179 THE ARM CIRCUMFERENCE AS A PUBLIC HEALTH INDEX OF PROTEIN-CALORIE MALNUTRITION OF EARLY CHILDHOOD (I) BACKGROUND by

E. F. PATRICE JELLIFFE AND DERRICK B. JELLIFFE

{Caribbean Food and Nutrition Institute, P.O. Box 140, Kingston 7, Jamaica)

The problem of protein-calorie malnutrition of early childhood (PCM)* can be considered as a public health "iceberg" (Fig. 1), in which the two main severe syndromeskwashiorkor and nutritional marasmusare easily detected and classified by inspection, and the many "intermediate" severe cases found between these two polar extremes can also be recognized clinically. However, in poorly nourished communities, far larger numbers of children with mild-moderate PCM exist, hidden and often unrecognized beneath the clinical surface (JELLIFFE, 1959 and 1969b).
KWASHIORKOR SEVERE MARASMUS

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MODERATE

FIG. 1. The Protein-Calorie Malnutrition (PCM) Iceberg.

MILD

ASSESSMENT OF MILD-MODERATE PCM

In|orderto assess the nutritional status of children in a community, tests have to be devised to identify and classify children with what is here termed "mild-moderate PCM," and has elsewhere been variously referred to as "early," or "clinically occult," or "pre-clinical," or "marginal" malnutrition. The problem of devising suitable methods is complicated by the fact that in some communities kwashiorkor is the main severe syndrome and in others, marasmus. Also, the clinical features vary in prevalence from one part of the world to another, depending on the interaction of numerous local variables, including genetic characteristics, associated nutrient deficiencies, types of microbiological and parasitic conditioning infections, the sequence, severity and rate of development of malnutrition and the age of onset. *AIternativeIy termed "protein-calorie deficiency diseases" (PLATT et al., 1961). The Journal of Tropical Pediatrics, December, 1969

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Three main direct methods of assessing PCM in the community have been used: (1) clinical signs, (2) biochemical tests, and (3) anthropometry (GOPALAN, 1970). (1) Clinical Signs. Eleven clinical signs* have been listed as being suggestive of proteincalorie malnutrition of early childhood (PCM) in community surveys (WHO, 1963; JELLIFFE, 1966). All have the disadvantage of being subjective, difficult to standardise, and, still more, to express quantitatively. In addition, these signs are not constantly present; especially in mild-moderate PCM (STANDARD et al., 1966), and also vary in prevalence from one part of the world to another, depending on the inter-action of many ecological factors, and whether the kwashiorkor "line-of-development" or the marasmus "line-of-development" is the main abnormality in the community (Fig. 2). However, the detection of clinical signs does not require costly apparatus and can be carried out rapidly on large numbers, provided the examiners have been carefully and practically trained, and the definition of the lesions sought for have been standardized, as far as possible.
Growth retardation (body weight) Mild
\
1
i

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K. "Line of flo Z
V

N. M. "Lin* of flow'

V
:

"Ear|y"<-Moderate kwashiorkor

O -1
V V*

- > "Early" nutritional marasmus

FIG. 2. Schematic attempt to correlate the development of mild, moderate and severe PCM in two main "lines of flow," that is leading to Kwashiorkor and to nutritional marasmus (From Jelliffe and Welbourn, 1963).

RME YN D R O

Severe

Kwashiorkor < j j
in

> Nutritional mar aim us

Despite the difficulties and ambiguities mentioned, both the eleven "suggestive" clinical signs and the occurrence of the two severe syndromes (kwashiorkor and marasmus) should be recorded in PCM surveys, as when analyzed, they help to give an understanding of the pattern and sequence of development of PCM in the particular community, which is helpful both to the investigators and also to workers elsewhere, who later try to interpret the report of the particular survey. The prevalence in the community of the two severe syndromes of marasmus and kwashiorkor will be important evidence, provided adjustment is made for possible hospitalized cases from the area, and provided that no assumptions are made that these advanced cases always represent a constant fraction of the quantum of PCM in the community. There may, for example, be considerable PCM in the community with few or no cases of kwashiorkor. Oedema, dyspigmentation of the hair, easy pluckability of the hair, thin sparse hair, straight hair, muscle wasting, depigmentation of the skin, psychomotor change, moon-face, hepatomegaly, flaky-paint dermatosis. December, 1969, The Journal of Tropical Pediatrics

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(2) Biochemical Tests. Various biochemical tests have been suggested for the detection of early PCM. The serum protein levels, particularly albumin, have been employed, but, according to most workers, significant changes are not demonstrable until clinically obvious PCM occurs. However, recent work suggests the need for further assessment in community surveys. Relatively recently, two new tests have been devised that seemed particularly appropriate for field surveys. These are the amino acid imbalance test (WHITEHEAD, 1964), which can be carried out on a capillary tube sample of blood collected in the field, and the hydroxyproline excretion test (WHITEHEAD, 1965), which only needs a few cubic centimetres of a randomly collected urine sample. Unfortunately, these tests need a sophisticated laboratory to carry them out, and recent work has shown that their interpretation is difficult in relation to the locally most prevalent form of PCM, to associated infections, to recent diet etc. (WHITEHEAD, 1968). Also, each of these investigations is, in fact, testing a different aspect of protein metabolism, and the best direct measure of body musculature would be the urinary creatihine excretion, preferably for a 24 hour period* (but possibly for a timed period of several hours) and with the results related to the child's body length (ARROYAVE and WILSON, 1961). Biochemical tests have the undoubted value of being independent of precise knowledge of age, but at the moment those presently available are not usually feasible in unelaborate community surveys or other forms of field assessment. . (3) Anthropometry. Growth failure and a variable degree of body disproportion are recognized features of severe malnutrition in experimental animals (MCCANCE, 1964) and in PCM (JELLIFFE, 1966), especially in the severe syndromes of kwashiorkor and marasmus. In community surveys, various body measurements have been suggested to assess the prevalence of all grades of PCM as judged by growth retardation and by body disproportion. If ages are verifiable, these include the weight, the length (or height), the arm circumference and the triceps skinfold (JELLIFFE, 1966); while if, as is often the case, precise ages of children are not known with accuracy, then the following ratios or "year constant" measurements have been suggested: weight-for-height, weight-for-head circumference, chest/head ratio and the arm circumference. Body weight has been the main measurement employed in community surveys of young ; children. However, it is less simple to measure accurately than usually realized, and insufficient attention has so far been given to producing an appropriate weighing device for use for young children in field circumstances.f Also, the interpretation of the weights of children during this rapidly growing phase of life depends on precise knowledge of the ages of those examined and on the selection of appropriate standards of comparison. There is, therefore, a considerable need for simple anthropometric measurements for use in field circumstances which have the following characteristics: (i) capable of being carried out by trained para-medical staff, (ii) require only inexpensive, easily available apparatus, (iii) give reasonably replicable and easy to interpret results independent of knowledge of the precise age, capable of giving scientifically valid, albeit approximate, information concerning the prevalence of PCM in the community that can lead to public health interpretation and action. *As a rough quantitative measurement, 50 mg. of creatinine per 24 hours indicates a muscle mass of
I kg. (WATERLOW, 1969).

