Seminars in Fetal & Neonatal Medicine
Volume 11, Issue 5 , Pages 317-326 , October 2006

Inflammation in preterm and term labour and delivery

  • Roberto Romero

      Affiliations

    • Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, MD, USA
    • Perinatology Research Branch, NICHD, NIH, DHHS, Detroit, MI, USA
    • Center for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, USA
    • Corresponding Author InformationCorresponding author. Perinatology Research Branch, NICHD, NIH, DHHS, Hutzel Women's Hospital – Box #4, 3990 John R., Detroit, MI 48201, USA. Tel.: +1 313 993 2700; fax: +1 313 993 2694.
  • ,
  • Jimmy Espinoza

      Affiliations

    • Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, MD, USA
    • Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA
  • ,
  • Luís F. Gonçalves

      Affiliations

    • Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, MD, USA
    • Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA
  • ,
  • Juan Pedro Kusanovic

      Affiliations

    • Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, MD, USA
  • ,
  • Lara A. Friel

      Affiliations

    • Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA
  • ,
  • Jyh Kae Nien

      Affiliations

    • Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, MD, USA

References 

  1. Romero R, Mazor M, Munoz H, Gomez R, Galasso M, Sherer DM. The preterm labor syndrome. Ann NY Acad Sci. 1994;734:414–429
  2. Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Romero R. Spontaneous labor at term is characterized by a genomic signature of acute inflammation in the chorioamniotic membranes but not in the systemic circulation. Am J Obstet Gynecol. 2004;191(6):S138
  3. Yoon BH, Romero R, Moon JB, Shim SS, Kim M, Kim G, et al. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol. 2001;185(5):1130–1136
  4. Yoon BH, Romero R, Park JS, Kim M, Oh SY, Kim CJ, et al. 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):1124–1129
  5. Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol. 1989;161(3):817–824
  6. Goncalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev. 2002;8(1):3–13
  7. McDuffie RS, Sherman MP, Gibbs RS. Amniotic fluid tumor necrosis factor-alpha and interleukin-1 in a rabbit model of bacterially induced preterm pregnancy loss. Am J Obstet Gynecol. 1992;167(6):1583–1588
  8. Fidel PL, Romero R, Wolf N, Cutright J, Ramirez M, Araneda H, et al. Systemic and local cytokine profiles in endotoxin-induced preterm parturition in mice. Am J Obstet Gynecol. 1994;170(5 Pt 1):1467–1475
  9. Gravett MG, Witkin SS, Haluska GJ, Edwards JL, Cook MJ, Novy MJ. An experimental model for intraamniotic infection and preterm labor in rhesus monkeys. Am J Obstet Gynecol. 1994;171:1660–1667
  10. Elovitz MA, Mrinalini C. Animal models of preterm birth. Trends Endocrinol Metab. 2004;15(10):479–487
  11. Gomez R, Ghezzi F, Romero R, Munoz H, Tolosa JE, Rojas I. Premature labor and intra-amniotic infection. Clinical aspects and role of the cytokines in diagnosis and pathophysiology. Clin Perinatol. 1995;22(2):281–342
  12. Romero R, Munoz H, Gomez R, Sherer DM, Ghezzi F, Gibbs RS, et al. Two thirds of spontaneous abortion/fetal deaths after genetic amniocentesis are the result of a pre-existing sub-clinical inflammatory process of the amniotic cavity. Am J Obstet Gynecol. 1995;172:S261
  13. Fidel P, Ghezzi F, Romero R, Chaiworapongsa T, Espinoza J, Cutright J, et al. The effect of antibiotic therapy on intrauterine infection-induced preterm parturition in rabbits. J Matern Fetal Neonatal Med. 2003;14(1):57–64
  14. Hassan S, Romero R, Hendler I, Gomez R, Khalek N, Espinoza J, et al. A sonographic short cervix as the only clinical manifestation of intra-amniotic infection. J Perinat Med. 2006;34(1):13–19
  15. Romero R, Quintero R, Oyarzun E, Wu YK, Sabo V, Mazor M, et al. Intraamniotic infection and the onset of labor in preterm premature rupture of the membranes. Am J Obstet Gynecol. 1988;159(3):661–666
  16. 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(3):351–357
