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Transcript of Am j clin nutr 1976-martorell-46-53
46 The American Journal of Clinical Nutrition 29: JANUARY 1976, pp. 46 53. Printed in U.S.A.
Upper arm anthropometric indicators ofnutritional status1’2
Reynaldo Martorell, Charles Yarbrough, A aron Lechtig,Herndn Delgado, and Robert E. Klein3
ABSTRACT The growth in arm muscle area and arm fat area of preschool children from rural
Guatemala is compared to that of a standard from the U.S.A. It was found that although the
Guatemalan cl�ildren have reduced arm muscle and fat areas, the relative reduction in arm fat area
was greater than in arm muscle area. Further, the upper arm cross-sectional area of Guatemalan
children had proportionately more muscle than fat when compared to that of U.S.A. children.
Lastly, for the same body weight, Guatemalan children had a similar arm muscle area but a clearly
smaller arm fat area than North American children. It is concluded that these findings suggest that
energy rather than protein is the main nutritional problem in these Guatemalan children. Am.
J. Clin. Nutr. 29: 46-53, 1976.
There has been much interest in the litera-
ture on the use of arm circumference, triceps
skinfold, and derivatives of these for nutri-tional assessment of muscle and fat bodyreserves (I). While arm circumference and
triceps skinfold may be useful rough mea-sures of body muscle and fat, they are not as
satisfactory theoretically as the cross-sec-tional arm muscle area and arm fat area. Forinstance, it has been pointed out by Gurneyand Jelliffe (2) that the triceps skinfold may
by itself be misleading given that “a thin ringon a muscular arm may contain as much fatas a thicker ring around a puny muscle.”Further, the use of cross-sectional arm areas
permits one to investigate whether any popu-lation at specified ages differs from theaccepted norms in the relative contribution of
fat and muscle to the total arm area. This
comparison of relative fatness and muscular-ity of a population, in addition to a direct
comparison of the “adequacy” of the armmuscle and fat areas with respect to the
accepted norms, in turn permits one to makeinferences as to the relative deficiencies inmuscle and fat.
The objective of this paper is to utilize
mid-arm anthropometric indicators to infer
protein and calorie nutritional status in rural
Guatemalan preschool children. To this end,we will compare the growth in arm muscle
area and arm fat area of the study population
to a recently proposed standard based on data
collected through the Ten State Nutrition
Survey (3).
Materials and methods
Sample
The data presented here are mixed longitudinal obser-vations on 1,240 rural (iuatemalan Ladino children,
under study by the Division of Human Development ofthe Institute of Nutrition of Central America and
Panama (4). The sample comprises approximately 84�
of all children who were 0 to 84 months of age within the
period of January 1969 through May I. 1973, in fourvillages in the department of El Progreso. northwest of
Guatemala City. The villages are on the Atlantic slopes
of the Guatemalan highlands at altitudes between 300
and 1,100 m. The median family income in these villages
is around U.S. $200/year. The typical house is built of
adobe and generally has only two rooms. Few homes
have sanitary facilities. Morbidity rates are high, particu-
larly gastrointestinal and respiratory problems. The
home diet staples are corn and beans, animal protein
comprising a small proportion (12%) of the total protein
ingested. One-day and 3-day recall dietary surveys
indicate that in children 2 to 5 years of age, the mean
‘From the Division of Human Development, Institute
of Nutrition of Central America and Panama (INCAP),
Carretera Roosevelt, Zone II, Guatemala City. Guate-
mala, CA.
2This research was supported by Contract NOl-
HD-5-0640 from the National Institute of Child Health
and Human Development (NICHD), National Institutes
of Health, Bethesda, Maryland.
$ Head, Division of Human Development of INCAP.
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ANTH ROPOMETR IC INDICATOR OF NUTR ITIONAL STATUS 47
intake is 71 calories and 2.0 g of protein/kg of bodyweight/day. An analysis of the dietary data indicates that
the risk of being protein-underfed is relatively low,varying between 6 and 13%. In contrast, the calories
available for growth and physical activity are between 25
and 65% of those observed in well-nourished populations
of the same age. Children are severely retarded in
physical growth. Some of the physical growth patterns of
this population have been described elsewhere (S � 10). In
summary, these data indicate that chronic moderate
malnutrition is highly prevalent and that calories are
probably limited in the diet of this population.
