Introduction

Gonadectomy is the surgical removal of both gonads under general anesthesia. In the female, gonadectomy (or spaying) is generally performed through removal of both ovaries (ovariectomy=OVX) or of ovaries and uterus (ovariohysterectomy=OVH) via an abdominal approach. Whether or not bitches and queens should be spayed, what is the best surgical procedure and what is the best age to perform it are issues which have many welfare implications, as well as advantages and disadvantages. Prepubertal gonadectomy is commonly performed on immature male and female animals aging from 6 to 14 weeks and has been routinely used at many shelter and academic institutions in the United States and Europe over the last quarter of a century to control pet overpopulation. Although regarded as a safe technique, prepuberal gonadectomy may carry some health concerns. Postpuberal gonadectomy still offers several advantages if performed early in life although the growth of reproductive organs and the potential presence of pathologic conditions may occasionally complicate the surgical approach. Also, the well-known advantage of a reduced risk of mammary neoplasia is often considerably reduced when gonadectomy is delayed beyond the third cycle in bitches and queens.

Surgical Technique

The midline incision should be done in the cranial third of the abdomen for bitches (ovaries are more difficult to exteriorize than the uterine body) and in the middle third of the abdomen for queens (uterine body more difficult to exteriorize than the ovaries). The length of the incision may be increased depending on uterine conditions (an enlarged uterus normally requires a longer incision). Once the ovary has been located, the proper ligament is clamped and the ovary is pulled up. When pulling up the ovary, the ovarian suspensory ligament is stretched and may be simply broken with the index finger. A hole is made in the mesovarium avoiding the ovarian vessels (normally caudal to the vessels), then 2 or 3 clamps are placed on the ovarian pedicle. An incision is made between the 2 clamps (or – if 3 clamps are used - between the clamp closest to the ovary and the adjacent one), the ovary is removed and the pedicle is ligated directly below the remaining clamp (in case of a young bitch or queen) or the third clamp (the one most distant from the ovary) is removed and the ligature is placed in the groove caused by the clamp. Removal of the ovary can also be done without using clamps but simply having the surgeon holding firmly the ovary and an operator ligate proximal to the ovary.

To remove the uterus, the broad ligament is exteriorized, inspected and severed with the thumb or index finger, or is ligated if highly vascularized. Once all potential sources of broad ligament bleeding have been eliminated, (2 or better) 3 clamps are placed on the most caudal aspect of the uterine body, which is then severed between the proximal and middle clamp. The uterine stump is ligated with a single ligature (for queens or small bitches) or a ligature is placed on each uterine artery. The caudal clamp is released and the remaining groove is used to facilitate placing the ligature on the uterine body. Resection of the uterine body can also be done without using clamps but simply having the surgeon hold firmly the uterine body and an operator ligate distal to the uterine body. The uterine stump is grasped with a hemostat and the clamp is released while checking for absence of bleeding, after which the uterine stump is replaced into the abdomen. Suture material is normally absorbable.

Ovariectomy vs. Ovariohysterectomy

Whether to remove only the ovaries or also the uterus is for many veterinarians a true dilemma. The “Anglo-Saxon” or “British” school of thought has always had the approach of removing everything based on the concept that what is removed cannot cause a disease, while the “Latin” approach has always been that of removing only the ovaries since the uterus quickly undergoes atrophy following OVX, and perhaps the risk of developing urinary incontinence could be lower because of anatomical reasons. Research done in Utrecht, in which 138 OVHed bitches and 126 OVXed bitches were followed up for 8–11 years, has clearly showed that between the 2 groups of dogs: a) there is no difference in short-term as well as long-term surgical complications; b) there is no difference in incidence of cystic endometrial hyperplasia, pyometra or any other uterine disease; c) there is no difference in incidence of urinary incontinence.¹

