Idil Bastan- Department of Internal Medicine, Faculty of Veterinary Medicine, Ankara University, Ankara, Türkiye
Gonadectomy, commonly known as neutering, is widely used to address dog overpopulation and reduce reproductive disease risks, such as mammary cancer and pyometra. It is also advocated for behavior modification. However, neutering is associated with an increased risk of certain musculoskeletal disorders, obesity, several types of cancer, immune-mediated diseases, and cognitive dysfunction. These conditions may necessitate ongoing care and treatment, that require special care that the caregiver must provide furthermore burdens the caregiver with daily tasks, which encompasses the emotional, physical, social, and financial impact on pet owners caring for chronically ill animals. This burden can result in burnout, health issues, depression, social isolation, and financial stress. The potential benefits and risk of gonadectomy can affect the quality of life of both humans and pets. Relevant research findings should therefore be incorporated into each pet's and owner's particular situation. The purpose of this review is to address the long-term neutering risks and the potential caregiver burden that arises from these risks.
1 Introduction
Gonadectomy, or more generally referred to as “neutering,” has become a common tool for controlling reproduction and eliminating the risk of reproductive diseases in dogs such as mammary gland cancer, pyometra and prostate hyperplasia/infection, testicular tumors (1–6). Additionally, neutering of dogs and is promoted for population control and behavior modification (1). On the other hand, numerous recent publications have been shown that gonadectomy increases the risk of musculoskeletal degenerative diseases (e.g., hip dysplasia, cranial cruciate rupture), obesity and associated diseases, several forms of cancer, some immune-mediated diseases, urinary incontinence and cognitive dysfunction syndrome (3, 4, 7–11). All these diseases associated with gonadectomy may require ongoing care and treatment, intermittent monitoring and protection. Caregiver burden is defined as the impact on the emotional health, physical health, social life, and the financial status of the pet owner as a result of adopting the caregiver role (12) which has recently been investigated in pet owners caring for chronically ill pets (13–15). Caregiver stress can lead to burnout, acute and chronic bodily illnesses, depression, social isolation, and financial worries, according to studies on owners of chronically ill companion animals (13–15).
The necessity of gonadectomy in dogs remains controversial. This controversy arises primarily from the fact that gonadectomy confers a mixture of benefits and adverse effects that vary depending on the age at neutering, sex and breed (4). Long-term neutering complications can impact not only dog's wellbeing but also the quality of life for the owner. Therefore, the potential long-term health risks related to routine gonadectomy may no longer be acceptable for all pet owners (16).
This review aims to consolidate and present information clearly and concisely, focusing on the possible risks of gonadectomy. Additionally, the review aims to identify possible long-term post neutering complications encountered by the owners of dogs.
1.1 Obesity
The owners' perception of their dog's weight is one of their primary concerns regarding neutering (17). Epidemiological studies have shown that neutered dogs of both sexes are more likely to be overweight or obese than intact dogs (18–21). Gonadectomy contributes to obesity through two primary pathways: increased appetite and a lowered metabolic rate. Other explanations for the effect of neutering on obesity include an alteration in feeding behavior leading to increased food intake (22–28) and decreased activity without a corresponding decrease in energy (27). A study found that overweight intact dogs of both sexes lost significantly more weight during the study period than overweight neutered dogs (28).
Overweight and obesity are major risk factors for a number of chronic diseases, including degenerative orthopedic disease (28), diabetes mellitus, insulin-resistance (29–31), urinary tract disease (29–31), skin disease (29, 30), liver dysfunction (32) and neoplasia (33). Obesity not only causes health problems in small pets, but also creates an emotional burden for pet owners (33, 34). Additionally, overweight and obesity also pose a significant financial burden on pet owners. According to a recent report, the owners of overweight dogs spent 17% more on health care and 25% more on medications compared with the owners of healthy-weight dogs (35).
The most important and critical components in reducing the risk of overweight after neutering include monitoring the pet's body weight, making necessary adjustments to the amount and type of food given, and the exercise routine (36). The biggest challenges with a weight-loss program are avoiding overfeeding and gradually cutting back on food intake (37).
Pet obesity have been shown to affect the quality of life in both humans and pets (20). It is the veterinarian's responsibility to discuss the risks of obesity with owners before neutering and to prescribe individual weight maintenance plans after neutering (36, 37).
1.2 Skeletal system
Sex hormones play an important role in regulating the elongation of the bones. In dogs that have undergone prepubertal gonadectomy (before 6 months of age), growth plate closure is delayed (38). Many studies have reported that neutered dogs have a significantly higher risk of developing orthopedic disorders than intact dogs. The most common orthopedic problems are cranial cruciate ligament rupture, hip dysplasia, elbow dysplasia, and osteoarthritis (39–41). The relationship between neutering and osteoarthritis is further complicated by the fact that neutered dogs are more likely to be obese (42).
