The aim of veterinary nurses, and indeed everyone working in veterinary practice, should be to help owners make the best decisions regarding the health and welfare of their pets. One of these decisions will involve neutering, including whether or not to neuter, and if so, when is the best time to do so. Many practices have neutering policies for pet dogs although the advice tends to vary between practices, particularly with regard to the recommended age for neutering and may also differ between male dogs and bitches (Diesel et al, 2010).
Surgical neutering has generally been regarded as an important means of population control in pet dogs, that also has both health-related and behavioural benefits. Perceived health-related benefits include prevention of mammary tumours and pyometra in bitches and testicular and prostatic disease in male dogs. Perceived behavioural benefits are associated with reduction in sexually-dimorphic behaviours including roaming, mounting and urine marking in male dogs, and problem behaviours associated with seasons or phantom pregnancies in bitches.
In recent years a number of research papers have been published suggesting that the health-related benefits of neutering may be less marked than was once believed. They also suggest that neutering may also have negative health-related effects, particularly associated with the development of joint disease and neoplasia (Root Kustritz, 2007; Sanborn, 2007; Reichler, 2009; Beauvais et al, 2012a; Beauvais et al, 2012b; Torres de la Riva et al, 2013; Hart et al, 2014; Zink et al, 2014, Hart et al, 2016; Belanger et al, 2017; Waters et al, 2017).
This paper will outline the current evidence available, particularly with regard to the health-and behaviour-related risks and benefits of neutering. It will indicate where evidence is unclear or possibly misleading, and where more evidence is needed before the findings can be generalised to all dogs. This will hopefully help practices make the best decisions regarding when and whether to neuter pet dogs based on the currently available evidence, although this advice may change in the light of future research.
Neutering dogs as a means of population control
According to the Pet Food Manufacturer's Association (PFMA, 2017) there are just over 8.5 million pet dogs in the UK. Although there are no accurate records of how many of these dogs are neutered, recent estimates range from 40% (VetCompass Infographics, 2017) to 81% (PDSA PAW report, 2017). According to Dogs Trust (2017) the number of stray dogs in the UK has fallen significantly over the last 6 years, from 126 000 in 2011 to 66 277 in 2017. The proportion of these dogs being put to sleep has also reduced from 7% (approximately 8800 dogs) to 3% (approximately 2230 dogs) within the same period. This is likely to reflect a number of different things including different practices in the management of stray dogs and more widespread microchipping (a legal requirement for all dogs over the age of 8 weeks since April 2016), which increases the chances of stray dogs being successfully returned to their owners.
It is not possible to say how significant a role neutering has played in reducing the numbers of unwanted dogs being born. However surgical neutering is currently the most reliable means of population control in dogs, particularly if dogs and bitches are neutered before puberty (McKenzie, 2010). If dogs that are not intended for breeding are not neutered, owners must be advised about the importance of using management to avoid unwanted matings, for example ensuring gardens are secure, keeping bitches on lead and away from popular dog-walking areas when they are in season, and keeping entire male dogs on lead and under control if there are bitches in season in the neighbourhood.
Neutering and effects on behaviour
Neutering mainly affects behaviour by removing the main sources of sex hormones: testosterone from the testes in male dogs, oestrogen and progesterone from the ovaries in bitches. Plasma levels of the sex hormones themselves will start to fall within hours of removal of the gonads, although levels of follicle stimulating hormone (FSH) and luteinising hormone (LH) increase after neutering due to loss of the negative feedback effect of the sex hormones on the anterior pituitary (de Gier et al, 2012; Overall, 2013). Sex hormones generally act as behaviour modulators: they do not cause behaviours but instead influence the likelihood of particular behaviours occurring (Overall, 2013).
It is generally accepted that neutering is most likely to influence behaviours that are directly influenced by sex hormones. In male dogs these include unwanted sexual behaviour including mounting, indoor urine marking, roaming and some cases of aggression to other entire male dogs (Hart and Eckstein, 1997; Maarschalkerweerd et al, 1997). In bitches these include behaviours associated with seasons (including roaming, urine marking and increased aggression to other bitches especially in the same household) or pseudopregnancy (which can include aggression) (Connolly, 2002). However neutering does not always reliably prevent or reduce these behaviours, especially in male dogs (Beach, 1974; Hart and Eckstein, 1997; Maarschalkerweerd et al, 1997). While neutering is likely to be part of the treatment plan for these behaviour problems, behaviour modification may also be needed to resolve them.
Some studies suggest that sex and neuter status can influence behaviours that are not directly linked to sex hormones including fearfulness and aggression in different contexts (including aggression directed towards people). However the findings are very variable. For example Borchelt (1983) and Lund et al (1996) suggest that aggression is generally more common in entire male dogs than in neutered male dogs or bitches. However Casey et al (2013a) found no influence of sex or neuter status on the likelihood of dogs showing aggression to other dogs, and Casey et al (2013b) found no difference in incidence of humandirected aggression in entire male dogs compared with neutered male and entire female dogs. In this study neutered bitches were the least likely to show human-directed aggression (Casey et al, 2013b). In contrast O'Farrell and Peachey (1990) and Kim et al (2006) showed an apparent increase in reactivity and/or aggression in bitches after they were spayed. These differences are likely to reflect differences in the study designs, the situations in which aggression was shown and the populations of dogs studied. Zink et al (2014) found an increased incidence of fear-related behaviour problems, particularly fear of thunderstorms, in neutered dogs compared with entire (Zink et al, 2014).
