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GERM CELLS MAY SURVIVE CLIPPING AND DIVISION OF THE SPERMATIC VESSELS IN SURGERY FOR INTRA-ABDOMINAL TESTES

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GERM CELLS MAY SURVIVE CLIPPING AND DIVISION OF THE SPERMATIC VESSELS IN SURGERY FOR INTRA-ABDOMINAL TESTES
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  0022-5347/99/1623-0872/0 THE JOURNAL O UROLOGY Copyright 1999 by MERIC N UROLOGICAL SOCUTION bc. Vol. 162, 72-874, September 1999 Printed in U.S.A. GERM CELLS MAY SURVIVE CLIPPING AND DIVISION OF 'I'HE SPERMATIC VESSELS IN SURGERY FOR INTRA-ABDOMINAL TESTES J. M. THORUP, DINA CORTES AND J. VISFELDT From the Departments of Paediatric Surgery nd Pathology Rigshospitalet University o Copenhagen Copenhagen Denmark ABSTRACT Purpose: Laparoscopy is a well described modality that provides an accurate visual diagnosis upon which further management of intra-abdominal testes may be based. Laparoscopic Ligation of spermatic vessels as stage 1 of the procedure is a natural extension of laparoscopy. A staged approach provides adequate viability of the intra-abdominal testis. However, it is uncertain whether the more sensitive germ cells survive this procedure in addition to the Sertoli and interstitial cells of the human testis. Survival of germ cells is a prerequisite of later fertility potential. Materials and Methods: We studied 17 nonpalpable testes in 10 patients 1 year and 7 months to 13 years old. Results of testicular biopsies of 13 intra-abdominal testes taken at stages 1 and 2 of surgery were available for histological comparison. Results: Median number of spermatogonia per tubular cross section of the biopsies taken at stage 2 was slightly lower (0.03) compared to the median number at stage 1 (0.06) of the operation but this difference was not significant (p = 0.2031). Conclusions: Our study shows that the spermatogonia may survive clipping and division of the spermatic vessels, although the number of spermatogonia per tubular transverse section de- creases slightly. KEY WORDS: cryptorchidism, germ cells, fertility, testis, laparoscopy At surgery about 5 of undescended testes are found in an intra-abdominal position.1.2 If the testis is far from the in- ternal ring or associated with short spermatic vessels, it is sometimes impossible to place the testis in the scrotum by means that maintain continuity of the spermatic vessels. Orchiopexy using the collateral vessels from the inferior epi- gastrium to maintain vascular adequacy of the testis was described in 1959 by Fowler and Stephens.3 Presently, lapa- roscopy is a well described modality that provides an accu- rate visual diagnosis upon which further management may be based. Laparoscopic ligation of spermatic vessels as stage 1 of the procedure is a natural extension of laparoscopy. A staged approach provides adequate viability of the intra- abdominal testis.* However, it is uncertain whether the more sensitive germ cells survive this procedure in addition to the Sertoli cells and the interstitial cells of the human testis. Survival of germ cells is a prerequisite of later fertility po- tential. A positive correlation exists between the size of the testis and the number of germ cells in the testicular biopsy at the time of surgery in adults treated with orchiopexy in childhood.5 If no germ cells and only Sertoli cells are present in the testicular tubular tissue the testis will be smaller. To our knowledge, only results from experimental animal stud- ies imply that germ cells actually survive ligation of sper- matic vessels. MATERIALS AND METHODS We studied 17 nonpalpable testes in 10 patients 1 year 7 months to 13 years old (median age 6 years 6 months). Patient 8 had bilateral intra-abdominal testes and an unbal- anced 13-20 chromosomal translocation, and was mentally retarded (see table). No other patient had associated anom- alies. Carbon dioxide pneumoperitoneum was established through a 3 mm. trocar and cannula. Intra-abdominal pressure between 9 and 12 cm water was recommended. A 4.5 mm 0 degree Accepted for publication April 9, 1999. laparoscope