Campylobacteriosis in urban versus rural areas: a case-case study integrated with molecular typing to validate risk factors and to attribute sources of infection

Abstract

Campylobacter infection is a leading cause of bacterial gastroenteritis worldwide, and most clinical cases appear as isolated, sporadic infections for which the source is rarely apparent. From July 2005 to December 2007 we conducted a prospective case-case study of sporadic, domestically-acquired Campylobacter enteritis in rural versus urban areas and a prevalence study of Campylobacter in animal and environmental sources in the Eastern Townships, Quebec. Isolates were typed using Multilocus Sequence Typing (MLST) to reinforce the case-case findings and to assign a source probability estimate for each human isolate. The risk of human campylobacteriosis was 1.89-fold higher in rural than urban areas. Unconditional multivariate logistic regression analysis identified two independent risk factors associated with human Campylobacter infections acquired in rural area: occupational exposure to animals (OR = 10.6, 95% CI: 1.2-91, p = 0.032), and household water coming from a private well (OR = 8.3, 95% CI: 3.4-20.4, p<0.0001). A total of 851 C. jejuni isolates (178 human, 257 chicken, 87 bovine, 266 water, 63 wild bird) were typed using MLST. Among human isolates, the incidence rates of clonal complexes (CC) CC-21, CC-45, and CC-61 were higher in rural than urban areas. MLST-based source attribution analysis indicated that 64.5% of human C. jejuni isolates were attributable to chicken, followed by cattle (25.8%), water (7.4%), and wild birds (2.3%). Chicken was the attributable source for the majority of cases, independent of residential area, sex and age. The increased incidence in rural compared to urban areas was associated with occupational exposure to animals, particularly cattle among those aged 15-34 years, and with consumption of private well water. Both bovine and water exposure appeared to contribute to the seasonal variation in campylobacteriosis. These results provide a basis for developing public education and preventive programs targeting the risk factors identified.

Figure 1.Quarterly. distribution of incidence rates of Campylobacter infections from July 2005 to December 2007 for urban and rural areas.

Figure 2. Distribution of incidence rates of Campylobacter infections by age group for urban and rural areas.

Figure 3. Incidence rates of Campylobacter infections in the Eastern Townships by age group and sex.

Figure 4. Quarterly distribution of the incidence rates of Campylobacter infections in humans from July, 2005 to December, 2007 (columns) and of the prevalence of Campylobacter in whole retail chickens from July, 2005 to October 2007 (line graph).

Figure 5. Distribution of attributable sources of human C. jejuni isolates by clonal complexes.

Only clonal complexes found in human isolates are represented. Human isolates are in black, chicken isolates are in yellow, bovine isolates are in red, water isolates are in blue and wild bird isolates are in green. The remaining 108 isolates were distributed among 74 STs which could not be assigned to any of the known lineages (unassigned STs; UA). Numbers at the top of the columns indicate the total number of isolates in each clonal complex.

Figure 6. Quarterly distribution of clonal complexes (in colors) among human isolates typed by MLST.

Incidence rates of Campylobacter infections in the Eastern Townships is indicated by the black line. UA: unassigned STs to a clonal complex.

Figure 7. The source probability assignment (y axis) of human campylobacteriosis cases (x axis) using the no-admixture model of STRUCTURE.

Each isolate is represented by a vertical bar, showing the estimated probability that it comes from each of the putative sources. Sources for Campylobacter jejuni were chickens (yellow), cattle (red), water (blue) and wild birds (green). Panel A showed all the 178 human cases typed, panel B cases from urban area and panel C from rural area. Isolates in panel A, B and C are ordered based on probability of source using the hierarchy chicken, bovine, water and wild bird. Panel D showed all the human cases sorted in the time by quarter of positive sampling.