British Medical Bulletin (1981) Vol. 37, No. 1, pp.



but they do not, in any way, distinguish causes in the same
manner that the term protein-energy malnutrition quite
specifically suggests a dietary cause.
We can therefore make clinical distinctions between kwashi-
THE BIOCHEMISTRY AND orkor and marasmus, but the object of many experimental
PHYSIOLOGY OF KWASHIORKOR studies, and of dietary surveys in different parts of the world,
has been to find differences in their dietary aetiology. It is well
AND MARASMUS known that it is necessary to feed experimental animals
unrestricted amounts of diets low in protein to produce a
W A COWARD PhD syndrome resembling kwashiorkor; restricting the intake of any
diet will result in severe wasting. Survey work in Uganda
P G LUNN PhD (Whitehead et al. 1977) also showed that, when diets with a
wide range of protein: energy ratios are available within a
University of Cambridge
and community, it is the children who habitually consume diets from
Medical Research Council the low end of the range (protein: energy, 0.04-0.06) who are at
Dunn Nutritional Laboratory, Cambridge risk of developing kwashiorkor. These observations contrast
with others typified by those of Gopalan (1968). He showed
that, in Indian children eating cereal-based diets with a relatively
Concepts and definitions: protein-energy malnutrition, constant protein: energy ratio (0.08), either kwashiorkor or
kwashiorkor and marasmus marasmus could emerge if energy intakes were low. Taking
Adaptation to a deficiency of energy: the pathogenesis of extreme views would therefore suggest that kwashiorkor and
marasmus marasmus represent different aspects of the same disease (as the
Failure of adaptation to protein deficiency: the pathogenesis
term protein-energy malnutrition suggests) or that they are
of kwashiorkor
Pathogenesis of intermediate forms of protein-energy different diseases with distinguishable aetiologies.
malnutrition Protagonists of each idea have ample support for their
Regulation of body fluid volumes in protein-energy arguments but it is unrewarding to initiate a discussion of the
malnutrition aetiology of kwashiorkor and marasmus by emphasizing one
a The distribution of extracellular fluid volume theory to the exclusion of the other. A more realistic approach
b Sodium and water balance is to accept that each idea makes a worthwhile contribution in a
c Membrane defects and the sodium pump
worldwide context but that causes can differ in individual,
Plasma proteins in kwashiorkor and marasmus
References regional circumstances.

It is just four years since Alleyne et al. (1977) published their 2 Adaptation to a Deficiency of Energy: the Pathogenesis
comprehensive treatise on protein-energy malnutrition. In this of Marasmus
paper we will focus on a few developments in biochemistry and
physiology that we believe are important for our understanding It is now widely accepted that the severe wasting seen in
of how the clinical features of the disease emerge in children marasmic children represents the end-product of metabolic
subjected to a hostile environment and inadequate diet. adaptation to an inadequate energy intake, mediated by changes
in hormonal pattern. Although a child is not clinically identified
as a case of marasmus until weight-for-age falls below 60%, the
1 Concepts and Definitions: Protein-Energy Malnutrition,
relevant metabolic changes can be detected, within a community
Kwashiorkor and Marasmus
where marasmus occurs, well before this stage is reached.
In recent years it has been customary to use the term Whitehead et al. (1977) and Lunn et al. (1979a) showed that
"protein-energy malnutrition" to describe a group or spectrum fasting plasma cortisol and growth hormone (GH) levels were
of diseases that often affect children living in poor communities high but insulin concentrations were low in Gambian children
in most developing countries. The expression suggests impor- with faltering growth rates, and insulin: cortisol ratios were
tant concepts. These are that inadequate intakes of energy or strongly correlated with growth velocities (Lunn et al. 1979a).
protein, or both, are causative factors and that there is a The changes seen when children are admitted to hospital
continuous connection in terms of biochemistry and physiology (reviewed by Alleyne et al. 1977) are only more exaggerated
between the extreme forms of protein-energy malnutrition, examples of the same pattern.
