Improvement in Spermatogenesis Following Depression of the Human Testis with Testosterone

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1 Improvement in Spermatogenesis Following Depression of the Human Testis with Testosterone Carl G. Heller, M.D., Ph.D.; Warren 0. Nelson, Ph.D.; Irvin B. Hill, M.D.; Edward Henderson, M.D.; William 0. Maddock, M.D., Ph.D.; Edwin C. Jungck, M.D., Ph.D.; C. Alvin Paulsen, B.A.; and Glenn E. Mortimore, B.S. T.sTOSTERONE IS WIDELY used for treating numerous clinical entities without regard for the functional status of the patient's testes. This study attempts to evaluate objectively the short- and long-term effects of testosterone administration on the testis by means of repeated histologic examinations of testicular biopsies taken from the same individual before, during, and many months after cessation of testosterone administration. Indirect evidence indicates that testosterone administration suppresses human testicular function as judged by the depression of sperm output (demonstrated by McCullagh and McGurP 0 11 and others ). Concomitant depression of urinary gonadotropins:; G, 7 occurs. Failure of pitui- From the Division of Endocrinology, Department of Medicine, University of Oregon Medical School, Portland, Oregon; the Department of Anatomy, University of Iowa College of Medicine, Iowa City, Iowa; State of Oregon Fairview Home, Salem, Oregon; and Medical Department, Schering Corporation, Bloomfield, New Jersey. Presented in part at the meeting of the Northwest group of the American Federation for Clinical Research, Seattle, Washington, Feb. 25, 1950 by C. Alvin Paulsen; at the Post Graduate Course in Endocrinology of the American College of Physicians, Chicago, Illinois, May 18, 1950 by Warren 0. Nelson; at the 32nd annual meeting of the Association for Study of Internal Secretions,8 San Francisco, California, June 23, 1950 by Carl G. Heller, and at the Sixth Annual Conference of the American Society for the Study of Sterility, San Francisco, California, June 25, 1950 by Carl G. Heller9 and W. 0. Nelson.l3 415

2 416 HELLER ET AL. [Fertility & Sterility tary stimulation of spermatogenesis is a probable resultant of such depression. Direct evidence derived from observation of testicular biopsies before and after testosterone administration is lacking. Occasionally observations have been made on testicular biopsies observed after treatment only, 7 in which case atrophy and degeneration of the seminiferous tubules were noted. Charny and Meranze performed testicular biopsies before and after testosterone treatment on a single hypogonadal patient and noted necrotic changes in the seminiferous tubules. The subjects studied were healthy young adult men age 15 to 46, residing at an institution for the mentally deficient. Pretreatment control testicular biopsies from 46 subjects were examined and found to vary from excellent to very poor, as in any unselected segment of the population. More men than anticipated exhibited defects in spermatogenesis. These defects were similar to those seen in testicular biopsies of infertile men having oligospermia. Twenty of these subjects were given testosterone. Thirteen received intramuscular injections of 25 mg. of testosterone propionate for twentyfour to ninety-nine consecutive days. Of these, 2 received, additionally, 100 mg. of pregnenolone and one received 25 mg. of progesterone daily with each injection of testosterone propionate. Seven subjects were implanted subcutaneously with from 3 to 7 pellets of unconjugated testosterone, each pellet weighing 75 mg. A second testicular biopsy was performed on the last day of treatment in each instance of injection therapy and at three, six, or twelve months from the time of implantation of the pellets. The histological findings were similar in each case and are summarized here: A. All exhibited damage to spermatogenesis as judged by: 1. Decrease in size of the seminiferous tubules. 2. Sclerosis and hyalinization of the basement membrane and tunica propria of the seminiferous tubules. 3. Necrosis and sloughing of germinal elements. 4. Arrest of sperm formation. 5. Decrease in numbers of germinal elements. Spermatids and spermatocytes disappeared more readily than spermatogonia. B. All exhibited damage to the interstitial cells of Leydig as judged by: 1. Absence of Leydig cells. 2. Atrophy of those interstitial cells that could be detected.

