Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T09:44:03.103Z Has data issue: false hasContentIssue false
  • English
  • Français

Auxological perspectives on ‘growth’ in DOHaD

Part of: Sir David Barker Symposium

Published online by Cambridge University Press:  13 August 2015

M. Lampl ,
A. Mummert  and
M. Schoen
M. Lampl*
Affiliation:
Center for the Study of Human Health, Emory University, Atlanta, GA, USA Department of Anthropology, Emory University, Atlanta, GAUSA
A. Mummert
Affiliation:
Center for the Study of Human Health, Emory University, Atlanta, GA, USA Department of Anthropology, Emory University, Atlanta, GAUSA
M. Schoen
Affiliation:
Center for the Study of Human Health, Emory University, Atlanta, GA, USA
*
*Address for correspondence: M. Lampl, Center for the Study of Human Health, Emory University, 107 Candler Library, 550 Asbury Circle, Atlanta, GA 30322, USA. (Email mlampl@emory.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

David Barker established growth as a seminal link between early development and later health attainment and disease risk. This was nothing less than a paradigm shift in health and medicine, turning the focus of disease causality away from contemporary environmental influences to earliest growth as a time when functional anatomy and physiology sets in place critical structures and function for a lifetime.

Barker’s prodigious work investigated time- and place-specific interactions between maternal condition and exogenous environmental influences, focusing on how growth unfolds across development to function as a mechanistic link to ensuing health. Subsequent applications do not always attend to the specificity and sensitivity issues included in his original work, and commonly overlook the long-standing methods and knowledge base of auxology. Methodological areas in need of refinement include enhanced precision in how growth is represented and assessed. For example, multiple variables have been used as a referent for ‘growth,’ which is problematic because different body dimensions grow by different biological clocks with unique functional physiologies. In addition, categorical clinical variables obscure the spectrum of variability in growth experienced at the individual level. Finally, size alone is a limited measure as it does not capture how individuals change across age, or actually grow.

The ground-breaking notion that prenatal influences are important for future health gave rise to robust interest in studying the fetus. Identifying the many pathways by which size is realized permits targeted interventions addressing meaningful mechanistic links between growth and disease risk to promote health across the lifespan.

Keywords

auxologydevelopmental originsfetal growthfetologylifespan health
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 6 , Issue 5: Themed Issue: David Barker commemorative meeting, September 2014; Prenatal Exposures and Health Outcomes , October 2015 , pp. 390 - 398
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Tanner, JM. Catch-up growth in man. Br Med Bull. 1981; 37, 233–238.CrossRefGoogle ScholarPubMed
2. Hammond, J. The fertilisation of rabbit ova in relation to time: a method of controlling the litter size, the duration of pregnancy and the weight of the young at birth. J Exp Biol. 1934; 11, 140–161.Google Scholar
3. Walton, A, Hammond, J. The maternal effects on growth and conformation in Shire Horse-Shetland pony crosses. Proc R Soc Lond B Biol Sci. 1938; 125, 311–335.Google Scholar
