World Journal of AIDS, 2011, 1, 169-181
doi:10.4236/wja.2011.14025 Published Online December 2011 (http://www.SciRP.org/journal/wja)
Copyright © 2011 SciRes. WJA
169
Effective Therapeutic Feeding with Chickpea
Sesame Based Ready-to-Use Therapeutic Food
(CS-RUTF) in Wasted Adults with Confirmed or
Suspected AIDS
Paluku Bahwere1,2, Hedwig Deconinck3, Theresa Banda1, Steve Collins1
1Valid International, Oxford, UK; 2School of Public Health, Free University of Brussels, Brussels, Belgium; 3Save the Children,
Westport, USA.
E-mail: {paluku, theresa, steve}@validinternational.org, hdeconinck@gmail.com
Received September 1st, 2011; revised October 7th, 2011; accepted October 23rd, 2011.
ABSTRACT
Wasting has been observed as a common feature of the human immunodeficiency virus (HIV) disease since the first
reports and its presence increases the risk of death. There is no consensus on how to manage wasting associated with
HIV. The goal of this study was to assess the effectiveness of a locally made Chickpea Sesame Based RUTF (CS-RUTF)
in treating wasting associated with HIV in developing countries. Chronically sick adults from Mangochi Health District
(Malawi) with wasting and confirmed or presumptive clinical diagnosis of HIV were recruited for the study. Subjects
received a daily ration of 500 grams of CS-RUTF for 3 to 5 months. Nutrition status changes and mortality were used
to assess the effectiveness of the intervention. There were 3 patterns of anthropometric responses continuous weight
gain (WG), static weight (SW) and continuation weight loss (WL). The distribution of the 3 patterns is 53.9% (82/154)
for the WG pattern, 9.1% (14/154) for the SW pattern and 37.0% (57/154) for the WL pattern. For the WG pattern, the
overall median weight gain was 4.6 (2.4 to 7.1) kg. It was 5.7 (3.5 to 7.8) kg for those who completed 3 months of sup-
plementation. MUAC and BMI changes followed similar pattern than weight change. Not being on HAART, acute diar-
rhoea during follow up, episode of reduced appetite during follow up, missing at least one visit were identified as risk
factors for intervention failure. Overall, 38.5% (72/187) of study participants died during the intervention. In conclu-
sion, despite that the study confirms the limited impact of food based interventions on mortality among wasted HIV pos-
itive individuals, it also suggests that supplementation with CS-RUTF may be an effective intervention for reversing
wasting associated with HIV if combined with HAART and specific treatment of severe opportunistic infection causing
diarrhoea and reducing appetite.
Keywords: AIDS, Wasting, Nutrition Therapy, Ready-to-Use Therapeutic Food
1. Introduction
HIV/AIDS is not just a public health problem but it is a
major developmental concern of the century [1-5]. The
pandemic has reduced the size and productivity of the
workforce as a result of excess mortality, prolonged ill-
ness that causes frequent absenteeism and a reduced
working capacity [4,6-8]. Wasting, defined convention-
ally as the involuntary loss of 10% or more of one’s
premorbid weight, contributes to this situation through an
association with fatigue and an increased risk of death
[9-12].
Wasting has been observed as a feature of HIV disease
since the first reports of the condition [13,14]. In indus-
trialized countries, the prevalence of wasting in People
Living with HIV (PLHIV) varies between 17 percent and
50% [15-18]. In developing countries, this prevalence is
difficult to determine as premorbid weight is rarely
known, however, studies using the criteria Body Mass
Index (BMI) < 18.5 kg/m2 or MUAC < 22.0 cm for
women and <23.0 cm for men, have demonstrated a
prevalence at the time of commencing HAART of up to
25% [12,19-22]. This is almost certainly an underestima-
tion of the true prevalence of wasting as many more
PLHIV loose more than 10% of their premorbid weight
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
170
in Wasted Adults with Confirmed or Suspected AIDS
without meeting the BMI or MUAC criteria mentioned
above.
There is now good evidence to confirm that the pres-
ence of wasting is associated with increasing risk of
mortality in PLHIV [11,12,16,19,23-25]. In the pre-
HAART era, studies conducted in high-income countries
showed that wasting was associated to up to 13.7% of
death with individuals with moderate to severe wasting
having 1.9 and 6.7 more risk of dying within the year,
respectively [25,26]. Similar results have been reported
in West Africa where Van der Sande et al. noted that the
baseline BMI recorded within three months of the diag-
nosis of HIV infection is a strong and independent pre-
dictor of mortality and the predictive power was as good
as that of CD4 cell count [19]. In their study, patients
with a BMI below 16 were 6.4 times more likely to die
than individuals with a BMI above 22 kg/m2 and those
with BMI below 18 kg/m2 were 3.4 times more likely to
die than those with a BMI above 18 kg/m2 [19]. Studies
have shown that even after the advent of Highly Active
AntiRetroviral Therapy (HAART), the mortality among
PLHIV with wasting at the time of commencing HAART
remain high [11,12,21]. In a retrospective study evaluat-
ing the outcomes of patients on HAART in Singapore,
Paton et al found that BMI < 17 was a strong independ-
ent predictor of death with an adjusted hazard ratio of 2.2
[11]. A study in Malawi also found that patients with
BMI < 16, 16 to 16.9 and 17 to 18.4 had, after adjust-
ment for confounding, a 6.0, 2.4 and 2.1 fold higher risk
of dying respectively within the first 3 months of
HAART treatment than those who had a BMI 18.5
kg/m2 at HAART commencement [12]. Similar results
have been reported for many other developing countries
including Burkina Faso, Tanzania and Zambia [21,
27-31].
At present there is no consensus on how to manage
PLHIV with wasting or other forms of malnutrition [32].
Various studies have examined nutritional interventions
in the form of oral supplementation or total parenteral
nutrition and many of these studies have reported persis-
tence of high mortality in wasted adults receiving nutri-
tion supplementation in combination or not with HAART
[23,32-34]. The most popular nutrition supplement used
in resource-poor countries to combat wasting in PLHIV
is corn soya blend mixed with vegetable oil. The first
scientific evaluation on the impact of this intervention
was conducted in Malawi within the Bangwe home based
care programme, indicated that it had a limited impact on
the nutritional status and the survival of PLHIV admitted
in the programme with advanced HIV [23]. In contrast to
the Bangwe findings, anecdotal results obtained with the
Ready to Use Therapeutic Food (RUTF) in Malawi in
children as well as in adults were encouraging [35-37].
