Microbiological and Histopathological Study of Enterotoxemia Caused by Clostridium perfringens in Syrian Lamb

Document Type : Original Article

Authors

1 College of Veterinary Medicine, University of Hama, Syria. The General Commission for Scientific Agricultural Research (GCSAR), Syria

2 College of Veterinary Medicine, Hama University, Syria

3 Department of Veterinary Public Health, College of veterinary Medicine, University of Mosul, Iraq

4 The General Commission for Scientific Agricultural Research (GCSAR), Syria

Abstract

Clostridium perfringens (C. perfringens) is one of the most common pathogens affecting sheep, causing significant economic losses due to high mortality rates. The aim of this study is to isolate and identify C. perfringens from lambs that had recently died from enterotoxemia and study the histopathological changes in their intestines, livers and kidneys. A total of forty-eight samples (16 swabs from each of the intestines, liver, and kidneys) were collected from the lambs. All the collected swabs from the internal cavity of the small intestine, liver or kidney were placed in sterile tubes prepared with thioglycolate broth. Tissue samples were also taken from the intestine, liver and kidney and placed in 10% formalin (NBF) containers. The samples were transferred to the scientific research unit at the College of Veterinary Medicine, Hama University for bacteriological and histological testing. All swabs underwent bacteriological examinations by both conventional and molecular techniques for the detection of C. perfringens. The cpa, cpb, etx, and ia genes were also investigated. The total isolation percentage was 79.16%, and the highest isolation percentage was recorded in intestine followed by liver and kidneys at 33.33%, 22.92%, and 22.92%, respectively. The study also revealed the presence of cpa, cpb, etx and ia genes at rates of 44.73%, 21.05%, 34.21%, and 5.26% among isolates. The results of the histopathological examination revealed that all the intestinal sections, liver and kidneys had various pathological lesions. This study provides an opportunity to know the pathogenic types in lambs that died as a result of C. perfringens infection and could serve as a useful control element for the development of vaccines to reduce and control this economic loss in lambs.

