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neoplasias due to spay neuter
Neoplastic conditions associated with spay/neuter status in the canine
Neoplasia, including malignant and non-malignant tumours, represents the single most important group of diseases in both veterinary and human medicine today. Recent studies have shown that cancer is the cause of death for 15-30% of dogs and 26% of cats. As a consequence, a large body of research focuses on the causes, diagnosis and treatment of this diverse group of conditions. As the study of cancer in pets evolved, it was quickly recognized in the 1960’s that some cancers were related to the presence or absence of a dog’s reproductive tract. A series of studies demonstrated that vaginal tumours, uterine tumours, ovarian tumours and mammary tumours could all be substantially reduced or eliminated by removal of the ovaries and uterus or of the ovaries alone.1,2 As a consequence of this work, and the wide-spread adoption of spay-neuter programs in the USA, these tumours represent a very small percentage of disease in this country. In contrast to this, mammary tumours represented the most common tumour submitted for histopathology in a Norwegian study. Mammary tumours accounted for 30% of submissions - approximately 9-13% of dogs - and 94% were malignant or pre-malignant based on modern criteria.3 Separately, mammary tumours were among the two main reimbursement claims in female dogs (the other was pyometra) in a recent Swedish study.4 However, while this stark difference may be interpreted as a success for US veterinarians, recent studies in regard to other tumours have demonstrated that ovariohysterectomy has the opposite effect on a number of other important tumours, including osteosarcoma, hemangiosarcoma, cardiac tumours, mast cell tumours and lymphoma.5-11 These data are widely available to owners and veterinarians and may be a source of confusion and frustration to both veterinarians and owners considering gonadectomy. There is an urgent need for veterinarians to develop scientifically sound recommendations that are sufficiently nuanced to educate owners and guide them in a decision-making process regarding their animal. There is further an urgent need for veterinarians to be prepared to discuss the benefits and risks of surgical gonadectomy with public interest groups and policy makers in order to serve as effective advocates for animal and human welfare in the USA and UK Only mast cell tumours approach the incidence of mammary tumours, accounting for 16-21% of cutaneous tumours (approximately 2.5-3% of dogs) in several studies from the USA,7 and 3-11% of tumours across all age groups in Norway.3 Across all breeds, the other tumours discussed affect a very small proportion of dogs (0.2-1% each). However, within specific breeds, the risk of developing specific tumours can be substantially higher. In Rottweilers, the incidence of osteosarcoma has been reported between 12-25% and the relative risk of diagnosis with mammary tumours or osteosarcoma was 100:1144, according to Gamlem and coworkers.3,5-6 In contrast, the relative risk of the same tumours on the Dachshund was 194:73.3 In addition to this source of variation, there are two other major sources of variation based on tumour type: differences in gender predilection toward tumours, and differences in response of tumours to ovariohysterectomy/neutering. In regard to the latter, mammary tumours are dramatically more common in female dogs than male dogs, and there is convincing evidence that removal of the gonads early in life results in the greatest reduction of tumour development (95%), with decreasing benefits as the animal ages to approximately a 25% reduction in tumour development after the third heat.12-14 In contrast, delaying ovarian removal beyond 1-4 years of age attenuates the increased risk of osteosarcoma in spayed Rottweilers5,6 A third response pattern for tumour-development is seen with several other tumours. Several studies have shown an increased risk for hemangiosarcoma and mast cell tumour in dogs spayed after seven to 12 months, compared to either dogs spayed early or intact dogs, whereas the effect of age at spay has been variable across breeds for lymphosarcoma These complicated relationships between gender, gonadal status, breed and tumour risk need to be addressed through proactive conversations between owners and veterinarians. The primary factors that should be accounted for when deciding if and when to perform a spay/neuter procedure are:
Owner’s willingness to accommodate for normal reproductive physiology and behaviour, and the owner’s ability to prevent unwanted breedings. - Breed of dog - Breed predisposition to development of specific tumour types or other complications - Relative morbidity/mortality associated with specific tumour types Other factors that should also be taken into consideration are: - “Family history” of lines within a given breed in regard to conditions known to be related to spay - Purpose of the dog - Health status of the dog prior to surgery Unfortunately, in many cases, insufficient information is available to make clear recommendations for different breeds. Even when information is available, it is often incomplete, or the research is subject to bias based on study design and the limitations of retrospective research.15 In addition, differing statistical terminology and methods complicate interpretation of data across studies.5,10- 11 As a consequence, it should be understood that in many cases a recommendation can only be made based on clinical experience, extrapolation from better-studied breeds and with significant input from owners. Generalizations, both by the veterinary community and by breeders/owners may not prove accurate as research in this field evolves and may cause significant harm to individual animals. They should be used only as a starting point for discussion.
