Paper - A suggestion as to the cause of the aspermatic condition of the imperfectly descended testis (1922)

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Crew FA. A suggestion as to the cause of the aspermatic condition of the imperfectly descended testis. (1922) J Anat. 56: 98-106. PMID 17103947

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This historic 1922 paper by Crew is an early description of undescended testis and aspermia.

Crew FA. (1922). A Suggestion as to the Cause of the Aspermatic Condition of the Imperfectly Descended Testis. J. Anat. , 56, 98-106. PMID: 17103947

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A Suggestion as to the Cause of the Aspermatic Condition of the Imperfectly Descended Testis

By F. A. E. CREW, M.D., D.Sc.

  • Paper from the Animal Breeding Research Department, The University, Edinburgh.


In all Vertebrates the testes are developed in contact with the ventral surface of the kidneys, behind the peritoneum covering the body-cavity. In some they remain permanently in this situation, but it is characteristic of the majority of mammals that during the course of development they leave their primitive lodgment and migrate posteriorly and ventrally to the terminal periphery where they protrude at the surface of the body-wall. This protrusion constitutes the scrotum which varies in character from that of a pair of small ill-defined slightly elevated areas to that of a capacious, definite, pedunculated sac.

A survey of the Vertebrates will show that the testes in different cases are found in positions which mark the stages in a complete migration from the primitive position near the kidneys to the peripheral scrotum. It will also be seen that the scrotal situation of the testis is characteristic of the more impulsively active mammals. In the case of the human, in whom the migration has been most thoroughly studied, it provides a very complete example of the manner in which ontogeny repeats and condenses phylogeny in whole or in part.

There is much diversity of opinion as to the exact mechanism of the migration and it is probable therefore that not one but several factors are involved. The process possibly may be explained thus. Mechanical forces resulting from the changing methods of progression compelled the dense, compact, suspended testis to pass from the primitive position towards the inguinal region of the abdominal cavity (Woodland). There it naturally came to lie in the line of the lymph-sinuses described by Sabin. With increasing impulsiveness of movement and with increased intra-abdominal pressure consequent upon the development of the diaphragm, the testis was forced along the lymph-track so that it came to occupy a sub-integumental position in the groin (Bramann, Eberth, Keith). Here the testis found itself in a situation which in several ways was different from the interior of the abdomen and it was obliged to adapt itself to the new conditions. But, owing to its decreased mobility and to the injurious effects of active flexion of the thigh upon the abdomen, it suffered repeated attacks of inflammation. The local peritoneum with the mesorchium became involved in this inflammation with the result that adhesions and bands were produced. The overlying skin became thinned and stretched. Then further increase of impulsive activity and of intra-abdominal pressure produced a hernia of the testis. So the scrotum and the inguinal fold could have been produced. The position of the testis was equivalent to the sub-integumental one in the groin but the organ was now secure from injury by muscular movements since its mobility had been restored.

This process would be repeated in every generation until at last variation succeeded modification, or, by adaptation, the migration became incorporated in the life-processes of the individual and anticipated by the development of a mechanism which would produce the descent of the testis during foetal life.

“Originally, the descent of the testes did not occur until sexual maturity in all cases, but in many Mammalia (e.g. Marsupials, Ungulates, Carnivores, Primates), the process has gradually become shifted backwards ontogenetically to earlier periods, so that the formation of the scrotum takes place independently in the embryo in the form of the external genital folds.” WIEDERSHEIM.

In the modern mammals in which the migration occurs, the testis is united to a mammary area—supra-pubic, inguinal, perineal, or scrotal, at first by the inguinal fold and later by the gubernaculum—the canal-former, the guide of the testis—which is attached by its upper end to the Wolffian duct, the epididymis, and at the point where the globus minor and vas deferens meet, and by its lower end to the subcutaneous tissues in the groin, the scrotum, the root of the penis, and on the pubis.

