Bacteriological and molecular typing of Clostridium perfringens strains isolated in retail beef in Beijing, China

Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef collected from Beijing, China. Among 221 beef samples collected, 53 samples were positive for C. perfringens, resulting in the average prevale...

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Published inJournal of Veterinary Medical Science Vol. 83; no. 10; pp. 1593 - 1596
Main Authors YANG, Xiao-Tong, SUN, Ming-Jun, LI, Qiao-Ling, SHEN, Qing-Chun, QIN, Yu-Ming, DING, Jia-Bo, ZHANG, Jian-Dong, FAN, Xue-Zheng, JIANG, Hui, WEI, Run-Yu, SUN, Jia-Li
Format Journal Article
LanguageEnglish
Published JAPANESE SOCIETY OF VETERINARY SCIENCE 2021
The Japanese Society of Veterinary Science
Subjects
Bacteriology
Clostridium perfringens
multi-locus sequence typing
retail beef
toxin type
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Abstract Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef collected from Beijing, China. Among 221 beef samples collected, 53 samples were positive for C. perfringens, resulting in the average prevalence as 23.98%. By toxin gene-based typing, the most C. perfringens strains belong to type A (96.23%, 51/53), only 2 strains were identified as type D. By a multi-locus sequence typing (MLST)-based analysis, a total of 36 sequence types (STs) were detected, and the most STs (n=30) represented just a single strain. These finding suggested that the prevalence of C. perfringens in retail beef in Beijing was considerably high and these bacteria displayed extreme diversity in genetics.
AbstractList Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef collected from Beijing, China. Among 221 beef samples collected, 53 samples were positive for C. perfringens, resulting in the average prevalence as 23.98%. By toxin gene-based typing, the most C. perfringens strains belong to type A (96.23%, 51/53), only 2 strains were identified as type D. By a multi-locus sequence typing (MLST)-based analysis, a total of 36 sequence types (STs) were detected, and the most STs (n=30) represented just a single strain. These finding suggested that the prevalence of C. perfringens in retail beef in Beijing was considerably high and these bacteria displayed extreme diversity in genetics.Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef collected from Beijing, China. Among 221 beef samples collected, 53 samples were positive for C. perfringens, resulting in the average prevalence as 23.98%. By toxin gene-based typing, the most C. perfringens strains belong to type A (96.23%, 51/53), only 2 strains were identified as type D. By a multi-locus sequence typing (MLST)-based analysis, a total of 36 sequence types (STs) were detected, and the most STs (n=30) represented just a single strain. These finding suggested that the prevalence of C. perfringens in retail beef in Beijing was considerably high and these bacteria displayed extreme diversity in genetics.
Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef collected from Beijing, China. Among 221 beef samples collected, 53 samples were positive for C. perfringens, resulting in the average prevalence as 23.98%. By toxin gene-based typing, the most C. perfringens strains belong to type A (96.23%, 51/53), only 2 strains were identified as type D. By a multi-locus sequence typing (MLST)-based analysis, a total of 36 sequence types (STs) were detected, and the most STs (n=30) represented just a single strain. These finding suggested that the prevalence of C. perfringens in retail beef in Beijing was considerably high and these bacteria displayed extreme diversity in genetics.
Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef collected from Beijing, China. Among 221 beef samples collected, 53 samples were positive for C. perfringens , resulting in the average prevalence as 23.98%. By toxin gene-based typing, the most C. perfringens strains belong to type A (96.23%, 51/53), only 2 strains were identified as type D. By a multi-locus sequence typing (MLST)-based analysis, a total of 36 sequence types (STs) were detected, and the most STs (n=30) represented just a single strain. These finding suggested that the prevalence of C. perfringens in retail beef in Beijing was considerably high and these bacteria displayed extreme diversity in genetics.
ArticleNumber 21-0129
Author SUN, Jia-Li
YANG, Xiao-Tong
DING, Jia-Bo
SHEN, Qing-Chun
JIANG, Hui
QIN, Yu-Ming
SUN, Ming-Jun
LI, Qiao-Ling
WEI, Run-Yu
ZHANG, Jian-Dong
FAN, Xue-Zheng
Author_xml – sequence: 1
  fullname: YANG, Xiao-Tong
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
– sequence: 1
  fullname: SUN, Ming-Jun
  organization: Laboratory of Zoonoses, China Animal Health and Epidemiology Center, Qingdao, 266032, China
– sequence: 1
  fullname: LI, Qiao-Ling
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
– sequence: 1
  fullname: SHEN, Qing-Chun
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
– sequence: 1
  fullname: QIN, Yu-Ming
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
– sequence: 1
  fullname: DING, Jia-Bo
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
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  fullname: ZHANG, Jian-Dong
  organization: Laboratory of Zoonoses, China Animal Health and Epidemiology Center, Qingdao, 266032, China
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  fullname: FAN, Xue-Zheng
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
– sequence: 1
  fullname: JIANG, Hui
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
– sequence: 1
  fullname: WEI, Run-Yu
  organization: Laboratory of Zoonoses, China Animal Health and Epidemiology Center, Qingdao, 266032, China
– sequence: 1
  fullname: SUN, Jia-Li
  organization: Department of Veterinary Technology, China Institute of Veterinary Drug Control, Beijing, 100081, China
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References 20. Rood, J. I., Adams, V., Lacey, J., Lyras, D., McClane, B. A., Melville, S. B., Moore, R. J., Popoff, M. R., Sarker, M. R., Songer, J. G., Uzal, F. A. and Van Immerseel, F. 2018. Expansion of the Clostridium perfringens toxin-based typing scheme. Anaerobe 53: 5–10.
1. Allaart, J. G., van Asten, A. J., Vernooij, J. C. and Gröne, A. 2014. Beta2 toxin is not involved in in vitro cell cytotoxicity caused by human and porcine cpb2-harbouring Clostridium perfringens. Vet. Microbiol. 171: 132–138.
4. Deguchi, A., Miyamoto, K., Kuwahara, T., Miki, Y., Kaneko, I., Li, J., McClane, B. A. and Akimoto, S. 2009. Genetic characterization of type A enterotoxigenic Clostridium perfringens strains. PLoS One 4: e5598.
24. Wen, Q. and McClane, B. A. 2004. Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Appl. Environ. Microbiol. 70: 2685–2691.
5. Feng, Y., Fan, X., Zhu, L., Yang, X., Liu, Y., Gao, S., Jin, X., Liu, D., Ding, J., Guo, Y. and Hu, Y. 2020. Phylogenetic and genomic analysis reveals high genomic openness and genetic diversity of Clostridium perfringens. Microb. Genom. 6: 10.
6. Filho, E. J., Carvalho, A. U., Assis, R. A., Lobato, F. F., Rachid, M. A., Carvalho, A. A., Ferreira, P. M., Nascimento, R. A., Fernandes, A. A., Vidal, J. E. and Uzal, F. A. 2009. Clinicopathologic features of experimental Clostridium perfringens type D enterotoxemia in cattle. Vet. Pathol. 46: 1213–1220.
10. Jang, Y. S., Kim, D. H., Bae, D., Kim, S. H., Kim, H., Moon, J. S., Song, K. Y., Chon, J. W. and Seo, K. H. 2020. Prevalence, toxin-typing, and antimicrobial susceptibility of Clostridium perfringens from retail meats in Seoul, Korea. Anaerobe 64: 102235.
8. Hibberd, M. C., Neumann, A. P., Rehberger, T. G. and Siragusa, G. R. 2011. Multilocus sequence typing subtypes of poultry Clostridium perfringens isolates demonstrate disease niche partitioning. J. Clin. Microbiol. 49: 1556–1567.
21. Uzal, F. A., Vidal, J. E., McClane, B. A. and Gurjar, A. A. 2010. Clostridium Perfringens Toxins Involved in Mammalian Veterinary Diseases. Open Toxinology J. 2: 24–42.
