Investigation of an Enteritis Outbreak Caused by Salmonella enterica Serovar Aberdeen in China
Salmonella enterica serovar Aberdeen is a pathogen that can cause severe gastroenteritis and is implicated in foodborne illnesses and international food-trade disputes. Despite its significance, the molecular biological characteristics of this organism have been rarely studied. This study aimed to assess the epidemiological and clinical characteristics of a foodborne outbreak caused by Salmonella Aberdeen in the Fushan district of Yantai, Shandong province, China, and to analyze the molecular biological characteristics of the outbreak isolates.
Epidemiological Investigation
From June 10 to 12, 2018, an enteritis outbreak affected 75 employees in the Fushan district of Yantai, including 33 males and 42 females. The mean age of the patients was 34.2 ± 5.3 years. An epidemiological investigation revealed that all infected employees had consumed lunch provided by a catering company on June 9, 2018. A total of 22 samples were collected, including four feces samples, five surplus food samples, eight cooking utensils used by the catering company, and five samples of chicken and eggs from the market where the food raw materials were purchased. Of these 22 samples, six (27.2%) tested positive for Salmonella Aberdeen (O11:Hi;1,2), including three isolates from feces (3/4, 75%) and three from surplus foods (3/5, 60%).
Molecular Biological Characteristics
Pulsed-field gel electrophoresis (PFGE) was used to analyze the genetic relatedness of the isolates. The PFGE results showed a high degree of similarity among the isolates, with digestion using the restriction enzyme nucleases XbaI (96.8%) and BlnI (100%) according to the PulseNet standardized PFGE protocol. The PFGE patterns were analyzed using BioNumerics, Version 6.0.
Nine virulence genes were detected in the Salmonella isolates, including Salmonella enterotoxin genes (stn), pilus gene Fimbrin (fimA), virulence island genes (invA, mgtC, siiE, sseL, sopB), virulence plasmid genes (spvC), and virK. The results showed that six virulence genes, namely stn, fimA, virK, invA, mgtC, and siiE, were detected in all six isolates, while sseL, sopB, and spvC were not detected.
Antimicrobial Susceptibility and Resistance Genes
Fifteen different antibiotic drugs were tested for antimicrobial susceptibility using the broth microdilution method of the Clinical and Laboratory Standards Institute. The results showed that all six isolates were sensitive to all tested drugs except cefazolin (CFZ). Thirteen drug-resistant genes of Salmonella were detected using polymerase chain reaction in capillary gel electrophoresis. The results showed that the CTX-M group II (351 bp) and CTX-M group IV (474 bp) genes were present in all isolates.
Clinical Symptoms and Incubation Period
The epidemiological investigation revealed that the shortest, longest, and average incubation periods were 1, 88, and 14 hours, respectively. The clinical symptoms of the 75 workers mainly included diarrhea (89.3%, 67/75), abdominal pain (89.3%, 67/75), increased C-reactive protein (CRP) level (77.3%, 58/75), nausea (65.3%, 49/75), fever (52.0%, 39/75), and vomiting (45.3%, 34/75).
Discussion
Salmonella Aberdeen is rarely reported and does not typically cause foodborne outbreaks abroad. In China, the first food poisoning caused by Aberdeen was reported in 1964. During 1976 to 1980, the detection rate of Aberdeen was 0.39% (105/27183) in Salmonella enterica. From 2006 to 2007, Aberdeen accounted for 3% of 807 Salmonella strains isolated from 24,895 fecal samples as China joined the WHO Global Salm-Surv.
The same serotypes were isolated from the retained food and patient stool samples of the outbreak, and the PFGE results showed that the isolated strain had a high similarity (≥96.8%), indicating that this foodborne outbreak was caused by Salmonella Aberdeen. The epidemiological evidence suggested that the outbreak occurred due to poor food processing hygiene and the lack of separation between raw and cooked foods during processing, leading to cross-contamination.
The incubation period of Aberdeen infection is similar to that of other Salmonella enterica, including Salmonella typhimurium/enteritidis. The clinical symptoms mainly include diarrhea, fever, abdominal pain, nausea, vomiting, and increased CRP levels. The isolates contained stn, fimA, virK, invA (Salmonella pathogenicity island [SPI]-1), mgtC (SPI-3), and siiE (SPI-4). Stn is an enterotoxin gene and an important virulence factor encoding products that can induce intestinal juice secretion. FimA, as a fimbriae gene, helps bacteria adhere to animal cells and promotes colonization. VirK is a regulatory gene that facilitates the diffusion of bacterial toxins in the host. InvA plays an important role in the invasion of Salmonella into intestinal M cells. MgtC is a virulence factor located in SPI-3 and allows bacteria to survive in macrophages and low-magnesium environments. SiiE is located in SPI-4 and aids bacterial adhesion to the epithelium.
All patients with severe symptoms showed remarkable improvement following cefotaxime (CTX) and levofloxacin injections after 3 to 7 days. The antimicrobial resistance and resistance genes of the isolates were investigated to analyze the relationship between their phenotypes and genotypes. The results showed that all six isolates were resistant to CFZ, but resistance genes showed they all contained CTX-M group II and CTX-M group IV. These results are consistent with the widespread distribution and prevalence of the CTX-M gene sub-type in Salmonella in China. CTX-M type extended-spectrum β-lactamases (ESBLs) are a new type of ESBL with an increasing number of family members. Their main phenotype shows elevated resistance to cephalosporin antibiotics. The resistance of Salmonella Aberdeen to first-generation CFZ should be a concern for healthcare professionals.
Conclusion
This study provides a comprehensive analysis of an enteritis outbreak caused by Salmonella enterica serovar Aberdeen in China. The epidemiological investigation, molecular biological characteristics, antimicrobial susceptibility, and clinical symptoms were thoroughly examined. The findings highlight the importance of proper food handling and processing hygiene to prevent such outbreaks and the need for continued surveillance of antimicrobial resistance in Salmonella strains.
doi.org/10.1097/CM9.0000000000000938
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