Up to 59% of HIV positive malnourished children treated
in Dowa community-based Therapeutic Care (CTC) pro-
gramme, recovered with RUTF alone in absence of
HAART. The majority of those who recovered retained a
good nutritional status after an average 15.5 months after
discharge from the programme [35]. A pilot programme
conducted by Valid International has also shown that
RUTF can be used to treat malnutrition in chronically
sick adults at home through home based care programme
structures [36]. In this programme, 54% of bedridden
adults improved their physical activity by at least one
grade in the Karnofsky score within the first 2 weeks of
the treatment; this was accompanied with improvements
in nutritional status [36]. The goal of the study was to
confirm the findings of the pilot study and identify fac-
tors affecting the effectiveness of therapeutic feeding
with RUTF and describe its benefits on a larger study
group. This paper reports on the impact of the therapeutic
feeding intervention on nutrition parameters, including
anthropometric parameters, haemoglobin, physical activ-
ity performance measured by the Karnofsky score and
the handgrip, and body composition.
2. Methods
2.1. Setting
The study was implemented in the Mangochi Health Dis-
trict, Malawi, between October 2006 and May 2007.
Mangochi lies at the southern tip of Lake Malawi. The
district had a population of around 778,338 in 2007. Al-
though fishing is the main income generating activity of
the district, subsistence farming employs 90% of the
population. The estimated prevalence of HIV in the dis-
trict was 21% in 2007. In the district, stigmatization is a
major barrier to access health care. As a consequence
both HIV testing and enrolment HAART programme are
often delayed and the compliance poor. Reasons cited for
this include fear of stigmatization, cost of transport and
food insecurity. Save the Children and ten Community
Based Organisations (CBOs) work to support PLHIV and
all the participants were recruited within their catch-
ment’s areas. Free HAART was available in the area
from government or mission hospital and one of the 10
CBOs offered transportation to their clients from the
CBO office to the HAART clinic.
2.2. Study Design and Procedures
Chronically sick adults were eligible for enrolment in the
study if they met one of the following criteria: 1) living
in the catchment area of a participating CBO; 2) con-
firmed or presumptive clinical diagnosis of HIV and 3)
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF) 171
in Wasted Adults with Confirmed or Suspected AIDS
MUAC < 22.0 cm or BMI < 17 kg/m2 or confirmed
weight loss > 10% or bilateral pitting oedema of the feet
or legs. Exclusion criteria included diabetes, hypertension,
known renal insufficiency, long term physical disability
or inability to eat.
The key interventions included 1) nutrition education
and counselling to participants and their caregivers and 2)
Nutrition Support with Chickpea Sesame Based RUTF
(CS-RUTF) and 3) Medical support: including Cotri-
moxazole prophylaxis and treatment for minor diseases,
referral and linkage with nearest health facility for man-
agement of severe medical conditions and the nearest
HAART clinic for treatment.
At admission, MUAC, weight, height, sitting height
and presence of bilateral oedema were checked to con-
firm nutrition status. Participants were classified as
wasted if they had a MUAC < 22.0 cm for women and
<23.0 cm for men or BMI < 18.5 kg/m2. They were clas-
sified as severely wasted when BMI was <16 kg/m2 or
MUAC < 18.5 kg/m2.
The physical activity performance was measured using
the Karnofsky scores and Eastern Cooperative Oncology
Group (ECOG) score and handgrip. A brief medical his-
tory and physical examination was conducted to deter-
mine the clinical WHO HIV stage and identify existing
morbidity. Blood was taken, to measure haemoglobin
and CD4 count. The haemoglobin level was determined
using a Hemacue haemoglobinometer (HeamaCue AB,
Angelholm,Sweden) and participants with haemoglobin
below 8 g/dl were classified as severely anaemic. Analy-
ses for estimation of CD4 count were done using Fluo-
rescence Activated Cell Sorter (FACS) count flow cy-
tometer (Becton Dickinson, Singapore) at the University
of North Carolina Project Laboratory in Lilongwe.
Study participants were followed up at week 2,
month1 and then monthly during the therapeutic feeding
phase. After discharge from the therapeutic feeding
phase, study participants were followed up quarterly
during 12 months. Clinical and nutrition data were col-
lected at each follow up. Additionally, information on
CS-RUTF intake was collected during the therapeutic
feeding phase. Calculation of CS-RUTF intake was
based on self-reporting (total number of pots eaten and
daily intake during the period under review). This infor-
mation was completed by the counting of terminated
empty pots. Household food security conditions and the
intake of additional foods were assessed at admission and
during follow up. The intake of additional foods was
assessed on a 24-hour and a 7-day food intake recall ap-
proach.
Study participants were discharged from the therapeu-
tic feeding phase if they reached the discharge criteria of
MUAC > 23.0 cm (minimum and maximum stay in the
programme of 12 and 20 weeks) or if they decided to
abandon the study or if they moved out from the study
catchment area of the study or if they died. For the fol-
low up after therapeutic feeding phase, participants were
censored if they completed the 12 months or if they
moved out of the study area or if they died.
For this study, the weight loss prior to admission was
estimated using the mean weight of rural adults Mala-
wian published by Zverev and Chisi. Nutrition status
improvement was assed using both physical activity per-
formance criteria and anthropometric criteria. The phy-
sical activity performance criteria included improvement
in Karnofsky score and increase in handgrip while the
anthropometric criteria include weight, MUAC and BMI
gains and achievement of the MUAC discharge criteria.
We arbitrary defined static weight as a weight change
500 g.
2.3. Study Food
The composition of the CS-RUTF has been previously
published [36]. Subjects were recommended to consume
two pots (500 g) providing 2600 kilocalories, 61.5 g of
proteins and >1 RDI for all the vitamins and minerals per
day. The aim was to provide the daily requirements but
participants were allowed to eat other family food be-
cause it was not suitable and impossible to impose a
monotonic diet for 3 to 5 months
2.4. Data Analyses and Statistics
Data analyses were performed using SPSS 10.0 for
Windows (SPSS Inc., Chicago, IL, USA). Quantitative
data for normally distributed variables were described
using means and standard deviation (SD) and compared
using Student’s t-test for 2 group comparisons and
ANOVA test for multiple group comparisons; non-nor-
mally distributed variables were described using median
and inter-quartile range (IQR) and compared using the
Kruskall Wallis test. Dichotomous variables were com-
pared using the Pearson or the McNemar χ2 test as ap-
propriate. The associations between change in nutrition
status and variables upon admission and follow up were
explored using the bivariate analysis followed by a step-
wise logistic regression. For the logistic regression
analysis, all the methods (enter, forward and backward)
were used to identify the potential independent predictors.
The enter method was used for the final models that in-
cluded all variables selected by each of the methods.
Wald statistics were used to test the statistical signifi-
cance of the variables retained in the final model.
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
in Wasted Adults with Confirmed or Suspected AIDS
Copyright © 2011 SciRes. WJA
172
2.5. Ethical Considerations
The research protocol was submitted to the National
Health Sciences Research Committee (NHSRC) and the
NHSRC provided ethical approval under the number 407.
Participation was voluntary. Before inclusion participants
signed a consent form after receiving complete informa-
tion on study objectives and procedures. The consent
form that was in englesh and local language included the
authorisation to participate into the study and of the pub-
lication of findings. The participant had the right to with-
draw from the study at any time, during the study period.