3 Vol. 1, No. 5, 1950] IMPROVEMENT IN SPERMATOGENESIS 417 Much of this marked change could be due to depression of gonadotropin secretion. In no instance were urinary gonadotropins detectable at this time (although they were detected before treatment was initiated and after treatment was discontinued in the majority of subjects). Where observations could be made it was noted that sperm output fell gradually to or near azoospermic levels. The majority of testicular changes could be attributed to withdrawal of gonadotrophic stimulation. The marked sclerosis of the seminiferous tubular membranes, is suspected as being a direct effect of testosterone upon the testis. In 3 subjects a third testicular biopsy was performed five to six months after cessation of treatment. Some recovery of germinal and interstitial elements was noted. Third biopsies were obtained twelve months after treatment was discontinued in 1 subject, seventeen months after in 2, twenty-seven months after in 1, twenty-nine months after in 2. Fourth biopsies were obtained seventeen months after stopping treatment in 1 individual. A fifth biopsy was performed thirty-one months after stopping treatment in another. (It was presumed that the pellets stopped exerting an effect in six months. This was arbitrarily taken as the time treatment was discontinued in those having testosterone pellet implantation.) Each of these biopsies revealed marked improvement over the biopsies studied at the end of the period of testosterone administration. Each, when compared to the initial biopsies (it should be remembered that the original biopsies were rated variously from excellent to very poor) was either remarkably better than the initial biopsy, or if the initial biopsy was rated excellent, was equally good. The most striking phenomenon was the disappearance of hyalinization of the seminiferous tubules in the biopsies obtained twelve to thirtyone months after discontinuing treatment. The sclerosis and hyalinization vanished whether it had been present initially or induced by testosterone administration. The tubules increased greatly in size, the germinal epithelium appeared or reappeared in orderly arrangement, and sperm were abundantly found in the tubules. Leydig cells were optimal in numberfi and appearance. The principle of depressing the testes and pituitary gonadotropin output and then allowing rebound recovery, which supersedes the initial state, in the event of original testicular damage, might well be applied to

4 418 HELLER ET AL. [Fertility & Sterility the problem of certain types of male infertility. One infertile male, having elevated gonadotrophins, moderate testicular damage and sperm output of 3 to 4 per low power field, was treated for one month with 100 mg. of testosterone proprionate daily. After initial suppression to azoospermic levels, sperm output rose to 63 and 58 million per cc. twenty-three months later. A B c FIGURE I. Testicular biopsies, showing the marked degree of sclerosis and hyalinization that Dccurs when an initially very poor testis is subjected to the administration of ninety-one consecutive injections of testosterone propionate, 25 mg. each. A, before treatment; B, at end of ninety-one days of treatment; C, seventeen months after cessation of treatment. Note, in C, the disappearance of hyalinization, the increase in size of the seminiferous tubules, and the appearance of fairly orderly spermatogenesis. Leydig cells, not shdwn here, were present seventeen. months after treatment was stopped. FM 3, right testis, age 42. Clinical application of the above observations should be sharply limited until thorough investigation of the phenomenon has been undertaken. In our opinion, treatment of infertile men with testosterone should not be undertaken until it has been proved that a given subject fails to respond to stimulatory therapy with gonadotropins containing follicle-stimulating hormone. We currently believe that only those infertile men having elevated gonadotropins and hyalinization of the membranes of the seminiferous tubules accompanied by marked germinal defects are potential candidates for investigative treatment with testosterone.

