Development of the placental villous tree and its consequences for fetal growth

European Journal of Obstetrics and Gynecology and Reproductive Biology

Volumn 92, Issue 1, 2000, Pages 35-43

  Kingdom, John ^a   Huppertz, Berthold ^b   Seaward, Gareth ^a   Kaufmann, Peter ^b  

^a Maternal and Fetal Medicine Division   (Canada)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

ARED; Doppler; Fetal growth; IUGR; Maldevelopment; Placental development; Umbilical artery

Indexed keywords

ANGIOPOIETIN; ANGIOSTATIN; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; OXYGEN; PLACENTAL GROWTH FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; BLOOD OXYGEN TENSION; FETUS DEVELOPMENT; FETUS GROWTH; HUMAN; INTRAUTERINE GROWTH RETARDATION; NONHUMAN; PATHOGENESIS; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PLACENTA VILLUS; PRIORITY JOURNAL; REVIEW; TROPHOBLAST;

EID: 0033795787     PISSN: 03012115     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-2115(00)00423-1     Document Type: Article

References (89)

1. Kingdom J. Adriana and Luisa Castellucci Award Lecture 1997. Placental pathology in obstetrics: adaptation or failure of the villous tree? Placenta. 19:1998;347-351.
2. Cross J.C. Formation of the placenta and extraembryonic membranes. Ann. NY Acad. Sci. 857:1998;23-32.
3. Rodesch F., Simon P., Donner C., Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet. Gynecol. 80:1992;283-285.
4. Caniggia I., Grisaru-Gravnosky S., Kuliszewsky M., Post M., Lye S.J. Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J. Clin. Invest. 103:1999;1641-1650.
5. Lyall F., Bulmer J.N., Kelly H., Duffie E., Robson S.C. Human trophoblast invasion and spiral artery transformation: the role of nitric oxide. Am. J. Pathol. 154:1999;1105-1114.
6. Aplin J.D., Haigh T., Jones C.J., Church H.J., Vicovac L. Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin alpha5beta1. Biol. Reprod. 60:1999;828-838.
7. Jaffe R., Jauniaux E., Hustin J. Maternal circulation in the first-trimester human placenta - myth or reality? Am. J. Obstet. Gynecol. 176:1997;695-705.
8. Risau W. Mechanisms of angiogenesis. Nature. 386:1999;671-674.
9. Demir R., Kaufmann P., Castellucci M., Erbengi T., Kotowski A. Fetal vasculogenesis and angiogenesis in human placental villi. Acta Anat. (Basel). 136:1989;190-203.
10. Fisk N.M., MacLachlan N., Ellis C., Tannirandorn Y., Tonge H.M., Rodeck C.H. Absent end-diastolic flow in first trimester umbilical artery (letter). Lancet. 2:1988;1256-1257.
11. Hendricks S.K., Sorensen T.K., Wang K.Y., Bushnell J.M., Seguin E.M., Zingheim R.W. Doppler umbilical artery waveform indices - normal values from fourteen to forty-two weeks. Am. J. Obstet. Gynecol. 161:1989;761-765.
12. Adamson S.L. Arterial pressure, vascular input impedance, and resistance as determinants of pulsatile blood flow in the umbilical artery (in process citation). Eur. J. Obstet. Gynecol. Reprod. Biol. 84:1999;119-125.
13. Castellucci M., Scheper M., Scheffen I., Celona A., Kaufmann P. The development of the human placental villous tree. Anat. Embryol. (Berl.). 181:1990;117-128.
14. Kadyrov M., Kosanke G., Kingdom J., Kaufmann P. Increased fetoplacental angiogenesis during first trimester in anaemic women. Lancet. 352:1998;1747-1749.
15. Kaufmann P. Development and differentiation of the human placental villous tree. Bibl Anat 1982;29-39.
16. Kaufmann P., Bruns U., Leiser R., Luckhardt M., Winterhager E. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat. Embryol. (Berl.). 173:1985;203-214.
17. Benirschke P, Kaufmann P. Pathology of the human placenta. Berlin: Springer, 2000.
18. Kaufmann P, Kingdom J. Development of the vascular system in the placenta. In: Risau W, editor. Morphogenesis of endothelium. Berlin: Springer, 2000.
19. Luckhardt M, Leiser R, Kingdom J, et al. Effect of physiologic perfusion-fixation on the morphometrically evaluated dimensions of the term placental cotyledon. J Soc Gynecol Invest 1996;3:166-71.
