Introduction

Salmonella is a rod-shaped gram-negative bacterium of the family Enterobacteriaceae that is commonly present in the gastrointestinal tract in humans and animals. Salmonella occurs worldwide in a variety of species and poses a public health issue because of its zoonotic potential. Humans are primarily infected with Salmonella as a food-borne illness. Dogs are exposed to Salmonella most commonly through the fecal–oral route. Common causes of inoculation in dogs include raw diets, contaminated water, hunting/scavenging of wildlife, and ingestion of feces from other carrier animals.¹ Reported risk factors for development of Salmonella infection in dogs are consumption of raw food, recent antibiotic or probiotic use, rural environments, and exposure to livestock.² Infection and severity of the disease relies on a variety of host and pathogen-related factors, including the amount of bacteria ingested, serovar, gastric acidity, and the host’s immune response.¹

Canine Salmonella can present as an acute or chronic gastrointestinal disease.³ Clinical signs can vary and include fever, malaise, anorexia, vomiting, diarrhea, and abdominal pain. By far, the most common type of infection in dogs is the carrier state, in which infected animals carry the pathogen for a variable period of time without showing any clinical signs.⁴ One study demonstrated that the prevalence of Salmonella in dogs is 2.5%, with only 55% of positive dogs experiencing diarrhea, highlighting the lack of correlation between clinical signs and isolation of Salmonella spp.² The prevalence of Salmonella shedding among dogs is extremely variable, ranging from approximately 1% to 20% for pet dogs to 70% to 90% for working dogs like racing greyhounds and sled dogs.^5–9

Extraintestinal infections are rare in both dogs and humans. Salmonella has been shown to be an inciting factor in cases including but not limited to pleuropulmonary disease, endocarditis, and urinary tract infections in humans.^10–12Salmonella has been connected to dogs with discospondylitis and isolated in the cerebrospinal fluid in a dog with meningoencephalitis.^13,14 This case study reports the first to describe an extraintestinal infection of Salmonella as an agent of bacteriuria and prostatitis in an immunocompetent dog with no history of a raw food diet.

Case Report

A 27.4 kg 7 yr old male Pit bull terrier mix from New Jersey was presented as a referral for a suspected prostatic cyst. He was presented to a primary emergency facility for a 3 day history of acute lethargy and anorexia. He was able to urinate, but his urine stream was noted to be prolonged. No significant previous medical history or medications were reported. His diet was commercial kibble with occasional hard-boiled eggs and cooked chicken. Physical examination revealed pain on caudal abdominal palpation. Cursory ultrasound revealed concern for a prostatic cyst. A complete blood count revealed a stress leukogram (white blood cell [WBC] 18,000 K/μL, reference range 5–16.5 K/μL; neutrophils 16.33 K/μL, reference range 2.95–11.64 K/μL). Serum biochemistry revealed a mixed hepatopathy with an increased alanine aminotransferase (ALT) activity (ALT 382 U/L, reference range 18–129 U/L) and alkaline phosphatase (ALP) activity (ALP 290 U/L, reference range 5–160 U/L). A mild hyperbilirubinemia (total bilirubin 0.5 mg/dL, reference range 0–0.3 mg/dL) was present without evidence of sample hemolysis. Urinalysis was performed that showed isosthenuria (specific gravity 1.008), pyuria (WBC 7/high-power field [HPF]; reference range 0–5 per HPF), and bacterial rods. The patient did not have antibodies to Anaplasma, Ehrlichia, or Borrelia as detectable by SNAP 4dx^a. The patient was prescribed carprofen^b (2.2 mg/kg per os [PO] q 12 hr) and enrofloxacin^c (10 mg/kg PO q 24 hr), and subsequently referred to a tertiary facility for further workup.

On presentation to the tertiary facility, the patient was estimated to be 5% dehydrated and was hypotensive, with a blood pressure of 60 mm Hg, which was responsive to crystalloid fluid boluses. He was extremely reactive and painful on caudal abdominal palpation. Rectal examination revealed a firm, enlarged, and painful prostate. A urinalysis via cystocentesis was repeated, which showed concentrated urine with a specific gravity of 1.032, marked pyuria (WBC >100/HPF, reference range 0–5/HPF), and marked rods present. Urine culture was submitted. An abdominal ultrasound was performed that showed marked prostatomegaly with multifocal echogenic fluid-filled cavitations and surrounding peritonitis (Figure 1). Ultrasound-guided percutaneous drainage of one of the prostatic cavitations was performed and submitted for bacterial culture. He was continued on enrofloxacin (10 mg/kg IV q 24 hr) pending the results of his urine and prostatic cultures.

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The following day, laboratory work revealed a progressive hepatopathy (ALT 229 U/dL, reference range 18–121 U/L; AST 191 U/L, reference range 15–55 U/L; ALP 939 U/L, reference range 5–160 U/L) with mild hyperbilirubinemia (total bilirubin 0.4 mg/dL, reference range 0–0.3 mg/dL). Because of concerns for sepsis, his antibiotic spectrum was broadened to include clindamycin^d (10 mg/kg IV q 12 hr) in addition to the enrofloxacin (10 mg/kg IV q 24 hr). He was discharged from the hospital, because of financial constraints, on gabapentin^e (10 mg/kg PO q 12 hr), carprofen (2.2 mg/kg PO q 12 hr) to be given when eating, mirtazapine^f (0.5 mg/kg PO q 24 hr), enrofloxacin (10 mg/kg PO q 24 hr), and clindamycin (11 mg/kg PO q 12 hr).

