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Reprod Dom Anim 47 (Suppl. 4), 214–222 (2012); doi: 10.1111/j.1439-0531.2012.02078.

x
ISSN 0936-6768

Effects of Surgical Sterilization on Canine and Feline Health and on Society


MV Root Kustritz
University of Minnesota College of Veterinary Medicine, St. Paul, MN, USA

Contents as gonadectomy at 8–16 weeks of age (Root Kustritz


Surgical sterilization of dogs and cats is a well-accepted 1999), and gonadectomy at any age after 16 weeks.
measure for population control in some countries, but is
considered unethical as an elective surgery in other countries.
This is a review of what is known regarding positive and Surgical and Anaesthetic Risk
negative effects of gonadectomy surgery on individual animals
and on societal management of unowned dog and cat General recommendations for anaesthesia are to mini-
populations. mize anaesthetic dose and time under anaesthesia.
A series of excellent studies evaluating morbidity and
mortality of dogs and cats identified general risk factors
Introduction and some specific risk factors that are easily countered
Elective gonadectomy, castration in males and either (Brodbelt et al. 2008; Brodbelt 2009, 2010). Cats were at
ovariectomy (OV) or ovariohysterectomy (OHE) in greater risk of morbidity or mortality than dogs because
females, is the most common small animal surgery of difficulties with intubation and prevalence of inap-
performed in some countries and is unethical or illegal in parent cardiomyopathy. If 6 months to 5 years of age is
other countries (Salmeri et al. 1991b; Gunzel-Apel 1998; set as a baseline, all other ages were at greater risk, with
Greenfield et al. 2004). There is no question that we a slight risk for younger animals and much greater risk
alter animals when we perform gonadectomy. This is a for geriatric animals. Hypothermia greatly increased
review of the specific changes associated with gonadec- risk of morbidity or mortality during an anaesthetic
tomy in dogs and cats and the evidence we have for episode. Profound hypothermia may develop as early as
cause-and-effect. Thorough reviews of the literature during induction and surgery prep. Body temperature
have been published (Root Kustritz 2007, 2010; Reichler should be monitored regularly and external sources of
2009). heat applied as needed. All animals, especially very
Some recognized reasons for the promotion of young animals, should be weighed to ensure overdosing
gonadectomy and some stated concerns are societal in of drugs does not occur. Intra-operative monitoring
nature, some refer to populations of animals, and some shown to be of great benefit included recording of body
are pertinent to health of individual animals. Veterinar- temperature, pain assessment and use of pulse oximetry.
ians are encouraged to help clients and those who write Concerns about anaesthesia are most commonly
public policy to understand which aspect is being voiced when considering gonadectomy of very young
addressed when specific recommendations for gonadec- animals. Concerns specific to animals <4–5 months of
tomy are being made. There also is great variability in age include altered ability to metabolize and excrete
number of studies supporting some of the findings anaesthetic agents and pain medication because of
described, and veterinarians are encouraged to be aware immature renal and hepatic function, decreased protein
of the amount of evidence to support any given claim. binding of medications in the bloodstream, predisposi-
Finally, breed predispositions exist for some of the tion to hypoglycaemia because of decreased gluconeo-
concerns described and must be included in decisions genesis and minimal glycogen stores in skeletal muscle,
about suitability of gonadectomy in a given animal. and decreased ability to maintain body temperature
Advantages of gonadectomy include decrease in (Root Kustritz 1999). Puppies and kittens <10 weeks of
reproductive tract disease, including pyometra and age should be fasted for no more than 3–4 h before
mammary neoplasia in bitches and queens, and testic- surgery and older animals fasted for no more than 8 h
ular neoplasia and prostate disease in male dogs. Other (Faggella and Aronsohn 1993, 1994). All surgical
advantages include: decrease in pregnancy and parturi- preparation fluids should be warmed and clipping of
tion-related disorders including metritis, mastitis and hair kept to a minimum. In studies of 98 puppies and 98
dystocia; decrease in hormone-associated disorders such kittens presented for elective gonadectomy, incidence of
as vaginal prolapse in bitches and mammary hypertro- anaesthetic complications was 0% for both groups
phy in queens; and decrease in undesirable sexual (Aronsohn and Faggella 1993; Faggella and Aronsohn
behaviours (Romagnoli 2008). Disadvantages of gonad- 1994). When looking at anaesthetic complications for
ectomy include surgical and anaesthetic complications, gonadectomy at all ages, cardiac dysrhythmias, gastric
increased risk of neoplasia of various organ systems, dilation and drug overdosage were identified as the most
increased incidence of some musculoskeletal and endo- common anaesthetic complications (Howe 1997).
crinologic disorders, obesity and urinary incontinence in Intra-operative and post-surgical complications are
bitches. All of these will be described in more detail. reported usually to be mild and self-limiting. Reported
This discussion incorporates early spay-neuter, defined incidence of surgical complications is 6.1–27% in bitches

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Small Animal Gonadectomy 215

