WHO reference values.
tics were compared by type of malnutrition (SAM or MAM) using the Fisher exact and Wilcoxon rank sum tests as appropriate and by outcome in the study (recovery, failure, or default).

Children’s characteris-

Cames et al 31 Table 1. Characteristics of HIV-Infected Children at Enrollment in the Study by Malnutrition Status.

Characteristics

Girls
Age, years
Mother deceased
In school
Food insecure household ART

First line

Second line
Duration on ART, years HIV status disclosed
Viral load < 300 copies/mL HAZ
BMIZ/WHZ

Children With MAM Median (IQR) or % n

38 9/24 11.0 (7.7 to 13.3)

30 7/23 91 21/23 83 19/23 96 23/24 61 14/23 39 9/23

5.0 (2.9 to 7.2)
29 7/24

75 18/24 􏰂1.0 (􏰂1.9 to 􏰂0.23)

􏰂2.4 (􏰂2.6 to 􏰂2.2)

Children With SAM Median (IQR) or %

26
13.3 (11.8 to 15.3)

n 5/19

P value for Differencea

.44 .02 .07 .09 .78 .31 .61

.95 .52 .12 .004 < .0001

Abbreviations: ART, antiretroviral treatment; BMIZ, body mass index-for-age z score; HAZ, height-for-age z score; IQR, interquartile range; MAM, moderate acute malnutrition; SAM, severe acute malnutrition; WHZ, weight-for-height z score. aStatistics are Fisher exact test and Wilcoxon rank sum test as appropriate.

Table 2. Characteristics of HIV-Infected Children at Enrollment and During the Intervention by Study Outcome.

60 9/15 67 10/15 87 13/15 84 16/19 69 11/16 31 5/16

5.1 (2.4 to 7.3) 42
50
􏰂2.0 (􏰂3.5 to 􏰂1.5) 􏰂3.4 (􏰂3.7 to 􏰂3.2)

8/19 9/18

Recovery

Median (IQR) or %

At enrollment
Age, years
Food insecure household
ART 92 Viral load <300 copies/mL 71 BMIZ/WHZ 􏰂2.5 (􏰂3.0 SAM 28

HAZ
During the intervention

Weight gain, g/d Duration, days

Failure

Median (IQR)
or % n

13.5 (11.9 to 14.9)
100 7/7

78 7/9

11 1/9 􏰂3.3 (􏰂3.5 to 􏰂3.1)

89 8/9 􏰂2.0 (􏰂2.5 to 􏰂1.8)

0.1 (􏰂0.2 to 0.7) 63 (34 to 97)

Default

Median (IQR)
or % n

14.3 (11.0 to 15.0)
78 7/9

100 9/9

100 9/9 􏰂2.9 (􏰂3.2 to 􏰂2.5)

44 4/9 􏰂1.5 (􏰂2.1 to 􏰂0.4)

0.4 (0 to 0.6) 63 (41 to 89)

Characteristics

n

18/22 23/25 17/24

7/25

10.7 (7.6 to 13.3) 82

to 􏰂0.6) 63 (35 to 114)

􏰂1.4 (􏰂2.1
1.3 (1.1 to 1.9)

to 􏰂2.3)

Abbreviations: ART, antiretroviral treatment; BMIZ, body mass index-for-age z score; HAZ, height-for-age z score; IQR, interquartile range; SAM, severe acute malnutrition; WHZ, weight-for-height z score.

Caregivers attested to sharing within the household—27% with other children, 7% with other adults, and 32% admitted to taking RUF for themselves. Many caregivers (59%) felt that they would need RUF therapy for themselves, whereas others stated that other adults and other children, living in the household, would also need RUF (43% and, 63% respectively). Chil- dren also reported sharing—22% with other

children and 12% with other adults in the household.

The data were also compared by product (RUTF or RUSF) and subsequent outcome in the study, and no remarkable association was found. Comparisons by age group revealed that younger children (<12 years) were more likely to need encouragement (P 1⁄4 .05) while eating and to hide from others (P 1⁄4 .004).

