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Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics
Abstract
Objective To investigate whether delivery mode (vaginal versus by caesarean section), maternal pre-pregnancy body mass index (BMI) and early exposure to antibiotics (<6 months of age) influence child's risk of overweight at age 7 years, hence supporting the hypotheses that environmental factors influencing the establishment and diversity of the gut microbiota are associated with later risk of overweight.Design Longitudinal, prospective study with measure of exposures in infancy and follow-up at age 7 years.Methods A total of 28 354 mother-child dyads from the Danish National Birth Cohort, with information on maternal pre-pregnancy BMI, delivery mode and antibiotic administration in infancy, were assessed. Logistic regression analyses were performed with childhood height and weight at the 7-year follow-up as outcome measures.Results Delivery mode was not significantly associated with childhood overweight (odds ratio (OR):1.18, 95% confidence interval (CI): 0.95-1.47). Antibiotics during the first 6 months of life led to increased risk of overweight among children of normal weight mothers (OR: 1.54, 95% CI: 1.09-2.17) and a decreased risk of overweight among children of overweight mothers (OR: 0.54, 95% CI: 0.30-0.98). The same tendency was observed among children of obese mothers (OR: 0.85, 95% CI: 0.41-1.76).Conclusion The present cohort study revealed that a combination of early exposures, including delivery mode, maternal pre-pregnancy BMI and antibiotics in infancy, influences the risk of overweight in later childhood. This effect may potentially be explained by an impact on establishment and diversity of the microbiota.
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“The use of antibiotics in early life is associated with obesity in both people and mice”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [122]
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“More recent publications have demonstrated that several weeks of subtherapeutic antibiotics increase fat mass and weight, particularly when begun during gestation (21, 22), and human epidemiological studies have demonstrated increased risk of becoming overweight when children were exposed early in life (23, 24).”
BackgroundMesquita, D. N., Barbieri, M. A., Goldani, H. A. S., Cardoso, V. C., Goldani, M. Z., Kac, G., da Sílva, A. A. M., & Bettiol, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066827 · Cited by 58
“[33].”
Intestinal microbiota during early life – impact on health and disease
Nylund, L., Satokari, R. M., Salminen, S., & de Vos, W. M. (2014) · Proceedings of The Nutrition Society · doi:10.1017/s0029665114000627 · Cited by 60
“Interestingly, early-life antibiotic treatment(s) have been associated with the increased risk for health problems later in life such as the risk for coeliac disease (CD) development((81)), allergic diseases((82)) and the increased risk of obesity at school age((83)).”
BackgroundAguayo, S. D., Schuh, C. M. A. P., Vicente, B., & Aguayo, L. G. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180319 · Cited by 62
Zhao, Y., Zhou, Y., Zhu, Q., Xia, B., Ma, W., Xiao, X., Shi, H., & Zhang, Y. (2018) · Environment International · doi:10.1016/j.envint.2018.11.053 · Cited by 57
Li, P., Chang, X., Chen, X., Wang, C., Shang, Y., Zheng, D., & Qi, K. (2022) · Annals of Clinical Microbiology and Antimicrobials · doi:10.1186/s12941-022-00535-1 · Cited by 60
Dey, P., Chaudhuri, S. R., Efferth, T., & Pal, S. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.09.026 · Cited by 59
Xiao, S., & Zhao, L. (2013) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12250 · Cited by 57
“, 2008), antibiotics administration (Ajslev et al., 2011), or gastrointestinal tract illnesses/surgery (Liou et al.”
BackgroundEarly‐life exercise may promote lasting brain and metabolic health through gut bacterial metabolites
Mika, A., & Fleshner, M. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.113 · Cited by 58
Chen, G., Chiang, W., Shu, B., Guo, Y. L., Chiou, S.-T., & Chiang, T. (2017) · BMJ Open · doi:10.1136/bmjopen-2017-017086 · Cited by 55
“16 Epidemiological studies also revealed an association between CS and overweight or obese preschool-aged children.(10) 11 Recently, a systematic review and meta-analysis indicated that CS is only moderately associated with overweight and obese children.”
