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Outpatient treatment of severe acute malnutrition: response to

treatment with a reduced schedule of therapeutic food distribution1,2


Sheila Isanaka,3–5* Stephen R Kodish,3 Fatou Berthé,6 Ian Alley,5 Fabienne Nackers,5 Kerstin E Hanson,7 and
Rebecca F Grais4,5

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3
Departments of Nutrition and 4Global Health and Population, Harvard T.H. Chan School of Public Health, Boston, MA; and 5Epicentre and 6Epicentre Niger,
and 7Médecins Sans Frontières, Operational Center Paris, Paris, France

ABSTRACT of severe acute malnutrition (SAM)8 (1). Today’s community-


Background: Community-based management of severe acute mal- based model represents a historic shift away from exclusive
nutrition (SAM) has been shown to be safe and cost-effective, but inpatient care in the clinical management of SAM, wherein the
program coverage remains low. Treatment models that maintain majority of children with SAM presenting without clinical
high levels of clinical effectiveness but allow for increased coverage complications and sufficient appetite benefit from outpatient
are still needed. A reduced schedule of follow-up, in which children care, and inpatient management is reserved for stabilization of
receive clinical follow-up and therapeutic foods on a monthly rather complicated cases. Outpatient care, including either weekly or
than weekly basis, may be one alternative. biweekly clinical follow-up at a health facility, was made pos-
Objective: We aimed to describe the safety and feasibility of a sible in part by the development of ready-to-use therapeutic
monthly distribution of ready-to-use therapeutic food (RUTF) in foods (RUTFs). RUTFs are energy-dense pastes that provide all
the treatment of uncomplicated SAM, in terms of clinical response of the macro- and micronutrients needed for recovery from
to treatment and household RUTF use. SAM, and they can be safely administered at home. The shift to
Design: We conducted a nonrandomized pilot intervention study in outpatient care places increased responsibility on caregivers to
which 115 children eligible for outpatient treatment of SAM were supervise therapeutic feeding at home, but adequate weight gain,
provided a monthly ration of RUTF. Anthropometric measurements high recovery (i.e., .80%), and low mortality (i.e., 1–5%) have
were taken weekly for 4 wk to monitor treatment response. Un- nevertheless been achieved across various settings (2–7).
announced household spot checks were conducted over 4 wk to Although community-based management of SAM can be cost-
assess household use of RUTF and storage practices. effective (8–10), program coverage remains exceedingly low:
Results: Adequate weight and midupper arm circumference (MUAC)
globally, only 7–13% of children with SAM received treatment
gain were found throughout the 4-wk follow-up period. Observed
in 2012 (11). New treatment models that maintain high levels of
mean 6 SD weight gain from admission was 9.8 6 6.8 g $ kg21 $ d21
clinical effectiveness but allow for increased coverage are still
in week 1 and 4.2 6 2.1 g $ kg21 $ d21 by week 4. Unplanned
needed. A reduced schedule of follow-up, in which children
household spot checks found an average surplus of RUTF sachets com-
receive clinical follow-up and RUTF on a monthly rather than
pared with the number expected based on the date of distribution and
weekly or biweekly basis, may be one alternative. A monthly
recommended dosing throughout the 4 wk of follow-up. The frequency
schedule of follow-up has the potential to reduce the burden on
at which more than the recommended dose was used (i.e., deviance
of .2 sachets between available and expected stocks) was 4% and 22% caregivers associated with frequent visits to a health facility,
of households visited in week 1 and week 4, respectively. reduce program costs through improved efficiency associated
Conclusion: Adequate treatment response and RUTF use in the with larger patient volumes, and offer greater operational flex-
outpatient treatment of SAM was maintained over 4 wk of ibility to provide treatment in contexts in which security or
follow-up with a monthly schedule of RUTF distribution. This study geography do not allow frequent visits. Such changes could be
was registered at clinicaltrials.gov as NCT02994212. Am J 1
Clin Nutr 2017;105:1191–7. Funding for this study was provided by Médecins Sans Frontières
Operational Center Paris.
2
Supplemental Figure 1 is available from the “Online Supporting Mate-
Keywords: ready-to-use therapeutic food, RUTF, severe acute rial” link in the online posting of the article and from the same link in the
malnutrition, SAM, community-based management of acute online table of contents at http://ajcn.nutrition.org.
malnutrition, CMAM, treatment response, household utilization *To whom correspondence should be addressed. E-mail: sheila.isanaka@
epicentre.msf.org.
8
Abbreviations used: MSF, Médecins Sans Frontières; MUAC, midupper
arm circumference; RUTF, ready-to-use therapeutic food; SAM, severe acute
INTRODUCTION
malnutrition; WHZ, weight-for-height z score.
Since 2007, the community-based management of acute Received November 3, 2016. Accepted for publication March 10, 2017.
malnutrition has become the standard of care for the management First published online April 12, 2017; doi: 10.3945/ajcn.116.148064.

