Use the current research to individualize your recommendations for canine sterilization.
Like most veterinarians, I believed for years that responsible people neuter their dogs, period. Most of my patients were neutered, and I believed that intact individuals would have dreadful health and behavioral problems. Many vets and laypeople still believe this, despite mounting evidence to the contrary.
Pet overpopulation is a serious problem, as can be seen by a casual perusal of ASPCA statistics.1 Vets aware of the negative effects of neutering still recommend sterilization to avoid unplanned litters, and the majority of shelters and rescue organizations require sterilization, often before adoption.
Animals are most often sterilized via removal of the gonads, accurately called gonadectomy, or neutering, in both sexes. “Neutering” is commonly used instead of the term “castration/orchiectomy” for males. In females, when gonadectomy/ovariectomy is accompanied by removal of the uterus, it is referred to as an ovariohysterectomy (OHE), often referred to as a spay.
Sterilization that does not remove the gonads includes vasectomy for male dogs; or complete hysterectomy (including the cervix), also called an ovary-sparing spay or OSS, for females. The AVMA now includes these among the sterilization options described to owners on the public information section of their website.2
QUESTIONING ROUTINE GONADECTOMY
In the late 1990s, I noticed that many of my neutered patients were obese, despite careful feeding practices. Spay incontinence was common in older spayed bitches. Several neutered canine athlete patients, including my own obedience Utility competitor, ruptured their cruciate ligaments. I reasoned that I was preventing unplanned litters and mammary cancer, yet I (subjectively) saw a similar incidence of mammary cancer in both intact and neutered bitches.
From 1999 to 2002, I studied homeopathy and holistic practice in the UK. Dogs are less commonly neutered in the UK, and we discussed the suppressive effects of removing the gonads. Our domestic animals do not naturally experience menopause, so removing the gonads in any animal suppresses a natural outlet, potentially increasing the incidence of diseases such as cancer.3
Vets in the US have limited experience with intact animals, as virtually all pet dogs and cats are gonadectomized due to shelter practices, breeder requirements, and veterinary recommendations. Since the late 90s, the sport and breeding communities have led the way on the question of neutering dogs, challenging the assumption that all dogs should have their gonads removed. The first article I saw regarding the potential negative effects of neutering dogs was a review by Margaret V. Root Kustritz, DVM, PhD, DACT.4 Many dog enthusiasts are now familiar with the potential issues associated with the early removal of sex hormones, so there is an increased interest in later sterilization, or sterilization that does not remove the gonads.
Animal bodies develop as a whole, with elegant homeostatic mechanisms and interrelated body systems. The gonads are an integral part of this system, and their removal will have consequences for the animal, depending on their individual susceptibility and the length of time they live without their gonads.
Consider the broad physiologic functions of the gonads and gonadal hormones, as summarized by Lawless:5
• Development of secondary sex characteristics
• Estrogen production and its role in bone and cartilage homeostasis for normal joint development and maintenance of bone and cartilage strength
• Gonadal androgen production and its role in maintenance of muscle mass and strength as well as regulation of fat deposition
• Neuroprotective function of testosterone and estrogen
• Sex steroid modulation of immune function by enhancing tissue self-recognition.
The increased risk of cancer in neutered animals may be related to the long-term effects of high blood levels of luteinizing hormone (LH), which are more than 30 times higher than the normal levels following gonad removal. LH increases so dramatically because of the loss of feedback inhibition from the gonadal steroids. This constant stimulation increases the number of LH receptors in tissues throughout the body, increasing their effect. LH binding to cell receptors stimulates cell division and nitric oxide release.6
Tissues with increased LH receptor sites that may show higher cancer incidence after neutering include the prostate, bladder, and urethra, vascular endothelium, heart, spleen smooth muscle, the skin, and lymphoid tissue.7
Certain non-cancerous diseases may also increase after neutering due to these artificially high LH levels. The tissues with potentially affected LH receptors include the intestinal and urinary tracts, certain areas of the brain, the pancreas and thyroid, and some cartilages and ligaments.7
Other researchers postulate that neutering may result in decreased vitamin D levels and increased cancer incidence, or that a decrease in thymocytes and consequent immune suppression could be involved.8
It is important to understand the constellation of steroid effects, and the susceptibility of various breeds and individuals. Patients will manifest disease in their weakest or most susceptible system. For a Dachshund or Corgi, that may be IVDD; for a Boxer or Golden Retriever, cancer; for a Vizsla or Springer Spaniel, anxiety may result.