4. Gregory, PW. The Early Embryology of the Rabbit, 1930. Carnegie Institution of Washington, Washington DC.Google Scholar
5. McLaren, A, Michie, D. Congenital Runts. In Ciba Foundation Symposium - Congenital Malformations (eds. Wolstenholme GEW, O’Connor CM), 1960; pp. 178–198. John Wiley & Sons, Ltd., Chichester, UK.Google Scholar
6. Cawley, R, McKeown, T, Record, R. Parental stature and birth weight. Am J Hum Genet. 1954; 6, 448–456.Google Scholar
7. McKeown, T, Gibson, J. Observations on all births (23,970) in Birmingham. II. Birth weight. Brit J Soc Med. 1951; 5, 98–112.Google Scholar
8. McKeown, T, Record, RG. Observations on fetal growth in multiple pregnancy in man. J Endocrinol. 1952; 8, 386–401.CrossRefGoogle ScholarPubMed
9. McKeown, T, Record, R. The influence of placental size on foetal growth in man, with special reference to multiple pregnancy. J Endocrinol. 1953; 9, 418–426.CrossRefGoogle ScholarPubMed
10. McKeown, T, Record, R. Influence of pre-natal environment on correlation between birth weight and parental height. Am J Hum Genet. 1954; 6, 456–463.Google Scholar
11. Gibson, J, McKeown, T. Observations on all births (23,790) in Birmingham. V. Birth weight related to economic circumstances of parents. Brit J Soc Med. 1951; 5, 259–264.Google Scholar
12. Lowe, C, McKeown, T. Incidence of infectious disease in the first three years of life, related to social circumstances. Brit J Prev Soc Med. 1954; 8, 24–28.Google Scholar
13. Gruenwald, P. Chronic fetal distress and placental insufficiency (Part 3 of 3). Neonatology. 1963; 5, 249–265.CrossRefGoogle Scholar
14. Ounsted, M. Maternal constraint of foetal growth in man. Dev Med Child Neurol. 1965; 7, 479–491.CrossRefGoogle ScholarPubMed
15. Ounsted, M, Ounsted, C. Maternal regulation of intra-uterine growth. Nature. 1966; 212, 995–997.Google Scholar
16. Wigglesworth, J. Foetal growth retardation. Br Med Bull. 1966; 22, 13–15.Google Scholar
17. Philip, A. The evolution of neonatalogy. Pediatr Res. 2005; 58, 799–815.CrossRefGoogle Scholar
18. Barker, DJP, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986; 327, 1077–1081.Google Scholar
19. Buck, C, Simpson, H. Infant diarrhoea and subsequent mortality from heart disease and cancer. J Epidemiol Community Health. 1982; 36, 27–30.Google Scholar
20. Forsdahl, A. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prev Soc Med. 1977; 31, 91–95.Google Scholar
21. Ben-Shlomo, Y, Smith, GD. Deprivation in infancy or in adult life: which is more important for mortality risk? Lancet. 1991; 337, 530–534.CrossRefGoogle ScholarPubMed
22. McEwen, B, Stellar, E. Stress and the individual. Mechanisms leading to disease. Arch Intern Med. 1993; 153, 2093–2101.Google Scholar
23. Barker, D, Osmond, C. Death rates from stroke in England and Wales predicted from past maternal mortality. BMJ. 1987; 295, 83–86.Google Scholar
24. Cawley, R, McKeown, T, Record, R. Influence of pre-natal environment on post-natal growth. Br J Prev Soc Med. 1954; 8, 66–69.Google ScholarPubMed
25. Thomson, J. Observations on weight gain in infants. Arch Dis Child. 1955; 30, 322–327.CrossRefGoogle ScholarPubMed
26. Smith, D, Truog, W, Rogers, J, et al. Shifting linear growth during infancy: illustration of genetic factors in growth from fetal life through infancy. J Pediatr. 1976; 89, 225–230.CrossRefGoogle ScholarPubMed
27. Ounsted, M, Cockburn, J, Moar, V, Redman, C. Factors associated with the blood pressures of children born to women who were hypertensive during pregnancy. Arch Dis Child. 1985; 60, 631–635.Google Scholar
