Skip to main content

Advertisement

SpringerLink
Log in

Synergy and Interactions Among Biological Pathways Leading to Preterm Premature Rupture of Membranes

  • Review
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Preterm premature rupture of membranes (PPROM) occurs in 1% to 2% of births. Impact of PPROM is greatest in low- and middle-income countries where prematurity-related deaths are most common. Recent investigations identify cytokine and matrix metalloproteinase activation, oxidative stress, and apoptosis as primary pathways to PPROM. These biological processes are initiated by heterogeneous etiologies including infection/inflammation, placental bleeding, uterine overdistention, and genetic polymorphisms. We hypothesize that pathways to PPROM overlap and act synergistically to weaken membranes. We focus our discussion on membrane composition and strength, pathways linking risk factors to membrane weakening, and future research directions to reduce the global burden of PPROM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371(9606):75–84.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Liu L, Johnson HL, Cousens S, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012;379(9832):2151–2161.

    Article  PubMed  Google Scholar 

  3. Ye G, Jiang Z, Lu S, Le Y. Premature infants born after preterm premature rupture of membranes with 24–34 weeks of gestation: a study of factors influencing length of neonatal intensive care unit stay. J Matern Fetal Neonatal Med. 2011;24(7):960–965.

    Article  PubMed  Google Scholar 

  4. Khashoggi TY. Outcome of pregnancies with preterm premature rupture of membranes. Saudi Med J. 2004;25(12):1957–1961.

    PubMed  Google Scholar 

  5. Stewart CJ, Tregoning SK, Moller G, Wainwright H. Preterm prelabour rupture of the membranes before 28 weeks: better than feared outcome of expectant management in Africa. Eur J Obstet Gynecol Reprod Biol. 2006;126(2):186–192.

    Article  PubMed  Google Scholar 

  6. Noor S, Nazar AF, Bashir R, Sultana R. Prevalence of PPROM and its outcome. J Ayub Med Coll Abbottabad. 2007;19(4):14–17.

    PubMed  Google Scholar 

  7. Obi SN, Ozumba BC. Pre-term premature rupture of fetal membranes: the dilemma of management in a developing nation. J Obstet Gynaecol. 2007;27(1):37–40.

    Article  CAS  PubMed  Google Scholar 

  8. Brace RA. Physiology of amniotic fluid volume regulation. Clin Obstetrics Gynecol. 1997;40(2):280–289.

    Article  CAS  Google Scholar 

  9. Parry S, Strauss JF III. Premature rupture of the fetal membranes. N Engl J Med. 1998;338(10):663–670.

    Article  CAS  PubMed  Google Scholar 

  10. Oxlund H, Helmig R, Halaburt JT, Uldbjerg N. Biomechanical analysis of human chorioamniotic membranes. Eur J Obstet Gynecol Reprod Biol. 1990;34(3):247–255.

    Article  CAS  PubMed  Google Scholar 

  11. Arikat S, Novince RW, Mercer BM, et al. Separation of amnion from choriodecidua is an integral event to the rupture of normal term fetal membranes and constitutes a significant component of the work required. Am J Obstet Gynecol. 2006;194(1):211–217.

    Article  PubMed  Google Scholar 

  12. Ockleford C, Malak T, Hubbard A, et al. Confocal and conventional immunofluorescence and ultrastructural localisation of intracellular strength-giving components of human amniochorion. J Anat. 1993;183 (pt 3):483–505.

    PubMed  PubMed Central  Google Scholar 

  13. Bourne G.The foetal membranes. A review of the anatomy of normal amnion and chorion and some aspects of their function. Postgrad Med J. 1962;38:193–201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Bryant-Greenwood GD. The extracellular matrix of the human fetal membranes: structure and function. Placenta. 1998; 19(1):1–11.

    Article  CAS  PubMed  Google Scholar 

  15. Malak TM, Bell SC. Structural characteristics of term human fetal membranes: a novel zone of extreme morphological alteration within the rupture site. Br J Obstet Gynaecol. 1994;101(5):375–386.

    Article  CAS  PubMed  Google Scholar 

  16. Meinert M, Eriksen GV, Petersen AC, Helmig RB, Laurent C, Uldbjerg N, et al. Proteoglycans and hyaluronan in human fetal membranes. American journal of obstetrics and gynecology. 2001;184(4):679–85.

    Article  CAS  PubMed  Google Scholar 

  17. Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, Macvicar J. Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta. 1993;14(4):385–406.

