History

A 3-year-old 2.96-kg (6.5-lb) sexually intact male Devon Rex was presented to the Bailey Small Animal Teaching Hospital at Auburn University College of Veterinary Medicine for breeding soundness evaluation. The owner, an established cat breeder, had acquired the tom when it was 5 months old, and it was the only tom in the household shared with 5 queens, 2 of which had each produced a litter sired by a different tom in the previous year. The owner also reported that the tom first showed interest in mating at approximately 1.5 years of age and had always had free access to mate with the 5 queens in the household. Although the owner reported observing numerous and seemingly successful matings between the tom and queens, no kittens were produced. The tom was up-to-date on its vaccinations and had tested negative for FeLV and FIV, all conducted by its regular veterinarian. Six months before the present examination, the tom's serum testosterone concentration was 193 ng/dL (reference range, > 40 ng/dL).

On physical examination, the tom was bright, alert, and responsive and had a rectal temperature of 38.5°C (101.3°F; reference range, 37.2°C to 39.2°C [99°F to 102.6°F]), heart rate of 168 beats/min (reference range, 90 to 240 beats/min), and respiratory rate of 28 breaths/min (reference range, 20 to 30 breaths/ min).¹ The remainder of the findings on physical examination were unremarkable.

Question

What diagnostic procedures are available for the assessment of fertility in a male cat?

Answer

After collection of a thorough patient history and a general physical examination, appropriate diagnostic procedures to assess fertility in a tom include assessment of the testicles through palpation and ultrasonography, evaluation of the penis, collection and evaluation of semen (ie, for sperm motility, morphology, and concentration), and measurement of serum concentrations of testosterone and estrogen.

Results

Because the client was an established cat breeder and had provided a comprehensive history, initial assessments for this tom focused on the tom's suspected infertility. The tom was sedated with dexmedetomidine (0.07 mg/kg [0.03 mg/lb], IM) to facilitate examination of the external reproductive tract while also stimulating chemical ejaculation to facilitate the evaluation of semen quality.

Testicular palpation revealed that both testicles were fully descended into the scrotum; however, they were subjectively smaller and softer than expected for a 3-year-old tom. The penile sheath was unremarkable, and the penis had subjectively under-developed penile spines (Figure 1).

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Diagram of the reproductive anatomy in a male cat that illustrates the ideal extent of urinary catheter advancement (green arrow) for semen collection with chemical ejaculation. The inset photograph shows the glans penis of a sedated 3-year-old 2.96-kg (6.5-lb) sexually intact male Devon Rex during breeding soundness examination, showing that the penile spines are appreciable but less robust than expected. The tom's head and dorsum are toward the right and top, respectively, of the inset image.

Citation: Journal of the American Veterinary Medical Association 259, 1; 10.2460/javma.259.1.37

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Urethral catheterization was performed to collect sperm. Although 3 samples were recovered with 3 subsequent passages of the catheter, the samples contained no spermatozoa and chemical ejaculation was considered unsuccessful. Therefore, the sedated tom was given ketamine (0.67 mg/kg [0.30 mg/lb], IM) to induce general anesthesia, intubated, then given isoflurane in oxygen to maintain general anesthesia for semen collection with electroejaculation (EEJ). Once a good plane of anesthesia was achieved, a 1-cm-diameter X 12-cm-long rectal EEJ probe was lubricated and gently inserted into the rectum (Figure 2). No fecal blockage was encountered; thus, evacuation of the rectum was not needed. The EEJ probe was positioned so that the 3 electrodes near the tip of the probe were ventral and stimulated the accessory sex glands and base of the penis. The penis was manually extended and cleaned with sterile gauze moistened with sterile saline (0.9% NaCl) solution, then the penis was dried with sterile gauze. A sterile 2.0-mL plastic conical tube was then placed over the penis, and the tube and penis were directed ventrally in preparation for semen collection. The EEJ procedure was conducted as previously described,² and 100 [.proportional]L of clear ejaculate with no noticeable opacity was collected. Furthermore, no spermatozoa were detected with light microscopy in any sample collected with EEJ. Therefore, ultrasound-guided cystocentesis was performed to assess the possibility of retrograde ejaculation into the urinary bladder. The owner declined fine-needle aspirate sampling of the testicles, and the tom recovered from anesthesia without complication.

