Molecular characterization of multidrug resistant Salmonella from chicken and human in Yaounde
Main Article Content
Abstract
Salmonella is one of the most common foodborne pathogens worldwide and chicken has been recognized as its main reservoir for human. The aim of this study was to investigate the occurrence of antimicrobial resistance genes in Salmonella isolates from chicken and human, and evaluate their genetic relationship. A total of 200 Salmonella strains (103 from Chicken and 97 from humans) were collected from 2006 to 2007 in Yaounde, and characterized for their antimicrobial susceptibility to a panel of 16 antimicrobials. Presence of antimicrobial resistance genes, class1 and class 2 integrons was investigated by PCR in Multidrug Resistant (MDR) isolates. Pulsed-Field Gel Electrophoresis (PFGE) analysis was used to investigate their genetic relatedness. Only serotypes Enteritidis, Hadar, Bareilly and II were recovered from both chicken and human. Overall, 16 isolates (8%) were susceptible to all antimicrobials including third generation cephalosporins and fluoroquinolons. Resistance was mostly observed to tetracycline (57%) in chicken isolates and to sulfonamides (78.3%) in human isolates. 78 (15.3%) strains were MDR. Class 1 integron was predominant in MDR Hadar and Typhimurium isolates. TEM-1 was the unique Extended Spectrum β-lactamase (ESBL) detected in the β-lactam resistant Typhimurium strain isolated from human. No qnr genes were identified in nalidixic acid resistant isolates. PFGE typing of Enteritidis isolates using XbaI restriction enzyme showed close genetic relationship between chicken and human isolates. For Hadar and Typhimurirum, variety of restriction patterns was observed. These results highlight the need for continuous surveillance of antimicrobial resistance in Salmonella isolates in Cameroon.
Article Details
How to Cite
NZOUANKEU, Ariane et al.
Molecular characterization of multidrug resistant Salmonella from chicken and human in Yaounde.
Medical Research Archives, [S.l.], v. 4, n. 8, dec. 2016.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/914>. Date accessed: 24 nov. 2024.
Keywords
Salmonella, Antimicrobial resistance, integrons, PFGE, Cameroon
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Aarestrup, F. M., Bager, F., Jensen, N. E., Madsen, M., Meyling, A., & Wegener, H. C. (1998). Resistance to antimicrobial agents used for animal therapy in pathogenic-, zoonotic and indicator bacteria isolated from different food animals in Denmark: a baseline study for the Danish Integrated Antimicrobial Resistance Monitoring Programme. DANMAP. (APMIS), 106, 745-770.
2. Aarestrup, F. M., Lertworapreecha, M., Evans, M. C., Bangtrakulnonth, A., Chalermchaikit, T., Hendriksen, R. S., & Wegener, H. C. (2003). Antimicrobial susceptibility and occurrence of resistance genes among Salmonella enterica serovar Weltevreden from different countries. J Antimicrob Chemother, 52, 715-718.
3. Ahmed, A.M., Furuta, K., Shimomura, K., Kasama, Y., & Shimamoto, T. (2006). Genetic characterization of multidrug resistance in Shigella spp. from Japan. J Med Microbiol, 55, 1685-1691.
4. An, V. T. T., Duijkeren, E. v., Fluit, A. C., & Gaastra, W. (2006). Characterization of resistance genes associated with class 1 integrons in non-typhoid Salmonella. Proceedings of International Workshop on Biotechnology in Agriculture, 92-95.
5. Angulo, F. J., & Swerdlow, D. L. (1998). Salmonella Enteritidis infections in the United States. J Am Vet Med Assoc 213, 1729-1731.
6. Antunes, P., Machado, J., Sousa, J. C., & Peixe, L. (2009). Dissemination of Sulfonamide Resistance Genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica Strains and Relation with Integrons. Antimicrob Agents Chemother, 49(2), 836-839.
7. Baümler, A. J., Hargis, B. M., & Tsolis, R. M. (2000). Tracing the origins of Salmonella outbreaks. Science, 287, 50-52.
8. Brenner, G. M., Butaye, P., Cloeckaert, A., & Schwarzt, S. (2006). Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microb Infect, 8, 1898-1914.
