ResearchDevelopment of behavior in adopted shelter kittens after gonadectomy performed at an early age or at a traditional age
Introduction
To date, surgical gonadectomy in cats is the most reliable and permanent method of contraception (Looney et al., 2008, Reichler, 2009; ACC&D 2013). Traditionally, gonadectomy is performed around the age of 6 months or later (Stubbs et al., 1995, Olson et al., 2001, Root Kustritz, 2007), but at that age, some cats will have already entered puberty and are able to produce litters (Jemmett and Evans, 1977, Jackson, 1984). Consequently, to ensure that adopted cats from shelters will not reproduce, prepubertal gonadectomy (PPG) has been promoted (Stubbs et al., 1995, Howe, 1997, Bushby and Griffin, 2011, Joyce and Yates, 2011, Root Kustritz, 2012, Polson et al., 2012; Root Kustritz, 2013).
Concerns about PPG, defined as gonadectomy between 6 and 16 weeks of age (Root Kustritz, 2013), have been voiced in the past, particularly by practicing veterinarians (Spain et al., 2002, Murray et al., 2008). Especially, the risks related to anesthesia and surgery and the possible development of certain medical conditions (e.g., obesity, feline urinary tract diseases, delayed physeal closure time, and so forth) were debated. To date, however, several studies have established safe anesthetic and surgical protocols for PPG (Porters et al., 2014; Porters et al., manuscript in revision; Aronsohn and Faggella, 1993, Faggella and Aronsohn, 1993, Howe, 1997, Robertson et al., 2003, Robertson, 2007, Joyce and Yates, 2011, Bushby, 2013). Furthermore, a number of studies have investigated physical development (e.g., diameter of the urethra, body weight, physeal closure time) after early-age neutering in cats without significant differences between cats neutered at 7 weeks or 7 months (Root et al., 1996, Stubbs et al., 1996, Root et al., 1997). Finally, there have also been concerns about the behavioral development after PPG in cats. Because PPG is performed during the sensitive socialization period, which lasts until 9-10 weeks of age (McCune, 1995, Adamelli et al., 2005, Overall et al., 2005), this intervention might affect the behavioral development, resulting in behavior problems.
Commonly reported behavior problems in cats are inappropriate elimination, fearful behavior, aggression to other cats or people, and destructive behavior (Heidenberger, 1997, Fatjo et al., 2006, Shore et al., 2008, Amat et al., 2009). Behavior problems may be caused by or result in fear and anxiety, thereby affecting animal welfare (Landsberg, 1996, Levine, 2008). Furthermore, many feline behavior problems can be a burden for the owner, affecting the owner–cat bond (Overall et al., 2005). Consequently, the risk for relinquishment or even euthanasia increases (Patronek et al., 1996, Salman et al., 1998, Shore et al., 2003, Casey et al., 2009). In order for PPG to be considered an acceptable alternative for traditional-age gonadectomy (TAG), it should have at least the same advantages without any additional disadvantages compared with TAG.
The link between age at the time of gonadectomy and behavioral development in cats has been scarcely investigated (Stubbs et al., 1996, Howe et al., 2000, Spain et al., 2004, Wright and Amoss, 2004). In the experimental study by Stubbs (1996) investigating the physical manifestations after (prepubertal) gonadectomy, behavioral manifestations were also assessed at 12 months of age: sexually intact cats displayed greater intraspecies aggression and less affection toward humans than did cats neutered at 7 weeks or 7 months. In one long-term follow-up study, no differences were detected in two age groups (gonadectomy at <24 and ≥24 weeks of age) for overall behavior problems, destructive behavior, inappropriate elimination, and other miscellaneous behavior problems (Howe et al., 2000). Spain et al. (2004), on the other hand, reported that early-age neutering was associated with a decreased occurrence of hyperactivity and increased shyness in the presence of strangers in both sexes and increased hiding in male cats, but significance disappeared when analysis was restricted to cats whose owners considered the behavior “serious.” Unfortunately, the reported studies have one or more methodological limitations. In some cases, a study design relying on an extensive recall ability by the owners of more than 1 year was used (Spain et al., 2004, Howe et al., 2000). Furthermore, the sample size could be quite small (Stubbs et al., 1996). Finally, early-age gonadectomy was sometimes defined as neutering cats up until 22-24 weeks of age (Howe et al., 2000, Spain et al., 2004), and therefore, there is a good chance that some cats would not have been prepubertal. In a more recent study, investigating the prevalence of house soiling and aggression in shelter kittens during the first year after adoption, no significant association between age at the time of gonadectomy (between 6 and 13 weeks or between 5 and 7 months of age) and the behaviors of interest was found (Wright and Amoss, 2004). Data collection occurred prospectively and at several time points but, unfortunately, ended at 52 weeks after adoption. Therefore, a prospective long-term study in cats, with randomized PPG and TAG groups, spanning the postadoption developmental stages into social maturity, is currently lacking.
