EARLY AGE NEUTERING IN THE 21st CENTURY – INCREASING ACCEPTANCE
1993: When this article was first researched and written, I discussed early neutering with both the Feline Advisory Bureau (FAB) and Cats Protection League (CPL). FAB were cautiously interested, especially in relation to feral cat control. CPL were opposed, citing health issues and the cost implications for shelters. My own vet would neuter at 12 weeks, but this was the exception rather than the rule. British vets appeared generally opposed to early neutering in spite of US studies.
2008: Early neutering is slowly gaining acceptance in the UK as a tool to address over-population, but is not routinely used by any of the major rescue organisations; this continues to prevent effective tackling of pet overpopulation. Some European countries consider neutering inhumane when it is used to tackle the problem of owner irresponsibility, rather than to treat a disease.
Traditionally, British vets neuter cats between 5 and 6 months of age, the onset of puberty. They may delay neutering even later if the cat is not showing signs of sexual maturity. Most were unwilling to neuter cats under 16 weeks of age, although better nutrition means cats may reach puberty and start breeding as early as 4 months. American animal shelters found, to their distress, that some people who adopted kittens either failed to have them neutered (despite signing a point-of-adoption neutering agreement) while others allowed females to have one or more litters before spaying. Despite insufficient homes for shelter cats and high euthanasia rates, people were still allowing their cats to breed.
The Neuter Before Adoption (NBA) policy in the USA is now vital to rescue organisations to ensure only neutered animals are adopted out. This makes them easier to adopt and avoids the risk of accidental litters or of owners that renege on the neutering clause in the adoption contract. It is also useful to breeders to ensure pet-quality kittens cannot be used for breeding by backyard breeders.
With modern surgical techniques, there is no sound scientific basis for the common recommendation to wait until 6 months for neutering. Vets already recommend that female cats be spayed prior to the first oestrus to reduce risk of mammary tumours. The time of first oestrus is related to the cat's bodyweight and with modern good nutrition, females may go into oestrus at 4-5 months old.
Early neutering is not a cure-all, but it isn't barbaric and it is a useful weapon against overpopulation and irresponsible refuse-to-neuter owners.
BIRTH CONTROL, NOT POPULATION CONTROL
In both the USA and UK, shelter workers often feel they are homing kittens only to see the offspring of those kittens brought into to the shelter a few months later because people failed to abide by neutering agreements. Owners may even insist the shelter takes the kittens because the mother had been obtained from that shelter. Occasionally, shelters unknowingly adopted out apparently pre-pubescent cats that were in the early stages of pregnancy. Some females were already pregnant when presented for spaying and some owners and vets are unwilling to abort the kittens. Lowering the neutering age would prevent these scenarios.
Six telephone surveys in the USA found an average of 85% of owned cats were neutered, but 20% of the owners had allowed female cats to produce 1 or more litters before spaying (Massachusetts Society for the Prevention of Cruelty to Animals (MSPCA) surveys conducted by the Dorr Research Corporation of Boston).
In the USA, the National Council on Pet Population Study and Policy (NCPPSP) was created in 1993. It includes various veterinary and non-veterinary organizations (including the Cat Fanciers Association). The NCPPSP carried out epidemiological studies into pet overpopulation:
1. The National Household Survey B to characterize the population of dog and cat owners and the acquisition, ownership, and disposition (disposal) of these pets
2. The Regional Shelter Survey B to characterize the dogs and cats entering shelters, the population of people relinquishing them, and the reasons for relinquishment
3. The Shelter Statistics Study B (ongoing) to update a list of all shelters and pounds in the USA and collect statistics of the number of animals entering these facilities and their disposition
Greater purchase price of the pet was associated with decreased risk of relinquishment. The majority of relinquished cats in the USA were between 5 months and 3 years of age and 35% had been owned for less than a year. Survey results from 1100 shelters in 1994, and 1041 in 1995 showed approximately 64% of the animals taken to a shelter were destroyed, 10% were reclaimed by the original owner and 24% were adopted. This covered 4.1 million cats and dogs in 1994 and 3.7 million in 1995, but accounts for only one fifth to one quarter of shelters in the USA. In the UK, euthanasia rates are less due to the country's no-kill philosophy.
NEUTERING CONTRACTS – NOT WORTH THE PAPER THEY'RE WRITTEN ON?
US studies found that adopters preferred to adopt cats that had already been neutered. The American Humane Association found that up to 50% of adopters failed comply with signed agreements to neuter their cats. Some owners permitted cats to breed at least once, in spite of signing a neutering contract at the point of adoption. This is in spite of the litigation-culture prevalent in the USA, suggesting that such contracts are unenforceable.