16. Liu, Y., Xiu, L., Miao, Z. and Wang, H. 2020. Occurrence and multilocus sequence typing of Clostridium perfringens isolated from retail duck products in Tai’an region, China. Anaerobe 62: 102102.
14. Lacey, J. A., Johanesen, P. A., Lyras, D. and Moore, R. J. 2016. Genomic diversity of necrotic enteritis-associated strains of Clostridium perfringens: a review. Avian Pathol. 45: 302–307.
3. Chalmers, G., Bruce, H. L., Hunter, D. B., Parreira, V. R., Kulkarni, R. R., Jiang, Y. F., Prescott, J. F. and Boerlin, P. 2008. Multilocus sequence typing analysis of Clostridium perfringens isolates from necrotic enteritis outbreaks in broiler chicken populations. J. Clin. Microbiol. 46: 3957–3964.
22. van Asten, A. J., Nikolaou, G. N. and Gröne, A. 2010. The occurrence of cpb2-toxigenic Clostridium perfringens and the possible role of the beta2-toxin in enteric disease of domestic animals, wild animals and humans. Vet. J. 183: 135–140.
7. Fohler, S., Klein, G., Hoedemaker, M., Scheu, T., Seyboldt, C., Campe, A., Jensen, K. C. and Abdulmawjood, A. 2016. Diversity of Clostridium perfringens toxin-genotypes from dairy farms. BMC Microbiol. 16: 199.
15. Lebrun, M., Filée, P., Mousset, B., Desmecht, D., Galleni, M., Mainil, J. G. and Linden, A. 2007. The expression of Clostridium perfringens consensus beta2 toxin is associated with bovine enterotoxaemia syndrome. Vet. Microbiol. 120: 151–157.
18. Nakano, V., Ignacio, A., Llanco, L., Bueris, V., Sircili, M. P. and Avila-Campos, M. J. 2017. Multilocus sequence typing analyses of Clostridium perfringens type A strains harboring tpeL and netB genes. Anaerobe 44: 99–105.
11. Jeong, D., Kim, D. H., Kang, I. B., Chon, J. W., Kim, H., Om, A. S., Lee, J. Y., Moon, J. S., Oh, D. H. and Seo, K. H. 2017. Prevalence and toxin type of Clostridium perfringens in beef from four different types of meat markets in Seoul, Korea. Food Sci. Biotechnol. 26: 545–548.
23. Wang, R. F., Cao, W. W., Franklin, W., Campbell, W. and Cerniglia, C. E. 1994. A 16S rDNA-based PCR method for rapid and specific detection of Clostridium perfringens in food. Mol. Cell. Probes 8: 131–137.
12. Jost, B. H., Trinh, H. T. and Songer, J. G. 2006. Clonal relationships among Clostridium perfringens of porcine origin as determined by multilocus sequence typing. Vet. Microbiol. 116: 158–165.
25. Xiao, Y., Wagendorp, A., Moezelaar, R., Abee, T. and Wells-Bennik, M. H. 2012. A wide variety of Clostridium perfringens type A food-borne isolates that carry a chromosomal cpe gene belong to one multilocus sequence typing cluster. Appl. Environ. Microbiol. 78: 7060–7068.
19. Regan, S. B., Anwar, Z., Miraflor, P., Williams, L. B., Shetty, S., Sepulveda, J., Moreh, J., Bogdanov, S., Haigh, S., Lustig, A., Gaehde, S., Vartanian, A., Rubin, N. and Linden, J. R. 2018. Identification of epsilon toxin-producing Clostridium perfringens strains in American retail food. Anaerobe 54: 124–127.
17. Milton, A. A. P., Sanjukta, R., Gogoi, A. P., Momin, K. M., Priya, G. B., Das, S., Ghatak, S., Sen, A. and Kandpal, B. K. 2020. Prevalence, molecular typing and antibiotic resistance of Clostridium perfringens in free range ducks in Northeast India. Anaerobe 64: 102242.