3. Results
Characteristics of Participants and Their
Households
Overall, 194 individuals were enrolled into the study.
Among them, 59.8% (116/194) had an HIV confirmed
diagnosis. From the remaining, 7 later tested HIV nega-
tive (Negative Eliza test and CD4 count between 645 and
1464 cells/µl.) and the others were later confirmed
HIV-infected. Based on the WHO clinical staging for
HIV, almost all participants had clinical advanced AIDS.
While 25.7% (48/187) had started HAART before en-
rolment, 5.9% (11/187) started HAART during the
therapeutic feeding phase. Tabl e 1 shows that the major-
ity of participants enrolled were female and young. More
than a third had never attended school. 79.4% of the
study participants had stopped working because of illness
and more than 60% were bedridden (Karnofsky score <
50%) and required considerable support in daily living
activities. Almost one third of them described their own
health condition as poor, very poor or terrible. Coping
strategies for household food insecurity were common
among participants: 93.0% (180/194) used certain coping
strategies before enrolment. Only 2.6% of participants
had eaten food from the 6 different food group the day
Table 1. Socio-demographic pr ofile and he alth condition of the participants at admission.
n %
Sex
Male 58 31.0
Female 129 69.0
Total 187 100.0
Age
Mean (SD) 34.1 (SD 9.2)
<18 year 3 16
18 - 49 years 164 88.2
>49 years 19 10.2
Total 186 100.0
Schooling level
Never attend school 65 34.8
Complete or incomplete primary school 105 56.1
Secondary school 12 6.4
Missing data 5 2.7
Total 187 100.0
Working status
Working 25 13.4
Not working 155 82.9
Missing data 7 3.7
Total 187 100.0
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF) 173
in Wasted Adults with Confirmed or Suspected AIDS
Karnofsky score
90: Able to perform normal activity; minor signs and symptoms of disease 7 3.7
80: Able to perform normal activity with effort;some signs/symptoms of disease 19 10.2
70: Cares for self, unable to perform normal activity or to do active work 81 43.3
60: Requires occasional assistance but is able to care for most of own needs 31 16.6
50: Requires considerable assistance and frequent medical care 31 16.6
40: Requires special care and assistance; disabled 8 4.3
30: Hospitalisation indicated although death not imminent; severely disabled 2 1.1
20:Hospitalisation necessary, active supportive treatment required; very sick 5 2.7
10: fatal processes progressing rapidly; moribong 1 0.5
Data missing 2 1.1
Total 187 100.0
Self rating of health condition
Good or Excellent 4 2.1
Fair 93 49.7
Poor 50 26.7
Very poor or terrible 39 20.9
Data missing 1 0.5
Total 187 100.0
HIV WHO clinical stage
Stage 3 74 39.6
Stage 4 113 60.4
Total 187 100.0
CD4 count (Cells/microliter)
Median (IQR) 165 (IQR 85.5 - 348.0)
<50 28 15.0
50 - < 100 16 8.6
100 - < 200 40 21.4
200 - < 350 32 17.1
>350 37 19.8
Data missing 34 18.2
Total 187 100.0
Handgrip (kg)
<19.3 74 39.6
<19.3 113 60.4
Total 187 100.0
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
in Wasted Adults with Confirmed or Suspected AIDS
Copyright © 2011 SciRes. WJA
174
before admission into the study.
The nutrition status at admission is described in Table
2. Of note, two third of the participants had an estimated
weight loss greater than 10% and more than one third of
participants were found to be severely wasted with some
having also bilateral pitting oedema. The average hae-
moglobin was very low and severe anaemia was ob-
served in more than a third of the participants. At the
time of enrolment, women had likely loss more weight
than men [mean % (SD) weight loss 18.1 (10.8)% for
women and 7.8 (13.4)% for men; p < 0.001]. Similarly,
the estimated reduction in MUAC was more important in
women [mean (SD) 2.6(0.7) cm for women and 1.6 (0.6)
cm for men; p < 0.001]
At admission, all the 187 participants accepted to eat
RUTF after tasting it but 9 later stopped taking CS-
RUTF giving an overall dropout rate of 4.8% (9/187).
Self reported intake average (SD) was 255.3 (139.0)
g/day corresponding to 32.1(19.2) kcal/kg/day.
Anthropometric response to the therapeutic feeding
could be calculated for 154 out of 187 participants who
had at least one follow up visit. The overall median (IQR)
of weight gain at discharge was 0.9 (1.9 - 5.1)kg. It was
2.8 (1.7 - 6.6) kg for those who received the supplement
for a minimum of 3 months. There were 3 patterns of
anthropometric responses based on weight change namely
continuous weight gain (WG), static weight (SW) and
continuation of weight loss (WL). The distribution of the
3 patterns is 53.9% (82/154) for the WG pattern, 9.1%
(14/154) for the SW pattern and 37.0% (57/154) for the
WL pattern. The mean (SD) of reported daily CS-RUTF
intake per body weight was 36.2 (20.0) Kcal/kg/day for
the WG pattern, 30.2 (18.7) Kcal/kg/day for the SW pat-
tern and 29.6 (15.1) Kcal/kg/day for the WL pattern (p =
0.104). The duration into the therapeutic phase was also
not significantly different and was 99.4 (24.9) days fro
the WG pattern, 108 (32.6) days for the SW pattern and
91.9 (35.5) days for the WL pattern, respectively (p =
0.135). The median (IQR) weight gain according to the
anthropometric pattern response were 4.6 (2.4 to 7.1) kg
for the WG pattern, 0.1 (0.4 to 0.2) kg for SW pattern
and 2.8 (3.9 to 1.7) kg, for the WL pattern. Among
those who remained in the programme for a minimum of
3 months, the median (IQR) weight gain were 5.7 (3.5 to
7.8) kg for WG pattern (n = 58), 0.4 (0.5 to 0.0) kg for
the SW pattern (n = 6) and 2.5 (4.5 to 1.8) kg for WL
pattern (n = 28). The changes in MUAC, BMI, and hand-
grip for the different patterns are presented in Table 3.
The differences in changes of MUAC, BMI and handgrip
from admission to discharge were statistically significant.
The difference was more important when only those who
received the therapeutic food for at least 3 months were
Table 2. Nutrition status at admission.
Variable n %
Estimated percentage weight loss
Mean (SD) 15.9 (SD 12.8)
10% 122 65.2
5% -< 10% 27 14.4
<5% 33 17.6
Missing 5 2,7
Total 187 100.0
MUAC
Mean (SD) 19.6 (SD 1.9)
<16.0 7 3.7
16.0 < 18.5 38 20.3
18.5 < 22.0 127 67.9
22.0 12 6.4
Data missing 3 1.6
Total 187 100.0
BMI
Mean (SD) 16.3 (SD 1.9)
<16.0 68 36.4
16.0 < 17.0 37 19.8
17.0 < 18.5 51 27.3
18.5 20 10.7
Data missing 11 5.9
Total 187 100.0
Oedema
Present 25 13.4
Absent 162 86.6
Total 187 100.0
Hemoglobin (g/l)
Mean (SD) 8.8 (SD 1.2)
<8.0 61 32.6
8.0 103 55.1
Data missing 23 12.3
Total 187 100.0
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF) 175
in Wasted Adults with Confirmed or Suspected AIDS
Table 3. Changes in anthropometric parameters and hand-
grip according to the response pattern.
