111 Protein-Energy Malnutrition

Protein-energy malnutrition (PEM) or, as it is still sometimes called, protein-calorie malnutrition (PCM), is a term of convenience that refers to a range of syndromes among infants and children of preschool age in whom manifestations of growth failure occur because of protein and energy deficiencies.

PEM is best described in its two clinical versions of kwashiorkor and marasmus. In the former, edema is always present, whereas extreme wasting (com­monly defined as below 60 percent that of normal weight for height) identifies the latter. Much of the research in the 1950s and 1960s focused on differ­entiating between the symptoms and etiologies of kwashiorkor and marasmus, but since then it has become evident that cases purely of one or the other are the exception rather than the rule. The majority display both edema and extreme wasting, plus a variable mix of other symptoms, that have earned them the rather inelegant designation of marasmic kwashiorkor. In addition, far more common than all of the three put together are numerous Subclinical syndromes, usually referred to as mild-to-moderate PEM. A frequent analogy for PEM, therefore, is an iceberg; only a very small proportion of the total is clearly visible. Most cases remain below the surface and go undetected except under close analysis.

Numerous attempts have been made to develop a logically ordered, comprehensive classification of PEM, but several problems have prevented the achievement of one that satisfies the demands of both clinicians and field workers.

Another problem is what to measure, especially in the Subclinical stages. Biochemical tests are expen­sive to perform, and in any event, they have not proved to be very reliable discriminators. As a re­sult, anthropometric characteristics are relied upon. The simplest such indicator, and longest in use, is that of weight-for-age, a measurement that gives a reasonably good picture of current nutritional sta­tus, assuming, of course, that age is known accu­rately, which all too often is not the case. More criti­cally, weight-for-age fails to differentiate between chronic and acute malnutrition. Because of these liabilities, the tendency today is to try to combine weight-for-height, which measures the degree of wasting, and thus the presence of acute malnutri­tion, with height-for-age, an indicator of stunting or chronic malnutrition. Other measures that have fre­quently been used in the field such as head and upper arm circumference and skin fold thicknesses add nothing to clarify the picture. They simply indi­cate if malnutrition is present but do not help in specifying the type.

Overriding the issue of anthropometric classifica­tion are the growth standards employed. Those in longest use were derived from studies of middle-class white Americans and are known as either the Har­vard or Boston standards. More recently these have been superseded in international comparisons by those developed at the U.S. National Center for Health Statistics (USNCHS) based on a larger sam­ple that cuts across ethnic and socioeconomic group­ings. Most authorities tend to accept the position that with proper nourishment and general good health there are no significant human differences in infant and child growth patterns.

Etiology

Traditional interpretations have stressed the pre­dominant role of diet in the etiology of PEM, with protein singled out as the most important missing ingredient. Critical shortages of protein alone, it was believed, would lead to kwashiorkor, and when these were combined with severe energy deficits, created by famine or other food crises, either ma­rasmus or marasmic kwashiorkor would result. Mild-to-moderate syndromes simply reflected lesser shortages of the two essential dietary requirements, protein and calories.

Beyond food supplies, the behavioral variables deemed most critical in the past appeared to be the duration of breastfeeding and subsequent food hab­its. Too early weaning onto poor-quality substitutes for mother’s milk such as rice water, sugar water, diluted milk or formula, and corn starch mixtures, was associated with marasmus. These substances are often contaminated with bacteria because of pol­luted water supplies and unsanitary preparation and cooking utensils, and consequently, repeated bouts of diarrhea were seen to accentuate the nutri­tional shortages. In addition, many cultures use star­vation to treat diarrhea, a therapy that has further negative repercussions for the victim. Later-aged weaning onto predominantly bulky carbohydrate- low amino acid foodstuffs, notably cassava and plan­tains, was seen as the pathway to kwashiorkor. Abrupt weaning was believed to be especially hazar­dous, particularly if the child had to compete for food from a “common pot” with older siblings and adult males who often monopolize the high-quality protein foods such as meat, fish, eggs, and milk.

This portrayal has proved to be not so much errone­ous as somewhat oversimplified. Clinical research has verified that kwashiorkor is always associated with low serum proteins, but considerable variation has been found in energy intake. Some cases show deficits, whereas in others energy levels are ade­quate and occasionally even excessive. Protein defi­ciency is clearly quite secondary to energy deficiency in marasmus and, in all probability, marasmic kwashiorkor. Indeed, if energy was not so severely restricted, it is unlikely that signs of protein short­ages would be observable.