The gubernaculum is an actively growing mass of fibro-muscular tissue which, starting from the muscular stratum in the mesorchium and inguinal fold in the inguinal fossa, invades the abdominal wall, every layer of which it carries with it as a prolongation within the scrotum. Upon the peritoneum thus drawn down the testis is dragged like a log upon a sledge. The gubernaculum forms the inguinal canal by the growth of its wedge-shaped end along the line of the lymph-sinuses, The canal is formed before the testis passes.

The final situation of the testis is decided in great part by the relative development of the different gubernacular insertions.

There is no physiological reason why the testis should not leave its primitive position. It does not stand in the same relation to the general economy of the individual as do the other organs of the body. It belongs to the race rather than to the individual, for though there cannot be an actual isolation yet there is distinctly an apartness of the germ-cells and the body is but the carrier of the testes. The migration to the periphery does not disturb the general economy for this reason and just as reproduction itself consists of a separating off of a portion of the organism so the organs of reproduction become separated, in consequence of their migration, from the viscera which belong entirely to the individual.

It is too difficult to conceive that the migration has imparted any advantage to the organism: the process bears no great relation to either advantage or disadvantage, though the scrotal position would appear to be one much exposed to danger, for the ease with which the scrotum is attacked and the devastating effects of contusion of the testes make of this region a veritable Achilles’ heel.

“...there remain many unsolved problems. Take, as an instance, the descent of the testis in the Mammalia. Neither direct nor indirect equilibration accounts for this. We cannot consider it an adaptive change, since there seems no way in which the production of sperm-cells, internally carried on in a bird, is made external by adjustment to the changed requirements of mammalian life. Nor can we ascribe it to the survival of the fittest; for it is incred- . ible that any mammal was over-advantaged in the struggle for life by this changed position of these organs. Contrariwise, the removal of them from a place of safety to a place of danger would seem to be negatived by natural selection. Nor can we regard the transposition as a concomitant of re-equilibration, since it can hardly be due to some change in the general physiological -balance.”” HERBERT SPENCER.

There certainly appears to be no compensatory physiological advantage _ offering benefits which outweigh the physical disadvantage and it would seem that the migration is, as suggested, but the inevitable concomitant of some other constant feature of the animal’s existence, and that it has not arisen in relation to ulterior ends.

A study of the conditions in which the testis fails to complete its migration will show that the testis has become so modified that while it will function perfectly when within the scrotum, it is incapable of producing spermatozoa when situated elsewhere. This would indicate that the conditions within the scrotum are different from those of the interior of the abdominal cavity.

“The descent of that testicle is very slow which is not complete before birth, often requiring years for that purpose; and it sometimes never reaches the scrotum, especially the lower part of it. There is oftener, I believe, an inequality in the situation of the two testicles than is commonly imagined; and I am of the opinion that the lowest is the more vigorous, having taken the lead readily, and come to its place at once.

“It is not easy to ascertain the cause of this failure in the descent of the testicle; but I am inclined to suspect that the fault originates in the testicles themselves. This, however, is certain, that the testicle, which has completed its descent is the largest, which is more evident in the quadruped than in the human subject; as in these we can have the opportunity of examining the parts when we please, and can determine how small in comparison with the other that testicle is which has exceeded the usual time of coming down; it never descends so low as the other.

“When one or both testicles remain through life in the belly, I believe that they are exceedingly imperfect, and probably incapable of performing their natural function, and that this imperfection prevents the disposition for descent from taking place.” Joun HuntTER.

Arrest of descent is commonly regarded as a symptom of arrest of testicular development. John Hunter regarded arrested descent of the testicle as due to an imperfection in its development; all recent observations support his opinion.” KErrH. *

“It is commonly believed that the imperfection of an undescended testicle is due to its failure to reach the scrotum. This I believe to be an error. An undescended testis fails to reach the scrotum because of its imperfection.” Bianb-SuTTON.

In spite of the great weight of these opinions it is difficult to accept them without question since it is generally understood that the testis plays but a passive réle in the migratory process. Imperfection of the local peritoneum during the development of the inguinal fold and mesorchium; of the gubernaculum; of the inguinal canal; or of the scrotum, these conditions also must lead to imperfect descent.

The long mesorchium may allow the testis to hang too freely in the abdominal cavity; there may be a deficiency or abnormality of the upper attachment of the gubernaculum; intra-uterine peritonitis may have caused adhesions which limit the mobility of the testis; shortness of the vas deferens and of the blood-vessels, though more likely to be an effect, may also be a cause of imperfect descent; the inguinal canal may be imperfectly formed or the scrotum ill-developed so that passage thereinto may be hindered. Overaction of the cremaster may be another possible cause, for in infants and children _ the action of this muscle occasionally draws the testicle up even beyond the external ring. Murard records a case in which the testis periodically disappeared into the abdominal cavity.

Imperfection of the testis most certainly can be a potent cause of its non-descent, but unless it is of such a size or of such a shape that it cannot pass along the passage prepared for it, surely the fault must lie with the powers, or with the passage, but not with the passenger.

“It is certain that in the majority of cases the imperfectly or abnormally descended testicle is functionless, at any rate as regards spermatogenesis. But though the function of spermatogenesis is absent, that of producing the internal secretion necessary for the development of the secondary sexual characters of the male is generally, but not always, carried out. That the function of spermatogenesis is lost is shown by the fact that such persons are unable to beget offspring and is also confirmed by the histological examination of retained testes after removal.

“In rare cases the spermatogenetic function is not lost, even when there is a double imperfect descent with very small testes, or when both organs are arrested within the abdominal cavity; this has been proved both by the presence of normal tubules and active spermatozoa, and also by the fact that these persons have proved capable of procreation. Many examples of this are recorded in medical literature. There is, however, evidence that those in which spermatogenesis is normally carried out are young men mostly under thirty years of age. In men over this age the imperfectly descended testis is nearly always functionless. In the majority of cases under thirty the spermatogenetie function is absent and the proportion of functional organs is probably small.”” Turner, P.

“ After careful observations extending over many years I only once found spermatozoa in an undescended testis.”

“It is not rare to find spermatozoa in testicles which have remained in the lower part of the inguinal canal, but in those in the upper part, and in those taken from the abdomen, this is exceptional.’’ Hoppay.

“In mammals the testes fail at times to pass through the inguinal canal, and, in consequence of their retention in the body-cavity, the germ-cells fail to develop. On the other hand, the interstitial cells of the testis develop normally. Cryptorchid individuals show the normal secondary sexual characters of their species.”” Morecan.

M’Fadyean, who examined a series of twenty-five imperfectly descended testes for Hobday, found that out of fourteen from the abdominal cavity, only two contained spermatozoa, and that.of eleven from the inguinal canal— three being from the upper part—only five were capable of functioning. Gurlt failed to find spermatozoa in testes removed from the abdomen; Wesche found that testes from.the inguinal canal were capable of producing functional spermatozoa; Paugoué records the case of a stallion in which both testes were undescended yet who sired many colts of which, however, five suffered from the same condition; Dollar states the opinion that testes retained within the abdomen contain degenerate spermatozoa or none at all.

As a result of the examination of a series of imperfectly descended testes from the horse, placed at my disposal by the courtesy of Mr Wm. Brown of the Veterinary Department, Marischal College, I am able to demonstrate the fact that the nearer the testis comes to lie to the normal scrotal position, the more likely it is that functional spermatozoa will be found therein. Testes removed from the lower part of the inguinal canal, though smaller in size than the normal and inclined to be of an unusual shape, are in the majority of cases imperfectly functional; testes removed from the abdominal cavity, so far as my experience goes, are invariably the seat of tumour growth, benign or malignant, even in the case of two-year old horses; testes removed from the upper part of the canal are usually atrophic and normal spermatozoa can be found therein only very exceptionally.

Russell Howard records that of twenty-seven cases of malignant disease of the testis, nine had occurred in imperfectly descended glands.

It would seem that when the testis occupies its normal position in the scrotum, the conditions are such that the activities of the other component tissues of the gland are restrained by the dominating activity of the germinal epithelium, but that when the testis is brought to rest in an abnormal situation, the function of spermatogenesis being in abeyance, the other tissues of the gonad take on an uncontrolled growth.

Griffiths, in an experimental investigation on dogs, found that when the testes of the puppy were replaced within the abdominal cavity they developed normally up to the time of puberty but that they never produced spermatozoa, . and that when the testes of grown dogs were similarly replaced within the abdomen they invariably atrophied and never remained functional.

In those mammals in which the testis periodically passes into a scrotum during the breeding period, it is found that they are spermatic only when in the scrotum, and aspermatic when within the abdomen.

To explain the relation between imperfect descent and imperfect functioning there are two theories: one, that the imperfection in functioning is the cause of the imperfect descent, the other, that it is the result. The first postulates that there is some abnormality of the germinal epithelium which prevents the normal development and migration. If this is so, then obviously no operative treatment can possibly restore the spermatogenic function. The second explanation is that full growth and development of the testis up to the time of puberty is possible in an abnormal situation, but that at the time when the final stages of spermatogenesis should occur, the abnormal situation reacts upon the testis in some way so that these stages cannot occur and atrophy of the testis ensues while various pathological processes easily attack the gland leading to degeneration and tumour growth. Ifthe fault lies with the situation and not with the testis, if the absence of the spermatogenic function is the result of the malposition, then the operation of Orchidopexy should restore this function. It may be accepted that if an immature imperfectly descended testis is secured within the scrotum without operative injury it will complete its development and function normally.

But if the final stages of spermatogenesis are effected in one situation, the scrotum, and not in another, the abdominal cavity, there must exist some great difference between these two situations.

Such a difference does exist. It is that the temperature within the tunica vaginalis is appreciably lower than that within the general abdominal cavity.

It was known to John Hunter that the temperature of the body is not the same throughout; he demonstrated this fact by several most ingenious experiments on mice and dogs. But more recently, and with much more critical methods, Benedict and Slack have shown that there is a temperature gradient of some 5° C, between the temperature of the abdominal cavity and that of the surface of the body. The temperature rises in proportion to the depth to which the thermometer is inserted until at 6-8 cms. a constant temperature is reached.

The testis within the scrotum is not exposed to the same temperature as that of the primitive position within the abdomen. Moreover, a consideration of the peculiar structure of the scrotum will show that this is a very specialised area of body surface extremely well equipped with a mechanism for local temperature-regulation.

The scrotum is a pouch composed of skin and the dartos tunic. It is divided on its surface by a median raphe into two lateral portions. The skin is very thin, of a brownish colour, and is usually thrown into rugae. It is well supplied with sebaceous follicles, the secretion of which has a peculiar odour, and is beset with thinly scattered crisp hairs, the roots of which are visible through the skin.

The dartos tunic is a thin layer of non-striated muscle, continuous around the base of the scrotum with the two layers of superficial fascia of the groin and of the perineum. It sends inwards a septum which extends between the median raphe and the under surface of the penis, as far as its root, and divides the scrotum into two cavities for the testes. It is closely applied to the skin externally and is connected with the subjacent parts by a delicate areolar tissue upon which it glides with the greatest facility. There is no fat in this areolar tissue; the scrotum is fat-free even in the fattest of entire animals. But in the castrate the scrotum is loaded with fat and the butcher’s test for prime beasts is the amount of fat in the scrotum.

Klaatsch has shown that in many mammals the site of the future scrotum is marked out by a certain area of skin, evident both by its naked-eye and microscopic characters. White and Martin state that in cases of ectopy in which, owing to an over-development of an insertion of the gubernaculum other than the usual, the testis comes to occupy a position beneath the skin of the perineum, the overlying skin assumes the peculiar characters of that of the scrotum.

The appearance of the scrotum varies with different conditions of atmospheric temperature. Under the influence of warmth, and in the debilitated and old, it is elongated and flaccid; under the influence of cold, and in the young and robust, it is short, corrugated, and closely applied to the testes. The amount of surface exposed is controlled by the action of the dartos. |

The scrotum stands well away from the body and is in an area where transpiration is well marked. The temperature within it is not only considerably lower than that within the general cavity but its regulation is controlled by a most efficient mechanism.

That the scrotum itself, by reason of its specialised structure, is concerned in the functioning of the testis is shown by the results of certain diseases in which the scrotal integument becomes very much thickened and inelastic, as in Elephantiasis arabum, for the testes become deformed and atrophied. The testis within such a scrotum is in a situation equivalent in many ways to the interior of the abdominal cavity.

John Hunter, Ashworth, Child, Marshall, Reamur, Semper, Graham Kerr, Bles, Spallanzani, Meek, Turner, C. L., and many others have produced considerable evidence which goes to show that reproductive activity is intimately related to external temperature in the case of the lower orders. In the fish, for example, it has been shown that the beginning of the annual decline in temperature is contemporaneous with the seasonal volumetric increase in the testes of the Perch, and that the beginning of the seasonal decrease in the testes is contemporaneous with the beginning of the seasonal rise in the temperature. It can be accepted that growth and reproduction vary in length and periodicity with temperature and though, undoubtedly, other factors also are concerned, it is sufficient to recognise that temperature itself is a factor.

In the case of the testiconda it is possible that some of the pharyngeal derivatives, such as the thymus, the function of which is not definitely known, control the activities of the testes throughout the individual’s whole lifetime, whereas in the case of the mammals whose testes normally migrate to the scrotal position, the action of the internal secretion of this gland has become restricted to inhibiting the too active development of the testis up to the time of puberty, when the body is sufficiently grown so that it can entertain the demands of spermatogenesis. The thymus is so situated that it can readily appreciate changes in the environmental temperature and its intimate association with the activities of the testes is acknowledged. In the case of the scrotal testis, the situation is such that the optimum temperature for spermatogenesis can be maintained throughout the year because of the development of the local temperature-regulating mechanism. The thymus becomes unnecessary after puberty and consequently atrophies.

But be it as it may, the fact remains that the testes of the testiconda, and of the other Vertebrates in which their normal position is abdominal, have never been required to adapt themselves to function in a situation in which the local temperature is markedly different to that of the general abdominal cavity. This also applies to the ovaries of all the Vertebrates. They are so organised as to function quite satisfactorily in an intra-abdominal situation, and so far as can be ascertained, should an ovary come to occupy an ectopic position, it does not produce functional ova. This great distinction between ovary and testis in the case of the higher mammals has a very direct bearing upon the question of hermaphroditism in the human and renders the postnatal reversal of the sex-organisation, such as occurs in the case of the Amphibians, for example, utterly impossible.

Since the capacity for functioning within a scrotum has been of the nature of an adaptation, it is not extraordinary that exceptionally an imperfectly descended testis should produce functional spermatozoa,


1. In the more impulsively active mammals the testis leaves its primitive position to pass into the scrotum. The process of migration has been shifted back ontogenetically so that now the formation of the inguinal canal and of the scrotum occurs in anticipation of the descent of the testis. The process bears no great relation to either advantage or disadvantage; it is but the inevitable concomitant of other ‘constant features of the animal’s existence and has not arisen in relation to ulterior ends. ,

2. The testis has become adapted to function in a situation, the conditions of which are markedly different from those of the general abdominal cavity. It can no longer function in the primitive position. The great difference between the two situations is one of temperature. The temperature within the tunica vaginalis is considerably lower than that within the abdomen. The scrotum is so constructed that it is exceedingly well equipped with a temperatureregulating mechanism. The final stages of spermatogenesis occur at a certain optimum temperature which is that within the scrotum and not that within the abdominal cavity.

3. The imperfectly descended testis is aspermatic because the temperature of the abnormal position is not that at which the final stages of spermatogenesis occur,




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