Phenotypic and molecular detection of metallo-β-lactamase genes of Salmonella enterica strains isolated from poultry meat

Document Type: Original Article

Author

Assistant Professor, University of Mohaghegh Ardabili, Ardabil, Iran

Abstract

The present study was carried out to detect Salmonella enterica in meat samples of commercial boilers (CB) and the spent hens (SH) in Ardabil, Iran. Metallo-β-lactamase (MBL) enzyme produced by Salmonella enterica strains isolated from poultry meat samples were detected by both biochemical and molecular methods. The study included 20 positive samples for Salmonella  enterica from boilers (CB) and spent hens (SH). The prevalence of Salmonella enterica for CB was 22% (11/50) and for SH was 18% (9/50). The antibiotic susceptibility testing for both CB and SH showed maximum number of Salmonella enterica isolates were resistant against Augmentin (30 μg), Cotrimaxazole (25 μg) and Tetracycline (25 μg) and susceptible against Ofloxacin (5 μg) and Gentamicin (10 μg). Screening phenotypic confirmatory test for Metallo-β-lactamase (MBL) for CB, (n= 11, 100%) were positive for MBL while for SH (n= 8, 88.88%) samples were positive for MBL. The results showed that MBL positive Salmonella enterica isolates from CB and SH meat samples contained gene blaVIM (n=11, 57.89%), blaIMP (n=6, 31.57%) and blaSPM-1(n=2, 10.52%). Since Salmonella infections in poultry are high due to large demand and antibiotic resistance to strains, so the purpose of the current study is to focus on the detection of MBL enzyme produced by Salmonella enterica isolates.

Keywords


Addis, Z., Kebede, N., Sisay, Z., Alemayehu, H., Wubetie, A., and Kassa, T. (2011). Prevalence and antimicrobial resistance of Salmonella isolated from lactating cows and in contact humans in dairy farms of Addis Ababa: a cross sectional study, BMC Infect Dis. 11, 222.

Bush, K. and Jacoby, G.A.  (2010). Updated functional classification of beta-lactamases. Antimicrob Agents Chemother, 54(3), 969-76.

Bahar, M.A., Jamali, S. and Samadikuchaksaraei, A. (2010). Imipenem-resistant Pseudomonas aeruginosa strains carry metallo-beta-lactamase gene bla(VIM) in a level I Iranian burn hospital. Burns, 36(6), 826-30.

Boroumand, M. A., Anvari, M. S., and Habibi, E., Detection of vim- and ipm-type metallo-beta-lactamases in Pseudomonas aeruginosa clinical isolates. Arch Iran Med, 2012. 15(11): p. 670-3.

Brenner, F. W., Villar, R. G., Angulo, F. J., Tauxe, R., and Swaminathan, B. (2000). Salmonella nomenclature. J Clin Microbiol, 38(7), 2465-7.

Brunelle, B.W., Bearson, B.L. and Allen, H.K. (2017). Prevalence, evolution, and dissemination of antibiotic-resistance in Salmonella. Foodborne Pathog Ant Res. Om V. Singh, 331–348.

Chika, E., Chijioke, E., Ifeanyichukwu, I., Jerry, O., Stanley, E., Emmanuel, U., Carissa, D. and Charles, E. (2016). Antibiogram and Detection of Metallo-Beta-Lactamase (MBL) positive Escherichia coli isolates from abattoir. Nat  Sci, 14(11), 65-69.

Chika, E., Malachy, U., Ifeanyichukwu, I., Peter, E., Thaddeus, G. and Charles, E.(2014)  Phenotypic detection of metallo-β-lactamase (MBL) enzyme in Enugu, Southeast Nigeria.Am J Biol chem pharm Sci, 2(2),1-6.

Clinical Laboratory Standard Institute, C. (2011). Performance standards for antimicrobial disk susceptibility test. Fifteenth informational supplement, CLSI document M100-S15, Wayne, USA.

Crowder, M.W., Spencer, J., and Vila, A. J. (2006). Metallo-beta-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc Chem Res, 39(10), 721-8.

Ejikeugwu, C. D.C., Eluu, S., Oguejiofor, B., Ezeador, C., Ogene, L., Iroha, I. (2017). Isolation and Phenotypic Detection of Metallo-Beta-Lactamase (MBL)-Producing Klebsiella Species from Cow Anal Swabs. Glob J Pharmaceu Sci, 2(3).

Ezekiel, C.N., Olarinmoye, A.O., Jnr, J.O., Olaoye, O.B. and Edun, A.O. (2011). Distribution, antibiogram and multidrug resistance in Enterobacteriaceae from commercial poultry feeds in Nigeria. Afr  j microbiol  res, 5(3), 294-301.

Gautam, V., Singhal, L., Arora, S., Jha, C.  and Ray, P. (2013). Reliability of Kirby-Bauer disk diffusion method for detecting carbapenem resistance in Acinetobacter baumannii-calcoaceticus complex isolates. Antimicrob Agents Chemother, 57(4), 2003-4.

Ghamgosha, M., Shahrekizahedani, S., Kafilzadeh, F., Bameri, Z., Taheri, R. A. and Farnoosh, G. (2015). Metallo-beta-Lactamase VIM-1, SPM-1, and IMP-1 Genes Among Clinical Pseudomonas aeruginosa Species Isolated in Zahedan, Iran. Jundishapur J Microbiol, 8(4), e17489.

