Virulence and Pathogenicity of Clostridium perfringens

Shler Ali Khorseed^✉

College of sciences, Kirkuk university, Iraq

Received: April 22, 2024/ Revised: May 20, 2024/Accepted: May 29, 2024

(✉) Corresponding Author: shler-ali@uokirkuk.edu.iq

Abstract

Clostridium perfringens is anaerobic bacterium, exhibits a broad spectrum of pathogenicity with significant implications for human and animal health. Its virulence is intricately linked to the production of various toxins, notably alpha toxin, beta toxin, and epsilon toxin, which play pivotal roles in tissue damage and disease manifestation. The pathogen makes convoluted host-pathogen interactions requiring some kind of adhesion, colonization, and evasion of the host immune response Epidemiologically, C. perfringens could be a main reason for foodborne diseases, with Enterotoxigenic strains making gastroenteritis. Improper food handling practices play part in outbreaks. The field of veterinary epidemiology links C. perfringens to necrotic enteritis in poultry, which affects animal welfare and agricultural productivity. The significance of making collaborations with a One Health perspective when coping with issues related with C. perfringens is important. Surveillance, preventive measures, and outbreak examinations are seen to be included within interventions of public health. Understanding the epidemiology of C. perfringens could be essential for sake of implementing targeted strategies aiming at diminishing foodborne infections.

Keywords: Clostridium perfringens, Pathogenicity, Virulence.

References

Abraham, L. J., & Rood, J. I. (1985). Cloning and analysis of the Clostridium perfringens tetracycline resistance plasmid, pCW3. Plasmid, 13(3), 155–162.

https://doi.org/10.1016/0147-619x(85)90038-1

Abraham, L. J., & Rood, J. I. (1985). Molecular analysis of transferable tetracycline resistance plasmids from Clostridium perfringens. Journal of Bacteriology, 161(2), 636–640.

https://doi.org/10.1128/jb.161.2.636-640.1985

Abraham, L. J., & Rood, J. I. (1987). Identification of Tn4451 and Tn4452, chloramphenicol resistance transposons from Clostridium perfringens. Journal of Bacteriology, 169(4), 1579–1584. https://doi.org/10.1128/jb.169.4.1579-1584.1987

Abraham, L. J., & Rood, J. I. (1988). The Clostridium perfringens chloramphenicol resistance transposon Tn4451 excises precisely in Escherichia coli. Plasmid, 19(2), 164–168.

https://doi.org/10.1016/0147-619x(88)90055-8

Abraham, L. J., Berryman, D. I., & Rood, J. I. (1988). Hybridization analysis of the class P tetracycline resistance determinant from the Clostridium perfringens R-plasmid, pCW3. Plasmid, 19(2), 113–120. https://doi.org/10.1016/0147-619x(88)90050-9

Alemayehu, T., Ali, M., Mitiku, E., & Hailemariam, M. (2019). The burden of antimicrobial resistance at tertiary care hospital, southern Ethiopia: a three years’ retrospective study. BMC Infectious Diseases, 19(1). https://doi.org/10.1186/s12879-019-4210-1

Alonso, D., McKane, A. J., & Pascual, M. (2006). Stochastic amplification in epidemics. Journal of the Royal Society Interface, 4(14), 575–582. https://doi.org/10.1098/rsif.2006.0192

Alsayed, S. S. R., & Gunosewoyo, H. (2023). Tuberculosis: Pathogenesis, Current Treatment Regimens and New Drug Targets. International Journal of Molecular Sciences, 24(6), 5202. https://doi.org/10.3390/ijms24065202

Aly, S. S., Anderson, R. J., Whitlock, R. H., Fyock, T. L., McAdams, S. C., Byrem, T. M., . . . Gardner, I. A. (2012). Cost-effectiveness of diagnostic strategies to identify Mycobacterium avium subspecies paratuberculosis super-shedder cows in a large dairy herd using antibody enzyme-linked immunosorbent assays, quantitative real-time polymerase chain reaction, and bacterial culture. Journal of Veterinary Diagnostic Investigation, 24(5), 821–832.

https://doi.org/10.1177/1040638712452107

Amon, J. D., Artzi, L., & Rudner, D. Z. (2022). Genetic Evidence for Signal Transduction within the Bacillus subtilis GerA Germinant Receptor. Journal of Bacteriology, 204(2).

