A national epidemic of campylobacteriosis in Iceland, lessons learned.

Epidemics often result in organizational, policy and technical changes within a country. In 1999, an epidemic of campylobacteriosis was reported in Iceland. The recent availability of fresh poultry products in the marketplace was suggested as the source of infection. This paper reports on the context of the epidemic, reviews interventions implemented to prevent campylobacteriosis, and discusses lessons learned. A retrospective study of interventions implemented in Iceland from June 1995 to December 2007 was conducted by interviewing key informants and reviewing Iceland's literature. Cumulative incidence rates of domestic campylobacteriosis by year and average incidence rates per epidemic period were calculated. Interventions included on-farm surveillance of Campylobacter, producer education, enhanced biosecurity measures, changes in poultry processing, a leak-proof packaging policy, a freezing policy for products from Campylobacter-positive poultry flocks, consumer education, and the creation of a legislated inter-organizational response committee. These interventions appear to have collectively contributed to a decrease in campylobacteriosis' incidence rate near pre-epidemic baseline levels. Expert consultations revealed that the implementation of a Campylobacter surveillance program in poultry and the freezing policy were critical to controlling the disease in the Icelandic population. It was also recognized that new multidisciplinary collaborations among public health, veterinary, and food safety authorities and a sustained co-operation from the poultry industry were integral factors to the mitigation of the epidemic. Iceland's response to the campylobacteriosis epidemic is a lesson learned of inter-disciplinary and inter-organizational precautionary public health action in the face of a complex public health issue.

Comparison of Campylobacter jejuni isolates from human, food, veterinary and environmental sources in Iceland using PFGE, MLST and fla-SVR sequencing.

AIMS: Campylobacter jejuni isolates from various sources in Iceland were genotyped with the aim of assessing the genetic diversity, population structure, source distribution and campylobacter transmission routes to humans. METHODS AND RESULTS: A collection of 584 Campylobacter isolates were collected from clinical cases, food, animals and environment in Iceland in 1999-2002, during a period of national Campylobacter epidemic in Iceland. All isolates were characterized by pulse field gel electrophoresis (PFGE), and selected subset of 52 isolates representing the diversity of the identified PFGE types was further genotyped using multilocus sequence typing (MLST) and fla-SVR sequencing to gain better insight into the population structure. CONCLUSIONS: The results show a substantial diversity within the Icelandic Campylobacter population. Majority of the human Campylobacter infections originated from domestic chicken and cattle isolates. MLST showed the isolates to be distributed among previously reported and common sequence type complexes in the MLST database. SIGNIFICANCE AND IMPACT OF THE STUDY: The genotyping of Campylobacter from various sources has not previously been reported from Iceland, and the results of the study gave a valuable insight into the population structure of Camp. jejuni in Iceland, source distribution and transmission routes to humans. The geographical isolation of Iceland in the north Atlantic provides new information on Campylobacter population dynamics on a global scale.

The impact of domestic travel on estimating regional rates of human campylobacteriosis.

Residential locations of cases are often used as proxy measures for the likely place of exposure and this assumption may result in biases affecting both surveillance and epidemiological studies. This study aimed to describe the importance of domestic travel in cases of human campylobacteriosis reported during routine surveillance in Iceland from 2001 to 2005. Various measures of disease frequency were calculated based upon the cases' region of residence, adjusting location of domestic travel cases to their travel region, as well as separate estimations for travellers and non-travellers. Of the 376 cases included in the analysis, 37% had travelled domestically during their incubation period. Five of the eight regions were identified as high-risk when considering domestic travel whereas there were no high-risk regions when considering only region of residence. The change in regional representation of disease occurrence indicates the importance of collecting domestic travel information in ongoing surveillance activities.

Trends in Campylobacter incidence in broilers and humans in six European countries, 1997-2007.

