The thrifty phenotype: An adaptation in growth or metabolism?

American Journal of Human Biology

Volumn 23, Issue 1, 2011, Pages 65-75

  Wells, Jonathan C K ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ADULT; ANIMAL; BIOLOGICAL MODEL; ENERGY METABOLISM; FEMALE; GROWTH; HUMAN; INSULIN RESISTANCE; MALE; OBESITY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ADIPOSITY; ADULT; ANIMALS; ENERGY METABOLISM; FEMALE; GROWTH; HUMANS; INSULIN RESISTANCE; MALE; MODELS, BIOLOGICAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

ARMERIA;

EID: 78650107153     PISSN: 10420533     EISSN: 15206300     Source Type: Journal    
DOI: 10.1002/ajhb.21100     Document Type: Review

References (130)

1. Abrams ET, Meshnick SR. 2009. Malaria during pregnancy in endemic areas: a lens for examining maternal-fetal conflict. Am J Hum Biol 21: 643-650.
2. Adair LS, Cole TJ. 2003. Rapid child growth raises blood pressure in adolescent boys who were thin at birth. Hypertension 41: 451-456.
3. Andersen LB, Harro M, Sardinha LB, Froberg K, Ekelund U, Brage S, Anderssen SA. 2006. Physical activity and clustered cardiovascular risk in children: a cross-sectional study (The European Youth Heart Study). Lancet 368: 299-304.
4. Asling-Monemi K, Naved RT, Persson LA. 2009. Violence against women and the risk of fetal and early childhood growth impairment: a cohort study in rural Bangladesh. Arch Dis Child 94: 775-779.
5. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. 1989a. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298: 564-567.
6. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. 1989b. Weight in infancy and death from ischaemic heart disease. Lancet 2: 577-580.
7. Barker DJ, Bull AR, Osmond C, Simmonds SJ. 1990. Fetal and placental size and risk of hypertension in adult life. BMJ 301: 259-262.
8. Barker DJ. 1991. The intrauterine environment and adult cardiovascular disease. Ciba Found Symp 156: 3-10.
9. Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life. BMJ 307: 1524-1527.
10. Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. 2005. Trajectories of growth among children who have coronary events as adults. N Engl J Med 353: 1802-1809.
11. Barker DJ, Osmond C, Kajantie E, Eriksson JG. 2009. Growth and chronic disease: findings in the Helsinki Birth Cohort. Ann Hum Biol 36: 445-458.
12. Bauer R, Walter B, Brust P, Fuchtner F, Zwiener U. 2003. Impact of asymmetric intrauterine growth restriction on organ function in newborn piglets. Eur J Obstet Gynecol Reprod Biol 110 (Suppl 1): S40-S49.
13. Bavdekar A, Yajnik CS, Fall CH, Bapat S, Pandit AN, Deshpande V, Bhave S, Kellingray SD, Joglekar C. 1999. Insulin resistance syndrome in 8-year-old Indian children: small at birth, big at 8 years, or both? Diabetes 48: 2422-2429.
14. Bhargava SK, Sachdev HS, Fall CH, Osmond C, Lakshmy R, Barker DJ, Biswas SK, Ramji S, Prabhakaran D, Reddy KS. 2004. Relation of serial changes in childhood body-mass index to impaired glucose tolerance in young adulthood. New Engl J Med 350: 865-875.
15. Breant B, Gesina E, Blondeau B. 2006. Nutrition, glucocorticoids and pancreas development. Horm Res 65 (Suppl 3): 98-104.
16. Carcopino X, Raoult D, Bretelle F, Boubli L, Stein A. 2009. Q Fever during pregnancy: a cause of poor fetal and maternal outcome. Ann N Y Acad Sci 1166: 79-89.
17. Centers for Disease Control and Prevention (CDC). Nutritional assessment of children after severe winter weather-Mongolia, June 2001. MMWR Morb Mortal Wkly Rep 51: 5-7.
18. Chomtho S, Wells JC, Williams JE, Davies PS, Lucas A, Fewtrell MS. 2008. Infant growth and later body composition: evidence from the 4-component model. Am J Clin Nutr 87: 1776-1784.