was placed through an umbilical port. With the patient in a mild Trendelenburg position, the space between the internal ring and colonic mesentery was inspected to locate the testis and visualize the testicular vessels and vas on both sides. A staged procedure was planned only if the testis size and shape, and testicular-epididymal association appeared satisfac- tory at laparoscopy. All testes were far from the internal ring, and either medial or lateral to the iliacal vessels. Two 5 mm. lateral ports were established at the lateral borders of the recti muscles, level with the umbilicus. The intra-abdominal testis was mobilized by dividing any adhesions between it and the pelvic wall or internal inguinal ring. Sharp and blunt dissection was performed to free the vessels from the peritoneum of the posterior abdominal wall. Two ligature clips were placed at the vessels and they were divided between the clips. The testis was fixed with a 5 111111 endoscopic clinch and a biopsy was taken with a 5 mm. biopsy punch forceps. Hemostasis was achieved with electrocautery using the tip of the scissor. Stage 2 was performed 3 to 7 months (median 4.5) later. The inguinal canal was opened and the gubernaculum, if present, was dissected free from its anchor to the testis. Care was taken not to divide it or any of the collateral circulation entering it at the deep ring. The vas was freed along its course to the testis. The blood supply to the vas was pre- served within a thin peritoneal pedicle. The abdominal testis was then freed from adhesions and placed in the scrotum. An open knife testicular biopsy was taken. The testicular biopsy specimens were fixed in Stieves fluid, and 4 Fm. sections were stained with iron hematoxylin and eosin. The examination was performed with a light micro- scope at a magnification of X840. The number of spermato- gonia per tubular cross section was measured from 100 tu- bular transverse sections determined by systematically stepwise movements of the stage (see figure). Normal num- bers of spermatogonia per tubular cross section depend on patient age. Therefore, the value was also expressed as a percent of the lowest normal value for age and referred to as the age matched number of spermatogonia per tubular cross 872  GERM CELLS MAY SURVIVE SURGERY FOR INTRA-ABDOMINAL TESTES 873 Clinical results and number of spermatogonia per tubular cross section o testicular biopsies taken at stages and of operation clipping and division of the spermatic uessels) for intraabdominal undescended testes. SDermatoeoniaPTubular Cross Section Pt No Affected Side Age Biopsy 1 No Stage Lowest Normal No Stage 9 Lowest Normal No Staee 1 No. Staee 2 Clinical Result 1 Lt 2 Rt Lt 3 Lt 4 Lt 5 Rt Lt 6 Rt Lt 7 Rt Lt 8 Rt Lt 9 Rt Lt 10 Rt Lt 4.9 7.5 7.5 9.9 1.7 13.5 13.5 2.5 2.5 7 8 7.8 11.5 11.5 5.2 5.2 5.7 5.7 0.02 0.06 0.03 0.02 0.45 0.31 0.77 0.02 0.13 0.26 0.14 0.01 0.02 0.12 0.10 3.0 9.2 4.6 3.0 132.4 17.2 42.7 5.9 38.2 40.0 21.5 0.6 3.0 18.5 15.4 0.01 0.01 0.01 0.01 0.20 0.09 0.71 0.02 0.03 0.17 0 0.12 0.23 1.5 1.5 1.5 1.5 58.8 5.0 39.4 5.9 8.9 26.2 0 18.5 35.4 Successful Atrophy Successful Successful Successful High position Successful Successful Successful Primary orchiectomy Successful Primary orchiectomy Successful Standard orchiopexy Successful Successful Standard orchiopexy Part of biopsy taken 6 months after clipping and division of spermatic vessels from abdominal testis demonstrates 4 spermatogonia. H E reduced from X40. section (see table). Normal values have been previously de- scribed.6 The clinical postoperative result of the operation was evaluated at 3-month followup. RESULTS Results of biopsies of 13 intra-abdominal testes taken at stages 1 and 2 of the operation were included in the statisti- cal calculations. We removed 2 small testes in an intra- abdominal position behind the bladder and separated from the epididymal structures. The remaining 2 testes were in an lntracanalicular position and standard orchiopexy was per- formed. The results of the spermatogonia per tubular cross section count of the testicular biopsies are shown in the table. Median number of