Classification of Villous Maldevelopment

  • Kurt Benirschke
  • Peter Kaufmann


The histopathology of villous maldevelopment is based on the light microscopy of paraffin sections. Thus, the normal and pathological features of the placenta are usually described in terms of the two dimensions apparent by light microscopy. These two-dimensional findings very often do not reflect the underlying three-dimensional malformation of villi, as becomes particularly obvious when considering the pathologically meaningful finding of “syncytial knotting” (Tenney—Parker changes).


Tangential Section Maternal Anemia Villous Tree Flat Section Terminal Villus 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alvarez, H., De Bejar, R. and Aladjem, S.: La placenta human Aspectos morfologicos y fisio-patologicos. In, 4th Uruguayan Congress for Obstetrics and Gynecology, Vol. 1, pp. 190–261, 1964.Google Scholar
  2. Alvarez, H., Morel, R.L., Benedetti, W.L. and Scavarelli, M.: Trophoblast hyperplasia and maternal arterial pressure at term. Am. J. Obstet. Gynecol. 105: 1015–1021, 1969.PubMedGoogle Scholar
  3. Alvarez, H., Benedetti, W.L., Morel, R.L. and Scavarelli, M.: Trophoblast development gradient and its relationship to placental hemodynamics. Am. J. Obstet. Gynecol. 106: 416–420, 1970.PubMedGoogle Scholar
  4. Amaladoss, A.S.P. and Burton, G.J.: Organ culture of human placental villi in hypoxic and hyperoxic conditions: a morphometric study. J. Dev. Physiol. (Oxf.) 7: 113–118, 1985.Google Scholar
  5. Bacon, B.J., Gilbert, R.D., Kaufmann, P., Smith A.D., Trevino, F.T. and Longo, L.D.: Placental anatomy and diffusing capacity in guinea pigs following long-term maternal hypoxia. Placenta 5: 475–488, 1984.PubMedCrossRefGoogle Scholar
  6. Becker, V.: Funktionelle Morphologie der Plazenta. Arch. Gynäkol. 198: 3–28, 1963.PubMedCrossRefGoogle Scholar
  7. Becker, V.: Pathologie der Ausreifung der Plazenta. In, Die Plazenta des Menschen. V. Becker, T.H. Schiebler and F. Kubli, eds., pp. 266–281. Thieme, Stuttgart, 1981.Google Scholar
  8. Becker, V. and Röckelein, G.: Pathologie der Plazenta und des Abortes. Springer, Heidelberg, 1989.Google Scholar
  9. Beischer, N.A., Sivasamboo, R., Vohra, S., Silpisornkosal, S. and Reid, S.: Placental hypertrophy in severe pregnancy anaemia. J. Obstet. Gynaecol. Br. Commonw. 77: 398–409, 1970.PubMedCrossRefGoogle Scholar
  10. Boyd, J.D. and Hamilton, W.J.: The Human Placenta. Heffer, Cambridge, 1970.Google Scholar
  11. Brosens, I.: The utero-placental vessels at term—the distribution and extent of physiological changes. Trophoblast Res. 3: 61–68, 1988.Google Scholar
  12. Brosens, I., Robertson, W.B. and Dixon, H.G.: The physiological response of the vessels of the placental bed to normal pregnancy. J. Pathol. Bacteriol. 93: 569–579, 1967.PubMedCrossRefGoogle Scholar
  13. Burton, G.J.: Intervillous connections in the mature human placenta: Instances of syncytial fusion or section artifacts? J. Anat. 145: 13–23, 1986a.PubMedGoogle Scholar
  14. Burton, G.J.: Scanning electron microscopy of intervillous connections in the mature human placenta. J. Anat. 147: 245–254, 1986b.PubMedGoogle Scholar
  15. Burton, G.J.:.The fine structure of the human placental villus as revealed by scanning electron microscopy. Scannings Microsc. 1: 1811–1828, 1987.Google Scholar
  16. Burton, G.J., Mayhew, T.M. and Robertson, L.A.: Stereological re-examination of the effects of varying oxygen tensions on human placental villi maintained in organ culture for up to 12 h. Placenta 10: 263–273, 1989.PubMedCrossRefGoogle Scholar