    Article  CAS  PubMed  Google Scholar 

  18. Hieber AD, Corcino D, Motosue J, et al. Detection of elastin in the human fetal membranes: proposed molecular basis for elasticity. Placenta. 1997;18(4):301–312.

    Article  CAS  PubMed  Google Scholar 

  19. Parry-Jones E, Priya S. A study of the elasticity and tension of fetal membranes and of the relation of the area of the gestational sac to the area of the uterine cavity. Br J Obstet Gynaecol. 1976;83(3):205–212.

    Article  CAS  PubMed  Google Scholar 

  20. Benirschke K, Kaufman P, Baergen RN. Anatomy and Pathology of the Human Membranes. Pathology of the Human Placenta. 5th ed. New York: Springer Science + Business Media, Inc.; 2006:321–379.

    Google Scholar 

  21. Joyce EM, Moore JJ, Sacks MS. Biomechanics of the fetal membrane prior to mechanical failure: review and implications. Eur J Obstet Gynecol Reprod Biol. 2009;144(suppl 1):S121–S127.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Artal R, Sokol RJ, Neuman M, Burstein AH, Stojkov J. The mechanical properties of prematurely and non–prematurely ruptured membranes. Methods and preliminary results. Am J Obstet Gynecol. 1976;125(5):655–659.

    Article  CAS  PubMed  Google Scholar 

  23. Manabe Y, Himeno N, Fukumoto M. Tensile strength and collagen content of amniotic membrane do not change after the second trimester or during delivery. Obstet Gynecol. 1991;78(1):24–27.

    CAS  PubMed  Google Scholar 

  24. El Khwad M, Stetzer B, Moore RM, et al. Term human fetal membranes have a weak zone overlying the lower uterine pole and cervix before onset of labor. Biol Reprod. 2005;72(3):720–726.

    Article  CAS  PubMed  Google Scholar 

  25. El Khwad M, Pandey V, Stetzer B, et al. Fetal membranes from term vaginal deliveries have a zone of weakness exhibiting characteristics of apoptosis and remodeling. J Soc Gynecol Investig. 2006;13(3):191–195.

    Article  PubMed  Google Scholar 

  26. Maclachlan TB. A Method for the investigation of the strength of the fetal membranes. Am J Obstet Gynecol. 1965;91:309–313.

    Article  CAS  PubMed  Google Scholar 

  27. Rangaswamy N, Abdelrahim A, Moore RM, et al. Biomechanical characteristics of human fetal membranes. Preterm fetal membranes are stronger than term fetal membranes [in French]. Gynecol Obstet Fertil. 2011;39(6):373–377.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Polishuk WZ, Kohane S, Pernaio A. The physical properties of fetal membranes. Obstet Gynecol. 1962;20(2):204–210.

    CAS  PubMed  Google Scholar 

  29. Lavery JP, Miller CE. The viscoelastic nature of chorioamniotic membranes. Obstet Gynecol. 1977;50(4):467–472.

    CAS  PubMed  Google Scholar 

  30. Lavery JP, Miller CE. Deformation and creep in the human chorioamniotic sac. Am J Obstet Gynecol. 1979;134(4):366–375.

    Article  CAS  PubMed  Google Scholar 

  31. Oyen ML, Cook RF, Calvin SE. Mechanical failure of human fetal membrane tissues. J Mater Sci Mater Med. 2004; 15(6):651–658.

    Article  CAS  PubMed  Google Scholar 

  32. Schober EA, Kusy RP, Whitley JQ, Savitz DA. Effect of thickness on the fracture characteristics of fetal membranes. J Mater Sci Mater Med. 1994;5(3):130–137.

    Article  Google Scholar 

  33. Oyen ML, Calvin SE, Landers DV. Premature rupture of the fetal membranes: is the amnion the major determinant? Am J Obstet Gynecol. 2006;195(2):510–515.

    Article  PubMed  Google Scholar 

  34. Canzoneri BJ, Feng L, Grotegut CA, Bentley RC, Heine RP, Murtha AP. The chorion layer of fetal membranes is prematurely destroyed in women with preterm premature rupture of the membranes. Reprod Sci. 2013;20(10):1246–1254.

    Article  PubMed  Google Scholar 

  35. Strauss JF III. Extracellular matrix dynamics and fetal membrane rupture. Reprod Sci. 2013;20(2):140–153.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Biggio JR Jr Ramsey PS, Cliver SP, Lyon MD, Goldenberg RL, Wenstrom KD. Midtrimester amniotic fluid matrix metalloproteinase-8 (MMP-8) levels above the 90th percentile are a marker for subsequent preterm premature rupture of membranes. Am J Obstet Gynecol. 2005;192(1):109–113.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Athayde N, Edwin SS, Romero R, et al. A role for matrix metalloproteinase-9 in spontaneous rupture of the fetal membranes. Am J Obstet Gynecol. 1998;179(5):1248–1253.

