Data were collected on 1260 cats owned by a random sample of UK households in 2007, by means of telephone questionnaires, which were completed by 33 per cent of the households contacted. Cats were owned by 26 per cent of these households, 42 per cent of which owned more than one cat. The owners of 622 female cats reported a total of 110 unplanned litters of kittens. Excluding cats with an unknown neutered status 92 per cent of the cats aged six months or more were neutered, but only 66 per cent of the cats aged six to 12 months were neutered. Multivariable logistic regression, based on data collected for one randomly selected cat aged four months or more in each cat-owning household, was used to identify factors affecting the cats' neutered status. Analysis of 48 sexually entire cats and 501 neutered cats showed that cats aged 10 months or more, with indoor access, that had been vaccinated within the last year or were currently registered with a veterinary practice, were more likely to be neutered than cats aged less than 10 months, without indoor access, that had been vaccinated more than one year ago or were not registered with a veterinary practice.
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VETERINARIANS and cat rescue charities recommend that cats that are not intended for breeding should be neutered as an effective means of population control that also provides benefits to individual cats. However, despite this recommendation, UK rescue charities admit and rehome large numbers of stray and unwanted cats and kittens every year. Increasing the proportion of cats that are neutered is crucial in avoiding overpopulation, and thus helping to reduce the number of unwanted cats that enter rescue charities. Neutering also provides health and behavioural benefits to the individual cat, despite being associated with an increased risk of obesity (Robertson 1999). For example, neutered cats are at less risk of reproductive system-related disorders and some infectious diseases (Schneider 1983, Rohrbach and others 2001). Neutered cats also make more suitable pets than entire cats because they are less likely to be aggressive towards other cats and are more affectionate towards people (Stubbs and others 1996).
The age traditionally recommended for neutering has been approximately six months (Olson and others 2001, Stalker 2004), but the British Small Animal Veterinary Association (BSAVA) and the Cat Group recommend that domestic kittens should be neutered at approximately four months of age for population control (BSAVA 2008, Cat Group 2008). Despite this recommendation, the results of a recent postal questionnaire survey have shown that only 3 per cent of a sample of 875 UK veterinarians reported that their practice recommended that cats should be neutered at four months of age (J. K. Murray, E. Skillings, T. J. Gruffydd-Jones, unpublished data) whereas 51 per cent recommended neutering at six months of age or older (Murray and others 2008).
Nassar and Mosier (1982) calculated that 76 to 88 per cent of female household cats in Manhattan, Kansas, USA would need to be neutered for zero population growth (based on the assumption that 50 to 100 per cent of all unspayed females would reproduce). Identical neutering rates of 80 per cent were reported for male and female household cats in St Joseph County, Indiana, USA (Patronek and others 1997), and studies in specific areas of the Southampton and Manchester regions of the UK (Chipman 1990, Horsfield 1998, Bradshaw and others 1999) reported neutering rates of 76 to 97 per cent and 89 to 99 per cent for male and female household cats, respectively. The authors are not aware of any investigations of either the rate of neutering of household cats sampled from across the UK or the factors that potentially influence whether cats are neutered.
The aims of this study were to produce descriptive statistics on cats owned by a random sample of UK households, to calculate the prevalence of neutered cats, and to identify the factors that increased or decreased the likelihood of a cat aged four months or more being sexually entire. Information about factors that could be modified could be used to recommend strategies to target specific groups of cats and/or owners, with the aim of increasing the neutering rate and helping with population control.
Materials and methods
A cross-sectional study was used to obtain data about the cats owned by households in the UK. A commercial company (Tracesmart) supplied contact details for a random sample of households listed in the UK electoral roll. Data were collected between July 16 and December 16, 2007, by means of a telephone questionnaire that was administered by six trained interviewers. Households that were listed as ‘ex-directory’ or were registered with the Telephone Preference Service (TPS) were excluded. The telephone calls were made on weekday evenings between 18.00 and 21.00, and at weekends between 10.00 and 17.00, and a maximum of three attempts were made to contact each household. A total of 13,795 household telephone numbers were used; contact was made with 8961 of these households, and the questionnaires were completed by 2978 of them, a 33·2 per cent response rate. In order to reduce any response bias resulting from the households being informed that the study was about cats, the study was described as a study of UK pets and it was stressed in the introduction that the interviewers needed to speak to people who did not own pets as well as people who did own pets. Data were collected on the numbers of cats and dogs owned by the respondents and on the age, sex and neutered status of the cats in each cat-owning household. The owners of female cats were asked to provide information on the number of litters of kittens born to each of them and whether these litters resulted from planned or unplanned pregnancies.