Exploring the microbiome in health and disease
Scotti, E., Boué, S., Sasso, G. L., Zanetti, F., Belcastro, V., Poussin, C., Sierro, N., Battey, J. N. D., Gimalac, A., Ivanov, N. V., et al. (2017) · Toxicology Research and Application · doi:10.1177/2397847317741884 · Cited by 56
Influence of the human intestinal microbiome on obesity and metabolic dysfunction
Tilg, H., & Adolph, T. E. (2015) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000234 · Cited by 54
“Several large prospective clinical studies have now also demonstrated that ‘disturbance’ of the intestinal microbiota by either mode of delivery or antibiotic use might lead to childhood obesity [40,41].”
BackgroundMicrobiota, Antibiotics, and Obesity
Jess, T. (2014) · New England Journal of Medicine · doi:10.1056/nejmcibr1409799 · Cited by 53
Self-citationCesarean section may increase the risk of both overweight and obesity in preschool children
Rutayisire, E., Wu, X., Huang, K., Tao, S., Chen, Y., & Tao, F. (2016) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-016-1131-5 · Cited by 53
“In contrast, few studies reported no significant association between CS and overweight/obesity in children at the age of 6 or 7 [10, 11].”
ResultSutharsan, R., Mannan, M. A., Doi, S. A. R., & Mamun, A. A. (2015) · Clinical Obesity · doi:10.1111/cob.12114 · Cited by 52
“Study populations were regionally diverse and from Europe (23,31,32,35); North America (22,25,27,29); South America (12,33,47) and the Asia Pacific (28,34,36).”
BackgroundDevaux, C. A., & Raoult, D. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01379 · Cited by 53
“A study performed on a Danish cohort of 28,000 mother-child pairs, revealed that antibiotic exposure of children during the first 6 months of life was associated with increased risk of being overweight at age of 7 years (Ajslev et al., 2011).”
Association of Repeated Antibiotic Exposure Up to Age 4 Years With Body Mass at Age 4.5 Years
Chelimo, C., Camargo, C. A., Morton, S., & Grant, C. C. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2019.17577 · Cited by 52
“19) 201 (6) 44 (4) 21 (5) Watching television, DVDs, or videos, weekday, h (n = 4929) 0 0.”
Isolauri, E. (2017) · Nestlé Nutrition Institute Workshop series · doi:10.1159/000455217 · Cited by 49
Beyond gut microbiota: understanding obesity and type 2 diabetes
Lau, E., Carvalho, D. M., Pina‐Vaz, C., Barbosa, J.-A., & Freitas, P. (2015) · HORMONES · doi:10.14310/horm.2002.1571 · Cited by 56
Does the Gut Microbiota Contribute to Obesity? Going beyond the Gut Feeling
Aguirre, M., & Venema, K. (2015) · Microorganisms · doi:10.3390/microorganisms3020213 · Cited by 52
Goldani, M. Z., Barbieri, M. A., da Sílva, A. A. M., Gutierrez, M. R. P., Bettiol, H., & Goldani, H. A. S. (2013) · Nutrition Journal · doi:10.1186/1475-2891-12-104 · Cited by 50
“However, they observed that antibiotic use before 6 months of age was associated with increased risk of overweight among children of normal weight mothers delivered by CS and also described a tendency towards increased risk of overweight in boys delivered by CS [18].”
