Factors Associated with Increased and Decreased Risk of Campylobacter Infection: A Prospective Case-Control Study in Norway

Georg Kapperud1,2 , Gyrid Espeland3, Erik Wahl4, Anna Walde5, Hallgeir Herikstad3, Stein Gustavsen4, Ingvar Tveit5, Olav Natås6, Lars Bevanger7 and Asbjørn Digranes8

1 Department of Foodborne Infections, Division of Infectious Disease Control, Norwegian Institute of Public Health, Oslo, Norway.
2 Section of Food Hygiene, Department of Microbiology, Pharmacology and Food Hygiene, Norwegian School of Veterinary Science, Oslo, Norway.
3 The Food Control Authority in Midt-Rogaland, Stavanger, Norway.
4 The Food Control Authority, City of Trondheim, Trondheim, Norway.
5 The Food Control Authority in the Bergen Region, Bergen, Norway.
6 Department of Medical Microbiology, Central Hospital of Rogaland, Stavanger, Norway.
7 Laboratory of Medical Microbiology, St. Olavs Hospital HF, University Hospital of Trondheim, Trondheim, Norway.
8 Department of Microbiology and Immunology, Haukeland University Hospital, Bergen, Norway.

Received for publication August 15, 2002; accepted for publication January 23, 2003.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In 1999–2000, a prospective case-control study of sporadic, domestically acquired campylobacteriosis was conducted in three counties in Norway to identify preventable risk factors and potentially protective factors. A total of 212 cases and 422 population controls matched by age, sex, and geographic area were enrolled. In conditional logistic regression analysis, the following factors were found to be independently associated with an increased risk of Campylobacter infection: drinking undisinfected water, eating at barbecues, eating poultry bought raw, having occupational exposure to animals, and eating undercooked pork. The following factors were independently related to a decreased risk: eating mutton, eating raw fruits or berries, and swimming. Results indicated that infection is more likely to occur as a result of cross-contamination from raw poultry products than because of poultry consumption per se. Drinking undisinfected water, reported by 53% of cases, was a leading risk factor in this study. Drinking water may constitute the common reservoir linking infection in humans and animals, including poultry and wild birds. Insight into the ecology of Campylobacter in freshwater ecosystems may be required to understand the epidemiology of campylobacteriosis. The possibility that certain foods confer protection against campylobacteriosis deserves exploration.

Campylobacter; Campylobacter infections; case-control studies; protective agents; risk factors


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Campylobacter jejuni and Campylobacter coli, two closely related bacterial species, are important agents of acute diarrheal illness worldwide (13). In most developed countries, the reported incidence of campylobacteriosis has increased substantially during the past decades, especially since 1990 (46). Campylobacter has exceeded or rivaled Salmonella as the leading cause of bacterial enteric infection in many countries (4). Although the medical consequences of campylobacteriosis are rarely severe (1, 2), the high and rapidly increasing incidence and the capacity of Campylobacter to cause large outbreaks make campylobacteriosis a public health problem of considerable magnitude. In Norway, the incidence recorded by the national surveillance system almost doubled from 1992 to 1997 (7). In the following years, reports of campylobacteriosis rose sharply and reached 2,890 cases (63.9 per 100,000 population) in 2001, a 145 percent increase from 1997. About 50–60 percent of patients have acquired their infection abroad. A parallel increase has been recorded in domestic and imported cases. The reason is unknown.

Although bacteriologic surveys have identified a number of possible sources of infection, there is still much uncertainty about their relative importance. Case-control studies of sporadic cases, including one from southeastern Norway (8), have identified a variety of risk and protective factors (825), but the results are complex and sometimes confusing. This article presents the results of a prospective case-control study conducted in three of Norway’s 19 counties during 1999–2000. The aim was to identify risk factors and potentially protective factors for sporadic, indigenous campylobacteriosis.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cases and controls
The study was conducted from July 1999 through June 2000 in the counties of Rogaland, Hordaland, and Sør-Trøndelag, which, according to the 1999 census, had a total of 1,061,800 inhabitants (24 percent of Norway’s population). Of the counties with a population larger than 250,000, these three were selected because they had the highest incidence of domestically acquired campylobacteriosis in 1998 (7).

