Background
Campylobacteriosis is the most frequently reported zoonosis in the European Union (EU) and the most common notified bacterial gastrointestinal disease in Germany [
1]. In contrast to other infectious diseases, e.g., salmonellosis, the annual number of notified campylobacteriosis cases has increased in many European countries in recent years [
1]. In the United States,
Campylobacter infection is the second most common cause of bacterial enteritis after salmonellosis
, with 2.4 million cases estimated to occur per year [
2,
3]. Thus, the burden of gastrointestinal disease due to
Campylobacter is substantial.
Several
Campylobacter species are known to be pathogenic to humans [
4], with
Campylobacter jejuni being the leading cause of campylobacteriosis worldwide, followed by
C. coli[
5].
Campylobacter can be transmitted human-to-human by the faecal-oral route. However, zoonotic or foodborne transmission predominates and
Campylobacter is held responsible for a considerable part of foodborne infections [
6].
The bacteria are widespread in the environment and have been detected in various animal reservoirs, for example, poultry, cattle, swine, and dogs [
5]. Prevalence of
Campylobacter is particularly high in chickens; therefore, contact to chickens and consumption of chicken meat are regarded as important risk factors for campylobacteriosis [
5,
7,
8]. Although
Campylobacter requires special growth conditions and is not able to multiply in an aerobic atmosphere, the bacteria may survive on food or in the environment for several days [
9,
10]. Additionally, the infective dose for humans is very low [
11].
The incubation period typically varies from one to seven days before diarrhoea, abdominal cramps and fever may occur as the most common symptoms [
4]. The disease is self-limiting and symptoms typically disappear within one to three weeks. Reactive arthritis and the Guillain–Barré syndrome are rarely observed sequelae of a
Campylobacter infection [
12].
The aim of this report is to describe demographic and geographic determinants and trends of campylobacteriosis in Germany from 2001 through 2010 in order to identify possible starting points for appropriate countermeasures and to provide a basis for disease management decisions.
Methods
According to the Protection against Infection Act that has been in effect in Germany since 2001, direct or indirect detection of enteropathogenic Campylobacter is notifiable, if indicating an acute infection in humans. Primary diagnostic laboratories are obligated to inform the responsible local health department in the district where the patient resides. Anonymised notification data are electronically forwarded by the local health department via the state health department to the Robert Koch Institute (RKI), the federal public health institute.
We analysed the national surveillance data on notified Campylobacter infections from 2001 through 2010. Only cases fulfilling the reference definition were included in data analysis, which comprises cases with at least one clinical symptom of campylobacteriosis (diarrhoea, abdominal pain, fever) and with either a laboratory confirmed Campylobacter infection or an epidemiological confirmation, which includes a link to a laboratory-confirmed case or to a contaminated food item.
Routine surveillance data include information on age, sex, district of place of residence, date of disease onset, country/district of exposure, hospitalisation (admittance to hospital) and the detected
Campylobacter species. We counted only hospitalisations with a disease onset before the hospitalisation date so that solely hospitalisations due to a campylobacteriosis were included in the analysis. These data are available through the national level database (SurvNet) at the RKI. Data are publically accessible via SurvStat@RKI (
http://www3.rki.de/SurvStat/). Population data provided by the Federal Statistical Office have been used for calculation of campylobacteriosis incidence. Urban and rural regions were classified according to the criteria proposed by the Federal Institute for Research on Building, Urban Affairs and Spatial Development (German: Bundesinstitut für Bau-, Stadt- und Raumforschung [BBSR]). Cities with more than 100,000 inhabitants and districts with more than 150 inhabitants per km
2 were defined as urban. Accordingly, cities with less than 100,000 inhabitants and districts with less than 150 inhabitants per km
2 were classified as rural [
13]. A variable termed “geographic setting” was formed with the two categories urban and rural.
Data analysis was conducted with Microsoft Excel 2010, and geographic maps were prepared with Regiograph version 11 (GfK GeoMarketing GmbH, Bruchsal, Germany). Statistical calculations were performed with Stata 12 (Stata Corporation, College Station, TX; USA). Poisson regression analysis with offset equal to the population size was conducted to estimate incidence and associated 95% confidence intervals (CI) and for group comparisons. P values <0.05 were considered statistically significant.
Discussion
German surveillance data on campylobacteriosis were analysed for a ten-year period from 2001 through 2010. The incidence of Campylobacter infections in Germany was high with a mean annual incidence of 72/100,000 population. The overall increase over the observed time period was mainly due to a rise of domestically acquired cases.
The disease burden of bacterial enteritis due to
Campylobacter is substantial in many European countries. In he EU, campylobacteriosis is the most commonly reported zoonosis with
C. jejuni accounting for most of the confirmed cases [
1,
2]. An upward trend of the incidence of
Campylobacter infections in the EU has been observed since 2005. The incidence in Germany exceeds the European average incidence of
Campylobacter infections (80/100,000 vs. 49/100,000 in 2010). However, the incidence of campylobacteriosis varies widely among the reporting EU countries, most likely due to different surveillance and health care systems. Also, differences in
Campylobacter related risk factors, e.g. diet patterns, contamination levels of different food items, or climatic factors, may play a role [
14]. Sero-epidemiological studies indicate that under-ascertainment of
Campylobacter infections is likely [
15‐
17]. Analysis of routine surveillance data is mainly limited by under-ascertainment and under-reporting. Notified cases may not be representative of all
Campylobacter infections in the population because diseased persons, especially those with mild infections, do not necessarily seek medical care and, in addition physicians do not always order stool analysis from patients with diarrheal diseases. Both are prerequisites for notification. Furthermore, diagnosed infections may not always be reported to the health authorities despite being mandatory by law.
