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Ageing, Testicular Tumours and the Pituitary–Testis Axis in Dogs

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Ageing, Testicular Tumours and the Pituitary–Testis Axis in Dogs 153 Ageing, testicular tumours and the pituitary–testis axis in dogs M A J Peters,FHdeJong4, K J Teerds1,DGdeRooij3, S J Dieleman2 and F J van Sluijs Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Universiteit Utrecht, The Netherlands 1Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Universiteit Utrecht, The Netherlands 2Department of Farm Animal Health, Faculty of Veterinary Medicine, Universiteit Utrecht, The Netherlands 3Department of Cell Biology, University Medical Center Utrecht, Universiteit Utrecht, The Netherlands 4Department of Endocrinology and Reproduction, Erasmus University Rotterdam, The Netherlands (Correspondence should be addressed toMAJPeterswhoisnowatDiedenweg 145, 6706 CN Wageningen; Email: [email protected]) (Requests for offprints should be addressed to F J van Sluijs, Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, P O Box 80154, 3508 TD Utrecht, The Netherlands; Email: [email protected]) Abstract Dogs of different ages without testicular diseases were dogs with Sertoli cell tumours without signs of feminis- evaluated to study possible age-related changes in hor- ation. Dogs with a Leydig cell tumour had greater concen- mone concentrations in serum. Dogs with testicular trations of oestradiol and inhibin-like immunoreactivity in tumours were also investigated to study the relation both peripheral venous and testicular venous blood than between tumour type and hormone concentrations; in this did dogs without a neoplasm (P<0·05). The testosterone study, dogs with Sertoli cell tumours, Leydig cell tumours concentration in testicular venous blood of these dogs was and seminomas were included. We measured testosterone, lower than that in dogs with normal testes. The concen- oestradiol, LH, FSH and inhibin-like immunoreactivity tration of LH in peripheral venous blood was also reduced concentrations in peripheral venous and testicular venous (P<0·05). Hormone concentrations in dogs with a semi- blood of these animals. noma were not different from those in normal dogs. In normal dogs there appeared to be no age-related It was concluded that seminomas are not endocrinologi- changes in the concentrations of the investigated hor- cally active. In contrast, both Sertoli cell tumours and mones, except for a significant age-related decrease Leydig cell tumours can cause increased oestrogen pro- in oestradiol concentrations in testicular venous blood duction leading to signs of feminisation. These tumours (P<0·02). Dogs with a Sertoli cell tumour had greater also have considerable amounts of inhibin-like immuno- oestradiol concentrations and inhibin-like immunoreactiv- reactivity, but only in Sertoli cell tumours does this result ity in both peripheral and testicular venous blood than did in a reduction in FSH concentrations, suggesting that dogs without a neoplasm (P<0·05). Testosterone concen- Sertoli cell tumours secrete dimeric inhibin, whereas trations were reduced in dogs with Sertoli cell tumours, as Leydig cell tumours presumably produce loose -subunits were FSH and LH. Feminisation occurred in eight of 13 that cross-react in the inhibin assay but are not biologically dogs with a Sertoli cell tumour and in two of 14 dogs with active. a Leydig cell tumour; it was accompanied by a significantly Journal of Endocrinology (2000) 166, 153–161 greater oestradiol concentration than in normal dogs and in Introduction one concentration has been reported (Karpas et al. 1983, Wang et al. 1993, Zirkin et al. 1993, Chen et al. 1994), in A decline in reproductive function is a well-known feature addition to a reduction in plasma gonadotrophin concen- of ageing in mammalian species (Meites 1986). Many trations, which is in contrast to the findings in men (Zirkin studies have revealed an age-dependent decrease in free et al. 1993). testosterone concentrations in the human male, in combi- In male dogs, conflicting results have been obtained in nation with unchanged or increased oestradiol concen- studies on the effect of ageing on plasma testosterone trations and increased concentrations of luteinizing concentrations. Either no reduction with age (Taha & hormone (LH) and follicle-stimulating hormone (FSH) Noakes 1982, Lowseth et al. 1990) or decreasing testos- (Neaves et al. 1984, Finch & Schneider 1985, Kaiser & terone concentrations has been reported (Bondarenko et al. Morley 1994). In ageing male rats, a decrease in testoster- 1979, Günzel Apel et al. 1990); in accordance with the Journal of Endocrinology (2000) 166, 153–161 Online version via http://www.endocrinology.org 0022–0795/00/0166–0153 2000 Society for Endocrinology Printed in Great Britain Downloaded from Bioscientifica.com at 09/27/2021 06:57:45PM via free access 154 M A J PETERS and others · Hormonal effects of testicular tumours in dogs Table 1 Weight and corresponding age at which dogs are considered to be