28. Eriksson, JG, Forsén, T, Tuomilehto, J, et al. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ. 1999; 318, 427–431.Google Scholar
29. Barker, DJP, Osmond, C, Golding, J, Kuh, D, Wadsworth, ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989; 298, 564–567.Google Scholar
30. Forsén, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176–182.CrossRefGoogle ScholarPubMed
31. Gennser, G, Rymark, P, Isbert, P. Low birth weight and risk of high blood pressure in adulthood. BMJ. 1988; 296, 1498–1500.CrossRefGoogle ScholarPubMed
32. Barker, DJ, Osmond, C, Law, CM. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health. 1989; 43, 237–240.Google Scholar
33. Barker, DJ, Osmond, C, Pannett, B. Why Londoners have low death rates from ischaemic heart disease and stroke. BMJ. 1992; 305, 1551–1554.Google Scholar
34. Cameron, N. The Measurement of Human Growth. 1984. Croom Helm: London.Google Scholar
35. Tanner, JM. Fetus into Man: Physical Growth from Conception to Maturity. 1990. Harvard University Press: Cambridge, MA.Google Scholar
36. Stevens, J, McClain, JE, Truesdale, KP. Selection of measures in epidemiologic studies of the consequences of obesity. Int J Obes. 2008; 32(Suppl. 3), S60–S66.Google Scholar
37. Lampl, M, Mummert, A. Historical approaches to human growth studies limit the present understanding of growth biology. Ann Nutr Metab. 2014; 65, 114–120.CrossRefGoogle ScholarPubMed
38. Forsén, T, Eriksson, JG, Tuomilehto, J, Osmond, C, Barker, DJP. Growth in utero and during childhood among women who developed coronary heart disease: longitudinal study. BMJ. 1999; 319, 1403–1407.Google Scholar
39. Godfrey, KM, Barker, DJ. Fetal programming and adult health. Public Health Nutr. 2001; 4, 611–624.Google Scholar
40. Widdowson, EM, McCance, RA. A review: new thoughts on growth. Pediatr Res. 1975; 9, 154–156.CrossRefGoogle ScholarPubMed
41. Lorenz, K. The companion in the bird’s world. The fellow-member of the species as releasing factor of social behavior. J Ornithol Beiblatt (Leipzig). 1935; 83, 137–213.Google Scholar
42. Bornstein, MH. Sensitive periods in development: structural characteristics and causal interpretations. Psychol Bull. 1989; 105, 179–197.Google Scholar
43. Spalding, DA. Instinct with original observations on young animals. Macmillan’s Magazine. 1873; 27, 282–293.Google Scholar
44. Hanson, MA, Gluckman, PD. Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev. 2014; 94, 1027–1076.Google Scholar
45. Dorner, G. Perinatal hormone levels and brain organization. In Anatomical Neuroendocrinology (eds. Stumpf WE, Grant LD), 1975; pp 245–252. Karger: Basel.Google Scholar
46. Hertzman, C. Putting the concept of biological embedding in historical perspective. Proc Natl Acad Sci U S A. 2012; 109(Suppl. 2), 17160–17167.Google Scholar
47. Koplan, JP, Liverman, CT, Kraak, VI. Preventing childhood obesity: health in the balance: executive summary. J Am Diet Assoc. 2005; 105, 131–138.CrossRefGoogle ScholarPubMed
48. Bedogni, G, Iughetti, L, Ferrari, M, et al. Sensitivity and specificity of body mass index and skinfold thicknesses in detecting excess adiposity in children aged 8-12 years. Ann Hum Biol. 2003; 30, 132–139.Google Scholar
49. Lee, M-J, Wu, Y, Fried, SK. Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol Aspects Med. 2013; 34, 1–11.CrossRefGoogle ScholarPubMed
50. Prentice, P, Viner, RM. Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes. 2013; 37, 1036–1043.Google Scholar
51. World Health Organization. The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines. 1992. World Health Organization: Geneva.Google Scholar
