Dog Neuter, Yes or No? A Summary of the Motivations, Benefits, and Harms, with Special Emphasis on the Behavioral Aspect
Simple Summary
Abstract
1. Introduction
2. The Behavior Consequences of Dog Neutering
2.1. The 1970–1990s
2.2. From the 2000s Onwards
3. Hormonal Changes Associated with Neutering
4. Alternatives to Gonadal Removal
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Statista. Available online: https://www.statista.com/statistics/515010/pet-population-european-union-eu-by-animal/ (accessed on 10 October 2024).
- World Population Review. Available online: https://worldpopulationreview.com/country-rankings/dog-population-by-country (accessed on 10 October 2024).
- Holland, K.E. Acquiring a Pet Dog: A Review of Factors Affecting the Decision-Making of Prospective Dog Owners. Animals 2019, 9, 124. [Google Scholar] [CrossRef]
- Holland, K.E.; Mead, R.; Casey, R.A.; Upjohn, M.M.; Christley, R.M. Why Do People Want Dogs? A Mixed-Methods Study of Motivations for Dog Acquisition in the United Kingdom. Front. Vet. Sci. 2022, 9, 877950. [Google Scholar] [CrossRef] [PubMed]
- Jagoe, A.; Serpell, J. Owner characteristics and interactions and the prevalence of canine behaviour problems. Appl. Anim. Behav. Sci. 1996, 47, 31–42. [Google Scholar] [CrossRef]
- Ortega-Pacheco, A.; Bolio-Gonzalez, M.E.; Colin-Flores, R.F.; Sauri-Arceo, C.H.; Gutierrez-Blanco, E.; Jimenez-Coello, M.; Linde Forsberg, C. Evaluation of a Burdizzo castrator for neutering of dogs. Reprod. Domest. Anim. 2006, 41, 227–232. [Google Scholar] [CrossRef] [PubMed]
- Packer, R.M.A.; Brand, C.L.; Belshaw, Z.; Pegram, C.L.; Stevens, K.B.; O’Neill, D.G. Pandemic Puppies: Characterising Motivations and Behaviours of UK Owners Who Purchased Puppies during the 2020 COVID-19 Pandemic. Animals 2021, 11, 2500. [Google Scholar] [CrossRef]
- Powell, L.; Chia, D.; McGreevy, P.; Podberscek, A.L.; Edwards, K.M.; Neilly, B.; Guastella, A.J.; Lee, V.; Stamatakis, E. Ex-pectations for dog ownership: Perceived physical, mental and psychosocial health consequences among prospective adopters. PLoS ONE 2018, 13, e0200276. [Google Scholar] [CrossRef] [PubMed]
- Bauman, A.E.; Russell, S.J.; Furber, S.E.; Dobson, A.J. The epidemiology of dog walking: An unmet need for human and canine health. Med. J. Aust. 2001, 175, 632–634. [Google Scholar] [CrossRef]
- Levine, G.N.; Allen, K.; Braun, L.T.; Christian, H.E.; Friedmann, E.; Taubert, K.A.; Thomas, S.A.; Wells, D.L.; Lange, R.A. Pet Ownership and Cardiovascular Risk. Circulation 2013, 127, 2353–2363. [Google Scholar] [CrossRef]
- Serpell, J. Beneficial Effects of Pet Ownership on Some Aspects of Human Health and Behaviour. J. R. Soc. Med. 1991, 84, 717–720. [Google Scholar] [CrossRef]
- Thorpe, R.J.; Simonsick, E.M.; Brach, J.S.; Ayonayon, H.; Satterfield, S.; Harris, T.B.; Garcia, M.; Kritchevsky, S.B. Dog Ownership, Walking Behavior, and Maintained Mobility in Late Life. J. Am. Geriatr. Soc. 2006, 54, 1419–1424. [Google Scholar] [CrossRef]
- Teo, J.T.; Johnstone, S.J.; Römer, S.S.; Thomas, S.J. Psychophysiological mechanisms underlying the potential health benefits of human-dog interactions: A systematic literature review. Int. J. Psychophysiol. 2022, 180, 27–48. [Google Scholar] [CrossRef]
- Pew Research Center. Available online: https://www.pewresearch.org/short-reads/2023/07/07/about-half-us-of-pet-owners-say-their-pets-are-as-much-a-part-of-their-family-as-a-human-member/ (accessed on 12 October 2024).
- Greenebaum, J. It’s a Dog’s Life: Elevating Status from Pet to “Fur Baby” at Yappy Hour. Soc. Anim. 2004, 12, 117–135. [Google Scholar] [CrossRef]
- Shelter Animal County. Available online: https://www.shelteranimalscount.org/2024-mid-year-report (accessed on 20 October 2024).
