Characteristic of multiple-antibiotic-resistant \(\textit{ Salmonella enteritica }\) from Muscovy duck in Hanoi

Trung Nguyen; Hoa Le; Yen Ta; Da Pham; Nam Nguyen; Hoang Nguyen

doi:10.15625/2615-9023/17499

Author affiliations

Authors

Trung Thanh Nguyen National Institute for Food Control, Cau Giay, Hanoi, Vietnam
Hoa Vinh Le National Institute for Food Control, Cau Giay, Hanoi, Vietnam
Yen Thi Ta National Institute for Food Control, Cau Giay, Hanoi, Vietnam
Da Pham Xuan Faculty of Medicine - Vietnam National University, Ho Chi Minh City, Vietnam
Nam Trung Nguyen Institute of Biotechnology, Vietnam Academy of Science and Technology, Cau Giay, Hanoi, Vietnam
Nguyen Huy Hoang Institute of Genome Research, Vietnam Academy of Science and Technology, Cau Giay, Hanoi, Vietnam

DOI:

https://doi.org/10.15625/2615-9023/17499

Keywords:

Whole-genome sequencing, Salmonella, antimicrobial resistance, virulence factor, serovar, Muscovy duck.

Abstract

Nowadays, as the global population grows, the demand for food is also becoming higher each day. Together with the rise in food demand, Muscovy duck has been gradually bred industrially as a poultry food supply along with the chicken. The change from traditional to industrial breeding poses a potential risk of pathogenic bacteria infection and antimicrobial resistance bacteria. Especially Salmonella, one of the leading pathogens worldwide, is also notable for its antimicrobial resistance. In this study, by using Muscovy duck carcasses collected from wet markets in 05 districts in Ha Noi, we assessed the rate of Salmonella infection at first, then conducted an antibiotic susceptibility test utilizing 15 types of antibiotics, from then whole genome sequencing was applied for 8 multidrug resistant isolates. Next, the genomic data after successfully sequenced was used for analyzing antibiotic resistance genes, genotypes, multi-locus sequence-based typing (MLST), virulence factors, and plasmids. 65% of Muscovy duck samples were positive for Salmonella, in which 95% (19/20 strains) of Salmonella isolated was multidrug resistant. The result of the antibiotics susceptibility test indicated that phenotypic resistance to ampicillin was the most observed (92.3%, 19/20), followed by tetracycline (90%, 18/20), cefuroxime (85%, 17/20), cefazolin (85%, 17/20), ceftriaxone (85%, 17/20), Cefotaxime (85%, 17/20), trimethoprim (70%, 14/20), gentamicin (60%, 12/20), chloramphenicol (55%, 11/20), nalidixic acid (55%, 11/20), ceftazidime (50%, 10/20), ciprofloxacin (2/20). However, all isolates were susceptible to cefoxitin and meropenem. Sixty-five antibiotic resistance genes were identified, including genes that are resistant to aminoglycoside, 3^rd generation antibiotics (cefotaxime, cefoperazone, ceftizoxime, ceftazidime, ceftriaxone, etc.). Col, IncA plasmids and some mobile genetic elements were identified. Simultaneously Salmonella pathogenic islands were found in all sequenced strains, exclusively SPI 1, SPI 3, and SPI 9 were carried in every isolate.

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References

Anhalt J. P. & Fenselau C., 1975. Identification of Bacteria using Mass Spectrometry. Analytical Chemistry, 47(2): 219–225. https://doi.org/10.1021/ AC60352A007/ASSET/AC60352A007.FP.PNG_V03

Carattoli A., Zankari E., Garciá-Fernández A., Larsen M. V., Lund O., Villa L., Aarestrup F. M. & Hasman H., 2014. In Silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrobial Agents and Chemotherapy, 58(7): 3895–3903. https://doi.org/10.1128/ AAC.02412-14

CDC, 2022. FoodNet Fast. https://wwwn.cdc.gov/foodnetfast/

Centers for Disease Control and Prevention (CDC), 2014. Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food-Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2006–2013. Morbidity and Mortality Weekly Report (MMWR). https://www.cdc.gov/mmwr/preview/mmwrhtml/mm6315a3.htm

Chen L., Yang J., Yu J., Yao Z., Sun L., Shen Y. & Jin Q., 2005. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Research: 33(Database issue). https://doi.org/10.1093/ NAR/GKI008

EFSA & ECDC, 2018. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal, 16(12): e05500. https://doi.org/10.2903/ J.EFSA.2018.5500

EFSA & ECDC, 2021. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2018/2019. EFSA Journal, 19(4). https://doi.org/10.2903/J.EFSA.2021.6490

Emanuella E. da S., Elisângela de S. L., Régis S. de C. T., Átilla H. de A., Roberta C. da R. e S., Valdez J. R. G. F., Ruben H. V. & William C. M., 2014. Survey of Enterobacteriaceae in domestic ducks (Cairina moschata) from properties located in four cities of the state of Ceará, Brazil. Arquivos Do Instituto Biológico.