19. Dahlgren J. 2006. Pregnancy and insulin resistance. Metab Syndr Relat Disord 4: 149-152.
20. de Meer K, Heymans HS, Zijlstra WG. 1995. Physical adaptation of children to life at high altitude. Eur J Pediatr 154: 263-272.
21. Delgado HL, Valverde VE, Martorell R, Klein RE. 1982. Relationship of maternal and infant nutrition to infant growth. Early Hum Dev 6: 273-286.
22. Desai M, Crowther NJ, Lucas A, Hales CN. 1996. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76: 591-603.
23. Dewey KG, Cohen RJ. 2007. Does birth spacing affect maternal or child nutritional status? A systematic literature review. Matern Child Nutr 3: 151-173.
24. Dezateux C, Lum S, Hoo AF, Hawdon J, Costeloe K, Stocks J. 2004. Low birth weight for gestation and airway function in infancy: exploring the fetal origins hypothesis. Thorax 59: 60-66.
25. Dos Santos Rizzi MC, Júnior EA, Nardozza LM, Diniz AL, Rolo LC, Moron AF. 2010. Nomogram of fetal liver volume by three-dimensional ultrasonography at 27 to 38 weeks of pregnancy using a new multiplanar technique. Am J Perinatol 27: 641-648.
26. Dulloo AG. 2008. Thrifty energy metabolism in catch-up growth trajectories to insulin and leptin resistance. Best Pract Res Clin Endocrinol Metab 22: 155-171.
27. Eaton SB, Konner M, Shostak M. 1988. Stone agers in the fast lane: chronic degenerative diseases in evolutionary perspective. Am J Med 84: 739-749.
28. Ekelund U, Ong K, Linne Y, Neovius M, Brage S, Dunger DB, Wareham NJ, Rossner S. 2006. Upward weight percentile crossing in infancy and early childhood independently predicts fat mass in young adults: the Stockholm Weight Development Study (SWEDES). Am J Clin Nutr 83: 324-330.
29. Ezzahir N, Alberti C, Deghmoun S, Zaccaria I, Czernichow P, Levy-Marchal C, Jaquet D. 2005. Time course of catch-up in adiposity influences adult anthropometry in individuals who were born small for gestational age. Pediatr Res 58: 243-247.
30. Fagerberg B, Bondjers L, Nilsson P. 2004. Low birth weight in combination with catch-up growth predicts the occurrence of the metabolic syndrome in men at late middle age: the Atherosclerosis and Insulin Resistance study. J Intern Med 256: 254-259.
31. Ford ES, Kohl HW, III, Mokdad AH, Ajani UA. 2005. Sedentary behavior, physical activity, and the metabolic syndrome among U.S. adults. Obes Res 13: 608-614.
32. Forsen T, Eriksson J, Tuomilehto J, Reunanen A, Osmond C, Barker D. 2000. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med 133: 176-182.
33. Fowden AL, Forhead AJ. 2009. Hormones as epigenetic signals in developmental programming. Exp Physiol 94: 607-625.
34. Galgani JE, Moro C, Ravussin E. Metabolic flexibility and insulin resistance. Am J Physiol EndocrinolMetab 2008; 295: E1009-E1017.
35. Gatford KL, Mohammad SN, Harland ML, De Blasio MJ, Fowden AL, Robinson JS, Owens JA. 2008. Impaired beta-cell function and inadequate compensatory increases in beta-cell mass after intrauterine growth restriction in sheep. Endocrinology 149: 5118-5127.
36. Gluckman PD, Hanson MA, Spencer HG. Predictive adaptive responses and human evolution. Trends Ecol Evol 2005; 20: 527-533.
37. Godfrey KM, Barker DJ, Robinson S, Osmond C. 1997. Maternal birthweight and diet in pregnancy in relation to the infant's thinness at birth. Br J Obstet Gynaecol 104: 663-667.
38. Godfrey KM, Gluckman PD, Hanson MA. 2010. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab 21: 199-205.
39. Haig D. 1993. Genetic conflicts in human pregnancy. Q Rev Biol 68: 495-532.
40. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD. 1991. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 303: 1019-1022.
41. Hales CN, Barker DJ. 1992. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35: 595-601.
42. Harrington TA, Thomas EL, Frost G, Modi N, Bell JD. 2004. Distribution of adipose tissue in the newborn. Pediatr Res 55: 437-441.
