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Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler

Year 2015, Volume: 62 Issue: 2, 113 - 117, 01.06.2015

Alireza Hanıfehnezhad Muammer Göncüoğlu İrfan Erol

https://doi.org/10.1501/Vetfak_0000002666

Abstract

The aim of the study was to determine the prevalance and molecular characterization of Clostridium perfringens in edible offal of broiler. For this purpose a total of 90 samples, including 45 heart-livers and 45 gizzards were obtained from different supermarkets and transported to the laboratory in an ice box and tested at the same day. Culture technique was used for the isolation and selected biochemical tests, including acid phosphatase and reverse-CAMP tests was used for the identification of C. perfringens from the samples. Twenty one (46.7%) of 45 heart-liver and eight (17.7%) of 45 gizzards were found to be contaminated with C. perfringens. Isolates were molecular characterized by using multiplex PCR with alpha (cpa), beta (cpb), beta 2 (cpb2), epsilon (etx), iota (iA) and enterotoxin (cpe) genes. Results showed that all isolates were carrying cpa gene and named as type A but none of them were positive for cpe gene. Only two gizzard isolates were positive for cpb2 gene. Our results indicate that edible offal of broiler are highly contaminated with C. perfringens type A which is mostly responsible for the foodborne poisoning worldwide. According to the high contamination rate edible offal should be considered as one of the important causes of C. perfringens type A foodborne disease