https://doi.org/10.1128/jb.00470-21

Amulic, B., Cazalet, C., Hayes, G. L., Metzler, K. D., & Zychlinsky, A. (2012). Neutrophil Function: From Mechanisms to Disease. Annual Review of Immunology, 30(1), 459–489.

https://doi.org/10.1146/annurev-immunol-020711-074942

BAŞ, B. (2022). WHAT TELL US THIS BIONUMBERS IN PLANT DEFENSE PROTEIN PHOSPHORYLATION. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi – C Yaşam Bilimleri Ve Biyoteknoloji, 11(1), 31–38.

https://doi.org/10.18036/estubtdc.907029

Benz, R., & Popoff, M. (2018). Clostridium perfringens Enterotoxin: The Toxin Forms Highly Cation-Selective Channels in Lipid Bilayers. Toxins, 10(9), 341.

https://doi.org/10.3390/toxins10090341

Camiade, E., Peltier, J., Bourgeois, I., Couture-Tosi, E., Courtin, P., Antunes, A., . . . Pons, J. L. (2010). Characterization of Acp, a Peptidoglycan Hydrolase of Clostridium perfringens with N -Acetylglucosaminidase Activity That Is Implicated in Cell Separation and Stress-Induced Autolysis. Journal of Bacteriology, 192(9), 2373–2384. https://doi.org/10.1128/jb.01546-09

Chauhan, A. (2023). Pearls in the Eye. Clinical Research and Clinical Reports, 02(03), 01–04.

https://doi.org/10.31579/2835-8325/017

Cheung, J. K., Adams, V., D’Souza, D., James, M., Day, C. J., Jennings, M. P., . . . Rood, J. I. (2020). The EngCP endo α-N-acetylgalactosaminidase is a virulence factor involved in Clostridium perfringens gas gangrene infections. International Journal of Medical Microbiology, 310(2), 151398.

https://doi.org/10.1016/j.ijmm.2020.151398

Edwards, R. T. (1905). Bacillus Mycogenes (Bacterium Mucogenum), Nov. Spec. An Organism Belonging To The Bacillus Mucosus Capsulatus Group. Journal of Infectious Diseases, 2(3), 431–435. https://doi.org/10.1093/infdis/2.3.431

Fernandez-Miyakawa, M. E., Marcellino, R., & Uzal, F. A. (2007). Clostridium perfringenstype A Toxin Production in 3 Commonly Used Culture Media. Journal of Veterinary Diagnostic Investigation, 19(2), 184–186 .

https://doi.org/10.1177/104063870701900208

Fjeld, J., Achten, N., Hilligoss, H., Nagy, A., & Srikumar, M. (2020). Principled Artificial Intelligence: Mapping Consensus in Ethical and Rights-Based Approaches to Principles for AI. SSRN Electronic Journal. https://doi.org/10.2139/ssrn.3518482

Food Microbiology: Fundamentals and Frontiers. Fourth Edition. Edited by Michael P. Doyle and Robert L. Buchanan. Washington (DC): ASM Press. $199.95. xix + 1118 p.; ill.; index. ISBN: 978-1-55581-626-1 (hc); 978-1-55581-846-3 (eb). 2013. (2013). The Quarterly Review of Biology, 88(2), 144–144. https://doi.org/10.1086/670570

Fragoulis, A., Tohidnezhad, M., Kubo, Y., Wruck, C. J., Craveiro, R. B., Bock, A., . . . Suhr, F. (2023). The Contribution of the Nrf2/ARE System to Mechanotransduction in Musculoskeletal and Periodontal Tissues. International Journal of Molecular Sciences, 24(9), 7722. https://doi.org/10.3390/ijms24097722

Garcia, J. P., Adams, V., Beingesser, J., Hughes, M. L., Poon, R., Lyras, D., . . . Uzal, F. A. (2013). Epsilon Toxin Is Essential for the Virulence of Clostridium perfringens Type D Infection in Sheep, Goats, and Mice. Infection and Immunity, 81(7), 2405–2414. https://doi.org/10.1128/iai.00238-13

GHONEIM, N., & HAMZA, D. (2017). Epidemiological studies on Clostridium perfringens food poisoning in retail foods. Revue Scientifique Et Technique De L’OIE, 36(3), 1025–1032. https://doi.org/10.20506/rst.36.3.2734

