World Journal of AIDS, 2012, 2, 252-258
doi:10.4236/wja.2012.23033 Published Online September 2012 ( 249
The Effect of Antiretroviral Therapy (ART) on Body
Composition and Clinical Markers of Lipodystrophy in
HIV-Infected Children Assessed in Follow-Up Study
Agnieszka B. Dzwonek1, Vas Novelli1, C. Smith2, Margaret Lawson3
1Clinical Infectious Diseases Unit, Great Ormond Street Children’s Hospital NHS Trust, London, UK; 2Research Department of In-
fection and Population Health, University College London Medical School, London, UK; 3Childhood Nutrition Research Centre,
Institute of Child Health, University College London, London, UK.
Email: Vas.
Received April 16th, 2012; revised May 16th, 2012; accepted June 1st, 2012
Objectives: An tiretroviral therapy (ART) has been associated with lipodystrophy in childr en. We evaluated chang es in
various anthropometric measurements for the assessment of lipodystrophy and assessed whether there was an associa-
tion with use of protease inhibitors (PI), non-PI containing ART and/or stavudine (d4T). Methods: Eighty-five
HIV-infected children attending the HIV clinic at Great Ormond Street Hospital (GOSH) were included. The average
follow-up was 8.4 months (range 3 - 12 months). Body fat redistribution was assessed by anthropometric measurements
including skinfold thickness and circumferences of upper and lower limbs. Measurements were converted to age- and
sex- adjusted z-scores through development stages including puberty. Results: Sixty children had taken ART; 37 re-
ceived PI-containing; 38 received d4T; 25 had never been treated. In the studied population, clinically important
changes with decreases in biceps (BSF), subscapular skinfolds and total body fat (4SFT) over period of 12 months were
observed. Some increase was noticed in triceps skinfolds (TSF). Limbs circumferences remained at the same level.
Further we looked at 4 months basis changes in anthropometric measurements stratified by baseline ART. Generally
z-scores of anthropometric measurements were lower in therapy naive children when compared to ART groups.
PI-based ART regimens resulted in significant increases in BSF with a trend towards increases in TSF, suprailiac and
4SFT. Mid-arm and thigh circumferences were higher in PI compared to naive group. Similarly, significant changes in
BSF z-scores were associated with d4T use. Increases were seen in TSF and mid-arm circumference and decreases were
observed in subscapular skinfolds and calf circumference z-scores. Conclusions: Body fat redistribution in HIV-in-
fected children with sub-clinical lipodystrophy could be detected by anthropometric measurements, particularly when
PI or d4T is included in ART. Over time, changes with increase in arm and trunk fat, and no change or decrease in leg
fat were more pronounced among ART-receiving children.
Keywords: Body Fat Redistribution; Anthropometric Measurements; HIV; Children; Art
1. Introduction
Although survival in HIV-infected children has greatly
improved with the introduction of antiretroviral therapy
(ART), a lipodystrophy syndrome has emerged [1-6].
This encompasses abnormal distribution of adipose tissue,
peripheral wasting, insulin-resistance and dyslipidaemia.
Children may be more vulnerable than adults because of
the potential impact of growth, as well as children’s
likely greater cumulative exposure [7].
The lipodystrophy syndrome has been mostly studied
via cross-sectional studies [2-6,8,9 ]. Determination of the
prevalence of lipodystrophy has b een compli cated by the
lack of an objective case definition for use in children.
Further, assessment of lipodystrophy is complicated by
the different methodologies used to assess its components
across studies.
The recent European Collaborative Study estimated a
42% prevalence of body fat abnormality in 426 HIV-
infected children and adolescents based on clinical ob-
servation (peripheral lipoatrophy and/or central lipo-
hypertrophy) [8]. A prevalence of fat abnormality in this
study was substantially higher than the proportion of
about 25% reported in other previous paediatric studies
Clinical lipodystrophy, metabolic changes and insu-
lin-resistance have been reported to worsen at puberty.
Some studies have shown that ethnicity, clinical condi-
tion, duration of HIV infection, nucleoside reverse tran-
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The Effect of Antiretroviral Therapy (ART) on Body Composition and Clinical Markers of Lipodystrophy
in HIV-Infected Children Assessed in Follow-Up Study 253
scriptase inhibitor (NRTI) and protease inhibitor (PI)
treatment were associated with lipodystrophy [9-12].