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Main Subjects

References

ALI, T., SARWAR, A., ANJUM, A. A., and RAZA, S., 2024. Alpha toxin production potential and antibiotic resistance patterns of clostridium perfringens isolates from meat samples. Animal Bioscience. https://doi.org/10.5713/ab.24.0210
AHSANI, M., MOHAMMADABADI, M., and SHAMSADDINI, M., 2010. Clostridium perfringens isolate typing by multiplex PCR. Journal of Venomous Animals and Toxins Including Tropical Diseases, 16(4), 573–578. https://doi.org/10.1590/S1678-91992010000400006
ASSIS, R. A., LOBATO, F. C. F., FACURY FILHO, E. J., UZAL, F. A., SANTANA, F. J. F., DIAS, L. D., and PARREIRAS, P. M., 2002. Isolation of Clostridium perfringens type D from a suckling calve with ulcerative abomasitis. Archivos de Medicina Veterinaria, 34(2). http://dx.doi.org/10.4067/S0301-732X2002000200015
BROWN, C., BAKER, D.C., and BAKER, I.K., 2007. Alimentary System in Jubb, Kennedy and Palmer’s: Pathology of domestic animals. 5th Ed. Elsevier Saunders, Philadelphia
DIAB, S. S., 2016. Diseases Produced by Clostridium perfringens Type C. Clostridial Diseases of Animals, 143–155. https://doi.org/10.1002/9781118728291.ch12
EL IDRISSI, A. H., and WARD, G. E., 1992. Evaluation of enzyme-linked immunosorbent assay for diagnosis of clostridium perfringens enterotoxemias. Veterinary Microbiology, 31(4), 389–396. https://doi.org/10.1016/0378-1135(92)90131-C
ELSIFY, A., TARABESS, R., NAYEL, M. A., SALAMA, A., ALLAAM, M., ABD, E. G. M., HASSAN, H., ZAGHAWA, A., and ELBALLAL, S., 2016. Bacteriological and molecular studies on Clostridium perfringens isolated from sheep in three Egyptian provinces. African Journal of Microbiology Research, 10(20), 725–732. https://doi.org/10.5897/AJMR2016.8023
FERNANDEZ-MIYAKAWA, M. E., FISHER, D. J., POON, R., SAYEED, S., ADAMS, V., ROOD, J. I., MCCLANE, B. A., and UZAL, F. A., 2007. Both Epsilon-Toxin and Beta-Toxin Are Important for the Lethal Properties of Clostridium perfringens Type B Isolates in the Mouse Intravenous Injection Model. Infection and Immunity, 75(3), 1443–1452. https://doi.org/10.1128/iai.01672-06
GÖKCE, H.I., GENÇ, O., SÖZMEN, M., GÖKÇE, G., 2007. Determination of Clostridium Perf-ringens Toxin-Types in Sheep with Suspected Enterotoxemia in Kars Province, Turkey. Turk J Vet & Anim Sci. 31(5): 355-360. https://journals.tubitak.gov.tr/veterinary/vol31/iss5/11/
GRECO, G., MADIO, A., BUONAVOGLIA, D., TOTARO, M., CORRENTE, M., MARTELLA, V., and BUONAVOGLIA, C., 2005. Clostridium perfringens toxin-types in lambs and kids affected with gastroenteric pathologies in Italy. The Veterinary Journal, 170(3), 346–350. https://doi.org/10.1016/j.tvjl.2004.08.001
HAMAD, M. A. (2010). A bacteriological study of Clostridium perfringens infections in sheep in Syria. PhD thesis, Faculty of Veterinary Medicine, Hama University, pp 167.
HASSANEIN, K. M. A., SAYED, M. M., and HASSAN, A. M., 2017. Pathological and biochemical studies on enterotoxemia in sheep. Comparative Clinical Pathology, 26(3), 513–518. https://doi.org/10.1007/s00580-017-2407-5
HUNTER, S.E.C., BROWN, E., OYSTON, P.C.F., SAKURAI, J. AND TIBALL, R.C., 1993. Molecular genetic analysis of beta-toxin of Clostridium perfingens reveals sequence homology with alphatoxin, gamma-toxin, and leukocidin of Staphylococcus aureus. Infection and Immunity 61, 3958-3965. https://doi.org/10.1128/iai.61.9.3958-3965.1993
HUNTER, S.E.C., CLARKE, I.N., KELLY, D.C. AND TITBALL, R.W., 1992. Cloning and nucleotide sequence of the Clostridium perfringens epsilon-toxin gene and its expression in Escherichia coli. Infection and Immunity 60, 102-1 10.
HUSSEIN, H. A., EL-AMIR, Y. O., AAMER, A. A., and ELGHAFFAR, S. KH. A., 2012. Bacillary hemoglobinuria in dairy cows: clinical, hematological, biochemical, and pathological alterations. Comparative Clinical Pathology, 22(6), 1137–1143. https://doi.org/10.1007/s00580-012-1541-3
