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Original Article

A subset of patients destined to develop spontaneous preterm labor has an abnormal angiogenic/anti-angiogenic profile in maternal plasma: Evidence in support of pathophysiologic heterogeneity of preterm labor derived from a longitudinal study

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Pages 1122-1139 | Received 13 Apr 2009, Accepted 23 Apr 2009, Published online: 16 Nov 2009

References

  • Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M. The preterm parturition syndrome. BJOG 2006;113(Suppl 3):17–42.
  • 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.
  • Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008;371:75–84.
  • Mathews TJ, MacDorman MF. Infant mortality statistics from the 2005 period linked birth/infant death data set. Natl Vital Stat Rep 2008;57:1–32.
  • Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, Sabo V, Athanassiadis AP, Hobbins JC. 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;161:817–824.
  • Romero R, Mazor M, Wu YK, Avila C, Oyarzun E, Mitchell MD. Bacterial endotoxin and tumor necrosis factor stimulate prostaglandin production by human decidua. Prostaglandins Leukot Essent Fatty Acids 1989;37:183–186.
  • Romero R, Avila C, Brekus CA, Morotti R. The role of systemic and intrauterine infection in preterm parturition. Ann N Y Acad Sci 1991;622:355–375.
  • Gibbs RS, Romero R, Hillier SL, Eschenbach DA, Sweet RL. A review of premature birth and subclinical infection. Am J Obstet Gynecol 1992;166:1515–1528.
  • Dudley DJ, Chen CL, Branch DW, Hammond E, Mitchell MD. A murine model of preterm labor: inflammatory mediators regulate the production of prostaglandin E2 and interleukin-6 by murine decidua. Biol Reprod 1993;48:33–39.
  • Yoon BH, Park KH, Koo JN, Kwon JH, Jun JK, Syn HC, Romero R. Intra-amniotic infection of twin pregnancies with preterm labor. Am J Obstet Gynecol 1997;3:127–130.
  • Wenstrom KD, Andrews WW, Hauth JC, Goldenberg RL, DuBard MB, Cliver SP. Elevated second-trimester amniotic fluid interleukin-6 levels predict preterm delivery. Am J Obstet Gynecol 1998;178:546–550.
  • Goldenberg RL, Andrews WW, Hauth JC. Choriodecidual infection and preterm birth. Nutr Rev 2002;60:S19–S25.
  • Kloeck FK, Jung H. In vitro release of prostaglandins from the human myometrium under the influence of stretching. Am J Obstet Gynecol 1973;115:1066–1069.
  • Laudanski T, Rocki W. The effects on stretching and prostaglandin F2alpha on the contractile and bioelectric activity of the uterus in rat. Acta Physiol Pol 1975;26:385–393.
  • Ou CW, Orsino A, Lye SJ. Expression of connexin-43 and connexin-26 in the rat myometrium during pregnancy and labor is differentially regulated by mechanical and hormonal signals. Endocrinology 1997;138:5398–5407.
  • Phelan JP, Park YW, Ahn MO, Rutherford SE. Polyhydramnios and perinatal outcome. J Perinatol 1990;10:347–350.
  • Romero R, Mazor M, Avila C, Quintero R, Munoz H. Uterine “allergy”: A novel mechanism for preterm labor. Am J Obstet Gynecol 1991;164:375.
  • Garfield RE, Bytautiene E, Vedernikov YP, Marshall JS, Romero R. Modulation of rat uterine contractility by mast cells and their mediators. Am J Obstet Gynecol 2000;183:118–125.
  • Bytautiene E, Romero R, Vedernikov YP, El-Zeky F, Saade GR, Garfield RE. Induction of labor and delivery by allergic reaction and prevention by histamine H1 receptor antagonist. Am J Obstet Gynecol. 2004;191:1356–1361.
  • Ludmir J, Samuels P, Brooks S, Mennuti MT. Pregnancy outcome of patients with uncorrected uterine anomalies managed in a high-risk obstetric setting. Obstet Gynecol 1990;75:906–910.
  • Iams JD, Johnson FF, Sonek J, Sachs L, Gebauer C, Samuels P. Cervical competence as a continuum: a study of ultrasonographic cervical length and obstetric performance. Am J Obstet Gynecol 1995;172:1097–1103.