Am J Clin Nutr 2017;105:1191–7. Printed in USA. Ó 2017 American Society for Nutrition 1191
1192 ISANAKA ET AL.

expected to reduce barriers to program uptake and make more Standard care
resources available, allowing programs to reach more children in All children received standard care for outpatient treatment of
need. A reduced schedule of follow-up, however, could in- uncomplicated SAM, as per MSF and government of Niger
fluence individual response to treatment. Between monthly guidelines. At the time of admission, children received RUTF
visits, adequate nutritional recovery would largely depend on (14 sachets/wk for those who weighed ,8 kg, and 21 sachets/wk
caregivers’ abilities to manage a larger household RUTF stock for those who weighed $8 kg in the routine nutrition program)
and adhere to treatment instructions over a longer period. and routine medicines (i.e., vitamin A, amoxicillin, and anti-
Task shifting has been shown to be effective in clinical settings helminthic treatment, and, if appropriate, measles vaccination
other than childhood malnutrition, such as in HIV care and and antimalarial treatment) to treat and prevent complications.
treatment (12). However, there is limited experience in how Follow-up in the outpatient nutritional program was conducted
increased responsibility placed on caregivers and a reduced on a weekly basis at the health center. At each visit, a physical
schedule of follow-up would influence individual treatment re-