The objectives of this observational follow up study
were to investigate changes in anthropometric measure-
ments in a cohort of HIV-infected children on different
ART regimens over study period and to assess whether
there was an association between PI and d4T use with
these measurements.
2. Methods
2.1. Patients Population
We studied HIV-infected children older than three years
attending the HIV Family Clinic at Great Ormond Street
Children’s Hospital (GOSH) NHS Trust, London, UK
between 2002 and 2004. Relevant ethical approval was
granted by the Institute of Child Health and GOSH Re-
search Ethics Committee and Informed consent was ob-
tained. Recent steroid therapy or wasting from other
causes (e.g. disuse atrophy) were criteria for exclusion.
Of the 128 HIV-infected children identified as eligible
during the study period, 113 (88%) participated but only
those with follow-up visits (n = 85) were included in the
analysis. Clinical details and drug history were extracted
from the Collaborative HIV Paediatric Study (CHIPS)
database. The HIV clinic at GOSH follows Paediatric
European Network for Treatment of AIDS (PENTA)
guidelines for initiating antiretroviral therapy [13]. Gen-
erally, ART is started in p atients with persistently low or
declining CD4 counts, or with clinical deterioration.
2.2. Anthropometric Measurements
After study enrolment, measurements were taken at clinic
visits scheduled every three to four months. Trained phy-
sician for taking anthropometric measurements (AD)
collected data over 3 year’s period and all children who
attended HIV Family Clinic and who agreed on that par-
ticular visit to participate in the study were included in
the analysis. Before anthropometric measurements were
obtained, all children had a general physical examination,
including observation for clinical features of peripheral
lipoatrophy and central lipohypertrophy. Weight and
height were recorded, and body mass index (BMI: kg/m2)
was calculated. Skinfold thickness, triceps (TSF), biceps
(BSF), subscapular and suprailiac, were measured using
the Harpenden Skinfold Calliper (Holtain Ltd., Crymych
UK). The sum of these four skinfold sites was calculated
as an indication of total body fat. Peripheral adiposity
was assessed by measuring midupper arm (MAC), thigh
and calf circumferences using a narrow one-metre tape
(Chasmors Ltd., London UK). Triplicate skinfold and
circumference measurements were undertaken by the
same trained researcher (AD). The mean value of the
three measurements was used in the analysis. Skinfold
and circumference measurements were converted to age-
and sex-adjusted z-scores (the distance of the value from
the age- and sex-appropriate mean) using Dutch refer-
ence data and a SPSS programme developed at the Insti-
tute of Child Health, UCL, described previously [9,14].
2.3. Statistical Analyses
The dates of the first anthropometric measurements per-
formed on each child were defined as baseline. The 4-
month measurements of the anthropometric markers
were found by creating a window 2 months either side
(i.e. from 2 - 6 months), and the nearest measurement
that took place within this window was taken as the four
month measurement. Similar approach was used for 8
and 12 months. The median and interquartile range val-
ues at baseline, 4, 8 and 12 months for each anthro-
pometric measurement were calculated. Furthermore, the
change from baseline at 4, 8 and 12 months was also
calculated. This analysis was then repeated stratified by
antiretroviral regimen at baseline and compared using a
Kruskall Wallis test. Analyses were performed using
SAS version 9.0 (SAS Institute Inc., Cary, NC, USA).
3. Results
Amongst 113 children enrolled in the study between
2002 and 2004, 85 children had follow up anthropomet-
ric measurements. Their median (range) age was 9.7
years (3.0 - 15.7 years). All had vertically acquired HIV-
1 infection and 90% were of black Sub-Saharan African
origin. Eighty five children included in analyses had two
or more visits. The majority (n = 38) had three visits,
with 34 children having 2 visits and 13 having four or
more. These resulted in total of 237 clinic visits when
measurements were taken over study period. The average
time of observation was 0.7 years ranging from 3 to 12
months. Characteristics of the studied group are pre-
sented in Table 1. At enrolment, 51 children (60%) were
receiving ART therapy. Of these, 24 children (47%) were
receiving a protease inhibitor (PI) based regimen. Forty
one per cent of currently treated (21/51) children with
ART at the entry to the study received d4T, including 8
children who were receiving both a PI-s and d4T therapy.