We defined a case as a person who 1) was a resident of the study area, 2) had culture-confirmed campylobacteriosis caused by C. jejuni or C. coli, 3) was diagnosed at one of the three medical microbiologic laboratories in the study area during the study period by cultivation of stool specimens on CCDA agar (Oxoid Ltd., Basingstoke, Hampshire, United Kingdom), and 4) had not traveled abroad in the 2 weeks prior to onset of illness. If stool specimens from more than one member of a household yielded Campylobacter spp. or if the case was part of a recognized outbreak (refer to Schmidt and Tirado (5) for a definition), only the first identified case was enrolled. Whenever a case was identified, a letter was mailed to the patient’s physician to request written informed consent from the patient to participate in the study.

Once enrolled, each case was matched by age, sex, and geographic area with controls selected from the Population Registry, a government register of all Norwegian residents. We aimed to enroll two controls per case. This goal was accomplished by selecting four sex-matched persons from the registry who were closest in age to the case and who lived in the same municipality or an adjacent one. The cases and their controls were never more than 5 years apart in age. For children aged 10 years or less, the age difference never exceeded 1 year. Potential controls were mailed information about the investigation and were then sequentially contacted by telephone. Criteria for exclusion of potential controls were 1) a history of diarrhea during the preceding 2 weeks, 2) travel abroad during the previous 2 weeks, or 3) inability to complete the questionnaire. If a person was not eligible for enrollment, or if he or she declined to be interviewed, additional controls were identified and were contacted until at least one control, preferably two, had been enrolled for each case.

Interviews
All eligible cases and their matched controls were mailed a structured questionnaire along with a standard letter in which they were encouraged to answer the questions. For persons under the age of 16 years, a parent was contacted. About 1 week later, the enrollee was telephoned by a trained interviewer who reviewed the answers to the questionnaire on the telephone or made an appointment to do so at a later date. The interviewers were not blinded to the case/control status of the study subjects. In most instances, the same interviewer questioned each case/control set. If an enrollee was under 16 years of age, a parent was interviewed. Cases were interviewed about exposures during the 2-week period before onset of their illness. Cases who could not specify an illness onset date were questioned about the 2 weeks before the first positive stool sample was submitted. The median interval between illness onset (or sample date) and completion of the questionnaire was 27 days (mean, 32 days; range, 8–130). To facilitate recall of exposures, controls were queried about the 2 weeks before the date on which they completed the questionnaire. A median of 41 days elapsed between the patients’ illness onset and the date on which their matched controls answered the queries (mean, 47 days; range, 9–150).

Questionnaires
The questionnaire covered personal, demographic, and socioeconomic data as well as specific exposures, including food and water consumption and contact with animals. For each variable, enrollees were first queried about whether they had been exposed. If the answer was positive, exposure frequency was recorded (e.g., number of days or times exposed or number of meals consumed). Information on the drinking water supply in the households was obtained from the files of the local food control authorities.

Statistical analyses
Univariate analysis of all risk factor variables was conducted in dichotomous as well as continuous format by using the procedure for conditional logistic regression in the computer program Egret (version 2.0; Statistics and Epidemiology Research Corporation, Seattle, Washington). This procedure was also implemented for multivariate analyses. In this paper, the results are reported as matched odds ratios with 95 percent confidence intervals and two-tailed p values.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A total of 212 patients satisfying the case criteria and 422 matched controls were enrolled. The response rate among controls was 87 percent. Two matched controls were enrolled for each case, except for 15 cases who were matched with three controls and 17 cases for whom only one eligible control could be found. Stool samples from 194 (92 percent) of the cases yielded C. jejuni, while the remaining 18 cases were infected with C. coli. Of the 212 cases, 120 (57 percent) were from Rogaland County, 50 (24 percent) were from Sør-Trøndelag County, and 42 (20 percent) were from Hordaland County. The median age of the cases was 22 years (mean, 25 years; range, 0.8–80). Eighty-two (39 percent) were female.