43. Holliday MA. 1978. Body composition and energy needs during growth. In: Falkner F, Tanner JM, editors. New York: Plenum. p 101-117.
44. Huxley RR, Shiell AW, Law CM. 2000. The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. J Hypertens 18: 815-831.
45. Ibanez L, Ong K, Dunger DB, de ZF. 2006. Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab 91: 2153-2158.
46. Ibanez L, Lopez-Bermejo A, Suarez L, Marcos MV, Diaz M, de ZF. 2008. Visceral adiposity without overweight in children born small-for-gestational-age. J Clin Endocrinol Metab 93: 2079-2083.
47. Isanaka S, Duggan C, Fawzi WW. 2009. Patterns of postnatal growth in HIV-infected and HIV-exposed children. Nutr Rev 67: 343-359.
48. Jacobson MS. 1987. Cholesterol oxides in Indian ghee: possible cause of unexplained high risk of atherosclerosis in Indian immigrant populations. Lancet 2: 656-658.
49. Jones JH. 2005. Fetal programming: adaptive life-history tactics or making the best of a bad start? Am J Hum Biol 17: 22-33.
50. Kalanda BF, van Buuren S, Verhoeff FH, Brabin BJ. 2005. Catch-up growth in Malawian babies, a longitudinal study of normal and low birthweight babies born in a malarious endemic area. Early Hum Dev 81: 841-850.
51. Kensara OA, Wootton SA, Phillips DI, Patel M, Jackson AA, Elia M. 2005. Fetal programming of body composition: relation between birth weight and body composition measured with dual-energy X-ray absorptiometry and anthropometric methods in older Englishmen. Am J Clin Nutr 82: 980-987.
52. Kieu NT, Yasugi E, Hung NT, Kido T, Kondo K, Yamamoto S, Chuyen NV, Oshima M. 2002. Serum fatty acids, lipoprotein (a) and apolipoprotein profiles of middle-aged men and women in South Vietnam. Asia Pac J Clin Nutr 11: 112-116.
53. Kilavuz O, Vetter K. 1999. Is the liver of the fetus the 4th preferential organ for arterial blood supply besides brain, heart, and adrenal glands? J Perinat Med 27: 103-106.
54. Kinare AS, Chinchwadkar MC, Natekar AS, Coyaji KJ, Wills AK, Joglekar CV, Yajnik CS, Fall CH. 2010. Patterns of fetal growth in a rural Indian cohort and comparison with a Western European population: data from the pune maternal nutrition study. J Ultrasound Med 29: 215-223.
55. Kramer MS. 1987. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ 65: 663-737.
56. Krishnaveni GV, Hill JC, Veena SR, Leary SD, Saperia J, Chachyamma KJ, Karat SC, Fall CH. 2005. Truncal adiposity is present at birth and in early childhood in South Indian children. Indian Pediatr 42: 527-538.
57. Kuller LH. 2004. Ethnic differences in atherosclerosis, cardiovascular disease and lipid metabolism. Curr Opin Lipidol 15: 109-113.
58. Kuzawa CW. 2005. Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? Am J Hum Biol 17: 5-21.
59. Latini G, De Mitri B, Del Vecchio A, Chitano G, De Felice C, Zetterstrom R. Foetal growth of kidneys, liver and spleen in intrauterine growth restriction: "programming" causing "metabolic syndrome" in adult age. Acta Paediatr. 2004; 93: 1635-1639.
60. Lawlor DA, Leon DA, Davey Smith G. 2005. The association of ambient outdoor temperature throughout pregnancy and offspring birthweight: findings from the Aberdeen Children of the 1950s cohort. BJOG 112: 647-657.
61. Lawson DW, Mace R. 2008. Sibling configuration and childhood growth in contemporary British families. Int J Epidemiol 37: 1408-1421.
62. Leon DA, Lithell HO, Vâgerö D, Koupilová I, Mohsen R, Berglund L, Lithell UB, McKeigue PM. 1998. Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915-29. BMJ 317: 241-245.
63. Lindeberg S, Nilsson-Ehle P, Terent A, Vessby B, Schersten B. 1994. Cardiovascular risk factors in a Melanesian population apparently free from stroke and ischaemic heart disease: the Kitava study. J Intern Med 236: 331-340.