IKHOMOVICH, K. O., and KHAITOVICH, S. I., 2024. Infectious enterotoxemia disease of sheep diagnostics and prevention. European Journal of Medical Genetics and Clinical Biology, 1(6), 162–166. https://doi.org/10.61796/jmgcb.v1i6.606
KALENDER, H., ONGOR, H., TIMURKAAN, N., KARGULLE, B., KARABULUT, B., LNCILI, C.A., 2023. Detection and molecular characterization of Clostridium perfringens, Paeniclostridium sordellii and Clostridium septicum from lambs and goat kids with hemorrhagic abomasitis in Turkey. https://doi.org/10.1186/s12917-023-03569-5
KIU, R., SHAW, A. G., SIM, K., ACUNA-GONZALEZ, A., PRICE, C. A., BEDWELL, H., DREGER, S. A., FOWLER, W. J., CORNWELL, E., PICKARD, D., BELTEKI, G., MALSOM, J., PHILLIPS, S., YOUNG, G. R., SCHOFIELD, Z., ALCON-GINER, C., BERRINGTON, J. E., STEWART, C. J., DOUGAN, G., HALL, L. J., 2023. Particular genomic and virulence traits associated with preterm infant-derived toxigenic Clostridium perfringens strains. Nature Microbiology, 8(6), 1160–1175. https://doi.org/10.1038/s41564-023-01385-z
MCDONEL, J. L., 1980. Clostridium perfringens toxins (type A, B, C, D, E). Pharmacology andamp; Therapeutics, 10(3), 617–655. https://doi.org/10.1016/0163-7258(80)90031-5
MIYASHIRO, S., NASSAR, A. F. C., DEL FAVA, C., CABRAL, A. D., and SILVA, M., 2007. Clostridium perfringens types A and D associated with enterotoxemia in an 18-month-old goat. Journal of Venomous Animals and Toxins Including Tropical Diseases, 13(4), 885–893. https://doi.org/10.1590/S1678-91992007000400017
MOUSTAFA, S., ZAKARIA, I., MOUSTAFA, A., ABOSAKAYA, R., and SELIM, A., 2022. Bacteriological and serological investigation of Clostridium perfringens in lambs. Scientific Reports, 12(1). https://doi.org/10.1038/s41598-022-21918-6
MUDENDAHANGOMBE, B., KOHDA, T., MUKAMOTO, M., and KOZAKI, S., 2006. Purification and sensitivity of Clostridium chauvoei hemolysin to various erythrocytes. Comparative Immunology, Microbiology and Infectious Diseases, 29(4), 263–268. https://doi.org/10.1016/j.cimid.2006.06.002
NASIR, A.A., YOUNUS, M., REHMAN, M.U., LATEEF, M., KHALIQ, S.A., AHMAD, I., ABBAS, M., 2013. Hematological and some biochemical alterations in sheep experimentally infected with Clostridium perfringens type D infection. The J of Anim and Plant Sci 23:1553–1558. https://thejaps.org.pk/docs/v-23-6/12.pdf
NAVARRO, M. A., and UZAL, F. A., 2019. Pathobiology and diagnosis of clostridial hepatitis in animals. Journal of Veterinary Diagnostic Investigation, 32(2), 192–202. https://doi.org/10.1177/1040638719886567
NAZKI, S., WANI, S. A., PARVEEN, R., AHANGAR, S. A., KASHOO, Z. A., HAMID, S., DAR, Z. A., DAR, T. A., and DAR, P. A., 2017. Isolation, molecular characterization and prevalence of Clostridium perfringens in sheep and goats of Kashmir Himalayas, India. Veterinary World, 10(12), 1501–1507. https://www.veterinaryworld.org/Vol.10/December-2017/14.html
PERELLE, S., GIBERT, M., BOQUET, P., and POPOFF, M.R., 199). Characterization of Clostridium perfingens iota-toxin genes and expression in Escherichia coli. Infection and Immunity 61, 5147- 5 156. https://doi.org/10.1128/iai.61.12.5147-5156.1993
PRESCOTT, J. F., 2022. Clostridium perfringens enteritis and enterotoxaemia [dataset]. In CABI Publishing. https://doi.org/10.1079/cabicompendium.88774
PRESCOTT, J. F., MENZIES, P. I., and FRASER, R. S., 2016. Clostridial Abomasitis. Clostridial Diseases of Animals, 205–220. Portico. https://doi.org/10.1002/9781118728291.ch17
QUINN, P.J.; MARKEY, B.K.; CARTER, M.E.; DONNELLY, W.J.C.; LEONARD, F.C., 2003. Veterinary Microbiology and Microbial Diseases. Blackwell publi-shing Company. USA.Pp.84-96.