  17. Cantle, S.J., Kaufmann, P., Luckhardt, M. and Schweikhart, G.: Interpretation of syncytial sprouts and bridges in the human placenta. Placenta 8: 221–234, 1987.PubMedCrossRefGoogle Scholar
  18. Castellucci, M., Scheper, M., Scheffen, I., Celona, A. and Kaufmann, P.: The development of the human placental villous tree. Anat. Embryol. (Berl.) 181: 117–128, 1990.CrossRefGoogle Scholar
  19. Emmrich, P. and Mälzer, G.: Zur Morphologie der Plazenta bei Übertragung. Pathol. Microbiol. 32: 285–302, 1968.Google Scholar
  20. Emmrich, P., Gödel, E., Amendt, P. and Müller, G.: Schwangerschaft bei Diabetikerinnen mit diabetischer Angiolopathie. Klinische Ergebnisse in Korrelation zu morphologischen Befunden an der Plazenta. Zentralbi. Gynäkol. 97: 875–883, 1975.Google Scholar
  21. Essbach, H. and Röse, I.: Plazenta und Eihäute. Fischer, Jena, 1966.Google Scholar
  22. Fox, H.: Villous immaturity in the term placenta. Obstet. Gynecol. 31: 9–12, 1968.PubMedCrossRefGoogle Scholar
  23. Fox, H.: Effect of hypoxia on trophoblast in organ culture. Am. J. Obstet. Gynecol. 107: 1058–1064, 1970.PubMedGoogle Scholar
  24. Fox, H.: Pathology of the Placenta. 2nd Ed. Saunders, London, 1997.Google Scholar
  25. Geisen, C., Mottaghy, K., Scheffen, I. and Kaufmann, P.: Effect of long-term hypoxia on oxygen transport properties of blood in pregnant guinea pigs. In, Oxygen Transport to Tissue, Vol. XII. J. Piiper, T.K. Goldstick and D. Meyer, eds., pp. 767–777. Plenum Press, New York, 1990.Google Scholar
  26. Gödel, E. and Emmrich, P.: Morphologie der Plazenta und Qualität der metabolischen Kontrolle während der Schwangerschaft bei Diabetes mellitus. Zentralbl. Gynäkol. 98: 1307–1311, 1976.PubMedGoogle Scholar
  27. Greco, M.A., Kamat, B.R. and Demopolulos, R.I.: Placental protein distribution in maternal diabetes mellitus: an immunocytochemical study. Pediatr. Pathol. 9: 679–690, 1989.PubMedCrossRefGoogle Scholar
  28. Huppertz, B., Frank, H.G., Kingdom, J.C.P., Reister, F. and Kaufmann, P.: Villous cytotrophoblast regulation of the syncytial apoptotic cascade in the human placenta. Histochem. Cell Biol. 110: 495–508, 1998.PubMedCrossRefGoogle Scholar
  29. Jackson, M.R., Mayhew, T.M. and Haas, J.D.: Morphometric studies on villi in human term placentae and the effects of altitude, ethnic grouping and sex of newborn. Placenta 8: 487–495, 1987.PubMedCrossRefGoogle Scholar
  30. Jackson, M.R., Mayhew, T.M. and Haas, J.D.: 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 9: 1–8, 1988a.PubMedCrossRefGoogle Scholar
  31. Jackson, M.R., Mayhew, T.M. and Haas, J.D.: On the factors which contribute to thinning of the villous membrane in human placentae at high altitude. II. An increase in the degree of peripheralization of fetal capillaries. Placenta 9: 9–18, 1988b.PubMedCrossRefGoogle Scholar
  32. Jones, C.J.P. and Fox, H.: Syncytial knots and intervillous bridges in the human placenta: an ultrastructural study. J. Anat. 124: 275–286, 1977.PubMedGoogle Scholar
  33. Kadyrov, M., Kosanke, G., Kingdom, J. and Kaufmann, P.: Increased fetoplacental angiogenesis during first trimester in anaemic women. Lancet 352: 1747–1749, 1998.PubMedCrossRefGoogle Scholar
  34. Kaufmann, P.: Entwicklung der Plazenta. In, Die Plazenta des Menschen. V. Becker, T.H. Schiebler and F. Kubli, eds., pp. 13–50. Thieme, Stuttgart, 1981.Google Scholar
  35. Kaufmann, R, Luckhardt, M., Schweikhart, G. and Cantle, S.J.: Cross-sectional features and three-dimensional structure of human placental villi. Placenta 8: 235–247, 1987.PubMedCrossRefGoogle Scholar