González-Sanz, R., Herrera-Leon, S., De la Fuente, M., Arroyo, M., and Echeita, M. A. (2009). Emergence of extended-spectrum β-lactamases and AmpC-type β-lactamases in human Salmonella isolated in Spain from 2001 to 2005. Journal of antimicrobial chemotherapy, 64(6), 1181-1186.

Graziani, C., Busani, L., Dionisi, A.M., Lucarelli, C., Owczarek, S., Ricci, A., Mancin, M., Caprioli, A. and Luzzi, I. (2008). Antimicrobial resistance in Salmonella enterica serovar Typhimurium from human and animal sources in Italy. Veterinary microbiology, 128(3-4), 414-418.

Hu, X. and Li, G. (2009). Advances in the relationship between integrons and drug resistance of bacteria. World Notes on Antibiotics, 30, 255-263.

Liakopoulos, A., Mavroidi, A., Katsifas, E. A., Theodosiou, A., Karagouni, A. D., Miriagou, V. and Petinaki, E. (2013). Carbapenemase-producing Pseudomonas aeruginosa from central Greece: molecular epidemiology and genetic analysis of class I integrons. BMC Infect Dis, 13, 505.

Miranda, J. M., Vázquez, B. I., Fente, C. A., Barros-Velázquez, J., Cepeda, A., and Franco, C.M. (2008). Evolution of resistance in poultry intestinal Escherichia coli during three commonly used antimicrobial therapeutic treatments in poultry. Poultry sci,  87(8), 1643-1648.

Moosavian, M. and Rahimzadeh, M. (2015). Molecular detection of metallo-beta-lactamase genes, bla IMP-1, bla VIM-2 and bla SPM-1 in imipenem resistant Pseudomonas aeruginosa isolated from clinical specimens in teaching hospitals of Ahvaz, Iran. Iran J Microbiol, 7(1), 2-6.

Murphy, T.A., Simm, A. M., Toleman, M. A., Jones, R. N., and Walsh, T. R. (2003). Biochemical characterization of the acquired metallo-β-lactamase SPM-1 from Pseudomonas aeruginosa. Antimicrobial agents and chemotherapy, 47(2), 582-587.

Qiao, J., et al., (2017). Characterization of extended-spectrum beta-lactamases (ESBLs)-producing Salmonella in retail raw chicken carcasses. Int J Food Microbiol, 248, 72-81.

Revathi, G., Shannon, K. P., Stapleton, P. D., Jain, B. K. and French, G. L. (1998). An outbreak of extended-spectrum, β-lactamase-producing Salmonella senftenberg in a burns ward. journal of Hospital Infection, 40(4), 295-302.

Rizek, C., Fu, L., dos Santos, L.C., Leite, G., Ramos, J., Rossi, F., and Costa, S. F. (2014). Characterization of carbapenem-resistant Pseudomonas aeruginosa clinical isolates, carrying multiple genes coding for this antibiotic resistance. Ann Clin Microbiol Antimicrob, 13, 43.

Rostagno, M.H., Wesley, I.V., Trampel, D.W., and Hurd, H.S. (2006). Salmonella prevalence in market-age turkeys on-farm and at slaughter. Poultry science, 85(10), 1838-1842.

RS, H. (2003). A global Salmonella surveillance and laboratory support project of the World Health Organization: Laboratory Protocols (Isolation of Salmonella) 4.

Sakaridis, I., Soultos, N., Iossifidou, E., Koidis, P., and Ambrosiadis, I. (2011). Prevalence and antimicrobial resistance of Salmonella serovars from chicken carcasses in northern Greece. J  Food Saf, 31(2), 203-210.

Schrader, K.N., Fernandez-Castro, A., Cheung, W. K., Crandall, C. M., and Abbott, S.L. (2008). Evaluation of commercial antisera for Salmonella serotyping. J Clin Microbiol, 46(2), 685-8.

Senda, K., Arakawa, Y., Ichiyama, S., Nakashima, K., Ito, H., Ohsuka, S., Shimokata, K., Kato, N. and Ohta, M. (1996). PCR detection of metallo-beta-lactamase gene (blaIMP) in gram-negative rods resistant to broad-spectrum beta-lactams. J  clin  microbiol, 34(12), 2909-2913.

Velge, P., Cloeckaert, A. and Barrow, P. (2005). Emergence of Salmonella epidemics: The problems related to Salmonella enterica serotyp Enteritidis and multiple antibiotic resistance in other major serotypes. Vet  res, 36(3), 267-288.

Walsh, T. R., Toleman, M. A., Poirel, L., and Nordmann, P. (2005). Metallo-β-lactamases: the quiet before the storm? Clin microbiol rev, 18(2), 306-325.

White, D.G., Zhao, S., Sudler, R., Ayers, S., Friedman, S., Chen, S., McDermott, P.F., McDermott, S., Wagner, D.D. and Meng, J. (2001). The isolation of antibiotic-resistant Salmonella from retail ground meats. New Eng   j  med, 345(16),1147-1154.

Yong, D., Toleman, M. A., Giske, C. G., Cho, H. S., Sundman, K., Lee, K. and Walsh, T. R. (2009). Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother, 53(12), 5046-54.