Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T11:44:27.310Z Has data issue: false hasContentIssue false

Increased maternal BMI is associated with infant wheezing in early life: a prospective cohort study

Published online by Cambridge University Press:  25 June 2014

A. de Vries*
Affiliation:
Endocrinology Unit, University/BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UK
R. M. Reynolds
Affiliation:
Endocrinology Unit, University/BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UK
J. R. Seckl
Affiliation:
Endocrinology Unit, University/BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UK
M. van der Wal
Affiliation:
Department of Epidemiology, Documentation and Health Promotion, Public Health Service of Amsterdam, the Netherlands
G. J. Bonsel
Affiliation:
Department of Obstetrics and Prenatal Medicine, Erasmus Medical Center, Rotterdam, the Netherlands
T. G. M. Vrijkotte
Affiliation:
Department of Public Health, Academic Medical Center, Amsterdam, the Netherlands
*
*Address for correspondence: A. de Vries, Endocrinology Unit, University/BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, EH16 4TJ Edinburgh, UK. (Email [email protected])

Abstract

Rates of obesity are increasing in women of child bearing age with negative impacts on maternal and offspring health. Emerging evidence suggests in utero origins of respiratory health in offspring of obese mothers but mechanisms are unknown. Changes in maternal cortisol levels are one potential factor as cortisol levels are altered in obesity and cortisol is separately implicated in development of offspring wheeze. We aimed to assess whether increased pre-pregnancy maternal body mass index (BMI) was associated with offspring early life wheezing, and whether this was mediated by altered cortisol levels in the mother. In a prospective community-based cohort (Amsterdam Born Children and their Development cohort), women completed questionnaires during pregnancy and at 3–5 months post-delivery regarding self-history of asthma and atopy, and of wheezing of their offspring (n=4860). Pre-pregnancy BMI was recorded and serum total cortisol levels were measured in a subset of women (n=2227) at their first antenatal visit. A total of 20.2% (n=984) women were overweight or obese and 10.3% reported wheezing in their offspring. Maternal BMI was associated with offspring wheezing (1 unit (kg/m2) increase, OR: 1.03; 95% CI: 1.00–1.05), after correction for confounders. Although maternal cortisol levels were lower in overweight mothers and those with a history of asthma, maternal cortisol levels did not mediate the increased offspring wheezing. Pre-pregnancy BMI impacts on baby wheezing, which is not mediated by lower cortisol levels. As the prevalence of obesity in women of child-bearing age is increasing, further studies are needed to investigate modifiable maternal factors to avoid risk of wheezing in young children.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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.Guelinckx, I, Devlieger, R, Beckers, K, Vansant, G. Maternal obesity: pregnancy complications, gestational weight gain and nutrition. Obes Rev. 2008; 9, 140150.Google Scholar
2.Gale, CR, Javaid, MK, Robinson, SM, et al. Maternal size in pregnancy and body composition in children. J Clin Endocrinol Metab. 2007; 92, 39043911.Google Scholar
3.Lawlor, DA, Smith, GD, O’Callaghan, M. Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes. Am J Epidemiol. 2007; 165, 418424.CrossRefGoogle ScholarPubMed