Variables n Median (IQR) p
ALL participants
MUAC (cm)
Continous weight gain 83 2.4 (1.2 to 3.8)
Static weight 14 0.2 (0.7 to 0.8)
Continous weight loss 57 0.8 (1.5 to 0.1)
p < 0.001
BMI (kg/m2)
Continous weight gain 83 1.7 (0.8 to 2.7)
Static weight 14 0.0 (0.2 to 0.0)
Continous weight loss 57 1.1 (1.6 to 0.7)
p < 0.001
Handgrip (kg)
Continous weight gain 82 2.6 (0.3 to 6.5)
Static weight 13 0.2 (4.0 to 1.5)
Continous weight loss 54 2.4 (4.5 to 0.4)
p < 0.001
Supplemented for at least
3 months
MUAC (cm)
Continous weight gain 59 3.2 (2.2 to 4.2)
Static weight 6 0.5 (1.2 to 1.7)
Continous weight loss 29 0.6 (1.8 to 0.7)
p < 0.001
BMI (kg/m2)
Continous weight gain 59 2.3 (1.1 to 3.0)
Static weight 6 0.1 (0.2 to 0.0)
Continous weight loss 29 1.2 (1.7 to 0.7)
p < 0.001
Handgrip (kg)
Continous weight gain 59 5.1 (1.7 to 8.7)
Static weight 6 1.6 (5.9 to 0.1)
Continous weight loss 29 2.2 (5.0 to 0.4)
p < 0.001
compared (Table 3).
The increase in proportion of participants able to per-
form all the activity of daily living increased from 18.3%
(15/82) to 69.5% (57/82) for the WG group (MacNemar
test p < 0.001) and from 13.9% (13/72) to 33.3% (24/72)
for the combined SW and WL group (MacNemar test p =
0.030). For self perception of health condition, the pro-
portion of those judging their health condition to be fair
to excellent increased significantly from 42.7% (35/82)
to 89.0% (73/82) for the WG group (p < 0.001) while the
increase that was from 43.7% (31/71) to 62.0% (44/71)
was not statistically significant for the combined SW and
WL group (p = 0.597). Overall, 38.5% (72/187) of study
participants died. The mortality was 19.3% (16/83) for
the WG group, 35.7% (5/14) for the SW group and
47.4% (27/57) for the WL group (p = 0.002). Out of the
33 for whom weight change profile could not be calcu-
lated, 72.7% (24/33) died. Among the WG group, 49.4%
(41/83) fulfilled the discharge criteria of MUAC 23 cm.
Table 4 presents the parameters recorded at admission
or during the supplementation phase associated with
weight gain in bivariate and logistic regression analyses.
Of note, being on HAART and adhering to the number of
visits were significantly and independently associated
with increased chances of nutritional status improvement
while the occurrence of episodes of acute diarrhoea, and
complaint of poor appetite during supplementation nega-
tively affected weight change.
As shown on Figure 1, the percentage of patients be-
longing to the WG varied according to the number of risk
factors (not yet on HAART, acute diarrhoea during fol-
low up, episode of reduced appetite during follow up,
missing at least one visit). All participants who did not
have any of the risk factors gained weight while only
14.3% of those with all the risk factors were classified as
belonging to WG pattern group (p < 0.001). The mean
(SD) weight gain was 6.1 (2.9) kg for those without any
of the risk factor, 3.9 (5.2) kg in presence of 1 risk factor,
1.4 (4.9) kg in presence of 2 risk factors, 0.8 (3.5) kg in
presence of 3 risk factors and 2.1 (2.9) kg in presence of
4 risk factors.
4. Discussion
The protocol for the management of wasting in HIV in-
dividuals from household from food insecure settings is
yet to be established [32,38-40]. This situation is blamed
on the absence of evidence that can help developing
sound guidelines [32,41]. The present study has contrib.-
uted on the development of the evidence by demonstrat-
ing that wasting in PLHIV living in a context of wide-
spread household food insecurity can be effectively re-
versed with fortified energy dense food such us CS-
RUTF and that the effectiveness may be enhanced when
the supplementation is integrated to other therapeutic
intervention including HAART and appropriate treatment
of underlying opportunistic infection.
Wasting remains an important comorbidity in AIDS
patients in populations with as it is associated with in-
creased mortality and its frequency remains high [11,
12,21,27,31,34]. A recent large study that evaluated the
prevalence among patient starting HAART in Lusaka
found that 17% of the 40,788 registered during the study
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
in Wasted Adults with Confirmed or Suspected AIDS
Copyright © 2011 SciRes. WJA
176
Table 4. Admission characteristics associated wit h weight gain pattern.
Unadjusted OR Adjusted OR
Variable n % gained weight OR (95% CI)p OR (95% CI) p
Model for admission parameters
ART status
Commenced prior to enrollment 39 76.9 4.0 (1.6 - 10.0)<0.001 2.7 (1.0 - 7.1) 0.042
Not commenced at enrollement 112 45.5 1.0 1.0
Oral diseases
Present 15 26.7 0.3 (0.1 - 1.0) 0.028 0.3 (0.1 - 1.1) 0.066
Absent 136 56.6 1.0 1.0
HIV testing status
Tested at enrollment 85 62.4 2.2 (0.9 - 4.3) 0.015 1.6 (0.7 - 3.5) 0.230
Not tested at enrollment 66 42.4 1.0 1.0
Gender
Male 46 65.2 2.0 (0.9 - 4.3) 0.059 0.6 (0.3 - 1.3) 0.222
Female 105 48.6 1.0 1.0
Model for incident events
ART status
Commenced† 50 70.0 2.8 (1.3 - 6.8) 0005 3.6 (1.6 - 8.1) 0.002
Not commenced 101 45.5 1.0 1.0
Missed visits
None 66 65.2 2.3 (1.3 - 4.7) 0.012 2.5 (1.2 - 5.3) 0.014
>=1 85 44.7 1.0 1.0
Complaint of reduced appetite
At least once during follow up 57 36.8 0.3 (0.2 - 0.7) 0.001 0.4 (0.2 - 0.9) 0.024
No complaint 94 63.2 1.0 1.0
New episode of acute diarrhea
At least once during follow up 48 43.8 0.6 (0.3 - 1.2) 0.096 0.4 (0.2 - 0.9) 0.036
None 94 58.3 1.0 1.0
New episode of fever
At least once during follow up 57 36.8 0.4 (0.2 - 0.9) 0.017 0.5 (0.2 - 1.1) 0.087
None 94 63.2 1.0 1.0
Combined model
ART status
Commenced† 50 70.0 2.8 (1.3 - 6.8) 0.005 3.4 (1.5 - 7.8) 0.003
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF) 177
in Wasted Adults with Confirmed or Suspected AIDS
Not commenced 101 45.5 1.0 1.0
Missed visits
None 66 65.2 2.3 (1.3 - 4.7) 0.012 2.5 (1.2 - 5.3) 0.016
>=1 85 44.7 1.0 1.0
Complaint of reduced appetite
At least once during follow up 57 36.8 0.3 (0.2 - 0.7) 0.001 0.4 (0.2 - 0.9) 0.028
No complaint 94 63.2 1.0 1.0
New episode of acute diarrhea
At least once during follow up 48 43.8 0.6 (0.3 - 1.2) 0.096 0.4 (0.2 - 1.0) 0.053
None 94 58.3 1.0 1.0
New episode of fever
At least once during follow up 57 36.8 0.4 (0.2 - 0.9) 0.017 0.6 (0.2 - 1.2) 0.126
None 94 63.2 1.0 1.0
Oral disease at admission
Yes 15 26.7 0.3 (0.1 - 1.0) 0.027 0.6(0.2 - 2.2) 0.370
No 136 53.6 1.0 1.0
Not retained: peristent fever, persistent diarrhea, severe cough, hemoglobin level, CD4 count, Karnofsky score, handgrip, self perception of health condition,
working status, walking status, marital status, food security condition, headache, BMI of admiss.