9. Byrne-Bailey, K. G., Gaze, W. H., Kay, P., Boxall, A. B. A., Hawkey, P. M., & Wellington, E. M. H. (2009). Prevalence of Sulfonamide Resistance Genes in Bacterial Isolates from Manured Agricultural Soils and Pig Slurry in the United Kingdom. Antimicrobial Agents and Chemotherapy, 53(2), 696-702.
10. Carattoli, A., Filetici, E., Villa, L., Dionisi, A. M., Ricci, A., & Luzzi, I. (2002). Antibiotic Resistance Genes and Salmonella Genomic Island 1 in Salmonella enterica Serovar Typhimurium Isolated in Italy. Antimicrob Agents Chemother, 46(9), 2821-2828.
11. CASFM (Comité de l'Antibiogramme de la Société Française de Microbiologie). (2007). Recommandations 2007. Paris, France.
12. Cruchaga, S., Echeitaa, A., Aladueñaa, A., García-Peñab, J., Friasb, N., & Useraa, A. (2001). Antimicrobial resistance in Salmonella from humans, food and animals in Spain in 1998. J Antimicrob Chemother, 47(3), 315-321.
13. Donado-Godoy, P., Clavijo, V., Leon, M., Taffur, M., Gonzales, S., Hume, M., . . . Doyle, M. P. (2012). Prevalence of Salmonella on Retail Broiler Chicken Meat Carcasses in Colombia. J Food Protect 75(6), 1134-1138.
14. Elgroud, R., Granier, S. A., Marault, M., Kerouanton, A., Lezzar, A., Bouzitouna-Bentchouala, C., . . . Millemann, Y. (2015). Contribution of Avian Salmonella enterica Isolates to Human Salmonellosis Cases in Constantine (Algeria). BioMed Res Int, 2015(1-7).
15. Fluit, A. C. (2005). Towards more virulent and antibiotic-resistant Salmonella? Fems Immunol Med Mic, 43, 1-11.
16. Foley, S., Nayak, R., Hanning, I. B., Johnson, T. J., Han, J., & Ricke, S. C. (2011). Population Dynamics of Salmonella enterica Serotypes in Commercial Egg and Poultry Production. Appl Environ Microbiol, 77(13), 4273-4279.
17. Fortini, D., Fashae, K., Garcia-Fernandez, A., Villa, L., & Carattoli, A. (2010). High prevalence of qnr genes in Escherichia coli and Salmonella from healthy animals in Nigeria. In Antimicrobial Resistance in zoonotic bacteria and foodborne pathogens in animals, humans and the environment. ASM conferences 2010, Toronto, Canada.
18. Garnier, F., Raked, N., Gassama, A., Denis, F., & Ploy, M. C. (2006). Genetic Environment of Quinolone Resistance Gene qnrB2 in a Complex sul1-Type Integron in the newly described Salmonella enterica serovar Keurmassar. Antimicrob Agents Chemother, 50(9), 3200-3202.
19. Gassama, S. A., Wane, A. A., Canu, N. A., Uzzau, S., Aidara-Kane, A., & Rubino, S. (2006). Characterization of virulence factors in the newly described Salmonella enterica serotype Keurmassar emerging in Senegal (sub-Saharan Africa). Epidemiology and Infection, 134, 741-743.
20. Govender, N., Smith, A. M., Karstaedt, A. S., & Keddy, K. H. (2009). Plasmid-mediated quinolone resistance in Salmonella from South Africa. 58J Med Microbiol, 10, 1393-1394.
21. Grimont, P. A. D., & Weill, F. X. (2007). Antigenic formulas of the Salmonella serovars. Paris, France.
22. Guardabassi, L., Dijkshoorn, L., Collard, J. M., Olsen, J. E., & Dalsgaard, A. (2000). Distribution and in-vitro transfer of tetracycline resistance determinants in clinical and aquatic Acinetobacter strains. J Med Microbiol, 49, 929-936.
23. http://www.pulsenetinternational.org/protocols. (2009). Standardized Laboratory Protocol for Molecular Subtyping of Escherichia coli O157:H7, Salmonella serotypes, Shigella sonnei, and Shigella flexneri by Pulsed Field Gel Electrophoresis (PFGE). Accessed on 22th may 2013.