4.Sewell, MF, Huston-Presley, L, Super, DM, Catalano, P. Increased neonatal fat mass, not lean body mass, is associated with maternal obesity. Am J Obstetr Gynecol. 2006; 195, 11001103.Google Scholar
5.Rizwan, S, Reid, J, Kelly, Y, et al. Trends in childhood and parental asthma prevalence in Merseyside, 1991–1998. J Public Health (Oxf). 2004; 26, 337342.Google Scholar
6.Epstein, LH, Wu, YW, Paluch, RA, Cerny, FJ, Dorn, JP. Asthma and maternal body mass index are related to pediatric body mass index and obesity: results from the Third National Health and Nutrition Examination Survey. Obes Res. 2000; 8, 575581.CrossRefGoogle ScholarPubMed
7.Sennhauser, FH, Braun-Fahrlander, C, Wildhaber, JH. The burden of asthma in children: a European perspective. Paediatr Respir Rev. 2005; 6, 27.Google Scholar
8.Pasquali, R, Vicennati, V, Cacciari, M, Pagotto, U. The hypothalamic-pituitary-adrenal axis activity in obesity and the metabolic syndrome. Ann N Y Acad Sci. 2006; 1083, 111128.Google Scholar
9.Strain, GW, Zumoff, B, Strain, JJ, Levin, J, Fukushima, DK. Cortisol production in obesity. Metabolism. 1980; 29, 980985.CrossRefGoogle ScholarPubMed
10.Staab, CA, Maser, E. 11beta-Hydroxysteroid dehydrogenase type 1 is an important regulator at the interface of obesity and inflammation. J Steroid Biochem Mol Biol. 2010; 119, 5672.Google Scholar
11.Benson, S, Arck, PC, Tan, S, et al. Effects of obesity on neuroendocrine, cardiovascular, and immune cell responses to acute psychosocial stress in premenopausal women. Psychoneuroendocrinology. 2009; 34, 181189.Google Scholar
12.Seckl, JR. Prenatal glucocorticoids and long-term programming. Eur J Endocrinol. 2004; 151(Suppl. 3), U49U62.Google Scholar
13.De Vries, A, Holmes, MC, Heijnis, A, et al. Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. J Clin Invest. 2007; 117, 10581067.Google Scholar
14.Benediktsson, R, Lindsay, RS, Noble, J, Seckl, JR, Edwards, CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet. 1993; 341, 339341.Google Scholar
15.Goedhart, G, Vrijkotte, TG, Roseboom, TJ, et al. Maternal cortisol and offspring birthweight: results from a large prospective cohort study. Psychoneuroendocrinology. 2010; 35, 644652.CrossRefGoogle ScholarPubMed
16.Phillips, DI, Walker, BR, Reynolds, RM, et al. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension. 2000; 35, 13011306.CrossRefGoogle ScholarPubMed
17.O’Reilly, JR, Riley, SC, Critchley, HO, et al. Reduced glucocorticoid action in obese pregnancy is associated with increased birthweight. Endocrine Abstracts. 2013; 31, p. 143.Google Scholar
18.Buske-Kirschbaum, A, von, AK, Krieger, S, et al. Blunted cortisol responses to psychosocial stress in asthmatic children: a general feature of atopic disease? Psychosom Med. 2003; 65, 806810.Google Scholar
19.Daniltchenko, M, de Vries, A, Tobin, DJ, et alAllergic dermatitis is aggravated by stress and alters the hypothalamic stress-response in mice. J Inves Dermatolo. 2005; 124.Google Scholar
20.Heim, C, Ehlert, U, Hellhammer, DH. The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology. 2000; 25, 135.Google Scholar
21.Priftis, KN, Papadimitriou, A, Nicolaidou, P, Chrousos, GP. Dysregulation of the stress response in asthmatic children. Allergy. 2009; 64, 1831.Google Scholar
22.Buske-Kirschbaum, A, Fischbach, S, Rauh, W, Hanker, J, Hellhammer, D. Increased responsiveness of the hypothalamus-pituitary-adrenal (HPA) axis to stress in newborns with atopic disposition. Psychoneuroendocrinology. 2004; 29, 705711.CrossRefGoogle ScholarPubMed
