Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century

doi:10.1016/j.psj.2020.12.007

. 2021 Mar;100(3):100894.

doi: 10.1016/j.psj.2020.12.007. Epub 2020 Dec 10.

Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century

Fan Sun¹, Xiu Li¹, Yan Wang¹, Fan Wang¹, Haojie Ge¹, Zhiming Pan¹, Yaohui Xu², Yanhong Wang¹, Xin'an Jiao¹, Xiang Chen³

Affiliations

¹ Jiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, China; Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, China.
² College of Veterinary Medicine, Henan University of Animal Husbandry and Economy, Henan, China.
³ Jiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, China; Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, China. Electronic address: chenxiang@yzu.edu.cn.

PMID: 33652525
PMCID: PMC7936142
DOI: 10.1016/j.psj.2020.12.007

Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century

Fan Sun et al. Poult Sci. 2021 Mar.

. 2021 Mar;100(3):100894.

doi: 10.1016/j.psj.2020.12.007. Epub 2020 Dec 10.

Authors

Fan Sun¹, Xiu Li¹, Yan Wang¹, Fan Wang¹, Haojie Ge¹, Zhiming Pan¹, Yaohui Xu², Yanhong Wang¹, Xin'an Jiao¹, Xiang Chen³

Affiliations

¹ Jiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, China; Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, China.
² College of Veterinary Medicine, Henan University of Animal Husbandry and Economy, Henan, China.
³ Jiangsu Key Laboratory of Zoonosis/Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, China; Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, Ministry of Agriculture and Rural Affairs, Yangzhou University, Yangzhou, China. Electronic address: chenxiang@yzu.edu.cn.

PMID: 33652525
PMCID: PMC7936142
DOI: 10.1016/j.psj.2020.12.007

Abstract

Pullorum is a chicken-specific systemic disease caused by Salmonella enterica serovar Gallinarum biovar Pullorum (S. Pullorum). This study was carried out to provide basic data for understanding the trends of S. Pullorum. A total of 652 S. Pullorum isolates collected in China during 1962-2019 were examined. Overall, 525 (80.5%) isolates were resistant to at least one antibiotic; 280 (42.9%) isolates resisted 3 or more classes of antibiotics and showed an increasing trend until 2015 and then decreased significantly. The most common multidrug-resistant pattern was ampicillin-tetracycline-nalidixic acid (13.6%). After 2008, 6 classes of antibiotic-resistant strains began to appear, and they have been prevalent ever since. In 2014, a strain resistant to 7 antibiotics (ampicillin-cefazolin-streptomycin-tetracycline-sulphonamides-nalidixic acid-nitrofurantoin) was isolated. The highest antimicrobial resistance was observed for nalidixic acid (71.9%), and the lowest was found for cefotaxime, meropenem, amikacin, gentamicin, fosfomycin, and polymyxin (0%). Our findings monitored the prevalence of the resistance of S. Pullorum during the past half-century in China. Continued surveillance of antimicrobial resistance and the rational use of antimicrobials is necessary and important to control the rapid increase in antimicrobial resistance in S. Pullorum.

Keywords: Salmonella enterica serovar Gallinarum biovar Pullorum; antimicrobial susceptibility; chicken; resistance trend.

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Figures

**Figure 1**
Antimicrobial resistance rate among S. Pullorum isolates collected from chickens in China during 1962–2019. Abbreviations: AMP, ampicillin; AMK, amikacin; ATM, aztreonam; CFZ, cefazolin; CHL, chloramphenicol; CIP, ciprofloxacin; CL, polymyxin; CTX, cefotaxime; FFC, florfenicol; FOS, fosfomycin; GEN, gentamicin; MEM, meropenem; NAL, nalidixic acid; NIT, nitrofurantoin; OLA, olaquindox; STR, streptomycin; SXT, sulphonamides; TET, tetracycline.

**Figure 2**
Multidrug resistance of S. Pullorum isolates collected from chickens in China between 1962 and 2019. Numbers “0” to “7” and the corresponding shadings indicate that isolates are resistant to 1, 2, 3, 4, 5, 6, and 7 antimicrobial agents, respectively.

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[1] Barrow P.A., Jones M.A., Smith A.L., Wigley P. The long view: Salmonella–the last forty years. Avian Pathol. 2012;41:413–420. - PubMed

[2] Barrow P.A., Jones M.A., Smith A.L., Wigley P. The long view: Salmonella–the last forty years. Avian Pathol. 2012;41:413–420. - PubMed

[3] Cheong H.J., Lee Y.J., Hwang I.S., Kee S.Y., Cheong H.W., Song J.Y., Kim J.M., Park Y.H., Jung J.H., Kim W.J. Characteristics of non–typhoidal Salmonella isolates from human and broiler–chickens in Southwestern Seoul, Korea. J. Korean Med. Sci. 2007;22:773–778. - PMC - PubMed

[4] Cheong H.J., Lee Y.J., Hwang I.S., Kee S.Y., Cheong H.W., Song J.Y., Kim J.M., Park Y.H., Jung J.H., Kim W.J. Characteristics of non–typhoidal Salmonella isolates from human and broiler–chickens in Southwestern Seoul, Korea. J. Korean Med. Sci. 2007;22:773–778. - PMC - PubMed

[5] Clinical and Laboratory Standards Institute . CLSI; Wayne. PA: 2013. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Second Informational Supplement VET01–S2.

[6] Clinical and Laboratory Standards Institute . CLSI; Wayne. PA: 2013. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Second Informational Supplement VET01–S2.

[7] Clinical and Laboratory Standards Institute . CLSI; Wayne. PA: 2015. Performance Standards for Antimicrobial Susceptibility Testing: Twenty–Fifth Informational Supplement M100–S25.

[8] Clinical and Laboratory Standards Institute . CLSI; Wayne. PA: 2015. Performance Standards for Antimicrobial Susceptibility Testing: Twenty–Fifth Informational Supplement M100–S25.

[9] Dey S., Mahanti A., Batabyal K., Joardar S.N., Samanta I., Isore D.P., Pakhira M.C. Identification and antimicrobial susceptibility of Salmonella Gallinarum isolated from fowl typhoid outbreak in backyard Vanaraja fowl. Explor. Anim. Med. Res. 2016;6:63–67.

[10] Dey S., Mahanti A., Batabyal K., Joardar S.N., Samanta I., Isore D.P., Pakhira M.C. Identification and antimicrobial susceptibility of Salmonella Gallinarum isolated from fowl typhoid outbreak in backyard Vanaraja fowl. Explor. Anim. Med. Res. 2016;6:63–67.

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Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century

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Epidemic patterns of antimicrobial resistance of Salmonella enterica serovar Gallinarum biovar Pullorum isolates in China during the past half-century

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