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One Affectionate Puppy: A Case of Septic Arthritis Due to Staphylococcus Pseudintermedius

Bowen, Stephen MD*; DeMarco, Arielle PA-C*; Villasis, Lorillaine MS, SM; Barsi, James MD*; Handel, Andrew S. MD

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The Pediatric Infectious Disease Journal: October 2021 - Volume 40 - Issue 10 - p e381-e383
doi: 10.1097/INF.0000000000003201
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Abstract

Staphylococcus pseudintermedius is a commensal organism and frequent pathogen of dogs that has been increasingly recognized as a zoonotic pathogen of humans. The first documented human case involved an adult with an implanted cardioverter-defibrillator pocket infection in 2006.1 Since then, S. pseudintermedius has most frequently been described as a cause of skin and soft-tissue infections (SSTIs) among veterinary workers, dog owners, and individuals bitten by dogs. Infections can lead to significant morbidity in humans and have been associated with tissue necrosis.2 Treatment may be complicated by frequent antibiotic resistance.3

In this report, we describe an otherwise healthy child with septic arthritis due to S. pseudintermedius. We are unaware of any prior cases of S. pseudintermedius native joint septic arthritis or infection in an otherwise healthy child. The patient and her parents provided assent/consent for case publication.

CASE REPORT

A previously healthy 7-year-old female presented to the emergency department with a complaint of right ankle pain starting approximately 48 hours prior. She denied recent trauma, fevers, skin breaks, puncture wounds, or animal bites. She lived at home with her parents, healthy sister, and a recently acquired puppy. The family’s home is in a heavily wooded area endemic to Lyme disease. She was afebrile and hemodynamically stable at presentation. Examination demonstrated a right ankle effusion with warmth, diffuse tenderness to palpation, and limited mobility of the ankle joint secondary to pain.

Laboratory serum analysis demonstrated a white blood cell count of 11.6 K/µL (reference: 6.0–11.0 K/µL), erythrocyte sedimentation rate (ESR) of 5 mm/h (reference: 0–20 mm/h), and C-reactive protein (CRP) of 0.9 mg/dL (reference: 0.0–0.5 mg/dL). Radiographs of the right ankle were normal. Needle aspiration of the ankle synovial fluid yielded 8-mL of cloudy fluid consisting of 37,330 white blood cells/µL with 89% neutrophils. No organisms were seen on Gram stain. Magnetic resonance imaging of the ankle showed synovial thickening, moderate joint effusion, and synovitis of the peroneal tendons, with no evidence of osteomyelitis (Fig. 1). She was admitted to the hospital and started on intravenous cefazolin while synovial fluid culture and Lyme disease serology were pending.

FIGURE 1.
FIGURE 1.:
Magnetic resonance imaging T2 sequence of right ankle. Axial sequence demonstrating synovial thickening and effusion of right ankle (A). Sagittal sequence demonstrating peroneal tenosynovitis of right ankle (B).

While admitted she remained afebrile, though her symptoms were unchanged despite antibiotics. On hospital day 2, Lyme disease serology returned negative. On hospital day 3, her inflammatory markers trended upward (ESR of 69 mm/h and CRP of 1.7 mg/dL) and the synovial fluid aspirate culture grew rare Gram-positive cocci in clusters. The organism was beta-hemolytic on blood agar, catalase positive, and pyrrolidonyl arylamidase (PYR) positive. Slide coagulase testing was weak/borderline positive. Following 4 hours incubation at 37 °C, a tube coagulase test was negative at 4 hours but positive at 24 hours. The organism was then identified as S. pseudintermedius by VITEK 2 (“excellent” confidence level by GP ID card, software version 9.01, bionumber 070412075723231; bioMérieux, Inc., Hazelwood, MO). Antimicrobial resistance testing showed susceptibility to all antibiotics tested, including oxacillin, vancomycin, tetracycline, macrolides, levofloxacin, trimethoprim-sulfamethoxazole, and linezolid. Upon further discussion, the patient reported having frequent close contact with the puppy, including licking of the patient’s mouth and feet.

Due to positive aspiration results and upward trending inflammatory markers, the patient underwent a right ankle arthrotomy through a 1-cm anteromedial incision on hospital day 5. The articular cartilage of the tibiotalar joint appeared healthy. Repeat synovial fluid cultures were obtained, which were ultimately negative for bacterial growth. She was discharged later that day on cephalexin (100 mg/kg/d divided every 8 hours). Postoperatively, she began protected weight bearing and physical therapy. Four weeks after surgery, her ESR normalized (11 mm/h) and she reported a slightly decreased ankle range of motion but no pain; cephalexin was discontinued at that time. One month later, she was symptom free, had full motion of her ankle, and returned to full activity.

DISCUSSION

Our case describes an otherwise healthy child with septic arthritis due to S. pseudintermedius, an uncommon pathogen of growing importance. Her case offers multiple important lessons for clinicians. S. pseudintermedius is a rarely described pathogen in humans, though identification is increasingly common due to the use of more accurate diagnostic tools.4 Similar to previous cases, our patient reported extensive physical contact with a dog, but unlike prior reports, she did not have predisposing medical conditions or suffer a traumatic bite. We hypothesize that her infection was due to either transient bacteremia from a distant colonized site or local spread from microtrauma to the foot, which the dog licked frequently, though she lacked evidence of overt spread directly from the skin.