Clinical signs associated with canine orthopedic disorders include limping or lameness, exercise intolerance, pain, inactivity stiffness, reduced willingness to jump up and/or down, willingness to play, aggression, vocalization, and postural shifting (43). Dogs with orthopedic diseases experience barriers such as difficulties with daily activities, which can make them dependent on their owners and dramatically compromise their welfare. Caring for dogs suffered from orthopedic diseases could be physically and emotionally demanding tasks for their caregivers. The multifaceted negative impacts of owning an osteoarthritic dog include: the stress of veterinary visits; feeling they had let their dog down by failing to find effective treatments; challenges of getting the dog to take medications; and keeping the dog at a reasonable weight and body condition score whilst on a restricted exercise regime. As a result of their pets' orthopedic conditions many dog owners have experience undesirable challenges such as financial difficulties due to treatment costs; quitting their jobs in order to take care of their dogs; changing work schedules, room layouts, vehicles and furniture; back pain from carrying or assisting big dogs up and down stairs or helping them in and out of the car (44).
1.3 Neoplasia
Neoplasia, a major cause of morbidity and mortality for pets, is one of the leading causes of concern among pet owners (45, 46). Associations have been made between the development of some types of neoplasms and neuter status as well as genetic predisposition, age, viral infection, chronic inflammation, and breed; however, the etiology is likely multifactorial and largely unknown (45–48).
Gonadectomy has the potential to decrease the incidence of certain types of neoplasia like mammary tumors, ovarian tumors, uterine neoplasms, vaginal and vulvar tumors in female (4, 5, 45–52); testicular tumors in males (53, 54). On the other hand, gonadectomy may be associated with increased risk of development of certain neoplasms such as canine prostate cancer, lymphoma, mast cell tumors, hemangiosarcoma and osteosarcoma (3, 11, 55–64).
Mammary tumors are the most frequent neoplasia in female dogs (4, 52). Delayed spaying increases the risk of developing mammary tumors (54–57). Intact female dogs are at four times greater risk of developing mammary tumors, compared to those spayed before 2 years of age (5). The incidence of mammary tumors in cats is less than half that of dogs (53). According to a study, the protective effect of spaying at an early age, displaying a 91% and 86% reduction in development of mammary tumors in cats spayed before 6 months and 7–12 months, respectively (57).
One of the most often diagnosed canine neoplasia is lymphoma (45–47). In dogs, the reported incidence of lymphoma is 1.1% (64). A comparative medicine study showed that sexually intact male dogs and neutered male and female dogs had twice the risk of developing lymphoma compared to sexually intact female dogs (65). In Golden Retrievers, neutered males were three times more likely to develop lymphoma than unaltered male. However, there was not a significant risk of developing lymphoma associated with spaying females at any age (56). Another study on Vizslas, analysis suggested that both neutered males and females were 4.3 times as likely as their sexually intact counterparts to have lymphoma. In addition, the study revealed that the odds of gonadectomized Vizslas of either sex developing mast cell tumors were 3.5 times the odds of sexually intact Vizslas developing mast cell tumors (55). However, there was not a significant difference between the incidence of mast cell tumors in males and females regardless of neuter status or time of gonadectomy in German Shepherd Dogs (57).
Neutering is associated with risk of developing splenic and cardiac hemangiosarcoma, in particular. Compared to dogs that were sexually intact, gonadectomized females younger than 12 months and gonadectomized males and females older than 12 months had a markedly higher risk of developing hemangiosarcoma (62). It has been found that spayed females have a higher risk of developing splenic and cardiac hemangioma compared to intact females (58, 66).
The most prevalent primary malignant bone tumor in dogs is osteosarcoma (49, 59, 60). Incidence of canine osteosarcoma is < 0.1% (67). Male and female Rottweilers underwent gonadectomy before the 1 year of age had an approximate one in four-lifetime risk for bone sarcoma and were significantly more likely to develop bone sarcoma than dogs that were sexually intact (61). Neuter status or age at gonadectomy does not affect development of osteosarcoma in German Shepherds (57).
Canine prostate cancers are rare (< 0.6% in necropsy studies) (68), but it is often aggressive, rapidly proliferative, and highly metastatic to the skeletal system (69). Although castration has both preventive and therapeutic effects on androgen-dependent diseases such as benign prostatic hyperplasia chronic prostatit and perineal adenomas (70–72). Several studies have shown that castrated male dogs exhibit an elevated risk of developing prostate cancer, with odds ratios ranging from 3.6 to 4.34 and experience more metastases than intact dogs (3, 11, 73–76).
Pet owners are particularly concerned about cancer since it is a major cause of morbidity and fatalities in pets (45, 46). Cancer is an emotionally charged disease (62). The burden of caregiving for a companion animal with cancer can be distressing for the owner. Recent studies indicate that pet owners experience depressive symptoms after their pet gets diagnosed with cancer (63). Silva et al. found that a significant portion of guardians of ailing animals with oncological pathologies, irrespective of their pets' conditions, faced substantial burdens, impacting their emotional, physical, and financial wellbeing (17).
1.4 Behavior
Behavioral problems are an important reason for relinquishment of pets by owners (77, 78). The most common behavioral problems of dogs include aggression toward people or other animals, inappropriate elimination, and fearful behavior (79). Neutering has a complex effect on behavior, with both beneficial and detrimental consequences documented (80, 81). Non-sexually dimorphic behaviors, such as fear-based aggression, are not affected by gonadectomy (81). Gonadectomy reduces reproductive behaviors by eliminating estrus-related actions in females and reducing roaming, mounting and urine marking in male dogs (82–84).
