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Does Pet-Keeping Modify the Association of Delivery Mode with Offspring Body Size?

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Abstract

Caesarean-section (CS) delivery increases risk of childhood obesity, and is associated with a distinct early-life gut microbiome, which may contribute to obesity. Household pets may alter human gut microbiome composition. We examined if pet-keeping modified the association of CS with obesity at age 2 years in 639 Wayne County Health, Environment, Allergy and Asthma Longitudinal Study birth cohort participants. Pet-keeping was defined as having a dog or cat (indoors ≥1 h/day) at child age 2 years. We used logistic regression to test for an interaction between CS and pet-keeping with obesity (BMI ≥ 95th percentile) at age 2 years, adjusted for maternal obesity. A total of 328 (51.3 %) children were male; 367 (57.4 %) were African American; 228 (35.7 %) were born by CS; and 55 (8.6 %) were obese. After adjusting for maternal obesity, CS-born children had a non-significant (P = 0.25) but elevated 1.4 (95 % CI 0.8, 2.5) higher odds of obesity compared to those born vaginally. There was evidence of effect modification between current pet-keeping and delivery mode with obesity at age 2 years (interaction P = 0.054). Compared to children born vaginally without a pet currently in the home, children born via CS without a pet currently in the home had a statistically significant (P = 0.043) higher odds (odds ratio 2.00; 95 % CI 1.02, 3.93) of being obese at age 2 years. Pets modified the CS–BMI relationship; whether the underlying mechanism is through effects on environmental or gut microbiome requires specific investigation.

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References

  1. Ogden, C. L., Carroll, M. D., Kit, B. K., et al. (2012). Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA, 307(5), 483–490. doi:10.1001/jama.2012.40.

    Article  PubMed  Google Scholar 

  2. Ogden, C. L., Flegal, K. M., Carroll, M. D., et al. (2002). Prevalence and trends in overweight among US children and adolescents, 1999–2000. JAMA, 288(14), 1728–1732.

    Article  PubMed  Google Scholar 

  3. Zahniser, S. C., Kendrick, J. S., Franks, A. L., et al. (1992). Trends in obstetric operative procedures, 1980 to 1987. American Journal of Public Health, 82(10), 1340–1344.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Menacker, F., & Hamilton, B. E. (2010). Recent trends in cesarean delivery in the United States. NCHS Data Brief, 35, 1–8.

    PubMed  Google Scholar 

  5. Huh, S. Y., Rifas-Shiman, S. L., Zera, C. A., et al. (2012). Delivery by caesarean section and risk of obesity in preschool age children: A prospective cohort study. Archives of Disease in Childhood, 97(7), 610–616.

    Article  PubMed Central  PubMed  Google Scholar 

  6. Goldani, H. A., Bettiol, H., Barbieri, M. A., et al. (2011). Cesarean delivery is associated with an increased risk of obesity in adulthood in a Brazilian birth cohort study. American Journal of Clinical Nutrition, 93(6), 1344–1347.

    Article  CAS  PubMed  Google Scholar 

  7. Li, H., Ye, R., Pei, L., et al. (2014). Caesarean delivery, caesarean delivery on maternal request and childhood overweight: A Chinese birth cohort study of 181,380 children. Pediatric Obesity, 9(1), 10–16. doi:10.1111/j.2047-6310.2013.00151.x.

    Article  CAS  PubMed  Google Scholar 

  8. Wang, L., Alamian, A., Southerland, J., et al. (2013). Cesarean section and the risk of overweight in grade 6 children. European Journal of Pediatrics, 172(10), 1341–1347. doi:10.1007/s00431-013-2043-2.

    Article  PubMed  Google Scholar 

  9. Barros, F. C., Matijasevich, A., Hallal, P. C., et al. (2012). Cesarean section and risk of obesity in childhood, adolescence, and early adulthood: Evidence from 3 Brazilian birth cohorts. American Journal of Clinical Nutrition, 95(2), 465–470.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Ajslev, T. A., Andersen, C. S., Gamborg, M., et al. (2011). Childhood overweight after establishment of the gut microbiota: The role of delivery mode, pre-pregnancy weight and early administration of antibiotics. International Journal of Obesity, 35(4), 522–529.

    Article  CAS  PubMed  Google Scholar 

  11. Lin, S. L., Leung, G. M., & Schooling, C. M. (2013). Mode of delivery and adiposity: Hong Kong’s “Children of 1997” birth cohort. Annals of Epidemiology, 23(11), 693–699. doi:10.1016/j.annepidem.2013.06.090.

