| |
CLICK
HERE TO DOWNLOAD THE PDF FILE
ORIGINAL RESEARCH article
Front. Vet. Sci., 07 July 2020
Sec. Animal Reproduction - Theriogenology
Volume 7 - 2020 | https://doi.org/10.3389/fvets.2020.00388
Assisting Decision-Making on Age of Neutering
for 35 Breeds of Dogs: Associated Joint Disorders, Cancers, and
Urinary Incontinence
Benjamin L. Hart1*, Lynette A. Hart2, Abigail P.
Thigpen2 and Neil H. Willits3
1Department of Anatomy, Physiology and Cell Biology,
School of Veterinary Medicine, University of California, Davis,
Davis, CA, United States 2Department of Population Health and Reproduction,
School of Veterinary Medicine, University of California, Davis,
Davis, CA, United States 3Department of Statistics, University of
California, Davis, Davis, CA, United States
Neutering (including spaying) of male and female dogs in the first
year after birth has become routine in the U.S. and much of Europe,
but recent research reveals that for some dog breeds, neutering
may be associated with increased risks of debilitating joint disorders
and some cancers, complicating pet owners' decisions on neutering.
The joint disorders include hip dysplasia, cranial cruciate ligament
tear or rupture, and elbow dysplasia. The cancers include lymphoma,
mast cell tumor, hemangiosarcoma, and osteosarcoma. In previous
studies on the Golden Retriever, Labrador Retriever and German Shepherd
Dog, neutering before a year of age was associated with increased
risks of one or more joint disorders, 2–4 times that of intact
dogs. The increase was particularly seen with dogs neutered by 6
months of age. In female Golden Retrievers, there was an increase
in one or more of the cancers followed to about 2–4 times
that of intact females with neutering at any age. The goal of the
present study was to expand and use the same data collection and
analyses to cover an additional 29 breeds, plus three varieties
of Poodles. There were major breed differences in vulnerability
to neutering, both with regard to joint disorders and cancers. In
most cases, the caregiver can choose the age of neutering without
increasing the risks of these joint disorders or cancers. Small-dog
breeds seemed to have no increased risks of joint disorders associated
with neutering, and in only two small breeds (Boston Terrier and
Shih Tzu) was there a significant increase in cancers. To assist
pet owners and veterinarians in deciding on the age of neutering
a specific dog, guidelines that avoid increasing the risks of a
dog acquiring these joint disorders or cancers are laid out for
neutering ages on a breed-by-breed and sex basis.
Introduction
In the U.S. and much of Europe, the practice of neutering male
and spaying female dogs (herein both referred to as neutering) has
become routine (1) and is increasingly being performed at, or before,
6 months of age. At the same time, several investigations have revealed
that joint disorders and some cancers may increase in association
with neutering of males and/or females. For example, in studies
that did not focus on specific breeds or ages of neutering, one
found that hip dysplasia and cranial cruciate ligament tears or
ruptures were significantly more likely in neutered than intact
males and females (2). Another study found that neutering was associated
with a 3-fold increase in excessive tibial plateau angle (3), which
is a risk factor for development of cranial cruciate ligament tears
or rupture. Neutering is reported to be a risk factor for canine
intervertebral disc herniation in Dachshunds (4). Certain cancers
are also known to be more likely in neutered than intact dogs. The
occurrence of lymphoma was found to be higher in spayed than intact
females (5), as was the occurrence of mast cell tumors (6) and hemangiosarcoma
(7). A study of over 40,000 dogs utilizing the Veterinary Medical
Database found that neutered males and females were more likely
to die of cancer than intact dogs (8). A recent finding was that
the absence of estrogen from spaying females was associated with
accelerated brain aging (9). Another recent report from the Golden
Retriever Lifetime Project is that neutering at <6 months increases
the risk of cranial cruciate ligament injury (10). Most of the studies
cited above offer no useful clinical information or guidelines with
regard to the various diseases that may occur in association with
neutering in a specific breed.
In an attempt to address the absence of breed-specific information
on joint disorders and cancers associated with neutering, we undertook
a project focusing on various specific breeds using data collection
and analyses with our extensive veterinary hospital database where
the same diagnostic criteria could be applied to all breeds. We
started with popular breeds well-represented in the database, initially
with the Golden Retriever (11, 12), Labrador Retriever (12) and
German Shepherd Dog (13). The joint disorders examined included
cranial cruciate ligament tears or rupture (CCL), hip dysplasia
(HD) and elbow dysplasia (ED). The cancers examined, which previous
studies found could be affected by neutering, were lymphoma/lymphosarcoma
(LSA), hemangiosarcoma (HSA), mast cell tumors (MCT), and osteosarcoma
(OSA).
In the Labrador Retrievers, Golden Retrievers, and German Shepherd
Dogs, there was an increase in the incidence of one or more of the
joint disorders with neutering in the first year in males and females
to 2–4 times >3–5% incidence in intact dogs. In female
Golden Retrievers, neutering at any age was associated with an occurrence
of one or more of the cancers followed to 2–4 times higher
than the 5 percent incidence in intact females. But in male Golden
Retrievers, and in male and female Labrador Retrievers and German
Shepherd Dogs, there was no evident increase in cancers above that
of the dogs left intact. Preliminary analyses from some small-dog
breeds revealed no apparent increased risks of joint disorders with
neutering. Thus, the research that had been undertaken revealed
a wide range of breed-specific differences in disease vulnerability
to neutering.
The purpose of this study was to analyze, in a variety of additional
breeds, the increased risks, if any, of the above specified joint
disorders and cancers associated with neutering male and female
dogs at various ages, so as to increase the information available
to pet owners and veterinarians for consideration when making decisions
regarding neutering specific dogs. We added 29 new breeds to the
study, separating three varieties of Poodles, for a total of 32
breed groups (referred to as breeds); this made a total of 35 breeds
with the Goldens, Labs and German Shepherds included. The goal was
to use the same veterinary hospital database and diagnostic criteria
for the diseases as was used with the published studies on the retrievers
and German Shepherds so as to allow for direct comparisons among
various breeds. The primary purpose was to offer readers some evidence-based
information on breed-specific differences with vulnerability to
neutering, including suggested guidelines for neutering ages to
avoid increasing long-term health risks of neutering, if any. A
secondary, unforeseen, purpose was to document breed-specific differences
in the increases in some cancers associated with removal of gonadal
hormones, as an area for possible research on genetic aspects of
cancer occurrence.
Methods
Ethics Statement
Hospital records of the Veterinary Medical Teaching Hospital (VMTH)
provided the retrospective dataset used. In conformity with the
campus policy, faculty of the University of California-Davis, School
of Veterinary Medicine, are allowed use of the record system for
research purposes. No animal care and use committee approval was
required, and strict confidentiality of the owners and their dogs
was maintained.
Subjects Breed Categories
In addition to the Golden Retriever, Labrador Retriever, and German
Shepherd Dog, the other breeds chosen for this project included
those most frequently occurring in the database and those chosen
to obtain a sampling of giant breeds or small-dog breeds. The final
list of 35 (including three varieties of Poodle) represented in
the present study are, alphabetically, the: Australian Cattle Dog,
Australian Shepherd, Beagle, Bernese Mountain Dog, Border Collie,
Boston Terrier, Boxer, Bulldog, Cavalier King Charles Spaniel, Chihuahua,
Cocker Spaniel, Collie, Corgi (Pembroke and Cardigan combined),
Dachshund, Doberman Pinscher, English Springer Spaniel, German Shepherd
Dog, Golden Retriever, Great Dane, Irish Wolfhound, Jack Russell
Terrier, Labrador Retriever, Maltese, Miniature Schnauzer, Pomeranian,
Poodle-Miniature, Poodle-Standard, Poodle-Toy, Pug, Rottweiler,
Saint Bernard, Shetland Sheepdog, Shih Tzu, West Highland White
Terrier, and Yorkshire Terrier.
Study Parameters
The present study examined the occurrence in both sexes of the
joint disorders: HD, CCL and ED. Also examined in both sexes were
the cancers LSA, HSA, MCT, and OSA, because these had been shown
in some multi-breed studies to be increased in risks with neutering.
In addition, mammary cancer (MC), pyometra (PYO), and urinary incontinence
(UI) were examined in female dogs. Of interest was the possible
association of early neutering and the occurrence of intervertebral
disc disorders (IDD) in the Corgi and Dachshund, two breeds known
to be at risk for these diseases. All of the above diseases were
examined with regard to dogs neutered in one of the age periods
of: <6 mo., 6–11 mo., 1 year (12 to <24 mo.) or 2–8
years, or left intact. The diseases were tracked until the dogs
were last seen at the hospital, or through 11 years of age, if seen
past their 12th birthday.
Mammary cancer is a late occurring cancer with the median age
of diagnosis being 10.1 years in one study (14). Tracking cancers
through 11 years of age would be presumably sufficient to catch
most cases of MC if the case record had information extending to
that age. However, most case records did not extend to that age.
As an additional point of comparison, percentages of MC occurrence
were looked at in just females tracked through 8 years of age or
beyond, including diagnosed MC cases beyond the 12th birthday cut-off,
which was the cut-off used for all other data.
Data Collection and Presentation
The computerized hospital record system of the VMTH provided the
dataset. The hospital, with currently over 50,000 cases admitted
per year, is a secondary and tertiary facility as well as being
a primary care facility. The statistical evaluations, with standardized
diagnostic criteria applied to various diseases and taking into
account sex and different ages of neutering, required a large database
with a computerized record system. The study focused on proportional
differences in disease occurrences between the neuter age groups
and intact dogs of the same breed and sex.
The study period represented 15 years of data for most breeds.
The inclusion criteria were date of birth, age at neutering (if
neutered), and age of diagnosis or onset of clinical signs for diseases
of interest. As mentioned, age at neutering was designated as <6
mo., 6–11 mo., 1 year (12 to <24 mo.), and 2–8 years
(2 to <9 years). The term “early neutering” is sometimes
used below to refer to neutering in the first year, combining cases
for both the <6 mo. and 6–11 mo. neuter periods. For MC,
PYO, and UI, only females were examined. While UI does occur in
males, it is predominantly an issue in females.
For all neutered dogs that developed a disease of interest, records
were examined to confirm that the dog was neutered prior to the
diagnosis or signs of the disease. If the dog developed signs of
the disease prior to neutering, the dog was considered intact for
analysis of that disease. However, for any disease that occurred
after neutering, the dog was considered neutered for analysis of
that disease. For any disease of interest that occurred before 12
months of age, the dog was removed from that disease analysis, but
included in analyses of other diseases. Therefore, the number of
cases for various diseases varied in the analyses for different
disease occurrences.
The age at neutering was sometimes not included in the hospital
records, so telephone calls to the referring veterinarians were
made to obtain the neutering dates or ages. Nonetheless, there were
many neutered dogs where age at neutering was not available from
the VMTH records or the referring veterinarian, so these dogs were
excluded from the study. Of course, this was not an issue with the
sample of intact dogs, so there were proportionately more intact
cases in the final dataset for each breed than would be expected
in the general population. However, the proportion of dogs with
a disease, whether intact or neutered, was not affected by the overrepresentation
of intact dogs in the database.
The criteria for disease diagnoses were the same as in previous
studies on the retrievers and German Shepherd Dog (11–13).
A dog was considered as having a disease of interest if the diagnosis
was made at the VMTH, or by a referring veterinarian and later confirmed
at the VMTH. For joint disorders (HD, ED, and/or CCL), dogs typically
presented with signs of lameness, difficulty in moving, and/or joint
pain. The diagnosis was confirmed by orthopedic examination, radiographic
evidence, and/or surgery. In Dachshunds and Corgis, where intervertebral
disc disorders (IDD) is a concern, the diagnosis included herniation,
rupture, extrusion, protrusion, fracture, compression, stenosis,
or spinal cord injury. For cancers (LSA, HSA, MCT, OSA, MC), the
diagnosis was based on the presence of a tissue mass, lumps on the
skin or enlarged lymph nodes, and confirmed by chemical panels,
appropriate blood cell analyses, imaging, histopathology, and/or
cytology. PYO was confirmed by ultrasonic evidence and/or post-surgically
after removal of the uterus. UI was confirmed by clinical signs
of abnormally frequent urination, urinalyses and exclusion of urinary
tract infection and/or other disease. If a diagnosis was listed
in the record as “suspected” based on some clinical
signs but not confirmed, the case was excluded from the analysis
for that specific disease, but the dog was included in other disease
analyses.
Although body condition scores have been reported to be a factor
in the occurrence of joint disorders (3, 15), our previous studies
on the retrievers and German Shepherd Dog found no significant relationship
when body condition scores were compared between dogs with and without
a joint disorder. Therefore, in the current paper the body condition
score is not reported for each breed.
Statistical Analyses
Survival analysis was used to test for differences with respect
to the hazard of a disease in the neutered and intact groups, while
adjusting for the differences in time at risk for a disease. The
groups were initially compared using a Kaplan Meier life table analysis.
Post-hoc comparisons among the subgroups were based on least squares
means of the hazard within each subgroup. For comparisons where
the Kaplan Meier test showed significance at the p <0.05 level,
both the log-rank and Wilcoxon tests were used for further analyses.
Because joint disorders are expected to be seen at a similar risk
throughout a dog's lifespan, regardless of age, the log-rank test
was used initially for the joint disorders. If the log-rank test
did not show significance but the Wilcoxon test did for joint disorders,
the Wilcoxon test result was reported with significance level and
an asterisk. The reverse rule of thumb was used with cancers where
the first test examined was the Wilcoxon test, since the risk of
cancer is expected to be higher in older dogs. If the Wilcoxon test
did not show significance but the log-rank test did for cancers,
the log-rank test result was reported with significance level and
an asterisk. For all statistical tests, the two-tailed statistical
level of significance was set at p <0.05 and reported as either
p < .05 or p <0.01. Each breed was analyzed separately, and
there were no statistical comparisons between breeds. However, the
overall findings with each breed allow for some general comparisons.
Data Presentation
For each breed represented on a separate page in Appendix 1, the
numbers of intact and neutered males and females are given. In the
tables, the percentage of dogs with each of the diseases and the
percentage having at least one of the joint disorders and at least
one of the cancers (except MC) was calculated for intact males and
intact females as well as those neutered at various age ranges.
Statistical analyses compared the occurrences of joint disorders
and cancers between each neuter period and intact dogs. If the comparison
was significant at either the p <0.05 or p <0.01 level, the
data were bolded and the p-value was given. The detailed datasets
are available online (Figshare, doi: 10.6084/m9.figshare.7231010).
Three breeds for which findings have been previously published (Golden
Retriever, Labrador Retriever, German Shepherd Dog) are included
to present an overall picture in the same Appendix 1. The data for
these three breeds were expanded through 11 years of age, to provide
continuity among breeds and diseases.
For each breed, a short paragraph summarizes the main findings on
joint disorders (HD, CCL, ED), cancers (LSA, HSA, MCT, OSA) for
both males and females, and MC, PYO and UI for females. For Dachshunds
and Corgis, the occurrence of IDD is listed for both sexes. Survival
analyses were not done on IDD occurrence because the condition represented
so many different disease diagnoses. Also included in the breed
summary information is a suggested guideline for neutering age for
males and females to avoid increasing the risks of a disease under
consideration. When there was no noticeable occurrence of an increase
in joint disorders or cancers with neutering, the guideline statement
was made that those wishing to neuter should decide on the appropriate
age (or briefly stated as choice in Table 1). When neutering at
<6 months was associated with an increased disease risk but no
increased risk was evident with neutering beyond 6 months, the default
recommended guideline was neutering beyond, 6 months.
Table 1. Suggested Guidelines by Breed for Age
of Neutering.
Results
The breed-by-breed findings are presented in four different formats.
One format, seen in this section below, is a short paragraph for
each breed. The occurrence of the joint disorders and the cancers
followed is reported for the intact and neutered dogs, and the increase
in the two disease types over that of the intact dogs, if significant,
is reported. Other findings are also mentioned if appropriate, such
as IDD occurrence in Dachshunds and Corgis. A second format, represented
in Table 1, is a very brief summary of spaying and neutering guidelines
based on findings regarding joint disorders and cancers for each
breed, allowing the reader to quickly scroll through the various
breeds. In the third format, the data-based findings, with statistical
notations for each breed, are reported in Appendix 1. In the fourth
format, the raw data allowing the reader to perform their own calculations,
if desirable, is available in Figshare.
The mean age of last entry was calculated for intact and neutered
males and females for each breed and presented in Appendix 2. Across
all breeds the mean age of last entry in the record for neutered
males was 5.5 years (range 3.71–6.54), for neutered females
5.7 years (range 4.21–6.97), for intact males 4.9 (range 4.15–7.11),
and intact females 4.7 (range 3.41–6.32). Upon perusal of
the data, it is evident that the mean age of data entry for intact
dogs was younger than that of neutered dogs, especially for females,
where there is disparity of almost 1 year. To address the issue
of whether the lower age of last entry for intact dogs could have
resulted in a lower rate of disease occurrence in intact dogs in
either joint disorders or cancers, we examined data of dogs where
the last entry was at 8 years or beyond. We looked at three breeds
with the largest databases (Golden Retrievers, Labrador Retrievers,
and German Shepherd Dogs) and where there were significant differences
in disease diagnoses between early neutered and intact dogs. Using
these parameters, the occurrences of joint disorders in Golden Retrievers
for those neutered at = 6mo. vs. intact, in males, there was a 6-fold
difference (18% vs. 3%) and in females 3-fold (25 vs. 8%). For male
Labrador Retrievers, the figures were 22 vs. 8% and in females 33
vs. 10%. For male German Shepherd Dogs, the figures were 33 vs.
2% and for females, 29 vs. 9%. For cancers in female Goldens, the
figures were 26 vs. 14%. The incidence figures, although not sufficient
for meaningful statistical analyses, are consistent with the larger
database where all ages are included. Thus, while the age of the
last visit is a limitation for analyses on late-occurring cancers
and joint disorders, the examples chosen for dogs seen at the age
of 8 years or beyond are consistent with the overall results presented
here; these results appear to represent what would be seen in the
general situation.
General Findings
Looking at the occurrences of these joint disorders and cancers,
it is clear that most breeds are unaffected for these diseases by
age of neutering. Vulnerability to joint disorders associated with
neutering is generally related to body size. Small-dog breeds –
Boston Terrier, Cavalier King Charles Spaniel, Chihuahua, Corgi,
Dachshund, Maltese, Pomeranian, Poodle-Toy, Pug, Shih Tzu, Yorkshire
Terrier – do not appear to have an increased risk in joint
disorders with neutering compared to the breeds of larger size.
However, in the breeds of larger body size there were differences
among the breeds with the two giant breeds – Great Danes and
Irish Wolfhounds – showing no indication of increase in one
or more joint disorders with neutering at any age.
Although the occurrence of MC was tracked, the female mean age at
the last hospital visit for all breeds ended short of the reported,
late-onset mean age of MC occurrence in intact female dogs. Thus,
the low occurrence of MC in intact females (typically under 6 percent)
cannot be expected to represent the actual incidence over a female's
lifetime. When the percentage of MC was calculated for only those
dogs seen through 8 years of age or older (including cases diagnosed
past the 12th birthday), the results did not appear appreciably
different than the percentages seen using the study age range. However,
the number of dogs seen through age 8 or beyond was fairly small,
so the analysis results might change with an increased sample size
of these older dogs.
The following are brief summaries for each of the breeds along
with suggested guidelines for age of neutering. See Appendix 1 for
the complete data set, including statistical analyses for each breed.
Australian Cattle Dog
The study population was 61 intact males, 58 neutered males, 48
intact females, and 70 spayed females for a total of 237 cases.
In this sample, 5 percent of intact males and 2 percent of intact
females were diagnosed with one or more joint disorders. Neutering
males was not associated with any increased risk in joint disorders,
but there was an association with spaying females at <6 mo. where
the risk of a joint disorder increased to 15 percent (p <0.05).
The occurrence of cancers was low for males and females left intact
(0 and 3 percent, respectively). There were no evident occurrences
of the cancers in dogs neutered at various ages. The occurrence
of MC in intact females was 6 percent and in those spayed at 2–8
years, 6 percent. For females left intact, 4 percent were reported
with PYO. UI was not reported in any of the spayed or intact females.
Lacking a noticeable occurrence of increased joint disorders or
cancers in neutered males, those wishing to neuter should decide
on the appropriate age. In females, the increased risk of a joint
disorder with spaying occurred only at the <6 mo. range, so the
suggested guideline is spaying at, or beyond, 6 months.
Australian Shepherd
The study population was 93 intact males, 135 neutered males, 76
intact females, and 136 spayed females for a total of 440 cases.
In this sample, 3 percent of intact males and 4 percent of intact
females were diagnosed with one or more joint disorders. Neutering
males and females was not associated with any evident increased
risk in joint disorders. The occurrence of cancers was 9 percent
for intact males and, in contrast, only about 1 percent for intact
females. Neutering males did not appear to be associated with an
overall increased risk of cancers above the rather high level of
intact males. However, spaying females at 6–11 mo. and at
2–8 years was associated with a 7–8 percent risk in
cancers which may have reached significance with a larger sample
size. The occurrence of MC in intact females was zero, but was 8
percent in females spayed at 2–8 years. For females left intact,
5 percent were reported with PYO. UI was reported in just 1 percent
of early-spayed females. Lacking a noticeable occurrence of increased
joint disorders or cancers in neutered males, those wishing to neuter
should decide on the appropriate age. The guideline for females
is the same while also maintaining vigilance for the cancers which
may be associated with spaying beyond 6 months, or else leaving
the female intact and being vigilant for MC.
Beagle
The study population was 42 intact males, 82 neutered males, 45
intact females and 87 spayed females for a total of 256 cases. Just
2 percent of intact males were diagnosed with one or more joint
disorders, but with neutering at 6–11 mo. joint disorders
increased 7-fold to 15 percent, which may have reached significance
with a larger sample size. None of the females left intact or spayed
had a joint disorder. None of the intact males or females was diagnosed
with any of the cancers followed. There was no evident increased
occurrence of cancers in neutered males and females. There was no
occurrence of MC in intact or late-spayed females. There was 1 case
of PYO in intact females (2 percent). UI was reported in only 2
percent of early-spayed females.
For males, in light of a possible increase in joint disorders for
those neutered at 6–11 mo., the suggested guideline is to
delay neutering males until beyond a year of age. Lacking a noticeable
occurrence of increased joint disorders or cancers in neutered females,
those wishing to neuter should decide on the appropriate age.
Bernese Mountain Dog
The study population was 59 intact males, 74 neutered males, 37
intact females, and 65 spayed females for a total of 235 cases.
The percentage of intact males with at least one joint disorder
was 4 percent and for intact females, 11 percent. Neutering males
any time prior to 2 years of age was associated with a significant
increase in at least one joint disorder to 23–24%, about a
6-fold increase over intact males (p <0.01). Spaying females
before 6 mo. increased the likelihood of a joint disorder to over
3-fold that of intact females, but this did not reach significance.
The occurrence of one or more of the cancers followed was 9 percent
for both intact males and intact females. There was no evident increase
in cancer risk in males related to neutering, but with females,
spaying at <6 mo. was associated with a 2-fold increase above
that of intact females. There was no occurrence of MC in females,
whether left intact or neutered at any age, and a 5 percent occurrence
of PYO in intact females. There was no occurrence of UI in intact
or spayed females. Reflecting the increased risk of joint disorders
for males, the suggested guideline for neutering males is delaying
neutering until well-beyond 2 years. Lacking a significant occurrence
of increased joint disorders or cancers in neutered females, those
wishing to neuter should decide on the appropriate age.
Border Collie
The study population was 105 intact males, 85 neutered males, 88
intact females, and 121 spayed females for a total of 399 cases.
In this sample 2–3% of intact males and females were diagnosed
with one or more joint disorders, and neutering males and females
was not associated with any evident increased risk in joint disorders.
The occurrence of one or more of the cancers followed in intact
males was 2 percent and none for females left intact. For males,
there was a significant increased risk in one or more of the cancers
to 13 percent with neutering at 6–11 mo. (p <0.05), and
for females there was a significant increase in the cancers to 11
percent with spaying at 6–11 mo. (p <0.01). The occurrence
of MC in intact females was just 1 percent, and for PYO, 4 percent.
UI was reported in just one spayed female. The suggested guideline
for neutering, given the significant risk of cancers, is holding
off neutering of both sexes until beyond a year of age.
Boston Terrier
The study population was 75 intact males, 67 neutered males, 54
intact females, and 96 spayed females for a total of 291 cases.
None of the intact or neutered males or females was diagnosed with
one or more joint disorders. For cancers, the story is a bit different
in that 5 percent of intact males were diagnosed with one or more
cancers and 10 percent of males neutered at <6 mo., and 12 percent
of males neutered at 6–11mo. had cancers (p <0.01, the
two neuter periods combined). For females, 2 percent of intact females
had one or more of the cancers and with spaying, there was no evident
increase of cancers. The occurrence of MC in intact females was
2 percent and for PYO, 7 percent. UI was 2 percent in early-spayed
females. In light of the significant increase in cancers in males
with neutering through 11 months of age, the suggested guideline
for males is delaying neutering to beyond a year of age. Lacking
a noticeable occurrence of increased joint disorders or cancers
in neutered females, those wishing to neuter should decide on the
appropriate age.
Boxer
The study population was 220 intact males, 203 neutered males, 128
intact females, and 210 spayed females, for a sample size of 761
cases. Males and females left intact had just a 2 percent occurrence
of joint disorders, with neutered males and females showing no apparent
increase in this measure. The occurrence of one or more of the cancers
followed in intact males was 17 percent, and for intact females,
11 percent. Neutering males before 2 years significantly raised
the risk of a cancer over that of intact males to 32 percent (p
<0.01). The same pattern of increase in cancers was seen in spaying
females with up to 20 percent of females having one or more of the
cancers with spaying done before 2 years, an increase that was not
significant, but with an expanded database may have been. There
was no occurrence of MC in intact females. PYO was diagnosed in
2 percent of intact females. Just 1 percent of spayed females were
diagnosed with UI. Given the risk of increased cancers, the suggested
guideline for both sexes is to delay neutering until beyond 2 years
of age.
Bulldog
The study population was 198 intact males, 156 neutered males, 90
intact females, and 114 spayed females for a sample of 558 cases.
The occurrence of joint disorders in intact males was 7 percent
and 5 percent in intact females. Neutering at <6 mo. raised the
incidence to 15 percent for males and to 18 percent for females,
which did not reach significance for either. The cancers followed
occurred at the 6 to 7 percent level in intact males and females.
There were no significant increases above this with neutering males
or females. The occurrence of MC in females left intact was 1 percent
and 2 percent with spaying at 2–8 years. There was a 2 percent
occurrence of PYO in intact females and no UI in early spayed females.
Lacking a significant occurrence of increased joint disorders or
cancers in neutered males or females, those wishing to neuter should
decide on the appropriate age, but some people may wish to be cautious
in view of the possible apparent risk in joint disorders.
Cavalier King Charles Spaniel
The study population was 51 intact males, 72 neutered males, 87
intact females, and 76 spayed females, for a sample size of 286
cases. For males and females left intact, the occurrences of one
or more joint disorders were just 4 and 1 percent, respectively,
and for both sexes neutering was not associated with any increase
in this measure. The occurrences of cancers in intact males were
2 percent and zero for intact females. For both sexes neutering
was not associated with any increase in this measure. The occurrence
of MC in females left intact was zero. The occurrence of PYO was
2 percent in intact females. There was no occurrence of UI in spayed
females. Lacking a noticeable occurrence of increased joint disorders
or cancers in neutered males or females, those wishing to neuter
should decide on the appropriate age.
Chihuahua
The study population was 261 intact males, 189 neutered males, 298
intact females, and 289 spayed females for a total sample of 1,037
cases. For both males and females, neither those left intact, nor
those neutered at any age had a noteworthy occurrence of a joint
disorder. The cancers followed in both intact and neutered males
and females were <5 percent with no evident increase with neutering
at any age. The occurrence of MC in females left intact was 1 percent,
and in females neutered at 2–8 mo., 4 percent. In intact females,
PYO was diagnosed in 2 percent. There was no UI diagnosed in any
of the spayed females. Lacking a noticeable occurrence of increased
joint disorders or cancers with neutering in either sex, those wishing
to neuter should decide on the appropriate age.
Cocker Spaniel
The study population was 71 intact males, 112 neutered males, 61
intact females, and 127 spayed females, for a sample size of 369
cases. The occurrence of at least one joint disorder was seen in
1 to 3 percent of the intact males and females. Neutering males
at <6 mo. was associated with a significant increase of this
measure to 11 percent (p <0.01). Spaying females was not associated
with an increase in joint disorders. The occurrence of one or more
of the cancers followed was 6 percent in intact males with no increase
with neutering. Although there was no occurrence of cancers in intact
females, this measure rose significantly to 17 percent in females
spayed between 1 and 2 years of age (p <0.01), entirely due to
MCT. For females left intact, 11 percent were diagnosed with MC
and 5 percent with PYO. None of the spayed females developed UI.
The suggested guideline for males is neutering beyond 6 months of
age. Given the increased cancer risk for females spayed at a year
of age, the suggested guideline is delaying spaying until beyond
2 years of age.
Collie
The study population was 29 intact males, 26 neutered males, 24
intact females, and 37 spayed females, for a sample size of 116
cases. The occurrence of at least one joint disorder was seen in
7 percent of the intact males and in none of the intact females.
None of the neutered males or females had a noteworthy occurrence
of a joint disorder. The occurrence of one or more of the cancers
followed was 11 percent for intact males and none for the intact
females. There was no evident increase of cancers in males with
neutering, and in females, there was an increase of cancer to 40
percent in those spayed at <6 mo., which may have reached significance
with a larger sample size. For females left intact, 4 percent were
diagnosed with MC, and 16 percent were diagnosed with PYO. Of females
spayed at 6–11 mo., 13 percent had UI. Lacking a noticeable
occurrence of increased joint disorders or cancers in neutered males,
those wishing to neuter a male should decide on the appropriate
age. For females, given the apparent risks of cancers with spaying
at <6 mo. and UI with spaying at 6–11 mo., the guideline
is to delay spaying until the female is a year old.
Corgi (Welsh), Pembroke and Cardigan
The study population was 42 intact males, 78 neutered males, 50
intact females, and 70 spayed females, for a total sample size of
240 cases. Although these are two breeds, they vary only a little
in size, so these two breeds are combined for statistical analyses
and display of data. The occurrence of at least one joint disorder
in intact males was 5 percent and for intact females 6 percent.
There was no significant increase in this measure in males or females
with neutering. This is one of the breeds where intervertebral disc
disorders are a concern, and in 3 percent of intact males and 8
percent of intact females, IDD was reported. In males neutered before
6 months, the occurrence of IDD reached 18 percent, and in females
there was no increase with neutering. The occurrence of one or more
of the cancers followed was 5 percent in intact males and 6 percent
in intact females. In neutered males and females, there was no evident
increase in cancers. For females left intact, the occurrence of
MC was 8 percent, and there was zero occurrence of PYO. There was
no diagnosis of UI in spayed females. The suggested guideline for
age of neutering for males, given the increase in IDD with neutering
at <6 mo., is beyond 6 months. Lacking a noticeable occurrence
of increased joint disorders, IDD, or cancers with neutering females,
those wishing to neuter a female should decide on the appropriate
age.
Dachshund
The study population was 177 intact males, 170 neutered males, 99
intact females, and 212 spayed females, for a total sample size
of 658 cases. Joint disorders were basically absent in males and
females, left intact or neutered. This is a breed plagued by intervertebral
disc disorders, and in this sample 53 percent of intact males and
38 percent of intact females were diagnosed with a form of IDD.
There was no evident increase in this measure with neutering of
males or females. The occurrence of the cancers followed was <1%
in both intact males and females, with no indication of an increased
risk with neutering. For females left intact, the occurrence of
MC was 1 percent and for PYO, 4 percent. None of the spayed females
developed UI. Lacking a noticeable occurrence of increased joint
disorders or cancers in neutered males or females, those wishing
to neuter should decide on the appropriate age.
Doberman Pinscher
The study population was 109 intact males, 91 neutered males, 53
intact females, and 108 spayed females, for a sample size of 358
cases. The percentage of intact males with at least one joint disorder
was 2 percent and 0 percent for intact females. There was no evident
increase in this measure with neutering males. For females, spaying
within 11 months resulted in an increase in joint disorders of 11
percent, which did not reach significance. The occurrence of one
or more of the cancers followed for both intact males and intact
females was 2 percent. In neutered males at the 1 year and 2–8
year periods, there was a non-significant increase in occurrence
of cancers to 6 percent and 13 percent, respectively. For females,
there was no noteworthy increase in cancers with spaying at any
time. The occurrence of MC in females left intact was 2 percent
and 4 percent for those spayed at 2–8 years. There was a 7
percent occurrence of PYO in intact females. UI was a significant
risk in females spayed at any age up to 2 years, ranging from 25
percent in the females spayed at <6 mo. (p <0.01) to 19 percent
for those spayed between 1 and 2 years (p <0.05). The suggested
guideline, based on fragmentary results, for males is to leave the
male intact or neuter before 1 year of age to avoid the possible
increased risk of cancers seen in those neutered beyond a year of
age. For females, the suggested guideline, also based on limited
data, given the risk of UI in early spayed females, and the possible
increased risk of a joint disorder, is to consider delaying spaying
until beyond 2 years of age.
English Springer Spaniel
The study population was 52 intact males, 57 neutered males, 37
intact females, and 66 spayed females for a total sample of 212
cases. In males and females left intact, the occurrence of one or
more joint disorders was 5 and 8 percent, respectively. Among males
and females neutered at various ages, there were no noteworthy increases
in joint disorders. The cancers followed occurred in the intact
males and females at a 6 percent level, and neutering at any age
was not associated with any evident increase in this measure in
either sex. In intact females, MC was diagnosed in 6 percent, and
for those spayed at 2–8 years, 15 percent. PYO was not reported
in any of the intact females. Spaying females at 6–11 mo.
was associated with a 13 percent occurrence of UI, which may have
reached significance with a larger sample size. Lacking a noticeable
occurrence of increased joint disorders or cancers in neutered males,
those wishing to neuter should decide on the appropriate age. For
females, given the increased risk of UI in those spayed before 1
year, the suggested guideline is to delay spaying until a year of
age.
German Shepherd Dog
The study population was 514 intact males, 272 neutered males, 173
intact females, and 298 spayed females for a total of 1,257 cases.
In males and females left intact, the occurrence of one or more
joint disorders was 6 and 5 percent, respectively. Neutering males
at <6 mo., 6–11 mo. and 1–2 years was associated
with increased risks of this measure to 19, 18 and 9 percent, respectively
(p <0.01). Spaying females at <6 mo. and 6–11 mo. was
associated with a 20 and 15 percent level of increased risk (p <0.01),
and spaying at 1–2 years with a 5 percent risk level (p <0.05).
The occurrence of one or more of the cancers followed for intact
males and females was 3 percent and 2 percent, respectively. Neutering
at the various ages was not associated with any appreciable increased
risk in cancers followed. The occurrence of MC in intact females
was 5 percent and for those spayed at 2–8 years, 6 percent.
Of intact females, 3 percent were reported with PYO. UI ranged up
to 9 percent for females spayed from <6 mo. through 1 year of
age (p <0.05–0.01). The suggested guideline for males,
given the risks of joint disorders, is delaying neutering until
over 2 years of age. For females, with the same joint issues as
males plus the risks of UI, the suggested guideline is delaying
spaying until over 2 years of age.
Golden Retriever
The study population was 318 intact males, 365 neutered males, 190
intact females, and 374 spayed females for a total of 1,247 cases.
In intact males and females, the level of occurrence of one or more
joint disorders was 5 percent and 4 percent, respectively. Neutering
males at <6 mo. and at 6–11 mo. was associated with risks
of 25 percent and 11 percent, respectively (p <0.01). In females,
spaying at <6 mo. and at 6–11 mo. was associated with risks
of 18 percent and 11 percent (p <0.01, when combined). The occurrence
of one or more of the cancers followed in intact males was a high
15 percent and for intact females 5 percent. Neutering males at
<6 mo. and at 6–11 mo. was associated with increased risks
of cancers to 19 and 16 percent, respectively (p <0.01). Spaying
females at <6 mo. and at 6–11 mo., was associated with
increases in cancers to 11 and 17 percent, respectively (p <0.05,
when combined) and spaying at 1 year and at 2–8 years was
associated with increased risks of 14 percent (p <0.01, when
combined). The occurrence of MC in intact females was 1 percent
and for those spayed at 2–8 years, 4 percent. For females
left intact, 4 percent were reported with PYO. No cases of UI were
reported in females spayed at any age. The suggested guideline for
males, based on the increased risks of joint disorders and cancers,
is delaying neutering until beyond a year of age. The suggested
guideline for females, based on the increased occurrence of cancers
at all spaying ages, is leaving the female intact or spaying at
one year and remaining vigilant for the cancers.
Great Dane
The study population was 90 intact males, 103 neutered males, 69
intact females, and 91 spayed females for a total sample of 353
cases. This is a giant breed where one might expect a high risk
of joint disorders. However, both intact males and females have
low levels of joint disorders, just 1 and 2 percent, respectively.
For both males and females, there was no evident increase in this
measure with neutering. The occurrence of one or more of the cancers
followed in intact males was 6 percent and for intact females, 3
percent. There was no evident increase in this measure of cancers
with neutering in either sex. In intact females, MC was diagnosed
in just 2 percent and PYO in 6 percent. In early-spayed females,
no UI was reported. Lacking a noticeable occurrence of increased
joint disorders or cancers in neutered males or females, those wishing
to neuter should decide on the appropriate age. However, given the
large body size, and physiology of late musculoskeletal development,
neutering well-beyond year 1 should be considered.
Irish Wolfhound
The study population was 30 intact males, 19 neutered males, 21
intact females, and 16 spayed females for a total of 86 cases. Even
with the small number of cases, this breed was chosen for analyses
because of the large body size: challenging the Great Dane for height,
and where one might expect an increased risk of joint disorders.
In this sample, 7 percent of intact males and none of the intact
females had a joint disorder. No joint disorders were seen in neutered
males or females. With the intact males and females, the incidences
of one or more cancers were 8 percent and 21 percent, respectively.
With neutering males at 1 year, there was an increase in cancer
occurrence to 25 percent (p <0.05). There was no evident increase
in cancers in neutered females above the relatively high level in
intact females. There was no occurrence of MC in intact females
or those spayed late. For females left intact, 5 percent were reported
with PYO. UI was not reported in any of the spayed or intact females.
The suggested guidelines for males given the increased occurrence
of cancers around at ages 1–2 years, is neutering beyond 2
years. Lacking a noticeable occurrence of increased joint disorders
or cancers in neutered females, those wishing to neuter should decide
on the appropriate age. However, given the large body size, and
physiology of late musculoskeletal development, some may want to
consider neutering females well-beyond year 1.
Jack Russell Terrier
The study population was 92 intact males, 87 neutered males, 84
intact females, and 113 spayed females for a total sample of 376
cases. As in other small dogs, joint disorders were rare; none of
the intact males, and just 2 percent of intact females had one or
more joint disorders. Neutering was not associated with any increase
in this measure in either sex. In intact males, 3 percent, and in
intact females none, had one or more of the cancers followed. There
was no evident increase in cancer occurrence in either sex with
neutering at any age. In females left intact, MC was seen in 1 percent,
as was PYO. In those spayed at 2–8 years, MC was diagnosed
in 3 percent. UI was not diagnosed in any females. Lacking a noticeable
occurrence of increased joint disorders or cancers in neutered males
or females, those wishing to neuter should decide on the appropriate
age.
Labrador Retriever
The study population was 714 intact males, 381 neutered males, 400
intact females, and 438 spayed females for a total of 1,933 cases.
One or more joint disorders were reported in 6 percent of both intact
males and intact females. This measure was significantly increased
to 13 percent for males neutered before 6 mo. (p <0.01). In females
spayed at <6 mo. and 6–11 mo., the risk of a joint disorder
was 11–12 percent for each period (p <0.01, spay periods
combined). The occurrence of cancers followed was 8 percent and
6 percent, respectively, for intact males and females. Neutering
at the various ages was not associated with any evident increased
risk in the cancers. The occurrence of MC in intact females was
1 percent and for those spayed at 2–8 years, 2 percent. For
females left intact, 2 percent were reported with PYO. UI was reported
at a low rate (2–3%) in females spayed at various ages though
1 year. Given the significant occurrence of joint disorders in males
neutered at <6 mo., the suggested guideline for males is neutering
beyond 6 months. For females, given the increased risks of joint
disorders with spaying through 11 months of age, the suggested guideline
is delaying spaying until beyond a year of age.
Maltese
The study population was 49 intact males, 72 neutered males, 65
intact females, and 86 spayed females for a total sample of 272
cases. As mentioned in Appendix 1, the Maltese and Chihuahua vie
for the smallest breeds and the Great Dane and Irish Wolfhound for
the largest, but all four breeds share a low predisposition to joint
disorders. For the Maltese in both sexes, there was no occurrence
of joint disorders in either those left intact or neutered. Virtually
the same picture emerges with cancers, with only one of 64 intact
females being diagnosed with a cancer. There was no occurrence of
MC in the intact females and only one case among the 19 females
spayed at 2–8 years. PYO was seen in none of the intact females.
UI did not occur in any of the females.
Lacking a noticeable occurrence of increased joint disorders or
cancers in neutered males or females, those wishing to neuter should
decide on the appropriate age.
Miniature Schnauzer
The study population for this small-dog breed was 47 intact males,
63 neutered males, 25 intact females and 96 spayed females for a
total sample of 231 cases. There was virtually no occurrence of
any joint disorders in males or females either left intact or neutered.
The incidence of cancers in intact males was 4 percent and in females,
zero percent. There was no indication of cancer increase related
to neutering in either sex. There was no occurrence of MC in any
of the females left intact or spayed, and a 4 percent occurrence
of PYO in intact females. None of the females was diagnosed with
UI. Lacking a noticeable occurrence of increased joint disorders
or cancers in neutered males or females, those wishing to neuter
should decide on the appropriate age.
Pomeranian
The study population was 84 intact males, 69 neutered males, 65
intact females, and 104 spayed females for a total sample of 322
cases. As with other dogs of small body size, both males and females
had no occurrences of joint disorders in either those left intact
or neutered. With regard to cancers, for both males and females
left intact, the occurrence of cancers was zero, and there was no
indication of increased cancer risk related to neutering in either
sex. There was just one case of MC in females left intact, and 7
percent with PYO. None of the females was diagnosed with UI. Lacking
a noticeable occurrence of increased joint disorders or cancers
in neutered males or females, those wishing to neuter should decide
on the appropriate age.
Poodle, Toy
The study population was 49 intact males, 53 neutered males, 58
intact females, and 78 spayed females for a total sample of 238
cases. While the AKC registers all the Poodle varieties as the same
breed, the three main varieties are dealt with separately here because
of differences in size. In intact males, 4 percent had one or more
joint disorders and in intact females there was no occurrence of
a joint disorder. In neutered males and females, there was no evident
increased risk of a joint disorder. There was a 2 percent occurrence
of cancers in intact males and none in intact females. In neutered
males and females, there was no noteworthy occurrence of cancers.
In intact females, there was only a single case of MC and no case
of PYO in intact females and no occurrence of UI in spayed females.
Lacking a noticeable occurrence of increased joint disorders or
cancers in neutered males or females, those wishing to neuter should
decide on the appropriate age.
Poodle, Miniature
The study population was 41 intact males, 60 neutered males, 30
intact females, and 69 spayed females for a total sample of 199
cases. The AKC registers the Toy, Miniature, and Standard Poodle
varieties, all as the same breed. However, because of differences
in size, the varieties of Poodles are dealt with separately here.
There was no occurrence of a joint disorder in intact males or females.
However, in males neutered at 6-11 mo., there was a significant
9 percent occurrence of joint disorders (p <0.01), reflecting
CCL. In spayed females, there was no occurrence of a joint disorder.
In intact males and females, there was a 5 and zero percent occurrence
of cancers, respectively. There was no indication of increased cancer
occurrence related to neutering in either sex. The only occurrence
of MC in females was one female that had been spayed at 2–8
years. Of intact females, 6 percent developed PYO. Just one female
spayed at <6 mo. developed UI. The suggested guideline for males,
based on the significant occurrence of a joint disorder with neutering
at 6-11 mo., is delaying neutering until a year of age. Lacking
a noticeable occurrence of increased joint disorders or cancers
in neutered females, those wishing to neuter should decide on the
appropriate age.
Poodle, Standard
The study population was 47 intact males, 88 neutered males, 53
intact females, and 87 spayed females for a total sample of 275
cases. The AKC registers the Toy and Miniature, along with the Standard
Poodle, as all being Poodles. However, because of differences in
size, the varieties of Poodles are dealt with separately here. There
was a 2 percent occurrence of joint disorders in both intact males
and females. In males neutered at <6 mo., there was a non-significant
increase to 8 percent, and in spayed females, there was no occurrence
of joint disorders. The occurrences of cancers in intact males and
females were 4 and 2 percent, respectively. In males neutered at
1 year of age, the occurrence of one or more cancers rose to a significant
27 percent (p <0.01), all due to the increased risk of LSA. In
females, there was no significant increase in cancers with spaying.
There was a 4 percent occurrence of MC, and a 2 percent occurrence
of PYO in the females left intact. Just one female spayed beyond
2 years later developed UI. The suggested guideline for males, based
on the occurrence of one or more cancers with neutering at 1 year,
is to delay neutering until 2 years of age. Lacking a noticeable
occurrence of increased joint disorders or cancers in neutered females,
those wishing to neuter should decide on the appropriate age.
Pug
The study population was 96 intact males, 106 neutered males, 63
intact females, and 118 spayed females for a total sample of 383
cases. In intact males and females, the occurrences of joint disorders
were zero and 2 percent, respectively. In neutered males and females,
there was no evident increased occurrence of joint disorders. The
level of occurrence of one or more cancers in intact males was 6
percent and in intact females, 8 percent. Neutering males and females
did not lead to any evident increase in risk of a cancer. There
were no cases of MC in females left intact or spayed at any time,
and there was a 5 percent occurrence of PYO in the intact females.
None of the females was diagnosed with UI. Lacking a noticeable
occurrence of increased joint disorders or cancers in neutered males
or females, those wishing to neuter should decide on the appropriate
age.
Rottweiler
The study population was 315 intact males, 152 neutered males, 143
intact females, and 239 spayed females for a total sample of 854
cases. Joint disorders are a major concern in this breed with 8
percent of intact males and 16 percent of intact females having
one or more joint disorders. In males, neutering at <6 mo. and
at 6-11 mo. resulted in 10 percent and 22 percent occurrences (combined
p <0.05). In females, spaying at <6 mo. resulted in a significant
43 percent occurrence (p <0.05), the main joint disorder being
CCL. The cancers followed occurred in the intact males and females
at 16 and 11 percent, respectively. These relatively high occurrences
of cancers in intact males and females were not increased by neutering
at any age. Of females left intact or spayed at 2–8 years,
8 and 5 percent were diagnosed with MC, respectively. In intact
females, 12 percent were diagnosed with PYO. With regard to UI,
1 percent of intact females had UI, and in females spayed at <6
mo. and 6-11 mo., 4 and 6 percent, respectively had UI. The suggested
guideline for males, given the risk of joint disorders for those
neutered at 6-11 mo. or earlier, is neutering beyond a year of age.
For females, given the increased risk of joint disorders with neutering
at <6 mo., the suggested guideline is spaying beyond 6 months.
Saint Bernard
The study population was 26 intact males, 27 neutered males, 18
intact females, and 23 spayed females for a total sample of 94 cases.
This breed was chosen because of the large size. In intact males
and females, the occurrences of one or more joint disorders were
8 percent and 6 percent, respectively. While there was no evident
increase in joint disorders with neutering males, in females spayed
at <6 mo., joint disorders increased to a significant 100 percent
(p <0.01). The cancers followed occurred in intact males and
females at 4 and 11 percent, respectively. With neutering males
and females, there were no noteworthy increases in cancers. There
was no occurrence of MC in either the intact or spayed females.
In intact females, PYO was diagnosed in 15 percent There was no
occurrence of UI in spayed females. Lacking a noticeable occurrence
of increased joint disorders or cancers in neutered males those
wishing to neuter should decide on the appropriate age. The suggested
guideline for females given in the increased risk of joint disorders
with neutering at <6 mo., is neutering beyond 6 months. However,
given the large body size, some may wish to consider neutering well-beyond
1 year of age.
Shetland Sheepdog
The study population was 31 intact males, 30 neutered males, 20
intact females, and 52 spayed females for a total sample of 133
cases. There were no joint disorders in intact males and just one
in the intact females. In neutered males, the only joint disorder
was in one of the males neutered at <6 mo. and in females there
was no joint disorder associated with spaying. The occurrence of
cancers in intact males was 6 percent and in intact females, zero.
There were no evident increases in cancers in neutered males or
females. There was no occurrence of MC in intact or spayed females
and a 14 percent occurrence of PYO in intact females. Spaying at
6-11 mo. resulted in a 6 percent occurrence of UI, but at 1 year
a 33 percent occurrence. Lacking a noticeable occurrence of increased
joint disorders or cancers in neutered males, those wishing to neuter
should decide on the appropriate age. However, to avoid the high
level of UI occurrence in females, one could consider spaying females
at, or beyond, 2 years.
Shih Tzu
The study population was 104 intact males, 112 neutered males, 77
intact females, and 139 spayed females for a total sample of 432
cases. In this small-dog breed there were no occurrences of joint
disorders in either intact or neutered males and females, revealing
virtually no vulnerability in this regard. There was no occurrence
of the cancers followed in intact males and females. In neutered
males there was no occurrence of cancers. However, in females, the
occurrence of cancers for those spayed at 6-11 mo. was 7 percent
and at 1 year this measure reached a significant 18 percent (p <0.01).
MC occurred in 3 percent of intact females. PYO occurred in 5 percent
of intact females. UI was not reported in any females. Lacking a
noticeable occurrence of increased joint disorders or cancers in
neutered males, those wishing to neuter should decide on the appropriate
age. The picture is very different for spaying females where the
increased risk of cancers started with spaying at 6-11 mo., reaching
18 percent with spaying at year 1. The suggested guideline for females
is to delay spaying until the female is 2 years of age. Another
possibility is to spay a female a month or two before 6 months to
avoid the increased risk of cancers.
West Highland White Terrier
The study population was 35 intact males, 33 neutered males, 28
intact females, and 46 spayed females for a total sample of 142
cases. Just one intact male had a joint disorder, and other than
this, no joint disorders were reported in intact females or in neutered
males or females. None of the intact males or females had any of
the cancers followed. There were no noteworthy occurrences of the
cancers in neutered males or females. There were no occurrences
of MC in either intact or neutered females, and a 7 percent occurrence
of PYO in intact females. The occurrence of UI was 14 percent for
females spayed at <6 mo. and 6 percent at 6-11 mo. Lacking a
noticeable occurrence of increased joint disorders or cancers in
neutered males or females, those wishing to neuter should decide
on the appropriate age. However, for females, one could consider
delaying spaying until a year of age to avoid the risk of UI.
Yorkshire Terrier
The study population was 134 intact males, 178 neutered males, 144
intact females, and 229 spayed females for a total sample of 685
cases. There were no joint disorders reported in intact males, and
in intact females, just 1 percent. In neutered males and females
there were no noteworthy occurrences of joint disorders. In intact
males and intact females, just 1 percent were reported with at least
one of the cancers followed. In both neutered males and females,
none of the cancer occurrences was noteworthy. In intact females,
the occurrence of MC was 1 percent as was the occurrence with spaying
at 2–8 years. PYO was reported in 7 percent of intact females.
No UI was reported in any of the intact or spayed females. Lacking
a noticeable occurrence of increased joint disorders or cancers
in neutered males or females, those wishing to neuter should decide
on the appropriate age.
Discussion
Since the reporting from this center of increased risks of joint
disorders and some cancers in Golden Retrievers, Labrador Retrievers,
and German Shepherd Dogs (11–13), the appropriate age of neutering
has become a common point of discussion (16–18). With the
evidence-based information on the risks, if any, of joint disorders,
cancers, PYO and UI associated with neutering at different ages
for males and females of various as dog breeds, dog owners, and
their veterinarians, can use this information to select an age for
neutering for the long-term health of their companion dogs on a
case-by-case basis.
The overall major finding from the present study is that there
are breed differences – and sometimes sex differences –
with regard to the increased risks of joint disorders and cancers
associated with neutering at various ages. For example, with the
Boston Terrier, neutering females at the standard 6 month age did
not increase the risks of joint disorders or cancers over that of
dogs left intact, but with males, neutering before a year of age
was associated with a significant increase in cancers. The opposite
effect with genders was seen in the Cocker Spaniel where neutering
at 6 months was not associated with an increase in joint disorders
or cancers in males, but in females there was a significant increase
in risk of cancers to 17 percent with neutering before 2 years.
Another important finding that holds across several breeds is
that with the small-dog breeds – Cavalier King Charles Spaniel,
Chihuahua, Corgi, Dachshund, Maltese, Pomeranian, Poodle-Toy, Pug,
Shih Tzu, Yorkshire Terrier –the occurrences of joint disorders
were close to zero in both the intact and neutered males and females.