Mea.surements
All measurements were taken by a trained and
standardized anthropometrist. Upper arm circumference
was measured to the nearest millimeter with a steel tapewith the left arm hanging relaxed. The measurement was
taken midway between the tip of the acromion and the
olecranon process. The midpoint was located by placing
the middle fingers of each hand on the acromial and
olecranon landmarks, respectively, and then estimating
the midpoint with the extended thumbs. This method was
quicker and more reliable than locating the midpoint bymeasurement. The triceps skinfold was measured to the
nearest tenth of a millimeter with a Harpenden skinfold
caliper over the triceps muscle midway between the
acromion and olecranon process. Both of these measures
are very reliable, the measuring standard deviation in
repeated measures carried out a week apart being 0.24
cm and 0.59 mm for arm circumference and triceps
skinfold, respectively (II).
These measures were carried out at 15 days of age and
at IS specific age intervals through 84 months (Table I).
The permitted variation around the measurement inter-
vals was ±3 days at IS days of age. ±5 days from 3
through 24 months of age, and ±7 days from 30 to 84
months of age.
Arm muscle area (M) and arm fat area (F) were
derived from measures of arm circumference (C) and
triceps skinfold (7). Arm muscle (M) area was calculated
by the formula (2, 3):
(C - �fl2M=
4ir
Fat area (F) was derived thus:
C2F=-- M.
4�
The formulas utilized assume that the upper arm is
cylindrical in form, an assumption subject to someinaccuracy. Further, the cstimation of muscle area does
not take into account the humeral diameter. Similarly,
the estimation of fat area does not adjust for variable
skinfold compressibility (3, 12). Therefore, arm muscle
area and fat area are to be viewed as approximate
measures.
Measurement variability estimates for arm muscle
area and arm fat area were computed by remeasuring
each week a random sample of 10% of all subjects
examined the previous week. The test-retest correlationwas 0.94 for arm muscle area, and 0.84 for arm fat area
(n = 146 replicates). The measurement standard devia-
tion was obtained by the formula:
‘ji >.(a-b)�SM= 2n
where a and b are the first and second measures on the
same individuals and n is the number of individuals. The
measurement standard deviation ofarm muscle area was
found to be 62.7 mm2 and that for fat area 44.5 mm2 (n =
146 replicates). The mean population standard deviations
for muscle and fat area are 164.0 mm2 and 106.1 mm2,
respectively (Tables I and 2). The statistic obtained by
expressing the measurement variance as a percentage of
the population variance estimates the proportion of the
population variance accounted for by measurement van-
ance and serves as an index of the relative reproducibility
of measurements (I I). It was found that this statistic was
14.6% for muscle area and 17.6% for fat area. That is,
14.6% of the population variance in muscle area and
17.6% of that of fat area is due to variability in
measurement and cannot serve to explain nor be cx-
plained by other variables such as nutrition. The come-
sponding statistics for arm circumference and triceps
skinfold are 5.8% and 12.8%, respectively. This indicates,therefore, that arm muscle and fat area measurements
are appropriate for individual assessments of the situa-
tion at a point in time and probably of changes within
individuals as well.
The standard values (3) used for comparison are based
on a cross-sectional sample derived from the Ten State
Nutrition Survey of 1968- 1970. The sample was derived
from low-, middle-, and upper-income white groups, the
mean average income per family being U.S. $13,122 (3).
Arm muscle area values for comparison were those
reported as the 50th percentile; all other measures such as
arm fat area and percentage of the area which is musclewere derived from 50th percentile values of arm circum-
ference and triceps skinfold.
Results
Tables I and 2 give the age-specific sample
size, mean, and standard deviation for fiveupper arm anthropometric indicators forGuatemalan boys and girls, respectively.
The growth curves of arm muscle area forGuatemalan and U.S.A. (3) children arecompared in Figure 1. The similarity of thegrowth curve of arm muscle area to that of
height is striking (10).Authors have referred to arm circumfer-
ence as an “age-independent indicator” ofnutritional status because it shows little
change with age from about 6 to 60 months(13). This is apparently not so in the standard
(3). Similarly, arm circumference is clearlynot age-independent in the Guatemalan studypopulation (Tables 1 and 2); although nochange is observed between 6 and 24 months