RESEARCH POINTS TO AREAS OF CONCERN
Evidence has been accumulating since the late 1980s that neutering has significant health implications. Literature reviews4,8,9,10 have compiled evidence across breed lines showing definite effects caused by removing the gonads, aside from population control. Studies have proliferated, both within and across breeds, revealing significant effects of neutering on the incidence of joint diseases and IVDD,11,12,13,14,15 cancer,12,14,15,16,17,18 behavior problems, including anxiety, aggression, and fearfulness,15,19,20,21,22,23,24 cognitive decline,25 immune disorders,26,27 and spatial performance as measured by maze learning and recall.28 Actual changes in the frequency of various conditions, and the breeds studied, are in the papers cited above. The increase or decrease in incidence is broadly summarized from the research as follows:
• Castration decreased roaming behavior.
• In one study, aggression toward strangers increased in animals neutered before puberty. In other studies, owner-directed aggression and reactivity increased with gonad removal. Every prospective controlled study of aggression and gonadectomy showed either no effect or an increase in aggression toward people in neutered animals. Gonadectomized dogs were more fearful, anxious, and excitable, and less trainable.
• Intact males were significantly less likely to experience cognitive dysfunction than castrates.
• Spatial learning was also affected. Intact females learned and recalled a maze better than neutered animals or intact males.
• Mammary tumors (malignant in half of cases) had a decreased incidence in spayed bitches in some studies.
• Prostatic tumors (almost always malignant) had an increased incidence in neutered dogs.
• Benign prostatic hypertrophy was common in intact older dogs; castration is curative.
• Bladder cancer (often malignant) was more prevalent in gonadectomized dogs.
• Testicular cancer (rarely metastasizes) occurred in aged male intact dogs; castration is curative.
• Ovarian cancer may be malignant and rarely occurs in intact females.
• Hemangiosarcoma (variably malignant), osteosarcoma (often malignant), lymphosarcoma, and mast cell tumors had an increased incidence in gonadectomized dogs.
Hip dysplasia, anterior cruciate ligament rupture, and intervertebral disc disease increased in gonadectomized dogs of susceptible breeds. These issues are worse in animals neutered before puberty, as the growth plates close later, and abnormal joint angles are subjected to more stress.29
• Urinary incontinence has an increased incidence in neutered female dogs. The collagen to muscle ratio changes after neutering, which negatively affects urethral function.30,31
• Pyometra occurs in roughly 25% of intact bitches over ten years of age. Surgery is curative, with a high incidence of complications.
• Hypothyroidism increased after gonadectomy in some studies, and was unaffected in others.
• Immune-mediated disease (atopic dermatitis, autoimmune hemolytic anemia, hypoadrenocorticism, hypothyroidism, and immune-mediated thrombocytopenia) increased in incidence in all gonadectomized animals, and lupus increased in neutered bitches.
• Obesity occurs in about 3% of the total canine population; however, up to 50% of gonadectomized dogs are obese.
• Longevity studies across breeds have shown that neutered dogs of both sexes live significantly longer than intact dogs.7 The neutered dogs were more likely to die of cancer, while the intact dogs were more likely to die of trauma (car accidents, etc.) or infectious disease. These studies did not assess if the dogs received similar levels of care. Were they intact due to overall lack of veterinary care sought by the owner, or were they cherished family members? Traumatic and infectious diseases tend to be more preventable than cancer.
BREED AND TIMING OF NEUTERING
We can see that this is not a simple choice; we certainly don’t want animals to breed indiscriminately, but we also want our patients to live long, healthy lives. As many animals are susceptible to the problems discussed above, it may be optimal for them to retain their gonads for some period of time, perhaps even lifelong, to see the beneficial effects on these health conditions.
The Hart research team has been at the forefront of current exploration into the consequences of neutering on dogs. They evaluated the effect of neutering on the incidence of joint problems (cranial cruciate tear, hip dysplasia, elbow dysplasia) and several cancers (lymphoma, mast cell tumour, hemangiosarcoma, osteosarcoma) in 35 breeds and mixed breeds of five weight categories.34,36 Roughly, they found that certain breeds and mixed breeds (mostly large) were more susceptible to joint disease when neutered before puberty, and that some breeds showed an increased incidence of cancer when neutered at any age, including two small breeds, Boston Terriers and Shih Tzus. Please note that this does not address other problems seen to increase in incidence with neutering, such as cognitive dysfunction, behavioral changes, and multiple metabolic diseases. A holistic approach will also consider an individual’s risk for such problems.