As a matter of fact, the only differences between the two approaches are the degree of invasiveness and length of the surgery, and therefore length of anesthesia, all of which are higher in the case of OVH. This causes a higher risk of surgical complications and a higher stress for the animal as well as a higher cost for the owner. The following conclusion of Okkens et al.¹, “There is no indication to remove also the uterus in elective castration procedures of healthy bitches, and therefore ovariectomy is to be considered the procedure of choice,” is currently shared by the majority of US as well as European authors^2-4. Therefore, it is currently considered unethical to perform ovariohysterectomy instead of ovariectomy, unless there are specific health reasons. Although such data are available only for bitches, it is likely that the same situation is true also for queens. In case of specific indications for OVH, it is advisable not to remove the cervix because of its important role in isolating the abdominal cavity from outside, even in the castrated female. Hysterectomy should not be performed, as bilateral development of ovarian cysts has been anecdotally reported, with bitches having to undergo laparotomy again to remove the cystic ovaries. Also, if a previously hysterectomized small litter size bitch is mated during heat by a large size dog, her vaginocervical suture may rupture with a consequent coital peritonitis.⁵

In Which Stage of the Reproductive Cycle?

While no specific choice of time during the adult life is necessary when castrating male dogs or cats, performing gonadectomy in adult females may have some health implications with regard to the reproductive cycle stage in which the female is at the time of surgery. This is particularly true for bitches, as when such surgery is performed in proestrus or estrus there is an increased risk of short-term post-surgical complications (see below), while when it is performed in diestrus there is an increased risk of false pregnancy (due to the sudden decrease in serum progesterone causing a peak in serum prolactin concentration which sets in mammary function and maternal instinct). In bitches, gonadectomy should best be performed during anestrus (2.5–5.5 months following onset of proestrus); serum progesterone assay may be of help in ruling out diestrus when history is not available. Although no specific study has ever looked at what is the best stage for performing gonadectomy in felines, the queen is not known to experience any such problems depending on when in her reproductive stage she is castrated due to lack of clinically evident effects of estrogens on vascularization of the reproductive tract and absence of false pregnancy in felines.

Advantages of Gonadectomy

There are several health advantages due to gonadectomy in male and female dogs and cats.⁶ The removal of the ovaries is associated in both bitches and queens with a reduced risk of mammary and uterine diseases (mammary neoplasia and pyometra, respectively), as well as absence of ovarian diseases (ovarian tumors, ovarian cysts), progesterone-related diseases (false pregnancy, feline mammary hypertrophy), pregnancy-related diseases (unwanted pregnancy, pregnancy complications, abortion) or parturition-related diseases (dystocia, uterine prolapse, and in the bitch only subinvolution of placental sites) and in bitches also estrogen-related diseases (vaginal hyperplasia/prolapse, persistent estrus, bone marrow aplasia). Bitches gonadectomized prior to puberty have a 95% reduction of the risk of developing mammary tumors as opposed to bitches spayed after 1st heat (92% risk reduction), after 2nd heat (74% risk reduction) or bitches spayed after 2.5 years of age or left intact (no difference in risk).⁷ Incidence of pyometra in adult intact bitches varies from 15% to 25%, but the risk tends to increase with increasing age.⁸ Libido, aggressiveness, urine marking and roaming are never displayed in male dogs and cats neutered prior to puberty, while they may persist at some degree in a few cases when a male animal is neutered as an adult.⁹ From a behavioural point of view it is commonly believed that, apart from not showing reproductive behavior, neutered animals have a more relaxed, somewhat lazy attitude. In male dogs, there is a significant reduction of all prostatic conditions⁶ and in male cats the decreased (or lack of) roaming attitude certainly decreases the risk of death due to trauma. Gonadectomy may play an important role in reducing pet overpopulation.

