WSAVA guidelines for the control of reproduction in dogs and cats

During the second half of the last century, dogs and cats have gained an important place in many households and their numbers have increased remarkably in many countries. While there are anecdotal estimates of pet ownership by country provided on websites and in the lay literature, there is a lack of peer-reviewed data on the actual world population of dogs and cats, both owned and unowned. These animals may easily reproduce once they achieve puberty if not constantly under control. Therefore, veterinarians are continuously presented with requests to contain or eliminate reproductive behaviour or fertility as a whole in owned dogs and cats.

The increased presence of small animals in our homes has been paralleled by an increase in dog and cat populations in suburban areas where free-roaming stray or unsupervised animals reproduce uncontrolled, causing public health concerns. Animal shelters in many areas are overcrowded by dogs and cats. Proactive rehoming, adoption and sterilisation policies are being promoted in many parts of the world. However, shelter populations seem to have remained stable and have, despite all these efforts, increased in some countries/areas/municipalities (Crawford et al., 2019). Therefore, controlling dog and cat reproduction has always been a key issue for veterinarians working in animal welfare organisations and for small animal practitioners alike.

The historical approach to controlling dog and cat reproduction has been through surgical gonadectomy. For males, multiple surgical methods, approaches and means of haemostasis have been utilised with success and precise technique is generally based on surgeon experience and preference. For females, removal of all (ovariohysterectomy, OHE) or part (subtotal ovariohysterectomy; SOHE) of the uterus may be performed concomitantly with removal of the gonads. While many veterinary textbooks describe the OHE procedure with ligatures placed and subsequent transection made at the level of the uterine body, it is important to recognise that this is both anatomically and physiologically incorrect. Some portion of the uterus will inevitably remain in the patient and therefore what is being performed, is a SOHE (Mejia et al., 2020). SOHE should be avoided as it exposes the female to the risk of developing a uterine stump condition should an ovarian remnant be present, or a progestogen treatment administered at a later date. Ovariectomy (OE) alone is quicker, uses a smaller incision and is associated with less potential complications (Okkens et al., 1997). Consequently, in the absence of uterine pathology, and if lack of gonadal hormones is both predicted and desired, these guidelines recommend OE as the preferred surgical procedure for sterilisation of female dogs and cats.

Laparoscopic sterilisation is less painful and provides better visualisation of all pertinent structures, especially in small breed dogs. Owner familiarity with minimally invasive surgery in humans is producing a large demand for its use in pets (Buote, 2022). Surgical sterilisation techniques that maintain gonadal hormones such as vasectomy and hysterectomy have also been proposed as effective and safe means of inhibiting reproduction in pets (Kutzler, 2020b; McCarthy, 2019; Zink et al., 2023).

Alternatives to the surgical removal of gonads for dogs and cats have existed since the second half of last century. The first drugs commercially available for the control of reproduction in small animals were synthetic analogues of progesterone (progestogens) that block the action of the hypothalamic–pituitary–gonadal (HPG) axis. Unfortunately, improper use in dogs and cats has led to several case reports of side effects from overdosing (Romagnoli & Ferre-Dolcet, 2022; Romagnoli & Lopate, 2017). After careful patient selection, progestogen use at the appropriate dose and duration can be a safe and effective method for reproduction control.

Earlier this century a new category of active principles, long-acting preparations of gonadotropin-releasing hormone (GnRH) agonists became available as veterinary drugs in some countries allowing for prolonged duration of reproduction control (Fontaine & Fontbonne, 2011; Goericke-Pesch et al., 2013; Romagnoli et al., 2009; Trigg et al., 2006). The effect of a single administration of a long-acting GnRH agonist implant varies from 6 to 12 months (depending on dosage) in dogs and is much longer in cats. Repeated administration is effective and appears to be safe based on the limited data available (Brändli et al., 2021; Romagnoli et al., 2023). Therefore, its use in bitches for which surgery is not an option may be considered. Long-acting GnRH agonists are approved in some countries for use in male dogs and cats and in prepuberal bitches; their off-label use is proving effective and safe in queens while more data is needed to warrant its use in postpubertal bitches. Male dogs and cats may also be rendered sterile by local administration of chemical agents (Oliveira et al., 2013). Approaches such as vaccination against GnRH or, more recently, gene therapy causing overexpression of Mullerian inhibiting substance are promising, particularly for females (Levy et al., 2005, 2011; Ochoa et al., 2023; Vansandt et al., 2023; Vargas-Pino et al., 2013). The remarkable extent of current knowledge on this topic makes it increasingly challenging for veterinarians to advise clients and stakeholders on the best approach to reproduction control for small animals. This is particularly true for small animal practitioners given the emotional value clients usually place on pets. Reproduction control as a presenting request has gone from the very simple “I would like my pet to be spayed/neutered” to a very elaborate set of questions the most intriguing of which are “how and at what age should it be done” and more recently and importantly “should we do it or not”? As a consequence of the more important role dogs and cats are playing in our lives, shelter conditions have also been receiving increased attention from the public and social media. Once in a shelter, rescued or captured animals are invariably gonadectomised, a practice which continues around the world using a standard surgical approach. Reproduction of shelter animals needs to be blocked permanently as this prevents further reproduction and increases their chances of being adopted. Therefore, surgical sterilization remains a valid solution in certain situations because of its ease and cost-effectiveness. However, evidence is accumulating in favour of the efficacy of newer surgical techniques which, in spite of maintaining reproductive behaviour, may offer the option of adopting healthier animals.