The Harts recommend that the owner and their veterinarian discuss the animal’s situation in light of their breed and weight.7,34,36 Many breeds show no apparent increase in joint
problems or cancers. Those animals could be neutered at any age, if none of the other diseases shown to increase in neutered animals are cause for concern. If joint problems are a concern, neutering should be delayed until sexual maturity. If cancer is a concern, the owner may choose to leave the pet intact or consider a vasectomy or ovary-sparing spay to retain the hormones lifelong.
As mentioned earlier, there are alternatives to gonadectomy for permanently sterilizing dogs. Males can be vasectomized, and females can have a complete hysterectomy (including the cervix), also called an ovary-sparing spay. These methods are safe and effective, like traditional OHE and castration, though typically more expensive. Gonad-sparing sterilization can be done at any age, even before puberty, as the dog will develop normally.
The ovary-sparing spay (OSS) was pioneered by Dr. Michelle Kutzler, DVM, PhD, DACT at Oregon State University. The procedure is not much more difficult than a traditional spay. The ovaries are left in place, and the entire uterus and cervix are removed, creating a slightly longer and lower midline incision than is typical. It is essential to remove the entire cervix in this procedure, as the ovaries will produce progesterone as normal, and hypertrophy of any uterus remaining could lead to an eventual pyometra. The female will still cycle and be attractive to males, but she will not bleed.
Some vets perform tubal ligations. This is not a safe sterilization option, as the uterus remains in the bitch, and the repeated cycling will result in endometrial hyperplasia and the possibility of pyometra.
Vasectomy accesses the vasa from the same prescrotal incision used for castration. Delicate separation of the vasa from the accompanying vessels is essential to ensure that testicular blood circulation is not compromised. Dr. Kutzler describes both the OSS and vasectomy;37 visit parsemus.org for more information and an OSS procedure video.38
CAVEATS TO GONAD-SPARING STERILIZATION
There are caveats to performing these surgeries. Ensure that owners understand what they are requesting.
A dog that is sterilized and retains its gonads is psychologically intact, with normal mating desires. This is not problematic for many individuals, as the lack of discharge decreases the spread of estrus pheromones, making bitches less attractive. Vasectomised males will mount, tie, and ejaculate, and hysterectomised females will flag and stand for breeding. This can result in injuries and/or venereal disease.
• Some males can develop intermale aggressive tendencies, and this can be severe enough that castration is the only sensible option.
• Vasectomised and hysterectomised individuals will still be at risk for developing physical problems more common in intact individuals: prostatomegaly, perianal hernias, perianal hyperplasia/tumors (males), mammary tumors (females), and gonadal cancers (both).
• Residual vaginal tissue could develop a cyst; a stump of any tissue can become cystic, and vaginal tissue does respond to hormones to some extent.
• Vasectomised dogs reabsorb their sperm, and there may be swelling of the testes/vasa until equilibrium develops.
• Hysterectomised bitches may develop behavioral and physical signs of pseudocyesis, like intact bitches. Some dog sport organisations do not allow bitches in heat to compete, and this could include hysterectomised bitches, as they might be attractive to males.
Clients vary widely in their healthcare goals, capabilities, and personal opinions, from those who see their dogs as cherished children to those with a more utilitarian view, and everything in between. When they seek advice about best practices for the longevity and well-being of their animal companions, we must advise based upon the entirety of the situation for each dog and owner.
It is possible that gonad-sparing sterilization will become the standard of care for well-managed dogs. We simply do not know everything about the delicate interrelationship of the gonads with other body systems. It may be ideal, for the animal’s health, to not sterilize at all. We don’t know if stopping the flow of sperm in a dog’s body, or removing the feedback effects of the uterus on the ovaries, could have deleterious effects. Based on the research evidence, it appears advantageous overall for animals to retain their gonads, if they must be sterilized. There are good reasons to neuter dogs in certain cases, though it should always be a considered decision, not a sweeping generalization.7
Some individuals and breeds appear to be less negatively affected by neutering. Many clients have never lived with an intact animal and are concerned that behavior will be a problem. Many vets have never lived with an intact dog and do not know how to discuss this with clients. People who cannot or will not supervise their dogs should not have a hormonally intact dog. Intact, vasectomized, and OSS dogs will all try to breed during a female’s estrus, and both parties can be seriously injured or contract venereal diseases in the attempt.
From a population control standpoint, it is vital for rescue groups and shelters to require sterilization. Vasectomy and ovary-sparing spay, as alternatives to conventional gonadectomy procedures, allow animals to retain their normal hormonal influences. These procedures sterilize, yet avoid the reported negative effects of gonadectomy. As with all medical practices, it behooves vets to understand the sterilization situation as well as possible, so that we can counsel owners regarding the best options for their individual dogs and circumstances.
