Marwa Halawa
Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh-33516, Egypt
Amgad Moawad
Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh-33516, Egypt
Ibrahim Eldesouky
Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh-33516, Egypt
Hazem Ramadan
Department of Hygiene and Zoonoses, Faculty of Veterinary Medicine, Mansoura University, Mansoura-35516, Egypt
ABSTRACT
This study was conducted to determine the occurrence, antimicrobial resistance profile, β-lactamase encoding genes and class I integrons (intI) of Salmonella serovars in broiler flocks. A total of 100 diseased chickens (5 samples per bird; cloacal swab, liver, gall bladder, spleen and intestinal content) were randomly selected from different broiler farms at Dakahliya and Kafrelsheikh Governorates, Egypt, during the period from September through December 2013. Conventional isolation and serotyping, antimicrobial resistance phenotyping, PCR identification of β-lactamase encoding genes and intI were performed. The culturing and serotyping identified 23 (23%) Salmonella isolates from diseased birds that belonged to 13 serotypes. The predominant serovars distinguished in this study were Salmonella Enteritidis, S. Typhimurium, S. Kentucky and S. Infantis that constituted 52.2% (12/23) of all isolates. By antimicrobial resistance testing, 87% (20/23) of isolates exhibited multidrug resistance (MDR; resistance to 5 or more antibiotics) mostly against vancomycin, oxacillin, amoxicillin, erythromycin and nalidixic acid. For 3rd generation cephalosporins, all the isolates were sensitive to cefoxitin and only 5 (21.7%) isolates displayed resistance to ceftriaxone and cefotaxime. Using PCR, all isolates were negative for blaSHV, blaCTX, blaCMY and blaOXA, while only 5 isolates (21.7%) harbored blaTEM (1080 bp). Variable amplicons with intI cassettes were detected by PCR from only 4 isolates (17.4%). Our findings highlighted the zoonotic potential of Salmonella in broilers with a possibility of antimicrobial resistance gene transmission to humans. Continuous surveillance is required to minimize the risk of human exposure to antimicrobial resistance pathogens from food producing animals.
PDF References Citation
How to cite this article
Marwa Halawa, Amgad Moawad, Ibrahim Eldesouky and Hazem Ramadan, 2016. Detection of Antimicrobial Phenotypes, β-Lactamase Encoding Genes and Class I Integrons in Salmonella Serovars Isolated from Broilers. International Journal of Poultry Science, 15: 1-7.
DOI: 10.3923/ijps.2016.1.7
URL: https://scialert.net/abstract/?doi=ijps.2016.1.7
DOI: 10.3923/ijps.2016.1.7
URL: https://scialert.net/abstract/?doi=ijps.2016.1.7
REFERENCES
- Abd-Elghany, S.M., K.I. Sallam, A. Abd-Elkhalek and T. Tamura, 2015. Occurrence, genetic characterization and antimicrobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol. Infect., 143: 997-1003.
CrossRefDirect Link - Abdellah, C., R.F. Fouzia, C. Abdelkader, S. Rachida and Z. Mouloud, 2009. Prevalence and anti-microbial susceptibility of Salmonella isolates from chicken carcasses and giblets in Meknes, Morocco. Afr. J. Microbiol. Res., 3: 215-219.
Direct Link - Ahmed, A.M. and T. Shimamoto, 2012. Genetic analysis of multiple antimicrobial resistance in Salmonella isolated from diseased broilers in Egypt. Microbiol. Immunol., 56: 254-261.
CrossRefDirect Link - Ahmed, A.M., H. Shimabukuro and T. Shimamoto, 2009. Isolation and molecular characterization of multidrug-resistant strains of Escherichia coli and Salmonella from retail chicken meat in Japan. J. Food Sci., 74: M405-M410.
CrossRefDirect Link - Ahmed, A.M., K. Furuta, K. Shimomura, Y. Kasama and T. Shimamoto, 2006. Genetic characterization of multidrug resistance in Shigella spp. from Japan. J. Med. Microbiol., 55: 1685-1691.
CrossRefDirect Link - Ahmed, A.M., Y. Motoi, M. Sato, A. Maruyama, H. Watanabe, Y. Fukumoto and T. Shimamoto, 2007. Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Applied Environ. Microbiol., 73: 6686-6690.
CrossRefDirect Link - Alcaine, S.D., L.D. Warnick and M. Wiedmann, 2007. Antimicrobial resistance in nontyphoidal Salmonella. J. Food Protect., 70: 780-790.
Direct Link - Asakura, H., O. Tajima, M. Watarai, T. Shirahata, H. Kurazono and S. Makino, 2001. Effects of rearing conditions on the colonization of Salmonella enteritidis in the cecum of chicks. J. Vet. Med. Sci., 63: 1221-1224.