and dogs and 2.6–33% in queens and toms (Pollari et al. females are more likely to be presented for gonadectomy
1996; Romagnoli 2008). The wide range reported most than are males in the United States (Manning and
likely is due to differing definitions of ‘complications’ in Rowan 1992; Alexander and Shane 1994; Mahlow 1999;
the papers cited. Most post-surgical complications are New et al. 2000).
reported to be mild, with most requiring only nursing Many pet owners have limited knowledge about
care and not veterinary intervention. Incidence of normal reproduction in dogs and cats. In the PetSmart
complications is lower in young animals than in older survey (PetSmart Charities A&U Barriers 2002), 13% of
animals, with one study identifying fewer complications dogs and 19% of cats purchased within the previous
in animals gonadectomized prepuberally and another year had borne litters, with over 50% of those
study identifying 2 years of age as a cut-off (Faggella unplanned. In one survey of dog- and cat-owning
and Aronsohn 1994; Pollari et al. 1996; Howe 1997; households, 56% of 154 canine litters and 68% of 317
Romagnoli 2008). feline litters were unplanned, with the majority of those
Reported short-term complications of OV or OHE owners reporting that they did not know the female had
include haemorrhage of the ovarian or uterine pedicle, been in heat (New et al. 2004). Because of this, many
passage of bloody vulvar discharge, onset of pseudocy- humane organizations in the United States are working
esis, dehiscence or infection of the incision and, very toward gonadectomy of all unowned animals prior to
rarely, peritonitis or evisceration (Romagnoli 2008). adoption. Other measures that will be required to stem
Long-term complications of OV or OHE include ovar- pet overpopulation include education of pet owners and
ian remnant syndrome, ligation of a ureter with increased availability of affordable, safe, readily pro-
subsequent hydroureter and ipsilateral renal dysfunc- vided non-surgical contraceptive or sterilization options.
tion, granuloma of the uterine or ovarian pedicle, and
disease of the uterine stump (Romagnoli 2008).
Reported incidence of complications is not correlated Behaviour
with age of the animal, ability of the surgeon or presence Many people request gonadectomy because they are
of reproductive disease (Miller 1995; Romagnoli 2008). unwilling or unable to tolerate normal breeding behav-
Complications associated with haemorrhage may be iours in their animals. Male cat normal breeding
more common when bitches and queens are spayed behaviour, which is aggressive and includes urine
while in oestrus under the influence of oestrogen, and spraying, is incompatible with life as a house pet (Root
increased incidence of complications is associated with Kustritz 1996). Male dogs may mount other animals,
increased surgery time and increased body weight of the people or inanimate objects and may urine mark.
patient (Howe 1997; Howe et al. 2000, 2001; Burrow Bitches and queens may show altered behaviours with
et al. 2005). oestrus, including increases in some forms of aggression,
and bitches may show nesting and mothering behav-
iours and lactation with false pregnancy.
Population Control Gonadectomy, especially castration, is a commonly
Pet overpopulation may occur due to attitudes of the recommended treatment for behavioural problems in
animal owning public permitting irresponsible breeding dogs including aggression. Not all behaviours are
or ready surrender of animals or due to free-roaming or altered by gonadectomy. Those most commonly affected
feral dogs and cats. Although it has been reported that are sexually dimorphic behaviours, defined as behav-
82% of cats and 64% of dogs in the US have undergone iours that vary between genders, and are likely to be at
gonadectomy (Trevejo et al. 2011), a recent study least partially mediated by sex hormones.
reported that only 52% of people who had purchased In male cats, the undesirable behaviours decreased to
a dog or cat within the last year had had that animal the greatest extent by castration are sexual behaviours,
gonadectomized (PetSmart Charities 2002). In the roaming and urine spraying (Hart 1973, 1979; Hart and
United States, millions of dogs and cats with no owner Barrett 1973). In male dogs, the undesirable behaviours
or guardian are euthanized annually (Nassar et al. 1992; decreased to the greatest extent by castration are
National Council on Pet Population Study and Policy mounting, urine marking and roaming (Hart 1979;
1994). Intact animals are more likely to be surrendered Neilson et al. 1997). Likelihood of response to castra-
to humane organizations (Patronek et al. 1996a,b; New tion is not associated with age at castration or duration
et al. 2000; Mondelli et al. 2004). Spay-neuter contracts of the behaviour prior to castration in male dogs or cats
are sent out with animals adopted while still intact but (Hart 1973; Hart and Barrett 1973; Hopkins et al. 1976;
compliance with these contracts, even with low-cost Neilson et al. 1997). The hormonal basis of these
surgical options readily available, is <60%, permitting behaviours is not always clear. Oestrogen stimulates
intact animals to re-populate those shelters from which arousal in females but also is associated with release of
they were adopted (Alexander and Shane 1994; oxytocin and opioids, which may have an anti-anxiety
Patronek et al. 1996a; New et al. 2000; Mondelli et al. effect (Mong and Pfaff 2003; Root Kustritz 2005).
2004). Lack of compliance with recommendations for Concerns vary regarding trainability of dogs after
surgery is multifactorial. Cultural and personal factors gonadectomy, with some suggesting that dogs will be
include religious affiliation, ethnic background, intended more attentive after gonadectomy as they are less likely
working life of the animal, urban or rural location of the to show behaviours related to copulation, such as
household and literacy status (Manning and Rowan roaming. It has been demonstrated in rats that attention
1992; Mahlow 1999; Eze and Eze 2002). Cats are more is not affected by rising or falling concentrations of
likely to be spayed or castrated than are dogs, and testosterone, but that acuity of spatial working memory

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216 MV Root Kustritz

is testosterone dependent (Johnson and Burk 2006; malignant tumours (Verstegen and Onclin 2003b;
Kritzer et al. 2007). Reichler 2009). Siamese cats and Japanese domestic
Aggression may or may not be affected by gonadec- breed cats are reported to be at greater risk of
tomy (Hart and Eckstein 1997; Neilson et al. 1997; developing mammary neoplasia, as are the boxer,
Duffy and Serpell 2006). A breed-specific increase in Brittany spaniel, cocker spaniel, dachshund, English
owner-directed aggression and in degree of reactivity setter, English springer spaniel, German shepherd dog,
was reported in both males and females after gonadec- Maltese, miniature poodle, pointer, toy poodle and
tomy and in bitches after OHE; in one study, this Yorkshire terrier (Dorn et al. 1968b; Hayes et al. 1981;
increase in aggression was most common in bitches Sorenmo 2003; Verstegen and Onclin 2003a). Cause-
spayed at <1 year of age who were showing aggression and-effect relationship between gonadectomy and de-
prior to surgery (Wright and Nesselrote 1987; O’Farrell creased incidence of mammary neoplasia is not clear. In
and Peachey 1990; Reisner et al. 2005; Duffy and Serpell human medicine, oestrogen is implicated in mammary
2006). The form of aggression best controlled by neoplasia. Oestrogen receptors have been identified in
castration in both male dogs and cats is intermale neoplastic mammary tissue of dogs and cats, with fewer
aggression (Hart 1979; Borchelt and Voith 1987). Other oestrogen receptors present as tissue becomes more
forms of aggression in cats include predation, play, fear anaplastic (Hamilton et al. 1977; Donnay et al. 1995;
or defence, territorial and redirected aggression; these Verstegen and Onclin 2003b). One study suggested that
are much less likely to be decreased by castration mammary neoplasia may be more common in bitches
(Borchelt 1983). Other forms of aggression in dogs that exhibited more than three episodes of overt false
include predation, fear or defence, dominance, pro- pregnancy in their lives, again supporting a role for
tectiveness, punishment and pain-related aggression hormonal stimulation of mammary tissue as a factor
(Borchelt 1983). associated with neoplastic transformation of that tissue
In one study of older male dogs with mild cognitive (Verstegen and Onclin 2003b).
impairment, those that were castrated were more likely
to progress to severe cognitive impairment than were
those left intact (Hart 2001). Androgen deprivation is Genitourinary
associated increased deposition of amyloid in brains of Prostate
humans and rodents and with decreased number of Prostatic neoplasia is uncommon in dogs, with reported
synaptic connections in brains of rodents and primates incidence of 0.2–0.6% (Bell et al. 1991; Teske et al.
(Janowsky 2006). However, studies directly evaluating 2002). Prostatic neoplasia in dogs virtually always is
the brain of aged dogs showed that among beagles aged malignant; both adenocarcinoma and transitional cell
approximately 10 years, intact dogs had more DNA carcinoma are described. Several studies have docu-
damage in the brain than did castrated dogs (Waters mented increased incidence of prostatic cancer in
et al. 2000). castrated dogs compared with intact dogs, with reported
increased risk ranging from 2.4 to 4.3 times (Obradovich
Neoplasia et al. 1987; Bell et al. 1991; Teske et al. 2002; Sorenmo
et al. 2003). Prostatic neoplasia is extremely uncommon
Mammary in cats, but in one case series of eight cats with prostatic
Mammary neoplasia is very common in dogs and cats, neoplasia, seven were castrated (Hawe 1983; Carpenter
with reported incidence of 3.4 and 2.5%, respectively, in et al. 1987; Hubbard et al. 1990; Caney et al. 1998;
the United States (Fidler and Brodey 1967; Dorn et al. LeRoy and Lech 2004). No breed predisposition is
1968a; Moe 2001; Richards et al. 2001; Verstegen and reported. Cause-and-effect relationship is not clear.
Onclin 2003a). In dogs, approximately half of all
mammary tumours are malignant; in cats, >90% of
mammary tumours are malignant (Cotchin 1951; Dorn Urinary bladder
et al. 1968a; Moulton et al. 1970; Hampe and Misdorp Incidence of transitional cell carcinoma is at most 1% of
1974; Hayes et al. 1981; Brodey et al. 1983). Despite the malignant tumours (Poirier et al. 2004). Incidence of
fact that many mammary tumours in bitches are benign, transitional cell carcinoma of the urinary bladder and
it was reported in one U.S. study that 59.7% of bitches urethra of female dogs and urethra of male dogs is
with mammary neoplasia were euthanized at the time of reported to be increased after gonadectomy, with
diagnosis (Misdorp and Hart 1979). It has been well increased risk of 2–4 times (Norris et al. 1992; Knapp
demonstrated that incidence of mammary cancer when et al. 2000). This has not been reported in cats. Dog
aged is greatly decreased in female dogs and cats by breeds at increased risk are the Airedale terrier, beagle,
ovariectomy, especially if performed before the first heat collie, Scottish terrier, Shetland sheepdog, West High-
cycle. Intact dogs and cats are seven times more likely land white terrier and wire-haired fox terrier (Ru et al.
than are spayed dogs and cats to develop mammary 1998). Cause-and-effect relationship is not clear.
neoplasia when aged (Dorn et al. 1968b). Risk for
bitches has been defined as 0.5% before the first oestrus,
8% after one oestrus, and 26% after two or more Testicular
oestrous cycles (Schneider et al. 1969). Some sparing Testicular neoplasia is very common in aged male dogs,
effect may be present with OHE up to 9 years of age, with reported incidence of 0.9% (Hahn et al. 1992). The
although that effect may be greater for benign than for three tumour types most commonly reported are Sertoli