64. Lucas A, Fewtrell MS, Cole TJ. 1999. Fetal origins of adult disease-the hypothesis revisited. BMJ 319: 245-249.
65. Lurbe E, Carvajal E, Torro I, Aguilar F, Alvarez J, Redon J. 2009. Influence of concurrent obesity and low birth weight on blood pressure phenotype in youth. Hypertension 53: 912-917.
66. Lustig RH. 2008. Which comes first? The obesity or the insulin? The behavior or the biochemistry? J Pediatr 152: 601-602.
67. Manalich R, Reyes L, Herrera M, Melendi C, Fundora I. 2000. Relationship between weight at birth and the number and size of renal glomeruli in humans: a histomorphometric study. Kidney Int 58: 770-773.
68. Martin-Gronert MS, Ozanne SE. 2005. Programming of appetite and type 2 diabetes. Early Hum Dev 81: 981-988.
69. McKeown NM, Meigs JB, Liu S, Saltzman E, Wilson PW, Jacques PF. 2004. Carbohydrate nutrition, insulin resistance, and the prevalence of the metabolic syndrome in the Framingham Offspring Cohort. Diabetes Care 27: 538-546.
70. Mericq V, Ong KK, Bazaes R, Pena V, Avila A, Salazar T, Soto N, Iniguez G, Dunger DB. 2005. Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children. Diabetologia 48: 2609-2614.
71. Misra A, Khurana L. 2009. The metabolic syndrome in South Asians: epidemiology, determinants, and prevention. Metab Syndr Relat Disord 7: 497-514.
72. Modi N, Thomas EL, Harrington TA, Uthaya S, Dore CJ, Bell JD. 2006. Determinants of adiposity during preweaning postnatal growth in appropriately grown and growth-restricted term infants. Pediatr Res 60: 345-348.
73. Modi N, Thomas EL, Uthaya SN, Umranikar S, Bell JD, Yajnik C. Whole body magnetic resonance imaging of healthy newborn infants demonstrates increased central adiposity in Asian Indians. Pediatr Res 2009; 65: 584-587.
74. Moore LG, Shriver M, Bemis L, Hickler B, Wilson M, Brutsaert T, Parra E, Vargas E. 2004. Maternal adaptation to high-altitude pregnancy: an experiment of nature-a review. Placenta 18: S60-S71.
75. Moore SE, Halsall I, Howarth D, Poskitt EM, Prentice AM. 2001. Glucose, insulin and lipid metabolism in rural Gambians exposed to early malnutrition. Diabet Med 18: 646-653.
76. Moses RG, Luebcke M, Davis WS, Coleman KJ, Tapsell LC, Petocz P, Brand-Miller JC. 2006. Effect of a low-glycemic-index diet during pregnancy on obstetric outcomes. Am J Clin Nutr 84: 807-812.
77. Mousseau TA, Fox CW. 1998. The adaptive significance of maternal effects. Trends Ecol Evol 13: 403-407.
78. Must A, Spadano J, Coakley EH, Field AE, Colditz G, Dietz WH. 1999. The disease burden associated with overweight and obesity. JAMA 282: 1523-1529.
79. Mukhopadhyay DK, Biswas R, Chakraborty M, Sadhukhan SK, Banik KK. 2009. Anthropometric failure, a new approach to measure undernutrition: an experience from a rural community of West Bengal, India. J Indian Med Assoc 107: 211-214, 236.
80. Muthayya S, Dwarkanath P, Thomas T, Vaz M, Mhaskar A, Mhaskar R, Thomas A, Bhat S, Kurpad A. 2006. Anthropometry and body composition of south Indian babies at birth. Public Health Nutr 9: 896-903.
81. Newsome CA, Shiell AW, Fall CH, Phillips DI, Shier R, Law CM. 2003. Is birth weight related to later glucose and insulin metabolism?-A systematic review. Diabet Med 20: 339-348.
82. Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. 2000. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 320: 967-971.
83. Ong KK, Petry CJ, Emmett PM, Sandhu MS, Kiess W, Hales CN, Ness AR, Dunger DB;ALSPAC study team. 2004. Insulin sensitivity and secretion in normal children related to size at birth, postnatal growth, and plasma insulin-like growth factor-I levels. Diabetologia 47: 1064-1070.