Neutering agreements are notoriously difficult to enforce should owners renege, move house or 'lose' the cat. Whether such agreements in the UK are legally binding (both the owner and a shelter representative are signatories) is unclear since no cases have been taken to court. When asked in 1994, the CPL said the agreement was not an enforceable contract. Even where the owner intends to honour the agreement, some cats breed before reaching 'neutering age'. Some were accidental pregnancies due to early maturation, but many are allowed to breed in the belief that females needed to have one litter before spaying.
Some adopters agree to have the cat neutered but have no intention of doing so and the inability or unwillingness to enforce neutering contracts allows them to get away with it. Shelter staff have faced verbal abuse regarding neutering agreements/contracts. Owners have even refused to reclaim their own cats because the cat was neutered (usually an emergency caesarean/spay) while in shelter care. The US policy of neuter-before-adoption (NBA) takes the choice out of the owner's hands and ensures no adopter can renege on a neutering agreement/contract. Many people acquire cats from sources that don't require neutering and don't do post-adoption checks.
Rescue societies deal with a vast number of cats, on tight budgets, and face a far harder task trying to enforce such agreements. Bodies governing pedigree cats seem no more able to enforce neutering contracts and there is always the concern that adopted pedigree kittens will end up with backyard breeders. Some shelters in the USA decided that this situation needed to be prevented in order to reduce the huge numbers of cats euthanised annually in animal shelters. Since most prospective cat owners preferred to adopt cats that were already neutered, it made sense to neuter kittens before rehoming them.
This policy paid dividends in areas where it was adopted. One Society For the Prevention of Cruelty to Animals (SPCA) in Boston reported a 68% decrease in the number of animals euthanised since the introduction of early neutering. The success of neutering before adoptions meant other shelters took the idea on board. Southern Oregon Human Society had been running an early-spaying scheme since 1974. Memphis Animal Control Shelter conducted a successful 3 month pilot program in 1987. Such shelters felt they were "taking away a problem before the pet owner has one." Those problems would otherwise fill up cat shelter cages.
EARLY NEUTERING FOR FERAL CAT CONTROL
The aim of early neutering is to prevent problems from being born and reduce the number of cats euthanised because they are unwanted. Birth control (birth prevention) is preferable to population control (the killing of healthy cats).
Early neutering proved invaluable to humane societies specialising in humane control of feral cats. Untameable feral kittens could be neutered and immediately returned to their colony instead of being euthanised or kept penned until they reached 6 months of age. The kittens could be returned almost immediately to familiar territory and did not have to contend with the problems endured by unneutered ferals (uncontrolled breeding, fighting, increased risk of infection via fight wounds). The neutered male kittens grew up as non-competitive cats, while males neutered in adulthood had to contend with their suddenly changed status.
Young ferals kept caged until 'neutering age' become stressed and risk losing their place in the colony or territory. The usual answer is to release them and re-trap when they reach the magical age, by which time they may have moved elsewhere or be trap-shy. Shelters cannot hold onto these cats until they reach the mythical 6 month mark. Filling up cages with cats awaiting neutering means turning away homeable cats because there is 'no room at the inn'. Those turned away face possible euthanasia while the ferals are stressed by captivity and are a drain on shelter resources. The logical and humane solution is the neuter them and release them at once.
LEGISLATION TO ENFORCE NEUTERING
In California, as of January 1, 2000, in counties of over 100,000 population, all shelters (public or private) and rescue groups must spay or neuter dogs and cats before adoption or collect a deposit of not less than $40. In addition, the medically delayed animal must be neutered within 30 days. Vets previously reluctant to early neuter had to rethink their policies or risk losing trade to clinics promoting early neuter services.
What about cats acquired from sources other than shelters? In the USA, studies found only 10-15% of newly acquired pets come from shelters; 85-90% of pets are acquired from other sources and are less likely to be neutered. Licensing has been suggested on numerous occasions, with a discount for neutered cats, but is usually accompanied by unpopular restrictions on the number of cats owned by a household.
Vets in the USA were encouraged to promote neutering as part of a package deal along with routine vaccinations. The last kitten vaccination is likely to be 12 weeks with cats and owners are encouraged to have the kitten neutered at the same time. Owners who phone a vet asking when is the best time to neuter are likely to be told "now is the best time" if their kitten is 8 weeks or older.