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Small Animal Gonadectomy 217

cell tumours, seminomas and Leydig (interstitial) cell diagnosed with hip dysplasia by a veterinarian. In one
tumours. Testicular neoplasia is uncommon in male study, it was demonstrated that neutered boxers were
cats. Castration is curative. 1.5 times as likely as intact boxers to develop hip
dysplasia; that study did not figure in possible contri-
bution of excess body weight (VanHagen et al. 2005).
Haematologic Hip dysplasia has a strong genetic component. Breeds at
Overall incidence of haemangiosarcoma in dogs is 0.2% risk include the Chesapeake Bay retriever, English
and in cats is 0.03% (Reichler 2009). Incidence of both setter, German shepherd dog, golden retriever, Labra-
splenic- and heart-based haemangiosarcoma are dor retriever, Samoyed and St. Bernard (Priester and
reported to be increased in dogs after gonadectomy; in Mulvihill 1972). A hypothesis for cause-and-effect is
bitches, splenic haemangiosarcoma risk after OHE asymmetry in closure of growth plates causing deformity
increases by a factor of 2.2 and cardiac haemangiosar- and laxity of the hip joint with subsequent arthritis.
coma risk increases by a factor of 5, and in male dogs,
overall risk of haemangiosarcoma increases by a factor
2.4 after castration (Prymak et al. 1988; Ware and Anterior Cruciate Ligament (ACL) Rupture
Hopper 1999). This has not been reported in cats. Rupture of the anterior or cranial cruciate ligament is
Breeds at increased risk are the boxer, English setter, more common after gonadectomy than in intact dogs
German shepherd dog, golden retriever, Great Dane, (Whitehair et al. 1993; Duval et al. 1999; Slauterbeck
Labrador retriever, pointer, poodle and Siberian husky et al. 2004). Breeds at risk for rupture of the ACL
(Smith 2003). Cause-and-effect relationship is not clear. include the Akita, American Staffordshire terrier, Ches-
apeake Bay retriever, German shepherd dog, golden
retriever, Labrador retriever, mastiff, Neopolitan mas-
Orthopaedic tiff, Newfoundland, poodle, rottweiler and St. Bernard
Osteosarcoma is an uncommon tumour with overall (Duval et al. 1999; Harasen 2003). Other risk factors
incidence of 0.2% (Root Kustritz 2007). Incidence is include obesity and abnormal angulation of the stifle
increased with gonadectomy, by a factor of 1.3–2 (Ragetly et al. 2011). One could argue that increased
(Priester and McKay 1980; Ru et al. 1998). Breeds at risk of ACL injury after gonadectomy is because of
increased risk are the Doberman pinscher, Great Dane, decreased athleticism and obesity in gonadectomized
Irish setter, Irish wolfhound, rottweiler and St. Bernard animals but the trend stands even in studies that
(Ru et al. 1998; Chun and DeLorimer 2003). Other risk statistically compensated for these effects in dogs. Joint
factors for osteosarcoma include increasing age and laxity may differ under varying hormonal stimuli,
increasing body weight (Ru et al. 1998; Cooley et al. suggesting one possible cause-and-effect mechanism.
2002). Cause-and-effect relationship is not clear. Another hypothesis is increasing stifle angulation with
asymmetry of growth plate closure in the femur and
tibia.
Dermatologic
Increase incidence of cutaneous mast cells tumours has
been reported in spayed female dogs compared with Genitourinary Disease
intact female dogs (White et al. 2011). Cause-and-effect Urinary incontinence
relationship is not clear. Urethral sphincter mechanism incompetence, formerly
called oestrogen-responsive urinary incontinence, is
leakage of urine from female dogs, usually as they lie
Musculoskeletal Disease relaxed. A similar clinical manifestation is seen in
Growth plate closure castrated male dogs but is less common than in females.
Growth plate closure in long bones is mediated by Urethral sphincter mechanism incompetence is much
gonadal hormones. It has been well demonstrated that more common in spayed than in intact female dogs with
growth plate closure is delayed in dogs and cats spayed reported incidence of 4.9–20.0% (Arnold 1997; Stocklin-
or castrated prepuberally (May et al. 1991; Salmeri et al. Gautschi et al. 2001; Angioletti et al. 2004; Spain et al.
1991a; Houlton and McGlennon 1992; Root et al. 2004b). One study identified 3 months of age as the age
1996c; Stubbs et al. 1996). Significance of this delay is before which OHE most greatly contributed to eventual
not clear. Increased incidence of growth plate fractures clinical manifestation of urinary incontinence (Spain
in cats spayed prepuberally was demonstrated in one et al. 2004b). Other contributing factors include higher
study; obesity may have contributed to the disorder in lean body weight (>20 kg); breed, with breeds at
those cats (McNicholas et al. 2002). increased risk including the boxer, Doberman pinscher,
giant schnauzer, Irish setter, old English sheepdog,
rottweiler, springer spaniel and Weimeraner; and ure-
Hip dysplasia thral length or resting position of the urinary bladder
One large study evaluating incidence of various disor- creating a pressure differential across the length of the
ders in dogs spayed at various ages in a humane urethra (Gregory et al. 1992, 1999; Holt and Thursfield
organization reported increased incidence of hip dys- 1993; Arnold 1997; Atalan et al. 1998; Holt 2004).
plasia in dogs spayed when young (Spain et al. 2004b). Urethral sphincter tone is mediated by the sympathetic
It was not clear in that study that all dogs were nervous system and function may be potentiated by

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218 MV Root Kustritz

oestrogen. Cause-and-effect for urinary incontinence of 100 proliferative adrenal lesions in ferrets, almost
after OHE has not been identified. Hypothesized causes 30% were from intact jills (Olson 1997). There have
include physical factors, alteration in gonadotropin been no reports of increased adrenal disease in cat
secretion after OHE, and change in muscle tone populations secondary to gonadectomy, and any impact
(Ponglowhapan et al. 2008a,b, 2011). on dog populations has not been reported.

Pyometra Diabetes Mellitus in Cats


Incidence of pyometra in dogs left intact is high, at 24– Cats have a 2- to 9-fold increased risk of developing of
25% by 10 years of age (Hagman et al. 2011). Pyometra diabetes mellitus after neutering, with Burmese cats
also occurs in cats, even in those queens not known to reported to be especially susceptible (Panciera et al.
have been induced to ovulate (Potter et al. 1991). 1990; Rand et al. 1997; McCann et al. 2007; Prahl et al.
Although OHE is considered curative, morbidity is 2007). One hypothesis is that this is because of decreased
relatively high and mortality with surgical management insulin sensitivity (Hoenig and Ferguson 2002; Kanchuk
is 0–17% in dogs and 8% in cats (Johnston et al. et al. 2002). Obesity also is associated with decreased
2001a,b). insulin sensitivity and may be a confounding factor.