84. Painter RC, Roseboom TJ, Bleker OP. 2005. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 20: 345-352.
85. Painter RC, de Rooij S, Bossuyt PM, Simmers TA, Osmond C, Barker DJ, Bleker OP, Roseboom TJ. 2006. Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr 84: 322-327.
86. Pardi G, Marconi AM, Cetin I. 2002. Placental-fetal interrelationship in IUGR fetuses-a review. Placenta 23 Suppl A: S136-S141.
87. Petry CJ, Desai M, Ozanne SE, Hales CN. 1997. Early and late nutritional windows for diabetes susceptibility. Proc Nutr Soc 56: 233-242.
88. Poston WS, Foreyt JP. 1999. Obesity is an environmental issue. Atherosclerosis 146: 201-209.
89. Prentice AM, Jebb SA. 2003. Fast foods, energy density and obesity: a possible mechanistic link. Obes Rev 4: 187-194.
90. Prentice AM, Cole TJ, Foord FA, Lamb WH, Whitehead RG. 1987. Increased birthweight after prenatal dietary supplementation of rural African women. Am J Clin Nutr 46: 912-925.
91. Prentice AM, Rayco-Solon P, Moore SE. 2005. Insights from the developing world: thrifty genotypes and thrifty phenotypes. Proc Nutr Soc 64: 153-161.
92. Rao S, Yajnik CS, Kanade A, Fall CH, Margetts BM, Jackson AA, Shier R, Joshi S, Rege S, Lubree H, Desai B. 2001. Intake of micronutrient-rich foods in rural Indian mothers is associated with the size of their babies at birth: Pune Maternal Nutrition Study. J Nutr 131: 1217-1224.
93. Ravelli GP, Stein ZA, Susser MW. 1976. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295: 349-353.
94. Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP. 1999. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 70: 811-816.
95. Reaven GM. 1988. Banting lecture. 1988. Role of insulin resistance in human disease. Diabetes 37: 1595-1607.
96. Rosenberg M. 1988. Birth weights in three Norwegian cities, 1860-1984. Secular trends and influencing factors. Ann Hum Biol 15: 275-288.
97. Sachdev HS, Fall CH, Osmond C, Lakshmy R, Dey Biswas SK, Leary SD, Reddy KS, Barker DJ, Bhargava SK. Anthropometric indicators of body composition in young adults: relation to size at birth and serial measurements of body mass index in childhood in the New Delhi birth cohort. Am J Clin Nutr 2005; 82: 456-466.
98. Samaras TT. 2007. Human Body Size and the Laws of Scaling: Physiological, Performance, Growth, Longevity and Ecological Ramifications. Nova Science Publishers, NY.
99. Sinclair KD, Lea RG, Rees WD, Young LE. 2007. The developmental origins of health and disease: current theories and epigenetic mechanisms. Soc Reprod Fertil Suppl 64: 425-443.
100. Singhal A, Lucas A. 2004. Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet 363: 1642-1645.
101. Soto N, Bazaes RA, Pena V, Salazar T, Avila A, Iniguez G, Ong KK, Dunger DB, Mericq MV. 2003. Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort. J Clin Endocrinol Metab 88: 3645-3650.
102. Speakman JR. 2008. Thrifty genes for obesity, an attractive but flawed idea, and an alternative perspective: the 'drifty gene' hypothesis. Int J Obes 32: 1611-1617.
103. Stanner SA, Yudkin JS. 2001. Fetal programming and the Leningrad Siege study. Twin Res 4: 287-292.
104. Stein CE, Fall CH, Kumaran K, Osmond C, Cox V, Barker DJ. 1996. Fetal growth and coronary heart disease in south India. Lancet 348: 1269-1273.
105. Stein AD, Zybert PA, van de Bor M, Lumey LH. 2004. Intrauterine famine exposure and body proportions at birth: the Dutch Hunger Winter. Int J Epidemiol 33: 831-836.
106. Stettler N, Zemel BS, Kumanyika S, Stallings VA. 2002. Infant weight gain and childhood overweight status in a multicenter, cohort study. Pediatrics 109: 194-199.
