Comprehensive Physiology Wiley Online Library

Human Adaptation to Energy Undernutrition

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Energy Undernutrition and Adaptation
1.1 Energy Undernutrition
1.2 Adaptation to Energy Undernutrition
2 Physiological Adaptation
2.1 Biochemical Changes
2.2 Body Weight and Composition Changes
2.3 Energy Expenditure
3 Functional Consequences
3.1 Reproduction and Fertility
3.2 Pregnancy and Lactation
3.3 Growth and Adolescence
3.4 Infection and Disease
3.5 Physical Working Capacity
3.6 Work Output and Productivity
4 Behavioral Strategies: Household and Community Responses and Strategies
5 Genetic Adaptation to Undernutrition
6 Conclusions
References
 1. Ashworth, A. An investigation of very low calorie intakes reported in Jamaica. Br. J. Nutr. 22: 341–355, 1968.
 2.Ategbo, E‐A. D., J. M. A. van Raaij, F. L. H. A. de Koning, and J. G. A. J. Hautvast. Resting metabolic rate and work efficiency of rural Beninese women: A 2‐y longitudinal study. Am. J. Clin. Nutr. 61: 466–472, 1995.
 3. Barac‐Nieto, M. Physical work determinants and undernutrition. World Rev. Nutr. Diet. 49: 22–65, 1987.
 4. Barac‐Nieto, M., G. B. Spurr, M. G. Maksud, and H. Lotero. Aerobic work capacity in chronically undernourished adult men. Am. J. Clin. Nutr. 32: 981–991, 1979.
 5. Barker, D. J. P. The effect of nutrition of the foetus and neonate on cardiovascular disease in adult life. Proc. Nutr. Soc. 51: 135–144, 1992.
 6. Barrett, D. E., and D. A. Frank. The Effects of Undernutrition on Children's Behavior. New York: Gordon and Breach, 1987.
 7. Beaton, G. H. Adaptation to and accommodation of long term low energy intake: a commentary on the conference on energy intake and activity. In: Energy Intake and Activity, edited by E. Pollitt and P. Amante. New York: Liss, 1984, p. 395–403.
 8. Beaton, G. H. The significance of adaptation in the definition of nutrient requirements and for nutrition policy. In: Nutritional Adaptation in Man, edited by Sir K. Blaxter and J. C. Waterlow. London: Libbey, 1985, p. 219–232.
 9. Beaton, G. H. Small but healthy? Are we asking the right questions? Hum. Org. 48: 30–39, 1989.
 10. Beattie, J., and P. H. Herbert. The estimation of metabolic rate in the starvation state. Br. J. Nutr. 1: 185–191, 1947.
 11. Benedict, F. G., W. R. Miles, P. Roth, and H. M. Smith. Human Vitality and Efficiency Under Prolonged Restricted Diet. Washington, DC: Carnegie Inst., Publ. 280, 1919.
 12. Bradley, P. J. Is obesity an advantageous adaptation? Int. J. Obes. 6: 43–52, 1982.
 13. Briend, A., B. Wojtyniak, and M. G. M. Rowland. Arm circumference and other factors in children at high risk of death in rural Bangladesh. Lancet ii: 725–728, 1987.
 14. Brooks, R. M., M. C. Latham, and D. W. T. Crompton. The relationship of nutrition and health to worker productivity in Kenya. East Afr. Med. J. 56: 413–421, 1979.
 15. Brozek, J., and B. Schürch. Malnutrition and behavior: critical assessment of key issues. Lausanne, Switzerland: Nestlé Foundation, 1984.
 16. Chandra, R. K. Nutrition and immunity in the elderly. Nutr. Res. Rev. 4: 83–95, 1991.
 17. Chen, L. C., A. K. M. A. Chowdhury, and S. L. Huffman. Anthropometric assessment of protein—energy malnutrition and subsequent risk of mortality among preschool aged children. Am. J. Clin. Nutr. 33: 1836–1845, 1984.
 18. Danforth, E. The role of thyroid hormones and insulin in the regulation of energy metabolism. Am. J. Clin. Nutr. 38: 1006–1017, 1983.
 19. Davies, C. T. M. Relationship of maximum aerobic power output to productivity and absenteeism of East African sugar cane workers. Br. J. Indust. Med. 30: 146–154, 1973.
