Antibiotic use during pregnancy: How bad is it?

BMC Medicine

Volumn 14, Issue 1, 2016, Pages

  Kuperman, Amir A ^a,b   Koren, Omry ^b  

^a WESTERN GALILEE HOSPITAL   (Israel)

^b BAR ILAN UNIVERSITY   (Israel)

Author keywords

Amniotic fluid; Antibiotics; Fetus; Gut; Immune system; Microbiome; Placenta; Pregnancy

Indexed keywords

ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; PROBIOTIC AGENT;

ACTINOBACTERIA; ACTINOMYCETALES; ARTICLE; BACTERIAL INFECTION; BACTEROIDALES; CLOSTRIDIALES; FETOPLACENTAL UNIT; HIGH RISK PREGNANCY; HUMAN; INTESTINE FLORA; INTRAUTERINE GROWTH RETARDATION; LACTOBACILLUS; NEISSERIA; NONHUMAN; PREECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATION; PREMATURE FETUS MEMBRANE RUPTURE; PREMATURE LABOR; PRESCRIPTION; PREVOTELLA; PROTEOBACTERIA; RISK ASSESSMENT; VAGINA FLORA; CHEMICALLY INDUCED; DRUG EFFECTS; DYSBIOSIS; FEMALE; MICROFLORA; PHYSIOLOGY; PREGNANCY COMPLICATIONS, INFECTIOUS; PRENATAL EXPOSURE;

ANTI-BACTERIAL AGENTS; DYSBIOSIS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; MICROBIOTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PRENATAL EXPOSURE DELAYED EFFECTS; PROBIOTICS;

EID: 84975284984     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/s12916-016-0636-0     Document Type: Article

References (73)

1. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207-14.
2. Ley RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010;26(1):5-11.
3. Tilg H, Moschen AR. Microbiota and diabetes: an evolving relationship. Gut. 2014;63(9):1513-21.
4. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Backhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470-80.
5. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 2013;339(6123):1084-8.
6. Newbern D, Freemark M. Placental hormones and the control of maternal metabolism and fetal growth. Curr Opin Endocrinol Diabetes Obes. 2011;18(6):409-16.
7. Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C, Raza S, Rosenbaum S, Van den Veyver I, Milosavljevic A, et al. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One. 2012;7(6), e36466.
8. Zhang D, Huang Y, Ye D. Intestinal dysbiosis: an emerging cause of pregnancy complications? Med Hypotheses. 2015;84(3):223-6.
9. Chernikova DA, Koestler DC, Hoen AG, Housman ML, Hibberd PL, Moore JH, Morrison HG, Sogin ML, Zain-Ul-Abideen M, Madan JC. Fetal exposures and perinatal influences on the stool microbiota of premature infants. J Matern Fetal Neonatal Med. 2016;29(1):99-105.
10. Branton WG, Ellestad KK, Maingat F, Wheatley BM, Rud E, Warren RL, Holt RA, Surette MG, Power C. Brain microbial populations in HIV/AIDS: alpha-proteobacteria predominate independent of host immune status. PLoS One. 2013;8(1), e54673.
11. Potgieter M, Bester J, Kell DB, Pretorius E. The dormant blood microbiome in chronic, inflammatory diseases. FEMS Microbiol Rev. 2015;39(4):567-91.
12. Marsland BJ, Gollwitzer ES. Host-microorganism interactions in lung diseases. Nat Rev Immunol. 2014;14(12):827-35.
13. Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL. The microbiome extends to subepidermal compartments of normal skin. Nat Commun. 2013;4:1431.
14. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra265.
15. Tissier H. Recherches sur la flore intestinale des nourrissons (e'tat normal et pathologique). Paris: G. Carre and C. Naud. 1900.
16. Kovalovszki L, Villanyi Z, Pataki I, Veszelowvsky I, Nagy ZB. Isolation of aerobic bacteria from the placenta. Acta Paediatr Acad Sci Hung. 1982;23(3):357-60.
17. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371(9606):75-84.
18. Goepfert AR, Jeffcoat MK, Andrews WW, Faye-Petersen O, Cliver SP, Goldenberg RL, Hauth JC. Periodontal disease and upper genital tract inflammation in early spontaneous preterm birth. Obstet Gynecol. 2004;104(4):777-83.
19. Galask RP, Varner MW, Petzold CR, Wilbur SL. Bacterial attachment to the chorioamniotic membranes. Am J Obstet Gynecol. 1984;148(7):915-28.
20. Doyle RM, Alber DG, Jones HE, Harris K, Fitzgerald F, Peebles D, Klein N. Term and preterm labour are associated with distinct microbial community structures in placental membranes which are independent of mode of delivery. Placenta. 2014;35(12):1099-101.
21. Kliman HJ. Comment on "the placenta harbors a unique microbiome". Sci Transl Med. 2014;6(254):254le254.
22. Bookstaver PB, Bland CM, Griffin B, Stover KR, Eiland LS, McLaughlin M. A review of antibiotic use in pregnancy. Pharmacotherapy. 2015;35(11):1052-62.
23. 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(4):250-60.
24. Stokholm J, Schjorring S, Eskildsen CE, Pedersen L, Bischoff AL, Folsgaard N, Carson CG, Chawes BL, Bonnelykke K, Molgaard A, et al. Antibiotic use during pregnancy alters the commensal vaginal microbiota. Clin Microbiol Infect. 2014;20(7):629-35.
25. Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG, Widen EM, Hassoun A, Perera F, Rundle A. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obesity. 2015;39(4):665-70.
26. Roberts DJ, Celi AC, Riley LE, Onderdonk AB, Boyd TK, Johnson LC, Lieberman E. Acute histologic chorioamnionitis at term: nearly always noninfectious. PLoS One. 2012;7(3), e31819.
27. Kenyon SL, Taylor DJ, Tarnow-Mordi W, ORACLE Collaborative Group. Broad-spectrum antibiotics for preterm, prelabour rupture of fetal membranes: the ORACLE I randomised trial. ORACLE Collaborative Group. Lancet. 2001;357(9261):979-88.
28. Kenyon S, Pike K, Jones DR, Brocklehurst P, Marlow N, Salt A, Taylor DJ. Childhood outcomes after prescription of antibiotics to pregnant women with spontaneous preterm labour: 7-year follow-up of the ORACLE II trial. Lancet. 2008;372(9646):1319-27.
29. Ledger WJ, Blaser MJ. Are we using too many antibiotics during pregnancy? BJOG. 2013;120(12):1450-2.
30. Flenady V, Hawley G, Stock OM, Kenyon S, Badawi N. Prophylactic antibiotics for inhibiting preterm labour with intact membranes. Cochrane Database Syst Rev. 2013;12, CD000246.