1 American Society for the Prevention of Cruelty to Animals. Shelter Intake and Surrender. American Society for the Prevention of Cruelty to Animals website. https://www.aspca.org/helping-people-pets/shelter-intake-and-surrender Accessed 11 July 2021.
2 American Veterinary Medical Association. Spaying and Neutering. American Veterinary Medical Association website. https://www.avma.org/resources/pet-owners/petcare/spaying-and-neutering Accessed 11 July 2021.
3 Saxton J, Gregory P. Textbook of Veterinary Homeopathy. Beaconsfield, UK: Beaconsfield Pub Ltd., 2005.
4 Root Kustritz MV. Effects of surgical sterilization on canine and feline health and on society. Reprod Dom Anim. 2012;47(s4):214–222. https://onlinelibrary.wiley.com/doi/full/10.1111/j.1439-0531.2012.02078.x Accessed 12 July 2021.
5 Lawless CW. Assessment of the general effects of gonadectomy on canines: Theriogenology research review paper. 2010 Ohio State University College of Veterinary Medicine. http://dogtorj.com/main-course/neutering-misconceptions/the-truth-about-gonadectomy/ Accessed 11 July 2021.
6 Zwida K, Kutzler MA. Non-reproductive long-term health complications of gonad removal in dogs as well as possible causal relationships with post-gonadectomy elevated Luteinizing Hormone (LH) concentrations. J. Etiol Anim Health. 2016;1:1-11. https://www.parsemus.org/wp-content/uploads/2015/03/Zwida-and-Kutzler-2016.pdf Accessed 12 July 2021.
7 Hart LA, Hart BL. An ancient practice but a new paradigm: Personal choice for the age to spay or neuter a dog. Front. Vet. Sci. 2021;8:244. https://www.frontiersin.org/articles/10.3389/fvets.2021.603257/full Accessed 11 July 2021.
8 Oberbauer AM, Belanger JM, Famula TR. A review of the impact of neuter status on expression of inherited conditions in dogs. Front. Vet. Sci. 2019;6:397. https://www.frontiersin.org/ articles/10.3389/fvets.2019.00397/full Accessed 11 July 2021.
9 Houlihan KE. A literature review of the welfare implications of gonadectomy in dogs. J Am Vet Med Assoc. 2017;250(10):1155-66.
10 Sanborn LJ. Long-term health risks and benefits associated with spay / neuter in dogs. National Animal Interest Alliance website. 2007.
11 Chai O, Harrosh T, Bdolah-Avram T, Mazaki-Tovi M, Shamir M. Characteristics of and risk factors for intervertebral disk extrusions in Pekingese. J Am Vet Med Assoc. 2018; 252(7):846-851. http://www.naiaonline.org/pdfs/LongTermHealthEffectsOfSpayNeuterInDogs.pdf Accessed 12 July 2021.
12 Hart BL, Hart LA, Thigpen AP, Willits NH. Long-term health effects of neutering dogs: Comparison of Labrador Retrievers with Golden Retrievers. PlosOne. 2014;9(7). http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0102241 Accessed 11 July 2021.
13 Packer RMA, Seath IJ, O’Neill DG, DeDecker S, Volk HA. DachsLife2015: an investigation of lifestyle associations with the risk of intervertebral disc disease in Dachshunds. Canine Genet Epidemiol. 2016;3:8. https://cgejournal.biomedcentral.com/articles/10.1186/s40575-016-0039-8#citeas Accessed 12 July 2021.
14 Torres de la Riva G, Hart BL, Farver TB, Oberbauer AM, McV.Messam LL, Willits N, Hart LA. Neutering dogs: effects on joint disorders and cancers in Golden Retrievers. Plos One. 2013; 8(2):e55937. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0055937 Accessed 12 July 2021.
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18 Obradovich J, Walshaw R, Goullaud E. The influence of castration on the development of prostatic carcinoma in the dog. 43 cases (1978-1985). J Vet Intern Med. 1987;1(4):183-7.
19 Farhoody P, Mallawaarachchi I, Tarwater PM, Serpell JA, Duffy DL, Zink C. Aggression toward familiar people, strangers, and conspecifics in gonadectomized and intact dogs. Front. Vet. Sci. 2018; 5:1-18. doi:10.3389/fvets.2018.00018
20 Farhoody P, Zink MC. Behavioral and physical effects of spaying and neutering domestic dogs: Summary of findings of a Masters thesis. New York: Hunter College, City U of NY, NYC. 2010. http://www.atftc.com/health/SNBehaviorBoneDataSnapShot.pdf Accessed 11 July 2021.
