Seminars in Fetal & Neonatal Medicine
Volume 17, Issue 1 , Pages 2-11 , February 2012

Diversity of microbes in amniotic fluid

  • Daniel B. DiGiulio

      Affiliations

    • Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA
    • Veterans Affairs Palo Alto Health Care System, Palo Alto, CA, USA
    • Corresponding Author InformationCorresponding author. Address: Division of Infectious Diseases and Geographic Medicine, Department of Medicine, Stanford University School of Medicine, 300 Pasteur Drive, Room S-101, Stanford, CA 94305-5107, USA. Tel.: +1 650 723 6661; fax: +1 650 433 8887.

References 

  1. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med. 2000;342:1500–1507
  2. Goncalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev. 2002;8:3–13
  3. Romero R, Gomez R, Chaiworapongsa T, Conoscenti G, Kim JC, Kim YM. The role of infection in preterm labor and delivery. Paediatr Perinat Epidemiol. 2001;15(Suppl. 2):41–56
  4. Lawn JE, Cousens S, Zupan J. 4 million neonatal deaths: when? where? why?. Lancet. 2005;365:891–900
  5. Harris JW, Brown H. Bacterial content of the uterus at cesarean section. Am J Obstet Gynecol. 1927;13:133
  6. Kustner O. Beitrag zur Lehre von der puerperalen Infection der Neugeborenen. Arch Gynak. 1877;11:256
  7. Stroup PE. Amniotic fluid infection and the intact fetal membrane. Obstet Gynecol. 1962;19:736–739
  8. Walsh H, Hildebrandt RJ, Prystowsky H. A microbiologic survey at cesarean section. Obstet Gynecol. 1965;26:665–668
  9. Benirschke K. Routes and types of infection in the fetus and the newborn. Am J Dis Child. 1960;99:714–721
  10. Benirschke K, Clifford SH. Intrauterine bacterial infection of the newborn infant: frozen sections of the cord as an aid to early detection. J Pediatr. 1959;54:11–18
  11. Hepner R, Stephens M. Congenital sepsis. Obstet Gynecol. 1955;6:547–549
  12. Harwick HJ, Iuppa JB, Fekety FR. Microorganisms and amniotic fluid. Obstet Gynecol. 1969;33:256–259
  13. Bobitt JR, Ledger WJ. Unrecognized amnionitis and prematurity: a preliminary report. J Reprod Med. 1977;19:8–12
  14. Cassell GH, Davis RO, Waites KB, et al. Isolation of Mycoplasma hominis and Ureaplasma urealyticum from amniotic fluid at 16–20 weeks of gestation: potential effect on outcome of pregnancy. Sex Transm Dis. 1983;10:294–302
  15. Romero R, Quintero R, Oyarzun E, et al. Intraamniotic infection and the onset of labor in preterm premature rupture of the membranes. Am J Obstet Gynecol. 1988;159:661–666
  16. 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–S279
  17. Blanchard A, Hentschel J, Duffy L, Baldus K, Cassell GH. Detection of Ureaplasma urealyticum by polymerase chain reaction in the urogenital tract of adults, in amniotic fluid, and in the respiratory tract of newborns. Clin Infect Dis. 1993;17(Suppl. 1):S148–S153
  18. Yoon BH, Romero R, Kim M, et al. Clinical implications of detection of Ureaplasma urealyticum in the amniotic cavity with the polymerase chain reaction. Am J Obstet Gynecol. 2000;183:1130–1137
  19. Yoon BH, Romero R, Lim JH, et al. The clinical significance of detecting Ureaplasma urealyticum by the polymerase chain reaction in the amniotic fluid of patients with preterm labor. Am J Obstet Gynecol. 2003;189:919–924
  20. 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;187:518–521
  21. Perni SC, Vardhana S, Korneeva I, et al. Mycoplasma hominis and Ureaplasma urealyticum in midtrimester amniotic fluid: association with amniotic fluid cytokine levels and pregnancy outcome. Am J Obstet Gynecol. 2004;191:1382–1386
  22. Bujold E, Morency AM, Rallu F, et al. Bacteriology of amniotic fluid in women with suspected cervical insufficiency. J Obstet Gynaecol Can. 2008;30:882–887
  23. Oyarzun E, Yamamoto M, Kato S, Gomez R, Lizama L, Moenne A. Specific detection of 16 micro-organisms in amniotic fluid by polymerase chain reaction and its correlation with preterm delivery occurrence. Am J Obstet Gynecol. 1998;179:1115–1119
  24. Leon R, Silva N, Ovalle A, et al. Detection of Porphyromonas gingivalis in the amniotic fluid in pregnant women with a diagnosis of threatened premature labor. J Periodontol. 2007;78:1249–1255
  25. Hitti J, Riley DE, Krohn MA, et al. Broad-spectrum bacterial rDNA polymerase chain reaction assay for detecting amniotic fluid infection among women in premature labor. Clin Infect Dis. 1997;24:1228–1232
