Regional Salmonella Differences in United States Broiler Production from 2016 to 2020 and the Contribution of Multiserovar Populations to Salmonella Surveillance

Abstract

Poultry remains a considerable source of foodborne salmonellosis despite significant reduction of Salmonella incidence during processing. There are multiple entry points for Salmonella during production that can lead to contamination during slaughter, and it is important to distinguish the serovars present between the different stages to enact appropriate controls. National Salmonella data from the U.S. Department of Agriculture-Food Safety Inspection Service (USDA-FSIS) monitoring of poultry processing was analyzed from 2016 to 2020. The overall Salmonella incidence at processing in broiler carcasses and intact parts (parts) decreased from 9.00 to 6.57% over this period. The incidence in parts was higher (11.15%) than in carcasses (4.78%). Regional differences include higher proportions of serovars Infantis and Typhimurium in the Atlantic and higher proportion of serovar Schwarzengrund in the Southeast. For Georgia, the largest broiler-producing state, USDA-FSIS data were compared to Salmonella monitoring data from breeder flocks over the same period, revealing serovar Kentucky as the major serovar in breeders (67.91%) during production but not at processing, suggesting that it is more effectively removed during antimicrobial interventions. CRISPR-SeroSeq was performed on breeder samples collected between 2020 and 2021 to explain the incongruence between pre- and postharvest and showed that 32% of samples contain multiple serovars, with up to 11 serovars found in a single flock. High-resolution sequencing identifies serovar patterns at the population level and can provide insight to develop targeted controls. The work presented may apply to other food production systems where Salmonella is a concern, since it overcomes limitations associated with conventional culture. IMPORTANCE Salmonella is a leading cause of bacterial foodborne illness in the United States, with poultry as a significant Salmonella reservoir. We show the relative decrease in Salmonella over a 5-year period from 2016 to 2020 in processed chicken parts and highlight regional differences with respect to the prevalence of clinically important Salmonella serovars. Our results show that the discrepancy between Salmonella serovars found in pre- and postharvest poultry during surveillance are due in part by the limited detection depth offered by traditional culture techniques. Despite the reduction of Salmonella at processing, the number of human salmonellosis cases has remained stable, which may be attributed to differences in virulence among serovars and their associated risk. When monitoring for Salmonella, it is imperative to identify all serovars present to appropriately assess public health risk and to implement the most effective Salmonella controls.

Keywords: CRISPR-SeroSeq; Salmonella; monitoring; poultry; salmonellosis; serovars.

FIG 1

Salmonella serovar distribution in broiler carcasses and intact parts at processing across the United States, 2016 to 2020. Pie charts depict the prevalence of different serovars in broiler processing establishments in the United States. The size of the circle reflects the number of positive samples, with the smallest (23 samples) and largest (540 samples) numbers shown in the dotted circle guide at the bottom. The regions are defined as follows: Atlantic (CT, DE, MA, MD, ME, NH, NJ, NY, PA, RI, VT, VA, and WV), Southeast (AL, GA, FL, KY, MS, NC, SC, and TN), South Central (AR, LA, OK, and TX), Midwest (IL, IN, IA, KS, MI, MN, MO, NE, ND, OH, SD, and WI), and Mountain & West (AZ, CA, CO, ID, MT, NV, NM, OR, UT, WA, and WY). Regions are ordered based on broiler production per region, according to the USDA (U.S. Department of Agriculture–National Agricultural Statistics Service, 2021). Select serovars are highlighted as shown, and others are indicated in different shades of gray; full serovar information is provided in Tables S1 and S2 in the supplemental material.

FIG 2

Serovar distribution for Salmonella-positive breeder, carcass, intact parts, and nonintact parts samples collected in Georgia, 2016 to 2020. Pie charts depict the prevalence of different serovars in breeder samples collected at 15 to 19 weeks and 40 to 45 weeks (top two rows) and samples from processing establishments in Georgia (bottom three rows). The size of the circle reflects the number of positive samples with the smallest (13 samples) and largest (162 samples) numbers shown in the dotted circle guide on the right. The values for the breeder samples are divided by 10. Select serovars are highlighted as indicated and others are shown in different shades of gray. For the samples from processing, the full serovar data are presented in Table S3 in the supplemental material.

FIG 3

Salmonella-positive breeder monitoring samples often contain multiple serovars. CRISPR-SeroSeq was used to determine the relative abundance of Salmonella serovars within each sample. Each column is an individual sample that was derived from the overnight tetrathionate enrichment culture from an environmental boot sock sample; these are arranged according to the date they were submitted, and the month is indicated. The individual serovars are shown on the left, and the heatmap shows the relative serovar abundance in each sample according to the key. Samples with more than one serovar are indicated in boldface (bottom row). The two serovar Kentucky lineages and four serovar Montevideo lineages are named as previously described (72, 73).