Grass, J. E., Gould, L. H., & Mahon, B. E. (2013). Epidemiology of Foodborne Disease Outbreaks Caused byClostridium perfringens, United States, 1998–2010. Foodborne Pathogens and Disease, 10(2), 131–136. https://doi.org/10.1089/fpd.2012.1316

Guidance on the risk assessment of food and feed from genetically modified animals and on animal health and welfare aspects. (2012). EFSA Journal, 10(1), 2501.

https://doi.org/10.2903/j.efsa.2012.2501

Ha, E., Chun, J., Kim, M., & Ryu, S. (2019). Capsular Polysaccharide Is a Receptor of a Clostridium perfringens Bacteriophage CPS1. Viruses, 11(11), 1002.

https://doi.org/10.3390/v11111002

Hall, A. J., Wikswo, M. E., Manikonda, K., Roberts, V. A., Yoder, J. S., & Gould, L. H. (2013). Acute Gastroenteritis Surveillance through the National Outbreak Reporting System, United States. Emerging Infectious Diseases, 19(8), 1305–1309.

https://doi.org/10.3201/eid1908.130482

Harwood, V. J., Staley, C., Badgley, B. D., Borges, K., & Korajkic, A. (2014). Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiology Reviews, 38(1), 1–40. https://doi.org/10.1111/1574-6976.12031

Hassan, K. A., Elbourne, L. D., Tetu, S. G., Melville, S. B., Rood, J. I., & Paulsen, I. T. (2015). Genomic analyses of Clostridium perfringens isolates from five toxinotypes. Research in Microbiology, 166(4), 255–263.

https://doi.org/10.1016/j.resmic.2014.10.003

Hatheway, C. L. (1990). Toxigenic clostridia. Clinical Microbiology Reviews, 3(1), 66–98.

https://doi.org/10.1128/cmr.3.1.66

Havelaar, A. H., Kirk, M. D., Torgerson, P. R., Gibb, H. J., Hald, T., Lake, R. J., . . . Devleesschauwer, B. (2015). World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLOS Medicine, 12(12), e1001923. https://doi.org/10.1371/journal.pmed.1001923

Huang, X. Y., Sun, W. Y., Yan, Z. Q., Shi, H. R., Yang, Q. L., Wang, P. F., . . . Gun, S. B. (2019). Novel Insights reveal Anti-microbial Gene Regulation of Piglet Intestine Immune in response to Clostridium perfringens Infection. Scientific Reports, 9(1).

https://doi.org/10.1038/s41598-018-37898-5

Hunter, S. E., Brown, J. E., Oyston, P. C., Sakurai, J., & Titball, R. W. (1993). Molecular genetic analysis of beta-toxin of Clostridium perfringens reveals sequence homology with alpha-toxin, gamma-toxin, and leukocidin of Staphylococcus aureus. Infection and Immunity, 61(9), 3958–3965.

https://doi.org/10.1128/iai.61.9.3958-3965.1993

Immerseel, F. V., Buck, J. D., Pasmans, F., Huyghebaert, G., Haesebrouck, F., & Ducatelle, R. (2004). Clostridium perfringensin poultry: an emerging threat for animal and public health. Avian Pathology, 33(6), 537–549. https://doi.org/10.1080/03079450400013162

Irikura, D., Monma, C., Suzuki, Y., Nakama, A., Kai, A., Fukui-Miyazaki, A., . . . Kamata, Y. (2015). Identification and Characterization of a New Enterotoxin Produced by Clostridium perfringens Isolated from Food Poisoning Outbreaks. PLOS ONE, 10(11), e0138183. https://doi.org/10.1371/journal.pone.0138183

Jobin, A., Ienca, M., & Vayena, E. (2019). The global landscape of AI ethics guidelines. Nature Machine Intelligence, 1(9), 389–399. https://doi.org/10.1038/s42256-019-0088-2

Johansson, A., Greko, C., Engström, B., & Karlsson, M. (2004). Antimicrobial susceptibility of Swedish, Norwegian and Danish isolates of Clostridium perfringens from poultry, and distribution of tetracycline resistance genes. Veterinary Microbiology, 99(3–4), 251–257. https://doi.org/10.1016/j.vetmic.2004.01.009

Kiu, R., & Hall, L. J. (2018). An update on the human and animal enteric pathogen Clostridium perfringens. Emerging Microbes & Infections, 7(1), 1–15.