23.Haberg, SE, Stigum, H, London, SJ, Nystad, W, Nafstad, P. Maternal obesity in pregnancy and respiratory health in early childhood. Paediatr Perinat Epidemiol. 2009; 23, 352362.Google Scholar
24.Harpsoe, MC, Basit, S, Bager, P, et al. Maternal obesity, gestational weight gain, and risk of asthma and atopic disease in offspring: a study within the Danish National Birth Cohort. J Allergy Clin Immunol. 2013; 131, 10331040.Google Scholar
25.Kumar, R, Story, RE, Pongracic, JA, et al. Maternal pre-pregnancy obesity and recurrent wheezing in early childhood. Pediatr Allergy Immunol Pulmonol. 2010; 23, 183190.Google Scholar
26.Patel, SP, Rodriguez, A, Little, MP, et al. Associations between pre-pregnancy obesity and asthma symptoms in adolescents. J Epidemiol Community Health. 2012; 66, 809814.Google Scholar
27.Leermakers, ET, Sonnenschein-van der Voort, AM, Gaillard, R, et al. Maternal weight, gestational weight gain and preschool wheezing: the Generation R Study. Eur Respir J. 2013; 42, 12341243.Google Scholar
28.Reichman, NE, Nepomnyaschy, L. Maternal pre-pregnancy obesity and diagnosis of asthma in offspring at age 3 years. Matern Child Health J. 2007; 12, 725733.Google Scholar
29.Scholtens, S, Wijga, AH, Brunekreef, B, et al. Maternal overweight before pregnancy and asthma in offspring followed for 8 years. Int J Obes (Lond). 2010; 34, 606613.Google Scholar
30.Lowe, AJ, Ekeus, C, Braback, L, et al. Impact of maternal obesity on inhaled corticosteroid use in childhood: a registry based analysis of first born children and a sibling pair analysis. PLoS One. 2013; 8, e67368.Google Scholar
31.Devereux, G, Litonjua, AA, Turner, SW, et al. Maternal vitamin D intake during pregnancy and early childhood wheezing. Am J Clin Nutr. 2007; 85, 853859.Google Scholar
32.Nagel, G, Buchele, G, Weinmayr, G, et al. Effect of breastfeeding on asthma, lung function and bronchial hyperreactivity in ISAAC Phase II. Eur Respir J. 2009; 33, 9931002.CrossRefGoogle ScholarPubMed
33.Reynolds, RM, Walker, BR, Phillips, DI, et al. Programming of hypertension: associations of plasma aldosterone in adult men and women with birthweight, cortisol, and blood pressure. Hypertension. 2009; 53, 932936.Google Scholar
34.van Eijsden, M, Vrijkotte, TG, Gemke, RJ, van der Wal, MF. Cohort profile: The Amsterdam Born Children and their Development (ABCD) Study. Int J Epidemiol. 2011; 40, 11761185.CrossRefGoogle ScholarPubMed
35.Tromp, M, van, EM, Ravelli, AC, Bonsel, GJ. Anonymous non-response analysis in the ABCD cohort study enabled by probabilistic record linkage. Paediatr Perinat Epidemiol. 2009; 23, 264272.Google Scholar
36.Just, J, Belfar, S, Wanin, S, et al. Impact of innate and environmental factors on wheezing persistence during childhood. J Asthma. 2010; 47, 412416.Google Scholar
37.Jedrychowski, W, Perera, FP, Maugeri, U, et al. Early wheezing phenotypes and severity of respiratory illness in very early childhood: study on intrauterine exposure to fine particle matter. Environ Int. 2009; 35, 877884.CrossRefGoogle Scholar
38.Koopman, LP, Wijga, A, Smit, HA, et al. Early respiratory and skin symptoms in relation to ethnic background: the importance of socioeconomic status; the PIAMA study. Arch Dis Child. 2002; 87, 482488.Google Scholar
39.Kurukulaaratchy, RJ, Matthews, S, Arshad, SH. Does environment mediate earlier onset of the persistent childhood asthma phenotype? Pediatrics. 2004; 113, 345350.Google Scholar
40.Franklin, KA, Holmgren, PA, Jonsson, F, et al. Snoring, pregnancy-induced hypertension, and growth retardation of the fetus. Chest. 2000; 117, 137141.Google Scholar
