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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003
syndromes, kwashiorkor and marasmus (Whitehead, 1980). In kwashiorkor, characterized by edema, there is a deficiency in the quantity and quality of dietary protein, whereas energy intake can be adequate; other clinical signs include hypoalbuminemia and consequent fatty liver, growth retardation, loss of weight and muscle mass, and dermal and hair changes (Wilgram et al., 1958; Whitehead, 1980; Coward and Lunn, 1981; Ausman et al., 1989; Murray et al., 1996). Marasmus is most commonly associated with energy-deficient diets, but there can be generalized wasting due to severe and prolonged restriction of both energy and protein and characterized by severe muscle and body-fat loss. To serve as valid models, the pathologic effects manifested in those two disorders should be produced under dietary and environmental circumstances (often including infection) as similar as possible to those of the human population that typically develops these syndromes (Whitehead, 1980). Furthermore, persons conducting animal studies designed to reproduce clinical signs of kwashiokor and marasmus in children should recognize that there are likely to be other essential-nutrient deficits coincidental with the protein and energy deficiencies.
Nonhuman primates (Macaca mulatta) have served as models of undernutrition in the study of prepubertal and pubertal reproductive events as related to nutrition and the neuroendocrine system (Steiner, 1987). Young rhesus macaques (M. mulatta) with a body mass of 1.5-2.0 kg exhibited PCMafter only 45 days when energy (undefined) and protein intake were restricted to an intake of 55 kcal·BWkg-1·day-1 and 2.42 g·BWkg-1·day-1, respectively (Mehta et al., 1980). Ad libitum intakes were 90 kcal·BWkg-1·day-1 and 3.0 g·BWkg-1·day-1, respectively. The degree of restriction proved severe, and 70% of the monkeys died during acclimatization or during different phases of the study, whereas the monkeys fed ad libitum thrived. PCMwas induced in male rhesus macaques 1-12 months old, when 50% of the allotted control diet was fed per day for 10-12 weeks. That restriction provided undefined energy at 55 kcal·BWkg-1·day-1 and protein at 2.32 g·BWkg-1·day-1 and resulted in a 36% loss in BW, decreased serum albumin concentrations, hair loss, easily peeled skin, muscular wasting, and decreased physical activity (Chopra et al., 1987).
During a study spanning several years, young rhesus macaques (M. mulatta) were subjected to various degrees of protein or calorie malnutrition to evaluate effects on physical growth (Kerr et al., 1970), organ size and skeletal growth (Kerr et al., 1973), cerebral lipids (Kerr and Helmuth, 1973), growth failure and “catch-up” growth (Kerr et al., 1975), and biochemical and cytochemical composition of major organs (Kerr et al., 1976). Nutritional rehabilitation of surviving monkeys produced responses comparable with those seen in rehabilitated undernourished children; 2 years later, the external dimensions of the monkeys were within the range of normal controls (Kerr et al., 1973). The study design included feeding the young monkeys (from 1 to 7 months of age) various combinations of five diets: a commercial human-infant milk preparation (ME at about 0.67 kcal·ml-1, protein at 0.0182 g· ml-1 [Kerr et al., 1969b]); a 1:1 milk:water dilution of the commercial milk; a 1:3 milk:water dilution of the commercial milk; and the commercial milk with 50% or 25% of normal protein concentration made isocaloric by lactose additions. Mortality of 44-54% was reported in monkeys fed the diet made isocaloric with lactose and containing only 25% of the normal protein level (Kerr et al., 1970; Kerr et al., 1973). Monkeys fed this adequate-energy, low-protein diet exhibited evidence of malnutrition: gastrointestinal distention, diarrhea, enteric infections, lymphoid hypoplasia, anemia, muscular wasting, reduced organ mass, and extensive fatty metamorphosis of the liver. It was noted that, whereas total intake by monkeys fed the low-protein diet was reduced below that appropriate for age, total intake per kilogram of body mass was comparable with that of the controls, owing primarily to weight loss in the protein-restricted monkeys (Kerr et al., 1970). However, during 5 months of rehabilitation, energy and protein deficits (expressed as intake of diet volume in liters, kilocalories of energy, and grams of protein) continued to increase in these animals compared with normal-weight controls (Kerr et al., 1975). A mortality of 17% was reported for monkeys fed the 1:3 diet, in which all nutrients were diluted (Kerr et al., 1970). These monkeys also exhibited marked growth failure despite satisfactory intake (they consumed 3-4 times the usual volume) of all nutrients except for an excess of water. Monkeys that did not consume enough of the dilute diet to provide a normal intake of nutrients had a nutrient deficit of about 20-30% in terms of kilograms of body mass (Kerr et al., 1973). By the age of 7 months, the monkeys fed the 1:3 dilute diet were consuming 217% of the volume of control animals, providing only 54% of the normal energy and protein intake (Kerr et al., 1975). Monkeys fed the dilute diet accumulated nutrient deficits that were not restored during nutritional rehabilitation, but the deficits did not continue to increase. Young (10-28 months old), pigtail macaques (M. nemestrina) were fed 400 g of synthetic diet per day, containing either 20% or 2% casein and ME at 3.96 or 3.24 kcal·g-1, respectively, for about 3 months to determine biochemical and morphologic alterations in response to PCM(Enwonwu et al., 1973). In a preliminary study, the protein content of the diet was gradually reduced over a period of 9 months from 8% through 6% to 2%. Monkeys fed the 8% or 6% casein diets ad libitum gained BW and showed no clinical or biochemical signs suggestive of PCM. After 3 months of the 2% casein diet, however, serum albumin concentration was reduced by 25%, plasma corticosteroid had increased by 132%, and impairment of liver-protein biosynthesis resulted in extensive fatty liver metamorphosis.