https://doi.org/10.1038/s41426-018-0144-8

Kiu, R., & Hall, L. J. (2018). An update on the human and animal enteric pathogen Clostridium perfringens. Emerging Microbes & Infections, 7(1), 1–15.

https://doi.org/10.1038/s41426-018-0144-8

Kiu, R., & Hall, L. J. (2018). An update on the human and animal enteric pathogen Clostridium perfringens. Emerging Microbes & Infections, 7(1), 1–15.

https://doi.org/10.1038/s41426-018-0144-8

Kolaczkowska, E., & Kubes, P. (2013). Neutrophil recruitment and function in health and inflammation. Nature Reviews Immunology, 13(3), 159–175. https://doi.org/10.1038/nri3399

Lassen, J., Gjerris, M., & Sandøe, P. (2006). After Dolly—Ethical limits to the use of biotechnology on farm animals. Theriogenology, 65(5), 992–1004.

https://doi.org/10.1016/j.theriogenology.2005.09.012

Li, C., Lillehoj, H. S., Gadde, U. D., Ritter, D., & Oh, S. (2017). Characterization ofClostridium perfringensStrains Isolated from Healthy and Necrotic Enteritis-Afflicted Broiler Chickens. Avian Diseases, 61(2), 178–185.

https://doi.org/10.1637/11507-093016-reg.1

Li, J., Chen, J., Vidal, J. E., & McClane, B. A. (2011). The Agr-Like Quorum-Sensing System Regulates Sporulation and Production of Enterotoxin and Beta2 Toxin by Clostridium perfringens Type A Non-Food-Borne Human Gastrointestinal Disease Strain F5603. Infection and Immunity, 79(6), 2451–2459.

https://doi.org/10.1128/iai.00169-11

Li, J., Uzal, F., & McClane, B. (2016). Clostridium perfringens Sialidases: Potential Contributors to Intestinal Pathogenesis and Therapeutic Targets. Toxins, 8(11), 341.

https://doi.org/10.3390/toxins8110341

Llanco, L. A., Nakano, V., Moraes, C. T. D., Piazza, R. M., & Avila-Campos, M. J. (2017). Adhesion and invasion of Clostridium perfringens type A into epithelial cells. Brazilian Journal of Microbiology, 48(4), 764–768. https://doi.org/10.1016/j.bjm.2017.06.002

M’ikanatha, N. M. (2007). Book Review Food Safety: Old Habits, New Perspectives By Phyllis Entis. 400 pp. Washington, DC, ASM Press, 2007. $49.95. 978-1-55581-417-5 Food Microbiology: Fundamentals and Frontiers Third edition. Edited by Michael P. Doyle and Larry R. Beuchat. 1038 pp., illustrated. Washington, DC, ASM Press, 2007. $169.95. 978-1-55581-407-6. New England Journal of Medicine, 357(12), 1266–1267. https://doi.org/10.1056/nejmbkrev58331

Ma, M., Gurjar, A., Theoret, J. R., Garcia, J. P., Beingesser, J., Freedman, J. C., . . . Uzal, F. A. (2014). Synergistic Effects of Clostridium perfringens Enterotoxin and Beta Toxin in Rabbit Small Intestinal Loops. Infection and Immunity, 82(7), 2958–2970.

https://doi.org/10.1128/iai.01848-14

Manz, M. G., & Boettcher, S. (2014). Emergency granulopoiesis. Nature Reviews Immunology, 14(5), 302–314.

https://doi.org/10.1038/nri3660

Mehdizadeh Gohari, I., A. Navarro, M., Li, J., Shrestha, A., Uzal, F., & A. McClane, B. (2021). Pathogenicity and virulence of Clostridium perfringens. Virulence, 12(1), 723–753. https://doi.org/10.1080/21505594.2021.1886777

Mehdizadeh Gohari, Li, Navarro, Uzal, & McClane. (2019). Effects of Claudin-1 on the Action of Clostridium perfringens Enterotoxin in Caco-2 Cells. Toxins, 11(10), 582.

https://doi.org/10.3390/toxins11100582

Melville, S., & Craig, L. (2013). Type IV Pili in Gram-Positive Bacteria. Microbiology and Molecular Biology Reviews, 77(3), 323–341. https://doi.org/10.1128/mmbr.00063-12