In these small-dog breeds, the occurrence of cancers was low in
both those kept intact and neutered. Two exceptions were the Boston
Terrier and Shih Tzu where there was there a significant increase
in cancers with neutering.
As noted in the results section, the mean date of last entry per
patient in the hospital record ranged from about 4.5 to 5.5 years,
which means the data especially represent rather early-occurring
joint disorders and cancers. 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 their dogs. To just delay neutering by a year or so to
lower the risk of a joint disorder or cancer in those breeds where
the issue is relevant, is a noteworthy goal, making it worthwhile
to discuss appropriate ages to neuter with caregivers who have a
new puppy.
A suggested guideline for the use of the data presented here for
those who may wish to focus on a breed or two, is to first scroll
through Table 1 to peruse the breeds for a brief look at the neutering
guidelines for the breeds of interest. The next step could be to
refer to summary paragraphs in the Results section, which present
the major findings with a suggested guideline for neutering age.
Then for a third step, one could turn to Appendix 1 for detailed
joint disorder and cancer tabular data as well as data on MC, PYO,
and UI. Our intention is to offer readers data-based information
to make case-by-case decisions about age of neutering. As is clearly
evident in the breed-specific data presented, one cannot make a
generalization for all dogs about age of neutering guidelines.
As mentioned, this study involved 35 breeds, counting the three
varieties of Poodles as three breeds. Thus, most breeds registered
by AKC or other comparable agencies were not covered. The breeds
chosen were the most popular, and with the largest dataset in our
records, or were included to sample the largest range of breed sizes
as was feasible. Hence, some of the largest breeds (e.g., Great
Dane, Irish Wolfhound) and smallest breeds (Miniature Schnauzer,
West Highland White Terrier) were included despite lower numbers
of patient records. While with some of the most popular breeds there
were over 1,000 cases in the database, most breeds ended up with
200 to 500 cases which was sufficient for statistical analyses where
the impact of neutering was substantial.
A suggestion for those interested in a breed not covered in this
study is to find a breed or two closest genetically to the breed
of their interest in order to get an estimate of the various disease
risks, if any, associated with neutering. However, one needs to
bear in mind that even genetically related breeds may vary a great
deal. An example is seen when comparing Golden and Labrador Retrievers,
using the data from this study, where in the Labrador, there was
no increase in cancer risk above that of intact dogs with neutering,
but in the female Golden, the risk of a cancer with neutering increased
to 2–4 times that of the 5 percent level of intact females.
The popular Poodle breed provides another example, where there are
three major varieties in size, the Standard, Miniature, and Toy.
In the Standard, neutering males at 1 year was associated with a
highly significant increase in the risk of a cancer (mainly LSA)
to over six times that of intact males, whereas in the Miniature,
there was no increase in cancers with neutering but a significant
increase in joint disorders (mainly CCL) with neutering at 6-11
mo.
A likely mechanism by which early neutering may lead to a joint
disorder is related to disturbance of the closure of the long-bone
growth plates by gonadal hormone secretion as the animal approaches
maturity (19, 20). We have proposed that neutering much before the
closure of growth plates allows the long bones to grow a little
longer than normal, and may sufficiently disturb joint alignments
in some neutered dogs to lead to a clinically-apparent joint disorder.
Given the frequency with which early neutering is performed in
dogs, it seems surprising that osteoporosis has not been examined
given that in humans, chronic loss of gonadal hormones is associated
with osteoporosis (21). It could be that the wolf ancestor of the
dog had one breeding season and that the bone structure of mature
dogs was not as affected by seasonal fluctuations of gonadal hormones
as with a permanent gonadal hormonal loss in humans.
One of the frequently mentioned advantages of early neutering
of female dogs is protection against MC (22). There may be important
genetic, breed-line differences in the occurrence of MC that are
not portrayed in our database. However, relevant to the discussion
of MC is the recent meta-analysis of published studies on neutering
females and MC, finding that the evidence linking neutering to a
reduced risk of MC is weak (23). In the data gathered in this study,
through 11 years of age, the occurrence of MC in females left intact
was rarely above 6 percent and frequently 2 percent or less. For
those neutered at <6 months, there was, as expected, no occurrence
of MC. Obviously with most cases of intact females not followed
through 11 years, and with the 12-year cut-off for those that were
followed, many occurrences of MC were missed. However, it seems
reasonable, that if MC was a common occurrence in intact females
that this disease would have been more frequent in the intact females
followed. Further, a very late onset of MC would seem less disturbing
to pet owners than the much earlier onsets of joint diseases and
other cancers.
For males, there is some concern that neutering beyond puberty
will increase the likelihood of a problem behavior such as aggression.
However, studies show that while neutering males can reduce aggression
to people or other dogs in about 25 percent of males, neutering
prior to puberty is no more effective in preventing this problem
than is neutering in adulthood in resolving the problem (24, 25).
This paper deals primarily with the risks of diseases that are
seen within a given breed and sex. Comparisons between breeds are
difficult to interpret, in part because of differences in developmental
and physiological factors between breeds including those between
smaller and larger breeds. In the text we have reported the occurrences
of various diseases in percentages but in statistical analyses the
actual data are used. When disease incidence is particularly low
in one or more neutering subgroups, the ability to detect significant
differences will be low, but there still could be differences which
may or may not have been evident in the statistical analyses.
There are at least two major limitations to this study. First,
relatively few breeds are covered compared to those included in
the various breed registries of kennel clubs and canine organizations.
This limitation was necessary so as to apply the same diagnostic
criteria for diseases covered across all breeds, using the same
database, and the necessity of having sufficient cases for analyses.
Second, no information is available as to the reasons the owners
or others chose to neuter, or not to neuter their dogs. In California,
the vast majority of dogs are neutered, and since 2005 it is legally
required for dogs to be neutered prior to adoption from an animal
shelter or humane society (26); many breeders impose the same requirement.
In conclusion, the data presented should provide to veterinarians
and interested puppy caregivers data-based information for the best
age for neutering to avoid increasing the risk of joint disorders
and some cancers beyond that of leaving the dog intact. Readers
can note that an elevated risk for a joint disorder or cancer occurs
in relatively few of these breeds. In other words, with most breeds
or sexes, neutering can apparently be done without referral to a
particular age, at least with regard to the joint disorders or cancers
covered in this study. Of course, individual factors must be taken
into account. For puppies of mixed breed, another paper that is
currently in press provides data-based information dealing with
age of neutering and the risk of one or more joint disorders as
a function of the dog adult weight category (27). This information
can also help inform decisions on age of recommended neuter in purebred
dogs where the breed is not covered in our data.
Data Availability Statement
The datasets presented in this study can be found in online repositories.
The names of the repository/repositories and accession number(s)
can be found below: (Figshare, doi: 10.6084/m9.figshare.7231010).
Author Contributions
BH, LH, and AT: conceived and designed study, collected and complied,
and analyzed data. NW: statistical analyses. BH, LH, AT, and NW:
drafted and edited manuscript. All authors contributed to the article
and approved the submitted version.
Funding
Supported by the Canine Health Foundation (#01488-A), the Center
for Companion Animal Health, University of California, Davis (#
2009-54-F/M), and Versatility in Poodles.
Conflict of Interest
The authors declare that the research was conducted in the absence
of any commercial or financial relationships that could be construed
as a potential conflict of interest.
Acknowledgments
We wish to acknowledge the assistance of the following individuals
in collecting the data: Siobhan Aamoth, Cristina Bustamante, Valerie
Caceres, Rhoda Coscetti, Madeline Courville, Elvira Covarrubias,
Aaron Frankel, Matthis Grupe, Vanessa Hsieh, Mi Hwangbo, Katrina
Larkin, Arielle Merlos, Emily Parker, Roger Pender, Venus Pun, Emily
Romanko, Sara Sewell, Sandra Walther, and Lexy Wetzel.
Supplementary Material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fvets.2020.00388/full#supplementary-material |
