Characterization and Source Investigation of Multidrug-Resistant Salmonella Anatum from a Sustained Outbreak, Taiwan

N ontyphoidal Salmonella (NTS) is a major cause for foodborne diseases worldwide.In Taiwan, the ambient climate and flourishing pig-raising industry makes NTS infections rampant.As in other countries, salmonellosis was primarily caused by Salmonella enterica serovars Enteritidis and Typhimurium in Taiwan (1), but rare serovars such as Salmonella Goldcoast have appeared in recent years (2).Recommended antimicrobial treatment options for salmonellosis include fluoroquinolones and extended-spectrum cephalosporins (1).However, resistance to these antibiotics has been emerging in many countries, leading to increased disease prevalence, disease severity, and death and the requirement of last-line antimicrobial drugs (e.g., carbapenems) (3-5).Since 2015, northern Taiwan has seen an increase in Salmonella infections, caused by previously rare Salmonella Anatum.The infections were also reported in central Taiwan, indicating that this outbreak had already prevailed throughout the entire island (6).Co-resistance to ceftriaxone and ciprofloxacin are the main feature of the outbreak clone.Evidence from epidemiologic, laboratory, and supply-chain investigations identified raw pork and poultry as the vehicle for spread of this strain.More important, genomic comparisons against the global public database indicated that this clone has appeared in Europe, Asia, and America.Given the increasing globalization of foodstuffs, these findings prompt an urgent global sharing of whole-genome sequencing (WGS) data to facilitate disease surveillance and early recognition of international foodborne outbreaks (7,8). The StudyChang Gung Memorial Hospital is a main referral hospital for cities in northern Taiwan, including Taipei, New Taipei, and Taoyuan.The population in this region is ≈7 million.In 2012, the hospital's clinical microbiology laboratory launched a program to monitor the NTS serovars causing human infections.All Salmonella isolates from patients were collected and serotyped.Before 2015, very few Salmonella Anatum isolates were recovered, and most were susceptible to antimicrobial agents.Since then, an increase has been observed, peaking in 2017 (Figure 1, panel A).As of June 2019, a total of 319 nonrepetitive isolates have been identified; of these, 197 (61.8%) isolates were ceftriaxone-resistant (MIC >2 µg/mL), 301 (94.4%) were ciprofloxacin-resistant (MIC >0.12 µg/mL), and 197 (61.8%) were resistant to both.In addition, 292 (91.5%) isolates were resistant to chloramphenic, and 295 (92.5%) were resistant to trimethoprim/