20. Cheung C.Y. Vascular endothelial growth factor: possible role in fetal development and placental function. J. Soc. Gynecol. Invest. 4:1997;169-177.
21. Jackson M.R., Carney E.W., Lye S.J., Ritchie J.W. Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation. Placenta. 15:1994;341-353.
22. Clark D.E., Smith S.K., Licence D., Evans A.L., Charnock-Jones D.S. Comparison of expression patterns for placenta growth factor, vascular endothelial growth factor (VEGF), VEGF-B and VEGF-C in the human placenta throughout gestation. J. Endocrinol. 159:1998;459-467.
23. Evans P.W., Wheeler T., Anthony F.W., Osmond C. A longitudinal study of maternal serum vascular endothelial growth factor in early pregnancy. Hum. Reprod. 13:1998;1057-1062.
24. Cooper J.C., Sharkey A.M., Charnock-Jones D.S., Palmer C.R., Smith S.K. VEGF mRNA levels in placentae from pregnancies complicated by pre-eclampsia (see comments). Br. J. Obstet. Gynaecol. 103:1996;1191-1196.
25. Semenza GL, Agani F, Iyer N, et al. Regulation of cardiovascular development and physiology by hypoxia-inducible factor 1. Ann NY Acad Sci 1999;874:262-8.
26. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, Post M. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGF-beta(3). J. Clin Invest 2000;105:577-87.
27. Breier G. Angiogenesis in embryonic development. Placenta 2000;21(suppl A):511-5.
28. Kurz H., Wilting J., Sandau K., Christ B. Automated evaluation of angiogenic effects mediated by VEGF and PlGF homo- and heterodimers. Microvasc. Res. 55:1998;92-102.
29. Ziche M, Maglione D, Ribatti D, et al. Placenta growth factor-1 is chemotactic, mitogenic, and angiogenic. Lab Invest 1997;76:517-31.
30. Khaliq A, Li XF, Shams M, et al. Localisation of placenta growth factor (PIGF) in human term placenta. Growth Factors 1996;13:243-50.
31. Crescimanno C, Marzioni D, Persico MG, Vuckovic M, Mulhauser J, Castellucci M. Expression of bFGF, PlGF and their receptors in the human placenta. Placenta 2000;16 (Abstract).
32. Maglione D., Guerriero V., Viglietto G., Delli-Bovi P., Persico M.G. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc. Natl. Acad. Sci. U. S. A. 88:1991;9267-9271.
33. Khaliq A, Dunk C, Jiang J, et al. 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;79:151-70.
34. Cao Y, Chen H, Zhou L, et al. Heterodimers of placenta growth factor/vascular endothelial growth factor. Endothelial activity, tumor cell expression, and high affinity binding to Flk-1/KDR. J Biol Chem 1996;271:3154-62.
35. Kim I, Kwak HJ, Ahn JE, et al. Molecular cloning and characterization of a novel angiopoietin family protein, angiopoietin-3. FEBS Lett 1999;443:353-6.
36. Lucas R, Holmgren L, Garcia I, et al. Multiple forms of angiostatin induce apoptosis in endothelial cells. Blood 1998;92:4730-41.
37. Kingdom JCP, Smith GN. Diagnosis and management of IUGR. In: Kingdom JCP, Baker PN, editors. Intrauterine growth restriction. London: Springer, 2000. p. 251-68.
38. Sandstedt B. The placenta and low birth weight. Curr. Top. Pathol. 66:1979;1-55.
39. FitzGerald D.E., Drumm J.E. Non-invasive measurement of human fetal circulation using ultrasound: a new method. Br. Med. J. 2:1977;1450-1451.
40. Trudinger B.J., Cook C.M., Giles W.B., Connelly A., Thompson R.S. Umbilical artery flow velocity waveforms in high-risk pregnancy. Randomised controlled trial. Lancet. 1:1987;188-190.
41. Reilly R.D., Russell P.T. Neurohistochemical evidence supporting an absence of adrenergic and cholinergic innervation in the human placenta and umbilical cord. Anat. Rec. 188:1977;277-286.
42. Myatt L., Rosenfield R.B., Eis A.L., Brockman D.E., Greer I., Lyall F. Nitrotyrosine residues in placenta. Evidence of peroxynitrite formation and action. Hypertension. 28:1996;488-493.
43. Chappell LC, Seed PT, Briley AL, et al. Effect of antioxidants on the occurrence of pre-eclampsia in women at increased risk: a randomised trial (in process citation). Lancet 1999;354:810-6.
44. Burke C.J., Tannenberg A.E. Prenatal brain damage and placental infarction - an autopsy study. Dev. Med. Child Neurol. 37:1995;555-562.
