Testing an ecological model for transmission of Salmonella enterica in swine production ecosystems using genotyping data

An ecological model for transmission of Salmonella enterica in swine production ecosystems was developed, identifying host species, environmental reservoirs, and temporal, spatial, and functional (i.e., stage of production) dimensions. It was hypothesized that transmission was most likely within spatial and functional compartments, between hosts of the same species and abiotic compartments of the same type. Eighteen swine production systems in Illinois, USA, were sampled in four collection cycles (1998, 1999, 2000, 2003). There were 11,873 samples collected, including feces from swine and other mammals and birds, and samples from insects, pen floors, boots, feed, and water. The 460 Salmonella isolates obtained were genotyped using repetitive sequence PCR with three primers—REP, BOX, and ERIC. All isolates from 2000 and 2003 were serotyped, as well as a subsample from 1998 and 1998. Genetic relatedness was estimated from the similarity of fragmentation patterns after gel electrophoresis of PCR products. Cluster analysis identified genetically related isolates. Linking of isolates in tight clusters (similarity ≥85%) was viewed as evidence for transmission. Five farms had a sufficient number of tight clusters for hypothesis testing. The factors most differentiating isolates genetically were farm of origin and time of sampling. Isolates were also differentiated genetically by site, building, room, and pen. There was no consistent association of genotype with stage of production or host/environment reservoir. Serotype analysis confirmed that Salmonella lineages were differentiated by visit and site. Thus, Salmonella transmission was primarily over short distances, i.e., within the same pen or room, with some transmission between rooms and buildings on the same site, but with limited transmission between sites. Transmission was observed across a variety of ecological niches represented by different host species and environmental reservoirs. Genetic differences over time reflected multiple introductions into the ecosystem of different Salmonella genotypes, as well as evolutionary changes within lineages. Intervention strategies to reduce Salmonella prevalence within swine production ecosystems would be best targeted at maintaining spatial barriers to transmission, whereas intervention targeted at specific biological hosts or environmental reservoirs is less likely to be effective.