Miyamoto, K., Li, J., Sayeed, S., Akimoto, S., & McClane, B. A. (2008). Sequencing and Diversity Analyses Reveal Extensive Similarities between Some Epsilon-Toxin-Encoding Plasmids and the pCPF5603Clostridium perfringensEnterotoxin Plasmid. Journal of Bacteriology, 190(21), 7178–7188.

https://doi.org/10.1128/jb.00939-08

Miyamoto, K., Yumine, N., Mimura, K., Nagahama, M., Li, J., McClane, B. A., & Akimoto, S. (2011). Identification of Novel Clostridium perfringens Type E Strains That Carry an Iota Toxin Plasmid with a Functional Enterotoxin Gene. PLoS ONE, 6(5), e20376. https://doi.org/10.1371/journal.pone.0020376

Moffatt, C. R., Musto, J., Pingault, N., Miller, M., Stafford, R., Gregory, J., . . . Kirk, M. D. (2016). Salmonella Typhimurium and Outbreaks of Egg-Associated Disease in Australia, 2001 to 2011. Foodborne Pathogens and Disease, 13(7), 379–385.

https://doi.org/10.1089/fpd.2015.2110

Morris, W. E., Dunleavy, M. V., Diodati, J., Berra, G., & Fernandez-Miyakawa, M. E. (2012). Effects of Clostridium perfringens alpha and epsilon toxins in the bovine gut. Anaerobe, 18(1), 143–147. https://doi.org/10.1016/j.anaerobe.2011.12.003

Nagahama, M., Ochi, S., Oda, M., Miyamoto, K., Takehara, M., & Kobayashi, K. (2015). Recent Insights into Clostridium perfringens Beta-Toxin. Toxins, 7(2), 396–406.

https://doi.org/10.3390/toxins7020396

Nauseef, W. M., & Borregaard, N. (2014). Neutrophils at work. Nature Immunology, 15(7), 602–611.

https://doi.org/10.1038/ni.2921

Navarro, M., McClane, B., & Uzal, F. (2018). Mechanisms of Action and Cell Death Associated with Clostridium perfringens Toxins. Toxins, 10(5), 212. https://doi.org/10.3390/toxins10050212

Oda, M., Kabura, M., Takagishi, T., Suzue, A., Tominaga, K., Urano, S., . . . Sakurai, J. (2012). Clostridium perfringens Alpha-toxin Recognizes the GM1a-TrkA Complex. Journal of Biological Chemistry, 287(39), 33070–33079.

https://doi.org/10.1074/jbc.m112.393801

Patel, M. M., Hall, A. J., Vinjé, J., & Parashar, U. D. (2009). Noroviruses: A comprehensive review. Journal of Clinical Virology, 44(1), 1–8. https://doi.org/10.1016/j.jcv.2008.10.009

Petit, L., Gibert, M., & Popoff, M. R. (1999). Clostridium perfringens: toxinotype and genotype. Trends in Microbiology, 7(3), 104–110. https://doi.org/10.1016/s0966-842x(98)01430-9

Powell, D. A. (1992). Report of the committee on infectious diseases, 21st ed. Committee on Infectious Diseases. Elk Grove Village, IL: American Academy of Pediatrics, 1991, 670 pp. Pediatric Pulmonology, 13(4), 269–269.

https://doi.org/10.1002/ppul.1950130418

Revitt-Mills, S. A., Rood, J. I., & Adams, V. (2015). Clostridium perfringens extracellular toxins and enzymes: 20 and counting. Microbiology Australia, 36(3), 114.

https://doi.org/10.1071/ma15039

Romero-García, N., Huete-Acevedo, J., Mas-Bargues, C., Sanz-Ros, J., Dromant, M., Badenes, R., & Borrás, C. (2023). Extracellular Vesicles: The Future of Diagnosis in Solid Organ Transplantation? International Journal of Molecular Sciences, 24(6), 5102. https://doi.org/10.3390/ijms24065102

Rood, J. I., Adams, V., Lacey, J., Lyras, D., McClane, B. A., Melville, S. B., . . . Van Immerseel, F. (2018). Expansion of the Clostridium perfringens toxin-based typing scheme. Anaerobe, 53, 5–10. https://doi.org/10.1016/j.anaerobe.2018.04.011

Rood, J. I., Keyburn, A. L., & Moore, R. J. (2016). NetB and necrotic enteritis: the hole movable story. Avian Pathology, 45(3), 295–301. https://doi.org/10.1080/03079457.2016.1158781