Changes Due to Pre- and Post-puberal Gonadectomy

Physical Changes

In dogs, growth plate closure is delayed when surgery is performed prior to puberty, but the delay is significantly longer when neutering is done at 7 weeks as compared to 7 months. The rate of growth is unaffected, but both radius and ulna become longer regardless of the age at neutering. Food intake is not affected nor is weight gain or back-fat depth during the first 15 months or until the age of 18 months when comparing 7 week- to 7 month-neutered puppies,^10,11 but weight gain later in life has been reported in non-working bitches. Although it is well known that neutering predisposes (non-working) dogs to develop a significant increase in body weight, the time at which gonadectomy is performed in these animals probably does not affect the clinical manifestation of this problem. External genitalia do not develop fully: penile and preputial immaturity and decreased radiodensity of the os penis are frequently observed (which rarely, if ever, constitute a problem). Vulvar development may be insufficient in bitches gonadectomised at 7 weeks. However, the incidence of infolding of vulvar lips leading to perivulvar dermatitis and chronic vaginitis is not different when compared to bitches neutered at 7 months.¹² When penile protrusion was attempted at the age of 22 months, it could be done in all intact cats, in only 60% of cats neutered at 7 months and in none of the cats neutered at 7 weeks.¹³

In cats neutered at 7 weeks or 7 months of age, physeal closure is delayed 5 to 7 months resulting in a 10% longer size of long bones when comparing neutered to intact cats. Physeal (Salter-Harris) fractures have been reported in neutered dogs and cats at 12–16 months of age.¹⁴  Salter-Harris fractures are a potential complication when prepubertal gonadectomy is performed, but appear to be as an extremely rare condition in both dogs and cats. No decrease in urethral diameter (and therefore no increased risk of lower urinary tract disease) has been observed in neutered male cats (regardless of age at neutering) compared to the intact population, with no difference in urethral closure pressure in neutered vs. intact female cats, while there was a significant decrease in the diameter of the pre-pelvic urethras in queens neutered at 7 weeks.¹³ Glucose metabolism (glucose half life, peak serum insulin concentrations, peak insulin response following intravenous glucose administration) was not altered in neutered (regardless of age at neutering) compared to intact cats when evaluated at 6, 12, 18 months of age, while at 24 months of age neutered male cats had a significantly later peak serum insulin response when compared to intact cats.¹³

Behavioral Changes

Effects of prepuberal gonadectomy on behaviour vary depending on species and sex and have not been completely investigated yet. In general, excitability and degree of activity are increased in males and females gonadectomised at 7 weeks or 7 months.^15-17 However, inappropriate behaviors as reasons for relinquishment have not been reported in dogs neutered at an early age when compared to those neutered as adults, and in Labrador/golden retriever crosses raised as guide dogs for the blind, neutering at 7 weeks or 7 months does not affect the degree of training success. No effect of early-age neutering on playfulness, excitement or frequency of vocalization has been reported in cats. In cats castrated prior to 5 months of age, there is a decrease in activity and an increase of shyness towards strangers.^15,16 In adult bitches, castration may exacerbate dominance regardless of their attitude prior to surgery. A significant increase in the degree of reactivity has been observed in German shepherd bitches 5 months following OVX.¹⁸ Owners should realize the importance of evaluating the behaviour of their bitches prior to deciding whether to castrate them, as castration may not be the appropriate treatment for behavioural problems.¹⁷

Obesity

Obesity is reported as a common side effect of neutering.⁷ No difference in food intake, weight gain or back-fat depth was reported for the first 15 months following neutering, when a total of 32 neutered and intact dogs were compared. However, food intake increases significantly in bitches during the first 90 days following OVX/OVH with respect to bitches receiving a sham-laparotomy. Larger studies indicate that, irrespective of age at surgery, spayed female dogs are about twice as likely to become obese as intact animals. The risk for obesity does not change in animals gonadectomized prepuberally. It is unknown whether there is a predisposition to obesity, but, if this is the case, gonadectomy seems to have the same stimulus, regardless of age. Obesity is also a side effect of neutering in cats, as intact animals have a lower weight and a lower fat thickness than cats neutered at 7 weeks or 7 months. The resting metabolic rate is lower and body condition scores are higher in gonadectomised (irrespective of age at neutering), compared to intact cats. Appetite increases significantly in gonadectomized cats 3 days after surgery. In castrated tomcats, a significant increase in body weight 35 weeks post-castration was preceded by significant increases in serum concentrations of insulin growth factor I, prolactin and leptin in castrate toms 1, 7 and 11 weeks following surgery, respectively.¹⁹

