THE SPAY/NEUTER DEBATE: ASSESSING RISK AND TIMING IN PUPPIES
Steve Thompson, DVM, DABVP (canine/feline) Saralyn Sharp, RVT, VTS (canine/feline)
Pet Wellness Clinic and Primary Care Service, Purdue University College of Veterinary Medicine
West Lafayette, IN USA
Overview of the Issue
In this day of municipalities passing mandatory spay/neuter ordinances and laws, it is a good time to revisit the benefits and detriments of spaying the female pet. The benefits to pet population seem to be
obvious. Less intact animals should result in fewer offspring, and with fewer total animals, this should
mean less unwanted animals turned over to shelters/rescues or running stray. Whether the benefits of
the surgery for an individual animal outweigh the detriments is not nearly as transparent. Traditionally,
the benefits of spaying your female dog or cat have been widely recommended as outweighing the
detriments. The overwhelming majorities of companion dogs maintained in the U.S. are spayed or
castrated. Increasingly in the U.S. neutering is being performed early, prior to one year of age. The
summary for the AVMA client brochure for Spaying/Neutering your pet is as follows, “By having your
dog or cat surgically sterilized, you will do your part to prevent the birth of unwanted puppies and
kittens and enhance your pet's health and quality of life.” Although inside the brochure it does list a few
detriments that are possible due to the surgery, overall, in the United States, the universal message has
been that a responsible owner, one who wants to ensure longevity and vitality in their pet, should spay
their pet, ideally before the pet’s first heat cycle.
Recent peer reviewed studies; however, have called this belief into question. After all, this societal
practice in the U.S. contrasts with the general attitudes in many European countries, where neutering is
commonly avoided and not generally promoted by animal health authorities. In Norway, for example, it
is illegal to neuter a dog without medical indication and a study of 461 dogs in Sweden reported that 99
percent of the dogs were intact, while 57 percent of dogs in Hungary were reported to be intact. In the
United Kingdom, 46 percent of dogs are reported as intact. These countries do not report
overwhelming stray populations, nor do they report excessive numbers of early deaths of individuals.
So what are the benefits and detriments of spaying a cat or dog?
Key Etiologic and Pathophysiologic Points
We will start with the benefits. As stated above, spaying a female dog/cat will prevent unwanted litters.
These unwanted litters are not able to become a burden on the community. Spaying (a complete
ovariohysterectomy) will prevent uterine issues, such as pyometra, or uterine tumors. Pet insurance
data in Sweden (where spaying is very uncommon) found that 23% of intact female dogs developed
pyometra before 10 years of age. Female dogs that have not whelped puppies are at elevated risk for
pyometra. Pyometra can usually be treated surgically or medically, but 4% of pyometra cases led to
death. Combined with the incidence of pyometra, this suggests that about 1% of intact female dogs will
die from pyometra. Ovarian tumors will also be prevented. Reduction in the risk of mammary tumors
is also a benefit of spaying your pet. In fact, in a study in Norway, mammary tumors are by far the most
common tumors in intact female dogs, constituting some 53% of all malignant tumors. Since
approximately 50-60% of mammary tumors in dogs are malignant, and there is a significant risk of
metastasis, these tumors are a significant cause of morbidity and mortality in intact female dogs.
Mammary tumors in dogs have been found to have estrogen receptors, and the published research
shows that the relative risk (odds ratio) that a female will develop mammary cancer compared to the
risk in intact females is dependent on how many estrus cycles she experiences.
Often behavioral benefits are touted as a reason to spay female dogs; however, studies have not
confirmed this. In one study, it was found that neutering was not associated with any differences in
trainability in female dogs in any breed (Serpell, Hsu 2012), and another study, found that relative to
intact female dogs of at least 1 year of age, the odds ratio for having bitten a member of the household
was highest for neutered male dogs, followed by neutered female dogs (Guy, et.al 2001). Neither of
these studies researched whether the dogs were neutered due to their aggressive behavior. In a breed
specific study of the English Cocker Spaniel (ECS), males were significantly more likely to show
aggression than females in situations and females were significantly more likely to show aggression
towards other dogs in the household. When ECSs which had been neutered before signs of aggression
were apparent, were compared with intact animals, neutered females were found to be more likely to
show aggression towards children in the household (Podberscek, Serpell 1997). While recommending
spaying females that show inappropriate aggression may prevent their genetics from being passed on, it
will not necessarily have a positive effect on ameliorating the aggression in the individual.