spermatogonia per tubular cross section in the biopsies taken at stage 2 of the operation was slightly lower than to the median number taken at stage 1 but this difference was not significant (p = 0.2031, paired rank sum test, Wilcoxon test). Based on stage 2 biopsies patients exhibited about 1% of the lowest normal number of spermato- gonia per tubular cross section. At 3-month followup 11 of the 13 testes were in the scrotum and of satisfactory size and consistency, 1 was in a high position and 1 was atrophic (volume less than 0.5 ml.). DISCUSSION Most of our patients were much older than the majority recommended presently for orchiopexy. We excluded from study candidates for standard orchiopexy (testis close to the internal ring), cases of unilateral abdominal testis removed as contralateral testis was normally placed in the scrotum and bilateral cases with severe associated abnormalities of- ten operated on with a 1-stage procedure.7 Generally, bilat- eral undescended testes (48.9 ), ncluding abdominal testes, are more often associated with other abnormalities than uni- lateral testis (7.5 h7 Only 1 of our 7 patients with bilateral undescended testes had associated abnormalities. The number of spermatogonia per tubular cross section in the testicular biopsies of undescended abdominal testes is often much lower compared to the number in inguinal or more distal testes.2.7 However, even in abdominal testes  874 GERM CELLS MAY SURVIVE SURGERY FOR INTRA-ABDOMINAL TESTES spermatogonia are always present and sometimes the num- ber is even normal when the patient is younger than 15 months at oueration.8 Therefore. it is oDtima1 to ouerate preserving technique.19-21 Otherwise the testicular vessels may be clipped, orchiopexy performed and some spermatogo- nia may survive, which may be sufficient for later paternity. before that aie. The older age of our patients may explain the low number of spermatogonia per tubular transverse section in the stage 1 testicular biopsies, and may be relevant to the outcome of stage 2 biopsy. Our youngest patient was 1 year 7 months old, and surgery was no more difficult than that of the older patients. Therefore, we believe that this technique also is appropriate for children younger than 1 year. The principle of preliminary in situ ligation of the sper- matic vessels was confirmed by Pascual et al.9 Spermatic vessel ligation in 350 to 450 gm Sprague-Dawley rats pro- duced an initial 80% decrease in blood flow to the normal testis in 1 hour but by 30 days normal flow was restored, usually with preservation of testicular integrity, and there was no change in gonadal weight by 54 days. Histological examination revealed intact parenchymal-to-stromal ratios, and normal Leydig and Sertoli cell populations. Tubular dis- turbances occurred but they were usually mild. However, Salman and Fonkalsrud showed that division of the main spermatic artery and vein in 3-month-old, 320 to 360 gm. Wistar albino rats produced atrophy of the previously normal testis with spermatogenic arrest and interstitial cell dysfunc- tion.10 Although collateral blood flow to the testis was dem- onstrated, tissue perfusion was inadequate for normal sper- matogenesis and endocrine function. In humans it has clearly been shown that the number of spermatogonia per tubular cross section in the undescended testis at surgery positively correlates with future fertility potential in adults.5.11 If the number of spermatogonia per tubular cross section is lower than 1 of the lowest normal value for age, the subsequent risk of infertility is 33% in cases of unilateral and 73 to 100 n cases of bilateral crypt- orchidism, the latter depending on whether the value was obtained from 1 or both sides. Furthermore spermatogonia tend to disappear if the testis is not satisfactorily placed in scrotum.s Our study confirms that spermatogonia survive clipping and division of the spermatic vessels, although the number of spermatogonia per tubular cross section decreased slightly. Of our patients 8 had a higher number of spermatogonia per tubular cross section on the first biopsy but some decrease in number of spermatogonia should be expected as the main vessels are divided. The reason why this decrease was not significant may be due to our small study sample. However, only 4 of the 10 patients are at great risk of later infertility as they exhibited about 1 of the lowest normal number of spermatogonia per tubular cross section, while in the remain- ing patients some spermatogonia survived. According to the literature approximately 90% of testes clinically survive stage 1 clipping or ligation of the spermatic vessels and stage 2 open*. 