which are kwashiorkor and marasmus. A reduction in plasma insulin concentration is a normal
For comprehensive clinical descriptions of the two syndromes response to a reduced food intake and extremely low values are
the reader may refer to Alleyne et al. (1977), but for the present seen in marasmic children admitted to hospital. Cahill (1970)
it will be sufficient to use a series of internationally accepted suggested that a decreased level of this hormone is the main
definitions suggested by a Wellcome Trust Working Party regulator for the release of energy metabolites from endogenous
(Lancet, 1970). The crucial diagnostic features are the degree sources. Raised plasma cortisol concentrations will augment
of body wasting and the presence of oedema. Thus, when the effect on the mobilization of skeletal muscle protein,
Harvard weight standards (Stuart & Stevenson, 1959) are used, releasing amino acids for gluconeogenesis and perhaps for the
children of 60-80% expected weight-for-age are called cases of hepatic synthesis of plasma proteins. Adipose tissue
kwashiorkor if oedema is present. Below 60% the diagnosis is mobilization will be enhanced by changes in GH concentra-
marasmic kwashiorkor if they have oedema or marasmus if tions, and free fatty acids will become available as alternative
oedema is absent. These definitions have the merit of simplicity sources of energy (Parra et al. 1973).


Vol. 37 No. 1

1977). metabolism is geared to survival. Mann et al. Tulp et al. The mechanisms we have discussed are clearly similar to 1968. By promoting muscle protein found in marasmic children with the same degree of anorexia synthesis. indicate that adding chromium to the diet produces a similar The endocrine pattern in non-hospitalized Ugandan pre. 1979). hospital (Alleyne et al. 1968) and Turkey (Giirson & Saner. 1977) and a markedly elevated tri-iodothyronine likely explanations (see section 4). 1977). it would explain to a fatty liver. effect. problem of adaptation is how to deal with the energy excess. amounts of cortisol adequate for adaptation to protein-energy Hypoalbuminaemia could lead to defects in body fluid homo. Anthony & even after a single meal. This view is substantially different from the eostasis and oedema. but there are some features not Plasma cortisol and GH levels were not elevated. Thus the rat is a poor model for kwashiorkor and a few days of feeding meals containing protein (Pimstone el al. but no fully understood. We believe. is the one adopted. very different from that which existed earlier in his illness but much more like that found in marasmus. malnutrition. 20 Br. 1974. as values 3 Failure of Adaptation to Protein Deficiency: the will be influenced by the duration and severity of the clinical Patbogenesls of Kwashlorkor phase of the illness. There is also an inverse relationship Edozien. and certainly it has been therefore. 1981) also exists in the response of children discussed by Pimstone et al. In general. (1973). Data from Jordan determine the kind of protein-energy malnutrition that even. The course taken may ultimately faster return to a normal insulin respose. 1968). Locking away cortisol may be a feature of kwashiorkor. If true. Lunn et al. becomes easier to understand. These non-essential amino acids typical of the developmental phases of results suggest that a defect in the adrenals' ability to produce kwashiorkor (Grimble & Whitehead. 1970). Kajubi & Okel. There need. endemic. Bull. (Hopkins et al. hied. be no hypoglycaemic stress and consequently no shown that short-term fasting in healthy subjects results in elevation of plasma cortisol or GH to cause wasting. from an early stage. high insulin concentrations will deplete the plasma of and infection. Fasting plasma insulin concentrations in these GH concentration is elevated and thyroid hormone concentra- children were higher than in children who had recovered from tions are either normal or reduced (Alleyne et al. that there are other more (Coward et al. 1968. There can be only two options: energy can be stored as fat or it potassium supplementation of rehabilitation diets results in a can be removed by oxidation. 1981 . However. 