1. Arm Circumference Public Health Index of Malnutrition, Jelliffe & Jelliffe 1969

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    179THE ARM CIRCUMFERENCE AS A PUBLIC HEALTH INDEX OF PROTEIN-CALORIEMALNUTRITION OF EARLY CHILDHOOD

    (I) BACKGROUNDby

    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 consideredas a public health "iceberg" (Fig. 1), in which the two main severe syndromeskwashiorkorand nutritional marasmusare easily detected and classified by inspection, and the many"intermediate" severe cases found between these two polar extremes can also be recognizedclinically. However, in poorly nourished communities, far larger numbers of children withmild-moderate PCM exist, hidden and often unrecognized beneath the clinical surface (JELLIFFE,1959 and 1969b).

    KWASHIORKOR MARASMUS

    FIG. 1. The Protein-CalorieMalnutrition (PCM) Iceberg.

    SEVERE

    MODERATE

    MILD

    ASSESSMENT OF MILD-MODERATE PCMIn|o rde rto assess the nutritional status of children in a community, tests have to be devisedto identify and classify children with what is here termed "mild-moderate PCM," and haselsewhere 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 communi-ties kwashiorkor is the main severe syndrome and in othe rs, marasm us. Also, the clinicalfeatures vary in prevalence from one part of the world to another, depending on the interactionof numerous local variables, including genetic characteristics, associated nutrient deficiencies,types of microbiological and parasitic conditioning infections, the sequence, severity and rate ofdevelopment 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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    180 E. F. PATRICE JELL1FFE AND DERRICK B. JELLIFFEThree main direct methods of assessing PCM in the community have been used: (1) clinicalsigns, (2) biochemical tests, and (3) anthropometry (GOPALAN, 1970).(1) Clinical Signs. Eleven clinical signs* have been listed as being suggestive of protein-calorie 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 constan tly present; especially inmild-moderate PCM (STANDARD et al., 1966), and also vary in prevalence from one part of theworld to another, depending on the inter-action of many ecological factors, and whether thekwashiorkor "line-of-development" or the marasmus "line-of-development" is the main abnorm-ality in the community (Fig. 2).However, the detection of clinical signs does not require costly apparatus and can becarried out rapidly on large num bers, provided th e examiners have been carefully and practicallytrained, and the definition of the lesions sought for have been standardized, as far as possible.

    Mild

    Moderate

    Severe

    \ 1K. "Line of flo

    V" E a r | y " < - -kwashiorkor

    V

    Growthretardation(body w eight)1

    Zm

    O-1V*

    Kwashiorkor

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    E. F. PATRICE JELLIFFE AND DERRICK B. JELLIFFE 181

    (2) Biochemical Tests. Various biochemical tests have been suggested for the detectionof early PCM. The serum protein levels, particularly albumin, have been employed, but,according to most workers, significant changes are not demonstrable until clinically obviousPCM occurs. However, recent work suggests the need for further assessment in communitysurveys.Relatively recently, two new tests have been devised that seemed particularly appropriatefor field surveys. These are the amino acid imbalance test (WHITEHEAD, 1964), which can becarried out on a capillary tube sample of blood collected in the field, and the hydroxyprolineexcretion test (WHITEHEAD, 1965), which only needs a few cubic centimetres of a randomlycollected urine sample.Unfortunately, these tests need a sophisticated laboratory to carry them out, and recentwork has shown that their interpretation is difficult in relation to the locally most prevalentform 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 theresults related to the child's body length (ARROYAVE and WILSON, 1961).Biochemical tests have the undoubted value of being independent of precise knowledge ofage, but at the moment those presently available are not usually feasible in unelaborate com-munity surveys or other forms of field assessment. .

