Introduction

Abortions in dogs can be broadly divided into infectious and noninfectious etiologies. Infectious etiologies can be further grouped into viral, bacterial, fungal, and protozoal. The noninfectious etiologies of abortion include but are not limited to systemic illness, trauma, neoplasia, drugs, endocrine abnormalities, and fetal defects/congenital abnormalities.¹Salmonella species are motile, non–spore-forming, gram-negative bacilli.² The clinical syndrome most commonly reported with Salmonella infection is gastroenteritis, but bacteremia, endotoxemia, abscesses, pyothorax, abortion, stillbirth, and birth of weak puppies have also been reported.²Salmonella-induced abortion is common in other species such as horses, sheep, and cattle but is not well documented in canines.^3–5Salmonella is a reported cause of abortion in canines based on two published case series.^6,7 This case report is unique because this dog had evidence of blood and uterine culture growth of Salmonella subgenus IV, demonstrating both bacteremia and abortion in a dog.

Case Report

A 5 yr old 18.0 kg female whippet was presented to an academic teaching hospital for hyperthermia, vulvar discharge, lethargy, and inappetence. The dog was 53 days pregnant and had been artificially inseminated from a stud dog. She had two previous uneventful pregnancies. The dog’s diet history included commercial dog food and raw ground beef, as well as eating lizards outside. On examination, the dog had brown-yellow-colored, nonodorous vulvar discharge and a mild elevation in temperature (39.1°C), and the remainder of the physical examination was within normal limits for a 53-day-gravid dog. Complete blood count and chemistry profile were within reference range. Point-of-care abdominal ultrasound showed fetal heart rates >200 beats per minute. The dog was discharged home for monitoring.

The following day, the dog was returned to the hospital’s satellite emergency clinic for evaluation following five stillborn puppies and hyperthermia. The dog had a mildly elevated temperature of 39.2°C, but the remainder of the physical examination was unremarkable for a 54-day-gravid dog. A point-of-care complete blood count revealed leukopenia (white blood cell count 4.85 × 10⁹/L; reference range, 5.05–16.76 10⁹/L) characterized by a severe degenerative left-shifted neutropenia (neut 0.12 × 10⁹/L; reference range, 2.95–11.64 × 10⁹/L), suspected bands, and monocytosis (monos 1.51 × 10⁹/L; reference range, 0.16–1.12 × 10³/μL). A blood smear reviewed by a staff emergency clinician confirmed leukopenia with band neutrophils and occasional lymphocytes seen. An ionized calcium was low normal (1.18 mmol/L; reference range, 1.18– 1.35 mmol/L). Aerobic and anaerobic venous blood cultures and a Brucella Rapid Slide Agglutination Test^a were submitted. Point-of-care abdominal ultrasound showed fetal heart rates >200 bpm. Ampicillin/sulbactam^b (30 mg/kg IV), enrofloxacin^c (10 mg/kg IV), and maropitant citrate^d (1 mg/kg IV) were administered and the dog was referred back to the primary academic teaching hospital.

On presentation, the dog’s vitals and physical examination were unremarkable. A venous blood gas showed a mild hyponatremia (Na 141.7 mmol/L; reference range, 146–151 mmol/L) but was otherwise unremarkable. Mild fever and neutropenia raised concerns for sepsis, suspected to be from a pyometra concurrent with pregnancy; therefore, an ovariohysterectomy was recommended for source control.

The dog was premedicated with methadone^e (0.25 mg/kg IV) and anesthesia was induced with ketamine^f (2 mg/kg IV and propofol^g (2.2 mg/kg IV) titrated to effect. A ventral midline celiotomy was performed and the uterus was exteriorized. Five nonviable fetuses were present in the uterus, four in the uterine horns and one in the uterine body/vaginal canal. An ovariohysterectomy was performed. Samples submitted included a sterile uterine sample for aerobic and anaerobic culture, uterine tissues for histopathology, and fetuses for necropsy. During anesthesia, she was administered lidocaine^h (2 mg/kg IV) and maintained on a ketamine^f constant rate infusion at 10 μ/kg/min for pain. Perianesthetic hypotension was reported with the lowest invasive arterial blood pressure measuring 110 mm Hg systolic, 38 mm Hg diastolic, and 54 mm Hg mean arterial pressure. Carprofenⁱ (4.4 mg/kg subcutaneously) was administered following anesthetic recovery. Postoperatively, the dog received ampicillin/sulbactam^b (30 mg/kg IV q 8 hr), methadone^e (0.1 mg/kg IV q 6 hr), gabapentin^j (6 mg/kg per os [PO] q 8 hr), and carprofen^k (1.5 mg/kg PO q 12 hr).

The dog was discharged approximately 24 hr postoperatively on gabapentin^j (6 mg/kg PO q 8 hr for 4 days), carprofen^k (1.5 mg/kg PO q 12 hr for 4 days), and amoxicillin/clavulanate^l (14 mg/kg PO q 12 hr for 8 days).

