Virulence-Related Gene Distribution Among Shigella Isolates in Anhui, China: The Association with Antimicrobial Resistance

Yanyan Liu; Weihua Shen; Yating Sun; Na Lv; Kaili Sun; Lifen Hu; Ying Ye; Yufeng Gao; Jiabin Li

doi:10.2147/IDR.S274862

Virulence-Related Gene Distribution Among Shigella Isolates in Anhui, China: The Association with Antimicrobial Resistance

Infect Drug Resist. 2020 Oct 19:13:3637-3647. doi: 10.2147/IDR.S274862. eCollection 2020.

Authors

Yanyan Liu^#^{1

2

3}, Weihua Shen^#⁴, Yating Sun^#¹, Na Lv¹, Kaili Sun⁵, Lifen Hu¹, Ying Ye^{1

2

3}, Yufeng Gao^{1

2

3}, Jiabin Li^{1

2

3

5}

Affiliations

¹ Department of Infectious Diseases, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, People's Republic of China.
² Anhui Center for Surveillance of Bacterial Resistance, Hefei, Anhui, People's Republic of China.
³ Institute of Bacterial Resistance, Anhui Medical University, Hefei, Anhui, People's Republic of China.
⁴ Department of Special Clinic, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, People's Republic of China.
⁵ Department of Infectious Diseases, The Chaohu Affiliated Hospital of Anhui Medical University, Hefei, Anhui, People's Republic of China.

^# Contributed equally.

Abstract

Objective: The aim of this study was to investigate the antimicrobial resistance profiles and distribution of virulence-related genes (VRGs) among Shigella isolates in Anhui, China, and to identify the correlation between the VRGs and antimicrobial resistance.

Materials and methods: A total of 525 non-duplicate Shigella isolates (449 S. flexneri, 68 S. sonnei, 3 S. boydii, and 5 S. dysenteriae) were collected in Anhui Province, China between September 2011 and September 2015. The antimicrobial resistance of the strains was determined by the agar dilution method according to CLSI guidelines. The presence of 16 VRGs, including ipaH, ipaA-D, ial, virB, virF, set, sen, icsA, icsB, sigA, sat, pic, and sepA, was evaluated using PCR amplification and sequencing.

Results: Shigella flexneri was the most abundant (85.5%), followed by S. sonnei (13.0%). The proportion of males with S. flexneri was higher than that of females (57% vs 43%; P<0.0001). The most common resistance pattern was the combination of ampicillin, nalidixic acid, and tetracycline for S. flexneri (90.2%) and S. sonnei (94.1%). Resistance to ciprofloxacin and levofloxacin was more common among S. flexneri than among S. sonnei (49.7% vs.19.1%, P<0.0001; 30.5% vs 10.3%, P=0.001, respectively). All the isolates were positive for the ipaH gene, while the set, sat, pic, and sepA genes were not detected among the S. sonnei isolates. Except for sigA and sen, resistance to chloramphenicol and ciprofloxacin was more common among VRG-positive S. flexneri than among VRG-negative S. flexneri (P<0.05). Furthermore, resistance to ceftriaxone and ceftazidime was more frequently detected among sat- and set-positive S. flexneri than among sat- and set-negative S. flexneri (P<0.05). However, gentamicin resistance was more prevalent among VRG-negative (ial, virF, set, sat, pic, and sepA) S. flexneri than among VRG-positive S. flexneri (P<0.05).

Conclusion: Shigella flexneri remains the predominant species in Anhui, China, and the resistance to fluoroquinolones was more widespread among S. flexneri than among S. sonnei. Shigella flexneri strains harboring specific VRGs were associated with antimicrobial resistance. To the best of our knowledge, this is the first report of the correlation between the VRGs and antimicrobial resistance in Anhui, China.

Keywords: Shigella flexneri; Shigella sonnei; antimicrobial resistance; type III secretion system; virulence-related gene.