Keywords

Broiler edible offal Clostridium perfringens molecular typing multiplex PCR

References

  • Altay G, Keskin O, Akan M (2003): Tavuklardan izole edilen stafilokok suslarının identifikasyonu ve bazı antibiyotiklere duyarlılıklarının belirlenmesi. Turk J Vet Anim Sci, 27, 595-600.
  • Barnes HJ (2008): Clostridial diseases. 865-866. In: Saif YM (Ed). Disaeses of Poultry, Blackwell Publishing, State Avenue, Ames, Iowa, twelfth edition.
  • Baumgart J (1997): Mikrobiologische Untersuchung von Lebensmitteln. Hamburg: Behr’s Verlag.
  • Baumgart J, Baum O, Lippert S (1990): Schneller und direkter Fleischwirtschaft,70, 1010–1014. Clostridium perfringens. 5. Brynestad S, Granum PE (2002): Clostridium perfringens and foodborne infections. Int J Food Microbiol, 74, 195-202.
  • Craven SE, Stern NJ, Bailey JS, Cox NA (2001a): Incidence of Clostridium perfringens in broiler chickens and their environment during production and processing. Avian Dis, 45, 887-896.
  • Craven SE, Cox NA, Stern NJ, Mauldin JM (2001b): Prevalence of Clostridium perfringens in commercial broiler hatcheries. Avian Dis, 45, 1050-1053.
  • Cakmak O, Bilir Ormancı FS, Tayfur M, Erol I (2006): Presence and contamination level of Clostridium perfringens in raw frozen ground poultry and poultry burgers. Turk J Vet Anim Sci, 30, 101-105.
  • Dalton CB, Gregory J, Kirk MD, Stafford RJ, Givney R, Kraa E, Gould D (2004): Foodborne disease outbreak in Australia, 1995 to 2000. Commun Dis Intell Q Rep, 28, 211-224.
  • Erol I, Sireli UT, Gundes B (1999): Piliç parça et ve iç organlarında Listeria türlerinin varlığı ve kontaminasyon düzeyinin belirlenmesi. Ankara Univ Vet Fak Derg, 46, 179-188.
  • Erol I, Goncuoglu M, Ayaz ND, Bilir Ormanci FS, Hildebrandt G (2008): Molecular typing of Clostridium perfringens isolated from turkey meat by multiplex PCR. Lett Appl Microbiol, 47, 31-34.
  • Erol I, Hildebrandt G, Goncuoglu M, Kleer J (2010): “Verteilung der Salmonella-Serotypen in Schlachtkörpern und essbaren Innereien von türkischen Broilern - Serotype distribution of Salmonella in broiler carcasses and edible offal in Turkey” Fleischwirtschaft, 90, 106-109.
  • Gormley FJ, Little CL, Rawal N, Gillespie IA, Lebaigue S, Adak GK (2011): A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992-2008). Epidemiol Infect, 139, 688-699.
  • Grass JE, Gould LH, Mahon, BE (2013): Epidemiology of foodborne disease outbreaks caused by Clostridium perfringens, United States, 1998-2010. Foodborne Pathog Dis, 10, 131-136.
  • Guran HS, Oksuztepe G (2013): Detection and typing of Clostridium perfringens from retail chicken parts. Lett Appl Microbiol, 57, 77-82.
  • Hatheway CL (1990): Toxigenic clostridia. Clin Microbiol Rev, 3, 66-98.
  • Immerseel FV, De Buck J, Pasmans F, Huyghebaert G, Haesebrouck F, Ducatelle R (2004): Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian Pathol, 33, 537-549.
  • Juneja VK, Novak JS, Labbe RL (2010): Clostridium perfringens. 53-70. In: Juneja VK, Sofos JN (Ed). Pathogens and Toxins in Foods: Challenges and Interventions, ASM Press, Washington D.C.
  • Kass PH, Riemann HP (2006): Epidemiology of foodborne disease. 3-26. In: Riemann HP, Cliver DO (Ed). Foodborne Infections and Intoxications, Academic Press, third edition.
  • Labbe RG, Juneja VK (2006): Clostridium perfringens gastroenteritis. 137-184. In: Riemann HP, Cliver DO (Ed). Foodborne Infections and Intoxications, Academic Press, third edition.
  • Lee KW, Lillehoj HS, Jeong W, Jeoung HY, An DJ (2011): Avian necrotic enteritis: Experimental models, host immunity, pathogenesis, risk factors, and vaccine development. Poultry Sci, 90, 1381-1390.
  • Lin Y-T, Labbe R (2003): Enterotoxigenicity and genetic relatedness of Clostridium perfringens isolates from retail foods in the United States. Appl Environ Microbiol, 69, 1642-1646.
  • Lovland A, Kaldhusdal M (2001): Severely impaired production performance in broiler flocks with high incidence of Clostridium perfringens-associated hepatitis. Avian Pathol, 30, 73-81.
  • Meer RR, Songer JG (1997): Multiplex polymerase chain reaction assay for genotyping Clostridium perfringens. Am J Vet Res, 58, 702–705.
  • McClane BA (2007): Clostridium perfringens. 423-444. In: Doyle MP, Beuchat LR (Ed). Food Microbiology, Fundementals and Frontiers, third edition, ASM Press, Washington D.C.
  • Miki Y, Miyamoto K, Kaneko-Hirano I, Fujiuchi K, Akimoto S (2008): Prevalence and characterization of enterotoxin gene-carrying Clostridium perfringens isolates from retail meat products in Japan. Appl Environ Microbiol, 74, 5366-5372.
  • Miwa N, Nishina T, Kubo S, Atsumi M, Honda H (1998): Amount of enterotoxigenic Clostridium perfringens in meat detected by nested PCR. Int J Food Microbiol, 42, 195-200.
  • Mutluer B, Yargülü B, Hartung M, Erol I (1992): Incidence and serovar distribution of Salmonella in market broilers in Turkey. 3rd World Congress Food Borne Infections and Intoxications. 16-19 June 1992 Berlin- Germany.
  • Schalch B, Eisgruber H, Geppert P, Stolle A (1996): Vergleich von vier Routineverfahren zur Bestaetigung von Clostridium Lebensmittelhyg, 47, 27–30. aus
  • Titball RW, Naylor CE, Basak AK (1999): The Clostridium perfringens α-toxin. Anaerobe, 5, 51-64.
  • Voidarou C, Vassos D, Rozos G, Alexopoulos A, Plessas A, Tsinas A, Skoufou M, Stavropoulou E, Bezirtzoglou E (2011): Microbial challenges of poultry meat production. Anaerobe, 17, 341-343.
  • Wen Q, McClane BA (2004): Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Appl Environ Microbiol, 70, 2685-2691.