5 Vol. I, No. 5, 1950] IMPROVEMENT IN SPERMATOGENESIS c 419 D FIGURE 2. Serial testicular biopsies obtained from the same patient, FM 10, age 41. A is a biopsy before treatment. B, three months after implantation of 3 pellets of unconjugated testosterone weighing 75 mg. each. C, biopsy taken eight months after pellet implantation, indicating some improvement. D, biopsy obtained thirty months after pellet implantation showing improvement in the seminiferous tubules beyond the initial status of the testis. SUMMARY Testosterone administered to men whose testicular biopsies revealed spermatogenesis ranging from excellent in some, to poor in others, invariably caused testicular damage. The damage included sclerosis and hyalinization of the membranes of the seminiferous tubules, atrophy and necrosis of germinal elements, and disappearance of the Leydig cells. The damage appears to be reversible. As a result of testosterone administration, in spite of temporary damage, testicular morphology and function was ultimately improved over the pre-treatment status, if the testis originally was less than excellent.

6 420 HELLER ET AL. [Fertility & Sterility REFERENCES 1. Charny, C. W., and Meranze, D. R.: Surg., Gynec. & Obst. 74:836, Heckel, N.J.: Proc. Soc. Exper. Bioi. & Med. 40:658, Heckel, N.J.: J. Urol. 43:286, Heckel, N.J.: Trans. Am. Assoc. Genito-Urin. Surgeons 34:237, Heller, C. G., Nelson, W. 0., and Roth, A. A.: J. Clin. Endocrinol. 3:573, Heller, C. G., and Myers, G. B.: J.A.M.A. 126:472, Heller, C. G., and Nelson, W. 0.: J. Clin. Endocrinol. 5:27, Heller, C. G., Nelson, W. 0., Hill, I. B., Henderson, E., Maddock, W. 0., and Jungck, E. C.: Assoc. Study Int. Secretion, Program, 32nd Annual Meeting, June 27, Heller, C. G.: Am. Soc. Study Sterility, Program, 6th Annual Conf., June 25, McCullagh, E. P., and McGurl, F. J.: J. Urol. 42:1265, McCullagh, E. P., and McGurl, F. J.: Endocrinol. 26:377, McCullagh, E. P., and Rossmiller, H. R.: J. Clin. Endocrinol. 1:496, Nelson, W. 0.: Am. Soc. Study Sterility, Program, 6th Annual Conf., June 25, DISCUSSION DR. JoHN MAcLEOD, Chairman, New York City: Dr. Henderson will open the discussion. DR. EDWARD HENDERSON, Bloomfield, New Jersey: This work was started about four years ago and no one could have been more surprised at the results than Dr. Heller himself and his associates. Two months ago in Chicago Dr. Heckel reported his first and preliminary findings of the clinical application of Dr. Heller's suggestion that testosterone could depress the testes and might be useful for treating certain cases of oligospermia. He now has 30 patients under treatment, but has presented results from only l. This patient had never had a sperm count of more than 35 million during the four years that Dr. Heckel had been treating him. He gave him 50 mg. of testosterone propionate three times a week for fifteen weeks until he showed complete azoospermia. Fourteen months later the sperm count was 160 million. So there may be promise in this treatment. DR. EDWARD C. REIFENSTEIN, JR., New York City: I shall mention four points: First, it is apparent that the selection of cases by the application of all of the diagnostic procedures now available may lead to a more rational use of therapy and to a higher percentage of favorable response to the therapy applied. Secondly, the exciting demonstration of the reversibility of some of the pathologic changes which have heretofore been considered as progressive and irreversible leads us to a much more cautious interpretation of the significance of testicular biopsies. May I emphasize again the importance of what I have spoken of as dynamic morphology rather than static morphology in the evaluation of results. Observations must be made over a long period of time. Third, another important point emerges from these studies. This has to do with the phenomenon which I would like to speak of as the "rebound phenomenon." In many physiologic processes there appears to be physiologic overreaction that follows in the wake of a change in function. Inhibition of hormone production, for