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exam and anthropometric assessment were conducted. Anthro-
sponses in the context of SAM treatment. To inform the safety pometric measurements [weight to the nearest 100 g, length (for
and feasibility of a reduced monthly schedule of follow-up in the children ,24 mo of age) or standing height (for children
treatment of uncomplicated SAM, we conducted a non- $24 mo of age) to the nearest 0.1 cm, and MUAC to the nearest
randomized pilot intervention study to assess the response to 0.1 cm] were assessed with the use of standard techniques (16).
treatment and household use of RUTF in a series of children with Nutritional recovery was determined at or after 3 wk if a child
SAM under a monthly schedule of RUTF distribution. had a WHZ $22 in 2 consecutive visits and a MUAC
$115 mm, no acute complication or edema for $7 d, and
completed all antibiotic and antimalaria treatment at the time of
METHODS discharge. Children were transferred to the hospital in the event
Study site and subjects of any clinical complication requiring inpatient management or
weight loss .5% between 2 consecutive visits or lack of weight
The study was carried out in the Madarounfa Health District of gain after 3 wk. Caregivers were instructed to return to the
the Maradi region of south-central Niger along the Nigerian health center for any health concerns between scheduled study
border. The area is rural and largely representative of the Sahel visits, and treatment was provided free of charge.
region, where subsistence agriculture and animal husbandry are
the primary livelihoods (13). Acute childhood malnutrition is
endemic, with seasonal peaks from May until October because of
food shortages and infectious illnesses. The study period (July to Study procedures
November) specifically coincided with a period of decreasing At admission, study nurses collected background information
food security before the annual harvest and an increased risk of from participating caregivers, including maternal age and edu-
malaria during the rainy season in this setting. In collaboration cational status, child feeding practices and vaccination history,
with the Ministry of Health of Niger, Médecins Sans Frontières and household socioeconomic status, with the use of standardized
(MSF) has supported pediatric care in the Madarounfa Health questionnaires.
District since 2001. In 2014, the MSF-supported therapeutic For study participants, a 4-wk supply of RUTF (56 sachets/4 wk
feeding program treated .13,000 children with SAM, with 94% for those weighing ,8 kg and 84 sachets/4 wk for those
recovery, 2% default, ,1% nonresponse, and 3% mortality. weighing $8 kg) was provided on admission. Sachets distrib-
Study enrollment was conducted at 2 outpatient nutritional uted in the monthly ration were individually marked by unique
treatment sites. Study inclusion criteria included the following: 1) identifiers to distinguish study and nonstudy sachets, which
being eligible for new admission to treatment of uncomplicated could coexist within a single household as a result of inter-
SAM, and 2) being resident within 15 km of the study health household sharing. A plastic bucket was provided to facilitate
center. In accordance with the national protocol, a child was eli- transport and storage at home. Oral instructions were given for
gible for outpatient SAM treatment if he or she was aged between 6 recommended storage conditions and appropriate use at home,
and 59 mo; had a weight-for-height z score (WHZ) ,23 according advising caregivers to keep RUTF in the provided bucket or
to the 2006 WHO Growth Standards (14) and/or a midupper arm another cool, dry place away from direct sunlight.
circumference (MUAC) ,115 mm; had sufficient appetite ac- At the end of each admission visit, participants were accom-
cording to a test feeding of RUTF; and was free of clinical com- panied to their home to record the location of their residence.
plications requiring hospitalization, including severe edema (15). Participants returned to the health center on a weekly basis for a
Study exclusion criteria included any child who had previously minimum of 4 wk for physical exams and anthropometric as-
defaulted from previous SAM treatment (i.e., missed 2 consec- sessments, but no additional RUTF or instructions were provided
utive weekly visits), was considered a relapse (i.e., readmitted during those visits. Although treatment programs eventually
within 3 mo of previous discharge), or was not accompanied by a adopting a reduced RUTF distribution schedule may not have
parent or legal guardian $18 y of age. required weekly clinical follow-up, weekly follow-up was ensured
Parents or legal guardians were provided information re- in this pilot study as a safety precaution in light of this new
garding the study objectives and procedures and provided written distribution model. In addition, after baseline consent, un-
informed consent for their child’s participation before the start of announced spot checks were made weekly by research members at
any study activities. The study was approved by the Comité the participant’s home. Information on availability of the marked
Consultatif National d’Ethique, Niger, and the Comité de Pro- RUTF sachets and conditions of at-home RUTF storage was
tection des Personnes, Ile-de-France XI. collected with the use of standardized observation checklists.
WEIGHT GAIN WITH MONTHLY RUTF DELIVERY 1193
A primary objective of the study was to assess the safety of a TABLE 1
monthly distribution of RUTF, for which the risk was thought to Baseline characteristics of participants1
be most acute early in treatment, when weight gain and energy Characteristic Value
needs were greatest. Therefore, study follow-up ceased after
Maternal
4 wk. Participants not yet eligible for discharge as per program
Caregiver participants, n 115
guidelines after 4 wk returned to the standard weekly distribution Age, y 29.6 6 8.0
of RUTF rations until discharge and in accordance with national Ever attended school (not including Quranic school) 12 (10.4)
guidelines. Ever attended the nutritional program before 63 (54.8)
Child
Age, mo 18.4 6 8.6
Statistical analysis
Sex, F 65 (56.5)
To estimate the proportion of caregivers adherent to the rec- WHZ 23.0 6 0.6

