Prevalence, Antibiotic Susceptibility, and Molecular Characterization of Cronobacter spp. Isolated From Edible Mushrooms in China

Abstract

Cronobacter spp. are foodborne pathogens that can infect and cause life-threatening diseases in all age groups, particularly in infants and immunocompromised elderly. This study aimed to investigate the prevalence, antibiotic susceptibility, and molecular characteristics of Cronobacter spp. isolates in edible mushrooms collected from 44 cities in China. In total, 668 edible mushrooms were collected from traditional retail markets and supermarkets and were analyzed by quantitative methods, PCR-based serotyping, multilocus sequence typing (MLST), and antibiotic susceptibility testing. Among the 668 samples tested, 89 (13.32%) were positive for Cronobacter spp., and the contamination levels exceeded the 110 most probable number (MPN)/g in 13.48% (12/89) of the samples. Flammulina velutipes samples had the highest contamination rate of 17.54% (37/211), whereas Hypsizygus marmoreus samples had the lowest contamination rate of 3.28% (2/61). Ten serotypes were identified among 115 isolates, of which the C. sakazakii serogroup O1 ( n = 32) was the primary serotype. MLST indicated that there was quite high genetic diversity in Cronobacter spp. and 72 sequence types were identified, 17 of which were new. Notably, C. sakazakii ST148 ( n = 10) was the most prevalent, followed by C. malonaticus ST7 ( n = 5). Antibiotic susceptibility testing revealed that the majority of Cronobacter spp. strains were susceptible to the 16 antibiotics tested. However, a portion of isolates exhibited relatively high resistance to cephalothin, with resistance and intermediate rates of 93.91 and 6.09%, respectively. One isolate (cro300A) was multidrug-resistant, with resistance to five antibiotics. Overall, this large-scale study revealed the relatively high prevalence and high genetic diversity of Cronobacter spp. on edible mushrooms in China, indicating a potential public health concern. To our knowledge, this is the first large-scale and systematic study on the prevalence of Cronobacter spp. on edible mushrooms in China, and the findings can provide valuable information that can guide the establishment of effective measures for the control and precaution of Cronobacter spp on edible mushrooms during production processes.

Cronobacter sakazakii, Cronobacter malonaticus, and Cronobacter dublinensis Genotyping Based on CRISPR Locus Diversity

“…The Cronobacter genus including seven species are opportunistic foodborne human pathogens that can cause rare but serious diseases in neonates and immune-compromised infants (Iversen et al, 2008; Kucerova et al, 2011; Joseph et al, 2012a). In our previous studies, C. sakazakii , C. malonaticus , and C. dublinensis were three prevalent species in food, however, we have never isolated C. universalis and C. condimenti strains (Xu et al, 2015; Ling et al, 2018; Li et al, 2019). In total, five C. turicensis and one C. muytjensii strains were isolated from vegetables and ready-to-eat foods (Xu et al, 2015; Ling et al, 2018) and we have successfully performed CRISPR arrays on these isolates using the same primers used for C. sakazakii .…”

“…All strains belonged to the large-scale and systematic investigation on the prevalence of Cronobacter spp. in food in China, and detailed information about these strains, including O serotypes, STs, and antibiotic-resistance profiles, are provided in Supplementary Data Sheets 1–3 (Zeng et al, 2017, 2018b; Ling et al, 2018; Li et al, 2019).…”

“…Latest study reported an acute gastroenteritis outbreak caused by C. sakazakii in a senior high school of China (Yong et al, 2018). Moreover, this genus has been isolated from the environment, food, and clinical sources (Ueda, 2017; Yong et al, 2018; Zeng et al, 2018a; Li et al, 2019). Further, C. sakazakii , C. malonaticus , and C. dublinensis are three prevalent species and some reports have indicated that the principal sources of these organisms might be soil, water, and vegetables (Ueda, 2017; Zeng et al, 2018b).…”

Prevalence and Genetic Diversity of Cronobacter Species Isolated From Four Infant Formula Production Factories in China

“…Cronobacter spp. are opportunistic foodborne pathogens that can cause severe infections in neonates and infants through the ingestion of contaminated PIF; therefore, they are of global interest to human health (Forsythe et al, 2014; Fei et al, 2018a; Li et al, 2019). Results of this study suggest that should Cronobacter be detected in clean area or quasi-clean areas, measures must be immediately implemented to prevent contamination of the end products’ subsequent greater contamination of the processing environment (Pei et al, 2019).…”

Application of Nucleic Acid Reference Material for Rapid Detection of Cronobacter sakazakii (Cronobacter spp.) in Flammulina velutipes

“…A recent study showed that the detection rate of Cronobacter spp. is 17.54% (37 positive in 211 samples) in Flammulina velutipes from 44 cities in China [10], indicating that the detection of F. velutipes contamination should be strengthened to avoid food safety issues.…”