- Houpt, K.A.; Honig, S.U.; Reisner, I.R. Breaking the human-companion animal bond. J. Am. Vet. Med. Assoc. 1996, 208, 1653–1659. [Google Scholar] [CrossRef] [PubMed]
- Diesel, G.; Brodbelt, D.; Pfeiffer, D.U. Characteristics of Relinquished Dogs and Their Owners at 14 Rehoming Centers in the United Kingdom. J. Appl. Anim. Welf. Sci. 2010, 13, 15–30. [Google Scholar] [CrossRef] [PubMed]
- Miller, D.D.; Staats, S.R.; Partlo, C.; Rada, K. Factors associated with the decision to surrender a pet to an animal shelter. J. Am. Vet. Med. Assoc. 1996, 209, 738–742. [Google Scholar] [CrossRef] [PubMed]
- Salman, M.D.; New, J.G., Jr.; Scarlett, J.M.; Kass, P.H.; Ruch-Gallie, R.; Hetts, S. Human and Animal Factors Related to Re-linquishment of Dogs and Cats in 12 Selected Animal Shelters in the United States. J. Appl. Anim. Welf. Sci. 1998, 1, 207–226. [Google Scholar] [CrossRef]
- Kisley, M.A.; Chung, E.J.; Levitt, H. Investigating the Reasons behind Companion Animal Relinquishment: A Systematic Content Analysis of Shelter Records for Cats and Dogs, 2018–2023. Animals 2024, 14, 2606. [Google Scholar] [CrossRef]
- Patronek, G.J.; Bradley, J.; Arps, E. Saving Normal: A new look at behavioral incompatibilities and dog relinquishment to shelters. J. Vet. Behav. 2021, 49, 36–45. [Google Scholar] [CrossRef]
- Trevejo, R.; Yang, M.; Lund, E.M. Epidemiology of surgical castration of dogs and cats in the United States. J. Am. Vet. Med. Assoc. 2011, 238, 898–904. [Google Scholar] [CrossRef]
- Diesel, G.; Brodbelt, D.; Laurence, C. Survey of veterinary practice policies and opinions on neutering dogs. Vet. Rec. 2010, 166, 455–458. [Google Scholar] [CrossRef]
- Downes, M.J.; Devitt, C.; Downes, M.T.; More, S.J. Neutering of cats and dogs in Ireland; pet owner self reported perceptions of enabling and disabling factors in the decision to neuter. Peer J. 2015, 3, e1196. [Google Scholar] [CrossRef]
- Michigan State University. Available online: https://www.animallaw.info/intro/state-spay-and-neuter-laws (accessed on 13 October 2024).
- Fossati, P. Spay/neuter laws as a debated approach to stabilizing the populations of dogs and cats: An overview of the European legal framework and remarks. J. Appl. Anim. Welf. Sci. 2022, 27, 281–293. [Google Scholar] [CrossRef]
- Houlihan, K.E. A literature review on the welfare implications of gonadectomy of dogs. J. Am. Vet. Med. Assoc. 2017, 250, 1155–1166. [Google Scholar] [CrossRef] [PubMed]
- Root Kustritz, M.V. Effects of surgical sterilization on canine and feline health and on society. Reprod. Domest. Anim. 2012, 47, 214–222. [Google Scholar] [CrossRef]
- Root Kustritz, M.V.; Slater, M.R.; Weedon, G.R.; Bushby, P.A. Determining optimal age for gonadectomy in the dog: A critical review of the literature to guide decision making. Clin. Theriogenology 2017, 9, 167–211. [Google Scholar]
- Mckenzie, B. Evaluating the benefits and risks of neutering dogs and cats. CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 2010, 5, 1–18. [Google Scholar] [CrossRef]
- Reichler, I.M. Gonadectomy in cats and dogs: A review of risks and benefits. Reprod. Domest. Anim. 2009, 44, 29–35. [Google Scholar] [CrossRef]
- Salmeri, K.R.; Olson, P.N.; Bloomberg, M.S. Elective gonadectomy in dogs: A review. J. Am. Vet. Med. Assoc. 1991, 198, 1183–1192. [Google Scholar]
- Urfer, S.R.; Kaeberlein, M. Desexing Dogs: A Review of the Current Literature. Animals 2019, 9, 1086. [Google Scholar] [CrossRef]
- Beauvais, W.; Cardwell, J.M.; Brodbelt, D.C. The effect of neutering on the risk of mammary tumours in dogs--a systematic review. J. Small Anim. Pract. 2012, 53, 314–322. [Google Scholar] [CrossRef]
- Schrank, M.; Romagnoli, S. Prostatic Neoplasia in the Intact and Castrated Dog: How Dangerous is Castration? Animals 2020, 10, 85. [Google Scholar] [CrossRef] [PubMed]
- Kutzler, M.A. Possible Relationship between Long-Term Adverse Health Effects of Gonad-Removing Surgical Sterilization and Luteinizing Hormone in Dogs. Animals 2020, 10, 599. [Google Scholar] [CrossRef]
- Zwida, K.; Kutzler, M.A. 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. [Google Scholar]
- Cocia, R.I.; Rusu, A.S. Attitudes of Romanian Pet Caretakers towards Sterilization of Their Animals: Gender Conflict Over Male, but Not Female, Companion Animals. Anthrozoös 2010, 23, 185–191. [Google Scholar] [CrossRef]
- McKay, S.A.; Farnworth, M.J.; Waran, N.K. Current Attitudes Toward, and Incidence of, Sterilization of Cats and Dogs by Caregivers (Owners) in Auckland, New Zealand. J. Appl. Anim. Welf. Sci. 2009, 12, 331–344. [Google Scholar] [CrossRef] [PubMed]