1973). (1975) have shown that. The those involved in the development of obesity and. 1968). or marasmus on identical diets. even when energy intakes could be argued that this might be expected in a child whose are lower than recommended requirements. feedback stimulus for GH release (Mohan & Jaya Rao. It must be a relative excess of energy. marasmus because they fail. 1977). (1973) showed that this response occurs Enwonwu & Sreebny. 1979). The considerable variation that exists between reports is not surprising. they are usually lower than those insulinaemia and fat deposition. in South African children. however. This change can be regarded as A child admitted to hospital with kwashiorkor is usually an effective adaptation. Children with all forms of protein-energy malnutrition have a When the low protein content of a diet limits growth there poor insulin response to a glucose load (Alleyne et al. then the situation described by Gopalan somatomedin concentrations are low in children with kwashi- (1968) in India. 1968). since lowering the basal metabolic rate described as apathetic and anorexic and the hormone profile is will conserve the meagre supplies of energy available. to produce including albumin and apo-proteins for (J-lipoprotein synthesis. cortisol values are often elevated complete source of information on the hormonal profiles of and correlate with the degree of wasting and the severity of pre-school children living in an area where kwashiorkor is intercurrent infections (Abbassy et al. the appearance of kwashiorkor in children who. This latter Plasma GH concentrations are high in children with response enables the animals to "burn-off' any energy excess kwashiorkor and are not reduced by glucose loads (Pimstone et and will prevent the development of changes we have described al. already in short supply.BIOCHEMISTRY AND PHYSIOLOGY OF KWASHIORKOR AND MARASMUS W A Coward & P G Lunn Reductions in the plasma concentration of thyroid hormones cance of a high variability in the unrelated individual require- have also been reported for marasmic children admitted to ments for protein and energy. assessed by plasma albumin concentrations (Pimstone el al. 1971) tually develops (see MacLean & Graham. The malnutrition. only by feeding diets virtually free of protein (Edozien. 1978. but a number of possibilities are (James & Trayhurn. because of in- Rats do not respond to low-protein diets in this way and adequate food intakes. 1967). plasma insulin concentrations The study of Lunn et al. it has been demonstrated that they fall after in children. However. 1979). 1977). The impaired glucose tolerance (Vance et al. Although plasma to low-protein diets. 1971. level (Edozien et al. If the excess energy is not removed. and by inhibiting Synacthen (synthetic P'~24 adrenocorticotrophic hormone) gluconeogenesis will cause an accumulation of alanine and other results in a poor response (Jaya Rao et al. 1967. 1975. Lunn el al. 1979) can this adaptation between GH levels and the severity of protein deficiency as be overcome. 1968). Robinson et al. 1974). children with kwashiorkor. where children can develop either kwashiorkor orkor. might otherwise be expected to become instead have a much reduced plasma insulin concentration marasmic. blood Although plasma cortisol concentrations are elevated • in glucose concentrations will tend to rise and result in hyper. 1973. anorexia and hypoglycaemia. and stimulation of the adrenal cortex with essential amino acids. if the mechanisms regulating plasma GH concentrations in kwashi- considerable degree of individual variation to over-eating orkor have not been identified. but this was not found to be the case in Egyptian children school children indicates that the first of these possible pathways (Carter et al. Philbrick & Hill. there is no evidence to support the suggestion (Grant el al. Fiorotto & Coward. Jaya Rao (1974) essential amino acids in muscle when protein intake is low is proposed that some children develop kwashiorkor rather than likely to produce a fall in hepatic synthesis of export proteins. (1973) in Uganda remains the most are reduced but can be normal. and deficiencies in (J-lipoprotein synthesis dietary ideas we have already outlined. 1973) that impaired somatomedin production might cause a Waterlow (1974) has previously pointed out the likely signifi. information on thyroid hormone concentrations was obtained. and much higher than those found in Gambian changes described are in most cases the expected responses to pre-school children of the same age (Whitehead et al.