48 MARTORELLETAL.
TABLE I
Upper arm muscle and fat indicators in Guatemalan boys
A Arm circumference Triceps skinfold Arm muscle area Arm fat area % of total arm area
group n (cm) (mm) (mm2) (mm2) which is muscle (%)(mo) t SD t SD t SD t SD t SD
0.5 181 9.9 1.0 4.8 1.1 570 109 224 64 72.1 4.3
3 236 12.3 1.2 7.1 1.5 819 168 399 100 67.2 5.4
6 251 13.0 1.6 6.9 1.7 943 175 414 121 69.6 6.1
9 257 13.1 1.2 6.4 1.7 981 187 386 118 71.9 6.0
12 251 13.1 1.1 6.2 1.5 999 188 378 98 72.4 5.7
IS 242 13.1 l.l 6.1 1.5 997 165 369 102 73.1 5.3
18 235 13.1 1.0 6.0 1.4 1007 l61 365 97 73.5 5.1
21 219 13.2 1.0 6.0 1.4 1027 160 370 98 73.7 4.7
24 240 13.4 1.0 6.2 1.4 1059 153 386 101 73.4 4.9
30 212 14.0 1.0 6.5 1.5 1132 165 425 109 72.8 5.1
36 223 14.3 0.9 6.7 1.5 1194 151 445 113 73.0 5.1
42 217 14.7 0.9 6.9 1.7 1256 164 469 128 73.0 5.7
48 210 14.8 0.9 6.4 1.4 1302 155 444 103 74.6 4.5
60 191 14.8 0.8 5.9 1.5 1345 150 412 109 76.6 4.8
72 179 14.9 0.8 5.2 1.3 1416 l68 367 94 79.5 4.3
84 158 15.3 0.9 5.0 1.4 1507 198 366 109 80.6 4.6
TABLE 2
Upper arm muscle a nd fat indicators in Guatemalan girls
Agr�p n
Arm circumference(cm)
Triceps skinfold(mm)
Arm muscle area(mm2)
Arm fat area(mm2)
% of total arm areawhichismuscle(%)
(mo)t SD S SD S SD S SD t SD
0.5 153 9.9 0.9 5.0 1.1 563 101 230 59 71.1 4.83 216 12.1 1.2 7.2 1.6 773 158 399 110 66.1 5.7
6 204 12.9 1.1 7.0 1.6 924 170 415 106 69.0 5.89 207 12.9 1.2 6.4 1.5 956 185 385 104 71.3 5.6
12 210 12.8 1.2 6.1 1.4 943 177 365 95 72.2 5.1
15 195 12.8 1.2 5.9 1.3 964 168 353 93 73.3 4.6
18 197 12.8 1.1 6.0 1.4 963 161 359 93 72.9 4.921 188 12.9 1.1 6.0 1.3 973 160 364 89 72.9 4.5
24 192 13.1 1.0 6.1 1.4 1008 165 374 94 73.0 4.9
30 199 13.7 1.0 6.7 1.6 1079 160 425 l14 71.8 5.4
36 194 14.2 1.0 7.1 1.8 1142 159 468 128 71.1 5.9
42 190 14.5 0.9 7.1 1.8 1192 160 477 130 71.6 6.0
48 179 14.7 0.9 6.9 1.8 1261 164 469 129 73.0 5.8
60 188 14.9 0.9 6.3 1.5 1342 166 442 114 75.4 4.8
72 175 15.2 0.9 6.0 1.6 1405 161 428 120 76.8 5.0
84 161 15.5 0.9 5.9 1.5 1508 182 409 114 78.8 4.9
of age, a mean change of approximately I .6 months of age and at all ages from 1 2 to 48cm, or roughly 16%, occurs between 24 and months of age. However, in contrast to the60 months of age. Figure 1 shows that age pattern in the standard, Guatemalan boys and
changes are more striking in growth in arm girls are similar from 60 to 84 months of agemuscle area than in arm circumference. For (P > 0.05). Relative to the standard, Guate-
instance, while the percentage increase from 6 malan children are significantly different at
to 84 months ofage is 19% for arm circumfer- all ages (P < 0.05). However, at 3 months ofence in the Guatemalan sample, it is 62% for age the differences are relatively small. By 12muscle area in the same sample. months of age, the differences are practically
As expected, in both populations boys have as large as those observed in later ages.larger muscle areas than girls; Guatemalan Figure 2 shows that the pattern of growthboys are significantly larger (P < 0.05) at 3 in arm fat area is substantially different from
1800
1700
1600
1500
1400
ARM 1300
MUSCLE 1200
AREA 1100
(mm2) 1000
900
800
700
600
500
4001
ARM
FAT
AREA
2(mm)
U.S A. Boys (50th perc.)
-�#{149}_--... U.S A. Girls (50th perc.)
.-_o--_- Guotemolan boys (R)--0---- Guotemalan girls (�)
48 60 72 84
700
600
500
400
300
200
100
Ii 19111 II 1 1 I I I
0.5 3 6 9 1215 1821 24 30 36 42 48 60 72 84
ANTHROPOM ETRIC INDICATOR OF NUTRITIONAL STATUS 49
I I I I I I I � I I I
0.5 3 6 9 1215 1821 24 30 36 42
AGE (months)
FIG. I. Growth in arm muscle area in U.S.A. (3) and Guatemalan boys and girls.
