Skip to main content
SpringerLink
Log in

Extrauterine Implantation and Involution of Implantation Site

  • Chapter
  • First Online:
Benirschke's Pathology of the Human Placenta

  • 1465 Accesses

Abstract

The blastocyst normally implants within the uterine cavity. An ectopic pregnancy refers to the implantation of an embryo outside of the uterus. Implantation at any of these ectopic sites is effectively part of the placenta accreta spectrum. Following cessation of pregnancy, morphological changes in the placental site that played a physiologic role in supporting development of the fetus and placenta during pregnancy are transformed back to a nonpregnant cyclical endometrium.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Andrew AC, Bulmer JB, Wells M, Morrison L, Buckley CH. Subinvolution of the uteroplacental arteries in the human placental bed. Histopathology. 1989;15:395–405.

    CAS  PubMed  Google Scholar 

  2. Andrew A, Bulmer JN, Morrison L, Wells M, Buckley CH. Subinvolution of the uteroplacental arteries: an immunohistochemical study. Int J Gynecol Pathol. 1993;12:28–33.

    CAS  PubMed  Google Scholar 

  3. Baba T, Endo T, Ikeda K, Shimizu A, Morishita M, Kuno Y, Honnma H, Kiya T, Ishioka S, Saito T. Assisted reproductive technique increases the risk of placental polyp. Gynecol Endocrinol. 2013;29:611–4.

    PubMed  Google Scholar 

  4. Boronow RC, McElin TW, West RH, Buckingham JC. Ovarian pregnancy: report of four cases and a thirteen-year survey of the English literature. Am J Obstet Gynecol. 1965;91:1095–106.

    CAS  PubMed  Google Scholar 

  5. Bouyer J, Coste J, Fernandez H, Pouly JL, Job-Spira N. Sites of ectopic pregnancy: a 10 year population-based study of 1800 cases. Hum Reprod. 2002;17:3224–30.

    CAS  PubMed  Google Scholar 

  6. Budowick M, Johnson TR Jr, Genadry R, Parmley TH, Woodruff JD. The histopathology of the developing tubal ectopic pregnancy. Fertil Steril. 1980;34(2):169–71.

    CAS  PubMed  Google Scholar 

  7. Chen L, Liu J, Shu J, Zeng W, Zhao X. Successful laparoscopic management of diaphragmatic pregnancy: a rare case report and brief review of literature. BMC Pregnancy Childbirth. 2019;19:99.

    PubMed  PubMed Central  Google Scholar 

  8. Choi JJ, Emmadi R. Incidental placental site nodule in a fallopian tube. Int J Surg Pathol. 2014;22:90–2.

    PubMed  Google Scholar 

  9. Chokroverty M, Caballes RL, Gear PE. An unruptured tubal pregnancy at term. Arch Pathol Lab Med. 1986;110:250–1.

    CAS  PubMed  Google Scholar 

  10. Dubinsky TJ, Guerra F, Gormaz G, Maklad N. Fetal survival in abdominal pregnancy: a review of 11 cases. J Clin Ultrasound. 1996;24:513–7.

    CAS  PubMed  Google Scholar 

  11. Dubuisson JB, Aubriot FX, Cardone V, Vacher-Lavenu MC. Tubal causes of ectopic pregnancy. Fertil Steril. 1986;46:970–2.

    CAS  PubMed  Google Scholar 

  12. Dyer I, Bradburn DM. An inquiry into the etiology of placental polyps. Am J Obstet Gynecol. 1971;109:858–67.

    CAS  PubMed  Google Scholar 

  13. Dziedzic JM, Patel PV. Cervical ectopic pregnancy: a rare site of implantation. J Emerg Med. 2019;56:e123–5.

    PubMed  Google Scholar 

  14. Elson CJ, Salim R, Potdar N, Chetty M, Ross JA, Kirk EJ on behalf of the Royal College of Obstetricians and Gynaecologists. Diagnosis and management of ectopic pregnancy. BJOG. 2016;123:e15–55.