but Fiorotto and W A Coward. This idea indicates that blood and plasma volumes will be reduced in kwashiorkor and the most recent observations with labelled erythrocytes (Viart. in the face of the unlikely that GH-mediated changes are directly involved in the circulation's reduced ability to hold retained fluid. irrespective of the presence of oedema. activity in oedematous malnourished rats but not in non- This represented a proportionally larger change in interstitial oedematous animals. BIOCHEMISTRY AND PHYSIOLOGY OF KWASHIORKOR AND MARASMUS WA Coward & P G Lunn Since plasma GH concentrations rise only in the terminal stages lost. 1973) and baboons (M tinguishes kwashiorkor from other forms of malnutrition. it is more insistence that changes in plasma albumin concentration are likely that non-nutritional factors modulate the effects of the functionally important in the development of kwashiorkor and diet. interstitial volume expansion will occur. preventing excessive those with kwashiorkor. because in normal animals the Westhuysen et al. experi- example of a failure of homoeostasis that specifically dis. 1 . in preparation) have shown that until recently little progress had been made in identifying its reductions in RPF and GFR are early effects of feeding cause. 1972). interstitial fluid protein oedema was present. the distribution of extracellular fluid between the vascular and (1973) found either normal or increased aldosterone secretion interstitial spaces. effects of diet and accelerate wasting in children developing marasmus. two distinctly different views can now be low-protein diets and are not associated with evidence of identified. They observed that. The differences could be attributed to different We have suggested that the endocrine response to a diet can methodologies. the concept that children with kwashiorkor are over-hydrated We have also recently suggested (Lunn et al. Alternatively. For example. However. published data show that renal plasma flow (RPF) and glomerular filtration rate (GFR) are decreased but. idea begins with kwashiorkor. sodium retention could result from a The Distribution of Extracellular Fluid Volume elevated plasma aldosterone levels and increased plasma renin Coward & Fiorotto (1979) and Fiorotto & Coward (1979) activity but. It was proposed that the incidence of infections that of any other plasma protein. the homoeostatic mech. al. 1975b) showed that children suffering from plasma: interstitial fluid concentration ratio is about 2. when plasma monkeys fed low-protein diets and found elevated levels when protein concentration is reduced by half. the same group of workers (Van der fluid protein concentration. when plasma protein rates in malnourished children but plasma concentrations were concentrations fall in protein-deficient rats. We believe that many children with the development of oedema. Worthington et range of plasma protein concentrations. because albumin synthesis admitted to hospital with oedema have the underlying rates are unalterably low (Patrick. Viart suggested that in malnutrition plasma determine how available nutrients are used. in preparation) showed that further reduction in plasma protein content will produce an changes in aldosterone concentration and plasma renin activity imbalance of the transcapillary forces and the organism's can precede the appearance of oedema by many months. Active renal salt and water retention might then occur to of the development of kwashiorkor (Lunn et al. excessive salt and water retention. result of an increased gastrointestinal loss of plasma proteins. At this stage any (M Fiorotto & W A Coward. At the tubular level. when a malnourished child develops sodium there may be another important way in which marasmic and water retention. further early pathogenesis of this disease. Migeon et al. while these 5 Regulation of Body Fluid Volumes In Protein-Energy changes will undoubtedly limit the potential for salt and water Malnutrition excretion. a normal balance of normal in children with marasmus and elevated in only half of transcapillary colloid osmotic pressures. Klahr & Alleyne (1973) identified factors that causes of such losses are a measles infection or the presence of could impair the ability of malnourished children to excrete intestinal helminths. by the recognition that the contribution of albumin to the total A conventional view was outlined by Whitehead & Lunn colloid osmotic pressure of plasma (>50%) is greater than that (1979). Furthermore. and it is theoretically volumes measured with protein-bound tracers could be mis- possible that. they are not specifically associated with the presence The appearance of oedema in malnourished children is an of oedema in children (Alleyne. With only one exception (Srikantia. as a result of the alternating dominance of energy leadingly large. 4 Pathogenesis of Intermediate Forms of Protein-Energy 1977) show that this is the case. again. or protein deficiencies. 37 No. While protein-energy malnutrition have elevated plasma renin ac- this adaptation to hypoproteinaemia is effective over a large tivities. although Van der water filtration. or perhaps complementary. Srikantia (1968) postulated a role for antidiuretic 21 Vol. control over the distribution of extracellular fluid volume will be Finally. evidence for a specific association with the believe that the most important factors are those that determine presence of oedema is ambiguous. ments with sheep (Rabinowitz et al. cumstances the task is to identify the reasons for phases of oedema and hypoproteinaemia have appeared precipitously as a sodium retention in malnourished children. In these cir- metabolic features of marasmus. Likely renal function. but our own serial studies with baboons concentrations reach values close to zero. marasmic kwashiorkor might emerge The development of these ideas was stimulated by an (Whitehead & Alleyne. in practice. severe wasting could be induced in b Sodium and Water Balance children who are otherwise likely to present as cases of The alternative. In addition. (1977) measured plasma aldosterone concentrations in anism does not possess infinite gain because. 1968). it is prevent plasma volume contraction but. 1979b) that and suggests that. was maintained by a reduction in the colloid Westhuysen et al. contradicting much of the Malnutrition earlier work. 1979). (1975a) found increased plasma renin content of interstitial fluid that matched the changes in plasma. sodium loads. plasma albumin concentrations will fall kwashiorkor can develop. 1973). 1967). but other abnormalities occur and elevate plasma glucocorticoid concentrations will alter the their importance has to be considered. not In a review of the effects of protein-energy malnutrition on compensated for by increased rates of protein synthesis. However. Superimposed on these.