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tThe ideal scale would probably be based on the beam-balance principle and would have the following :haracteristics: (i) low cost; (ii) accuracy to 50 gm.; (iii) sturdiness; (iy) easy transportability by hand weighing as little as possible, compact, with carrying handle and locking device); (v) clear readability scale markings facing observer and with different colours for the two unitse.g. kilogrammes and grammes); vi) weighing surfaces, with a rail round, suitable and safe for baby to be placed on and for older subject to tand on, and (vii) weight range up to 80 kg. (to permit weighing frightened, struggling pre-school children n the arms of a mother or attendant). (JELLIFFE, 1968). The Journal of Tropical Pediatrics, December, 1969

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MUSCLE DEFICIT AND PCM

Muscle is the largest protein containing "organ" in the body and the major component of the "lean body mass." There is considerable clinical, anthropometric, morphological and metabolic evidence that, as might be expected, the myoglobin protein reservoirs of the musculature are particularly depleted in protein-calorie malnutrition of early childhood. (i) Clinical Evidence. The muscle deficit seen in severe PCM received emphasis in clinical descriptions by some of the earlier investigators, but by no means all. In their early publication, "Kwashiorkor," TROWELL, DAVIES and DEAN (1954) noted that "the limbs are moved spontaneously very little" and that oedema tended to mask the depleted muscles (which could, however, be palpated, especially "the attenuated bellies of the upper limbs"). OOMEN (1953) in his studies in Indonesia stressed "muscle atrophy" as one of the commonest features. He notes that this was often not included in descriptions of the characteristic picture of kwashiorkor, and he emphasised its significance as an important sign of protein depletion, which could be "judged from outside." The palpable muscle tissue was observed to be lax and small, and the question of the relative degree of atrophy and of atony was discussed. Oomen also commented on the functional effects of muscle deficit and weakness, including previously active toddlers developing kwashiorkor and "going off their feet" (which could in part be related to apathy and psychomotor change), and showing lordosis, potbelly, winged scapulae and hanging heads. Numerous more recent accounts stress muscle deficit as a constant clinical feature in both kwashiorkor (Fig. 3) and marasmus (Fig. 4) (JELLIFFE and DEAN, 1959); while SMYTHE (1958) suggested that muscle weakness could be roughly tested functionally by gently pulling the supine child up by his arms into a sitting position and noting his ability to hold his head up and to sit without support. However, in addition to being difficult to measure objectively, weakness is complicated as a measure of muscle mass, both by psychological changes increasing the child's unwillingness to cooperate, and by possible decreased muscle tone associated with depleted body electrolytes, especially potassium (GARROW et al., 1968). (ii) Anthropometric Evidence. The anthropometric assessment of muscle deficit has been attempted by measurement of limb circumferences, especially the upper arm, and by various calculations designed to estimate underlying muscle substance. The mid-upper arm circumference was used in afieldsurvey in Haiti in 1958 (JELLIFFE, 1959; JELLIFFE and JELLIFFE, 1960); while MALCOLM (1956) measured the calf circumference in numerous surveys in Samoa and other South Pacific countries, where she found that typical "weaning" retardation of weight gain was associated with considerable and prolonged reduction in calf girth. In young children with severe PCM, the limb circumferences have been shown to be among the most markedly affected body measurements. Thus, in a large scale study in India, GOPALAN weisht (1968) found that weight, -, calf circumference and arm circumference showed the height2 maximum difference between normal children and those with PCM. Likewise, Ugandan children with -kwashiorkor were found to have very diminished arm and calf circumference (Table I). The approximate underlying muscle circumference can be calculated from measurements of the arm circumference and overlying skinfolds (JELLIFFE and JELLIFFE, 1960); and MCFIE and WELBOURN (1962) found a positive correlation between muscle size in the arm as calculated from anthropometry and as revealed by soft tissue radiography. The most elegant study to-date was carried out by STANDARD, WILLS and WATERLOW (1959) who calculated upper arm muscle thickness and muscle bulk from external measurements and radiography in young Jamaican children hospitalized with severe PCM and during recovery. December, 1969, The Journal of Tropical Pediatrics

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Their results suggested that the decrease in muscle mass was greater In these malnourished babies than body weight deficit. Also, the calculated muscle measurements increased with . nutritional rehabilitation, and were significantly correlated with increased urinary outputs of creatinine, considered the most direct biochemical index of muscle mass (Fig. 5).

