Molecular epidemiology and antimicrobial resistance of invasive non-typhoidal Salmonella in China, 2007-2016

Zeqiang Zhan; Xuebin Xu; Zhen Gu; Jianghong Meng; Xiayidan Wufuer; Mingliu Wang; Meilian Huang; Jianhui Chen; Chunmei Jing; Zhiying Xiong; Mei Zeng; Ming Liao; Jianmin Zhang

doi:10.2147/IDR.S210961

Molecular epidemiology and antimicrobial resistance of invasive non-typhoidal Salmonella in China, 2007-2016

Infect Drug Resist. 2019 Sep 12:12:2885-2897. doi: 10.2147/IDR.S210961. eCollection 2019.

Authors

Zeqiang Zhan¹, Xuebin Xu², Zhen Gu³, Jianghong Meng⁴, Xiayidan Wufuer⁵, Mingliu Wang⁶, Meilian Huang⁷, Jianhui Chen⁸, Chunmei Jing⁹, Zhiying Xiong¹, Mei Zeng¹⁰, Ming Liao¹, Jianmin Zhang¹

Affiliations

¹ National and Regional Joint Engineering Laboratory for Medicament of Zoonoses Prevention and Control, Key Laboratory of Zoonoses, Ministry of Agriculture, Key Laboratory of Zoonoses Prevention and Control of Guangdong Province, Animal Infectious Diseases Laboratory, College of Veterinary Medicine, South China Agricultural University, Guangzhou, 510642, China.
² Shanghai Municipal Center for Disease Control and Prevention, Shanghai 200336, China.
³ Emerging Infections Program China Office, Beijing, 102206, China.
⁴ Department of Food Science and Nutrition, University of Maryland, College Park, Maryland 20742, USA.
⁵ Xinjiang Uygur Autonomous Region Center for Disease Control and Prevention, Urumchi 830001, China.
⁶ Guangxi Zhuang Autonomous Region Disease Prevention and Control Center, Nanning 530028, China.
⁷ Xiamen City Children's Hospital, Xiamen 361006, China.
⁸ Fujian Provincial Center for Disease Control and Prevention, Fuzhou 350001, China.
⁹ Chongqing City Children's Hospital, Chongqing 400014, China.
¹⁰ Department of Infectious Diseases, Children's Hospital of Fudan University, Shanghai 200336, China.

Abstract

Purpose: Human infections caused by invasive non-typhoidal Salmonella (iNTS) are highly prevalent worldwide. However, data for such infections in China are scarce. This study reports the epidemiology of iNTS in China.

Methods: INTS isolates were recovered from blood and other clinical specimens collected during 2007-2016 across five provinces (Shanghai, Xinjiang, Fujian, Guangxi, and Chongqing) in China. Antimicrobial susceptibility was performed using the agar dilution method and molecular epidemiology was performed using standard microbiological techniques.

Results: A total of 178 iNTS isolates were recovered from approximately 9700 patient specimens during 2007-2016. The predominant serovars were Salmonella Enteritidis (57/178, 32%), Salmonella Choleraesuis (47/178, 26.4%), and Salmonella Typhimurium (24/178, 13.5%). Up to 50 isolates (28.1%) were from patients who were ≤1 year of age, while 28 (15.7%) were from patients who were ≥60 years. Among these isolates, high rates of resistance to nalidixic acid (114/178, 64%), sulfisoxazole (59%), ciprofloxacin (15.2%), and cefotaxime (8.4%) were found. Moreover, 53.4% (95/178) exhibited multidrug resistance, and 3.9% (7/178) showed co-resistance to third-generation cephalosporins and ciprofloxacin. Steadily increasing numbers of nalidixic acid, cefotaxime, and ciprofloxacin-resistant isolates, but decreasing numbers of multidrug resistance isolates were detected during the study period. Detection of quinolone genes in 114 nalidixic acid-resistant isolates showed that 58.3% (67/114) harbored plasmid-mediated quinolone resistance (PMQR) genes [aac(6´)-Ib-cr, qnrA, qnrB, oqxAB, qepA, qnrS, and qnrD] and 98.2% (112/114) exhibited mutations in quinolone resistance determining regions [gyrA, parC, and parE]. Furthermore, we detected beta-lactamases genes in the ceftriaxone-resistant isolates. The most common were bla_TEM-1 (93.3%), followed by bla_CTX-M-55 (40%), bla_CMY-2 (33.3%), and bla_OXA-1 (33.3%). Finally, a range of pulsed-field gel electrophoresis patterns were detected among the Salmonella Enteritidis and Salmonella Typhimurium isolates.

Conclusion: High rates of multidrug resistance and steadily increasing cefotaxime and ciprofloxacin-resistant iNTS could pose a significant challenge for the effective treatment of salmonellosis in China.

Keywords: China; beta-lactamases; fluoroquinolones; invasive non-typhoidal Salmonella; multidrug resistant; pulsed field gel electrophoresis.