In Australia, early neutering may be introduced into cat control legislation. Increasingly strict cat-ownership laws attempt to protect native wildlife and it may become illegal to sell or rehome a kitten that has not been neutered (except registered pedigree kittens in breeding programs under the auspices of a cat fancy) and the registration fee for an unneutered cat may be as much as 40 times that for a neutered cat.
There is no intention at the present time to pass legislation in the UK to enforce neutering of all cats not part of a registered breeding programme.
VETERINARY OPINIONS - MIXED VIEWS
Early spay/neuter has been performed on 2 – 3 month old pets prior to the 1950s in the USA. Early sterilisation is normal in farm livestock (W Marvin Mackie, DVM, Animal Birth Control, San Pedro, California). In the UK, castration of male kittens under 6 months was common until the time anaesthesia became compulsory rather than advisory. The limitations of available anaesthetics meant many vets felt it safer to wait until the cats were adult.
In the UK, one vet reported having practised early neutering since 1971 with no detrimental effects. Another neutered over 600 kittens aged between 8 and 20 weeks in 1988-89 and again reported no adverse effects. During the 1990s, when I first looked into this topic to present it to the FAB and CPL, veterinary associations in the UK appeared unwilling to accept information from early neutering studies performed in the US. One veterinarian told me that kittens should only undergo major operations (he considered neutering to be a major operation) in life or death situations.
In 1987, Leo L Lieberman, DVM presented his study "A Case for Neutering Pups and Kittens at Two Months of Age" based on information from the few US vets and shelters that routinely neutered puppies and kittens aged 3 to 5 months and at 8 to 12 weeks. This was negatively received at the time as the conventional wisdom was neuter at or after 6 months. Some even considered it inhumane or barbaric.
Early neutering, as part of neuter-before-adoption, is becoming the norm in the US. The American Veterinary Medical Association in its "Position on Early-Age (Prepubertal) Spay/Neuter of Dogs and Cats", approved by its Executive Board in April, 1999 supported neutering between 8 to 16 weeks old to help reduce the number of unwanted cats and dogs. As with all procedures, the surgery date would depend on the animal's physical condition.
In Britain, while there are still reservations about early neutering, vets are become more open-minded about neutering kittens at 8-12 weeks old, particularly if the kittens are feral and being returned to their colony.
Where did the mythical 6 month mark for spaying and castration come from? It was partly based on the older barbiturate anaesthetics being less safe than modern anaesthetics; a barrier to performing any kind of surgery on kittens or immature cats. In that case, surely cats should have been assessed for anaesthesia based on their size and weight? The magical date of 6 months seems to have come from dogs. It was believed bitches should have one season before spaying and this fallacy may have been extended to cats. With few feline specialist vets, cats were treated as though they were small dogs.
Modern anaesthetic drugs, and better training of veterinary staff, have made surgery much safer for very young or very old animals. Any surgical procedure, on an animal of any age or size, carries a degree of risk. It is unsafe to neuter sickly kittens because of infection/stress. There will always be a few cats, of any age, at high risk from surgery, but they are outnumbered by current euthanasia rates due to feline overpopulation. The vet that told me that kittens should only undergo surgery in life or death situations had lost sight of the fact that overpopulation and rates of euthanasia of healthy cats has made this a life or death situation, particularly for young ferals.
In an article in DVM Magazine, Dr. Johnny Hoskins, DVM, PhD, ACVIM, and author of Veterinary Pediatrics addressed the legitimate list of concerns. He found no evidence in the literature to support claims that early age sterilization increased risk. He stated that the advantages far out-weighed the risks.
STUDIES OF RISKS
Many of the risks are the same as those associated with any early age surgery. There are additional anaesthetic considerations because kittens have greater oxygen consumption than adults. There is a greater risk of hypothermia during anaesthesia because of a kitten's small size, but this presents no difficulty to vets used to operating on comparably sized small pets. There is greater difficulty of intubation due to the smaller size and less rigid structure of kitten's tracheal cartilage. Overall, there is a need to carefully monitor a kitten's body temperature, breathing and heart rate.
Anaesthetic complication rates following early age altering reported in the literature are very low. One study of 96 kittens reported no complications. At the Massachusetts SPCA over 350 6- to 14-week old dogs and cats were neutered without serious complications or mortality. The same was true in the 2 early neutering studies at the University of Florida.