  36. Kemnitz, P. and Theuring, E: Makroskopische, licht-und elektronenmikroskopische Plazentabefunde bei Übertragung. Zentralbi. Allg. Pathol. 118: 43–54, 1974.Google Scholar
  37. Kingdom, J.C.P. and Kaufmann, P.: Oxygen and placental villous development: origins of fetal hypoxia. Placenta 18: 613–621, 1997.PubMedCrossRefGoogle Scholar
  38. Kingdom, J.C.P., Macara, L.M., Krebs, C., Leiser, R. and Kaufmann, R: Pathological basis for abnormal umbilical artery Doppler waveforms in pregnancies complicated by intrauterine growth restriction. Trophoblast Res. 10: 291–309, 1997.Google Scholar
  39. Kloos, K. and Vogel, M.: Pathologie der Perinatalperiode. Grundlage, Methodik und erste Ergebnisse einer Kyematopathologie. Thieme, Stuttgart, 1974.Google Scholar
  40. Kosanke, G., Kadyrov, M., Korr, H. and Kaufmann, P.: Maternal anemia results in increased proliferation in human placental villi. Trophoblast Res. 11: 339–357, 1998.Google Scholar
  41. Krebs, C., Macara, L.M., Leiser, R., Bowman, A.W., Greer, I.A. and Kingdom, J.C.P.: 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: 1534–1542, 1996.PubMedCrossRefGoogle Scholar
  42. Krebs, C., Longo, L.D. and Leiser, R.: Term ovine placental vasculature: comparison of sea level and high altitude conditions by corrosion cast and histomorphometry. Placenta 18: 43–51, 1997.PubMedCrossRefGoogle Scholar
  43. Küstermann, W.: Über “Proliferationsknoten” und “Syncytialknoten” der menschlichen Placenta. Anat. Anz. 150: 144–157, 1981.PubMedGoogle Scholar
  44. Macara, L., Kingdom, J.C.P., Kaufmann, R, Kohnen, G., Hair, J., More, I.A.R., Lyall, E. and Greer, I.A.: Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta 17: 37–48, 1996.PubMedCrossRefGoogle Scholar
  45. Martin, B.J. and Spicer, S.S.: Ultrastructural features of cellular maturation and aging in human trophoblast. J. Ultrastruct. Res. 43: 133–149, 1973.PubMedCrossRefGoogle Scholar
  46. Mikolajczak, J., Ruhrberg, A., Fetzer, M., Kaufmann, P. and Goecke, C.: Irreguläre Zottenreifung bei Frühgeburtlichkeit und Übertragung, und ihre Darstellbarkeit im Ultraschall. Gynäkol. Rundsch. 27: 145–146, 1987.CrossRefGoogle Scholar
  47. Mohr, H.: Zur Histologie der übertragenen Plazenta. Zentralbi. Gynäkol. 72: 1530, 1950.Google Scholar
  48. Ong, P.J. and Burton, G J. Thinning of the placental villous membrane during maintenance in hypoxic organ culture: structural adaptation or syncytial degeneration? Eur. J. Obstet. Gynecol. Reprod. Biol. 39: 103–110, 1991.PubMedCrossRefGoogle Scholar
  49. Panigel, M. and Myers, R.E.: Histological and ultrastructural changes in rhesus monkey placenta following interruption of fetal placental circulation by fetectomy or interplacental umbilical vessel ligation. Acta Anat. (Basel) 81: 481–506, 1972.CrossRefGoogle Scholar
  50. Pilz, I., Schweikhart, G. and Kaufmann, R: Zur Abgrenzung normaler, artefizieller und pathologischer Struckturen in reifen menschlichen Plazentazotten. III. Morphometrische Untersuchungen bei Rh-Inkompatibilität. Arch. Gynecol. Obstet. 229: 137–154, 1980.Google Scholar
  51. Piotrowicz, B., Niebroj, T,K. and Sieron, G.: The morphology and histochemistry of the full term placenta in anaemic patients. Folia Histochem. Cytochem. (Krakow) 7: 435–444, 1969.Google Scholar
  52. Reshetnikova, O.S., Burton, G.J. and Milovanov, A.P.: The effects of hypobaric hypoxia on the terminal villi of the human placenta. J. Physiol. (Lond.) 459: 308P, 1993.Google Scholar