The dog was negative for Brucella canis antibody by Rapid Slide Agglutination test^a. The venous blood and uterine cultures grew a gram-negative bacillus that was speciated as Salmonella subgenus IV. Based on in vitro sensitivities, the bacteria was not sensitive to amoxicillin/clavulanate. A phone call to the owner at this time indicated that the dog was doing well with no reported clinical signs.

The dog was re-evaluated 2 wk later for an incision recheck. The incision was clean, dry, intact, and appropriately healed. Venous aerobic and anaerobic blood cultures and fecal Salmonella screening were all submitted at this visit. Cultures submitted at the recheck appointment were negative for bacterial growth. The owner was notified by phone and reported that the dog was doing well with no evidence of persistent clinical signs. To the authors’ knowledge, this is the first case report of a Salmonella species suspected to be causing both bacteremia and late-term abortion in a dog.

Discussion

Salmonella is a reported cause of abortion in canines based on two published case series. Two boxer dogs cultured Salmonella panama reportedly causing abortion in 1983.⁶ There is also a case series reporting abortion in a pack of foxhounds with Salmonella montevideo isolated on rectal swabs after gaining access to a pit containing dead ewes and aborted fetuses.⁷ These previous case reports isolated Salmonella organisms from aborted fetuses and rectal swabs. This case report is relevant because this dog had evidence of blood and uterine culture growth of Salmonella subgenus IV, demonstrating bacteremia and concurrent intrauterine infection likely causing abortion in this dog.

Bacteremia is usually a transient, subclinical feature of Salmonella gastroenteritis that becomes clinically significant in immunosuppressed animals.² Some animals with bacteremia have severe gastroenteritis whereas others have a fever and no gastrointestinal signs. This dog had a fever and inappetence but no severe gastrointestinal signs such as vomiting, abdominal pain, or diarrhea.

In the present case, both the uterus and blood contained the Salmonella organism on culture. In utero Salmonella infection can cause abortions, but bacteremia and systemic illness have also been linked to abortion.^1,2 It is unclear whether the intrauterine Salmonella or bacteremia, or a combination of both, led to abortion in the dog. It is not routine practice to perform blood cultures in patients with pyometra, making the prevalence of bacteremia in pyometra unknown. One study states that pyometra results in sepsis in ∼60% of cases but bases the diagnosis of sepsis on physical examination and biochemical parameters rather than a positive blood culture.⁸

The dog’s susceptibility results showed resistance to amoxicillin/clavulanic acid and susceptibility to enrofloxacin. The dog received one dose of enrofloxacin and was continued on amoxicillin/clavulanic acid after her ovariohysterectomy. Although the bacteria was resistant to amoxicillin/clavulanic acid, the dog proceeded to make a full recovery. Source control via an ovariohysterectomy was likely the most important aspect of treatment. Source control has been repeatedly shown to be a vital aspect of the management of sepsis.^8–10

Only speculations can be made regarding the source of the Salmonella infection in this dog. The diet history noted that the dog often ate lizards while outside and also was occasionally fed raw ground beef. Infection of dogs and cats with Salmonella has been associated with the feeding of raw meat diets.^11–13 Also, many reptiles, if not all, carry some species of Salmonella,¹⁴ so this also may have served as a source of infection in this dog.

The culture performed grew Salmonella subgenus IV and was not further speciated. This is the main limitation of this case report. Further speciation may have helped to identify the source of salmonellosis in this dog, as well as helped identify the microbiological and zoonotic impact of this organism. Approximately 99% of Salmonella infections in humans and warm-blooded animals are from Salmonella subspecies I. The remainder of the Salmonella subspecies (II, IIIa, IIIb, IV, and VI) are usually isolated from cold-blooded animals and the environment.¹⁵

Potential zoonotic causes of abortion in canines include Brucella canis, Campylobacter, Leptospira, and Salmonella.¹ Vaginal discharges, placenta, and meconium have been reported to contain Salmonella organisms.² Zoonotic potential exists with other species of Salmonella; however, subgenus IV is not documented well in the literature.

Perianesthetic use of ketamine during pregnancy is controversial. Puppies were reportedly viable based on point-of-care ultrasonographic assessment of fetal heart rates before referral for ovariohysterectomy. Intraoperatively, all fetuses were nonviable. Ketamine, as a premedication or injectable induction agent in dogs undergoing caesarian section, has been associated with depressed respirations and neurological reflexes in puppies.^16,17 In human medicine, ketamine is used for spinal anesthesia during caesarian section and has been shown to delay requests from women for postoperative analgesics. The paucity of data available on neonatal outcome precludes recommendations in women for general anesthesia.¹⁸

Conclusion

This case report describes a unique presentation of salmonellosis in the dog. This dog had bacteremia and late-term abortion that grew an uncommon Salmonella species on blood and uterine culture. Salmonella should be included as a differential diagnosis for bacteremia and abortion. This case also serves as a reminder that dogs presenting for late-term abortion should be handled as a zoonotic risk.