1,820
Views
48
CrossRef citations to date
0
Altmetric
Review

The role of antimicrobial treatment during pregnancy on the neonatal gut microbiome and the development of atopy, asthma, allergy and obesity in childhood

, &
Pages 173-185 | Received 12 Nov 2018, Accepted 04 Feb 2019, Published online: 22 Feb 2019

References

  • Klein EY, Van Boeckel TP, Martinez EM, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA. 2018;115(15):E3463–E70.
  • Broe A, Pottegard A, Lamont R, et al. Increasing use of antibiotics in pregnancy during the period 2000-2010: prevalence, timing, category, and demographics. BJOG. 2014;121(8):988–996.
  • de Jonge L, Bos HJ, van Langen IM, et al. Antibiotics prescribed before, during and after pregnancy in the Netherlands: a drug utilization study. Pharmacoepidemiol Drug Saf. 2014;23(1):60–68.
  • Bookstaver PB, Bland CM, Griffin B, et al. A review of antibiotic use in pregnancy. Pharmacotherapy. 2015;35(11):1052–1062.
  • Zhang M, Litonjua AA, Mueller NT. Maternal antibiotic use and child asthma: is the association causal? Eur Respir J. 2018;52:1.
  • Heikkila AM. Antibiotics in pregnancy–a prospective cohort study on the policy of antibiotic prescription. Ann Med. 1993;25(5):467–471.
  • Guinto VT, De Guia B, Festin MR, et al. Different antibiotic regimens for treating asymptomatic bacteriuria in pregnancy. Cochrane Database Syst Rev. 2010 (9):CD007855.
  • Vazquez Juan C, Abalos E. Treatments for symptomatic urinary tract infections during pregnancy. Cochrane Database Syst Rev. 2011 (1). Available from: http://onlinelibrary.wiley.com/doi/10.1002/14651858.CD002256.pub2/abstract
  • Santos F, Oraichi D, Berard A. Prevalence and predictors of anti-infective use during pregnancy. Pharmacoepidemiol Drug Saf. 2010;19(4):418–427.
  • Zou ZH, Liu D, Li HD, et al. Prenatal and postnatal antibiotic exposure influences the gut microbiota of preterm infants in neonatal intensive care units. Ann Clin Microbiol Antimicrob. 2018;17(1):9.
  • Chernikova DA, Koestler DC, Hoen AG, et al. Fetal exposures and perinatal influences on the stool microbiota of premature infants. J Matern Fetal Neonatal Med. 2016;29(1):99–105.
  • Lamont HF, Blogg H, Lamont RF. Safety of antimicrobial treatment during pregnancy: a current review of resistance, immunomodulation and teratogenicity. Expert Opin Drug Saf. 2014;12:1569–1581.
  • Turnbaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature. 2007;449(7164):804–810.
  • Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–1359.
  • Sidhu H, Allison MJ, Chow JM, et al. Rapid reversal of hyperoxaluria in a rat model after probiotic administration of oxalobacter formigenes. J Urol. 2001;166(4):1487–1491.
  • Lamont RF, Sobel JD, Akins RA, et al. The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG. 2011;118(5):533–549.
  • Redondo-Lopez V, Cook RL, Sobel JD. Emerging role of lactobacilli in the control and maintenance of the vaginal bacterial microflora. Rev Infect Dis. 1990;12(5):856–872.
  • Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2010;108(Suppl 1)::4680–7.
  • Tanaka M, Nakayama J. Development of the gut microbiota in infancy and its impact on health in later life. Allergol Int. 2017;66(4):515–522.
  • Francino MP. Antibiotics and the human gut microbiome: dysbioses and accumulation of resistances. Front Microbiol. 2015;6:1543.
  • Walker RW, Clemente JC, Peter I, et al. The prenatal gut microbiome: are we colonized with bacteria in utero? Pediatr Obes. 2017;12(Suppl 1):3–17.
  • Mueller NT, Bakacs E, Combellick J, et al. The infant microbiome development: mom matters. Trends Mol Med. 2015;21(2):109–117.