Figure 1. Percentage of participant with nutrition status improvement according to number of indepe nde nt risk fac t or s.
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
in Wasted Adults with Confirmed or Suspected AIDS
Copyright © 2011 SciRes. WJA
178
period had a BMI < 17 kg/m2 and the figure was 34% if
the cutoff of 18.5 kg/m2 was used [31]. In addition,
evaluation of various HAART programmes have demon-
strated that the presence of wasting at the time of com-
mencing HAART, increases, by up to 6 times, the early
(3-month) mortality [12,21,27]. The present study that
was conducted at the start of the scale up of free HAART
confirms that wasting is likely to remain common at the
time of diagnosing HIV as most of the HIV infected
wasted individuals enrolled into the study were not yet
tested. Thus, for Malawi and most resource-poor coun-
tries wasting in PLHIV remains an important public
health problem given the contribution of this pandemic to
the overall mortality of young adults [42].
Given the public health importance of wasting of
PLHIV, it is essential for countries affected by the HIV
pandemic to identify an effective intervention that can
reverse the wasting process while improving the quality
of life of PLHIV. Several studies have now shown that
therapeutic feeding with RUTF is a promising interven-
tion [32,34-37]. A pilot study that included 60 HIV
wasted adults already demonstrated the acceptability and
tolerance of CS-RUTF used in the present study [36].
The pilot study also demonstrated a clear link between
the amount of CS-RUTF intake and weight gain [36]. In
a cohort of wasted individuals staring HAART in Malawi,
supplementary feeding with RUTF was associated with
higher weight gain than supplementary feeding with por-
ridge made from a corn soya fortified blended floor [34].
Several findings of the present study confirm the CS-
RUTF effectiveness. Despite the overall low weight gain
observed in the present study and the low recovery rate,
the fact that adherence to the programme doubled the
chances of gaining weight, the impressive weight gain of
6 kg when there were no detrimental risk factor, the
higher increase in proportion of those with normal
physical activity performance and those rating their
health condition as fair to excellent among the WG pat-
tern group when compared to the other groups, strongly
suggest that the intervention was effective.
The results of the present study showing that some of
the patients had static weight or continued to loose
weight despite good intake of CS-RUTF don’t have to be
interpreted as an indication of ineffective therapeutic
feeding. The apparently poor response was rather the
consequence of the chronic inflammatory process that
can be controlled by the adjunction of HAART as sug-
gested by the strong independent relationship between
HAART and the response pattern. It also outlines the fact
that these patients usually present other comorbidity that
interfere with nutrition recovery such us diarrhoea and
oral candidiasis. HIV infection and many other chronic
infections contribute to the development of wasting
through an inflammatory process leading to cachexia and
authors have observed that a food based intervention
alone cannot reverse the cachexia process [43]. Thus, the
judgment on the effectiveness of a therapeutic feeding
intervention in PLHIV should take into account the qual-
ity of the management of HIV itself and of the other co-
morbidities.
The detrimental effect on the response to therapeutic
feeding interventions targeting PLHIV of factors identi-
fied in this study namely absence of HAART, diarrhoea
and oral disease have been reported before [44-47]. In
study carried out in the pre-HAART era, Howard et al.
obtained 8% recovery rate with home parenteral nutrition
after 12 months in studies conducted in north America
and Europe [48]. For diarrhoea, Beaugerie et al found a
direct interrelation between the clinical severity of diar-
rhoea and malnutrition in PLHIV, Carbonnel et al. noted
that most HIV adults with weight loss of a cohort of 66
individuals had diarrhoea associated with malabsorption
and Stack et al showed that weight loss in wasted HIV
infected individuals with diarrhoea can occur despite a
good intake of therapeutic food [44,46,49]. In regards of
our findings and that of the literature cited, severe wast-
ing should be considered as an independent criterion for
initiating HAART. Interestingly, the WHO staging crite-
ria currently include moderate involuntary weight loss
(<10%) as a stage 3 condition and severe involuntary
weight loss (>10%) as a stage 4 condition. Unfortunately,
these criteria are not practical as in many resource-poor
countries premorbid weight is unknown. Consequently,
the level of wasting is not always used for initiating
HAART. Thus, we suggest the replacement of the weight
loss criteria by criteria based on anthropometric meas-
urement as already suggested by other authors [50,51].
The high mortality rate of 38.5% observed in the pre-
sent study has to be interpreted taking into account the
fact that most of people enrolled were very sick. Almost
half of them rated their health condition at admission as
poor or very poor, a quarter was bedridden and unable to
care for self and a third of the deaths occurred among
those for whom we could not calculate weight change
because the death occurred within 2 weeks of admission
before the second visit. Also, only 25.7% of them have
started HAART at the time of admission. However, the
mortality we observed is not very much higher than the
3.5-month mortality of 27% reported by Ndekha et al.
among wasted individuals treated at the teaching hospital
of Malawi for whom nutritional therapy was instituted at
the same time with HAART [34]. A similar high mortal-
ity of up to 88% was reported for small cohorts of AIDS
patients on home parenteral nutrition in industrialized
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF) 179
in Wasted Adults with Confirmed or Suspected AIDS
countries during the pre-HAART era [52-57]. This situa-
tion suggests that further reduction of the mortality of
wasted PLHIV will probably depends in addition to early
HAART initiation and effective therapeutic feeding, on
the capacity of HAART programmes to diagnose and
treat specific life threatening opportunistic infections.