24. Iwanaga, M., Toma, C., Miyazato, T., Insisiengmay, S., Nakasone, N., & Masahiko, E. (2004). Antibiotic resistance conferred by a class I integron and SXT constin in Vibrio cholerae O1 strains isolated in Laos. Antimicrob Agents Chemother , 48, 2364-2369.
25. Jacoby, G. A., Chow, N., & Waites, K.B. (2003). Prevalence of plasmid-mediated quinolone resistance. Antimicrob Agents Chemother, 47, 559–562.
26. Kabir, S. M. L. (2010). Avian Colibacillosis and Salmonellosis: A Closer Look at Epidemiology, Pathogenesis, diagnosis, Control and Public Health Concerns. Int. J. Environ. Res. Public Health, 7(1), 89-114.
27. Kern, M. B., Klemmensen, T., Frimodt-Moller, T., & Espersen, F. (2002). Suceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamides resistance. J Antimicrob Chemother, 52, 1022-1024.
28. Leader, B. T., Frye, J. G., Hu, J., Fedorka-Cray, P. J., & Boyle, D. S. (2009). High-Throughput Molecular Determination of Salmonella enterica Serovars by Use of Multiplex PCR and Capillary Electrophoresis Analysis. J Clin Microbiol, 47(5), 1290-1299.
29. Lévesque, C., Piché, L., Larose, C., & Roy, P. H. (1995). PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother, 39, 185-191.
30. M'ikanatha, N. M., Sandt, C. H., Localio, A. R., Tewari, D., Rankin, S. C., Whichard, J. M., . . . McDermott, P. F. (2010). Multidrug-resistant Salmonella isolates from retail chicken meat compared with human clinical isolates. Foodborne Pathog Dis, 7(8), 929-934.
31. Morpeth, S. C., Ramadhani, H. O., & Crump, J. A. (2009). Invasive Non-Typhi Salmonella Disease in Africa. Clin Infect Dis, 49, 606-611.
32. Okamoto, A. S., Andreatti, F. R. L., Rocha, T. S., Menconi, A., & Marietto-Gonçalves, G. A. (2009). Detection and Transfer of Antimicrobial Resistance Gene Integron in Salmonella Enteritidis Derived from Avian Material. Braz J Poult Sci, 3(11), 195 - 201.
33. Olesen, I., Hasman, H., & Aarestrup, F. M. (2004). Prevalence of β-lactamases among ampicillin resistant Escherichia coli and Salmonella isolated from food animals in Denmark. Microb Drug Resis, 10, 334-340.
34. Pezzella, C., Ricci, A., DiGiannatale, E., Luzzi, I., & Carattoli, A. (2004). Tetracycline and Streptomycin Resistance Genes, Transposons, and Plasmids in Salmonella enterica Isolates from Animals in Italy. Antimicrob Agents Chemother, 8(3), 903-908.
35. Phillipa, M. A. S., Jesudason, M. V., Thomson, C. J., & Amyes, S. G. B. (1998). Molecular Analysis of and Identification of Antibiotic Resistance Genes in Clinical Isolates of Salmonella Typhi from India. J Clin Microbiol, 36(6), 1595-1600.
36. Ploy, M. C., Gassama, A., Chainier, D., & Denis, F. (2005). Les intégrons en tant que support génétique de résistance aux antibiotiques. Immuno Anal Biol Spe, 20, 343-352.
37. REMIC (Référentiel en microbiologie médicale (bactériologie et mycologie)). (2007). Société Française de Microbiologie, 4ème édition, 370 pages. .
38. Ruiz, J., Castro, D., Goni, P., Santamaria, J. A., Borrego, J. J., & Vila, J. (2000). Analysis of the mechanism of quinolone resistance in nalidixic acid-resistant clinical isolates of Salmonella serotype Typhimurium. J Med Microbiol, 46, 623-628.
39. Turner, S. A., Luck, S. N., Sakellaris, H., Rajakumar, K., & Adler, B. (2003). Molecular epidemiology of the SRL pathogenicity island. Antimicrob Agents Chemother, 47, 727-734. (2003).
40. Walker, R. A., Lawson, A. J., Lindsay, E. A., Ward, L. R., Wright, P. A., Bolton, F. J., . . . Threlfall, E. J. (2000). Decreased susceptibility to ciprofloxacin in outbreak-associated multiresistant Salmonella Typhimurium DT104. Vet Rec, 147, 395-396.
