Staphylococcus schleiferi subspecies coagulans septic shock in an immunocompetent male following canine otitis externa

Abstract

Staphylococcus schleiferi bacteremia is an underappreciated cause of septic shock in the critical care department. Although nominally a coagulase variable Staphylococcus and associated with otitis externa infections in canine species, it has been associated with the metastatic infection including osteomyelitis, endocarditis, nephritis, and meningitis in humans. This report records a possible zoonotic case of S. schleiferi subspecies coagulans bacteremia following canine otitis externa associated with septic shock and endovascular infection precipitating intensive care admission for vasopressor support in an immunocompetent male.

Introduction

Zoonotic transmission of Staphylococcus schleiferi from dogs to humans is an uncommon presentation, with only sporadic cases reported since it was first described in 1988.[1,2] Less commonly still, is it implicated with sepsis, where there is a paucity of data related to its management in critical care environments around the world.[3] A lack of virulence factors typically found in Staphylococcus aureus such as hyaluronidase (employed in tissue penetration) and traditional isolation in canine otitis externa, has led to its presumption as an uncommon opportunistic human pathogen. [4 6] However, the coagulase variable S.schleiferi has been implicated in metastatic infections in immunocompromised hosts including endocarditis, osteomyelitis, and meningitis.[1,7] Therefore, recognition of this association has pertinent implications for the management of undifferentiated septic patients. Given Staphylococcus aureus and S. schleiferi subspecies (ssp.) coagulans can both be coagulase positive, misidentification can occur if only coagulase testing is used to guide management in critically unwell patients.[5] This case report describes the importance of recognizing zoonotic exposure history in the prevention of S. schleiferi misidentification and rationalizing antibiotic management when encountering sepsis in critical care settings, including among immunocompetent patients.

Case Report

An 84 year old immunocompetent male presented with a 2-3 days history of right inguinal pain with associated fever, decreased appetite, and limited mobility. His history was significant for obesity, permanent atrial fibrillation on apixaban, chronic kidney disease stage IIIb, a distant repaired abdominal aortic aneurysm with an endovascular graft, and a motor vehicle accident 3 months prior resulting in a left knee hemarthrosis complicated by left lower limb cellulitis, subsequently treated and resolved. On arrival to the emergency department, he was found to be hypotensive with a blood pressure of 95/61 mmHg, borderline febrile to 37.8°C, hypoxic with an oxygen saturation of 90% on room air, and a heart rate of 75/min. His weight on admission was 114.4 kg. He remained alert and oriented throughout his presentation. Cardiovascular, inguinal, and ocular examinations were unremarkable, and there were no peripheral stigmata of infective endocarditis. Cellulitis was noted in the left lower limb, with erythema extending from his previous hemarthrosis scar, concerning for possible inoculation. Laboratory data revealed an acute on chronic renal impairment (creatinine: 111 μmol/L compared to 149 μmol/L 2 months prior (normal range: 64 - 128 μmol/L), albumin 32 g/L (35 - 50 g/L), total bilirubin 18 μmol/L which did not rise further (<20 μmol/L), creatinine kinase 72 U/L (46 - 171 U/L), aspartate aminotransferase/alanine transferase 14 (<45 U/L)/10 (<35 U/L), white cell count 8.7 × 10⁹/L (3.5-11.0×10⁹/L), neutrophil count 7.24×10⁹/L(2.00 - 8.00×10⁹/L), lymphocytes 0.66 × 10⁹/L (1.00 - 4.00 × 10⁹/L), pH 7.45 (7.35 - 7.45), HCO₃ 22 mmol/L (22 - 32 mmol/L), and lactate 2.3 mmol/L (0.5 - 2.2 mmol/L). Coagulation profile, lymphocyte subsets, immunoglobulin subsets, and HIV serology were unremarkable. C reactive protein was 95 mg/L initially, rising to 150 mg/L within 48 h. Within 24 h of presentation, Sequential Organ Failure Assessment (SOFA) score was 3. Early computer tomography (CT) angiography revealed no acute aortic syndrome and no vascular graft involvement. For empirical antibiotic therapy, he was commenced on intravenous (IV) flucloxacillin 2 g, gentamicin 420 mg, and vancomycin 1 g, in addition to IV crystalloid fluid resuscitation. Despite receiving three liters of fluid resuscitation, he required a metaraminol infusion to maintain a mean arterial pressure (MAP) >65 mmHg. Metaraminol infusion was chosen for shock over other vasopressors given his anticipated short duration of hemodynamic support, and the low doses (0.5 mg/h) required to maintain MAP > 65 mmHg. He was admitted to the intensive care unit for 3 days for ongoing hemodynamic monitoring. Hypoxia subsequently improved. Multiple daily blood cultures were positive, with S. schleiferi ssp. coagulans identified on associated Gram stain [Figure 1], and matrix assisted laser desorption/ionization time of flight mass spectrometry. Subspecies were confirmed with urease and coagulase positive testing. Blood cultures were repeatedly positive despite broadened antimicrobial therapy with IV piperacillin/tazobactam 4.5 g 6 h and IV vancomycin 2 g loading dose then 1 g twice daily. Once susceptibilities returned [Table 1], antimicrobials were rationalized to IV flucloxacillin.

Figure 1. Blood agar plate reading of blood culture result and subsequent Gram Stain of Staphylococcus schleiferi subspecies coagulans

Table 1. Antimicrobial susceptibility profile of Staphylococcus schleiferi subspecies coagulans

Transthoracic and transesophageal echocardiography were unremarkable for signs of infective endocarditis. Later, CT position emission tomography indicated moderate focal FDG uptake(SUVmax: 4.9) localizing to the proximal left iliac graft at the aortic bifurcation [Figure 2].