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ommendations of the monthly RUTF ration at 4 wk with a ,23 59 (51.3)
precision of 610%, assuming a 50% risk, a = 0.05, and 15% MUAC 117.5 6 6.1
loss to follow-up, the minimum sample size was 114 caregivers ,115 34 (29.6)
HAZ 22.8 6 1.4
and children. Participant characteristics, including maternal
,23 48 (41.7)
characteristics and child anthropometric status, were summa- Times previously admitted to nutritional program
rized with the use of means 6 SDs for continuous measures and 0 65 (56.5)
proportions for discrete measures. Response to treatment in re- 1 32 (27.8)
covered children was summarized with the use of mean 6 SD $2 18 (15.7)
weight gain (grams per kilograms per day) and MUAC gain Values are means 6 SDs or n (%). HAZ, height-for-age z score;
1
(millimeters per day) from admission until program discharge MUAC, midupper arm circumference; WHZ, weight-for-height z score.
#4 wk from admission, as well as the count and proportion of
children with .5% weight loss or the development or worsening
of nutritional edema. loss .5% during follow-up in week 3 (n = 1) and week 4
RUTF use was assessed with weekly spot-check data as the (n = 1). No child developed or increased nutritional edema, and
deviance between the number of marked RUTF sachets available none died. Response to treatment under the monthly schedule of
and the number of sachets expected, based on the time since RUTF distribution is shown in Table 3. Both adequate weight
admission and prescribed dose of RUTF per child. and MUAC gains were found during the 4 wk of follow-up.
All data were double-entered into EpiData 3.1. SAS statistical Observed mean 6 SD weight gain from admission was 9.8 6
software version 9.3 was used for analysis. 6.8 g $ kg21 $ d21 in week 1, 7.4 6 4.0 g $ kg21 $ d21 by
week 2, 5.3 6 2.7 g $ kg21 $ d21 by week 3, and 4.2 6 2.1
g $ kg21 $ d21 by week 4. Observed mean 6 SD MUAC gain
RESULTS from admission was 0.6 6 0.6 mm/d in week 1, 0.5 6 0.3 mm/d
Between July and November 2014, 115 caregivers and their by week 2, 0.3 6 0.2 mm/d by week 3, and 0.3 6 0.2 mm/d by
children with uncomplicated SAM were included in the study week 4.
(Table 1). Caregivers were a mean of 29.6 6 8.0 y of age. Ten All 115 households were visited by the study team $1 time
percent of caregivers had ever attended school, and more than during follow-up, with a mean 6 SD 3.12 6 0.66 visits/
one-half (54.8%) had previous experience in nutritional pro- household over 4 wk. Household spot checks found a positive
grams. The mean 6 SD age of children was 18.4 6 8.6 mo. mean deviance over the 4 wk of follow-up, indicating a con-
More than one-half of the children were enrolled with a WHZ sistent average surplus of marked sachets compared with the
,23, and approximately one-third had a MUAC ,115 mm. number expected based on the date of distribution and recom-
Follow-up in the nutritional program from admission to week 4 mended dosing (Figure 1). Among households visited in week
is shown in Table 2 and Supplemental Figure 1. Weight loss 1, 68% of households were found with the correct RUTF use
.5% was infrequent, with 2 of 115 children (2%) receiving the (i.e., a deviance of 62 sachets between available and expected
monthly RUTF ration transferred to inpatient care for weight stocks), 4% of households having used more than expected and

TABLE 2
Follow-up in the nutritional program #4 wk1
Week 1 Week 2 Week 3 Week 4

Undergoing follow-up 104 (90.4) 80 (69.6) 62 (53.9) 31 (26.9)