  • Hassan SS, Romero R, Berry SM, Dang K, Blackwell SC, Treadwell MC, Wolfe HM. Patients with an ultrasonographic cervical length <or =15 mm have nearly a 50% risk of early spontaneous preterm delivery. Am J Obstet Gynecol 2000;182:1458–1467.
  • Check JH, Lee G, Epstein R, Vetter B. Increased rate of preterm deliveries in untreated women with luteal phase deficiencies. Preliminary report. Gynecol Obstet Invest 1992;33:183–184.
  • Keirse MJ. Progestogen administration in pregnancy may prevent preterm delivery. Br J Obstet Gynaecol 1990;97:149–154.
  • Dudley DJ, Branch DW, Edwin SS, Mitchell MD. Induction of preterm birth in mice by RU486. Biol Reprod 1996;55:992–995.
  • Meis PJ, Klebanoff M, Thom E, Dombrowski MP, Sibai B, Moawad AH, Spong CY, Hauth JC, Miodovnik M, Varner MW, et al Prevention of recurrent preterm delivery by 17 alpha-hydroxyprogesterone caproate. N Engl J Med 2003;348:2379–2385.
  • Liggins GC. Premature parturition after infusion of corticotrophin or cortisol into foetal lambs. J Endocrinol 1968;42:323–329.
  • Jones SA, Challis JR. Steroid corticotrophin-releasing hormone, ACTH and prostaglandin interactions in the amnion and placenta of early pregnancy in man. J Endocrinol 1990;125:153–159.
  • Challis JR. CRH, a placental clock and preterm labour. Nat Med 1995;1:416.
  • Copper RL, Goldenberg RL, Das A, Elder N, Swain M, Norman G, Ramsey R, Cotroneo P, Collins BA, Johnson F, et al The preterm prediction study: maternal stress is associated with spontaneous preterm birth at less than thirty-five weeks' gestation. National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Am J Obstet Gynecol 1996;175:1286–1292.
  • Hobel CJ, Dunkel-Schetter C, Roesch SC, Castro LC, Arora CP. Maternal plasma corticotropin-releasing hormone associated with stress at 20 weeks' gestation in pregnancies ending in preterm delivery. Am J Obstet Gynecol 1999;180:S257–S263.
  • Combs CA, Katz MA, Kitzmiller JL, Brescia RJ. Experimental preeclampsia produced by chronic constriction of the lower aorta: validation with longitudinal blood pressure measurements in conscious rhesus monkeys. Am J Obstet Gynecol 1993;169:215–223.
  • Kim YM, Bujold E, Chaiworapongsa T, Gomez R, Yoon BH, Thaler HT, Rotmensch S, Romero R. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2003;189:1063–1069.
  • Kim YM, Chaiworapongsa T, Gomez R, Bujold E, Yoon BH, Rotmensch S, Thaler HT, Romero R. Failure of physiologic transformation of the spiral arteries in the placental bed in preterm premature rupture of membranes. Am J Obstet Gynecol 2002;187:1137–1142.
  • Fonseca E, Yu CK, Singh M, Papageorghiou AT, Nicolaides KH. Relationship between second-trimester uterine artery Doppler and spontaneous early preterm delivery. Ultrasound Obstet Gynecol 2006;27:301–305.
  • Brar HS, Medearis AL, DeVore GR, Platt LD. Maternal and fetal blood flow velocity waveforms in patients with preterm labor: prediction of successful tocolysis. Am J Obstet Gynecol 1988;159:947–950.
  • Arias F, Rodriquez L, Rayne SC, Kraus FT. Maternal placental vasculopathy and infection: two distinct subgroups among patients with preterm labor and preterm ruptured membranes. Am J Obstet Gynecol 1993;168:585–591.
  • Torry DS, Wang HS, Wang TH, Caudle MR, Torry RJ. Preeclampsia is associated with reduced serum levels of placenta growth factor. Am J Obstet Gynecol 1998;179:1539–1544.
  • Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 2003;188:177–182.
  • Reuvekamp A, Velsing-Aarts FV, Poulina IE, Capello JJ, Duits AJ. Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre-eclampsia. Br J Obstet Gynaecol 1999;106:1019–1022.
  • Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003;88:2348–2351.
  • Tsatsaris V, Goffin F, Munaut C, Brichant JF, Pignon MR, Noel A, Schaaps JP, Cabrol D, Frankenne F, Foidart JM. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 2003;88:5555–5563.
  • Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, et al Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003;111:649–658.
  • Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, et al Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004;350:672–683.
  • Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee KY, Goncalves LF, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol 2004;190:1541–1547.
  • Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, et al Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005;17:3–18.
  • Park CW, Park JS, Shim SS, Jun JK, Yoon BH, Romero R. An elevated maternal plasma, but not amniotic fluid, soluble fms-like tyrosine kinase-1 (sFlt-1) at the time of mid-trimester genetic amniocentesis is a risk factor for preeclampsia. Am J Obstet Gynecol 2005;193:984–989.
  • Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, et al Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642–649.
  • Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, et al Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006;355:992–1005.
  • Robinson CJ, Johnson DD, Chang EY, Armstrong DM, Wang W. Evaluation of placenta growth factor and soluble Fms-like tyrosine kinase 1 receptor levels in mild and severe preeclampsia. Am J Obstet Gynecol 2006;195:255–259.
  • Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, Gotsch F, Erez O, Mazaki-Tovi S, et al A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med 2008;21:9–23.
  • Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, Goncalves L, Edwin S, Kim YM, Erez O, Kusanovic JP, et al Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonatal Med 2008;21:41–52.
  • Vatten LJ, Eskild A, Nilsen TI, Jeansson S, Jenum PA, Staff AC. Changes in circulating level of angiogenic factors from the first to second trimester as predictors of preeclampsia. Am J Obstet Gynecol 2007;196:239–236.
  • Wikstrom AK, Larsson A, Eriksson UJ, Nash P, Norden-Lindeberg S, Olovsson M. Placental growth factor and soluble FMS-like tyrosine kinase-1 in early-onset and late-onset preeclampsia. Obstet Gynecol 2007;109:1368–1374.
  • Unal ER, Robinson CJ, Johnson DD, Chang EY. Second-trimester angiogenic factors as biomarkers for future-onset preeclampsia. Am J Obstet Gynecol 2007;197:211–214.
  • Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic JP, Gotsch F, Edwin S, Nien JK, Chaiworapongsa T, et al The change in concentrations of angiogenic and anti-angiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age. J Matern Fetal Neonatal Med 2008;21:279–287.
  • Crispi F, Llurba E, Dominguez C, Martin-Gallan P, Cabero L, Gratacos E. Predictive value of angiogenic factors and uterine artery Doppler for early- versus late-onset pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 2008;31:303–309.
  • Savvidou MD, Noori M, Anderson JM, Hingorani AD, Nicolaides KH. Maternal endothelial function and serum concentrations of placental growth factor and soluble endoglin in women with abnormal placentation. Ultrasound Obstet Gynecol 2008;32:871–876.
  • Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, Goncalves LF, Edwin S, Kusanovic JP, Erez O, Than NG, et al The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation. J Matern Fetal Neonatal Med 2008;21:25–40.
  • Signore C, Mills JL, Qian C, Yu K, Lam C, Epstein FH, Karumanchi SA, Levine RJ. Circulating angiogenic factors and placental abruption. Obstet Gynecol 2006;108:338–344.
  • Espinoza J, Romero R, Nien JK, Kusanovic JP, Richani K, Gomez R, Kim CJ, Mittal P, Gotsh F, Erez O, et al A role of the anti-angiogenic factor sVEGFR-1 in the ‘mirror syndrome’ (Ballantyne's syndrome). J Matern Fetal Neonatal Med 2006;19:607–613.
  • Kusanovic JP, Romero R, Espinoza J, Nien JK, Kim CJ, Mittal P, Edwin S, Erez O, Gotsch F, Mazaki-Tovi S, et al Twin-to-twin transfusion syndrome: an antiangiogenic state? Am J Obstet Gynecol 2008;198:382–388.
  • Espinoza J, Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Nien JK, Kusanovic JP, Erez O, Bujold E, Goncalves LF, et al Unexplained fetal death: another anti-angiogenic state. J Matern Fetal Neonatal Med 2007;20:495–507.
  • Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature 2000;407:242–248.
  • Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669–676.
  • Shibuya M. Vascular endothelial growth factor-dependent and -independent regulation of angiogenesis. BMB Rep 2008;41:278–286.
  • Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 1998;273:30336–30343.
  • Ferrara N. The role of VEGF in the regulation of physiological and pathological angiogenesis. EXS 2005;94:209–231.
  • Shibuya M. Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 2006.
