Incidence trend and risk factors for campylobacterinfections in humans in Norway

The reported incidence of human campylobacteriosis in Norway increased steadily, like in many other countries during the 90's and reached a maximum of 2890 cases in 2001 (64 reported cases per 100,000 inhabitants in 2001 [1, 2]). The proportion of domestically acquired cases has been stable at about 40–50%. A few outbreaks have been reported, however the majority of Campylobacter infections seem to be sporadic as has also been observed in other developed countries [3, 4].

Campylobacter jejuni ssp. jejuni (C. jejuni) is the most frequently isolated Campylobacter from humans with campylobacteriosis in Norway (personal communication, Kapperud, Georg the National Reference Laboratory, Norwegian Institute for Public Health) as observed in other developed countries [3]. However, the exact distribution of species in the reported human cases remains to be revealed and there are indications of that other species also can be important in some countries and in some age groups [5].

Case control studies and epidemiological surveys have identified risk factors for Campylobacter infections in humans, the most frequently revealed being untreated drinking water, consumption of broiler meat bought raw, raw milk, contact with cats and dogs and other animals and eating other types of meat at barbecue [6–12]. The risk connected to "consumption of broiler meat bought raw" might imply inadequate cooking of the meat or more likely; cross contamination in the kitchen to products that are not cooked before being eaten.

A rather high seasonal prevalence of Campylobacter in some surface water sources used as drinking water in Norway were found in the survey by Brennhovd et al. [13] and is also found elsewhere [14, 15]. Most of the water works in Norway apply sanitation before releasing the drinking water into the net work. In some geographical areas however, there are still a high number of private water sources often localised on farms and also in houses for recreation purposes, (an aspect of the lifestyle which is common in Norway).

Case-control studies, analysis of some outbreak and comparison of strains isolated from various sources with those causing infections in humans have provided evidence that poultry represent an important risk factor [3, 4, 6–11, 16, 17]. The official import of chicken in Norway is negligible, but an unknown volume is imported through travelling and illegal import may be substantial in some areas. Because of the increased sale and consumption of fresh chicken (61% increase from 1995 to 2000), transmission of Campylobacter from raw or insufficient heat-treated broiler meat has been the main theory explaining the increased incidence of domestically acquired infections since 1995. However, no substantial evidence supporting this theory has been provided so far [18].

Although many studies of risk factors for campylobacteriosis in humans have been conducted world wide, there are still uncertainties related to the relative importance of the probable causal factors. As most case control studies have been matched on geography, identifying risk-factors associated with geographical location has not been possible. In regard to geographical differences in the number of sporadic and outbreak related cases, the modelling of human exposure to Campylobacter taking geographical areas into account can supplement traditional case-control studies and help identify risk factors of geographical origin.

Climatic variables have very often a specific geographical pattern. The association between rainfall and the incidence of Campylobacter infections in humans in different geographical regions in Norway has so far not been examined. Temperature is another variable that could be included in such a model in order to account for the observed north south gradient difference in the reported incidences during the summer season [7, 19].

Ecological studies have featured prominently in environmental epidemiology because exposure has often been measured at the group level, or because limited resources for conducting the study prohibit collection of individual-level data [20].

The objectives of this study were to describe the reported incidence of domestically acquired campylobacteriosis from 1995 to 2001 in Norway, and to investigate whether the increase in incidence was statistically significant when accounting for variations between counties.

Moreover, we wanted to investigate the association between reported domestically acquired human Campylobacter infections in 2000 and 2001 and assumed biological risk factors such as consumption of chicken, proportion of people drinking treated water, density of dogs, cattle, sheep and goats, rainfall, temperature (accounting for the north south gradient in the reported incidence) and whether the population is urban/suburban or rural.

No differences in the culturing of human stool samples for Campylobacter were implemented in the period 1995–2001, the results from the trend model are therefore assumed to fairly represent the real trend (Figure 2).

Similar trends for age and sex as in this dataset were reported in the period 1979 to 1988 [7]. Numbers can, however, not be directly compared between these periods, as changes in the reporting system occurred when the infection became notifiable in 1995. The high number of recorded incidences in some municipalities at the west coast of Norway was partly due to outbreaks during summertime [1]. The number of reported cases is regarded as a highly biased estimate of the true incidence of campylobacteriosis due to a probable major underreporting of cases. Classification of cases in the county where the infection was acquired is biased to some extent in both datasets as a consequence of ignorance about the source of infection.