45. Burke C.J., Tannenberg A.E., Payton D.J. Ischaemic cerebral injury, intrauterine growth retardation and placental infarction. Dev. Med. Child Neurol. 39:1997;726-730.
46. Jackson M.R., Walsh A.J., Morrow R.J., Mullen J.B., Lye S.J., Ritchie J.W. Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms. Am. J. Obstet. Gynecol. 172:1995;518-525.
47. Hitschold T.P. Doppler flow velocity waveforms of the umbilical arteries correlate with intravillous blood volume. Am. J. Obstet. Gynecol. 179:1998;540-543.
48. Trudinger B, Beutler L, Wang J, Placental vascular disease causes a fetal acute inflammatory cytokine and chemokine response. J Soc Gynecol Invest 2000;6:185A (Abstract).
49. von Dadelszen P., Ornstein M.P., Bull S.B., Logan A.G., Koren G., Magee L.A. Fall in mean arterial pressure and fetal growth restriction in pregnancy hypertension. Lancet. 355:2000;87-92.
50. Kingdom J.C., Burrell S.J., Kaufmann P. Pathology and clinical implications of abnormal umbilical artery Doppler waveforms. Ultrasound Obstet. Gynecol. 9:1997;271-286.
51. Trudinger B.J., Giles W.B., Cook C.M., Bombardieri J., Collins L. Fetal umbilical artery flow velocity waveforms and placental resistance: clinical significance. Br. J. Obstet. Gynaecol. 92:1985;23-30.
52. Bracero L.A., Beneck D., Kirshenbaum N., Peiffer M., Stalter P., Schulman H. Doppler velocimetry and placental disease. Am. J. Obstet. Gynecol. 161:1989;388-393.
53. McCowan L.M., Mullen B.M., Ritchie K. Umbilical artery flow velocity waveforms and the placental vascular bed. Am. J. Obstet. Gynecol. 157:1987;900-902.
54. Macara L., Kingdom J.C., Kohnen G., Bowman A.W., Greer I.A., Kaufmann P. Elaboration of stem villous vessels in growth restricted pregnancies with abnormal umbilical artery Doppler waveforms (see comments). Br. J. Obstet. Gynaecol. 102:1995;807-812.
55. Templeton A.G., McGrath J.C., Whittle M.J. The role of endogenous thromboxane in contractions to U46619, oxygen, 5-HT and 5-CT in the human isolated umbilical artery. Br. J. Pharmacol. 103:1991;1079-1084.
56. Kinmond S., Aitchison T.C., Holland B.M., Jones J.G., Turner T.L., Wardrop C.A. Umbilical cord clamping and preterm infants a randomised trial. BMJ. 306:1993;172-175.
57. Las H.J., Baskerville J.C., Harding P.G., Haust M.D. Morphometric studies of fetal placental stem arteries in hypertensive disorders ('toxaemia') of pregnancy. Placenta. 6:1985;217-227.
58. Fok R.Y., Pavlova Z., Benirschke K., Paul R.H., Platt L.D. The correlation of arterial lesions with umbilical artery Doppler velocimetry in the placentas of small-for-dates pregnancies. Obstet. Gynecol. 75:1990;578-583.
59. Salafia C.M., Pezzullo J.C., Minior V.K., Divon M.Y. Placental pathology of absent and reversed end-diastolic flow in growth-restricted fetuses. Obstet. Gynecol. 90:1997;830-836.
60. Trudinger BJ, Stevens D, Connelly A, et al. Umbilical artery flow velocity waveforms and placental resistance: the effects of embolization of the umbilical circulation. Am J Obstet Gynecol 1987;157:1443-8.
61. Adamson S.L., Morrow R.J., Bascom P.A., Mo L.Y., Ritchie J.W. Effect of placental resistance, arterial diameter, and blood pressure on the uterine arterial velocity waveform: a computer modeling approach. Ultrasound Med. Biol. 15:1989;437-442.
62. Khong T.Y., De Wolf F., Robertson W.B., Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br. J. Obstet. Gynaecol. 93:1986;1049-1059.
63. Nylund L., Lunell N.O., Lewander R., Sarby B. Uteroplacental blood flow index in intrauterine growth retardation of fetal or maternal origin. Br. J. Obstet. Gynaecol. 90:1983;16-20.
64. Bower S., Bewley S., Campbell S. Improved prediction of preeclampsia by two-stage screening of uterine arteries using the early diastolic notch and color Doppler imaging. Obstet. Gynecol. 82:1993;78-83.
65. Chappell L., Bewley S. Pre-eclamptic toxaemia: the role of uterine artery Doppler. Br. J. Obstet. Gynaecol. 105:1998;379-382.
