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Should I spay or should I no..?  -- pros and cons of Spay-neuter

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  Should I spay or should I no..? - the pros and cons of neutering

This is a work in progress.  Some of you may have seen earlier versions that I’ve posted to email lists… 

Neutering terms and attitudes

     Advantages of spay or neuter

     Disadvantages of spay or neuter

Surgical complications

Testicular cancer

Prostatic cancer and prostatic problems

Female reproductive tract cancer and infection

Mammary cancer

Bladder cancer

Bone cancer, bones and ligaments

Perianal tumours

Other tumours

Incontinence

Diseases with possible immune-mediated mechanisms

Vaccination

Obesity

Longevity

Behaviour

Cognitive impairment

Other conditions

Early-age neutering

     Surgical complications

     Gender characteristics

     Longevity, cancer and obesity

     Bones and ligaments

     Incontinence

     Peri-vulvar dermatitis/vaginitis

     Cystitis

     Behaviour

     Other conditions

Neutering terms and attitudes:  Note:  Neuter applies to either sex.
Neutering of dogs has been performed for a number of years, and in some countries is a widely accepted practice.  The Guide Dogs for the Blind neuter dogs not earmarked for breeding, and many of us share our homes with neutered pets.  Neutering of pet dogs is often recommended using vague terms such as it ‘improves pet health and behaviour’ [1, 2], though this is not universally correct (eg [3-8]).  There is often scant mention of possible benefits outside that of reducing pet numbers, nor discussion of possible downsides.  Some disadvantages are minor, some may be of larger importance.  The following may be seen as “politically incorrect” in that it is not a wholesale endorsement of neutering.  This is because like most things in biology, I find the pros and cons of neutering are neither black nor white.  In some ways, our veterinarians may be caught in between – veterinarians are often presented with cases of pyometra or behavioural problems – which neutering would have in the case of pyometra, and may have in the case of behavioural issues prevented (would also prevent nasty tempered dogs being used in breeding).  So promoting neutering may actually reduce the potential cases they would see – even though some people see promotion of neutering as a money-making ploy by the veterinary profession.

Generally, the terms used are spayed, neutered, castrated, gonadectomised or desexed.  Neutering, castration, desexing and gonadectomy can apply to either sex.  Spay is reserved for females, which have an ovariohysterectomy (ovaries and uterus are removed), or ovariectomy (ovaries are removed).  In males, permanent sterilisation is most commonly achieved through removal of testes (sometimes called orchiectomy or orchidectomy).  There was a product on the market in the USA that is injected into testes to achieve permanent sterilization, but I believe it may now be difficult to obtain.  In Australia and some other countries there is also a product available for reversible suppression of reproductive function of male dogs (yes, dogs have been used to sire litters after the effect of the product has ‘worn off’).  It is available as an implant like a microchip and renders a dog infertile for at least 6 months, with newer implants effective for longer periods in the pipeline [9]. 

Early age neutering has largely come about through efforts to reduce unwanted pet numbers in the USA, mainly because a proportion of young animals rehomed through shelters never presented to be neutered, despite having been provided with vouchers for the procedure to be performed.  Sometimes early age neutering is called prepubertal or prepuberal neutering.  The terms prepubertal/prepuberal may be confusing, as although they mean sterilization of sexually immature animals (before the first oestrus, or before spermatozoa are present in an ejaculate), this can be at different physiologic ages in different breeds of dog.  Age at puberty may vary from anywhere from 6 months in smaller breeds to up to 24 months of age in larger breed dogs.  Husbandry (nutrition, kenneling) may also alter this timeframe [10].  Root Kustritz [11] defines early neutering or prepuberal gonadectomy as occurring in pups up to 14 weeks of age.  Others use ‘early age’ to refer to neutering performed earlier than the more traditional age of around 6 months (eg [12-14]).  (The reported benefits/risks of early age neutering a presented separately, below.)

Not all countries have similar rates of, or attitudes towards, neutering.  Thus, discussions as to the pros and cons of neutering, especially in young animals, are largely confined to the USA where general policy is that dogs are neutered before leaving animal shelters.  This is supported by the assertion that “dogs and cats benefit from gonadectomy performed at any age” [11].  In general, neutering of dogs is less common in Europe than in North America.  Neutering unless for medical reasons was prohibited in Sweden until 1988.  In one study of Swedish dogs born 1993-1995, only1-3% had been neutered [15].  Until fairly recently spaying except on medical grounds was also prohibited in Norway [16].  Thus data comparing health of intact versus neutered animals is not necessarily available everywhere even when studies have been undertaken.

Some people’s decisions to spay/neuter, or at what age to neuter may be different depending upon their breed and its predispositions (also note that some studies are unable to provide breed related information as there were insufficient dogs of a breed available in the study in order to make sound statistical analyses from which to draw meaningful information).

