Advertisement

Villous Development and the Pathogenesis of IUGR

  • Gaby Kohnen
  • John Kingdom

Abstract

Successful human pregnancy depends upon a coordinated series of events in developmental biology - not only of the embryo, but also of the placenta. The initial events in placentation involve the formation of a spheroidal trophoblastic shell that functions as a barrier to the diffusion of oxygen during embryogenesis until the end of the first trimester (see Chs 6,12 and [1]). By contrast the embryonic placental circulation perfuses the placental villi from 7 postmenstrual weeks of gestation. Diffusion of oxygen to the embryo appears less important in these circumstances, which is in marked contrast to the situation in the third trimester when adequate oxygen transfer to the fetus depends on well-developed uteroplacental and fetoplacental vascular beds. This chapter describes the development of placental villi during normal pregnancy, leading to a discussion of the evidence supporting the concept of villous maldevelopment in IUGR. For more detailed discussion of this topic the reader is referred to one of the following specialised texts [2–4].

Keywords

Umbilical Artery Intrauterine Growth Restriction Placental Villus Villous Tree Intervillous Space 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Jaffe R, Jauniaux E, Hustin J. Maternal circulation in the first-trimester human placenta - myth or reality? Am J Obstet Gynecol 1997;176:695–705.PubMedCrossRefGoogle Scholar
  2. 2.
    Boyd JD, Hamilton WJ. The human placenta. Cambridge: W Heffer, 1970.Google Scholar
  3. 3.
    Benirschke K, Kaufmann P. The pathology of the human placenta, 3rd edn. New York, Berlin, Heidelberg: Springer-Verlag, 1995.Google Scholar
  4. 4.
    Fox H. Pathology of the placenta, 2nd edn. London: WB Saunders, 1997.Google Scholar
  5. 5.
    Luckett WP. Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am J Anat 1978;152:59–97.PubMedCrossRefGoogle Scholar
  6. 6.
    King BF. Ultrastructural differentiation of stromal and vascular components in early macaque placental villi. Am J Anat 1987;178:30–44.PubMedCrossRefGoogle Scholar
  7. 7.
    Demir R, Kaufmann P, Castellucci M, Erbengi T, Kotowski A. Fetal vasculogenesis and angiogenesis inhuman placental villi. Acta Anat (Basel) 1989;136:190–203.CrossRefGoogle Scholar
  8. 8.
    Fisk NM, MacLachlan N, Ellis C, Tannirandorn Y, Tonge HM, Rodeck CH. Absent end-diastolic flow in first trimester umbilical artery. Lancet 1988;2:1256–7.PubMedCrossRefGoogle Scholar
  9. 9.
    Castellucci M, Scheper M, Scheffen I, Celona A, Kaufmann P. The development of the human placental villous tree. Anat Embryol 1990; 181:117–28.PubMedCrossRefGoogle Scholar
  10. 10.
    Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992;80:283–5.PubMedGoogle Scholar
  11. 11.
    Jackson MR, Mayhew TM, Boyd PA. Quantitative description of the elaboration and maturation of villi from 10 weeks of gestation to term. Placenta 1992;13:357–70.PubMedCrossRefGoogle Scholar
  12. 12.
    Luckhardt M, Leiser R, Kingdom J, Malek A, Sager R, Kaisig C, 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.CrossRefGoogle Scholar
  13. 13.
    Kadyrov M, Kosanke G, Kingdom JCP, Kaufmann P. Increased fetoplacental angiogenesis during first trimester in anaemic women. Lancet 1998;52:1747–9.CrossRefGoogle Scholar
  14. 14.
    Jackson MR, Walsh AJ, Morrow RJ, Mullen JB, Lye SJ, Ritchie JW. Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms. Am J Obstet Gynecol 1995;172:518–25.PubMedCrossRefGoogle Scholar
  15. 15.
    Todros T, Sciarrone A, Piccoli E, Guiot C, Kaufmann P, Kingdom J. Umbilical Doppler waveforms and placental villous angiogenesis in pregnancies complicated by fetal growth restriction. Obstet Gynecol 1999; 93:499–503.PubMedCrossRefGoogle Scholar
