Early-life antibiotic exposure, gut microbiome, and colonization resistance
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Published:
Dec 27, 2019
Keywords:
gut microbiota antibiotic exposure
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Abstract
Antibiotics are chemical compounds that inhibit the growth of microorganisms to fight bacterial infections and, therefore, have been a central pillar of modern medicine. In recent years, there has been increasing awareness of the rising rate of their global consumption, especially in younger age groups. Exposure to antibiotics could happen not only during the first few months of newborns, but also indirectly through maternal consumption during pregnancy as well as during delivery. Indeed, epidemiological findings and meta-analyses have confirmed the association between early antibiotic exposures and risks for allergenic diseases and obesity. Recent gut microbiome studies have provided mechanistic evidence supporting the role of antibiotic-induced dysbiotic gut microbiota in developing those diseases. However, no mechanistic evidence is available to convince restorative powers of breastfeeding on the disrupted gut microbiome and intestinal barrier function following antibiotic exposures in early-life. To address the fundamental questions related to complex traits of both exposure to antibiotic and breastfeeding’s impacts in early-life, new experimental models are needed to differentiate short- and long-term effects of prenatal vs early postnatal exposure to antibiotics on gut microbiome and resistome (i.e., the collection of antibiotic resistance genes) of newborns.
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TUN, H. M., & BRUZZONE, R. (2019). Early-life antibiotic exposure, gut microbiome, and colonization resistance. Journal of Health Science and Alternative Medicine, 1(3), 1–5. Retrieved from https://he01.tci-thaijo.org/index.php/jhealthscialternmed/article/view/227149
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References
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[29] Lynn MA, Tumes DJ, Choo JM, Sribnaia A, Blake SJ, Leong LEX, et al. Early-life antibiotic-driven dysbiosis leads to dysregulated vaccine immune responses in mice. Cell Host Microbe. 2018;23:653-60 e5.
[30] Jin S, Zhao D, Cai C, Song D, Shen J, Xu A, et al. Low-dose penicillin exposure in early life decreases Th17 and the susceptibility to DSS colitis in mice through gut microbiota modification. Sci Rep. 2017;7:43662.
[31] Gonzalez-Perez G, Hicks AL, Tekieli TM, Radens CM, Williams BL, Lamouse-Smith ES. Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J Immunol. 2016;196:3768-79.
[32] Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Teitler I, et al. Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun. 2015;6:7486.
[33] Greenwood C, Morrow AL, Lagomarcino AJ, Altaye M, Taft DH, Yu Z, et al. Early empiric antibiotic use in preterm infants is associated with lower bacterial diversity and higher relative abundance of Enterobacter. J Pediatr. 2014;165:23-9.
[34] Tanaka S, Kobayashi T, Songjinda P, Tateyama A, Tsubouchi M, Kiyohara C, et al. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol Med Microbiol. 2009;56:80-7.
[35] Stokholm J, Schjorring S, Pedersen L, Bischoff AL, Folsgaard N, Carson CG, et al. Prevalence and predictors of antibiotic administration during pregnancy and birth. PLoS One. 2013;8:e82932.
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[37] Gosalbes MJ, Valles Y, Jimenez-Hernandez N, Balle C, Riva P, Miravet-Verde S, et al. High frequencies of antibiotic resistance genes in infants' meconium and early fecal samples. J Dev Orig Health Dis. 2016;7:35-44.
[38] Gueimonde M, Salminen S, Isolauri E. Presence of specific antibiotic (tet) resistance genes in infant faecal microbiota. FEMS Immunol Med Microbiol. 2006;48:21-5.
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[41] Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197:435-8.
[42] Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, Young VB. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes. 2011;2:145-58.
[43] Schubert AM, Sinani H, Schloss PD. Antibiotic-induced alterations of the murine gut microbiota and subsequent effects on colonization resistance against Clostridium difficile. MBio. 2015;6:e00974.