Thirty-four children (40%) were not on any treatment at
enrolment, including 9 who had been previously treated,
but had stopped therapy in the 6 months before entry.
Twenty five children had never been treated with ART.
In the past, 37 children had been exposed to PI-based
ART and 38 children to d4T.
3.1. Study Population
The median (range) age- and sex-adjusted z-scores at the
Copyright © 2012 SciRes. WJA
The Effect of Antiretroviral Therapy (ART) on Body Composition and Clinical Markers of Lipodystrophy
in HIV-Infected Children Assessed in Follow-Up Study
Copyright © 2012 SciRes. WJA
Table 1. Characteristics of children included in the analysis at time of the first measurements.
N (%)
Number 85
Gender Male 37 (43.5%)
Female 48 (56.5%)
Age (years) Median (range) 9.7 (3.0 - 15.7)
CD4 T cells percentage <15% 17 (20.0%)
15% - 25% 27 (31.8%)
>25% 36 (42.3%)
Unknown 5 (5.9%)
Weight (kg) Median (range) 29.9 (14.8 - 68.4)
Height (cm) Median (range) 130.8 (93.7 - 181.9)
BMI (kg/m2) Median (range) 17.4 (13.6 - 25.8)
CDC stage A 23 (27.0%)
B 42 (49.4%)
C 20 (23.6%)
ART use Current 51 (60.0%)
Previous 9 (10.6%)
Never 25 (29.4%)
Total period of ART use (years) Median (range) 4.6 (0.0 - 13.9)
PI use Current 24 (28.25%)
Previous 37 (43.5%)
Never 24 (28.25%)
Total period of P I use (years) Median (range) 3.8 (0.0 - 5.5)
D4T use Current 21 (24.7%)
Previous 38 (44.7%)
Never 26 (30.6%)
Total period of d4T use (years) Median (range) 2.7 (0.0 - 5.4)
first visit when baseline anthropometric measurements
were taken for the 85 children for biceps, triceps, sub-
scapular, suprailiac skin folds and sum of four skin folds
were 1.22 (+0.22 - +2.5), +0.21 (–0.61 - +1.56), +1.34
(+0.12 - +3.14) , –0.43 (–1.00 - +0 .41) and +0.58 (–0 .37 -
+1.93), respectively. For mid arm, thigh and calf cir-
cumferences, these z-scores were –0.76 (–1.73 - +0.35),
–0.83 (–1.92 - –0.11) and -1.26 (–2.28 - –0.22). These
data are presented in Table 2. Clinically important
changes were observed in biceps skinfold thickness (BSF)
and subscapular skinfolds z-scores, with decrease in
z-scores measured over period of 12 months. Triceps
skinfolds (TSF) z-score showed some increase in 12
months, in comparison to baseline measurements. Mid-
arm (MAC), thigh and calf circumferences z-scores in-
creased over studied time when compare to baseline
z-scores measurements. Sum of four skinfolds z-scores
measurements did not appear to change over 12 months
observation period.
3.2. PI-s vs Naive Group 4-Month Changes
Table 3 shows changes in body skinfolds measurements
at 4 months stratified by baseline ART regimen. There
are some changes in regional fat measured by skinfolds
The Effect of Antiretroviral Therapy (ART) on Body Composition and Clinical Markers of Lipodystrophy
in HIV-Infected Children Assessed in Follow-Up Study 255
Table 2. Changes in body fold measurements at 4, 8 and 12 months.