1975. remains. 1965.23-30 of thiiBuBttm. Children with kwashiorkor can that a decrease in transferrin concentration caused by mal- lose their oedema and decrease their total body water from 77% nutrition can be masked by an increase due to a lack of iron to 63% of body weight when they are fed diets not known to (Ismadi et al. In contrast to this situation. PP. 1980). produce substantial changes in rates of plasma protein synthesis. and in protein deficiency reduced rates of urea for malnutrition. three plasma proteins results obtained for erythrocytes. but this idea has not been 1965). where the functional significance c Membrane Defects and the Sodium Pump of changes in the concentration of a plasma protein is In following up lines of thought developed by Metcoff (1975). include those with marasmus. (1970) and Gabr et observations and. It is unlikely that changes in only one aspect of universally accepted. There associated with a poor prognosis in children with kwashiorkor. pp. It could be argued (Fiorotto. BIOCHEMISTRY AND PHYSIOLOGY OF KWASHIORKOR AND MARASMUS W A Coward & P G Lunn hormone in oedema formation. recognized. Furthermore. Delpeuch et al. Bull. however. For also on utilization and catabolism. Wright & Briggs (1979) have recently reviewed the butes to oedema formation. In this way it is possible to build normal children. 1980) that measurement of plasma protein concentrations for the assess- hypoproteinaemia and low plasma oncotic pressure in the ment of nutritional status. 1978. and sensitivity to reduced protein intake responsible for the distribution of body water between plasma. Observations made by Patrick et al. if mirrored at the level of the renal tubule. secondly. 1981 . never elevated in malnourished children. and in these circumstances other indices of malnutrition However. (1971) showed that low transferrin concentrations were could cause increased fractional sodium resorption. essentially because urine osmolality is regulative physiology will be able to explain these findings. Ingenbleek et al. which could be balance between these processes that determines whether the achieved only by an increase in membrane permeability to concentration of a specific protein reflects the degree of sodium and subsequent stimulation of the sodium pump. Nichols et There are a multitude of reports on the usefulness of the al. it is clear that its measurement is evidence for the existence of a mechanism by which GFR in a useful in communities where kwashiorkor is the predominant single nephron is regulated by the composition or rate of flow of form of malnutrition. since the plasma con- tubule cell physiology in malnutrition. (1969). malnourished children can complicate the situation to the extent (1978) illustrate the problem. other workers report even indicators of nutritional status (Ingenbleek et al. There is no information on this aspect of renal This strategy is inevitably empirical. 22 Br. However. 1973). In these circumstances the manner in which convenient to classify children according to their albumin the kidney regulates salt and water balance in relationship to concentration and to relate other biochemical changes to these intake may not have the precision of response available in values (Whitehead et al. McFarlane et al. total body water from 64% to over 70% of body weight in 14 Plasma RBP and TBPA have also been proposed as sensitive days but oedema does not appear.and substrate-dependent component) but (Kaplay. The connection between these observations and those 6 Plasma Proteins in Kwashiorkor and Marasmus showing that fractional sodium reabsorption can be decreased in malnourished oedematous children (Alleyne. The protein-energy malnutrition. 1973) is not clear. if an energy intake in excess of requirements is a related to deficits in weight. but it is suggested that centration of any protein is dependent not only on rates of findings for leucocytes (Patrick. S « Nirumg* R«o. rates of intravascular- leucocytes it was shown that there were dramatically increased extravascular exchange and the degree of hydration. 1971. 