Benign prostatic hypertrophy Hypothyroidism


Benign prostatic hyperplasia is very common in aged Risk of hypothyroidism in dogs was reported to be
dogs, with reported incidence of 50% by 2.4 years of increased with neutering in some studies (Milne and
age and 75–80% in dogs aged 6 years or more (Zirkin Hayes 1981; Panciera 1994) and not to be associated
and Strandberg 1984; Berry et al. 1986; Lowseth et al. with neutering in other studies (Dixon and Mooney
1990). BPH is not reported in cats. Castration is 1999a; Dixon et al. 1999b) Gonadectomy is associated
curative. with persistent increase in blood concentrations of
gonadotropins (Lofstedt and VanLeeuwen 2002), many
of which share molecular configuration with TSH in
Disorders of the lower urinary tract protein subunit chains and in glycosylation. It can be
Multiple studies have failed to show any correlation hypothesized that persistent high concentrations of
between castration, urethral diameter, and incidence of gonadotropins lead to altered formation or glycosyla-
urinary tract obstruction in male cats (Foster 1967; tion of TSH, and subsequent change in thyroid function.
Herron 1972; Duch et al. 1978; Root et al. 1996a; Spain However, one study showed no change in resting serum
et al. 2004a). The balanopreputial fold, a tissue that TSH or thyroxin concentrations, or alterations in
connects the penile and preputial mucosa in early stimulus testing with thyroid releasing hormone when
embryonic development, is androgen dependent. The comparing castrated to intact male beagles (Gunzel-
fold undergoes dissolution as serum testosterone con- Apel et al. 2009).
centrations rise. In male cats, it has been demonstrated
that at 12–22 months of age, 0–100% of cats castrated
before 7 weeks of age could extrude their penis from the Metabolic Disorders
prepuce, whereas 40–100% of cats castrated at 7 months Obesity
of age were capable of complete penile extrusion In retrospective studies, up to 2.8% of the canine
(Herron 1972; Root et al. 1996a; Stubbs et al. 1996). population has been demonstrated to be obese, with up
Clinical significance of inability to extrude the penis is to 50% of gonadectomized dogs and cats designated as
unclear. Similarly, dogs castrated at <7 weeks of age obese (Mason 1970; David and Rajendran 1980).
had smaller penile diameter, decreased size and radio- Increase in indiscrimate appetite was reported in
density of the os penis, and immature preputial devel- spayed bitches in one study but in another study of
opment compared with male dogs castrated at 7 months spayed and castrated dogs, no change in food intake or
of age or left intact (Salmeri et al. 1991a). Again, clinical depth of back fat was reported by 15 months of age
significance is unclear. (O’Farrell and Peachey 1990; Salmeri et al. 1991a).
Risk factors other than gonadectomy include housing
Endocrinologic Disease of the animal; increasing age; ownership by an over-
weight person or a person over 40 years of age; and
Adrenal Disease breed, with the beagle, cairn terrier, cavalier King
In ferrets in the United States, most of which are spayed Charles spaniel, cocker spaniel, dachshund and Labra-
or castrated prepuberally, there is increased incidence of dor retriever among those breeds at greatest risk
adrenocortical tumours and nodular adrenal hyperpla- (Mason 1970; Edney and Smith 1986; Crane 1991;
sia (Lawrence et al. 1993; Rosenthal et al. 1993). The Sloth 1992; Colliard et al. 2006). In cats, castration and
hypothesis is that lack of down-regulation of sex OHE are associated with increased risk of obesity, with
steroids or increased blood concentrations of gonado- one paper describing a 3.4-fold risk factor (Fettman
tropins cause adrenal gland hyperplasia and neoplastic et al. 1997; Kanchuk et al. 2002; Nguyen et al. 2004).
transformation (Babon et al. 1996; Schoemaker et al. Gonadectomized cats have increased body weight,
2002; Johnson-Delaney 2006). However, in one survey increased body mass index, increased depth of the

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Small Animal Gonadectomy 219

falciform fat pad, decreased activity and decreased One study evaluating lifespan in a group of exception-
metabolic rate (Root 1995; Root et al. 1996b; Stubbs ally long-lived rottweilers showed increased lifespan if left
et al. 1996; Fettman et al. 1997). Castrated cats also intact (Waters et al. 2009). This could be due to specific
have an increase in serum concentrations of insulin genetic factors in this population of dogs, to hormonal
growth factor I, prolactin and leptin, all of which are changes not yet identified, or to a lower incidence of
associated with metabolic rate and fat metabolism obesity in this group; obesity itself has a negative effect on
(Martin et al. 2006). life expectancy (Greer et al. 2007).
It has been suggested that studies that separate dogs
into intact or neutered categories at the time of disease
Lifespan onset or death create an artificial black-or-white eval-
Most studies evaluating lifespan suggest that neutered uation of data regarding benefits and detriments of
animals live longer than intact animals (Kraft 1998; gonadectomy (Waters et al. 2011). Future studies that
Greer et al. 2007). Increased lifespan in castrated male will guide this debate include those defining lifelong
dogs may be due to a decrease in risky sexually effects of exposure to gonadal hormones or better
dimorphic behaviours such as roaming, or to increased relating time of neuter to onset of disease.
owner investment in the animal’s care (Bronson 1982;
Michell 1999; Moore et al. 2001). Castrated cats have
reduced mortality compared with intact cats (Kalz Conflicts of interest
2001). None of the authors have any conflicts of interest to declare.