Baseline 4 months 8 months 12 months
Median (IQR) value N Median (IQR)
change N Median (IQR)
change N Median (IQR)
Biceps SKF +1.22
+0.22 - +2.50 37 +0.50
–0.22 - +1.26 29 +0.95
–0.65 - +1.21 21 +0.72
–0.36 - +1.67
Triceps SKF +0.21
–0.61 - +1.56 41 +0.25
–0.31 - +0.56 37 –0.11
–0.42 - +0.32 24 +0.55
+0.09 - +1.92
Subscapular SKF +1.34
+0.12 - +3.14 39 +0.36
–0.16 - +1.10 37 +0.20
–0.52 - +1.29 23 +0.71
–0.21 - +2.21
Suprailiac SKF –0.43
–1.00 - +0.41 40 +0.10
–0.24 - +0.38 37 –0.21
–0.45 - +0.10 23 +0.24
–0.15 - +0.56
Sum of 4 skinfolds +0.58
–0.37 - +1.93 34 +0.14
–0.20 - +0.60 29 –0.14
–0.57 - +0.57 21 +0.44
–0.17 - +1.38
Circumference –0.76
–1.73 - +0.35 41 +0.07
–0.08 - +0.44 37 +0.29
–0.26 - +0.76 24 +0.25
–0.28 - +1.07
circumference –0.83
–1.92 - –0.11 40 +0.01
–0.25 - +0.38 34 0.00
–0.36 - +0.37 24 +0.25
–0.09 - +0.80
Calf circumference –1.26
–2.28 - –0.22 40 +0.08
–0.26 - +0.54 34 +0.07
–0.49 - +0.44 24 +0.17
–0.03 - +0.94
Table 3. Changes in body fold measurements at 4 months stratified by baseline ART regimen
Non-PI or no cur rent ART, ART
experienced PI ART naive p-value
N Median (IQR) change N Median (IQR) change N Median (IQR)
Biceps SKF 14 +0.80
+0.14 - +1.57 15 +0.74
+0.05 - +1.51 8 –0.84
–1.92 - –0.03 0.016
Triceps SKF 17 +0.28
–0.17 - +0.45 15 +0.34
–0.25 - +0.77 9 –0.05
–0.53 - +0.25 0.19
Subscapular SKF 16 +0.32
–0.41 - +1.30 15 +0.37
–0.15 - +1.23 8 +0.36
–0.37 - +0.58 0.69
Suprailiac SKF 16 +0.08
–0.23 - +0.43 15 +0.18
–0.11 - +0.39 9 –0.16
–0.40 - +0.25 0.24
Sum of 4 skinfolds 12 +0.18
–0.19 - +0.96 15 +0.37
+0.07 - +0.77 7 +0.11
–0.80 - +0.14 0.26
circumference 17 +0.07
–0.26 - +0.44 15 +0.17
0.00 - +0.72 9 0.00
–0.13 - +0.46 0.11
circumference 17 +0.24
–0.12 - +0.47 14 –0.04
–0.27 - +0.27 9 –0.18
–0.23 - +0.19 0.64
Calf circumference 17 +0.05
–0.21 - +0.66 14 +0.11
–0.29 - +0.44 9 +0.11
–0.54 - +0.65 0.76
and limbs circumferences as well in total body fat as-
sessed by 4 SKFs. There are differences in skinfolds
changes in arm measurements i.e. BSF and TSF, an in-
crease over 4 months period, with marked increase in
BSF (p < 0.05) whereas TSF changed +0.34 z-scores
when compared to negligible change of –0.05 z-score in
naive group of patients. Arm measured by MAC changed
+0.17 z-score, whereas no difference was observed in
naive group of patients. Overall, three anthropometric
measurements (biceps, triceps skinfolds and mid-arm
circumference) assessing arm fat distribution increased
over period of 4 months when compared to naive group.
This observation may suggest increased upper limbs fat
accumulation in PIs treated group. Potential lower limb
extremities fat was estimated by thigh and calf circum-
ferences z-scores measurements. There were no differ-
ences in changes observed in calf circumference z-scores
in both groups (+0.11 z-score). Thigh circumference
measurements did not change over time in PIs groups
whereas in naive group some decrease in z-scores was
observed (–0.18 z-score). Central trunk fat can be as-
sessed by measuring of subscapular and suprailiac skin-
folds. Subscapular skinfold changed equally in both
groups and remained the same with some increase over
time +0.37 z-score. There was no difference in sub-
scapular skinfold z-scores changes between PIs receiving
and naive group of patients. In contrast, suprailiac skin-
folds increased over time (+0.18 z-score) in PIs group
while it decreased (–0.16 z-score) in naive group. This
may suggest some central fat accumulation in PIs treated
Copyright © 2012 SciRes. WJA
The Effect of Antiretroviral Therapy (ART) on Body Composition and Clinical Markers of Lipodystrophy
in HIV-Infected Children Assessed in Follow-Up Study
group. Interestingly, in children on other than PIs therapy,
suprailiac skinfold did not change over time. Overall,
total body fat as measured by sum of four skinfolds
showed an increase of +0.37 z-score in PIs group, with
changes of +0.11 z-score in naive group.