Although neutering is generally thought to reduce the incidence of various types of aggression, there is some evidence that it may increase some aggressive behaviors. Several studies of dogs referred for treatment of behavior problems have identified a higher proportion of spayed than intact females among animals exhibiting aggression (85, 86). Early age gonadectomy has been reported to increase noise phobia and decrease separation-related disorders, escape behaviors, and elimination when frightened (83, 87). Male and female neutered dogs are more prone to exhibit symptoms of obsessive-compulsive disorder (88, 89), stranger-directed aggression (90, 91).
Behavioral problems are a prevalent cause of the disruption of the human-animal bond, jeopardizing their mutual wellbeing and may result in pet abandonment and euthanasia (78, 92, 93).
The owners of pets with behavioral problems often feel isolated and judged due to the lack of understanding and unsupportive reactions of the trainers, veterinarians, strangers, friends, and family members (93). In order to improve the welfare of both owners and pets, practical behavioral support for the dog-human dyad, social and psychological support for owners should be provided (94). Many behavioral disorders require complex multimodal therapy including environmental management, behavior modification, changes in owner behavior and routines, and medication administration; thus, the emotional and financial efforts committed to managing a pet with behavioral disorders would be expected to lead to burdening the caregiver (93–95). Owners of pet with behavioral disorders face many challenges in their daily lives. These challenges include the extra time required for management and training, the difficulties in handling the pet in public and when alone at home, the level of planning and attention required to keep their pet and others safe, the cost of behavioral support for their pet, and how the problem limits the owner's time away from home (78).
1.5 Urinary system
In intact female dogs, the risk of urine incontinence (UI) is low (96). Approximately 75% of female dogs become incontinent within 3 years after gonadectomy, whereas UI following spaying can occur right away or up to 10 years after gonadectomy (83). Several variables, including body weight, breed, and timing of neutering, contribute to the risk of developing UI (97). O'Neill et al. reported that urinary incontinence affects just over 3% of female dogs overall but affects more than 15% of female dogs in high-risk breeds including the Irish setter, Dobermann, Bearded Collie, Rough Collie and Dalmatian (97).
Urinary incontinence is a life-long condition that requires continuous medication. UI can be distressing and frustrating for the owner and may negatively impact the interactions between owners and their pets (98). A total of 10%−20% of affected families have reported unfavorable outcomes of UI, with owners describing feelings of anger and discomfort (99) and with euthanasia of the affected animal considered in certain circumstances (100). Long-term soiling of the house due to urinary incontinence can be exasperating and put strain on the owner-pet bond, as well as requiring the investment of time and money in cleaning, repairing and sometimes even replacing soiled possessions (101).
1.6 Other disease risks
Sundburg et al. evaluated the potential association between neutering and diseases associated with immune function compromise in dogs. The authors concluded that neutered dogs had a significantly greater risk of hypoadrenocorticism, autoimmune hemolytic anemia, atopic dermatitis, hypothyroidism, inflammatory bowel disease and thrombocytopenia than intact dogs with neutered females being at greater risk than neutered males for all but hypoadrenocorticism and autoimmune hemolytic anemia. Neutered females, but not males, had a significantly greater risk of Lupus erythematosus than intact females (102). Diabetes mellitus has been reported to be more common in neutered males, but not female dogs compared to intact dogs across the whole dog population (103).
A chronic disease is a condition requiring lifelong support, protection, intermittent monitoring, and continuous treatment (104). Caregiver burden is related to treatment complexity, and notably the relationship to treatment complexity is not related to the diseases' severity. Chronic diseases like atopic dermatitis (105), inflammatory bowel disease (106), and hypoadrenocorticism (107) in a companion animal causes burden for the owner. Chronic illness also has an impact on the owners' social life, daily activities, job, finances, leisure time, travel, and family relationships (105, 108, 109).
2 Conclusions
Decision-making in gonadectomy remains controversial. It is apparent that gonadectomy has both benefits and risks for individual dogs. Given the multitude of interacting etiological factors that play a role in most serious behavioral and medical conditions, it is impossible to predict the exact outcome of neutering for any individual. Any decision to neuter a particular pet should be made considering individual circumstances, the owners' values and goals, as well as the risks and benefits determined by epidemiological data.
Veterinarians should consider possibility of caregiver burden that affects family relationships, social life, daily activities, work, finances, leisure time, and travel of the owner when recommending neutering. They should also discuss with their clients about the potential long-term complications associated with neutering and the burdens that the owners may face.
Author contributions
IB: Writing – original draft, Writing – review & editing.
Funding
The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.
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References
1. Looney AL, Bohling MW, Bushby PA, Howe LM, Griffin B, Levy JK, et al. The association of shelter veterinarians veterinary medical care guidelines for spay-neuter programs. J Am Vet Med Assoc. (2008) 233:74–86. doi: 10.2460/javma.233.1.74
2. Rosser EJ. Castration-responsive dermatosis in the dog. In:von Tscharner C, Halliwell REW, , editors. Advances in Veterinary Dermatology. London: Baillière Tindall (1990). p. 34–42.