Campylobacteriosis is assumed to be mainly a food-borne disease and the consumption of poultry is one major risk factor [
5,
7,
8]. In contrast to the consumption of pork or beef, the annual consumption of poultry increased from 1996 to 2006 in Germany (from 8.4 to 9.9 kg per capita) [
18]. This may partly explain the increase in the incidence of
Campylobacter infections in Germany, as poultry is frequently contaminated with
Campylobacter. Routine monitoring of zoonotic pathogens in food and farmed animals in Germany revealed that the prevalence of
Campylobacter in poultry meat ranged from 14% to 34% per year. In contrast, contamination of beef and pork with
Campylobacter was markedly lower [
1,
19]. The prevalence of
Campylobacter in chickens ranged from 6% to 64% per year [
1,
19]. However, a distinct trend in the annual prevalence of
Campylobacter in poulty meat and in chickens was not observed for the years 2001–2010. In contrast to
Campylobacter infections, the number of human infections due to
Salmonella enterica serovar Enteritidis has decreased in recent years, which is mainly attributed to successful
Salmonella control programmes in poultry including immunisation [
1,
19]. To date, programmes to control
Campylobacter in poultry have not been implemented successfully.
In Germany, incidence of campylobacteriosis was particularly high in the years 2002, 2005 and 2007. Several explanations are possible. The low number of
Campylobacter cases reported in 2001 may reflect an artefact of reporting because the Protection against Infection Act was newly introduced that year and the surveillance system was still in its infancy. In 2002, the surveillance system was fully established resulting in a higher number of notified cases. In 2004, diagnostic criteria for the campylobacteriosis case definition for notifications were modified to include EIA and enzyme-linked immunosorbent assays (ELISA) [
20]. Using these antigenic tests, non-culturable bacteria can be detected as well. Thus, the enhanced use of these test systems most likely resulted in the strong increase in notified cases in 2005. Various possible reasons have been discussed for the elevated case numbers in 2007 [
20]. For instance, the prevalence of
Campylobacter in routinely tested chickens and chicken herds was higher in 2007 and the prevalence of
Campylobacter in poultry and chicken meat was increased in this year compared to previous years [
21]. Furthermore, warm weather in the spring of 2007 may have triggered recreational activities with enhanced exposure to possible risk factors, for example consumption of undercooked meat at barbecues [
8], or swimming in contaminated water bodies [
7].
A correlation between temperature and number of campylobacteriosis cases has been described before and may also explain the seasonal pattern of the disease with an incidence peak in the summer months, which has been described for many countries [
22,
23]. In Germany,
Campylobacter incidence peaks both in rural as well as urban areas in the summer. Such a seasonal pattern is also characteristic for other zoonotic enteric diseases of bacterial origin, e.g., salmonellosis
, indicating similar transmission routes [
1,
22]. Contamination of broilers and chicken meat with
Campylobacter tends to be higher in the summer months. The contamination rate of
Campylobacter in broilers was found to be highest in August [
24]. Chicken legs at retail examined during a one-year study in Germany showed two peaks of contamination, one from February to March and the second from July to August [
25].
Interestingly, in addition to the incidence peak in the summer months, we observed a second, smaller incidence peak of campylobacteriosis in January. This peak was not due to a reporting delay over the Christmas and New Year’s holidays but was caused by an increase of infections with disease onset in the early days of January, which may indicate exposure of patients to Campylobacter-contaminated food items at the end of the previous year, possibly on New Year’s eve. Further studies would have to be conducted to elucidate this incidence increase.
In Germany as well as in the EU, incidence was highest among children under four years of age and, in particular, one-year-old boys were affected. This is in line with the epidemiology of other gastrointestinal infectious diseases showing a comparable demographic pattern, e.g., infections with
Yersinia enterocolitica,
Salmonella spp., and Shiga toxin-producing
Escherichia coli (STEC) with peak incidence in young children [
26‐
28]. The immune response in infants has not fully established, which may explain their susceptibility to various infectious diseases. However, other age-specific risk factors, like e.g. insufficient hand hygiene or close contact to animals or to the environment, may also play a role.
A high incidence of campylobacteriosis was also found in adults aged 20–29 years in Germany. Interestingly, women were more frequently affected than men in this age group in contrast to all other age groups, in which men were more frequently infected. This age and gender distribution has also been reported for other countries (England, Wales, and the Netherlands) [
15,
29]. Possible reasons may be a higher risk of exposure in women of this age group due to human-to-human transmission from young children they take care of or because they prepare and eat chicken more frequently than men of this age group, possibly resulting in
Campylobacter infections if food items are not sufficiently heated or cross-contaminated.
The German surveillance data show that children living in rural regions were more frequently affected by
Campylobacter infections than children living in urban areas. In contrast, this effect was not observed or even reversed in older persons (Figure
4). Our result is consistent with a study conducted in the German federal state of Hesse from 2005–2006 [
30] that examined the association between age-specific
Campylobacter incidence and the degree of urbanicity of the district of the place of residence also showing an increased incidence in children living in rural areas. This has also been demonstrated by other studies in Europe [
23,
31]. It is conceivable that children in rural areas may be more exposed to farm animals, including chickens, and to other possible sources of
Campylobacter (e.g., contaminated water, wild birds) than children living in urban areas [
8].
Competing interests
The authors declare that they have no competing interests.