In a study at Texas A & M University, the short-term complications of early neutering vs traditional age neutering were investigated. 1988 cats and dogs from 2 local shelters were neutered at various ages by fourth year veterinary students, in a teaching environment, for the humane organizations. Group I was neutered at less than 12 weeks old; Group II was neutered at 12-24 weeks old; Group III was neutered at older than 24 weeks. Group III animals had more surgical complications (10.8%) and surgery took longer. Group I, the animals younger than 12 weeks, had fewer complications (6.5%) and duration of surgery was found to be shorter. The study concluded that early neutering did not increase morbidity (illness) or mortality (death) during the intra- or postoperative period (7 days after surgery).
Early age sterilizations involves less bleeding (the animals are never in heat), can be performed with a much smaller incision (though it may seem large relative to the kitten's size) and takes less time. There is excellent visualisation of the uterus since there is no body fat, the tissue is very elastic, recovery time and healing is much quicker and there is less patient discomfort. Basically, because the kitten is still growing, its tissues heal faster.
The Journal of American Veterinary Medical Association in 1997 studied 775 cats and 1213 dogs. Significant findings comparing neutering surgery on older and younger animals included:
* decreased surgical time for younger animals
* increased number of minor complications in older animals
* infectious diseases were comparable
* no difference in hypothermia (surgical time shorter for younger patients)
* after 3 years, there was an increased incidence of urinary problems in animals neutered after 24 weeks of age (note: results on this differ in other studies)
Information from various early neuter studies concluded:
* growth is not stunted by early neutering, usually the opposite is true
* urinary function was not affected; urethral pressure profiles showed no statistical difference; the diameter of the urethra in early vs. traditional sterilisations was the same.
* secondary sex characteristics were affected (infantile genitalia in males and females), but did not cause health issues.
* the immune system was not affected
PRACTICAL CONSIDERATIONS FOR VET STAFF
Unlike adult cats, kittens presented for neutering need some food 2-3 hours before surgery because their glycogen reserves must be replenished frequently. They also need feeding about 1 hour after surgery to restore their glycogen levels. Their large surface area and small body size means more care is needed to maintain their body temperature during and after surgery. A kitten's oxygen consumption is 2-3 times greater than adults and their heart rate will be more rapid (200+ beats per minute) as will their respiratory rate (15 to 35 per minute). These elevated rates are normal.
Additional guidelines given to American vets include:
* ensure the kittens have a complete physical exam prior to surgery; ideally, they should be vaccinated and treated for parasites several days before surgery (this is not always possible in a cat rescue situation).
* surgery should be postponed if any abnormalities are found (e.g cryptorchidism).
* kittens must be weighed accurately i.e. to the nearest 100g to calculate drug doses.
* combat hypoglycaemia by withholding food for only 3-4 hours before surgery and feed a small meal within 1 hour of recovery from the anaesthetic. Kittens are normally active and eating within an hour after surgery, but those that take longer to recover or who will not eat after recovery should be given 50% dextrose solution orally.
* before surgery, keep kittens (with their littermates if possible) in a warm, quiet environment to decrease excitement and stress. Keep handling to a minimum so they don't get excited.
* use intra-muscular injections rather than intra-venous injections since IV can be excessively fiddly due to the small veins and the kitten may get stressed and need to be restrained more.
* combat hypothermia during induction (being given anaesthesia) and surgery: keep fur clipping to a minimum; avoid use of alcohol in surgical preps and warm surgical prep solutions. Check the kitten's rectal temperature at the end of the surgery. Continue to keep the kitten warm after surgery and during recovery.
Operating on a small animal is always fiddly. In male kittens the testicles may be undescended. In female kittens, the spaying incision is larger in proportion to size and the tissues more fragile, however, there is less fat in the abdomen. It may be preferable to do a midline (abdominal) spay in kittens than the traditional British flank incision. Operations on cats of any age carry a degree of risk, but a good vet and anaesthetist can overcome these additional concerns when operating on kittens.
PHYSICAL EFFECTS OF EARLY NEUTERING
Reasons cited against early neutering have included: stunted growth, obesity, perivulvar dermatitis, vaginitis, urinary incontinence, malformation of the preputial cavity, increased risk of urethral obstruction, behavioural changes and general risk of surgery on a young animals.
A neutered kitten's growth is not stunted, although males do not develop the characteristic tomcat "jowls". In a parallel scheme for dogs, early-neutered puppies grew into "leggier" adults than those neutered at the more usual age as the sex hormones affects the 'switching off' of bone growth. Though no data has been collected, the same may be true of early-neutered kittens. Fears about stunted growth are therefore unfounded. Legginess and the absence of tomcat jowls is only of concern to exhibitors and breed standards should make provision for neutered cats having a slightly different appearance.