Figure 2. Coronal, sagittal, and axial CT‑PET images indicating moderate FDG uptake of the left iliac vascular graft at the aortic bifurcation. FDG: Fluorodeoxyglucose, CT‑PET: Computed tomography‑positron emission tomography

The patient’s history was revisited, and inadvertent close exposure to his unwell pet Maltese terrier’s otorrhea was noted. The canine’s otitis externa preceded the patient’s illness by a week and was treated with topical 23 mg/mL miconazole nitrate, 5 mg/mL prednisolone acetate, and 0.696 mg/mL polymyxin B twice daily for 10 days by the local veterinarian. The canine was known to lick the patient, and it was during the attempted application of antimicrobial treatment by the patient to his pet canine’s ears, that ocular and lower limb exposure to his canine’s otorrhea was noted on a background of his left knee hemarthrosis. Canine aural samples posttreatment tested positive for the Staphylococcus intermedius group (including Staphylococcus pseudintermedius) only.

Given the concern for iliac graft infection, a vascular surgical opinion was obtained. A consensus multidisciplinary team discussion concluded indefinite antimicrobial suppression with oral flucloxacillin 1 g twice a day following a 6 week course of IV flucloxacillin 2 g 4 h for presumptive vascular infection given comorbidities and age. Following complications including pulmonary edema secondary to fluid resuscitation, he underwent successful diuresis with daily furosemide and was discharged with outpatient parental antimicrobial therapy and oral antimicrobial suppression as planned.

Discussion

S. schleiferi is a coagulase variable Staphylococcus predominantly associated with canine otitis externa. S. schleiferi ssp. coagulans is rarely found in humans but is frequently isolated from healthy dogs from the skin, as well as being associated with otitis externa.[8,9] Although canine isolates were negative in this case, swabs were taken posttreatment which may have masked growth given the known efficacy of miconazole against Staphylococcus species, with preceding chronology suggestive of transmission.[10] In rare human cases, it is associated with metastatic infection in immunocompromised hosts but has not been previously described to require vasopressor support or intensive care monitoring, nor endovascular involvement.[1] In this described case, the patient required vasopressor support within 24 h of presentation, reaching a SOFA score of 3. The implications are pertinent, given how underrecognized this relationship between zoonotic exposure and endovascular infection with S. schleiferi may be. S. schleiferi ssp. coagulans is documented to be less pathogenic than S. schleiferi ssp. schleiferi.[11,12] This is relevant, given the S.schleiferi ssp. coagulans identified in this patient, his immunocompetent status, and the severe clinical sequelae as a result of bacteremia following probable zoonotic canine transmission. Although lacking in hyaluronidase found in Staphylococcus aureus, pathogenicity may be related to other virulence factors including β hemolysin, and the ability to form biofilms.[13] It is important to explore exposure history and recognize this in the critical care setting to rationalize investigations and antimicrobial therapy. Although not found in our microbiology results, S. schleiferi is associated with up to 57% oxacillin resistance and can have implications on an empirical antimicrobial choice until susceptibilities return.[9] This is pertinent in the acute care setting, given the impetus on rapid antimicrobial administration in sepsis. There is potential misidentification between S. schleiferi ssp. coagulans and Staphylococcus aureus if only coagulase testing is employed. Whereas S. schleiferi ssp. coagulans test negative with slide agglutination (clumping factor), Staphylococcus aureus tests positive.[14] Biochemical commercial systems, such as API Staph System (bioMérieux, Marcy l’Etoile, France), VITEK 2 (bioMérieux, Marcy l’Etoile, France), or BBL Crystal identification systems (Gram Positive ID Kit and Rapid Gram Positive ID Kit; Becton Dickinson), in conjunction with clumping factor and coagulase testing, can differentiate S. schleiferi ssp. coagulans from other coagulase positive Staphylococci by urease production and lack of maltose/mannose production, among others.[14,15] Therefore, early recognition by treating clinicians may lead to more appropriate antimicrobial choices and improved clinical outcomes for patients.

Conclusion

In summary, we describe the first documented case of probable zoonotic transmission of S. schleiferi in an otherwise immunocompetent human host resulting in septic shock requiring vasopressor support in the intensive care setting. Recognizing zoonotic exposure history is important in optimizing critical care investigations and antimicrobial therapy when encountering septic patients in the critical care setting. Furthermore, appropriate identification of S. schleiferi ssp. coagulans can avoid misdiagnosis and confusion with other Staphylococci in the management of unwell patients.

How to cite this article: K. Nguyen AD, Moran D, Eland CL, Wilks K. Staphylococcus schleiferi subspecies coagulans septic shock in an immunocompetent male following canine otitis externa. Turk J Emerg Med 2023;23:184-7.

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient has given his consent for his images and other clinical information to be reported in the journal. The patient understands that his name and initial will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

• Conceptualization: ADKN, DM, KW
• Data curation: ADK, CE, KW
• Methodology: ADKN
• Project administration: ADKN, KW
• Formal analysis: ADKN, KW
• Visualization: CE, KW
• Writing – original draft: ADKN, DM
• Writing – review and editing: ADKN, DM, KW, CE
• Supervision: KW.

None declared.

Informed Consent
Written and signed informed consent was obtained from the patient for the publication of this case report including accompanying images.

None declared.

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The authors would like to acknowledge all healthcare workers and microbiology staff at Pathology Queensland who were involved in the care of this patient.