41. Weill, F. X., Demartin, M., Tande, D., Espié, E., Rakotoarivony, .I, & Grimont PAD (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.
42. White, P. A., Mclver, C. J., & Rawlinson, W. D. (2001). Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother, 45, 2658- 2661.
43. WHO. (2013). Salmonella (non-typhoidal) Fact sheet N°139. http://www.who.int/mediacentre/factsheets/fs139/en/ accessed on 18/11/2015.
44. Wouafo, M., Nzouankeu, A., Kinfack, J. A., Fonkoua, M. C., Ejenguele, G., Njine, T., & Ngandjio, A. (2010). Prevalence and Antimicrobial Resistance of Salmonella Serotypes in Chickens from Retail Markets in Yaounde (Cameroon). Microb Drug Resis, 16(2), 171- 176.
45. Zhao, S., McDermott, P. F., Friedman, S., Abbott, J., Ayers, S., Glenn, A., . . . White, D. G. (2006). Antimicrobial resistance and genetic relatedness among Salmonella from retail foods of animal origin: NARMS retail meat surveillance. Foodborne Pathog Dis, 3(1), 106-117.
2. Aarestrup, F. M., Lertworapreecha, M., Evans, M. C., Bangtrakulnonth, A., Chalermchaikit, T., Hendriksen, R. S., & Wegener, H. C. (2003). Antimicrobial susceptibility and occurrence of resistance genes among Salmonella enterica serovar Weltevreden from different countries. J Antimicrob Chemother, 52, 715-718.
3. Ahmed, A.M., Furuta, K., Shimomura, K., Kasama, Y., & Shimamoto, T. (2006). Genetic characterization of multidrug resistance in Shigella spp. from Japan. J Med Microbiol, 55, 1685-1691.
4. An, V. T. T., Duijkeren, E. v., Fluit, A. C., & Gaastra, W. (2006). Characterization of resistance genes associated with class 1 integrons in non-typhoid Salmonella. Proceedings of International Workshop on Biotechnology in Agriculture, 92-95.
5. Angulo, F. J., & Swerdlow, D. L. (1998). Salmonella Enteritidis infections in the United States. J Am Vet Med Assoc 213, 1729-1731.
6. Antunes, P., Machado, J., Sousa, J. C., & Peixe, L. (2009). Dissemination of Sulfonamide Resistance Genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica Strains and Relation with Integrons. Antimicrob Agents Chemother, 49(2), 836-839.
7. Baümler, A. J., Hargis, B. M., & Tsolis, R. M. (2000). Tracing the origins of Salmonella outbreaks. Science, 287, 50-52.
8. Brenner, G. M., Butaye, P., Cloeckaert, A., & Schwarzt, S. (2006). Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microb Infect, 8, 1898-1914.
9. Byrne-Bailey, K. G., Gaze, W. H., Kay, P., Boxall, A. B. A., Hawkey, P. M., & Wellington, E. M. H. (2009). Prevalence of Sulfonamide Resistance Genes in Bacterial Isolates from Manured Agricultural Soils and Pig Slurry in the United Kingdom. Antimicrobial Agents and Chemotherapy, 53(2), 696-702.
10. Carattoli, A., Filetici, E., Villa, L., Dionisi, A. M., Ricci, A., & Luzzi, I. (2002). Antibiotic Resistance Genes and Salmonella Genomic Island 1 in Salmonella enterica Serovar Typhimurium Isolated in Italy. Antimicrob Agents Chemother, 46(9), 2821-2828.
11. CASFM (Comité de l'Antibiogramme de la Société Française de Microbiologie). (2007). Recommandations 2007. Paris, France.
12. Cruchaga, S., Echeitaa, A., Aladueñaa, A., García-Peñab, J., Friasb, N., & Useraa, A. (2001). Antimicrobial resistance in Salmonella from humans, food and animals in Spain in 1998. J Antimicrob Chemother, 47(3), 315-321.
13. Donado-Godoy, P., Clavijo, V., Leon, M., Taffur, M., Gonzales, S., Hume, M., . . . Doyle, M. P. (2012). Prevalence of Salmonella on Retail Broiler Chicken Meat Carcasses in Colombia. J Food Protect 75(6), 1134-1138.