One reason given for delaying the neutering of males until 6 months is to allow the urinary system to become fully grown. Neutered males may be more prone to urinary tract blockages, especially if fed mainly dry cat food. However, advances in cat food formulation to control the acidity of the urine appear to have eliminated this problem. The nutritional needs of early neutered kittens appear to be no different to those of unneutered kittens and it does not necessarily follow that a neutered cat or kitten grows fat and lazy. Neutered adults apparently need fewer calories than unneutered adults but overweight and laziness, often cited as inevitable side-effects of neutering, are most usually due to overfeeding and boredom.
It is hard to assess whether earlier neutering has any additional positive effects on behaviour (other than preventing sex-related behaviours), but no adverse behavioural effects have been noted. In dogs, a positive effect on behaviour was noted.
Studies at the University of Florida looked at the effect of early neutering on skeletal growth, weight gain, food intake, body fat, secondary sex characteristics, behaviour and urethral function Group I was neutered at 7 weeks; Group II at 7 months and Group III (control) were unneutered.
Although not essential to growth, testosterone and oestrogen affect cartilage growth and maturation. Group I and II dogs showed significantly delayed closure of the radial/ulnar growth plates and the long bones of the legs grew longer resulting in taller animals. This did not occur in Group II and II cats. Growth is not stunted by early neutering. Group III (unneutered) cats weighed less and had less body fat than those in Groups I and II. Group I and II cats had similar bodyweights to each other.
Group I male cats had virtually no penile spines but the penis could be fully extended from the preputial cavity indicating complete separation of the balanopreputial fold. This contrasted another study that noted persistent preputial adhesions in 4 out of 10 male cats castrated at 5 months old. The latter study concluded that early castration could result in incomplete separation of the prepuce from the penis and debris could become trapped within the preputial cavity, increasing the risk of urinary tract infections. The vulvas of Group I females remained infantile, but there were no problems with vaginitis or perivulvar dermatitis.
Behavioural development was not adversely affected by neutering at either 7 weeks or 7 months. It did not result in lethargy or inactivity. Neutered cats showed less aggression towards each other and more displays of affection compared to unneutered cats. Sex-dependent behaviour patterns are laid down as the embryo develops and the brain is organised. Exposure to sex hormones after birth only activates or intensifies sex-dependent behaviours. In male cats, this means the ability to spray still exists, but the urge to spray is much reduced or eliminated.
Concerns about urethral obstruction in cats have been used as arguments against early neutering. The University of Florida studies found it had no effect on urethral function. Male cats of all three groups had similar urethral diameter. In another study, the urethral diameter of adult males castrated at 5 months was similar to that of uncastrated males and that castration at 5 months did not predispose neutered toms to urethral obstruction.
Much information has been gathered to support the safety of early neutering as young as 7 weeks old. More information and long-term studies are needed for example into long-term effects on behaviour, however studies of dogs have thus far found a positive effect on behaviour. Since behaviour is a major reason cats and dogs are relinquished to shelters, this is another benefit of early neutering. 12% of cats and dogs relinquished by the owner to shelters were because of behavioural issues.
IDENTIFYING NEUTERED CATS
One drawback for cat rescuers is the added cost of having kittens neutered before adoption and it may take some years before cat-workers reap the benefits of having fewer kittens or pregnant cats come into care. Long term early neutering policies have proven successful abroad and both cat owners and cat workers (especially those dealing with feral cats) may wish to discuss the possibility of early neutering with their own vets.
There needs to be some way of identifying neutered cats so that they do not undergo a second, unnecessary operation should they be found as strays or rehomed without any medical history. Almost all cat-workers have encountered this problem. Ear-tipping is used in feral, but is not acceptable for pets, especially for pedigree cats. Microchipping is the most obvious solution as the cat's neutered/unneutered status is recorded on the database. Early neutering would be beneficial here as it currently costs to have the database record updated; if the kitten was already neutered there would be no need to update the database at 6 months old.
Some feral carers avoid ear-tipping feral cats as it makes them recognisable as unowned cats and a target for cat-haters. Mass microchipping is not feasible for ferals. Tattooing is one option, though tattoos fade and are not visible on dark coloured cats. Freeze-marking (e.g. inside the thigh) while still under anaesthetic is a possibility and is already used to identify horses.