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[45] Hendrickx AP, Top J, Bayjanov JR, Kemperman H, Rogers MR, Paganelli FL. Antibiotic-driven dysbiosis mediates intraluminal agglutination and alternative segregation of Enterococcus faecium from the intestinal epithelium. MBio. 2015;6:e01346-15.
[46] Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790-801.
[47] Kim S, Covington A, Pamer EG. The intestinal microbiota: antibiotics, colonization resistance, and enteric pathogens. Immunol Rev. 2017;279:90-105.
[48] Rautava S. Early microbial contact, the breast milk microbiome and child health. J Dev Orig Health Dis. 2016;7:5-14.
[49] Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21:109-117.
[50] Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511-21.
[51] Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690-703.
[52] Forbes JD, Azad MB, Vehling L, Tun HM, Konya TB, Guttman DS, et al. Association of exposure to formula in the hospital and subsequent infant feeding practices with gut microbiota and risk of overweight in the first year of life. JAMA Pediatr. 2018;172:e181161.
[53] Parnanen K, Karkman A, Hultman J, Lyra C, Bengtsson-Palme J, Larsson DGJ, et al. Maternal gut and breast milk microbiota affect infant gut antibiotic resistome and mobile genetic elements. Nat Commun. 2018;9:3891.
[54] Bonang G, Monintja HE, Sujudi, van der Waaij D. Influence of breastmilk on the development of resistance to intestinal colonization in infants born at the Atma Jaya Hospital, Jakarta. Scand J Infect Dis. 2000;32:189-96.
[2] Youngster I, Avorn J, Belleudi V, Cantarutti A, Díez-Domingo J, Kirchmayer U et al. Antibiotic use in children–a cross-national analysis of 6 countries. J Pediatr. 2017;182:239-244.
[3] Shulman ST, Bisno AL, Clegg HW, Gerber MA, Kaplan EL, Lee G, et al. Clinical practice guideline for the diagnosis and management of group A streptococcal pharyngitis: 2012 update by the Infectious Diseases Society of America. Clin Infect Dis. 2012;55:1279-82.
[4] Robinson JL, Finlay JC, Lang ME, Bortolussi R, Canadian Paediatric Society ID, Immunization Committee CPC. Urinary tract infections in infants and children: diagnosis and management. Paediatr Child Health. 2014;19:315-25.
[5] Obiakor CV, Tun HM, Bridgman SL, Arrieta MC, Kozyrskyj AL. The association between early life antibiotic use and allergic disease in young children: recent insights and their implications. Expert Rev Clin Immunol. 2018;14:841-55.
[6] Steinman MA, Gonzales R, Linder JA, Landefeld CS. Changing use of antibiotics in community-based outpatient practice, 1991-1999. Ann Intern Med. 2003;138:525-33.
[7] Versporten A, Bielicki J, Drapier N, Sharland M, Goossens H, group Ap. The Worldwide Antibiotic Resistance and Prescribing in European Children (ARPEC) point prevalence survey: developing hospital-quality indicators of antibiotic prescribing for children. J Antimicrob Chemother. 2016;71:1106-17.
[8] Persaud RR, Azad MB, Chari RS, Sears MR, Becker AB, Kozyrskyj AL, et al. Perinatal antibiotic exposure of neonates in Canada and associated risk factors: a population-based study. J Matern Fetal Neonatal Med. 2015;28:1190-5.
[9] Murk W, Risnes KR, Bracken MB. Prenatal or early-life exposure to antibiotics and risk of childhood asthma: a systematic review. Pediatrics. 2011;127:1125-38.
[10] Penders J, Kummeling I, Thijs C. Infant antibiotic use and wheeze and asthma risk: a systematic review and meta-analysis. Eur Respir J. 2011;38:295-302.