32 Food and Nutrition Bulletin 38(1)

Table 3. Organoleptic Appreciation of RUTF/RUSF Among Undernourished HIV-Infected Children and Their Caregivers 2 Weeks After Enrollment in the Study.

Organoleptic Appreciation Rated as Gooda

Color
Taste
Smell Mouthfeeling

n %

33 80 31 76 28 68 28 68

Children with RUTF/RUSF, N 1⁄4 41
Organoleptic Appreciation Rated as Fair to Poor: Main Commentaries

‘‘Toougly,’’‘‘Wouldlikeityellow’’ ‘‘Aftertasteofpeanutflouristoostrong,’’‘‘Toosweet,’’‘‘Toosalty,’’‘‘Toosour’’ ‘‘Smellofpeanutflouristoostrong,’’‘‘Smellslikemedicine,’’‘‘Makesmewanttovomit’’ ‘‘Fillsthemouth,’’‘‘Difficulttoswallow,’’‘‘Toosoft,’’‘‘Makesmewanttovomit,’’‘‘Hardto

chew if not hungry’’
Abbreviations: RUSF, ready-to-use supplementary food; RUTF, ready-to-use therapeutic food.

aAll questions were posed to children 􏰁5 years or to the caregiver if children <5 years.

Table 4. RUTF/RUSF Consumption Practices Among Undernourished HIV-Infected Children and Their Caregivers 2 Weeks After Enrollment in the Study.

were 50% (50-95), 71% (32-87), 50% (33-89), 50% (45-89), and 50% (50-93) at week 2, 4, 6, 8, and 10, respectively. There was no difference between malnutrition groups in the rates of RUF consumption.

Discussion

With regard to initial acceptability, most children participating in this outpatient nutritional rehabi- litation protocol reported a positive organoleptic appreciation of RUF. This result is consistent with those of a previous study that also assessed organoleptic qualities using a structured question-RUF Intake Modalitiesa Responsible for RUF intake Caregiver Child Both
Support needed when eating Single dose consumed over several feedings Intake duration >30 minutes Time of intake

As breakfast
As a snack
Just before meals Just after meals

Mode of intake
Direct feeding from the sachet Diluted in gruel
Spread on bread

Children with RUTF/RUSF, N 1⁄4 41

n %

24 58 10 24 7 16 25 61 18 44

19 46

23 56 23 56 16 39

9 22

41 100 14 34 7 17

naire in a similar context.
quantitative approach might insufficiently explore the children’s actual perception as they may answer what they think is the ‘‘desirable response,’’ particularly in the context of a food aid program. In our study, extensive investiga- tions revealed that most children needed contin- uous encouragement from the caregiver and that feelings of nausea, disgust, and refusals were common. Moreover, organoleptic acceptability is likely to decrease over time, due to saturation with RUF’s taste and dietary monotony. Qualita- tive studies conducted in HIV-infected adults on ART enrolled in similar RUF protocols (Plumpy Nut or Plumpy Sup) reported that most outpati- ents were pleased to receive RUF and perceived it to be beneficial as a therapeutic product for

Abbreviations: RUF, ready-to-use food; RUSF, ready-to-use supplementary food; RUTF, ready-to-use therapeutic food. aAll questions were posed to children 􏰁5 years or to the caregiver if children <5 years.

Consumption of RUF in children who recovered. The rate of RUF consumption was assessed at each follow-up visit up to week 10, which is approxi- mately the median duration of the study among children who recovered. Median proportions of RUF consumed compared to RUF prescribed

improving general health.
most of them indicated that they disliked the RUF taste, which was perceived to induce nausea and vomiting, and that both the taste and consistency

However, such a

In spite of this,

Cames et al

made it difficult to swallow. A leading reason for nonadherence in these studies was boredom with having to consume the product so frequently over a long period of time. In low-income settings, Plumpy Nut and Plumpy Sup are thus far the most widely available and accessible products for out- patient therapy. Studies comparing the accept- ability of a novel milk-free soy–maize–sorghum RUTF versus peanut-based RUTF (Plumpy Nut) in healthy children24 and not-wasted HIV/tuber- culosis adults25 could not demonstrate the super- iority of this alternative product. As palatability of therapeutic foods constitutes a primary criter- ion for the acceptability of rehabilitation proto- cols, further research is urgently needed to offer products with improved organoleptic qualities, particularly for adolescents and adults.

