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Extraparenchymal ovarian and testicular Leydig cells: ectopic/heterotopic or orthotopic?

  • Gynecologic Endocrinology and Reproductive Medicine
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

We are conducting a prospective study trying to determine, in both sexes, the frequency of appearance of ectopic Leydig cells, their preferred location, their relationship with nerve structures and the possible causes of their appearance.

Methods

We have studied 86 cases that were removed according to different clinical indications for pathological study: uterine leyomiomas (n = 12), ovarian cystadenoma (n = 4), endometrial hyperplasia (n = 8), endometrial carcinoma (n = 12), cervical carcinoma (n = 4), seminoma (n = 4), fallopian tube ligatures (n = 24), vasectomies (n = 8), nonspecific orchiepididymitis (n = 2), and unknown (n = 8).

Results

We have observed ectopic Leydig cells in 13/86 cases (15.11%), 9/72 in the female samples (12.50%) and 4/14 in male samples (28.57%). The most frequent location was the mesosalpinx (4 of 13: 30.76%).

Conclusions

These high figures lead us to believe that the ectopia of Leydig cells is not really a pathologic entity, but a finding related to specific functions yet to be determined.

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(Adapted from Langman J. Medical embryology and human development-normal and abnormal, 2nd ed. Williams & Wilkins, Baltimore, 1969, pp 169)

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References

  1. Trainer TD (1997) Testis and excretory duct system. In: Sternberg SS (ed) Histology for pathologists, 2nd edn. Lippincott-Raven, Philadelphia, pp 1019–1038

    Google Scholar 

  2. Sternberg WH (1949) The morphology, androgenic function, hyperplasia, and tumors of the human ovarian hilus cells. Am J Pathol 25:493–521

    PubMed  PubMed Central  CAS  Google Scholar 

  3. Carrasco-Juan JL, Álvarez-Argüelles Cabrera H, Martín Corriente MC, González-Gómez M, Valladares Parrilla F, Gutiérrez García R, Díaz-Flores L (2017) Ovarian Leydig cells (OLC): a histomorphological and immunohistochemical study. Histol Histopathol 32:1089–1097

    PubMed  CAS  Google Scholar 

  4. Nelson AA (1938) Giant interstitial cells and extraparenchymal interstitial cells of the human testis. Am J Pathol 14:831–841

    PubMed  PubMed Central  CAS  Google Scholar 

  5. Nistal M, Paniagua R (1979) Histogenesis of human extraparenchymal Leydig cells. Acta Anat 105:188–197

    Article  PubMed  CAS  Google Scholar 

  6. Mori H, Tamai M, Fushimi H, Fukuda H, Maeda T (1987) Leydig cells within the aspermatogenic seminiferous tubules. Hum Pathol 18:1227–1231

    Article  PubMed  CAS  Google Scholar 

  7. Ulbright TM, Amin MB, Young RH (1999) Tumor-like lesions of testis, paratestis, and spermatic cord. In: Rosai J, Sobin LH (eds) Atlas of tumor pathology. Tumors of the testis, adnexa, spermatic cord, and scrotum. Armed Forces Institute of Pathology [3rd series. Fascicle 25], Washington DC, pp 291–342

    Google Scholar 

  8. Verocay J (1915) Hat Unwegsamkeit des Ductus deferens Atrophie des Hodens zur Folge? Prag Med Wchschr 40:113–115

    Google Scholar 

  9. Okkels H, Sand K (1940) Morphological relationship between testicular nerves and Leydig cells in man. J Endocrinol 2:38–46

    Article  Google Scholar 

  10. Jun SY, Ro JY, Park YW, Kim KR, Ayala AG (2008) Ectopic Leydig cells of testis. An immunohistochemical study on tissue microarray. Ann Diagn Pathol 12:29–32

    Article  PubMed  Google Scholar 

  11. Halley JB (1960) Relation of Leydig cells in the human testicle to the tubules and testicular function. Nature 185:865–866

    Article  PubMed  CAS  Google Scholar 

  12. Brack E (1923) Zur pathologischen Anatomie der Leydig Zelle. Virchows Arch Path Anat Physiol 240:127–143

    Article  Google Scholar 

  13. McDonald JH, Calams JA (1958) A histological study of extraparenchymal Leydig cell-like cells. J Urol 79:850–858

    Article  PubMed  CAS  Google Scholar 

  14. Mori H, Shiraishi T, Matsumoto K (1978) Ectopic Leydig cells in seminiferous tubules of an infertile male with a chromosomal aberration. Andrologia 10:434–443

    Article  PubMed  CAS  Google Scholar 

  15. Schulze C, Holstein AF (1978) Leydig cells within the lamina propria of seminiferous tubules in four patients with azoospermia. Andrologia 10:444–452

    Article  PubMed  CAS  Google Scholar 

  16. Regadera J, Codesal J, Paniagua R, Gonzalez-Peramato P, Nistal M (1991) Immunohistochemical and quantitative study of interstitial and intratubular Leydig cells in normal men, cryptorchidism, and Klinefelter´s syndrome. J Pathol 164:299–306

    Article  PubMed  CAS  Google Scholar 

  17. Priesel A (1924) Über das Verhalten von Hoden und Nevenhoden bei angeborenem von Zwischenzellen in menschliche Nebenhoden. Virchows Arch Path Anat Physiol 249:246–304

