Anatomy and Embryology

, Volume 207, Issue 4–5, pp 343–353 | Cite as

Ultrastructure of the seminiferous tubules in human testes before and after varicocelectomy

Original Article
First Online:
Accepted:

Abstract

Ultrastructure of the membrana propria and the seminiferous epithelium was studied in infertile human testis both before and 3–6 months after varicocelectomy. The frequent alterations, observed before and after the operation, were extremely thickened membrana propria, deep invaginations, multilamination and knob-like formation of basal laminae and formation of multinucleated spermatids, which were all considered as the common response of the testis to different noxious agents. Although the cells of the seminiferous epithelium were clearly affected by varicocele before varicocelectomy, many areas exhibited normal features after the operation. Furthermore, multinucleated cells, sharing common features of Sertoli cell and spermatogonium, were observed, as well as presence of well-developed annulate lamellae in the Sertoli cells, exhibiting centrioles in the vicinity of their nuclei after varicocelectomy. These multiple ultrastructural observations indicate that Sertoli cell division takes place. This study suggests that if the observation period of the tissue samples after varicocelectomy is long enough, the reversible changes of the tubular cells would be seen much more frequently.

Keywords

Testis Varicocelectomy Ultrastructure Annulate lamellae 
This is a preview of subscription content, log in to check access.