- Egwu, G.O.; Mamza, S.A.; Mshelia, G.D.; UBA, M.A. Preponderances of dog owners to neutering of companion animals: A survey of dog owners in Maiduguri metropolis, Borno State, Nigeria. Med. Res. Chron. 2016, 3, 388–399. [Google Scholar]
- Wongsaengchan, C.; McKeegan, D. The Views of the UK Public Towards Routine Neutering of Dogs and Cats. Animals 2019, 9, 138. [Google Scholar] [CrossRef]
- Ong, D.; Barboza de Moura Santos, M.J.; Thomsen, D.A.; Feakes, A.M. Australian owners’ attitudes and experiences of having a dog neutered. Aust. Vet. Pract. 2017, 47, 102–108. [Google Scholar]
- Kriese, M.; Kuźniewska, E.; Gugołek, A.; Strychalski, J. Reasons for and Behavioral Consequences of Male Dog Castration—A Questionnaire Study in Poland. Animals 2022, 12, 1883. [Google Scholar] [CrossRef]
- Roulaux, P.E.M.; van Herwijnen, I.R.; Beerda, B. Self-reports of Dutch dog owners on received professional advice, their opinions on castration and behavioural reasons for castrating male dogs. PLoS ONE 2020, 15, e0234917. [Google Scholar] [CrossRef]
- Da Costa, R.E.P.; Kinsman, R.H.; Owczarczak-Garstecka, S.C.; Casey, R.A.; Tasker, S.; Knowles, T.G.; Woodward, J.L.; Lord, M.S.; Murray, J.K. Age of sexual maturity and factors associated with neutering dogs in the UK and the Republic of Ireland. Vet. Rec. 2022, 191, e1265. [Google Scholar] [CrossRef] [PubMed]
- Reisner, I.R.; Houpt, K.A.; Shofer, F.S. National survey of owner-directed aggression in English Springer Spaniels. J. Am. Vet. Med. Assoc. 2005, 227, 1594–1603. [Google Scholar] [CrossRef]
- Hopkins, S.G.; Schubert, T.A.; Hart, B.L. Castration of adult male dogs: Effects on roaming, aggression, urine marking, and mounting. J. Am. Vet. Med. Assoc. 1976, 168, 1108–1110. [Google Scholar] [CrossRef] [PubMed]
- Maarschalkerweerd, R.J.; Endenburg, N.; Kirpensteijn, J.; Knol, B.W. Influence of orchiectomy on canine behaviour. Vet. Rec. 1997, 140, 617–619. [Google Scholar] [CrossRef] [PubMed]
- Knol, B.W.; Egberink-Alink, S.T. Treatment of problem behaviour in dogs and cats by castration and progestagen admin-istration: A review. Vet. Q. 1989, 11, 102–107. [Google Scholar] [CrossRef]
- Neilson, J.C.; Eckstein, R.A.; Hart, B.L. Effects of castration on problem behaviors in male dogs with reference to age and duration of behavior. J. Am. Vet. Med. Assoc. 1997, 211, 180–182. [Google Scholar]
- Hakanen, E.; Mikkola, S.; Salonen, M.; Puurunen, J.; Sulkama, S.; Araujo, C.; Lohi, H. Active and social life is associated with lower non-social fearfulness in pet dogs. Sci. Rep. 2020, 10, 13774. [Google Scholar] [CrossRef]
- Kaufmann, C.A.; 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, 22–37. [Google Scholar] [CrossRef]
- Kolkmeyer, C.A.; Schmitz, J.; Gansloßer, U. Behavioural correlates of Neutering Male Dogs—A question of Breed. J. Veter. Sci. Med. 2021, 9, 1–6. [Google Scholar] [CrossRef]
- Kolkmeyer, C.A.; Zambrano Cardona, A.M.; Gansloßer, U. Personality Unleashed: Surveying Correlation of Neuter Status and Social Behaviour in Mixed-Breed Male Dogs across Weight Classes. Animals 2024, 14, 2445. [Google Scholar] [CrossRef]
- McGreevy, P.D.; Wilson, B.; Starling, M.J.; Serpell, J.A. Behavioural risks in male dogs with minimal lifetime exposure to gonadal hormones may complicate population-control benefits of desexing. PLoS ONE 2018, 13, e0196284. [Google Scholar] [CrossRef] [PubMed]
- Starling, M.; Fawcett, A.; Wilson, B.; Serpell, J.; McGreevy, P. Behavioural risks in female dogs with minimal lifetime exposure to gonadal hormones. PLoS ONE 2019, 14, e0223709. [Google Scholar] [CrossRef]
- Farhoody, P.; Mallawaarachchi, I.; Tarwater, P.M.; Serpell, J.A.; Duffy, D.L.; Zink, C. Aggression toward Familiar People, Strangers, and Conspecifics in Gonadectomized and Intact Dogs. Front. Vet. Sci. 2018, 5, 18. [Google Scholar] [CrossRef]
- Spain, C.V.; Scarlett, J.M.; Houpt, K.A. Long-term risks and benefits of early-age gonadectomy in dogs. J. Am. Vet. Med. Assoc. 2004, 224, 380–387. [Google Scholar] [CrossRef]
- Zink, M.C.; Farhoody, P.; Elser, S.E.; Ruffini, L.D.; Gibbons, T.A.; Rieger, R.H. Evaluation of the risk and age of onset of cancer and behavioral disorders in gonadectomized Vizslas. J. Am. Vet. Med. Assoc. 2014, 244, 309–319. [Google Scholar] [CrossRef]
- Kolkmeyer, C.A.; Baum, J.; Warlich-Zach, N.; Gansloßer, U. From “Husky” to “Bulldog”- behavioural correlates between castration and breed groups in the domestic dog (Canis lupus familiaris). BMC Vet. Res. 2024, 20, 238. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Mackenzie, S.A.; Oltenacu, E.A.; Houpt, K.A. Canine behavioral genetics—A review. Appl. Anim. Behav. Sci. 1986, 15, 365–393. [Google Scholar] [CrossRef]