2. Athira, C. K., Milton, A. A. P., Reddy, A., Mekhemadhom Rajendrakumar, A., Abhishek, ., Verma, M. R., Kumar, A., Nagaleekar, V. K. and Agarwal, R. K. 2018. Diversity of toxin-genotypes among Clostridium perfringens isolated from healthy and diarrheic neonatal cattle and buffalo calves. Anaerobe 49: 99–102.
9. Hunter, P. R. and Gaston, M. A. 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J. Clin. Microbiol. 26: 2465–2466.
13. Khan, M., Nazir, J., Anjum, A. A., Ahmad, M. U., Nawaz, M. and Shabbir, M. Z. 2015. Toxinotyping and antimicrobial susceptibility of enterotoxigenic Clostridium perfring
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References_xml – reference: 14. Lacey, J. A., Johanesen, P. A., Lyras, D. and Moore, R. J. 2016. Genomic diversity of necrotic enteritis-associated strains of Clostridium perfringens: a review. Avian Pathol. 45: 302–307.
– reference: 6. Filho, E. J., Carvalho, A. U., Assis, R. A., Lobato, F. F., Rachid, M. A., Carvalho, A. A., Ferreira, P. M., Nascimento, R. A., Fernandes, A. A., Vidal, J. E. and Uzal, F. A. 2009. Clinicopathologic features of experimental Clostridium perfringens type D enterotoxemia in cattle. Vet. Pathol. 46: 1213–1220.
– reference: 11. Jeong, D., Kim, D. H., Kang, I. B., Chon, J. W., Kim, H., Om, A. S., Lee, J. Y., Moon, J. S., Oh, D. H. and Seo, K. H. 2017. Prevalence and toxin type of Clostridium perfringens in beef from four different types of meat markets in Seoul, Korea. Food Sci. Biotechnol. 26: 545–548.
– reference: 8. Hibberd, M. C., Neumann, A. P., Rehberger, T. G. and Siragusa, G. R. 2011. Multilocus sequence typing subtypes of poultry Clostridium perfringens isolates demonstrate disease niche partitioning. J. Clin. Microbiol. 49: 1556–1567.
– reference: 18. Nakano, V., Ignacio, A., Llanco, L., Bueris, V., Sircili, M. P. and Avila-Campos, M. J. 2017. Multilocus sequence typing analyses of Clostridium perfringens type A strains harboring tpeL and netB genes. Anaerobe 44: 99–105.
– reference: 20. Rood, J. I., Adams, V., Lacey, J., Lyras, D., McClane, B. A., Melville, S. B., Moore, R. J., Popoff, M. R., Sarker, M. R., Songer, J. G., Uzal, F. A. and Van Immerseel, F. 2018. Expansion of the Clostridium perfringens toxin-based typing scheme. Anaerobe 53: 5–10.
– reference: 23. Wang, R. F., Cao, W. W., Franklin, W., Campbell, W. and Cerniglia, C. E. 1994. A 16S rDNA-based PCR method for rapid and specific detection of Clostridium perfringens in food. Mol. Cell. Probes 8: 131–137.
– reference: 25. Xiao, Y., Wagendorp, A., Moezelaar, R., Abee, T. and Wells-Bennik, M. H. 2012. A wide variety of Clostridium perfringens type A food-borne isolates that carry a chromosomal cpe gene belong to one multilocus sequence typing cluster. Appl. Environ. Microbiol. 78: 7060–7068.
– reference: 9. Hunter, P. R. and Gaston, M. A. 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J. Clin. Microbiol. 26: 2465–2466.
– reference: 1. Allaart, J. G., van Asten, A. J., Vernooij, J. C. and Gröne, A. 2014. Beta2 toxin is not involved in in vitro cell cytotoxicity caused by human and porcine cpb2-harbouring Clostridium perfringens. Vet. Microbiol. 171: 132–138.