  16. 16.
    Kohnen G, Castellucci M, Hsi BL, Yeh CJ, Kaufmann P. The monoclonal antibody GB 42 - a useful marker for the differentiation of myofibroblasts. Cell Tissue Res 1995;281:231–42.PubMedCrossRefGoogle Scholar
  17. 17.
    Kohnen G, Kertschanska S, Demir R, Kaufmann P. Placental villous stroma as a model system for myofibroblast differentiation. Histochem Cell Biol 1996;105:415–29.PubMedCrossRefGoogle Scholar
  18. 18.
    Leiser R, Luckhardt M, Kaufmann P, Winterhager E, Bruns U. The fetal vascularisation of term human placental villi. I. Peripheral stem villi. Anat Embryol 1985;173:71–80.Google Scholar
  19. 19.
    Kingdom JC, Burreil SJ, Kaufmann P. Pathology and clinical implications of abnormal umbilical artery Doppler waveforms. Ultrasound Obstet Gynecol 1997;9:271–86.PubMedCrossRefGoogle Scholar
  20. 20.
    Graf R, Langer JU, Schonfelder G, Oeney T, Hartel-Schenk S, Reutter W, et al. The extravascular contractile system in the human placenta. Morphological and immunocytochemical investigations. Anat Embryol 1994;190:541–8.Google Scholar
  21. 21.
    Graf R, Schoenfelder G, Muhlberger M, Gutsmann M. The perivascular contractile sheath of human placental stem villi: its isolation and characterization. Placenta 1995;16:57–66.PubMedCrossRefGoogle Scholar
  22. 22.
    Kingdom JCP, Poston L. Stem villous arteries as regulators of fetal placental blood flow. Troph Res 1998;12:403–8.Google Scholar
  23. 23.
    Krantz KE, Parker JC. Contractile properties of the smooth muscle in the human placenta. Clin Obstet Gynecol 1963;6:26–38.CrossRefGoogle Scholar
  24. 24.
    Castellucci M, Kaufmann P. A three-dimensional study of the normal human placental villous core: II. Stromal architecture. Placenta 1982;3:269–85.CrossRefGoogle Scholar
  25. 25.
    Graf R, Neudeck H, Gossrau R, Vetter K. Elastic fibres are an essential component of human placental stem villous stroma and an integrated part of the perivascular contractile sheath. Cell Tissue Res 1996;283:133–41.PubMedCrossRefGoogle Scholar
  26. 26.
    Demir R, Kosanke G, Kohnen G, Kertschanska S, Kaufmann P. Classification of human placental stem villi: review of structural and functional aspects. Microsc Res Tech 1997; 38:29–41.PubMedCrossRefGoogle Scholar
  27. 27.
    Kingdom JC, Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta 1997;18:613–21.PubMedCrossRefGoogle Scholar
  28. 28.
    Ahmed A, Kilby MD. Hypoxia or hyperoxia in placental insufficiency? Lancet 1997;350:826–7.PubMedCrossRefGoogle Scholar
  29. 29.
    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 1985;173:203–14.Google Scholar
  30. 30.
    Sandstedt B. The placenta and low birth weight. Curr Top Pathol 1979;66:1–55.PubMedCrossRefGoogle Scholar
  31. 31.
    FitzGerald DE, Stuart B, Drumm JE, Duignan NM. The assessment of the feto-placental circulation with continuous wave Doppler ultrasound. Ultrasound Med Biol 1984;10:371–6.PubMedCrossRefGoogle Scholar
  32. 32.
    Trudinger BJ, Stevens D, Connelly A, Hales JR, Alexander G, Bradley L, 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.PubMedGoogle Scholar
  33. 33.
    Adamson SL, Morrow RJ, Langille BL, Bull SB, Ritchie JW. Site-dependent effects of increases in placental vascular resistance on the umbilical arterial velocity waveform in fetal sheep. Ultrasound Med Biol 1990;16:19–27.PubMedCrossRefGoogle Scholar
  34. 34.
    De Catte L, Burrini D, Mares C, Waterschoot T. Single umbilical artery: analysis of Doppler flow indices and arterial diameters in normal and small-for-gestational age fetuses [see comments]. Ultrasound Obstet Gynecol 1996;8:27–30.PubMedCrossRefGoogle Scholar