52. Butler, NR, Bonham, DG. Perinatal Mortality. The First Report of the 1958 British Perinatal Mortality Survey. 1963. Livingstone: Edinburgh.Google Scholar
53. Altman, DG, Hytten, FE. Intrauterine growth retardation: let’s be clear about it. Br J Obstet Gynecol. 1989; 96, 27–32.CrossRefGoogle Scholar
54. Royston, P, Altman, DG, Sauerbrie, W. Dichotomizing continuous predictors in multiple regression: always a bad idea. Stat Med. 2006; 25, 127–141.Google Scholar
55. Wilcox, AJ. Intrauterine growth retardation: beyond birthweight criteria. Early Hum Dev. 1983; 8, 189–193.Google Scholar
56. Kramer, MS, Martin, RM, Bogdanovich, N, et al. Is restricted fetal growth associated with later adiposity? Observational analysis of a randomized trial. Am J Clin Nutr. 2014; 100, 176–181.Google Scholar
57. Dearden, L, Ozanne, SE. The road between early growth and obesity: new twists and turns. Am J Clin Nutr. 2014; 100, 6–7.CrossRefGoogle ScholarPubMed
58. Campbell, S, Thoms, A. Ultrasound measurement of the fetal head to abdomen circumference ratio in the assessment of growth retardation. Int J Gynaecol Obstet. 1977; 84, ;165–174.Google Scholar
59. Nardozza, LMM, Júnior, EA, Barbosa, MM, et al. Fetal growth restriction: current knowledge to the general Obs/Gyn. Arch Gynecol Obstet. 2012; 286, 1–13.Google Scholar
60. Weinberg, CR. Invited commentary: Barker meets Simpson. Am J Epidemiol. 2005; 161, 33–35.CrossRefGoogle ScholarPubMed
61. Lin, C-C, Santolaya-Forgas, J. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol. 1998; 92, 1044–1055.Google ScholarPubMed
62. Dashe, JS, McIntire, DD, Lucas, MJ, Leveno, KJ. Effects of symmetric and asymmetric fetal growth on pregnancy outcomes. Obstet Gynecol. 2000; 96, 321–327.Google Scholar
63. Lin, C-C, Su, S-J, River, LP. Comparison of associated high-risk factors and perinatal outcome between symmetric and asymmetric fetal intrauterine growth retardation. Am J Obstet Gynecol. 1991; 164(6 Pt 1), 1535–1542.Google Scholar
64. Lampl, M, Kusanovic, JP, Erez, O, et al. Early rapid growth, early birth: accelerated fetal growth and spontaneous late preterm birth. Am J Hum Biol. 2009; 21, 141–150.Google Scholar
65. Lampl, M, Kusanovic, JP, Erez, O, et al. Growth perturbations in a phenotype with rapid fetal growth preceding preterm labor and term birth. Am J Hum Biol. 2009; 21, 782–792.Google Scholar
66. Prader, A, Tanner, JM, von Harnack, GA. Catch-up growth following illness or starvation: an example of developmental canalization in man. J Pediatr. 1963; 62, 646–659.Google Scholar
67. Prader, A. Catch-up growth. Postgrad Med J. 1978; 54(Suppl. 1), 133–146.Google Scholar
68. Borghi, E, de Onis, M, Garza, C, et al. Construction of the World Health Organization child growth standards: selection of methods for attained growth curves. Stats Med. 2006; 25, 247–265.Google Scholar
69. Lampl, M. Limitations of growth chart curves in terms of individual growth biology. In Handbook of Growth and Growth Monitoring in Health and Disease (ed. Preedy V), 2011; pp. 3013–3028. Springer-Verlag: New York.Google Scholar
70. Lampl, M, Veldhuis, JD, Johnson, ML. Saltation and stasis: a model of human growth. Science. 1992; 258, 801–803.Google Scholar
71. Hermanussen, M. The analysis of short-term growth. Horm Res. 1998; 49, 53–64.Google Scholar
72. Lampl, M, Johnson, ML. Infant head circumference growth is saltatory and coupled to length growth. Early Hum Dev. 2011; 87, 361–368.Google Scholar
73. Caino, S, Kelmansky, D, Adamo, P, Lejarraga, H. Short-term growth in head circumference and its relationship with supine length in healthy infants. Ann Hum Biol. 2011; 37, 108–116.Google Scholar