Although children and caregivers were advised to eat the sachets at snack time to pre- serve family meals, many substituted their habi- tual breakfast with RUF and/or consumed a sachet at an inopportune time, just before or just after meals. Almost half of the children could not consume a full RUF dose in a single feeding. To cope with nausea and lack of appetite, children were advised to have small bites of RUF through- out the day until the amount prescribed was con- sumed. Feeding strategies, which consist of alternating RUF consumption with meals and dividing intake throughout the day, may not be feasible in practice, due to school and transporta- tion constraints, especially when a child is pre- scribed up to 4 sachets per day.

Moreover, self-stigma was reported by some children who so feared adverse reactions that they hid from others when eating RUF. In this study, where barely one-third of children were informed of their HIV status, HIV-associated stigma with RUF was not mentioned. In Southern Africa, where HIV-associated stigma with RUF is wide- spread, this has ultimately led to poor adherence

9,10,22

Sharing of RUF with people beyond the imme- diate family was common (and probably under- reported) in our study, thus depleting the nutritional supplement available to the child. Food insecurity was highly prevalent in these

HIV-affected households, and it is likely that other family members would need nutritional support. Sharing were commonly reported in individual-targeted HIV food programs where ‘‘food by prescription’’ is mostly used to focus

evaluated.
In this study, overall adherence with ‘‘by

weight’’ RUF prescription was rather low and stable from the beginning, at around 50%, corre- sponding to an average of 2 sachets consumed daily. Similar to our results, a study in Vietnam reported that 65% and 81% of RUTF prescription was consumed by HIV-infected children <5 years

in adult outpatients.
prevalence country, RUF seems at this time to remain associated with child health and nutrition.

In Senegal, a low HIV

The effectiveness and feasibility of food-based interventions for the entire family, distributed by HIV clinics to com- plement individual-targeted food aid, need to be on HIV-related wasting. and adults, respectively.

Of note, in that study,

children received 1 dose and adults received 2

doses daily during a 4-week period. The combi-

nation of previously mentioned factors, such as

boredom with RUF, lack of time to consume,

self-stigmatization, and sharing within family,

may explain this poor adherence result. Assess-

ment of adherence to RUF in HIV-infected

adults, prescribed 2 to 4 sachets daily for 3 to

12 months, suggested that 2 sachets would be a

physiologically and socially acceptable

outpatient RUF-based protocols had a successful weight recovery. Median duration to recovery in MAM children was 54 days, whereas for SAM children, it was nearly twice as long, at 114 days. Daily weight gains, 1.4 and 1.3 g/kg in MAM and SAM children, respectively, were by far lower than those reported in HIV-infected SAM chil- dren <5 years under similar RUTF protocols27-31 but were found to be highly consistent with

8 HIV-infected adults’ weight gain outcomes. In

older children and adolescents, slow weight gain and its corollary, longer recovery duration, are likely to strongly affect acceptability of such out- patient RUF-based protocols. Effectively, improvement in weight is hardly perceptible by the patient, his/her caregiver, and the health worker and might present a risk of discourage- ment (such situations were observed within the study). In addition, coming to the HIV clinic

9,22,23

option.
Ultimately, 25 of the 43 children enrolled in

34

Food and Nutrition Bulletin 38(1)