7 Vol. 1, No. 5, 1950] IMPROVEMENT IN SPERMATOGENESIS 421 example, appears to be followed by a phase of increased hormone production or release. These hormone alterations may possibly be utilized in therapy as Dr. Heller has suggested. The deliberate suppression of a hormone in order to obtain its subsequent release appears to me to be entirely rational therapy. Fourth, these studies also emphasize the importance of dosage in relation to therapy. Small doses and large doses of any agent may be very different-indeed opposite-in their effects. Thus, small doses of testosterone are needed to stimulate the tubules, while large doses appear to inhibit. The same type of response may occur with other agents. The need for more study of this phase is apparent. DR. JAMES WHITELAW, Phoenix, Arizona: All of us have been stimulated and excited by this exceptional demonstration of the reversibility of pathologic processes in the testicles. I shall show two slides from a patient treated for thirty days with 100 mg. of testosterone each day. One biopsy was taken on this patient previous to therapy; the other biopsy was taken about the thirty-fifth day after the first injection. This, of course, differs from Dr. Nelson's and Dr. Heller's cases because our period of stimulation was only thirty days. We have not yet taken a third biopsy on these patients. Our patients have been normal individuals, as far as they knew, except for infertility. The sperm counts have been followed in 2 cases without change but the time has not been as long as reported by Drs. Heller and Nelson. May I ask Dr. Heller and Dr. Nelson whether the 17-ketosteroids have been markedly reduced after the discontinuation of therapy? I emphasize Dr. Engle's suggestion that this may be a collagen disease and in addition to depressant action on the testicles there also may be a depressant action on the pituitary followed after withdrawal by a release of ACTH, FSH, and ICSH which may stimulate the testicles. Perhaps we could improve spermatogenesis by giving ACTH in small doses over a long period of time. DR. MAcLEoD: Dr. Engle, do you have any comments? DR. ENGLE: No. DR. WILLARD THOMPSON, Chicago: In the first place, I think the details of the interrelation between the Leydig cells and the seminiferous tubules are extremely. important. There appears to be an optimum concentration of androgen at which the seminiferous tubules function best. Apparently, they can function without much hormone because in rare instances we do observe eunuchoid individuals with a marked hormone deficiency who nevertheless have spermatazoa counts within normal limits. I am reminded of a patient that we had some years ago-a eunuchoid individual in whom the deficiency was secondary to a pituitary deficiency-who, during the administration of chorionic gonadotropin which stimulated his Leydig cells, developed enough spermatozoa to impregnate his wife, although he had none before. The observations of inhibitions of the testis with large doses of androgen and the recovery from the damage which results, are most interesting. Many years ago, Dr. Heckel, in Chicago, noted that in a man with a normal spermatozoa count the administration of large doses of androgen would cause azoospermia; but that when treatment was discontinued recovery took place

8 422 HELLER ET AL. [Fertility & Sterility and the spermatozoa count returned to normal. At that time (about twelve or fifteen years ago), Dr. Heckel did not correlate his observations with testicular biopsy. Neither did he at that time note that the spermatozoa count became better than it was originally. However, he has within the last two years, as Dr. Henderson pointed out, made observations similar to those of Drs. Heller and Nelson and their associates and there seems to be no doubt whatever about this striking recovery of the testis. Dr. Hurxthal, in Boston, some time ago noted that in eunuchoidal individuals with azoospermia the administration of testosterone was sometimes followed by the development of spermatogenesis. It would be interesting to know just what the mechanism is. Dn. CARL HELLER, Portland Oregon: I wish to point out that these results are hints. I don't believe they constitute definitive treatment in any way. I think it's bad therapy to give a patient testosterone at this particular stage of our knowledge before we know what kind of a testis will respond, what kind will recover, what kind will be depressed and stay depressed. Certainly the kind of case that Dr. Whitelaw described (apparently without gonadotropins) is not one that we would consider treating without further study. Such patients need stimulating therapy, and we have no good stimulating therapy. He was producing some sperm and to depress his sperm count to zero or to a very low figure for a year or longer doesn't seem wise to me.

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