1979) and erythrocytes synthesis (the diet. changes in its plasma environment in the renal medulla needed for salt and water concentration should be meaningful in terms of the ultimate reabsorption in later segments. al. In the first instance it should be responsive to synthesis would lead to the dissipation of the hypertonic changes in nutrient intake and. the latter workers Trace element deficiencies1 could provide the link (Patrick. malnutrition.—ED. Fondu et al. ouabain-sensitive Na-K adenosinetriphosphatase activity is thyroxine-binding prealbumin (TBPA) and retinol-binding pro- increased (compared with normal and recovery values) in tein (RBP). kwashiorkor but not in marasmus. up a comprehensive picture of the development and resolution of kwashiorkor. in experimental animals (Olusi et al. where it was found that have consistently attracted attention: these are transferrin. Our general view is that malnutrition because of its rapid response to refeeding in there is a need to separate the influence of those factors malnourished children. 1979) may be relevant. 1975.and length-for-age in under- significant dietary component. hied. 1972. we can describe the "sensitivity" of a particular Patrick (1979) commented on the significance of changes in protein in malnutrition without simultaneously considering membrane permeability and the activity of the sodium pump in nutrient intake or the final form of malnutrition that emerges. a thermogenic response involving nourished children although albumin concentrations were not increased sodium pumping might be relevant Others have also advocated the use of plasma transferrin It will be clear that we are some way from integrating all these concentration as a most sensitive index of protein-energy observations into a concise framework. the the interstitium and cells. and those controlling the general frequency with which iron-deficiency anaemia2 occurs in degree of hydration. are compatible with these McFarlane et al. Delpeuch et al. higher values in oedema-free marasmic children (Hansen et al. Thus. It is the transport rates of sodium in kwashiorkor. However. 1975). but before discussing them it is peritubular capillaries would limit sodium reabsorption in the necessary to develop a concept that describes an ideal marker proximal tubules. Thus excessive sodium and pathology of protein-energy malnutrition. marasmic children fed high-energy diets increase their are likely to be less ambiguous. because their concentrations are greatly 1 1 See Golden & Golden.—ED. We have therefore often found it distal tubule fluid. showed that serum transferrin concentrations were linearly 1980) or. the problem of the relationship of these and Reeds & Laditan (1976) extended this observation to changes to dietary and environmental causes of kwashiorkor. 1980). if we accept water losses could be prevented only by reductions in RPF and that a low plasma albumin concentration specifically contri- GFR. 31-36 of this Bulletin.

21-31 13. CahiU G F Jr (1970) New Engl. awakening an interest in the latter disease. BIOCHEMISTRY AND PHYSIOLOGY OF KWASHIORKOR AND MARASMUS WA Coward & P G Lunn reduced in malnourished children admitted to hospital and tion and more appropriate to suggest instead that they are rapidly return to normal with refeeding. but it needs related to the accumulated surplus of native RBP in the liver experimental investigation and further studies on malnourished before dosing. 74. Clin.g.106-109 108. marasmic kwashiorkor and al. nutritional problem most frequently encountered by doctors In reviewing the relationship between diet and plasma protein working in developing countries. Kattab A. Whitehead R G & Lunn P G (1977) Br.375-379 Hopkins L L Jr. Med. malnutrition (Thesis for PhD degree). Chim. (3. This is an intriguing. proconvertin. between proteinases and their inhibitors is destroyed. (1978). 