3.3. D4T vs Naive Group 4-Month Changes
Table 4 shows changes in body skinfolds measurements
at 4 months stratified by baseline d4T regimen. An in-
crease in all anthropometric z-scores measurements was
observed in therapy groups, both d4T containing and no
d4T therapy group, when compared to therapy naive
children, except for subscapular skinfolds z-scores ch ange
which was comparable in no-d4T therapy group and na-
ive (+0.38, + 0.36 z-scores, respectively). Changes in
z-scores were clinically important in no-d4T therapy
group with significant changes in biceps skinfold (BSF)
z-scores with an increase in d4T therapy group and de-
crease in therapy naive group. In naive group z-score
decreased to –0.84 whereas in d4T therapy groups in-
creased to +0.19 and to +0.81 z-score in no-d4T group.
Remaining anthropometric z-scores measurements ch an g ed
in therapy group s with an increase in z-scores except calf
circumference z-score which changed to decrease to
–0.13 when compared to naive group z-score change to
+0.11 over 4 months period. Although increase in z-
scores changes were observed for remaining anthropom-
etric measurements these positive changes in z-scores
were more clear/ pronounced in no-d4T group of chil-
dren than in d4T therapy based regimen. This may sug-
gest that children on d4T are exposed to fat wasting
rather than accumulation.
4. Discussion
The most significant effect of ART therapy in our study
was on upper limbs as measured by BSF. In the whole
group of children, total (n = 85), BSF and subscapular
skinfolds decreased over period of observation indicating
a decrease in peripheral adiposity. The remaining body
fat measurements increased or remained unchanged
when compared with baseline measurements. Analyses
of changes were rather presented as degree of increase in
anthropometric measurements z-scores to assess potential
body fat dep osition.
Since the groups were ethnically similar, these differ-
ences could be associated with the treatment given. Nor-
mally, all anthropometric measurements increase through-
out the growth period, and a plateauing or decrease in
circumferences is likely to be clinically important which
was observed in our cohort of patients analysed as a
whole. Although changes in skinfold thickness meas-
urements were noticed these measurements are difficult
to make accurately and are prone to error. Therefore an-
thropometric assessments should be done by one trained
health practitioner. Evaluation of skinfold measurement
is less straightforward than for circumference data since
values vary throughout childhood and centile charts are
required. Biceps skinfold thickness centile charts are not
generally available and normal values also vary accord-
ing to age. We recommend that baseline and regular rou-
tine anthropometric measurements should be recorded
for all HIV-infected children.
Table 4. Changes in body fold measurements at 4 months stratified by baseline d4T use.
No d4T/Other d4T Naive P-value
N Median (IQR) change N
Median (IQR)
change N Median (IQR) change
Biceps SKF 19 +0.81
+0.49 - +1.96 10 +0.19
–0.90 - +1.26 8 –0.84
–1.92 - –0.03 0.0036
Triceps SKF 20 +0.15
–0.34 - +0.45 12 +0.53
+0.10 - +0.77 9 –0.05
–0.53 - +0.25 0.07
SKF 19 +0.38
–0.24 - +2.01 12 +0.25
–0.08 - +0.84 8 +0.36
–0.37 - +0.58 0.78
Suprailiac SKF 19 +0.18
–0.25 - +0.44 12 +0.10
–0.10 - +0.40 9 –0.16
–0.40 - +0.25 0.25
Sum of 4
skinfolds 17 +0.38
–0.11 - +0.82 10 +0.20
–0.09 - +0.77 7 +0.11
–0.80 - +0.14 0.28
circumference 20 +0.13
–0.06 - +0.50 12 +0.19
0.00 - +0.49 9 0.00
–0.13 - +0.05 0.22
circumference 19 +0.14
–0.29 - +0.47 12 0.00
–0.18 - +0.26 9 –0.18
–0.23 - +0.19 0.91
circumference 19 +0.21
–0.04 - +0.82 12 –0.13
–0.36 - +0.36 9 +0.11
–0.54 - +0.65 0.30
Copyright © 2012 SciRes. WJA
The Effect of Antiretroviral Therapy (ART) on Body Composition and Clinical Markers of Lipodystrophy
in HIV-Infected Children Assessed in Follow-Up Study 257
In order to compare growth in a heterogeneous group
of children it is necessary to derive z-scores, which
compare measurements with the age and sex-specific
population mean. Th ere is no reference group with which
to compare our group of mainly sub-Saharan African
children. The WHO growth charts only include children
up to the age of 5 years so European charts were used to
calculate z-scores [14]. As we were comparing growth
velocity rather than growth itself comparing with ART-
naive group of the same ethnic original, we felt this ap-
proach wa s re asonabl e .
