2017 review article on welfare implications of spay/neutering in dogs.

[pstinard]

Hi. I decided to start a separate thread here on the welfare implications of spaying and neutering dogs rather than hijacking a thread in the General forum. I started by doing a research literature search on the effect of spaying and neutering on the behavior of dogs and found about a dozen relevant articles. Of these, I discarded the ones where the discussion was only incidental to the article, older articles, as well as articles that were only about small studies. I found this really REALLY good review article from May of 2017 that I thought was the best of the best: https://avmajournals.avma.org/doi/pd...ma.250.10.1155

This article will undoubtedly be behind a paywall for most Yorkietalk readers, but I have access to the full article, so I will post the section on the effect of spay/neutering on behavior in its entirety. There are other good sections on the effect of spay/neutering on health issues such as cancer, ACL tears, and luxating patella that I'll either post later or summarize if there is interest.

Here is the section on behavior:

(Definition of terms: gonadectomy = spaying/neutering. OHE = spaying.)

Behavior

Inappropriate or unacceptable behaviors disrupt the human-animal bond and are one of the most common reasons for relinquishment or rehoming of dogs. Because some owners pursue gonadectomy to prevent or resolve behavioral problems of their pets, they should be given realistic expectations for potential postsurgical behavioral changes.

Gonadectomy and the resultant decrease in gonadal steroid hormones typically result in a marked reduction or elimination of sexually dimorphic behaviors, including roaming, hormonal aggression (fighting with other males or females), and urine marking. In males, the age at castration or duration of the behavior does not change the likelihood that surgery will alter these unwanted behaviors.

The literature provides consistent results regarding the effects of gonadectomy on behaviors driven by testosterone or estrogen; however, studies involving behaviors not directly related to gonadal steroid hormones have resulted in mixed findings. Although the most serious bite injuries in the United States involve sexually intact dogs, gonadectomy has not been found to be a useful measure to prevent aggressive behavior in male or female dogs. Gonadectomy consistently reduces only intermale aggression and may actually contribute to increased aggression in female dogs. In a study conducted to evaluate canine patients referred for management of behavioral problems, sexually intact males and neutered females were significantly more likely to be referred because of aggression and stimulus reactivity than were neutered males and sexually intact females. A prospective controlled study of German Shepherd Dogs revealed increased reactivity to unfamiliar people and unknown dogs following OHE performed between 5 and 10 months of age, compared with results for dogs allowed to remain sexually intact. A study based on responses of 150 owners of dogs to questionnaires administered at the time of spaying and again 6 months later revealed a significant increase in dominance aggression toward family members by bitches following OHE, compared with the response of sexually intact female dogs of similar age and breed assessed at the same time periods. Female puppies that already had displayed signs of aggression were at highest risk for an increase in dominance aggression following gonadectomy, and there was little risk of increased aggression in older dogs that had not already displayed aggressive behavior. Therefore, consideration should be given to postponing OHE in female puppies with a history of aggression.

Differences in study designs and results create additional challenges when the potential consequences of gonadectomy on behavior are evaluated. Investigators of 1 study reported decreased activity in 50% of male dogs neutered as adults, contrary to results of an earlier study in which there was no indication that neutered male dogs become more inactive or lethargic. Additional differences were for dogs gonadectomized at 7 weeks or 7 months of age, which were judged to be more excitable than were sexually intact dogs. When dogs gonadectomized before or after 5.5 months of age were compared, those neutered before 5.5 months of age were more likely to display noise phobias and sexual behaviors. However, separation anxiety, urination due to fear, and the likelihood a dog would escape were less likely. Male puppies neutered prior to 5.5 months of age had increased aggression toward family members and also were more likely to bark excessively at visitors or household members. In another study conducted to evaluate gonadectomy in dogs before or after 24 weeks of age, investigators concluded that there was no increase in the incidence of behavioral problems or return rate to shelters for prepubertally gonadectomized dogs. Vizslas gonadectomized before 6 months of age reportedly have an increase of undesirable behaviors related to fear and anxiety. Investigators of that study did not evaluate sexual behaviors such as mounting and urine marking. When bitches of various breeds spayed between 2 and 4 years of age were compared with a sexually intact control group, no behavioral differences were observed during the 2 months after gonadectomy.

Interpretation of the literature related to behavioral changes after gonadectomy is further complicated by various definitions of aggression as well as comparisons of similar-appearing but potentially unrelated behaviors (eg, aggression, reactivity or energy level, and excitability). It is also possible that gonadectomy was recommended for some dogs as part of a behavior treatment plan, which would artificially increase the number of spayed or neutered dogs with behavioral problems. Because of these complicating factors, additional research is needed before conclusions can be confidently made about the effects of gonadectomy beyond the reduction of reproductive behaviors. Specific evaluation of potential behavioral consequences of surgery during critical periods of behavioral development could help guide general recommendations on the most appropriate time for gonadectomy of puppies.

[pstinard]

Other major sections of this review article deal with the following topics: Neoplasia (cancers), Orthopedic Diseases (CCL tears and hip dysplasia), Behavior (already posted above), Other Medical Implications (including pyometra and urinary incontinence), Lifespan (neutered dogs live much longer than unneutered dogs), Population Management, and Anesthetic and Surgical complications. I'd be willing to briefly summarize specific concerns addressed in this article if there is interest--just ask.

[chattiesmom]

Phil, thank you so very much for taking your time and effort to provide YTers with this information.

[ladyjane]

Thank you for responding so quickly to this....always appreciate your input Phil. I will read this later when I have more time.

[ladyjane]

Originally Posted by pstinard

Other major sections of this review article deal with the following topics: Neoplasia (cancers), Orthopedic Diseases (CCL tears and hip dysplasia), Behavior (already posted above), Other Medical Implications (including pyometra and urinary incontinence), Lifespan (neutered dogs live much longer than unneutered dogs), Population Management, and Anesthetic and Surgical complications. I'd be willing to briefly summarize specific concerns addressed in this article if there is interest--just ask.

I must say I got a tad bit confused by the behavioral stuff....I am definitely interested in some of the above mentioned....especially Orthopedic issues. My understanding is that ortho issues commonly show in larger breeds, but not smaller?? Would like your input on those studies. Also, your takeaway on this behavioral thing....

What stood out to me on the behavioral one is the part about females and the part about holding off on spays with aggressive female puppies. Funny that it didn't change the male aggression.

Correct me if I am wrong, but my take away on all of this is that there isn't anything really concrete that would suggest people avoid altering a male or female pup.... AND, that the reason to do it should not be affected by the belief that it will change certain behaviors. ??? I hope this makes sense. I have seen people advise early neutering as a way to prevent male pups from marking and/or hiking legs ... I would never guarantee that to a person since I have seen pups that were altered still mark their territory.

I alter pups for one main reason: I want to avoid health issues. Of course I also have zero desire to breed. Yes, rescue alters them to prevent breeding.....but, they also are looking at overall health of their pups.

[ladyjane]

Reading that thing reminded me of why I rely on folks like you to interpret research data. I think I am too ADD

[pstinard]

Originally Posted by ladyjane

I must say I got a tad bit confused by the behavioral stuff....I am definitely interested in some of the above mentioned....especially Orthopedic issues. My understanding is that ortho issues commonly show in larger breeds, but not smaller?? Would like your input on those studies. Also, your takeaway on this behavioral thing....

What stood out to me on the behavioral one is the part about females and the part about holding off on spays with aggressive female puppies. Funny that it didn't change the male aggression.

Correct me if I am wrong, but my take away on all of this is that there isn't anything really concrete that would suggest people avoid altering a male or female pup.... AND, that the reason to do it should not be affected by the belief that it will change certain behaviors. ??? I hope this makes sense. I have seen people advise early neutering as a way to prevent male pups from marking and/or hiking legs ... I would never guarantee that to a person since I have seen pups that were altered still mark their territory.

I alter pups for one main reason: I want to avoid health issues. Of course I also have zero desire to breed. Yes, rescue alters them to prevent breeding.....but, they also are looking at overall health of their pups.

My takeaway on the behavior part is that studies do show that female dogs are (at least at a statistically significant level) more aggressive than unspayed dogs. However, the author notes that the people who published those studies didn't take into account the possibility that the dogs that were spayed already had previously existing behavioral issues. Therefore, he issued caution in interpreting those results and basically said that more studies need to be done to be sure. You mention spaying for the overall health of the dog. What knocked me over (and something I alluded to in my summary if the paper) is the section on Lifespan. I'll quote from that below, because it's very very important, and rather shocking (I'll address orthopedic issues in my next post):

Lifespan

Overall, gonadectomy appears to be associated with an increase in lifespan. This has great importance for veterinary medicine, whereby euthanasia is considered when quality of life is substantially compromised and cannot be expected to reasonably improve. A retrospective study that included data from the VMDB found that neutering was strongly associated with an increased lifespan (life expectancy of spayed females was increased by 26.3%, and that of castrated males was increased by 13.8%). Although gonadectomy increased the risk of death attributable to neoplasia (except for mammary gland neoplasia, which had a significantly lower prevalence) and immune-mediated disease, it decreased the risk of death attributable to other causes, including infectious disease and trauma. Similarly, analysis of patient data evaluated in a 2013 report that included data from primary care veterinary hospitals revealed that spayed dogs typically lived 23% longer and neutered dogs lived 18% longer than did sexually intact female and male dogs, respectively. That report also revealed that sexually intact dogs were more than twice as likely as gonadectomized dogs to be hit by a car or bitten by another animal. Results of a survey of owners of > 3,000 British dogs indicated that spayed females lived significantly longer than did males and sexually intact females.

[Lovetodream88]

Thanks for the post and the time you put into it. I definitely would be interested to hear about the CCL tears and stuff because last I heard there was no difference is small dogs but it was an issue for large dogs so I'm still wondering if that is true.

[matese]

Phil thank you so much for taking the time to post this, so help full to many ppl. I read only a portion, will read it later when I have more time. You're the best.

[pstinard]

The section on orthopedic issues is rather long, but I'll quote it below, since I think you will find it worthwhile:

Orthopedic Diseases

Musculoskeletal diseases such as CCL disease and hip dysplasia are not inherently life-threatening conditions, but they do affect physical performance and quality of life of patients. Surgical correction of CCL disease and hip dysplasia can also be cost prohibitive for owners. In situations whereby chronic orthopedic pain of animals cannot be adequately managed, especially in large-breed dogs, euthanasia may be considered. The incidence of CCL disease and hip dysplasia is 1.7% and 1.8%, respectively. The true disease prevalence of hip dysplasia is difficult to determine because of selection bias for those dogs provided for evaluation or that are typically screened, membership bias for the groups of the canine population being considered, and differences in case definition when determining a positive result. This could result in a gross underestimation of the prevalence within the general canine population or within specific breeds.

Gonadectomy is a risk factor for development of CCL disease and hip dysplasia in both male and female dogs. The complex pathophysiologic processes of these orthopedic diseases make it challenging to connect cause and effect. Although heritability is the primary factor for the development of hip dysplasia, it is a multifactorial condition. Hip dysplasia most commonly affects large-breed dogs. Similarly, most dogs treated for CCL disease are young, active, large-breed dogs. Development of CCL disease may result from degenerative or traumatic causes. Ligament degeneration has also been associated with aging, conformational abnormalities, and immunemediated arthropathies.

Investigators of 1 study found an overall prevalence for CCL disease of 3.48%, with gonadectomized dogs having a significantly higher prevalence than their sexually intact counterparts, and neutered females having the highest prevalence. This supported results of another study that revealed an increased prevalence of CCL disease in female dogs and that the age at the time of OHE did not appear to be a factor. The finding that large dogs were more likely to have CCL rupture is consistent throughout several studies. A retrospective study conducted to evaluate both musculoskeletal diseases found that gonadectomy increased the prevalence of CCL disease in male and female dogs and that hip dysplasia was more prevalent among neutered male dogs and less common among female dogs regardless of their neuter status.

Breed predisposition may also play a major role in the development of CCL disease and hip dysplasia. Four breed-specific studies revealed a significant increase in orthopedic disorders in gonadectomized dogs, compared with results for their sexually intact counterparts, although the incidence differed widely among breeds. Prepubertal gonadectomy of Golden Retrievers resulted in an increased incidence of joint disorders (3 to 5 times as high as the incidence for sexually intact dogs), whereas prepubertal gonadectomy of Labrador Retrievers was associated with an incidence that was twice as high as that for sexually intact dogs. The incidence of hip dysplasia increased significantly only in male Golden Retrievers neutered before 1 year of age. Elbow joint dysplasia increased significantly only for male Labrador Retrievers neutered before 6 months of age (incidence, 2%), compared with that for sexually intact males (incidence, 0.57%). Boxers that were gonadectomized at least 6 months prior to diagnosis of hip dysplasia, (mean age at gonadectomy, 3 years) were 1.5 times as likely as sexually intact Boxers to develop hip dysplasia. Male and female German Shepherd Dogs gonadectomized before 12 months of age were at an increased risk for CCL tears, compared with the risk for those remaining sexually intact. There was not a significant association between gonadectomy and hip dysplasia or elbow joint dysplasia in German Shepherd Dogs. Prepubertal gonadectomy is associated with increased bone length attributable to delayed closure of growth plates. Although it has been speculated that this subsequently leads to the development of certain orthopedic diseases, the speculated association has not been explained or confirmed.

The effect of sex hormones on orthopedic disease has also been explored via comparisons between gonadectomy performed at early and traditional ages. Comparison of outcomes for shelter dogs gonadectomized before or after 24 weeks of age revealed no association between age at gonadectomy and frequency of musculoskeletal problems during the 4 years after gonadectomy. A few dogs developed hip dysplasia, but they did not require surgical or prolonged medical management. A similar study for which follow-up monitoring was available for as long as 11 years after gonadectomy revealed a significant increase in the incidence of hip dysplasia among dogs gonadectomized before 5.5 months of age, compared with the incidence for those gonadectomized after 5.5 months of age. However, there was a lower rate for euthanasia among the early-age gonadectomized dogs with hip dysplasia. Although neither of these studies included a comparison with sexually intact animals and it was unclear as to the diagnostic tests used to diagnose hip dysplasia, the low incidence and severity of orthopedic problems in prepubertally gonadectomized dogs makes it worthwhile to consider early-age neutering.

[pstinard]

Originally Posted by Lovetodream88

Thanks for the post and the time you put into it. I definitely would be interested to hear about the CCL tears and stuff because last I heard there was no difference is small dogs but it was an issue for large dogs so I'm still wondering if that is true.

I believe that this review article still supports the understanding that spaying has a much greater effect on large breed dogs than small breed dogs with respect to increased rates of CCL tears and hip dysplasia. When I last checked with researchers at UC Davis a year ago, this was still the case. I'll take another look and see if any new research has been published since.

[Lovetodream88]

Originally Posted by pstinard

The section on orthopedic issues is rather long, but I'll quote it below, since I think you will find it worthwhile:

Orthopedic Diseases

Musculoskeletal diseases such as CCL disease and hip dysplasia are not inherently life-threatening conditions, but they do affect physical performance and quality of life of patients. Surgical correction of CCL disease and hip dysplasia can also be cost prohibitive for owners. In situations whereby chronic orthopedic pain of animals cannot be adequately managed, especially in large-breed dogs, euthanasia may be considered. The incidence of CCL disease and hip dysplasia is 1.7% and 1.8%, respectively. The true disease prevalence of hip dysplasia is difficult to determine because of selection bias for those dogs provided for evaluation or that are typically screened, membership bias for the groups of the canine population being considered, and differences in case definition when determining a positive result. This could result in a gross underestimation of the prevalence within the general canine population or within specific breeds.

Gonadectomy is a risk factor for development of CCL disease and hip dysplasia in both male and female dogs. The complex pathophysiologic processes of these orthopedic diseases make it challenging to connect cause and effect. Although heritability is the primary factor for the development of hip dysplasia, it is a multifactorial condition. Hip dysplasia most commonly affects large-breed dogs. Similarly, most dogs treated for CCL disease are young, active, large-breed dogs. Development of CCL disease may result from degenerative or traumatic causes. Ligament degeneration has also been associated with aging, conformational abnormalities, and immunemediated arthropathies.

Investigators of 1 study found an overall prevalence for CCL disease of 3.48%, with gonadectomized dogs having a significantly higher prevalence than their sexually intact counterparts, and neutered females having the highest prevalence. This supported results of another study that revealed an increased prevalence of CCL disease in female dogs and that the age at the time of OHE did not appear to be a factor. The finding that large dogs were more likely to have CCL rupture is consistent throughout several studies. A retrospective study conducted to evaluate both musculoskeletal diseases found that gonadectomy increased the prevalence of CCL disease in male and female dogs and that hip dysplasia was more prevalent among neutered male dogs and less common among female dogs regardless of their neuter status.

Breed predisposition may also play a major role in the development of CCL disease and hip dysplasia. Four breed-specific studies revealed a significant increase in orthopedic disorders in gonadectomized dogs, compared with results for their sexually intact counterparts, although the incidence differed widely among breeds. Prepubertal gonadectomy of Golden Retrievers resulted in an increased incidence of joint disorders (3 to 5 times as high as the incidence for sexually intact dogs), whereas prepubertal gonadectomy of Labrador Retrievers was associated with an incidence that was twice as high as that for sexually intact dogs. The incidence of hip dysplasia increased significantly only in male Golden Retrievers neutered before 1 year of age. Elbow joint dysplasia increased significantly only for male Labrador Retrievers neutered before 6 months of age (incidence, 2%), compared with that for sexually intact males (incidence, 0.57%). Boxers that were gonadectomized at least 6 months prior to diagnosis of hip dysplasia, (mean age at gonadectomy, 3 years) were 1.5 times as likely as sexually intact Boxers to develop hip dysplasia. Male and female German Shepherd Dogs gonadectomized before 12 months of age were at an increased risk for CCL tears, compared with the risk for those remaining sexually intact. There was not a significant association between gonadectomy and hip dysplasia or elbow joint dysplasia in German Shepherd Dogs. Prepubertal gonadectomy is associated with increased bone length attributable to delayed closure of growth plates. Although it has been speculated that this subsequently leads to the development of certain orthopedic diseases, the speculated association has not been explained or confirmed.

The effect of sex hormones on orthopedic disease has also been explored via comparisons between gonadectomy performed at early and traditional ages. Comparison of outcomes for shelter dogs gonadectomized before or after 24 weeks of age revealed no association between age at gonadectomy and frequency of musculoskeletal problems during the 4 years after gonadectomy. A few dogs developed hip dysplasia, but they did not require surgical or prolonged medical management. A similar study for which follow-up monitoring was available for as long as 11 years after gonadectomy revealed a significant increase in the incidence of hip dysplasia among dogs gonadectomized before 5.5 months of age, compared with the incidence for those gonadectomized after 5.5 months of age. However, there was a lower rate for euthanasia among the early-age gonadectomized dogs with hip dysplasia. Although neither of these studies included a comparison with sexually intact animals and it was unclear as to the diagnostic tests used to diagnose hip dysplasia, the low incidence and severity of orthopedic problems in prepubertally gonadectomized dogs makes it worthwhile to consider early-age neutering.

Am I correct that it looks like this refers to larger breed dogs then small breeds? Still interesting.

[Lovetodream88]

Originally Posted by pstinard

I believe that this review article still supports the understanding that spaying has a much greater effect on large breed dogs than small breed dogs with respect to increased rates of CCL tears and hip dysplasia. When I last checked with researchers at UC Davis a year ago, this was still the case. I'll take another look and see if any new research has been published since.

Ignore my other response lol it pretty much says what I said here. Snow is making me crazy lol.

[pstinard]

Originally Posted by Lovetodream88

Ignore my other response lol it pretty much says what I said here. Snow is making me crazy lol.

That's okay. It made me look to see if there were any new studies since the UC Davis Golden Retriever and German Shepherd studies. There have been no new studies published since then. Enjoy the snow (if you can) .

[pstinard]

Originally Posted by Lovetodream88

Am I correct that it looks like this refers to larger breed dogs then small breeds? Still interesting.

Yes. I actually wrote to the main author of the UC Davis studies and asked specifically about small breed dogs like Yorkshire Terriers and he told me that the effect of spaying is much less on small breed dogs and that they will be publishing a new paper eventually. It looks like the new paper still hasn't come out yet.