14. Elgroud, R., Granier, S. A., Marault, M., Kerouanton, A., Lezzar, A., Bouzitouna-Bentchouala, C., . . . Millemann, Y. (2015). Contribution of Avian Salmonella enterica Isolates to Human Salmonellosis Cases in Constantine (Algeria). BioMed Res Int, 2015(1-7).
15. Fluit, A. C. (2005). Towards more virulent and antibiotic-resistant Salmonella? Fems Immunol Med Mic, 43, 1-11.
16. Foley, S., Nayak, R., Hanning, I. B., Johnson, T. J., Han, J., & Ricke, S. C. (2011). Population Dynamics of Salmonella enterica Serotypes in Commercial Egg and Poultry Production. Appl Environ Microbiol, 77(13), 4273-4279.
17. Fortini, D., Fashae, K., Garcia-Fernandez, A., Villa, L., & Carattoli, A. (2010). High prevalence of qnr genes in Escherichia coli and Salmonella from healthy animals in Nigeria. In Antimicrobial Resistance in zoonotic bacteria and foodborne pathogens in animals, humans and the environment. ASM conferences 2010, Toronto, Canada.
18. Garnier, F., Raked, N., Gassama, A., Denis, F., & Ploy, M. C. (2006). Genetic Environment of Quinolone Resistance Gene qnrB2 in a Complex sul1-Type Integron in the newly described Salmonella enterica serovar Keurmassar. Antimicrob Agents Chemother, 50(9), 3200-3202.
19. Gassama, S. A., Wane, A. A., Canu, N. A., Uzzau, S., Aidara-Kane, A., & Rubino, S. (2006). Characterization of virulence factors in the newly described Salmonella enterica serotype Keurmassar emerging in Senegal (sub-Saharan Africa). Epidemiology and Infection, 134, 741-743.
20. Govender, N., Smith, A. M., Karstaedt, A. S., & Keddy, K. H. (2009). Plasmid-mediated quinolone resistance in Salmonella from South Africa. 58J Med Microbiol, 10, 1393-1394.
21. Grimont, P. A. D., & Weill, F. X. (2007). Antigenic formulas of the Salmonella serovars. Paris, France.
22. Guardabassi, L., Dijkshoorn, L., Collard, J. M., Olsen, J. E., & Dalsgaard, A. (2000). Distribution and in-vitro transfer of tetracycline resistance determinants in clinical and aquatic Acinetobacter strains. J Med Microbiol, 49, 929-936.
23. http://www.pulsenetinternational.org/protocols. (2009). Standardized Laboratory Protocol for Molecular Subtyping of Escherichia coli O157:H7, Salmonella serotypes, Shigella sonnei, and Shigella flexneri by Pulsed Field Gel Electrophoresis (PFGE). Accessed on 22th may 2013.
24. Iwanaga, M., Toma, C., Miyazato, T., Insisiengmay, S., Nakasone, N., & Masahiko, E. (2004). Antibiotic resistance conferred by a class I integron and SXT constin in Vibrio cholerae O1 strains isolated in Laos. Antimicrob Agents Chemother , 48, 2364-2369.
25. Jacoby, G. A., Chow, N., & Waites, K.B. (2003). Prevalence of plasmid-mediated quinolone resistance. Antimicrob Agents Chemother, 47, 559–562.
26. Kabir, S. M. L. (2010). Avian Colibacillosis and Salmonellosis: A Closer Look at Epidemiology, Pathogenesis, diagnosis, Control and Public Health Concerns. Int. J. Environ. Res. Public Health, 7(1), 89-114.
27. Kern, M. B., Klemmensen, T., Frimodt-Moller, T., & Espersen, F. (2002). Suceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamides resistance. J Antimicrob Chemother, 52, 1022-1024.
28. Leader, B. T., Frye, J. G., Hu, J., Fedorka-Cray, P. J., & Boyle, D. S. (2009). High-Throughput Molecular Determination of Salmonella enterica Serovars by Use of Multiplex PCR and Capillary Electrophoresis Analysis. J Clin Microbiol, 47(5), 1290-1299.
