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Exercise during pregnancy and its impact on mothers and offspring in humans and mice

Part of: Advancing the DOHaD Agenda in Africa

Published online by Cambridge University Press:  07 August 2017

N. Ferrari ,
I. Bae-Gartz ,
C. Bauer ,
R. Janoschek ,
I. Koxholt ,
E. Mahabir ,
S. Appel ,
M. A. Alejandre Alcazar ,
N. Grossmann  and
C. Vohlen
...Show all authors
N. Ferrari*
Affiliation:
Cologne Center for Prevention in Childhood and Youth, Heart Center Cologne, University Hospital of Cologne, Cologne, Germany Department for Physical Activity in Public Health, Institute of Movement and Neurosciences, German Sport University Cologne, Cologne, Germany
I. Bae-Gartz
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
C. Bauer
Affiliation:
Department for Physical Activity in Public Health, Institute of Movement and Neurosciences, German Sport University Cologne, Cologne, Germany
R. Janoschek
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
I. Koxholt
Affiliation:
Comparative Medicine, Center for Molecular Medicine, University of Cologne, Cologne, Germany Cologne Center for Musculoskeletal Biomechanics, Medical Faculty, University Hospital of Cologne, Cologne, Germany
E. Mahabir
Affiliation:
Comparative Medicine, Center for Molecular Medicine, University of Cologne, Cologne, Germany Cologne Center for Musculoskeletal Biomechanics, Medical Faculty, University Hospital of Cologne, Cologne, Germany
S. Appel
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
M. A. Alejandre Alcazar
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
N. Grossmann
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
C. Vohlen
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
K. Brockmeier
Affiliation:
Cologne Center for Prevention in Childhood and Youth, Heart Center Cologne, University Hospital of Cologne, Cologne, Germany Department of Pediatric Cardiology, Heart Center Cologne, University Hospital of Cologne, Cologne, Germany
J. Dötsch
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
E. Hucklenbruch-Rother
Affiliation:
Department of Pediatrics and Adolescent Medicine, University Hospital of Cologne, Cologne, Germany
C. Graf
Affiliation:
Cologne Center for Prevention in Childhood and Youth, Heart Center Cologne, University Hospital of Cologne, Cologne, Germany Department for Physical Activity in Public Health, Institute of Movement and Neurosciences, German Sport University Cologne, Cologne, Germany
*
*Address for correspondence: N. Ferrari, Cologne Center for Prevention in Childhood and Youth, Heart Center Cologne, University Hospital of Cologne, Kerpener Str. 62, 50937 Cologne, Germany. (Email nina.ferrari@uk-koeln.de)
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Abstract

Exercise during pregnancy has beneficial effects on maternal and offspring’s health in humans and mice. The underlying mechanisms remain unclear. This comparative study aimed to determine the long-term effects of an exercise program on metabolism, weight gain, body composition and changes in hormones [insulin, leptin, brain-derived neurotrophic factor (BDNF)]. Pregnant women (n=34) and mouse dams (n=44) were subjected to an exercise program compared with matched controls (period I). Follow-up in the offspring was performed over 6 months in humans, corresponding to postnatal day (P) 21 in mice (period II). Half of the mouse offspring was challenged with a high-fat diet (HFD) for 6 weeks between P70 and P112 (period III). In period I, exercise during pregnancy led to 6% lower fat content, 40% lower leptin levels and an increase of 50% BDNF levels in humans compared with controls, which was not observed in mice. After period II in humans and mice, offspring body weight did not differ from that of the controls. Further differences were observed in period III. Offspring of exercising mouse dams had significantly lower fat mass and leptin levels compared with controls. In addition, at P112, BDNF levels in offspring were significantly higher from exercising mothers while this effect was completely blunted by HFD feeding. In this study, we found comparable effects on maternal and offspring’s weight gain in humans and mice but different effects in insulin, leptin and BDNF. The long-term potential protective effects of exercise on biomarkers should be examined in human studies.

Keywords

brain-derived neurotrophic factorcomparative studyhigh-fat feedingleptinphysical activity
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 1: Themed Issue: DOHaD AFRICA , February 2018 , pp. 63 - 76
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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Footnotes

†

Nina Ferrari and Inga Bae-Gartz contributed equally to this work.