References

  1. Abdelrahim F, Mostafa A, Hamdy A, Mabrouk M, El-Kholy M, Hassan O (1993) Testicular morphology and function in varicocele patients: pre-operative and post-operative histopathology. Br J Urol 72:643–647PubMedGoogle Scholar
  2. Adamopoulos DA, Kontogeorgos L, Abrahamian-Michalakis A, Terzis T, Vassilopoulos P (1987) Raised sodium, potassium, and urea concentrations in spermatic venous blood: an additional causative factor in the testicular dysfunction of varicocele? Fertil Steril 48:331–333PubMedGoogle Scholar
  3. Allan DJ, Gobe GC, Harmon BV (1988) Sertoli cell death by apoptosis in the immature rat testis following x-irradiation. Scanning Microsc 2:503–512PubMedGoogle Scholar
  4. Cameron DF, Snydle FE, Ross MH, Drylie DM (1980) Ultrastructural alterations in the adluminal testicular compartment in men with varicocele. Fertil Steril 33:526–533PubMedGoogle Scholar
  5. Chakraborty J, Nelson L, Jhunjhunwala J, Young M, Kropp K (1976) Basal Lamina of human seminiferous tubule–its role in material transport. 1. In presence of tunica vaginal hydrocele. Cell Tiss Res 174:261–271Google Scholar
  6. Chakraborty J, Sinha Hikim AP, Jhunjhunwala J (1985) Effect of experimental torsion of the spermatic cord on sustentacular cells in the Guinea-Pig testis. Acta Anat 124:234–240Google Scholar
  7. Cockett ATK, Takihara H, Cosentino MJ (1984) The varicocele. Fertil Steril 41:5–11PubMedGoogle Scholar
  8. Cohen MS, Plaine L, Brown JS (1975) The role of internal spermatic vein plasma catecholamine determinations in subfertile men with varicoceles. Fertil Steril 26:1243–1249PubMedGoogle Scholar
  9. Comhaire F, Vermeulen A (1974) Varicocele sterility: cortisol and catecholamines. Fertil Steril 25:88–95PubMedGoogle Scholar
  10. Coolsaet BLRA (1980) The varicocele syndrome: venography determining the optimal level for surgical management. J Urol 124:833–839PubMedGoogle Scholar
  11. Donohue RE, Brown JS (1969) Blood gases and pH determination in the internal spermatic vein of subfertile men with varicocele. Fertil Steril 20:365–369PubMedGoogle Scholar
  12. Gasinska A, Hill S (1990) The effect of hyperthermia on the mouse testis. Neoplasma 37:357–366PubMedGoogle Scholar
  13. Haider SG, Passia D, Servos G, Hettwer H (1986) Electron microscopic evidence for deep invaginations of the lamina propria towards the seminiferous tubule lumen in a patient with varicocele. Int J Androl 9:27–37PubMedGoogle Scholar
  14. Hendin BN, Kolettis PN, Sharma RK, Thomas AJ, Agarwal A (1999) Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity. J Urol 161:1831–1834PubMedGoogle Scholar
  15. Hudson RW, Perez-Marrero RA, Crawford VA, McKay DE (1985) Hormonal parameters in men with varicoceles before and after varicocelectomy. Fertil Steril 43:905–910PubMedGoogle Scholar
  16. Kanwar KC, Bawa SR, Singal PK (1971) Mode of formation of giant cells in testicular hyperthermia. Fertil Steril 22:778–783PubMedGoogle Scholar
  17. Kaya M, Harrison RG (1975) An analysis of the effect of ischaemia on testicular ultrastructure. J Pathol 117:105–117PubMedGoogle Scholar
  18. Kaya M, Türkyilmaz R (1985) An ultrastructural study on the presence of various types of crystals in the infertile human testis. Anat Embryol 172:217–225PubMedGoogle Scholar
  19. Kaya M (1986) Sertoli cells and various types of multinucleates in the rat seminiferous tubules following temporary ligation of the testicular artery. J Anat 144:15–29PubMedGoogle Scholar
  20. Kerr JB, Rich KA, de Kretser DM (1979) Effects of experimental cryptorchidism on the ultrastructure and function of the Sertoli cell and peritubular tissue of the rat testis. Biol Reprod 21:828–839Google Scholar
  21. Kessel RG (1992) Annulate lamellae: a last frontier in cellular organelles. Int Review Cytol 133:43–120Google Scholar
  22. Kim ED, Leibman BB, Grinblat DB, Lipshultz LI (1999) Varicocele repair improves semen parameters in azoospermic men with spermatogenic failure. J Urol 162:737–740PubMedGoogle Scholar
  23. Köksal IT, Tefekli A, Usta M, Erol H, Abbasoğlu S, Kadioğlu A (2000) The role of reactive oxygen species in testicular dysfunction associated with varicocele. BJU Int 86:549–552CrossRefPubMedGoogle Scholar
  24. Leeson TS, Leeson CR, Paparo AA (1988) Text-Atlas of histology. Saunders, PhiladelphiaGoogle Scholar
  25. Lindholmer C, Thulin L, Eliasson R (1973) Concentration of cortisol and renin in the internal spermatic vein of men with varicocele. Andrologia 5:21–22Google Scholar
  26. Lue Y, Rao PN, Sinha Hikim AP, Im M, Salameh WA, Yen PH, Wang C, Swerdloff RS (2001) XXY male mice: an experimental model for Klinefelter syndrome. Endocrinology 142:1461–1470PubMedGoogle Scholar
  27. Martin R, Santamaria L, Nistal M, Fraile B, Paniagua R (1992) The peritubular myofibroblasts in the testes from normal men and men with Klinefelter’s syndrome. A quantitative, ultrastructural, and immunohistochemical study. J Pathol 168:59–66PubMedGoogle Scholar
  28. Millonig G (1961) Advantages of a phosphate buffer for OsO4 solutions in fixation. J Appl Physics 32:1637Google Scholar
