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.
Similar content being viewed by others
References
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 72:643–647
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 48:331–333
Allan DJ, Gobe GC, Harmon BV (1988) Sertoli cell death by apoptosis in the immature rat testis following x-irradiation. Scanning Microsc 2:503–512
Cameron DF, Snydle FE, Ross MH, Drylie DM (1980) Ultrastructural alterations in the adluminal testicular compartment in men with varicocele. Fertil Steril 33:526–533
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 174:261–271
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 124:234–240
Cockett ATK, Takihara H, Cosentino MJ (1984) The varicocele. Fertil Steril 41:5–11
Cohen MS, Plaine L, Brown JS (1975) The role of internal spermatic vein plasma catecholamine determinations in subfertile men with varicoceles. Fertil Steril 26:1243–1249
Comhaire F, Vermeulen A (1974) Varicocele sterility: cortisol and catecholamines. Fertil Steril 25:88–95
Coolsaet BLRA (1980) The varicocele syndrome: venography determining the optimal level for surgical management. J Urol 124:833–839
Donohue RE, Brown JS (1969) Blood gases and pH determination in the internal spermatic vein of subfertile men with varicocele. Fertil Steril 20:365–369
Gasinska A, Hill S (1990) The effect of hyperthermia on the mouse testis. Neoplasma 37:357–366
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 9:27–37
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 161:1831–1834
Hudson RW, Perez-Marrero RA, Crawford VA, McKay DE (1985) Hormonal parameters in men with varicoceles before and after varicocelectomy. Fertil Steril 43:905–910
Kanwar KC, Bawa SR, Singal PK (1971) Mode of formation of giant cells in testicular hyperthermia. Fertil Steril 22:778–783
Kaya M, Harrison RG (1975) An analysis of the effect of ischaemia on testicular ultrastructure. J Pathol 117:105–117
Kaya M, Türkyilmaz R (1985) An ultrastructural study on the presence of various types of crystals in the infertile human testis. Anat Embryol 172:217–225
Kaya M (1986) Sertoli cells and various types of multinucleates in the rat seminiferous tubules following temporary ligation of the testicular artery. J Anat 144:15–29
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 21:828–839
Kessel RG (1992) Annulate lamellae: a last frontier in cellular organelles. Int Review Cytol 133:43–120
Kim ED, Leibman BB, Grinblat DB, Lipshultz LI (1999) Varicocele repair improves semen parameters in azoospermic men with spermatogenic failure. J Urol 162:737–740
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 86:549–552
Leeson TS, Leeson CR, Paparo AA (1988) Text-Atlas of histology. Saunders, Philadelphia
Lindholmer C, Thulin L, Eliasson R (1973) Concentration of cortisol and renin in the internal spermatic vein of men with varicocele. Andrologia 5:21–22
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 142:1461–1470
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 168:59–66
Millonig G (1961) Advantages of a phosphate buffer for OsO4 solutions in fixation. J Appl Physics 32:1637
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 156:1952–1958
Narbaitz R, Tolnai G, Jolly EE, Barwin N, McKay DE (1978) Ultrastructural studies on testicular biopsies from eighteen cases of hypospermatogenesis. Fertil Steril 30:679–686
Nistal M, Paniagua R, Abaurrea MA, Santamaria L (1982) Hyperplasia and the immature appearance of Sertoli cells in primary testicular disorders. Hum Pathol 13:3–12
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 34:107–115
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 64:273–297
Palomo A (1949) Radical cure of varicocele by a new technique. Preliminary report. J Urol 61:604–607
Pasqualotto FF, Lucon AM, Hallak J, Goes PM, Saldanha LB, Arap S (2003) Induction of spermatogenesis in azoospermic men after varicocele repair. Hum Reprod 18:108–112
Pinart E, Sancho S, Briz MD, Bonet S, Garcia N, Badia E (2000) Ultrastructural study of the boar seminiferous epithelium: in cryptorchidism. J Morphol 244:190–202
Powers JM, Schaumburg HH (1981) The testis adreno-leukodystrophy. Am J Pathol 102:90–98
Pryor JL, Howards SS (1987) Varicocele. Urol Clin North Am 14:499–513
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 54:300–304
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 18:26–29
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 13:349–367
Sadler TW (1985) Langman’s medical embryology. Williams, Baltimore
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 25:23–30
Salomon F, Hedinger CE (1982) Abnormal basement membrane structures of seminiferous tubules in infertile men. Lab Invest 47:543–554
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 83:828–832
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 36:302–306
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 715
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 10:73–78
Stranock SD (1979) Annulate lamellae from the reproductive tissues of a fish parasite. J Anat 129:885
Takihara H, Sakatoku J, Cockett ATK (1991) The pathophysiology of varicocele in male infertility. Fertil Steril 55:861–868
Terguem A, Dadoune J-P(1981) Morphological findings in varicocele. An ultrastructural study of 30 bilateral testicular biopsies. Int J Androl 4:515–531
Turner TT (1983) Varicocele: still an enigma. J Urol 129:695–699
Vydra G (1980) Ultrastructure of testicular damage caused by varicocele. Acta Chirur Acad Scien Hung 21:77–85
Zorgniotti AW, MacLeod J (1973) Studies in temperature, human semen quality, and varicocele. Fertil Steril 24:854–863
Author information
Authors and Affiliations
Corresponding author
Additional information
Part of this study was submitted as a PhD thesis by Asst. Prof. Hülya Özgür and presented at the 12th National Congress on Electron Microscopy held in Antalya, Turkey, 1995
Rights and permissions
About this article
Cite this article
Özgür, H., Kaya, M., Doran, Ş. et al. Ultrastructure of the seminiferous tubules in human testes before and after varicocelectomy. Anat Embryol 207, 343–353 (2003). https://doi.org/10.1007/s00429-003-0352-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-003-0352-3