geriatric (modified from Goldston et al. (1989)), numbers of dogs with normal testes and with testis tumours per weight category and their age range, and type of tumour and the numbers of dogs with such tumours Normal testes Tumorous testes Geriatric age Age range Age range (years) No. (years) Type/No. (years) Weight category Small dogs 11·5 3 2–11 SCT/1 10 (0–9 kg) SEM/1 7 LCT/3 12–14 Medium dogs 10·9 22 1–11 SCT/4 6–11 (10–23 kg) SEM/6 7–14 LCT/6 10–14 Large dogs 8·9 17 2–11 SCT/7 4–11 (24–40 kg) SEM/9 5–11 LCT/4 7–12 Giant dogs 7·5 7 2–11 SCT/1 8 (>40 kg) SEM/3 6–10 LCT/1 16 Normal, dogs with normal testes; SCT, Sertoli cell tumour; SEM, seminoma; LCT, Leydig cell tumour. latter observation, lower LH concentrations were observed the tumour. Sertoli cell tumours are known to produce in aged dogs also (Günzel Apel et al. 1990). oestrogens (Rijnberk 1996), but it is not clear whether Testicular neoplasia and Leydig cell hyperplasia are Leydig cell tumours and seminomas also secrete oestro- common findings in aged dogs. The prevalence of testicu- gens. In humans, oestradiol in blood is derived mainly lar tumours can be as high as 60% in old dogs (Mosier from Leydig cells and adipocytes after conversion from 1989). In men, however, testicular tumours occur most testosterone, but Sertoli cells and germ cells can also often in adults younger than 40 years of age (Looijenga produce oestrogen (Sharpe 1998). et al. 1994). The three main types of testicular tumours in To investigate possible effects of reproductive ageing dogs are Sertoli cell tumours, seminomas and Leydig cell and testicular tumours on pituitary–testicular function in tumours; mixed tumours are often observed (Nielsen & dogs, we have measured testosterone, oestradiol, LH, FSH Kennedy 1990). Cryptorchidism is an important risk factor and inhibin-like immunoreactivity in peripheral venous for the development of testicular tumours, causing a and testicular venous blood. Dogs of different ages without 26-fold increase in the risk for Sertoli cell tumours and testicular diseases and dogs with Sertoli cell tumours, a 15-fold increase for seminomas (Hayes et al. 1985). seminomas and Leydig cell tumours were studied. Although Sertoli cell tumours and seminomas are con- sidered to be potentially malignant, they seldom metasta- sise in the dog, whereas seminomas in men are highly Materials and Methods malignant (Swerdlow 1993). In dogs, testicular tumours may be associated with Animals clinical signs such as feminisation and alopecia, especially Peripheral venous and testicular venous blood was col- when a Sertoli cell tumour is involved (Theilen & lected from 95 dogs of different breeds and ages before Madewell 1987). This syndrome is characterised by bi- castration. This operation was performed for a variety of lateral symmetrical alopecia, gynaecomastia, atrophy of the reasons not related to testicular diseases (n=49: benign contralateral testis, a pendulous prepuce, attractiveness to prostatic hyperplasia (BPH), balanoposthitis, perineal other male dogs and, in severe cases, bone marrow hernia or unwanted behaviour), or because of a testicular depression. The last of these may be irreversible and is a tumour (n=46; tumour types are shown in Table 1). In potentially lethal complication (Rijnberk 1996). Feminis- some cases it was not possible to collect blood from both ation occurs in 19% of dogs with a histologically diagnosed the peripheral and the testicular vein. Cryptorchid dogs Sertoli cell tumour and in 5% of dogs with a Leydig cell without testis tumours were excluded from this study. tumour (Peters & van Sluijs 1996). Feminisation is attrib- Nine of the 46 dogs with testicular tumours were uted to the secretion of excessive amounts of oestrogens by cryptorchid. Journal of Endocrinology (2000) 166, 153–161 www.endocrinology.org Downloaded from Bioscientifica.com at 09/27/2021 06:57:45PM via free access Hormonal effects of testicular tumours in dogs · M A J PETERS and others 155 In order to compare data from dogs of different breeds, sensitivity of the assay was 0·2 ng/ml. Plasma LH concen- we applied a correction factor based on the fact that dogs tration was measured by a heterologous RIA as described of small breeds live longer than those of large breeds. We by Knol et al. (1993). A sheep antibody, CSU-204 (a gift expressed the age of a dog at the time of castration as the from Dr Niswender, Colorado State University, Fort percentage of its geriatric age, using the method of Collins, CO, USA), radioiodinated NIAMDD-bLH-4 Goldston et al. (1989). This method groups dogs into and canine pituitary standard LER 1685–1 were used in categories according to body weight and the age at which this assay. The sensitivity of the LH assay was 1 ng/ml. they become geriatric (Table 1). Hence, we considered dogs to be old (geriatric) when their age was equal to or Characterisation of tumours greater than 100% of the geriatric age according to their Tumours were classified microscopically according to the category of body weight.
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