  • Vidal AC, Murphy SK, Murtha AP, 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):907–913.
  • Mueller NT, Rifas-Shiman SL, Blaser MJ, et al. Association of prenatal antibiotics with foetal size and cord blood leptin and adiponectin. Pediatr Obes. 2017;12(2):129–136.
  • Keski-Nisula L, Kyynarainen HR, Karkkainen U, et al. Maternal intrapartum antibiotics and decreased vertical transmission of lactobacillus to neonates during birth. Acta Paediatr. 2013;102(5):480–485.
  • Jaureguy F, Carton M, Panel P, et al. Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J Clin Microbiol. 2004;42(11):5184–5188.
  • Azad MB, Konya T, Persaud RR, 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(6):983–993.
  • Thomas M, Price D. Prenatal antibiotic exposure and subsequent atopy. Am J Respir Crit Care Med. 2003;167(11):1578. author reply −9.
  • Vuillermin PJ, Macia L, Nanan R, et al. The maternal microbiome during pregnancy and allergic disease in the offspring. Semin Immunopathol. 2017;39(6):669–675.
  • Thorburn AN, McKenzie CI, Shen S, et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat Commun. 2015;6:7320.
  • McKeever TM, Lewis SA, Smith C, et al. The importance of prenatal exposures on the development of allergic disease: a birth cohort study using the West Midlands general practice database. Am J Respir Crit Care Med. 2002;166(6):827–832.
  • Tsakok T, McKeever TM, Yeo L, et al. Does early life exposure to antibiotics increase the risk of eczema? A systematic review. Br J Dermatol. 2013;169(5):983–991.
  • Wang JWJ, Lei H. Allergic disease epidemiology. In: Tao A, Raz E, editors, Allergy Bioinformatics. Netherlands: Sprimger; 2015. p. 15–41.
  • Strachan DP, Wong HJ, Spector TD. Concordance and interrelationship of atopic diseases and markers of allergic sensitization among adult female twins. J Allergy Clin Immunol. 2001;108(6):901–907.
  • Strachan DP. Hay fever, hygiene, and household size. BMJ (Clin Res Ed). 1989;299(6710):1259–1260.
  • Willing BP, Russell SL, Finlay BB. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol. 2011;9(4):233–243.
  • Benn CS, Thorsen P, Jensen JS, et al. Maternal vaginal microflora during pregnancy and the risk of asthma hospitalization and use of antiasthma medication in early childhood. J Allergy Clin Immunol. 2002;110(1):72–77.
  • Soto A, Martin V, Jimenez E, et al. Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr. 2014;59(1):78–88.
  • Loewen K, Monchka B, Mahmud SM, et al. Prenatal antibiotic exposure and childhood asthma: a population-based study. Eur Respir J. 2018;52:1.
  • Murk W, Risnes KR, Bracken MB. Prenatal or early-life exposure to antibiotics and risk of childhood asthma: a systematic review. Pediatrics. 2011;127(6):1125–1138.
  • Jedrychowski W, Galas A, Whyatt R, et al. The prenatal use of antibiotics and the development of allergic disease in one year old infants. A preliminary study. Int J Occup Med Environ Health. 2006;19(1):70–76.
  • Sariachvili M, Droste J, Dom S, et al. Is breast feeding a risk factor for eczema during the first year of life? Pediatr Allergy Immunol. 2007;18(5):410–417.
  • Bisgaard H, Halkjaer LB, Hinge R, et al. Risk analysis of early childhood eczema. J Allergy Clin Immunol. 2009;123(6):1355–60 e5.
  • Schmitt J, Schmitt NM, Kirch W, et al. Early exposure to antibiotics and infections and the incidence of atopic eczema: a population-based cohort study. Pediatr Allergy Immunol. 2010;21(2 Pt 1):292–300.
  • Wegienka G, Havstad S, Zoratti EM, et al. Combined effects of prenatal medication use and delivery type are associated with eczema at age 2 years. Clin Exp Allergy. 2015;45(3):660–668.