Yes neutering will 100% guarantee your male will not get testicular cancer, nor your bitch uterine cancer or ovarian cancer, because these are the bits which are removed – if they’re not there, they can’t develop cancer.  And nor can infections of these organs occur (when a complete ovariohysterectomy is performed), nor can your dog or bitch sire or whelp a litter.  And there are not many 100% guarantees in biology!  On a population level general statements can be made regarding any health benefit/risk, but on an individual basis (ie, *your* dog), there are generally no guarantees.

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Some people have asked for a quick summary of the pros and cons of neutering, and this is below.  Further explanations are below the summary.

Advantages of spay or neuter

•  Eliminates risk of testicular cancer (most are benign in behaviour)
•  Reduces risk of mammary cancer (if performed before 2.5 years of age)
•  Reduces risk of pyometra (uterine infection)
•  Eliminates risk of uterine tumours (given uterus is removed) 
•  Eliminates risk of ovarian cancer
•  Reduces risk of prostatic hyperplasia and inflammation 
•  Reduces risk of benign perianal tumours in dogs
•  Reduces urine marking, mounting.  May reduce roaming

Disadvantages of spay or neuter

•  Decreased life span
•  Increases risk of urinary incontinence (in both bitches and dogs)
•  Increases risk of obesity
•  Increases risk of osteosarcoma (bone cancer)
•  Increases risk of prostatic cancer
•  Increases risk of bladder cancer
•  Increases risk of cardiac haemangiosarcoma
•  Increases risk of splenic haemangiosarcoma in spayed bitches
•  Increases risk of cholangiocarcinoma (cancer of bile ducts) in spayed bitches
•  Increases risk of cranial cruciate ligament injury
•  Increases risk of patellar luxation in small- and medium-sized dogs
•  Increases risk of adverse vaccine reactions
•  Increases risk of myasthenia gravis in spayed bitches
•  Increases risk of pancreatitis in spayed bitches
•  Increases risk of aggression, fearfulness
•  Increases cognitive impairment in aged dogs already showing signs of disease
•  Increases risk of benign perianal tumours in spayed bitches
•  Increases risk of peri-vulvar dermatitis, vaginitis, cystitis and recurrent urinary tract infections in early-age spayed bitches

  

Surgical complications:  Neutering of dogs and bitches is a surgical procedure.  All surgery carries risk, but the risk of major complications following neuter surgery is low – which is probably self-explanatory given how often the procedure is performed.  Complications were reported to occur more frequently in dogs older than 1 year of age than those neutered at a younger age [17].  Overall complication rates are approximately 20% [17, 18], with major complications occurring in up to 4% of cases [17, 19], and death in less than 0.1% of cases [17].

Testicular cancer:  Testicular cancers with malignant (nasty) behaviour in dogs are uncommon.  Many older dogs have tumours in their testes, and these go largely undetected [20].  Testes that are cryptorchid (don’t descend) have something like 13.6 times increased risk of developing a cancer, and it is recommended these be removed [21].

Prostatic cancer and prostatic problems:  Neutering will prevent the vast majority of prostatic problems that arise in dogs (infections and symptoms associated with hyperplasia (a benign enlargement)), but, contrary to some reported benefits of neutering eg [1], it may increase the risk of development of prostatic cancer by up to 4.3 times that of an intact dog [22, 23,119].  An older study reported that a higher prevalence of prostatic cancer was not found in neutered dogs compared with intact dogs “than could be explained by the number of neutered males in the population” [24].  The conflicting information aside, canine prostatic carcinoma is an uncommon neoplasm.  How uncommon/common is difficult to determine, with reports ranging from no cases diagnosed in one ten year Japanese study [25] to an incidence of less than 1% of cases [26, 27].  That said, of 17 cases of cancer of the prostate I saw in a 5 year period, only 5 had gone to necropsy (or post mortem, as we tend to call it here).  Some of these 17 cases were only diagnosed post mortem.  Only ~ 40% of dogs which had been diagnosed with prostatic tumours had a biopsy or necropsy confirm the condition (diagnosis was made on prostatic wash or massage).  So, there is “more of it about” than the rates of 0-<1% in necropsy studies would indicate.  Generally, prostate cancer is described as a disease dogs aged around 10.  One paper included two Vizslas in its study population of 35 dogs with prostatic cancer (dogs attended U Penn 1997 - 2001) [23].  This is the only paper that I have seen that has included Vizslas in its study group.

Dogs that are neutered do not develop benign prostatic hyperplasia (BPH).  BPH is a hormone-dependent disorder, relying on testosterone.  The testes produce around 95% of the testosterone in the male dog.  So without the testes, the prostate doesn’t develop hyperplasia.  BPH occurs so frequently in aged dogs that it might be considered an age-related physiologic process – BPH occurs in 50-100% of dogs over the age of 5, though it is generally not a clinically significant problem, with only around 1.5% of dogs displaying clinical signs [22].