Small animal practitioners need to acquaint themselves with current knowledge regarding reproductive control offering a host of novel approaches replacing the potentially harmful practice of routine gonadectomy of young dogs and cats. The best options for reproduction control in dogs and cats are the ones that have the least long-term health concerns which may be more pronounced particularly in large and giant breed dogs (Benka et al., 2023). For owned pets, such a decision should be made on a case-by-case basis in consultation with the owner with due consideration of species, sex, breed, purpose and lifestyle of the pet as well as financial constraints. Albeit less ideal for the individual pet, methods for reproduction control in the shelter environment may differ to that of owned animals. Effective strategies to curb reproduction of stray dogs and cats are lacking, may be cost- and labour-intensive and are often regarded as controversial (Read et al., 2020; Wolf et al., 2019). Shelter policy makers will only agree to the selection of permanent sterilisation options that are affordable and they oppose alternative options which maintain sexual behaviour in pets as that may lessen the probability of adoption and increase pet abandonment. Veterinarians are in a key position to educate policy makers and the pet-adopting public about alternative approaches with less long-term health concerns. Their action may in time lead to acceptance of reproduction control options that better align with the health concerns of individual pets.

Sterilisation of dogs and cats is the most common surgical procedure performed by small animal practitioners worldwide (Greenfield et al., 2004). Numerous methods are employed successfully and can be divided into those that remove the source of gonadal hormones and those that preserve them. The role of gonadal hormones on long term health is debated, and this issue is discussed in detail later in this document.

Gonadectomy leads to the irreversible loss of reproductive hormones, which coincides with a loss of the negative feedback of gonadal steroids on the hypothalamic–pituitary axis (HPA). The latter causes permanently increased blood concentrations of LH and FSH (Beijerink et al. 2007b). The impact of these facts on the development of certain diseases in gonadectomised dogs is currently under investigation (Ettinger et al., 2019; Kiefel & Kutzler, 2020; Kutzler, 2020a, 2023; Zwida & Kutzler, 2022) and may vary between individuals. Several beneficial effects of gonadectomy have been described and are reported here. Concluding statements on benefits of gonadectomy for each condition should not be regarded as final but should be considered in view of corresponding detriment/s of gonadectomy for the same or connected condition/s. Furthermore, new evidence in this field is continually emerging and may shift the risk/ benefit calculation over time. Where appropriate, the effect of paediatric (at 6 to 16 weeks of age) and prepubertal gonadectomy is emphasised (see Table 2).

Gonadectomy leads to the irreversible loss of reproductive hormones, which coincides with a loss of the negative feedback of gonadal steroids on the HPA. The latter causes permanently increased blood concentrations of LH and FSH (Beijerink et al. 2007b). The impact of these facts on the development of certain diseases in gonadectomised dogs is currently under investigation (Ettinger et al., 2019; Kiefel & Kutzler, 2020; Kutzler, 2020a, 2023; Zwida & Kutzler, 2022) and may vary between individuals. However, other detrimental effects of gonadectomy are proven and referenced in the current document (Tables 8–10). Concluding statements on detriments of gonadectomy for each condition should not be regarded as final but should be considered in view of corresponding benefits of gonadectomy for the same or connected condition/s. Furthermore, new evidence in this field is continually emerging and may shift the risk/ benefit assessment over time. The effect of age at gonadectomy on incidence of pathological conditions and longevity needs to be addressed in research. Some older studies, veterinary medical and animal hospital associations as well as the American College of Theriogenologists claimed that paediatric gonadectomy (at 6 to 16 weeks of age) is necessary to prevent unwanted pregnancies and to increase adoption rates in shelters by preventing reproductive behaviour (Hoad, 2018; Kustritz, 1999, 2002). Their main argument was that long-term effects of gonadectomy before the age of 16 weeks or until the age of 7 months do not differ significantly (Kustritz, 2002) and even if present, far outweigh the risk of pregnancy. However, the assumption was that shelter dogs and cats generally benefit from gonadectomy. While the quest for sterility as well as arresting reproductive behaviours in shelter dogs are plausible motives in favour of gonadectomy, alternative methods may be an option for that proportion of the adoptee large and giant breed population at increased risk of gonadectomy associated health concerns, particularly when adopted by responsible pet owner.