During the study period, the national surveillance system recorded 350 culture-confirmed cases of sporadic campylobacteriosis from the study area in which the patient had no reported history of traveling abroad before the onset of illness. Fifteen cases were not eligible for enrollment because they were part of interfamilial clusters. No recognized outbreaks occurred during the study period. Therefore, 63 percent of all eligible cases were enrolled. The cases recorded by surveillance were similar to the study enrollees with respect to age and sex distribution. The median age was 25 years (mean, 28 years; range, <1–88). Forty-four percent were female. Among cases reported from the study area, Rogaland County accounted for 39 percent, while Sør-Trøndelag County and Hordaland County included 23 and 38 percent, respectively.

Univariate analysis
Poultry consumption
Eating chicken products was not identified as a significant risk. However, eating chicken that was bought raw as opposed to cooked was associated with an increased risk of campylobacteriosis (table 1). Consumption of hens, turkeys, ducks, geese, or minced poultry products was not significantly related to illness, but each of these exposures was reported by fewer than 10 cases (data not shown). When all poultry consumption variables were aggregated, we found that cases had eaten significantly more meals containing poultry products than their controls had (table 2). They had also eaten more poultry items that had been brought into the house raw. The corresponding dichotomous variables were not associated with an increased risk. Preparing raw poultry in the kitchen was identified as a risk factor. However, since the majority of those who prepared raw poultry also ate it (42 of 51), we were unable to determine whether this factor was independently related to infection. Persons who had eaten undercooked poultry did not have an increased risk, but only 10 cases and 12 controls reported such exposure. Likewise, consumption of poultry purchased during visits to neighboring countries was not associated with illness. No significant difference between cases and controls was detected for eating poultry at barbecues.


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TABLE 1. Matched univariate analysis of selected dichotomous risk factors for sporadic indigenous campylobacteriosis, Norway, 1999–2000
 

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TABLE 2. Matched univariate analysis of selected continuous risk factors for sporadic indigenous campylobacteriosis, Norway, 1999–2000*
 
Red meat consumption
Cases were no more likely than controls to report consumption of beef, pork, mutton, or minced meat products, including hamburgers and sausages. However, eating mutton was associated with a reduced risk. Eating undercooked pork was related to an increased risk of infection when analyzed in dichotomous as well as continuous format (tables 1 and 2), while undercooked beef, mutton, or minced meat products were not (data not shown). None of the 10 cases who had eaten undercooked pork was infected with C. coli, the predominant Campylobacter species in pigs (3, 26). Eating undercooked meat of any kind was marginally associated with an increased risk (p = 0.07). Persons preparing raw meat products in the kitchen were not at risk. Tasting or nibbling raw meat while preparing food was not identified as a risk factor. In addition, eating red meat products purchased abroad did not significantly increase the risk of infection, regardless of the type of meat consumed (data not shown).

Contact with animals
Cases were more likely than controls to report contact with farm animals (cattle, pigs, sheep, or poultry) or their feces. When these animal species were analyzed separately, daily contact with cattle, sheep, or poultry was associated with increased risks of infection. Any contacts with these animals, regardless of the number of days, were also related to an increased risk when these variables were analyzed in dichotomous and in continuous format. Persons in contact with pigs were not at risk (data not shown). Living in a household with a dog was not associated with an increased risk, but living in a household with a cat was marginally so (p = 0.07). The number of days in contact with cats was significantly higher for cases. Cases were more likely than their controls to report occupational exposure to animals. Of the 18 cases who mentioned such exposure, 12 worked with cows, seven with sheep, six with poultry, three with pigs, two with dogs, one with goats, and one with caged birds (nine persons reported exposure to more than one animal species). Feeding wild-living birds or having other contacts with wild birds did not increase the risk of infection. However, children playing in an area in which bird droppings were observed were at increased risk.

