Skip to main content
×
×
Home

Auxological perspectives on ‘growth’ in DOHaD

  • M. Lampl (a1) (a2), A. Mummert (a1) (a2) and M. Schoen (a1)
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.

Copyright
Corresponding author
*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)
References
Hide All
1. Tanner, JM. Catch-up growth in man. Br Med Bull. 1981; 37, 233238.
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, 140161.
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, 311335.
4. Gregory, PW. The Early Embryology of the Rabbit, 1930. Carnegie Institution of Washington, Washington DC.
5. McLaren, A, Michie, D. Congenital Runts. In Ciba Foundation Symposium - Congenital Malformations (eds. Wolstenholme GEW, O’Connor CM), 1960; pp. 178198. John Wiley & Sons, Ltd., Chichester, UK.
6. Cawley, R, McKeown, T, Record, R. Parental stature and birth weight. Am J Hum Genet. 1954; 6, 448456.
7. McKeown, T, Gibson, J. Observations on all births (23,970) in Birmingham. II. Birth weight. Brit J Soc Med. 1951; 5, 98112.
8. McKeown, T, Record, RG. Observations on fetal growth in multiple pregnancy in man. J Endocrinol. 1952; 8, 386401.
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, 418426.
10. McKeown, T, Record, R. Influence of pre-natal environment on correlation between birth weight and parental height. Am J Hum Genet. 1954; 6, 456463.
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, 259264.
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, 2428.
13. Gruenwald, P. Chronic fetal distress and placental insufficiency (Part 3 of 3). Neonatology. 1963; 5, 249265.
14. Ounsted, M. Maternal constraint of foetal growth in man. Dev Med Child Neurol. 1965; 7, 479491.
15. Ounsted, M, Ounsted, C. Maternal regulation of intra-uterine growth. Nature. 1966; 212, 995997.
16. Wigglesworth, J. Foetal growth retardation. Br Med Bull. 1966; 22, 1315.
17. Philip, A. The evolution of neonatalogy. Pediatr Res. 2005; 58, 799815.
18. Barker, DJP, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986; 327, 10771081.
19. Buck, C, Simpson, H. Infant diarrhoea and subsequent mortality from heart disease and cancer. J Epidemiol Community Health. 1982; 36, 2730.
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, 9195.
21. Ben-Shlomo, Y, Smith, GD. Deprivation in infancy or in adult life: which is more important for mortality risk? Lancet. 1991; 337, 530534.
22. McEwen, B, Stellar, E. Stress and the individual. Mechanisms leading to disease. Arch Intern Med. 1993; 153, 20932101.
23. Barker, D, Osmond, C. Death rates from stroke in England and Wales predicted from past maternal mortality. BMJ. 1987; 295, 8386.
24. Cawley, R, McKeown, T, Record, R. Influence of pre-natal environment on post-natal growth. Br J Prev Soc Med. 1954; 8, 6669.
25. Thomson, J. Observations on weight gain in infants. Arch Dis Child. 1955; 30, 322327.
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, 225230.
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, 631635.
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, 427431.
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, 564567.
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, 176182.
31. Gennser, G, Rymark, P, Isbert, P. Low birth weight and risk of high blood pressure in adulthood. BMJ. 1988; 296, 14981500.
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, 237240.
33. Barker, DJ, Osmond, C, Pannett, B. Why Londoners have low death rates from ischaemic heart disease and stroke. BMJ. 1992; 305, 15511554.
34. Cameron, N. The Measurement of Human Growth. 1984. Croom Helm: London.
35. Tanner, JM. Fetus into Man: Physical Growth from Conception to Maturity. 1990. Harvard University Press: Cambridge, MA.
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), S60S66.
37. Lampl, M, Mummert, A. Historical approaches to human growth studies limit the present understanding of growth biology. Ann Nutr Metab. 2014; 65, 114120.
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, 14031407.
39. Godfrey, KM, Barker, DJ. Fetal programming and adult health. Public Health Nutr. 2001; 4, 611624.
40. Widdowson, EM, McCance, RA. A review: new thoughts on growth. Pediatr Res. 1975; 9, 154156.
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, 137213.
42. Bornstein, MH. Sensitive periods in development: structural characteristics and causal interpretations. Psychol Bull. 1989; 105, 179197.
43. Spalding, DA. Instinct with original observations on young animals. Macmillan’s Magazine. 1873; 27, 282293.
44. Hanson, MA, Gluckman, PD. Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev. 2014; 94, 10271076.
45. Dorner, G. Perinatal hormone levels and brain organization. In Anatomical Neuroendocrinology (eds. Stumpf WE, Grant LD), 1975; pp 245252. Karger: Basel.
46. Hertzman, C. Putting the concept of biological embedding in historical perspective. Proc Natl Acad Sci U S A. 2012; 109(Suppl. 2), 1716017167.
47. Koplan, JP, Liverman, CT, Kraak, VI. Preventing childhood obesity: health in the balance: executive summary. J Am Diet Assoc. 2005; 105, 131138.
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, 132139.
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, 111.
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, 10361043.
51. World Health Organization. The ICD-10 Classification of Mental and Behavioural Disorders: Clinical Descriptions and Diagnostic Guidelines. 1992. World Health Organization: Geneva.
52. Butler, NR, Bonham, DG. Perinatal Mortality. The First Report of the 1958 British Perinatal Mortality Survey. 1963. Livingstone: Edinburgh.