Recently, several studies have shown the benefits of leaving a female dog intact. One study revealed
that in Rottweiler dogs, like in humans, there is a strong female sex advantage for reaching exceptional
longevity. Interestingly, it appears that the longevity advantage over males is abolished in females that
undergo early or mid-life ovariohysterectomy. It was shown that in a population of 237 female
Rottweiler dogs who died between 1.3 years and 12.9 years, females that were intact for the first 4.5
years of life had 37% lower mortality than females that underwent elective OHE before then. The
researchers considered that observed associations between exposures and outcomes may not
necessarily be causal, therefore they explored alternative explanations for the association between dogs
remaining intact and exceptional longevity. They found no evidence that factors which may influence a
pet owner’s decision on age at OHE – such as earlier spay in dogs that were substandard in
conformation, or keeping superior specimens intact longer to obtain more offspring, could adequately
account for the strong association.
With regard to cancers, many studies appear to show an increase in incidence in neutered animals when
compared to intact animals for a number of different cancers.
A study on osteosarcoma (OSA) in several breeds has shown a 2-fold increase in occurrence in neutered
dogs relative to intact dogs. And another study on OSA in Rottweilers specifically, found that neutering
prior to 1 year of age was associated with an increased occurrence of 3-4 times that of intact dogs. The
combination of breed risk and early spay/neuter mean that Rottweilers spayed/neutered before one
year of age had a 25.1% (females) risk of developing osteosarcoma. These results are consistent with the
earlier multi-breed study, but also assess risk as a function of age at neuter. Combining the findings of
these two studies suggests that spaying of dogs before 1 year of age is associated with a significantly
increased risk of osteosarcoma in the Rottweiler breed.
Studies have shown that Hemangiosarcoma is a cancer that is affected by neutering in females. A study
of cardiac tumors in dogs found that cardiac Hemangioscarcoma risk for spayed females was greater
than 4 times that of intact females. A study on splenic Hemangiosarcomas found the spayed females
had more than 2 times the risk of developing this tumor as intact females. Early- versus late-spayed
females with regard to increased risk were not explored in either of these studies, and neither focused
on just one breed. In a study that focused solely on Golden Retrievers, Hemangiosarcoma was
diagnosed over 4 times more frequently in late-neutered females at 7.4 percent than intact females with
1.6 percent and early-neutered females with 1.8 percent, both significant differences.
Intact females had a significantly lower risk of developing LSA (lymphoma) in one study on the
epidemiology of LSA (lymphoma) in dogs, for comparison with human lymphoma, than spayed females
or neutered males or intact males. However, in the Golden Retriever study, although the rates of
occurrence of LSA were lower in both male and female intact dogs, than in the early-neutered dogs, the
difference was statistically significant only in males.
A study on cutaneous mast cell tumors (MCT) in several dog breeds, including the Golden Retriever,
examined risk factors such as breed, size, and neuter status, and the results showed a significant
increase in frequency of MCT in spayed females; four times greater than that of intact females. Again,
early- versus late-spayed relative risk for females was not explored.
The role of gonadal hormone removal in the occurrence of various cancers appears to be complicated.
The effects of early neutering on the increased rate of LSA, contrasts with the effects of late neutering in
females on MCT and HSA. The effects of late neutering associated with the increased occurrence of MCT
and HSA in females bring up the issue of the role of timing of estrogen alteration. It is postulated that
estrogen secretion may sensitize the pathways involved in microsatellite instability. While estrogen
remains in the system, it is protective against microsatellite instability-positive cancer cell activation and
reduces the risk of cancer. However, upon estrogen removal, microsatellite instability-positive cancer
cells become activated resulting in an increased occurrence of cancer. Neutering can be expected to
have an effect on the normal physiological development role of gonadal hormones on multiple organ
systems and therefore, have an effect on the occurrence of diseases, and such effects would be
influenced by gender and age at which neutering is performed.
Many involved in canine sports have long considered early spaying as a factor in the numerous joint
disorders that plague domestic dogs. It has been suggested that the occurrence of Hip Dysplasia (HD)
and Cranial Cruciate Ligament Disorder (CCL) in early-neutered dogs is a combined function of the effect
of neutering on growth plates, as well as the increase in weight on the joints brought on by neutering. It
is certainly true that gonadal hormones play a role in controlling the closure of bone growth plates.
Therefore, atypical growth plate closure, resulting from the absence of gonadal hormones, may play a
role in the appearance of a joint disorder, such as HD, CCL, and possibly Elbow Dysplasia (ED). Breedspecific gender vulnerabilities, including growth rate differences, and the timing of growth plate closure
(which is quicker in males than females) are all confounding factors that have an influence on the
expression of joint disorders and change the effect of neutering on it. For instance, in this study, the
occurrence of HD was doubled in early neutered cases, but in females, spaying did not appear to be
associated with an increased expression of HD. This may be due to the effect of gender on growth plate
development. Interestingly, growth plate disturbances in both males and females seem to have played
a role in the occurrence of CCL in early neutered dogs. One study documents a 3-fold increase in
excessive tibial plateau angle – a known risk factor for development of CCL – in large dogs. It has been
documented, across all breeds, neutered males and females were 2 to 3 times more likely than intact
dogs to have CCL than intact animals. In the aforementioned Golden Retriever study, there was no
occurrence of CCL in either intact male or intact female dogs, or in late-neutered females. However, in
early-neutered dogs, the occurrence reached 5.1 percent in males and 7.7 percent in females,
representing significant differences in occurrence from both intact and late neutered dogs.
While neutering has long been implicated to lead to a greater gain in body weight, and such a gain
would presumably complicate joint disorders, in the Golden Retriever study, when the BCS of earlyneutered dogs with joint disorders was compared to the BCS of early-neutered dogs without joint
disorders, the two were not significantly different. This would indicate that excess weight on the joint
was less a determinant in the occurrence of joint disorders, than a complicating factor. For females, the
timing of neutering is problematical because early neutering significantly increases the incidence rate of
CCL from near zero to almost 8 percent, and late neutering increases the rates of HSA to 4 times that of
the 1.6 percent rate for intact females and to 5.7 percent for MCT, which was not diagnosed in intact
females.
And finally, an increased risk of urinary incontinence (due to sphincter mechanism incompetence, also
known as hormonal urinary incontinence) in females has been attributed to spaying, particularly if
performed before the first estrous. Studies which compared neutered and entire dogs and found that
neutering was associated with an approximate eight-fold increase in rate of urinary incontinence.
Studies that attempted to prove that early-neutering was more likely to induce incontinence, however,
have had mixed results. Two UK studies found no evidence of an association between urinary
incontinence and age at spay and in one of these there was a trend towards a decrease in odds of
urinary incontinence with decreased age at spay, although this relationship was not statistically
significant. A study of re-homed dogs in the USA, on the other hand, reported a linear relationship
between age at spay and rate of urinary incontinence in dogs spayed between 6 weeks and 12 months
of age, with each one month decrease in age at spay associated with an increased rate of incontinence.
The different results may be explained in part by differences in age at neutering: in the UK studies, no
dogs were neutered before 4·5 months, whereas in the USA study, many were neutered before 4·5
months and some as young as six weeks. There is some weak evidence that the risk of urinary
incontinence decreases as the age at spay increases, up to 12 months of age, after which there is no
evidence of an effect of age at spay.
Before we begin to recommend that owners keep their animals intact, we want to share the results of a
study that looked at age of death, and cause of death in both neutered and intact dogs in a study in
university veterinary hospitals in the U.S. The study examined causes of death in over 40,000 domestic
dogs that died in veterinary teaching hospitals from 1984 to 2004. By comparing causes of death in dogs
that had undergone elective surgical sterilization and those that had not, they were able to measure the
lifespan cost of maintaining reproductive capability, and to determine the categories of disease
associated with this cost.
The initial dataset contained 80,958 records of dog death. When juvenile dogs and those with unknown
sterilization status were removed there were 70,574 dogs, representing 185 breeds. The average
number of diagnoses recorded per dog was 2.9 (range 1–32). Overall, 30,770 (43.6%) dogs were intact
and 39,804 (56.4%) dogs were neutered at the time of death. The mean age of death for intact dogs was
7.9 years versus 9.4 years for neutered dogs. Neutering increased life expectancy by 13.8% in males and
26.3% in females. Neutered dogs were dramatically less likely to die of infectious disease, trauma,
vascular disease, and degenerative disease. In contrast, neutered dogs died more commonly from
neoplasia and immune mediated disease. While intact reproductive capability was associated with
decreased lifespan in dogs, some causes of death were less frequent in intact dogs. Interestingly, the
largest–and opposite–effects were observed in two of the most common causes of death among dogs
within the dataset: neoplasia and infectious disease.
