The epidemiology and ecology of Escherichia coli O157 on U.S. dairies

Abstract

Escherichia coli O157 (O157) is a bacterium that causes human foodborne disease outbreaks worldwide. Beef and dairy cattle are reservoirs for O157, as they harbor the bacteria in their lower gastrointestinal (GI) tracts and shed it in feces without clinical illness. Humans become infected with O157 after contacting cows or manure, or ingesting the bacteria on dairy, meat or produce products. Dairy cattle are a central part of the U.S food supply, providing milk for a multitude of dairy products, and 15-20% of the beef produced. Transmission of O157 from dairy cattle to humans is reduced by techniques that limit bacterial survival after food is harvested (i.e. post-harvest). However, O157 outbreaks occur after post-harvest dairy pasteurization and slaughter laws are applied across the U.S food chain. Due to these outbreaks, an emphasis has been placed on developing methods that reduce O157 presence prior to harvest (i.e pre-harvest) at the dairy farm. An understanding of dairy cow O157 prevalence and magnitude of shedding, and animal-level correlates for shedding, may aid in the development of pre-harvest O157 strategies. We hypothesized that life history features (parity, history of disease, others) would be associated with O157 shedding by adult cows on Colorado dairies, and that shedding in early lactation would be correlated with shedding detected during the pre-weaning period of these dams' calves. Although overall prevalence was low (3.0%) and only one individual shed O157 at a high magnitude (>103 CFU/g feces), a higher number of adult cows shed O157 between June and October. Dams were at increased risk of shedding if they were a lower parity, earlier days in milk, or had a history of antibiotic use. Calf shedding was not detected on the Colorado dairies studied; no correlation between dam and calf O157 shedding was present. We hypothesized that the lack of calf shedding was due to the sampling time-frame, calf management, and the geographic region of study. Using fecal samples collected by the National Animal Health Monitoring System (NAHMS) from dairy calves across the U.S, we estimated the prevalence of O157 shedding and managerial, environmental, and calf-level variables associated with pathogen presence. U.S calf shedding of O157 was low (2.5 %) and not influenced by geographic region. Calves were at increased risk to shed if they received colostrum from their own dam, which suggests that increased time spent with the dam is associated with shedding. Results indicated that the passive transfer status of calves also influenced shedding, but was affected by the temperature and humidity index (THI) calves were exposed to during pre-weaning. Calves experiencing thermoneutral or heat-stress THIs were more likely to shed O157 if they had poor or moderate passive transfer. Calves were unlikely to shed if they had excellent passive transfer, regardless of THI. Herds of cattle likely have uniform levels of O157 exposure, but only some individuals shed the bacteria. We hypothesized that the GI microbial community influenced which cows become colonized with O157 post-ingestion. After measuring microbial communities in naturally infected cows on Colorado dairies, lower microbial richness (i.e. total number of unique species) was associated with intermittent or multi-day shedding of O157. The species Bacillus coagulans was lower in abundance in fecal samples that contained O157, while the genus Moryella spp was higher in abundance. The results of this dissertation highlight factors associated with O157 shedding by dairy cows and calves. This information may be used when developing techniques that reduce transmission between dairy cows, or dissemination of O157 beyond the dairy. Because O157 does not adversely affect cows, the future adoption of O157 mitigation strategies relies on whether or not these approaches benefit the dairy operation. Based on our results, we hypothesize that ill health and cow stress is associated with shedding, but is difficult to measure and monetarily quantify. At the current time, development of reduction strategies should focus on methods that reduce O157 while simultaneously improving cow health and production (e. g reducing stress during cow transition periods, improving passive transfer and limiting dam exposure of calves, feeding probiotics that improve GI health, creating multi-pathogen vaccines). We propose that future studies should also focus on determining whether O157 augments milk production and cow fertility.