31. De La Cochetiere MF, Durand T, Lepage P, Bourreille A, Galmiche JP, Dore J. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J Clin Microbiol. 2005;43(11):5588-92.
32. Lapin B, Piorkowski J, Ownby D, Freels S, Chavez N, Hernandez E, Wagner-Cassanova C, Pelzel D, Vergara C, Persky V. Relationship between prenatal antibiotic use and asthma in at-risk children. Ann Allergy Asthma Immunol. 2015;114(3):203-7.
33. Metsala J, Lundqvist A, Virta LJ, Kaila M, Gissler M, Virtanen SM. Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin Exp Allergy. 2015;45(1):137-45.
34. Stensballe LG, Simonsen J, Jensen SM, Bonnelykke K, Bisgaard H. Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr. 2013;162(4):832-8. e3.
35. Rakoff-Nahoum S, Kong Y, Kleinstein SH, Subramanian S, Ahern PP, Gordon JI, Medzhitov R. Analysis of gene-environment interactions in postnatal development of the mammalian intestine. Proc Natl Acad Sci U S A. 2015;112(7):1929-36.
36. Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;351(6279):1296-302.
37. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG. 2002;109(5):527-33.
38. Cahill RJ, Tan S, Dougan G, O'Gaora P, Pickard D, Kennea N, Sullivan MH, Feldman RG, Edwards AD. Universal DNA primers amplify bacterial DNA from human fetal membranes and link Fusobacterium nucleatum with prolonged preterm membrane rupture. Mol Hum Reprod. 2005;11(10):761-6.
39. Kim MJ, Romero R, Gervasi MT, Kim JS, Yoo W, Lee DC, Mittal P, Erez O, Kusanovic JP, Hassan SS, et al. Widespread microbial invasion of the chorioamniotic membranes is a consequence and not a cause of intra-amniotic infection. Lab Invest. 2009;89(8):924-36.
40. Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q, Roehl KA, Nelson DM, Macones GA, Mysorekar IU. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol. 2013;208(3):e1-7.
41. Barak S, Oettinger-Barak O, Machtei EE, Sprecher H, Ohel G. Evidence of periopathogenic microorganisms in placentas of women with preeclampsia. J Periodontol. 2007;78(4):670-6.
42. Bhola K, Al-Kindi H, Fadia M, Kent AL, Collignon P, Dahlstrom JE. Placental cultures in the era of peripartum antibiotic use. Aust N Z J Obstet Gynaecol. 2008;48(2):179-84.
43. Daoud GA, Suzuki Y, Yamamoto T, Suzuki T, Suzumori N, Tanemura M. Establishment of a polymerase chain reaction method for detection of Escherichia coli in amniotic fluid in patients with chorioamnionitis. Fetal Diagn Ther. 2008;24(2):132-9.
44. Gomez R, Romero R, Nien JK, Medina L, Carstens M, Kim YM, Espinoza J, Chaiworapongsa T, Gonzalez R, Iams JD,et al. Antibiotic administration to patients with preterm premature rupture of membranes does not eradicate intra-amniotic infection. J Matern Fetal Neonatal Med. 2007;20(2):167-73.
45. Nguyen DP, Gerber S, Hohlfeld P, Sandrine G, Witkin SS. Mycoplasma hominis in mid-trimester amniotic fluid: relation to pregnancy outcome. J Perinat Med. 2004;32(4):323-6.
46. Onderdonk AB, Hecht JL, McElrath TF, Delaney ML, Allred EN, Leviton A, Investigators ES. Colonization of second-trimester placenta parenchyma. Am J Obstet Gynecol. 2008;199(1):52. e1-52.
47. Pankuch GA, Appelbaum PC, Lorenz RP, Botti JJ, Schachter J, Naeye RL. Placental microbiology and histology and the pathogenesis of chorioamnionitis. Obstet Gynecol. 1984;64(6):802-6.
48. Patrascu A, Berceanu S, Popescu CF, Gheorman V, Berceanu C. Clinical and histopathological correlations of the modifications of fetal membranes in amniochorial infection. Rom J Morphol Embryol. 2009;50(1):67-72.
49. Queiros da Mota V, Prodhom G, Yan P, Hohlfheld P, Greub G, Rouleau C. Correlation between placental bacterial culture results and histological chorioamnionitis: a prospective study on 376 placentas. J Clin Pathol. 2013;66(3):243-8.
50. Romero R, Miranda J, Chaiworapongsa T, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, Kim CJ,et al. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-amniotic infection in preterm labor with intact membranes. Am J Reprod Immunol. 2014;71(4):330-58.
51. Amarasekara R, Jayasekara RW, Senanayake H, Dissanayake VH. Microbiome of the placenta in pre-eclampsia supports the role of bacteria in the multifactorial cause of pre-eclampsia. J Obstet Gynaecol Res. 2015;41(5):662-9.
52. Antony KM, Ma J, Mitchell KB, Racusin DA, Versalovic J, Aagaard K. The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol. 2015;212(5):653. e1-16.