    Article  CAS  PubMed  Google Scholar 

  38. Menon R, Fortunato SJ. The role of matrix degrading enzymes and apoptosis in rupture of membranes. J Soc Gynecol Investig. 2004;11(7):427–437.

    Article  CAS  PubMed  Google Scholar 

  39. Menon R, Fortunato SJ. Infection and the role of inflammation in preterm premature rupture of the membranes. Best Pract Res Clin Obstet Gynaecol. 2007;21(3):467–478.

    Article  PubMed  Google Scholar 

  40. Paavola LG, Furth EE, Delgado V, et al. Striking changes in the structure and organization of rat fetal membranes precede parturition. Biol Reprod. 1995;53(2):321–338.

    Article  CAS  PubMed  Google Scholar 

  41. Saglam A, Ozgur C, Derwig I, Unlu BS, Gode F, Mungan T. The role of apoptosis in preterm premature rupture of the human fetal membranes. Arch Gynecol Obstet. 2013;288(3):501–505.

    Article  CAS  PubMed  Google Scholar 

  42. Fortunato SJ, Menon R, Bryant C, Lombardi SJ. Programmed cell death (apoptosis) as a possible pathway to metalloproteinase activation and fetal membrane degradation in premature rupture of membranes. Am J Obstet Gynecol. 2000;182(6):1468–1476.

    Article  CAS  PubMed  Google Scholar 

  43. Fortunato SJ, Menon R, Lombardi SJ. Support for an infectioninduced apoptotic pathway in human fetal membranes. Am J Obstet Gynecol. 2001;184(7):1392–1397.

    Article  CAS  PubMed  Google Scholar 

  44. Menon R, Fortunato SJ, Yu J, et al. Cigarette smoke induces oxidative stress and apoptosis in normal term fetal membranes. Placenta. 2011;32(4):317–322.

    Article  CAS  PubMed  Google Scholar 

  45. Longini M, Perrone S, Vezzosi P, et al. Association between oxidative stress in pregnancy and preterm premature rupture of membranes. Clin Biochem. 2007;40(11):793–797.

    Article  CAS  PubMed  Google Scholar 

  46. Woods JR Jr. Reactive oxygen species and preterm premature rupture of membranes-a review. Placenta. 2001;22(suppl A):S38–S44.

    Article  PubMed  Google Scholar 

  47. Barrera G. Oxidative Stress and Lipid Peroxidation Products in Cancer Progression and Therapy. ISRN Oncology. 2012;137289:21. doi:10.5402/2012/137289

    Google Scholar 

  48. Plessinger MA, Woods JR Jr Miller RK. Pretreatment of human amnion-chorion with vitamins C and E prevents hypochlorous acid-induced damage. Am J Obstet Gynecol. 2000;183(4):979–985.

    Article  CAS  PubMed  Google Scholar 

  49. Mercer BM, Abdelrahim A, Moore RM, et al. The impact of vitamin C supplementation in pregnancy and in vitro upon fetal membrane strength and remodeling. Reprod Sci. 2010;17(7):685–695.

    Article  CAS  PubMed  Google Scholar 

  50. Spinnato JA II, Freire S, Pinto e Silva JL, et al. Antioxidant supplementation and premature rupture of the membranes: a planned secondary analysis. Am J Obstet Gynecol. 2008;199(4):433.e1–e8.

    Article  CAS  Google Scholar 

  51. Moore RM, Schatz F, Kumar D, et al. Alpha-lipoic acid inhibits thrombin-induced fetal membrane weakening in vitro. Placenta. 2010;31(10):886–892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lim R, Barker G, Wall CA, Lappas M. Dietary phytophenols curcumin, naringenin and apigenin reduce infection-induced inflammatory and contractile pathways in human placenta, foetal membranes and myometrium. Mol Hum Reprod. 2013;19(7):451–462.

    Article  CAS  PubMed  Google Scholar 

  53. Joaquin SF, Romero R, Espinoza J, et al. Prelabor rupture of membranes. In: Reece EA, John CH, eds. Clinical Obstetrics: The Fetus and The Mother. 3rd ed. Malden, MA: Blackwell Publishing; 2007:1130–1188.