  • Rusconi F, Galassi C, Forastiere F, et al. Maternal complications and procedures in pregnancy and at birth and wheezing phenotypes in children. Am J Respir Crit Care Med. 2007;175(1):16–21.
  • Martel MJ, Rey E, Malo JL, et al. Determinants of the incidence of childhood asthma: a two-stage case-control study. Am J Epidemiol. 2009;169(2):195–205.
  • Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107(26):11971–11975.
  • Schmitt J, Chen CM, Apfelbacher C, et al. Infant eczema, infant sleeping problems, and mental health at 10 years of age: the prospective birth cohort study LISAplus. Allergy. 2011;66(3):404–411.
  • Dubakiene R, Rudzeviciene O, Butiene I, et al. Studies on early allergic sensitization in the Lithuanian birth cohort. Sci World J. 2012;2012:909524.
  • Wegienka G, Havstad S, Zoratti EM, et al. Association between vitamin D levels and allergy-related outcomes vary by race and other factors. J Allergy Clin Immunol. 2015;136(5):1309-14e1-4.
  • Asher I, Pearce N. Global burden of asthma among children. Int J Tuberc Lung Dis. 2014;18(11):1269–1278.
  • Croisant S. Epidemiology of asthma: prevalence and burden of disease. Adv Exp Med Biol. 2014;795:17–29.
  • Lavigne E, Belair MA, Rodriguez Duque D, et al. Effect modification of perinatal exposure to air pollution and childhood asthma incidence. Eur Respir J. 2018.
  • Ferrante G, Antona R, Malizia V, et al. Smoke exposure as a risk factor for asthma in childhood: a review of current evidence. Allergy Asthma Proc. 2014;35(6):454–461.
  • Sonnenschein-van der Voort AM, Arends LR, de Jongste JC, et al. Preterm birth, infant weight gain, and childhood asthma risk: a meta-analysis of 147,000 European children. J Allergy Clin Immunol. 2014;133(5):1317–1329.
  • Lapin B, Piorkowski J, Ownby D, et al. Relationship between prenatal antibiotic use and asthma in at-risk children. Ann Allergy Asthma Immunol. 2015;114(3):203–207.
  • Metsala J, Lundqvist A, Virta LJ, et al. Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin Exp Allergy. 2015;45(1):137–145.
  • Mulder B, Pouwels KB, Schuiling-Veninga CC, et al. Antibiotic use during pregnancy and asthma in preschool children: the influence of confounding. Clin Exp Allergy. 2016;46(9):1214–1226.
  • Stensballe LG, Simonsen J, Jensen SM, et al. Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr. 2013;162(4):832–8.e3.
  • Ortqvist AK, Lundholm C, Kieler H, et al. Antibiotics in fetal and early life and subsequent childhood asthma: nationwide population based study with sibling analysis. BMJ (Clin Res Ed). 2014;349:g6979.
  • Stokholm J, Sevelsted A, Bonnelykke K, et al. Maternal propensity for infections and risk of childhood asthma: a registry-based cohort study. Lancet Respir Med. 2014;2(8):631–637.
  • Christesen HT, Falkenberg T, Lamont RF, et al. The impact of vitamin D on pregnancy: a systematic review. Acta Obstet Gynecol Scand. 2012;91(12):1357–1367.
  • Christesen HT, Elvander C, Lamont RF, et al. The impact of vitamin D in pregnancy on extraskeletal health in children: a systematic review. Acta Obstet Gynecol Scand. 2012;91(12):1368–1380.
  • Lamont RF. Advances in the prevention of infection-related preterm birth. Front Immunol. 2015;6:566.
  • Bodnar LM, Krohn MA, Simhan HN. Maternal vitamin D deficiency is associated with bacterial vaginosis in the first trimester of pregnancy. J Nutr. 2009;139(6):1157–1161.
  • Davis LM, Chang SC, Mancini J, et al. Vitamin D insufficiency is prevalent among pregnant African American adolescents. J Pediatr Adolesc Gynecol. 2010;23(1):45–52.
  • Akoh CC, Pressman EK, Cooper E, et al. Low vitamin D is associated with infections and proinflammatory cytokines during pregnancy. Reprod Sci. 2018;25(3):414–423.
