Advertisement

Maternal and Child Health Journal

, Volume 19, Issue 6, pp 1426–1433 | Cite as

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

  • Andrea E. Cassidy-Bushrow
  • Ganesa Wegienka
  • Suzanne Havstad
  • Albert M. Levin
  • Susan V. Lynch
  • Dennis R. Ownby
  • Andrew G. Rundle
  • Kimberley J. Woodcroft
  • Edward M. Zoratti
  • Christine Cole Johnson
Article

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.

Keywords

Birth cohort Childhood obesity Delivery mode Companion animals 

Notes

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.

References

  1. 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.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  4. 4.
    Menacker, F., & Hamilton, B. E. (2010). Recent trends in cesarean delivery in the United States. NCHS Data Brief, 35, 1–8.PubMedGoogle Scholar
  5. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  17. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. 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.PubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  25. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  26. 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. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  28. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  31. 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. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  33. 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. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  38. 38.
    Greenland, S. (1989). Modeling and variable selection in epidemiologic analysis. American Journal of Public Health, 79(3), 340–349.CrossRefPubMedCentralPubMedGoogle Scholar
  39. 39.
    Selvin, S. (1996). Statistical analysis of epidemiologic data (2nd ed.). New York: Oxford University Press.Google Scholar
  40. 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.PubMedCentralPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  46. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 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. 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.CrossRefPubMedGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 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.PubMedGoogle Scholar
  52. 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.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 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.CrossRefPubMedGoogle Scholar
  57. 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.CrossRefPubMedGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Andrea E. Cassidy-Bushrow
    • 1
    • 2
  • Ganesa Wegienka
    • 1
    • 2
  • Suzanne Havstad
    • 1
    • 2
  • Albert M. Levin
    • 1
    • 2
  • Susan V. Lynch
    • 3
  • Dennis R. Ownby
    • 2
    • 4
  • Andrew G. Rundle
    • 5
  • Kimberley J. Woodcroft
    • 1
    • 2
  • Edward M. Zoratti
    • 2
    • 6
  • Christine Cole Johnson
    • 1
    • 2
  1. 1.Department of Public Health SciencesHenry Ford HospitalDetroitUSA
  2. 2.Center for Allergy, Asthma and Immunology ResearchHenry Ford HospitalDetroitUSA
  3. 3.Department of MedicineUniversity of CaliforniaSan FranciscoUSA
  4. 4.Division of Allergy and Clinical Immunology, Department of PediatricsGeorgia Regents UniversityAugustaUSA
  5. 5.Department of Epidemiology, Mailman School of Public HealthColumbia UniversityNew YorkUSA
  6. 6.Division of Allergy and Clinical ImmunologyHenry Ford HospitalDetroitUSA

Personalised recommendations