3. Teske E, Naan EC, Van Dijk EM, Van Garderen E, Schalken JA. Canine prostate carcinoma: Epidemiological evidence of an increased risk in castrated dogs. Mol Cell Endocrinol. (2002) 197:251–5. doi: 10.1016/S0303-7207(02)00261-7
4. Reichler I. Gonadectomy in cats and dogs: a review of risks and benefits. Reprod Domest Anim. (2009) 44:29–35. doi: 10.1111/j.1439-0531.2009.01437.x
5. Schneider R, Dorn CR, Taylor DO. Factors influencing canine mammary cancer development and postsurgical survival. J Natl Cancer Inst. (1969) 43:1249–61.
6. Kustritz MV. Population control in small animals. Vet Clin. (2018) 48:721–32. doi: 10.1016/j.cvsm.2018.02.013
7. Hart BL. Effect of gonadectomy on subsequent development of age-related cognitive impairment in dogs. J Am Vet Med Assoc. (2001) 219:51–6. doi: 10.2460/javma.2001.219.51
8. Fulkerson CM, Dhawan D, Ratliff TL, Hahn NM, Knapp DW. Naturally occurring canine invasive urinary bladder cancer: a complementary animal model to improve the success rate in human clinical trials of new cancer drugs. Int J Genomics. (2017) 2017:1–9. doi: 10.1155/2017/6589529
9. Hart BL, Hart LA, Thigpen AP, Willits NH. 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
10. Cooley DM, Beranek BC, Schlittler DL, Glickman NW, Glickman LT, Waters DJ. Endogenous gonadal hormone exposure and bone sarcoma risk. Cancer Epidemiol Biomarkers Prev. (2002) 11:1434–40.
11. Polisca A, Troisi A, Fontaine E, Menchetti L, Fontbonne A, A. retrospective study of canine prostatic diseases from 2002 to 2009 at the Alfort Veterinary College in France. Theriogenology. (2016) 85:835–40. doi: 10.1016/j.theriogenology.2015.10.030
12. Zarit SH, Todd PA, Zarit JM. Subjective burden of husbands and wives as caregivers: a longitudinal study. Gerontologist. (1986) 26:260–6. doi: 10.1093/geront/26.3.260
13. Spitznagel MB, Jacobson DM, Cox MD, Carlson MD. Caregiver burden in owners of a sick companion animal: a cross-sectional observational study. Vet Rec. (2017) 181:321. doi: 10.1136/vr.104295
14. Spitznagel MB, Jacobson DM, Cox MD, Carlson MD. Predicting caregiver burden in general veterinary clients: contribution of companion animal clinical signs and problem behaviors. Vet J. (2018) 236:23–30. doi: 10.1016/j.tvjl.2018.04.007
15. Silva PT, Coura FM, Costa-Val AP. Caregiver burden in small animal clinics: a comparative analysis of dermatological and oncological cases. Animals. (2024) 14:276. doi: 10.3390/ani14020276
16. Romagnoli S, Krekeler N, de Cramer K, Kutzler M, McCarthy R, Schaefer-Somi S. WSAVA guidelines for the control of reproduction in dogs and cats. J Small Animal Pract. (2024) 65:424–559. doi: 10.1111/jsap.13724
17. Palestrini C, Mazzola SM, Caione B, Groppetti D, Pecile AM, Minero M, et al. Influence of gonadectomy on canine behavior. Animals. (2021) 11:553. doi: 10.3390/ani11020553
18. Colliard L, Ancel J, Benet JJ, Paragon BM, Blanchard G. Risk factors for obesity in dogs in France. J Nutr. (2006) 136:1951S–4S. doi: 10.1093/jn/136.7.1951S
19. McGreevy PD, Thomson PC, Pride C, Fawcett A, Grassi T, Jones B. Prevalence of obesity in dogs examined by Australian veterinary practices and the risk factors involved. Vet Rec. (2005) 156:695–702. doi: 10.1136/vr.156.22.695
20. Colliard L, Paragon BM, Lemuet B, Bénet JJ, Blanchard G. Prevalence and risk factors of obesity in an urban population of healthy cats. J Feline Med Surg. (2009) 11:135–40. doi: 10.1016/j.jfms.2008.07.002
21. German A. The growing problem of obesity in dogs and cats. J Nutr. (2006) 13:1940S–5S. doi: 10.1093/jn/136.7.1940S
22. Flynn MF, Hardie EM, Armstrong PJ. Effect of ovariohysterectomy on maintenance energy requirement in cats. J Am Vet Med Assoc. (1996) 209:1572–81. doi: 10.2460/javma.1996.209.09.1572
23. Kanchuk ML, Backus RC, Morris JG, Rogers QR, Calvert CC. Weight gain in gonadectomized normal and lipoprotein lipase–deficient male domestic cats results from increased food intake and not decreased energy expenditure. J Nutr. (2003) 133:1866–74. doi: 10.1093/jn/133.6.1866
24. Martin L, Siliart B, Dumon H, Backus R, Biourge V, Nguyen P. Leptin, body fat content and energy expenditure in intact and gonadectomized adult cats: a preliminary study. J Animal Physiol Animal Nutr. (2001) 85:195–9. doi: 10.1046/j.1439-0396.2001.00322.x
25. Nguyen PG, Dumon HJ, Siliart BS, Martin LJ, Sergheraert R, Biourge VC. Effects of dietary fat and energy on body weight and composition after gonadectomy in cats. Am J Vet Res. (2004) 65:1708–13. doi: 10.2460/ajvr.2004.65.1708
26. Goggin JM, Schryver HF, Hintz HF. The effects of ad libitum feeding and caloric dilution on the domestic cat's ability to maintain energy balance. Feline Pract. (1993) 21:7–11. Available at: https://www.cabidigitallibrary.org/doi/full/10.5555/19942204457
27. Houpt KA, Coren B, Hintz HF, Hilderbrant JE. Effect of sex and reproductive status on sucrose preference, food intake, and body weight of dogs. J Am Vet Med Assoc. (1979) 174:1083–5.
