Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Maternal and pediatric nutrition

Slow early growers have more muscle in relation to adult activity: evidence from Cebu, Philippines

European Journal of Clinical Nutrition volume 69, pages 1350–1355 (2015)Cite this article

Subjects

Abstract

Background/Objectives:

Adult skeletal muscle mass (SMM) protects against type 2 diabetes, but little is known about its developmental antecedents. We examined whether pace of early weight gain predicted adult SMM in a birth cohort from Cebu City, Philippines. In addition, we examined whether increases in SMM associated with adult muscle-building exercise varied according to the early growth.

Subjects/Methods:

Data came from 1472 participants of the Cebu Longitudinal Health and Nutrition Survey. Weight was measured at birth and at 6-month intervals through the age of 24 months. Adult SMM was estimated from anthropometric measurements when participants were 20–22-years old. Interviews provided the information on adult exercise/lifestyle habits.

Results:

SMM (mean±s.d.) was 20.8±3.9 kg (men) and 13.6±3.4 kg (women). Faster early weight gain predicted a higher adult SMM. After adjustment for height and lifestyle factors, strongest associations with SMM were found for 6–12 months growth in men (β=0.17, P=0.001) and for birth weight in women (β=0.14, P=0.001). Individuals who had grown slowly displayed greater SMM in association with adult weightlifting, basketball playing and physically demanding forms of employment (men) or household chores (women).

Conclusions:

These results suggest heightened sensitivity of activity-induced muscle hypertrophy among the adults who were born light or who gained weight slowly as infants. Future research should test this finding by comparing responses of muscle mass to an intervention in slow vs fast early growers. Findings suggest that adults who display a reduced SMM following suboptimal early growth may be good candidates for new anti-diabetes interventions that promote muscle-building activities.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  1. DeFronzo RA, Tripathy D . Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 2009; 32: S157–S163.

    Article  CAS  Google Scholar 

  2. Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S et al. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci USA 2007; 104: 12587–12594.

    Article  CAS  Google Scholar 

  3. Srikanthan P, Karlamangla AS . Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the Third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab 2011; 96: 2898–2903.

    Article  CAS  Google Scholar 

  4. Srikanthan P, Hevener AL, Karlamangla AS . Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One 2010; 5: e10805.

    Article  Google Scholar 

  5. Atlantis E, Martin SA, Haren MT, Taylor AW, Wittert GA . Inverse associations between muscle mass, strength, and the metabolic syndrome. Metabolism 2009; 58: 1013–1022.

    Article  CAS  Google Scholar 

  6. Bakker LEH, Sleddering MA, Schoones JW, Meinders AE, Jazet IM . Mechanisms in endocrinology: pathogenesis of type 2 diabetes in South Asians. Eur J Endocrinol 2013; 169: R99–R114.

    Article  CAS  Google Scholar 

  7. Chan JC, Malik V, Jia W, Kadowaki R, Yajnik CS, Yoon KH et al. Diabetes in Asia: epidemiology, risk factors, and pathophysiology. J Am Med Assoc 2009; 301: 2129–2140.

    Article  CAS  Google Scholar 

  8. Yajnik CS . Early life origins of insulin resistance and type 2 diabetes in india and other Asian countries. J Nutr 2004; 134: 205–210.

    Article  CAS  Google Scholar 

  9. Yliharsila H, Kajantie E, Osmond C, Forsen T, Barker DJP, Eriksson JG . Birth size, adult body composition and muscle strength later in life. Int J Obes 2007; 31: 1392–1399.

    Article  CAS  Google Scholar 

  10. Kensara OA, Wooton SA, Phillips DI, Patel M, Jackson AA, Elia M . Fetal programming of body composition: relation between birth weight and body composition measure with dual-energy X-ray absorptiometry and anthropometric methods in older Englishmen. Am J Clin Nutr 2005; 82: 980–987.

    Article  CAS  Google Scholar 

  11. Li H, Stein AD, Barnhart HX, Ramakrishnan U, Martorell R . Associations between prenatal and postnatal growth and adult body size and composition. Am J Clin Nutr 2003; 77: 1498–1505.

    Article  CAS  Google Scholar 

  12. Loos RJF, Beunen G, Fagard R, Derom C, Vlietinck R . Birth weight and body composition in young adult men—a prospective twin study. Int J Obes 2001; 25: 1537–1545.

    Article  CAS  Google Scholar 

  13. Loos RJF, Beunen G, Fagard R, Derom C, Vlietinck R . Birth weight and body composition in young women: a prospective twin study. Am J Clin Nutr 2002; 75: 676–682.

    Article  CAS  Google Scholar 

  14. Weyer C, Pratley RE, Lindsay RS, Tataranni PA . Relationship between birth weight and body composition, energy metabolism, and sympathetic nervous system activity later in life. Obes Res 2000; 8: 559–565.

    Article  CAS  Google Scholar 

  15. Inskip HM, Godfrey KM, Martin HJ, Simmonds SJ, Cooper C, Aihie Sayer A . Size at birth and its relation to muscle strength in young adult women. J Intern Med 2007; 262: 368–374.