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FIG, 3. Classical kwashiorkor (Uganda),

FIG. 4. Classical marasmus (C. America).

TABLE I. Mean arm and leg circumferences of Ugandan children with and without oedema (DEAN, 1966). Arm circumference (cm.) (Age in months) Sex Male Condition Kwashiorkor Healthy Female Kwashiorkor Healthy Oedema Slight Marked Absent Slight Marked Absent 10-15 | 15-21 11.3 11.9 14.8 11.0 11.6 14.5 1 11.4 I 12.4 j 14.8 1 11,6 | 12.8 14.2 21-26 11.3 12.2 15.6 11.4 12,5 14.6 Leg circumference (cm.) (Age in months) 10-15 | 15-21 14.0 15.8 18.2 14.5 14.8 17.6 14.2 16.9 18.1 15.2 16.9 18.9 21-26 14.7 16.9 18.7 14.4 .16.8 19.7

Note: The grading of oedema was by the scale used in the M.R.C. Unit in which "marked" indicates a degree of swelling that is easily visible. The healthy children were 39 boys and 25 girls from a specially selected group. The Journal of Tropical Pediatrics, December, 1969

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E. F. PATRICE JELLIFFE AND DERRICK B, JELLIFFE

Correlation coefficient r * + 0-74P = o-oot

4*

3 I-5
C s)

M e 5. Relation between increase ia muscle thickness and increase in creatinine output in malnourished infants during treatment (From Standard, Wills and Waterlow, 1959).
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i-o

1-0

IS

2-0

2-5

Increase in creatinine output

(iii) Morphological Evidence. Gross wasting of musculature is a characteristic autopsy finding in fatal severe PCM. The muscles are often noted to be pale and reddish-grey. Histoiogieal evidence of severe muscle change was documented by WATERLOW (1948), who noted in autopsies that "the muscles are shrunken and small. The fibres are atrophic and with gross loss of sarcoplasm. The fibres having shrunk away from the surrounding perimysium so that'in cross section the nuclei are seen to be surrounded by only a thin rim of cytoplasm." More recently, MONTGOMERY (1962) has confirmed these findings, and shown that striated muscle shows extreme reduction in the size of individual muscle fibres relative to the normal, with crowding of the sub-sarcolemmal nuclei. The most striking feature of his study was the remarkable decrease in muscle cross-section in severe PCM. Thus, the sartorius muscle of a malnourished infant of 12 months approximated in cross-sectional area only to that of a normal foetus of 31 weeks' gestation (Fig; 6), despite the known occurrence of "oedematous muscle"
(G ARROW, 1968).

(iv) Metabolic Evidence. Picou and WATERLOW (1961) emphasize the importance of concept of the dynamic state of body proteins, especially that the turnover rate varies with different proteins in different tissues. In the gut mucosa, pancreas, liver and plasma, the turnover rate is fast; while in the liver and especially muscle tissue, it is relatively slow.
SCHOPNHEIMER'S

FIG. 6. Transverse section of whole sartorius muscle in malnourished infant aged 12 months (top left), compared with foetus at 31 weeks gestation (top right) and a well nourished infant aged 13 months (below) (From Montgomery, 1962).

December, 1969, The Journal of Tropical Pediatrics

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Muscle and liver tissue have been shown to have lost up to 50% of their protein in severe PCM, as judged by biopsy results (WATERLOW and MENDES, 1597); while whole body analysis has shown that in "severe infantile malnutrition" the total protein is reduced to of normal for a child of the same length (GARROW et al., 1965).
SELECTION OF ARM CIRCUMFERENCE