S. pseudintermedius is a skin and mucosal commensal organism estimated to colonize 90% of healthy dogs,5 and, less frequently, cats and horses. Initially classified as Staphylococcus intermedius, S. pseudintermedius was reclassified as its own species in 2005 based on biochemical and genetic distinctions. At the same time, the S. intermedius group (SIG) was formed, with the other two members being S. intermedius and Staphylococcus delphini. Over time, S. pseudintermedius has become a well-recognized cause of skin infections, otitis externa, and urinary tract infections in dogs.5 Among humans, the majority of published cases describe SSTIs.5

S. pseudintermedius possesses virulence factors responsible for severe necrotic infections. Similar to Staphylococcus aureus, S. pseudintermedius induces cell damage through the production of pathogenic enzymes including protease, DNase, and coagulase. S pseudintermedius also produces a secreted leukotoxin, Luk-I, that induces neutrophil lysis. Another class of staphylococcal toxins, phenol-soluble modulins, have also been identified and are responsible for the death of nonprofessional phagocytic cells.2

The recent increase in identification of S. pseudintermedius and other SIG members is likely due to prior species misclassification.6 SIG members share many biochemical similarities with S. aureus, making it difficult to distinguish these coagulase-positive staphylococcal species by conventional microbiologic techniques. Accordingly, one study of veterinary isolates found that, of 112 S. pseudintermedius isolates identified by matrix assisted laser desorption ionization-time of flight mass spectrometry (MALDI-ToF MS), VITEK assigned 13 as S. aureus, 85 as S. intermedius, and only 19 as S. pseudintermedius.6 Additionally, one study of S. delphini isolates found that 57.1% were identified as S. pseudintermedius,4 underscoring the challenges in differentiating SIG members. Alternatively, identification of S. aureus as an SIG member appears uncommon.6 Although MALDI-ToF MS is considered more accurate, incorrect species allocations also occur.4

Methicillin-resistant and multidrug resistant strains of S. pseudintermedius have been described and are increasingly common. A recent case series3 of S. pseudintermedius among 33 patients with chronic rhinosinusitis found an 82% resistance rate to penicillin and 27% to oxacillin. Resistance rates were also high for clindamycin (58%), erythromycin (58%), trimethoprim-sulfamethoxazole (45%), doxycycline (33%), and ciprofloxacin (30%). All isolates were susceptible to vancomycin. Alternatively, one review of 24 adults (mostly SSTIs) with S. pseudintermedius infections showed a 12.5% methicillin resistance rate.5 Notably, the conventional technique of using cefoxitin to determine methicillin susceptibility among S. aureus isolates may be unreliable in S pseudintermedius, which relies on oxacillin testing. Correct species identification is therefore crucial for accurately determining methicillin susceptibility. Direct detection of the mecA gene may also be considered.

We are aware of only two prior pediatric cases of S. pseudintermedius infection. The first describes a 6-year-old with hemophilia B and a pet dog who developed a pocket infection of his implanted intravascular port.7 A second case describes a 4-month-old boy with extensive eczema and recent surgical treatment of neuroblastoma who developed bacteremia after being licked by his dog.8 As the SIG had not been divided into subspecies including S. pseudintermedius until 2005, prior literature may include relevant cases. Previously described were 3 healthy children with S. intermedius infections, including a 13-year-old with infected sutures, a healthy 4-year-old with a brain abscess, and a healthy 11-month-old with meningitis.9 It is unknown if those isolates were actually S. pseudintermedius.

Our case describes the first known episode of native joint septic arthritis due to S. pseudintermedius. Pediatric septic arthritis is a relatively uncommon infection, with rates estimated as low as 1 per 100,000 in the United States.10 Aspiration is an important part of the diagnostic work up and can help identify a pathogen. Early antibiotic treatment and surgical joint irrigation is crucial to prevent chondrolysis and morbidity. Broad-spectrum antibiotics may be needed in the case of resistant S. pseudintermedius strains.

Although S. pseudintermedius was not confirmed in our case by a second assay, evidence supports that identification. The patient reported extensive preceding contact with a dog, and VITEK 2 appears unlikely to classify S. aureus isolates as an SIG member.6 Furthermore, the benchside testing showed PYR positivity, weak slide coagulase positivity, and a delayed tube coagulase-positive result, all consistent with S. pseudintermedius and inconsistent with S. aureus.

S. pseudintermedius is a rare pathogen with the potential to cause severe necrotic infections. With the expanding use of more accurate technology, particularly MALDI-ToF MS, a growing number of cases have been identified and reported. Although uncommon, S. pseudintermedius should be considered if the patient has regular contact with dogs. In such cases, close attention should be paid to drug-resistance patterns. As in vitro methicillin susceptibility may be misleading, patients should be monitored closely for their response to antimicrobials.

REFERENCES

1. Van Hoovels L, Vankeerberghen A, Boel A, et al. First case of Staphylococcus pseudintermedius infection in a human. J Clin Microbiol. 2006;44:4609–4612.
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4. Canver MC, Tekle T, Compton ST, et al. Performance of five commercial identification platforms for identification of Staphylococcus delphini. J Clin Microbiol. 2019;57:e00721–e00719.
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7. Chuang CY, Yang YL, Hsueh PR, et al. Catheter-related bacteremia caused by Staphylococcus pseudintermedius refractory to antibiotic-lock therapy in a hemophilic child with dog exposure. J Clin Microbiol. 2010;48:1497–1498.
8. Blondeau LD, Rubin JE, Deneer H, et al. Bacteremia with Staphylococcus pseudintermedius in a 4 month old pediatric oncology patient. J Chemother. 2020;32:260–262.
9. Frank MG, Kenison A, Madinger N, et al. Staphylococcus intermedius group infections in humans: report of four cases and a literature review. JMM Case Rep. 2015;2. doi: 10.1099/jmmcr.0.000066.
10. Kang SN, Sanghera T, Mangwani J, et al. The management of septic arthritis in children: systematic review of the English language literature. J Bone Joint Surg Br. 2009;91:1127–1133.
Keywords:

septic arthritis; Staphylococcus pseudintermedius; zoonotic infection; dogs

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