Archives of Gynecology and Obstetrics

, Volume 294, Issue 3, pp 657–664 | Cite as

Characterization of endometriosis-associated immune cell infiltrates (EMaICI)

  • Claudia Scheerer
  • Petia Bauer
  • Vito Chiantera
  • Jalid Sehouli
  • Andreas Kaufmann
  • Sylvia Mechsner
Gynecologic Endocrinology and Reproductive Medicine

Abstract

Objective

To identify and characterize endometriosis-associated immune cell infiltrates (EMaICI). Furthermore, to define occurrence and size of EMaICI in various types of endometriosis.

Methods

Immune cells were characterized in samples of 60 premenopausal women with histological proven endometriosis. Therefore, immunohistochemical staining with monoclonal antibodies for CD3, CD4, CD8, CD45RO, CD25, CD56, CD68, and CD20 on sections of paraffin-embedded endometriotic tissue was performed.

Results

EMaICI were observed in all the types of endometriosis, and characterized as T lymphocytes (CD3+), helper T lymphocytes (CD4+), cytotoxic T lymphocytes (CD8+), antigen-experienced T lymphocytes”memory cells” (CD45RO+), macrophages (CD68+), and B lymphocytes (CD20+). The maximum frequency of EMaICI and their distribution per endometriotic lesion (EML) was observed in peritoneal endometriosis (pEM) and in ovarian endometriosis (Ov. EM). In myometrium from adenomyosis (M/AM), EMaICI occurrence was lower and smaller in size in comparison with EMaICI seen in other forms of endometriosis. EMaICI were negative for regulatory T cells (CD25+ high, FoxP3+) and natural killer cells (NK cells, CD56+).

Conclusion

Numerous and brisk EMaICI comprising several types of immune cells in all endometriosis forms suggest acute immunological reactions within the microenvironment of endometriosis lesions.

Keywords

Endometriosis Immune cell infiltrates Chronic inflammatory disease Immune cell defect 