Yenilebilir piliç iç organlarında Clostridium perfringens prevalansı ve moleküler tiplendirilmesi

Year 2015, Volume: 62 Issue: 2, 113 - 117, 01.06.2015

Alireza Hanıfehnezhad Muammer Göncüoğlu İrfan Erol

https://doi.org/10.1501/Vetfak_0000002666

Abstract

Bu çalışmada yenilebilir piliç iç organlarında Clostridium perfringens prevalansı ve elde edilen izolatların moleküler karakterizasyonlarının belirlenmesi amaçlanmıştır. Çalışmada farklı süpermarketlerde satışa sunulan 45 kalp-karaciğer ve 45 taşlık olmak üzere toplam 90 yenilebilir iç organ soğuk zincir altında laboratuvara getirilerek aynı gün içerisinde analize alınmıştır. Örneklerden C. perfringens izolasyon ve identifikasyonunda klasik kültür tekniği ile asit fosfataz ve reverse-CAMP gibi biyokimyasal testler kullanılmıştır. Kırk beş kalp-karaciğer örneğinin 21’inin (% 46.7) ve 45 taşlık örneğinin sekizinin (% 17.7) C. perfringens ile kontamine olduğu saptanmıştır. Elde edilen izolatların alfa (cpa), beta (cpb), beta 2 (cpb2), epsilon (etx), iota (iA) ve enterotoksin (cpe) genlerine ait primer dizilimleri kullanılarak multipleks PCR ile moleküler tiplendirilmeleri yapılmıştır. Sonuçlar incelendiğinde bütün izolatların cpa geni taşıdığı belirlenmiş ve tip A olarak sınıflandırılmıştır, bununla beraber hiçbir izolatın cpe genine sahip olmadığı saptanmıştır. İki farklı taşlık örneğinden elde edilen izolatların cpa yanında cpb2 genini de taşıdıkları belirlenmiştir. Sonuç olarak yenilebilir piliç iç organlarının dünya genelinde gıda zehirlenmelerinde en sıklıkla rastlanan C. perfringens tip A ile yüksek oranda kontamine olduğu belirlenmiştir. Yüksek kontaminasyona bağlı olarak yenilebilir piliç iç organlarının C. perfringens tip A zehirlenmeleri açısından önemli birer kaynak oldukları saptanmıştır

Keywords

Clostridium perfringens moleküler tiplendirme multipleks PCR yenilebilir piliç iç organ

