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The effect of male hormone upon the descent of the testes.

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THE EFFECT O F MALE HORIRIONE UPON THE
DESC'EXT O F THE TESTES
JAMES X. HAMILTON
Depclrt)we)Lt of A?iufonly, Yale Uniltcrsrty ArltooE of M d i c i l z e , arid Departinent of
A n a t o m y and Physiology, Albany Xcdical College
o m PLATE (FIVE FIGURES)
Xale hornioiie substances arc known to affect the growth,
maintenance and function of the male accessory organs of reproduction and secondary sexual characteristics. These hormones a r e also capable of maintaining syermatogenesis
(llTalsh, Cuyler and McCullagh, '34 ; Nelson and Gallagher,
'36 ; IIamilton, '36) and of influencing crpptoi*chid testicles
(Hamilton and Leonard, ' 3 7 ) in the hypophysectomized rat.
Tlie present paper presents evidence that iiiale liorniones a r e
also implicated in the phenomenon of testicular descent.
Although sterility lias been long recognized as a sequel of
cryptorchidism, the sigiiificaiice and necessity of the sei~otum
as a thermoregulator f o r spermatogenesis was not appreciated until after the illuminating esperirnents by Noore and
co-workers ('32). Shapiro ( ' 3 0 ) in humans a n d Engle ('32)
in moiikeys demonstrated that anterior pituitary-like hormones were able t o induce testicular descent, a lead that has
heen followed by many clinical investigators (Goldman and
Stern, '33 ; hberle arid Jenkins, '34 ; Werner, Kelling, Ellersieck and Johns, '36). The data of the present paper show'
that male hormone substance is an agent actually respousible
f o r growth processes of the reproduetke organs w-liicli result
in descent of the testes, and indicate that descent of retained
testes obtained hy anterior pituitary-like substances may be
due in part at least to the procluction of male hormone
substance.
'Aided bv grants from the Committee on Scientific Research of the American
Medic a1 Association and the International Cancer Research Foiiiidation.
533
T l l E A N A T O N I C 4 L IILCORU, \UI.
70. NO. 5
MATERIAL A S D METHODS
As described by n'islocki ( ' 3 5 ) arid utilized 1))- Engle ( '32)
and others, the immature monkey, IbIacaeus rhesus, exhibits a
cryptorchid condition from soon after birth until the onset of
maturity, &ich is at the age of 4 to 5 years. T ~ U Sthe
,
macaque between the age of 1to 3 years and under 3 kg. body
weight affords a naturally-occurring state of cryptorchidism
upon which to test the efficacy of substances purported to
cause tcsticular descent.
Twelve monkeys mere given injections of testosterone acctate or testosterone propionate2 in dosages of 1, 2, 3, 5 or
15 mg. Trial was made of the effect of varying the frequency
of injections from two to seven times weekly. One cubic
centimeter of peanut oil was used a s a standard vehicle, since
the type and amount of oil influences the absorption of the
hormone (Parkes, '36).
Six monkeys were kept as controls, receiving the same
dose of the oil vehicle a t the intervals of atlininistration
employed in the experimental animals. The testes of one of
these monkeys were zlmost completely descended, although
the animal weighed only 2.8 kg. and had not received injections. The testes of the other five animals were as those of
the experimental animals previous to injection (figs. 1 and 2 )
in that they rested about 4 to 6 em. abovc the scrotum. CTpoii
palpation they could be moved with ease 1 or 2 em. caidally
but returned spontaneously t o a high cryptorchid site after
palpation was complcted. The scrota were flat, small and
iinpouchetl (figs. 1and 2).
O K 8 ERVA7'TONS
1. Desceiit of t e s t ~ s . In all hut one of the eight monkeys
which received doses of 5 mg. or more descent of the testes
occurred within 3 wecks of treatment, usually about the fifteenth day after the beginning of treatment in thosc animals
which received daily injections (figs. 3, 4 and 5). Four
* Testosterone acetate a i d testosterone propionate under t h e trade name
Peraiidrrii were f ornished through the courtesy of the C'ibn C'oinpaiiy.
ANDROGENS A N D TESTICULAR DESCENT
535
animals which received 1 to 3 mg. doses twice weekly showed
partial or no descent in 60 days. These doses mliich mere
insufficient to cause descent were also ineffective in producing
the nasal changes of swelling and coiigestion i n the area of the
upper turbinate. Increase of the dose to 15 ma. administered at the same interval (twice weekly) procluced descent in all four animals within 3 weeks and was accompanied
by pronounced nasal changes (Nortimer, Wright and Collip,
'36 a and b ; Hamilton, '37 c).
Injections of 5 mg. and 15 mg. respectively were continued
in three monkeys f o r 100 days. The testes remained in descent
and the animals showed continued response to the androgenic
material i n the form of growth, maintenance and function
of the accessory reproductive organs. This included a
tendency toward a penile erection (Hamilton, '37 b).
When an animal was frightened the testes were on occasion
retracted from the scrotum, but were returned when the
animal relaxed o r sat upon his haunches. I n two monkeys
which were not sacrificed a t the end of the period of injections,
the testes reapproached but never quite reached the original
cryptorchid condition. A second series of injections with
androgenic substance residted in a more rapid lowering of the
testes than in animals which had not previously received
injections.
2. Growth of accessory structures. Preceding the descent
there was enlargement of the prostate, seminal vesicles, penis,
cord elements, and scrotum. The length of the inguineal structures enclosed by the cremaster muscles was 2 to 5 em. in
the unin,jecled moiikeps, 5 to 7 em. in injected animals. Gross
enlargement and hyperplasia of the cremaster muscle, vas
deferens, epidiclymis aiid attendant blood vessels were similar
to, but of somewhat slighter degree than, the growth of these
structures depicted after administration of anterior pitujtary
extracts (Deming, '36). The scrotum was usually transformed from a flat transverse band into a bilobed sac more
pouched, dependent aiid rugose. The raphe became red and
prominent. Sometimes the scrotum contained a small amount
536
JAMES B. HSMILTON
of mucoid-like matter, but the edema and mucoid-like material
never resulted in an approach to the great degree of scrota1
swelling observed after administration of pitutary extracts
(Engle, '32). Nevertheless, the more caudal position of the
testes, their retainment in the scrotum, and the elongation of
the inguinal structures, all o€ which followed androgenic injections, are interpreted by the author as evidence of testicular
descent. Further indication of an effect of androgens on descent was in the lowering of testes mlieri injections were given,
c~levatioaof the testes when injections were stopped and descent again when administration was begun once more,
DISCUSSIOK
Although an understanding of the embryological processes
involved in the normally-occurring descent of the testes is
necessary for an appreciation of the influence of male hormones upon testicular descent, such discussions must he left
to other sources save to state that these processes can be
hormonally influencecl and even the processus vaginalis a€fected (Burrows, '36).
Testicular retention can be charged to mechanical, physiological and hormonal cmses. Under mechanical may be listed
such factors as adhesions, obstructions, strictures of the abdominal rings and faulty guberiiacular attachments. t'hpsiologically, reflex contraction of the cremasteric muscle is capable of intermittently returning llie testis through a patent
external ring into the inguinal canal, where secondary retention may take place arid rnasqneracle as organic cryptorchidism. Under hormonal causes may be considered hypodeveloprrieiit 1) of cord structures and accompanying blood vessels
(plus in the monkey at least, the creniaster muscle) which are
of insnfficient length to permit lowwing of the testes to a
scrotal site, and 2) of the scrotal sac mliich map be so rudimentary as to afford little pocket to liold the testes. Surgeons
are agreed that underdevelopment of iriguiiial strncturcs and
scrotum oEers the two chief difficulties to successful orcltiopesy ;lieiicc it is significant that this underdevelopment may be
AXDROGENS A N D TESTICULAR DESCENT
537
treated hormonally either by pregnancy urine extracts
(Shapiro, '30) or by inale liormone substance. Presumably the
pregnancy urine extracts act in part by stimulating the testes
to produce male hormone substaiiccs or their prccursors whicli
can be agents at least iii part actually responsible for testicular descent (Hamilton, '3'7 a ) . Advantages of synthetic male
hormone substances ovcr anterior pituitary-like material
(pregnancy urine extracts) have been described briefly elsewhere (Hamilton, '37 b). Evaluation of androgenic substances in humans will be reported in the near future, but it
should be remembered that critical study (Thompson et al.,
'37) of the descent obtained by gonadotropic substance revealed less than one-fourth of truly cryptorchid cases responded to endocrine treatment. I t would seem optimistic to
expect any high percentage of descent with androgenic substance ; presumably mechanical causes account for a large
number of cryptorchid cases and androgenic material should
be expected t o induce descent only where hormonal and
perhaps physiological factors are at fault. Further, it is necessary that caution be used in the selection of human cryptorchidic cases, for spastic retraction of the testicle o r false
cryptorchidism forms a large percentage of the cases diagnosed as cryptorcliid (Hamilton and Hubert,, ' 3 7 ) . Of the first
sixteen patients referred by pediatricians to the author, ten
were but cases of spastic retraction. Surgery, Iiormonal
treatment 01- merely waiting until tomorrow might effectively
produce clcscent. One wonders horn much of the success of
some methods has been in part due to the use of these cases,
as when a testis has been said to descend within 3 hours after
hormonal treatment (Harris, '35). I t .c~-ouldseem well to
use special means (Hamilton and Hubert, ' 3 i ) to differentiate
true from pseudo-cryptorchidism, altliough i n the few cases
o f intermittent retention >t udied by the author, androgenic
substance lias been also found of value in that retraction is
minimized o r prevented following treatment.
538
JAMES 33. .HAMILTON
Thus, the administration of hormone substances to the
young cryptorchid child to produce a n early and a n acceiituated ‘pubertal state’ may prove of value 1) in producing nonoperative descent i n some cases (especially such as those of
hypopituitarism where endocrine stimulation has been lacking) and i n avoiding waiting until puberty to ascertain
whether or not spontaneous descent may occur 2 ) i n selecting
for early operation those cases where descent is prevented
because of mechanical or other factors; thus, hernia, malignancy, testicular atrophy, pain, anxiety, and other conditions
possibly attendant upon cryptorchidism may be minimized ;
and 3 ) in aiding surgery pre- and post-operatively in the dcvelopment of the cord elements and scrotum.
SUM XARY
1. Cryptorchid testes of the irnmature macaque have been
observed to descend into the scrotum following adequate administration of the male hormones, testosterone acetate and
testosterone propionate. There is less edema and scrota1
swelling than in descent produced by gonadotropic substance.
2. Processes coilsidered largely responsible in the production of this descent a r e 1) growth and elongation of cord
elements and 2 ) slight development of the scrotum to form
more of a pouch for retainment of the testes.
3. It is suggested that descent produced by anterior pituitary-like substances may be i n part due to stirnulation of the
secretion of male hormone snbstances.
4. Hormone treatment may be of value in a ) prodiicing
descent i n certain cryptorchid cases, b) authorizing surgery
at ail early age instead of waiting until puberty to see if
spontaneous descent might occur ; thus, some of the objectionable phenomena attendant upon cryptorchidism may possibly
be avoided, and c ) aiding surgery prc-operatively by the development of cord structures and post-operatively by preventing retraction and tension.
ATXDROGENS AKL) TESTICULAR DESCEST
539
L I T E R A T U R E CITED
ADERLE,S. B., A N D R. H. JFNKINS
1934 TJndescendcd testes in ma11 and rhesuq
monkeys. J. Bm. Med. Assoc., vol. 103, pp. 314-318.
BURROWL,
H. 1936 Influence of oestrogenic compounds i n causing hernia and
descent of testis in mice. Brit. J. Surg., vol. 23, pp. 658-661.
DEMIKG,C. L. 1936 The gonadotropic factor as a n aid t o surgery in the treat
ment of the undescended testicle. d. Urol., vol. 36, pp. 274-285.
ENGLE,5:. T. 1932 Experimentally indured descent of testis of Macacus monkey
by hormones from the anterior pituitary and pregnancy urine : the role
of gonadokinetic hormones in yregnanry blood in the normal dcseent
of the testis in man. EndOcrindogp, vol. 16, pp. 513-520.
GOLDMAN,
A., AND A. STERN1933 Treatment of nndescendcd testes b y injection of prolan. New York State a. Med., vol. 33, pp. 1095-1096.
~IaafrLToh-,J. 13. 1936 Endocrine control of the scrotum and a ‘sexual skiti’
in the male rat. Exp. Biol. and &Id.,
vol. 35, pp. 386-38i.
1937 a Production of testicular descent in monkeys by inale honnoue
substancc. Am. J. Physiol., vol. 119, p. 325.
_.___1937 b
Induction of penile erection by male hormone substances.
Endocrinology, vol. 21, pp. $44-749.
_____ 1937c Changes i n nasal mucosa of monkejs (Macaca rhesi) and
humans by inalc hormone substances. Proc. Soc. Exp. Biol. and &fed.,
VOI. 37, pp. 36F-369.
HAXILTON,
J. B., AND G. IIUDERT
1937 Diffcrential diagnosis of pseudorrpp
torchidism and t i u e rryptorchidisni. Eiidorrinology, vol. 21, pp.
644-648.
HAMILTON,
J . R . , AND S. L. LEONAXD
1938 The effect of male liornione sub
stance upon thc testes and upon spermatogenesis. ( I n press.)
HARRIS,
F. 1. 1935 Treatment of undescended testicle. Am. J. Surg., to]. 27.
pp. 447-454.
MOORE,C. R. 1932 Se, and Intc~rnal Secretions. Edited hy F:. Allen. The
Williams and Wilkins Company, Baltimore.
MORTIMER,II., R. P. WRIGHTAND J. K. C 0 L r . r ~ 1 9 3 6 a The effect of the administration of estrogenic hormones on t h e nasal Inucosa of the monkey
Maraca mulatta). Canad. Mcd. Assoc. J., vol. 35, pp. 503-513.
I936 h The effect of oevtrogcnic hormones on the nasal niurosa;
their role in the naso-sexual relationship, and their sigiiificanre in
clinical rhinology. Canad. Med. Assnc. J., vol. 35, pp. 615-621.
NELSON,W. O., AND T. F. GALLAGIIER1936 Some effects of nndrogenir substances in the rat. Science. vol. 84, pp. 2:$0-232.
PARIZES,A. S. 1936 Increasing the cffcctiveness of testosterone. Tmicet, vol. 2,
pp. 674-676.
SHAPIRO,
6. 1930 Knnn man init Hvpophgscnvorrlerlappen den unterentwirkelten
mZnnlichen Genitalapparat brim Menschen ziim Wachstum anregen f
Deutache med. Wrhnschr., vol. 56, pp. 1605-1607.
TIIOMPSON, w. o., A. D. BEVAN,H. J. HFCKEL,
E. R. MCCBRTHY AND P. I<.
THOMPSON 1937 Treatment of undescendecl testes with anterior
pituitarv-like substances. Endocrinologv, vol. 21, pp. 220-229.
540
JAMES B. I-IAMILTOX’
WALSH, E. L., W. K. CUYLERAND D. R. MCCFLLAOII1934 The physiologic
maintenance of thc rriale sex glands. A m . J. Physiol., vol. 107, pp.
508-512.
WEBXER,-4.A., D. KELLINC;,
D. ELLERSIECX
AXD G. A. JOHNS
1936 Effcet
of gonadotropic extract of tlie pituitary in cryptorchidism. J. Am.
Ned. Assoc., v-ol. 106, pp. 1541-1643.
WISLOCKI,
C;. B. 1935 Ohservations on the descent of the testes in the macaque
and in the chimpanzee. Anat. Rec., vol. 5 7 , pp. 133-148.
PLATE 1
EXPLA4WAPION OF FIQURES
1 Flat, empty scrotum and cryptorchid condition of a n immature untreated
macaque of 3.0 kg.
2 Ventral view of cryptorchid condition in an immature untrc.atcd macaque of
0.3 kg. S o t e the testes lie i n a high inguinal position on either side of the
pointer.
3 Testkular position of testes following trcatment of an 1.8 kg. macaque
with daily injections of 15 mg. of testosterone propionate i n peanut oil for
25 days. The penis and scrotum show de~elopmentand adult characteristics. Note
the glans penis and scrotal rugae. The raphe has beeoiiie red.
4 l k s c e n d d testes of 1.7 kg. animal which received 5 mg. of testosterone
propionate f o r 40 days. Notc the enlarged scrotum. The bulging lying lateral
t o each side of the penis is the eremaster muscle ensheathing tlie elements of the
cord. Note developmeut of the penis and frenulum, the latter and the scrotal
raphe being red-pink in color.
5 Rear view; 1.9 kg. androgen-injected monkey, illustrating pendulous scrotum
and the testes contained with the scrotum. The androgen dosage was 5 nig. of
tesosterone acetate daily for 40 days.
t'l'.\'I"
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