    Google Scholar 

  54. Garite TJ, Freeman RK, Linzey EM, Braly P. The use of amniocentesis in patients with premature rupture of membranes. Obstet Gynecol. 1979;54(2):226–230.

    CAS  PubMed  Google Scholar 

  55. 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(3):661–666.

    Article  CAS  PubMed  Google Scholar 

  56. Kim KW, Romero R, Park HS, et al. 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–e5.

    Article  CAS  Google Scholar 

  57. Shim SS, Romero R, Hong JS, et al. Clinical significance of intraamniotic inflammation in patients with preterm premature rupture of membranes. Am J Obstet Gynecol. 2004;191(4):1339–1345.

    Article  PubMed  Google Scholar 

  58. Romero R, Baumann P, Gomez R, et al. The relationship between spontaneous rupture of membranes, labor, and microbial invasion of the amniotic cavity and amniotic fluid concentrations of prostaglandins and thromboxane B2 in term pregnancy. Am J Obstet Gynecol. 1993;168(6 pt 1):1654–1664.

    Article  CAS  PubMed  Google Scholar 

  59. 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 prelabor rupture of membranes. Am J Reprod Immunol. 2010;64(1):38–57.

    PubMed  PubMed Central  Google Scholar 

  60. Hillier SL, Krohn MA, Kiviat NB, Watts DH, Eschenbach DA. Microbiologic causes and neonatal outcomes associated with chorioamnion infection. Am J Obstet Gynecol. 1991;165(4 pt 1):955–961.

    Article  CAS  PubMed  Google Scholar 

  61. Guinn DA, Goldenberg RL, Hauth JC, Andrews WW, Thom E, Romero R. Risk factors for the development of preterm premature rupture of the membranes after arrest of preterm labor. Am J Obstet Gynecol. 1995;173(4):1310–1315.

    Article  CAS  PubMed  Google Scholar 

  62. McDonald HM, O’Loughlin JA, Jolley PT, Vigneswaran R, McDonald PJ. Changes in vaginal flora during pregnancy and association with preterm birth. J Infect Dis. 1994;170(3):724–728.

    Article  CAS  PubMed  Google Scholar 

  63. Regan JA, Chao S, James LS. Premature rupture of membranes, preterm delivery, and group B streptococcal colonization of mothers. Am J Obstet Gynecol. 1981;141(2):184–186.

    Article  CAS  PubMed  Google Scholar 

  64. Alger LS, Lovchik JC, Hebel JR, Blackmon LR, Crenshaw MC. The association of Chlamydia trachomatis, Neisseria gonorrhoeae, and group B streptococci with preterm rupture of the membranes and pregnancy outcome. Am J Obstetrics Gynecol. 1988;159(2):397–404.

    Article  CAS  Google Scholar 

  65. Ekwo EE, Gosselink CA, Woolson R, Moawad A. Risks for premature rupture of amniotic membranes. Int J Epidemiol. 1993; 22(3):495–503.

    Article  CAS  PubMed  Google Scholar 

  66. Cotch MF, Pastorek JG II, Nugent RP, et al. Trichomonas vaginalis associated with low birth weight and preterm delivery. The vaginal infections and prematurity study group. Sex Transm Dis. 1997;24(6):353–360.

    Article  CAS  PubMed  Google Scholar 

  67. Whidbey C, Harrell MI, Burnside K, et al. A hemolytic pigment of Group B Streptococcus allows bacterial penetration of human placenta. J Exp Med. in press. 2013;210(6):1265–1281.

    Article  CAS  Google Scholar 

  68. Cobo T, Kacerovsky M, Palacio M, et al. Intra-amniotic inflammatory response in subgroups of women with preterm prelabor rupture of the membranes. PloS ONE. 2012;7(8):e43677.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Fortunato SJ, Menon R, Lombardi SJ. Role of tumor necrosis factor-alpha in the premature rupture of membranes and preterm labor pathways. Am J Obstet Gynecol. 2002;187(5):1159–1162.

    Article  CAS  PubMed  Google Scholar 

  70. Jacobsson B, Aaltonen R, Rantakokko-Jalava K, Morken NH, Alanen A. Quantification of Ureaplasma urealyticum DNA in the amniotic fluid from patients in PTL and pPROM and its relation to inflammatory cytokine levels. Acta obstetricia et gynecologica Scandinavica. 2009;88(1):63–70.