Sakaue, M., Ota, K., Nakamura, E., Nitta, M., Oka, M., Oishi, Y., . . . Takasu, A. (2019). Type A fulminant Clostridium perfringens sepsis indicated RBC/Hb discrepancy; a case report. BMC Infectious Diseases, 19(1). https://doi.org/10.1186/s12879-019-4350-3

Sakurai, J., & Duncan, C. L. (1978). Some properties of beta-toxin produced by Clostridium perfringens type C. Infection and Immunity, 21(2), 678–680.

https://doi.org/10.1128/iai.21.2.678-680.1978

Scallan, E., Griffin, P. M., Angulo, F. J., Tauxe, R. V., & Hoekstra, R. M. (2011). Foodborne Illness Acquired in the United States—Unspecified Agents. Emerging Infectious Diseases, 17(1), 16–22. https://doi.org/10.3201/eid1701.p21101

Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., . . . Griffin, P. M. (2011). Foodborne Illness Acquired in the United States—Major Pathogens. Emerging Infectious Diseases, 17(1), 7–15.

https://doi.org/10.3201/eid1701.09-1101p1

Sharp, P. M., & Hahn, B. H. (2011). Origins of HIV and the AIDS Pandemic. Cold Spring Harbor Perspectives in Medicine, 1(1), a006841–a006841. https://doi.org/10.1101/cshperspect.a006841

Shrestha, A., Uzal, F. A., & McClane, B. A. (2016). The interaction of Clostridium perfringens enterotoxin with receptor claudins. Anaerobe, 41, 18–26.

https://doi.org/10.1016/j.anaerobe.2016.04.011

Uzal, F. A., Freedman, J. C., Shrestha, A., Theoret, J. R., Garcia, J., Awad, M. M., . . . McClane, B. A. (2014). Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease. Future Microbiology, 9(3), 361–377.

https://doi.org/10.2217/fmb.13.168

Wade, B., Keyburn, A. L., Haring, V., Ford, M., Rood, J. I., & Moore, R. J. (2020). Two putative zinc metalloproteases contribute to the virulence of Clostridium perfringens strains that cause avian necrotic enteritis. Journal of Veterinary Diagnostic Investigation, 32(2), 259–267. https://doi.org/10.1177/1040638719898689

Wagley, S., Bokori-Brown, M., Morcrette, H., Malaspina, A., D’Arcy, C., Gnanapavan, S., . . . Titball, R. W. (2018). Evidence of Clostridium perfringens epsilon toxin associated with multiple sclerosis. Multiple Sclerosis Journal, 25(5), 653–660. https://doi.org/10.1177/1352458518767327

Wambui, J., Cernela, N., Stevens, M. J. A., & Stephan, R. (2021). Whole Genome Sequence-Based Identification of Clostridium estertheticum Complex Strains Supports the Need for Taxonomic Reclassification Within the Species Clostridium estertheticum. Frontiers in Microbiology, 12.

https://doi.org/10.3389/fmicb.2021.727022

Wang, H., Latorre, J. D., Bansal, M., Abraha, M., Al-Rubaye, B., Tellez-Isaias, G., . . . Sun, X. (2019). Microbial metabolite deoxycholic acid controls Clostridium perfringens-induced chicken necrotic enteritis through attenuating inflammatory cyclooxygenase signaling. Scientific Reports, 9(1).

https://doi.org/10.1038/s41598-019-51104-0

Worobey, M., Han, G. Z., & Rambaut, A. (2014). A synchronized global sweep of the internal genes of modern avian influenza virus. Nature, 508(7495), 254–257.

https://doi.org/10.1038/nature13016

Yonogi, S., Matsuda, S., Kawai, T., Yoda, T., Harada, T., Kumeda, Y., Iida, T. (2014). BEC, a Novel Enterotoxin of Clostridium perfringens Found in Human Clinical Isolates from Acute Gastroenteritis Outbreaks. Infection and Immunity, 82(6), 2390–2399. https://doi.org/10.1128/iai.01759-14

How to cite this article

Khorsheed, S. A. (2024). Virulence and Pathogenicity of Clostridium perfringens. Microbial Science Archives, Vol. 4(2), 6-12. https://doi.org/10.47587/MSA.2024.4201

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