Treated drinking water came out as a protective factor, however categorisation of the number of people that received disinfected or not disinfected water in the dataset was complicated; the main problem being that some waterworks supplied water from different sources. All the groundwater sources were expected to supply water of high quality [25, 29]. Therefore all the people that received water from groundwater and from the waterworks that had sufficient disinfections of the water to kill Campylobacter were counted as having received treated drinking water. Table 2 shows that in some counties (South Middle, South West and in the Northern part of Norway) only 50% of the inhabitants receive treated drinking water.

Drinking water from waterworks is not always representative of the drinking-water quality received by the consumer. Besides being exposed to drinking water in their home, people could be exposed to untreated water during vacations and week-end trips into forests, mountains and to recreational houses with private water supplies.

A further problem is the network of water pipes being very old in some areas and therefore of poor quality. Events such as pressure drops in the water pipe system can lead to influx of contaminants from the surroundings outside the water pipes. A Norwegian cohort study, where such pressure drops were recorded indicated that there was an association between low-pressure incidents and diarrhoea in humans [30]. Influx of contaminated ground water into the water pipelines due to bad pipe quality and/or low pressure events has also been shown to be a serious problem elsewhere [31, 32].

Unlike the other independent variables, rainfall and temperature were aggregated at a county level which introduces more uncertainty and difficulties in the interpretation of the results. Currently the registration spots for rainfalls are distributed unequally in the different municipalities. As far as the authors are aware, the number of measuring spots is not connected to the size of the municipalities and consequently the resolution of the measurements could be very different from one geographical area to another. An ecological or aggregate study focuses on the comparison of groups rather than individuals. The fact that we do not know the joint distribution of the study factors and the disease incidence within each group, means that an ecological study could lead us into the classic ecological fallacy (i.e. making causal interferences about an individual phenomenon or process when the observations are made at group level (aggregated) [20]. Rainfall is, however, a very plausible explanation for an increased Campylobacter incidence in humans, resulting from the washing-out of Campylobacter contaminated faeces from the soil into the drinking water sources for humans and animals. Even though the result from the multivariable ecological model was not statistically significant for geographical location (counties) (Table 3), there was an association between higher rainfall and the incidence of Campylobacter infections in humans. Generally, more rain falls on the Southwest coast of Norway than in the rest of the country and that was also the case during the study period (Table 2).

A major problem with regard to intervention and control of campylobacteriosis in humans is the high number of potential sources of infection. Since broiler chicken has been regarded as a very important source of infection and also as a possible point of control some countries have implemented Action Plans or similar activities in broiler production [2]. A great step forward with regard to the lowering of the Campylobacter prevalence in Norwegian broiler flocks has taken place from 2001 up to the present time [33, 34]. The number of Campylobacter counts on the carcasses that enters the market has also been reduced by implementing the freezing of the infected carcasses for 3 weeks as a risk-reducing measure in the Norwegian Action Plan against Campylobacter [35].

In addition to food there are also several environmental Campylobacter sources including water, for drinking and recreation, and contact with food production animals and pets, and exposure to soil. How significant the different risk factors for Campylobacter infections are in different countries is hard to evaluate. Surface drinking water supplies seems to be a risk factor for high Campylobacter incidence. Disinfection of drinking water at the water works is, as mentioned earlier not always sufficient, and improvement of the water pipelines or the control of pressure drops are interventions that should be implemented. Modern equipment for control of pressure drops is available on the market [31].

Most of the Campylobacter infections are still regarded as not being a part of an outbreak but sporadic. The relative importance of the different risk factors for sporadic Campylobacter infections is likely to be variable and the importance of them individually will vary over time and space. Effort should therefore be taken to control all the known risk factors for Campylobacter infections in man. There are however, many sources of Campylobacter bacteria from which it seems impossible to control all possible transmission routes i.e. contact with pets and exposure to contaminated soil. Therefore, in order to prevent Campylobacter infections, we conclude that it is very important to maintain a satisfactory overall level of hygiene, especially for children and people with compromised immunological status.

The increase in incidence of campylobacteriosis in humans from 1995 to 2001 was statistically significant from 1998 and thereafter.

Treated water was a protective factor against Campylobacter infections in humans with an IRR of 0.78 per percentage increase in people supplied.

The two-level modelling technique revealed that campylobacteriosis was not clustered in any particular county which for practical purposes indicates that there are not any specific local risk factors for human Campylobacter infections in Norway. This is consistent with the hypothesis that several risk factors are of differing importance at different time for the incidence of sporadic Campylobacter infections.