References Brodbelt DC, 2010: Feline anesthetic deaths health, hypothyroidism and non-thyroidal
in veterinary practice. Top Comp Anim illness. Res Vet Sci 66, 243–246.
Alexander SA, Shane SM, 1994: Character- Med 25, 189–194. Dixon RM, Reid SW, Mooney CT, 1999b:
istics of animals adopted from an animal Brodbelt DC, Pfeiffer DU, Young LE, Epidemiological, clinical haematological
control center whose owners complied Wood JL, 2008: Results of the confiden- and biochemical characteristics of canine
with a spaying ⁄ neutering program. J Am tial enquiry into perioperative small ani- hypothyroidism. Vet Rec 145, 481–487.
Vet Med Assoc 205, 472–476. mal fatalities regarding risk factors for Donnay I, Rauis J, Devleeshouwer N,
Angioletti A, DeFrancesco I, Vergottini M, anesthetic-related death in dogs. J Amer- Wouters-Ballman P, Leclercq G, Verste-
Battocchio ML, 2004: Urinary inconti- Vet Med Assoc 233, 1096–1104. gen J, 1995: Comparison of estrogen and
nence after spaying in the bitch: incidence Brodey RS, Goldschmidt MH, Roszel JR, progesterone receptor expression in nor-
and oestrogen therapy. Vet Res Commun 1983: Canine mammary gland neoplasms. mal and tumor mammary tissues from
28(Suppl 1), 153–155. J Amer Anim Hosp Assoc 19, 61–90. dogs. Amer J Vet Res 56, 1188–1194.
Arnold S, 1997: Urinary incontinence in Bronson RT, 1982: Variation in age at death Dorn CR, Taylor DON, Frye FL, Hibbard
castrated bitches. Part I. Significance, of dogs of different sexes and breeds. HH, 1968a: Survey of animal neoplasms
clinical aspects and etiopathogenesis. Amer J Vet Res 43, 2057–2059. in Alameda and Contra Costa Counties,
Schweiz Arch Tierheilkd 139, 271–276. Burrow B, Batchelor D, Cripps P, 2005: California. I. Methodology and descrip-
Aronsohn MG, Faggella AM, 1993: Surgical Complications observed during and after tion of cases. J Natl Canc Inst 40, 295–
techniques for neutering 6 to 14-week-old ovariohysterectomy of 142 bitches at a 305.
kittens. J Amer Vet Med Assoc 202, veterinary teaching hospital. Vet Rec 157, Dorn CR, Taylor DON, Schneider R,
53–55. 829–833. Hibbard HH, Klauber MR, 1968b: Sur-
Atalan G, Holt PE, Barr FJ, 1998: Ultraso- Caney SM, Holt PE, Day MJ, Rudorf H, vey of animal neoplasms in Alameda and
nographic assessment of bladder neck Gruffydd-Jones TJ, 1998: Prostatic carci- Contra Costa Counties, California. II.
mobility in continent bitches and bitches noma in two cats. J Sm Anim Prac 39, Cancer morbidity in dogs and cats from
with urinary incontinence attributable to 140–143. Alameda County. J Natl Canc Inst 40,
urethral sphincter mechanism incompe- Carpenter J, Andrews L, Holsworth J, 1987: 307–318.
tence. Amer J Vet Res 59, 673–679. Tumors and tumor-like lesions. In: Duch DS, Chow FC, Hamar DW, Lewis
Babon JE, Li X, Lei ZM, Sanfilippo JS, Holzworth J (ed), Diseases of the Cat. LD, 1978: The effect of castration and
Yussman MA, Rao CV, 1996: Novel WB Saunders, Philadelphia PA, pp. 406– body weight on the occurrence of the
presence of luteinising hormone ⁄ chori- 411. feline urological syndrome. Fel Prac 8,
onic gonadotropin receptors in human Chun R, DeLorimer L-P, 2003: Update on 35–40.
adrenal glands. J Clin Endocrinol Metab the biology and management of canine Duffy DL, Serpell JA, 2006: Non-reproduc-
81, 2397–2400. osteosarcoma. Vet Clin NA 33, 491–516. tive effects of spaying and neutering on
Bell FW, Klausner JS, Hayden DW, Feeney Colliard L, Ancel J, Benet JJ, Paragon BM, behavior in dogs. Proceedings, Sympo-
DA, Johnston SD, 1991: Clinical and Blanchard G, 2006: Risk factors for sium on non-surgical contraceptive meth-
pathologic features of prostatic adenocar- obesity in dogs in France. J Nutr 136, ods for pet population control, Alexandra
cinoma in sexually intact and castrated 1951S–1954S. VA.
dogs: 31 cases (1970–1987). J Amer Vet Cooley DM, Beranek BC, Schlittler DL, Duval JM, Budsberg SC, Flo GL,
Med Assoc 199, 1623–1630. Glickman NW, Glickman LT, Waters DJ, Sammarco JL, 1999: Breed, sex, and body
Berry SJ, Strandberg JD, Saunders WJ, 2002: Endogenous gonadal hormone weight as risk factors for rupture of the
Coffey DS, 1986: Development of canine exposure and bone sarcoma risk. Canc cranial cruciate ligament in young dogs. J
benign prostatic hyperplasia with age. Epidemiol Biomark Prev 11, 1434–1440. Amer Vet Med Assoc 215, 811–814.
Prostate 9, 363–373. Cotchin E, 1951: Neoplasms in small ani- Edney ATB, Smith PM, 1986: Study of
Borchelt PL, 1983: Aggressive behavior of mals. Vet Rec 63, 67–72. obesity in dogs visiting veterinary prac-
dogs kept as companion animals: classifi- Crane SW, 1991: Occurrence and manage- tices in the United Kingdom. Vet Rec 118,
cation and influence of sex, reproductive ment of obesity in companion animals. J 391–396.
status and breed. Appl Anim Ethol 10, Sm Anim Prac 32, 275–282. Eze CA, Eze MC, 2002: Castration, other
45–61. David G, Rajendran EI, 1980: The after- management practices and socio-eco-
Borchelt PL, Voith VL, 1987: Aggressive effects of spaying in bitches and cats. nomic implications for dog keepers in
behavior in cats. Comp Cont Ed 9, 49–57. Cheiron 9, 193–195. Nsukka area, Enugu State, Nigeria. Prev
Brodbelt D, 2009: Perioperative mortality in Dixon RM, Mooney CT, 1999a: Canine Vet Med 55, 273–280.
small animal anaesthesia. Vet J 182, 152– serum thyroglobulin autoantibodies in
161.