28. Flanagan J, Bissot T, Hours MA, Moreno B, Feugier A, German AJ. Success of a weight loss plan for overweight dogs: the results of an international weight loss study. PLoS ONE. (2017) 12:e0184199 doi: 10.1371/journal.pone.0184199
29. Lund EM, Armstrong PJ, Kirk CA, Klausner JS. Prevalence and risk factors for obesity in adult cats from private US veterinary practices. Intern J Appl Res Vet Med. (2005) 3:88–96. Available at: https://citeseerx.ist.psu.edu/document?repid=rep1&type=pdf&doi=c86945c7ff47c2bc22f01dc58f82c518f2219c92
30. Lund EM, Armstrong PJ, Kirk CA, Klausner JS. Prevalence and risk factors for obesity in adult dogs from private US veterinary practices. Int J Appl Res Vet Med. (2006) 4:177. Available at: https://opis-cdn.tinkoffjournal.ru/mercury/expensive-dogs-Lund.pdf
31. Lekcharoensuk C, Lulich JP, Osborne CA, Koehler LA, Urlich LK, Carpenter KA, et al. Association between patient-related factors and risk of calcium oxalate and magnesium ammonium phosphate urolithiasis in cats. J Am Vet Med Assoc. (2000) 217:520–5. doi: 10.2460/javma.2000.217.520
32. Weeth LP. Other risks/possible benefits of obesity. Vet Clin. (2016) 46:843–53. doi: 10.1016/j.cvsm.2016.04.007
33. Bomberg E, Birch L, Endenburg N, German AJ, Neilson J, Seligman H, et al. The financial costs, behaviour and psychology of obesity: a one health analysis. J Comp Pathol. (2017) 156:310–25. doi: 10.1016/j.jcpa.2017.03.007
34. Shepherd M. Canine and feline obesity management. Vet Clin. (2021) 51:653–67. doi: 10.1016/j.cvsm.2021.01.005
35. Banfield® Pet Hospitals. Obesity in dogs and cats – state of pet health report. In: Obesity in Dogs and Cats – State of Pet Health Report. Available at: https://www.banfield.com/state-of-pet-health/obesity (accessed 1 November 2024).
36. Larsen JA. Risk of obesity in the neutered cat. J Feline Med Surg. (2017) 19:779–83. doi: 10.1177/1098612X16660605
37. Baptista da Silva C, Lyu Y, Ruiz-Suárez N, Pastoor F, Heip L, Wambacq W, et al. Survey of Belgian owners' perspectives on quality of life and difficulties during a weight-loss programme in obese cats. J Feline Med Surg. (2022) 24:e513–23. doi: 10.1177/1098612X221121920
38. Kustritz MV. Determining the optimal age for gonadectomy of dogs and cats. J Am Vet Med Assoc. (2007) 231:1665–75. doi: 10.2460/javma.231.11.1665
39. Whitehair JG, Vasseur PB, Willits NH. Epidemiology of cranial cruciate ligament rupture in dogs. J Am Vet Med Assoc. (1993) 203:1016–9. doi: 10.2460/javma.1993.203.07.1016
40. Duval JM, Budsberg SC, Flo GL, Sammarco JL. Breed, sex, and body weight as risk factors for rupture of the cranial cruciate ligament in young dogs. J Am Vet Med Assoc. (1999) 215:811–4. doi: 10.2460/javma.1999.215.06.811
41. Slauterbeck JR, Pankratz K, Xu KT, Bozeman SC, Hardy DM. Canine ovariohysterectomy and orchiectomy increases the prevalence of ACL injury. Clin Orthop Relat Res. (2004) 429:301–5. doi: 10.1097/01.blo.0000146469.08655.e2
42. Graves JL, McKenzie BA, Koch Z, Naka A, Spofford N, Morrison J. Body weight, gonadectomy, and other risk factors for diagnosis of osteoarthritis in companion dogs. Front Vet Sci. (2023) 10:1275964. doi: 10.3389/fvets.2023.1275964
43. Belshaw Z, Dean R, Asher L. Could it be osteoarthritis? How dog owners and veterinary surgeons describe identifying canine osteoarthritis in a general practice setting. Prevent Vet Med. (2020) 185:105198. doi: 10.1016/j.prevetmed.2020.105198
44. Belshaw Z, Dean R, Asher L. “You can be blind because of loving them so much”: the impact on owners in the United Kingdom of living with a dog with osteoarthritis. BMC Vet Res. (2020) 16:190. doi: 10.1186/s12917-020-02404-5
45. Dobson JM. Breed-predispositions to cancer in pedigree dogs. Int Scholar Res Notices. (2013) 2013:941275. doi: 10.1155/2013/941275
46. Adams VJ, Evans KM, Sampson J, Wood JL. Methods and mortality results of a health survey of purebred dogs in the UK. J Small Animal Pract. (2010) 51:512–24. doi: 10.1111/j.1748-5827.2010.00974.x
47. Vail DM, Thamm DH, Liptak JM. Hematopoietic tumors. Withrow MacEwen's Small Animal Clin Oncol. (2019) 2019:688–772. doi: 10.1016/B978-0-323-59496-7.00033-5
48. Houlihan KE. A literature review on the welfare implications of gonadectomy of dogs. J Am Vet Med Assoc. (2017) 250:1155–66. doi: 10.2460/javma.250.10.1155
49. Robbins M. Reproductive oncology. In:Slatter DH, , editor. Textbook of Small Animal Surgery. London: Saunders (2003). p. 2437–43.