This study is an extension of a previously published
cross-sectional analysis and confirmed our earlier find-
ings that although physical features of lipodystrophy
were seen in only 5% of patients in our cohort, children
with no clinical evidence of lipodystrophy had altered
body fat distribution [9]. Up to date, two longitudinal
studies in HIV-infected children estimated that 25% -
54% have changes in body fat distribution [10,11].
Clinical diagnosis of lipodystrophy is subjective, espe-
cially in a paediatric population where growth hormones
and pubertal effects may play a role. Therefore, use of
more objective measures, such as anthropometric meas-
urements, may be particularly useful in this population.
In an American study significant fat redistribution was
described in pubertal children receiving PI based therapy,
although duration of PI therapy and the length of expo-
sure to ART did not appear to be risk factors for lipodys-
trophy [12]. Clinical signs of lipodystrophy appear to be
less common in children compared to adults and it may
be that factors such as growth hormone and insulin sensi-
tivity mitigate the dev elopment of the lipodystrophy syn-
drome in pre-pubertal children.
There were some limitations of the current study. The
study was purely observational looking at the signs of
lipodystrophy in cohort of HIV-infected children above 3
years of age attending the HIV family clinic at GOSH,
and who fulfilled the inclusion criteria. Patients received
ART therapy according to national guideline at the time
[13]. Some patients received ART therapy for varying
lengths of time prior to the study. However, we com-
pared ART treated patients with ART naive. Anthro-
pometric measurements were taken during regular visits
at the HIV clinic. Some children only had one time point
measurements due to parental refusal for further assess-
ment therefore were not included in the follow up study.
Duration of follow up varied from 3 to 12 months. Al-
though the number of visits varied (2 - 6), most children
were followed up for 3 visits with 4 months period be-
tween visits. Longer observation period is required. This
is one of the limitations of the study; short observation
period which maybe not long enough to show persisted
pattern of changes over time.
The average time of observation in our study was 0.7
years which may not be long enough to de tect changes in
other parts of the body. Computed tomography (CT),
nuclear magnetic imaging (MR) and dual-energy X-ray
absorptiometry (DEXA) are objective reference methods
but are expensive for routine follow-up and diagnosis.
Therefore, anthropometry and other non-invasive bedside
methods should be evaluated. There is evidence of cor-
relation between fat mass measured by anthropometric
skinfolds thickness and DEXA in HIV-infected patients
with lipodystrophy [15]. Therefore anthropometry meth-
ods can be used in healthcare services as one of validated
methods for estimating body fat in HIV-infected patients.
In conclusion, our study supports previously reported
evidence of body fat changes in children receiving PI or
d4T. Although d4T is no longer used as a routine th erapy
in Europe it does still form part of first- and second-line
regimens in some countries and clinicians should be
aware of this association in children. Further long-term
observational studies over a longer time period, with dif-
ferent ART regimens, are required to fully evaluate the
long term effects of ART therapy on growth and body
composition in HIV-infected children.
To our knowledge this is the first follow-up observa-
tional study looking at the effects of ART therapy on
body composition in HIV-infected children in the UK
using anthropometric assessment. These methods could
be used worldwide particularly where access to more
advanced radiological methods CT, MR or DEXA scan is
limited. Early intervention by altering ART can make a
difference in management of HIV-infected children [16].
5. Acknowledgements
Dr Agnieszka Dzwonek received an unrestricted educa-
tional grant from Ovita Nutricia Research Foundation,
Warsaw, Poland. The authors would like to thank Pro-
fessors T. Cole and N. Klein, Specialist HIV nurse: M.
Clapson, and statistician K. Drew.
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