Meat and meat products as potential sources of emerging MDR Bacillus cereus: groEL gene sequencing, toxigenic and antimicrobial resistance

Abdelazeem M Algammal; Hamza M Eid; Saad Alghamdi; Hanaa Ghabban; Roba Alatawy; Enas A Almanzalawi; Tahani M Alqahtani; Sabreen G Elfouly; Gihan M Mohammed; Helal F Hetta; Reham M El-Tarabili

doi:10.1186/s12866-024-03204-9

Meat and meat products as potential sources of emerging MDR Bacillus cereus: groEL gene sequencing, toxigenic and antimicrobial resistance

BMC Microbiol. 2024 Feb 7;24(1):50. doi: 10.1186/s12866-024-03204-9.

Authors

Affiliations

¹ Department of Bacteriology, Immunology and Mycology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, 41522, Egypt. abdelazeem.algammal@vet.suez.edu.eg.
² Department of Microbiology, Faculty of Veterinary Medicine, Ain Shams University, Cairo, 11566, Egypt.
³ Department of Clinical Laboratory Sciences, Faculty of Applied Medical Sciences, Umm Al-Qura University, Makkah, 24381, Saudi Arabia.
⁴ Department of Biology, Faculty of Science, University of Tabuk, Tabuk, 71491, Saudi Arabia.
⁵ Medical Microbiology Department, School of Medicine, University of Tabuk, Tabuk, 71491, Saudi Arabia.
⁶ Department of Biological Sciences, Faculty of Sciences, King Abdulaziz University, Jeddah, 21589, Saudi Arabia.
⁷ Department of Bacteriology, Animal Health Research Institute, Port-Said branch, Port Said, 42511, Egypt.
⁸ Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University, Assiut, 71515, Egypt.
⁹ Department of Bacteriology, Immunology and Mycology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, 41522, Egypt.

Abstract

Background: Bacillus cereus is implicated in severe foodborne infection in humans. This study intended to assess the occurrence, groEL gene sequencing, biofilm production, and resistance profiles of emerged multidrug resistant (MDR) B. cereus in meat and meat product samples. Moreover, this work highlights the virulence and toxigenic genes (hblABCD complex, nheABC complex, cytK, ces, and pc-plc) and antimicrobial resistance genes (bla1, tetA, bla2, tetB, and ermA).

Methods: Consequently, 200 samples (sausage, minced meat, luncheon, beef meat, and liver; n = 40 for each) were indiscriminately collected from commercial supermarkets in Port Said Province, Egypt, from March to May 2021. Subsequently, food samples were bacteriologically examined. The obtained isolates were tested for groEL gene sequence analysis, antibiotic susceptibility, biofilm production, and PCR screening of toxigenic and resistance genes.

Results: The overall prevalence of B. cereus among the inspected food samples was 21%, where the highest predominance was detected in minced meat (42.5%), followed by beef meat (30%). The phylogenetic analysis of the groEL gene exposed that the examined B. cereus strain disclosed a notable genetic identity with other strains from the USA and China. Moreover, the obtained B. cereus strains revealed β-hemolytic activity, and 88.1% of the recovered strains tested positive for biofilm production. PCR evidenced that the obtained B. cereus strains usually inherited the nhe complex genes (nheA and nheC: 100%, and nheB: 83.3%), followed by cytK (76.2%), hbl complex (hblC and hblD: 59.5%, hblB: 16.6%, and hblA: 11.9%), ces (54.7%), and pc-plc (30.9%) virulence genes. Likewise, 42.9% of the examined B. cereus strains were MDR to six antimicrobial classes and encoded bla1, bla2, ermA, and tetA genes.

Conclusion: In summary, this study highlights the presence of MDR B. cereus in meat and meat products, posing a significant public health risk. The contamination by B. cereus is common in minced meat and beef meat. The molecular assay is a reliable fundamental tool for screening emerging MDR B. cereus strains in meat and meat products.

Keywords: MDR B. cereus; Meat and meat products; Resistance genes; Resistance patterns; Toxigenic genes.

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Bacillus cereus
Cattle
Drug Resistance, Bacterial / genetics
Enterotoxins / genetics
Food Microbiology*
Humans
Meat
Meat Products*
Phylogeny

Substances

Enterotoxins
Anti-Bacterial Agents