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Female reproductive tract cancer and infection:  Spaying a bitch will reduce the occurrence of uterine infection (pyometra) and prevent development of uterine cancer.  Uterine tumours are very uncommon (0.3-0.4% of all canine tumours), the majority of which are benign [21].  Pyometra can be life threatening.  Incidence and risk rates for pyometra are confounded by spay rates.  One text quotes pyometra as occurring in around 0.6% of bitches, increasing to 66% of bitches over 9.  Another study identified 9% of female admissions were for pyometra (reviewed by [28]).  In Sweden where approximately 7% of bitches are spayed, risk of pyometra differed with age, breed and where the dogs lived [29].  Where dogs live may influence the proportion of dogs receiving veterinary care.  Approximately 25% of insured Swedish dogs develop pyometra by age 10, with age-related differences observed between breeds.  Approximately 4% of cases resulted in death [30].  In a colony of Beagles, 15% of bitches over the age of 4 developed pyometra [31].  ‘Stump pyometra’ may occur in spayed bitches, thus spaying does not completely eliminate the risk of pyometra.

Ovarian tumours, which are also uncommon, (accounting up to 1.2% of tumours, of which approximately 17% are benign) and for which incidence or risk rates will be altered by spay rates, will also be prevented as long as the bitch also has her ovaries removed [21, 32]. 

Mammary cancer:  Mammary tumours in bitches are reported to be the most common growth to arise in bitches.  Incidence increases with age.  Only about half of these are malignant growths.  And of these, around half of the malignancies are likely to recur or spread to other organs.  It is generally reported that the risk of mammary tumours occurring is related to spaying, and to the age of the bitch when the spay procedure is performed.  The risk of developing mammary cancer is reported to be significantly reduced if bitches are spayed before 2.5 years of age [33].  Risks compared with risk in intact bitches (not all of whom develop mammary tumours) increase from 0.5%, to 8%, to 26%, depending upon whether a bitch is spayed before her first heat, second, or third season and thereafter, respectively [34].  In comparison, a UK study found no difference in the odds ratio for a diagnosis of mammary neoplasia from intact or spayed bitches, but age at spay was not known [35].  Interestingly, it has been reported that age at diagnosis for intact and spayed bitches were not significantly different [33] – which is not the expected behaviour of a tumour that is believed to be hormonally initiated.  The risk of mammary tumour in spayed dogs is also reduced in those that are thin when aged 9-12 months of age [33].

It is generally agreed that mammary lumps are like skin lumps – in that they are more easily detected (visualised/palpated) and likely to be excised than tumours occurring in internal organs, so this also skews the true incidence rates as a proportion of all tumours.

Under the umbrella term ‘mammary carcinoma’ there is more than one type of cancer.  They are all called ‘mammary carcinoma’, because that’s where they arise.  The different types can have different origins within the mammary tissue (different cell of origin), and varying biologic behaviour.  For example, although the least common type of carcinoma occurring in canine mammary tissue is a carcinosarcoma, it is the type most likely to spread and recur.  Not all the studies on mammary tumours in dogs use the same criteria to include cases for study.  For instance, the Schneider et al paper [34] above was based on adenocarcinomas and mixed mammary tumours.  Sonnenschein et al [33] excluded mixed mammary tumours and sarcomas from their study.  Note also, that in different countries exogenous hormones are often used more widely to control oestrous patterns in the bitch, and these may alter the risk of development of mammary lumps.

Increased risk for mammary tumours in one breed over another varies by study.  Several including Egenvall et al [36] have reported increased risk for English Springer spaniels.  Dobermans and Boxers were also identified as at increased risk.

It has also been reported that spaying a bitch within 2 years of removal of her mammary carcinoma increases survival compared with the survival of intact bitches and with the survival of bitches spayed more than 2 years prior to tumour removal [37].  The authors of this study wrote; “The risk reduction for developing mammary tumors by performing ovariohysterectomy after 2.5 years is minimal, and the positive effect of ovariohysterectomy is strongest when performed concurrent with tumour surgery.  Should we advise our clients that if they do not spay their dogs before the second oestrus, it is better to wait until they are much older or till they develop mammary gland tumors?” [37].  In contrast, another recent study did not find hormonal status or time of spay influenced survival for bitches with malignant mammary tumours [38].

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Bladder cancer:  The risk for development of transitional cell carcinoma of the bladder is 4 times greater for neutered animals than for intact animals.  Around 2% of cancers in dogs are bladder cancer, with some breeds at increased risk (eg Scottish terriers have a 19 times increased risk over mixed breed dogs).  An increased prevalence of bladder cancer has been seen at teaching hospitals in recent years [39].

Bone cancer, bones and ligaments:  In a study of 683 Rottweilers, a breed at risk for development of osteosarcoma (bone cancer), the “Risk for bone sarcoma was significantly influenced by age at gonadectomy.  Male and female dogs that underwent gonadectomy before 1 year of age had an approximate one in four lifetime risk for bone sarcoma and were significantly more likely to develop bone sarcoma than dogs that were sexually intact” [40].  When neutered before 1 year of age, dogs were 3.8 times, and bitches 3.1 times more likely to develop an osteosarcoma than an intact dog or bitch.  This risk was independent of size and weight of the adult dogs [40].  A separate study on various breeds reported that the risk of osteosarcoma doubles with neutering [4].

Neutering is associated with twice the increased risk of cranial cruciate ligament rupture (CCL) [41-43].  Age at spay was not associated with prevalence of ruptures, though age at spay was not known for many dogs [43].  Association between obesity following neutering and CCL was not able to be determined [43].  A later study on dogs less than 2 years of age found heavier dogs were more likely to have CCL [41].  Vizslas were not considered a breed at increased risk of CCL [43].

Neutering is associated with a 3-fold increase in risk of patellar luxation in small- and medium-sized dogs, though this may be related to age as the neutered dogs were older than intact dogs, and risk of patellar luxation also increases with age [44].

Boxer dogs that had been neutered at least 6 months before examination were 1.5 times more likely to have clinical hip dysplasia than intact Boxers (a 50% increase).  This clinical presentation was attributed to increased body weight post-neutering [45].

In the Airedale Club of America health survey, bitches and dogs with a musculoskeletal disorder were more likely to be neutered than intact, but it is not clear if these animals were neutered to remove them from a breeding programme, or whether neutering predisposed the dogs to the conditions [46].

Studies in male Beagles found a loss of bone volume (reduced bone formation compared with resorption) in neutered dogs [47].  Although these results suggest male dogs are a suitable model for osteoporosis, other studies have found bitches to be unsuitable for such studies due to lack of sustained bone loss [48, 49].

Perianal tumours:  Benign perianal gland tumours (perianal adenoma) are androgen sensitive (many regress when a dog is castrated), and thus, the majority, but not all, occur in intact males.  Reported as the most common epithelial skin tumour in dogs [50], the risk of perianal tumours is also increased in spayed females, and it is suggested oestrogen is protective against their development [51].  Goldschmidt and Shofer [50] saw thirteen cases of this benign tumour in Vizslas, and they reported a 1.8 times increased risk of this condition in the breed.

There are conflicting reports concerning perianal gland adenocarcinoma (which occurs far less frequently than benign perianal gland lesions, comprising approximately 1% of skin tumours [50]); some authors have noted no gender differences, whilst other studies found the majority occur in intact males [51, 52], or that when compared with intact bitches, neutered bitches are at increased risk [51]. 

Although anal sac adenocarcinoma (occur as approx 2% of skin tumours in dogs) is considered to arise independent of hormonal influence, the majority of affected dogs have been neutered [50, 52].  A recent study of 113 cases found no gender bias [53].

Other tumours:  Neutering increases the risk of splenic haemangiosarcomas in bitches (2 times risk in spayed over intact) [54], and cardiac haemangiosarcomas in dogs and in bitches (spayed females > 5 times greater relative risk than intact females; and “The risk for castrated males was slightly greater than that for intact males, which had 2.4 times the relative risk of intact females”) [55].  Spayed bitches have a 1.5 times increased risk of cholangiocarcinoma (bile duct cancer) than do intact bitches.  Cholangiocarcinoma is uncommon, comprising less than 1% of tumours seen in dogs [56].

A decrease in odds of tumours (benign and malignant) from the mouth/pharynx and reproductive systems was found for neutered dogs of both sexes, over intact dogs [35].  Part of this should not be surprising given the information concerning testicular tumours and mammary tumours.  The study however also found no difference in the odds ratio for a diagnosis of mammary neoplasia from intact or spayed bitches (age at spay was not known). 

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Incontinence:  Neutering increases the risk of urinary incontinence in both bitches and dogs [5, 57].  Spayed bitches are up to 7.8 times more likely to develop urinary incontinence [5].  Incontinence may affect up to 20% of bitches, with breed dispositions (especially large breeds) and geographical differences observed – one study reporting up to 65% of Boxer bitches developing post-spay incontinence, whilst only 10% of German Shepherd bitches were affected, whilst in the USA [58, 59] and Netherlands, Dobermanns are at increased risk [60].  Neutering also substantially increases the risk of incontinence in Airedales and Irish setter bitches [46, 61].

The condition is uncommon in dogs (one study reported 1/122 dogs neutered for behavioural reasons developed incontinence following neuter surgery [62]), but unlike in many bitches, responds poorly to treatment [57, 59].  When bitches are spayed the levels of gonadotropin hormones (follicle stimulating hormone and luteinising hormone) increase as the feedback loop for the hypothalamic-pituitary system is no longer present.  The levels of these hormones are now being thought to play a role in development of incontinence in spayed bitches, but the associations are not clearly understood as yet – gonadotropin levels in spayed incontinent bitches are significantly lower than levels in spayed continent bitches [58].

Diseases with possible immune-mediated mechanisms:  The effect of neutering and risk of hypothyroidism is unclear.  Neutering has been associated with a significant increase in risk of hypothyroidism [63, 64].  In Golden retrievers there appears to be an association between neutering and hypothyroidism [65].  In contrast, a study in the UK did not find neuter status a risk factor for hypothyroidism [66].  It has recently been reported that certain major histocompatibility complex (MHC) antigens may be associated with hypothyroidism in some breeds [67, 68], though how hormonal status may/ not influence this is not known.

It has been reported that neutering increases the risk diabetes in neutered males, though the findings have not been universal in all populations studied [69].  Spayed bitches are more likely to be diagnosed with pure red cell aplasia [70], and compared with other University hospital dogs, one study reported neutered dogs and bitches were over-represented in cases with immune-mediated haemolytic anaemia [71].  MHC antigens have also recently been reported to be associated with both diabetes and haemolytic anaemia [72, 73], and as with hypothyroidism, how hormones may influence the development of disease is not known.

Compared with intact, spayed bitches have been found to be at increased risk of developing myasthenia gravis [74].  This study included six affected Vizslas, and it was reported that compared with mixed breed dogs, Vizslas had a 3.3 times increased risk of myasthenia gravis.

Vaccination:  Following vaccination (excluding dogs that also received heartworm vaccination), neutered dogs and bitches were found to be at increased risk (27-38% compared with intact animals) of adverse reactions, none of which were life threatening.  This was attributed to alterations in immune function following neutering.  The risk was inversely related to the dog’s weight (smaller dogs/breeds more likely to have an adverse reaction than larger dogs), and the risk was greatest in dogs of 1-3 years of age compared with dogs of other ages [75].  Following rabies vaccination both intact and young animals were less likely to produce appropriate levels of antibodies for entry into the UK.  There were also differences in sero-conversion rates depending upon the breed of dog and what country the dog was from [76].

Increased incidence of parvoviral enteritis has been reported in shelter animals neutered before 24 weeks of age when compared with those neutered over the age of 24 weeks, though it was postulated that differences in rate of infection were attributable to different shelter practices [13].  Neutered males are less likely to contract parvovirus enteritis than intact dogs [77].  The authors attributed this to neutered dogs being less likely to roam, and thus come into contact with infectious agents.

Obesity:  Several studies have reported neutered dogs were significantly more likely to be overweight or obese than of normal weight, and the number of obese and overweight dogs increased as their age increased [78-80].  Obesity after neutering was found to be strongly influenced by breed [79, 80], and after adjusting for increasing weight with increased age, significantly more gundogs were obese or overweight after neutering compared with intact gundogs [79].  Similarly, Golden retriever bitches neutered at < 1 year of age are significantly heavier than those neutered at age 1 or more [65], and neutered Wirehaired Pointing Griffons (WPGs) weigh more than intact WPGs [81].  Other studies have been less emphatic; less than half the 122 males in one study had increased weight following neutering [62], whilst in another study 25 of 48 dogs that were castrated had an increased bodyweight [82].

Spayed bitches are more likely to have increased ‘indiscriminate appetite’ (eats rapidly, eats any commercial dog food, eats rubbish) than intact bitches [83] or increased food intake [84], which probably accounts for the observations that neutered bitches gain weight [84] and are twice as likely to be obese [85].  In one study, the weight gain in bitches was not related to increased deposition of subcutaneous fat [84].  In a 15-month study by Salmeri et al [86], although a trend for increased body fat was found in neutered animals, no statistical difference in obesity occurrence was attributable to neutering.  It is unknown what the long-term result might have been (ie years).  Others however, have reported body weight increases post-spay due to increased body fat [87].  In a separate study that followed neutered pets for 4 years, owners did not perceive animals neutered either before or after 24 weeks of age as being obese, though the author does acknowledge owners might not be the best judge of obesity in their pets [13]. 

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Longevity:  Information on the effect of neutering on longevity has only recently taken into account at what age dogs were neutered.  It is generally claimed that neutered dogs and bitches live longer [1, 2].  One report found neutered bitches lived longer than intact females [88], and whilst there was no statistical difference, neutered dogs and bitches tended to live longer [89] (also, see below regarding Golden retrievers and height/early age neutering).  Most studies however fail to take into account the age at neutering, and that with increasing age more dogs in a population are likely to be neutered.  Thus, intact versus neutered represents census data at that time point, rather than lifetime risk.  In a 10-year study of Boxers, when the population was simply considered as neutered or intact, being neutered was associated with a decreased risk of death.  When age at neutering was considered, neutered was associated with increased risk of death [3]. 

Behaviour:  Regarding other people’s experience with changes in behaviour following neutering, it would be wise to bear in mind the following; “One cannot extrapolate from experience with one or two dogs or cats in predicting the effects of castration or ovariectomy” [90].  

In contrast with the oft claimed behavioural benefits of neutering to ‘improve pet behaviour’ [1], where neutered pets ‘become more affectionate and become better companions’ [1, 2], several reports have found otherwise [6, 7, 83], with both breed and sex differences noted [6].  An open access web-based survey reported neutered dogs and bitches more aggressive to owners and were more aggressive towards, or fearful of, other dogs, and were more sensitive to touch than intact animals.  Breed and sex differences of touch sensitivity were noted [6].  A breed Club based survey by the same author found similar; spayed bitches were more aggressive towards strangers, more fearful, and more sensitive to touch than intact bitches.  “For most behaviours, spaying/neutering was associated with worse behavior, contrary to conventional wisdom.  A few behaviours (e.g., energy level, urine marking) were reduced in spayed/neutered dogs" [6].  Increased aggression towards strangers has previously been reported [7].