  35. 35.
    Dolkart LA, Reimers FT, Kuonen CA. Discordant umbilical arteries: ultrasonographic and Doppler analysis. Obstet Gynecol 1992;79:59–63.PubMedGoogle Scholar
  36. 36.
    Raio L, Ghezzi F, Di Naro E, Gomez R, Saile G, Bruhwiler H. The clinical significance of antenatal detection of discordant umbilical arteries. Obstet Gynecol 1998;91:86–91.PubMedCrossRefGoogle Scholar
  37. 37.
    Bruch JF, Sibony O, Benali K, Challier JC, Blot P, Nessmann C. Computerized microscope morphometry of umbilical vessels from pregnancies with intrauterine growth retardation and abnormal umbilical artery Doppler. Hum Pathol 1997;28:1139–45.PubMedCrossRefGoogle Scholar
  38. 38.
    Templeton AG, Kingdom JC, Whittle MJ, McGrath JC. Contractile responses of the human umbilical artery from pregnancies complicated by intrauterine growth retardation. Placenta 1993;14:563–70.PubMedCrossRefGoogle Scholar
  39. 39.
    Adamson SL, Whiteley KJ, Langille BL. Pulsatile pressure-flow relations and pulse-wave propagation in the umbilical circulation of fetal sheep. Circ Res 1992;70:761–72.PubMedGoogle Scholar
  40. 40.
    Rizzo G, Capponi A, Talone PE, Arduini D, Romanini C. Doppler indices from inferior vena cava and ductus venosus in predicting pH and oxygen tension in umbilical blood at cordocentesis in growth-retarded fetuses. Ultrasound Obstet Gynecol 1996;7:401–10.PubMedCrossRefGoogle Scholar
  41. 41.
    Sexton AJ, Loesch A, Turmaine M, Miah S, Burnstock G. Electron-microscopic immunolabelling of vasoactive substances in human umbilical endothelial cells and their actions in early and late pregnancy. Cell Tissue Res 1996;284:167–75.PubMedCrossRefGoogle Scholar
  42. 42.
    Giles WB, Trudinger BJ, Baird PJ. Fetal umbilical artery flow velocity waveforms and placental resistance: pathological correlation. Br J Obstet Gynaecol 1985;92:31–8.PubMedCrossRefGoogle Scholar
  43. 43.
    Bracero LA, Beneck D, Kirshenbaum N, Peiffer M, Stalter P, Schulman H. Doppler velocimetry and placental disease. Am J Obstet Gynecol 1989;161:388–93.PubMedGoogle Scholar
  44. 44.
    McCowan LM, Mullen BM, Ritchie K. Umbilical artery flow velocity waveforms and the placental vascular bed. Am J Obstet Gynecol 1987;157:900–2.PubMedGoogle Scholar
  45. 45.
    Jauniaux ER, Burton GJ. Correlation of umbilical Doppler features and placental morphometry: the need for uniform methodology. Ultrasound Obstet Gynecol 1993:3;233–5.PubMedCrossRefGoogle Scholar
  46. 46.
    Mayhew TM, Burton GJ. Stereology and its impact on our understanding of human placental functional morphology. Microsc Res Tech 1997;38:195–205.PubMedCrossRefGoogle Scholar
  47. 47.
    Macara L, Kingdom JC, Kohnen G, Bowman AW, Greer IA, Kaufmann P. Elaboration of stem villous vessels in growth restricted pregnancies with abnormal umbilical artery Doppler waveforms. Br J Obstet Gynaecol 1995;102:807–12.PubMedCrossRefGoogle Scholar
  48. Bouw GM, Stolte LAM, Baak JPA, Oort J. Quantitative morphology of the placenta. 1. Standardization of sampling. Eur J Obstet Gynecol Reprod Biol 1976;6:325–31. Google Scholar
  49. 49.
    Templeton AG, McGrath JC, Whittle MJ. The role of endogenous thromboxane in contractions to U46619, oxygen, 5- HT and 5-CT in the human isolated umbilical artery. Br J Pharmacol 1991;103:1079–84.PubMedGoogle Scholar
  50. Las Heras J, Haust MD. Ultrastructure of fetal stem arteries of human placenta in normal pregnancy. Virchows Arch A, 1981;393:133–44. Google Scholar
  51. 51.
    Fok RY, Pavlova Z, Benirschke K, Paul RH, Platt LD. The correlation of arterial lesions with umbilical artery Doppler velocimetry in the placentas of small-for-dates pregnancies. Obstet Gynecol 1990;75:578–3.PubMedGoogle Scholar