    Article  CAS  PubMed  Google Scholar 

  71. Romero R, Mazor M, Sepulveda W, Avila C, Copeland D, Williams J. Tumor necrosis factor in preterm and term labor. Am J Obstet Gynecol. 1992;166(5):1576–1587.

    Article  CAS  PubMed  Google Scholar 

  72. Yui J, Garcia-Lloret M, Wegmann TG, Guilbert LJ. Cytotoxicity of tumour necrosis factor-alpha and gamma-interferon against primary human placental trophoblasts. Placenta. 1994;15(8):819–835.

    Article  CAS  PubMed  Google Scholar 

  73. Kumar D, Schatz F, Moore RM, et al. The effects of thrombin and cytokines upon the biomechanics and remodeling of isolated amnion membrane, in vitro. Placenta. 2011;32(3):206–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Li W, Unlugedik E, Bocking AD, Challis JR. The role of prostaglandins in the mechanism of lipopolysaccharide-induced proMMP9 secretion from human placenta and fetal membrane cells. Biol Reprod. 2007;76(4):654–659.

    Article  CAS  PubMed  Google Scholar 

  75. McLaren J, Taylor DJ, Bell SC. Prostaglandin E(2)-dependent production of latent matrix metalloproteinase-9 in cultures of human fetal membranes. Mol Hum Reprod. 2000;6(11):1033–1040.

    Article  CAS  PubMed  Google Scholar 

  76. Ulug U, Goldman S, Ben-Shlomo I, Shalev E. Matrixmetalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F(2alpha) and indomethacin. Mol Hum Reprod. 2001;7(12):1187–1193.

    Article  CAS  PubMed  Google Scholar 

  77. Kodali R, Hajjou M, Berman AB, et al. Chemokines induce matrix metalloproteinase-2 through activation of epidermal growth factor receptor in arterial smooth muscle cells. Cardiovasc Res. 2006;69(3):706–715.

    Article  CAS  PubMed  Google Scholar 

  78. Groom KM, Shennan AH, Jones BA, Seed P, Bennett PR. TOCOX–a randomised, double-blind, placebo-controlled trial of rofecoxib (a COX-2-specific prostaglandin inhibitor) for the prevention of preterm delivery in women at high risk. BJOG. 2005;112(6):725–730.

    Article  CAS  PubMed  Google Scholar 

  79. Khanprakob T, Laopaiboon M, Lumbiganon P, Sangkomkamhang US. Cyclo-oxygenase (COX) inhibitors for preventing preterm labour. Cochrane Database Syst Rev. 2012;10:CD007748.

    PubMed  Google Scholar 

  80. Vanderhoeven JP, Bierle CJ, Kapur RP, et al. Group B streptococcal infection of the choriodecidua induces dysfunction of the cytokeratin network in amniotic epithelium: a pathway to membrane weakening. PLoS Pathog. 2014;10(3):e1003920.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Jones HE, Harris KA, Azizia M, et al. Differing prevalence and diversity of bacterial species in fetal membranes from very preterm and term labor. PLoS One. 2009;4(12):e8205.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. 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(8):e3056.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. 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.

    Article  PubMed  CAS  Google Scholar 

  84. Stout MJ, Conlon B, Landeau M, et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol. 2013;208(3):226. e1–e7.

    Article  Google Scholar 

  85. Stephenson CD, Lockwood CJ, Ma Y, Guller S. Thrombin-dependent regulation of matrix metalloproteinase (MMP)-9 levels in human fetal membranes. J Matern Fetal Neona. 2005;18(1): 17–22.

    Article  CAS  Google Scholar 

  86. Chen D, Dorling A. Critical roles for thrombin in acute and chronic inflammation. J Thromb Haemost. 2009;7(suppl 1):122–126.

    Article  CAS  PubMed  Google Scholar 

  87. Park KW, Jin BK. Thrombin-induced oxidative stress contributes to the death of hippocampal neurons: role of neuronal NADPH oxidase. J Neurosci Res. 2008;86(5):1053–1063.

    Article  CAS  PubMed  Google Scholar 

  88. Lopez JJ, Salido GM, Gomez-Arteta E, Rosado JA, Pariente JA. Thrombin induces apoptotic events through the generation of reactive oxygen species in human platelets. J Thromb Haemost. 2007;5(6):1283–1291.

    Article  CAS  PubMed  Google Scholar 

  89. Harger JH, Hsing AW, Tuomala RE, et al. Risk factors for preterm premature rupture of fetal membranes: a multicenter casecontrol study. Am J Obstet Gynecol. 1990;163(1 pt 1):130–137.