  53. Salvatore, C.A.: The placenta in acute toxemia. A comparative study. Am. J. Obstet. Gynecol. 102: 347–353, 1968.PubMedGoogle Scholar
  54. Scheffen, I., Kaufmann, P., Philippens, L., Leiser, R., Geisen, C. and Mottaghy, K.: Alterations of the fetal capillary bed in the guinea pig placenta following long-term hypoxia. In, Oxygen Transfer to Tissue, Vol. XII. J. Piiper, T.K. Goldstick and D. Meyer, eds., pp. 779–790. Plenum Press, New York, 1990.Google Scholar
  55. Schiebler, T.H. and Kaufmann, P.: Reife Plazenta. In, Die Plazenta des Menschen. V. Becker, T.H. Schiebler and E. Kubli, eds., pp. 51–111. Thieme, Stuttgart, 1981.Google Scholar
  56. Schuhmann, R. and Geier, G.: Histomorphologische Placentabefunde bei EPG-Gestose. Arch. Gynäkol. 213: 31–47, 1972.PubMedCrossRefGoogle Scholar
  57. Schweikhart, G.: Morphologie des Zottenbaumes der menschlichen Plazenta—Orthologische und pathologische Entwicklung und ihre klinische Relevanz. Thesis, Medical Faculty, University of Mainz, 1985.Google Scholar
  58. Schweikhart, G. and Kaufmann, P.: Histologie und Morphometrie der Plazenta bei intrauteriner Mangelentwicklung des Feten. Arch. Gynäkol. 235: 566–567, 1983.Google Scholar
  59. Schweikhart, G. and Kaufmann, P.: Endzottenmangel und klinische Relevanz. Gynäkol. Rundsch. 27 (suppl. 2): 147–148, 1987.CrossRefGoogle Scholar
  60. Schweikhart, G., Kaufmann, P. and Beck, T.: Morphology of placental villi after premature delivery and its clinical relevance. Arch. Gynecol. Obstet. 239: 101–114, 1986.Google Scholar
  61. Stoz, E, Schuhmann, R.A. and Schebesta, B.: The development of the placental villus during normal pregnancy: morphometric data base. Arch. Gynecol. Obstet. 244: 23–32, 1988.PubMedCrossRefGoogle Scholar
  62. Tenney, B. and Parker, E: The placenta in toxemia of pregnancy. Am. J. Obstet. Gynecol. 39: 1000–1005, 1940.Google Scholar
  63. Todros, T., Sciarrone, A., Piccoli, E., Guiot, C., Kaufmann, P. and Kingdom, J.: Umbilical Doppler waveforms and placental villous angiogenesis in pregnancies complicated by fetal growth restriction. Obstet. Gynecol. 93: 499–503, 1999.PubMedCrossRefGoogle Scholar
  64. Tominaga, T. and Page, E.W.: Accommodation of the human placenta to hypoxia. Am. J. Obstet. Gynecol. 94: 679–691, 1966.PubMedGoogle Scholar
  65. Vogel, M.: Pathologie der Schwangerschaft, der Plazenta und des Neugeborenen. In, Pathologie, Vol. 3. Remmele, W., ed. Springer-Verlag, Heidelberg, 1984.Google Scholar
  66. Vogel, M.: Histologische Entwicklungsstadien der Chorionzotten in der Embryonal-und der frühen Fetalperiode (5. bis 20. SSW). Pathologe 7: 59–61, 1986.PubMedGoogle Scholar
  67. Vogel, M.: Atlas der morphologischen Plazentadiagnostik. 2nd Ed. Springer, Berlin, 1996.CrossRefGoogle Scholar
  68. Wentworth, D.: The placenta in cases of hemolytic disease of the newborn. Am. J. Obstet. Gynecol. 98: 283–289, 1967.PubMedGoogle Scholar
  69. Werner, C. and Schneiderhan, W.: Plazentamorphologie und Plazentafunktion in Abhängigkeit von der diabetischen Stoffwechselführung. Geburtsh. Frauenheilkd. 32: 959–966, 1972.Google Scholar
  70. Werner, C., Göbel, U., Kramartz, N., Werners, P. and Haering, M.: Plazentareifungsstörungen und Schweregrad des Morbus haemolyticus neonatorum. Geburtsh. Frauenheilkd. 33: 776–785, 1973.Google Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Kurt Benirschke
    • 1
  • Peter Kaufmann
    • 2
  1. 1.University Medical CenterUniversity of California, San DiegoSan DiegoUSA
  2. 2.Institut für Anatomie der Medizinischen FakultätRheinisch-Westfälische Technische Hochschule AachenAachenGermany

Personalised recommendations