 20. Della Bianca, P., E. Jequier, and Y. Schutz. High level of free‐living energy expenditure in rural Gambian men: lack of behavioural adaptation between low and normal BMI groups. Eur. J. Clin. Nutr. 48: 273–278, 1994.
 21. Della Bianca, P., E. Jequier, and Y. Schutz. Lack of metabolic and behavioral adaptations in rural Gambian men with low body mass index. Am. J. Clin. Nutr. 60: 37–42, 1994.
 22. Desai, I. D., C. Wadell, S. Dutra, E. Duarte, M. L. Robazzi, L. S. Cevallos Romero, M. I. Desai, F. L. Vichi, R. B. Bradfield, and J. E. Dutra de Olivreira. Marginal malnutrition and reduced physical work capacity in migrant adolescent boys in Southern Brazil. Am. J. Clin. Nutr. 40: 135–145, 1984.
 23. Durnin, J. V. G. A. Energy balance in man with particular reference to low intakes. Bibl. Nutr. Dieta. 27: 1–10, 1979.
 24. Edmundson, W. Adaptation to undernutrition: how much food does man need? Soc. Sci. Med. 14D: 119–126, 1980.
 25. Elia, M. Organ and tissue contribution to metabolic rate. In: Energy Metabolism: Tissue Determinants and Cellular Corollaries, edited by J. M. Kinney and H. N. Tucker. New York: Raven, 1992, p. 61–77.
 26. Eveleth, P. B. Nutritional implications of differences in adolescent growth and maturation and in adult body size. In: Nutritional Adaptation in Man, edited by Sir K. Blaxter and J. C. Waterlow. London: Libbey, 1985, p. 31–43.
 27. FAO/WHO. Nutrition and Development—A Global Assessment. Rome: F. A. O., 1992.
 28. FAO/WHO/UNU. Energy and Protein Requirements. World Health Org. Tech. Rep. Ser. 724. Geneva: World Health Organisation, 1985, p. 12.
 29. Ferro‐Luzzi, A. Work capacity and productivity in long‐term adaptation to low energy intakes. In: Nutritional Adaptation in Man, edited by Sir K. Blaxter and J. C. Waterlow. London: Libbey, 1985, p. 61–68.
 30. Ferro‐Luzzi, A. Range of variation in energy expenditure and scope for regulation. In: Proc. XIII Int. Congr. Nutr. edited by T. G. Taylor and N. K. Jenkins. London: Libbey, 1986, p. 393–399.
 31. Ferro‐Luzzi, A. Marginal energy malnutrition: some speculations on primary energy sparing mechanism. In: Capacity for Work in the Tropics, edited by K. J. Collins and D. F. Roberts. Cambridge: Cambridge University Press, 1988, p. 140–164.
 32. Ferro‐Luzzi, A. Seasonal energy stress in marginally nourished rural women: interpretation and integrated conclusions of a multicentre study in three developing countries. Eur. J. Clin. Nutr. 44 (suppl. 1): 41–46, 1990.
 33. Ferro‐Luzzi, A. Social and public health issues in adaptation to low energy intakes. Am. J. Clin. Nutr. 51: 309–315, 1990.
 34. Ferro‐Luzzi, A., F. Branca, and G. Pastore. Body mass index defines risk of seasonal energy stress in the Third World. Eur. J. Clin. Nutr. 48, Supp 13: S165–S178, 1994.
 35. Ferro‐Luzzi, A., G. Pastore, and S. Sette. Seasonality in energy metabolism. In: Chronic Energy Deficiency: Consequences and Related Issues, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDEGG, 1988, p. 37–58.
 36. Ferro‐Luzzi, A., C. Scaccini, S. Taffese, B. Aberra, and T. Demeke. Seasonal energy deficiency in Ethiopian rural women. Eur. J. Clin. Nutr. 44 (suppl. 1): 7–18, 1990.
 37. Ferro‐Luzzi, A., S. Sette, M. Franklin, and W. P. T. James. A simplified approach of assessing adult chronic energy deficiency. Eur. J. Clin. Nutr. 46: 173–176, 1992.
 38. Flatt, J. P. The biochemistry of energy expenditure. In: Recent Advances in Obesity Research II, edited by G. Bray. Westport, CT: Food Nutrition, 1978, p. 211–228.
