Rapid Multilateral and Integrated Public Health Response to a Cross-City Outbreak of Salmonella Enteritidis Infections Combining Analytical, Molecular, and Genomic Epidemiological Analysis

Min Jiang; Chao Yang; Patrick S L Kwan; Liping Zhang; Hang Fan; Yujuan Jin; Lifang Sun; Hongyu Chen; Baisheng Li; Qiuxia Chen; Yarong Wu; Yan Guo; Yuanguo Shi; Min Liao; Xiaolu Shi; Jianping Liu; Lijuan Jiang; Rui Cai; Yinhua Deng; Qun Sun; Ruifu Yang; Qiaoli Zhang; Yujun Cui; Qinghua Hu

doi:10.3389/fmicb.2022.772489

Rapid Multilateral and Integrated Public Health Response to a Cross-City Outbreak of Salmonella Enteritidis Infections Combining Analytical, Molecular, and Genomic Epidemiological Analysis

Front Microbiol. 2022 May 4:13:772489. doi: 10.3389/fmicb.2022.772489. eCollection 2022.

Authors

Min Jiang¹, Chao Yang¹, Patrick S L Kwan¹, Liping Zhang², Hang Fan³, Yujuan Jin⁴, Lifang Sun⁵, Hongyu Chen⁵, Baisheng Li⁶, Qiuxia Chen⁶, Yarong Wu³, Yan Guo³, Yuanguo Shi⁷, Min Liao⁷, Xiaolu Shi¹, Jianping Liu¹, Lijuan Jiang¹, Rui Cai¹, Yinhua Deng¹, Qun Sun⁸, Ruifu Yang³, Qiaoli Zhang², Yujun Cui³, Qinghua Hu¹

Affiliations

¹ Shenzhen Major Infectious Disease Control Key Laboratory, Shenzhen Center for Disease Control and Prevention, Shenzhen, China.
² Microbiology Laboratory, Dongguan Center for Disease Control and Prevention, Guangdong, China.
³ State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China.
⁴ Microbiology Laboratory, Longgang District Center for Disease Control and Prevention, Shenzhen, China.
⁵ Department of Laboratory Medicine, Shenzhen Children's Hospital, Shenzhen, China.
⁶ Microbiology Laboratory, Guangdong Center for Disease Control and Prevention, Guangdong, China.
⁷ Division of Biohazard Inspection and Testing, Shenzhen Institute of Quality & Safety Inspection and Research, Shenzhen, China.
⁸ Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

Abstract

On September 21, 2019, the Shenzhen and Dongguan Centers for Disease Control and Prevention received notification of a large cluster of suspected gastroenteritis involving primarily children who sought medical care at hospitals throughout two adjacent cities in China, Shenzhen, and Dongguan. A joint outbreak response was promptly initiated across jurisdictions in a concerted effort between clinical microbiologists, epidemiologists, and public health scientists. Concurrently, multiplex PCRs were used for rapid laboratory diagnosis of suspected cases; epidemiological investigations were conducted to identify the outbreak source, complemented by near real-time multicenter whole-genome analyses completed within 34 h. Epidemiological evidence indicated that all patients had consumed egg sandwiches served on September 20 as snacks to children and staff at a nursery in Dongguan, located near Shenzhen. Salmonella Enteritidis was isolated from case-patients, food handlers, kitchenware, and sandwiches with kitchen-made mayonnaise. Whole-genome single-nucleotide polymorphism (SNP)-based phylogenetic analysis demonstrated a well-supported cluster with pairwise distances of ≤1 SNP between genomes for outbreak-associated isolates, providing the definitive link between all samples. In comparison with historical isolates from the same geographical region, the minimum pairwise distance was >14 SNPs, suggesting a non-local outbreak source. Genomic source tracing revealed the possible transmission dynamics of a S. Enteritidis clone throughout a multi-provincial egg distribution network. The efficiency and scale with which multidisciplinary and integrated approaches were coordinated in this foodborne disease outbreak response was unprecedented in China, leading to the timely intervention of a large cross-jurisdiction Salmonella outbreak.

Keywords: Salmonella; genomic epidemiology; metagenomics; outbreak response; serotype Enteritidis; single-nucleotide polymorphism; whole-genome sequencing.