Neutering of males often reduces the sexually dimorphic behaviours – urine marking, roaming and mounting [62, 91, 92].  If a dog has repeated or learned these behaviours over some time, it is often suggested neutering will be less likely to be successful.  However neither age of the dog nor duration of the problem behaviour is predictive as to whether castration will have a beneficial effect as changes in behaviour do not occur in all dogs following neutering [82, 90-92].  In a study of 42 dogs with behaviour problems, roaming was the behaviour reported as being most affected by neutering – in 15/16 cases [92].  Another study of roaming in 25 dogs found no alteration in 80% of dogs whose roaming was not induced by bitches in oestrus, and an increase occurred post-neuter for 4% of dogs.  In dogs roaming because of a bitch in oestrus, a reduction occurred in 64% of dogs [62].  Five of ten dogs which were urine marking in the house had the behaviour decline in the house following neutering, but marking when taken for a walk did not alter [92].  Other studies have reported reduction of urine marking inside the house for 69% of dogs [62], and no decrease in urine marking for 35/48 (73%) dogs [82].  Ten of 15 dogs which were reported as mounting other people or animals had the behaviour decline after neutering [92], whilst another study found improvement in all six dogs studied with this behavioural problem [82].  It has also been reported that 5/48 male dogs appeared more affectionate post-castration [82]. 

Regarding aggression, in one study neutering in five out of eight dogs reduced aggression towards other dogs [92], whilst another study reported 6/9 dogs that were aggressive had a post-castration reduction in aggression, and of 48 dogs that were castrated (includes the 9 aggressive dogs), two had an increase in aggressive behaviour, and two had an increase in barking [82].  Another study found intermale aggression was reduced in 57% of dogs, but it also increased in 4% [62].  Neutering did not alter territorial aggression in eight dogs, nor fear-induced aggression in four dogs [92].  Perhaps it may be that neutering does not change behaviour for some male dogs as much as it changes their environment so to speak – because they are no longer smelling like intact male dogs to other male dogs, other dogs react different to them and they are challenged less often?  And speaking of smelling like intact males, or not – 6% of neutered males became attractive to intact male dogs [62].

A recent study of one year old dogs found bitches more likely to be fearful, and males aggressive, and that these behaviours were more extreme in neutered animals [93].  In dogs over a year of age, a significant association between aggression and neuter status has also been reported – the odds ratio for a member of the household being bitten by their dog were 3.23 for neutered males and 2.13 for neutered bitches, but age and reasons for neutering were not known [94].  Guy et al [94] also cited previous studies (Wright & Nesselwrote, 1987 and [95] both papers in the journal Applied Animal Behaviour Science) which found a disproportionate percentage of spayed bitches were presented for aggression problems compared to their relative frequency in the referral population.  Spaying may increase dominance aggression tendencies, especially in those bitches that are already aggressive [83].  The risk of an increase in aggression was reported to be greatest in bitches who were spayed at less than one year of age [83].  A study of Cocker Spaniels (which excluded dogs and bitches that were neutered once showing signs of aggression) found that neutered bitches were more likely to show aggression towards children in the household than were intact bitches [95].  German shepherd bitches who were spayed between 5 and 10 months of age were more reactive to approach by strangers than non-neutered bitches of the same age [96].  An Australian study of owner-companion dog interactions recently reported neutered dogs “were considered to be more nervous or timid than sexually intact dogs”, they were also rated as less anxious and engaged in fewer destructive behaviours” [97].

In English Springer Spaniels (ESS), neutering is associated with increased risk of biting (either sex); neutered males were more aggressive than intact males in 14 of 18 contexts (eg hug, stare, remove special food), and spayed females were more aggressive than intact females in 10 contexts (eg nudge on bed or couch, push off furniture).  As I’ve suggested with the examples in parentheses, these contexts were not necessarily the same for dogs and bitches.  Neutered of either sex were more likely to have bitten than intact ESS [98].  Male Cocker Spaniels neutered before showing any aggressive signs were no more likely to be aggressive in a variety of different situations than were intact males [95].  

Intact dogs and bitches are a third as likely to have separation anxiety as neutered ones [99].  This is also supported by the observation that in Europe where the percentage of dogs that are neutered is lower, a lower proportion of behaviour referrals are for separation anxiety.

Reports on general activity levels following neutering vary.  Spayed bitches were reported to be less energetic than intact bitches [6, 7].  Following castration 8/48 dogs were lethargic or appeared calmer (14/48 dogs) [82], though it was noted the dogs were generally around 8 years of age, and this may be age- rather than castration-related.  Other studies have reported neutered dogs and bitches were less anxious and engaged in fewer destructive behaviours [97], or that they were more active and excitable than sexually intact dogs and bitches [86].

