A short overview of Clostridium perfringens: Relevancy, Toxinotypes, Clinical Impacts, and the Challenges of Biofilm Formation
Keywords:
Clostridium perfringens, infection and pathogenesis, toxinotypes, clinical manifestations, biofilm formationAbstract
C.perfringens, a ubiquitous bacterium, is implicated in a series of recent outbreaks across Europe, reflecting its significance in public health. The organism manifests different clinical presentations in both human and animal hosts. In the realm of veterinary science, its pathogenesis in species such as poultry, cattle, swine, and equines is of particular concern due to the economic implications stemming from morbidity and mortality rates. The enterotoxins produced by this bacterium is the primary cause of symptoms like watery diarrhea, abdominal pains, and cramps in humans, and leads to conditions such as clostridial myonecrosis and necrotic enteritis in animals. An important aspect of its virulence strategy is its ability to form biofilms. These sophisticated microbial assemblages confer an augmented resistance against environmental challenges and antimicrobial interventions. This review consolidates information about C. perfringens outbreaks in Europe, mode of infection, pathogenesis in various animals, associated clinical symptoms, and the nuances of its biofilm formation. The present literature synthesis could provide valuable insights for forthcoming preventive and therapeutic initiatives.
References
Lucey, B.P. and G.M. Hutchins, William H. Welch, MD, and the discovery of Bacillus welchii. Arch Pathol Lab Med, 2004. 128(10): p. 1193-5.
Kiu, R. and L.J. Hall, An update on the human and animal enteric pathogen Clostridium perfringens. Emerg Microbes Infect, 2018. 7(1): p. 141.
Stevens, D.L. and A.E. Bryant, The role of clostridial toxins in the pathogenesis of gas gangrene. Clin Infect Dis, 2002. 35(Suppl 1): p. S93-s100.
Kiu, R., et al., Probing Genomic Aspects of the Multi-Host Pathogen Clostridium perfringens Reveals Significant Pangenome Diversity, and a Diverse Array of Virulence Factors. Front Microbiol, 2017. 8: p. 2485.
Charlebois, A., M. Jacques, and M. Archambault, Biofilm formation of Clostridium perfringens and its exposure to low-dose antimicrobials. Front Microbiol, 2014. 5: p. 183.
Uzal, F.A., et al., Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease. Future Microbiol, 2014. 9(3): p. 361-77.
Kevenk, T.O., et al., Detection of Clostridium perfringens and determination of enterotoxin genes (cpa and cpe) in traditional turkish chicken doner kebab. 2022.
Takehara, M., et al., Clostridium perfringens α-Toxin Impairs Innate Immunity via Inhibition of Neutrophil Differentiation. Sci Rep, 2016. 6: p. 28192.
Ma, Y., et al., Epsilon toxin–producing Clostridium perfringens colonize the multiple sclerosis gut microbiome overcoming CNS immune privilege. The Journal of Clinical Investigation, 2023. 133(9).
Maikanov, B., et al., Clostridium botulinum and Clostridium perfringens occurrence in Kazakh honey samples. Toxins, 2019. 11(8): p. 472.
Mandal, M.D. and S. Mandal, Honey: its medicinal property and antibacterial activity. Asian Pacific journal of tropical biomedicine, 2011. 1(2): p. 154-160.
Wang, G., et al., Analysis of the germination of individual Clostridium perfringens spores and its heterogeneity. Journal of applied microbiology, 2011. 111(5): p. 1212-1223.
Labbé, R.G. and V.K. Juneja, Chapter 6 - Clostridium perfringens Gastroenteritis, in Foodborne Infections and Intoxications (Fourth Edition), J.G. Morris and M.E. Potter, Editors. 2013, Academic Press: San Diego. p. 99-112.
Boqvist, S., K. Söderqvist, and I. Vågsholm, Food safety challenges and One Health within Europe. Acta Veterinaria Scandinavica, 2018. 60(1): p. 1.
Gharieb, R., et al., Insights on toxin genotyping, virulence, antibiogram profiling, biofilm formation and efficacy of disinfectants on biofilms of Clostridium perfringens isolated from poultry, animals and humans. J Appl Microbiol, 2021. 130(3): p. 819-831.
Hailegebreal, G., A Review on Clostridium Perfringens Food Poisoning. 2017.
Fourie, J.C.J., et al., Inside environmental Clostridium perfringens genomes: antibiotic resistance genes, virulence factors and genomic features. Journal of Water and Health, 2020. 18(4): p. 477-493.
Beres, C., et al., Prevalence and Characterisation of Clostridium perfringens Isolates in Food-Producing Animals in Romania. Microorganisms, 2023. 11(6): p. 1373.
Varga, J.J., B. Therit, and S.B. Melville, Type IV pili and the CcpA protein are needed for maximal biofilm formation by the gram-positive anaerobic pathogen Clostridium perfringens. Infect Immun, 2008. 76(11): p. 4944-51.
Butucel, E., et al., Farm Biosecurity Measures and Interventions with an Impact on Bacterial Biofilms. Agriculture, 2022. 12(8): p. 1251.
Carey, J., et al., Determination of genomic epidemiology of historical Clostridium perfringens outbreaks in New York State by use of two web-based platforms: National Center for Biotechnology Information Pathogen Detection and FDA GalaxyTrakr. Journal of Clinical Microbiology, 2021. 59(2): p. 10.1128/jcm. 02200-20.
Mahamat Abdelrahim, A., et al., Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France. Front Microbiol, 2019. 10: p. 777.