An extremely important finding is that diet does not seem to play quite the overarching role in PEM that was initially believed. What is critical is the availability of nutrients to the cells, and thus infec­tions can act as an equal if not more important limiting factor. Included in these infections are not only the various diarrhea-producing gastrointesti­nal disorders, but also such widespread childhood diseases as pneumonia, measles, tuberculosis, and malaria. All can initiate symptoms of PEM by induc­ing anorexia and by lowering amino acid levels, and it is clear that malnourished children are more sus­ceptible to serious episodes of infection. The various syndromes of PEM, therefore, are best construed as resulting from complex nutrition-infection interac­tions. Based on current knowledge, it would appear that how they develop depends on how the life his­tory of a child unfolds within a particular environ­mental context.

Many cases undoubtedly begin in the uterus. Be­cause of widespread maternal malnutrition, low birthweights are common throughout Asia, Africa, and Latin America. Breastfeeding on demand dur­ing the first 4 to 6 months of life tends to compensate for any fetal growth deficit, while at the same time providing important disease immunities, but those infants who are not so fortunate as to be breastfed are well along a pathway to some PEM syndrome.

After about the first half year of life, breastfeeding alone no longer provides adequate nutrition, and it is now that many children often begin to show signs of mild-to-moderate PEM. Food supplies might be limited generally, or perhaps there is little knowl­edge of proper supplements. In any event, the course PEM takes will depend on the severity of the food shortage - a “hungry season” seems to be especially dangerous - and once again on the infections to which the child is exposed. When nutrition-infec­tion stress is extreme, then overt clinical symptoms of PEM can be expected.

Weaning is frequently a time of stress, and, when it occurs after 18 to 24 months of age, symptoms of kwashiorkor tend to predominate over those of ma­rasmus, assuming that there is not a gross defi­ciency of energy in the new diet. However, weaning by itself does not appear to produce kwashiorkor; this is true even if the staple foods are overwhelm­ingly of the starchy variety. The child must enter this stage of life already nutritionally disadvan­taged or otherwise in poor health before discernible symptoms of kwashiorkor emerge. Some analysts refer to a “prekwashiorkor state,” but how such a state differs from other mild-to-moderate syndromes has not been demonstrated.

The overriding etiologic issue, of course, is pov­erty, and PEM is a problem only where poverty is pervasive. Poverty means that local food shortages cannot be overcome by purchases, that living condi­tions will foster recurring infections, that education for effective intervention will be inadequate, that proper parental supervision of the feeding of infants and young children is likely to be missing, and that preventive and curative health services will not be readily available. In a very real sense, then, PEM is the outcome of “total deprivation.” An acceptance of this fact has led to recent shifts in policies designed to combat it.

Clinical Manifestations and Pathology

In the earliest stages of PEM, the child simply ap­pears smaller than he or she should be for that age. If the condition deteriorates further, however, clini­cal symptoms will begin to emerge. Although the mix is likely to be complex, for ease of description the symptoms are still best portrayed as those char- acterstics of either kwashiorkor or marasmus.

The edema that defines all cases of kwashiorkor varies. It can be mild and localized on the extremi­ties and sacrum or more severe and general. Al­though muscle wasting is discernible, subcutaneous fat is usually retained, and consequently the child takes on a bloated appearance, known as the “sugar baby” look in the West Indies. There also tends to be some growth retardation in head length and circumference.

More often than not there are skin changes, includ­ing ulcerating areas, open and healed sores, scabies, and a condition known as “flaky-paint dermatosis,” in which removal of the flakes reveals lighter patches of skin. When kwashiorkor persists, the hair begins to be affected; it loses its luster, and dark hair becomes lighter. Curly hair straightens, and eventu­ally the hair becomes brittle and falls out, leaving bare areas of scalp clearly visible.

Upon examination, the liver and spleen fre­quently are found to be enlarged, and a range of other symptoms have been documented. Among the more common are anemia and vitamin A deficiency, with some vision impairment, a range of micro­nutrient deficiencies, plus tendencies to hypother­mia, higher bilirubin, hyponatremia, hypoglycemia, and very low plasma albumin.

Behavioral changes are quite marked. Vomiting and diarrhea become persistent; without resolution, anorexia usually sets in. As the child’s strength wanes, motor skills regress, and eventually he or she becomes almost totally apathetic to external stimuli. It is as if the burden of life has become too great to bear. Because of this withdrawal, treatment is diffi­cult outside of a clinical setting where the child can be fed intravenously.

The overt symptoms of classical marasmus are far fewer and less medically unusual. There is extreme wasting of both muscles and subcutaneous tissues, and stunting is quite marked. Because the victim is so emaciated, the head appears abnormally large, especially the eyes. The skin tends to be dry and patchy, but dermatosis is not seen, nor are there any significant hair changes. Anorexia is uncommon, and, in fact, the appetite is usually good, which helps to simplify therapy. As in kwashiorkor, there is likely to be hypothermia and a tendency to hypogly­cemia. Dehydration is a problem as marasmus wors­ens, and behavior changes from being fretful and highly irritable to a Semicomatose state that immedi­ately precedes death.