References

1. Riley, L, Guthold, R, Cowan, M, et al. The World Health Organization STEPwise approach to noncommunicable disease risk-factor surveillance: methods, challenges, and opportunities. Am J Public Health. 2016; 106, 74–78.Google Scholar
2. Hanson, MA, Gluckman, PD. Developmental origins of health and disease: moving from biological concepts to interventions and policy. Int J Gynaecol Obstet. 2011; 115(Suppl. 1), S3–S5.Google Scholar
3. Thangaratinam, S, Rogozinska, E, Jolly, K, et al. Interventions to reduce or prevent obesity in pregnant women: a systematic review. Health Technol Assess. 2012; 16, iii–iv, 1–191.Google Scholar
4. Sanabria-Martinez, G, Garcia-Hermoso, A, Poyatos-Leon, R, et al. Effectiveness of physical activity interventions on preventing gestational diabetes mellitus and excessive maternal weight gain: a meta-analysis. BJOG. 2015; 122, 1167–1174.CrossRefGoogle ScholarPubMed
5. Melzer, K, Schutz, Y, Boulvain, M, Kayser, B. Physical activity and pregnancy. Cardiovascular adaptations, recommendations and pregnancy outcomes. Sports Med. 2010; 40, 493–507.CrossRefGoogle ScholarPubMed
6. Bae-Gartz, I, Janoschek, R, Kloppe, CS, et al. Running exercise in obese pregnancies prevents IL-6 trans-signaling in male offspring. Med Sci Sports Exerc. 2016; 48, 829–838.Google Scholar
7. Carter, LG, Lewis, KN, Wilkerson, DC, et al. Perinatal exercise improves glucose homeostasis in adult offspring. Am J Physiol Endocrinol Metab. 2012; 303, E1061–E1068.Google Scholar
8. D’Ippolito, S, Tersigni, C, Scambia, G, Di Simone, N. Adipokines, an adipose tissue and placental product with biological functions during pregnancy. BioFactors.. 2012; 38, 14–23.CrossRefGoogle ScholarPubMed
9. Embaby, H, Elsayed, E, Fawzy, M. Insulin sensitivity and plasma glucose response to aerobic exercise in pregnant women at risk for gestational diabetes mellitus. Ethiop J Health Sci. 2016; 26, 409–414.Google Scholar
10. Sagedal, LR, Vistad, I, Overby, NC, et al. The effect of a prenatal lifestyle intervention on glucose metabolism: results of the Norwegian Fit for Delivery randomized controlled trial. BMC Pregnancy Childbirth. 2017; 17, 167.CrossRefGoogle ScholarPubMed
11. Parnpiansil, P, Jutapakdeegul, N, Chentanez, T, Kotchabhakdi, N. Exercise during pregnancy increases hippocampal brain-derived neurotrophic factor mRNA expression and spatial learning in neonatal rat pup. Neurosci Letters. 2003; 352, 45–48.Google Scholar
12. Cotman, CW, Berchtold, NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002; 25, 295–301.Google Scholar
13. Vega, SR, Kleinert, J, Sulprizio, M, et al. Responses of serum neurotrophic factors to exercise in pregnant and postpartum women. Psychoneuroendocrinology. 2011; 36, 220–227.Google Scholar
14. Jen, KL, Buison, A, Pellizzon, M, et al. Differential effects of fatty acids and exercise on body weight regulation and metabolism in female Wistar rats. Exp Biol Med. 2003; 228, 843–849.Google Scholar
15. Hopkins, SA, Baldi, JC, Cutfield, WS, McCowan, L, Hofman, PL. Effects of exercise training on maternal hormonal changes in pregnancy. Clin Endocrinol. 2011; 74, 495–500.Google Scholar
16. Aksu, I, Baykara, B, Ozbal, S, et al. Maternal treadmill exercise during pregnancy decreases anxiety and increases prefrontal cortex VEGF and BDNF levels of rat pups in early and late periods of life. Neurosci Lett. 2012; 516, 221–225.Google Scholar
17. Gomes da Silva, S, de Almeida, AA, Fernandes, J, et al. Maternal exercise during pregnancy increases BDNF levels and cell numbers in the hippocampal formation but not in the cerebral cortex of adult rat offspring. PloS One. 2016; 11, e0147200.CrossRefGoogle Scholar