Absent from scheduled visit 5 (4.3) 6 (5.2) 10 (8.7) 3 (2.6)
Discharged as recovered at this visit 0 (0) 22 (19.1) 11 (9.6) 36 (31.3)
Total discharged as recovered 0 (0) 22 (19.1) 33 (28.7) 69 (60.0)
Transferred to inpatient care at this visit 6 (5.2) 1 (0.9) 3 (0.9) 2 (1.7)
Weight loss .5% 0 (0) 0 (0) 1 (0) 1(0)
Development or worsening of 0 (0) 0 (0) 0 (0) 0 (0)
nutritional edema
Died 0 (0) 0 (0) 0 (0) 0 (0)
1
Values are n (%). n = 115.
1194 ISANAKA ET AL.
TABLE 3
Response to treatment over 4 wk of follow-up from admission1
Monthly RUTF distribution, Weekly RUTF distribution,2
Niger 2014 Niger 2012–2014

Weight gain, g $ kg21 $ d21 MUAC gain, mm/d Weight gain, g $ kg21 $ d21 MUAC gain, mm/d

n 106 101 1199 1199


Week 1 9.83 6 6.81 0.61 6 0.56 11.10 6 7.71 0.57 6 0.49
Week 2 7.39 6 4.04 0.48 6 0.33 6.97 6 4.33 0.39 6 0.31
Week 3 5.28 6 2.66 0.33 6 0.22 5.75 6 3.11 0.35 6 0.24
Week 4 4.20 6 2.05 0.28 6 0.19 5.03 6 2.54 0.32 6 0.20
1
Values are means 6 SDs unless otherwise indicated. MUAC, midupper arm circumference; RUTF, ready-to-use

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therapeutic food.
2
From reference 17.

29% of households having used less than expected at the time of throughout the 4 wk of follow-up. Study personnel observed the
the visit. Among households visited in week 4, the frequency of monthly ration to be most often stored inside the home (range:
correct use was 36% of households, with 22% having used more 95.8–98.8% across weeks 1–4), with no stock stored in direct
and 43% having used less than expected. sunlight. Most participants (range: 85.0–91.1%) used the plastic
Household spot checks revealed high levels of compli- bucket provided by the study for storage of the ration at home as
ance with adherence with suggested RUTF storage practices instructed.

FIGURE 1 Distribution of ready-to-use therapeutic food stocks available compared with those expected by week of follow-up: week 1 (A), week 2 (B),
week 3 (C), and week 4 (D).
WEIGHT GAIN WITH MONTHLY RUTF DELIVERY 1195
DISCUSSION the target child, including an improvement in child health, as
Among children receiving the monthly distribution of RUTF, well as prevention of diseases and malnutrition (C Langendorf,
both weight gain and MUAC gain were satisfactory. Anthro- Epicentre, personal communication, 2016).
pometric measurements, combined with household spot checks, Other reports describing the use of RUTFs are largely limited
suggested largely appropriate RUTF usage over the 4-wk follow- to the use of small-quantity formulations (#20 g) provided in the
up period. Use of the monthly ration represented more often prevention of malnutrition (26–30). The greater perceived risk
under- rather than overconsumption, based on the standard dosing associated with SAM, a life-threatening condition that requires
recommendations, and sufficient to maintain an adequate re- vigilant attention and care, may be an important determinant of
sponse to treatment. Few children experienced weight loss, and high compliance in our study in comparison with reports related
no child developed or had worsening edema during 4 wk of to the small-quantity formulations used in the context of pre-
follow-up. These results represent the first clinical experience vention. This, however, was not the case in Ethiopia, where
RUTF provided in SAM treatment was still perceived to be a