    Article  CAS  PubMed  Google Scholar 

  90. Erez O, Espinoza J, Chaiworapongsa T, et al. A link between a hemostatic disorder and preterm PROM: a role for tissue factor and tissue factor pathway inhibitor. J Matern Fetal Neona. 2008;21(10):732–744.

    Article  CAS  Google Scholar 

  91. 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 Maternal Fetal Med. 2001;10(5):297–300.

    Article  CAS  Google Scholar 

  92. Rosen T, Schatz F, Kuczynski E, Lam H, Koo AB, Lockwood CJ. Thrombin-enhanced matrix metalloproteinase-1 expression: a mechanism linking placental abruption with premature rupture of the membranes. J Matern Fetal Neona. 2002;11(1):11–17.

    Article  CAS  Google Scholar 

  93. Matta P, Lockwood CJ, Schatz F, et al. Thrombin regulates monocyte chemoattractant protein-1 expression in human first trimester and term decidual cells. Am J Obstet Gynecol. 2007;196(3):268.e1–e8.

    Article  CAS  Google Scholar 

  94. Puthiyachirakkal M, Lemerand K, Kumar D, et al. Thrombin weakens the amnion extracellular matrix (ECM) directly rather than through protease activated receptors. Placenta. 2013;34(10):924–931.

    Article  CAS  PubMed  Google Scholar 

  95. England MC, Benjamin A, Abenhaim HA. Increased risk of preterm premature rupture of membranes at early gestational ages among maternal cigarette smokers. Am J Perinatol. 2013;30(10):821–826.

    Article  PubMed  Google Scholar 

  96. Henderson JJ, McWilliam OA, Newnham JP, Pennell CE. Preterm birth aetiology 2004–2008. Maternal factors associated with three phenotypes: spontaneous preterm labour, preterm prelabour rupture of membranes and medically indicated preterm birth. J Matern Fetal Neona. 2012;25(6):642–647.

    Article  Google Scholar 

  97. Burlingame JM, Esfandiari N, Sharma RK, Mascha E, Falcone T. Total antioxidant capacity and reactive oxygen species in amniotic fluid. Obstet Gynecol. 2003;101(4):756–761.

    CAS  PubMed  Google Scholar 

  98. Falk SJ, Campbell LJ, Lee-Parritz A, et al. Expectant management in spontaneous preterm premature rupture of membranes between 14 and 24 weeks’ gestation. J Perinatol. 2004;24(10):611–616.

    Article  PubMed  Google Scholar 

  99. Sooranna SR, Lee Y, Kim LU, Mohan AR, Bennett PR, Johnson MR. Mechanical stretch activates type 2 cyclooxygenase via activator protein-1 transcription factor in human myometrial cells. Mol Hum Reprod. 2004;10(2):109–113.

    Article  CAS  PubMed  Google Scholar 

  100. Terzidou V, Sooranna SR, Kim LU, Thornton S, Bennett PR, Johnson MR. Mechanical stretch up-regulates the human oxytocin receptor in primary human uterine myocytes. J Clin Endocrinol Metab. 2005;90(1):237–246.

    Article  CAS  PubMed  Google Scholar 

  101. Loudon JA, Sooranna SR, Bennett PR, Johnson MR. Mechanical stretch of human uterine smooth muscle cells increases IL-8 mRNA expression and peptide synthesis. Mol Hum Reprod. 2004;10(12):895–899.

    Article  CAS  PubMed  Google Scholar 

  102. Hua R, Pease JE, Sooranna SR, et al. Stretch and inflammatory cytokines drive myometrial chemokine expression via NF-kappaB activation. Endocrinology. 2012;153(1):481–491.

    Article  CAS  PubMed  Google Scholar 

  103. Zhao Y, Koga K, Osuga Y, et al. Cyclic stretch augments production of neutrophil chemokines and matrix metalloproteinases-1 (MMP-1) from human decidual cells, and the production was reduced by progesterone. Am J Reprod Immunol. 2013;69(5):454–462.

    Article  CAS  PubMed  Google Scholar 

  104. Durnwald CP, Momirova V, Rouse DJ, et al. Second trimester cervical length and risk of preterm birth in women with twin gestations treated with 17-alpha hydroxyprogesterone caproate. J Matern Fetal Neona. 2010;23(12):1360–1364.

    Article  CAS  Google Scholar 

  105. Manabe Y, Manabe A, Takahashi A. F prostaglandin levels in amniotic fluid during balloon-induced cervical softening and labor at term. Prostaglandins. 1982;23(2):247–256.