    (3) Anthropometry. Growth failure and a variable degree of body disproportion arerecognized features of severe malnutrition in experimental animals ( M CCA N CE, 1964) and inPCM (JELLIFFE, 1966), especially in the severe syndromes of kwashiorkor and marasmus.In community surveys, various body measurements have been suggested to assess theprevalence 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 circumferenceand the triceps skinfold (JELLIFFE, 1966); while if, as is often the case, precise ages of childrenare not known with accuracy, then the following ratios or "year constant" measurements havebeen suggested: weight-for-height, weight-for-head circumference, chest/head ratio and thearm circumference.; Body weight has been the main measurement employed in community surveys of youngchildren. However, it is less simple to measure accurately than usually realized, and insufficientattention has so far been given to producing an appropriate weighing device for use for youngchildren in field circumstances.f Also, the interpretation of the weights of children duringthis rapidly growing phase of life depends on precise knowledge of the ages of those examinedand on the selection of appropriate standards of comparison.There is, therefore, a considerable need for simple anthropometric measurements for usein field circumstances which have the following characteristics: (i) capable of being carried outby trained para-medical staff, (ii) require only inexpensive, easily available apparatus, (iii) givereasonably replicable and easy to interpret results independent of knowledge of the precise age,capable of giving scientifically valid, albeit approximate, information concerning the prevalenceof 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 ofI kg. (WATERLOW, 1969).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 handweighing as little as possible, compact, with carrying handle and locking device); (v) clear readabilityscale 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 totand on, and (vii) weight range up to 80 kg. (to permit weighing frightened, struggling pre-school childrenn the arms of a mother or attendant). (JELLIFFE, 1968).The Journal of Tropical Pediatrics, December, 1969

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    1 8 2 E. F. PATRICE JELLIFFE AN D DERRICK B. JELLIFFE

    MUSCLE DEFICIT AND PCMMuscle is the largest protein containing "organ" in the body and the major componentof the "lean body mass ." There is considerable clinical, anthropom etric, morphological andmetabolic evidence that, as might be expected, the myoglobin protein reservoirs of the mus-culature are particularly depleted in protein-calorie malnutrition of early childhood.(i) Clinical Evidence. The muscle deficit seen in severe PCM received emphasis in clinicaldescriptions 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 depletedmuscles (which could, however, be palpated, especially "the attenuated bellies of the upperlimbs").OOMEN (1953) in his studies in Indon esia stressed "m uscle atr op hy " as one of the commonest

    features. He notes that this was often no t included in descriptions of the characteristic pictureof kwashiorkor, and he emphasised its significance as an important sign of protein depletion,which could be "judged from o utsi de." The palpab le muscle tissue was observed to be laxand 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, includingpreviously active toddlers developing kwashiorkor and "going off their feet" (which could inpart be related to apathy and psychomotor change), and showing lordosis, potbelly, wingedscapulae and hanging heads.Numerous more recent accounts stress muscle deficit as a constant clinical feature in bothkwashiorkor (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 thesupine child up by his arms into a sitting position and noting his ability to hold his head up andto sit without su ppo rt. However, in addition to being difficult t o measure objectively, weaknessis complicated as a measure of muscle mass, both by psychological changes increasing the child'sunwillingness to cooperate, and by possible decreased muscle tone associated with depletedbody electrolytes, especially potassium (GARROW et al., 1968).(ii) Anthropometric Evidence. The anthropometric assessment of muscle deficit has beenattempted by measurement of limb circumferences, especially the upper arm, and by variouscalculations 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 innumerous surveys in Samoa and other South Pacific countries, where she found that typical"wean ing" retard ation of weight gain was associated w ith considerable an d prolonged reductionin calf girth.In young children with severe PCM, the limb circumferences have been shown to be amongthe most markedly affected bo dy measurements. Th us , in a large scale study in India , GOPALANweisht(1968) found that weight, -, calf circumference and arm circumference showed theheight2maximum difference between normal children and those with PCM.Likewise, Ugan dan children with -kwashiorkor were found to have very diminished armand calf circumference (Table I).The approximate underlying muscle circumference can be calculated from measurementsof the arm circumference and overlying skinfolds (JELLIFFE and JELLIFFE, 1960); and M C F I Eand WELBOURN (1962) found a positive correlation between muscle size in the arm as calculatedfrom 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 andradiography in young Jamaican children hospitalized with severe PCM and during recovery.