CrossRefDirect Link - Bronzwaer, S.L., O. Cars, U. Buchholz, S. Moelstad and W. Goettsch et al., 2002. A European study on the relationship between antimicrobial use and antimicrobial resistance. Emerg. Infect. Dis., 8: 278-282.
PubMed - Capita, R., M. Alvarez-Astorga, C. Alonso-Calleja, B. Moreno and M.D.C. Garcia-Fernandez, 2003. Occurrence of salmonellae in retail chicken carcasses and their products in Spain. Int. J. Food Microbiol., 81: 169-173.
CrossRefDirect Link - Cardinale, E., J.D.P. Gros-Claude, K. Rivoal, V. Rose, F. Tall, G.C. Mead and G. Salvat, 2005. Epidemiological analysis of Salmonella enterica ssp. enterica serovars Hadar, Brancaster and Enteritidis from humans and broiler chickens in Senegal using pulsed-field gel electrophoresis and antibiotic susceptibility. J. Applied Microbiol., 99: 968-977.
CrossRefDirect Link - Carraminana, J.J., C. Rota, I. Agustin and A. Herrera, 2004. High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain. Vet. Microbiol., 104: 133-139.
CrossRefDirect Link - De Oliveira, D.S., F.S. Flores, L.R. dos Santos and A. Brandelli, 2005. Antimicrobial resistance in Salmonella enteritidis strains isolated from broiler carcasses, food, human and poultry-related samples. Int. J. Food Microbiol., 97: 297-305.
CrossRefDirect Link - Elumalai, S., G. Muthu, R.E.M. Selvam and S. Ramesh, 2014. Detection of TEM-, SHV- and CTX-M-type β-lactamase production among clinical isolates of Salmonella species. J. Med. Microbiol., 63: 962-967.
CrossRefDirect Link - Gantois, I., R. Ducatelle, F. Pasmans, F. Haesebrouck, R. Gast, T.J. Humphrey and F. van Immerseel, 2009. Mechanisms of egg contamination by Salmonella enteritidis. FEMS Microbiol. Rev., 33: 718-738.
CrossRefPubMedDirect Link - Hendriksen, R.S., A.R. Vieira, S. Karlsmose, D.M. Lo Fo Wong, A.B. Jensen, H.C. Wegener and F.M. Aarestrup, 2011. Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: Results of quality assured laboratories from 2001 to 2007. Foodborne Pathog. Dis., 8: 887-900.
CrossRefDirect Link - Hur, J., C. Jawale and J.H. Lee, 2012. Antimicrobial resistance of Salmonella isolated from food animals: A review. Food Res. Int., 45: 819-830.
CrossRefDirect Link - Kim, M.S., T.H. Lim, J.H. Jang, D.H. Lee and B.Y. Kim et al., 2012. Prevalence and antimicrobial resistance of Salmonella species isolated from chicken meats produced by different integrated broiler operations in Korea. Poult. Sci., 91: 2370-2375.
CrossRefPubMedDirect Link - Landers, T.F., B. Cohen, T.E. Wittum and E.L. Larson, 2012. A review of antibiotic use in food animals: Perspective, policy and potential. Public Health Rep., 127: 4-22.
Direct Link - Le Bouquin, S., V. Allain, S. Rouxel, I. Petetin, M. Picherot, V. Michel and M. Chemaly, 2010. Prevalence and risk factors for Salmonella spp. contamination in French broiler-chicken flocks at the end of the rearing period. Prev. Vet. Med., 97: 245-251.
CrossRefDirect Link - Lu, Y., H. Zhao, J. Sun, Y. Liu and X. Zhou et al., 2014. Characterization of multidrug-resistant Salmonella enterica serovars indiana and enteritidis from chickens in eastern China. PLoS ONE, Vol. 9.
CrossRefDirect Link - Madhulika, U., B.N. Harish and S.C. Parija, 2004. Current pattern in antimicrobial susceptibility of Salmonella Typhi isolates in Pondicherry. Indian J. Med. Res., 120: 111-114.
PubMed - Malek, M.M., F.A. Amer, A.A. Allam, R.H. El-Sokkary, T. Gheith and M.A. Arafa, 2015. Occurrence of classes I and II integrons in Enterobacteriaceae collected from Zagazig university hospitals, Egypt. Front. Microbiol., Vol. 6.
CrossRefDirect Link - Mazel, D., 2006. Integrons: Agents of bacterial evolution. Nat. Rev. Microbiol., 4: 608-620.
CrossRefDirect Link - Mihaiu, L., A. Lapusan, R. Tanasuica, R. Sobolu, R. Mihaiu, O. Oniga and M. Mihaiu, 2014. First study of Salmonella in meat in Romania. J. Infect. Dev. Countries, 8: 50-58.
CrossRefDirect Link - Mollenhorst, H., C.J. van Woudenbergh, E.G.M. Bokkers and I.J.M. de Boer, 2005. Risk factors for Salmonella enteritidis infections in laying hens Poult. Sci., 84: 1308-1313.