    Article  CAS  PubMed  Google Scholar 

  106. Anum EA, Hill LD, Pandya A, Strauss JF III. Connective tissue and related disorders and preterm birth: clues to genes contributing to prematurity. Placenta. 2009;30(3):207–215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Barabas AP. Ehlers-Danlos syndrome: associated with prematurity and premature rupture of foetal membranes; possible increase in incidence. Br Med J. 1966;2(5515):682–684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Rossiter JP, Repke JT, Morales AJ, Murphy EA, Pyeritz RE. A prospective longitudinal evaluation of pregnancy in the Marfan syndrome. Am J Obstet Gynecol. 1995;173(5):1599–1606.

    Article  CAS  PubMed  Google Scholar 

  109. Rocnik EF, van der Veer E, Cao H, Hegele RA, Pickering JG. Functional linkage between the endoplasmic reticulum protein Hsp47 and procollagen expression in human vascular smooth muscle cells. J Biol Chem. 2002;277(41):38571–38578.

    Article  CAS  PubMed  Google Scholar 

  110. Wang H, Parry S, Macones G, et al. A functional SNP in the promoter of the SERPINH1 gene increases risk of preterm premature rupture of membranes in African Americans. Proc Natl Acad Sci U S A. 2006;103(36):13463–13467.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Fujimoto T, Parry S, Urbanek M, et al. A single nucleotide polymorphism in the matrix metalloproteinase-1 (MMP-1) promoter influences amnion cell MMP-1 expression and risk for preterm premature rupture of the fetal membranes. J Biol Chem. 2002;277(8):6296–6302.

    Article  CAS  PubMed  Google Scholar 

  112. Kalish RB, Nguyen DP, Vardhana S, Gupta M, Perni SC, Witkin SS. A single nucleotide A>G polymorphism at position -670 in the Fas gene promoter: relationship to preterm premature rupture of fetal membranes in multifetal pregnancies. Am J Obstet Gynecol. 2005;192(1):208–212.

    Article  CAS  PubMed  Google Scholar 

  113. Kalish RB, Vardhana S, Normand NJ, Gupta M, Witkin SS. Association of a maternal CD14 - 159 gene polymorphism with preterm premature rupture of membranes and spontaneous preterm birth in multi-fetal pregnancies. J Reprod Immunol. 2006;70(1–2):109–117.

    Article  CAS  PubMed  Google Scholar 

  114. Annells MF, Hart PH, Mullighan CG, et al. Interleukins-1, -4, -6, -10, tumor necrosis factor, transforming growth factor-beta, FAS, and mannose-binding protein C gene polymorphisms in Australian women: Risk of preterm birth. Am J Obstet Gynecol. 2004;191(6):2056–2067.

    Article  CAS  PubMed  Google Scholar 

  115. Roberts AK, Monzon-Bordonaba F, Van Deerlin PG, et al. Association of polymorphism within the promoter of the tumor necrosis factor alpha gene with increased risk of preterm premature rupture of the fetal membranes. Am J Obstet Gynecol. 1999;180(5):1297–1302.

    Article  CAS  PubMed  Google Scholar 

  116. Fuks A, Parton LA, Polavarapu S, et al. Polymorphism of Fas and Fas ligand in preterm premature rupture of membranes in singleton pregnancies. Am J Obstet Gynecol. 2005;193(3 pt 2):1132–1136.

    Article  CAS  PubMed  Google Scholar 

  117. Romero R, Friel LA, Velez Edwards DR, et al. A genetic association study of maternal and fetal candidate genes that predispose to preterm prelabor rupture of membranes (PROM). Am J Obstet Gynecol. 2010;203(4):361. e1–e30.

    Article  CAS  Google Scholar 

  118. Asrat T, Lewis DF, Garite TJ, et al. Rate of recurrence of preterm premature rupture of membranes in consecutive pregnancies. Am J Obstet Gynecol. 1991;165(4 pt 1):1111–1115.

    Article  CAS  PubMed  Google Scholar 

  119. Ekwo EE, Gosselink CA, Moawad A. Unfavorable outcome in penultimate pregnancy and premature rupture of membranes in successive pregnancy. Obstet Gynecol. 1992;80(2):166–172.

    CAS  PubMed  Google Scholar 

  120. Lee T, Carpenter MW, Heber WW, Silver HM. Preterm premature rupture of membranes: risks of recurrent complications in the next pregnancy among a population-based sample of gravid women. Am J Obstet Gynecol. 2003;188(1):209–213.