Early (pre-pubertal) neutering has become fairly common in the UK in the last 20 years, but again we do not have much information regarding how this affects behaviour in dogs. Pre-pubertal neutering will prevent any problem behaviours associated with seasons or pseudopregnancy in bitches and in theory should reduce the likelihood of male dogs showing sexually-dimorphic behaviours such as mounting, urine marking and aggression to other entire male dogs. However Spain et al (2004) found an increased incidence of unwanted sexual behaviour in dogs and bitches neutered before 5.5 months compared with those neutered at 5.5 months or later. This study also found an increased risk of developing noise phobias, and a reduced risk of developing separation anxiety in earlier neutered dogs of both sexes, and male dogs neutered before 5.5 months were more likely to show aggression to family members and bark or growl at visitors than those neutered later (Spain et al, 2004).
Neutering and effects on health
Neutering has generally been perceived as having health benefits for dogs, particularly with regard to reducing the incidence of diseases of the mammary glands and uterus in bitches and testicular and prostatic disease in male dogs. However, over the last 10 years or so various studies have suggested that neutering may also be associated with adverse health effects. Some studies have looked at the incidence of a range of health problems in large populations of dogs, and compared differences in incidence between males and females, neutered and entire (Root Kustritz, 2007; Sanborn, 2007; Reichler, 2009; Belanger et al, 2017). Others have looked at the incidence of health problems in individual breeds of dogs, including Golden Retrievers (Torres de la Riva et al, 2013; Hart et al, 2014), Labradors (Hart et al, 2014), Hungarian Viszlas (Zink et al, 2014), German Shepherds (Hart et al, 2016) and Rottweilers (Cooley et al, 2002; Waters et al, 2017) associated with sex, neuter status and age of neutering.
While the findings vary a little from one study to another, in general they show an increased incidence of joint diseases including hip dysplasia and cranial cruciate ligament rupture, and of various types of cancers including haemangiosarcoma, mast cell tumours, lymphosarcoma, osteosarcoma and lymphoma in neutered dogs compared with entire dogs. Where age of neutering was considered (Cooley et al, 2002; Torres de la Riva et al, 2013; Hart et al, 2014; Zink et al, 2014; Hart et al, 2016), in many cases the risks of developing individual joint diseases and cancers appeared to be higher in dogs neutered earlier (generally under 12 months of age) compared with later. However this effect was not consistent either within or between studies, and Torres de la Riva et al (2013) found an increased risk of haemangiosarcoma and mast cell tumours in bitches neutered at 12 months of age or over compared with those neutered earlier.
With regard to the perceived health benefits of neutering, there certainly appears to be a relationship between earlier age of spaying and a reduced incidence of developing mammary tumours. However this effect may not be as marked as was previously suggested (e.g. Schneider et al, 1969), as there are flaws in the design of some of the earlier studies (Beauvais et al, 2012a), and the greatest benefit appears to be associated with spaying bitches before 2.5 years of age (Beauvais et al, 2012a; Waters et al, 2017). Spaying can also prevent bitches developing pyometra, although stump ‘pyometra’ or granuloma is a rare potential complication of ovariohysterectomy (McKenzie, 2010). Beauvais et al (2012b) also demonstrated that the risk of bitches developing urinary incontinence after spaying is smaller than had previously been thought. Castration removes the risk of male dogs developing testicular tumours and reduces the risk of other diseases influenced by testosterone including benign prostatic hyperplasia, although castration is associated with an increased risk of prostatic carcinoma (Figure 1) (Root Kustritz, 2007; Sanborn, 2007; Reichler, 2009).
Validity of study results
With all the studies looking at the relationship between neutering and health there are factors that may influence the validity of the results and the degree to which they can be reliably extended to all dogs (McKenzie, 2010). Many of these points also apply to the studies looking at the relationship between neutering and behaviour.
Most importantly, all the studies are retrospective, so there is no control over why decisions regarding neutering were made in individual animals. The decision to neuter or not in a particular animal could potentially have been influenced by the presence or absence of individual behaviour or health problems. For example Belanger et al (2017) found an increased incidence of congenital heart defects including aortic stenosis, patent ductus arteriosus and ventral septal defect in entire compared with neutered dogs. However dogs with heart defects may have been regarded as having a poorer anaesthetic risk than dogs without heart defects, and this may have influenced the decision to leave them entire. It is also possible that dogs were left entire because they had particular physical or behavioural characteristics that made them suitable for breeding, and that differed from those present in dogs that were neutered. Even where there is a strong correlation between neuter status and disease or behaviour incidence it is not possible to prove causality from a retrospective study (Olson, 2016).
