Antibiotic exposure in early life increases risk of childhood obesity: A systematic review and meta-analysis

Frontiers in Endocrinology

Volumn 8, Issue JUL, 2017, Pages

  Shao, Xiaoqing ^a   Ding, Xiaolian ^b   Wang, Bin ^a   Li, Ling ^a   An, Xiaofei ^a   Yao, Qiuming ^a   Song, Ronghua ^a   Zhang, Jin An ^a  

^a JINSHAN HOSPITAL OF FUDAN UNIVERSITY   (China)

^b Central Hospital of Weinan City   (China)

Author keywords

Antibiotics; Childhood obesity; Meta analysis; Overweight; Risk factor

Indexed keywords

ANTIBIOTIC AGENT;

ARTICLE; BODY MASS; BODY WEIGHT; CHILDHOOD OBESITY; DRUG EXPOSURE; HUMAN; PRENATAL EXPOSURE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK FACTOR; SYSTEMATIC REVIEW;

EID: 85025664354     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2017.00170     Document Type: Article

References (69)

1. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet (2014) 384(9945):766-81. doi:10.1016/S0140-6736(14)60460-8
2. Cunningham SA, Kramer MR, Narayan KM. Incidence of childhood obesity in the United States. N Engl J Med (2014) 370(5):403-11. doi:10.1056/NEJMoa1309753
3. Ogden CL, Carroll MD, Lawman HG, Fryar CD, Kruszon-Moran D, Kit BK, et al. Trends in obesity prevalence among children and adolescents in the United States, 1988-1994 through 2013-2014. JAMA (2016) 315(21):2292-9. doi:10.1001/jama.2016.6361
4. Simmonds M, Llewellyn A, Owen CG, Woolacott N. Predicting adult obesity from childhood obesity: a systematic review and meta-analysis. Obes Rev (2016) 17(2):95-107. doi:10.1111/obr.12334
5. Llewellyn A, Simmonds M, Owen CG, Woolacott N. Childhood obesity as a predictor of morbidity in adulthood: a systematic review and meta-analysis. Obes Rev (2016) 17(1):56-67. doi:10.1111/obr.12316
6. Sherman M. The relationship between obesity and depression in children and adolescents. Obes Rev (2016) 17(9):915-6. doi:10.1111/obr.12438
7. Munthali RJ, Kagura J, Lombard Z, Norris SA. Childhood adiposity trajectories are associated with late adolescent blood pressure: birth to twenty cohort. BMC Public Health (2016) 16:665. doi:10.1186/s12889-016-3337-x
8. Black MH, Zhou H, Takayanagi M, Jacobsen SJ, Koebnick C. Increased asthma risk and asthma-related health care complications associated with childhood obesity. Am J Epidemiol (2013) 178(7):1120-8. doi:10.1093/aje/kwt093
9. Cote AT, Harris KC, Panagiotopoulos C, Sandor GG, Devlin AM. Childhood obesity and cardiovascular dysfunction. J Am Coll Cardiol (2013) 62(15):1309-19. doi:10.1016/j.jacc.2013.07.042
10. Skinner AC, Skelton JA. Prevalence and trends in obesity and severe obesity among children in the United States, 1999-2012. JAMA Pediatr (2014) 168(6):561-6. doi:10.1001/jamapediatrics.2014.21
11. Lemas DJ, Yee S, Cacho N, Miller D, Cardel M, Gurka M, et al. Exploring the contribution of maternal antibiotics and breastfeeding to development of the infant microbiome and pediatric obesity. Semin Fetal Neonatal Med (2016) 21:406-9. doi:10.1016/j.siny.2016.04.013
12. Yallapragada SG, Nash CB, Robinson DT. Early-life exposure to antibiotics, alterations in the intestinal microbiome, and risk of metabolic disease in children and adults. Pediatr Ann (2015) 44(11):e265-9. doi:10.3928/00904481-20151112-09
13. Mikkelsen KH, Allin KH, Knop FK. Effect of antibiotics on gut microbiota, glucose metabolism and body weight regulation: a review of the literature. Diabetes Obes Metab (2016) 18(5):444-53. doi:10.1111/dom.12637
14. Jess T. Microbiota, antibiotics, and obesity. N Engl J Med (2014) 371(26):2526-8. doi:10.1056/NEJMcibr1409799