800
0
- U.S.A. boys (derived)
#{149}--- U.S.A. girls (derived)
-._o--- Guatemalon boys �()- - � Guotemolon girls Q()
AGE (months)
FIG. 2. Growth in arm fat area in U.S.A. (3) and Guatemalan boys and girls.
-0--
--0--
U.S.A. boys (derived)
U.S.A. girls (derived)Guotemalon boys (X)
Guotemalon girls (X)
----.�
50 MARTORELL ET AL.
FIG. 3. Percentage of total arm area which is muscle in U.S.A. (3) and Guatemalan boys and girls.
that of arm muscle area. Specifically, growthin arm fat area, particularly in the Guatema-
lan population, appears to be unrelated toage. The mean arm fat area in the Guatema-Ian population is smallest at birth (230 mm2);by 3 months it reaches a value for 400 mm2.
Although changes occur thereafter (i.e., 361mm2 at 15 months, 473 at 42 months), theyvary within a narrow range.
Guatemalan boys and girls have similararm fat areas till 42 months (P > 0.5);
thereafter, girls are clearly higher in thisrespect (P < 0.05). Relative to the standard,
Guatemalan children are markedly lowerfrom 12 months onward.
The percentage of the total arm area which
is muscle at the different ages for U.S.A. andGuatemalan children is shown in Figure 3.Clearly, the arm of Guatemalan children isrelatively more “muscular” (or less “fatty”)than that of U.S.A. children. As expected,there is a tendency in both populations forboys to be relatively more muscular thangirls. Significant differences in this respect
%
80.0
75.0
70.0
65.0 -
60.0
are observed in Guatemalan children at 0.5and 3 months of age and at all ages from 36 to84 months (P < 0.05). Save for a dip in the
curve at 3 months of age, the arm becomesrelatively more muscular in both populationsas age increases.
In Table 3 the arm muscle and fat areas ofthe Guatemalan sample have been expressedas a percentage of the age-sex-specific stan-
dard value (3). These indicators are thereforesimilar to the G#{243}mezscale in the manner inwhich they are calculated. Table 3 shows that
percentage arm muscle area for age is consist-
ently higher than percentage arm fat area forage. Except for females at 3 months of age, at
all ages and for both sexes percentage arm
muscle area for age is significantly greater
than percentage arm fat area for age (P <0.05). While girls have a significantly greater
percentage arm muscle area for age (P < 0.5)at 84 months of age they have, in contrast,
smaller percentage arm fat area for age than
boys (P < 0.05).The humeral diameter as measured in
I I I I I I I I I -- I
0.5 3 6 9 12151821 24 30 36 42 48 60 72 84
AGE (months)
ANTHROPOMETRIC INDICATOR OF NUTRITIONAL STATUS 51
TABLE 3
Percentage muscle area for age and percentage arm fat area for age in Guatemalan boys and girls
% arm muscl e area for age % arm fata rca for age
(rn�3)Boys Girls
S
Boys
SD S
Girls
SDn S SD n S SD
3 236 91.8 18.9 216 89.3 18.2 74.3 18.5 95.5 26.2
12 251 83.2 15.6 210 87.0 16.3 59.3 15.4 60.0 15.6
24 240 82.4 11.9 192 81.2 13.3 57.0 15.0 55.7 14.1
36 223 86.3 10.9 194 87.9 12.2 65.5 16.6 70.5 19.3
48 210 89.7 10.6 179 90.7 11.8 62.1 14.5 67.3 18.5
60 191 85.1 9.5 188 88.5 10.9 59.4 15.7 58.4 15.1
72 179 83.3 9.9 175 89.9 10.3 56.1 14.4 58.1 16.3
84 158 83.0 10.9 161 88.7 10.7 56.2 16.7 49.8 13.9
radiographs is 13.4 and 13.9 mm in 6- and7-year-old boys, respectively. The bone andmuscle diameter is 52.9 and 53.4 mm at 6 and
7 years of age, respectively (14). Therefore,the contribution of bone to the bone andmuscle area (here called arm muscle area) isaround 6 to 7%. Consequently, correcting forhumeral area would not lead to proportionalreductions relative to the standard in arm
muscle and arm fat area in Guatemalanchildren. Table 3 would show, therefore, thatarm fat area is much more reduced than arm
muscle area even after correcting for humeralarea.