The study designs also mean that the populations of dogs studied may differ from the general pet population. Some studies (Torres de la Riva et al, 2013; Hart et al, 2014; Hart et al, 2016) used the databases of University Veterinary clinics, which include a high proportion of referral cases as well as primary care patients. There were also significant variations in the effects of neutering on incidences of health problems between two different breeds (Golden Retrievers and Labradors) within the same study (Hart et al, 2014), which again suggests that the results of individual studies are unlikely to be generalisable to the entire population of pet dogs.
Most of these studies look at the relative risk of developing health problems without taking into consideration the actual risk, which can make the risk of developing a particular disease seem much higher than it actually is (McKenzie, 2010). Even a fairly large increase in relative risk of developing a particular disease after neutering may not be that significant if the disease is extremely rare in dogs, which may apply to prostatic tumours (Root Kustritz, 2007; Sanborn, 2007). Unfortunately the actual risk of developing individual diseases is not always known, although projects such as VetCompass (https://www.rvc.ac.uk/vetcompass), which collects and analyses anonymised patient data from contributing practices, will hopefully start to rectify this. Because of this, and because some diseases are more easily treated and managed than others, it has been argued that rather than considering the effects of neutering on the incidence of specific diseases, we should be looking more widely at how neutering impacts on longevity and quality of life (Waters et al, 2017).
Neutering and longevity
Studies looking at the influence of neutering on longevity in dogs all show slightly different results, probably due to the different study designs and differences in the populations of dogs studied. Hoffman et al (2013) found a strong positive relationship between neutering and longevity in dogs, with lifespan being increased by 13.8% in neutered compared with entire males, and by 26.3% in neutered compared with entire females. In this study neutered dogs were less likely to die of infectious disease, trauma, vascular disease and degenerative disease, but more likely to die from neoplasic and immune-related diseases, than entire dogs (Hoffman et al, 2013). O'Neill et al (2013), using information from the VetCompass database, found entire females had reduced longevity (-0.8 years) compared with neutered females, but no significant differences between longevity between entire and neutered males (both +0.4 years compared with entire females). Waters et al (2017) assessed the impact of pyometra and mammary tumours on longevity in Rottweiler bitches and found that, although entire bitches had an increased risk of developing both pyometra and mammary tumours compared with neutered bitches, neither of these diseases were associated with a reduction in overall longevity. This was presumably because, in most cases, treatment including surgery was curative (Waters et al, 2017).
Future research into health and behavioural effects of neutering
In order to make clearer associations between neutering and effects on health and behaviour we need large-scale longitudinal studies, following dogs through their lifetimes from puppyhood to old age and looking at the different factors that can influence both health and behaviour, including neutering. Generation Pup, a large-scale prospective cohort study is just being set up by Dogs Trust and the Royal Veterinary College (http://generationpup.ac.uk/) (Figure 2). They aim to recruit at least 5000 pups aged 16 weeks and under over the next 2 years, and will follow them throughout their lifetimes. Veterinary practices are strongly encouraged to promote this to their puppy owning clients as the more pups that are recruited the more valuable the information gained will be. Other data-gathering projects such as VetCompass will also deliver more information regarding the risks for developing health problems, including effects of neutering and age of neutering, over time. Again, the more practices that contribute to these, the more generalisable the information will be.
Summary of the risks and benefits of neutering dogs based on current information
Population control
Surgical neutering is currently the most reliable permanent means of preventing unwanted breeding in dogs. Dogs that are not destined for breeding should either be neutered, or, if left entire, carefully managed to prevent unwanted matings.
Health
Recent research suggests that neutering can potentially increase the risk of some health problems in dogs while it reduces the risk of others, and that earlier neutering (under 12 months of age) may be associated with an increased risk of some health problems compared with later neutering. However there is not currently enough evidence to know how reliable these findings are and whether they apply to all dogs or just certain populations of dogs. Until more research becomes available decisions regarding neutering should be based more strongly on its effects on population control and sexually-dimorphic behaviours rather than health.
Behaviour
Neutering can potentially reduce the likelihood of dogs showing behaviours that are directly influenced by sex hormones, including behaviour associated with seasons or pseudopregnancy in bitches and roaming, mounting and urine marking in male dogs. This also includes aggression shown by bitches to other bitches specifically during a season or pseudopregnancy and some cases of aggression shown by entire male dogs to other entire males. However neutering alone may not resolve these problem behaviours completely and behavioural intervention will also be needed.
There is currently not enough evidence regarding the effects of neutering on the incidence of behaviours that are not directly influenced by sex hormones, including fearfulness and aggression in other situations, to influence decisions about neutering. However, for dogs that are already nervous, it is important to take care with handling and managing the dog during the process of being neutered, in order to prevent exacerbation of fear-related behaviour problems. It would also be sensible to do some work on accustoming a nervous dog to being handled in the surgery before arranging the neutering operation.
Conclusion
In the absence of clear information particularly regarding the health-related effects of neutering it is currently very difficult to give neutering guidelines that will be suitable for all dogs, and that will reliably reduce the risks of developing specific diseases. This may change as more research becomes available. Until then, it is better to work out the risks and benefits of neutering for each individual dog based on the risk of unwanted matings occurring and the presence or absence of problem behaviours influenced by sex hormones, as well as the owner's preference.