The objective of this study was to examine incidences of Campylobacter in broilers and humans, and to describe seasonal variation and long-term trends by comparing longitudinal surveillance data in six Northern European countries (Denmark, Finland, Iceland, Norway, Sweden and the Netherlands). Due to high degree of seasonality and autocorrelation, seasonally adjusted (de-seasonalized) and trend adjusted data (de-trended) were used for comparing incidences within and between the six countries. De-seasonalized time series were obtained by fitting the incidence time series to mean monthly temperature and then removing this effect from the data. Long-term trends were fitted to the de-seasonalized time series. The incidence of Campylobacter colonization in broiler flocks and incidence of campylobacteriosis in humans showed a concordant seasonality for all the countries. There was a strong association between the incidence in both broilers and humans in a given month and the mean temperature of the northern hemisphere in the same month, as well as the preceding month, as shown by the cross-correlations and the chosen Generalized Additive Model. Denmark and Sweden showed a steadily decreasing trend for Campylobacter in broilers and human campylobacteriosis in the period 2001-2007. In Iceland, there was a decreasing trend for campylobacteriosis in humans from 1999 to 2007, whilst the broiler trend for Campylobacter was stable from 2001 to 2004, then falling thereafter. In Norway, the human campylobacteriosis trend showed a steady increase throughout the period. On the other hand, the Norwegian broiler trend for Campylobacter showed a decrease from 2001 until 2004, but was thereafter stable. There was no significant decrease or increase in incidence for human campylobacteriosis in the Netherlands, and the trend for Campylobacter in broilers was close to stable. The seasonality seen in broiler and human closely follows the temperature, and was probably caused, at least partly, by temperature related factors.

Temperature-related risk factors associated with the colonization of broiler-chicken flocks with Campylobacter spp. in Iceland, 2001-2004.

Our objective was to identify temperature-related risk factors associated with the colonization of broiler-chicken flocks with Campylobacter spp. in Iceland, with an underlying assumption that at minimum ambient temperatures, flies (Musca domestica) play a role in the epidemiology and seasonality of Campylobacter. At slaughter, pooled caecal samples were obtained from 792 flocks that hatched between March 15 and September 15 each year from 2001 to 2004, and cultured for Campylobacter. Daily temperature data (average, maximum and minimum temperatures) were obtained from the Icelandic Meteorological Office. We determined the closest weather station to each farm using ArcGIS 9. We then used logistic-regression models (with a random-effects term for farm) to examine associations between flock positivity and temperature-related predictors. The overall prevalence of Campylobacter was 27.4%, and the month with the highest prevalence (54.4%) was August. The final model included cumulative degree-days (CDD) above an average temperature of 4.4 degrees C and the presence of 1 or more days below a maximum temperature of 8.9 degrees C (threshold below which fly activity was expected to be substantially reduced and egg laying was not expected to occur) during the period 2-4 weeks (i.e. days 8-28) before slaughter. Below 79 CDD, the risk of flock Campylobacter colonization was generally low. Between 79 and 139 CDD, the risk increased gradually, but was lower for flocks raised during periods with 1 or more days <8.9 degrees C than flocks raised without days <8.9 degrees C. The risk increased sharply under conditions of high CDD (>139) and when the maximum temperature remained >8.9 degrees C during the period 2-4 weeks before slaughter.

Frequency and enumeration of Campylobacter species from processed broiler carcasses by weep and rinse samples.