 39. Forbes, G. B. Composition of weight gains and losses. Human Body Composition. New York: Springer‐Verlag, 1987, p. 225–247.
 40. Forbes, G. B. Lean body mass‐body fat interrelationships in humans. Nutr. Rev. 45: 225–231, 1987.
 41. Frisch, R. E., and R. Revelle. Height and weight at menarche and a hypothesis of critical body weight and adolescent events. Science 169: 397–399, 1970.
 42. Garby, L. Metabolic adaptation to decreases in energy intake due to changes in the energy cost of low energy expenditure regimen. World Rev. Nutr. Diet. 61: 173–208, 1990.
 43. Garby, L., and O. Lammert. An explanation for the non‐linearity of the relation between energy expenditure and fat‐free mass. Eur. J. Clin. Nutr. 46: 235–236, 1992.
 44. Garrow, J. S., and J. D. Webster. Thermogenesis to small stimuli. In: Human Energy Metabolism, edited by A. J. H. van Es. Wageningen, Netherlands: Euro‐Nut., 1985, p. 215–224.
 45. Gopalan, C. Stunting: significance and implications for public health policy. In: Linear Growth Retardation in Less Developed Countries, edited by J. C. Waterlow. New York: Raven, 1988, p. 265–279.
 46. Gopalan, C. Undernutrition: Measurement and implications. In: Nutrition and Poverty, edited by S. R. Osmani. Oxford: Clarendon Press, 1992, p. 17–47.
 47. Gorsky, R. D., and D. H. Calloway. Activity pattern changes with decreases in food energy intake. Hum. Biol. 55: 577–586, 1983.
 48. Gould, S. J., and R. C. Lewontin. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. In: The Evolution of Adaptation by Natural Selection, edited by J. Maynard Smith and R. Holliday. London: Royal Society, 1979, p. 147–164.
 49. Grande, F. Man under caloric deficiency. In: Handbook of Physiology. Adaptation to the Environment, edited by D. B. Dill and E. F. Adolph. Washington, DC: Am. Physiol. Soc., 1964, sect. 4, p. 911–936.
 50. Grande, F., J. T. Anderson, and A. Keys. Changes of basal metabolic rate in man in semistarvation and refeeding. J. Appl. Physiol. 12: 230–238, 1958.
 51. Grantham‐McGregor, S., J. M. Meeks Gardener, S. Walker, and C. Powell. The relationship between undernutrition, activity levels and development in young children. In: Activity, Energy Expenditure and Energy Requirements of Infants and Children, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1991, p. 361–383.
 52. Grantham‐McGregor, S., C. Powell, and P. Fletcher. Stunting, severe malnutrition and mental development in young children. Eur. J. Clin. Nutr. 43: 403–409, 1989.
 53. Henriksson, J. Energy metabolism in muscle: Its possible role in the adaptation to energy deficiency. In: Energy Metabolism: Tissue Determinants and Cellular Corollaries, edited by J. M. Kinney and H. N. Tucker. New York: Raven Press, 1992, p. 345–363.
 54. Henry, C. J. K., and D. G. Rees. New predictive equations for the estimation of basal metabolic rate in tropical peoples. Eur. J. Clin. Nutr. 45: 177–185, 1991.
 55. Himms‐Hagen, J. Thyroid hormones and thermogenesis. In: Mammalian Thermogenesis, edited by L. Girardier and M. J. Stock. London: Chapman Hall, 1983, p. 141–177.
 56. Horton, E. S. Effects of low energy diets on work performance. Am. J. Clin. Nutr. 35: 1228–1233, 1982.
 57. Immink, M. D. C. Economic effects of chronic energy deficiency. In: Chronic Energy Deficiency: Consequences and Related Issues, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1988, p. 153–174.
 58. Immink, M. D. C., and F. E. Viteri. Energy intake and productivity of Guatemalan sugar‐cane cutters: an empirical test of the efficiency wage hypothesis. J. Dev. Econ. 9: 251–287, 1981.
 59. James, W. P. T. Research relating to energy adaptation in man. In: Chronic Energy Deficiency: Consequences and Related Issues, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1988, p. 7–36.