  • Chawes BL, Bonnelykke K, Jensen PF, et al. Cord blood 25(OH)-vitamin D deficiency and childhood asthma, allergy and eczema: the COPSAC2000 birth cohort study. PLoS One. 2014;9(6):e99856.
  • Tran B, Armstrong BK, Ebeling PR, et al. Effect of vitamin D supplementation on antibiotic use: a randomized controlled trial. Am J Clin Nutr. 2014;99(1):156–161.
  • Caffarelli C, Baldi F, Bendandi B, et al. Cow’s milk protein allergy in children: a practical guide. Ital J Pediatr. 2010;36:5.
  • Metsala J, Lundqvist A, Virta LJ, et al. Mother’s and offspring’s use of antibiotics and infant allergy to cow’s milk. Epidemiology. 2013;24(2):303–309.
  • Toro Monjaraz EM, Ramirez Mayans JA, Cervantes Bustamante R, et al. Perinatal factors associated with the development of cow’s milk protein allergy. Rev Gastroenterol Mex. 2015;80(1):27–31.
  • Wohl DL, Curry WJ, Mauger D, et al. Intrapartum antibiotics and childhood atopic dermatitis. J Am Board Fam Med. 2015;28(1):82–89.
  • Lee SY, Yu J, Ahn KM, et al. Additive effect between IL-13 polymorphism and cesarean section delivery/prenatal antibiotics use on atopic dermatitis: a birth cohort study (COCOA). PloS one. 2014;9(5):e96603.
  • Vinter CA, Frederiksen-Moller B, Weile LK, et al. Second Nordic Congress on Obesity in Gynecology and Obstetrics (NOCOGO). Acta Obstet Gynecol Scand. 2016;95(1):121–128.
  • Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214.
  • Mor A, Antonsen S, Kahlert 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):1450–1455.
  • Mueller NT, Whyatt R, Hoepner L, et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes (Lond). 2015;39(4):665–670.
  • Cassidy-Bushrow AE, Burmeister C, Havstad S, et al. Prenatal antimicrobial use and early-childhood body mass index. Int J Obes (Lond). 2018;42(1):1–7.
  • Poulsen MN, Pollak J, Bailey-Davis L, et al. Associations of prenatal and childhood antibiotic use with child body mass index at age 3 years. Obesity (Silver Spring). 2017;25(2):438–444.
  • Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22(3):250–253.
  • Cunnington AJ, Sim K, Deierl A, et al. “Vaginal seeding” of infants born by caesarean section. BMJ (Clin Res Ed). 2016;352:i227.
  • Kenchington AL, Lamont RF. Group B streptococcal immunisation of pregnant women for the prevention of early and late onset Group B streptococcal infection of the neonate as well as adult disease. Expert Rev Vaccines. 2017;16(1):15–25.
  • Haahr T, Glavind J, Axelsson P, et al. Vaginal seeding or vaginal microbial transfer from the mother to the caesarean-born neonate: a commentary regarding clinical management. BJOG. 2018;125(5):533–536.
  • Eschenbach DA. Vaginal seeding: more questions than answers. BJOG. 2018;125(5):537.
  • Haahr T, Clausen TD. Authors’ reply re: vaginal seeding or vaginal microbial transfer from the mother to the caesarean-born neonate: a commentary regarding clinical management. Bjog. 2018;125(5):632–633.
  • Marasinghe JP, Khot N. Re: vaginal seeding or vaginal microbial transfer from the mother to the caesarean-born neonate: a commentary regarding clinical management. Bjog. 2018;125(5):631–632.
  • Reid G. Cervicovaginal microbiomes-threats and possibilities. Trends Endocrinol Metab. 2016;27(7):446–454.
  • Reid G. Therapeutic opportunities in the vaginal microbiome. Microbiol Spectr. 2017;5:3.
  • Chong CYL, Bloomfield FH, O’Sullivan JM. Factors affecting gastrointestinal microbiome development in neonates. Nutrients. 2018;10:3.