The "mid-upper arm circumference"abbreviated to "arm circumference" (arm girth) has, therefore, been suggested as a potentially useful, simple field index for the assessment of PCM (JELLIFFE, 1959 and 1966). It was felt that there was evidence that the measurement would give composite information simultaneously on three important effects of PCMdeficit in the muscle protein reservoirs, availability of calorie stores in the form of subcutaneous fat, and growth failure. The arm was selected because of its easy accessibility, approximately circular shape and lesser involvement with clinical oedema (and, presumably, with subclinical water retention). However, as noted earlier, MALCOLM (1956) has found the calf circumference a useful measurement in field circumstances, and GOPALAN (1968) noted that the circumference of the calf was more affected than the arm in Indian children with severe PCM. The arm circumference measurement as an index of protein depletion is based on the assumption that all the body musculature is uniformly affected in PCM which seems likely, although unproven. Its value as a measurement of local muscle mass has to bear in mind the effects of possible clinical or subclinical oedema, excess subcutaneous fat, and changes in dimensions of other tissues in the arm, including the diameter of the humerus. Despite its apparent simplicity, anthropometric opinion emphasized that the mid-point of the upper arm should be measured accurately with the arm flexed to a right angle (Fig. 7), and the actual measurement should be made at the mid-point with the arm hanging loosely (Fig. 8), employing "firm" constant pressure with a flexible, non-stretch, steel or fibre-glass /tape (JELLIFFE, 1966). Tentative standards of comparison were suggested based on data collected by Dr. NAPOLEON WOLANSKI of the Institute of Mother and Child, Warsaw on healthy, well-fed Polish children. It was noted that little difference was found between the sexes, and, as the arm circumference increased only very gradually during the second to fifth years, the possibility of using the follow ing so-called "year-constant" standards was proposed: second year16 cm.; third year16.25 cm.; four year16.5 cm.; fifth year16.75 cm. It was felt that these measurements could be of special value in community child nutrition surveys where precise documentary verification of age was not available. It was suggested that results could be presented in relation to 10% levels below the standard (JELLIFFE, 1966; JELLIFFE, 1967). As in many parts of the world, varying degrees of PCM affect the secotrant,* it was felt that the "year-constant" standard for the second year of life (16 cm.) might be used in communities where exact ages were not known during what has been termed the "dental second year"possibly defined all children with from 6-18 teeth (JELLIFFE and JELLIFFE, 1968). Arm muscle circumference. The mid-upper arm muscle circumferencefabbreviated to arm muscle circumferencecan be calculated from the formula C2 = Cl -s (Fig. 9). Various skinfold thicknesses (s) have been used, including the biceps (JELLIFFE and JELLIFFE, 1960), an average of the biceps and triceps (STANDARD et al., 1959), or the triceps along (Fig. 10) 'MCFIE and WELBOURN, 1962; JELLIFFE, 1966). For practical purposes, the triceps skinfold las been considered preferable, as standards are readily available, so that the measurement :an also be used as a rough gauge of calorie reserves. In any case, it is important to convert he skinfold reading from millimetres to centimetres when calculating the arm muscle circumference, as the arm circumference is usually measured in these units.
JELLIFFE, 1969a).

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*The term "secotrant" has been suggested for a child in the second year of lifea secondyear transitional
(MCFIE

tAlternatively, the "inner arm diameter" has been calculated t al., 1963). 'he Journal of Tropical Pediatrics, December, 1969

and

WELBOURN,

1962;

MASON

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0 51159

51160

FIG. 8. Measuring arm circumference (From JellifTe, 1966).

FIG. 7. Assessing mid-point of arm (From Jelliffe, 1966).

FIG. 9. Calculation of the arm muscle circumference d =.arm circumference; S = skinfold (2 x subcutaneous fat); di = arm diameter; d. = muscle diameter; S = d t d; G> (muscle circumference) d ( d d) C

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E. F. PATRICE JELLIFFE AND DERRICK B. JELLIFFE DISCUSSION

187

As it became apparent that the arm circumference was being tried out as a public health index of PCM in different parts of the world, the following papers and notes concerning experience with this measurement were collected from colleagues to form the present symposium. It was hoped by this means to gain more insight into the value and limitations of the arm circumference as a simple field index of PCM, including such technical aspects as method of measurement, reproducibility and preferred type of tape measure; its comparison "with other methods of assessment, especially the weight-for-age and its limits of normality, and usefulness as a quantitative measure of the degree of malnutrition.