41.Mallol, J, Garcia-Marcos, L, Sole, D, Brand, P. International prevalence of recurrent wheezing during the first year of life: variability, treatment patterns and use of health resources. Thorax. 2010; 65, 10041009.Google Scholar
42.Chong Neto, HJ, Rosario, N, la Bianca, AC, Sole, D, Mallol, J. Validation of a questionnaire for epidemiologic studies of wheezing in infants. Pediatr Allergy Immunol. 2007; 18, 8687.Google Scholar
43.Mallol, J, Garcia-Marcos, L, Aguirre, V, et al. The International Study of Wheezing in Infants: questionnaire validation. Int Arch Allergy Immunol. 2007; 144, 4450.Google Scholar
44.Dekkers, JC, van Wier, MF, Hendriksen, IJ, Twisk, JW, van, MW. Accuracy of self-reported body weight, height and waist circumference in a Dutch overweight working population. BMC Med Res Methodol. 2008; 8, 69.Google Scholar
45.Mesman, I, Roseboom, TJ, Bonsel, GJ, et al. Maternal pre-pregnancy body mass index explains infant's weight and BMI at 14 months: results from a multi-ethnic birth cohort study. Arch Dis Child. 2009.Google Scholar
46.Harley, KG, Macher, JM, Lipsett, M, et al. Fungi and pollen exposure in the first months of life and risk of early childhood wheezing. Thorax. 2009; 64, 353358.Google Scholar
47.Baron, RM, Kenny, DA. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986; 51, 11731182.CrossRefGoogle ScholarPubMed
48.Kusunoki, T, Morimoto, T, Nishikomori, R, et al. Obesity and the prevalence of allergic diseases in schoolchildren Pediatr Allergy Immunol. 2008; 19, 527534.Google Scholar
49.Carroll, KN, Wu, P, Gebretsadik, T, et al. Season of infant bronchiolitis and estimates of subsequent risk and burden of early childhood asthma. J Allergy Clin Immunol. 2009; 123, 964966.Google Scholar
50.Yeh, J, Shelton, JA. Increasing prepregnancy body mass index: analysis of trends and contributing variables. Am J Obstetr Gynecol. 2005; 193, 19941998.CrossRefGoogle ScholarPubMed
51.Duncan, JM, Sears, MR. Breastfeeding and allergies: time for a change in paradigm? Curr Opin Allergy Clin Immunol. 2008; 8, 398405.Google Scholar
52.Anderson, J, Malley, K, Snell, R. Is 6 months still the best for exclusive breastfeeding and introduction of solids? A literature review with consideration to the risk of the development of allergies. Breastfeed Rev. 2009; 17, 2331.Google Scholar
53.Tooley, KL, El-Merhibi, A, Cummins, AG, et al. Maternal milk, but not formula, regulates the immune response to beta-lactoglobulin in allergy-prone rat pups. J Nutr. 2009; 139, 21452151.Google Scholar
54.Polte, T, Hansen, G. Maternal tolerance achieved during pregnancy is transferred to the offspring via breast milk and persistently protects the offspring from allergic asthma. Clin Exp Allergy. 2008; 38, 19501958.Google Scholar
55.Wamboldt, MZ, Laudenslager, M, Wamboldt, FS, Kelsay, K, Hewitt, J. Adolescents with atopic disorders have an attenuated cortisol response to laboratory stress. J Allergy Clin Immunol. 2003; 111, 509514.Google Scholar
56.Buske-Kirschbaum, A, Jobst, S, Wustmans, A, et al. Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosom Med. 1997; 59, 419426.Google Scholar
57.Lumeng, CN, Bodzin, JL, Saltiel, AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007; 117, 175184.Google Scholar
58.Lumeng, CN, Deyoung, SM, Bodzin, JL, Saltiel, AR. Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes. 2007; 56, 1623.Google Scholar
59.Ramsay, JE, Ferrell, WR, Crawford, L, et al. Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways. J Clin Endocrinol Metab. 2002; 87, 42314237.CrossRefGoogle ScholarPubMed