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Cognitive impairment:  Regarding age/longevity, cancers are not the only consideration to be made; testosterone slows the progression of behavioural changes associated with cognitive impairment in aging dogs already showing clinical signs of disease [100].  Unfortunately insufficient sexually intact bitches were available in the study to evaluate the effect of neutering on bitches.  Whilst by itself inappropriate elimination as frequently occurs with cognitive dysfunction is not life threatening, this problem may result in euthanasia of the dog. 

Other conditions:  An increased risk of pancreatitis has been reported for neutered bitches [101, 102], and for neutered dogs in one study [101].

Perineal hernias are most likely to occur in intact, middle-aged dogs.  Dogs with perineal hernias have lower concentrations of androgen receptors in the muscles associated with the herniation.  Castration is often used as part of the treatment to reduce prostatic size, and thus possible straining that might be associated with enlargement of the prostate [82].

And whilst not directly health related; some dogs can develop skin and coat changes (thin, dry skin and woolly coat) after neutering , with an increase in hair growth (3/48) or change in coat colour (1/48) observed in dogs that were castrated [82].  This is more pronounced in coated breeds such as spaniels, golden retrievers, Irish setters (eg [103-105]).  The ill-understood coat condition observed in double coated breeds and variously referred to as ‘black skin disease’, ‘coat funk’, adult-onset growth hormone deficiency, growth hormone-responsive alopecia, castration-responsive alopecia, biopsy-responsive alopecia, congenital adrenal hyperplasia-like syndrome and alopecia X is not as some names might suggest, a condition that necessarily improves, nor maintains improvement upon neutering.  It has recently been suggested the term hair cycle arrest be used for this condition [106].

Early-age neutering:

Surgical complications:  It has been reported that dogs and bitches neutered below 12 weeks of age have significantly fewer minor surgical complications than those neutered aged over 24 weeks [107].

Gender characteristics:  Neutering of dogs and bitches before sexual maturity can inhibit the development of ‘gender characteristics’, such as broader bones in legs and skull and broader chest in dogs, and of muscular development.  Because the hormonal surge of puberty causes the growth plates in the bones to close, dogs neutered before puberty grow taller than they would have otherwise as the period of growth is prolonged (but the growth rate is unaltered [86]).  This does not mean your Vizsla will grow to the size of an Irish Wolfhound!  The taller stature may also be accentuated by the reduced muscle mass in neutered animals.  Salmeri et al [86] found that for dogs neutered at 7 weeks and 7 months of age when compared against intact litter mates, the younger a dog was neutered, the taller the dog became.  In bitches however, the bone length was not significantly different between intact bitches and those neutered at 7 months of age, but was between those neutered at 7 weeks and all the other bitches.  Thus, whilst slight alterations in eventual height and body mass may be irrelevant in a dog of unknown parentage obtained from a shelter, people who choose to neuter their purebred may prefer to defer neutering a very young animal.

Longevity, cancer and obesity:  Healthwise, Canine Companions for Independence (provide trained assistance dogs) found that early age neutered dogs had increased incidence of osteosarcoma, haemangiosarcoma, and obesity [8].

Not early age neutering specifically, but related to neutering at a young age and resultant increased height and/or weight; in Golden retrievers, “Both bitches and dogs neutered at < 1 year of age were significantly taller as adults than those neutered at > or = 1 year of age or intact animals.”  Further, “Among bitches and dogs, the taller the animal as an adult, the shorter the lifespan.” [65].  Similarly, the Wirehaired Pointing Griffon survey also reported taller and heavier WPG bitches died at an earlier age than shorter and lighter bitches [81], and taller and heavier Akitas were more likely to develop neoplasia [108].  One study reported that early-age neutered dogs were less likely to be overweight than those neutered at later ages [14].  (In relation to weight, diet restriction in Labrador retrievers delays the onset of arthritis and increases median life span compared to litter mates whose feed intake was not restricted [109].) 

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Bones and ligaments:  Early-age neutered dogs have increased incidence of orthopaedic problems (type not specified) [8], and hip dysplasia (CHD) [14].  Similarly, a correlation between increased incidence of CHD and increased time for growth plate closure has been reported in Labradors [110].  Although rates of CHD were increased in early neutered dogs, one study found the disease was significantly less severe than in dogs that were neutered at a later age; dogs with hip dysplasia that had been neutered at 5.5 months or older were “3 times as likely to be euthanatized for the condition as those with hip dysplasia and gonadectomized before 5.5 months of age.” [14].  This study was done on dogs obtained from a shelter – not a population of dogs that would normally be screened for CHD.  I assume therefore, the dogs presented with clinical signs.  In contrast, one study that followed early-age neutered pets for a 4-year period found no statistical difference in CHD rates between pre-pubertal (< 24 weeks of age), and traditional age (>/= 24 weeks of age) neutered pets [13].

Again, relating to neutering at a young age and resultant increased height/weight; Akita dogs (not bitches) “with any musculoskeletal disorder were 2-times as likely to be in the highest weight/height category than were dogs never diagnosed with a musculoskeletal disease.” [108].