5. Conclusions
In conclusion, despite some methodological limitations
including the observational design of the study that pre-
vent us from confidently attributing the observed effect
to this intervention only, the limited number of partici-
pants that prevented some sub-analyses, the use of self-
reported intake to estimate intake that may have resulted
in overestimation of intake and adherence, the present
study suggest that supplementation with CS-RUTF is an
effective intervention for reversing wasting in PLHIV but
has limited impact on mortality. Its effectiveness is likely
to be improved by concomitant initiation of HAART and
specific treatment of severe opportunistic infection. Thus,
we recommend the use of CS-RUTF or other similar
products for the management of wasting of PLHIV. In
patients not yet on HAART, this intervention should not
delay HAART initiation but should be used to enable and
faster initiate HAART.
6. Competing Interests
HD had no competing interest. But all the authors work
for Valid International, a company sister to Valid Nutri-
tion a charity organization that promotes local production
of Ready-To-Use Therapeutic Food. SC is also an unpaid
director of Valid Nutrition. The Chickpea Sesame Ready-
To-Use Therapeutic Food used for the study was bought
from Valid Nutrition in Malawi with funding from Save
The Children US.
7. Authors’ Contribution
All the authors contributed to the design, implementation,
interpretation of the findings and write up.
8. Acknowledgements
The authors would like to acknowledge the invaluable
assistance of the Save Children Malawi country office
and staff and all the program participants and their fami-
lies. They also acknowledge the great contribution of all
Valid International Malawi staff for the success of the
study. Special thanks for Laura Banks, for editing the
manuscript. Funding for this work was provided by Save
Children US. All the authors contributed to the design,
implementation, interpretation of the findings and write
up. Written consent for publication was obtained from
the patients.
REFERENCES
[1] G. Anabwani and P. Navario, “Nutrition and HIV/AIDS
in Sub-Saharan Africa: An Overview,” Nutrition, Vol. 21,
No. 1, 2005, pp. 96-99. doi:10.1016/j.nut.2004.09.013
[2] T. Atinmo and D. Oyewole, “Finding Solutions to the
Nutritional Dilemmas in Africa for Child Health: HIV/
AIDS Orphans, Poverty and Hunger,” Asia Pacific Jour-
nal of Clinical Nutrition, Vol. 13, 2004, p. S6.
[3] R. Danziger, “The Social Impact of HIV/AIDS in Devel-
oping Countries,” Social Science & Medicine, Vol. 39,
No. 7, 1994, pp. 905-917.
doi:10.1016/0277-9536(94)90203-8
[4] K. Ojo and M. Delaney, “Economic and Demographic
Consequences of AIDS in Namibia: Rapid Assessment of
the Costs,” International Journal of Health Planning and
Management, Vol. 12, No. 4, 1997, pp. 315-326.
doi:10.1002/(SICI)1099-1751(199710/12)12:4<315::AID
-HPM492>3.0.CO;2-A
[5] W. Hladik, J. Musinguzi, W. Kirungi, et al., “The Esti-
mated Burden of HIV/AIDS in Uganda, 2005-2010,”
AIDS, Vol. 22, No. 4, 2008, pp. 503-510.
doi:10.1097/QAD.0b013e3282f470be
[6] M. O. Bachmann and F. L. Booysen, “Health and Eco-
nomic Impact of HIV/AIDS on South African House-
holds: A Cohort Study,” BMC Public Health, Vol. 3, No.
4, 2003, p. 14. doi:10.1186/1471-2458-3-14
[7] M. O. Bachmann and F. L. Booysen, “Relationships be-
tween HIV/AIDS, Income and Expenditure over Time in
Deprived South African Households,” AIDS Care, Vol.
16, No. 7, 2004, pp. 817-826.
doi:10.1080/09540120412331290220
[8] M. Bakari, W. Urassa, K. Pallangyo, et al., “The Natural
Course of Disease Following HIV-1 Infection in dar es
Salaam, Tanzania: A Study among Hotel Workers Relat-
ing Clinical Events to CD4 T-Lymphocyte Counts,”
Scandinavian Journal of Infectious Diseases, Vol. 36, No.
6-7, 2004, pp. 466-473.
doi:10.1080/00365540410016249
[9] D. P. Kotler, J. Wang and R. N. Pierson, “Body Compo-
sition Studies in Patients with the Acquired Immunodefi-
ciency Syndrome,” American Journal of Clinical Nutri-
tion, Vol. 42, No. 6, 1985, pp. 1255-1265.
[10] D. P. Kotler, A. R. Tierney, J. Wang and R. N. Pierson Jr.,
“Magnitude of Body-Cell-Mass Depletion and the Timing
of Death from Wasting in AIDS,” American Journal of
Clinical Nutrition, Vol. 50, No. 3, 1989, pp. 444-447.
[11] N. Paton, S. Sangeetha, A. Earnest and R. Bellamy, “The
Impact of Malnutrition on Survival and the CD4 Count
Response in HIV Infected Patients Starting Antiretroviral
Therapy,” HIV Medicine, Vol. 7, No. 5, 2006, pp. 323-
330. doi:10.1111/j.1468-1293.2006.00383.x
[12] R. Zachariah, M. Fitzgerald, M. Massaquoi, et al., “Risk
Factors for High Early Mortality in Patients on Antiretro-
viral Treatment in a Rural District of Malawi,” AIDS, Vol.
20, No. 18, 2006, pp. 2355-2360.
doi:10.1097/QAD.0b013e32801086b0
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
180
in Wasted Adults with Confirmed or Suspected AIDS
[13] R. D. Mugerwa, L. H. Marum and D. Serwadda, “Human
Immunodeficiency Virus and AIDS in Uganda,” East Af-
rican Medical Journal, Vol. 73, No. 1, 1996, pp. 20-26.
[14] D. Serwadda, R. D. Mugerwa, N. K. Sewankambo, et al.,
“Slim Disease: A New Disease in Uganda and Its Asso-
ciation with HTLV-III Infection,” Lancet, Vol. 326, No.
8460, 1985, pp. 849-852.
doi:10.1016/S0140-6736(85)90122-9
[15] J. Ockenga, R. Grimble, C. Jonkers-Schuitema, et al.,
“ESPEN Guidelines on Enteral Nutrition: Wasting in HIV
and Other Chronic Infectious Diseases,” Clinical Nutri-
tion, Vol. 25, No. 2, 2006, pp. 319-329.
doi:10.1016/j.clnu.2006.01.016
[16] A. M. Tang, “Weight Loss, Wasting, and Survival in
HIV-Positive Patients: Current Strategies,” AIDS Read,
Vol. 13, Suppl. 12, 2003, pp. S23-S27.
[17] G. O. Coodley, M. O. Loveless and T. M. Merrill, “The
HIV Wasting Syndrome: A Review,” Journal of Acquired
Immune Deficiency Syndromes, Vol. 7, No. 7, 1994, pp.
681-694.
[18] U. Suttmann, J. Ockenga, O. Selberg, L. Hoogestraat, H.