60.Challier, JC, Basu, S, Bintein, T, et al. Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta. 2008; 29, 274281.Google Scholar
61.Rothenbacher, D, Weyermann, M, Fantuzzi, G, Brenner, H. Adipokines in cord blood and risk of wheezing disorders within the first two years of life. Clin Expl Allergy. 2007; 37, 11431149.Google Scholar
62.Scirica, CV, Gold, DR, Ryan, L, et al. Predictors of cord blood IgE levels in children at risk for asthma and atopy. J Allergy Clin Immunol. 2007; 119, 8188.Google Scholar
63.Ly, NP, Rifas-Shiman, SL, Litonjua, AA, et al. Cord blood cytokines and acute lower respiratory illnesses in the first year of life. Pediatrics. 2007; 119, e171e178.Google Scholar
64.Delgado, J, Barranco, P, Quirce, S. Obesity and asthma. J Investig Allergol Clin Immunol. 2008; 18, 420425.Google Scholar
65.Clark, JM, Hulme, E, Devendrakumar, V, et al. Effect of maternal asthma on birthweight and neonatal outcome in a British inner-city population. Paediatr Perinat Epidemiol. 2007; 21, 154162.Google Scholar
66.Lim, RH, Kobzik, L, Dahl, M. Risk for asthma in offspring of asthmatic mothers versus fathers: a meta-analysis. PLoS One. 2010; 5, e10134.Google Scholar
67.Mallol, J, Garcia-Marcos, L, Aguirre, V, et al. The International Study of Wheezing in Infants: questionnaire validation. Int Arch Allergy Immunol. 2007; 144, 4450.Google Scholar
68.Chong Neto, HJ, Rosario, N, la Bianca, AC, Sole, D, Mallol, J. Validation of a questionnaire for epidemiologic studies of wheezing in infants. Pediatr Allergy Immunol. 2007; 18, 8687.Google Scholar
69.Mallol, J, Garcia-Marcos, L, Sole, D, Brand, P. International prevalence of recurrent wheezing during the first year of life: variability, treatment patterns and use of health resources. Thorax. 2010; 65, 10041009.Google Scholar
70.Willers, SM, Devereux, G, Craig, LC, et al. Maternal food consumption during pregnancy and asthma, respiratory and atopic symptoms in 5-year-old children. Thorax. 2007; 62, 773779.Google Scholar
71.Stommel, M, Schoenborn, CA. Accuracy and usefulness of BMI measures based on self-reported weight and height: findings from the NHANES & NHIS 2001–2006. BMC Public Health. 2009; 9, 421.CrossRefGoogle ScholarPubMed
72.Niedhammer, I, Bugel, I, Bonenfant, S, Goldberg, M, Leclerc, A. Validity of self-reported weight and height in the French GAZEL cohort. Int J Obes Relat Metab Disord. 2000; 24, 11111118.Google Scholar
73.Engstrom, JL, Paterson, SA, Doherty, A, Trabulsi, M, Speer, KL. Accuracy of self-reported height and weight in women: an integrative review of the literature. J Midwifery Womens Health. 2003; 48, 338345.Google Scholar
74.Krul, AJ, Daanen, HA, Choi, H. Self-reported and measured weight, height and body mass index (BMI) in Italy, the Netherlands and North America. Eur J Public Health. 2011; 21, 414419.Google Scholar
75.Dekkers, JC, van Wier, MF, Hendriksen, IJ, Twisk, JW, van, MW. Accuracy of self-reported body weight, height and waist circumference in a Dutch overweight working population. BMC Med Res Methodol. 2008; 8, 69.Google Scholar
76.Callaway, LK, O’Callaghan, MJ, McIntyre, HD. Barriers to addressing overweight and obesity before conception. Med J Aust. 2009; 191, 425428.Google Scholar
77.Maiorino, MI, Schisano, B, Di, PC, et al. Interleukin-20 circulating levels in obese women: effect of weight loss. Nutr Metab Cardiovasc Dis. 2009; 20, 180185.Google Scholar
78.Mai, XM, Chen, Y, Krewski, D. Does leptin play a role in obesity-asthma relationship? Pediatr Allergy Immunol. 2009; 20, 207212.Google Scholar