- Scott, J.P.; Fuller, J.L. Genetics and the Social Behavior of the Dog; University of Chicago Press: Chicago, IL, USA, 1965; ISBN 0-226-74335-7. [Google Scholar]
- Borchelt, P.L. Aggressive behavior of dogs kept as companion animals: Classification and influence of sex, reproductive status and breed. Appl.Anim. Ethol. 1983, 10, 45–61. [Google Scholar] [CrossRef]
- Wright, J.C.; Nesselrote, M.S. Classification of behavior problems in dogs: Distributions of age, breed, sex and reproductive status. Appl. Anim. Behav. Sci. 1987, 19, 169–178. [Google Scholar] [CrossRef]
- Heidenberger, E.; Unshelm, J. Changes in the behavior of dogs after castration. Tierarztl. Prax. 1990, 18, 69–75. [Google Scholar]
- O’Farrell, V.; Peachey, E. Behavioural effects of ovariohysterectomy on hitches. J. Small Anim. Pract. 2008, 31, 595–598. [Google Scholar] [CrossRef]
- Salmeri, K.R.; Bloomberg, M.S.; Scruggs, S.L.; Shille, V. Gonadectomy in immature dogs: Effects on skeletal, physical, and behavioral development. J. Am. Vet. Med. Assoc. 1991, 198, 1193–1203. [Google Scholar] [CrossRef]
- Kim, H.H.; Yeon, S.C.; Houpt, K.A.; Lee, H.C.; Chang, H.H.; Lee, H.J. Acoustic feature of barks of ovariohysterectomized and intact German Shepherd bitches. J. Vet. Med. Sci. 2005, 67, 281–285. [Google Scholar] [CrossRef] [PubMed]
- Serpell, J.A.; Hsu, Y.A. Effects of breed, sex, and neuter status on trainability in dogs. Anthrozoös 2005, 18, 196–207. [Google Scholar] [CrossRef]
- Kim, H.H.; Yeon, S.C.; Houpt, K.A.; Lee, H.C.; Chang, H.H.; Lee, H.J. Effects of ovariohysterectomy on reactivity in German Shepherd dogs. Vet. J. 2006, 172, 154–159. [Google Scholar] [CrossRef]
- Bennett, P.C.; Rohlf, V.I. Owner-companion dog interactions: Relationships between demographic variables, potentially problematic behaviours, training engagement and shared activities. Appl. Anim. Behav. Sci. 2007, 102, 65–84. [Google Scholar] [CrossRef]
- Kubinyi, E.; Turcsán, B.; Miklósi, Á. Dog and owner demographic characteristics and dog personality trait associations. Behav. Process. 2009, 81, 392–401. [Google Scholar] [CrossRef]
- Starling, M.J.; Branson, N.; Thomson, P.C.; McGreevy, P.D. Age, sex and reproductive status affect boldness in dogs. Vet. J. 2013, 197, 868–872. [Google Scholar] [CrossRef]
- Tiira, K.; Sulkama, S.; Lohi, H. Prevalence, comorbidity, and behavioral variation in canine anxiety. J. Vet. Behav. 2016, 16, 36–44. [Google Scholar] [CrossRef]
- Balint, A.; Rieger, G.; Miklosi, A.; Pongracz, P. Assessment of owner-directed aggressive behavioural tendencies of dogs in situations of possession and manipulation. R. Soc. Open Sci. 2017, 4, 171040. [Google Scholar] [CrossRef]
- Balogh, O.; Borruat, N.; Andrea Meier, A.; Hartnack, S.; Reichler, I.M. The influence of spaying and its timing relative to the onset of puberty on urinary and general behaviour in Labrador Retrievers. Reprod. Domest. Anim. 2018, 53, 1184–1190. [Google Scholar] [CrossRef] [PubMed]
- Jacobs, J.A.; Coe, J.B.; Pearl, D.L.; Widowski, T.M.; Niel, L. Factors associated with canine resource guarding behaviour in the presence of dogs: A cross-sectional survey of dog owners. Prev. Vet. Med. 2018, 161, 134–142. [Google Scholar] [CrossRef]
- Lorenz, K.P.; Kolkmeyer, C.A.; Ganslosser, U. Comparison of the Social Behaviour of Intact and Neutered Female Domestic Dogs (Canis lupus familiaris): Questionnaires and Case Studies. Dairy Vet. Sci. J. 2019, 12, 1–8. [Google Scholar]
- Fattah, A.; Hamid, S. Influence of gender, neuter status, and training method on police dog narcotics olfaction performance, behavior and welfare. J. Adv. Vet. and Anim. Res. 2020, 7, 655. [Google Scholar] [CrossRef]
- Palestrini, C.; Mazzola, S.M.; Caione, B.; Groppetti, D.; Pecile, A.M.; Minero, M.; Cannas, S. Influence of Gonadectomy on Canine Behavior. Animals 2021, 11, 553. [Google Scholar] [CrossRef]
- Moxon, R.; Freeman, S.; Payne, R.; Corr, S.A.; England, W. A Prospective Cohort Study Investigating the Behavioural De-velopment of Bitches in a Guide Dog Training Programme Neutered Prepubertally or Post-Pubertally. Front. Vet. Sci. 2022, 9, 902775. [Google Scholar] [CrossRef]
- Hsu, Y.; Serpell, J.A. Development and validation of a questionnaire for measuring behavior and temperament traits in pet dogs. J. Am.Vet. Med. Assoc. 2003, 223, 1293–1300. [Google Scholar] [CrossRef] [PubMed]
- Salonen, M.; Mikkola, S.; Hakanen, E.; Sulkama, S.; Puurunen, J.; Lohi, H. Reliability and Validity of a Dog Personality and Unwanted Behavior Survey. Animals 2021, 11, 1234. [Google Scholar] [CrossRef]
- Turcsán, B.; Kubinyi, E.; Miklósi, Á. Trainability and boldness traits differ between dog breed clusters based on conventional breed categories and genetic relatedness. Appl. Anim. Behav. Sci. 2011, 132, 61–70. [Google Scholar] [CrossRef]
- Starling, M.J.; Branson, N.; Thomson, P.C.; McGreevy, P.D. “Boldness” in the domestic dog differs among breeds and breed groups. Behav. Process. 2013, 97, 53–62. [Google Scholar] [CrossRef]
- Tong, W.H.; Abdulai-Saiku, S.; Vyas, A. Testosterone Reduces Fear and Causes Drastic Hypomethylation of Arginine Vaso-pressin Promoter in Medial Extended Amygdala of Male Mice. Front. Behav. Neurosci. 2019, 13, 33. [Google Scholar] [CrossRef]
- King, J.A.; De Oliveira, W.L.; Patel, N. Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology 2005, 30, 333–340. [Google Scholar] [CrossRef] [PubMed]
- Boissy, A.; Bouissou, M.F. Effects of Androgen Treatment on Behavioral and Physiological Responses of Heifers to Fear-Eliciting Situations. Horm. Behav. 1994, 28, 66–83. [Google Scholar] [CrossRef] [PubMed]
- Zitzmann, M. Testosterone, mood, behaviour and quality of life. Andrology 2020, 8, 1598–1605. [Google Scholar] [CrossRef] [PubMed]
- Wójcik, A.; Powierża, K. The Influence of Breed, Sex, Origin and Housing Conditions on Undesirable Behaviors in Ancient Dog Breeds. Animals 2021, 11, 1435. [Google Scholar] [CrossRef]
- Simpson, K. The Role of Testosterone in Aggression. McGill J. Med. 2020, 6. [Google Scholar] [CrossRef]
- Ayrosa, F.; Savalli, C.; Resende, B. Beyond Breeding: Re-Interpreting Paradigms in Domestic Dog Aggression Research. Estud. Psicol. 2023, 28, 26–35. [Google Scholar] [CrossRef]
- Duffy, D.L.; Hsu, Y.; Serpell, J.A. Breed differences in canine aggression. Appl. Anim. Behav. Sci. 2020, 114, 441–460. [Google Scholar] [CrossRef]
- McGreevy, P.D.; Georgevsky, D.; Carrasco, J.; Valenzuela, M.; Duffy, D.L.; Serpell, J.A. Dog behavior co-varies with height, bodyweight and skull shape. PLoS ONE. 2013, 8, e80529. [Google Scholar] [CrossRef]
- Mariti, C.; Gazzano, A.; Moore, J.L.; Baragli, P.; Chelli, L.; Sighieri, C. Perception of dogs’ stress by their owners. J. Vet. Behav. 2012, 7, 213–219. [Google Scholar] [CrossRef]
- Olson, P.N.; Bowen, R.A.; Behrendt, M.D.; Olson, J.D.; Nett, T.M. Concentrations of testosterone in canine serum during late anestrus, proestrus, estrus, and early diestrus. Am. J. Vet. Res. 1984, 45, 145–148. [Google Scholar] [CrossRef] [PubMed]
- Hydbring-Sandberg, E.; Larsson, E.; Madej, A.; Hoglund, O.V. Short-term effect of ovariohysterectomy on urine serotonin, cortisol, testosterone and progesterone in bitches. BMC Res. Notes 2021, 14, 265. [Google Scholar] [CrossRef]
- Turcu, A.; Smith, J.M.; Auchus, R.; Rainey, W.E. Adrenal androgens and androgen precursors-definition, synthesis, regulation and physiologic actions. Compr. Physiol. 2014, 4, 1369–1381. [Google Scholar] [CrossRef]
- Rosenfeld, A.J.; Lieberman, J.A.; Jarskog, L.F. Oxytocin, Dopamine, and the Amygdala: A Neurofunctional Model of Social Cognitive Deficits in Schizophrenia. Schizoph. Bull. 2010, 37, 1077–1087.doi. [Google Scholar] [CrossRef] [PubMed]
- Kirsch, P. Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans. J. Neurosci. 2005, 25, 11489–11493. [Google Scholar] [CrossRef]
- Takayanagi, Y.; Onaka, T. Roles of Oxytocin in Stress Responses, Allostasis and Resilience. Int. J. Mol. Sci. 2021, 23, 150. [Google Scholar] [CrossRef]
- Campbell, A. Oxytocin and human social behavior. Pers. Soc. Psychol. Rev. 2010, 14, 281–295. [Google Scholar] [CrossRef] [PubMed]
- Kis, A.; Ciobica, A.; Topál, J. The effect of oxytocin on human-directed social behaviour in dogs (Canis familiaris). Horm. Behav. 2017, 94, 40–52. [Google Scholar] [CrossRef]
- Nagasawa, M.; Mitsui, S.; En, S.; Ohtani, N.; Ohta, M.; Sakuma, Y.; Onaka, T.; Mogi, K.; Kikusui, T. Oxytocin-gaze positive loop and the coevolution of human-dog bonds. Science 2015, 348, 333–336. [Google Scholar] [CrossRef]
- Romero, T.; Nagasawa, M.; Mogi, K.; Hasegawa, T.; Kikusui, T. Intranasal administration of oxytocin promotes social play in domestic dogs. Commun. Integr. Biol. 2015, 8, 1–3. [Google Scholar] [CrossRef]
- Guvenc-Bayram, G.; Semen, Z.; Yalcin, M. Investigation of the Relationship between Plasma Nesfatin-1 Levels and Neutering in Dogs. Animals 2024, 14, 2854. [Google Scholar] [CrossRef]
- Nguyen, T.V.; Ducharme, S.; Karama, S. Effects of Sex Steroids in the Human Brain. Mol. Neurobiol. 2017, 54, 7507–7519. [Google Scholar] [CrossRef] [PubMed]
- Moraga-Amaro, R.; van Waarde, A.; Doorduin, J.; de Vries, E.F.J. Sex steroid hormones and brain function: PET imaging as a tool for research. J. Neuroendocrinol. 2018, 30, e12565. [Google Scholar] [CrossRef]
- Berger, M.; Gray, J.A.; Roth, B.L. The expanded biology of serotonin. Annu. Rev. Med. 2009, 60, 355–366. [Google Scholar] [CrossRef] [PubMed]
- Nordquist, N.; Oreland, L. Serotonin, genetic variability, behaviour, and psychiatric disorders—A review. Ups. J. Med. Sci. 2010, 115, 2–10. [Google Scholar] [CrossRef]
- Seo, D.; Patrick, C.J.; Kennealy, P.J. Role of Serotonin and Dopamine System Interactions in the Neurobiology of Impulsive Aggression and its Comorbidity with other Clinical Disorders. Aggress. Violent Behav. 2008, 13, 383–395. [Google Scholar] [CrossRef] [PubMed]
- Wise, R.A.; Jordan, C.J. Dopamine, behavior, and addiction. J. Biomed. Sci. 2021, 28, 83. [Google Scholar] [CrossRef]
- Mârza, S.M.; Munteanu, C.; Papuc, I.; Radu, L.; Diana, P.; Purdoiu, R.C. Behavioral, Physiological, and Pathological Approaches of Cortisol in Dogs. Animals 2024, 14, 3536. [Google Scholar] [CrossRef]
- Rosado, B.; García-Belenguer, S.; León, M.; Chacón, G.; Villegas, A.; Palacio, J. Blood concentrations of serotonin, cortisol and dehydroepiandrosterone in aggressive dogs. Appl. Anim. Behav. Sci. 2010, 123, 124–130. [Google Scholar] [CrossRef]
- Sandri, M.; Colussi, A.; Perrotta, M.G.; Stefanon, B. Salivary cortisol concentration in healthy dogs is affected by size, sex, and housing context. J. Vet. Behav. 2015, 10, 302–306. [Google Scholar] [CrossRef]
- Frank, L.A.; Rohrbach, B.W.; Bailey, E.M.; West, J.R.; Oliver, J.W. Steroid hormone concentration profiles in healthy intact and neutered dogs before and after cosyntropin administration. Domest. Anim. Endocrinol. 2003, 24, 43–57. [Google Scholar] [CrossRef] [PubMed]
- Bencker, C.; Gschwandtner, L.; Nayman, S.; Grikšienė, R.; Nguyen, B.; Nater, U.M.; Guennoun, R.; Sundström-Poromaa, I.; Pletzer, B.; Bixo, M.; et al. Progestagens and progesterone receptor modulation: Effects on the brain, mood, stress, and cognition in females. Front. Neuroendocrinol. 2024, 76, 101160. [Google Scholar] [CrossRef]
- Kutzler, M.A. Gonad-sparing surgical sterilization in dogs. Front. Vet. Sci. 2020, 7, 342. [Google Scholar] [CrossRef] [PubMed]
- Romagnoli, S.; Diana, A.; Ferré-Dolcet, L.; Fontaine, C.; Milani, C. Chronic Use of Deslorelin in Dogs: Six Cases (2005–2022). Animals 2023, 13, 265. [Google Scholar] [CrossRef]
- Masson, S.; Medam, T.; Raibon, E.; Fontaine, C.; Levy, X. Double-Blind, Placebo-Controlled Trial of Cyproterone Acetate to Prevent Flare-up Effect on Dogs Implanted with Deslorelin. Front. Vet. Sci. 2021, 8, 1–8. [Google Scholar] [CrossRef]
Research Study | Year | Sample Categorization | Study Design | Results |
---|---|---|---|---|
Spain and Houpt [59] | 2004 | 1842 dogs adopted from shelter. Both sexes. | Retrospective cohort study | Males and females neutered at an early age had an increase in noise phobias and sexual behaviors; separation anxiety, escaping behaviors, inappropriate elimination when frightened, and relinquishment for any reason were decreased. Aggression toward family members was more frequent among male dogs gonadectomized at an early age. |
Reisner et al. [47] | 2005 | 1053 adult English Springer Spaniels. Both sexes. | Prevalence survey | Sex and neuter status were two variables related to aggressive behavior toward familiar people. Neutered males and females were more aggressive than intact ones in the majority of contexts of owner-directed aggression. Neutered males and females were significantly more likely to have bitten. Neutered females were also more aggressive toward unfamiliar adults who approached. |
Kim et al. [69] | 2005 | 60 German Sheperd females. | Prospective study | There was a reported increase in territorial aggression in the ovariohysterectomy group. Neutered females showed more posture and aggressive expressions than the control. The acoustic feature changed, with a higher rate of barking call in the ovariohysterectomy group. |
Serpell and Hsu [70] | 2005 | 1593 dogs. Both sexes. | Cross- sectional study | Dogs were assessed for trainability. Neutering was not associated with any differences in trainability in female dogs in any breed but was associated with positive effects on trainability in male Shetland sheepdogs. |
Kim et al. [71] | 2006 | 14 German Sheperd females. | Prospective study | Dogs in the ovariohysterectomy group showed an increase in reactivity. Neutered females showed a more offensive posture and aggressive expressions than the control. |
Bennett and Rohlf [72] | 2007 | 413 participants. Both sexes. | Cross- sectional survey | When associating the frequency of potentially problematic behaviors with demographic variables, involvement in dog training activities, and participation in other dog–human interactions, neutered dogs of both sexes were found to be more nervous or timid than intact ones. Neutered dogs were also rated as less anxious and engaged in fewer destructive behaviors. |
Kubinyi et al. [73] | 2009 | 10,519 dogs. Both sexes. | Cross- sectional study | In both sexes (more significant in males), dogs with the lowest mean calmness were neutered and less than 2.5 years old. Neutered females and intact males were considered more trainable then their counterparts. Neutered dogs who spent less than 3 h with their owner daily were reported to be bolder and less bold if more than 3 h. |
Starling et al. [74] | 2013 | 1054 dogs. Both sexes. | Cross- sectional study | Male dogs were bolder than female dogs, and intact dogs were bolder than neutered ones. The study also suggests that neutering alters a dog’s willingness to engage in social behaviors and/or their desire to avoid novel or potentially frightening nonsocial objects. |
Zink et al. [60] | 2014 | 2505 Vizlas. Both sexes. | Retrospective cohort study | Neutered Vizlas are more at risk of developing several behavioral problems (for example, fear and aggression) than intact ones, but this was entirely influenced by the age at which dogs were gonadectomized. Neutering at ≤6 months poses a greater risk. |
Tiira et al. [75] | 2016 | 3284 dogs. Both sexes. | Cross- sectional survey | Neutered females presented more avoidance behaviors, intact males more urinating/defecating and destroying behavior, and neutered dogs of both sexes more panting and pacing and less vocalization toward loud noises. Males and neutered dogs had a more excited/active type of behavior in new situations. |
Bálint et al. [76] | 2017 | 93 dogs. Both sexes | Experimental study | A relationship was found between dogs’ age and reproductive status. Dogs between 2 and 6 years of age showed a difference based on their reproductive status; intact dogs were significantly less “obedient” than the neutered ones. A significant interaction between behavior type based on the “roll over” test and the reproductive status of the dog was found. The intact “resistant” dogs showed the lowest “aggressive towards owner” scores, but neutered “resistant” dogs had the highest scores for aggression. |
Kaufmann et al. [53] | 2017 | 18 intact male dogs and 16 neutered male dogs, 104 male dogs for questionnaires, 54 case studies on male dogs. | Observational study | Intact dogs are socially more active toward neutered ones (smelling and licking the genital area, chin rest, tooth chatter, and molesting). As for the questionnaires, intact dogs seem to be bolder, more sociable, and less trainable. As for the case studies, the biggest difference was fearful behavior. Neutered males seemed more anxious during walks and more aggressive toward other dogs. Neutering may have a negative influence on the behavior of male dogs. |
Balogh et al. [77] | 2018 | 58 female Labrador Retrievers. | Experimental study | The owners of neutered females described their dogs as having more intense or more frequent fear reactions in response to loud noises, strange or unfamiliar objects on or near the sidewalk, or if unknown jumping, barking, or growling dogs were approaching them (this last one occurred mostly in females neutered after puberty). |
Farhoody et al. [58] | 2018 | 13,500 dogs. Both sexes. | Cross- sectional study | There was a minimal increase in aggression toward strangers for all neutered dogs compared with intact dogs, which was mostly seen in the group of dogs gonadectomized at 7–12 months of age. |
Jacobs et al. [78] | 2018 | 3589 dogs Both sexes. | Cross- sectional study | Among other characteristics, neutered males were more likely to be resource guarding aggressive compared to dogs of other sexes and neuter statuses. |
McGreevy et al. [56] | 2018 | 6235 neutered male dogs. | Cross- sectional survey | Some forms of aggression, mainly related to fear, were significantly and positively associated with lower age at neutering and percentage of lifetime exposure to gonadal hormones (PLGH). Other behaviors, like indoor marking, increased with PLGH. |