    Article  PubMed  Google Scholar 

  121. Mercer BM, Goldenberg RL, Meis PJ, et al. The preterm prediction study: prediction of preterm premature rupture of membranes through clinical findings and ancillary testing, the national institute of child health and human development maternal-fetal medicine units network. Am J Obstet Gynecol. 2000;183(3):738–745.

    Article  CAS  PubMed  Google Scholar 

  122. Keirse MJ. Progestogen administration in pregnancy may prevent preterm delivery. Br J Obstet Gynaecol. 1990;97(2):149–154.

    Article  CAS  PubMed  Google Scholar 

  123. Meis PJ, Klebanoff M, Thom E, et al. Prevention of recurrent preterm delivery by 17 alpha-hydroxyprogesterone caproate. N Engl J Med. 2003;348(24):2379–2385.

    Article  CAS  PubMed  Google Scholar 

  124. da Fonseca EB, Bittar RE, Carvalho MH, Zugaib M. Prophylactic administration of progesterone by vaginal suppository to reduce the incidence of spontaneous preterm birth in women at increased risk: a randomized placebo-controlled double-blind study. Am J Obstet Gynecol. 2003;188(2):419–424.

    Article  CAS  PubMed  Google Scholar 

  125. O’Brien JM, Adair CD, Lewis DF, et al. Progesterone vaginal gel for the reduction of recurrent preterm birth: primary results from a randomized, double-blind, placebo-controlled trial. Ultrasound Obstet Gynecol. 2007;30(5):687–696.

    Article  PubMed  Google Scholar 

  126. Fonseca EB, Celik E, Parra M, Singh M, Nicolaides KH, Fetal Medicine Foundation Second Trimester Screening G. Progesterone and the risk of preterm birth among women with a short cervix. N Engl J Med. 2007;357(5):462–469.

    Article  CAS  PubMed  Google Scholar 

  127. Rouse DJ, Caritis SN, Peaceman AM, et al. A trial of 17 alphahydroxyprogesterone caproate to prevent prematurity in twins. N Engl J Med. 2007;357(5):454–461.

    Article  CAS  PubMed  Google Scholar 

  128. Keirse MJ. Progesterone and preterm: seventy years of “deja vu” or “still to be seen”? Birth. 2004;31(3):230–235.

    Article  PubMed  Google Scholar 

  129. Briery CM, Veillon EW, Klauser CK, et al. Women with preterm premature rupture of the membranes do not benefit from weekly progesterone. Am J Obstet Gynecol. 2011;204(1):54.e1–e5.

    Article  Google Scholar 

  130. Merlino A, Welsh T, Erdonmez T, et al. Nuclear progesterone receptor expression in the human fetal membranes and decidua at term before and after labor. Reprod Sci. 2009;16(4):357–363.

    Article  CAS  PubMed  Google Scholar 

  131. Sfakianaki AK, Norwitz ER. Mechanisms of progesterone action in inhibiting prematurity. J Matern Fetal Neonatal Med. 2006;19(12):763–772.

    Article  CAS  PubMed  Google Scholar 

  132. 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(9607):164–175.

    Article  PubMed  Google Scholar 

  133. Luo G, Abrahams VM, Tadesse S, et al. Progesterone inhibits basal and TNF-alpha-induced apoptosis in fetal membranes: a novel mechanism to explain progesterone-mediated prevention of preterm birth. Reprod Sci. 2010;17(6):532–539.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department Obstetrics & Gynecology, University of Washington, 1959 NE Pacific St, Campus Box 356460, Seattle, WA, USA

    Sophia M. R. Lannon MD, MPH, David A. Eschenbach MD, Michael G. Gravett MD & Kristina M. Adams Waldorf MD

  2. Swedish Medical Center, Seattle, WA, USA

    Jeroen P. Vanderhoeven MD

  3. Global Alliance to Prevent Prematurity & Stillbirth, Seattle, WA, USA

    Michael G. Gravett MD

Authors
  1. Sophia M. R. Lannon MD, MPH
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeroen P. Vanderhoeven MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David A. Eschenbach MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael G. Gravett MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kristina M. Adams Waldorf MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sophia M. R. Lannon MD, MPH.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lannon, S.M.R., Vanderhoeven, J.P., Eschenbach, D.A. et al. Synergy and Interactions Among Biological Pathways Leading to Preterm Premature Rupture of Membranes. Reprod. Sci. 21, 1215–1227 (2014). https://doi.org/10.1177/1933719114534535

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719114534535

Keywords

Search

Navigation