53. Blanchard A, Hamrick W, Duffy L, Baldus K, Cassell GH. Use of the polymerase chain reaction for detection of Mycoplasma fermentans and Mycoplasma genitalium in the urogenital tract and amniotic fluid. Clin Infect Dis. 1993;17 Suppl 1:S272-9.
54. Clark P, Trickett A, Stark D, Vowels M. Factors affecting microbial contamination rate of cord blood collected for transplantation. Transfusion. 2012;52(8):1770-7.
55. Gerber S, Vial Y, Hohlfeld P, Witkin SS. Detection of Ureaplasma urealyticum in second-trimester amniotic fluid by polymerase chain reaction correlates with subsequent preterm labor and delivery. J Infect Dis. 2003;187(3):518-21.
56. Harvey BS, Koeuth T, Versalovic J, Woods CR, Lupski JR. Vertical transmission of Citrobacter diversus documented by DNA fingerprinting. Infect Control Hosp Epidemiol. 1995;16(10):564-9.
57. Hitti J, Riley DE, Krohn MA, Hillier SL, Agnew KJ, Krieger JN, Eschenbach DA. Broad-spectrum bacterial rDNA polymerase chain reaction assay for detecting amniotic fluid infection among women in premature labor. Clin Infect Dis. 1997;24(6):1228-32.
58. Jalava J, Mantymaa ML, Ekblad U, Toivanen P, Skurnik M, Lassila O, Alanen A. Bacterial 16S rDNA polymerase chain reaction in the detection of intra-amniotic infection. Br J Obstet Gynaecol. 1996;103(7):664-9.
59. Markenson GR, Adams LA, Hoffman DE, Reece MT. Prevalence of Mycoplasma bacteria in amniotic fluid at the time of genetic amniocentesis using the polymerase chain reaction. J Reprod Med. 2003;48(10):775-9.
60. Mostajeran F, Arbabi B. Is there any difference between preeclamptic and healthy pregnant women regarding the presence of periopathogenic bacteria in the placenta? Int J Prev Med. 2013;4(3):322-6.
61. Satokari R, Gronroos T, Laitinen K, Salminen S, Isolauri E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol. 2009;48(1):8-12.
62. Watt S, Lanotte P, Mereghetti L, Moulin-Schouleur M, Picard B, Quentin R. Escherichia coli strains from pregnant women and neonates: intraspecies genetic distribution and prevalence of virulence factors. J Clin Microbiol. 2003;41(5):1929-35.
63. Gomez R, Romero R, Nien JK, Medina L, Carstens M, Kim YM, Chaiworapongsa T, Espinoza J, Gonzalez R. Idiopathic vaginal bleeding during pregnancy as the only clinical manifestation of intrauterine infection. J Matern Fetal Neonatal Med. 2005;18(1):31-7.
64. Han YW, Ikegami A, Bissada NF, Herbst M, Redline RW, Ashmead GG. Transmission of an uncultivated Bergeyella strain from the oral cavity to amniotic fluid in a case of preterm birth. J Clin Microbiol. 2006;44(4):1475-83.
65. Hassan S, Romero R, Hendler I, Gomez R, Khalek N, Espinoza J, Nien JK, Berry SM, Bujold E, Camacho N, et al. A sonographic short cervix as the only clinical manifestation of intra-amniotic infection. J Perinat Med. 2006;34(1):13-9.
66. Kim KW, Romero R, Park HS, Park CW, Shim SS, Jun JK, Yoon BH. A rapid matrix metalloproteinase-8 bedside test for the detection of intraamniotic inflammation in women with preterm premature rupture of membranes. Am J Obstet Gynecol. 2007;197(3):292. e1-5.
67. Kirchner L, Helmer H, Heinze G, Wald M, Brunbauer M, Weninger M, Zaknun D. Amnionitis with Ureaplasma urealyticum or other microbes leads to increased morbidity and prolonged hospitalization in very low birth weight infants. Eur J Obstet Gynecol Reprod Biol. 2007;134(1):44-50.
68. Musilova I, Pliskova L, Kutova R, Jacobsson B, Paterova P, Kacerovsky M. Streptococcus agalactiae in pregnancies complicated by preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med. 2016;29(7):1036-40.
69. Yoon BH, Romero R, Park JS, Kim M, Oh SY, Kim CJ, Jun JK. The relationship among inflammatory lesions of the umbilical cord (funisitis), umbilical cord plasma interleukin 6 concentration, amniotic fluid infection, and neonatal sepsis. Am J Obstet Gynecol. 2000;183(5):1124-9.
70. Han YW, Shen T, Chung P, Buhimschi IA, Buhimschi CS. Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol. 2009;47(1):38-47.
71. DiGiulio DB, Gervasi MT, Romero R, Vaisbuch E, Mazaki-Tovi S, Kusanovic JP, Seok KS, Gomez R, Mittal P, Gotsch F, et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinat Med. 2010;38(5):495-502.
72. DiGiulio DB, Gervasi M, Romero R, Mazaki-Tovi S, Vaisbuch E, Kusanovic JP, Seok KS, Gomez R, Mittal P, Gotsch F, et al. Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J Perinat Med. 2010;38(5):503-13.
73. Onderdonk AB, Delaney ML, DuBois AM, Allred EN, Leviton A. Extremely Low Gestational Age Newborns (ELGAN) Study Investigators. Detection of bacteria in placental tissues obtained from extremely low gestational age neonates. Am J Obstet Gynecol. 2008;198(1):110. e1-7.