References

  • Altay G, Keskin O, Akan M (2003): Tavuklardan izole edilen stafilokok suslarının identifikasyonu ve bazı antibiyotiklere duyarlılıklarının belirlenmesi. Turk J Vet Anim Sci, 27, 595-600.
  • Barnes HJ (2008): Clostridial diseases. 865-866. In: Saif YM (Ed). Disaeses of Poultry, Blackwell Publishing, State Avenue, Ames, Iowa, twelfth edition.
  • Baumgart J (1997): Mikrobiologische Untersuchung von Lebensmitteln. Hamburg: Behr’s Verlag.
  • Baumgart J, Baum O, Lippert S (1990): Schneller und direkter Fleischwirtschaft,70, 1010–1014. Clostridium perfringens. 5. Brynestad S, Granum PE (2002): Clostridium perfringens and foodborne infections. Int J Food Microbiol, 74, 195-202.
  • Craven SE, Stern NJ, Bailey JS, Cox NA (2001a): Incidence of Clostridium perfringens in broiler chickens and their environment during production and processing. Avian Dis, 45, 887-896.
  • Craven SE, Cox NA, Stern NJ, Mauldin JM (2001b): Prevalence of Clostridium perfringens in commercial broiler hatcheries. Avian Dis, 45, 1050-1053.
  • Cakmak O, Bilir Ormancı FS, Tayfur M, Erol I (2006): Presence and contamination level of Clostridium perfringens in raw frozen ground poultry and poultry burgers. Turk J Vet Anim Sci, 30, 101-105.
  • Dalton CB, Gregory J, Kirk MD, Stafford RJ, Givney R, Kraa E, Gould D (2004): Foodborne disease outbreak in Australia, 1995 to 2000. Commun Dis Intell Q Rep, 28, 211-224.
  • Erol I, Sireli UT, Gundes B (1999): Piliç parça et ve iç organlarında Listeria türlerinin varlığı ve kontaminasyon düzeyinin belirlenmesi. Ankara Univ Vet Fak Derg, 46, 179-188.
  • Erol I, Goncuoglu M, Ayaz ND, Bilir Ormanci FS, Hildebrandt G (2008): Molecular typing of Clostridium perfringens isolated from turkey meat by multiplex PCR. Lett Appl Microbiol, 47, 31-34.
  • Erol I, Hildebrandt G, Goncuoglu M, Kleer J (2010): “Verteilung der Salmonella-Serotypen in Schlachtkörpern und essbaren Innereien von türkischen Broilern - Serotype distribution of Salmonella in broiler carcasses and edible offal in Turkey” Fleischwirtschaft, 90, 106-109.
  • Gormley FJ, Little CL, Rawal N, Gillespie IA, Lebaigue S, Adak GK (2011): A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992-2008). Epidemiol Infect, 139, 688-699.
  • Grass JE, Gould LH, Mahon, BE (2013): Epidemiology of foodborne disease outbreaks caused by Clostridium perfringens, United States, 1998-2010. Foodborne Pathog Dis, 10, 131-136.
  • Guran HS, Oksuztepe G (2013): Detection and typing of Clostridium perfringens from retail chicken parts. Lett Appl Microbiol, 57, 77-82.
  • Hatheway CL (1990): Toxigenic clostridia. Clin Microbiol Rev, 3, 66-98.
  • Immerseel FV, De Buck J, Pasmans F, Huyghebaert G, Haesebrouck F, Ducatelle R (2004): Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian Pathol, 33, 537-549.
  • Juneja VK, Novak JS, Labbe RL (2010): Clostridium perfringens. 53-70. In: Juneja VK, Sofos JN (Ed). Pathogens and Toxins in Foods: Challenges and Interventions, ASM Press, Washington D.C.
  • Kass PH, Riemann HP (2006): Epidemiology of foodborne disease. 3-26. In: Riemann HP, Cliver DO (Ed). Foodborne Infections and Intoxications, Academic Press, third edition.
  • Labbe RG, Juneja VK (2006): Clostridium perfringens gastroenteritis. 137-184. In: Riemann HP, Cliver DO (Ed). Foodborne Infections and Intoxications, Academic Press, third edition.
  • Lee KW, Lillehoj HS, Jeong W, Jeoung HY, An DJ (2011): Avian necrotic enteritis: Experimental models, host immunity, pathogenesis, risk factors, and vaccine development. Poultry Sci, 90, 1381-1390.
  • Lin Y-T, Labbe R (2003): Enterotoxigenicity and genetic relatedness of Clostridium perfringens isolates from retail foods in the United States. Appl Environ Microbiol, 69, 1642-1646.
  • Lovland A, Kaldhusdal M (2001): Severely impaired production performance in broiler flocks with high incidence of Clostridium perfringens-associated hepatitis. Avian Pathol, 30, 73-81.
  • Meer RR, Songer JG (1997): Multiplex polymerase chain reaction assay for genotyping Clostridium perfringens. Am J Vet Res, 58, 702–705.
  • McClane BA (2007): Clostridium perfringens. 423-444. In: Doyle MP, Beuchat LR (Ed). Food Microbiology, Fundementals and Frontiers, third edition, ASM Press, Washington D.C.
  • Miki Y, Miyamoto K, Kaneko-Hirano I, Fujiuchi K, Akimoto S (2008): Prevalence and characterization of enterotoxin gene-carrying Clostridium perfringens isolates from retail meat products in Japan. Appl Environ Microbiol, 74, 5366-5372.
  • Miwa N, Nishina T, Kubo S, Atsumi M, Honda H (1998): Amount of enterotoxigenic Clostridium perfringens in meat detected by nested PCR. Int J Food Microbiol, 42, 195-200.
  • Mutluer B, Yargülü B, Hartung M, Erol I (1992): Incidence and serovar distribution of Salmonella in market broilers in Turkey. 3rd World Congress Food Borne Infections and Intoxications. 16-19 June 1992 Berlin- Germany.
  • Schalch B, Eisgruber H, Geppert P, Stolle A (1996): Vergleich von vier Routineverfahren zur Bestaetigung von Clostridium Lebensmittelhyg, 47, 27–30. aus
  • Titball RW, Naylor CE, Basak AK (1999): The Clostridium perfringens α-toxin. Anaerobe, 5, 51-64.
  • Voidarou C, Vassos D, Rozos G, Alexopoulos A, Plessas A, Tsinas A, Skoufou M, Stavropoulou E, Bezirtzoglou E (2011): Microbial challenges of poultry meat production. Anaerobe, 17, 341-343.
  • Wen Q, McClane BA (2004): Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Appl Environ Microbiol, 70, 2685-2691.
There are 31 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Other ID JA45CU55ZN
Journal Section Research Article
Authors

