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American Journal of Epidemiology Advance Access originally published online on December 8, 2006
American Journal of Epidemiology 2007 165(4):425-434; doi:10.1093/aje/kwk023
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American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Shiga Toxin-producing Escherichia coli Infection in Germany—Different Risk Factors for Different Age Groups

Dirk Werber1, Susanne C. Behnke1, Angelika Fruth2, Roswitha Merle3, Susanne Menzler4, Sabine Glaser4, Lothar Kreienbrock3,4, Rita Prager2, Helmut Tschäpe2, Peter Roggentin5, Jochen Bockemühl5 and Andrea Ammon1

1 Department of Infectious Disease Epidemiology, Robert Koch Institute, Berlin, Germany
2 National Reference Center for Salmonella and Other Bacterial Enteric Pathogens, Robert Koch Institute, Wernigerode, Germany
3 World Health Organization Collaborating Center for Research and Training in Veterinary Public Health, University of Veterinary Medicine Hannover, Hannover, Germany
4 Department of Biometry, Epidemiology and Information Processing, University of Veterinary Medicine Hannover, Hannover, Germany
5 National Reference Center for Salmonella and Other Bacterial Enteric Pathogens, Institute for Hygiene and the Environment, Hamburg, Germany

Correspondence to Dr. Dirk Werber, Department of Infectious Disease Epidemiology, Robert Koch Institute, Seestrasse 10, Berlin 13353, Germany (e-mail: werberd{at}rki.de).

Received for publication March 20, 2006. Accepted for publication July 13, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The authors conducted a matched case-control study in Germany to identify risk factors for sporadic illness associated with Shiga toxin-producing Escherichia coli (STEC) infection, regardless of serogroup. From April 2001 through March 2003, cases were prospectively enrolled through a laboratory-based sentinel surveillance system located in 14 of the 16 German federal states. One control was identified per case, matched by age and region. Conditional logistic regression was used in the analysis, which was conducted separately for three age groups (<3 years, 3–9 years, and ≥10 years). The median age of the 202 enrolled cases was 2.5 years (range, 3 months–89 years). Hemolytic uremic syndrome developed in five patients. Non-O157 strains accounted for 85% of the isolated STEC. In children under 3 years of age, having touched a ruminant had the highest odds of disease, and raw milk was the only food identified as a risk factor. In contrast, in persons aged 10 years or older, only food items (i.e., lamb meat, raw spreadable sausages) were significantly associated with illness. In this study, risk factors were age-specific. Direct transmission through food played a lesser role in children under 3 years of age, the population at greatest risk of both acquiring STEC infection and developing hemolytic uremic syndrome.

case-control studies; Escherichia coli O157; hemolytic-uremic syndrome; public health; risk factors; Shiga toxins; zoonoses

Abbreviations: CI, confidence interval; OR, odds ratio; STEC, Shiga toxin-producing Escherichia coli


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Infection with Shiga toxin-producing Escherichia coli (STEC) is the primary cause of hemolytic uremic syndrome in children (1). STEC infection and hemolytic uremic syndrome predominantly occur sporadically, that is, without any apparent link to other cases, and both have their peak incidence in early childhood (1–8). To our knowledge, no study thus far has systematically addressed whether risk factors for sporadic STEC infection in young children differ from those in older persons. Furthermore, all published case-control studies, except one (9), that have investigated risk factors for sporadic STEC infection have been restricted to serogroup O157 (10–17). Nonetheless, the ability of STEC serogroups other than O157 ("non-O157 STEC") to cause diarrhea and hemolytic uremic syndrome has been well documented (7, 18, 19). These strains probably account for a substantial proportion of human STEC infection, even in countries where the diagnostic focus is on STEC O157 (e.g., the United States (20, 21)). In Germany, STEC diagnosis is based on detection of Shiga toxin in stool or identification of a Shiga toxin gene (stx) in plated stool enrichment cultures (22). Approximately 80 percent of serotyped STEC reported in Germany at the federal level, to the Robert Koch Institute, belongs to non-O157 serogroups (23). STEC of serogroup O103 is the most frequently isolated non-O157 serogroup among cases reported to the Robert Koch Institute (23).

We conducted a case-control study of risk factors for sporadic illness associated with STEC infection in Germany, where risk factors were examined separately for different age groups and the majority of cases were infected with non-O157 STEC.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Case ascertainment
Cases were prospectively recruited via a laboratory-based sentinel surveillance system coordinated by the National Reference Center. In this sentinel surveillance system, 45 laboratories located in 14 of the 16 German federal states participated voluntarily. They consented to screen stool specimens for the presence of Shiga toxin according to prespecified criteria, as described elsewhere (19), and to follow a standardized diagnostic procedure (22). In brief, 250 µg of stool suspension was pre-enriched in EHEC-Direktmedium (Heipha, Heidelberg, Germany) for 18 hours at 37°C under aeration on a rotary mixer (160 revolutions/minute). After centrifugation, the supernatant was tested for the presence of Shiga toxin 1 and Shiga toxin 2 with a commercial enzyme immunoassay (Ridascreen; R-Biopharm AG, Darmstadt, Germany). Swabs of positive pre-enriched cultures were sent to the National Reference Center, where presumptive STEC were isolated, confirmed by polymerase chain reaction, and subsequently subtyped.