The questionnaires took approximately two to three minutes to complete by households without cats and approximately 10 minutes to complete by households with cats.
The number of households owning cats and dogs were compared by chi-squared analysis. Significance was set at P<0·05.
Factors affecting the neutered status of the cats
In addition to data on the age, sex and neutered status of all the cats, additional data were collected from one cat (aged four months or more) in each cat-owning household. This cat was selected by the interviewer, who used a random number generator to select the ‘questionnaire cat’ once preliminary details had been obtained for all the household's cats. Selecting one cat per household to be included in the analysis of the factors affecting the cats' neutered status eliminated the need to account for clustering by household in the analysis, and ensured that collecting data from multiple-cat households was not excessively time-consuming. The minimum age for inclusion in the study of the risk factors for neutered status was set at four months because it is the age at which current guidelines recommend neutering (BSAVA 2008, Cat Group 2008). Cats less than four months of age were not included because it was assumed that very few domestic cats of this age would be neutered, and therefore most, if not all, cats aged less than four months would have entered the study as entire cats, thus reducing the ability to detect potentially modifiable factors affecting the cats' neutered status. Data relating to the potential factors summarised in Table 1 were collected for each of the selected cats.
The outcome under investigation was the neutered status of the cat, that is, whether it was neutered or entire.
The potential risk factors were tested for their association with the cats' neutered status using univariable logistic regression models. The statistical package Egret (Cytel Software Corporation) was used to analyse the data. All variables with a univariable P<0·2 were considered for inclusion in a multivariable model, which was built using the technique of backward elimination. Variables were retained in the model if they were shown to improve the fit of the model significantly by assessing the change in deviance, (assuming that the change in deviance follows a chi-squared distribution with n degrees of freedom, where n is the number of extra parameters fitted). Continuous variables were categorised into quintiles in the univariable analysis and quadratic and piecewise linear terms were also derived for each continuous variable. Different forms of continuous variables were compared (by assessing the change in deviance) as recommended by Parkin and others (2005), to determine which best described the shape of the relationship between the variable and the neutered status of the cat. The effect of plausible interactions between variables was also tested for in the model.
Questionnaires had been completed by 119 respondents before an additional question about whether the cat was registered with a veterinary practice was included. Two multivariable models were built, including and excluding this variable, which was significant in the univariable analysis. The multivariable models were very similar (data not shown) and the model including the registration status was therefore selected as the final model, because it was considered that it provided the most useful information, despite being based on a smaller sample.
Power of the study
The study was designed to have 80 per cent power to detect an odds ratio of 2·0; however, the prevalence of entire cats was lower than expected and reduced the power of the study. Revised calculations, based on the ratio of neutered:entire cats in the final analysis, show that, due to the reduced number of entire cats, the study had 80 per cent power to detect an odds ratio of 2·6, based on a 0·05 probability of a Type I error (95 per cent confidence) and assuming that 20 per cent of the neutered cats were exposed to the factors affecting neutered status (Epi-Info 6; CDC).
Cats were owned by 25·5 per cent (760 of the 2978 households), dogs were owned by 30·6 per cent (911 of 2974) of the households, there were no data for four households, and 7·1 per cent (210 of 2974) of the households owned one or more cats and dogs. Significantly fewer households owned cats than dogs (P<0·001).
Four hundred and forty-three (58·3 per cent) of the 760 households owning cats had one cat, 223 (29·3 per cent) had two, 55 (7·2 per cent) had three, 16 (2·1 per cent) had four, 11 (1·4 per cent) had five and 12 (1·6 per cent) had between six and 12 cats. A total of 1260 cats were owned by the 760 cat-owning households, but there were no data relating to the age and sex of 26 of them, and these cats are therefore not included in Table 2. Excluding the cats aged less than six months and these with an unknown neutered status, 91·5 per cent (1068 of 1167) were neutered and 8·5 per cent (99) were entire. Twenty-three (42 per cent) of the 55 cats aged five months or less were less than four months old. The mean and median numbers of cats owned per household were 1·66 and one, respectively. The median age of the cats was seven years (range seven weeks to 22 years).
