Diversity, Antibiotic Resistance, and Biofilm-Forming Ability of Enterobacteria Isolated from Red Meat and Poultry Preparations

Abstract

A total of 44 samples of beef, pork, and poultry preparations were tested. Average counts (log cfu/g) of enterobacteria were 1.99 ± 0.99 (beef preparations), 1.96 ± 1.44 (pork), 2.09 ± 0.92 (chicken), and 2.17 ± 1.06 (turkey) (p > 0.05). Two hundred enterobacterial strains were identified and 13 genera (21 species) were distinguished, including species that are a significant cause of infection. The most common genera were Escherichia (32.5% of strains), Serratia (17.0%), Hafnia (12.5%), and Salmonella (12.0%). Isolates were screened by disc diffusion for susceptibility to 15 antibiotics. A total of 126 strains (63% of the isolates) were multirresistant (having resistance to two or more antibiotics), 46 (23%) were resistant to one antibiotic, and 28 (14%) were sensitive to all antibiotics. The average number of resistances per strain was 2.53 ± 2.05. A higher (p < 0.05) average number of resistances was observed in strains from turkey (3.14 ± 2.55) than in strains from beef (2.15 ± 1.22), pork (2.16 ± 1.39), or chicken (2.44 ± 2.22). At least 50% of strains showed resistance or reduced susceptibility to ampicillin, cefotaxime, ceftazidime, or streptomycin, considered to be “critically important” antimicrobial agents in human medicine. Seventy-nine strains (39.5%), 60 strains (30.0%), and 46 strains (23.0%) were weak, moderate, and strong biofilm producers (crystal violet assay), respectively. This investigation provides evidence that bacteria from red meat and poultry preparations pose major potential risk to consumers.

Quantification of Total and Viable Cells and Determination of Serogroups and Antibiotic Resistance Patterns of Listeria monocytogenes in Chicken Meat from the North-Western Iberian Peninsula

“…Various studies refer to lower levels of enterobacteria in poultry, both in Spain, where a figure of 2.89 ± 0.77 log 10 cfu/g was recorded by Buzón-Durán et al [ 4 ], and in other areas within the European Union, with 2 log 10 cfu/g noted by Fraqueza et al [ 38 ]. Previous studies also carried out in north-western Spain [ 3 ] indicated a lower load of enterobacteria in meat preparations based on beef, at 1.99 ± 0.99 log 10 cfu/g, and pork, at 1.96 ± 1.44 log 10 cfu/g. This greater count of enterobacteria in poultry products when compared to foodstuffs of other types may have been an outcome of the higher initial pH in birds’ muscle meat [ 39 ].…”

“…A certain proportion of meat is eaten in the form of meat preparations. Regulation (EC) 853/2004 defines meat preparations (e.g., minced meat), as fresh meat, including meat that has been reduced to fragments, which has had foodstuffs, seasonings or additives added to it, or which has undergone processes insufficient to modify the internal muscle fibre structure of the meat, and thus to eliminate the characteristics of fresh meat [ 3 ]. Meat preparations are suitable for a range of cooking techniques, and thus satisfy the demands of consumers, who prefer meat products ready to cook, since saving time in the preparation of food has become a priority for most families [ 4 , 5 ].…”

Prevalence, antibiotic resistance patterns, and biofilm formation ability of Enterobacterales recovered from food of animal origin in Egypt

“…In addition, XDR patterns were identified in 100% of the isolates of K. oxytoca and K. pneumoniae. These MDR Enterobacteriaceae isolates, also referred to as superbugs, are capable of horizontally transferring their resistance genes to other pathogenic microorganisms at various points along the food chain and have few effective treatments for their infections [17,67]. The increasing role of animal-derived food to MDR Enterobacteriaceae, including Enterobacter, Klebsiella, and Serratia, have previously been documented in raw milk, red meat, and chicken meat this trend continues [17,34,[68][69][70].…”

“…These MDR Enterobacteriaceae isolates, also referred to as superbugs, are capable of horizontally transferring their resistance genes to other pathogenic microorganisms at various points along the food chain and have few effective treatments for their infections [17,67]. The increasing role of animal-derived food to MDR Enterobacteriaceae, including Enterobacter, Klebsiella, and Serratia, have previously been documented in raw milk, red meat, and chicken meat this trend continues [17,34,[68][69][70]. Of these health significances, according to a Centers for Disease Control and Prevention report from 2013, fluoroquinolone-resistant P. aeruginosa and other antibiotic-resistant infections sickened more than two million people each year, with at least 23,000 dying [71].…”

“…In addition, the ability of microorganisms to form biofilms, which differ greatly between bacterial populations, is one of the factors that determine their virulence and ability to survive in unfavorable environments like preservation. Therefore, the prevalence and associated potential risk level of biofilm-forming Enterobacteriaceae was a focus of earlier studies [ 16 , 17 ].…”