Identification of Potential Environmentally Adapted Campylobacter jejuni Strain, United Kingdom

In a study of Campylobacter infection in northwestern England, 2003–2006, C. jejuni multilocus sequence type (ST)–45 was associated with early summer onset and was the most prevalent C. jejuni type in surface waters. ST-45 is likely more adapted to survival outside a host, making it a key driver of transmission between livestock, environmental, and human settings.

likely to be reported in early summer than during the rest of the year (odds ratio 2.79, confi dence interval 1.56-4.99, p = 0.001; 1,008 observations), and this relationship was not seen with other prevalent sequence types.
Seventy-four (37%) of 198 river water samples were positive for C. jejuni, and among these, 28 sequence types (Table 1) were identifi ed, 11 of which were also reported among human cases in the study population. The most prevalent sequence type identifi ed was ST-45, and the seasonality of isolation appears to closely correlate with the seasonality of human disease onset caused by this type (Figure 2).
Univariate logistic regression analysis identifi ed that, in addition to illness during early summer, the statistically strongest associations (p<0.1) with ST-45 were being <5 years of age and living in the more rural part of the study area. These 3 factors remained signifi cantly and independently more associated with ST-45 infection than with other sequence types when combined in a multivariate model (tested by using likelihood ratio tests) ( Table 2). When this model was used, subsequent estimation of the association of food and exposure variables showed that consumption of chicken at least once was less associated and consumption of home-delivered milk and going fi shing were more associated with ST-45 than with other types. This fi nding was sustained in a multivariate model (also including the demographic variables previously mentioned) ( Table 2).   However, information on exposure variables was not available for all 1,008 cases of C. jejuni, which resulted in a loss of statistical power.

Conclusions
We have shown that a single prevalent human strain of C. jejuni, ST-45, is strongly associated with the early summer seasonal peak of campylobacteriosis incidence described previously in northwestern England (7). This strain is also frequently isolated from recreational surface waters adjacent to the populations studied, from which other prevalent strains have rarely been isolated. The concordance between period of ST-45 isolation in water and reported incidence in humans is striking and suggests a relationship between the presence of this strain in the environment and human infection. When compared with case-patients infected by other sequence types of C. jejuni, persons infected with ST-45 are more likely to live in rural areas, to be <5 years of age, to have gone fi shing before illness, or to have consumed home-delivered milk, and were much less likely to have eaten any chicken in the 2 weeks before illness.
The coincident seasonal presence of ST-45 in both surface water and in case-patients may arise simply through seasonal excretion of ST-45, resulting from well-characterized seasonal infection in humans (1,3,7) or livestock. The river systems sampled were both urban and rural in character, and contamination through human sewage discharge or animal feces from adjoining pastures is possible. However, other common human and animal Campylobacter sequence types were largely absent from the water sampled.
Although ingestion of untreated surface waters has previously been shown to be a risk factor for campylobacteriosis in a UK-wide case-control study (9), these new data are not suffi ciently robust to demonstrate a causal link for ST-45 infection. Although data were collected on proxy exposures to water, reported exposures were very low. Fur-  thermore, systematic water sampling would be required to confi rm the apparent seasonal positivity of ST-45 in these data. The potential role of pets, and in particular dogs, in bridging the gap between exposure to surface water (for example, while being exercised) and domestic exposure settings remains to be investigated. Although cases of infection caused by ST-45 were no more associated with owning dogs than were cases of other sequence types (data not shown), the exposures of those dogs were not recorded. In a recent study, cases of ST-45 clonal complex were more associated with contact with pet dogs and cats than were other clonal complexes identifi ed (10); pet-mediated transmission of ST-45 might be supported in this study by the observed association of ST-45 with young children.
Despite the evidence presented of a potential environmental transmission route for ST-45, it is also a type well recognized to colonize poultry (10)(11)(12), and the incidence among humans may be a result of consumption of seasonally contaminated poultry (2). However, the absence of strong early summer seasonality among other recognized chicken-adapted sequence types suggests that this is not the case (data not shown). Also, the evidence from our study is strong that consumption of chicken (a common human exposure) is less associated with human ST-45 infection than with other types.
An explanation for these observations may be that ST-45 represents a strain of Campylobacter that is comparatively well adapted to survival outside an animal host, as has been hypothesized for some strains of C. coli (13). Other studies have reported that ST-45 is more widely distributed in terms of host and ecologic niche, including water, than other common sequence types (12,14). Evidence also has indicated that ST-45 is more resilient to physical stress than other sequence types (15). This would certainly support the hypothesis that ST-45 was more available to infect humans through transmission routes other than food, either through direct exposure to water or the countryside through outdoor activities or by indirect exposure through pets. The hypothesis is further supported by the association of human ST-45 with more rural area of residence in these data. The availability of ST-45 to humans due to its hypothesized adaptive survival outside animal hosts would apply even more so to poultry, because of their increased environmental exposure, and 1 study has demonstrated that contamination of a new fl ock with ST-45 arose from an isolate in a puddle outside a chicken house (12). Thus, through an as-yet-uncharacterized adaptation, ST-45 may be a strain of C. jejuni that is able to bridge the various recognized environmental, livestock, and human transmission settings for disease, making it a key target for intervention in reducing Campylobacter prevalence. It may also be a key driver for the early summer rise in human incidence, both through nonfoodborne exposure and contamination of food animals.