 60. James, W. P. T., A. Ferro‐Luzzi, and J. C. Waterlow. Definition of chronic energy deficiency in adults. Eur. J. Clin. Nutr. 42: 969–981, 1988.
 61. James, W. P. T., G. McNeill, and A. Ralph. Metabolism and nutritional adaptation to altered intakes of energy substrates. Am. J. Clin. Nutr. 51: 264–269, 1990.
 62. James, W. P. T., and P. S. Shetty. Metabolic adaptation and energy requirements in developing countries. Hum. Nutr. Clin. Nutr. 36C: 331–336, 1982.
 63. Jones, C. D. R., M. S. Jarjou, R. G. Whitehead, and E. Jequier. Fatness and the energy cost of carrying loads in African women. Lancet ii: 1331–1332, 1987.
 64. Kennedy, E., and M. Garcia. Body mass index and economic productivity. Eur. J. Clin. Nutr. 48, Suppl 3: S45–S55, 1994.
 65. Keys, A., J. Brozek, A. Henschell, O. Mickelsen, and H. L. Taylor. The Biology of Human Starvation. Minneapolis: University of Minnesota Press, 1950.
 66. Kielmann, A. A., I. S. Uberoi, R. K. Chandra, and V. L. Mehra. The effect of nutritional status on immune capacity and immune response in pre‐school children in a rural community in India. Bull. WHO 54: 477–483, 1976.
 67. Koong, L.‐J., J. A. Nienaber, J. C. Pekas, and J.‐T. Yen. Effects of plane of nutrition on organ size and fasting heat production in pigs. J. Nutr. 112: 1638–1642, 1982.
 68. Kulkarni, R. N., A. V. Kurpad, and P. S. Shetty. Aerobic capacity and post‐exercise recovery characteristics of chronically energy‐deficient labourers. Proc. Nutr. Soc. 50: 27A, 1991.
 69. Kulkarni, R. N., and P. S. Shetty. Increased net mechanical efficiency during stepping in chronically energy deficient human subjects. Ann. Hum. Biol. 19: 421–425, 1992.
 70. Kurpad, A. V., R. N. Kulkarni, and P. S. Shetty. Reduced thermo‐regulatory thermogenesis in undernutrition. Eur. J. Clin. Nutr. 43: 27–33, 1989.
 71. Landsberg, L., and J. B. Young. Effects of nutritional status on autonomic nervous system function. Am. J. Clin. Nutr. 35: 1234–1240, 1982.
 72. Landsberg, L., and J. B. Young. Insulin‐mediated glucose metabolism in the relationship between dietary intake and sympathetic nervous system activity. Int. J. Obes. 9 (suppl. 2): 63–68, 1985.
 73. Lawrence, M., K. Thongprasert, and J. V. G. A. Durnin. Between‐group differences in basal metabolic rates: an analysis of data collected in Scotland, The Gambia and Thailand. Eur. J. Clin. Nutr. 42: 877–891, 1988.
 74. Malina, R. M. Physical activity and motor development/performance in populations nutritionally at risk. In: Energy Intake and Activity, edited by E. Pollitt and P. Amante. New York: Liss, 1984, p. 285–302.
 75. Malina, R. M. Motor development and performance of children and youth in undernourished populations. In: Sport, Health and Nutrition, edited by F. I. Katch. Champaign, II: Human Kinetics, 1985, p. 213–226.
 76. Maloiy, G. M. O., N. C. Hegland, L. M. Prager, G. Cavagna, and C. R. Taylor. Energetic cost of carrying loads: have African women discovered an economic way? Nature 319: 668–669, 1986.
 77. Mansell, P. I., and I. A. MacDonald. The effect of underfeeding on the physiological response to food ingestion in normal weight women. Br. J. Nutr. 60: 39–48, 1988.
 78. Martorell, R. Child growth retardation: a discussion of its causes and its relation to health. In: Nutritional Adaptation in Man, edited by Sir K. Blaxter and J. C. Waterlow. London: Libbey, 1985, p. 13–29.
 79. Martorell, R. Body size, adaptation and function. Hum. Org. 48: 15–20, 1989.
 80. Martorell, R., and G. Arroyave. Malnutrition, work output and energy needs. In: Capacity for Work in the Tropics, edited by K. J. Collins and D. F. Roberts. Cambridge: Cambridge University Press, 1988, p. 57–75.
