An imbalance between angiogenic and anti-angiogenic factors precedes fetal death in a subset of patients: Results of a longitudinal study

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 23, Issue 12, 2010, Pages 1384-1399

  Romero, Roberto ^a,b,c,d   Chaiworapongsa, Tinnakorn ^a,b,d   Erez, Offer ^a,b,d   Tarca, Adi L ^a,b,e   Gervasi, Maria Teresa ^f   Kusanovic, Juan Pedro ^a,b,d   Mittal, Pooja ^a,b,d   Ogge, Giovanna ^a,b   Vaisbuch, Edi ^a,b,d   Mazaki Tovi, Shali ^a,b,d   Dong, Zhong ^a,b   Kim, Sun Kwon ^a,b   Yeo, Lami ^a,b,d   Hassan, Sonia S ^a,b,d  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HUTZEL HOSPITAL   (United States)

^e Wayne State University   (United States)

^f UNIVERSITY HOSPITAL OF PADOVA   (Italy)

Author keywords

anti angiogenic state; fetal demise; mixed effect model; placental growth factor; pregnancy; sFlt 1; soluble endoglin; Soluble VEGF receptor 1; stillbirth

Indexed keywords

ANGIOGENIC FACTOR; PLACENTAL GROWTH FACTOR; VASCULOTROPIN RECEPTOR;

ADOLESCENT; ADULT; ARTICLE; BIRTH WEIGHT; BLOOD SAMPLING; CASE CONTROL STUDY; CONTROLLED STUDY; DOPPLER FLOWMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FETUS DEATH; FIRST TRIMESTER PREGNANCY; GESTATIONAL AGE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INFANT; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MATERNAL DISEASE; MATERNAL PLASMA; PLACENTA; PREGNANCY; PREGNANT WOMAN; PRENATAL CARE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SENSITIVITY ANALYSIS; UMBILICAL ARTERY; UTERINE ARTERY;

ADOLESCENT; ADULT; ANTIGENS, CD; FEMALE; FETAL DEATH; GESTATIONAL AGE; HUMANS; LONGITUDINAL STUDIES; MIDDLE AGED; NEOVASCULARIZATION, PHYSIOLOGIC; PREGNANCY; PREGNANCY PROTEINS; RECEPTORS, CELL SURFACE; RETROSPECTIVE STUDIES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 78249244123     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767051003681121     Document Type: Article

References (116)