29. Lévesque, C., Piché, L., Larose, C., & Roy, P. H. (1995). PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother, 39, 185-191.
30. M'ikanatha, N. M., Sandt, C. H., Localio, A. R., Tewari, D., Rankin, S. C., Whichard, J. M., . . . McDermott, P. F. (2010). Multidrug-resistant Salmonella isolates from retail chicken meat compared with human clinical isolates. Foodborne Pathog Dis, 7(8), 929-934.
31. Morpeth, S. C., Ramadhani, H. O., & Crump, J. A. (2009). Invasive Non-Typhi Salmonella Disease in Africa. Clin Infect Dis, 49, 606-611.
32. Okamoto, A. S., Andreatti, F. R. L., Rocha, T. S., Menconi, A., & Marietto-Gonçalves, G. A. (2009). Detection and Transfer of Antimicrobial Resistance Gene Integron in Salmonella Enteritidis Derived from Avian Material. Braz J Poult Sci, 3(11), 195 - 201.
33. Olesen, I., Hasman, H., & Aarestrup, F. M. (2004). Prevalence of β-lactamases among ampicillin resistant Escherichia coli and Salmonella isolated from food animals in Denmark. Microb Drug Resis, 10, 334-340.
34. Pezzella, C., Ricci, A., DiGiannatale, E., Luzzi, I., & Carattoli, A. (2004). Tetracycline and Streptomycin Resistance Genes, Transposons, and Plasmids in Salmonella enterica Isolates from Animals in Italy. Antimicrob Agents Chemother, 8(3), 903-908.
35. Phillipa, M. A. S., Jesudason, M. V., Thomson, C. J., & Amyes, S. G. B. (1998). Molecular Analysis of and Identification of Antibiotic Resistance Genes in Clinical Isolates of Salmonella Typhi from India. J Clin Microbiol, 36(6), 1595-1600.
36. Ploy, M. C., Gassama, A., Chainier, D., & Denis, F. (2005). Les intégrons en tant que support génétique de résistance aux antibiotiques. Immuno Anal Biol Spe, 20, 343-352.
37. REMIC (Référentiel en microbiologie médicale (bactériologie et mycologie)). (2007). Société Française de Microbiologie, 4ème édition, 370 pages. .
38. Ruiz, J., Castro, D., Goni, P., Santamaria, J. A., Borrego, J. J., & Vila, J. (2000). Analysis of the mechanism of quinolone resistance in nalidixic acid-resistant clinical isolates of Salmonella serotype Typhimurium. J Med Microbiol, 46, 623-628.
39. Turner, S. A., Luck, S. N., Sakellaris, H., Rajakumar, K., & Adler, B. (2003). Molecular epidemiology of the SRL pathogenicity island. Antimicrob Agents Chemother, 47, 727-734. (2003).
40. Walker, R. A., Lawson, A. J., Lindsay, E. A., Ward, L. R., Wright, P. A., Bolton, F. J., . . . Threlfall, E. J. (2000). Decreased susceptibility to ciprofloxacin in outbreak-associated multiresistant Salmonella Typhimurium DT104. Vet Rec, 147, 395-396.
41. Weill, F. X., Demartin, M., Tande, D., Espié, E., Rakotoarivony, .I, & Grimont PAD (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.
42. White, P. A., Mclver, C. J., & Rawlinson, W. D. (2001). Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother, 45, 2658- 2661.
43. WHO. (2013). Salmonella (non-typhoidal) Fact sheet N°139. http://www.who.int/mediacentre/factsheets/fs139/en/ accessed on 18/11/2015.
44. Wouafo, M., Nzouankeu, A., Kinfack, J. A., Fonkoua, M. C., Ejenguele, G., Njine, T., & Ngandjio, A. (2010). Prevalence and Antimicrobial Resistance of Salmonella Serotypes in Chickens from Retail Markets in Yaounde (Cameroon). Microb Drug Resis, 16(2), 171- 176.
45. Zhao, S., McDermott, P. F., Friedman, S., Abbott, J., Ayers, S., Glenn, A., . . . White, D. G. (2006). Antimicrobial resistance and genetic relatedness among Salmonella from retail foods of animal origin: NARMS retail meat surveillance. Foodborne Pathog Dis, 3(1), 106-117.