Drinking water consumption
Drinking undisinfected wa-ter in the 2 weeks prior to onset of illness was associated with an increased risk of infection. Twenty-nine of the 101 cases and 41 of the 149 controls who had drunk undisinfected water had done so directly from a surface water source during outdoor activities such as hiking or camping, and cases had consumed such water significantly more times than their matched controls. The corresponding dichotomous factor did not achieve statistical significance. Cases were more likely than controls to use undisinfected water in their household. Thirty-three of 39 cases who used undisinfected water in the home received water from a private well (for three, values were missing).

Other factors
Eating at barbecues was associated with an increased risk of infection. However, when the individual food items listed on the questionnaire were analyzed separately, no significant difference between cases and controls was identified for any of the nine items, including five red meat products, poultry, fish, or vegetables (data not shown). Persons who lived on a farm were at increased risk of infection. Drinking unpasteurized milk was also a risk factor. Cases were less likely than controls to have eaten raw vegetables and fruits or berries. These factors were associated with a decreased risk when analyzed in dichotomous and in continuous format. Likewise, eating fish significantly reduced the risk of infection. Swimming in the sea, a lake, or a pool was also found to be protective.

Eating outside of the home or eating food prepared by a catering establishment was not identified as a risk factor even when the number of meals consumed was taken into account. Cases and controls did not differ with regard to any of the following factors (data not shown): attending or working in a kindergarten or day-care center; eating snow, sand, or soil; playing in a sandbox; educational level; annual income; time spent with food preparation; frequency of eating out; or recent foreign travel by household members.

In 44 case households and five control households, diarrhea was reported among other household members in the month after the patient became ill (for the cases) or in the month before the questionnaire was completed (for the controls) (odds ratio = 17.5, 95 percent confidence interval: 6.2, 49.5; p < 0.001). In seven case households, Campylobacter was recovered from family members who became ill after the patient did.

Multivariate analysis
Since interpretation of factors associated with reduced risk is uncertain, two multivariate models were fitted, with and without including potentially protective factors (table 3). In both models, the following factors were found to be independently associated with an increased risk of Campylobacter infection: drinking undisinfected water, eating at barbecues, eating poultry bought raw (number of meals consumed), having occupational exposure to animals, and eating undercooked pork. When protective factors were included, the following factors were found to be independently associated with a reduced risk: eating mutton, eating fruits or berries (number of meals), and swimming in the sea, a lake, or a pool (number of times) (model 2). No significant first-order interactions were detected among the factors included in the analysis.


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TABLE 3. Multivariate analysis* of factors associated with increased or decreased risk of sporadic indigenous campylobacteriosis, Norway, 1999–2000
 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Poultry consumption
Most case-control studies of sporadic campylobacteriosis, including the present one, have identified consumption or preparation of poultry as risk factors (815, 17, 1921, 24, 25). The form of poultry found to be a risk, where it was consumed (i.e., at home vs. restaurants), and the relative importance of such consumption has varied. In Norway, poultry consumption has increased steadily over the last 10 years, and raw refrigerated products have become increasingly popular; in previous years, a majority of the products were frozen. While frozen storage has been shown to reduce the number of viable campylobacters (26, 27), Campylobacter survives well throughout the shelf life of fresh poultry products stored at refrigeration temperature in modified and normal atmospheres (28). Increased consumption of fresh poultry may have contributed to the rising incidence of campylobacteriosis in Norway as well as in other countries.