  26. Markenson GR, Martin RK, Tillotson-Criss M, Foley KS, Stewart RS, Yancey M. The use of the polymerase chain reaction to detect bacteria in amniotic fluid in pregnancies complicated by preterm labor. Am J Obstet Gynecol. 1997;177:1471–1477
  27. DiGiulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008;3:e3056
  28. 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;47:38–47
  29. Marconi C, de Andrade Ramos BR, Peracoli JC, Donders GG, da Silva MG. Amniotic fluid interleukin-1 beta and interleukin-6, but not interleukin-8 correlate with microbial invasion of the amniotic cavity in preterm labor. Am J Reprod Immunol. 2011;65:549–556
  30. Jalava J, Mantymaa ML, Ekblad U, et al. Bacterial 16S rDNA polymerase chain reaction in the detection of intra-amniotic infection. Br J Obstet Gynaecol. 1996;103:664–669
  31. DiGiulio DB, Romero R, Kusanovic JP, et al. Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am J Reprod Immunol. 2010;64:38–57
  32. Gardella C, Riley DE, Hitti J, Agnew K, Krieger JN, Eschenbach D. Identification and sequencing of bacterial rDNAs in culture-negative amniotic fluid from women in premature labor. Am J Perinatol. 2004;21:319–323
  33. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human–microbe mutualism and disease. Nature. 2007;449:811–818
  34. Eribe ER, Olsen I. Leptotrichia species in human infections. Anaerobe. 2008;14:131–137
  35. DiGiulio DB, Gervasi M, Romero R, et al. Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J Perinat Med. 2010;38:503–513
  36. DiGiulio DB, Gervasi MT, Romero R, et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinat Med. 2010;38:495–502
  37. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG. 2002;109:527–533
  38. Alanen A, Laurikainen E. Second-trimester abortion caused by Capnocytophaga sputigena: case report. Am J Perinatol. 1999;16:181–183
  39. 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;44:1475–1483
  40. Miralles R, Hodge R, McParland PC, et al. Relationship between antenatal inflammation and antenatal infection identified by detection of microbial genes by polymerase chain reaction. Pediatr Res. 2005;57:570–577
  41. Rallu F, Morency AM, Laferriere C, Bujold E. Invasion of the amniotic cavity by an uncultured bacterium, a gram-positive coccus. J Matern Fetal Neonatal Med. 2007;20:185–187
  42. Bruner JP, Elliott JP, Kilbride HW, Garite TJ, Knox GE. Candida chorioamnionitis diagnosed by amniocentesis with subsequent fetal infection. Am J Perinatol. 1986;3:213–218
  43. Kellogg SG, Davis C, Benirschke K. Candida parapsilosis: previously unknown cause of fetal infection. A report of two cases. J Reprod Med. 1974;12:159–162
  44. Chaim W, Mazor M, Wiznitzer A. The prevalence and clinical significance of intraamniotic infection with Candida species in women with preterm labor. Arch Gynecol Obstet. 1992;251:9–15
  45. Parveen N, Munir AA, Din I, Majeed R. Frequency of vaginal candidiasis in pregnant women attending routine antenatal clinic. J Coll Physicians Surg Pak. 2008;18:154–157
  46. Misenhimer HR, Garcia-Bunuel R. Failure of intrauterine contraceptive device and fungal infection in the fetus. Obstet Gynecol. 1969;34:368–372
  47. Romero R, Reece EA, Duff GW, Coultrip L, Hobbins JC. Prenatal diagnosis of Candida albicans chorioamnionitis. Am J Perinatol. 1985;2:121–122
  48. Whyte RK, Hussain Z, deSa D. Antenatal infections with Candida species. Arch Dis Child. 1982;57:528–535
  49. Kim SK, Romero R, Kusanovic JP, et al. The prognosis of pregnancy conceived despite the presence of an intrauterine device (IUD). J Perinat Med. 2009;38:45–53
  50. Romero R, Gonzalez R, Sepulveda W, et al. Infection and labor. VIII. Microbial invasion of the amniotic cavity in patients with suspected cervical incompetence: prevalence and clinical significance. Am J Obstet Gynecol. 1992;167:1086–1091
  51. Auler ME, Morreira D, Rodrigues FF, et al. Biofilm formation on intrauterine devices in patients with recurrent vulvovaginal candidiasis. Med Mycol. 2010;48:211–216
  52. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA. 1990;87:4576–4579
  53. Wenstrom KD, Andrews WW, Bowles NE, Towbin JA, Hauth JC, Goldenberg RL. Intrauterine viral infection at the time of second trimester genetic amniocentesis. Obstet Gynecol. 1998;92:420–424