 81. McNeill, G., A. McBride, and W. P. T. James. The energy expenditure of large and small eaters. Proc. Nutr. Soc. 47: 138A, 1988.
 82. McNeill, G., P. Payne, and J. Rivers. Patterns of Adult Energy Expenditure in a South Indian Village. Occasional paper 11. London: London School Hyg. Trop. Med. 1988.
 83. McNeill, G., J. P. W. Rivers, P. R. Payne, J. J. De Britto, and R. Abel. Basal metabolic rate of Indian men: no evidence of metabolic adaptation to a low plane of nutrition. Hum. Nutr. Clin. Nutr. 41C: 473–483, 1987.
 84. Minghelli, G., Y. Schutz, A. Charbonnier, R. Whitehead, and E. Jequier. Twenty‐four‐hour energy expenditure and basal metabolic rate measured in a whole‐body indirect calorimeter in Gambian men. Am. J. Clin. Nutr. 51: 563–570, 1990.
 85. Naidu, A. N., and N. P. Rao. Body mass index: a measure of the nutritional status in Indian populations. Eur. J. Clin. Nutr. 48, Suppl 3: S131–S160. 1991.
 86. Neel, J. M. Diabetes mellitus: a thrifty genotype rendered detrimental by “progress.” Ann. Hum. Genet. 14: 354–362, 1962.
 87. Norgan, N. G. Adaptation of energy balance to level of energy intake. In: Energy Expenditure Under Field Conditions, edited by J. Parizkova. Prague: Charles University Press, 1983, p. 56–64.
 88. Norgan, N. G. Chronic energy deficiency and the effects of energy supplementation. In: Chronic Energy Deficiency: Consequences and Related Issues, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1988, p. 59–76.
 89. Norgan, N. G. Thermogenesis above maintenance. Proc. Nutr. Soc. 49: 217–226, 1990.
 90. Norgan, N. G., A. Ferro‐Luzzi, and J. V. G. A. Durnin. The energy and nutrient intake and the energy expenditure of 204 New Guinean adults. Phil. Trans. R. Soc. Lond. B 268: 309–348, 1974.
 91. Osmani, S. R. On some controversies in the measurement of undernutrition. In: Nutrition and Poverty, edited by S. R. Osmani. Oxford: Clarendon Press, 1992, p. 121–164.
 92. Owen, O. E., A. P. Morgan, H. G. Kemp, J. M. Sullivan, M. G. Herrera, and G. F. Cahill. Brain metabolism during fasting. J. Clin. Invest. 46: 1589–1595, 1967.
 93. Park, H. S., J. M. Kelly, and L. P. Milligan. Energetics and cell membranes. In: Energy Metabolism: Tissue Determinants and Cellular Corollaries, edited by J. M. Kinney and H. N. Tucker. New York: Raven, 1992, p. 411–435.
 94. Payne, P. R. Assessing undernutrition: The need for a recon‐ceptualisation. In: Nutrition and Poverty, edited by S. R. Osmani. Oxford: Clarendon Press, 1992, p. 49–96.
 95. Payne, P. R., and M. Lipton. How Third World households adapt to dietary energy stress. The evidence and the issues. Food Policy Research Review, 2. Washington, DC: International Food Policy Research Institute, 1994.
 96. Pelto, G. H., and P. J. Pelto. Small but healthy? An anthropological perspective. Hum. Org. 48: 11–15, 1989.
 97. Piers, L. S., M. J. Soares, and P. S. Shetty. Thermic effect of a meal 2. Role in chronic undernutrition. Br. J. Nutr. 67: 177–185, 1992.
 98. Poehlman, E. T., and M. J. Toth. Mathematical ratios lead to spurious conclusions regarding age‐ and sex‐related differences in resting metabolic rate. Am. J. Clin. Nutr. 61: 482–485, 1995.
 99. Pollitt, E. A critical view of three decades of research on the effects of chronic energy malnutrition on behavioural development. In: Chronic Energy Deficiency: Consequences and Related Issues, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1988, p. 77–93.
 100. Poole, D. C., and L. C. Henson. Effect of acute caloric restriction on work efficiency. Am. J. Clin. Nutr. 47: 15–18, 1988.