    Article  PubMed  Google Scholar 

  12. Flemming, K., Woolcott, C. G., Allen, A. C., et al. (2013). The association between caesarean section and childhood obesity revisited: A cohort study. Archives of Disease in Childhood, 98(7), 526–532. doi:10.1136/archdischild-2012-303459.

    Article  PubMed  Google Scholar 

  13. Pei, Z., Heinrich, J., Fuertes, E., et al. (2014). Cesarean delivery and risk of childhood obesity. The Journal of Pediatrics, 164(5), 1068–1073. doi:10.1016/j.jpeds.2013.12.044.

    Article  PubMed  Google Scholar 

  14. Li, H., Zhou, Y., & Liu, J. (2013). The impact of cesarean section on offspring overweight and obesity: A systematic review and meta-analysis. International Journal of Obesity, 37(7), 893–899.

    Article  PubMed  Google Scholar 

  15. Li, H. T., Zhou, Y. B., & Liu, J. M. (2012). Cesarean section might moderately increase offspring obesity risk. American Journal of Clinical Nutrition, 96(1), 215–216.

    Article  CAS  PubMed  Google Scholar 

  16. Dominguez-Bello, M. G., Costello, E. K., Contreras, M., et al. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the United States of America, 107(26), 11971–11975. doi:10.1073/pnas.1002601107.

    Article  PubMed Central  PubMed  Google Scholar 

  17. Azad, M. B., Konya, T., Maughan, H., et al. (2013). Gut microbiota of healthy Canadian infants: Profiles by mode of delivery and infant diet at 4 months. CMAJ, 185(5), 385–394.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Ridaura, V. K., Faith, J. J., Rey, F. E., et al. (2013). Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science, 341(6150), 1241214. doi:10.1126/science.1241214.

    Article  PubMed  Google Scholar 

  19. Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., et al. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122), 1027–1031.

    Article  PubMed  Google Scholar 

  20. Kalliomaki, M., Collado, M. C., Salminen, S., et al. (2008). Early differences in fecal microbiota composition in children may predict overweight. American Journal of Clinical Nutrition, 87(3), 534–538.

    CAS  PubMed  Google Scholar 

  21. Luoto, R., Kalliomaki, M., Laitinen, K., et al. (2011). Initial dietary and microbiological environments deviate in normal-weight compared to overweight children at 10 years of age. Journal of Pediatric Gastroenterology and Nutrition, 52(1), 90–95.

    Article  PubMed  Google Scholar 

  22. Karlsson, C. L., Onnerfalt, J., Xu, J., et al. (2012). The microbiota of the gut in preschool children with normal and excessive body weight. Obesity, 20(11), 2257–2261.

    Article  PubMed  Google Scholar 

  23. Balamurugan, R., George, G., Kabeerdoss, J., et al. (2010). Quantitative differences in intestinal Faecalibacterium prausnitzii in obese Indian children. British Journal of Nutrition, 103(3), 335–338. doi:10.1017/s0007114509992182.

    Article  CAS  PubMed  Google Scholar 

  24. Wegienka, G., Johnson, C. C., Havstad, S., et al. (2011). Lifetime dog and cat exposure and dog- and cat-specific sensitization at age 18 years. Clinical and Experimental Allergy, 41(7), 979–986.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Fujimura, K. E., Johnson, C. C., Ownby, D. R., et al. (2010). Man’s best friend? The effect of pet ownership on house dust microbial communities. The Journal of Allergy and Clinical Immunology, 126(2), 410.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Song, S. J., Lauber, C., Costello, E. K., et al. (2013). Cohabiting family members share microbiota with one another and with their dogs. eLife. doi:10.7554/eLife.00458.

    Google Scholar 

  27. Azad, M. B., Konya, T., Maughan, H., et al. (2013). Infant gut microbiota and the hygiene hypothesis of allergic disease: Impact of household pets and siblings on microbiota composition and diversity. Allergy, Asthma, and Clinical Immunology, 9(1), 15. doi:10.1186/1710-1492-9-15.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Fujimura, K. E., Demoor, T., Rauch, M., et al. (2014). House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proceedings of the National Academy of Sciences of the United States of America, 111(2), 805–810. doi:10.1073/pnas.1310750111.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Bager, P., Wohlfahrt, J., & Westergaard, T. (2008). Caesarean delivery and risk of atopy and allergic disease: Meta-analyses. Clinical and Experimental Allergy, 38(4), 634–642. doi:10.1111/j.1365-2222.2008.02939.x.