74. Johnson, ML, Lampl, M. Methods for the evaluation of saltatory growth in infants. Met Neurosci. 1995; 28, 364–387.Google Scholar
75. Lampl, M. Perspectives on modelling human growth: mathematical models and growth biology. Ann Hum Biol. 2012; 39, 342–352.Google Scholar
76. World Health Organization. Multicentre Growth Reference Study Group. Child growth standards. Boys percentiles for length/height-for-age: birth to 6 months. Retrieved from http://www.who.int/childgrowth/standards/chts_lhfa_boys_p/en/ Google Scholar
77. Noonan, KJ, Farnum, CE, Leiferman, EM, et al. Growing pains: are they due to increased growth during recumbency as documented in a lamb model? J Pediatr Orthop. 2004; 24, 726–731.Google Scholar
78. Goldsmith, MI, Fisher, S, Waterman, R, Johnson, SL. Saltatory control of isometric growth in the zebrafish caudal fin is disrupted in long fin and Rapunzel mutants. Dev Biol. 2003; 15, 303–317.Google Scholar
79. Lampl, M, Thompson, AL. Growth chart curves do not describe individual growth biology. Am J Hum Biol. 2007; 19, 643–653.CrossRefGoogle Scholar
80. Mei, Z, Grummer-Strawn, LM, Thompson, D, Dietz, WH. Shifts in percentiles of growth during early childhood: analysis of longitudinal data from the California Child Health and Development Study. Pediatrics. 2004; 113, e617–e627.Google Scholar
81. Taveras, EM, Rifas-Shiman, SL, Sherry, B, et al. Crossing growth percentiles in infancy and risk of obesity in childhood. Arch Pediatr Adolesc Med. 2011; 165, 993–998.Google Scholar
82. Bohman, VR. Compensatory growth of beef cattle: the effect of hay maturity. J Anim Sci. 1955; 14, 249–255.Google Scholar
83. Williams, JP. Catch-up growth. J Embryol Exp Morphol. 1981; 65(Suppl.), 89–101.Google Scholar
84. Forsén, T, Osmond, C, Eriksson, JG, Barker, DJP. Growth of girls who later develop coronary heart disease. Heart. 2004; 90, 20–24.Google Scholar
85. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.Google Scholar
86. Raubenheimer, D, Simpson, SJ, Tait, AH. Match and mismatch: conservation physiology, nutritional ecology and the timescales of biological adaptation. Phil Trans R Soc B. 2012; 367, 1628–1646.Google Scholar
87. Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20, 527–533.Google Scholar
88. Halfon, N, Hochstein, M. Life course health development: an integrated framework for developing health, policy, and research. Milbank Q. 2002; 80, 433–479.Google Scholar
89. Fleming, TP, Velazquez, MA, Eckert, JJ. Embryos, DOHaD and David Barker. J Dev Orig Health Dis. 2015 [Epub ahead of print].Google Scholar
90. Thornburg, KL, Challis, JR. How to build a healthy heart from scratch. Adv Exp Med Biol. 2014; 814, 205–216.Google Scholar
91. Phillips, DI, Barker, DJ. Association between low birthweight and high resting pulse in adult life: is the sympathetic nervous system involved in programming the insulin resistance syndrome? Diabet Med. 1997; 14, 673–677.Google Scholar
92. Danielson, L, McMillen, IC, Dyer, JL, Morrison, JL. Restriction of placental growth results in greater hypotensive response to a-adrenergic blockade in fetal sheep during late gestation. J Physiol. 2005; 563, 611–620.Google Scholar
93. Jirtle, RL. The Agouti mouse: a biosensor for environmental epigenomics studies investigating the developmental origins of health and disease. Epigenomics. 2014; 6, 447–450.Google Scholar
94. Eveleth, P, Tanner, J. Worldwide Variation in Human Growth. 1990. Cambridge University Press: Cambridge.Google Scholar