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FIG. 10. Measuring the triceps skinfold with Harpenden calipers (From JellifTe, 1966).

It was also hoped to obtain information on its practical utility in different field situations, such as community surveys or the screening of young children in emergency food distribution programmes.
REFERENCES

Arroyave, G. and Wilson, D. (1961). Amer. J. Clin. Nutr., 9, 170. Dean, R. F. A. (1965). Counter, 15, 73. Garrow, J. S., Fletcher, K. and Halliday, D. (1965). J. Clin. Investig., 44, 417. , Smith, R. and Ward, E. E. (1968). Electrolyte metabolism in severe infantile malnutrition. Pergamon Press: Oxford & London. Gopalan, C. (1968). Assessment of protein nutritional status. Unpublished data. (1970). Amer. J. Clin. Nutr., in press. Report of IUNS Committee on Assessment of Protein Malnutrition. Jelliffe, D. B. (1959). J. Pediat:, 54, 277. (1966). The assessment of the nutritional status of the community. WHO Monograph No. 53. (1967). J. trop. Pediat., 13, 67.

The Journal of Tropical Pediatrics, December, 1969

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(1968). Lancet. A weighing machine for developing countries. (1969a). J. Pediat., 74, 808. (1969b). Amer. J.Clin. Nutr., 22, 1159. and Dean, R. F. A. (1959). J. trap. Pecliat., 5, 96. and Jelliffe, E. F. P. (1960). Amer.}. Publ. Hllh., 50, 1355. and Welbourn, H. F. (1963). In: Mild-Moderate Protein-latric Malnutrition, p. 12 Symposia of Swedish Nutrition Foundation I. Jelliffe, E. F. P. and Jelliffe, D. B. (1968). J. trop. Pediat., 14, 71. Malcolm, S. (1956). Nutrition investigations in Samoa. South Pacific Commission. Noumea, New Caledonia. Mason, E. D., Mundkur, V. and Jacob, M. (1963). Ind. J. wed. Res., 51, 925. McCance, R. A. (1964). J. Pediat., 65, 1008. McFie, J. and Welbourn, H. F. (1962). J. Nutrit., 76, 97. Montgomery, R. D. (1962). / . Clin. Path., 15, 511. Oomen, H. A. P. C. (1953). Bull. World Hllh Org., 9, 371. Picou, D. and Waterlow, J. C. (1961). West Ind. med. J., 10, 36. Platt, B. S., Miller, D. S. and Payne, P. R. (1961). In: Recent Advances in Human Nutrition, p. 35. London. Smythe, P. M. (1958). Lancet, ii, 274. Standard, K. L., Lovell, H. and Garrow, J. S. (1966). J. trop. Pediat., II, 100. , Wills, V. G. and Waterlow, J. C. (1959). Amer. J. Clin. Nutr., 7, 271. Trowell, H. C , Davies, J. N. P. and Dean, R. F. A. (1954). Kwashiorkor. Edward Arnold: London. Waterlow, J. C. (1948). Fatty liver disease in infants in the British West Indies, Spec. Rep. med. Res. Coun. No. 263. (1963). Proc. Nutr. Soc, 22, 66. , Cravioto, J. and Stephen, J. M. (1960). Adv. in Prot. Client., 15, 131. and Mendes, C. B. (1957). Nature, 180, 1361. and Scrinshaw, N. S (1957). Bull. World Hllh Org., 16, 458. (1969). Personal communication. Whitehead, R. G. (1964). Lancet, 1, 250. (1965). Lancet,!, 567. (1968). Unpublished data. World Health Organization (1963). Expert Committee on Medical Assessment of Nutritional Status. Techn. Rep. Series No. 258.

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December, 1969, The Journal of Tropical Pediatrics