    Article  CAS  Google Scholar 

  16. Kuh D, Bassey J, Hardy R, Sayer AA, Wadsworth M, Cooper C . Birth weight, childhood size, and muscle strength in adult life: evidence from a birth cohort study. Am J Epidemiol 2002; 156: 627–633.

    Article  Google Scholar 

  17. Kahn HS, Narayan KM, Williamson DF, Valez R . Relation of birth weight to lean and fat thigh tissue in young men. Int J Obes 2000; 24: 667–672.

    Article  CAS  Google Scholar 

  18. Euser AM, Finken MJ, Keijzer-Veen MF, Hille ET, Wit JM, Dekker FW . Associations between prenatal and infancy weight gain and BMI, fat mass, and fat distribution in young adulthood: a prospective cohort study in males and females born very preterm. Am J Clin Nutr 2005; 81: 480–487.

    CAS  PubMed  Google Scholar 

  19. Sayer AA, Syddall HE, Dennison EM, Gilbody HJ, Duggleby SL, Cooper C et al. Birth weight, weight at 1 y of age, and body composition in older men: findings form the Hertfordshire Cohort Study. Am J Clin Nutr 2004; 80: 199–203.

    Article  CAS  Google Scholar 

  20. Sachdev HS, Fall CH, Osmond C, Lakshmy R, Biswas SKD, Leary SD et al. 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.

    Article  CAS  Google Scholar 

  21. Kuzawa CW, McDade TW, Adair LS, Lee N . Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males. Proc Natl Acad Sci USA 2010; 107: 16800–16805.

    Article  CAS  Google Scholar 

  22. Kuzawa CW, Hallal PC, Adair LS, Bhargava SK, Fall CH, Lee CH et al. Birth weight, postnatal weight gain and adult body composition in five low and middle income countries. Am J Hum Biol 2012; 24: 5–13.

    Article  Google Scholar 

  23. Siebel AL, Carey AL, Kingwell BA . Can exercise training rescue the adverse cardiometabolic effects of low birth weight and prematurity? Proc Aust Physiol Soc 2012; 43: 101–116.

    Google Scholar 

  24. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J, Felber JP . The effect of insulin on the disposal of intravenous glucose, results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 1981; 30: 1000–1007.

    Article  CAS  Google Scholar 

  25. Grontved A, Rimm EB, Willett CW, Andersen LB, Hu FB . A prospective study of weight training and risk of type 2 diabetes mellitus in men. Arch Intern Med 2012; 172: 1306–1312.

    Article  Google Scholar 

  26. Croymans DM, Paparisto E, Lee MM, Brandt N, Le BK, Lohan D et al. Resistance training improves indices of muscle insulin sensitivity and β-cell function in overweight/obese, sedentary young men. J Appl Physiol 2013; 115: 1245–1253.

    Article  CAS  Google Scholar 

  27. Colin Bell A, Adair LS, Popkin BM . Ethnic differences in the association between body mass index and hypertension. Am J Epidemiol 2002; 155: 346–353.

    Article  CAS  Google Scholar 

  28. Adair LS, Popkin BM, Akin JS, Guilkey DK, Gultiano S, Borja J et al. Cohort profile: the Cebu longitudinal health and nutrition survey. Int J Epidemiol 2011; 40: 619–625.

    Article  Google Scholar 

  29. Ballard J, Novak H, Driver M . A simplified score for assessment of fetal maturation in newly born infants. J Pediatr 1979; 95: 769–774.

    Article  CAS  Google Scholar 

  30. Lohman TG, Roche AF, Martorell R . Anthropometric Standardization Reference Manual. Human Kinetics Books: Champaign, IL, USA, 1988.

    Google Scholar 

  31. Heymsfield SB, McManus C, Smith J, Stevens V, Nixon DW . Anthropometric measures of muscle mass: revised equations for calculating bone-free arm muscle area. Am J Clin Nutr 1982; 36: 680–690.

    Article  CAS  Google Scholar 

  32. Perez TLL, Borja JB, Bas IN, Attrition in the Cebu Longitudinal Health and Nutrition Survey. USC-Office of Population Studies Foundation, Inc., University of San Carlos: Cebu City, Philippines, 2014. OPS Report Series no. 1.

  33. Adair LS, Martorell R, Stein AD, Hallal PD, Sachdev HS, Prabhakaran D et al. Size at birth, weight gain in infancy and childhood, and adult blood pressure in 5 low- and middle-income-country cohorts: when does weight gain matter? Am J Clin Nutr 2009; 89: 1983–1392.

    Article  Google Scholar 

  34. Norris SA, Osmond C, Gigante D, Kuzawa CW, Ramakrishnan L, Lee NR et al. Size at birth, weight gain in infancy and childhood, and adult diabetes risk in five low- or middle-income country birth cohorts. Diabetes Care 2012; 35: 72–79.