FAO & WHO, 2002. Risk assessments of Salmonella in eggs and broiler chickens.

FAO & WHO, 2009. M I C R O B I O Salmonella and Campylobacter in chicken meat. www.who.int/foodsafety

Gilbert M., Nicolas G., Cinardi G., van Boeckel T. P., Vanwambeke S. O., Wint G. R. W. & Robinson T. P., 2018. Global distribution data for cattle, buffaloes, horses, sheep, goats, pigs, chickens and ducks in 2010. Scientific Data, 5(1): 1–11. https://doi.org/10.1038/sdata.2018.227

Gonzalez-Santamarina B., Busch A., Garcia-Soto S., Abdel-Glil M. Y., Linde J., Fries R., Meemken D., Hotzel H. & Tomaso H., 2020. Draft genome sequence of multi-resistant Salmonella enterica subsp. enterica serovar Rissen strain 19CS0416 isolated from Vietnam reveals mcr-1 plasmid mediated resistance to colistin already in 2013. Journal of Genomics, 8(2020): 76–79. https://doi.org/10.7150/ jgen.42790

Gupta S. K., Padmanabhan B. R., Diene S. M., Lopez-Rojas R., Kempf M., Landraud L. & Rolain J. M., 2014. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrobial Agents and Chemotherapy, 58(1): 212–220. https://doi.org/10.1128/AAC.01310-13

Hasman H., Agersø Y., Hendriksen R., Cavaco L. M., Guerra-Roman B., Bortolaia V. & Pedersen S. K., 2014. Laboratory Protocol: Isolation of ESBL, AmpC and carbapenemase producing E. coli from caecal samples. Final protocol, November: 1–11.

Iwamoto M., Reynolds J., Karp B. E., Tate H., Fedorka-Cray P. J., Plumblee J. R., Hoekstra R. M., Whichard J. M. & Mahon B. E., 2017. Ceftriaxone-Resistant Nontyphoidal Salmonella from Humans, Retail Meats, and Food Animals in the United States, 1996–2013. Foodborne Pathogens and Disease, 14(2): 74–83. https://doi.org/10.1089/FPD.2016.2180

Khan A. S., Georges K., Rahaman S., Abdela W. & Adesiyun A. A., 2018. Prevalence and serotypes of Salmonella spp. on chickens sold at retail outlets in Trinidad. PLoS One, 13(8). https://doi.org/10.1371/ journal.pone.0202108

Lamas A., Miranda J. M., Regal P., Vázquez B., Franco C. M. & Cepeda A., 2018. A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiological Research, 206: 60–73. https://doi.org/10.1016/J.MICRES.2017.09.010

Leekitcharoenphon P., Nielsen E. M., Kaas R. S., Lund O. & Aarestrup F. M., 2014. Evaluation of whole genome sequencing for outbreak detection of Salmonella enterica. PloS One, 9(2). https://doi.org/ 10.1371/JOURNAL.PONE.0087991

Little C. L., Richardson J. F., Owen R. J., de Pinna E. & Threlfall E. J., 2008. Prevalence, characterisation and antimicrobial resistance of Campylobacter and Salmonella in raw poultrymeat in the UK, 2003–2005. International Journal of Environmental Health Research, 18(6): 403–414. https://doi.org/10.1080/ 09603120802100220

Ljubojević Pelić D., Vidaković Knežević S., Pelić M., Živkov Baloš M. & Milanov D., 2021. The epidemiological significance of duck meat as a source of Salmonella spp. a review. World’s Poultry Science Journal, 77(1): 105–114. https://doi.org/ 10.1080/00439339.2020.1866960