18. Clapp, JF 3rd. Morphometric and neurodevelopmental outcome at age five years of the offspring of women who continued to exercise regularly throughout pregnancy. J Pediatr. 1996; 129, 856–863.Google Scholar
19. Kilkenny, C, Browne, WJ, Cuthill, IC, Emerson, M, Altman, DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010; 8, e1000412.Google Scholar
20. Dutta, S, Sengupta, P. Men and mice: relating their ages. Life Sci. 2016; 152, 244–248.Google Scholar
21. Artal, R, O’Toole, M. Guidelines of the American College of Obstetricians and Gynecologists for exercise during pregnancy and the postpartum period. Br J Sports Med. 2003; 37, 6–12.Google Scholar
22. ACOG Committee Opinion No. 650. Physical activity and exercise during pregnancy and the postpartum period. Obstet Gynecol. 2015; 126, e135–e142.Google Scholar
23. Rother, E, Kuschewski, R, Alcazar, MA, et al. Hypothalamic JNK1 and IKKbeta activation and impaired early postnatal glucose metabolism after maternal perinatal high-fat feeding. Endocrinology. 2012; 153, 770–781.Google Scholar
24. Stanford, KI, Lee, MY, Getchell, KM, et al. Exercise before and during pregnancy prevents the deleterious effects of maternal high-fat feeding on metabolic health of male offspring. Diabetes. 2015; 64, 427–433.Google Scholar
25. Oteng-Ntim, E, Varma, R, Croker, H, Poston, L, Doyle, P. Lifestyle interventions for overweight and obese pregnant women to improve pregnancy outcome: systematic review and meta-analysis. BMC Med. 2012; 10, 47.Google Scholar
26. Retnakaran, R, Qi, Y, Sermer, M, et al. Pre-gravid physical activity and reduced risk of glucose intolerance in pregnancy: the role of insulin sensitivity. Clin Endocrinol. 2009; 70, 615–622.Google Scholar
27. Tobias, DK, Zhang, C, van Dam, RM, Bowers, K, Hu, FB. Physical activity before and during pregnancy and risk of gestational diabetes mellitus: a meta-analysis. Diabetes Care. 2011; 34, 223–229.Google Scholar
28. Song, C, Li, J, Leng, J, Ma, RC, Yang, X. Lifestyle intervention can reduce the risk of gestational diabetes: a meta-analysis of randomized controlled trials. Obes Rev. 2016; 17, 960–969.Google Scholar
29. Highman, TJ, Friedman, JE, Huston, LP, Wong, WW, Catalano, PM. Longitudinal changes in maternal serum leptin concentrations, body composition, and resting metabolic rate in pregnancy. Am J Obstet Gynecol. 1998; 178, 1010–1015.Google Scholar
30. Clapp, JF 3rd, Kiess, W. Effects of pregnancy and exercise on concentrations of the metabolic markers tumor necrosis factor alpha and leptin. Am J Obstet Gynecol. 2000; 182, 300–306.Google Scholar
31. Cinti, S, Frederich, RC, Zingaretti, MC, et al. Immunohistochemical localization of leptin and uncoupling protein in white and brown adipose tissue. Endocrinology. 1997; 138, 797–804.Google Scholar
32. Masuyama, H, Nakatsukasa, H, Takamoto, N, Hiramatsu, Y. Correlation between soluble endoglin, vascular endothelial growth factor receptor-1, and adipocytokines in preeclampsia. J Clin Endocrinol Metab. 2007; 92, 2672–2679.Google Scholar
33. Bouassida, A, Chamari, K, Zaouali, M, et al. Review on leptin and adiponectin responses and adaptations to acute and chronic exercise. Br J Sports Med. 2010; 44, 620–630.Google Scholar
34. van der Wijden, CL, Delemarre-van de Waal, HA, van Mechelen, W, van Poppel, MN. The relationship between moderate-to-vigorous intensity physical activity and insulin resistance, insulin-like growth factor (IGF-1)-system 1, leptin and weight change in healthy women during pregnancy and after delivery. Clin Endocrinol. 2015; 82, 68–75.Google Scholar