Frequency and numbers of Campylobacter spp. were assessed per freshly processed, contaminated broiler carcass. Campylobacter-positive flocks were identified by cecal sample analysis at slaughter. These flocks had been tested as Campylobacter negative at 4.1 +/- 0.9 d prior to slaughter. Levels of contamination were estimated using 2 sampling approaches per carcass: (1) free weep fluids and (2) whole-carcass, 100 mL of distilled water rinses. Estimations of counts were determined by directly plating dilutions of weeps and rinses onto Campy-Cefex agar and incubating the plates at 41.5 degrees C under microaerobic atmosphere. Confirmation was provided by latex agglutination to quantify levels per milliliter of weep and per 100 mL of rinse. Thirty-two slaughter groups ( approximately 20 carcasses per group) were compared from 2003 to 2004. The Campylobacter-positive weep frequency was 84.8%, whereas the frequency for rinse samples was 74.4% (P < 0.001). Enumeration of Campylobacter spp. on positive samples ranged from 0.70 to 6.13 log(10) cfu/mL of weep (geometric mean of 2.84) and from 2.30 to 7.72 log(10) cfu/100 mL of rinse (geometric mean of 4.38). The correlations between weep and rinse were 0.814 with 0.5 mL of rinse and 0.6294 when applying 0.1 mL of rinse The quantitative regression analyses for these 2 corresponding tests were log(10) rinse (for 0.5 mL of inoculum) = 1.1965 log(10) weep + 0.4979, and log(10) rinse (for 0.1 mL of inoculum) = 1.322 log(10) weep - 0.1521. FlaA SVR sequencing of isolates indicated that the same genotypes were found in weep and rinse samples. Weep and rinse sampling led to different proportions of Campylobacter-positive carcasses detection, but we demonstrated that this difference was reduced by increasing the amount of rinse fluid used for plating.

Occurrence of Campylobacter spp. in cecal contents among commercial broilers in iceland.

Campylobacter jejuni remains the most frequently reported bacterial cause of human gastroenteritis in Nordic countries. The primary source of transmission to humans is suggested as mishandled raw poultry or consuming improperly prepared chicken. The focus of this report was to characterize the prevalence and cell numbers of the organism within the commercial Icelandic poultry industry. Commercial broiler flocks were sampled from May 2001 through 2003 in a total population study. At the slaughter plant, 40 randomly selected ceca were obtained from each flock, pooled into four samples containing 10 ceca each, and analyzed. Cell numbers and prevalence of Campylobacter spp. were estimated by direct plating of dilutions onto Campy-Cefex agar and incubating the plates at 42 degrees C under microaerobic atmosphere; colonies were confirmed as Campylobacter spp. by microscopy and latex agglutination to provide quantification of cell numbers per gm of cecal material. A total of 15.4% of the flocks carried the organism at at a maximum cell number of 8.1 x 10(7) cfu/g, having a mean raw count of colonized birds at 1.3 x 10(7) cfu/g (geometric mean of 1.5 x 10(6)). During the 3 years of sampling, the prevalence ranged from 17.6% to 17.3% to 12.7% for slaughter years 2001, 2002, and 2003, respectively. Isolation rates varied with numbers of catch lots (groups of birds taken for slaughter)/flock; with one catch lot/flock, the prevalence was 13.7%, with two 17.5%, and with three 33.3%. With increased flock size, isolation rates also increased; flocks of greater than 5,000 birds had a prevalence of 12.0% positive, 14.0% of flocks with 5,000-10,000 birds were positive, and 25.5% of flocks with more than 10,000 birds were positive for Campylobacter spp. Isolation rates varied with the processing lines: M was positive at 17.3%, B was positive at 10.1%, and G at 17.2%. Flocks were more frequently colonized in the warmer months, and younger birds were less frequently colonized than were older slaughtered birds. This study provides descriptive microbiology pertaining to Iceland broilers in a total population study.

Campylobacter spp. in Icelandic poultry operations and human disease.

We describe the observed relationship of campylobacter in poultry operations to human cases in a closed environment. During 1999 in Iceland, domestic cases of campylobacteriosis reached peak levels at 116/100,000 and in 2000 dropped to 33/100,000. Approximately 62% of broiler carcass rinses were contaminated with Campylobacter spp. in 1999. During 2000, only 15% of the broiler flocks tested Campylobacter spp. positive. In 2000, carcasses from flocks which tested positive on the farms at 4 weeks of age were subsequently frozen prior to distribution. We suggest that public education, enhanced on-farm biological security measures, carcass freezing and other unidentified factors, such as variations in weather, contributed to the large reduction in poultry-borne campylobacteriosis. There is no immediate basis for assigning credit to any specific intervention. We continue to seek additional information to understand the decline in campylobacteriosis and to create a risk assessment model for Campylobacter spp. transmission through this well defined system.