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Photograph of the cat described in Figure 1 undergoing general anesthesia for electroejaculation with the rectal probe (red arrow) in place and the rheostat (yellow arrow) rostral to the patient.

Citation: Journal of the American Veterinary Medical Association 259, 1; 10.2460/javma.259.1.37

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The urine sample was centrifuged at 5,000 X g for 10 minutes and then visually evaluated for a spermatozoal pellet, which was absent. The sediment was evaluated with light microscopy, and no spermatozoa were detected. To ensure that a complete ejaculation had been stimulated, samples collected during EEJ were pooled and submitted for alkaline phosphatase analysis. The pooled sample alkaline phosphatase activity was 27,068 U/L (lower reference limit, > 5,000 U/L), which indicated the presence of seminal fluid from a testicle or epididymis; thus, an azoospermic ejaculate had been collected.

Discussion

An accurate reproductive history is beneficial when devising a systematic approach to investigate a complaint of infertility.^1–5 Fertility is dynamic and can be influenced by the environment, temperament, age, nutrition, disease, and other factors.^1,3,4 Furthermore, infertility can be transient or permanent and can be associated with various prognoses.^3,4

An important reproductive characteristic of queens is that they are induced ovulators.^1–6 Induced ovulation indicates that the physical act of mating is required to stimulate the release of luteinizing hormone (LH), compared with the spontaneous release that occurs in most other domestic species. During coitus, caudally directed, keratinized spines along the glans penis of a tom are believed to stimulate the queen's reproductive tract and, through a neuroendocrine reflex, contribute to the release of LH from the queen's anterior pituitary gland.^1,3,4,6 Multiple matings are needed for the queen's serum concentration of LH to surge and trigger ovulation, and ovulation success nears 100% in queens mated at least 4 times during a given estrus.^5,6

For toms, infertility may be poorly characterized owing to the difficulty in obtaining semen samples.^2,3 Additionally, requests for veterinarians to assess characteristics of sperm from domestic cats are infrequent because many toms are castrated at an early age in efforts to decrease feral cat overpopulation and to diminish undesirable pet behaviors such as aggression, roaming, urine marking, and urine odor.^1,3 Oth er changes also related to castration are regression of the penile spines (reference range, 0.1 to 0.7 mm in length in toms) and atrophy of the prostate because these structures are androgen dependent.^1,3

Ultrasonography can be useful for breeding soundness examinations of toms. Ultrasound-guided cystocentesis was performed for the tom of the present report to collect a urine sample that was then assessed for whether retrograde ejaculation into the bladder had occurred. During normal ejaculation in toms, a portion of spermatozoa travels retrograde through the urethra and into the bladder, with 15% to 90% of the ejaculate traveling retrograde into the bladder.³ As performed for the tom of the present report, a urine sample collected by cystocentesis can be centrifuged and then the sample can be assessed for the visual presence or absence of a spermatozoal pellet at the bottom of the sample tube, the sediment can be evaluated with light microscopy, or both.

Ultrasonography can be used to assess accessory sex glands; however, to our knowledge, problems with and ultrasonic examination of accessory sex glands are rare in cats. Furthermore, ultrasonographic examination of a tom's testicles is most useful in assessing gross testicular architecture and size and, in anesthetized patients, guiding tissue sampling by fine-needle aspiration.