    Google Scholar 

  15. Farley NJ, Kohlmeier RE. A death due to subinvolution of the uteroplacental arteries. J Forensic Sci. 2011;56:803–5.

    PubMed  Google Scholar 

  16. Frachtman KG. Unruptured tubal term pregnancy. Am J Surg. 1953;86:161–8.

    CAS  PubMed  Google Scholar 

  17. Friedländer C. Physiologisch-anatomische Untersuchungen über den Uterus. Leipzig: Simmel and Co; 1870.

    Google Scholar 

  18. Gainey HL, Nicolay KS, Lapi A. Noninvolution of the placental site: clinical and pathological studies. Am J Obstet Gynecol. 1955;69:558–72.

    CAS  PubMed  Google Scholar 

  19. Huang S-S, Hsu T-Y. Term tubal pregnancy with a liveborn healthy baby. Pediatr Dev Pathol. 2007;10:69–71.

    PubMed  Google Scholar 

  20. Huang K, Song L, Wang L, Gao Z, Meng Y, Lu Y. Advanced abdominal pregnancy: an increasingly challenging clinical concern for obstetricians. Int J Clin Exp Pathol. 2014;7:5461–72.

    PubMed  PubMed Central  Google Scholar 

  21. Hymel JA, Hughes DS, Gehlot A, Ramseyer AM, Magann EF. Late abdominal pregnancies (≥20 weeks gestation): a review from 1965 to 2012. Gynecol Obstet Investig. 2015;80:253–8.

    Google Scholar 

  22. Jaffe RB, Lee PA, Midgley AR. Serum gonadotropins before, at the inception of, and following human pregnancy. J Clin Endocrinol Metab. 1969;29:1281–3.

    CAS  PubMed  Google Scholar 

  23. Joseph RJ, Irvine LM. Ovarian ectopic pregnancy: aetiology, diagnosis, and challenges in surgical management. J Obstet Gynaecol. 2012;32:472–4.

    CAS  PubMed  Google Scholar 

  24. Kavalar R, Arko D, Fokter Dovnik N, Takač I. Subinvolution of placental bed vessels: case report and review of the literature. Wien Klin Wochenschr. 2012;124:725–30.

    PubMed  Google Scholar 

  25. Khong TY, Abdul Rahman H. Bcl-2 expression delays postpartum involution of pregnancy-induced vascular changes in the human placental bed. Int J Gynecol Pathol. 1997;16:138–42.

    CAS  PubMed  Google Scholar 

  26. Khong TY, Chin MM. Subinvolution of the placental bed after molar pregnancy. J Reprod Med. 1996;41:352–4.

    CAS  PubMed  Google Scholar 

  27. Khong TY, Khong TK. Delayed postpartum hemorrhage: a morphologic study of causes and their relation to other pregnancy disorders. Obstet Gynecol. 1993;82:17–22.

    CAS  PubMed  Google Scholar 

  28. Khong TY, Adema ED, Erwich. On anatomical basis for the increase in birth weight in second and subsequent born children. Placenta. 2003;24:348–53.

    CAS  PubMed  Google Scholar 

  29. Kinder JM, Stelzer IA, Arck PC, Way SS. Immunological implications of pregnancy-induced microchimerism. Nat Rev Immunol. 2017;17:483–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kochi K, Hidaka T, Yasoshima K, Yoneda K, Arai K, Arai T. Four cases of cervical pregnancy. J Obstet Gynaecol Res. 2014;40:603–6.

    PubMed  Google Scholar 

  31. Lawrence WD, Qureshi F, Bonakdar MI. “Placental polyp”: light microscopic and immunohistochemical observations. Hum Pathol. 1988;19:1467–70.

    CAS  PubMed  Google Scholar 

  32. Li TC, Tristram A, Hill AS, Cooke ID. A review of 254 ectopic pregnancies in a teaching hospital in the Trent Region, 1977-1990. Hum Reprod. 1991;6:1002–7.

    CAS  PubMed  Google Scholar 

  33. Ludwig H. Surface structure of the human term placenta and of the uterine wall post partum in the screen scan electron microscope. Am J Obstet Gynecol. 1971;111:328–44.

    CAS  PubMed  Google Scholar 

  34. Ludwig H, Metzger H. Das uterine Placentarbett post partum im Rasterelektronenmikroskop, zugleich ein Beitrag zur Frage der extravasalen Fibrinbildung. Arch Gynakol. 1971;210:251–66.