    Article  Google Scholar 

  18. Berger L (1922) Sur l´existence de glands sympathicotropes dans l´ovaire et le testicule humains; leur rapport avec la glande interstitielle du testicule. Compt Rend Acad Sci Paris 175:907–909

    Google Scholar 

  19. Peters KH (1977) Ultrastructure of human heterotopic Leydig cells. Andrologia 9:337–348

    Article  PubMed  CAS  Google Scholar 

  20. Chougule A, Dey P (2017) Hilus cell heterotopia with intraneural eutopia. Int J Gynecol Pathol 36:200–202

    Article  PubMed  Google Scholar 

  21. He HL, Lee YE, Chang CC (2014) Hilus cell heterotopia accompanying bilateral ovarian serous cystadenomas: a case report and review of the literature. Int J Clin Exp Pathol 7:1246–1249

    PubMed  PubMed Central  Google Scholar 

  22. Hirschowitz L, Salomons N, Ganesan R (2011) Ovarian hilus cell heterotopia. Int J Gynecol Pathol 30:46–52

    Article  PubMed  Google Scholar 

  23. Honoré LH, O’Hara KE (1979) Ovarian hilus cell heterotopia. Obstet Gynecol 53:461–464

    PubMed  Google Scholar 

  24. Neupert G, Appel P, Braun S, Tonus C (2007) Heterotopic pancreas in the gallbladder. Diagnosis, therapy, and course of a rare developmental anomaly of the pancreas. Chirurg 78:261–264

    Article  PubMed  CAS  Google Scholar 

  25. Carrasco-Juan JL, Álvarez-Argüelles Cabrera H, Martín Corriente MC, Valladares Parrilla F, Gutiérrez García R, Díaz-Flores L (2017) Ovarian leydig cells (OLC): about their heterotopia or eutopia. Int J Gynecol Pathol. https://doi.org/10.1097/PGP.0000000000000448

    Article  PubMed  Google Scholar 

  26. Regadera J, Cobo P, Martínez-García F, Nistal M, Paniagua R (1993) Testosterone immunoexpression in human Leydig cells of the tunica albuginea testis and spermatic cord. A quantitative study in normal foetuses, young adults, elderly men and patients with cryptorchidism. Andrologia 25:115–122

    Article  PubMed  CAS  Google Scholar 

  27. Jost A (1953) Problems of fetal endocrinology: the gonadal and hypophyseal hormones. Recent Prog Horm Res 8:379–418

    Google Scholar 

  28. Murashima A, Bingfans X, Hinton BT (2015) Understanding normal and abnormal development of the Wolffian/epididymal duct using transgenic mice. Asian J Androl 17:749–755

    PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Patrick Dennis for revising the English language in this manuscript. This work has been possible thanks to the existing research agreement between the University of La Laguna and the Clinical Laboratory Dr. Gonzalez Santiago (CI02020401).

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Authors and Affiliations

  1. Department of Basic Medical Sciences, Faculty of Health Sciences, Medicine Section, University of La Laguna, C/Sta. María Soledad, s/n. Apartado 456, Código Postal 38200, San Cristóbal de La Laguna, Tenerife, Islas Canarias, Spain

    José L. Carrasco-Juan, Hugo Álvarez-Argüelles-Cabrera, Ricardo Gutiérrez-García, Rafael Méndez-Medina & Lucio Díaz-Flores

  2. Service of Pathology, Canary University Hospital Complex, Tenerife, Spain

    Hugo Álvarez-Argüelles-Cabrera, Carmen Martín-Corriente, Abián Vega-Falcón, Idaira Expósito-Afonso & Rafael Méndez-Medina

Authors
  1. José L. Carrasco-Juan
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  2. Hugo Álvarez-Argüelles-Cabrera
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  3. Carmen Martín-Corriente
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  4. Ricardo Gutiérrez-García
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  7. Rafael Méndez-Medina
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  8. Lucio Díaz-Flores
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Contributions

JLC: project development, data collection, manuscript writing. HÁ: project development, data collection, manuscript writing. CM: project development, manuscript writing. RG: project development, manuscript writing. AV: project development, data collection. IE: project development, data collection. RM: project development, data collection. LD: project development, data collection, manuscript writing.

Corresponding author

Correspondence to José L. Carrasco-Juan.

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Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The Institutional Ethics Committee of the University of La Laguna approved this study (CEIBA2018-0289).

Informed consent

Additional informed consent was not required since our standard hospital consent form for surgical or other procedure specifically states that “I understand that the Hospital may use for teaching or scientific purposes, or may otherwise dispose of, tissues, fluids or organs removed during the procedure”.

Conflict of interest

The authors declare that they have no conflict of interest.

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Carrasco-Juan, J.L., Álvarez-Argüelles-Cabrera, H., Martín-Corriente, C. et al. Extraparenchymal ovarian and testicular Leydig cells: ectopic/heterotopic or orthotopic?. Arch Gynecol Obstet 298, 655–661 (2018). https://doi.org/10.1007/s00404-018-4846-x

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  • DOI: https://doi.org/10.1007/s00404-018-4846-x

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