53. Altman, DG, Hytten, FE. Intrauterine growth retardation: let’s be clear about it. Br J Obstet Gynecol. 1989; 96, 2732.
54. Royston, P, Altman, DG, Sauerbrie, W. Dichotomizing continuous predictors in multiple regression: always a bad idea. Stat Med. 2006; 25, 127141.
55. Wilcox, AJ. Intrauterine growth retardation: beyond birthweight criteria. Early Hum Dev. 1983; 8, 189193.
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, 176181.
57. Dearden, L, Ozanne, SE. The road between early growth and obesity: new twists and turns. Am J Clin Nutr. 2014; 100, 67.
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, ;165174.
59. Nardozza, LMM, Júnior, EA, Barbosa, MM, et al. Fetal growth restriction: current knowledge to the general Obs/Gyn. Arch Gynecol Obstet. 2012; 286, 113.
60. Weinberg, CR. Invited commentary: Barker meets Simpson. Am J Epidemiol. 2005; 161, 3335.
61. Lin, C-C, Santolaya-Forgas, J. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol. 1998; 92, 10441055.
62. Dashe, JS, McIntire, DD, Lucas, MJ, Leveno, KJ. Effects of symmetric and asymmetric fetal growth on pregnancy outcomes. Obstet Gynecol. 2000; 96, 321327.
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), 15351542.
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, 141150.
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, 782792.
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, 646659.
67. Prader, A. Catch-up growth. Postgrad Med J. 1978; 54(Suppl. 1), 133146.
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, 247265.
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. 30133028. Springer-Verlag: New York.
70. Lampl, M, Veldhuis, JD, Johnson, ML. Saltation and stasis: a model of human growth. Science. 1992; 258, 801803.
71. Hermanussen, M. The analysis of short-term growth. Horm Res. 1998; 49, 5364.
72. Lampl, M, Johnson, ML. Infant head circumference growth is saltatory and coupled to length growth. Early Hum Dev. 2011; 87, 361368.
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, 108116.
74. Johnson, ML, Lampl, M. Methods for the evaluation of saltatory growth in infants. Met Neurosci. 1995; 28, 364387.
75. Lampl, M. Perspectives on modelling human growth: mathematical models and growth biology. Ann Hum Biol. 2012; 39, 342352.
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/
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, 726731.
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, 303317.
79. Lampl, M, Thompson, AL. Growth chart curves do not describe individual growth biology. Am J Hum Biol. 2007; 19, 643653.
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, e617e627.
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, 993998.
82. Bohman, VR. Compensatory growth of beef cattle: the effect of hay maturity. J Anim Sci. 1955; 14, 249255.
83. Williams, JP. Catch-up growth. J Embryol Exp Morphol. 1981; 65(Suppl.), 89101.
84. Forsén, T, Osmond, C, Eriksson, JG, Barker, DJP. Growth of girls who later develop coronary heart disease. Heart. 2004; 90, 2024.
85. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595601.
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, 16281646.
87. Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20, 527533.
88. Halfon, N, Hochstein, M. Life course health development: an integrated framework for developing health, policy, and research. Milbank Q. 2002; 80, 433479.
89. Fleming, TP, Velazquez, MA, Eckert, JJ. Embryos, DOHaD and David Barker. J Dev Orig Health Dis. 2015 [Epub ahead of print].
90. Thornburg, KL, Challis, JR. How to build a healthy heart from scratch. Adv Exp Med Biol. 2014; 814, 205216.
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, 673677.
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, 611620.
93. Jirtle, RL. The Agouti mouse: a biosensor for environmental epigenomics studies investigating the developmental origins of health and disease. Epigenomics. 2014; 6, 447450.
94. Eveleth, P, Tanner, J. Worldwide Variation in Human Growth. 1990. Cambridge University Press: Cambridge.
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, 19.
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, 640647.
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, 12431249.
98. Gardosi, J. Customized growth curves. Clin Obstet Gynecol. 1997; 40, 715722.
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, 869879.
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
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, 431443.
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, 766767.
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, 773774.
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, 773774.
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, 173180.
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, 91101.
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, 490494.
108. Bigham, AW, Lee, FS. Human high-altitude adaptation: forward genetics meets the HIF pathway. Genes Dev. 2014; 28, 21892204.
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, 327.
110. Paneth, N, Susser, M. Early origin of coronary heart disease (the “Barker hypothesis”). BMJ. 1995; 310, 411412.
111. Susser, M, Levin, B. Ordeals for the fetal programming hypothesis. BMJ. 1999; 318, 885886.
112. Barker, DJP, Barker, M, Fleming, T, Lampl, M. Developmental biology: support mothers to secure future public health. Nature. 2013; 504, 209211.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of Developmental Origins of Health and Disease
  • ISSN: 2040-1744
  • EISSN: 2040-1752
  • URL: /core/journals/journal-of-developmental-origins-of-health-and-disease
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed