Pearl 2020

Photo by Annie Conklin

David Nardone and Linda Cohen searched for more than a year to find the perfect dog. They got Pearl in December, and are waiting until after her first heat to spay her. They hope the delay will help her avoid joint issues down the road.

When Linda Cohen and David Nardone adopted an 8-week-old German shepherd-Labrador retriever in December, they assumed they would spay her early, just as most of their dog-owning friends had done with their pets. However, when the North Seattle couple took the pup they named Pearl to the veterinarian, she told them about a trend toward letting dogs' bodies mature before the surgery.

She gave them a copy of a paper by researchers at the University of California, Davis, School of Veterinary Medicine, published in 2013, which tied early neutering to increased risk of joint disorders and cancer. That information caused them to reconsider their plans.

Pearl and her owners have a front row seat for the evolving debate about the benefits and detriments of gonadectomy, the most common elective surgery for dogs in the United States. Also known as desexing, spay/neuter or, more simply, neuter, gonadectomy in females is the removal of ovaries and the uterus (ovariohysterectomy) or just the ovaries (ovariectomy); and in males the testicles (castration) to render them infertile. 

The health of the individual dog has not been the foremost concern in the widespread adoption of elective neutering. It has been pursued primarily for the convenience and benefit of owners and society. While it's been de rigueur to neuter owned dogs by about 6 months of age, and even earlier in the case of unowned dogs, a growing body of research finds that when dogs are very young, removal of the sex hormones produced by gonads might increase the risk of medical disorders in some cases.

A recently published sequel to the earlier UC Davis research is further challenging paradigms and feeding momentum to reexamine current practices. Titled Assisting decision-making on age of neutering for 35 breeds of dogs: associated joint disorders, cancers, and urinary incontinence, the study claims to find "major breed differences in vulnerability to neutering, both with regard to joint disorders and cancers." The authors recommend delaying neutering for males and/or females dogs in 19 breeds and skipping neutering altogether in two breeds.

The message of the study is bold and controversial. Critics say the conclusions and recommendations are based on small sample sizes and fail to factor in the health benefits of early neutering. Others applaud the work for challenging a one-size-fits-all approach to sterilization.

Since its publication in July, the new study has been viewed more than 210,000 times, surpassing page views generated by nearly all other articles on the online journal Frontiers in Veterinary Science. The original UC Davis study, which focused on golden retrievers, has generated more than 385,000 views and 84 citations since appearing in the journal Plos One seven years ago.

The theory that desexing dogs early might later harm them appears to be gaining ground among veterinarians. Anecdotally, many practitioners accept that early neutering might put dogs at greater risk for joint problems such as tears of cranial cruciate ligament, which stablizes the knee. Links between early sterilization and increased risk for cancers such as lymphoma, mast cell tumor and hemangiosarcoma draw more skepticism.

Dr. Philip Bushby, a professor specializing in shelter medicine at Mississippi State University College of Veterinary Medicine, speaks regularly at conferences about the optimal age for gonadectomy and says his feelings are mixed about the study's conclusions and recommendations. "[It] is going to create more confusion than less confusion; more controversy than less controversy," he told the VIN News Service. 

That's a dilemma for Dr. Joe Frost, a Chicago-area practitioner who's flummoxed by the revolving standards for sterilization. He aired his frustration last year in a message board discussion of the Veterinary Information Network, an online community for the profession and parent of the VIN News Service. 

"Our current recommendations are all over the freaking map!" he wrote on VIN. "We are literally 'reinventing the wheel' with every single patient, and clients receive widely varying advice from different doctors. This makes us look like we don't know what we are talking about. I'm getting tired of saying, 'We don't know the optimal age to neuter Fluffy. Honestly, we don't even know if we should neuter Fluffy!' "

Other veterinarians welcome the stimulus to rethink conventional sterilization guidance. 

When he graduated from veterinary school 20 years ago, Dr. Jamie Mulcahy, a small animal practitioner in Australia, didn't give much thought to the health impacts of neutering. Australia is like the United States, he said, where pets are desexed as a matter of course and clients feel like they have little choice in the matter.

That changed a few years ago, Mulcahy said, when suggestions that early sterilization might harm some dogs began to infiltrate his practice's collective consciousness.

"Now my attitude has changed a lot," he said by email. "My thinking is that cats and dogs have had their gonads for millions of years. In the last 100 or so, we have been removing them en masse. In hindsight, it is strange to think that we as a collective of veterinary scientists never considered that this action might have unintended consequences."

The spay/neuter boom

By custom, gonadectomy is often performed by the time a dog is 6 months old. How did that custom arise? Experts such as UC Davis researcher Dr. Benjamin Hart and Bushby, the MSU professor, say they know of no scientific rationale for the standard to desex puppies by 6 months of age. Both point out that such blanket guidance ignores the fact that small and large dog breeds reach maturity at different times. 

For unowned dogs, neutering can happen even earlier. Many shelters and rescues require that dogs are neutered before they are adopted out. In much of the U.S., it's required by law. That can mean desexing puppies younger than 8 weeks old.

Sterilizing dogs wasn't always common practice in the United States; throughout much of the 20th century, few dogs were neutered. That changed during the 1970s, when animal welfare groups began to advocate for sterilization as a means for reducing unplanned litters and curbing the euthanization of unwanted animals. Today, between 69% and 78% of dogs in the U.S. are neutered, according to surveys by the American Veterinary Medical Association and the American Pet Products Association, respectively. 

Neutering also has been embraced as a way to mitigate undesirable behaviors in dogs, such as roaming and aggression, both of which are common reasons for relinquishment. It's also endorsed as a way to reduce the risk of reproductive conditions and diseases, such as pyometra, an infection of the uterus with a reported incidence of almost 25% in intact females by age 10 years of age. 

The expansion of spay/neuter widely has been deemed a success. Euthanasia rates for shelter dogs have dropped dramatically in the past few decades. In 1973, the Humane Society of the U.S. estimated that about 13.5 million dogs and cats were euthanized annually because no homes could be found for them. Today about 670,000 dogs and 860,000 cats are euthanized in shelters every year, according to the American Society for the Prevention of Cruelty to Animals. 

There also is evidence that neutered dogs, particularly females, live longer than their intact counterparts, although it's not understood why. 

The idea that neutering impacts the health of animals, especially when performed during adolescence, is not new. Dr. Margaret Root Kustritz, a veterinary theriogenologist (reproductive specialist) said as much in a 2007 review paper published in the Journal of the American Veterinary Medical Association. In the review, Kustritz, an academic at the University of Minnesota College of Veterinary Medicine, cited more than 180 research papers dating back to the mid-20th century in which researchers examined societal impacts, behavioral effects and rates of diseases as they relate to neutering.

In 2017, the journal Clinical Theriogenology published another literature review, penned by Kustritz, Bushby and others. They evaluated scores of studies, more than 50 of which claimed to show that neutered dogs exhibited increased incidences of medical problems, ranging from osteosarcoma and hip dysplasia to atopic dermatitis and urinary incontinence.

The authors concluded that while the research suggested a connection between neutering and disease, the studies stopped short of proving that desexing dogs, even early, increased disease risks.

A breed-by-breed look

Harts UK

Photo courtesy of Dr. Lynette Hart

Drs. Lynette and Benjamin Hart of the University of California, Davis, School of Veterinary Medicine, draw praise and criticism for their research linking early sterilization of dogs to increased risks for joint disorders and cancers in some breeds. The husband-and-wife research team is pictured participating in a raptor demonstration in 2014.

The UC Davis study of 35 dog breeds, published in early July, culminates a 10-year research effort to understand the impact of the timing of gonadectomy surgery, led by Dr. Benjamin Hart, a professor emeritus in the Department of Anatomy, Physiology and Cell Biology. He told VIN News he started seeing reports of potential adverse effects of spay/neuter about 11 years ago, when there wasn't much meaningful data on the topic. So when the UC Davis Center for Companion Animal Health offered to fund the research, he jumped in.

He was joined by other researchers, including his wife Dr. Lynette Hart, a professor in the veterinary school's Department of Population Health and Reproduction. "We knew there would be big consequences of neutering, but we hadn't planned to research it," Lynette Hart said. The team's early research reviewing some 750 medical records at the UC Davis Veterinary Medical Teaching Hospital is reflected in the landmark 2013 study, Neutering dogs: effects on joint disorders and cancers in golden retrievers.

The authors concluded that goldens of both sexes neutered before they were a year old had a greater occurrence than intact goldens of hip dysplasia and cranial cruciate ligament tears. (This ligament, known as the CCL, connects the bones above and below the knee in back, and is similar to an ACL in people.) In addition, they found that neutered females had higher incidences of cancer than intact females, regardless of the age of neutering.

"Turns out, [golden retrievers are] about the worst breeds for some of these issues," Benjamin Hart said. He recalled that the study generated some press and "a lot of pushback" from veterinarians and shelter personnel believing that the research would sow doubts about the benefits of neutering.

Follow-up papers by the Hart team expanded the number of medical records examined for goldens and included the records of the two most popular breeds in the country: Labrador retrievers and German shepherds.

The authors reported "notable differences" between Labradors and goldens. For example, Labradors neutered in their first year were more frequently diagnosed with joint disorders than intact Labradors, but at a rate well below what was seen in goldens. Neutered goldens stood out from Labradors for their susceptibility to cancers.

A study on German shepherds found increased risk for joint disorders among neutered males and for joint disorders and urinary incontinence among neutered females. 

The paper published this summer, the fourth in the series, adds 29 breeds and three varieties of poodles to the mix. The researchers reviewed between 200 and 500 medical cases for most breeds represented in the study. Sample size varied greatly ranging from 86 (wolfhounds) to 1,933 (Labrador retrievers).

Overall, the authors found that "an elevated risk for joint disorder or cancer occurs in relatively few of the breeds." Small dog breeds had low to no increased risks of joint issues associated with neutering, and only two small breeds (Boston terrier and shih tzu) showed "a significant increase" in cancers after neutering.

Guidelines provided by the authors recommend delaying neutering in 19 breeds. The authors recommend leaving female goldens intact due to increased occurrence of cancers at all spaying ages. For the male Doberman pinschers, given the increase in cancer starting at neutering beyond one year, the recommendation is to neuter males before age 1, or consider leaving the male intact.

The Harts contend that the study's findings reinforce the need for the profession to move beyond a blanket approach to neutering because desexing impacts dogs differently, depending on breed, sex and age at the time of surgery.

"Once you've shown these individual differences, then you've really taken the steam out of the objections," Benjamin Hart said.

'Laudable' effort vs. 'suspect' data

Dr. Silvan Urfer, a researcher with the Dog Aging Project at the University of Washington, is the lead author of another review of gonadectomy research. He said in an email, "I think this is a very laudable effort that follows the general tendency to move away from a one-size-fits-all approach in veterinary medicine and to acknowledge the fact that the same interventions can have different effects when applied to different sub-populations."

MSU's Bushby agrees that research that parses different breeds is valuable. "But the dilemma is with so many breeds, you end up using small numbers," he said, explaining that small subject groups and a handful of incidents make it hard to extrapolate risk to general populations, which is key to making recommendations.

Dr. Mark Rishniw, director of clinical research for VIN, has criticized many of the methods and conclusions in the latest UC Davis study. (Working with veterinary oncology colleagues, Rishniw helped draft a list of study flaws, a document available to members of VIN.) He said the critical issue isn't so much sample size as the "event rate." The number of events, i.e., the diagnosis of any of the studied disorders, are so low in the sample groups that they could simply be a matter of chance. 

Part of Bushby's criticism about the UC Davis studies holds true for veterinary research in general.

Kusteritz, Urfer and two others who have researched gonadectomy in animals, Drs. Lisa Howe and Kendall Houlihan, allow that retrospective studies that rely on medical records have inherent selection bias. The experts say this is especially true for records from referral or specialty hospitals, which tend to feature unusual, hard-to-treat and expensive cases. As such, they aren't a true reflection of the general health of all dogs in the country. 

What's needed, everyone agrees, are randomized clinical trials with unbiased subject selection and adequate sample size — all of which are extremely rare in veterinary medicine.

That gold standard can be hard to achieve, according to Dr. Carolyn Gates, an associate professor at Massey University School of Veterinary Science in New Zealand, whose research specialty is evidence-based medicine.

Exploring effects of age of neutering on animal health is difficult to do through "prospective" studies, she explained in an email, because it can take many years for complications such as cancer, joint disease or urinary incontinence to develop; the incidence of some of the complications is quite low; and there are other confounding factors like breed and management that need to be accounted for when estimating risks.

"Together, this means you would need to recruit a lot of animals and follow them for many years in order to end up with enough diseased and non-diseased animals to do a robust statistical comparison," she said.

"They are doing the best job they can with the data they have," Bushby said. "It's just, the data they have is suspect."

Asked about this criticism, Benjamin Hart said it's not true that all the survey populations are small. There were more than 1,000 dogs each in the golden retriever, Labrador retriever, German shepherd and Chihuahua groups.

"This allows us to draw conclusions by looking at results from many angles," Hart said. "There is no reason to conclude that the data is suspect. To imply that the majority of veterinary research done by qualified researchers is suspect is a statement itself that is suspect."

As a result, Bushby said: "We all end up making decisions based on flawed data. That's just the world we live in." He advises veterinarians to balance what's known of the benefits of neutering with the owner's past experiences with pets and breed-related risks to make a whole-health decision. He also warns against extrapolating risks in one breed to another.

With that in mind, he faults the 35-breed paper for ignoring evidence that neutered dogs live longer than intact dogs, and for "dismissing" widely accepted evidence that early spaying in female dogs is protective against mammary tumors later in life. On average, about half of all mammary tumors are malignant.

Mammary neoplasia is among the most common types of cancer seen in intact female dogs. It is believed that the risk of mammary cancer is 0.5% in dogs spayed before their first heat, around 8% in dogs spayed between first and second heat, and around 26% in dogs spayed after a second heat. Overall incidence in the U.S., where the majority of female dogs are spayed, is 3.4%, much lower than in countries where elective gonadectomy is rare. In Norway, for example, where it is illegal to neuter a dog unless it is deemed medically necessary, the incidence is 53.3%, according to a 2001 study. 

The UC Davis study bucks what it calls "the frequently mentioned advantages of early neutering of female dogs" as "protection" against mammary cancer and the consensus embrace of the research. Instead, the authors invoke 2012 meta-analysis from veterinarians at the Royal Veterinary College, saying they found that "the evidence linking neutering to a reduced risk of MC [mammary cancer] is weak."

Speaking to the back-and-forth on mammary cancer, Benjamin Hart said, "This will probably be debated for quite a while. A main point is that no study has looked at a lot of breeds for an idea of breed differences. If we identified which breeds are significantly more likely to have this cancer, the guideline would be to neuter those breeds early." He also pointed out that mammary cancer is more treatable than other cancers.

The UC Davis researchers found the incidence of mammary cancer in 2,971 intact female dogs in the study to be around 6%. The authors speculate that the low occurrence may be because the medical records for intact females were not followed beyond age 11, so late-onset cancers could have been missed.

Bushby offered another reason that the UC Davis study may undercount mammary cancer cases in intact dogs, as well as overcount other cancers: General practitioners are less likely to refer mammary cancer cases to a specialist since treatment is the relatively straightforward procedure of removing a tumor. General practitioners are more likely to refer osteosarcoma — which is reported to have an overall incidence of 0.2% in dogs — to a specialist, since treating bone cancer can involve amputation, chemotherapy and/or radiation.

Like Bushby, VIN's Rishniw also faults the study for tuning out the bigger picture. In particular, he points out that the study claims that increased cancer risks come with desexing for some dogs, while ignoring data showing an association between sterilization and greater longevity.

To explain, he offered this car-accident analogy: "I could die from the airbags ... or the seatbelt might break my sternum … but the risk of that is quite small," he said, adding that without the airbags and seatbelt, the risk of a serious, even fatal, injury is quite high. "So, yes, there are injuries associated with seatbelts, but they are far outweighed by injuries sustained if I don't wear one. So that's the sort of analysis that ultimately needs to go on."

Bone concerns gain traction

Bushby credits the Hart team with convincingly raising suspicions about the effect of neutering on orthopedic conditions. "I've adjusted my thinking for large breed male dogs," he said, making an exception for those allowed to roam freely. He credits the UC Davis studies with providing enough data in these cases to support delaying neutering until growth plates are closed.

At the end of July, a few weeks after the 35-breed study was published, UC Davis released the final paper in the series, a study of mixed breed dogs by size. This study found no significant increased occurrence of the studied cancers, compared with intact dogs, in any weight category. However, the authors reported increased incidences of joint disorders among larger neutered dogs. In the guidelines for age of neutering, the authors suggested neutering after 11 months of age for standard, large and giant females and standard and large males, and waiting until after 23 months for giant males. 

There is broad acceptance of early neutering as a risk for bone and joint issues in large dogs, in part because the role of sex hormones in keeping the development of a dog's bones is well understood. Sex hormones (mostly androgens) close growth plates earlier. So if you remove them, the bones tend to mature later, resulting in taller (longer), leaner animals.

Dr. Debra Tacium, who works at a small animal practice and municipal shelter in southern Quebec, Canada, prefers to delay neutering for larger responsibly-owned dogs because of the role of hormones in growth-plate closure. Her conversion began about six years ago, when she saw a presentation by an orthopedic specialist who demonstrated convincingly "that there's a significant difference in joint biomechanics when the angles are changed due to the growth plates being open for longer in early-neutered dogs," she said in an email. "This angle modification gets more significant the larger the breed."

She also said it is better for dogs to develop muscle mass under the influence of hormones to protect their joints and "to reduce the chances that any underlying genetic probability will lead to a debilitating joint disorder."

The decision is straightforward for male dogs; for females, she said, "it's a bit trickier." She prefers to spay right before the first heat or between the first and second heats to reduce the risk of mammary tumors.

In balancing risks and benefits of neutering, the UC Davis researchers contend that mammary cancer is a lesser of possible ills. "The perspective taken here is that it is the early occurring joint disorders and cancers that are the most impactful on the human caregivers, both emotionally and financially, as well as [on] their dogs," they write in the paper.

Not everyone would agree. Bushby expressed astonishment by the assumption that it's more devastating for a young dog to have an orthopedic condition than an old dog to have mammary cancer. "I was kind of blown away by this," Bushby said.

Shifting paradigm

Nardone and Cohen, the couple from North Seattle, decided to delay surgery until after their dog Pearl's first heat, which they expect to happen soon. Although they said they don't fully understand the science in the UC Davis golden retriever study, they are persuaded by the argument that sex hormones and related enzymes are key to a puppy's healthy development. Among their friends who have dogs, Nardone and Cohen said, many haven't heard about the research. When they learn about the plan for Pearl, they are curious to know more.

And they seem receptive. "I don't think people are looking at us like we are anti-vaxxers," Nardone said with a laugh.

Benjamin Hart makes no excuses for his role in helping upend established practice. "We realized what we were really working on was a kind of paradigm shift," he told VIN News, "from the automatic, 'Your dog is 6 months old, you better get it in here to get spayed or neutered,' to where you sit down with a client and say, 'Let's talk about spay and neutering now.' "

He suggests veterinarians start the conversation about neutering with clients early, treating each dog as an individual case, and proffering the latest relevant research so that pet owners can make informed decisions.

Dr. Joni Freshman, who consults for VIN in the areas of canine and feline reproduction, genetics and pediatrics, points out there are other factors to consider in addition to disease. Clients need to know what it may be like to live with intact pubertal animals and what special arrangements may need to be made, especially with regards to other canine household members, she explaine in an email. Owners who intend for their dogs to have the appearance of mature dogs of that breed need to understand what timing of spay means to breed type appearance, she added. 

There are signs that pet owners are helping steer the conversation about desexing. Veterinarians posting on the VIN message boards report an uptick in questions from pet owners on this topic during the past few years, with some citing research they found on their own, such as a 2009 study that found "exceptional longevity" in intact female Rottweilers. Other veterinarians report pet owners asking about hormone-sparing surgery, such as vasectomy or hysterectomy.

The reported percentage of dogs that are neutered in the U.S. dipped from 86% in 2015 to 78% in 2019, according to surveys by the American Pet Products Association.

Dr. Patty Khuly has seen a raised awareness around this issue in her small animal practice in Miami. Pet owners "simply want their pet treated as an individual," she wrote on a VIN message board. "Given the state of flux of our research into the ideal timing of spay and neuter … it makes sense to me that they would have legitimate questions and concerns that should not be discarded out of hand simply because 'that's what we've always done.'

"I'm not saying we shouldn't spay and neuter," she continued. "I'm just saying that one size does not fit all in many private practice settings, and our more involved clients are justifiably concerned."