RADOSTITS, O.M., GAY, C.C., HINCHCLIFF, K.W., CONSTABLE, P.D., 2007. Veterinary medicine: a textbook of the diseases of cattle, sheep, goats, pigs, and horses, 10th edn. Saunders, Philadelphia, pp 834–836. https://www.scirp.org/reference/ReferencesPapers?ReferenceID=1679700
REDONDO, L. M., FARBER, M., VENZANO, A., JOST, B. H., PARMA, Y. R., and FERNANDEZ-MIYAKAWA, M. E., 2013. Sudden death syndrome in adult cows associated with Clostridium perfringens type E. Anaerobe, 20, 1–4. https://doi.org/10.1016/j.anaerobe.2013.01.001
RENU, BOYAL, P. K., and DADHICH, H., 2022. Pathological findings in lungs of sheep affected with Clostridium perfringens type D enterotoxemia. Indian Journal of Veterinary Pathology, 46(1), 70–72. http://dx.doi.org/10.5958/0973-970X.2022.00009.8
SAEID HOSSEINZADEH, BAHADORI, M., POORMONTASERI, M., DEHGHANI, M., FAZELI, M., and NAZIFI, S., 2018. Molecular characterization of Clostridium perfringens isolated from cattle and sheep carcasses and its antibiotic resistance patterns in Shiraz slaughterhouse, southern Iran. Veterinarski Arhiv, 88(5), 581–591. https://doi.org/10.24099/vet.arhiv.0009
SIMPSON, K. M., CALLAN, R. J., and VAN METRE, D. C., 2018. Clostridial Abomasitis and Enteritis in Ruminants. Veterinary Clinics of North America: Food Animal Practice, 34(1), 155–184. https://doi.org/10.1016/j.cvfa.2017.10.010
SIPOS, W., FISCHER, L., SCHINDLER, M., and SCHMOLL, F., 2003. Genotyping of Clostridium perfringens Isolated from Domestic and Exotic Ruminants and Swine. Journal of Veterinary Medicine, Series B, 50(7), 360–362. Portico. https://doi.org/10.1046/j.1439-0450.2003.00690.x
SONGER, J. G. 1997. Molecular and Immunological Methods for the Diagnosis of Clostridial Diseases. The Clostridia, 491–503. https://doi.org/10.1016/B978-012595020-6/50030-9
SONGER, J. G., and MISKIMMINS, D. W., 2004) Clostridium perfringens type E enteritis in calves: two cases and a brief review of the literature. Anaerobe, 10(4), 239–242. https://doi.org/10.1016/j.anaerobe.2004.05.001
TITBALL, R.W., HUNTER, S.E., MARTIN, K.L., MORRIS, B., SHUTTLEWORTH, A.D., RUBIDGE, T., ANDERSON, D.W., and KELLY, D.C., 2003. Molecular cloning and nucleotide sequence of the alphatoxin (phospholipase C) of Clostridium perfringens. Infection and Immunity 57, 367-376. https://doi.org/10.1128/iai.57.2.367-376.1989
TOOLOEI, M., and MASODEI, M.H., 2008. The Distribution and Prevalence Rate of Enterotoxaemia in Sheep in East Azerbaijan Province, Northwestern Iran in Spring 2008. Journal of Animal and Veterinary Advances, 7, 1434-1439. https://www.scirp.org/reference/referencespapers?referenceid=2749764
UZAL, F. A., GIANNITTI, F., and ASIN, J., 2022. Yellow Lamb Disease (Clostridium perfringens Type A Enterotoxemia of Sheep): A Review. Animals, 12(12), 1590. https://doi.org/10.3390/ani12121590
 UZAL, F.A., KELLY, W.R., MORRIS, W.E., BERMUDEZ, J., and BAISON, M., 2004. The pathology of peracute experimental Clostridium perfringens type D enterotoxemia in sheep. J. Vet. Diagn. Invest.16:403-411. https://doi.org/10.1177/104063870401600506
UZAL, F. A., and SONGER, J. G. (2008). Diagnosis of Clostridium Perfringens Intestinal Infections in Sheep and Goats. Journal of Veterinary Diagnostic Investigation, 20(3), 253–265. https://doi.org/10.1177/104063870802000301
VINOD KUMAR, N., SREENIVASULU, D., and REDDY, Y. N., 2014. Prevalence of Clostridium perfringens toxin genotypes in enterotoxemia suspected sheep flocks of Andhra Pradesh. Veterinary World, 7(12), 1132–1136. https://www.veterinaryworld.org/Vol.7/December-2014/19.html

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History

  • Receive Date: 19 September 2024
  • Revise Date: 12 November 2024
  • Accept Date: 17 November 2024

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