    CAS  PubMed  Google Scholar 

  35. Marques K, Looney C, Hayslip C, Gavrilova-Jordan L. Modern management of hypervascular placental polypoid mass following spontaneous abortion: a case report and literature review. Am J Obstet Gynecol. 2011;205:e9–e11.

    PubMed  Google Scholar 

  36. McElin TW, Randall LM. Intratubal term pregnancy without rupture: review of the literature and presentation of diagnostic criteria. Am J Obstet Gynecol. 1951;61:130–7.

    CAS  PubMed  Google Scholar 

  37. Midgley AR, Jaffe RB. Regulation of human gonadotropins. II. Disappearance of human hCG following delivery. J Clin Endocrinol Metab. 1968;28:1712–8.

    CAS  PubMed  Google Scholar 

  38. Nayar R, Snell J, Silverberg SG, Lage JM. Placental site nodule occurring in a fallopian tube. Hum Pathol. 1996;27:1243–5.

    CAS  PubMed  Google Scholar 

  39. Neuman WL, Ponto K, Farber RA, Shangold GA. DNA analysis of unilateral twin ectopic gestation. Obstet Gynecol. 1990;75:479–83.

    CAS  PubMed  Google Scholar 

  40. Norén H, Lindblom B. A unique case of abdominal pregnancy: what are the minimal requirements for placental contact with the maternal vascular bed? Am J Obstet Gynecol. 1986;155:394–6.

    PubMed  Google Scholar 

  41. O’Connell CP. Full-term tubal pregnancy. Am J Obstet Gynecol. 1952;63:1305–11.

    PubMed  Google Scholar 

  42. Ober WB, Grady HG. Subinvolution of the placental site. Bull N Y Acad Med. 1961;37:713–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Paalman RJ, McElin TW. Noninvolution of the placental site. Am J Obstet Gynecol. 1959;78:898–907.

    CAS  PubMed  Google Scholar 

  44. Panelli DM, Phillips CH, Brady PC. Incidence, diagnosis and management of tubal and nontubal ectopic pregnancies: a review. Fertil Res Pract. 2015;1:15.

    PubMed  PubMed Central  Google Scholar 

  45. Philippe E, Ritter J, Renaud R, Dellenbach P, Fonck-Cussac Y, Gandar R. Les métrorrhagies tardives du post-partum par anomalie d’involution des artères utéro-placentaires. Rev Fr Gynécol. 1968;63:255–62.

    CAS  Google Scholar 

  46. Philippe E, Ritter J, Lefakis P, Laedlein-Greilsammer D, Itten S, Foussereau S. Grossesse tubaire, ovulation tardive et anomalie de nidation. Gynécol Obstét (Paris). 1970;69:617–28.

    Google Scholar 

  47. Practice Committee of American Society for Reproductive Medicine. Medical treatment of ectopic pregnancy: a committee opinion. Fertil Steril. 2013;100:638–44.

    Google Scholar 

  48. Randall S, Buckley CH, Fox H. Placentation in the fallopian tube. Int J Gynecol Pathol. 1987;6:132–9.

    CAS  PubMed  Google Scholar 

  49. Rewell RE. Extra-uterine decidua. J Pathol. 1971;105:219–22.

    CAS  PubMed  Google Scholar 

  50. Roberts RV, Dickinson JE, Leung Y, Charles AK. Advanced abdominal pregnancy: still an occurrence in modern medicine. Aust N Z J Obstet Gynaecol. 2005;45:518–21.

    PubMed  Google Scholar 

  51. Robertson WB, Brosens I, Landells WN. Abnormal placentation. Obstet Gynecol Annu. 1985;14:411–26.

    CAS  PubMed  Google Scholar 

  52. Rutherford RN, Hertig AT. Noninvolution of the placental site. Am J Obstet Gynecol. 1945;49:378–84.

    Google Scholar 

  53. Sharman A. Post-partum regeneration of the human endometrium. J Anat. 1953;87:1–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Shen L, Fu J, Huang W, Zhu H, Wang Q, Yang S, Wu T. Interventions for non-tubal ectopic pregnancy. Cochrane Database Syst Rev. 2014;7:CD011174.