– reference: 7. Fohler, S., Klein, G., Hoedemaker, M., Scheu, T., Seyboldt, C., Campe, A., Jensen, K. C. and Abdulmawjood, A. 2016. Diversity of Clostridium perfringens toxin-genotypes from dairy farms. BMC Microbiol. 16: 199.
– reference: 3. Chalmers, G., Bruce, H. L., Hunter, D. B., Parreira, V. R., Kulkarni, R. R., Jiang, Y. F., Prescott, J. F. and Boerlin, P. 2008. Multilocus sequence typing analysis of Clostridium perfringens isolates from necrotic enteritis outbreaks in broiler chicken populations. J. Clin. Microbiol. 46: 3957–3964.
– reference: 16. Liu, Y., Xiu, L., Miao, Z. and Wang, H. 2020. Occurrence and multilocus sequence typing of Clostridium perfringens isolated from retail duck products in Tai’an region, China. Anaerobe 62: 102102.
– reference: 12. Jost, B. H., Trinh, H. T. and Songer, J. G. 2006. Clonal relationships among Clostridium perfringens of porcine origin as determined by multilocus sequence typing. Vet. Microbiol. 116: 158–165.
– reference: 22. van Asten, A. J., Nikolaou, G. N. and Gröne, A. 2010. The occurrence of cpb2-toxigenic Clostridium perfringens and the possible role of the beta2-toxin in enteric disease of domestic animals, wild animals and humans. Vet. J. 183: 135–140.
– reference: 15. Lebrun, M., Filée, P., Mousset, B., Desmecht, D., Galleni, M., Mainil, J. G. and Linden, A. 2007. The expression of Clostridium perfringens consensus beta2 toxin is associated with bovine enterotoxaemia syndrome. Vet. Microbiol. 120: 151–157.
– reference: 17. Milton, A. A. P., Sanjukta, R., Gogoi, A. P., Momin, K. M., Priya, G. B., Das, S., Ghatak, S., Sen, A. and Kandpal, B. K. 2020. Prevalence, molecular typing and antibiotic resistance of Clostridium perfringens in free range ducks in Northeast India. Anaerobe 64: 102242.
– reference: 4. Deguchi, A., Miyamoto, K., Kuwahara, T., Miki, Y., Kaneko, I., Li, J., McClane, B. A. and Akimoto, S. 2009. Genetic characterization of type A enterotoxigenic Clostridium perfringens strains. PLoS One 4: e5598.
– reference: 21. Uzal, F. A., Vidal, J. E., McClane, B. A. and Gurjar, A. A. 2010. Clostridium Perfringens Toxins Involved in Mammalian Veterinary Diseases. Open Toxinology J. 2: 24–42.
– reference: 5. Feng, Y., Fan, X., Zhu, L., Yang, X., Liu, Y., Gao, S., Jin, X., Liu, D., Ding, J., Guo, Y. and Hu, Y. 2020. Phylogenetic and genomic analysis reveals high genomic openness and genetic diversity of Clostridium perfringens. Microb. Genom. 6: 10.
– reference: 13. Khan, M., Nazir, J., Anjum, A. A., Ahmad, M. U., Nawaz, M. and Shabbir, M. Z. 2015. Toxinotyping and antimicrobial susceptibility of enterotoxigenic Clostridium perfringens isolates from mutton, beef and chicken meat. J. Food Sci. Technol. 52: 5323–5328.
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Snippet Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef...
Clostridium perfringens is an important zoonotic pathogen. This study was designed to explore the prevalence and toxin types of C. perfringens in retail beef...
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SubjectTerms Bacteriology
Clostridium perfringens
multi-locus sequence typing
retail beef
toxin type
Title Bacteriological and molecular typing of Clostridium perfringens strains isolated in retail beef in Beijing, China
URI https://www.jstage.jst.go.jp/article/jvms/83/10/83_21-0129/_article/-char/en
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https://pubmed.ncbi.nlm.nih.gov/PMC8569878
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