 101. Poppitt, S. D., A. M. Prentice, E. Jequier, E. Schutz, and R. G. Whitehead. Evidence of energy sparing in Gambian women during pregnancy: A longitudinal study using whole‐body calorimetry. Am. J. Clin. Nutr. 57: 353–364, 1993.
 102. Prentice, A. M. Adaptations to long‐term low energy intake. In: Energy Intake and Activity, edited by E. Pollitt and P Amante. New York: Liss, 1984, p. 3–31.
 103. Prentice, A. M., G. R. Goldberg, H. L. Davies, P. R. Murgatroyd, and W. Scott. Energy‐sparing adaptations in human pregnancy assessed by whole‐body calorimetry. Br. J. Nutr. 62: 5–22, 1989.
 104. Prentice, A. M., G. R. Goldberg, and A. Prentice. Body mass index and lactation performance. Eur. J. Clin. Nutr. 48, Suppl 3: S78–S89, 1994.
 105. Prentice, A. M., and A. Prentice. Energy costs of lactation. Annu. Rev. Nutr. 8: 63–79, 1988.
 106. Prentice, A. M., and R. G. Whitehead. The energetics of human reproduction. Symp. Zool. Soc. Lond. 57: 275–304, 1987.
 107. Prentice, A. M., R. G. Whitehead, S. B. Roberts, and A. Paul. Long‐term energy balance in child‐bearing Gambian women. Am. J. Clin. Nutr. 34: 2790–2799, 1981.
 108. Ravussin, E., and C. Bogardus. Relationship of genetics, age, and physical‐fitness to daily energy‐expenditure and fuel utilization. Am. J. Clin. Nutr. 49: 968–975, 1989.
 109. Ravussin, E., S. Lillioja, W. C. Knowler, L. Christin, D. Freymond, W. G. H. Abbott, V. Boyce, B. V. Howard, and C. Bogardus. Reduced rate of energy expenditure as a risk factor for body‐weight gain. N. Engl. J. Med. 318: 467–472, 1988.
 110. Reddy, V. Malnutrition and immune response. Ind. J. Nutr. Diet. 16: 165–169, 1979.
 111. Robinson, A. M., and D. H. Williamson. Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiol. Rev. 60: 143–187, 1980.
 112. Rose, G. A., and R. T. Williams. Metabolic studies on large and small eaters. Br. J. Nutr. 15: 1–9, 1961.
 113. Rothwell, N. J., and M. J. Stock. A role for brown adipose tissue in diet‐induced thermogenesis. Nature 281: 31–35, 1979.
 114. Rutishauser, I. H. E., and R. G. Whitehead. Energy intake and expenditure in 1‐3 year old Ugandan children living in a rural environment. Br. J. Nutr. 28: 145–152, 1972.
 115. Sabiene, F. The mechanisms for minimizing energy expenditure in human locomotion. Eur. J. Clin. Nutr. 44 (suppl. 1): 65–71, 1990.
 116. Satyanarayana, K., A. D. Naidu, B. Chatterjee, and B. S. N. Rao. Body size and work output. Am. J. Clin. Nutr. 30: 322–325, 1977.
 117. Satyanarayana, K., A. N. Naidu, and B. S. N. Rao. Agricultural employment, wage earnings and nutritional status of teenage rural Hyderabad boys. Ind. J. Nutr. Diet. 17: 281–286, 1980.
 118. Satyanarayana, K., G. Radhaiah, K. R. Munali‐Mohan, B. S. Thimmayanmma, N. P. Rao, and B. S. N. Rao. The adolescent growth spurt and height among rural Indian boys in relation to childhood nutrition background; an 18‐year longitudinal study. Ann. Hum. Biol. 16: 289–300, 1989.
 119. Schofield, W. N., E. C. Schofield, and W. P. T. James. Basal metabolic rates: review and prediction. Hum. Nutr. Clin. Nutr. 39C (suppl. 1): 1–96, 1985.
 120. Scott, E. C., and F. E. Johnston. Science, nutrition, fat, and policy: tests of the critical‐fat hypothesis. Curr. Anthropol. 26: 463–473, 1985.