Deicher and M. J. Muller, “Incidence and Prognostic
Value of Malnutrition and Wasting in Human Immunode-
ficiency Virus-Infected Outpatients,” Journal of Acquired
Immune Deficiency Syndromes & Human Retrovirology,
Vol. 8, No. 3, 1995, pp. 239-246.
doi:10.1097/00042560-199503010-00004
[19] M. A. van der Sande, M. F. Schim van der Loeff, A. A.
Aveika, et al., “Body Mass Index at Time of HIV Diag-
nosis: A Strong and Independent Predictor of Survival,”
Journal of Acquired Immune Deficiency Syndromes, Vol.
37, No. 2, 2004, pp. 1288-1294.
doi:10.1097/01.qai.0000122708.59121.03
[20] S. Siziya, R. Mwendapole and A. F. Fleming, “Clinical
Features of HIV Seropositive Zambian Subjects,” African
Journal of Medicine & Medical Sciences, Vol. 24, 1995,
pp. 173-178.
[21] J. S. Stringer, I. Zulu, J. Levy, et al., “Rapid Scale-Up of
Antiretroviral Therapy at Primary Care Sites in Zambia:
Feasibility and Early Outcomes,” Journal of the Ameri-
can Medical Association, Vol. 296, No. 7, 2006, pp. 782-
793. doi:10.1001/jama.296.7.782
[22] A. Dannhauser, A. M. van Staden, R. E. van der, et al.,
“Nutritional Status of HIV-1 Seropositive Patients in the
Free State Province of South Africa: Anthropometric and
Dietary Profile,” European Journal of Clinical Nutrition,
Vol. 53, No. 3, 1999, pp. 165-173.
doi:10.1038/sj.ejcn.1600691
[23] C. Bowie, L. Kalilani, R. Marsh, H. Misiri and P. Cleary,
“An Assessment of Food Supplementation to Chronically
Sick Patients Receiving Home Based Care in Bangwe,
Malawi: A Descriptive Study,” Nutrition Journal, Vol. 4,
2005, p. 12. doi:10.1186/1475-2891-4-12
[24] A. M. Tang, J. Forrester, D. Spiegelman, T. A. Knox, E.
Tchetgen and S. L. Gorbach, “Weight Loss and Survival
in HIV-Positive Patients in the Era of Highly Active
Antiretroviral Therapy,” Journal of Acquired Immune De-
ficiency Syndromes, Vol. 31, No. 2, 2002, pp. 230-236.
doi:10.1097/00126334-200210010-00014
[25] R. Thiebaut, D. Malvy, C. Marimoutou and F. Davis,
“Anthropometric Indices as Predictors of Survival in AIDS
Adults. Aquitaine Cohort, France, 1985-1997,” European
Journal of Epidemiology, Vol. 16, No. 7, 2000, pp. 633-
639. doi:10.1023/A:1007696530440
[26] D. A. Wheeler, C. L. Gibert, C. A. Launer, et al., “Weight
Loss as a Predictor of Survival and Disease Progression
in HIV Infection. Terry Beirn Community Programs for
Clinical Research on AIDS,” Journal of Acquired Im-
mune Deficiency Syndromes & Human Retrovirology,
Vol. 18, No. 1, 1998, pp. 80-85.
doi:10.1097/00042560-199805010-00012
[27] A. Johannessen, E. Naman, B. J. Ngowi, et al., “Predic-
tors of Mortality in HIV-Infected Patients Starting Anti-
retroviral Therapy in a Rural Hospital in Tanzania,” BMC
Infectious Diseases, Vol. 8, 2008, p. 52.
doi:10.1186/1471-2334-8-52
[28] N. Saleri, S. Capone, V. Pietra, et al., “Outcome and Pre-
dictive Factors of Mortality in Hospitalized HIV-Patients
in Burkina Faso,” Infection, Vol. 37, No. 2, 2009, pp.
142-147. doi:10.1007/s15010-008-7406-7
[29] S. D. Lawn, A. D. Harries and R. Wood, “Strategies to
Reduce Early Morbidity and Mortality in Adults Receiv-
ing Antiretroviral Therapy in Resource-Limited Settings,”
Current Opinion in HIV and AIDS, Vol. 5, 2010, pp.
18-26.
[30] J. R. Koethe and D. C. Heimburger, “Nutritional Aspects
of HIV-Associated Wasting in Sub-Saharan Africa,”
American Journal of Clinical Nutrition, Vol. 91, No. 4,
2010, pp. 1138S-1142S. doi:10.3945/ajcn.2010.28608D
[31] J. R. Koethe, A. Lukusa, M. J. Giganti, et al., “Associa-
tion between Weight Gain and Clinical Outcomes among
Malnourished Adults Initiating Antiretroviral Therapy in
Lusaka, Zambia,” Journal of Acquired Immune Deficiency
Syndromes, Vol. 53, No. 4, 2010, pp. 507-513.
doi:10.1097/QAI.0b013e3181b32baf
[32] J. R. Koethe, B. H. Chi, K. M. Megazzini, D. C. Heim-
burger and J. S. Stringer, “Macronutrient Supplementa-
tion for Malnourished HIV-Infected Adults: A Review of
the Evidence in Resource-Adequate and Resource-Con-
strained Settings,” Clinical Infectious Diseases, Vol. 49,
No. 5, 2009, pp. 787-798. doi:10.1086/605285
[33] S. Mahlungulu, L. A. Grobler, M. E. Visser and J. Vol-
mink, “Nutritional Interventions for Reducing Morbidity
and Mortality in People with HIV,” Cochrane Database
of Systematic Reviews, Vol. 18, No. 3, 2007, CD004536.
[34] M. J. Ndekha, J. J. van Oosterhout, E. E. Zijlstra, M.
Manary, H. Saloojee and M. J. Manary, “Supplementary
Feeding with Either Ready-to-Use Fortified Spread or
Corn-Soy Blend in Wasted Adults Starting Antiretroviral
Therapy in Malawi: Randomised, Investigator Blinded,
Controlled Trial,” British Medical Journal, Vol. 338,
2009, b1867.
Copyright © 2011 SciRes. WJA
Effective Therapeutic Feeding with Chickpea Sesame Based Ready-to-Use Therapeutic Food (CS-RUTF)
in Wasted Adults with Confirmed or Suspected AIDS
Copyright © 2011 SciRes. WJA
181
[35] P. Bahwere, E. Piwoz, M. C. Joshua, et al., “Uptake of
HIV Testing and Outcomes within a Community-Based
Therapeutic Care (CTC) Programme to Treat Severe
Acute Malnutrition in Malawi: A Descriptive Study,”
BMC Infectious Diseases, Vol. 8, 2008, p. 106.
doi:10.1186/1471-2334-8-106
[36] P. Bahwere, K. Sadler and S. Collins, “Acceptability and
Effectiveness of Chickpea Sesame-Based Ready-to-Use
Therapeutic Food in Malnourished HIV-Positive Adults,”
Patient Preference and Adherence, Vol. 3, 2009, pp. 67-75.