21 Kaufmann CA, Forndran S, Stauber C, Woerner K, Ganslosser U. The social behaviour of neutered male dogs compared to intact dogs (Canis lupus familiaris): Video analyses, questionnaires and case studies. Vet Med Open J. 2017; 2(1): 22-37. doi:10.17140/VMOJ-2-113.
22 Kim HH, Yeon SC, Houpt KA, Kee HC, Chang HH, Lee HJ. Effects of ovariohysterectomy on reactivity in German Shepherd dogs. Vet. J. 2006;172(1):154-159.
23 McGreevy PD, Wilson B, Starling MJ, Serpell JA. Behavioural risks in male dogs with minimal lifetime exposure to gonadal hormones may complicate population-control benefits of desexing. PlosOne 2018; 13(5):e0196284. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0196284 Accessed 11 July 2021.
24 Neilson JC, Eckstein RA, Hart BL. Effects of castration on problem behaviors in male dogs with reference to age and duration of behavior. J Am Vet Med Assoc. 1997;211(2):180-182.
25 Hart BL. Effect of gonadectomy on subsequent development of age-related cognitive impairment in dogs. J Am Vet Med Assoc. 2001;219(1):51-6.
26 Sundburg CR, Belanger JM, Bannasch DL, Famula TR, Oberbauer AM. Gonadectomy effects on the risk of immune disorders in the dog: a retrospective study. BMC Vet Res 2016;12:278. https://bmcvetres.biomedcentral.com/articles/10.1186/s12917-016-0911-5 Accessed 12 July 2021.
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28 Mongillo P, Scandurra A, D’Aniello B, Marinelli L. Effect of sex and gonadectomy on dogs’ spatial performance. Applied An Behav Sci. 2017;191:84–89.
29 Salmeri KR, Bloomberg MS, Scruggs SL, Shille V. Gonadectomy in immature dogs: effects on skeletal, physical, and behavioral development. J Am Vet Med Assoc. 1991;198(7):1193-203.
30 Ponglowhapan S, Church DB, Khalid M. Differences in the proportion of collagen and muscle in the canine lower urinary tract with regard to gonadal status and gender.Theriogenology. 2008;70(9):1516-24.
31 Salomon JF, et al. “Experimental study of urodynamic changes after ovariectomy in 10 dogs.” Vet Rec. 2006;159(24):807-11.
32 Schneider R, Dorn CR, Taylor DON. Factors influencing canine mammary cancer development and postsurgical survival (Summary). J Natl Cancer Inst. December 1969;43(6):1249-61. https://academic.oup.com/jnci/article-abstract/43/6/1249/910225 Accessed 12 July 2021.
33 Beauvais W, Cardwell JM, Brodbelt DC. The effect of neutering on the risk of mammary tumours in dogs – a systematic review. J Small Animal Prac. 2012; 53: 314-322. doi: 10.1111/j.1748-5827.2012.01220.x
34 Hart BL, Hart LA, Thigpen AP, Willits NH. Assisting decision making on age of neutering for 35 breeds of dogs: Associated joint disorders, cancers, and urinary incontinence. Front. Vet. Sci. 2020;7:388. https://www.frontiersin.org/articles/10.3389/fvets.2020.00388/full Accessed 11 July 2021.
35 Jitpean S, Hagman R, Ström Holst B, Höglund OV, Pettersson A, Egenvall A. Breed variations in the incidence of pyometra and mammary tumours in Swedish dogs. Reproduction in Domestic Animals. 2012;s6:347–350. https://onlinelibrary.wiley.com/doi/full/10.1111/rda.12103 Accessed 11 July 2021.
36 Hart BL, Hart LA, Thigpen AP, Willits NH. Assisting decision making on age of neutering for mixed breed dogs of five weight categories: Associated joint disorders and cancers. Front. Vet. Sci. 2020;7:472. https://www.frontiersin.org/articles/10.3389/fvets.2020.00472/full Accessed 11 July 2021.
37 Parsemus Foundation. Pet Health: Hormone-sparing sterilization. Parsemus Foundation website. https://www.parsemus.org/pethealth/hormone-sparing-sterilization/ Accessed 12 July 2021.
38 Kutzler MA. Gonad-sparing surgical sterilization in dogs. Front. Vet. Sci. 2020;7:342.