Disinfectant and antimicrobial susceptibility profiles of the big six non-O157 Shiga toxin-producing Escherichia coli strains from food animals and humans

Authors: Beier, Ross; FRANZ, EELCO - National Institute For Public Health And The Environment (RIVM); Bono, James - Jim; Mandrell, Robert; Fratamico, Pina; Callaway, Todd; Andrews, Kathleen - Kate; Poole, Toni; Crippen, Tawni - Tc; Sheffield, Cynthia; Anderson, Robin; Nisbet, David

Submitted to: Journal of Food Protection
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/24/2016
Publication Date: 8/1/2016
Publication URL: https://handle.nal.usda.gov/10113/5491326
Citation: Beier, R.C., Franz, E., Bono, J.L., Mandrell, R.E., Fratamico, P.M., Callaway, T.R., Andrews, K., Poole, T.L., Crippen, T.L., Sheffield, C.L., Anderson, R.C., Nisbet, D.J. 2016. Disinfectant and antimicrobial susceptibility profiles of the big six non-O157 Shiga toxin-producing Escherichia coli strains from food animals and humans. Journal of Food Protection. 79(8):1355-1370.

Interpretive Summary: Many different kinds of disinfectants are used on farms, in food processing plants, in hospitals, and in homes. In each of these places there is also widespread use of a variety of antibiotics. Little is known about the impact of disinfectants on the spread of antibiotic resistance. Certain bacteria named non-O157 Shiga toxin-producing Escherichia coli (non-O157 STECs) are a major health hazard. The major six serogroups of the non-O157 STECs have recently been added to the Zero Tolerance Policy by the USDA because of their association with foodborne disease. We found that non-O157 STECs isolated from animals had a lower prevalence of antimicrobial resistance (AMR) of 35.4% compared to isolates from humans having AMR of 43.9%. The decreasing prevalence of AMR in animal strains followed O145 > O45 > O121 > O111 > O26 > O103 and in human strains followed O145 > O103 > O26 > O111 > O121 > O45. A high prevalence of AMR in O45 and O121 animal strains, and no resistance or a low prevalence in human strains in these serogroups suggests another source of human exposure to O45 and O121 infections than food animals. There was no observed correlation between disinfectant resistance and antibiotic resistance. All strains were susceptible to triclosan. Animal strains had a higher prevalence of resistance to chlorhexidine than human strains. Both animal and human strains had a similar low prevalence of low-level benzalkonium chloride (BKC) resistance. Due to the prevalence of resistance to BKC in O145 and chlorhexidine in O45 animal strains, in contrast, both serogroups from human strains were susceptible, suggesting another source of human exposure to O145 and O45 infections than food animals. Benzyldimethylammonium chlorides (BACs) and C10AC were primary active components in DC&R and P-128, respectively, against non-O157 STECs. A high prevalence (61.5%) of FS512 MICs greater than or equal 8 ug/ml in O121 food animal strains compared to a lower prevalence (25%) in O121 human strains suggests another source of human exposure to non-O157 STEC O121 infections than food animals. Bacterial inhibition was not dependent solely on pH or [H+], but was correlated with dissociated organic acid species and with some undissociated acids. Inhibition may be occurring by both acid species.

Technical Abstract: The disinfectant and antimicrobial susceptibility profiles of 144 non-O157 Shiga toxin-producing Escherichia coli (STECs) from food animals and humans were determined. An overall moderate prevalence of 38.9% antimicrobial resistance (AMR) was observed in these strains. Animal strains had a lower prevalence of AMR (35.4%) compared to human strains (43.9%), but a higher prevalence of the resistance profile GEN, KAN and TET. The decreasing prevalence of AMR in animal strains followed O145 > O45 > O121 > O111 > O26 > O103 and in human strains followed O145 > O103 > O26 > O111 > O121 > O45. One animal strain each of serogroups O121 and O145 and one human strain of serogroup O26 had extensive drug resistance (XDR). A high prevalence of AMR in O45 and O121 animal strains and no resistance or a low prevalence in human strains in these serogroups suggests another source of human exposure to O45 and O121 infections than food animals. All strains were susceptible to triclosan. Animal strains had a higher prevalence of resistance to chlorhexidine than human strains. Both animal and human strains had a similar low prevalence of low-level benzalkonium chloride (BKC) resistance. Due to the prevalence of resistance to BKC in O145 and chlorhexidine in O45 animal strains, in contrast, both serogroups from human strains were susceptible, suggesting another source of human exposure to O145 and O45 infections than food animals. Benzyldimethylammonium chlorides (BACs) and C10AC were primary active components in DC&R and P-128, respectively, against non-O157 STECs. A high prevalence (61.5%) of FS512 MICs greater than or equal to 8 ug/ml in O121 food animal strains compared to a lower prevalence (25%) in O121 human strains suggests another source of human exposure to non-O157 STEC O121 infections than food animals. Bacterial inhibition was not dependent solely on pH or [H+], but correlated with dissociated organic acid species and with some undissociated acids. Inhibition may be occurring by both acid species.