50. Salas Y, Márquez A, Diaz D, Romero L. Epidemiological study of mammary tumors in female dogs diagnosed during the period 2002-2012: a growing animal health problem. PLoS ONE. (2015) 10:e0127381. doi: 10.1371/journal.pone.0127381
51. Benavente M, Bianchi P, Aba M. Canine mammary tumors: risk factors, prognosis and treatments. J Vet Adv. (2016) 6:1291–300. doi: 10.5455/jva.20160916045115
52. Overley B, Shofer FS, Goldschmidt MH, Sherer D, Sorenmo KU. Association between ovariohysterectomy and feline mammary carcinoma. J Vet Intern Med. (2005) 19:560–3. doi: 10.1111/j.1939-1676.2005.tb02727.x
53. Ley WB, Holyoak GR, Digrassie WA. Testicular and epididymal disorders. In:Kustritz VR, , editor. Small Animal Theriogenology. Philadelphia, PA: Elsevier (2003). p. 457–91. doi: 10.1016/B978-0-7506-7408-9.50022-0
54. White RA. British small animal veterinary association. Man Small Animal Oncol. (1991) 1991:306–7.
55. Zink MC, Farhoody P, Elser SE, Ruffini LD, Gibbons TA, Rieger RH. Evaluation of the risk and age of onset of cancer and behavioral disorders in gonadectomized Vizslas. J Am Vet Med Assoc. (2014) 244:309–19. doi: 10.2460/javma.244.3.309
56. de la Riva GT, Hart BL, Farver TB, Oberbauer AM, Messam LL, Willits N, et al. Neutering dogs: effects on joint disorders and cancers in golden retrievers. PLoS ONE. (2013) 8:e55937. doi: 10.1371/journal.pone.0055937
57. Hart BL, Hart LA, Thigpen AP, Willits NH. Neutering of German shepherd dogs: associated joint disorders, cancers and urinary incontinence. Vet Med Sci. (2016) 2:191–9. doi: 10.1002/vms3.34
58. Prymak C, McKee LJ, Goldschmidt MH, Glickman LT. Epidemiologic, clinical, pathologic, and prognostic characteristics of splenic hemangiosarcoma and splenic hematoma in dogs: 217 cases (1985). J Am Vet Med Assoc. (1988) 193:706–12.
59. Endicott M. Principles of treatment for osteosarcoma. Clin Techniq Small Animal Pract. (2003) 18:110–4. doi: 10.1053/svms.2003.36626
60. Hart BL, Brodey RS, Riser WH. 7 Canine osteosarcoma: a clinicopathologic study of 194 cases. Clin Orthop Related Res. (1969) 62:54–64. doi: 10.1097/00003086-196901000-00008
61. Ru G, Terracini B, Glickman LT. Host related risk factors for canine osteosarcoma. Vet J. (1998) 156:31–9. doi: 10.1016/S1090-0233(98)80059-2
62. Hetts S, Lagoni L. The owner of the pet with cancer. Vet Clin N Am. (1990) 20:879–96. doi: 10.1016/S0195-5616(90)50076-5
63. Shaevitz MH, Tullius JA, Callahan RT, Fulkerson CM, Spitznagel MB. Early caregiver burden in owners of pets with suspected cancer: owner psychosocial outcomes, communication behavior, and treatment factors. J Vet Int Med. (2020) 34:2636–44. doi: 10.1111/jvim.15905
64. Dobson JM, Samuel S, Milstein H, Rogers K, Wood JL. Canine neoplasia in the UK: estimates of incidence rates from a population of insured dogs. J Small Animal Pract. (2002) 43:240–6. doi: 10.1111/j.1748-5827.2002.tb00066.x
65. Villamil JA, Henry CJ, Hahn AW, Bryan JN, Tyler JW, Caldwell CW. Hormonal and sex impact on the epidemiology of canine lymphoma. J Cancer Epidemiol. (2009) 2009:591753. doi: 10.1155/2009/591753
66. Ware WA, Hopper DL. Cardiac tumors in dogs: 1982–1995. J Vet Internal Med. (1999) 13:95–103. doi: 10.1111/j.1939-1676.1999.tb01136.x
67. Dorn CR, Taylor DO, Schneider R, Hibbard HH, Klauber MR. 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) 40:307–18.