    Article  Google Scholar 

  35. Wells JCK, Hallal PC, Wright A, Singhal A, Victora CG . Fetal, infant and childhood growth: relationships with body composition in Brazilian boys aged 9 years. Int J Obes 2005; 29: 1192–1198.

    Article  CAS  Google Scholar 

  36. Gettler LT, Agustin SS, Kuzawa CW . Testosterone, physical activity, and somatic outcomes among Filipino males. Am J Phys Anth 2010; 142: 590–599.

    Article  Google Scholar 

  37. Ivey FM, Roth SM, Ferrel RE, Tracy BL, Lemmer JT, Hurlbut DE et al. Effects of age, gender, and myostatin genotype on the hypertrophic response to heavy resistance strength training. J Gerontol 2000; 55: M641–M648.

    Article  CAS  Google Scholar 

  38. Clarkson PM, Devaney JM, Gordish-Dressman H, Thompson PD, Hubal MJ, Urso M et al. ACTN3 genotype is associated with increases in muscle strength and response to resistance training in women. J Appl Physiol 2005; 99: 564–569.

    Article  CAS  Google Scholar 

  39. Pescatello LS, Kostek MA, Gordish-Dressman H, Thompson PD, Seip RL, Price TB et al. ACE ID genotype and the muscle strength and size response to unilateral resistance training. Med Sci Sports Exerc 2005; 38: 1074–1081.

    Article  Google Scholar 

  40. Deschenes MR, Kraemer WJ . Performance and physiologic adaptations to resistance training. Am J Phys Med Rehabil 2002; 81: S3–S16.

    Article  Google Scholar 

  41. Wernbom M, Augustsson J, Thomee R . The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Med 2007; 37: 225–264.

    Article  Google Scholar 

  42. Tremblay MS, Copeland JL, Van Helder W . Effect of training status and exercise mode on endogenous steroid hormones in men. J Appl Physiol 2003; 96: 531–539.

    Article  Google Scholar 

  43. Kraemer WJ, Hakkinen K, Newton RU, Nindl BC, Vlok JS, McCormick M et al. Effects of heavy- resistance training on hormonal response patterns in younger vs older men. J Appl Physiol 1999; 87: 982–992.

    Article  CAS  Google Scholar 

  44. Nindl BC, Kraemer WJ, Gotshalk LA, Marx JO, Volek JS, Bush FM et al. Testosterone responses after resistance exercise in women: influence of regional fat distribution. Int J Sport Nutr Exerc Metab 2001; 11: 451–465.

    Article  CAS  Google Scholar 

  45. Nindl BC, Kraemer WJ, Hymer WC . Immunofunctional vs immunoreactive growth hormone responses after resistance exercise in men and women. Growth Horm IGF Res 2000; 10: 99–103.

    Article  CAS  Google Scholar 

  46. McCall GE, Byrnes WC, Fleck SJ, Dickenson A, Kraemer WJ . Acute and chronic hormonal responses to resistance training designed to promote muscle hypertrophy. Can J Appl Physiol 1999; 24: 96–107.

    Article  CAS  Google Scholar 

  47. Kuzawa CW, McDade TW, Adair LS, Lee N . Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males. PNAS 107: 16800–16805.

  48. Eriksson JG, Yliharsila H, Forsen T, Osmond C, Barker DJP . Exercise protects against glucose intolerance in individuals with a small body size at birth. Prev Med 2004; 39: 164–167.

    Article  CAS  Google Scholar 

  49. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L et al. Maternal and child undernutrition: consequences for adult health and human capital. Lancet 2008; 371: 340–357.

    Article  CAS  Google Scholar 

  50. Gallagher D, Visser M, De Meersman RE, Sepulveda D, Baumgartner RN, Pierson RN et al. Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol 1997; 83: 229–239.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the US National Institute of Child Health and Human Development (1R01 HD054501). We thank Lorna Perez, who provided information on sample attrition, and the many researchers at the Office of Population Studies who were instrumental in study design and data collection. We also thank the study participants who generously provided their time. This research was supported by the US National Institute of Child Health and Human Development, grant # 1R01 HD054501.

Author information

Authors and Affiliations

  1. Department of Anthropology, Northwestern University, Evanston, IL, USA

    M Workman, T W McDade & C W Kuzawa

  2. Cells to Society, Center on Social Disparities and Health at the Institute for Policy Research, Northwestern University, Evanston, IL, USA

    T W McDade & C W Kuzawa

  3. Department of Nutrition, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    L S Adair

  4. Carolina Population Center, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    L S Adair

Authors
  1. M Workman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T W McDade
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L S Adair
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C W Kuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M Workman.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies this paper on European Journal of Clinical Nutrition website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Workman, M., McDade, T., Adair, L. et al. Slow early growers have more muscle in relation to adult activity: evidence from Cebu, Philippines. Eur J Clin Nutr 69, 1350–1355 (2015). https://doi.org/10.1038/ejcn.2015.18

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2015.18

Search

Advanced search

Quick links