38. Churchill. Nutr. novel idea. Zeitoun M M & Ragab M (1967)/. Ada. Brinkman G L & Bowie M D (1965) S. London Anthony L E & Edozien J C (1975) / . Trop. Hyg. 1975). Schrieck Van den H-G.115—126 491-195 Delpeuch F. Cornu A & Chevalier P (1980) Br. 1979) attach crucial 1979) indicate that TBPA and RBP concentrations are sensitive metabolic importance to changes in the plasma concentration of to changes in either energy or protein intake and this finding a1-antitrypsin and a1-antichymotrypsin in the development of supports the observations that TBPA and RBP concentrations malnutrition. It would be wrong to suggest stresses interact to produce the diseases identified as kwashi- that RBP and TBPA are better indices than albumin concentra. Afr. Stanfield J P & Whitehead R G (1977) deficiencies and protein deficiencies. This result therefore indicates that RBP synthesis is less affected in marasmus than in We recognize that marasmus. Nutr. The values achieved are kwashiorkor. Workers in metrically. with an energy therapy. J. many aspects of the biochemistry and tion when only 1 g protein/kg body weight per day was fed physiology of kwashiorkor have not yet been explained. London colloquium held in Cambridge. 2. so the authors considered that the peak concentrations provided some measure of the liver's ability to synthesize RBP from the outset. 21. 1. Med. e d Calorie Alleyne G A O. Hay R W.51-59 Hansen J D L. The peak levels were lowest in kwashi. 32. 1978. peaking at 3 result of infection. Nuxr. or to their sites of synthesis. 668-675 48. 43. 101. plasma levels of holo-RBP (native homoeostasis. Mandelbaum I M & Vis H L (1979) Am.631-648 Grant D B. Picou D I. 63. Abd-FJ-Hadi K. Edozien J C (1968) Nature (London) 220. The immunoglobulins (IgA. Clin. Experimental studies on obese women (Shetty et al. April 1967). 21. 37 No. but suggests that proteinase have recently investigated RBP and TBPA in children suffering inhibitor levels determine the extent to which a malnourished the combined effects of vitamin A deficiency and protein-energy child can mobilize endogenous proteins to provide amino acids malnutrition and have shown that. Dis. Niehaus N.400-411 Gopalan C (1968) In: McCance R A & Widdowson E M. 1 . 282. but lead to improvements in the prevention and treatment of the differences illustrate the difficulties that exist when the nutritional disease. Pediatr. However. It was not possible convincingly minority of the world's malnourished children are likely to suffer to relate these differences in responsiveness to normal fractional from it. Mikhail M.721-722 Alleyne G A O (1965) Renal and cardiac function In severely malnourished Gabr M. Davis I T . Trop.61-67 Fiorotto M (1980) Studies on oedema/unction in experimental protein-energy Ismadi S D. it is possible that a balanced relationship hours after treatment. De Visscher M & De Nayer P (1972) Lancet.J. Ogunshina & Hussain different indices from the dietary and metabolic points of view. Jamaican children (Thesis for MD degree). Med. Olson (1975) found it possible to distinguish view (McLaren. When proteinase inhibitor levels are high as a protein with the ligand retinol attached) increased. 38. Nutr. transferrin.917-919 203-211 Edozien J C. Arnold. Clin. 105. we accept the concentrations. Soc. J. 42. However. J. / . Nutr. is most important. De Nayer P & De Visscher M (1975) Enwonwu C O & Sreebny L M (1971)/. following intramuscular for the synthesis of proteins (e. 39. J. recognizes that kwashiorkor and marasmus are marasmus (Smith et al. IgG and IgM) were gap rather than a protein gap. rather than kwashiorkor. Ransome-Kuti O & Majaj A S (1968) Am. University of London 216-221 Alleyne G A O (1967) Pediatrics (Springfield) 39. Fiorotto M & Coward W A (1979) Br. / . Ingenbleek Y.918-921 Patwardhan V N (1968) Am.J. Becker D & Pimstone B L (1973) Arch.1313-1319 Coward W A S Fiorotto M (1979) Proc.501-514 Clin. Coward W A. Thailand (Schelp et al. 1974) that in a universal context it is necessary groups of proteins on the basis of the responsiveness to dietary to appreciate that a lack of nutrients in general. Nutr. Fondu P. Clin. marasmus appears. Mar M-H. orkor.87-95.195-202 Gurson C T & Saner G (\91\)Am. 49—58 (Proceedings of a Protein-energy malnutrition. attention are the plasma proteinase inhibitors. For (prothrombin. El-Hawary M F S & El-Dali M. marasmus and marasmic kwashiorkor. 1977. RBP from the liver. Res. REFERENCES Abbassy A S. Elucidation of the mechanisms involved will not only or absolute rates of synthesis. Nutr. 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