The number of litters that each female cat had produced and whether these litters were planned or unplanned are summarised in Table 3. Owners of 60 of the 682 female cats (8·8 per cent) were unsure whether their cat had ever produced any litters, and these cats were excluded from Table 3. Some respondents knew that their cat had had one or more litters of kittens with a previous owner, but were unable to state whether the litter was planned or unplanned. One non-pedigree cat was reported to have produced 15 litters, all of which resulted from planned pregnancies.
Randomly selected cats aged four months or older
Ninety-eight per cent (748 of the 760 cat-owning households) owned one or more cats aged four months or more and provided data for the study of the factors affecting the cats' neutered status. Sixty-six of the 748 (8·8 per cent) randomly selected cats were reported to be entire; six (0·8 per cent) were of unknown neutered status, and were excluded from the analysis.
Data were thus obtained for 66 entire cats and 676 neutered cats; however, data relating to variables included in the multivariable model were missing for 18 of the entire cats and 175 of the neutered cats. The multivariable analysis was therefore based on data relating to 48 entire cats and 501 neutered cats.
Non-significant univariable results included the cat's geographical location, its sex and its breed.
The final multivariable logistic regression model for risk factors associated with neutered status is summarised in Table 4. A piecewise linear form of the variable ‘age of the cat (in months)’ was the best fitting form of the variable when compared with categorical, linear and quadratic forms. Fig 1 illustrates how the probability of a cat being entire varied according to its age, on the basis of the results of the multivariable model. For clarity, the probability of being entire is shown only for cats aged up to two years. Plausible interactions, for example, between age and registration status, and age and indoor or outdoor lifestyle, were tested for, but none was found to be significant.
The results of this study were based on data collected by a telephone questionnaire survey of a sample of 2978 randomly selected UK households. Higher response rates than those obtained in this study (22 per cent from all the selected households and 33 per cent from the contacted householders) would be expected from using door-to-door surveys, and were recorded in a study of dog ownership by Westgarth and others (2007), who obtained responses from 84 per cent of all households and 94 per cent of contacted households. However, the sampling method used in the study reported here made it possible to collect data from across the UK, and data were collected from cat owners who could not have been traced through veterinary practice records. These advantages were considered to outweigh any disadvantages associated with the low response rate, because it was considered unlikely that the analysis of risk factors for neutered status would be affected by any non-response bias. In addition, the estimate of the prevalence of neutered cats in the UK was likely to be less biased by non-response bias than an estimate obtained through contacting the owners of cats registered with veterinary practices.
A significantly (P<0·001) smaller proportion of the households sampled owned cats (25·5 per cent) than dogs (30·6 per cent), in agreement with the findings of Westgarth and others (2007) and the Pet Food Manufacturers' Association (PFMA) (2008), which both reported that fewer UK households owned cats than dogs (22 per cent v 24 per cent, and 18 per cent v 22 per cent, respectively). The differences in the reported percentages are likely to result from differences in the data collection methods, although detailed information on the data collection methods used by the PFMA are not available. The present study was described to potential respondents as a study of pets in the UK, and it was stressed that participation was required from non-pet owners as well as pet owners; nevertheless, it is likely that the non-pet owners would have been less likely than the pet owners to participate. As a result, the percentage of cat-owning and dog-owning households may have been overestimated.
Nassar and Mosier (1982) estimated that 76 to 88 per cent of female household cats in the Manhattan area of Kansas, USA, needed to be neutered for zero population growth, but they did not specify the age at which neutering should be done in order to obtain zero population growth. The age at which female cats are neutered, together with factors such as population density and their indoor or outdoor lifestyle, undoubtedly has important implications for their potential to breed; hence the current guideline that domestic kittens should be neutered at approximately four months of age (BSAVA 2008, Cat Group 2008), before they reach sexual maturity at approximately six months (Turner and Turner 1994). There were only 41 female cats aged six to 12 months in this study, and only 28 (68·3 per cent) of them had been neutered (Table 2). No data were collected on the age at which female cats had produced litters, but 119 of 622 female cats (19·1 per cent) had produced one or more litters, and of those litters that were known to be planned or unplanned 110 of 156 (70·5 per cent) were unplanned. However, this percentage rises to 78 per cent if the unusual case of one non-pedigree cat that had produced 15 planned litters is removed from the dataset. It therefore appears that there is scope to reduce the number of unplanned litters by increasing the proportion of female cats that are neutered before they reach sexual maturity.