  17. Hitti J, Riley DE, Krohn MA, Hillier SL, Agnew KJ, Krieger JN, 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(6):1228–1232
  18. 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(6):319–323
  19. Yoon BH, Romero R, Kim M, Kim EC, Kim T, Park JS, et al. Clinical implications of detection of Ureaplasma urealyticum in the amniotic cavity with the polymerase chain reaction. Am J Obstet Gynecol. 2000;183(5):1130–1137
  20. Yoon BH, Romero R, Lim JH, Shim SS, Hong JS, Shim JY, 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(4):919–924
  21. Steel JH, O'donoghue K, Kennea NL, Sullivan MH, Edwards AD. Maternal origin of inflammatory leukocytes in preterm fetal membranes, shown by fluorescence in situ hybridisation. Placenta. 2005;26(8–9):672–677
  22. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG: An International Journal of Obstetrics and Gynaecology. 2002;109(5):527–533
  23. Romero R, Mazor M, Morrotti R, Avila C, Oyarzun E, Insunza A, et al. Infection and labor. VII. Microbial invasion of the amniotic cavity in spontaneous rupture of membranes at term. Am J Obstet Gynecol. 1992;166(1 Pt 1):129–133
  24. Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol. 1988;31(3):553–584
  25. Romero R, Roslansky P, Oyarzun E, Wan M, Emamian M, Novitsky TJ, et al. Labor and infection. II. Bacterial endotoxin in amniotic fluid and its relationship to the onset of preterm labor. Am J Obstet Gynecol. 1988;158(5):1044–1049
  26. 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(3):420–424
  27. Van den Veyver I, Ni J, Bowles N, Carpenter RJ, Weiner CP, Yankowitz J, et al. Detection of intrauterine viral infection using the polymerase chain reaction. Mol Genet Metab. 1998;63(2):85–95
  28. Burguete T, Rabreau M, Fontanges-Darriet M, Roset E, Hager HD, Koppel A, et al. Evidence for infection of the human embryo with adeno-associated virus in pregnancy. Hum Reprod. 1999;14(9):2396–2401
  29. Galask RP, Varner MW, Petzold CR, Wilbur SL. Bacterial attachment to the chorioamniotic membranes. Am J Obstet Gynecol. 1984;148(7):915–928
  30. Abrahams VM, Bole-Aldo P, Kim YM, Straszewski-Chavez SL, Chaiworapongsa T, Romero R, et al. Divergent trophoblast responses to bacterial products mediated by TLRs. J Immunol. 2004;173(7):4286–4296
  31. Elovitz MA, Wang Z, Chien EK, Rychlik DF, Phillippe M. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and Toll-like receptor-4. Am J Pathol. 2003;163(5):2103–2111
  32. Kim YM, Romero R, Chaiworapongsa T, Kim GJ, Kim MR, Kuivaniemi H, et al. Toll-like receptor-2 and -4 in the chorioamniotic membranes in spontaneous labor at term and in preterm parturition that are associated with chorioamnionitis. Am J Obstet Gynecol. 2004;191(4):1346–1355
  33. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition-a review. Placenta. 2003;24(Suppl. A):S33–S46
  34. Romero R, Brody DT, Oyarzun E, Mazor M, Wu YK, Hobbins JC, et al. Infection and labor. III. Interleukin-1: a signal for the onset of parturition. Am J Obstet Gynecol. 1989;160(5 Pt 1):1117–1123
  35. Romero R, Tartakovsky B. The natural interleukin-1 receptor antagonist prevents interleukin-1-induced preterm delivery in mice. Am J Obstet Gynecol. 1992;167(4 Pt 1):1041–1045
  36. Casey ML, Cox SM, Beutler B, Milewich L, MacDonald PC. Cachectin/tumor necrosis factor-alpha formation in human decidua. Potential role of cytokines in infection-induced preterm labor. J Clin Invest. 1989;83(2):430–436
  37. Romero R, Manogue KR, Mitchell MD, Wu YK, Oyarzun E, Hobbins JC, et al. Infection and labor. IV. Cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am J Obstet Gynecol. 1989;161:336–341
  38. Chwalisz K, Benson M, Scholz P, Daum J, Beier HM, Hegele-Hartung C. Cervical ripening with the cytokines interleukin 8, interleukin 1[beta] and tumour necrosis factor [alpha] in guinea-pigs. Hum Reprod. 1994;9(11):2173–2181
  39. Hirsch E, Filipovich Y. The IL-1 type I and the TNF type I receptors are essential mediators of bacterially induced preterm labor in a murine model. J Soc Gynecol Inv. 2004;11:
  40. Hanna N, Hanna I, Hleb M, Wagner E, Dougherty J, Balkundi D, et al. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J Immunol. 2000;164:5721–5728
  41. Terrone DA, Rinehart BK, Granger JP, Barrilleaux PS, Martin JN, Bennett WA. Interleukin-10 administration and bacterial endotoxin-induced preterm birth in a rat model. Obstet Gynecol. 2001;98(3):476–480
  42. Elovitz MA, Saunders T, Ascher-Landsberg J, Phillippe M. Effects of thrombin on myometrial contractions in vitro and in vivo. Am J Obstet Gynecol. 2000;183(4):799–804
  43. Chaiworapongsa T, Espinoza J, Yoshimatsu J, Kim YM, Bujold E, Edwin S, et al. Activation of coagulation system in preterm labor and preterm premature rupture of membranes. J Matern Fetal Neonatal Med. 2002;11(6):368–373
  44. Gomez R, Athayde N, Pacora P, Mazor M, Yoon BH, Romero R. Increased thrombin in intrauterine inflammation. Am J Obstet Gynecol. 1998;178(1):S62
  45. Rosen T, Kuczynski E, O'Neill LM, Funai EF, Lockwood CJ. Plasma levels of thrombin-antithrombin complexes predict preterm premature rupture of the fetal membranes. J Matern Fetal Med. 2001;10(5):297–300
  46. Signore CC, Sood AK, Richards DS. Second-trimester vaginal bleeding: correlation of ultrasonographic findings with perinatal outcome. Am J Obstet Gynecol. 1998;178(2):336–340
  47. Williams MA, Mittendorf R, Lieberman E, Monson RR. Adverse infant outcomes associated with first-trimester vaginal bleeding. Obstet Gynecol. 1991;78(1):14–18
  48. Gomez R, Ghezzi F, Romero R, Yoon BH, Mazor M, Berry SM. Two thirds of human fetuses with microbial invasion of the amniotic cavity have a detectable systemic cytokine response before birth. Am J Obstet Gynecol. 1997;176:514
  49. Gomez R, Romero R, Ghezzi F, Yoon BH, Mazor M, Berry SM. The fetal inflammatory response syndrome. Am J Obstet Gynecol. 1998;179(1):194–202
  50. Pacora P, Chaiworapongsa T, Maymon E, Kim YM, Gomez R, Yoon BH, et al. Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med. 2002;11(1):18–25
  51. Yoon BH, Romero R, Park JS, Kim CJ, Kim SH, Choi JH, et al. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol. 2000;182(3):675–681
  52. Sampson JE, Theve RP, Blatman RN, Shipp TD, Bianchi DW, Ward BE, et al. Fetal origin of amniotic fluid polymorphonuclear leukocytes. Am J Obstet Gynecol. 1997;176(1 Pt 1):77–81
  53. Shim SS, Yoon BH, Romero R, Hong JS, Kim G, Sohn YK, et al. The frequency and clinical significance on intra-amniotic inflammation in patients with preterm premature rupture of the membranes. Am J Obstet Gynecol. 2003;189(6):S83
  54. Romero R, Gomez R, Ghezzi F, Yoon BH, Mazor M, Edwin SS, et al. A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition. Am J Obstet Gynecol. 1998;179(1):186–193
  55. Romero R, Nores J, Mazor M, Sepulveda W, Oyarzun E, Parra M, et al. Microbial invasion of the amniotic cavity during term labor. Prevalence and clinical significance. J Reprod Med. 1993;38(7):543–548
  56. Romero R, Mazor M, Morretti R, Avila C, Oyarzun E, Insunza A, et al. Infection and labor. VII: Microbial invasion of the amniotic cavity in spontaneous rupture of membranes at term. Am J Obstet Gynecol. 1992;166:129
  57. Yoon BH, Romero R, Moon J, Chaiworapongsa T, Espinoza J, Kim YM, et al. Differences in the fetal interleukin-6 response to microbial invasion of the amniotic cavity between term and preterm gestation. J Matern Fetal Neonatal Med. 2003;13(1):32–38
  58. Condon JC, Jeyasuria P, Faust JM, Mendelson CR. Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition. Proc Natl Acad Sci USA. 2004;101(14):4978–4983
  59. Gervasi MT, Chaiworapongsa T, Naccasha N, Blackwell S, Yoon BH, Maymon E, et al. Phenotypic and metabolic characteristics of maternal monocytes and granulocytes in preterm labor with intact membranes. Am J Obstet Gynecol. 2001;185(5):1124–1129
  60. Gervasi MT, Chaiworapongsa T, Naccasha N, Pacora P, Berman S, Maymon E, et al. Maternal intravascular inflammation in preterm premature rupture of membranes. J Matern Fetal Neonatal Med. 2002;11(3):171–175

PII: S1744-165X(06)00054-0

doi: 10.1016/j.siny.2006.05.001

Seminars in Fetal & Neonatal Medicine
Volume 11, Issue 5 , Pages 317-326 , October 2006