With severe PEM, mortality is high - over 20 per­cent. It is seldom, however, that starvation is the final cause of death; rather it is one or more of the infections that brought on the condition, and these usually run their fatal course in just a few days. Although there is some debate among authorities, the onset of hypothermia and hypoglycemia proba­bly signals the need for immediate treatment.

For those children who have suffered mild-to- moderate PEM or who have recovered from one of the clinical syndromes, the question of long-term effects remains. The available evidence does support a relationship between chronic PEM and some per­manent stunting, but this by itself cannot be consid­ered a serious impairment to performance later in life. Indeed, stunting can be viewed as an adaptation to food shortages that conserves energy supplies. Nevertheless, there is one possible impact on skele­tal development that does have serious repercus­sions. In areas where chronic PEM is prevalent, there also appears to be a high incidence of cephalo- pelvic disproportion among women, a condition that leads to birth difficulties, notably miscarriages, still­births, and heightened maternal mortality. The theory is that PEM somehow interferes with calcium metabolism, thereby producing incomplete pelvic de­velopment, but this has yet to be proven conclu­sively. Although the data are even less adequate, there is also some suggestion that later-aged cardio­vascular, liver, and pancreas diseases might some­how be connected with childhood PEM.

The issue that has stimulated the most interest and controversy, however, is the effect of PEM on the brain. A considerable amount of research has shown that subnormal mental and psychomotor functioning tends to follow PEM₁ and during the 1960s and 1970s it was common for direct causal connections to be made. Some investigators even hypothesized that se­vere attacks of PEM resulted in permanent mental disabilities. But once again important reassessments have been forthcoming. The earlier tests generally failed to control for the learning environment of their subjects, and thus to sort out all the other factors that might be contributing to poor performance, such as reduced mother-child interaction and a lack of stimu­lating Sinroundings upon which the child could act in order to learn. This illustrates yet another dimension of the “total deprivation” that surrounds PEM. Cur­rently, the prevailing view is that neither mild-to- moderate nor acute clinical PEM seems to be associ­ated with long-term intellectual and psychological disabilities, assuming, of course, that the necessary social interventions are made. The matter of perma­nent injury caused by chronic PEM, notably of the marasmic variety during the first year of life, how­ever, remains unresolved. There may very well be irreversible brain damage in the more serious of these cases, as is strongly suggested by research on laboratory animals.

History and Geography

In one form or another, PEM is undoubtedly as old as humankind, and indeed, the term marasmus has been used to refer to starvation for centuries. How­ever, other than implying its incidence on the basis of reported past famines and general living condi­tions, the medical literature fails to mention PEM specifically until about the middle of the nineteenth century. It was around this time that concepts of malnutrition were beginning to develop, most nota­bly among the new pediatric specialists in France and Germany, who were treating the numerous seri­ous health problems of childhood, especially ill­nesses seen among foundlings and infants sent out to wet-nurse. One disorder, in particular, began to receive considerable attention. Known as mehlnahr- schaden, it was attributed to diets that were based excessively on flour, usually breads or thin gruels, with little milk or meat included.

At the same time, in the wake of colonial expan­sion, doctors in the field began to send back reports of a similar disorder from many tropical areas. Al­though the disease was initially thought to be caused by parasites (as virtually all diseases of the tropics were thought to be in the early days of diagno­sis), by the 1920s a dietary etiology began to gain some acceptance. A proliferation of terms ensued, the more common being infantile pellagra, nutri­tional edema, infantile edema, starchy dystrophy, and fatty-liver disease. These were all describing, of course, what is now known as kwashiorkor, a term that was first used by Cecily Williams in the 1931-2 Annual Medical Report of the Gold Coast (now Ghana). She took the term from the local Ga lan­guage, in which it designates an ill child who has been “deposed” from the breast because of a new pregnancy.

Although terminological and etiologic arguments continued, by the 1950s the concept of kwashiorkor had become firmly entrenched in the nutrition litera­ture and accepted by the medical community as a certifiable human disease resulting from a deficiency of protein. Continuing research into its causes and consequences led to the discovery of other syndromes and to the formulation of the more general concept of protein-calorie malnutrition. The word “calorie,” however, was subsequently replaced by “energy” in the early 1970s when the international system of unit measures was adopted by the United Nations.

Some analysts argue that too much attention has been paid to kwashiorkor. They feel that research­ers’ obsession with this condition has diverted atten­tion away from more important PEM problems and, in the process, has led to many inappropriate policy decisions because of a mistaken emphasis placed on the limiting role of protein. But a more plausible argument can be made that far less would be known about PEM today had it not been for the efforts expended on kwashiorkor. It provided the important first entry into the maze that PEM is now under­stood to be. In time, we hope, the full maze will eventually be mapped.