McArthur A. G., Waglechner N., Nizam F., Yan A., Azad M. A., Baylay A. J., Bhullar K., Canova M. J., de Pascale G., Ejim L., Kalan L., King A. M., Koteva K., Morar M., Mulvey M. R., O’Brien J. S., Pawlowski A. C., Piddock L. J. V., Spanogiannopoulos P., … Wright G. D., 2013. The comprehensive antibiotic resistance database. Antimicrobial Agents and Chemotherapy, 57(7): 3348. https://doi.org/10.1128/AAC.00419-13

Monte D. F. M., Nethery M. A., Barrangou R., Landgraf M. & Fedorka-Cray P. J., 2021. Whole-genome sequencing analysis and CRISPR genotyping of rare antibiotic-resistant Salmonella enterica serovars isolated from food and related sources. Food Microbiology: 93. https://doi.org/10.1016/j.fm.2020.103601

Nghiem M. N., Nguyen V. T., Jeung E. B. & Vo T. T. B., 2019. Alternate antimicrobial resistance genes in multidrug resistant Salmonella spp. isolated from retail meats in Vietnam using RNA-sequencing analysis. Journal of Food Safety, 39(6). https://doi.org/10.1111/jfs.12707

Nguyen T. K., Nguyen L. T., Chau T. T. H., Nguyen T. T., Tran B. N., Taniguchi T., Hayashidani H. & Ly K. T. L., 2021. Prevalence and antibiotic resistance of Salmonella isolated from poultry and its environment in the Mekong Delta, Vietnam. Veterinary World, 14(12): 3216. https://doi.org/10.14202/VETWORLD.2021.3216-3223

Nguyen T. V., Nghiem N. M. & Vo T. B. T., 2018. Determination of antibiotic resistance of Salmonella isolated from pork, beef, and chicken meat at the retail markets in Hanoi. Vietnam Journal of Biotechnology, 16(3): 553–564.

Nguyen V. K., Pham T. N., Dinh X. T., Ma Lucila L., Unger F., Nguyen V. H., Pham D. P., Pham T. N. & Gilbert J. G., 2012. Hygienic practices and microbial contamination of small - scale poultry slaughter houses at peri - urban areas of Hanoi, Vietnam. Agriculture and Rural Development, 12(2): 60–67.

Noble D. J., Lane C., Little C. L., Davies R., de Pinna E., Larkin L. & Morgan D., 2012. Revival of an old problem: an increase in Salmonella enterica serovar Typhimurium definitive phage type 8 infections in 2010 in England and Northern Ireland linked to duck eggs. Epidemiology and Infection, 140(1):

–149. https://doi.org/10.1017/ S0950268811000586

Rampersad J., Johnson J., Brown G., Samlal M. & Ammons D., 2008. Comparison of polymerase chain reaction and bacterial culture for Salmonella detection in the Muscovy duck in Trinidad and Tobago. Revista Panamericana de Salud Pública, 23(4): 264–267.

Seemann T., 2016. ABRicate: mass screening of contigs for antiobiotic resistance genes. https://github.com/tseemann/abricate

Trongjit S., Angkititrakul S., Tuttle R. E., Poungseree J., Padungtod P. & Chuanchuen R., 2017. Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand–Cambodia border provinces. Microbiology and Immunology, 61(1): 23–33. https://doi.org/10.1111/1348-0421.12462

USDA, 2019. Isolation and identification of Salmonella from meat, poultry, pasteurized egg, and siluriformes (fish) products and carcass and environmental sponges. Laboratory Guidebook.

WHO., 2015. Who estimates of the global burden of foodborne diseases. www.who.int

Yoshida C. E., Kruczkiewicz P., Laing C. R., Lingohr E. J., Gannon V. P. J., Nash J. H. E. & Taboada E. N., 2016. The Salmonella In Silico typing resource (SISTR): An open web-accessible tool for rapidly typing and subtyping draft Salmonella genome assemblies. PLoS One, 11(1). https://doi.org/10.1371/ journal.pone.0147101

Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., Aarestrup F. M. & Larsen M. V., 2012. Identification of acquired antimicrobial resistance genes. The Journal of Antimicrobial Chemotherapy, 67(11): 2640–2644. https://doi.org/10.1093/ JAC/DKS261

Zhang L., Fu Y., Xiong Z., Ma Y., Wei Y., Qu X., Zhang H., Zhang J. & Liao M., 2018. Highly prevalent multidrug-resistant Salmonella from chicken and pork meat at retail markets in Guangdong, China. Frontiers in Microbiology, pp. 9. https://doi.org/10.3389/FMICB.2018.02104