107. Taubes G. 2008. The diet delusion. London: Vermillion.
108. Ticconi C, Mapfumo M, Dorrucci M, Naha N, Tarira E, Pietropolli A, Rezza G. 2003. Effect of maternal HIV and malaria infection on pregnancy and perinatal outcome in Zimbabwe. J Acquir Immune Defic Syndr 34: 289-294.
109. Torre P, Ladaki C, Scire G, Spadoni GL, Cianfarani S. 2008. Catch-up growth in body mass index is associated neither with reduced insulin sensitivity nor with altered lipid profile in children born small for gestational age. J Endocrinol Invest 31: 760-764.
110. Tzoulaki J, Jarvelin MR, Hartikainen AL, Leinonen M, Pouta A, Paldanius M, Ruokonen A, Canoy D, Sovio U, Saikku P, Elliott P. 2008. Size at birth, weight gain over the life course, and low-grade inflammation in young adulthood: northern Finland 1966 Birth Cohort Study. Eur Heart J 29: 1049-1056.
111. van Steijn L, Karamali NS, Kanhai HH, Ariens GA, Fall CH, Yajnik CS, Middelkoop BJ, Tamsma JT. 2009. Neonatal anthropometry: thin-fat phenotype in fourth to fifth generation South Asian neonates in Surinam. Int J Obes 33: 1326-1329.
112. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L, Sachdev HS. 2008. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 371: 340-357.
113. Waterland RA, Michels KB. 2007. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr 27: 363-388.
114. Weder AB, Schork NJ. 1994. Adaptation, allometry, and hypertension. Hypertension 24: 145-156.
115. Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW, Allen K, Lopes M, Savoye M, Morrison J, Sherwin RS, Caprio S. 2004. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350: 2362-2374.
116. Wells JC. 2000. Environmental temperature and human growth in early life. J Theor Biol 204: 299-305.
117. Wells JC. 2003. The thrifty phenotype hypothesis: thrifty offspring or thrifty mother? J Theor Biol 221: 143-161.
118. Wells JC. 2007a. Flaws in the theory of predictive adaptive responses. Trends Endocrinol Metab 18: 331-337.
119. Wells JC. 2007b. The thrifty phenotype as an adaptive maternal effect. Biol Rev Camb Philos Soc 82: 143-172.
120. Wells JCK. 2009a. Historical cohort studies and the early origins of disease hypothesis: making sense of the evidence. Proc Nutr Soc 68: 179-188.
121. Wells JC. 2009b. Thrift: a guide to thrifty genes, thrifty phenotypes and thrifty norms. Int J Obes 33: 1331-1338.
122. Wells JC. 2010. Maternal capital and the metabolic ghetto: an evolutionary perspective on the transgenerational basis of health inequalities. Am J Hum Biol 22: 1-17.
123. Wells JC, Cole TJ. 2002. Birth weight and environmental heat load: a between-population analysis. Am J Phys Anthropol 119: 276-282.
124. Wells JC, Davies PS. 1998. Estimation of the energy cost of physical activity in infancy. Arch Dis Child 78: 131-136.
125. Wells JC, Stock JT. 2007. The biology of the colonizing ape. Am J Phys Anthropol Suppl. 45: 191-222.
126. Wells JC, Hallal PC, Wright A, Singhal A, Victora CG. 2005. Fetal, infant and childhood growth: relationships with body composition in Brazilian boys aged 9 years. Int J Obes 29: 1192-1198.
127. Wells JC, Chomtho S, Fewtrell MS. 2007. Programming of body composition by early growth and nutrition. Proc Nutr Soc 66: 423-434.
128. Willett W, Manson J, Liu S. 2002. Glycemic index, glycemic load, and risk of type 2 diabetes. Am J Clin Nutr 76: 274S-280S.
129. Yajnik CS, Fall CH, Coyaji KJ, Hirve SS, Rao S, Barker DJ, Joglekar C, Kellingray S. 2003. Neonatal anthropometry: the thin-fat Indian baby. The Pune Maternal Nutrition Study. Int J Obes Relat Metab Disord 27: 173-180.
130. Yajnik CS, Lubree HG, Rege SS, Naik SS, Deshpande JA, Deshpande SS, Joglekar CV, Yudkin JS. 2002. Adiposity and hyperinsulinemia in Indians are present at birth. J Clin Endocrinol Metab 87: 5575-5580.