Five independent variables retained significance in the final multivariable model of risk factors affecting neutered status (Table 4). Cats that lived strictly outdoors were approximately 10 times more likely to be entire than cats that lived indoors (with or without outdoor access). Sexually entire cats that live outdoors are likely to have opportunities to mate with local owned, stray or feral cats and could contribute to the number of unwanted cats in the UK. It was predicted that ‘indoor’ cats with no outdoor access, and particularly indoor cats with no opportunity to mate, might be more likely to be entire than cats with an indoor/ outdoor lifestyle, because their owners might be less likely to consider it necessary to have them neutered; however, there was no significant difference between these two groups, and they were combined in the multivariable analysis.
As expected, the age of the cat significantly affected the likelihood that it had been neutered; however, the exact relationship between age and neutered status was not predictable. In the final model the relationship was best described by a piecewise linear form of the variable, consisting of two straight lines. The ‘best fitting’ form of the relationship was a linear decrease in the likelihood of a cat being sexually entire as its age increased from four to nine months, followed by a more gradual linear decrease as its age increased beyond nine months. Establishing the age at which the first linear component stopped and the second started (nine months) provides valuable information on the age at which future interventions should be targeted to increase the proportion of cats aged less than 10 months that are neutered. No data were obtained on whether the owners had received veterinary advice on neutering and, if so, the age at which neutering had been recommended, but Murray and others (2008) showed that 51 per cent of a sample of 875 UK veterinarians recommended neutering cats at six months of age or older. Hence, it might be useful to try to increase the proportion of veterinarians who recommend neutering cats before six months of age.
Cats that had not been vaccinated during the previous year were nearly seven times as likely to be entire as cats that had been vaccinated. This association was expected in young cats, because neutering appointments are often made when they are brought to a veterinary practice for vaccination. However, this association was independent of the effect of age, (as age was also in the multivariable model), and thus also applied to older cats. This association might reflect that owners who perceive neutering to be essential to prevent unwanted pregnancies and/or to provide health and behavioural benefits also perceive vaccination to be important for preventing infectious disease, and continue to have their cat vaccinated regularly, long after it has been neutered. In contrast, owners who elect not to have their cats neutered may be less likely to have their cats vaccinated regularly, possibly because they are not aware of the potential consequences of failing to have their cats neutered and vaccinated. Alternatively, it could be due to an inability or reluctance of some owners to spend money on their cats, whether for vaccination or neutering.
The cats that were reported to not be registered with a veterinary practice were nearly eight times more likely to be entire than the cats that were registered. This association had been expected, because a neutering appointment leads to registration; however, a prospective study would be needed to evaluate the extent to which factors such as the education of owners by veterinarians may influence their decision to have a cat neutered.
The respondents were asked to state whether they agreed or disagreed with a series of statements about neutering. Only four respondents disagreed, either strongly or slightly, with the statement that neutering was a good method of helping to control the number of unwanted cats, and they were significantly more likely (P<0·001) to own an entire cat than a neutered cat; however, this result should be treated with caution because the confidence interval surrounding the odds ratio (371) was very wide.
Although 91·5 per cent of the female cats aged six months or more had been neutered, only 68·3 per cent of those aged six to 12 months had been neutered, leaving 31·7 per cent of them with the potential to breed. In fact, 19·1 per cent of the female cats for which appropriate data were available had produced one or more litters, 70·5 per cent of them resulting from unplanned pregnancies. The data also show that the rate at which the cats were neutered decreased markedly after they reached 10 months of age. Further research may help to identify effective means for increasing the proportion of cats aged four to nine months that are neutered. In particular, owners who plan to have their cats neutered should be encouraged to have it done before the cat reaches sexual maturity, to help to reduce the number of unplanned pregnancies and the number of unwanted cats in the UK. This strategy might be more effective in terms of population control than attempting to persuade the small number of owners of older entire cats to have their cats neutered.
The authors would like to thank all the respondents to the questionnaire who provided data for the study. Laura Cockerell, Hannah Gritti, Lauren Guthrie, Anna Moore, Katy Rossiter and Jennnifer Sinclair are thanked for data collection and data entry. Professor Bill Browne and Professor Nigel French are thanked for providing advice on the data analysis. Cats Protection funds J. M.'s post. The questionnaire is available on the University of Bristol website (www.vetschool.bris.ac.uk/projects/NeuteringQuestionnaire072007.swf).
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