 2012 Blackwell Verlag GmbH


220 MV Root Kustritz

Faggella AM, Aronsohn MG, 1993: Anes- therapeutic use of castration and proges- uterine tubes (oviducts). In Johnston SD,
thetic techniques for neutering 6- to tins. Comp Cont Ed 1, 461–465. Root Kustritz MV, Olson PN (eds),
14-week-old kittens. J Amer Vet Med Hart BL, 2001: Effect of gonadectomy on Canine and Feline Theriogenology. WB
Assoc 202, 56–62. subsequent development of age-related Saunders, Philadelphia PA, pp. 206–224.
Faggella AM, Aronsohn MG, 1994: Evalu- cognitive impairment in dogs. J Amer Johnston SD, Root Kustritz MV, Olson PN,
ation of anesthetic protocols for neutering Vet Med Assoc 219, 51–56. 2001b: Disorders of the feline uterus and
6–14-week old pups. J Amer Vet Med Hart BL, Barrett RE, 1973: Effects of uterine tubes (oviducts). In Johnston SD,
Assoc 205, 308–314. castration on righting, roaming, and urine Root Kustritz MV, Olson PN (eds),
Fettman MJ, Stanton CA, Banks LL, spraying in adult male cats. J Amer Vet Canine and Feline Theriogenology. WB
Hamar DW, Johnson DE, Hegstad RL, Med Assoc 163, 290–292. Saunders, Philadelphia PA, pp. 463–471.
Johnston S, 1997: Effects of neutering on Hart BL, Eckstein RA, 1997: The role of Kalz B, 2001: Population biology, space use
bodyweight, metabolic rate and glucose gonadal hormones in the occurrence of and behavior of feral cats and measures to
tolerance of domestic cats. Res Vet Sci 62, objectionable behaviours in dogs and control reproduction. Inaugural disserta-
131–136. cats. Appl Anim Behav Sci 52, 331–344. tion, Mathematics and Science Faculty,
Fidler IJ, Brodey RS, 1967: The biological Hawe RS, 1983: What is your diagnosis? Humboldt University, Berlin [German].
behavior of canine mammary neoplasms. Prostatic adenocarcinoma. J Amer Vet Kanchuk ML, Backus RC, Calvert CC,
J Amer Vet Med Assoc 151, 1311–1318. Med Assoc 182, 1257–1258. Morris JG, Rogers QR, 2002: Neutering
Foster SJ, 1967: The ‘urolithiasis’ syndrome Hayes HM, Milne KL, Mandel CP, 1981: induces changes in food intake, body
in male cats: a statistical analysis of the Epidemiological features of feline mam- weight, plasma insulin and leptin con-
problems, with clinical observations. J Sm mary carcinoma. Vet Rec 108, 476–479. centrations in normal and lipoprotein
Anim Prac 8, 207–214. Herron MA, 1972: The effect of prepubertal lipase-deficient male cats. J Nutr 132,
Greenfield CL, Johnson SL, Schaeffer DJ, castration on the penile urethra of the cat. 1730–1732.
2004: Frequency of use of various proce- J Amer Vet Med Assoc 160, 208–211. Knapp DW, Glickman NW, DeNicola DB,
dures, skills, and areas of knowledge Hoenig M, Ferguson DC, 2002: Effects of Bonney PL, Lin TL, Glickman LT, 2000:
among veterinarians in private small ani- neutering on hormonal concentrations Naturally-occurring canine transitional
mal exclusive or predominant practice and energy requirements in male and cell carcinoma of the urinary bladder. A
and proficiency expected of new veteri- female cats. Amer J Vet Res 63, 634–649. relevant model of human invasive bladder
nary school graduates. J Amer Vet Med Holt PE, 2004: Urinary incontinence in the cancer. Urol Oncol 5, 47–59.
Assoc 224, 1780–1787. male and female dog or does sex matter? Kraft W, 1998: Geriatrics in canine and
Greer KA, Canterberry SC, Murphy KE, http://www.vin.com (accessed 1 October feline internal medicine. Eur J Med Res 3,
2007: Statistical analysis regarding the 2004).. 31–41.
effects of height and weight on life span Holt PE, Thursfield MV, 1993: Association Kritzer MF, Brewer A, Montalmant F,
of the domestic dog. Res Vet Sci 82, 208– in bitches between breed, size, neutering Davenport M, Robinson JK, 2007:
214. and docking, and acquired urinary incon- Effects of gonadectomy on performance
Gregory SP, Parkinson TJ, Holt PE, 1992: tinence due to incompetence of the ure- in operant tasks measuring prefrontal
Urethral conformation and position in thral sphincter mechanism. Vet Rec 133, cortical function in adult male rats. Horm
relation to urinary incontinence in the 177–180. Beh 51, 183–194.
bitch. Vet Rec 131, 167–170. Hopkins SG, Schubert TA, Hart BL, 1976: Lawrence HJ, Gould WJ, Flanders JA,
Gregory SP, Holt PE, Parkinson TJ, Wathes Castration of adult male dogs: effects on Rowland PH, Yaeger AE, 1993: Unilat-
CM, 1999: Vaginal position and length in roaming, aggression, urine marking, and eral adrenalectomy as a treatment for
the bitch: relationship to spaying urinary mounting. J Amer Vet Med Assoc 168, adrenocortical tumors in ferrets: five cases
incontinence. J Sm Anim Prac 40, 180– 1108–1110. (1990–1992). J Amer Vet Med Assoc 203,
184. Houlton JEF, McGlennon NJ, 1992: Cas- 267–270.
Gunzel-Apel AR, 1998: Early castration of tration and physeal closure in the cat. Vet LeRoy BE, Lech ME, 2004: Prostatic carci-
dogs and cats from the point of view of Rec 131, 466–467. noma causing urethral obstruction and
animal welfare. Dtsch Tierarztl Woc- Howe LM, 1997: Short-term results and obstipation in a cat. J Fel Med Surg 6,
henschr 105, 95–98. complications of prerpubertal gonadec- 397–400.
Gunzel-Apel AR, Seefeldt A, Eschricht FM, tomy in cats and dogs. J Amer Vet Med Lofstedt RM, VanLeeuwen JA, 2002: Eval-
Urhausen C, Kramer S, Mischke R, Assoc 211, 57–62. uation of a commercially available lutein-
Hoppen HO, Beyerbach M, Koivisto M, Howe LM, Slater MR, Boothe HW, Hobson izing hormone test for its ability to
Dieleman SJ, 2009: Effects of gonadec- HP, Fossum TW, Spann AC, Wilkie WS, distinguish between ovariectomized and
tomy on prolactin and LH secretion and 2000: Long-term outcome of gonadec- sexually intact bitches. J Amer Vet Med
the pituitary-thyroid axis in male dogs. tomy performed at an early age or tradi- Assoc 220, 1331–1335.
Theriogenology 71, 746–753. tional age in cats. J Amer Vet Med Assoc Lowseth LA, Gerlach RF, Gillett NA,
Hagman R, Lagerstedt AS, Hedhammer A, 217, 1661–1665. Muggenburg BA, 1990: Age-related
Egenvall A, 2011: A breed-matched case- Howe LM, Slater MR, Boothe HW, Hobson changes in the prostate and testes of the
control study of potential risk-factors for HP, Holcom JL, Spann AC, 2001: Long- beagle dog. Vet Path 27, 347–353.
canine pyometra. Theriogenology 75, term outcome of gonadectomy per- Mahlow JC, 1999: Estimation of the pro-
1251–1257. formed at an early age or traditional portions of dogs and cats that are surgi-
Hahn KA, VonDerHaar MA, Teclaw RF, age in dogs. J Amer Vet Med Assoc 218, cally sterilized. J Amer Vet Med Assoc
1992: An epidemiological evaluation of 217–221. 215, 640–643.
1202 dogs with testicular neoplasia [Ab- Hubbard BS, Vulgamott LC, Liska WD, Manning AM, Rowan AN, 1992: Compan-
stract]. J Vet Intern Med 6, 121. 1990: Prostatic adenocarcinoma in a cat. ion animal demographics and sterilization
Hamilton JM, Else RW, Forshaw P, 1977: J Amer Vet Med Assoc 197, 1493–1494. status: results from a survey in four
Oestrogen receptors in canine mammary Janowsky JS, 2006: The role of androgens in Massachusetts towns. Anthrozoos 5,
tumours. Vet Rec 101, 258–260. cognition and brain aging in men. Neu- 192–201.
Hampe JF, Misdorp W, 1974: Tumours and roscience 138, 1015–1020. Martin LJM, Siliart B, Dumon HJW,
dysplasias of the mammary gland. Bull Johnson RT, Burk JA, 2006: Effects of Nguyen P, 2006: Spontaneous hormonal
World Health Org 50, 111–133. gonadectomy and androgen supplemen- variations in male cats following gonad-
Harasen G, 2003: Canine cranial cruciate tation on attention in male rats. Neuro- ectomy. J Fel Med Surg 8, 309–314.
ligament rupture in profile. CanVet J 44, biol Learn Memory 85, 219–227. Mason E, 1970: Obesity in pet dogs. Vet Rec
845–846. Johnson-Delaney CA, 2006: Ferret adrenal 86, 612–616.
Hart BL, 1973: Behavioral effects of castra- disease: 2006 perspective. Exotic DVM 8, May C, Bennett D, Downham DY, 1991:
tion. Fel Prac 3, 10–12. 31–34. Delayed physeal closure with castration in
Hart BL, 1979: Problems with objectionable Johnston SD, Root Kustritz MV, Olson PN, cats. J Sm Anim Prac 32, 326–328.
sociosexual behavior of dogs and cats: 2001a: Disorders of the canine uterus and