66. Valensise H. Uterine artery Doppler velocimetry as a screening test: where we are and where we go? Ultrasound Obstet. Gynecol. 12:1998;83.
67. Ochi H., Matsubara K., Kusanagi Y., Taniguchi H., Ito M. Significance of a diastolic notch in the uterine artery flow velocity waveform induced by uterine embolisation in the pregnant ewe. Br. J. Obstet. Gynaecol. 105:1998;1118-1121.
68. Francis S.T., Duncan K.R., Moore R.J., Baker P.N., Johnson I.R., Gowland P.A. Non-invasive mapping of placental perfusion. Lancet. 351:1998;1397-1399.
69. Molina R.D., Meschia G., Wilkening R.B. Uterine blood flow, oxygen and glucose uptakes at mid-gestation in the sheep. Proc. Soc. Exp. Biol. Med. 195:1990;379-385.
70. Kingdom J.C., Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta. 18:1997;613-621.
71. Fox H. Effect of hypoxia on trophoblast in organ culture. A morphologic and autoradiographic study. Am. J. Obstet. Gynecol. 107:1970;1058-1064.
72. Scheffen I., Kaufmann P., Philippens L., Leiser R., Geisen C., Mottaghy K. Alterations of the fetal capillary bed in the guinea pig placenta following long-term hypoxia. Adv. Exp. Med. Biol. 277:1990;779-790.
73. Jackson M.R., Mayhew T.M., Haas J.D., Thinning I. Regional variation in thickness of trophoblast. Placenta. 9:1988;1-8.
74. Burton G.J., Reshetnikova O.S., Milovanov A.P., Teleshova O.V. Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress. Placenta. 17:1996;49-55.
75. Pfarrer C., Macara L., Leiser R., Kingdom J. Adaptive angiogenesis in placentas of heavy smokers. Lancet. 354:1999;303.
76. Proud J., Grant A.M. Third trimester placental grading by ultrasonography as a test of fetal wellbeing. Br. Med. J. 294:1987;1641-1644.
77. Burton G.J., Jauniaux E. Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity. Br. J. Obstet. Gynaecol. 102:1995;818-825.
78. Hershkovitz R, Kingdom JCP, Geary M, Rodeck CH. Fetal cerebral blood flow redistribution in late gestation: identification of compromise in small fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 2000;15:209-12.
79. Huppertz B., Frank H.G., Kingdom J.C., Reister F., Kaufmann P. Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem. Cell Biol. 110:1998;495-508.
80. Huppertz B., Frank H.G., Reister F., Kingdom J., Korr H., Kaufmann P. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab. Invest. 79:1999;1687-1702.
81. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 2000;25;311-4.
82. Mayhew T.M., Leach L., McGee R., Ismail W.W., Myklebust R., Lammiman M.J. Proliferation, differentiation and apoptosis in villous trophoblast at 13-41 weeks of gestation (including observations on annulate lamellae and nuclear pore complexes). Placenta. 20:1999;407-422.
83. Krebs C., Macara L.M., Leiser R., Bowman A.W., Greer I.A., Kingdom J.C. Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree. Am. J. Obstet. Gynecol. 175:1996;1534-1542.
84. Pardi G, Cetin I, Marconi AM, et al. Venous drainage of the human uterus: respiratory gas studies in normal and fetal growth-retarded pregnancies. Am J Obstet Gynecol 1992;166:699-706.
85. Ahmed A., Kilby M.D. Hypoxia or hyperoxia in placental insufficiency? Lancet. 350:1997;826-827.
86. Cacciatore B., Halmesmaki E., Kaaja R., Teramo K., Ylikorkala O. Effects of transdermal nitroglycerin on impedance to flow in the uterine, umbilical, and fetal middle cerebral arteries in pregnancies complicated by preeclampsia and intrauterine growth retardation. Am. J. Obstet. Gynecol. 179:1998;140-145.
87. Nakatsuka M, Tada K, Kimura Y, et al. Clinical experience of long-term transdermal treatment with nitric oxide donor for women with preeclampsia. Gynecol Obstet Invest 1999;47:13-9.
88. Poston L. Nitrovasodilators - will they be useful in lowering uterine artery resistance in pre-eclampsia and intrauterine growth restriction? Ultrasound Obstet. Gynecol. 11:1998;92-93.
89. 2 therapy and bedrest on fetuses with absent end-diastolic flow on umbilical artery Doppler waveform analysis. Br. J. Obstet. Gynaecol. 102:1995;662-665.