  • Tchaikovski V, Fellbrich G, Waltenberger J. The molecular basis of VEGFR-1 signal transduction pathways in primary human monocytes. Arterioscler Thromb Vasc Biol 2008;28:322–328.
  • Ebos JM, Bocci G, Man S, Thorpe PE, Hicklin DJ, Zhou D, Jia X, Kerbel RS. A naturally occurring soluble form of vascular endothelial growth factor receptor 2 detected in mouse and human plasma. Mol Cancer Res 2004;2:315–326.
  • Lin P, Sankar S, Shan S, Dewhirst MW, Polverini PJ, Quinn TQ, Peters KG. Inhibition of tumor growth by targeting tumor endothelium using a soluble vascular endothelial growth factor receptor. Cell Growth Differ 1998;9:49–58.
  • McLeod DS, Taomoto M, Cao J, Zhu Z, Witte L, Lutty GA. Localization of VEGF receptor-2 (KDR/Flk-1) and effects of blocking it in oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 2002;43:474–482.
  • Ten DP, Goumans MJ, Pardali E. Endoglin in angiogenesis and vascular diseases. Angiogenesis 2008;11:79–89.
  • Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, et al Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996;380:435–439.
  • Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380:439–442.
  • Fong GH, Zhang L, Bryce DM, Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 1999;126:3015–3025.
  • Cheung CY. Vascular endothelial growth factor: possible role in fetal development and placental function. J Soc Gynecol Investig 1997;4:169–117.
  • Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163–168.
  • Pacora P, Chaiworapongsa T, Maymon E, Kim YM, Gomez R, Yoon BH, Ghezzi F, Berry SM, Qureshi F, Jacques SM, et al Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med 2002;11:18–25.
  • Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation – a workshop report. Placenta 2005;26(Suppl A):S114–S117.
  • Tsai J, Klebanoff MA, Qian C, Yu K, Levine RJ. Circulating angiogenic factors in spontaneous preterm labor and delivery. Am J Obstet Gynecol 2009;197:S7.
  • Haddad R, Romero R, Gould BR, Tromp G, Gotsch F, Edwin SS, Zingg HH. Angiogenesis gene expression in mouse uterus during the common pathway of parturition. Am J Obstet Gynecol 2008;198:539–548.
  • Gu Y, Lewis DF, Wang Y. Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1, and placental growth factor in normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2008;93:260–266.
  • Caniggia I, Taylor CV, Ritchie JW, Lye SJ, Letarte M. Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 1997;138:4977–4988.
  • Caniggia I, Grisaru-Gravnosky S, Kuliszewsky M, Post M, Lye SJ. Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J Clin Invest 1999;103:1641–1650.
  • Soregaroli M, Valcamonico A, Scalvi L, Danti L, Frusca T. Late normalisation of uterine artery velocimetry in high risk pregnancy. Eur J Obstet Gynecol Reprod Biol 2001;95:42–45.
  • Dumont N, O'Connor-McCourt MD, Philip A. Transforming growth factor-beta receptors on human endometrial cells: identification of the type I, II, and III receptors and glycosyl-phosphatidylinositol anchored TGF-beta binding proteins. Mol Cell Endocrinol 1995;111:57–66.
  • Ouellette MJ, Hamel L, Tremblay N, Lamothe M, St-Jacques S. Characterization of endoglin on mouse uterine stromal cells. J Reprod Fertil 1999;117:229–239.
  • Godkin JD, Dore JJ. Transforming growth factor beta and the endometrium. Rev Reprod 1998;3:1–6.
  • Shynlova O, Tsui P, Dorogin A, Langille BL, Lye SJ. The expression of transforming growth factor beta in pregnant rat myometrium is hormone and stretch dependent. Reproduction 2007;134:503–511.
  • Kuscu NK, Lacin S, Vatansever S, Yildirim Y, Var A, Uyanik BS, Koyuncu F. Immunolocalization of transforming growth factor-beta 3 in pregnant human myometrium. Acta Obstet Gynecol Scand 2001;80:1079–1083.
  • Awad SS, Lamb HK, Morgan JM, Dunlop W, Gillespie JI. Differential expression of ryanodine receptor RyR2 mRNA in the non-pregnant and pregnant human myometrium. Biochem J 1997;322:777–783.
  • Hatthachote P, Morgan J, Dunlop W, Europe-Finner GN, Gillespie JI. Gestational changes in the levels of transforming growth factor-beta1 (TGFbeta1) and TGFbeta receptor types I and II in the human myometrium. J Clin Endocrinol Metab 1998;83:2987–2992.