35. Hoggard, N, Hunter, L, Lea, RG, Trayhurn, P, Mercer, JG. Ontogeny of the expression of leptin and its receptor in the murine fetus and placenta. Br J Nutr. 2000; 83, 317–326.Google Scholar
36. Malik, NM, Carter, ND, Wilson, CA, et al. Leptin expression in the fetus and placenta during mouse pregnancy. Placenta. 2005; 26, 47–52.CrossRefGoogle ScholarPubMed
37. Appel, S, Turnwald, EM, Alejandre-Alcazar, MA, et al. Leptin does not induce an inflammatory response in the murine placenta. Horm Metab Res. 2014; 46, 384–389.Google Scholar
38. Yamaguchi, M, Murakami, T, Yasui, Y, et al. Mouse placental cells secrete soluble leptin receptor (sOB-R): cAMP inhibits sOB-R production. Biochem Biophys Res Commun. 1998; 252, 363–367.Google Scholar
39. Huang, T, Larsen, KT, Ried-Larsen, M, Moller, NC, Andersen, LB. The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: a review. Scand J Med Sci Sports. 2014; 24, 1–10.CrossRefGoogle ScholarPubMed
40. Seifert, T, Brassard, P, Wissenberg, M, et al. Endurance training enhances BDNF release from the human brain. Am J Physiol Regul Integr Comp Physiol. 2010; 298, R372–R377.CrossRefGoogle ScholarPubMed
41. Rojas Vega, S, Struder, HK, Vera Wahrmann, B, et al. Acute BDNF and cortisol response to low intensity exercise and following ramp incremental exercise to exhaustion in humans. Brain Res. 2006; 1121, 59–65.Google Scholar
42. Zoladz, JA, Pilc, A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J Physiol Pharmacol. 2010; 61, 533–541.Google Scholar
43. Zoladz, JA, Pilc, A, Majerczak, J, et al. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol. 2008; 59(Suppl. 7), 119–132.Google Scholar
44. Dearden, L, Ozanne, SE. Early life origins of metabolic disease: developmental programming of hypothalamic pathways controlling energy homeostasis. Front Neuroendocrinol. 2015; 39, 3–16.Google Scholar
45. Kelly, SA, Hua, K, Wallace, JN, et al. Maternal exercise before and during pregnancy does not impact offspring exercise or body composition in mice. J Negat Results Biomed. 2015; 14, 13.Google Scholar
46. Barakat, R, Lucia, A, Ruiz, JR. Resistance exercise training during pregnancy and newborn’s birth size: a randomised controlled trial. Int J Obes. 2009; 33, 1048–1057.Google Scholar
47. Hopkins, SA, Cutfield, WS. Exercise in pregnancy: weighing up the long-term impact on the next generation. Exerc Sport Sci Rev. 2011; 39, 120–127.Google Scholar
48. Contarteze, RV, Manchado Fde, B, Gobatto, CA, De Mello, MA. Stress biomarkers in rats submitted to swimming and treadmill running exercises. Comp Biochem Physiol A Mol Integr Physiol. 2008; 151, 415–422.Google Scholar
49. Wasinski, F, Estrela, GR, Arakaki, AM, et al. Maternal forced swimming reduces cell proliferation in the postnatal dentate gyrus of mouse offspring. Front Neurosci. 2016; 10, 402.Google Scholar
50. Wasinski, F, Bacurau, RF, Estrela, GR, et al. Exercise during pregnancy protects adult mouse offspring from diet-induced obesity. Nutr Metab. 2015; 12, 56.Google Scholar
51. Stanford, KI, Middelbeek, RJ, Townsend, KL, et al. A novel role for subcutaneous adipose tissue in exercise-induced improvements in glucose homeostasis. Diabetes. 2015; 64, 2002–2014.Google Scholar
52. Stanford, KI, Middelbeek, RJ, Goodyear, LJ. Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes. 2015; 64, 2361–2368.Google Scholar
53. Dayi, A, Agilkaya, S, Ozbal, S, et al. Maternal aerobic exercise during pregnancy can increase spatial learning by affecting leptin expression on offspring’s early and late period in life depending on gender. ScientificWorldJournal. 2012; 2012, 429803.Google Scholar