[11] Shao X, Ding X, Wang B, Li L, An X, Yao Q, et al. Antibiotic exposure in early life increases risk of childhood obesity: a systematic review and meta-analysis. Front Endocrinol (Lausanne). 2017;8:170.
[12] Blaser MJ. Antibiotic use and its consequences for the normal microbiome. Science. 2016;352:544-5.
[13] Yassour M, Vatanen T, Siljander H, Hämäläinen AM, Härkönen T, Ryhänen SJ. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med. 2016;8:343ra81-343ra81.
[14] Kumar P, Magon N. Hormones in pregnancy. Niger Med J. 2012;53:179-83.
[15] Nuriel-Ohayon M, Neuman H, Koren O. Microbial changes during pregnancy, birth, and infancy. Front Microbiol. 2016;7:1031.
[16] Stokholm J, Schjorring S, Eskildsen CE, Pedersen L, Bischoff AL, Folsgaard N, et al. Antibiotic use during pregnancy alters the commensal vaginal microbiota. Clin Microbiol Infect. 2014;20:629-35.
[17] Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;351:1296-302.
[18] Unicef. Breastfeeding: a mother’s gift, for every child. Unicef. 2018.
[19] WHO. Guideline: protecting, promoting and supporting breastfeeding in facilities providing maternity and newborn services (No. 9789241550086). WHO. 2017.
[20] Azad MB, Konya T, Persaud RR, Guttman DS, Chari RS, Field CJ, et al. Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: a prospective cohort study. BJOG. 2016;123:983-93.
[21] Yassour M, Vatanen T, Siljander H, Hamalainen AM, Harkonen T, Ryhanen SJ, et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med. 2016;8:343ra81.
[22] Yasmin F, Tun HM, Konya TB, Guttman DS, Chari RS, Field CJ, et al. Cesarean section, formula feeding, and infant antibiotic exposure: separate and combined impacts on gut microbial changes in later infancy. Front Pediatr. 2017;5:200.
[23] Yoshimoto A, Uebanso T, Nakahashi M, Shimohata T, Mawatari K, Takahashi A. Effect of prenatal administration of low dose antibiotics on gut microbiota and body fat composition of newborn mice. J Clin Biochem Nutr. 2018;62:155-60.
[24] Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 2012;13:440-7.
[25] Leclercq S, Mian FM, Stanisz AM, Bindels LB, Cambier E, Ben-Amram H, et al. Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat Commun. 2017;8:15062.
[26] 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;488:621-6.
[27] Candon S, Perez-Arroyo A, Marquet C, Valette F, Foray AP, Pelletier B, et al. Antibiotics in early life alter the gut microbiome and increase disease incidence in a spontaneous mouse model of autoimmune insulin-dependent diabetes. PLoS One. 2015;10:e0125448.
[28] Tormo-Badia N, Hakansson A, Vasudevan K, Molin G, Ahrne S, Cilio CM. Antibiotic treatment of pregnant non-obese diabetic mice leads to altered gut microbiota and intestinal immunological changes in the offspring. Scand J Immunol. 2014;80:250-60.
[29] Lynn MA, Tumes DJ, Choo JM, Sribnaia A, Blake SJ, Leong LEX, et al. Early-life antibiotic-driven dysbiosis leads to dysregulated vaccine immune responses in mice. Cell Host Microbe. 2018;23:653-60 e5.
[30] Jin S, Zhao D, Cai C, Song D, Shen J, Xu A, et al. Low-dose penicillin exposure in early life decreases Th17 and the susceptibility to DSS colitis in mice through gut microbiota modification. Sci Rep. 2017;7:43662.
[31] Gonzalez-Perez G, Hicks AL, Tekieli TM, Radens CM, Williams BL, Lamouse-Smith ES. Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J Immunol. 2016;196:3768-79.
[32] Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Teitler I, et al. Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun. 2015;6:7486.