  • Challis JRG, Matthews SG, Gibb W, Lye SJ. Endocrine and paracrine regulation of birth at term and preterm. Endocrinol Rev 2000;21:514–550.
  • Bry K, Lappalainen U. Interleukin-4 and transforming growth factor-beta 1 modulate the production of interleukin-1 receptor antagonist and of prostaglandin E2 by decidual cells. Am J Obstet Gynecol 1994;170:1194–1198.
  • Bry K, Lappalainen U, Hallman M. Interleukin-1 binding and prostaglandin E2 synthesis by amnion cells in culture: regulation by tumor necrosis factor-alpha, transforming growth factor-beta, and interleukin-1 receptor antagonist. Biochim Biophys Acta 1993;1181:31–36.
  • Romero R. Prenatal medicine: the child is the father of the man. Prenat Neonatal Med 1996;1:8–11.
  • Redman CW, Sacks GP, Sargent IL. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999;180:499–506.
  • Sacks GP, Studena K, Sargent K, Redman CW. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998;179:80–86.
  • Gervasi MT, Chaiworapongsa T, Pacora P, Naccasha N, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001;185:792–797.
  • Naccasha N, Gervasi MT, Chaiworapongsa T, Berman S, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in normal pregnancy and maternal infection. Am J Obstet Gynecol 2001;185:1118–1123.
  • Bujold E, Chaiworapongsa T, Romero R, Gervasi MT, Espinoza J, Goncalves LF, Berman S, Yoon BH, Kim YM. Neonates born to pre-eclamptic mothers have a higher percentage of natural killer cells (CD3-/CD56+16+) in umbilical cord blood than those without pre-eclampsia. J Matern Fetal Neonatal Med 2003;14:305–312.
  • Chaiworapongsa T, Gervasi MT, Refuerzo J, Espinoza J, Yoshimatsu J, Berman S, Romero R. Maternal lymphocyte subpopulations (CD45RA+ and CD45RO+) in pre-eclampsia. Am J Obstet Gynecol 2002;187:889–893.
  • Chaiworapongsa T, Gervasi MT, Espinoza J, Bujold E, Kim YM, Blackwell SC, Romero R. Preeclampsia and SGA differ by the extent of monocyte but not neutrophil, metabolic activity and oxidative burst. Am J Obstet Gynecol 2002;187:S220.
  • Gervasi MT, Chaiworapongsa T, Naccasha N, Blackwell S, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of maternal monocytes and granulocytes in preterm labor with intact membranes. Am J Obstet Gynecol 2001;185:1124–1129.
  • Gervasi MT, Chaiworapongsa T, Naccasha N, Pacora P, Berman S, Maymon E, Kim JC, Kim YM, Yoshimatsu J, Espinoza J, et al Maternal intravascular inflammation in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2002;11:171–175.
  • Blackwell S, Romero R, Chaiworapongsa T, Refuerzo J, Gervasi MT, Yoshimatsu J, Espinoza J, Berman S, Yoon BH. Unexplained fetal death is associated with changes in the adaptive limb of the maternal immune response consistent with prior antigenic exposure. J Matern Fetal Neonatal Med 2003;14:241–246.
  • Wu WX, Zhang Q, Ma XH, Unno N, Nathanielsz PW. Suppression subtractive hybridization identified a marked increase in thrombospondin-1 associated with parturition in pregnant sheep myometrium. Endocrinology 1999;140:2364–2371.
  • Charpigny G, Leroy MJ, Breuiller-Fouche M, Tanfin Z, Mhaouty-Kodja S, Robin P, Leiber D, Cohen-Tannoudji J, Cabrol D, Barberis C, et al A functional genomic study to identify differential gene expression in the preterm and term human myometrium. Biol Reprod 2003;68:2289–2296.
  • Esplin MS, Fausett MB, Peltier MR, Hamblin S, Silver RM, Branch DW, Adashi EY, Whiting D. The use of cDNA microarray to identify differentially expressed labor-associated genes within the human myometrium during labor. Am J Obstet Gynecol 2005;193:404–413.
  • Bukowski R, Hankins GD, Saade GR, Anderson GD, Thornton S. Labor-associated gene expression in the human uterine fundus, lower segment, and cervix. PLoS.Med. 2006;3:e169.