1. Romero R. The child is the father of the man. Prenat Neonat Med 1996;1:8-11.
2. Romero R. Prenatal medicine: the child is the father of the man. 1996. J Matern.Fetal Neonatal Med 2009;22:636-639.
3. Di Renzo GC. The great obstetrical syndromes. J Matern. Fetal Neonatal Med 2009;22:633-635.
4. Sarhanis P Pugh DH. Resolution of pre-eclampsia following intrauterine death of one twin. Br J Obstet Gynaecol 1992;99:159-160.
5. Heyborne KD, Porreco RP. Selective fetocide reverses preeclampsia in discordant twins. Am J Obstet Gynecol 2004;191:477-480.
6. Bschierl F, Beinder E. Temporary resolution ofpreeclamptic symptoms after intrauterine death of one twin. Hypertens Pregnancy 2005;24:313-317.
7. Audibert F, Saloman LJ, Frydman R. Selective fetocide reverses preeclampsia in discordant twins. Am J Obstet Gynecol 2005;193:894-895.
8. Fretts RC. Etiology and prevention ofstillbirth. Am J Obstet Gynecol 2005;193:1923-1935.
9. Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classi-fication ofstillbirth by relevant condition at death (ReCoDe): populationbased cohortstudy. BMJ 2005;331:1113-1117.
10. Korteweg, FJ, Gordijn, SJ, Timmer, A, Erwich, JJ, Bergman, KA, Bouman, K, Ravise, JM, Heringa, MP, Holm, JP. The Tulip classification of perinatal mortality: introduction and multidisciplinary inter-rater agreement. BJOG. 2006;113: 393-401.
11. Silver, RM. Fetal death. Obstet Gynecol 2007;109:153-167.
12. Reddy UM, Goldenberg R, Silver R, Smith GC, Pauli RM, Wapner RJ, Gardosi J, Pinar H, Grafe M, Kupferminc M, et al. Stillbirth classification-developing an international consensus for research: executive summary of a National Institute of Child Health and Human Development work-shop. Obstet Gynecol 2009;114:901-914.
13. Vergani P, Cozzolino S, Pozzi E, Cuttin MS, Greco M, Ornaghi S, Lucchini V. Identifying the causes of stillbirth: a comparison of four classification systems. Am J Obstet Gynecol 2008;199:319-314.
14. Flenady V, Froen JF, Pinar H, Torabi R, Saastad E, Guyon G, Russell L, Charles A, Harrison C, Chauke L, et al. An evaluation of classification systems for stillbirth. BMC Pregnancy Childbirth 2009;9:24.
15. Lu JR, McCowan L. A comparison of the Perinatal Society of Australia and New Zealand-Perinatal Death Classifica-tion system and relevant condition at death stillbirth classification systems. Aust N Z J Obstet Gynaecol 2009; 49:467-471.
16. Froen JF, Pinar H, Flenady V, Bahrin S, Charles A, Chauke L, Day K, Duke CW, Facchinetti F, Fretts RC, et al. Causes of death and associated conditions (Codac): a utilitarian approach to the classification of perinatal deaths. BMC Pregnancy Childbirth 2009;9:22.
17. Varli IH, Petersson K, Bottinga R, Bremme K, Hofsjo A, Holm M, Holste C, Kublickas M, Norman M, Pilo C, et al. The Stockholm classification of stillbirth. Acta Obstet Gynecol Scand 2008;87:1202-1212.
18. Korteweg FJ, Gordijn SJ, Timmer A, Holm JP, Ravise JM, Erwich JJ. A placental cause of intra-uterine fetal death depends on the perinatal mortality classification system used. Placenta 2008;29:71-80.
19. Goldenberg RL, Thompson C. The infectious origins of stillbirth. Am J Obstet Gynecol 2003;189:861-873.
20. Blackwell S, Romero R, Chaiworapongsa T, Kim YM, Bujold E, Espinoza J, Camacho N, Hassan S, Yoon BH, Refuerzo JS. Maternal and fetal inflammatory responses in unexplained fetal death. J Matern.Fetal Neonatal Med 2003; 14:151-157.
21. McClure EM, Goldenberg RL. Infection and stillbirth. Semin. Fetal Neonatal Med 2009;14:182-189.
22. Measey MA, Charles A, d'Espaignet ET, Harrison C, Deklerk N, Douglass C. Aetiology of stillbirth: unexplored is not unexplained. Aust N Z J Public Health 2007;31:444-449.
23. Froen JF, Gardosi JO, Thurmann A, Francis A, Stray-Pedersen B. Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet Gynecol Scand 2004;83: 801-807.
24. Pedersen NG, Figueras F, Wojdemann KR, Tabor A, Gardosi J. Early fetal size and growth as predictors ofadverse outcome. Obstet Gynecol 2008;112:765-771.
25. Gardosi J, Clausson B, Francis A. The value ofcustomised centiles in assessing perinatal mortality risk associated with parity and maternal size. BJOG 2009;116:1356-1363.
26. Smith SK, He Y, Clark DE, Charnock-Jones DS. Angio-genic growth factor expression in placenta. Semin Perinatol 2000;24:82-86.
27. Zygmunt M, Herr F, Munstedt K, Lang U, Liang OD. Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol 2003;110 (Suppl 1):S10-S18.
28. 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.
29. 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.
30. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly ofvascular endothelium. Nature 1995;376:66-70.