95. Kierans, WJ, Joseph, KS, Luo, ZC, et al. Does one size fit all? The case for ethnic-specific standards of fetal growth. BMC Preg Childbirth. 2008; 8, 1–9.Google Scholar
96. Lampl, M, Lee, W, Koo, W, et al. Ethnic differences in the accumulation of fat and lean mass in late gestation. Am J Hum Biol. 2012; 24, 640–647.Google Scholar
97. Painter, RC, Osmond, C, Gluckman, PD, et al. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG. 2008; 115, 1243–1249.Google Scholar
98. Gardosi, J. Customized growth curves. Clin Obstet Gynecol. 1997; 40, 715–722.Google Scholar
99. Papageorghiou, AT, Ohuma, EO, Altman, DG, et al. International standards for fetal growth based on serial ultrasound measurements: the Fetal Growth Longitudinal Study of the INTERGROWTH-21st Project. Lancet Diabetes Endocrinol. 2014; 384, 869–879.Google Scholar
100. International Fetal and Newborn Growth Consortium. The International Fetal and Newborn Growth Standards for the 21st Century (INTERGROWTH-21st) Study Protocol, 2008. Retrieved 15 May 2015 from http://www.intergrowth21.org.uk Google Scholar
101. Lampl, M, Gotsch, F, Kusanovic, J, et al. Sex differences in fetal growth responses to maternal height and weight. Am J Hum Biol. 2010; 22, 431–443.Google Scholar
102. Steer, PJ. Possible differences in fetal size by racial origin. Comment on: the likeness of fetal growth and newborn size across non-isolated populations in the INTERGROWTH-21st Project: the fetal growth longitudinal study and newborn cross-sectional study. Lancet Diabetes Endocrinol. 2014; 2, 766–767.Google Scholar
103. Gardosi, J. Fetal growth and ethnic variation. Comment on: the likeness of fetal growth and newborn size across non-isolated populations in the INTERGROWTH-21st Project: the fetal growth longitudinal study and newborn cross-sectional study. Lancet Diabetes Endocrinol. 2014; 2, 773–774.CrossRefGoogle Scholar
104. Albert, PS, Grantz, KL. Fetal growth and ethnic variation. Comment on: the likeness of fetal growth and newborn size across non-isolated populations in the INTERGROWTH-21st Project: the fetal growth longitudinal study and newborn cross-sectional study. Lancet Diabetes Endocrinol. 2014; 2, 773–774.Google Scholar
105. Yajnik, CS, Fall, CH, Coyaji, KJ, et al. Neonatal anthropometry: the thin-fat Indian baby. The pune maternal nutrition study. Int J Obes Relat Metab Disord. 2003; 27, 173–180.Google Scholar
106. Johnson, W, Vazir, S, Renandez-Rao, S, et al. Using the WHO 2012 child growth standard to assess the growth and nutritional status of rural south Indian infants. Ann Hum Biol. 2012; 39, 91–101.Google Scholar
107. Giussani, DA, Phillips, PS, Anstee, S, Barker, DJP. Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr Res. 2001; 49, 490–494.Google Scholar
108. Bigham, AW, Lee, FS. Human high-altitude adaptation: forward genetics meets the HIF pathway. Genes Dev. 2014; 28, 2189–2204.CrossRefGoogle ScholarPubMed
109. Johnson, NB, Hayes, LD, Brown, K, Hoo, EC, Ethier, KA, Centers for Disease Control and Prevention. CDC National Health Report: leading causes of morbidity and mortality and associated behavioral risk and protective factors—United States, 2005–2013. MMWR Surveill Summ. 2014; 63, 3–27.Google Scholar
110. Paneth, N, Susser, M. Early origin of coronary heart disease (the “Barker hypothesis”). BMJ. 1995; 310, 411–412.Google Scholar
111. Susser, M, Levin, B. Ordeals for the fetal programming hypothesis. BMJ. 1999; 318, 885–886.Google Scholar
112. Barker, DJP, Barker, M, Fleming, T, Lampl, M. Developmental biology: support mothers to secure future public health. Nature. 2013; 504, 209–211.Google Scholar