EARLY AGE NEUTERING - PREVENTED BY TRADITION
It is tradition that dictates neutering age. In the light of the increasing feline population and pressure on rescue organisation, the improved modern anaesthetic/surgical techniques, and better nutrition, the customary neutering age needs to be re-assessed and lowered in the UK. To compound the current problem, there remains a major problem of some low-cost neutering clinics only performing castrations; a policy which is short-sighted as kittens need to be prevented at source i.e. through spaying the females.
Although there are those who find the thought of neutering kittens abhorrent or even barbaric, it's worth remembering that some alternatives are even more abhorrent - euthanasia of healthy unwanted cats and regular culling of ferals.
Sterilant drugs are being currently developed and tested. Field testing is now being conducted with a testicular schlerosing agent (Florida) and a zona-pellucida vaccine (Georgia) in dogs and cats. Researchers are working on a sterilant drug to selectively eliminate gonadotrophs in the canine and feline pituitary and cause sterility in both males and females (Colorado).
REFERENCES AND FURTHER READING
American Humane Association, The case for early neutering B a tool for companion animal population control. 1996. Englewood, Colorado.
Aronsohn MG, Fagella AM. Surgical techniques for neutering 6- to 14-week old kittens. J Am Vet Med Assoc 1993;202:53-55.
California Assembly Bill 1856, Vincent, Dogs and Cats: Overpopulation: Spaying and Neutering, Sacramento, CA, 1998.
Crenshaw, W.E., D.V.M., and Carter, C.N., M.S., D.V.M., Ph.D., Should Dogs in Animal Shelters Be Neutered Early?, Veterinary Medicine, Aug., 1995.
Fagella AM, Aronsohn MG. Evaluation of anesthetic protocols for neutering 6- to 14-week old kittens. J Am Vet Med Assoc 1993;202:56-62.
Herron MA. A potential consequence of prepubertal feline castration. Feline Pract 1971;1:17-19.
Herron MA. The effects of prepubertal castration on the penile urethra of the cat. J Am Vet Med Assoc. 1972;160:208-211.
Hoskins, Johnny, D.V.M., Ph.D., Early-age Spay/Neuter Advantages Outweigh Risks, DVM Magazine, Nov. 1966.
Howe, Lisa M., D.V.M., Ph.D., Short-term Results and Complications of Prepubertal Gonadectomy in Cats and Dogs, JAVMA, Vol. 211:57-62, 1997.
Howe LM: Prepuberal gonadectomy in dogs and cats Part I. Compend Contin Educ Pract Vet 1999;21:103-111.
Howe LM: Prepuberal gonadectomy in dogs and cats Part II. Compend Contin Educ Pract Vet 1999;21:197-201.
Lieberman, Leo, D.V.M., A Case for Neutering Pups and Kittens at Two Months of Age, JAVMA, Vol. 191:518-521, 1987.
Olson P, Moulton C, Nett T, Salman M: Pet overpopulation: a challenge for companion animal veterinarians in the 1990s; J Am Vet Med Assoc 1991;198:1151-1152
Root MV: The effect of prepuberal and postpuberal gonadectomy on the general health and development of obesity in the male and female domestic cat, PhD Thesis, University of Minnesota, Saint Paul, Minnesota, 1995.
Salman M, New J, Scarlett J, Kass P, Ruch-Gallie R, Hetts S: Human and animal factors related to the relinquishment of dogs and cats in 12 selected animal shelters in the United States, Journal of Applied Animal Welfare Science 1998;1(3):207-226
Salmeri KR, Bloomberg MS, Scruggs SL, Shille V: Gonadectomy in immature dogs: effects on skeletal, physical, and behavioral development, J Am Vet Med Assoc 1991;198:1193-1203.
Scarlett J, Salman M, New J, Kass P: Reasons for relinquishment of companion animals in U.S. animal shelters: selected health and personal issues, Journal of Applied An Welfare Sci 1999; 2(1):41-57.
Stubbs PW, Salmeri KR, Bloomberg MS. Early neutering of the dog and cat, In Bonagura JD, Kirk RW eds. Current Veterinary Therapy X. Philadelphia: WB Saunders Co 1995;1037-1039.
Texas House Bill 948 and Senate Bill 1259, Dog and Cat Sterilization Act, Austin, TX, 1991.
Theran P. Early-age neutering of dogs and cats. J Am Vet Med Assoc 1993;202:914-917.
Zawistowski S, Morris J, Salman M, Ruch-Gallie R: Population dynamics, overpopulation, and the welfare of companion animals: new insights on old and new data, JappAnWelfareSci 1998;1(3):193-206.