2-15 or laparoscopic1~17 rchio- pexy. Koff and Sethi reported clinical success with a standard orchiopexy approach from the groin, which allows for a 1-stage Fowler-Stephens maneuver.18 In conclusion, the ad- vantage of a primarily laparoscopic procedure is visualiza- tion of the anatomy and the ability to plan a spermatic vessel REFERENCES 1. Cendron M. Huff D. S., Keating M. A. Snyder H. McC. and Duckett J. W.: Anatomical morphological and volumetric analysis: review of 759 cases of testicular maldescent. J. Urol. 149 570 1993. 2. Thorup J. Kvist N. Larsen P. Tygstrup I. and Mauritzen K.: Clinical results of early and late operative correction of non descended testes. Brit. J. Urol. 56: 322 1984. 3. Fowler R. and Stephens F. D.: The role of testicular vascular anatomy in the salvage of high undescended testis. Aust. New Zeal. J. Surg. 29 92 1959. 4. Law G. S., Perez L. M. and Joseph D. B.: Two-stage Fowler- Stephens orchiopexy with laparoscopic clipping of the sper- matic vessels. J. Urol. part 2 158 1205 1997. 5. Cortes D. and Thorup J.: Histology of testicular biopsies taken at operation for bilateral maldescended testes in relation to fertility in adulthood. Brit. J. Urol. 68 285 1991. 6. Cortes D.: Histological versus stereological methods applied at spermatogonia during normal human development. Scand. J. Urol. Nephrol. 24 11 1990. 7. Cortes D. Thorup J. M. Lenz K. Beck B. L. and Nielsen 0. H.: Laparoscopy in 100 consecutive patients with 128 im- palpable testes. Brit. J. Urol. 75 281 1995. 8. Cortes D. Thorup J. M. and Beck B. L.: Quantitative histology of germ cells in the undescended testes of human fetuses neonates and infants. J. Urol. 154: 1188, 1995. 9. Pascual J. A Villanueva-Meyer J. Salido E. Ehrlich R. M. Mena I. and Rajfer J.: Recovery of testicular blood flow fol- lowing ligation of testicular vessels. J. Urol. 142 549 1989. 10. Salman F. T. and Fonkalsrud E. W.: Effects of spermatic vas- cular division for correction of the high undescended testis on testicular function. Amer. J. Surg. 160 506 1990. 11. Cortes D.: Cryptorchidism-aspects of pathogenesis histology and treatment. Scand. J. Urol. Nephrol. suppl. 32 196 1998. 12. Bloom D. A.: Two-step orchiopexy with pelviscopic clip ligation of the spermatic vessels. J. Urol. 145 1030 1991. 13. Ferro F. Lais A. and Gonzalez-Serva L.: Benefits and after- thoughts of laparoscopy for the nonpalpable testis. J. Urol. part 2 166 795 1996. 14. Froeling F. M. Sorber M. J. de la Rosette J. J. and de Vries J. D.: he nonpalpable testis and the changing role of laparos- copy. Urology 43 222 1994. 15. Bogaert G. A. Kogan B. A. and Mevorach R. A.: Therapeutic laparoscopy for intra-abdominal testes. Urology 42 182 1993. 16. Caldamone A. A. and Amaral J. F.: Laparoscopic stage 2 Fowler-Stephens orchiopexy. J. Urol. 152: 1253 1994. 17. Esposito C. and Garipoli V.: The value of 2-step laparoscopic Fowler-Stephens orchiopexy for intra-abdominal testes. J. Urol. 158 1952 1997. 18. Koff S. A. and Sethi P. S.: Treatment of high undescended testes by low spermatic vessel ligation: an alternative to the Fowler-Stephens technique. J. Urol. part 2 156 799 1996. 19. Docimo S. G. Moore R. G. Adams J. and Kavoussi L. R.: Laparoscopic orchiopexy for high palpable undescended testis: preliminary experience. J. Urol. 154: 1513 1995. 20. El-Gohary M. A.: The role of laparoscopy in the management of impalpable testes. Ped. Surg. Int. 12 63 1997. 21. Nassar A. H.: Laparoscopic-assisted orchiopexy: a new approach to the impalpable testis. J. Ped. Surg. 30 39 1995.
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