 2012 Blackwell Verlag GmbH


Small Animal Gonadectomy 221

McCann TM, Simpson KE, Shaw DJ, Butt weight and composition after gonadec- metritis in cats: 79 cases (1980–1985).
JA, Gunn-Moore DA, 2007: Feline dia- tomy in cats. Amer J Vet Res 65, 1708– J Amer Vet Med Assoc 198, 1427–1431.
betes mellitus in the UK: the prevalence 1713. Prahl A, Guptill L, Glickman NW, Tetrick
within an insured cat population and a Norris AM, Laing EJ, Valli VE, Withrow M, Glickman LT, 2007: Time trends and
questionnaire-based putative risk factor SJ, Macy DW, Ogilvie GK, Tomlinson J, risk factors for diabetes mellitus in cats
analysis. J Fel Med Surg 9, 289–299. McCaw D, Pidgeon G, Jacobs RM, 1992: presented to veterinary teaching hospitals.
McNicholas WT, Wilkens BE, Blevins WE, Canine bladder and urethral tumors: a J Fel Med Surg 9, 351–358.
Snyder PW, McCabe GP, Applewhite retrospective study of 115 cases (1980- Priester WA, McKay FW, 1980: The occur-
AA, Laverty PH, Breur GJ, 2002: 1985). J Vet Intern Med 6, 145–153. rence of tumors in domestic animals. Natl
Spontaneous femoral capital physeal Obradovich J, Walshaw R, Goulland E, Canc Inst Monogr 54, 169.
fractures in adults cats: 26 cases (1996– 1987: The influence of castration on the Priester WA, Mulvihill JJ, 1972: Canine hip
2001). J Amer Vet Med Assoc 221, 1731– development of prostatic carcinoma in the dysplasia: relative risk by sex, size, and
1736. dog: 43 cases (1978–1985). J Vet Intern breed, and comparative aspects. J Amer
Michell AR, 1999: Longevity of British Med 1, 183–187. Vet Med Assoc 160, 735–739.
breeds of dogs and its relationship with O’Farrell V, Peachey E, 1990: Behavioural Prymak C, McKee LJ, Goldschmidt MH,
sex, size, cardiovascular variables and effects of ovariohysterectomy on bitches. Glickman LT, 1988: Epidemiologic, clin-
disease. Vet Rec 145, 625–629. J Sm Anim Prac 31, 595–598. ical, pathologic, and prognostic charac-
Miller DM, 1995: Ovarian remnant syn- Olson PN, 1997: Early spay and neuter. teristics of splenic hemangiosarcoma and
drome in dogs and cats: 46 cases (1988– Proceedings, North American Veterinary splenic hematoma in dogs: 217 cases
1992). J Vet Diagn Invest 7, 572–574. Conference, Orlando FL. (1985). J Amer Vet Med Assoc 193, 706–
Milne KL, Hayes HM, 1981: Epidemiologic Panciera DL, 1994: Hypothyroidism in dogs: 712.
features of canine hypothyroidism. Cor- 66 cases (1987–1992). J Amer Vet Med Ragetly CA, Evans R, Mostafa AA, Griffon
nell Vet 71, 3–14. Assoc 204, 761–767. DJ, 2011: Multivariate analysis of mor-
Misdorp W, Hart AAM, 1979: Canine Panciera DL, Thomas CB, Eicker SW, phometric characteristics to evaluate risk
mammary cancer. II. Therapy and causes Atkins CE, 1990: Epizootiologic patterns factors for cranial cruciate ligament defi-
of death. J Sm Anim Prac 20, 395–404. of diabetes mellitus in cats: 333 cases ciency in Labrador retrievers. Vet Surg
Moe L, 2001: Population-based incidence of (1980–1986). J Amer Vet Med Assoc 197, 40, 327–333.
mammary tumors in some dogs breeds. 1504–1508. Rand JS, Bobbermien LM, Hendrikz JK,
J Reprod Fert Suppl 57, 439–443. Patronek GJ, Glickman LT, Beck AM, Copland M, 1997: Over representation of
Mondelli F, Previde EP, Verga M, Levi D, McCabe GC, Ecker C, 1996a: Risk fac- Burmese cats with diabetes mellitus. Aust
Magistrelli S, Valsecchi P, 2004: The bond tors for relinquishment of dogs to an Vet J 75, 402–405.
that never developed: adoption and relin- animal shelter. J Amer Vet Med Assoc Reichler IM, 2009: Gonadectomy in cats and
quishment of dogs in a rescue shelter. 209, 572–581. dogs: a review of risks and benefits.
J Appl Anim Welf Sci 7, 253–266. Patronek GJ, Glickman LT, Beck AM, Reprod Dom Anim 44(Suppl 2), 29–35.
Mong JA, Pfaff DW, 2003: Hormonal and McCabe GC, Ecker C, 1996b: Risk fac- Reisner IR, Houpt KA, Shofer FS, 2005:
genetic influences underlying arousal as it tors for relinquishment of cats to an National survey of owner-directed aggres-
drives sex and aggression in animal and animal shelter. J Amer Vet Med Assoc sion in English Springer Spaniels. J Amer
human brains. Neurobiol Aging 24, 583– 209, 582–588. Vet Med Assoc 227, 1594–1603.
588. PetSmart Charities A&U Barriers, 2002: Richards HG, McNeil PE, Thompson H,
Moore GE, Burkman KD, Carter MN, http://www.petsmartcharities.org/resources/ Reid SWJ, 2001: An epidemiological
Peterson MR, 2001: Causes of death or resources-documents/PetSmartCharities_ analysis of canine-biopsies database com-
reasons for euthanasia in military work- Research_AUBarriers.pdf (accessed 19 piled by a diagnostic histopathology ser-
ing dogs: 927 cases (1993–1996). J Am Vet December 2011). vice. Prev Vet Med 51, 125–136.
Med Assoc 219, 209–214. Poirier VJ, Forrest JL, Adams WM, Vail Romagnoli S, 2008: Surgical gonadectomy
Moulton JE, Taylor DON, Dorn CR, DM, 2004: Piroxicam, mitoxantrone, and in the bitch and queen: should it be done
Andersen AC, 1970: Canine mammary coarse fraction radiotherapy for the treat- and at what age? Proceedings, Southern
tumors. Path Vet 7, 289–320. ment of transitional cell carcinoma of the European Veterinary Conference and
Nassar R, Talboy J, Moulton C, 1992: bladder in 10 dogs: a pilot study. J Amer Congreso Nacional AVEPA, Barcelona
Animal Shelter Reporting Study 1990. Anim Hosp Assoc 40, 131–136. Spain.
American Humane Association, Engle- Pollari FL, Bonnett BN, Bamsey SC, Meek Root MV, 1995: Early spay-neuter in the
wood CO. AH, Allen DG, 1996: Postoperative com- cat: effect on development of obesity and
National Council on Pet Population Study plications of elective surgeries in dogs and metabolic rate. Vet Clin Nutr 2, 132–134.
and Policy, 1994: National Shelter cats determined by examining electronic Root Kustritz MV, 1996: Elective gonadec-
Census: 1994 Results. NCCPPSP, Fort and paper medical records. J Amer Vet tomy in the cat. Fel Prac 24, 36–39.
Collins CO. Med Assoc 208, 1882–1886. Root Kustritz MV, 1999: Early spay-neuter
Neilson JC, Eckstein RA, Hart BL, 1997: Ponglowhapan S, Church DB, Khalid M, in the dog and cat. Vet Clin NA 29, 935–
Effects of castration on problem behav- 2008a: Differences in the expression of 943.
iors in male dogs with reference to age luteinizing hormone and follicle-stimulat- Root Kustritz MV, 2005: Reproductive
and duration of behavior. J Amer Vet ing hormone receptors in the lower uri- behavior of small animals. Theriogenology
Med Assoc 211, 180–182. nary tract between intact and 64, 743–746.
New JG, Salman MD, King M, Scarlett JM, gonadectomised male and female dogs. Root Kustritz MV, 2007: Determining the
Kass PH, Hutchison JM, 2000: Shelter Dom Anim Endo 34, 339–351. optimal age for gonadectomy of dogs and
relinquishment: characteristics of shelter- Ponglowhapan S, Church DB, Khalid M, cats. J Amer Vet Med Assoc 231, 1665–
relinquished animals their owners com- 2008b: Differences in the proportion of 1675.
pared with animals and their owners in collagen and muscle in the canine lower Root Kustritz MV, 2010: Optimal age
US pet-owning households. J Appl Anim urinary tract with regard to gonadal for gonadectomy in dogs and cats. Clin
Welf Sci 3, 179–201. status and gender. Theriogenology 70, Therio 2, 177–181.
New JC, Kelch WJ, Hutchison JM, Salman 1516–1524. Root MV, Johnston SD, Johnston GR,
MD, King M, Scarlett JM, Kass PH, Ponglowhapan S, Church DB, Khalid M, Olson PN, 1996a: The effect of prepuberal
2004: Birth and death rate estimates of 2011: Effect of the gonadal status and the and postpuberal gonadectomy on penile
cats and dogs in U.S. households and gender on glycosaminoglycans profile in extrusion and urethral diameter in the
related factors. J Appl Anim Welf Sci 7, the lower urinary tract of dogs. Theriog- domestic cat. Vet Radiol Ultrasound 37,
229–241. enology 76, 1284–1292. 363–366.
Nguyen PG, Dumon HJ, Siliart BS, Martin Potter K, Hancock DH, Gallina AM, 1991: Root MV, Johnston SD, Olson PN, 1996b:
LJ, Sergheraert R, Biourge VC, 2004: Clinical and pathologic features of endo- Effect of prepuberal and postpuberal
Effects of dietary fat and energy on body metrial hyperplasia, pyometra, and endo- gonadectomy on heat production mea-