68. Weaver AD. Fifteen cases of prostatic carcinoma in the dog. Vet Rec. (1981) 109:71–5. doi: 10.1136/vr.109.4.71
69. Waters DJ, Sakr WA, Hayden DW, Lang CM, McKinney L, Murphy GP, et al. Workgroup 4: spontaneous prostate carcinoma in dogs and nonhuman primates. Prostate. (1998) 36:64–7. doi: 10.1002/(SICI)1097-0045(19980615)36:1<64::AID-PROS12>3.0.CO;2-G
70. Juniewicz PE, Berry SJ, Coffey DS, Strandberg JD, Ewing LL. The requirement of the testis in establishing the sensitivity of the canine prostate to develop benign prostatic hyperplasia. J Urol. (1994) 152:996–1001. doi: 10.1016/S0022-5347(17)32641-1
71. Renggli M, Padrutt I, Michel E, Reichler I. Benign prostatic hyperplasia: treatment options in the dog. Schweizer Archiv fur Tierheilkunde. (2010) 152:279–84. doi: 10.1024/0036-7281/a000065
72. Park C, Yoo JH, Kim HJ, Lim CY, Kim JW, Lee SY, et al. Cyclosporine treatment of perianal gland adenoma concurrent with benign prostatic hyperplasia in a dog. Canad Vet J. (2010) 51:1279.
73. Sorenmo KU, Goldschmidt M, Shofer F, Goldkamp C, Ferracone J. Immunohistochemical characterization of canine prostatic carcinoma and correlation with castration status and castration time. Vet Comp Oncol. (2003) 1:48–56. doi: 10.1046/j.1476-5829.2003.00007.x
74. Bryan JN, Keeler MR, Henry CJ, Bryan ME, Hahn AW, Caldwell CW. A population study of neutering status as a risk factor for canine prostate cancer. Prostate. (2007) 67:1174–81. doi: 10.1002/pros.20590
75. Cornell KK, Bostwick DG, Cooley DM, Hall G, Harvey HJ, Hendrick MJ, et al. Clinical and pathologic aspects of spontaneous canine prostate carcinoma: a retrospective analysis of 76 cases. Prostate. (2000) 45:173–83. doi: 10.1002/1097-0045(20001001)45:2<173::AID-PROS12>3.3.CO;2-I
76. Bell FW, Klausner JS, Hayden DW, Feeney DA, Johnston SD. Clinical and pathologic features of prostatic adenocarcinoma in sexually intact and castrated dogs: 31 cases (1970-1987). J Am Vet Med Assoc. (1991) 199:1623–30. doi: 10.2460/javma.1991.199.11.1623
77. Casey RA, Vandenbussche S, Bradshaw JWS, Roberts MA. Reasons for relinquishment and return of domestic cats (Felis Silvestris Catus) to rescue shelters in the UK. Anthrozoös. (2009) 22:347–58. doi: 10.2752/089279309X12538695316185
78. Kwan JY, Bain MJ. Owner attachment and problem behaviors related to relinquishment and training techniques of dogs. J Appl Anim Welf Sci. (2013) 16:168–83. doi: 10.1080/10888705.2013.768923
80. McKenzie B. Evaluating the benefits and risks of neutering dogs and cats. CABI Rev. (2010) 5:1–18. doi: 10.1079/PAVSNNR20105045
82. Phoenix CH, Slob AK, Goy RW. Effects of castration and replacement therapy on sexual behavior of adult male rhesuses. J Comp Physiol Psychol. (1973) 84:472. doi: 10.1037/h0034855
83. Spain CV, Scarlett JM, Houpt KA. Long-term risks and benefits of early-age gonadectomy in dogs. J Am Vet Med Assoc. (2004) 224:380–7. doi: 10.2460/javma.2004.224.380
84. Col R, Day C, Phillips CJ. An epidemiological analysis of dog behavior problems presented to an Australian behavior clinic, with associated risk factors. J Vet Behav. (2016) 15:1–11. doi: 10.1016/j.jveb.2016.07.001
85. Borchelt PL. Aggressive behavior of dogs kept as companion animals: classification and influence of sex, reproductive status, and breed. Appl Anim Ethol. (1983) 10:45–61. doi: 10.1016/0304-3762(83)90111-6
86. Gershman KA, Sacks JJ, Wright JC. Which dogs bite? A case-control study of risk factors. Pediatrics. (1994) 93:913–7. doi: 10.1542/peds.93.6.913
87. Balogh O, Borruat N, Andrea Meier A, Hartnack S, Reichler IM. The influence of spaying and its timing relative to the onset of puberty on urinary and general behaviour in Labrador Retrievers. Reproduct Domestic Animals. (2018) 53:1184–90. doi: 10.1111/rda.13225
88. Overall KL, Dunham AE. Clinical features and outcome in dogs and cats with obsessive-compulsive disorder: 126 cases (1989–2000). J Am Vet Med Assoc. (2002) 221:1445–52. doi: 10.2460/javma.2002.221.1445
89. 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) 5:18. doi: 10.3389/fvets.2018.00018
90. Dinwoodie IR, Dwyer B, Zottola V, Gleason D, Dodman NH. Demographics and comorbidity of behavior problems in dogs. J Vet Behav. (2019) 32:62–71. doi: 10.1016/j.jveb.2019.04.007