Lorenz et al. [79] | 2019 | 180 female dogs. | Observational study | Intact female dogs were significantly calmer and more trainable and sociable toward other dogs. Neutered females tended to be less bold than intact ones, more anxious and nervous, trembled more often, and were more aggressive toward humans in general and specific objects. |
Starling et al. [57] | 2019 | 8981 neutered female dogs. | Cross- sectional survey | Female dogs with less exposure to their natural gonadal hormones (decreased PLGH) showed greater incidence of several fear/anxiety, aggressive, and excitable behaviors than intact female dogs in several contexts. |
Fattah and Hamid [80] | 2020 | 120 German Sheperd dogs. Both sexes. | Experimental design | Males were significantly more trainable than females. As for sexual status, both intact males and females were significantly more trainable than the neutered ones. |
Hakanen et al. [52] | 2020 | 13,700 dogs. Both sexes. | Cross- sectional survey | Neutered dogs showed more non-social fears. They were more likely to show fear of fireworks and thunder than intact dogs. Intact males were less fearful in novel situations, and intact females were less fearful when compared to neutered females. |
Palestrini et al. [81] | 2021 | 96 dogs. Both sexes. | Cross-sectional study | Neutered dogs were reported to show less mounting behavior, pulling on the leash, and roaming behaviors. Marking behavior did not vary across time for both groups of dogs. A tendency to reduce owner-directed aggression was observed at the interview 9 months after surgery for male dogs, while no change was observed for male controls. |
Kolkmeyer et al. [54] | 2021 | 230 dogs. Both sexes. | Cross- sectional study | Intact males were more open-minded and less fearful than neutered dogs. Neutered dogs showed significantly greater panic reactions compared to intact ones and higher values for aggressive behavior. |
Moxon et al. [82] | 2022 | 155 and 151 Labrador and Golden Retrievers crossbred. Females. | Prospective cohort study | The results suggest that for Labrador and Golden Retriever crossbred bitches, neutering before or after puberty has little to no effect on future behavior. |
Kriese et al. [44] | 2022 | 396 male dogs. | Online survey | Neutering reduced aggressive behaviors toward dogs and other animals. An increase in the number of dogs that were fearful of unfamiliar dogs/humans was reported, as well as sound phobias. The surgery greatly decreased incidences of roaming, mounting, and urine marking as well as the dog’s overall activity. |
Kolkmeyer et al. [55] | 2024 | 230 mixed-breed dogs. Male dogs. | Correlational study | Neutered dogs appeared more stressed than intact ones, especially related to human noises and other reasons like car rides or unfamiliar environments. Neutered dogs differed significantly from intact dogs in terms of general aggression and emotional stability; they were much less social, less trainable, emotionally calm, and extroverted than intact dogs. |
Kolkmeyer et al. [61] | 2024 | 136 dogs from Huskie and Bulldog clades. Male dogs. | Cross- sectional study | An increase in aggression toward humans is described for neutered males in both clades. An increase in aggression in walks and toward dogs in mostly seen in the Bulldog clade. As for stress-related responses, there is a significant difference in stress due to other dogs and noises and more panic reactions, stress, and uncertainty in neutered dogs. |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Arroube, A.; Pereira, A.F. Dog Neuter, Yes or No? A Summary of the Motivations, Benefits, and Harms, with Special Emphasis on the Behavioral Aspect. Animals 2025, 15, 1063. https://doi.org/10.3390/ani15071063
Arroube A, Pereira AF. Dog Neuter, Yes or No? A Summary of the Motivations, Benefits, and Harms, with Special Emphasis on the Behavioral Aspect. Animals. 2025; 15(7):1063. https://doi.org/10.3390/ani15071063
Chicago/Turabian StyleArroube, Ana, and Alfredo F. Pereira. 2025. "Dog Neuter, Yes or No? A Summary of the Motivations, Benefits, and Harms, with Special Emphasis on the Behavioral Aspect" Animals 15, no. 7: 1063. https://doi.org/10.3390/ani15071063
APA StyleArroube, A., & Pereira, A. F. (2025). Dog Neuter, Yes or No? A Summary of the Motivations, Benefits, and Harms, with Special Emphasis on the Behavioral Aspect. Animals, 15(7), 1063. https://doi.org/10.3390/ani15071063