Molecular evidence for zoonotic transmission of an emergent, highly pathogenic Campylobacter jejuni clone in the United States

Abstract

Campylobacter jejuni is a major zoonotic pathogen. A highly virulent, tetracycline-resistant C. jejuni clone (clone SA) has recently emerged in ruminant reservoirs and has become the predominant cause of sheep abortion in the United States. To determine whether clone SA is associated with human disease, we compared the clinical isolates of clone SA from sheep abortions with the human isolates of the PulseNet National Campylobacter databases at the CDC and the FDA using pulsed-field gel electrophoresis (PFGE), multilocus sequence typing (MLST), and serotyping. The combined SmaI and KpnI PFGE pattern designations of clone SA from sheep were indistinguishable from those of 123 (9.03%) human C. jejuni isolates (total, 1,361) in the CDC database, among which 56 were associated with sporadic infections and 67 were associated with outbreaks that occurred in multiple states from 2003 to 2010. Most of the outbreaks were attributed to raw milk, while the sources for most of the sporadic cases were unknown. All clone SA isolates examined, including PFGE-matched human isolates, belong to sequence type 8 (ST-8) by MLST and serotype HS:1,8, further indicating the clonality of the related isolates from different host species. Additionally, C. jejuni clone SA was identified in raw milk, cattle feces, the feces and bile of healthy sheep, and abortion cases of cattle and goats, indicating the broad distribution of this pathogenic clone in ruminants. These results provide strong molecular and epidemiological evidence for zoonotic transmission of this emergent clone from ruminants to humans and indicate that C. jejuni clone SA is an important threat to public health.

Fig 1

PFGE analysis of C. jejuni isolates from different sources using SmaI (A) or KpnI (B). The isolates were FDA 17848 and FDA 17817 (lanes 1 and 2; from human), FDA N337 and FDA N342 (lanes 3 and 4; from chicken), clone SA subtype I (IA5908; lane 5) and subtype II (IA3902; lane 6), a goat abortion isolate (IA625; lane 7), and C. jejuni NCTC 11168 (lane 8). M, size marker (Salmonella sp. strain Braenderup H9812 genomic DNA digested with XbaI).

Fig 2

PFGE-based dendrogram depicting the relatedness of 48 C. jejuni isolates from a lamb slaughterhouse. Strain names and STs are given next to the restriction profiles. The components of the strain prefixes, from left to right, are as follows: number 1 or 2, sampling occasion; E or L, ewe or lamb, respectively; lot number; B or F, bile or fecal sample, respectively; sample number; a or b, identifier of the C. jejuni colony when multiple colonies from the same sample were saved.

Fig 3

eBURST diagram depicting the evolutionary descent of the entire ST-21 complex in the Campylobacter MLST database. The database was accessed on 10 February 2010. The largest eBURST group with the default group definition (six of seven shared alleles), in which all STs are single locus variants of least one other ST in the group, is displayed. Each circle denotes an ST (only the major ones are shown for clarity), and the size of the circle is proportional to the number of isolates present in that genotype. Group and subgroup founders are shown as blue and yellow circles, respectively. The predicted group founder (ST-21; 99% bootstrap support) and clone SA (ST-8) are labeled.