Alireza Hanıfehnezhad

Muammer Göncüoğlu

İrfan Erol

Publication Date June 1, 2015
Published in Issue Year 2015Volume: 62 Issue: 2

Cite

APA Hanıfehnezhad, A., Göncüoğlu, M., & Erol, İ. (2015). Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 62(2), 113-117. https://doi.org/10.1501/Vetfak_0000002666
AMA Hanıfehnezhad A, Göncüoğlu M, Erol İ. Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler. Ankara Univ Vet Fak Derg. June 2015;62(2):113-117. doi:10.1501/Vetfak_0000002666
Chicago Hanıfehnezhad, Alireza, Muammer Göncüoğlu, and İrfan Erol. “Prevalence and Molecular Typing of Clostridium Perfringens Isolates from Edible Offal of Broiler”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 62, no. 2 (June 2015): 113-17. https://doi.org/10.1501/Vetfak_0000002666.
EndNote Hanıfehnezhad A, Göncüoğlu M, Erol İ (June 1, 2015) Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler. Ankara Üniversitesi Veteriner Fakültesi Dergisi 62 2 113–117.
IEEE A. Hanıfehnezhad, M. Göncüoğlu, and İ. Erol, “Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler”, Ankara Univ Vet Fak Derg, vol. 62, no. 2, pp. 113–117, 2015, doi: 10.1501/Vetfak_0000002666.
ISNAD Hanıfehnezhad, Alireza et al. “Prevalence and Molecular Typing of Clostridium Perfringens Isolates from Edible Offal of Broiler”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 62/2 (June 2015), 113-117. https://doi.org/10.1501/Vetfak_0000002666.
JAMA Hanıfehnezhad A, Göncüoğlu M, Erol İ. Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler. Ankara Univ Vet Fak Derg. 2015;62:113–117.
MLA Hanıfehnezhad, Alireza et al. “Prevalence and Molecular Typing of Clostridium Perfringens Isolates from Edible Offal of Broiler”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 62, no. 2, 2015, pp. 113-7, doi:10.1501/Vetfak_0000002666.
Vancouver Hanıfehnezhad A, Göncüoğlu M, Erol İ. Prevalence and molecular typing of Clostridium perfringens isolates from edible offal of broiler. Ankara Univ Vet Fak Derg. 2015;62(2):113-7.