  • Hassan SS, Romero R, Haddad R, Hendler I, Khalek N, Tromp G, Diamond MP, Sorokin Y, Malone J Jr. The transcriptome of the uterine cervix before and after spontaneous term parturition. Am J Obstet Gynecol 2006;195:778–786.
  • Klimaviciute A, Calciolari J, Bertucci E, Belin-Tornblom S, Stjernholm-Vladic Y, Bystrom B, Petraglia F, Ekman-Ordeberg G. Corticotropin-releasing hormone, its binding protein and receptors in human cervical tissue at preterm and term labor in comparison to non-pregnant state. Reprod Biol Endocrinol 2006;4:29.
  • Hassan SS, Romero R, Tarca AL, Draghici S, Pineles B, Bugrim A, Khalek N, Camacho N, Mittal P, Yoon BH, et al Signature pathways identified from gene expression profiles in the human uterine cervix before and after spontaneous term parturition. Am J Obstet Gynecol 2007;197:250–257.
  • Marvin KW, Keelan JA, Eykholt RL, Sato TA, Mitchell MD. Expression of angiogenic and neurotrophic factors in the human amnion and choriodecidua. Am J Obstet Gynecol 2002;187:728–734.
  • Daneshmand SS, Chmait RH, Moore TR, Bogic L. Preterm premature rupture of membranes: vascular endothelial growth factor and its association with histologic chorioamnionitis. Am J Obstet Gynecol 2002;187:1131–1136.
  • Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Mazor M, Romero R. Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am J Obstet Gynecol 2006;195:394–424.
  • Montenegro D, Romero R, Kim SS, Tarca AL, Draghici S, Kusanovic JP, Kim JS, Lee DC, Erez O, Gotsch F, et al Expression patterns of microRNAs in the chorioamniotic membranes: a role for microRNAs in human pregnancy and parturition. J Pathol 2009;217:113–121.
  • Kramer BW, Kaemmerer U, Kapp M, Herbst D, Marx A, Berg D, Groneck PA, Speer CP. Decreased expression of angiogenic factors in placentas with chorioamnionitis after preterm birth. Pediatr Res 2005;58:607–612.
  • Bollopragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S. Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am J Obstet Gynecol 2009;200:104–111.
  • Romero R, Espinoza J, Gotsch F, Kusanovic JP, Friel LA, Erez O, Mazaki-Tovi S, Than NG, Hassan S, Tromp G. The use of high-dimensional biology (genomics, transcriptomics, proteomics, and metabolomics) to understand the preterm parturition syndrome. BJOG 2006;113(Suppl 3):118–135.
  • Romero R, Gonzalez R, Sepulveda W, Brandt F, Ramirez M, Sorokin Y, Mazor M, Treadwell MC, Cotton DB. 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.
  • Romero R, Yoon BH, Mazor M, Gomez R, Diamond MP, Kenney JS, Ramirez M, Fidel PL, Sorokin Y, Cotton D. The diagnostic and prognostic value of amniotic fluid white blood cell count, glucose, interleukin-6, and gram stain in patients with preterm labor and intact membranes. Am J Obstet Gynecol 1993;169:805–816.
  • Romero R, Espinoza J, Chaiworapongsa T, Kalache K. Infection and prematurity and the role of preventative strategies. Sem Neonatal. 2002;7:259–274.
  • Romero R, Gomez R, Chaiworapongsa T, Conoscenti G, Kim JC, Kim YM. The role of infection in preterm labour and delivery. Paediatr Perinat Epidemiol 2001;15:41–56.
  • 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.
  • Hitti J, Tarczy-Hornoch P, Murphy J, Hillier SL, Aura J, Eschenbach DA. Amniotic fluid infection, cytokines, and adverse outcome among infants at 34 weeks' gestation or less. Obstet Gynecol 2001;98:1080–1088.
  • Gibbs RS, Romero R, Hillier SL, Eschenbach DA, Sweet RL. A review of premature birth and subclinical infection. Am J Obstet Gynecol 1992;166:1515–1528.
  • Gupta M, Mestan KK, Martin CR, Pearson C, Ortiz K, Fu L, Stubblefield P, Cerda S, Kasznica JM, Wang X. Impact of clinical and histologic correlates of maternal and fetal inflammatory response on gestational age in preterm births. J Matern.Fetal Neonatal Med. 2007;20:39–46.

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