Neutered dogs had a decreased risk of death due to infection, and avoidance of infection may partly
explain their longer lifespans. The relationship between neutering and infectious disease could arise due
to increased levels of progesterone and testosterone in intact dogs, both of which can be
immunosuppressive. Neutering increased the risk of death due to neoplasia, but did not increase risk
for all specific kinds of cancer. Female dogs spayed before sexual maturity are unlikely to develop
mammary cancer because of the decrease in cumulative estrogen exposure associated with the absence
of the estrus cycle. However, it is not clear why the frequency of some cancers outside the reproductive
system, including lymphoma and osteosarcoma, is influenced by neutering, while the frequency of
others, such as melanoma and squamous cell carcinoma, is not. The increased risk of death due to
cancer observed in neutered dogs could be due to the fact that in both sexes, dogs neutered before the
onset of puberty grow taller than their intact counterparts as a result of reduced estrogen signaling.
Recent studies in humans suggest that growth is a risk factor for a number of different cancers.
Additionally, neutering and disease risk might both be correlated with specific canine behaviors. If
allowed, intact male dogs are more likely than neutered dogs to roam, and to fight with other dogs, and
intact female dogs show more dominance aggression than spayed females. These behaviors might
increase the risks of both infectious and traumatic causes of death among intact dogs.
Summary including 5 KEY “TAKE HOME” POINTS
1.
2.
3.
4.
5.
Spaying benefits include controlling reproduction and reduced mammary tumor incidence
Specific cancer and orthopedic risks are increased in some dog breeds post spaying.
Spaying does not typically mitigate aggressive behavior in female dogs
Urinary incontinence risk may be reduced by delaying spaying but ideal time is still unclear
More studies needed to examine lifetime estrogen exposure and health risks and benefits
Summary
To better understand the lifelong health consequences of ovariohysterectomy, we need studies
situating the health hazards of keeping ovaries. We need to definitively discover the risk of developing
and dying from mammary cancer and pyometra–within the context of duration of lifetime ovary
exposure and longevity. We need studies that will provide insights on how the timing of spaying effects
trade-offs that impact overall health. More research should be performed to decide if an ovariectomy,
hysterectomy, or an ovariohysterectomy is the healthiest alternative as a spaying procedure, or if a
chemical birth control could have a more healthful effect. It seems that neutering pets, like most things
in life, is not black/white. If the pet has a responsible owner, spaying, and age of the pet at spaying,
should be discussed and decided for each pet as an individual, rather than at an arbitrary age.
References/Suggested Reading
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Multidisciplinary Journal of The Interactions of People & Animals, 18:3, 96-207. 2012
Guy NC, et. al. Demographic and aggressive characteristics of dogs in a general veterinary caseload,
Applied Animal Behaviour Science. 4:1,15–28. 2001
Bradshaw JWS, et al. Feral cats: their role in the population dynamics of Felis catus, Appl Anim Behav Sci
65:3, Pages 273–283.1999
Tasker L. Stray Animal Control Practices (Europe), A report into the strategies for controlling stray dog
and cat populations adopted in thirty-one countries. World Society for the Protection of Animals. 2007
Palmer C, Corr S, Sandøe P. Inconvenient desires: should we routinely neuter companion animals?
Anthrozoos, 25(Suppl.), S153-S172. 2012
Water DJ, et. al. Exploring mechanisms of sex differences in longevity: lifetime ovary exposure and
exceptional longevity in dogs. Aging Cell 8:752–755. 2009
Root Kustritz, MV. Determining the optimal age for gonadectomy of dogs and cats, JAVMA, 231:11,
1665 – 1675. 2007
Cooley DM, et al. Exceptional Longevity in Pet Dogs Is Accompanied by Cancer Resistance and Delayed
Onset of Major Diseases. J Gerontology 58:12, 1078-84. 2003
Waters, DJ. In search of a strategic disturbance: some thoughts on the timing of spaying, Clinical
Theriogenology. 3:433-37. 2011