Persons eating undercooked poultry were not at increased risk, a finding in contrast to some other studies (10, 11, 14, 18). Although this observation may be explained by insufficient statistical power, it has been suggested that sporadic campylobacteriosis is more likely to occur because of cross-contamination from raw products than because of consumption per se (21). Our finding that consumption of poultry brought raw into the house was a risk factor, whereas undercooked poultry was not, supports this suggestion. Some studies have demonstrated an association with kitchen hygiene parameters (13, 18); others have failed to do so (8, 21). It is conceivable that study subjects are reluctant to disclose unhygienic behaviors, making such factors difficult to measure (21). However, a more worrying explanation is that kitchen hygiene practices perceived as acceptable are insufficient to prevent low-level cross-contamination, which nevertheless may be sufficient to cause disease (21). Low-level exposure during handling of raw poultry may also be sufficient to cause campylobacteriosis. Our investigation supports results showing that preparing raw poultry, as opposed to eating it, is a risk factor (15), but we could not determine whether this exposure was independently related to risk.

Red meat consumption
Although a number of domestic mammals are carriers of Campylobacter, consumption of red meat products has rarely been identified as a risk factor for campylobacteriosis (8, 18, 25). During the slaughtering process, carcasses may be contaminated as a result of intestinal spillage, but contamination is less common than it is in poultry processing, and the level of contamination is relatively low (29). The number of bacteria is further reduced during chilling and storage of the carcasses. Our observation that eating undercooked pork was associated with infection is in accordance with two Scandinavian case-control studies that found an association between pork consumption and campylobacteriosis (18, 25).

Contact with animals
Our finding that occupational exposure to animals was an independent risk factor is supported by bacteriologic surveys demonstrating intestinal carriage of Campylobacter by several domestic animal species in Norway and other countries (26, 2931). Our study indicates that direct contact with farm animals or their feces may be important in transmitting the infection in rural populations in the study area. This finding is in accordance with case-control studies conducted elsewhere that have identified contacts with domestic animals or pets as risk factors (812, 14, 17, 18, 22, 25). Wild-living birds frequently are healthy carriers of Campylobacter spp. (26, 29, 32). In addition, drinking milk from bottles pecked by birds has been associated with campylobacteriosis (16). In the present study, playing in an area in which bird droppings were observed was more frequently reported by cases than controls.

Drinking water consumption
Domestic animals and wild birds may effectively spread Campylobacter by contaminating surface water sources. Untreated drinking water has been incriminated as the source of infection in sporadic cases as well as outbreaks of campylobacteriosis (3, 6, 8, 9, 11, 12, 14, 18). In many parts of the developed and developing world, undisinfected surface water is frequently used for human consumption and in animal husbandry; thus, drinking water may contribute substantially to the burden of campylobacteriosis in such countries, including Norway. In the present study, drinking undisinfected water, reported by 53 percent of the cases, was independently related to infection. This result is particularly striking considering how closely matched the cases and controls were. Since study enrollees were matched by geographic area, risk factors related to geography, such as drinking water supply, may have been underestimated. In Norway and the United Kingdom, the water supply has also been identified as an important source of Campylobacter in broiler chicken flocks (31, 33).

These results support the suggestion that the waterborne route of infection may be the common underlying pathway linking infection in humans, poultry, other domestic animals, and wild birds (3). Surface waters may be the major reservoir pool from which Campylobacter is distributed to smaller cycling pools that are exchanging rapidly between mammalian and avian host species and between those species and their immediate environment. In areas in which undisinfected surface water is used for human consumption, direct access to the reservoir pool is established, and the incidence of campylobacteriosis is expectedly high. Our understanding of the epidemiology of campylobacteriosis may depend on increased insight into the ecology of Campylobacter in freshwater ecosystems, including the microhabitats and ecologic niches occupied by the bacterium, possible symbiotic relations, and its survival strategies in response to competition and changing environmental factors.

Other risk factors
Barbecuing was identified as a risk factor for campylobacteriosis in earlier case-control studies (8, 18, 20, 25), including one in Norway (8). Barbecuing provides many opportunities for undercooking, recontamination of cooked foods, and cross-contamination of other food items. Unpasteurized milk has been incriminated in outbreaks as well as sporadic cases of campylobacteriosis (11, 12, 14, 23, 25, 26, 29), but this factor was not independently associated with risk in our analysis. Person-to-person transmission appears to be uncommon with Campylobacter infection (3, 29). In our study, diarrheal illness was more commonly reported in members of case households than control households, and, in seven case households, Campylobacter was isolated from other family members who became ill after the patient did. However, it is impossible to determine whether this observation reflects common source coinfection, selective recall of unrelated illness, or transmission within the family.