15. Keeney KM, Yurist-Doutsch S, Arrieta MC, Finlay BB. Effects of antibiotics on human microbiota and subsequent disease. Annu Rev Microbiol (2014) 68:217-35. doi:10.1146/annurev-micro-091313-103456
16. Principi N, Esposito S. Antibiotic administration and the development of obesity in children. Int J Antimicrob Agents (2016) 47(3):171-7. doi:10.1016/j.ijantimicag.2015.12.017
17. Ajslev TA, Andersen CS, Gamborg M, Sorensen TI, Jess T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes (Lond) (2011) 35(4):522-9. doi:10.1038/ijo.2011.27
18. Murphy R, Thompson JM, Mitchell EA. Early antibiotic exposure and body mass index in children born small for gestational age. Acta Paediatr (2013) 102(9):e434-5. doi:10.1111/apa.12307
19. Bailey LC, Forrest CB, Zhang P, Richards TM, Livshits A, DeRusso PA. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr (2014) 168(11):1063-9. doi:10.1001/jamapediatrics.2014.1539
20. Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG, Widen EM, et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes (Lond) (2015) 39(4):665-70. doi:10.1038/ijo.2014.180
21. Gerber JS, Bryan M, Ross RK, Daymont C, Parks EP, Localio AR, et al. Antibiotic exposure during the first 6 months of life and weight gain during childhood. JAMA (2016) 315(12):1258-65. doi:10.1001/jama.2016.2395
22. Mbakwa CA, Scheres L, Penders J, Mommers M, Thijs C, Arts IC. Early life antibiotic exposure and weight development in children. J Pediatr (2016) 176:105-13.e2. doi:10.1016/j.jpeds.2016.06.015
23. Trasande L, Blustein J, Liu M, Corwin E, Cox LM, Blaser MJ. Infant antibiotic exposures and early-life body mass. Int J Obes (Lond) (2013) 37(1):16-23. doi:10.1038/ijo.2012.132
24. Azad M, Bridgman SL, Becker AB, Kozyrskyj AL. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Int J Obes (Lond) (2014) 38(10):1290-8. doi:10.1038/ijo.2014.119
25. Wells G, Shea B, O'connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses. Ottawa: Ottawa Health Research Institute (2015). Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
26. Cochran WG. The combination of estimates from different experiments. Biometrics (1954) 10(1):101-29. doi:10.2307/3001666
27. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ (2003) 327(7414):557-60. doi:10.1136/bmj.327.7414.557
28. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials (1986) 7(3):177-88. doi:10.1016/0197-2456(86)90046-2
29. Li DK, Chen H, Ferber J, Odouli R. Infection and antibiotic use in infancy and risk of childhood obesity: a longitudinal birth cohort study. Lancet Diabetes Endocrinol (2016) 5:18-25. doi:10.1016/S2213-8587(16)30281-9
30. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ (1997) 315(7109):629-34. doi:10.1136/bmj.315.7109.629
31. Orsini N, Bellocco R, Greenland S. Generalized least squares for trend estimation of summarized dose-response data. Stata J (2006) 6(1):40-57
32. Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol (2012) 175(1):66-73. doi:10.1093/aje/kwr265
33. Halldorsson T, Rytter D, Haug LS, Bech BH, Danielsen I, Becher G, et al. Prenatal exposure to perfluorooctanoate and risk of overweight at 20 years of age: a prospective cohort study. Environ Health Perspect (2012) 120(5):668-73. doi:10.1289/ehp.1104034
34. Trehan I, Goldbach HS, LaGrone LN, Meuli GJ, Wang RJ, Maleta KM, et al. Antibiotics as part of the management of severe acute malnutrition. N Engl J Med (2013) 368(5):425-35. doi:10.1056/NEJMoa1202851
35. Vidal AC, Murphy SK, Murtha AP, Schildkraut JM, Soubry A, Huang Z, et al. Associations between antibiotic exposure during pregnancy, birth weight and aberrant methylation at imprinted genes among offspring. Int J Obes (Lond) (2013) 37(7):907-13. doi:10.1038/ijo.2013.47