    Google Scholar 

  55. Studdiford WE. Primary peritoneal pregnancy. Am J Obstet Gynecol. 1942;44:487–91.

    Google Scholar 

  56. Swan RW, Woodruff JD. Retained products of conception. Histologic viability of placental polyps. Obstet Gynecol. 1969;34:506–14.

    CAS  PubMed  Google Scholar 

  57. Takeda A, Koyama K, Imoto S, Mori M, Sakai K, Nakamura H. Placental polyp with prominent neovascularization. Fertil Steril. 2010;93:1324–6.

    PubMed  Google Scholar 

  58. Thorsteinsson VT, Kempers RD. Delayed postpartum bleeding. Am J Obstet Gynecol. 1970;107:565–71.

    CAS  PubMed  Google Scholar 

  59. Tulchinsky D, Ryan KJ. Maternal-fetal endocrinology. Philadelphia: W.B. Saunders; 1980.

    Google Scholar 

  60. Wachter DL, Thiel F, Agaimy A. Subinvolution of the placental site 6 years after last delivery. Int J Gynecol Pathol. 2011;30:581–2.

    PubMed  Google Scholar 

  61. Wakuda K, Yoshida Y. DNA ploidy and proliferative characteristics of human trophoblasts. Acta Obstet Gynecol Scand. 1992;71:12–6.

    CAS  PubMed  Google Scholar 

  62. Walsh SZ. Maternal effects of early and late clamping of the umbilical cord. Lancet. 1968;1:996–7.

    CAS  PubMed  Google Scholar 

  63. White RG. Advanced abdominal pregnancy – a review of 23 cases. Ir J Med Sci. 1989;158:77–8.

    CAS  PubMed  Google Scholar 

  64. Williams J. Remarks on subinvolution of the uterus. Br Med J. 1882;2:405–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Williams JW. Regeneration of the uterine mucosa after delivery, with especial reference to the placental site. Am J Obstet Gynecol. 1931;22(664–696):793–6.

    Google Scholar 

  66. Williams PC, Malvar TC, Kraft JR. Term ovarian pregnancy with delivery of a live female infant. Am J Obstet Gynecol. 1982;142:589–91.

    CAS  PubMed  Google Scholar 

  67. Wolfe SA, Pedowitz P. Late postpartum haemorrhage. Am J Obstet Gynecol. 1947;53:84–99.

    CAS  PubMed  Google Scholar 

  68. Wong JA, Clark JF. Correlation of symptoms with age and location of gestation in tubal pregnancy. J Natl Med Assoc. 1968;60:221–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Young RH, Kurman RJ, Scully RE. Placental site nodules and plaques. An analysis of 20 cases. Am J Surg Pathol. 1990;14:1001–9.

    CAS  PubMed  Google Scholar 

  70. Yu TJ, Iwasaki I, Teratani T, Tanaka T, Aoki M. Primary ovarian pregnancy in a cystic teratoma. Obstet Gynecol. 1984;64:52s–4s.

    CAS  PubMed  Google Scholar 

  71. Yu SC, Lee SW, Jiang P, Leung TY, Allen Chan KC, Chiu RWK, Lo YMD. High-resolution profiling of fetal DNA clearance from maternal plasma by massively parallel sequencing. Clin Chem. 2013;59:1228–37.

    CAS  PubMed  Google Scholar 

  72. Zhang J, Li F, Sheng Q. Full-term abdominal pregnancy: a case report and review of the literature. Gynecol Obstet Investig. 2008;65:139–41.

    Google Scholar 

  73. Zubor P, Kajo K, Dokus K, Krivus S, Straka L, Biskupska Bodova K, Danko J. Recurrent secondary postpartum hemorrhages due to placental site vessel subinvolution and local uterine tissue coagulopathy. BMC Pregnancy Childbirth. 2014;14:80.

    PubMed  PubMed Central  Google Scholar 

  74. Anderson WR, Davis J. Placental site involution. Am J Obstet Gynecol 1968;102:23–33.

    Google Scholar 

  75. Geiger W. Radioimmunological determination of human chorionic gonadotropin, human placental lactogen, growth hormone and thyrotropin in the serum of mother and child during the early puerperium. Horm Metab Res. 1973;5:342–6.