CrossRefDirect Link - Namata, H., E. Meroc, M. Aerts, C. Faes, J.C. Abrahantes, H. Imberechts and K. Mintiens, 2008. Salmonella in belgian laying hens: An identification of risk factors. Prev. Vet. Med., 83: 323-336.
CrossRefPubMedDirect Link - Paterson, D.L., 2006. Resistance in gram-negative bacteria: Enterobacteriaceae. Am. J. Med., 119: S20-S28.
CrossRefPubMedDirect Link - Rostagno, M.H., I.V. Wesley, D.W. Trampel and H.S. Hurd, 2006. Salmonella prevalence in market-age Turkeys on-farm and at slaughter. Poult. Sci., 85: 1838-1842.
CrossRefDirect Link - Rowe-Magnus, D.A., A.M. Guerout and D. Mazel, 2002. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol. Microbiol., 43: 1657-1669.
CrossRefDirect Link - Sallam, K.I., M.A. Mohammed, M.A. Hassan and T. Tamura, 2014. Prevalence, molecular identification and antimicrobial resistance profile of Salmonella serovars isolated from retail beef products in Mansoura, Egypt. Food Control, 38: 209-214.
CrossRefDirect Link - Samanta, I., S.N. Joardar, P.K. Das, T.K. Sar, S. Bandyopadhyay, T.K. Dutta and U. Sarkar, 2014. Prevalence and antibiotic resistance profiles of Salmonella serotypes isolated from backyard poultry flocks in West Bengal, India. J. Applied Poult. Res., 23: 536-545.
CrossRefDirect Link - Shahada, F., T. Chuma, K. Okamoto and M. Sueyoshi, 2008. Temporal distribution and genetic fingerprinting of Salmonella in broiler flocks from Southern Japan. Poult. Sci., 87: 968-972.
CrossRefDirect Link - Shrestha, A., P. Regmi and R.K. Dutta, 2010. First report of antimicrobial resistance of Salmonella isolated from poultry in Nepal. Vet. Microbiol., 144: 522-524.
CrossRefDirect Link - Singer, R.S. and C.L. Hofacre, 2006. Potential impacts of antibiotic use in poultry production. Avian Dis., 50: 161-172.
CrossRefDirect Link - Siu, L.K., J.Y.C. Lo, K.Y. Yuen, P.Y. Chau, M.H. Ng and P.L. Ho, 2000. β-Lactamases in Shigella flexneri isolates from Hong Kong and Shanghai and a novel OXA-1-like β-lactamase, OXA-30. Antimicrob. Agents Chemother., 44: 2034-2038.
CrossRefDirect Link - Sow, A.G., A.A. Wane, M.H. Diallo, C.S.B. Boye and A. Aidara-Kane, 2007. Genotypic characterization of antibiotic-resistant Salmonella enteritidis isolates in Dakar, Senegal. J. Infect. Dev. Countries, 1: 284-288.
PubMedDirect Link - Srinivasan, P., G.A. Balasubramaniam, T.R.G.K. Murthy, S. Saravanan and P. Balachandran, 2014. Prevalence and pathology of salmonellosis in commercial layer chicken from Namakkal, India. Pak. Vet. J., 34: 324-328.
Direct Link - Trampel, D.W., T.G. Holder and R.K. Gast, 2014. Integrated farm management to prevent Salmonella Enteritidis contamination of eggs. J. Applied Poult. Res., 23: 353-365.
CrossRefDirect Link - Volkova, V.V., R.W. Wills, S.A. Hubbard, D. Magee, J.A. Byrd and R.H. Bailey, 2011. Associations between vaccinations against protozoal and viral infections and Salmonella in broiler flocks. Epidemiol. Infect., 139: 206-215.
CrossRefDirect Link - Weill, F.X., M. Demartin, D. Tande, E. Espie, I. Rakotoarivony and P.A. Grimont, 2004. SHV-12-like extended-spectrum-β-lactamase-producing strains of Salmonella enterica serotypes Babelsberg and Enteritidis isolated in France among infants adopted from Mali. J. Clin. Microbiol., 42: 2432-2437.
CrossRefDirect Link - White, P.A., C.J. McIver and W.D. Rawlinson, 2001. Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob. Agents Chemother., 45: 2658-2661.
CrossRefDirect Link - Yildirim, Y., Z. Gonulalan, S. Pamuk and N. Ertas, 2011. Incidence and antibiotic resistance of Salmonella spp. on raw chicken carcasses. Food Res. Int., 44: 725-728.
CrossRefDirect Link - Zhao, S., S. Qaiyumi, S. Friedman, R. Singh and S.L. Foley et al., 2003. Characterization of Salmonella enterica serotype newport isolated from humans and food animals. J. Clin. Microbiol., 41: 5366-5371.
CrossRefDirect Link