Wide but Variable Distribution of a Hypervirulent Campylobacter jejuni Clone in Beef and Dairy Cattle in the United States

Abstract

Campylobacter jejuni clone SA is the major cause of sheep abortion and contributes significantly to foodborne illnesses in the United States. Clone SA is hypervirulent because of its distinct ability to produce systemic infection and its predominant role in clinical sheep abortion. Despite the importance of clone SA, little is known about its distribution and epidemiological features in cattle. Here we describe a prospective study on C. jejuni clone SA prevalence in 35 feedlots in 5 different states in the United States and a retrospective analysis of clone SA in C. jejuni isolates collected by National Animal Health Monitoring System (NAHMS) dairy studies in 2002, 2007, and 2014. In feedlot cattle feces, the overall prevalence of Campylobacter organisms was 72.2%, 82.1% of which were C. jejuni Clone SA accounted for 5.8% of the total C. jejuni isolates, but its prevalence varied by feedlot and state. Interestingly, starlings on the feedlots harbored C. jejuni in feces, including clone SA, suggesting that these birds may play a role in the transmission of Campylobacter In dairy cattle, the overall prevalence of clone SA was 7.2%, but a significant decrease in the prevalence was observed from 2002 to 2014. Whole-genome sequence analysis of the dairy clone SA isolates revealed that it was genetically stable over the years and most of the isolates carried the tetracycline resistance gene tet(O) in the chromosome. These findings indicate that clone SA is widely distributed in both beef and dairy cattle and provide new insights into the molecular epidemiology of clone SA in ruminants.IMPORTANCEC. jejuni clone SA is a major cause of small-ruminant abortion and an emerging threat to food safety because of its association with foodborne outbreaks. Cattle appear to serve as a major reservoir for this pathogenic organism, but there is a major gap in our knowledge about the epidemiology of clone SA in beef and dairy cattle. By taking advantage of surveillance studies conducted on a national scale, we found a wide but variable distribution of clone SA in feedlot cattle and dairy cows in the United States. Additionally, the work revealed important genomic features of clone SA isolates from cattle. These findings provide critically needed information for the development of preharvest interventions to control the transmission of this zoonotic pathogen. Control of C. jejuni clone SA will benefit both animal health and public health, as it is a zoonotic pathogen causing disease in both ruminants and humans.

Keywords: Campylobacter jejuni; cattle; clone SA; prevalence.

FIG 1

Dendrogram showing the PFGE patterns (KpnI) of C. jejuni isolates from feces of feedlot cattle and starlings. The clone SA strains are represented by two closely associated PFGE patterns (I and II), as was the case for sheep clone SA isolates (29). IA3902 is a known isolate of clone SA and was used as a reference. The isolates' names are listed on the right of the dendrogram. Starling isolates are marked with stars. TX, Texas; CO, Colorado; MO, Missouri; IA, Iowa; KS, Kansas; FC, feedlot cattle; ST, starling. The numbers in the names of the isolates are arbitrary numbers assigned to feedlots and samples. Please note that the starling isolates represent the total C. jejuni population isolated from the birds, while the cattle isolates included in the PFGE analysis were preselected for putative clones SA by the PCR.

FIG 2

Maximum likelihood phylogenetic tree constructed with the pan-genome (a) and core genome (b) differences among 170 C. jejuni clone SA isolates from sheep and cattle. The clone SA strains are intermixed between sheep and cattle and among the isolation years (2002, 2007, and 2014). The isolates are color-coded based on their source hosts and isolation years: red for sheep, blue for NAHMS Dairy 2002 cattle, green for NAHMS Dairy 2007 cattle, and black for NAHMS Dairy 2014 cattle.