36. Angelakis E, Million M, Kankoe S, Lagier JC, Armougom F, Giorgi R, et al. Abnormal weight gain and gut microbiota modifications are side effects of long-term doxycycline and hydroxychloroquine treatment. Antimicrob Agents Chemother (2014) 58(6):3342-7. doi:10.1128/AAC.02437-14
37. Murphy R, Stewart AW, Braithwaite I, Beasley R, Hancox RJ, Mitchell EA, et al. Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obes (Lond) (2014) 38(8):1115-9. doi:10.1038/ijo.2013.218
38. Krenz-Niedbala M, Koscinski K, Puch EA, Zelent A, Breborowicz A. Is the relationship between breastfeeding and childhood risk of asthma and obesity mediated by infant antibiotic treatment? Breastfeed Med (2015) 10(6):326-33. doi:10.1089/bfm.2014.0173
39. Mor A, Antonsen S, Kahlert J, Holsteen V, Jorgensen S, Holm-Pedersen J, et al. Prenatal exposure to systemic antibacterials and overweight and obesity in Danish schoolchildren: a prevalence study. Int J Obes (Lond) (2015) 39(10):1450-5. doi:10.1038/ijo.2015.129
40. Rogawski ET, Westreich DJ, Adair LS, Becker-Dreps S, Sandler RS, Sarkar R, et al. Early life antibiotic exposure is not associated with growth in young children of Vellore, India. J Pediatr (2015) 167(5):1096-2.e3. doi:10.1016/j.jpeds.2015.08.015
41. Saari A, Virta LJ, Sankilampi U, Dunkel L, Saxen H. Antibiotic exposure in infancy and risk of being overweight in the first 24 months of life. Pediatrics (2015) 135(4):617-26. doi:10.1542/peds.2014-3407
42. Korpela K, Salonen A, Virta LJ, Kekkonen RA, de Vos WM. Association of early-life antibiotic use and protective effects of breastfeeding: role of the intestinal microbiota. JAMA Pediatr (2016) 170(8):750-7. doi:10.1001/jamapediatrics.2016.0585
43. Korpela K, Salonen A, Virta LJ, Kekkonen RA, Forslund K, Bork P, et al. Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children. Nat Commun (2016) 7:10410. doi:10.1038/ncomms10410
44. Schwartz BS, Pollak J, Bailey-Davis L, Hirsch AG, Cosgrove SE, Nau C, et al. Antibiotic use and childhood body mass index trajectory. Int J Obes (Lond) (2016) 40(4):615-21. doi:10.1038/ijo.2015.218
45. Scott FI, Horton DB, Mamtani R, Haynes K, Goldberg DS, Lee DY, et al. Administration of antibiotics to children before age 2 years increases risk for childhood obesity. Gastroenterology (2016) 151(1):120-9.e5. doi:10.1053/j.gastro.2016.03.006
46. Wang H, Wang N, Wang B, Fang H, Fu C, Tang C, et al. Antibiotics detected in urines and adipogenesis in school children. Environ Int (2016) 89-90:204-11. doi:10.1016/j.envint.2016.02.005
47. Reijnders D, Goossens GH, Hermes GD, Neis EP, van der Beek CM, Most J, et al. Effects of gut microbiota manipulation by antibiotics on host metabolism in obese humans: a randomized double-blind placebo-controlled trial. Cell Metab (2016) 24(1):63-74. doi:10.1016/j.cmet.2016.06.016
48. Ville A, Heyman MB, Medrano R, Wojcicki JM. Early antibiotic exposure and risk of childhood obesity in Latinos. Child Obes (2017) 13:231-5. doi:10.1089/chi.2016.0235
49. Poulsen M, Pollak J, Bailey-Davis L, Hirsch AG, Glass TA, Schwartz BS. Associations of prenatal and childhood antibiotic use with child body mass index at age 3 years. Obesity (Silver Spring) (2017) 25(2):438-44. doi:10.1002/oby.21719
50. Manco M, Putignani L, Bottazzo GF. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev (2010) 31(6):817-44. doi:10.1210/er.2009-0030
51. Guyenet SJ, Schwartz MW. Clinical review: regulation of food intake, energy balance, and body fat mass: implications for the pathogenesis and treatment of obesity. J Clin Endocrinol Metab (2012) 97(3):745-55. doi:10.1210/jc.2011-2525
52. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science (2013) 341(6150):1241214. doi:10.1126/science.1241214
53. Winer DA, Luck H, Tsai S, Winer S. The intestinal immune system in obesity and insulin resistance. Cell Metab (2016) 23(3):413-26. doi:10.1016/j.cmet.2016.01.003
54. Ussar S, Griffin NW, Bezy O, Fujisaka S, Vienberg S, Softic S, et al. Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metab (2015) 22(3):516-30. doi:10.1016/j.cmet.2015.07.007
55. Hersoug LG, Moller P, Loft S. Gut microbiota-derived lipopolysaccharide uptake and trafficking to adipose tissue: implications for inflammation and obesity. Obes Rev (2016) 17(4):297-312. doi:10.1111/obr.12370
56. Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol Metab (2015) 26(9):493-501. doi:10.1016/j.tem.2015.07.002
57. Pihl AF, Fonvig CE, Stjernholm T, Hansen T, Pedersen O, Holm JC. The role of the gut microbiota in childhood obesity. Child Obes (2016) 12(4):292-9. doi:10.1089/chi.2015.0220
58. Nicolucci AC, Hume MP, Martinez I, Mayengbam S, Walter J, Reimer RA. Prebiotic reduces body fat and alters intestinal microbiota in children with overweight or obesity. Gastroenterology (2017). doi:10.1053/j.gastro.2017.05.055
59. Angelakis E, Merhej V, Raoult D. Related actions of probiotics and antibiotics on gut microbiota and weight modification. Lancet Infect Dis (2013) 13(10):889-99. doi:10.1016/S1473-3099(13)70179-8
60. Mahana D, Trent CM, Kurtz ZD, Bokulich NA, Battaglia T, Chung J, et al. Antibiotic perturbation of the murine gut microbiome enhances the adiposity, insulin resistance, and liver disease associated with high-fat diet. Genome Med (2016) 8(1):48. doi:10.1186/s13073-016-0297-9
61. Hwang I, Park YJ, Kim YR, Kim YN, Ka S, Lee HY, et al. Alteration of gut microbiota by vancomycin and bacitracin improves insulin resistance via glucagon-like peptide 1 in diet-induced obesity. FASEB J (2015) 29(6):2397-411. doi:10.1096/fj.14-265983
62. Cho I, Yamanishi S, Cox L, Methe BA, Zavadil J, Li K, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature (2012) 488(7413):621-6. doi:10.1038/nature11400
63. Uijtdewilligen L, Waters CN, Muller-Riemenschneider F, Lim YW. Preventing childhood obesity in Asia: an overview of intervention programmes. Obes Rev (2016) 17:1103-15. doi:10.1111/obr.12435
64. Nishtar S, Gluckman P, Armstrong T. Ending childhood obesity: a time for action. Lancet (2016) 387(10021):825-7. doi:10.1016/S0140-6736(16)00140-9
65. Cauchi D, Glonti K, Petticrew M, Knai C. Environmental components of childhood obesity prevention interventions: an overview of systematic reviews. Obes Rev (2016) 17:1116-30. doi:10.1111/obr.12441
66. Barker CI, Standing JF, Turner MA, McElnay JC, Sharland M. Antibiotic dosing in children in Europe: can we grade the evidence from pharmacokinetic/pharmacodynamic studies-and when is enough data enough? Curr Opin Infect Dis (2012) 25(3):235-42. doi:10.1097/QCO.0b013e328353105c
67. Kaliannan K, Wang B, Li XY, Bhan AK, Kang JX. Omega-3 fatty acids prevent early-life antibiotic exposure-induced gut microbiota dysbiosis and later-life obesity. Int J Obes (Lond) (2016) 40(6):1039-42. doi:10.1038/ijo.2016.27
68. Economopoulos KP, Ward NL, Phillips CD, Teshager A, Patel P, Mohamed MM, et al. Prevention of antibiotic-associated metabolic syndrome in mice by intestinal alkaline phosphatase. Diabetes Obes Metab (2016) 18(5):519-27. doi:10.1111/dom.12645
69. Forrest CB, Block JP, Bailey LC. Antibiotics, infections, and childhood obesity. Lancet Diabetes Endocrinol (2016) 5:2-3. doi:10.1016/S2213-8587(16)30314-X