every 2 weeks for a long period of time involves huge effort and constraints for undernourished children, who are largely at school and have a long commute to reach the clinic. This was the reason given by 9 children, all on ART and with undetectable viral load, for discontinuing their participation in the study after 63 days on aver- age. To partly alleviate this burden, monthly follow-up visits would be more appropriate for children in school. However, it would involve massive RUF provision (1 box 1⁄4 12 kg), which in turn could create difficulties with transporta- tion because of physical weakness and stigmati- zation due to noticeable branded boxes, household storage, and increased sharing as pilot intervention, it was designed for a short duration and had limited funding, so thus enrolled only a small number of patients as and when they came to their routine care. Second, the results were obtained in a research context, providing free medical support and remuneration for travel costs to attend the frequent visits. Although the findings may not be generalizable to all under- nourished HIV-infected children and adolescents, they provide initial data on the overall acceptabil- ity and feasibility of outpatient RUF-based pro- tocols among undernourished HIV-infected children 􏰁5 years. As such, they allowed for the funding and scaling up of these therapeutic pro- tocols within an operational research study in HIV-infected children that started in early 2015 and is currently ongoing at the national level in Senegal.

We reported a satisfactory rate of successful weight recovery in children on ART, despite high levels of food insecurity and a suboptimal con- sumption of RUF. However, this pilot study high- lights several acceptability issues of major concern, as they may lead to decreasing adher- ence to RUF protocols in the long term and directly impact the effectiveness of outpatient therapies. All in all, nutritional rehabilitation is likely to remain a long-term challenging experi- ence that is mainly tolerated by the young patients. Beyond the organoleptic barriers con- cerning RUF, a simplified intervention design as well as strengthened and continuous psychosocial support appear to be determinant and beneficial areas to invest in order to improve the social acceptability of outpatient nutritional rehabilitation. As such, our findings are a source of operational evidence on the management of nutritional rehabilitation in this vulnerable population.

Authors’ Note

CC and MV formulated the research question and designed the study. MV, NGH, and ABD conducted the study. CC performed the analysis and wrote the first draft of the manuscript. All authors read and com- mented on drafts and approved the final version of the manuscript. No donor had any part in the study design, analysis or writing of this manuscript.

The ANRS 12279 MAGGSEN Cohort Study Group

Study sites: (1) Centre Hospitalier National d’Enfants Albert Royer (Dakar, Senegal): Haby Sy Signate (investigator); Aminata Diack Mbaye, Helene Mbodj, Ndeye Fatou Diallo and Ndeye Rama Diagne (study clinicians and coinvestigators); Aissata Ba, Aicha Dia (study clinicians); Ndeye Ngone Have, Astou Dieye (social workers); Henriette Faye (mid- wife); Oumy Fall (nurse); Rosine Sonko (laboratory technician); and Natalia Laschina (psychologist). (2) Synergie pour l’Enfance/Centre Hospitalier Roi Bau- douin (Guediawaye, Senegal): Ngagne Mbaye (inves- tigator); Baly Ouattara and Maty Diouf (study clinicians and coinvestigators); Abdou Kader Niang (nurse); Alhadji Bassine Diom, Adama Ndour (social workers); and Bigue Badiane (laboratory technician). Supporting institutions: Agence Nationale de Recherches sur le SIDA et les he ́patites virales, France: Brigitte Bazin (Sponsor Representative). Study Coor- dination: Institut de Recherche pour le De ́veloppement (IRD), Montpellier, France: Cecile Cames (study coor- dinator), Philippe Msellati (investigator), Lea Pascal (study analyst), Amady Ndiaye (study technician), Suzanne Izard (data manager), Caroline Desclaux- Sall (doctoral fellow), Ousseynou Ndiaye and Binta Seck (biologists), and Ibrahima Diallo (study monitor, until June 2013).

Acknowledgments

The authors gratefully acknowledge all the participat- ing children and their caregivers. They also acknowl- edge the United Nations Child’s Fund and the World Food Programme country offices in Senegal for the provision of Plumpy Nut and Plumpy Sup, respec- tively, within the study. They sincerely thank David Masson (Sidaction) for his critical review of the

reported in HIV-infected adults.
This study has 2 important limitations. As a

Cames et al 35

manuscript and his valuable advice in the interpretation of the results.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publi- cation of this article.

Funding

The author(s) disclosed receipt of the following finan- cial support for the research, authorship, and/or publi- cation of this article: Financial support to the MAGGSEN Cohort was provided by the Agence Nationale de Recherche sur le SIDA et les he ́patites virales (ANRS) (grant number: 12279).

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