Freedman, J.C., A. Shrestha, and B.A. McClane, Clostridium perfringens Enterotoxin: Action, Genetics, and Translational Applications. Toxins (Basel), 2016. 8(3).
Zamanpour, S., G. Shakeri, and A. Afshari, Epidemiological Evaluation of Water-and Foodborne Outbreaks in the United States and Europe. Journal of Nutrition, Fasting & Health, 2022. 10(3).
Álvarez-Pérez, S., et al., Prevalence and characteristics of Clostridium perfringens and Clostridium difficile in dogs and cats attended in diverse veterinary clinics from the Madrid region. Anaerobe, 2017. 48: p. 47-55.
Neumann, T., et al., Innovative and Highly Sensitive Detection of Clostridium perfringens Enterotoxin Based on Receptor Interaction and Monoclonal Antibodies. Toxins (Basel), 2021. 13(4).
Abdel-Glil, M.Y., et al., Comparative in silico genome analysis of Clostridium perfringens unravels stable phylogroups with different genome characteristics and pathogenic potential. Scientific Reports, 2021. 11(1): p. 6756.
Timbermont, L., et al., Necrotic enteritis in broilers: an updated review on the pathogenesis. Avian Pathol, 2011. 40(4): p. 341-7.
Arshi, A., et al., Incidence of Clostridium perfringens in Intestinal Contents of Domestic Livestock Detected by PCR. 2017. 1: p. 1-6.
Feng, Y., et al., Phylogenetic and genomic analysis reveals high genomic openness and genetic diversity of Clostridium perfringens. Microbial Genomics, 2020. 6(10).
Li, G., et al., An outbreak of gangrenous dermatitis in commercial broiler chickens. Avian Pathol, 2010. 39(4): p. 247-53.
Hussain, R., et al., Clostridium perfringens Types A and D Involved in Peracute Deaths in Goats Kept in Cholistan Ecosystem During Winter Season. Front Vet Sci, 2022. 9: p. 849856.
Petit, L., M. Gibert, and M.R. Popoff, Clostridium perfringens: toxinotype and genotype. Trends in Microbiology, 1999. 7(3): p. 104-110.
Posthaus, H., et al., Clostridium perfringens type C necrotic enteritis in pigs: diagnosis, pathogenesis, and prevention. J Vet Diagn Invest, 2020. 32(2): p. 203-212.
Li, J., et al., Toxin Plasmids of Clostridium perfringens. Microbiology and Molecular Biology Reviews, 2013. 77(2): p. 208-233.
Finnie, J.W. and F.A. Uzal, Pathology and Pathogenesis of Brain Lesions Produced by Clostridium perfringens Type D Epsilon Toxin. International Journal of Molecular Sciences, 2022. 23(16): p. 9050.
Wang, J., et al., Type identification and histopathological analysis of Clostridium perfringens type D infection in Suffolk rams. Journal of Biotech Research, 2023. 15: p. 151-161.
Redondo, L.M., et al., Clostridium perfringens Type E Virulence Traits Involved in Gut Colonization. PLOS ONE, 2015. 10(3): p. e0121305.
Bhunia, A.K. and A.K. Bhunia, Clostridium botulinum, Clostridium perfringens, Clostridium difficile. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis, 2018: p. 209-228.
Lee, K.W. and H.S. Lillehoj, Role of Clostridium perfringens Necrotic Enteritis B-like Toxin in Disease Pathogenesis. Vaccines (Basel), 2021. 10(1).
Fernandez Miyakawa, M.E., O. Zabal, and C. Silberstein, Clostridium perfringens epsilon toxin is cytotoxic for human renal tubular epithelial cells. Human & experimental toxicology, 2011. 30(4): p. 275-282.
Li, J., et al., Characterization of NanR Regulation of Sialidase Production, Sporulation and Enterotoxin Production by Clostridium perfringens Type F Strains Carrying a Chromosomal Enterotoxin Gene. Toxins, 2022. 14(12): p. 872.
Caserta, J.A., et al., Development and application of a mouse intestinal loop model to study the in vivo action of Clostridium perfringens enterotoxin. Infect Immun, 2011. 79(8): p. 3020-7.
Mehdizadeh Gohari, I., et al., NetF-producing Clostridium perfringens and its associated diseases in dogs and foals. J Vet Diagn Invest, 2020. 32(2): p. 230-238.
Bryant, A.E. and D.L. Stevens, Clostridial myonecrosis: new insights in pathogenesis and management. Current infectious disease reports, 2010. 12: p. 383-391.
Uzal, F.A., et al., Clostridial Diseases of Horses: A Review. Vaccines, 2022. 10(2): p. 318.
Fu, Y., T. Alenezi, and X. Sun, Clostridium perfringens-Induced Necrotic Diseases: An Overview. Immuno, 2022. 2(2): p. 387-407.
Mehdizadeh Gohari, I., et al., Pathogenicity and virulence of Clostridium perfringens. Virulence, 2021. 12(1): p. 723-753.
Meyer, A., J. Liess, and K. Piepenbrink, Clostridium perfringens Adhesion Through Type IV Pili. 2020.
Hu, W.S., et al., Biofilm and Spore Formation of Clostridium perfringens and Its Resistance to Disinfectant and Oxidative Stress. Antibiotics, 2021. 10(4): p. 396.
Charlebois, A., M. Jacques, and M. Archambault, Comparative transcriptomic analysis of Clostridium perfringens biofilms and planktonic cells. Avian pathology, 2016. 45(5): p. 593-601.