Distribution

At one time the general geography of PEM seemed straightforward. Kwashiorkor existed in the year- round wet tropical forest zones of Asia, Africa, and Latin America, where root and tree crops make up the predominant food staples. By contrast, marasmus was found in wet/dry areas because of seasonal or longer shortages of the staple cereal grains. Ma­rasmus also predominated in the cities as a result of the substitution of bottlefeeding for breastfeeding. Changing etiologic knowledge has put this neat gen­eralization to rest, and, in point of fact, little can be said about the precise distribution of PEM. Field sur­veys are limited in number, and many of them are of small sample size. Additionally, studies are difficult to compare because of temporal differences and differ­ences in measurements. About the best that can be done with the data at hand is to portray a rough re­gional patterning, knowing that there will be many shortcomings and, in the process, hope to identify the main trouble spots. Two recent studies have at­tempted just such an exercise; one has used the more widely available weight-for-age information, where­as the other has relied upon weight-for-height (wast­ing) calculations, converting other measures where possible. Both have employed USNCHS growth stan­dards and a variable sample of countries within the parameters of the World Health Organization’s re­gionalization scheme.

What emerges from these two efforts is a focus of PEM in the Southeast Asia region. Some 52 percent of preschool children are estimated to fall below 80 percent of the weight-for-age standard, led by Ban­gladesh with 91 percent and India with 75 percent. No country in the region shows a prevalence of wast­ing (defined as greater than 2 standard deviations below the norm) among 12- to 23-month-olds under 10 percent. Once again, Bangladesh and India are at the upper extreme, with 53 percent and 43 percent, respectively.

Both the Africa and Eastern Mediterranean re­gions show 35 percent deficient by the weight-for­age criteria, and of the countries included in the surveys, only Yemen and Mali stand above 50 per­cent. Wasting totals are generally in the vicinity of 10 percent, but there are two countries that register exceptionally high totals: Malawi (36 percent) and Somalia (66 percent).

On both measurement scales, the less developed countries in the Americas fare much better. The regional below-weight-for-age average is 21 percent, and all countries except one show a less than 10 percent incidence of wasting. That lone exception is Haiti, where the figure is calculated at 18 percent, still far lower than figures for many places in Asia and Africa.

Limited trend data suggest some lessening of the incidence of PEM since the 1960s, an observation supported by declining infant and child mortality rates. This is true even in Africa, where scenes of famine have created the image of spreading malnu­trition. Still, there is little room for complacency, given the magnitude of the problem that remains and the fact that poverty has proved to be intracta­ble in many areas. Certain populations, notably land­less rural laborers and the rapidly growing numbers of urban unemployed, seem to be sinking ever deeper into poverty and therefore could well be expe­riencing an increase in PEM. Also, wars and civil strife provide ideal breeding grounds for PEM. The examples of Ethiopia and Kampuchea are vivid re­minders of what can happen in the wake of political turmoil.

James L. Newman

Bibliography

Alleyne, G. A. O., et al. 1977. Protein-energy malnutri­tion. London.

Baxter, K., and J. C. Waterlow. 1985. Nutritional adapta­tion in man. London.

Bhandari, B., and S. L. Mandowara. 1982. Does grading of PEM with reference to the Harvard standard need a change? Indian Journal OfPediatrics 49: 161-6.

Bhattacharyya, A. K. 1986. Protein-energy malnutrition (kwashiorkor-marasmus syndrome): Terminology, classification and evolution. World Review of Nutrition and Dietetics 47: 80-133.

Diener, P. 1980. Meat, markets, and mechanical material­ism: The great protein fiasco in anthropology. Dialecti­cal Anthropology 5: 171-92.

Greene, L. S., ed. 1977. Malnutrition, behavior, and social organization. New York.

Haaga, J., et al. 1985. An estimate of the prevalence of child malnutrition in developing countries. World Health Statistics Quarterly 38: 331-47.

Keller, W., and C. M. Fillmore. 1983. Prevalence of protein-energy malnutrition. World Health Statistics Quarterly 36: 129-67.

Kerpel-Fronius, E. 1983. The pathophysiology Ofinfantile malnutrition, protein—energy malnutrition, and fail­ure to thrive. Budapest.

Pan American Health Organization. 1984. Global trends in protein—energy malnutrition. Pan American Health Organization Bulletin 18: 404-6.

Tomkins, A. M. 1986. Protein-energy malnutrition and risk of infection. Proceedings of the Nutrition Society 45:289-304.

Trowell, H. C., J. N. P. Davies, and R. F. A. Dean. 1954. Kwashiorkor. London.

White, P. L., and N. Selvey 1984. Malnutrition: Determi­nants and consequences. New York.