Abbreviations

AM

Adenomyosis

CD

Cluster of differentiation

DIE

Deep infiltrating rectovaginal endometriosis

EDT

Endometriosis disease theory

EM

Endometriosis

EMaICI

Endometriosis-associated immune cell infiltrates

EML

Endometriotic lesions

EN1/pEM

Endometrium from patients with peritoneal EM

EN2/AM

Endometrium from adenomyosis

EN3k/UM

Endometrium from uterus myomatosus, used as control

ICI

Immune cell infiltrates

IHC

Immunohistochemistry

M/AM

Myometrium from adenomyosis

M/UM

Myometrium from myomatosus uterus, used as control

NK

Natural killer cells

NLP

Non-lesional peritoneum, used as control

NLO

Non-lesional ovarium, used as control

Ov. EM

Ovarian endometriosis

p EM

Peritoneal endometriosis

p

Proliferative phase

s

Secretory phase

References

  1. 1.
    Ebert A (2006) Endometriose. Walter de Gruyter, Berlin. In: Update 2006Google Scholar
  2. 2.
    Meyer R (1919) Uber den Stand der Frage der Adenomyositis und Adenomyome in allgemeinen und insbesondere über Adenomyositis serosoepithlialis und Adenomyometritis sarcomatosa. ZentralblGynäkol 43:745–750Google Scholar
  3. 3.
    Sampson JA (1927) Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol 3(2):93–110, 143Google Scholar
  4. 4.
    Leyendecker G, Kunz G, Noe M, Herbertz M, Mall G (1998) Endometriosis: a dysfunction and disease of the archimetra. Hum Reprod Update 4(5):752–762CrossRefPubMedGoogle Scholar
  5. 5.
    Leyendecker G, Wildt L, Mall G (2009) The pathophysiology of endometriosis and adenomyosis: tissue injury and repair. Arch Gynecol Obstet 280(4):529–538CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Dmowski WP, Steele RW, Baker GF (1981) Deficient cellular immunity in endometriosis. Am J Obstet Gynecol 141(4):377–383CrossRefPubMedGoogle Scholar
  7. 7.
    Morris H, Edwards J, Tiltman A, Emms M (1985) Endometrial lymphoid tissue: an immunohistological study. J Clin Pathol 38(6):644–652CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Kamat BR, Isaacson PG (1987) The immunocytochemical distribution of leukocytic subpopulations in human endometrium. Am J Pathol 127(1):66–73PubMedPubMedCentralGoogle Scholar
  9. 9.
    Marshall RJ, Jones DB (1988) An immunohistochemical study of lymphoid tissue in human endometrium. Int J Gynecol Pathol 7(3):225–235CrossRefPubMedGoogle Scholar
  10. 10.
    Witz CA, Montoya IA, Dey TD, Schenken RS (1994) Characterization of lymphocyte subpopulations and T cell activation in endometriosis. Am J Reprod Immunol 32(3):173–179CrossRefPubMedGoogle Scholar
  11. 11.
    Oosterlynck DJ, Cornillie FJ, Waer M, Koninckx PR (1993) Immunohistochemical characterization of leucocyte subpopulations in endometriotic lesions. Arch Gynecol Obstet 253(4):197–206CrossRefPubMedGoogle Scholar
  12. 12.
    Startseva NV (1980) Clinical immunological aspects of genital endometriosis. Akush Ginekol (Mosk) 3:23–26Google Scholar
  13. 13.
    Mettler L, Volkov NI, Kulakov VI et al (1996) Lymphocyte Subsets in the Endometrium of patients with Endometriosis throughout the Menstrual Cycle. Am J Reprod Immunol 36:342–348Google Scholar
  14. 14.
    Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997, 67(5):817–821Google Scholar
  15. 15.
    Wang Y, Zhang L, Wang X (2001) Study on the distribution of lymphocyte subsets in the eutopic and ectopic endometrium of women with endometriosis. Zhonghua fu chan ke za zhi 36(2):85–88PubMedGoogle Scholar
  16. 16.
    Bulun SE (2009) Endometriosis. N Engl J Med 360(3):268–279CrossRefPubMedGoogle Scholar
  17. 17.
    Szyllo K, Tchorzewski H, Banasik M, Glowacka E, Lewkowicz P, Kamer-Bartosinska A (2003) The involvement of T lymphocytes in the pathogenesis of endometriotic tissues overgrowth in women with endometriosis. Mediators Inflamm 12(3):131–138CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Agic A, Xu H, Finas D, Banz C, Diedrich K, Hornung D (2006) Is endometriosis associated with systemic subclinical inflammation? Gynecol Obstet Invest 62(3):139–147CrossRefPubMedGoogle Scholar
  19. 19.
    Braun DP, Muriana A, Gebel H, Rotman C, Rana N, Dmowski WP (1994) Monocyte-mediated enhancement of endometrial cell proliferation in women with endometriosis. Fertil Steril 61(1):78–84CrossRefPubMedGoogle Scholar
  20. 20.
    Berbic M, Hey-Cunningham AJ, Ng C, Tokushige N, Ganewatta S, Markham R, Russell P, Fraser IS. The role of Foxp3+ regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum Reprod 25(4):900–907Google Scholar
  21. 21.
    Osuga Y, Koga K, Hirota Y, Hirata T, Yoshino O, Taketani Y. Lymphocytes in endometriosis. Am J Reprod ImmunolGoogle Scholar
  22. 22.
    Oosterlynck DJ, Cornillie FJ, Waer M, Vandeputte M, Koninckx PR (1991) Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 56(1):45–51CrossRefPubMedGoogle Scholar
  23. 23.
    Wilson TJ, Hertzog PJ, Angus D, Munnery L, Wood EC, Kola I (1994) Decreased natural killer cell activity in endometriosis patients: relationship to disease pathogenesis. Fertil Steril 62(5):1086–1088CrossRefPubMedGoogle Scholar
  24. 24.
    Antsiferova YS, Sotnikova NY, Posiseeva LV, Shor AL (2005) Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis. Fertil Steril 84(6):1705–1711CrossRefPubMedGoogle Scholar
  25. 25.
    Confino E, Harlow L, Gleicher N (1990) Peritoneal fluid and serum autoantibody levels in patients with endometriosis. Fertil Steril 53(2):242–245CrossRefPubMedGoogle Scholar
  26. 26.
    Jones RK, Bulmer JN, Searle RF (1995) Immunohistochemical characterization of proliferation, oestrogen receptor and progesterone receptor expression in endometriosis: comparison of eutopic and ectopic endometrium with normal cycling endometrium. Hum Reprod (Oxford, England) 10(12):3272–3279Google Scholar
  27. 27.
    Jones RK, Bulmer JN, Searle RF (1996) Immunohistochemical characterization of stromal leukocytes in ovarian endometriosis: comparison of eutopic and ectopic endometrium with normal endometrium. Fertil Steril 66(1):81–89CrossRefPubMedGoogle Scholar
  28. 28.
    Isaacson KB, Xu Q, Lyttle CR (1991) The effect of estradiol on the production and secretion of complement component 3 by the rat uterus and surgically induced endometriotic tissue. Fertil Steril 55(2):395–402CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Claudia Scheerer
    • 1
  • Petia Bauer
    • 1
  • Vito Chiantera
    • 1
  • Jalid Sehouli
    • 1
  • Andreas Kaufmann
    • 1
  • Sylvia Mechsner
    • 1
  1. 1.Department of Gynecology, CharitéEndometriosis Research Center CharitéBerlinGermany

Personalised recommendations