    Google Scholar 

  76. Korhonen J, Alfthan H, Ylöstalo P, Veldhuis J, Stenman UH. Disappearance of human chorionic gonadotropin and its alpha- and beta-subunits after term pregnancy. Clin Chem. 1997;43:2155–63.

    Google Scholar 

  77. Costa MA, Calejo LI, Martinez-de-oliveira J, Laurini R. Late-onset postpartum hemorrhage from placental bed subinvolution: a case report. J Reprod Med. 2005;50:557–60.

    Google Scholar 

  78. Al-Mehaisen L, Al-Kuran O, Amarin ZO, Matalka I, Beitawi S, Muhtaseb A. Secondary postpartum hemorrhage following placental site vessel subinvolution: a case report. Arch Gynecol Obstet. 2008;278:585–7.

    Google Scholar 

  79. Augensen K. Unruptured tubal pregnancy at term with survival of mother and child. Obstet Gynecol. 1983;61:259–61.

    Google Scholar 

  80. Willemen FW, Bol JJ, van Unnik AJ. Een voldragen tubaire zwangerschap [Tubal pregnancy brought to term]. Ned Tijdschr Geneeskd. 1965:;109:2339–41.

    Google Scholar 

  81. Gustafson GW, Bowman HE, Stout FE. Extrauterine pregnancy at term. Obstet Gynecol 1953;2:17–21.

    Google Scholar 

  82. Eddib A, Olawaiye A, Withiam-Leitch M, Rodgers B, Yeh J. Live twin tubal ectopic pregnancy. Int J Gynaecol Obstet. 2006;93:154–5.

    Google Scholar 

  83. Holzer E, Pickel H. Ausgetragene ektopische Schwangerschaft mit lebendem Kind [Ectopic pregnancy carried to full term with a living infant]. Zentralbl Gynakol. 1976;98:52–5.

    Google Scholar 

  84. Schneider L. Uber Vorkommen und Bedeutung leukocytärer Infiltrate im Ablösungsbereich der spontan geborenen Placenta [The occurrence and importance of leukocytic infiltrates in the region of detachment of spontaneously delivered placentas]. Arch Gynakol. 1970;208:247–54.

    Google Scholar 

  85. Mukaida T, Yoshida K, Soma H. A surface ultrastructural study of the placental separation site. J Clin Electron Microsc 1975;8:5–6

    Google Scholar 

  86. Maher JA. Morphologic and histochemical changes in postpartum uterine blood vessels. AMA Arch Pathol. 1959;67:175–80.

    Google Scholar 

  87. DeVoe RW, Pratt JH. Simultaneous intrauterine and extrauterine pregnancy. Am J Obstet Gynecol. 1948;56:1119–26.

    Google Scholar 

  88. Fox H. Morphological changes in the human placenta following fetal death. J Obstet Gynaecol Br Commonw. 196875:839–43.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Women’s and Children’s Hospital, Department of Anatomical Pathology, North Adelaide, SA, Australia

    T. Yee Khong

  2. Sidra Medicine, Department of Pathology, Doha, Qatar

    Adrian Charles

Authors
  1. T. Yee Khong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adrian Charles
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Yee Khong .

Editor information

Editors and Affiliations

  1. Professor of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York Presbyterian Hospital, New York, NY, USA

    Rebecca N. Baergen

  2. Centre for Trophoblast Research, University of Cambridge, Cambridge, UK

    Graham J. Burton

  3. Professor Emeritus of Pathology, State University of New York, Stony Brook, NY, USA

    Cynthia G. Kaplan

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Khong, T.Y., Charles, A. (2022). Extrauterine Implantation and Involution of Implantation Site. In: Baergen, R.N., Burton, G.J., Kaplan, C.G. (eds) Benirschke's Pathology of the Human Placenta. Springer, Cham. https://doi.org/10.1007/978-3-030-84725-8_13

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-84725-8_13

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-84724-1

  • Online ISBN: 978-3-030-84725-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation