Proliferative Lesions of Serous Membranes in Ovariectomised Female and Entire Male Dogs After Stilboestrol Administration

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1 Vet. Path. 8: (1971) Proliferative Lesions of Serous Membranes in Ovariectomised Female and Entire Male Dogs After Stilboestrol Administration J.D. O SHEA and ANNE G. JABARA Departments of Veterinary Preclinical Sciences and Veterinary Paraclinical Sciences, University of Melbourne, Melbourne, Vic. Abstract. It was shown previously that ovarian tumours, which frequently metastasise to serous surfaces, can be produced in dogs by prolonged administration of stilboestrol. The ability of non-ovarian serous surfaces to proliferate in response to stilboestrol, independently of ovarian metastases, was studied in 5 ovariectomised females and 4 entire males. Papillary proliferations occurred on the uterine serosae in 3 females and on the testicular and epididymal serosae in 2 males. In no case was there papillary proliferation on serous membranes of non-genital organs. One of 2 entire females given stillboestrol had proliferations regarded as metastases of ovarian origin on non-genital serous membranes. It is concluded that, in addition to ovarian changes, stilboestrol can cause primary proliferative lesions in the serous membranes of certain genital organs in both sexes. There is no evidence that serous membranes of non-genital organs be capable of a primary proliferative response to stilboestrol. JABARA [I, 21 found that ovarian tumours could be produced in dogs by the prolonged administration of stilboestrol. Proliferative lesions of similar structure found on other serous surfaces and in lymph nodes of many of these dogs were regarded as metastases of ovarian origin. This interpretation was supported in a subsequent study by O SHEA and JABARA [6] in which histochemical methods for much were used as an aid to determine the histogenesis of the ovarian tumours. MAWDESLEY-THOMAS and SORTWELL [4] observed extensive serosal proliferations on the uterus and mesometrium in dogs given high doses of synthetic oestrogens over long periods. These proliferations, which resembled histologically those previously observed by JABARA [1, 21, developed in the

2 82 ushea/jabara absence of any evidence of ovarian malignancy. MAWDESLEY-THOMAS and SORTWELL [4] believed the uterine lesions they described were derived directly from the uterine serosa and were not metastases from the ovary. No lesion was reported on any other, non-genital, serous membrane. This report led us to reconsider the possibility that other non-ovarian serosal proliferations, previously regarded as ovarian metastases [ 1, 2, 61, might also have been independent primary responses to stilboestrol administration. The ability of non-ovarian serous surfaces to proliferate in response to oestrogens, independently of ovarian metastasis, is most readily studied in dogs without ovaries. This paper reports effects of prolonged stilboestrol administration in ovariectomised female dogs and some observations on the effects of this hormone on a group of male dogs, details of which were reported previously [3]. Materials and Methods Seven bitches, 5 of which were bilaterally ovariectomised 3 to 6 weeks before the first injection of stilboestrol, were used in this experiment (table I). Stilboestrol was injected subcutaneously at 8-week intervals via a Vet-Jecta gun 1. The stilboestrol was dissolved at a level of 71.4 mg/ml in a polyethylene glycol base1 to provide a slowly absorbed depot. The rate of dosing per 8 weeks was initially 60 mg stilboestrol for dogs weighing up to 20 kg, and 75 mg for dogs over 20 kg. Twenty-four weeks after commencement of the experiment the doses were raised, because of the relative lack of external evidence of hyperoestrogenism, to: t20 kg - 75 mg; 20 to 25 kg - 90 mg; 25 to 30 kg mg; >30 kg mg stilboestrol. Total amounts of stilboestrol given to individual dogs ranged from 180 to 570 mg (table I). It was originally intended to administer stilboestrol over a period of 48 weeks (7 injections per dog), but 4 dogs were destroyed earlier than this for various reasons (table I). All dogs were destroyed by intravenous injection of pentobarbitone sodium. At autopsy, confirmation of the completeness of ovariectomy was obtained, and particular attention was paid to the examination of serous surfaces in the abdominal and thoracic cavities. Tissues for histological examination were fixed in 10% form01 salineand in Born s fluid, and paraffin sections were stained with haematoxylin and eosin (HE) or the colloidal iron (CI) method [5] for acid mucopolysaccharides. Tissues routinely collected for histological examination were from uterus (multiple blocks from horns and cervical region), broad ligament, vagina, kidney, urinary bladder, urethra, liver, spleen, intestine, diaphragm, and lymph nodes (including internal iliac and mesenteric nodes). Other tissues with gross changes suggestive of abnormality were also examined histologically. In addition, histological sections of uteri from 15 normal bitches aged 1 to 4 years were examined for evidence of serosal papillary formation. 1 E.R.Squibb & Sons, Noble Park, Victoria.

3 Stilboestrol and Serous Membrane Lesions in Dogs 83 Table I. Details of individual female dogs given stilboestrol Dog Breed Age at Weight Duration Total Reason for No. first range of amount of euthanasia injection of during experiment, stilboestrol stilboestrol, experiment, days received, months kg mg 1 Golden labrador to Injuries from fighting 2 Golden labrador to End of experiment 3 XGolden labrador to End of experiment 4 X-bred1 approx to End of experiment 5 X-bred1 approx to Troublesome disposition 6 Golden to Cystitis and labrador pyometra 7 Golden labrador to Pyometra and lams ness r. hind leg 1 Bilaterally ovariectomised bitches Entire bitches Histological sections from 4 stilboestrol-treated male dogs previously described under thereferencenumbers D/PM 17, 19,37, and 47 [3] were also examined. The tissues examined were from testis and epididymis, kidney, urinary bladder, ureter, stomach, intestine, pancreas, liver, spleen, lung, heart, and lymph nodes. At the start of stilboestroladministration, these dogs were 4 months to 3 years old, and they received 300 to 750 mg stilboestrol over a period of 262 to 578 days. Results Entire Females Both animals had ovarian lesions, which were more marked in dog 7. These lesions (fig. 1) were confined to the surface of the ovary and consisted of papillary outgrowths with connective tissue cores as previously described [6]. There was no recently formed corpus luteum or large antral follicle in

4 these ovaries but there were many apparently normal primary, secondary, and early antral follicles. CI staining revealed superficial, intraluminal, and intracellular distribution of material containing acid mucopolysaccharide similar to that previously described [6]. The uterine serosal surface in both animals had focal areas of papillae accompanied by an increase in the height of the serosal cells (fig. 5, 6). The papillae were generally small and possessed cores of fibrous connective tissue continuous with that underlying the neighbouring mesothelium. The appearance of these small papillae was suggestive of a direct proliferation of the uterine mesothelium and subjacent connective tissue. In addition, a few examples of larger, more complex, papillary lesions containing epithelial cell groups and psammoma bodies [l] were on the uterus of dog 7. CIpositive material was on the surfaces of the epithelium covering the papillae, within the lumina of hollow cell groups, and within large and small vacuoles in individual serosal cells (fig. 6). In dog 6 there was a single small cluster of epithelial cells below the uterine serosa, apparently lying within a small lymphatic vessel. The remaining serous surfaces in dog 6 appeared normal, macroscopically and histologically. However, in dog 7 lesions were widespread on serous surfaces throughout the abdominal cavity. These lesions involved focal areas of the surface of the body wall, diaphragm, liver, gall bladder, mesentery, broad ligament, uterus, spleen, and rectum. They appeared grossly as yellowish or whitish thickened and roughened areas of the affected surfaces and were frequently the sites of adhesion between neighbouring viscera. Many of these lesions were accompanied by congestion. Other areas of the affected viscera, and other abdominal serous surfaces, appeared normal. There was no ascites nor any serosal lesion in the thoracic cavity. Histologically these lesions (fig. 3,4) were similar to those previously illustrated [l]. The affected surfaces were markedly thickened by the development of extensive and complex papillary outgrowths that in many places appeared to have coalesced. There was no invasion of the subserosal tissues. Generally the epithelium over the surfaces of the lesions appeared healthy, while much of the underlying tissue was degenerate and relatively acellular. Many of these degenerate areas contained psammoma bodies, apparently often derived from the connective tissue cores of papillae. Inflammatory changes were frequent. The secretion of material containing acid mucopolysaccharide by the epithelial cells was again confirmed by CI staining.

5 Fig.1. Ovary of dog 7. Extensive formation of papillae (P) on the surface, cortical tissue containing small follicles (F), and the edge of the medulla (M) at bottom left. HE, x48. Fig.2. Renal cortex from dog 4. Normal cortical tissue (top) and squamous metaplasia of renal tubules (arrows). HE, x 48. Fig.3. Metastatic lesion on the abdominal surface of the diaphragm of dog 7. The lesion involves the serosa only, without invasion of the underlying muscle (M). HE, x 48. Fig.4. Detail from figure 3, showing superficial papillae (P), psammoma bodies (PB), and inflammatory cells scattered throughout the connective tissue stroma. HE, x 120.

6 Fig.5. Papillary lesions of the uterine serosa and condensation of the subepithelial connective tissue in an entire bitch (dog 7). HE, x 120. Fig.6. Detail from figure 5. Vacuoles in serosal cells (arrows), whose contents stained positively with colloidal iron. HE, x 300. Fig. 7. Papillary lesions of the uterine serosa in an ovariectomised bitch (dog 1). HE, x 160. Fig.8. Papillary lesions of the serosa of the epididymis in a male 19). HE, x 120. Fig. 9. Detail from figure 8. x 300.

7 Stilboestrol and Serous Membrane Lesions in Dogs 87 No metastatic epithelial lesion was found in any lymph node from either animal. However, there were papillary lesions, detected only on histological examination, on the serosa adjoining one lymph node in dog 7. The same animal also had mild papillary lesions of the serosa overlying a kidney. The vaginal epithelium in both of these animals was of a cornified stratified squamous type. There were also areas of squamous metaplasia of the epithelium of the cervix and urethra of both animals, of the urinary bladder of dog 7, and of the renal pelvis of dog 6. Ovariectomised Females At autopsy, no lesion of serous surfaces was detected in any animal. Furthermore, histological examination failed to reveal any instance of papillary proliferation of serous surfaces other than those of the uterus and broad ligament. Three of these 5 animals (dogs 1, 4, and 5, table I) had very mild uterine serosal lesions. These lesions, which extended onto the broad ligament, consisted of localised clusters of small, simple papillae covered as a rule by cuboidal epithelium (fig. 7). There was also some hyperplasia of nearby serosal epithelial cells, and a minor degree of thickening and hyalinisation of the underlying fibrous connective tissue. Much of the uterine serosa appeared normal. The vaginal lining in all animals was a cornified stratified squamous epithelium. Squamous metaplasia was also observed in the cervix, urethra, urinary bladder, and, in 2 animals, kidney. In dog 1 metaplasia was confined to focal areas in the renal pelvic epithelium, while in dog 4 many tubules in the cortex and medulla also had this metaplastic change (fig. 2). Uteri from Normal Bitches No papillary lesion was observed on the serous surfaces of the uterus or broad ligament of any of these 15 animals. Males No macroscopic lesion of serosal surfaces was detected at autopsy in these 4 dogs. Mild papillary lesions (fig. 8, 9), involving only small focal areas of the serosa of the testis and epididymis, were observed histologically in one (D/PM 19). In other areas of these affected serous membranes, local thickenings were produced by an increase in subepithelial connective tissue into which serosal epithelial cords extended. There were also papillary lesions on the testicular serosa of another dog (D/PM 17), but to a lesser degree. In

8 88 O'SHEA/JABARA the remaining 2 dogs the testicular serosa was normal. There was no papillary lesion on non-genital serous surfaces. Discussion The observations reported here, taken together with the data of MAWDES- LEY-THOMAS and SORTWELL [4], require some modification of previous conclusions on the nature of serosal changes induced in the bitch by the administration of stilboestrol. It is clear that a primary serosal response to this oestrogen is not entirely confined to the surface of the ovary. Positive evidence has been produced that at least a mild degree of proliferation and papillary formation can be induced in the uterine serosa and broad ligament in the absence of the ovary and that some response can be obtained in the serosa of the testis and epididymis. Previous interpretations [1, 2, 61 must therefore be modified to account for the probability that some or all of the uterine serosal lesions previously regarded as ovarian metastases were in fact primary uterine proliferations. This tends to confirm the interpretation of MAWDESLEY-THOMAS and SORT- WELL [4] that the uterine lesions they described had a common aetiology with the ovarian lesions, but did not result from them. The reason for the marked differences between the hdings of JABARA [l, 21 and MAWDESLEY-THOMAS and SORTWELL [4] is not clear. These differences included the greater severity of uterine changes, the less marked ovarian changes, and the absence of extra-genital serosal and nodal lesions in the latter study. Probably the explanation lies in differences in the nature of the oestrogens used, the dosage, or the route of administration. In the experiments of MAWDESLEY-THOMAS and SORTWELL [4] the oestrogens used did not include stilboestrol, the rates of dosing were considerably higher, and the oestrogens were administered orallyz. The question remains as to the origins of the serosal lesions affecting nongenital organs in this and previous [l, 21 studies, and the lymph nodal lesions described previously. We still favour the view that these lesions were metastases of ovarian origin. The evidence in support of this view can be summarised as follows. While these lesions have been found in a high percentage of entire bitches in previous studies [l, 21, and in 1 of 2 entire bitches in the present study, they were consistently absent in 5 ovariectomised bitches and MAWDESLEY-THOMAS, L.E. : Personal communication (1968).

9 Stilboestrol and Serous Membrane Lesions in Dogs 89 4 male dogs given comparable doses of stilboestrol. This strongly suggests that the presence of the ovaries be in some way essential to the formation of these extra-genital lesions. No extra-genital serosal lesions were ever found in entire dogs that did not have ovarian lesions [l, 21. Nor were there such lesions in oestrogen-treated dogs whose ovaries had only minimal evidence of proliferation of the superficial epithelium [4]. The nature of the lesions themselves was suggestive of implantational metastases in that they were almost invariably confined to the abdominal cavity, were focal, with other areas of the serosa of affected organs remaining normal, and frequently involved apposed surfaces of neighbouring organs. Close histological and histochemical similarities existed between the ovarian lesions, the normal ovarian elements from which they were believed to be derived, and the extragenital serosal lesions [6]. While the extra-genital serosal lesions observed could conceivably have been independent primary lesions derived locally from the serosa, this does not seem feasible in the case of lesions within lymph nodes. On the assumption that the extra-genital serosal and nodal lesions were in fact metastases of ovarian origin, the ovarian lesions giving rise to them are still regarded as malignant tumours. This interpretation is supported particularly strongly in the case of metastasis to lymph nodal sinuses, which may be presumed to have involved the entry of ovarian epithelial cells into lymphatic vessels. In addition to the ovarian response it is also clear that the serous membranes of certain other parts of the male and female genital tract can respond to the administration of oestrogen by proliferation and the formation of papillae. There is no evidence that these extra-ovarian primary lesions be capable of metastasis. They do, however, appear to indicate a functional individuality, in terms of responsiveness to oestrogen, on the part of the serous membranes of genital organs. In conclusion, the available evidence suggests that different levels of responsiveness to stilboestrol administration occur in different serous membranes. The most marked response is seen in the modified serosa that covers the surface of the ovary. Here local proliferation and evidence of malignancy in the form of metastases are found. Secondly, local proliferation can be induced in the serosa of other parts of the female and male genital systems. Metastasis has not been demonstrated in any of these cases. Finally, there is no evidence that serous membranes of non-genital organs be capable of a primary proliferative response to stilboestrol. They may be, however, the sites of metastases of ovarian origin.

10 90 O'SHEAIJABARA Acknowledgements We are grateful to Mr. T. A. MASON and Mr. D. H. CARR who performed the ovariectomies, and to Dr. L. RIKARD-BELL of E. R. Squibb & Sons who kindly donated the polyethylene glycol. References 1 JABARA, A.G. : Canine ovarian tumours following stilboestrol administration. Austr. J. exp.biol.med. Sci.37: (1959). 2 JABARA, A.G. : Induction of canine ovarian tumours by diethylstilboestrol and progesterone. Austr. J.exp.Biol.med. Sci.40: (1962). 3 JABARA, A.G. : Some tissue changes in the dog following stilboestrol administration. Austr. J.exp.Biol.med. Sci.40: (1962). 4 MAWDESLEY-THOMAS, L.E. and SORTWELL, R.J.: Proliferative lesions of the canine uterus associated with high dose oestrogen administration. Vet. Rec.82: (1968). 5 MOWRY, R.W.: Improved procedure for the staining of acidic polysaccharides by Muller's colloidal (hydrous) ferric oxide and its combination with the Feulgen and the periodic acid-schift reactions. Lab.Invest. 7: (1958). 6 O'SHEA, J.D. and JABARA, A.G.: The histogenesis of canine ovarian tumours induced by stilboestrol administration. Path. vet. 4: (1 967). Author's address: Dr. J. D. O'SHEA, Department of Veterinary Preclinical Sciences, University of Melbourne, Melbourne, Victoria (Australia)

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