54. Rasmussen, P, Brassard, P, Adser, H, et al. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol. 2009; 94, 1062–1069.Google Scholar
55. Karege, F, Schwald, M, Cisse, M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett. 2002; 328, 261–264.Google Scholar
56. Lommatzsch, M, Zingler, D, Schuhbaeck, K, et al. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging. 2005; 26, 115–123.Google Scholar
57. Pan, W, Banks, WA, Fasold, MB, Bluth, J, Kastin, AJ. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology. 1998; 37, 1553–1561.Google Scholar
58. Flock, A, Weber, SK, Ferrari, N, et al. Determinants of brain-derived neurotrophic factor (BDNF) in umbilical cord and maternal serum. Psychoneuroendocrinology. 2016; 63, 191–197.Google Scholar
59. Kim, H, Lee, SH, Kim, SS, Yoo, JH, Kim, CJ. The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int J Dev Neurosci. 2007; 25, 243–249.Google Scholar
60. Domingues, MR, Matijasevich, A, Barros, AJ, et al. Physical activity during pregnancy and offspring neurodevelopment and IQ in the first 4 years of life. PLoS One.. 2014; 9, e110050.Google Scholar
61. Dearden, L, Ozanne, SE. Early life origins of metabolic disease: developmental programming of hypothalamic pathways controlling energy homeostasis. Front Neuroendocrinol. 2015; 39, 3–16.Google Scholar
62. Kahn, BB. Alterations in glucose transporter expression and function in diabetes: mechanisms for insulin resistance. J Cell Biochem. 1992; 48, 122–128.Google Scholar
63. Hirshman, MF, Wardzala, LJ, Goodyear, LJ, et al. Exercise training increases the number of glucose transporters in rat adipose cells. Am J Physiol. 1989; 257(Pt 1), E520–E530.Google Scholar
64. Raipuria, M, Bahari, H, Morris, MJ. Effects of maternal diet and exercise during pregnancy on glucose metabolism in skeletal muscle and fat of weanling rats. PloS One. 2015; 10, e0120980.Google Scholar
65. Li, Y, Qi, Y, Huang, TH, Yamahara, J, Roufogalis, BD. Pomegranate flower: a unique traditional antidiabetic medicine with dual PPAR-alpha/-gamma activator properties. Diabetes Obes Metab. 2008; 10, 10–17.Google Scholar
66. Althuizen, E, van der Wijden, CL, van Mechelen, W, Seidell, JC, van Poppel, MN. The effect of a counselling intervention on weight changes during and after pregnancy: a randomised trial. BJOG. 2013; 120, 92–99.Google Scholar
67. Kinnunen, TI, Raitanen, J, Aittasalo, M, Luoto, R. Preventing excessive gestational weight gain – a secondary analysis of a cluster-randomised controlled trial. Eur J Clin Nutr. 2012; 66, 1344–1350.Google Scholar
68. Haakstad, LA, Bo, K. Effect of regular exercise on prevention of excessive weight gain in pregnancy: a randomised controlled trial. Eur J Contracept Reprod Health Care. 2011; 16, 116–125.Google Scholar
69. Ong, MJ, Guelfi, KJ, Hunter, T, et al. Supervised home-based exercise may attenuate the decline of glucose tolerance in obese pregnant women. Diabetes Metab. 2009; 35, 418–421.Google Scholar
70. Muktabhant, B, Lumbiganon, P, Ngamjarus, C, Dowswell, T. Interventions for preventing excessive weight gain during pregnancy. Cochrane Database Systematic Rev. 2012; 4, CD007145.Google Scholar
71. Hui, AL, Back, L, Ludwig, S, et al. Effects of lifestyle intervention on dietary intake, physical activity level, and gestational weight gain in pregnant women with different pre-pregnancy Body Mass Index in a randomized control trial. BMC Pregnancy Childbirth. 2014; 14, 331.Google Scholar
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