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    E, F, PATRICE JELL1FFE AND DERRICK B, JELLIfFE 183Their results suggested that the decrease in muscle mass was greater In these malnourishedbabies than bo dy weight deficit. Also, the calculated mu scle measureme nts increased with .nutri t io nal reh abili tat ion, and were significantly c orrelated with increased urinar y outp uts ofcreatinine, considered the most direct biochemical index of muscle mass (Fig. 5).

    FIG, 3. Classical kwashiorkor (Uganda), FIG. 4. Classical marasmu s (C. America).

    TABLE I. Mean arm and leg circumferences of Ugandan children with and without oedema (DEAN, 1966).

    SexMale

    Female

    ConditionKwashiorkorHealthyKwashiorkorHealthy

    OedemaSlightMarkedAbsentSlightMarkedAbsent

    Arm circumference (cm.)(Age in months)10-15 | 15-2111.3 1 11.411.9 I 12.414.8 j 14.811.0 1 11,611.6 | 12.814.5 14.2

    21-2611.312.215.611.412,514.6

    Leg circumference (cm.)(Age in months)10-15 | 15-2114.015.818.214.514.817.6

    14.216.918.115.216.918.9

    21-2614.716.918.714.4.16.819.7

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

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    184 E. F . PATRICE JELLIFFE AND DERRICK B, JELLIFFE

    4 *

    3Cs)a

    I-5

    i-o

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

    M e 5. Relation between in-crease ia muscle thickness andincrease in creatinine outputin malnourished infants duringtreatment (From Standard,Wills and Waterlow, 1959).

    1-0 I S 2-0Increase in creatinine output 2- 5(iii) Morphological Evidence. Gross wasting of musculature is a characteristic autopsyfinding in fatal severe PC M. The muscles are often noted to be pale and reddish-grey. Histoiogieal evidence of severe muscle change was documented by WATERLOW (1948), whonoted in autopsies that "the muscles are shrunken and small. The fibres are atrop hic and withgross loss of sarcoplasm. The fibres having shrunk away from the surroundin g perimysiumso 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 striatedmuscle 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 theremark able decrease in muscle cross-section in severe PCM . Thu s, the sartorius muscle of amalnourished infant of 12 months approximated in cross-sectional area only to that of a normalfoetus 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

    SCHOPNHEIMER'S concept of the dynamic state of body proteins, especially that the turnoverrate varies with different proteins in different tissues. In the gut mucosa, pancreas, liver andplasma, the turnover rate is fast; while in the liver and especially muscle tissue, it is relativelyslow.

    FIG. 6. Transve rse section of whole sartoriu smuscle in malnourished infant aged 12 months(top left), compared with foetus at 31 weeksgestation (top right) and a well nourished infantaged 13 months (below) (From Montgom ery,1962).

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    E. r. PATRICE JELLIFFE AN D DERRICK B. JELLIFFE 1 8 5Muscle and liver tissue have been shown to have lost up to 50% of their protein in severe

    PCM, as judged by biopsy results (WATERLOW an d MENDES, 1597); while whole body analysishas shown that in "severe infantile malnutrition" the total protein is reduced to of normal fora child of the same length (GARROW et al., 1965).SELECTION OF ARM CIRCUMFERENCEThe "mid-upper arm circumference"abbreviated to "arm circumference" (arm girth)has, therefore, been suggested as a potentially useful, simple field index for the assessment ofPC M (JELLIFFE, 1959 and 1966). It was felt tha t there was evidence that the m easurementwould give composite information simultaneously on three important effects of PCMdeficitin 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 andlesser involvement with clinical oedema (and, presumably, with subclinical water retention).However, as noted earlier, MALCOLM (1956) has found the calf circumference a useful measure-ment 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 theassumption that all the body musculature is uniformly affected in PCM which seems likely,althoug h unp roven . Its value as a measurement of local muscle mass has to bear in mindthe effects of possible clinical or subclinical oedema, excess subcutaneous fat, and changes indimensions of other tissues in the arm, including the diameter of the humerus.Despite its apparent simplicity, anthropometric opinion emphasized that the mid-pointof 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 " co nstant pressure with a flexible, non-stretch, steel or fibre-glass/tape (JELLIFFE, 1966).Tentative stand ards of comparison were suggested based on data collected by Dr . NAPOLEONWOLANSKI 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 circumferenceincreased only very gradually during the second to fifth years, the possibility of using the following so-called "year-con stant" standards was proposed : second year16 cm.; third year16.25cm.; four year16.5 cm .; fifth year16.75 cm. It was felt that these measurements could be ofspecial value in community child nutrition surveys where precise documentary verification ofage 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 feltthat the "year-constant" standard for the second year of life (16 cm.) might be used in com-munities where exact ages were not known during what has been termed the "dental secondyear"possibly defined all children with from 6-18 teeth (JELLIFFE an d JELLIFFE, 1968).Arm muscle circumference. The mid-upper arm muscle circumferencefabbreviated toarm muscle circumferencecan be calculated from th e formula C2 = Cl -s (Fig. 9).Various skinfold thicknesses (s) have been used, including th e biceps (JELLIFFE and JELLIFFE,1960), an average of the biceps and triceps (STANDARD et al., 1959), or the triceps along (Fig . 10)' M C F I E and WELBOURN, 1962; JELLIFFE, 1966). For practical purposes, the triceps skinfoldlas 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 imp ortant to converthe skinfold reading from millimetres to centimetres when calculating the arm muscle cir-cumference, as the arm circumference is usually measured in these units.

    *The term "secotrant" has been suggested for a child in the second year of lifea secondyear transitionalJELLIFFE, 1969a).tAlternatively, the "inner arm diameter" has been calculated (MCFIE and WELBOURN, 1962; MASONt al., 1963). 'he Journal of Tropical Pediatrics, December, 1969

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    18 6 E. F. PATRICE JELLIFFE AND DERRICK B. JELLIFFE

    51160FIG. 7. Assessing mid-po int of arm (From Jelliffe,1966).

    0 51159

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

    FIG. 9. Calculation of the arm muscle circumference d =. ar m circumference; S = skinfold (2 x su b-cutaneous fat); di = arm diameter; d. = muscle diameter; S = d t d; G> (muscle circumference)d ( d d ) CDecember, 1969, The Journal of Tropical Pediatrics

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    E. F. PATRICE JELLIFFE AND DERRICK B. JELLIFFE 187DI SC USSI ON

    As it became apparent that the arm circumference was being tried out as a public healthindex of PCM in different parts of the world, the following papers and notes concerning experi-ence 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 l imitations of the armcircumference as a simple field index of PCM, including such technical aspects as method ofmeas ureme nt, reprod ucibil i ty and preferred typ e of tape measu re; its com pariso n "with othermethods of assessment, especially the weight-for-age and i ts l imits of normality, and usefulnessas a quantitative measure of the degree of malnutri t ion.

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

    It was also hoped to obtain information on i ts practical uti l i ty in different field si tuations,such as community surveys or the screening of young children in emergency food distributionprogrammes .REFERENCES

    Arroyave, G. and Wilson, D. (1961). Amer . J. C lin. 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 W ard, E. E. (1968). Electrolyte metabolism in severe infantile malnutrition. Perg-amon Press: Oxford & London.Gop alan, C. (1968). Assessment of protein nutritional status. Unpublished data.(1970). Amer. J. Clin. Nutr., in press. Report of IUN S Comm ittee on Assessment of ProteinMalnutrition.Jelliffe, D. B. (1959). J. Pediat:, 54, 277.(1966). The assessment of the nutritional status of the comm unity. WH O Monograp h 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). Ame r. J.Clin. Nutr., 22, 1159.and Dean, R. F. A. (1959). J. trap. Pecliat., 5, 96.and Jelliffe, E. F. P. (1960). Ame r.}. Publ. Hllh., 50, 1355.and Welbourn, H. F. (1963). In: Mild-Mod erate Protein-latric Malnutrition, p. 12 Symposiaof 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. Noum ea, NewCaledonia.Mason, E. D., M undkur, 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 Hum an 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 H ealth Organization (1963). Expert Committee on Medical Assessment of Nutritional S tatus.Techn. Rep. Series No. 258.

    December, 1969, The Journal of Tropical Pediatrics

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