[37] M. J. Ndekha, M. J. Manary, P. Ashorn and A. Briend,
“Home-Based Therapy with Ready-to-Use Therapeutic
Food Is of Benefit to Malnourished, HIV-Infected Mala-
wian Children,” Acta Paediatrica, Vol. 94, No. 2, 2005,
pp. 222-225. doi:10.1111/j.1651-2227.2005.tb01895.x
[38] C. Fields-Gardner and P. Fergusson, “Nutrition Interven-
tion in the Care of Persons with Human Immunodefi-
ciency Virus Infection: Position of the American Dietetic
Association and Dietitians of Canada,” Canadian Journal
of Dietetic Practice and Research, Vol. 65, No. 3, 2004,
pp. 132-135. doi:10.3148/65.3.2004.132
[39] S. Grinspoon and K. Mulligan, “Weight Loss and Wast-
ing in Patients Infected with Human Immunodeficiency
Virus,” Clinical Infectious Diseases, Vol. 36, Suppl. 2,
2003, pp. S69-S78. doi:10.1086/367561
[40] D. P. Kotler, “Nutritional Alterations Associated with
HIV Infection,” Journal of Acquired Immune Deficiency
Syndromes, Vol. 25, Suppl. 1, 2000, pp. S81-S87.
doi:10.1097/00042560-200010001-00013
[41] J. W. C. Hsu, P. B. Pencharz, D. C. Macallan and A.
Tomkins, “Macronutrients and HIV/AIDS: A Review of
Current Evidence,” World Health Organization, Durban,
10-13 April 2005.
[42] H. V. Doctor and A. A. Weinreb, “Estimation of AIDS
Adult Mortality by Verbal Autopsy in Rural Malawi,”
AIDS, Vol. 17, No. 17, 2003, pp. 2509-2513.
doi:10.1097/00002030-200311210-00014
[43] L. Howard, L. Heaphey, C. R. Fleming, L. Lininger and E.
Steiger, “Four Years of North American Registry Home
Parenteral Nutrition Outcome Data and Their Implica-
tions for Patient Management,” Journal of Parenteral and
Enteral Nutrition, Vol. 15, No. 4, 1991, pp. 384-393.
doi:10.1177/0148607191015004384
[44] L. Beaugerie, F. Carbonnel, F. Carrat, et al., “Factors of
Weight Loss in Patients with HIV and Chronic Diarrhea,”
Journal of Acquired Immune Deficiency Syndromes &
Human Retrovirology, Vol. 19, No. 1, 1998, pp. 34-39.
doi:10.1097/00042560-199809010-00005
[45] O. Y. Bushen, J. A. Davenport, A. B. Lima, et al., “Diar-
rhea and Reduced Levels of Antiretroviral Drugs: Im-
provement with Glutamine or Alanyl-Glutamine in a
Randomized Controlled Trial in Northeast Brazil,” Clini-
cal Infectious Diseases, Vol. 38, No. 12, 2004, pp. 1764-
1770. doi:10.1086/421394
[46] J. A. Stack, S. J. Bell, P. A. Burke and R. A. Forse,
“High-Energy, High-Protein, Oral, Liquid, Nutrition Su-
pplementation in Patients with HIV Infection: Effect on
Weight Status in Relation to Incidence of Secondary In-
fection,” Journal of the American Dietetic Association,
Vol. 96, No. 4, 1996, pp. 337-341.
doi:10.1016/S0002-8223(96)00095-8
[47] D. L. Jacobson, I. Bica, T. A. Knox, et al., “Difficulty
Swallowing and Lack of Receipt of Highly Active Anti-
retroviral Therapy Predict Acute Weight Loss in Human
Immunodeficiency Virus Disease,” Clinical Infectious
Diseases, Vol. 37, No. 10, 2003, pp. 1349-1356.
doi:10.1086/379072
[48] L. Howard, “Home Parenteral Nutrition: Survival, Cost,
and Quality of Life,” Gastroenterology, Vol. 130, No. 2,
2006, pp. S52-S59. doi:10.1053/j.gastro.2005.09.065
[49] F. Carbonnel, L. Beaugerie, R. A. Abou, et al., “Macro-
nutrient Intake and Malabsorption in HIV Infection: A
Comparison with Other Malabsorptive States,” Gut, Vol.
41, No. 6, 1997, pp. 805-810. doi:10.1136/gut.41.6.805
[50] P. J. Peters, I. Zulu, N. G. Kancheya, et al., “Modified
Kigali Combined Staging Predicts Risk of Mortality in
HIV-Infected Adults in Lusaka, Zambia,” AIDS Research
and Human Retroviruses, Vol. 24, No. 7, 2008, pp.
919-924. doi:10.1089/aid.2007.0297
[51] A. R. Lifson, S. Allen, W. Wolf, et al., “Classification of
HIV Infection and Disease in Women from Rwanda.
Evaluation of the World Health Organization HIV Stag-
ing System and Recommended Modifications,” Annals of
Internal Medicine, Vol. 122, 1995, pp. 262-270.
[52] H. Bakker, F. Bozzetti, M. Staun, et al., “Home Par- en-
teral Nutrition in Adults: A European Multicentre Survey
in 1997. ESPEN-Home Artificial Nutrition Working
Group,” Clinical Nutrition, Vol. 18, 1999, pp. 135-140.
[53] D. M. Richards, J. J. Deeks, T. A. Sheldon and J. L.
Shaffer, “Home Parenteral Nutrition: A Systematic Re-
view,” Health Technology Assessment, Vol. 1, No. 1,
1997, pp. 1-59.
[54] J. C. Melchior, C. Chastang, P. Gelas, et al., “Efficacy of
2-Month Total Parenteral Nutrition in AIDS Patients: A
Controlled Randomized Prospective Trial. The French
Multicenter Total Parenteral Nutrition Cooperative Group
Study,” AIDS, Vol. 10, No. 4, 1996, pp. 379-384.
doi:10.1097/00002030-199604000-00005
[55] P. Bouletreau, M. Gerard, B. Messing, et al., “Home
Parenteral Nutrition and AIDS,” Clinical Nutrition, Vol.
14, Vol. 85, 1995, pp. 213-218.
doi:10.1016/S0261-5614(95)80002-6
[56] P. Singer, M. M. Rothkopf, V. Kvetan, O. Kirvela, J.
Gaare and J. Askanazi, “Risks and Benefits of Home
Parenteral Nutrition in the Acquired Immunodeficiency
Syndrome,” Journal of Parenteral and Enteral Nutrition,
Vol. 15, No. 1, 1991, pp. 75-79.
doi:10.1177/014860719101500175
[57] B. Messing, D. Barnoud, P. Beau, et al., “A 1993-1995 Epi-
demiological Survey of Home Parenteral Nutrition in Ap-
proved Centers for Adults in France,” Gastroenterologie
Clinique et Biologique, Vol. 22, No. 4, 1998, pp. 413-418.