    Article  CAS  PubMed  Google Scholar 

  30. Havstad, S., Wegienka, G., Zoratti, E. M., et al. (2011). Effect of prenatal indoor pet exposure on the trajectory of total IgE levels in early childhood. The Journal of Allergy and Clinical Immunology, 128(4), 880–885.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Wegienka, G., Havstad, S., Joseph, C. L., et al. (2011). Racial disparities in allergic outcomes in African Americans emerge as early as age 2 years. Clinical and Experimental Allergy, 42(6), 909–917. doi:10.1111/j.1365-2222.2011.03946.x.

    Google Scholar 

  32. Oken, E., Kleinman, K. P., Rich-Edwards, J., et al. (2003). A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatrics, 3, 6.

    Article  PubMed Central  PubMed  Google Scholar 

  33. Kuczmarski, R. J., Ogden, C. L., Guo, S. S., et al. (2002). 2000 CDC growth charts for the United States: Methods and development. Vital Health Statistics, 11(246), 1–190.

    Google Scholar 

  34. Rabinowitz, P., & Conti, L. (2013). Links among human health, animal health, and ecosystem health. Annual Review of Public Health, 34, 189–204. doi:10.1146/annurev-publhealth-031912-114426.

    Article  PubMed  Google Scholar 

  35. Wells, D. L. (2007). Domestic dogs and human health: An overview. British Journal of Health Psychology, 12(Pt 1), 145–156. doi:10.1348/135910706x103284.

    Article  PubMed  Google Scholar 

  36. Levine, G. N., Allen, K., Braun, L. T., et al. (2013). Pet ownership and cardiovascular risk: A scientific statement from the American Heart Association. Circulation, 127(23), 2353–2363. doi:10.1161/CIR.0b013e31829201e1.

    Article  PubMed  Google Scholar 

  37. Lovasi, G. S., Underhill, L. J., Jack, D., et al. (2012). At odds: Concerns raised by using odds ratios for continuous or common dichotomous outcomes in research on physical activity and obesity. The Open Epidemiology Journal, 5, 13–17. doi:10.2174/1874297101205010013.

    Article  PubMed Central  PubMed  Google Scholar 

  38. Greenland, S. (1989). Modeling and variable selection in epidemiologic analysis. American Journal of Public Health, 79(3), 340–349.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Selvin, S. (1996). Statistical analysis of epidemiologic data (2nd ed.). New York: Oxford University Press.

    Google Scholar 

  40. Ezell, J., Cassidy-Bushrow, A., Joseph, C., et al. (2014). Prenatal dog-keeping practices vary by race—speculations on implications for disparities in childhood health and disease. Ethnicity and Disease, 24(1), 104–109.

    PubMed Central  PubMed  Google Scholar 

  41. Bryant, A. S., Washington, S., Kuppermann, M., et al. (2009). Quality and equality in obstetric care: Racial and ethnic differences in caesarean section delivery rates. Paediatric and Perinatal Epidemiology, 23(5), 454–462. doi:10.1111/j.1365-3016.2009.01059.x.

    Article  PubMed  Google Scholar 

  42. Kabir, A. A., Pridjian, G., Steinmann, W. C., et al. (2005). Racial differences in cesareans: an analysis of U.S. 2001 national inpatient sample data. Obstetrics and Gynecology, 105(4), 710–718. doi:10.1097/01.AOG.0000154154.02581.ce.

    Article  PubMed  Google Scholar 

  43. American College of Obstetricians and Gynecologists. (2013). ACOG committee opinion no. 559: Cesarean delivery on maternal request. Obstetrics and Gynecology, 121(4), 904–907. doi:10.1097/01.AOG.0000428647.67925.d3.

    Article  Google Scholar 

  44. Kaplan, J. L., & Walker, W. A. (2012). Early gut colonization and subsequent obesity risk. Current Opinion in Clinical Nutrition and Metabolic Care, 15(3), 278–284.

    Article  PubMed  Google Scholar 

  45. Wolf, K. J., & Lorenz, R. G. (2012). Gut microbiota and obesity. Current Obesity Reports, 1(1), 1–8. doi:10.1007/s13679-011-0001-8.

    Article  PubMed Central  PubMed  Google Scholar 

  46. Musso, G., Gambino, R., & Cassader, M. (2010). Obesity, diabetes, and gut microbiota: The hygiene hypothesis expanded? Diabetes Care, 33(10), 2277–2284. doi:10.2337/dc10-0556.

    Article  PubMed Central  PubMed  Google Scholar 

  47. Salmon, J., Timperio, A., Chu, B., et al. (2010). Dog ownership, dog walking, and children’s and parents’ physical activity. Research Quarterly for Exercise and Sport, 81(3), 264–271.

    Article  PubMed  Google Scholar 

  48. Timperio, A., Salmon, J., Chu, B., et al. (2008). Is dog ownership or dog walking associated with weight status in children and their parents? Health Promotion Journal of Australia: Official Journal of Australian Association of Health Promotion Professionals, 19(1), 60–63.