91. 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) 211:180–2. doi: 10.2460/javma.1997.211.02.180
92. New Jr JC, Salman MD, King M, Scarlett JM, Kass PH, Hutchison JM. Characteristics of shelter-relinquished animals and their owners compared with animals and their owners in US pet-owning households. J Appl Animal Welfare Sci. (2000) 3:179–201. doi: 10.1207/S15327604JAWS0303_1
93. Buller K, Ballantyne KC. Living with and loving a pet with behavioral problems: pet owners' experiences. J Vet Behav. (2020) 37:41–7. doi: 10.1016/j.jveb.2020.04.003
94. Barcelos AM, Kargas N, Mills D. The effects of dog behavioural problems on owner well-being: a review of the literature and future directions. InPets. (2024) 1:53–69. doi: 10.3390/pets1010007
95. Kuntz K, Ballantyne KC, Cousins E, Spitznagel MB. Assessment of caregiver burden in owners of dogs with behavioral problems and factors related to its presence. J Vet Behav. (2023) 64:41–6. doi: 10.1016/j.jveb.2023.05.006
96. Angioletti A, De Francesco I, Vergottini M, Battocchio ML. Urinary incontinence after spaying in the bitch: incidence and oestrogen-therapy. Vet Res Commun. (2004) 28:153–5. doi: 10.1023/B:VERC.0000045394.31433.9e
97. O'Neill DG, Riddell A, Church DB, Owen L, Brodbelt DC, Hall JL. Urinary incontinence in bitches under primary veterinary care in England: prevalence and risk factors. J Small Animal Pract. (2017) 58:685–93. doi: 10.1111/jsap.12731
98. Borns-Weil S. Inappropriate urination. Vet Clin Small Animal Pract. (2019) 49:141–55. doi: 10.1016/j.cvsm.2018.10.003
99. De Bleser B, Brodbelt DC, Gregory NG, Martinez TA. The association between acquired urinary sphincter mechanism incompetence in bitches and early spaying: a case-control study. Vet J. (2011) 187:42–7. doi: 10.1016/j.tvjl.2009.11.004
100. Schaer M, Gaschen F, Walton S, editors. Clinical Medicine of the Dog and Cat. CRC Press (2022). doi: 10.1201/9781003254591
101. Tomlinson C. Toileting troubles part 1: factors influencing house soiling in cats and dogs. Comp Animal. (2016) 21:351–7. doi: 10.12968/coan.2016.21.6.351
102. Sundburg CR, Belanger JM, Bannasch DL, et al. Gonadectomy effects on the risk of immune disorders in the dog: a retrospective study. BMC Vet Res. (2016) 12:278–88. doi: 10.1186/s12917-016-0911-5
103. Mattin MJ, O'Neill D, Church D, McGreevy PD, Thomson PC, Brodbelt D. An epidemiological study of diabetes mellitus in dogs attending first opinion practice in the UK. Vet Rec. (2014) 174:349. doi: 10.1136/vr.101950
104. Yigitalp G, Surucu HA, Gumus F, Evinc E. Predictors of caregiver burden in primary caregivers of chronic patients. Int J Caring Sci. (2017) 10:1168. Available at: http://www.internationaljournalofcaringsciences.org/docs/7_3.pdf
105. Spitznagel MB, Hillier A, Gober M, Carlson MD. Treatment complexity and caregiver burden are linked in owners of dogs with allergic/atopic dermatitis. Vet Dermatol. (2021) 32:e192–e50. doi: 10.1111/vde.12938
106. Díaz-Regañón D, Sainz Á, Rodríguez-Franco F, Villaescusa A, Olmeda P, Morcillo A, et al. Assessing the quality of life of dogs with inflammatory bowel disease and their owners. Vet Sci. (2023) 10:405. doi: 10.3390/vetsci10070405
107. Hupfeld J, Dölle M, Volk H, Rieder J. Effect of long-term management of hypoadrenocorticism on the quality of life of affected dogs and their owners. Vet Rec. (2022) 191:1977. doi: 10.1002/vetr.1977
108. Freeman LM, Rush JE, Clark MA, Bulmer BJ. Validation and preliminary data from a health-related quality of life questionnaire for owners of dogs with cardiac disease. J Vet Internal Med. (2020) 34:1119–26. doi: 10.1111/jvim.15791
Keywords: gonadectomy, neutering, dog, neutering risks, caregiver burden
Citation: Bastan I (2025) Possible relationship between long-term post neutering complications in dogs and caregiver burden in the owners. Front. Vet. Sci. 12:1532039. doi: 10.3389/fvets.2025.1532039
Received: 21 November 2024; Accepted: 02 January 2025;
Published: 17 January 2025.
Edited by:
Calogero Stelletta, University of Padua, ItalyReviewed by:
Sven Reese, Ludwig Maximilian University of Munich, GermanyCopyright © 2025 Bastan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Idil Bastan, aWRpbGJhc3RhbkBnbWFpbC5jb20=