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with a monthly rather than weekly distribution of RUTF and
suggest this modality to be both safe and feasible for outpatient food or commodity for selling (31, 32).
management of uncomplicated SAM. In high-burden settings, the number of children with SAM who
Adequate treatment response in the outpatient management receive treatment may be constrained by limited human resources
of SAM relies in large part on appropriate therapeutic feeding and infrastructure to provide facility-based clinical follow-up.
at home. Experience has shown that adequate recovery from Using a reduced frequency of follow-up in such contexts
uncomplicated SAM can be achieved with weekly and bi- could allow more children to access care. A recent cost analysis
of SAM treatment in Niger suggested that important economies
weekly follow-up and distributions of RUTF (18). A reduced
of scale were possible, with per-child costs decreasing as patient
schedule of follow-up, however, would require caregivers to
volume increased because of fixed costs associated with per-
manage large RUTF stocks and adhere to dosing instructions
sonnel and infrastructure (33). The same cost analysis tool
over a longer period of time, potentially challenging the out-
suggests that a monthly schedule of follow-up, which simply
patient response to treatment.
increases the number of children who receive outpatient treat-
Despite the greater burden on caregivers, mean weight and
ment by 4-fold compared with a weekly schedule of follow-up,
MUAC gains in our study cohort compared favorably to min-
could reduce the cost per child treated by 52% ($166.39 com-
imum global program standards (19). Observed weight and
pared with $79.53). Although many interrelated factors con-
MUAC gains were consistent with other community-based
tribute to program coverage (e.g., physical access, opportunity
nutritional programs in which mean weight gain varied be-
costs, and awareness of the illness and available services), only
tween 3.0 and 6.8 g $ kg21 $ d21 (20) and mean MUAC gain
some of these would be addressed by a reduced schedule of
varied between 0.3 and 0.6 mm/d (21, 22) during recovery.
follow-up. The potential cost efficiencies, coupled with our
Response to treatment was also similar to those recorded in findings supporting the safety and feasibility of monthly follow-
children enrolled in a randomized trial in the same setting in up, however, suggest that this approach may be a promising
which a weekly distribution of RUTF and standard medical model to increase program coverage and reduce costs in the
care was provided (Table 3) (17). The favorable treatment re- treatment of uncomplicated SAM.
sponses noted in our study cohort thus suggest the clinical Our study had several strengths. First, we assessed household
safety of a monthly RUTF distribution in the management of RUTF compliance by triangulating data from household spot
uncomplicated SAM. checks with important clinical outcomes representing response to
Household use of ready-to-use products has been recognized treatment. Doing so was, to our knowledge, a novel way to
as an important barrier to program effectiveness (23), but data describe household RUTF use, as well as assess the safety and
on household use remains limited. Household spot-check data feasibility of an alternative RUTF distribution schedule. Second,
suggest that the majority of participants correctly used the although caregivers were aware of weekly spot checks, the home
monthly ration early in treatment, but this proportion decreased visits were conducted on unannounced days per times, lending
by the end of follow-up. Because weight gain did not appear to credibility to the findings observed. Repeated spot checks, as
falter, incorrect use does not appear to be at the expense of used in this study, may be a more valid measure of compliance
recovery. Anecdotal reports suggest that households may de- than self-report (34), which could be subject to social desirability
crease therapeutic feeding later in treatment once a child’s and recall biases.
weight and clinical status is recovered. In 2010, our group Limitations of the study include not being able to conduct
found that 65–80% of households enrolled in a large-scale in-home observations of RUTF use to determine individual
preventative program in Niger reported never sharing the intake. Directly observing household behaviors may have
provided ready-to-use supplement (24). In 2011, only 30–51% presented additional information on factors that influence
of households in Niger that were enrolled in a preventive compliance. However, more intrusive observations may have
program that provided supplemental foods to young children, been less acceptable. Because of safety concerns, a monthly
household food rations, and/or cash reported not sharing the ration was distributed, but the children enrolled in the study
provided supplement (25). Considering the limitations of self- continued weekly follow-up at the health facility. No guidance
report, compliance may have been even lower. However, ac- related to RUTF use or additional stock was provided during
companying qualitative interviews with participants conducted weekly facility visits to reduce any undue influence from the
by an independent study team confirmed the high value placed safety visits, but the study is not an exact representation of the
on RUTF by caregivers. The women perceived positive medi- model in question because of safety considerations. In addition,
cal and nutritional impacts from the nutritional supplements on given one of the study’s objectives to assess the early safety of
1196 ISANAKA ET AL.

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