BackgroundResultThe association between caesarean section and childhood obesity revisited: a cohort study
Flemming, K., Woolcott, C. G., Allen, A. C., Veugelers, P. J., & Kuhle, S. (2013) · Archives of Disease in Childhood · doi:10.1136/archdischild-2012-303459 · Cited by 50
Klančič, T., & Reimer, R. A. (2019) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2019.04.004 · Cited by 53
Antibiotic administration and the development of obesity in children
Principi, N., & Esposito, S. (2016) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2015.12.017 · Cited by 70
Cesarean section and the risk of overweight in grade 6 children
Wang, L., Alamian, A., Southerland, J. L., Wang, K.-S., Anderson, J. L., & Stevens, M. (2013) · European Journal of Pediatrics · doi:10.1007/s00431-013-2043-2 · Cited by 40
Rooney, A. M., Timberlake, K., Brown, K. A., Bansal, S., Tomlinson, C., Lee, K., Science, M. E., & Coburn, B. A. (2019) · Clinical Infectious Diseases · doi:10.1093/cid/ciz698 · Cited by 46
“…anti-microbial exposure (greater than 3 or 5 days) is associated with short-term complications including necrotizing enterocolitis (NEC), hospital-acquired infection, and mortality [3, 4], as well as long-term health outcomes including obesity, allergy, and inflammatory bowel disease [5–7].”
Gut Microbiota Drives Metabolic Disease in Immunologically Altered Mice
Chassaing, B., Aitken, J. D., Gewirtz, A. T., & Vijay–Kumar, M. (2012) · Advances in immunology · doi:10.1016/b978-0-12-394300-2.00003-x · Cited by 51
Meier, T., Senftleben, K., Deumelandt, P., Christen, O., Riedel, K., & Langer, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135990 · Cited by 55
“Recent work by Ajslev et al. (2011) [58], Cho et al. (2012) [59] and Trasande et al. (2013) [60] has shown in animal and human trials that antibiotic treatments in early youth/ childhood may stimulate overweight/obesity by way of an altered gut…”
Preterm gut microbiota and metabolome following discharge from intensive care
Stewart, C. J., Skeath, T., Nelson, A., Fernstad, S. J., Marrs, E. C. L., Perry, J. D., Cummings, S. P., Berrington, J. E., & Embleton, N. D. (2015) · Scientific Reports · doi:10.1038/srep17141 · Cited by 48
Fouhy, F., Ronan, N. J., O’Sullivan, Ó., McCarthy, Y., Walsh, A. M., Murphy, D. M., Daly, M., Flanagan, E., Fleming, C., McCarthy, M. M., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-06880-y · Cited by 49
Potential Role of Curcumin Against Biofilm‐Producing Organisms on the Skin: A Review
Vaughn, A. R., Haas, K. N., Burney, W. A., Andersen, E., Clark, A. K., Crawford, R., & Sivamani, R. K. (2017) · Phytotherapy Research · doi:10.1002/ptr.5912 · Cited by 51
“In addition to antibiotic resistance, overprescription of antibiotics may contribute to childhood obesity and respiratory and urinary tract infections even after treatment has ended (Ajslev et al., 2011; Margolis et al., 2005).”
Background
Metadata
- Authors
- Ajslev, T. A., Andersen, C. S., Gamborg, M., Sørensen, T. I. A., & Jess, T.
- Affiliations
- Copenhagen University Hospital (DK)
- Corresponding author
- Ajslev, T A
- Venue
- International Journal of Obesity
- Published
- 2011-03-08
- Volume
- 35
- Issue
- 4
- Pages
- 522-529
- ISSN
- 0307-0565 (ISSN-L)
- 1476-5497
- OpenAlex
- W2003202328
- Cited by
- 534
- References
- 36
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 17 · 2023: 20 · 2022: 27 · 2021: 36 · 2020: 51 · 2019: 54 · 2018: 51 · 2017: 51 · 2016: 54 · 2015: 59 · 2014: 32 · 2013: 33 · 2012: 21
- FWCI
- 11.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- International Journal of Obesity (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Obesity, Physical Activity, Diet
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- childhood overweight, gut microbiota, mode of delivery, cesarean section, vaginal delivery, maternal pre-pregnancy BMI, maternal obesity, early antibiotic exposure, infancy, environmental risk factors
- MeSH terms
- Adolescent, Adult, Anti-Bacterial Agents, Cesarean Section, Child, Female, Humans, Infant, Newborn, Longitudinal Studies, Male, Mothers, Obesity, Pregnancy, Prospective Studies, Surveys and Questionnaires, Risk Factors, Body Mass Index, Delivery, Obstetric, Gastrointestinal Tract, Metagenome, Young Adult
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