Discussion
The data examined suggest that the upperarm cross-sectional area of children of rural
Guatemala has proportionately more musclethan fat when compared to children from the
United States (3). This is due not to a largerarm muscle area, which in fact is below
standard values, but to a marked reduction inarm fat area. It appears that the Guatemalansample begins to differ from the standardvalues for both arm muscle and fat area
sometime during the 1st year of life. At allages, the relative differences are greater inarm fat than in arm muscle area.
A previous publication (10) on the samestudy population showed that the childrenfrom Guatemala, although absolutely smallerwhen compared to children of similar agefrom Denver (15), have similar body weightswhen compared to children from Denver of
similar heights. The findings presented here
indicate that the Guatemalan children have
relatively larger arm muscle areas than the
standard. Assuming that arm areas are prox-
ies of body composition, the above two factssuggest that the body composition of Guate-malan children is different from that ofwell-nourished populations, namely propor-tionately more lean body mass and less bodyfat per kilogram of body weight in the
Guatemalan sample. An indirect test of thisquestion is presented in Figures 4 and 5,which show the relationship between fat area
and muscle area to body weight in theGuatemalan sample, the Denver sample ( I 3)which has data on arm circumference and
triceps skinfold at 48 months of age and up,and the Ten State Survey Sample (3). Tograph the latter sample, for which no weightinformation was given, the age-sex-specific
body weights given for the Denver samplewere utilized. Figure 4 clearly shows that ifweight is held constant, there is considerablyless arm fat area in the moderately malnour-
ished Guatemalan sample than in the two
presumably well-nourished populations from
the United States. In contrast, Figure 5
indicates that for the same body weight, allthree populations compared are fairly similar
in arm muscle area. Similar results were
obtained with height as opposed to weight.
The data presented in Figures 4 and 5 suggest,therefore, that the body composition of themoderately malnourished Guatemalan sam-pie is different from that of well-nourished
populations. Specifically, the data suggest
that for the same body weight, the studypopulation has an adequate amount of muscleprotein reserves but a clearly deficientamount of fat when compared to the acceptednorms. This could be the result of several
mechanisms, greater limitations in caloric as
MEAN
FAT
AREA
(mm2)
0
x
x A
& #{149}t��
300’
200.
100.
0
5 10 15 20 25
WEIGHT (��): kg
x
MEAN
MUSCLE
AREA 1000.
(mm2)
750-
500�
. Oi
#{149}..#{128}c
‘p.#{149}
I
0
WEIGHT (i): kg
25
52 MARTORELL ET AL.
FIG. 5. Relationship between mean muscle area and mean body weight.
FIG. 4. Relationship between mean fat area and mean body weight.
#{149}Guotemolan boys� Ten State Survey boysL� Denver boys
(� Guatemalan girls
0 Ten State Survey girls
O Denver girls
1750.
1500.
1250-
#{149}G uotemolon boysc Ten State Survey boys
#{163}Denver boys
#{128})Guatemalon girls#{149}Ten State Survsy girls
Denver girls
I I
5 10
I I
15 20
ANTHROPOM ETRIC INDICATOR OF NUTRITIONAL STATUS 53
opposed to protein ingestion or intensivephysical activity being two possibilities. Pre-liminary investigations of the dietary intake
pattern of this population indicate that perkilogram of body weight, the risk of caloric
underfeeding is higher than that of proteinunderfeeding (see “Materials and methods”).Therefore, it is tentatively concluded that thefindings reviewed suggest that energy ratherthan protein is the main nutritional problemin these Guatemalan children.
Given the potential public health utility ofthe upper arm for nutritional assessments, itis imperative that the measures of area bevalidated against body composition studies. It
is realized that such studies are expensive anddifficult to carry out in young children. It isnot surprising, therefore, that there have beenpractically no studies of the body composition
of young children in general and of moder-ately malnourished children in particular.Nonetheless, studies of this nature are ur-
gently needed to adequately assess the valid-
ity of arm muscle and fat areas.
References
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circumference as a public health index of protein-cal-
one malnutrition ofearly childhood. J. Trop. Pediat.
IS: 176, 1969.
2. GURNEY, J. M., AND D. B. JELLIEfE. Arm an-thropometry in nutritional assessment: monogram
for rapid calculation of muscle circumference andcross-sectional muscle and fat areas. Am. J. Clin.Nutr. 26: 912, 1973.
3. FRISANCIIO, A. R. Triceps skinfold and upper arm
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4. KLEIN, R. E., i-P. HABICIIT ANE) C. YARBROUGEI.
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