Factors related to reduced risk
Case-control studies have identified a number of factors associated with reduced risk of Campylobacter infection (9, 11, 17, 18, 21, 23, 24). Such factors include not only markers of good hygienic practice but also consumption of certain food items, contact with animals, and behavioral traits. The broad spectrum of protective foods identified includes poultry, red meat, and dairy products as well as vegetables and fruits. Interpretation of these findings is uncertain, and several explanations have been suggested, including statistical coincidence, bias, confounding, immunity in frequently exposed subpopulations, and causal effect (18, 21). Interestingly, several studies have found that raw vegetables, fruits, or both were more frequently consumed by controls than by cases (11, 18, 23). In addition, our study suggests that swimming and that eating mutton and fish were protective, although fish consumption was not an independent factor. These exposures likely represent dietary behaviors or reflect a healthy lifestyle generally conferring a lower risk of infection, thereby creating spurious protective effects. On the other hand, fruits and vegetables may contain high amounts of antioxidants and carotenoids, some of which have been shown to inhibit the growth of bacteria (34, 35).

Possible causal mechanisms for protection also include the effect of diet and dietary probiotic bacteria on the intestinal microflora (21), stimulation of general immunity to infection mediated by micronutrients (21), the effect of vitamin A to reduce the duration and severity of intestinal infections (36, 37), the inhibitory effect of herbs and spices on the growth of intestinal pathogens (34, 38, 39), stimulation of intestinal motility by dietary fiber, and inhibition of bacterial adherence by sugars and lectins (4042). Thus, the possibility that consumption of certain foods provides genuine protection cannot be rejected and requires exploration.

Limitations of this study
Some caution is needed in interpreting the results. The delay between illness onset and interview may have introduced a recall bias, leading to underestimation of risk factors susceptible to recall problems. Likewise, possible geographic overmatching may have led to underestimation of factors closely associated with geographic area, such as drinking water quality. The interviewers, who were aware of the case/control status of enrollees, may have introduced an additional type of bias. The study was limited to laboratory-diagnosed cases, and the pattern of risk factors and their relative importance may be different among nondiagnosed cases. Finally, the results are not necessarily representative of the whole population of Norway because only three counties were included. In these counties, only 63 percent of all eligible cases were enrolled, and the geographic distribution of the cases differed from that recorded by surveillance during the study period. The results did not explain the marked increase in the incidence of campylobacteriosis in Norway. Although this study identified factors not detected in our previous investigation (8), this difference may have been due to statistical coincidence or different study areas rather than reflecting a trend in the relative importance of risks.

Conclusions
Results indicate that improved drinking water quality, modified kitchen hygiene practices during barbecuing and preparation of poultry, modified animal contact patterns, and a reduced Campylobacter prevalence in poultry offer the potential for a substantial reduction in the burden of indigenous campylobacteriosis in the study area. To understand the complex epidemiology of campylobacteriosis and guide prevention, further studies are needed to 1) identify the failures in kitchen hygiene practices and animal contact patterns sufficient to cause campylobacteriosis; 2) explore the ecology of Campylobacter in freshwater ecosystems; 3) identify factors responsible for the increasing incidence, including the potential emergence of new genetic subtypes; and 4) investigate the possibility that certain foods confer protection.


    NOTES
 
Correspondence to Dr. Georg Kapperud, Department of Foodborne Infections, Division of Infectious Disease Control, Norwegian Institute of Public Health, P.O. Box 4404 Nydalen, N-0403 Oslo, Norway (e-mail: georg.kapperud{at}fhi.no). Back


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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