Incontinence:  Age of spay - pre-pubertal, and traditional age - has been reported not to influence the development of urinary incontinence in bitches [13, 59].  One study observed 20/206 early spayed bitches developed incontinence, and when compared with a different earlier study that reported around 20% of bitches spayed after their first oestrus developed incontinence, ascertained that the risk of incontinence in early-spayed bitches was lower [111].  The clinical signs in bitches spayed prior to their first oestrus were however, increased, though the authors consider that because most bitches respond to treatment, and that incontinence risk is lower, “This relative disadvantage of early spaying is negligible when compared with the benefits, such as lower incidence of urinary incontinence and the protection against mammary tumours.” [111].

In contrast, an increased risk of urinary incontinence in bitches spayed before, compared with after their first heat cycle at the 10% level of significance, but not at the more conventional 5% level has been reported [5].  This is supported by increased incontinence seen in early-age spayed assistance dogs [8], and a study on early neutering referred to earlier [14], where a scale was noticed for incontinence risk and age at spaying – bitches neutered at less than 3 months of age were at greater risk of incontinence than those neutered at 3 months of age or more, and also in the WPG study where; “..the average age at neuter for neutered bitches with urinary incontinence was lower compared with the average age at neuter for bitches with no history of urinary incontinence.  This raises a concern about the current movement to neuter dogs at a much earlier age.” [81].

Peri-vulvar dermatitis/vaginitis:  With early-age neutering external genitalia remain infantile in appearance [86].  Peri-vulvar dermatitis has been associated with an infantile vulva, but the reports of its significance vary.  Increased rates of peri-vulvar dermatitis [59, 112-114] and/or vaginitis (reviewed in [10]), [114] have been reported in neutered compared with intact bitches, but the dermatitis may be uncommon [112], and was not demonstrated in a study of early-age and traditional age neutered bitches [86].  Conversely recent preliminary studies found a higher incidence of recessed vulva, peri-vulvar dermatitis, vaginitis, and recurrent urinary tract infections in spayed than in intact bitches, and the incidence was significantly higher in bitches spayed before puberty compared with those spayed later [114].

Cystitis:  Spain et al [14] also reported an increased risk of cystitis in early neutered bitches.  In a health survey of Old English Sheepdogs, 6/7 cases of cystitis in male dogs were in neutered males (total of 275 neutered males) and 35/48 cases of cystitis in bitches were in those who had been spayed (total 200 spayed bitches) [115].  All cases of vaginitis occurred in spayed bitches (40/200 spayed bitches and 0/253 intact bitches) [115].

Behaviour:  Prepubertal neutered dogs were more likely to succeed in becoming guide dogs than littermates neutered at a later age Canine Companions for Independence who provide assistance dogs found early age neutered dogs were more likely to fail training [8], and “ovariectomized police dogs have been reported to show unsatisfactory work performance when compared with sexually intact females” [117]  Perhaps these differences relate to the nature of the required tasks?  I do not know how the assessment was performed on the Guide Dogs – whether there was a statistically significant difference, nor if other factors were considered, etc – as it was just referencing a personal communication.

Behaviour-wise, Spain et al [14] reported “escaping considered a serious problem declined with decreasing age at gonadectomy”.  Increased rates of noise phobias and sexual behaviours were observed in early-age neutered dogs, whilst separation anxiety was decreased in early-age neutered dogs, though the authors suggested that these 3 results may represent Type I (false positive) errors.

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Other conditions:  The long-term study of early age neutered dogs included 167 dogs that had more than 10 years follow-up (median period of the study was 4.5 years).  Rare occurrences of autoimmune disorders, chronic renal failure, diabetes mellitus, mammary tumours, pancreatitis, hepatic disease, patellar luxation and urinary stones were reported

The risks and benefits (e.g. reduce risk of mammary cancer, increased risk of cranial cruciate ligament injuries, etc) that have been reported for dogs neutered at later ages should also still apply.

Someone I 'know' by email in northern California has said that the clinic near her no longer recommends neutering of males at 6 months, or necessarily at all if they are in a responsible home.  If they are going to be done, then they wait until around a year, and the same age for bitches.  The pendulum swinging?

And if you planned to do serious performance events with your dog – apart from the increased risk of cruciate ligament injury, there is reduced muscle mass in the absence of testosterone – not exactly performance enhancing ;/  It would be interesting to know the effect of this in old age – are neutered pets more prone to arthritic pain as their muscles are less well developed and able to support the joints? 

… and one last thing, some people have suggested vasectomy might be acceptable for the purposes of sterilization for owners who do not want their dog’s testes removed.  Studies on dogs before and after vasectomy reported that following vasectomy there was an increase in aggressiveness between some dogs and also greater libido [118].  Conditions such as roaming, mounting and marking which are associated with androgens may still be expected to still occur.

 

References

Note: the above information is not intended as a substitute for veterinary advice.

Revised:
15 February, 2007
20 April, 2007
1 September, 2007

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