  • Lemas DJ, Yee S, Cacho N, 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(6):406–409.
  • Breastfeeding and the use of human milk. Pediatrics. 2012;129(3):e827–e841.
  • Sudo N, Yu XN, Aiba Y, et al. An oral introduction of intestinal bacteria prevents the development of a long-term Th2-skewed immunological memory induced by neonatal antibiotic treatment in mice. Clin Exp Allergy. 2002;32(7):1112–1116.
  • Smits HH, Engering A, van der Kleij D, et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol. 2005;115(6):1260–1267.
  • Quin C, Estaki M, Vollman DM, et al. Probiotic supplementation and associated infant gut microbiome and health: a cautionary retrospective clinical comparison. Sci Rep. 2018;8(1):8283.
  • Ejima K, Li P, Smith DL Jr., et al. Observational research rigour alone does not justify causal inference. Eur J Clin Invest. 2016;46(12):985–993.
  • Shrestha GS, Kwizera A, Lundeg G, et al. International surviving sepsis campaign guidelines 2016: the perspective from low-income and middle-income countries. Lancet Infect Dis. 2017;17(9):893–895.
  • Fleming-Dutra KE, Hersh AL, Shapiro DJ, et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. JAMA. 2016;315(17):1864–1873.
  • ACOG Committee Opinion No. 494: sulfonamides, nitrofurantoin, and risk of birth defects. Obstet Gynecol. 2011;117(6):1484–1485.
  • Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489):1077–1081.
  • Romero R. Prenatal medicine: the child is the father of the man. 1996 1. J Matern Fetal Neonatal Med. 2009;22(8):636–639.
  • Hawkes N. Childhood leukaemia may be preventable by exposure to infections in early life. BMJ (Clin Res Ed). 2018;361:k2246.
  • Nguyen HQ, Jumaan AO, Seward JF. Decline in mortality due to varicella after implementation of varicella vaccination in the United States. N Engl J Med. 2005;352(5):450–458.
  • Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121):860–867.
  • Greaves M. A causal mechanism for childhood acute lymphoblastic leukaemia. Nat Rev Cancer. 2018;18(8):471–484.
  • Lamont RF, Sobel JD, Kusanovic JP, et al. Current debate on the use of antibiotic prophylaxis for caesarean section. BJOG. 2011;118(2):193–201.
  • Lamont RF, Keelan JA, Larsson PG, et al. The treatment of bacterial vaginosis in pregnancy with clindamycin to reduce the risk of infection-related preterm birth: a response to the Danish society of obstetrics and gynecology guideline group’s clinical recommendations. Acta Obstet Gynecol Scand. 2017;96(2):139–143.
  • Lamont RF, Nhan-Chang CL, Sobel JD, et al. Treatment of abnormal vaginal flora in early pregnancy with clindamycin for the prevention of spontaneous preterm birth: a systematic review and metaanalysis. Am J Obstet Gynecol. 2011;205(3):177–190.
  • Lamont RF, Duncan SL, Mandal D, et al. Intravaginal clindamycin to reduce preterm birth in women with abnormal genital tract flora. Obstet Gynecol. 2003;101(3):516–522.
  • Ugwumadu A, Manyonda I, Reid F, et al. Effect of early oral clindamycin on late miscarriage and preterm delivery in asymptomatic women with abnormal vaginal flora and bacterial vaginosis: a randomised controlled trial. Lancet. 2003;361(9362):983–988.
  • Larsson PG, Fahraeus L, Carlsson B, et al. Late miscarriage and preterm birth after treatment with clindamycin: a randomised consent design study according to Zelen. BJOG. 2006;113(6):629–637.
  • Carey JC, Klebanoff MA, Hauth JC, et al. Metronidazole to prevent preterm delivery in pregnant women with asymptomatic bacterial vaginosis. National institute of child health and human development network of maternal-fetal medicine units. N Engl J Med. 2000;342(8):534–540.
  • Cheng HG, Phillips MR. Secondary analysis of existing data: opportunities and implementation. Shanghai Arch Psychiatry. 2014;26(6):371–375.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.