Urine culture and prostatic fluid both isolated Salmonella (>100,000 colony-forming units/mL), which was resistant to both gentamicin and amikacin but sensitive to enrofloxacin. Clindamycin was discontinued, and enrofloxacin was continued for a total of 8 wk.

Once Salmonella was diagnosed, the owner practiced prudent cleaning recommendations to prevent zoonotic transmission. Specifically, gloves were recommended when handling the patient’s feces and urine.³ Routine cleaning with disinfectants and cleaners were used in the household if he was to eliminate inappropriately in the house. It was recommended to keep the pet away from immunocompromised and/or young individuals. Recommendations were made to seek medical care if any family members became ill, febrile, or exhibited gastrointestinal signs like vomiting and diarrhea.

The patient was rechecked 1 mo later. At home, he was reportedly doing well with no overt concerns. He was only on enrofloxacin, no longer requiring pain medications or appetite stimulants. Repeat ultrasound revealed persistent but now anechoic prostatic cysts (Figure 2). Recheck blood work revealed a resolution of the previous noted abnormalities, including a resolved mixed hepatopathy and hyperbilirubinemia. Repeat urine culture collected via catheterization revealed no bacterial growth.

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Recheck evaluation was recommended 1 wk following cessation of antibiotic therapy. Because of noncompliance, the patient was rechecked 1 mo after completing the course of enrofloxacin. Repeat prostatic ultrasound showed similar anechoic cystic regions. Repeat prostatic and urine cultures were negative for growth, which confirmed successful clearance of Salmonella from the prostate and urine.

Based on the American College of Internal Medicine consensus statement, given the low sensitivity of fecal cultures when compared to polymerase chain reaction and intermittent shedding of Salmonella, multiple fecal cultures should be performed to rule out Salmonella infection.³ Repeat fecal cultures were recommended 1 wk after completing antibiotics to confirm clearance of Salmonella but were performed 1 mo following. Because of owner noncompliance, two serial fecal cultures were performed and were both negative. All fecal cultures remained negative, which confirmed no active infection with Salmonella. Once cleared from the infection, castration was recommended for the patient.¹⁵

Informed consent was obtained from the pet owner before case study publication. The patient described in this study was clinically managed according to contemporary standards of care as described in JAAHA Instructions for Authors.

Discussion

Salmonella bacteriuria has only been described in a few case reports in immunosuppressed dogs. The primary host of this specific serovar of Salmonella isolated in this case is poultry.¹⁸ Most hens are colonized through the fecal oral route with Salmonella Enteritidis but are asymptomatic carriers and intermittently shed the bacteria. Salmonella Enteritidis colonizes the avian reproductive organs and contaminates the internal contents of the egg. Undercooked or uncooked poultry meat and eggs pose a public health risk. To our knowledge, this is the first reported case of Salmonella in an immunocompetent dog with no known risk factors for development of infection.

There are three case reports that described Salmonella bacteriuria in dogs with all of them receiving immunosuppressive agents. In one report, a 5 yr old castrated male German shepherd dog being treated with immunosuppressive doses of prednisone (1.1 mg/kg q 12 hr for 10 wk) for immune-mediated polyarthropathy developed malodorous urine that cultured positive for Salmonella.¹⁹ It is suspected that the corticosteroid-mediated immunosuppression predisposed this patient to ascending bacteriuria, although enteric infection with Salmonella was never proven. Another case report described an estimated 5 yr old male stray Labrador retriever mix who developed Salmonella prostatitis after being on prednisone (1.1 mg/kg q 12 hr for 2 wk) and then prednisone (0.8 mg/kg q 12 hr for 3 wk) while being treated for a severe thrombocytopenia and Dirofilaria immitis, Ehrlichia, and Anaplasma infections.²⁰Salmonella was cultured both on urine and prostatic wash culture. An additional case report noted Salmonella bacteriuria in a young boxer after 2 mo of immunosuppressive therapy with prednisone (initially 1.6 mg/kg/day, then increased to 2.3 mg/kg/day) and azathioprine (2 mg/kg/day for 14 days, then 2 mg/kg q 48 hr) as treatment for a suspected relapse of steroid responsive meningoencephalomyelitis.¹⁴ Two months later, the dog presented for acute onset of neurologic signs. Urine culture and cerebrospinal fluid both isolated Salmonella enterica.

In humans, Salmonella bacteriuria has been described in older patients with underlying comorbidities or immunocompromise.^11,21 There are a few isolated reports of acute bacterial prostatitis and prostatic abscesses due to Salmonella infections in immunocompetent humans.^22,23 In one case report, recent travel to Africa played an important role in infection.²² In another report, the route of infection remained unconfirmed but was thought to either be hematogenous or an ascending infection via the urethra.²³

Conclusion

Extraintestinal Salmonella infections, especially of the urinary tract, are rare, in both humans and dogs. The few case reports in dogs describe Salmonella urinary tract infections in patients who are on immunosuppressive medications. This report describes a presumptively immunocompetent dog with acute prostatitis and prostatic abscessation due to Salmonella. This patient had physical examination and biochemical markers of early sepsis. The prostate was considered as the source of potential bacteremia in this case. Because the patient received no medications, was on a commercial diet, and had no exposure to livestock (i.e., poultry), the route of infection remains open, but an ascending infection via the urethra or hematogenous spread via the gastrointestinal system is considered likely. Enrofloxacin was chosen based on antimicrobial susceptibility testing results because this class of medication can cross an intact blood–prostate barrier. This case highlights the importance of considering Salmonella in bacterial prostatitis and urinary tract infections in immunocompetent patients. This should remain an uncommon differential when discussing canine prostatitis and prostatic abscessation.