Urinary Incontinence

A decreased capacity of the external urethral sphincter is observed following gonadectomy in bitches, but not in queens. Average urethral closure pressure in intact bitches is 18.6±10.5 cm H₂O, 12 months following gonadectomy is 10.3±6.7 cm H₂O in continent bitches, and may fall to 4.6±2.3 cm H₂O in incontinent animals. Urinary incontinence (UI) is a common sequel of spaying in bitches, with the interval between spaying and diagnosis of incontinence varying from days to months or even years. Incidence of UI in the normal canine population varies from 0.3 to 2.0%, while it increases to 5–10% in the spayed bitches population. In a long-term study on risks and benefits of early-age neutering in dogs, the incidence of UI was reported to increase in bitches neutered prior to 3 months of age when compared to that of bitches neutered after 3 months; therefore the age of 3 months was indicated as a threshold after which female puppies could be safely neutered.¹⁵ However, many authors think that going through puberty may have a beneficial effect as it allows the reproductive system to reach its final stage of growth, thereby perhaps limiting the incidence of side effects such as UI as well as those due to insufficient growth of external genitalia.

Osteoporosis

Osteoporosis (loss of trabecular bone) is the most important complication of menopause in women and is thought to be due to a lack of estrogen stimulation, causing reduced secretion of calcitonin. Loss of trabecular bone has been observed in beagle bitches 11 months following OVH,²⁰ although, at present, it is unclear whether this bears any clinical significance, presumably because of the short life-span of most of the dogs used as companion animals.

Surgical Complications

Generic surgical risk may be significant in females due to the laparotomy access and of little, if any, significance in males. Side effects of gonadectomy in bitches and queens have been reported^11,21-25 and include haemorrhage/granuloma of the ovarian or (more commonly) uterine pedicle, suture dehiscence/infection/abscess/edema, peritonitis, evisceration, formation of suture fistulas, retention of a cotton gauze, ureteral ligation with secondary hydronephrosis, formation of vesicovaginal fistula with secondary hydroureter, ovarian remnant syndrome with or without secondary uterine stump inflammation (Table 1). Incidence of these conditions varies depending on OVX or OVH from 7% to 27% in the bitch and 33% in the queen. There is no correlation between incidence of complications and age of the animal, ability of the veterinarian or presence of reproductive diseases. There is no breed predisposition. The complication observed most frequently seems to be (vaginal or intra-abdominal) haemorrhage, which is much more common in large (80% incidence) as opposed to small (20% incidence) size bitches. Vulvar blood loss may occur following OVH (blood coming from the uterine pedicle, the suspensory ligament or the broad ligament) as well as following OVX (blood coming from the ovarian pedicle). Some complications may be due to the stage of the reproductive cycle in which spaying is performed: intraoperative bleeding is more common during proestrus and estrus (due to high estrogen concentrations), while false pregnancy may follow when spaying is performed during diestrus (due to rising prolactin concentrations following a sudden progesterone fall).

Table 1. Short- or long-term complications due to ovariectomy (OVX) or ovariohysterectomy (OVH) in bitches and queens

Based on personal experience and data from literature (a): total number of short- and long-term complications; (b): haemorrhage of the uterine or ovarian pedicle because of incomplete ligature or rupture of blood vessels). (*) the risk of complications is higher following OVH than OVX.

Heat after gonadectomy in bitches and queens is a well-known surgical complication of both OVX/OVH. Ovarian remnants are more commonly found on the right side, and may (but this is not proven) occur more frequently following OVH than OVX because of the fact that the abdominal incision tends to be more caudal in OVH, therefore making it more difficult to reach the ovaries. Ureteral obstruction, due to the inclusion of the ureter into the ligature, or the development of a ureterovaginal fistula are reported only following OVH. Granulomas of the ovarian (less common) or uterine (more common) pedicle may be due to the use of non-absorbable suture material, while inflammation of the uterine pedicle may occur if the most caudal part of the uterus is accidentally caught in the suture during OVH performed for a presenting complaint of pyometra. Pyometra may develop following OVX if an ovarian remnant is left in place and the bitch/queen resumes regular cycling following surgery, or if progestins are administered for medical reasons later in life.

Anesthetic and Surgical Issues for Early-Age Patients

Early-age patients should be in healthy conditions and normally hydrated before anesthesia and surgery. Also, proper immunization for the most common infectious diseases should have been previously performed. Although vaccination should be a prerequisite, vaccination failures may occur and death of immunized young dogs/cats entering a veterinary facility for castration purposes has been reported during the 7-day period following surgery. From a surgical point of view, neutering at a very early age is a very simple and quick, low-risk procedure. The incidence of short-term post-surgical complications is lower in young (<12 weeks of age) than in young adult (>24 weeks of age) animals and most of the complications are minor problems, such as swelling of the abdominal suture.

The following guidelines should be followed when performing surgical procedures in very young animals:

• In order to avoid hypoglycaemia, fasting prior to surgery should not be longer than 1 hour; also, eating should be allowed as soon as the patient is able to stand.
• The use of heating pads and a warm environment during and after surgery is recommended in order to avoid hypothermia, which occurs very commonly in young patients; hypothermia prolongs recovery time and slows the metabolism of anesthetic drugs.
• Controlling postoperative pain is fundamental to help return to normality, thereby stimulating appetite. Anti-inflammatory drugs are known to cause physeal cartilage damage following chronic use, but they may not be harmful following [sic] (although there is no information about side effects due to single treatments).
• The opioid pethidine provides analgesia and sedation without causing bradycardia; pethidine must be given exclusively IM because releases histamine causing pain when given IV.
• Avoid bradycardia-inducing drugs (such as alpha-agonists like medetomidine).
• Avoid long-acting drugs (such as acepromazine or tiletamine-zolazepam) as they prolong recovery time.
• Use short-acting drugs for induction of anesthesia (such as propofol or alfaxalone) to avoid drug residues during the recovery phase.
• Benzodiazepine can be used to increase sedation (thanks to its cardiovascular-sparing effect).
• If possible, use only volatile anesthesia during surgery.
• Atropine or glycopyrrolate are not advised as they decrease respiratory secretions by reducing the serous component, thereby potentially causing the development of dangerous mucous plugs.
• Buprenorphine can be associated as a single shot as it gives a long analgesic effect without CVS depression.
• The association ketamine-midazolam can be safely used in kittens as it stimulates the central nervous system without causing any depression of the cardiorespiratory function.

Conclusions

Prepubertal neutering is probably an acceptable technique for dogs and cats when it is performed at a shelter. Health risks are minimal and there are advantages due to the lower incidence of side effects when compared to performing it in adult animals. However, the choice of neutering a very young (<3 months) or even an adult pet should be thoroughly discussed with the owner, carefully highlighting advantages and disadvantages. Once a decision on neutering has been taken, the option of delaying neutering until the anestrus following puberty in bitches should be considered because of the potential beneficial effects on the development of the urogenital system.

References

1.  Okkens AC, Kooistra HS, Nickel RF. Comparison of long-term effects of ovariectomy vs ovariohysterectomy in bitches. J Reprod Fertil Suppl. 1997;51:227–231.

2.  Johnston SD, Root-Kustritz MV, Olson PNS. Prevention and termination of canine pregnancy. In: Johnston SD, Root-Kustritz MV, Olson PNS, eds. Canine and Feline Theriogenology. WB Saunders; 2001:165–192.

3.  van Goethem B, Schaefers-Okkens A, Kirpensteijn J. Making a rational choice between ovariectomy and ovariohysterectomy in the dog: a discussion of the benefits of either technique. Vet Surg. 2006;35:136–143.