[33] Greenwood C, Morrow AL, Lagomarcino AJ, Altaye M, Taft DH, Yu Z, et al. Early empiric antibiotic use in preterm infants is associated with lower bacterial diversity and higher relative abundance of Enterobacter. J Pediatr. 2014;165:23-9.
[34] Tanaka S, Kobayashi T, Songjinda P, Tateyama A, Tsubouchi M, Kiyohara C, et al. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol Med Microbiol. 2009;56:80-7.
[35] Stokholm J, Schjorring S, Pedersen L, Bischoff AL, Folsgaard N, Carson CG, et al. Prevalence and predictors of antibiotic administration during pregnancy and birth. PLoS One. 2013;8:e82932.
[36] Gibson MK, Crofts TS, Dantas G. Antibiotics and the developing infant gut microbiota and resistome. Curr Opin Microbiol. 2015;27:51-6.
[37] Gosalbes MJ, Valles Y, Jimenez-Hernandez N, Balle C, Riva P, Miravet-Verde S, et al. High frequencies of antibiotic resistance genes in infants' meconium and early fecal samples. J Dev Orig Health Dis. 2016;7:35-44.
[38] Gueimonde M, Salminen S, Isolauri E. Presence of specific antibiotic (tet) resistance genes in infant faecal microbiota. FEMS Immunol Med Microbiol. 2006;48:21-5.
[39] Nogacka A, Salazar N, Suarez M, Milani C, Arboleya S, Solis G, et al. Impact of intrapartum antimicrobial prophylaxis upon the intestinal microbiota and the prevalence of antibiotic resistance genes in vaginally delivered full-term neonates. Microbiome. 2017;5:93.
[40] Gomez-Arango LF, Barrett HL, McIntyre HD, Callaway LK, Morrison M, Dekker Nitert M. Antibiotic treatment at delivery shapes the initial oral microbiome in neonates. Sci Rep. 2017;7:43481.
[41] Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197:435-8.
[42] Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, Young VB. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes. 2011;2:145-58.
[43] Schubert AM, Sinani H, Schloss PD. Antibiotic-induced alterations of the murine gut microbiota and subsequent effects on colonization resistance against Clostridium difficile. MBio. 2015;6:e00974.
[44] Bartoloni A, Pallecchi L, Benedetti M, Fernandez C, Vallejos Y, Guzman E, et al. Multidrug-resistant commensal Escherichia coli in children, Peru and Bolivia. Emerg Infect Dis. 2006;12:907-13.
[45] Hendrickx AP, Top J, Bayjanov JR, Kemperman H, Rogers MR, Paganelli FL. Antibiotic-driven dysbiosis mediates intraluminal agglutination and alternative segregation of Enterococcus faecium from the intestinal epithelium. MBio. 2015;6:e01346-15.
[46] Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790-801.
[47] Kim S, Covington A, Pamer EG. The intestinal microbiota: antibiotics, colonization resistance, and enteric pathogens. Immunol Rev. 2017;279:90-105.
[48] Rautava S. Early microbial contact, the breast milk microbiome and child health. J Dev Orig Health Dis. 2016;7:5-14.
[49] Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21:109-117.
[50] Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511-21.
[51] Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690-703.
[52] Forbes JD, Azad MB, Vehling L, Tun HM, Konya TB, Guttman DS, et al. Association of exposure to formula in the hospital and subsequent infant feeding practices with gut microbiota and risk of overweight in the first year of life. JAMA Pediatr. 2018;172:e181161.
[53] Parnanen K, Karkman A, Hultman J, Lyra C, Bengtsson-Palme J, Larsson DGJ, et al. Maternal gut and breast milk microbiota affect infant gut antibiotic resistome and mobile genetic elements. Nat Commun. 2018;9:3891.
[54] Bonang G, Monintja HE, Sujudi, van der Waaij D. Influence of breastmilk on the development of resistance to intestinal colonization in infants born at the Atma Jaya Hospital, Jakarta. Scand J Infect Dis. 2000;32:189-96.