The present study is part of a larger project on early-age gonadectomy in cats, supported by the Belgian government. The use of the term “behavior problem” was avoided as this is commonly used to refer to a clinical problem, which is difficult to establish without a detailed behavioral history. Instead, the behaviors as reported by the owner were examined, including the “undesirability” thereof, as it is the personal perceptual element which defines the concept of an “undesirable” or “problematic” behavior (Blackwell et al., 2008, Ramos and Mills, 2009). Consequently, the term potentially undesirable behavior will be used to describe behavior that is reported by the owner and that might potentially become troublesome to the owner (Blackwell et al., 2008). The term undesirable behavior, on the other hand, refers to behavior that has been indicated by the owner to be truly troublesome or problematic and thus considered to be unacceptable to the owner (Blackwell et al., 2008, Amat et al., 2009). The main aim of the present study was to investigate the effect of age at gonadectomy in both sexes on the mean number of potentially undesirable and undesirable behaviors in shelter cats during the first month after adoption (short term, potentially undesirable behavior only) and during 24 months after adoption (long term, both potentially undesirable behavior and undesirable behavior). Furthermore, the present study also aims to investigate the association of age at gonadectomy and other selected social and environmental factors on the most common (potentially) undesirable behaviors in cats as reported in literature: inappropriate elimination, fearfulness, (non)play-related aggression toward people or animals, and destruction (Heidenberger, 1997, Fatjo et al., 2006, Shore et al., 2008, Amat et al., 2009).
Section snippets
Materials and methods
The study protocol was approved by the local Ethical Committee (Faculty of Veterinary Medicine, Ghent University, Belgium) (licence numbers EC 2010/019 and EC 2011/077) and the Deontological Committee (Federal Public Service Health, Food Chain Safety and Environment, Brussels, Belgium).
Results
Of a total of 800 recruited kittens, the general information survey was completed for 678 kittens (PPG, n = 465 and TAG, n = 213). For most of the kittens, the responding owner was a female (PPG, 65% and TAG, 62%), between 18 and 38 years of age (PPG, 60% and TAG, 65%), and without children (PPG, 56% and TAG, 62%). Most kittens lived in a house (PPG, 81% and TAG, 80%) and/or had access to a garden, a terrace, and/or a court (PPG, 91% and TAG, 91%). More than half of all PPG and TAG kittens
Discussion
The present study was designed to provide short- and long-term information regarding behavioral characteristics in shelter cats undergoing PPG compared with TAG. To our knowledge, this is the only prospective study to date, with randomized PPG and TAG groups and short-term and long-term follow-ups, spanning the postadoption developmental stages into social maturity. In shelter cats, age at the time of gonadectomy (8-12 weeks vs. 6-8 months of age) did not affect the mean number of potentially
Conclusion
This study found no evidence that age at the time of gonadectomy (PPG vs. TAG) in cats has an effect on the mean number of (potentially) undesirable behaviors or on the occurrence of commonly reported behaviors (inappropriate elimination, non–play-related aggression, fearful behavior, or destruction) in literature during 24 months after adoption from a shelter. Consequently, also from a behavioral point of view, PPG can be recommended for shelter cats. In addition, various social and
Acknowledgments
This research was funded by the Belgian Federal Public Service Health, Food Chain Safety and Environment (RT 09/12 Sterycat project). The authors thank the shelters and cat owners for their participation in this research project. S. Merciny is acknowledged for assistance with the functional analysis of the survey platform and C. Corridan for sharing her insights about survey methodology. Finally, T. De Keuster, I. de Cock, E. Peeters, A. Bru, and M. Stolting are acknowledged for their
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