    Google Scholar 

  49. Chu, S. Y., Kim, S. Y., Schmid, C. H., et al. (2007). Maternal obesity and risk of cesarean delivery: A meta-analysis. Obesity Reviews, 8(5), 385–394. doi:10.1111/j.1467-789X.2007.00397.x.

    Article  CAS  PubMed  Google Scholar 

  50. Pham, M. T., Brubaker, K., Pruett, K., et al. (2013). Risk of childhood obesity in the toddler offspring of mothers with gestational diabetes. Obstetrics and Gynecology, 121(5), 976–982. doi:10.1097/AOG.0b013e31828bf70d.

    Article  PubMed  Google Scholar 

  51. Collado, M. C., Isolauri, E., Laitinen, K., et al. (2008). Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. American Journal of Clinical Nutrition, 88(4), 894–899.

    CAS  PubMed  Google Scholar 

  52. Santacruz, A., Collado, M. C., Garcia-Valdes, L., et al. (2010). Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. British Journal of Nutrition, 104(1), 83–92. doi:10.1017/s0007114510000176.

    Article  CAS  PubMed  Google Scholar 

  53. Collado, M. C., Isolauri, E., Laitinen, K., et al. (2010). Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: A prospective follow-up study initiated in early pregnancy. American Journal of Clinical Nutrition, 92(5), 1023–1030. doi:10.3945/ajcn.2010.29877.

    Article  CAS  PubMed  Google Scholar 

  54. Luoto, R., Kalliomaki, M., Laitinen, K., et al. (2010). The impact of perinatal probiotic intervention on the development of overweight and obesity: Follow-up study from birth to 10 years. International Journal of Obesity, 34(10), 1531–1537. doi:10.1038/ijo.2010.50.

    Article  CAS  PubMed  Google Scholar 

  55. Yancey, A. K., Ortega, A. N., & Kumanyika, S. K. (2006). Effective recruitment and retention of minority research participants. Annual Review of Public Health, 27, 1–28. doi:10.1146/annurev.publhealth.27.021405.102113.

    Article  PubMed  Google Scholar 

  56. Flores, G., & Lin, H. (2013). Factors predicting overweight in US kindergartners. American Journal of Clinical Nutrition, 97(6), 1178–1187. doi:10.3945/ajcn.112.052019.

    Article  CAS  PubMed  Google Scholar 

  57. Lawlor, D. A., & Chaturvedi, N. (2006). Treatment and prevention of obesity—are there critical periods for intervention? International Journal of Epidemiology, 35(1), 3–9. doi:10.1093/ije/dyi309.

    Article  PubMed  Google Scholar 

  58. Blustein, J., Attina, T., Liu, M., et al. (2013). Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. International Journal of Obesity, 37(7), 900–906. doi:10.1038/ijo.2013.49.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the National Institutes of Health (R01 AI050681, R01 HL113010 and P01 AI089473) and the Fund for Henry Ford Hospital.

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Authors and Affiliations

  1. Department of Public Health Sciences, Henry Ford Hospital, 1 Ford Place, 5C, Detroit, MI, 48202, USA

    Andrea E. Cassidy-Bushrow, Ganesa Wegienka, Suzanne Havstad, Albert M. Levin, Kimberley J. Woodcroft & Christine Cole Johnson

  2. Center for Allergy, Asthma and Immunology Research, Henry Ford Hospital, Detroit, MI, USA

    Andrea E. Cassidy-Bushrow, Ganesa Wegienka, Suzanne Havstad, Albert M. Levin, Dennis R. Ownby, Kimberley J. Woodcroft, Edward M. Zoratti & Christine Cole Johnson

  3. Department of Medicine, University of California, San Francisco, CA, USA

    Susan V. Lynch

  4. Division of Allergy and Clinical Immunology, Department of Pediatrics, Georgia Regents University, Augusta, GA, USA

    Dennis R. Ownby

  5. Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA

    Andrew G. Rundle

  6. Division of Allergy and Clinical Immunology, Henry Ford Hospital, Detroit, MI, USA

    Edward M. Zoratti

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  1. Andrea E. Cassidy-Bushrow
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  2. Ganesa Wegienka
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Correspondence to Andrea E. Cassidy-Bushrow.

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Cassidy-Bushrow, A.E., Wegienka, G., Havstad, S. et al. Does Pet-Keeping Modify the Association of Delivery Mode with Offspring Body Size?. Matern Child Health J 19, 1426–1433 (2015). https://doi.org/10.1007/s10995-014-1649-y

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