  29. Mitropoulos D, Deliconstantinos G, Zervas A, Villiotou V, Dimopoulos C, Stavrides J (1996) Nitric oxide synthase and xanthine oxidase activities in the spermatic vein of patients with varicocele: a potential role for nitric oxide and peroxynitrite in sperm dysfunction. J Urol 156:1952–1958PubMedGoogle Scholar
  30. Narbaitz R, Tolnai G, Jolly EE, Barwin N, McKay DE (1978) Ultrastructural studies on testicular biopsies from eighteen cases of hypospermatogenesis. Fertil Steril 30:679–686PubMedGoogle Scholar
  31. Nistal M, Paniagua R, Abaurrea MA, Santamaria L (1982) Hyperplasia and the immature appearance of Sertoli cells in primary testicular disorders. Hum Pathol 13:3–12PubMedGoogle Scholar
  32. Nistal M, Santamaria L, Paniagua R, Regadera J (1986) Changes in the connective tissue and decrease in the number of mast cells in the testes of men with alcoholic and non-alcoholic cirrhosis. Acta Morphol Hung 34:107–115PubMedGoogle Scholar
  33. Oettle AG, Harrison RG (1952) The histological changes produced in the rat testis by temporary and permanent occlusion of the testicular artery. J Path Bact 64:273–297Google Scholar
  34. Palomo A (1949) Radical cure of varicocele by a new technique. Preliminary report. J Urol 61:604–607Google Scholar
  35. Pasqualotto FF, Lucon AM, Hallak J, Goes PM, Saldanha LB, Arap S (2003) Induction of spermatogenesis in azoospermic men after varicocele repair. Hum Reprod 18:108–112CrossRefPubMedGoogle Scholar
  36. Pinart E, Sancho S, Briz MD, Bonet S, Garcia N, Badia E (2000) Ultrastructural study of the boar seminiferous epithelium: in cryptorchidism. J Morphol 244:190–202CrossRefPubMedGoogle Scholar
  37. Powers JM, Schaumburg HH (1981) The testis adreno-leukodystrophy. Am J Pathol 102:90–98PubMedGoogle Scholar
  38. Pryor JL, Howards SS (1987) Varicocele. Urol Clin North Am 14:499–513PubMedGoogle Scholar
  39. Pujol A, Tolra J, Navarro MA, Bonnin R, Sirvent JJ, Pladellorens M, Bernat R (1982) The hormonal pattern in varicocele and its relationship with the findings of testicular biopsy: preliminary results. Br J Urol 54:300–304PubMedGoogle Scholar
  40. Romeo C, Ientile R, Impellizzeri P, Turiaco N, Teletta M, Antonuccio P, Basile M, Gentile C (2003) Preliminary report on nitric oxyde—mediated oxydative damage in adolescent varicocele. Hum Reprod 18:26–29CrossRefPubMedGoogle Scholar
  41. Russell LD, Malone JP, MacCurdy DS (1981) Effect of the microtubule disrupting agents, colchicine and vinblastine, on seminiferous tubule structure in the rat. Tissue Cell 13:349–367CrossRefPubMedGoogle Scholar
  42. Sadler TW (1985) Langman’s medical embryology. Williams, BaltimoreGoogle Scholar
  43. Sailer BL, Jost LK, Erickson KR, Tajiran MA, Evenson DP (1995) Effects of x-irradiation on mouse testicular cells and sperm chromatin structure. Envirol Mol Mutagen 25:23–30Google Scholar
  44. Salomon F, Hedinger CE (1982) Abnormal basement membrane structures of seminiferous tubules in infertile men. Lab Invest 47:543–554PubMedGoogle Scholar
  45. Santoro G, Romeo C, Impellizzeri P, Arco A, Rizzo G, Gentile C (1999) A morphometric and ultrastructural study of the changes in the lamina propria in adolescents with varicocele. BJU Int 83:828–832CrossRefPubMedGoogle Scholar
  46. Savaş C, Özogul C, Karaöz E, Bezir M (2002) Ischaemia, whether from ligation or torsion, causes ultrastructural changes on the contralateral testis. Scan J Urol Nephrol 36:302–306CrossRefGoogle Scholar
  47. Sherins RJ, Howards SS (1978) Male infertility. In: Harrison JH, Gittes RF, Perlmutter AD, Stamey TA, Walsh PC (eds). Campbell’s urology. Saunders, Philadelphia, pp 715Google Scholar
  48. Spera G, Medolago-Albani L, Coia L, Morgia C, Gonnelli S, Ghilardi C (1983) Histological, histochemical and ultrastructural aspects of interstitiel tissue from the contralateral testis in infertile men with monolateral varicocele. Arch Androl 10:73–78PubMedGoogle Scholar
  49. Stranock SD (1979) Annulate lamellae from the reproductive tissues of a fish parasite. J Anat 129:885Google Scholar
  50. Takihara H, Sakatoku J, Cockett ATK (1991) The pathophysiology of varicocele in male infertility. Fertil Steril 55:861–868PubMedGoogle Scholar
  51. Terguem A, Dadoune J-P(1981) Morphological findings in varicocele. An ultrastructural study of 30 bilateral testicular biopsies. Int J Androl 4:515–531PubMedGoogle Scholar
  52. Turner TT (1983) Varicocele: still an enigma. J Urol 129:695–699PubMedGoogle Scholar
  53. Vydra G (1980) Ultrastructure of testicular damage caused by varicocele. Acta Chirur Acad Scien Hung 21:77–85Google Scholar
  54. Zorgniotti AW, MacLeod J (1973) Studies in temperature, human semen quality, and varicocele. Fertil Steril 24:854–863PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Histology–Embryology, Faculty of MedicineUniversity of ÇukurovaBalcali-AdanaTurkey
  2. 2.Department of Urology, Faculty of MedicineUniversity of ÇukurovaBalcali-AdanaTurkey

Personalised recommendations