 121. Scrimshaw, N. S., and V. R. Young. Adaptation to low protein and energy intakes. Hum. Org. 48: 20–30, 1989.
 122. Seckler, D. “Small but healthy”: a basic hypothesis in the theory, measurement and policy of malnutrition. In: Newer Concepts in Nutrition and Their Implications for Policy, edited by P. V. Sukhatme. Pune, India: Maharashtra Assoc., 1982, p. 127–137.
 123. Shephard, R. J. Factors associated with population variation in physiological working capacity. Yearbook Phys. Anthropol. 28: 97–122, 1985.
 124. Shephard, R. J. Body Composition in Biological Anthropology. Cambridge: Cambridge University Press, 1991, p. 215–216.
 125. Shetty, P. S. Adaptive changes in basal metabolic rate and lean body mass in chronic undernutrition. Hum. Nutr. Clin. Nutr. 38C: 443–451, 1984.
 126. Shetty, P. S. Physiological mechanisms in the adaptive response of metabolic rates to energy restriction. Nutr. Res. Rev. 3: 49–74, 1990.
 127. Shetty, P. S., R. T. Yung, and W. P. T. James. Effect of catecholamine replacement with levodopa on the metabolic response to semistarvation. Lancet i: 77–79, 1979.
 128. Simeon, D. T., and S. M. Grantham‐McGregor. Nutritional deficiencies and children's behaviour and mental development. Nutr. Res. Rev. 3: 1–24, 1990.
 129. Soares, M. J., L. S. Piers, P. S. Shetty, S. Robinson, A. A. Jackson, and J. C. Waterlow. Basal metabolic rate, body composition and whole‐body protein turnover in Indian men with differing nutritional status. Clin. Sci. 81: 419–425, 1991.
 130. Soares, M. J., and P. S. Shetty. Basal metabolics rates and metabolic economy in chronic undernutrition. Eur. J. Clin. Nutr. 45: 363–373, 1991.
 131. Spurr, G. B. Nutritional status and physical working capacity. Yearbook Phys. Anthropol. 26: 1–35, 1983.
 132. Spurr, G. B. Physical activity, nutritional status, and physical work capacity in relation to agricultural productivity. In: Energy Intake and Activity, edited by E. Pollitt and P Amante. New York: Liss, 1984, p. 207–261.
 133. Spurr, G. B. Effects of chronic energy deficiency on stature, work capacity and productivity. In: Chronic Energy Deficiency: Consequences and Related Issues, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1988, p. 95–134.
 134. Spurr, G. B. Marginal malnutrition in childhood: implications for adult work capacity and productivity. In: Capacity for Work in the Tropics, edited by K. J. Collins and D. F. Roberts. Cambridge: Cambridge University Press, 1988, p. 107–140.
 135. Spurr, G. B. The impact of chronic undernutrition on physical work capacity and daily energy expenditure. In: Diet and Disease in Traditional and Developing Societies, edited by G. A. Harrison and J. C. Waterlow. Cambridge: Cambridge University Press, 1990, p. 24–61.
 136. Spurr, G. B., M. Barac‐Nieto, and M. G. Maksud. Productivity and maximal oxygen consumption in sugar cane cutters. Am. J. Clin. Nutr. 30: 316–321, 1977.
 137. Spurr, G. B., M. Barac‐Nieto, and M. G. Maksud. Functional assessment of nutritional status: heart rate response to submaximal work. Am. J. Clin. Nutr. 32: 767–778, 1979.
 138. Spurr, G. B., M. Barac‐Nieto, J. C. Reina, and R. Ramirez. Marginal malnutrition in school‐aged Colombian boys: efficiency of treadmill walking in submaximal exercise. Am. J. Clin. Nutr. 39: 452–459, 1984.
 139. Spurr, G. B., and J. C. Reina. Marginal malnutrition in school‐aged Colombian girls: dietary intervention and daily energy expenditure. Hum. Nutr. Clin. Nutr. 41C: 93–104, 1987.
 140. Spurr, G. B., J. C. Reina, H. W. Dahners, and M. Barac‐Nieto. Marginal malnutrition in school‐aged Colombian boys: functional consequences in maximum exercise. Am. J. Clin. Nutr. 37: 834–847, 1983.
 141. Stein, Z., M. Susser, G. Saenger, and F. Marolla. Famine and human development. New York: Oxford University Press, 1975, p. 71–86.
 142. Stinson, S. Nutritional adaptation. Ann. Rev. Anthropology 21: 143–170, 1992.
 143. Strickland, S. S. Traditional economies and patterns of disease. In: Diet and Disease in Traditional and Developing Societies, edited by G. A. Harrison and J. C. Waterlow. Cambridge: Cambridge University Press, 1990, 209–239.
 144. Sukhatme, P. V., and S. Margen. Auto‐regulatory homeostatic nature of energy balance. In: Newer Concepts in Nutrition and Their Implications for Policy, edited by P. V. Sukhatme. Pune, India: Maharashtra Assoc. 1982, p. 101–114.
 145. Thomas, R. B. Energy flow at high altitude. In: Man in the Andes, edited by P. T. Baker and M. A. Little. Stroudsburg, PA: Dowden, Hutchinson and Ross, 1976, p. 379–404.
 146. Thomas, R. B., and T. Leatherman. Household coping strategies and contradictions in response to seasonal food shortage. Eur. J. Clin. Nutr. 44 (suppl 1): 103–112, 1990.
 147. Tomkins, A. M. Nutritonal status and severity of diarrhoea among preschool children in rural Nigeria. Lancet i: 860–862, 1981.
 148. Tomkins, A. M. Protein energy malnutrition and risk of infection. Proc. Nutr. Soc. 45: 289–304, 1986.
 149. Torun, B. Short‐ and long‐term effects of low or restricted energy intakes on the activity of infants and children. In: Activity, Energy Expenditure and Energy Requirements of Infants and Children, edited by B. Schürch and N. S. Scrimshaw. Lausanne, Switzerland: IDECG, 1990, p. 335–358.
 150. Torun, B., and F. E. Viteri. Energy requirements of pre‐school children and effects of varying energy intakes on protein metabolism. U. N. Univ. Food Nutr. Bull. (suppl. 5): 210–228.
 151. Trussell, J. Statistical flaws in evidence for the Frisch hypothesis that fatness triggers menarche. Hum. Biol. 52: 711–720, 1980.
 152. Viteri, F. E. Considerations on the effects of nutrition on body composition and physical working capacity of young Guatemalan adults. In: Amino‐Acid Fortification of Protein Foods, edited by N. S. Scrimshaw and A. M. Altschul. Cambridge, MA: MIT, 1971, p. 350–375.
 153. Waterlow, J. C. Postscript. In: Nutritional Adaptation in Man, edited by Sir K. Blaxter and J. C. Waterlow. London: Libbey, 1985, p. 233–235.
 154. Waterlow, J. C. What do we mean by adaptation? In: Nutritional Adaptation in Man, edited by Sir K. Blaxter and J. C. Waterlow. London: Libbey, 1985, p. 1–11.
 155. Waterlow, J. C. Metabolic adaptation to low intakes of energy and protein. Annu. Rev. Nutr. 6: 495–526, 1986.
 156. Waterlow, J. C. Mechanisms of adaptation to low energy intakes. In: Diet and Disease in Traditional and Developing Societies, edited by G. A. Harrison and J. C. Waterlow. Cambridge: Cambridge University Press, 1990, p. 5–23.
 157. Waterlow, J. C. Nutritional adaptation in man; general introduction and concepts. Am. J. Clin. Nutr. 51: 259–263, 1990.
 158. Waterlow, J. C., R. Buzina, W. Keller, J. M. Lane, M. Z. Nichaman, and J. M. Tanner. The presentation and use of height and weight data for comparing the nutritional status of groups of children under the age of 10 years. Bull. WHO 55: 489–498, 1977.
 159. Weindruch, R. H., M. K. Cheung, A. Verity, and R. L. Walford. Modification of mitochondrial respiration by aging and dietary restriction. Mech. Ageing Dev. 12: 375–392, 1980.
 160. Welle, S. and R. G. Campbell. Lack of catecholamine mediated thermogenesis during carbohydrate overfeeding in man. J. Clin. Invest. 71: 916–925, 1983.
 161. Widdowson, E. M. The responses of the sexes to nutritional stress. Proc. Nutr. Soc. 35: 175–180, 1976.

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N. G. Norgan, A. Ferro‐Luzzi. Human Adaptation to Energy Undernutrition. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 1391-1409. First published in print 1996. doi: 10.1002/cphy.cp040261