 2012 Blackwell Verlag GmbH


222 MV Root Kustritz

sured by indirect calorimetry in male and Sorenmo K, 2003: Canine mammary gland species. Proceedings, Society for Theriog-
female domestic cats. Amer J Vet Res 57, tumors. Vet Clin NA 33, 573–596. enology Annual Meeting, Columbus OH.
371–374. Sorenmo KU, Goldschmidt M, Shofer F, Ware WA, Hopper DL, 1999: Cardiac
Root MV, Johnston SD, Olson PN, 1996c: Goldkamp C, Ferracone J, 2003: Immu- tumors in dogs: 1982-1995. J Vet Intern
The effect of prepuberal and postpuberal nohistochemical characterization of ca- Med 13, 95–103.
gonadectomy on radial physeal closure in nine prostatic carcinoma and correlation Waters DJ, Shen S, Glickman LT, 2000: Life
male and female domestic cats. Vet with castration status and castration time. expectancy, antagonistic pleiotropy, and
Radiol Ultrasound 38, 42–47. Vet Comp Oncol 1, 48–56. the testis of dogs and men. Prostate 43,
Rosenthal KL, Peterson ME, Quesenberry Spain CV, Scarlett JM, Houpt KA, 2004a: 272–277.
KE, Hillyer EV, Beeber NL, Moroff SD, Long-term risks and benefits of early-age Waters DJ, Kengeri SS, Clever B, Booth JA,
Lothrop CD, 1993: Hyperadrenocortic- gonadectomy in cats. J Amer Vet Med Maras AH, Schlittler DL, Hayek MG,
ism associated with adrenocortical tumor Assoc 224, 372–379. 2009: Exploring mechanisms of sex differ-
or nodular hyperplasia of the adrenal Spain CV, Scarlett JM, Houpt KA, 2004b: ences in longevity: lifetime ovary exposure
gland in ferrets: 50 cases (1987–1991). Long-term risks and benefits of early-age and exceptional longevity in dogs. Aging
J Amer Vet Med Assoc 203, 271–275. gonadectomy in dogs. J Amer Vet Med Cell 8, 752–755.
Ru G, Terracini B, Glickman LT, 1998: Assoc 224, 380–387. Waters DJ, Kengeri SS, Maras AH, Chiang
Host related risk factors for canine oste- Stocklin-Gautschi NM, Hassig M, Reichler EC, 2011: Probing the perils of dichoto-
osarcoma. Vet J 156, 31–39. IM, 2001: The relationship of urinary mous binning: how categorizing female
Salmeri KR, Bloomberg MS, Scruggs SL, incontinence to early spaying in bitches. dogs as spayed or intact can misinform
Shille V, 1991a: Gonadectomy in imma- J Reprod Fertil 57, 233–236. our assumptions about the lifelong health
ture dogs: effects of skeletal, physical, and Stubbs WP, Bloomberg MS, Scruggs SL, consequences of ovariohysterectomy.
behavioral development. J Amer Vet Med Shille VM, Lane TJ, 1996: Effects of Theriogenology 76, 1496–1500.
Assoc 198, 1193–1203. prepubertal gonadectomy on physical White CR, Hohenhaus AE, Kelsey J, Procter-
Salmeri KR, Olson PN, Bloomberg MS, and behavioral development in cats. Gray E, 2006: Cutaneous MCTs: associa-
1991b: Elective gonadectomy in dogs: a J Amer Vet Med Assoc 209, 1864–1871. tions with spay ⁄ neuter status, breed, body
review. J Amer Vet Med Assoc 198, 1183– Teske E, Naan EC, VanDijk EM, VanGard- size, and phylogenetic cluster. J Amer
1192. eren E, Schalken JA, 2002: Canine pros- Anim Hosp Assoc 47, 210–216.
Schneider R, Dorn CR, Taylor DON, 1969: tate carcinoma: epidemiological evidence Whitehair JG, Vasseur PB, Willits NH,
Factors influencing canine mammary can- of an increased risk in castrated dogs. Mol 1993: Epidemiology of cranial cruciate
cer development and postsurgical sur- Cell Endocrinol 197, 251–255. ligament rupture in dogs. J Amer Vet
vival. J Natl Canc Inst 43, 1249–1261. Trevejo R, Yang M, Lund EM, 2011: Med Assoc 203, 1016–1019.
Schoemaker NJ, Teerds KJ, Mol JA, 2002: Epidemiology of surgical castration in Wright JC, Nesselrote MS, 1987: Classifica-
The role of luteinizing hormone in the dogs and cats in the United States. tion of behavior problems in dogs: distri-
pathogenesis of hyperadrenocorticism in J Amer Vet Med Assoc 238, 898–904. butions of age, breed, sex and reproductive
neutered ferrets. Mol Cell Endocrinol 197, VanHagen MA, Ducro BJ, VanDenBroek J, status. Appl Anim Beh Sci 19, 169–178.
117–125. Knol BW, 2005: Incidence, risk factors, and Zirkin BR, Strandberg JD, 1984: Quantita-
Slauterbeck JR, Pankratz K, Xu KT, heritability estimates of hind limb lameness tive changes in the morphology of the
Bozeman SC, Hardy DM, 2004: Canine caused by hip dysplasia in a birth cohort of aging canine prostate. Anat Rec 208, 207–
ovariohysterectomy and orchiectomy in- boxers. Amer J Vet Res 66, 307–312. 214.
creases the prevalence of ACL injury. Clin Verstegen J, Onclin K, 2003a: Mammary
Orthop 429, 301–305. tumors in the queen. Proceedings, Society Author’s address (for correspondence):
Sloth C, 1992: Practical management of for Theriogenology Annual Meeting, Dr MV Root Kustritz, University of Min-
obesity in dogs and cats. J Sm Anim Prac Columbus OH. nesota College of Veterinary Medicine, 1352
33, 178–182. Verstegen J, Onclin K, 2003b: Etiopatho- Boyd Avenue, St. Paul, MN 55108, USA.
Smith AN, 2003: Hemangiosarcoma in dogs genesis, classification and prognosis of E-mail: rootk001@umn.edu
and cats. Vet Clin NA 33, 533–552. mammary tumors in the canine and feline

 2012 Blackwell Verlag GmbH

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