31. 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.
32. Tidwell SC, Ho HN, Chiu WH, Torry RJ, Torry DS. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001;184:1267-1272.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. Torry DS, Wang HS, Wang TH, Caudle MR, Torry RJ, Preeclampisa is associated with reduced serum levels of placental growth factor. Am J Obstet Gynecol 1998;179: 1539-1544.
40. McKeeman GC, Ardill JE, Caldwell CM, Hunter AJ, McClure N. Soluble vascular endothelial growth factor receptor-1 (sFlt-1) is increased throughout gestation in patients who have preeclampsia develop. Am J Obstet Gynecol 2004;191:1240-1246.
41. 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.
42. Bujold E, Romero R, Chaiworapongsa T, Kim YM, Kim GJ, Kim MR, Espinoza J, Goncalves LF, Edwin S, Mazor, M. Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin. J Matern Fetal Neonatal Med 2005; 18:9-16.
43. 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 pre-eclampsia. Am J Obstet Gynecol 2005;193:984-989.
44. Staff AC, Braekke K, Harsem NK, Lyberg T, Holthe MR Circulating concentrations ofsFlt1 (soluble fms-like tyrosine kinase 1) in fetal and maternal serum during pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 2005;122:33-39.
45. Nadar SK, Karalis I, Al Yemeni E, Blann AD, Lip GY. Plasma markers of angiogenesis in pregnancy included induced hypertension. Thromb Haemost 2005;94:1071-1076.
46. 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.
47. Masuyama H, Suwaki N, Nakatsukasa H, Masumoto A, Tateishi Y, Hiramatrsu Y. Circulating angiogenic factors in preeclampsia, gestational proteinuria, and preeclampsia superimposed on chronic glomerulonephritis. Am J Obstet Gynecol 2006;194:551-556.
48. 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.
49. Wathen KA, Tuutti E, Stenman UH, Alfthan H, Halmesmaki E, Finne P, Ylikorkala O, Vuorela P. Maternal serum-soluble vascular endothelial growth factor receptor-1 in earlypregnancy ending in preeclampsia or intrauterine growth retardation. J Clin Endocrinol Metab 2006;91:180-184.
50. Schlembach D, Wallner W, Sengenberger R, Stiegler E, Mortl M, Beckmann MW, Lang U. Angiogenic growth factor levels in maternal and fetal blood: correlation with Doppler ultrasound parameters in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. Ultra-sound Obstet Gynecol 2007;29:407-413.
51. Vatten LJ, Eskild A, Nilsen TI, Jeansson S, Jenum PA, Staff AC Changes in circulating level ofangiogenic factors from the first to second trimester as predictors of preeclampsia. Am J Obstet Gynecol 2007;196:239-246.
52. Espinoza J, Romero R, Nien JK, Gomez R, Kusanovic JP, Goncalves LF, Medina L, Edwin S, Hassan S, Carstens M, et al. Identification ofpatients at risk for early onset and/or severe preeclampsia with the use of uterine artery Doppler velocimetry and placental growth factor. Am J Obstet Gynecol 2007;196:326.e1-326.e13.
53. Ohkuchi A, Hirashima C, Matsubara S, Suzuki H, Takahashi K, Arai F, Watanabe T, Kario K, Suzuki M. Alterations in placental growth factor levels before and after the onset of preeclampsia are more pronounced in women with early onset severe preeclampsia. Hypertens Res 2007;30: 151-159.
54. 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.
55. 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-onsetpreeclampsia. Obstet Gynecol 2007;109:1368-1374.
56. Rana S, Karumanchi SA, Levine RJ, Venkatesha S, Rauh-Hain JA, Tamez H, Thadhani R. Sequential changes in antiangiogenic factors in early pregnancy and risk of developing preeclampsia. Hypertension 2007;50:137-142.
57. Smith GC, Crossley JA, Aitken DA, Jenkins N, Lyall F, Cameron AD, Connor JM, Dobbie R. Circulating angio-genic factors in early pregnancy and the risk of preeclampsia, intrauterine growth restriction, spontaneous preterm birth, and stillbirth. Obstet Gynecol 2007;109:1316-1324.
58. Salahuddin S, Lee Y, Vadnais M, Sachs BP, Karumanchi SA, Lim KH. Diagnostic utility of soluble fms-like tyrosine kinase 1 and soluble endoglin in hypertensive diseases of pregnancy. Am J Obstet Gynecol 2007;197:28-36.
59. 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.
60. Sibai BM, Koch MA, Freire S, Pinto e Silva JL, Rudge MV, Martins-Costa S, Bartz J, de Barros SC, Cecatti JG, Costa R, et al. Serum inhibin A and angiogenic factor levels in pre-gnancies with previous preeclampsia and/or chronic hyperten-sion: are they useful markers for prediction of subsequent preeclampsia? Am J Obstet Gynecol 2008;199: 268-269.
61. Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Edwin SS, Gomez R, et al. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identifica-tion of patients destined to develop preeclampsia. J Matern Fetal Neonatal Med 2009;22:1021-1038.
62. Shokry M, Bedaiwy MA, Fathalla MM, Alsemary A, Elwakil S, Murphy A. Maternal serum placental growth factor and soluble fms-like tyrosine kinase 1 as early predictors of preeclampsia. Acta Obstet Gynecol Scand 2010;89:143-146.
63. Staff AC, Braekke K, Johnsen GM, Karumanchi SA, Harsem NK. Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 2007;197:176.
64. Robinson CJ, Johnson DD. Soluble endoglin as a second-trimester marker for preeclampsia. Am J Obstet Gynecol 2007;197:174-175.
65. Stepan H, Geipel A, Schwarz F, Kramer T, Wessel N, Faber R. Circulatory soluble endoglin and its predictive value for preeclampsia in second-trimester pregnancies with ab-normal uterine perfusion. Am J Obstet Gynecol 2008;198: 175-176.
66. Savvidou MD, Yu CK, Harland LC, Hingorani AD, Nicolaides KH. Maternal serum concentration of soluble fms-like tyrosine kinase 1 and vascular endothelial growth factor in women with abnormal uterine artery Doppler and in those with fetal growth restriction. Am J Obstet Gynecol 2006;195:1668-1673.
67. Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 2006;195:201-207.
68. Stepan H, Kramer T, Faber R. Maternal plasma concentra-tions of soluble endoglin in pregnancies with intrauterine growth restriction. J Clin Endocrinol Metab 2007;92:2831-2834.
69. Wallner W, Sengenberger R, Strick R, Strissel PL, Meurer B, Beckmann MW, Schlembach D. Angiogenic growth factors in maternal and fetal serum in pregnancies compli-cated by intrauterine growth restriction. Clin Sci (Lond) 2007;112:51-57.
70. 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.
71. 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.
72. 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 syn-drome' (Ballantyne's syndrome). J Matern Fetal Neonatal Med 2006;19:607-613.
73. Stepan H, Faber R. Elevated sFlt1 level and preeclampsia with parvovirus-induced hydrops. N Engl J Med 2006;354: 1857-1858.
74. Stepan H, Faber R. Cytomegalovirus-induced mirror syn-drome associated with elevated levels of angiogenic factors. Obstet Gynecol 2007;109:1205-1206.
75. 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 antiangio-genic state? Am J Obstet Gynecol 2008;198:382-388.
76. Smulian JC, Ananth CV, Vintzileos AM, Scorza WE, Knuppel RA. Fetal deaths in the United States. Influence of high-risk conditions and implications for management. Obstet Gynecol 2002;100:1183-1189.
77. Gruenberger W, Gerstner GJ. The causes ofantepartum fetal death: a clinico-pathological study. Clin Exp Obstet Gynecol 1980;7:210-214.
78. Page EW, Christianson R. The impact of mean arterial pressure in the middle trimester upon the outcome of pregnancy. Am J Obstet Gynecol 1976;125: 740-746.
79. Ngoc NT, Merialdi M, bdel-Aleem H, Carroli G, Purwar M, Zavaleta N, Campodonico L, Ali MM, Hofmeyr GJ, Mathai M, et al. Causes of stillbirths and early neonatal deaths: data from 7993 pregnancies in six develop-ing countries. Bull World Health Organ 2006;84:699-705.
80. de Courcy-Wheeler RH, Wolfe CD, Warburton F, Good-man J, Reynolds F, Gamsu H. The association between small size for gestational age and perinatal and neonatal death in a UK Regional Health Authority. Paediatr Perinat Epidemiol 1995;9:431-440.
81. Cnattingius S, Haglund B, Kramer MS. Differences in late fetal death rates in association with determinants of small for gestational age fetuses: population based cohort study. BMJ 1998;316:1483-1487.
82. 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.
83. Hladunewich MA, Steinberg G, Karumanchi SA, Levine RJ, Keating S, Kingdom J, Keunen J. Angiogenic factor abnormalities and fetal demise in a twin pregnancy. Nat Rev Nephrol 2009;5:658-662.
84. 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.
85. Gonzalez RP, Gomez RM, Castro RS, Nien JK, Merino PO, Etchegaray AB, Carstens MR, Medina LH, Viviani PG, Rojas IT. A national birth weight distribution curve according to gestational age in chile from 1993 to 2000. Rev Med Chil 2004;132:1155-1165.
86. Gomez O, Figueras F, Fernandez S, Bennasar M, Martinez JM, Puerto B, Gratacos E. Reference ranges for uterine artery mean pulsatility index at 11-41 weeks ofgestation. Ultrasound Obstet Gynecol 2008;32:128-132.
87. Arduini D, Rizzo G. Normal values ofPulsatility Index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. JPerinat.Med 1990;18:165-172.
88. Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation-a workshop report. Placenta 2005;26 (Suppl A):S114-S117.
89. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, Ecker J, Karumanchi SA. First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 2004; 89:770-775.
90. Chaiworapongsa T, Romero R, Tarca A, Pedro KJ, Mittal P, Kwon KS, Gotsch F, Erez O, Vaisbuch E, Mazaki-Tovi S, et al. A subset of patients destined to develop spontaneous preterm labor has an abnormal angiogenic/anti-angiogenic profile in maternal plasma: evidence in support of patho-physiologic heterogeneity of preterm labor derived from a longitudinal study. J Matern Fetal Neonatal Med 2009;22: 1122-1139.
91. Hustin J, Schaaps JP. Echographic [corrected] and anatomic studies of the maternotrophoblastic border during the first trimester ofpregnancy. Am J Obstet Gynecol 1987;157:162-168.
92. Hamilton WJ, Boyd JD. Developmentofthehuman placenta in the first three months ofgestation. J Anat 1960;94:297-328.
93. Burton GJ, Jauniaux E, Watson AL. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: the Boyd collection revisited. Am J Obstet Gynecol 1999;181:718-724.
94. Jauniaux E, Jurkovic D, Campbell S. In vivo investigations of the anatomy and the physiology of early human pla-cental circulations. Ultrasound Obstet Gynecol 1991;1:435-445.
95. Jaffe R, Woods JR, Jr. Color Doppler imaging and in vivo assessment of the anatomy and physiology of the early uteroplacental circulation. Fertil Steril 1993;60:293-297.
96. Coppens M, Loquet P, Kollen M, De NF, Buytaert P. Longitudinal evaluation of uteroplacental and umbilical blood flow changes in normal early pregnancy. Ultrasound Obstet Gynecol 1996;7:114-121.
97. Carbillon L, Challier JC, Alouini S, Uzan M, Uzan S. Uteroplacental circulation development: Doppler assessment and clinical importance. Placenta 2001;22:795-799.
98. Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during earlypregnancy. Obstet Gynecol 1992;80:283-285.
99. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 2000;157:2111-2122.
100. Jauniaux E, Watson A, Ozturk O, Quick D, Burton G. In-vivo measurement ofintrauterine gases and acid-base values early in human pregnancy. Hum Reprod 1999;14:2901-2904.
101. Kliman HJ. Uteroplacental blood flow. The story of decidualization, menstruation, and trophoblast invasion. Am J Pathol 2000;157:1759-1768.
102. Graham CH, Postovit LM, Park H, Canning MT, Fitzpatrick TE. Adriana and Luisa Castellucci award lecture 1999: role of oxygen in the regulation of trophoblast gene expression and invasion. Placenta 2000;21:443-450.
103. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science 1997;277:1669-1672.
104. Jauniaux E, Gulbis B, Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the fetus-a review. Placenta 2003;24 (Suppl A):S86-S93.
105. Watson AL, Palmer ME, Jauniaux E, Burton GJ. Variations in expression of copper/zinc superoxide dismutase in villous trophoblast of the human placenta with gestational age. Placenta 1997;18:295-299.
106. Watson AL, Skepper JN, Jauniaux E, Burton GJ. Suscept-ibility of human placental syncytiotrophoblastic mitochon-dria to oxygen-mediated damage in relation to gestational age. J Clin Endocrinol Metab 1998;83:1697-1705.
107. Jauniaux E, Hempstock J, Greenwold N, Burton GJ. Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 2003;162:115-125.
108. Hempstock J, Jauniaux E, Greenwold N, Burton GJ. The contribution of placental oxidative stress to early pregnancy failure. Hum Pathol 2003;34:1265-1275.
109. Jauniaux E, Poston L, Burton GJ. Placental-related diseases of pregnancy: involvement ofoxidative stress and implications in human evolution. Hum Reprod Update 2006;12:747-755.
110. Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004;11:342-352.
111. Jauniaux E, Burton GJ. Pathophysiology of histological changes in early pregnancy loss. Placenta 2005;26:114-123.
112. Carter AM. Placental oxygen consumption. Part I: in vivo studies-a review. Placenta 2000;21 (Suppl A):S31-S37.
113. Muttukrishna S, Suri S, Groome N, Jauniaux E. Relation-ships between TGFbeta proteins and oxygen concentrations inside the first trimester human gestational sac. PLoS One 2008;3:e2302.
114. Ahmed A, Dunk C, Ahmad S, Khaliq A. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen-a review. Placenta 2000;21 (Suppl A):S16-S24.
115. Khaliq A, Dunk C, Jiang J, Shams M, Li XF, Acevedo C, Weich H, Whittle M, Ahmed A. Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for 'placental hyperoxia' in intrauterine growth restriction. Lab Invest 1999;79:151-170.
116. Korteweg FJ, Erwich JJ, Holm JP, Ravise JM, van der MJ, Veeger NJ, Timmer A. Diverse placental pathologies as the main causes offetal death. Obstet Gynecol 2009;114:809-817.