Additional information about relative risk of disease among breeds is not readily available from any source. Specific retrospective studies have now been completed on some tumours for the Rottweiler, Golden Retriever and Vizla in the USA, while Gamlem and co-authors described the relative risk of tumour development among breeds in Norway.3-5,8,10,11 Together with this, veterinary experience and knowledge of historical disease within a line of dogs can guide a decision-making process to determine when or whether to neuter dogs. Across breeds, removal of ovarian hormones has a strong benefit of reducing the lifetime risk of mammary tumours and pyometra. These conditions affect a large proportion of un-spayed females (mammary tumours 13% by age 10, pyometra 19% by age 10) and are associated with mortality of 50% or higher.12-14,16 Within breeds, the incidence of specific tumours, as well as other conditions affecting animal health, may outweigh this benefit. To exemplify this, two breeds in which recent research has characterized the relative tumour risks are discussed below: In Vizlas (breed specific risk for mammary tumours was not reported), the frequency of reported cancer was 24% of animals, with frequencies of 5.9%, 2.8% and 1.8% for mast cell tumour, hemangiosarcoma and lymphoma, respectively.11 The risk for each of these specific tumour-types was elevated in spayed animals and the onset of cancer in general was earlier for spayed animals. Cumulatively, the risk for these tumours, which may have a higher mortality and earlier onset than mammary tumours, may outweigh the risk of mammary tumour development in intact Vizlas. Furthermore, the tumour-types studied in this breed appear to be most common after delayed ovariohysterectomy or castration. Thus, recommendations to delay sterilization beyond the first heat or first year of age may not be beneficial. To be able to make a sound recommendation, the breed-specific risk for mammary tumours should be assessed. In Rottweilers, the risk of dying due to osteosarcoma is as much as 2x higher than the risk of dying due to mammary tumors.4,6 Furthermore, benefits of ovarian hormones for tumour prevention have been recognized up to one to four years of age5,6 whereas pyometra and mammary tumours commonly are seen after that age.4 Thus, animals can be spayed prior to the most common onset of reproductive conditions and after benefits of ovarian hormones have had an effect. This approach will reduce the likelihood of an animal developing pyometra, provide some (25%) reduction in development of mammary tumours, while maximizing the preventive effect of ovarian hormones of osteosarcoma development. In conclusion, it is increasingly recognized that the approach of “individualized medicine” is particularly important in regard to a question that was long considered settled among the veterinary community, namely whether animals benefit from surgical sterilization. As researchers expand the body of knowledge, easy answers may not be readily available and a recommendation to spay or castrate should be made after consideration of health-risks associated with specific breeds or lines of dogs, and in conversation with the owner.
References 1. MV Root Kustritz: Effects of surgical sterilization on canine and feline health and on society. Reprod Domest Anim 2012;47(Suppl 4):214-222. 2. IM Reichler: Gonadectomy in cats and dogs: a review of risks and benefits. Reprod Domest Anim 2009;449(Suppl 2):29-35. 3. Gamlem H, Nordstoga K, Glatter E: Canine neoplasia-introductory paper. APMIS Suppl 2008;125:5-18. 4. Jitpean S, Hagman R, Holst B et al: Breed variations in the incidence in mammary tumors and pyometra in swedish dogs. Reprod Domest Anim 2012;47(Suppl 6):347-350. 5. Waters DJ, Kengeri SS, Clever B, et al: Exploring the mechanisms of sex differences in longevity: ovarian influence on exceptional longevity in dogs. Aging Cell 2009;8:752-755 6. Cooley DM, Beranek BC, Schlittler DL, et al: Endogenous gonadal hormone exposure and bone sarcoma risk. Cancer Epidemiol Biomarkers Prev 2002;11:1434-1440. 7. White C, Hohenhaus A, Kelsey J, et al: Cutaneous MCTs: associations with spay/neuter status, breed, body size, and phylogenetic cluster. J Am Anim Hosp Assoc 2011;47:210-216. 8. Hart BL, Hart LA, Thigpen AP, et al: Long-term health effects of neutering dogs: comparison of Labrador Retrievers with Golden Retrievers. PLoS ONE 2014; 9: e102241. doi:10.1371/journal.pone.0102241 9. Smith A: The role of neutering in cancer development. Vet Clin North Am Small Anim Pract 2014; 44:965-975 10. Torres de la Riva G, Hart BL, Farver TB, et al: Neutering dogs: effects on joint disorders and cancers in Golden Retrievers. PLoS ONE 8(2): e55937. doi:10.1371/journal.pone.0055937 11. Zink MC, Farhoody P, Elser SE, et al: Evaluation of the risk and age of onsetof cancer and behavioral disorders in gonadectomized Vizslas. J Am Vet Med Assoc 2014;244:309-319. 12. Dorn CR, Taylor DO, Schneider R, et al: Survey of animal neoplasms in Alameda and Contra Costa Counties, California. II. Cancer morbidity in dogs and cats from Alameda County. J Natl Cancer Inst 1968;40:307-318. 13. Moe L: Population-based incidence of mammary tumors in some dogs breeds. J Reprod Fertil 2001;Suppl 57:439-443. 14. Kristiansen VM, Nødtvedt A, Breen AM, et al: Effect of ovariohysterectomy at the time of tumor removal in dogs with benign mammary tumors and hyperplastic lesions: a randomized controlled clinical trial.J Vet Intern Med 2013;27:935-942. 15. Beauvais W, Cardwell JM, Brodbelt DC: The effect of neutering on the risk of mammary tumours in dogs –a systematic review. J Small Anim Pract 2012;53:314-322. 16. Sorenmo KU, Kristiansen VM, Cofone MA et al: Canine mammary gland tumours; a histological continuum from benign to malignant; clinical and histopathological evidence. Vet Comp Oncol 2009;7:162-172
C. Scott Bailey College of Veterinary Medicine, North Carolina State University, Raleigh, NC

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