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Pathogenic Characterization of Clostridium perfringens Strains Isolated From Patients With Massive Intravascular
Ai Suzaki1,2, Kaori Ohtani3, Shihoko Komine-Aizawa1
1Division of Microbiology, Department of Pathology and Microbiology, Nihon University School of Medicine, Tokyo, Japan.
Abstract:
Sepsis caused by Clostridium perfringens infection is rare but often fatal. The most serious complication leading to poor prognosis is massive intravascular hemolysis (MIH). However, the molecular mechanism underlying this fulminant form of hemolysis is unclear. In the present study, we employed 11 clinical strains isolated from patients with C. perfringens septicemia and subdivided these isolates into groups H and NH: septicemia with (n = 5) or without (n = 6) MIH, respectively. To elucidate the major pathogenic factors of MIH, biological features were compared between these groups. The isolates of two groups did not differ in growth rate, virulence-related gene expression, or phospholipase C (CPA) production. Erythrocyte hemolysis was predominantly observed in culture supernatants of the strains in group H, and the human erythrocyte hemolysis rate was significantly correlated with perfringolysin O (PFO) production. Correlations were also found among PFO production, human peripheral blood mononuclear cell (PBMC) cytotoxicity, and production of interleukin-6 (IL-6) and interleukin-8 (IL-8) by human PBMCs. Analysis of proinflammatory cytokines showed that PFO induced tumor necrosis factor-α (TNF-α), IL-5, IL-6, and IL-8 production more strongly than did CPA. PFO exerted potent cytotoxic and proinflammatory cytokine induction effects on human blood cells. PFO may be a major virulence factor of sepsis with MIH, and potent proinflammatory cytokine production induced by PFO may influence the rapid progression of this fatal disease caused by C. perfringens.
Insights
Clostridium perfringens sepsis can cause fatal massive intravascular hemolysis (MIH). Perfringolysin O (PFO) production strongly correlates with hemolysis and cytokine release, identifying it as a key virulence factor in this severe condition.
Area of Science:
- Microbiology
- Immunology
- Pathogenesis
Background:
- Sepsis from Clostridium perfringens is rare but frequently fatal.
- Massive intravascular hemolysis (MIH) is a severe complication associated with poor prognosis in C. perfringens sepsis.
- The molecular mechanisms driving MIH in C. perfringens sepsis remain poorly understood.
Purpose of the Study:
- To investigate the pathogenic factors contributing to massive intravascular hemolysis (MIH) in Clostridium perfringens sepsis.
- To compare biological features of C. perfringens strains isolated from patients with and without MIH.
- To elucidate the role of specific toxins, such as perfringolysin O (PFO) and phospholipase C (CPA), in the pathogenesis of MIH and associated inflammatory responses.
Main Methods:
- Clinical strains of C. perfringens from septicemia patients were isolated and categorized into groups with (H) or without (NH) MIH.
- Growth rates, virulence-related gene expression, CPA production, and erythrocyte hemolysis were compared between the groups.
- Perfringolysin O (PFO) production was quantified and correlated with hemolysis rates and human peripheral blood mononuclear cell (PBMC) cytotoxicity.
- Pro-inflammatory cytokine production (TNF-α, IL-5, IL-6, IL-8) by PBMCs in response to PFO and CPA was analyzed.
Main Results:
- C. perfringens isolates from patients with MIH (Group H) showed significantly higher erythrocyte hemolysis rates correlated with PFO production.
- PFO production correlated with PBMC cytotoxicity and the release of IL-6 and IL-8.
- PFO induced significantly stronger production of TNF-α, IL-5, IL-6, and IL-8 compared to CPA.
- No significant differences were observed in growth rate, general virulence gene expression, or CPA production between Group H and Group NH isolates.
Conclusions:
- Perfringolysin O (PFO) is identified as a major virulence factor in Clostridium perfringens sepsis associated with massive intravascular hemolysis (MIH).
- PFO's potent ability to induce cytotoxic effects and potent pro-inflammatory cytokine production likely contributes to the rapid progression and poor prognosis of this fatal condition.
- Targeting PFO may be a crucial strategy for managing severe C. perfringens infections complicated by MIH.
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