Semen analysis is an important component of breeding soundness examinations and may be diffi-cult in toms. Urethral catheterization as an option for collecting semen from a male cat is a relatively recent method with an approach that is familiar to most veterinarians.² A drawback to urethral catheterization is that it does not provide maximal sperm recovery.⁷ To facilitate ejaculation, cats undergoing urethral catheterization for semen collection should be heavily sedated with dexmedetomidine (65 to 70 [.proportional]g/kg [29.5 to 31.8 [.proportional]g/lb], IM), and waiting 20 minutes after administration of dexmedetomidine to pass the urinary catheter may improve sample collection.² The penis of the sedated tom is cleaned with sterile saline solution and gauze, then an open-ended tomcat urinary catheter is passed into the urethra for a distance of 9 cm for average-sized domestic cats (Figure 1), left in place for 1 to 2 minutes, and then removed.² Caution should be taken (eg, marking the catheter at 9 cm before placement) to avoid entry into the cat's bladder. Once removed, the urethral catheter is flushed with an appropriate semen extender and the collected sample is evaluated.

Semen can also be collected from cats by use of general anesthesia and EEJ, which consistently allows the collection of spermatozoa from fertile toms.^2,3 Drawbacks of this general anesthetic procedure largely relate to its need for specialized equipment, including a rheostat and cat-sized rectal probe. Operator training in EEJ is also essential. Ejaculates collected by EEJ are generally higher in volume and lower in spermatozoal concentration, compared with samples collected with the urethral catheterization method.

Although not used for the cat of the present report, another option for collecting semen is the use of an artificial vagina.^2,3 In cats, the use of an artificial vagina results in natural ejaculation and collection of the most representative sample for semen analysis; however, toms require conditioning to the process, and the conditioning may take approximately 4 months.²

After a semen sample is obtained from a cat, a complete semen analysis should be performed and include assessment of sperm motility (total and progressive), morphology, and concentration. When a complete semen evaluation fails to explain infertility in a tom, other diagnostic tests, such as hypo-osmotic swelling testing (to assess sperm cell membrane integrity) and sperm chromatin structure assay (to identify DNA fragmentation), should be performed to detect other spermatozoal defects that may be present.

Outcome

The owner elected to have the cat castrated. The surgery was scheduled and performed routinely, and removed testicles (Figure 3) were submitted for histologic evaluation.

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Photograph of the testicles removed from the tom described in Figure 1, showing a size discrepancy between the testicles. A No. 10 scalpel blade is included for size reference.

Citation: Journal of the American Veterinary Medical Association 259, 1; 10.2460/javma.259.1.37

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Histologic examination of the testicles revealed widespread, moderate sperm maturation arrest (Figure 4). Most of the seminiferous tubules had spermatogenic epithelium with germ cells to the level of primary spermatocytes; however, no maturation beyond the primary spermatocyte stage was observed.

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Photomicrograph of a section of testicular tissue from the tom described in Figure 1. Primary spermatocytes (red arrows) are the only stage of spermatogenesis present at the perimeter of the seminiferous tubules, and the tubule lumens lack mature spermatozoa, consistent with moderate sperm maturation arrest. Both Sertoli cells (black arrows) and Leydig cells (yellow arrow) are present. H&E stain; magnification 200X. Image courtesy of the Reproductive Pathology Service, The Ohio State University.

Citation: Journal of the American Veterinary Medical Association 259, 1; 10.2460/javma.259.1.37

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Sperm maturation arrest in domestic cats is an uncommon finding. In humans, the disorder may have genetic, idiopathic, iatrogenic, or acquired causes (eg, chemotherapy, radiation, endocrinopathy).⁸ The underlying cause of sperm maturation arrest in the cat of the present report was unknown, and despite azoospermia, this cat had adequate serum concentrations of testosterone 6 months earlier and displayed appropriate libido in its household with 5 queens. Castration was a suitable choice for this cat, given that the owner wanted to keep the cat in the household with intact queens. Mating of a queen by an azoospermic tom will likely induce ovulation and end the queen's estrus period, preventing any planned matings with a fertile tom from being successful and possibly increasing the likelihood of pyometra in the queen. Each time ovulation is induced in a queen, high serum progesterone concentrations are maintained, resulting in a state of pseudopregnancy, and return to estrus is prevented for approximately 40 days.⁴ Thus, castration and removal of this cat with azoospermia from a breeding role helped to preserve the fertility of the queens in the household.