  52. S alafia CM, Pezzullo JC, Minior VK, Divon MY. Placental pathology of absent and reversed end-diastolic flow in growth-restricted fetuses. Obstet Gynecol 1997;90:830–6. Google Scholar
  53. 53.
    Morrow RJ, Adamson SL, Bull SB, Ritchie JW. Effect of placental embolization on the umbilical arterial velocity waveform in fetal sheep. Am J Obstet Gynecol 1989;161:1055–60.PubMedGoogle Scholar
  54. 54.
    Nicolaides KH, Bilardo CM, Soothill PW, Campbell S. Absence of end diastolic frequencies in umbilical artery: a sign of fetal hypoxia and acidosis. BMJ 1988;297:1026–7.PubMedCrossRefGoogle Scholar
  55. 55.
    Nicolini U, Nicolaidis P, Fisk NM, Vaughan JI, Fusi L, Gleeson R, et al. Limited role of fetal blood sampling in prediction of outcome in intrauterine growth retardation. Lancet 1990;336:768–72.PubMedCrossRefGoogle Scholar
  56. 56.
    Hitschold TP. Doppler flow velocity waveforms of the umbilical arteries correlate with intra- villous blood volume. Am J Obstet Gynecol 1998;179:540–3.PubMedCrossRefGoogle Scholar
  57. 57.
    Krebs C, Macara LM, Leiser R, Bowman AW, Greer IA, Kingdom JC. 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 1996;175:1534–42.PubMedCrossRefGoogle Scholar
  58. 58.
    Macara L, Kingdom JC, Kaufmann P, Kohnen G, Hair J, More IA, et al. Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta 1996;17:37–48.PubMedCrossRefGoogle Scholar
  59. 59.
    Lyall F, Young A, Boswell F, Kingdom JC, Greer IA. Placental expression of vascular endothelial growth factor in placentae from pregnancies complicated by pre-eclampsia and intrauterine growth restriction does not support placental hypoxia at delivery. Placenta 1997;18:269–76.PubMedCrossRefGoogle Scholar
  60. 60.
    Pardi G, Cetin I, Marconi AM, Bozzetti P, Buscagli M, Makowski EL 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.PubMedGoogle Scholar
  61. 61.
    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 1993;82:78–83.PubMedGoogle Scholar
  62. 62.
    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 1998; 105:1118–21.PubMedCrossRefGoogle Scholar
  63. Jackson MR, Mayhew TM, Haas JD. On the factors which contribute to thinning of the villous membrane in human placentae at high altitude. I. Thinning and regional variation in thickness of trophoblast. Placenta 1988;9:1–8. Google Scholar
  64. Kingdom J. Adriana and Luisa Castellucci Award Lecture 1997. Placental pathology in obstetrics: adaptation or failure of the villous tree? Placenta 1998;19:347–51. Google Scholar
  65. Geary M, Kingdom J, Persaud M, Wilshin J, Hindmarsh P, Rodeck C. Incidence of uterine notching in the third trimester and association with obstetric outcome. J Obstet Gynaecol 1998;18 Suppl 1:S58. Google Scholar
  66. 66.
    Fox H. The villous cytotrophoblast as an index of placental ischaemia. J Obstet Gynaecol Br Commonwlth 1964;71:885–93.CrossRefGoogle Scholar
  67. 67.
    Fox H. Effect of hypoxia on trophoblast in organ culture. A morphologic and autoradiographic study. Am J Obstet Gynecol 1970;107:1058–64.Google Scholar
  68. 68.
    Olofsson P, Saldeen P, Marsal K. Association between a low umbilical artery pulsatility index and fetal distress in very prolonged pregnancies. Eur J Obstet Gynecol Reprod Biol 1997;73:23–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Hitschold T, Muentefering H, Ulrich S, Berle P. Does extremely low fetoplacental impedance as estimated by umbilical artery Doppler velocimetry also indicate fetuses at risk? Ultrasound Obstet Gynecol 1996;8:S39.Google Scholar

Copyright information

© Springer-Verlag London Limited 2000

Authors and Affiliations

  • Gaby Kohnen
  • John Kingdom

There are no affiliations available

Personalised recommendations