4.  Whitehead M. Ovariectomy versus ovariohysterectomy (Letter). Vet Rec. 2006;159:723–724.

5.  Becker RL, Giles RC, Hildebrandt PK. Coitally induced peritonitis in a dog. Vet Med Small Anim Clin. 1974;10:53–54.

6.  Kustritz MV. Determining the optimal age for gonadectomy of dogs and cats. J Am Vet Med Assoc. 2007;231(11):1665–1674.

7.  Schneider R, Dorn CR, Taylor DO. Factors influencing canine mammary cancer development and postsurgical survival. J Natl Cancer Inst. 1969;43:1249–1261.

8.  Niskanen M, Thrusfield MV. Associations between age, parity, hormonal therapy and breed, and pyometra in Finnish dogs. Vet Rec. 1998;143:493–498.

9.  Hart BL. Problems with objectionable sociosexual behavior in dogs and cats: therapeutic use of castration and progestins. Comp Cont Ed Pract Vet. 1979;1:461–465.

10.  Salmeri KR, Olson PN, Bloomberg MS. Elective gonadectomy in dogs: a review. J Am Vet Med Assoc. 1991;198:1183.

11.  Howe LM. Short-term results and complications of prepubertal gonadectomy in cats and dogs. J Am Vet Med Assoc. 1997;211:57–62.

12.  Olson PN, Kustritz MV, Johnston SD. Early-age neutering of dogs and cats in the United States. J Reprod Fertil Suppl. 2001;57:223–32.

13.  Root MV, Johnston SD, Olson PN. The effect of prepuberal and postpuberal gonadectomy on radial physeal closure in male and female domestic cats. Vet Radiol Ultrasound. 1997;38(1):42–7.

14.  Langley-Hobbs SJ. A Salter Harris type II fracture of the distal ulna in a fourteen month female neutered Great Dane. Vet Comp Orthop Traumatol. 2005;18(1):43–5.

15.  Spain CV, Scarlett JM, Houpt KA. Long-term risks and benefits of early-age gonadectomy in dogs. J Am Vet Med Assoc. 2004a;224:380.

16.  Spain CV, Scarlett JM, Houpt KA. Long-term risks and benefits of early-age gonadectomy in cats. J Am Vet Med Assoc. 2004b;224:372.

17.  Overall KL. Working bitches and the neutering myth: sticking to science. Vet J. 2007;173:9–11.

18.  Kim HH, Yeon SC, Houpt KA, Lee HC, Chang HH, Lee HJ. Effects of ovariohysterectomy on reactivity in German shepherd dogs. Vet J. 2006;172(1):154–9.

19.  Martin LJM, Siliart B, Dumon HJW, Nguyen P. Spontaneous hormonal variations in male cats following gonadectomy. J Feline Med Surg. 2006;8:309–314.

20.  Dannucci GA, Martin RB, Patterson-Buckendahl P. Ovariectomy and trabecular bone remodeling in the dog. Calcif Tissue Int. 1987;40:194–199.

21.  Pearson H. The complications of ovariohysterectomy in the bitch. J Small Anim Pract. 1973;14:257–266.

22.  Dorn AS, Swist RA. Complications of canine ovariohysterectomy. J Am Anim Hosp Assoc. 1977;13:720–724.

23.  Berzon JL. Complications of elective ovariohysterectomies in the dog and cat at a teaching institution: clinical review of 853 cases. Vet Surg. 1979;8:89–91.

24.  Pollari F, Bonnet BN, Bamsey SC, et al. Postoperative complications of elective surgeries in dogs and cats determined by examining electronic and paper records. J Am Vet Med Assoc. 1996;208:1882–1886.

25.  Burrow R, Batchelor D, Cripps P. Complications observed during and after ovariohysterectomy of 142 bitches at a veterinary teaching hospital. Vet Rec. 2005;157:829–833.