Submitted to: PLoS One
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/8/2013
Publication Date: 10/8/2013
Citation: Sandt, C.H., Cray, P.J., Tewari, D., Ostroff, S., Joyce, K., Mikanatha, N.M. 2013. A comparison of non-typhoidal Salmonella from humans and food animals using pulsed-field gel electrophoresis and antimicrobial susceptibility patterns. PLoS One. 8(10): e77836. doi: 10.1371/journal.pone.0077836. Interpretive Summary: Salmonella is a food borne pathogen that can be acquired from eating contaminated foods. When food borne outbreaks occur, the public health community attempts to identify the food source of the infection. Typically, a clinically ill person will submit a stool specimen to a local or state public health clinical laboratory for work-up. Once Salmonella is obtained from the specimen a special molecular genetic test called pulsed field gel electrophoresis or PFGE for short is conducted at state public health laboratories. During PFGE procedure the DNA of the Salmonella is broken into small fragments which are subjected to an electric current in an agarose gel matrix allowing them to be separated by size. The end result is a series of vertical bands, called a ‘pattern or fingerprint’ which is specific for that particular Salmonella isolate. This fingerprint is stable and remains the same every time the PFGE is run on that particular Salmonella isolate. We also routinely sample food animal products from cattle, chickens, swine and turkeys from federally inspected slaughter and processing facilities throughout the U.S. and look for Salmonella. When we isolate Salmonella, it is also subjected to PFGE and the information along with the animal source is kept in a database to use for comparison to human data during food borne outbreaks. In this study Salmonella isolates from ill humans in Pennsylvania and food animal Salmonella isolates from the Northeast U.S. which included Pennsylvania were subjected to PFGE and compared. These isolates were collected during the period 2005 through 2011. In addition to PFGE, both human and food animal isolates were tested for antimicrobial susceptibility to a panel of antimicrobials important in both human and veterinary medicine. We were also able to serotype, or name, all of the Salmonella isolates. We found that even though Salmonella isolates may have the same serotype (name) and PFGE pattern some will be resistance to certain antimicrobials while others will be susceptible. Sixteen (80%) of the 20 most common PFGE patterns observed in humans were also observed in food animals. The most common human pattern, Enteritidis pattern JEGX01.0004 (JEGX01.003ARS) was associated with 16.5% of reported cases of human Salmonella illness; this pattern was almost exclusively (99%) found in Salmonella recovered from chickens in every year of our study. Interestingly, the human isolate associated with this pattern was susceptible to 94.7% of the antimicrobials tested while the food animal isolate was susceptible to 97.2% of the antimicrobials. Resistance to three or more classes of antimicrobials (defined as multidrug resistance) was observed in five serotypes of Salmonella recovered from both human and food animal sources. Taken together this information is important to the public health community as they look to match specific serotypes of Salmonella with food animal sources, for outbreak investigations, and for tailoring of interventions to maximize their impact on prevention. It is also important to scientists who design and maintain surveillance programs.
Technical Abstract: Salmonellosis is one of the most important foodborne diseases affecting humans. To characterize the relationship between Salmonella causing human infections and their food animal reservoirs, we compared pulsed-field gel electrophoresis (PFGE) and antimicrobial susceptibility patterns of non-typhoidal Salmonella isolated from ill humans in Pennsylvania and from food animals prior to retail. Human clinical isolates were received from 2005 through 2011 during routine public health operations in Pennsylvania. Isolates from cattle, chickens, swine and turkeys were recovered during the same period from federally inspected slaughter and processing facilities in the northeastern United States. We found that subtyping Salmonella isolates by PFGE revealed differences in antimicrobial susceptibility patterns and, for human Salmonella, differences in food animal sources and invasiveness that were not evident from serotyping alone. Sixteen (80%) of the 20 most common human Salmonella PFGE patterns were identified in Salmonella recovered from food animals (“shared common patterns”). The most common human Salmonella PFGE pattern, Enteritidis pattern JEGX01.0004 (JEGX01.0003ARS), was associated with 16.5% of all reported cases of human salmonellosis and 20% of all reported cases of invasive salmonellosis. In food animals, this pattern was almost exclusively (99%) found in Salmonella recovered from chickens and was present in poultry meat in every year of the study. Enteritidis pattern JEGX01.0004 (JEGX01.0003ARS) was associated with susceptibility to all antimicrobial agents tested in 94.7% of human and 97.2% of food animal Salmonella isolates. In contrast, multidrug resistance (resistance to three or more classes of antimicrobial agents) was observed in five PFGE patterns. Berta pattern JAXX01.0001 (JAXX01.0003 ARS) was associated with multidrug resistance in 33% of human Salmonella isolates and 100% of food animal Salmonella isolates. Considered together, Typhimurium patterns JPXX01.0003 (JPXX01.0003 ARS) and JPXX01.0018 (JPXX01.0002 ARS) were associated with resistance to five or more classes of antimicrobial agents, ampicillin, chloramphenicol, streptomycin, sulfa and tetracycline (ACSSuT), in 92% of human and 80% of food animal Salmonella isolates. The information from our study can assist in source attribution, outbreak investigations, and tailoring of interventions to maximize their impact on prevention.