  54. Baschat AA, Towbin J, Bowles NE, Harman CR, Weiner CP. Prevalence of viral DNA in amniotic fluid of low-risk pregnancies in the second trimester. J Matern Fetal Neonatal Med. 2003;13:381–384
  55. Miller JL, Harman C, Weiner C, Baschat AA. Perinatal outcomes after second trimester detection of amniotic fluid viral genome in asymptomatic patients. J Perinat Med. 2009;37:140–143
  56. Kim MJ, Romero R, Gervasi MT, et al. Widespread microbial invasion of the chorioamniotic membranes is a consequence and not a cause of intra-amniotic infection. Lab Invest. 2009;89:924–936
  57. Papantoniou NE, Antsaklis AJ, Protopapas AG, Vogiatzi AI, Aravantinos DI. Predictive value of amniotic fluid and fetal blood cultures in pregnancy outcome in preterm prelabor rupture of membranes. J Obstet Gynaecol. 1997;17:18–22
  58. Virreira M, Martinez S, Alonso-Vega C, et al. Amniotic fluid is not useful for diagnosis of congenital Trypanosoma cruzi infection. Am J Trop Med Hyg. 2006;75:1082–1084
  59. Sibley CD, Duan K, Fischer C, et al. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog. 2008;4:e1000184
  60. Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol. 1988;31:553–584
  61. Watts DH, Krohn MA, Hillier SL, Eschenbach DA. The association of occult amniotic fluid infection with gestational age and neonatal outcome among women in preterm labor. Obstet Gynecol. 1992;79:351–357
  62. Bucher HU, Ochsner Y, Fauchere JC. Two years outcome of very pre-term and very low birthweight infants in Switzerland. Swiss Med Wkly. 2003;133:93–99
  63. Fredericks DN, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates. Clin Microbiol Rev. 1996;9:18–33
  64. Hill AB. The environment and disease: association or causation?. Proc R Soc Med. 1965;58:295–300
  65. Gravett MG, Adams KM, Sadowsky DW, et al. Immunomodulators plus antibiotics delay preterm delivery after experimental intraamniotic infection in a nonhuman primate model. Am J Obstet Gynecol. 2007;197:518.e1–518.e8
  66. Antonio MA, Hawes SE, Hillier SL. The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis. 1999;180:1950–1956
  67. Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2010;108(Suppl. 1):4680–4687
  68. Hillier SL, Nugent RP, Eschenbach DA, et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med. 1995;333:1737–1742
  69. Vallor AC, Antonio MA, Hawes SE, Hillier SL. Factors associated with acquisition of, or persistent colonization by, vaginal lactobacilli: role of hydrogen peroxide production. J Infect Dis. 2001;184:1431–1436
  70. Wilks M, Wiggins R, Whiley A, et al. Identification and H(2)O(2) production of vaginal lactobacilli from pregnant women at high risk of preterm birth and relation with outcome. J Clin Microbiol. 2004;42:713–717
  71. Grice EA, Kong HH, Conlan S, et al. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324:1190–1192
  72. Waites KB, Katz B, Schelonka RL. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin Microbiol Rev. 2005;18:757–789
  73. Menon R, Peltier MR, Eckardt J, Fortunato SJ. Diversity in cytokine response to bacteria associated with preterm birth by fetal membranes. Am J Obstet Gynecol. 2009;201:306.e1–306.e6
  74. Romero R, Schaudinn C, Kusanovic JP, et al. Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol. 2008;198:135.e1–135.e5
  75. McDonald H, Brocklehurst P, Parsons J, Vigneswaran R. Antibiotics for treating bacterial vaginosis in pregnancy. Cochrane Database Syst Rev. 2003;CD000262
  76. Kenyon SL, Taylor DJ, Tarnow-Mordi W. Broad-spectrum antibiotics for spontaneous preterm labor: the ORACLE II randomised trial. ORACLE Collaborative Group. Lancet. 2001;357:989–994
  77. Iams JD, Romero R, Culhane JF, Goldenberg RL. Primary, secondary, and tertiary interventions to reduce the morbidity and mortality of preterm birth. Lancet. 2008;371:164–175
  78. Lamont RF. Can antibiotics prevent preterm birth – the pro and con debate. BJOG. 2005;112(Suppl. 1):67–73
  79. Lamont RF, Nhan-Chang CL, Sobel JD, Workowski K, Conde-Agudelo A, Romero R. 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;205:177–190

PII: S1744-165X(11)00108-9

doi: 10.1016/j.siny.2011.10.001

Seminars in Fetal & Neonatal Medicine
Volume 17, Issue 1 , Pages 2-11 , February 2012