Case definition and control selection
A case was defined as a non-outbreak-related illness in a person whose plated stool enrichment culture yielded an stx gene, who was recruited in one of the designated 14 German federal states between April 1, 2001 and March 31, 2003, and who reported at least one of the following: abdominal pain, nausea, vomiting, fever, diarrhea, visible blood in stool, or signs of hemolytic uremic syndrome. The latter condition was cross-validated with information from the local health department, since hemolytic uremic syndrome is a notifiable condition in Germany (case definition: at least two of the following—hemolytic anemia, thrombocytopenia with platelet count ≤150,000 cells/mm3, and renal dysfunction). Cases were excluded if the date of symptom onset could not be ascertained (e.g., chronic gastrointestinal problems) or if another enteric infection was confirmed simultaneously. One control was identified for each case and was pair-matched by age (0–2 years, 3–5 years, 6–9 years, 10–18 years, 19–29 years, 30–59 years, and ≥60 years) and telephone exchange (by randomly changing the last two digits of the case's home telephone number). Controls were not enrolled if they reported having had diarrhea during the 10 days prior to the interview. Case-control pairs were excluded from the analysis if the time interval between symptom onset and case interview exceeded 60 days or if the time interval between the case interview and the control interview exceeded 30 days.

Questionnaire
A standard, structured questionnaire was used to collect information from cases and controls on risk factors identified in the literature and on some additional exposures we suspected could be related to STEC infection in Germany. The questionnaire inquired about risk factor information for approximately 100 variables. Exposure history covered food consumption and preparation, direct contact with animals, drinking water sources and water-related recreational activities, occupation, recent travel, and indicators of person-to-person transmission (e.g., preceding diarrhea in a household member). In addition, cases were asked about symptoms and duration of illness, hospitalization, and treatment. Cases were asked about the 10-day period prior to symptom onset and controls about the 10 days preceding the interview. For persons under 18 years of age, information was obtained from consenting parents or guardians.

Local health authorities responsible for case management conducted the interviews. We requested that each consenting case and matched control be interviewed by the same person and in a consistent manner (either by telephone or face-to-face).

Isolate typing
Typing of O and H antigens (serotyping) was performed by agglutination with specific antisera on microtiter plates (24). The sera were produced by the National Reference Center using the reference strains of the World Health Organization Collaborating Reference Laboratory in Copenhagen, Denmark, in accordance with their recommendation. The presence of stx genes and the eaeA gene, encoding for the adherence factor intimin, was determined by polymerase chain reaction, using primers and conditions described elsewhere (25, 26).

Data handling and statistical analysis
Epidemiologic data were validated by means of double data entry and then merged with the microbiologic typing information of the National Reference Center database. SAS, version 8.12 (SAS Institute, Inc., Cary, North Carolina), was used in the statistical analysis.

To reduce both the number of covariates examined and the collinearity among several exposures, we created candidate variables by summarizing several items measured on the questionnaire, on biologic grounds, prior to analysis. For example, the candidate variable "touched a ruminant" comprised the three items "touched a cow/calf," "touched a sheep/lamb," and "touched a goat." Missing values were replaced by a simple imputation method that was based on the prevalence in controls for each variable. An exposure had to be reported by at least six participants to be considered for analysis.

Owing to suspected differences in behavior and consumption patterns among infants, children, and older persons, we examined risk factors separately for three different age groups (<3 years, 3–9 years, and ≥10 years). The groups were chosen according to biologic plausibility and sample size, using cutoffs given by the matching age strata. We constructed multivariable conditional logistic regression models to investigate the relation between sporadic STEC-associated illness and the set of exposure variables. A backward selection procedure using the p values of Wald's test (cutoff value 0.10) was applied. To select variables for the starting set of the modeling, the Robert Koch Institute and the University of Veterinary Medicine Hannover independently ranked candidate variables according to perceived importance. We chose variables that were considered important by both institutes or that had a p value of <0.1 in univariate analysis in at least one age group. Starting sets for the age groups were not entirely identical, because some exposures did not apply for persons of all age groups (e.g., attending child care), and for a few risk factors we used the composite variable (e.g., eating ruminant meat) in one age group and the single covariates of that risk factor (e.g., eating veal or beef, eating lamb) in the other age group. Univariate analysis was conducted by calculating Mantel-Haenszel odds ratios, 95 percent confidence intervals, and the exact p value from McNemar's chi-squared test for each candidate variable.

To estimate the proportion of sporadic STEC-associated illness in Germany that could be ascribed to the risk factors, assuming causality, we estimated the population attributable fraction for each significant risk factor in the final multivariable models (age groups 1 and 3) using methods described by Bruzzi et al. (27).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Case ascertainment
During the study period, the National Reference Center detected stx in the plated stool enrichment cultures (which had not tested positive for another enteric pathogen) of 473 non-outbreak-related patients for whom samples were submitted to a laboratory within the sentinel surveillance system. Eighteen patients (4 percent) did not give their consent, and 83 (17 percent) were not enrolled for other reasons (e.g., the case could not be located, did not speak or understand German sufficiently, or did not meet the case definition). For 170 patients (36 percent), the health department could not enroll a control by means of the given telephone method, did not interview the case or control in time, or declined to participate. Overall, 202 cases from 12 different German federal states were enrolled. The median age was 2.5 years (range, 3 months–89 years), and 101 (50 percent) were female. Cases who were enrolled and those not enrolled were similar with respect to age and gender. Case interviews were conducted a median of 24 days after symptom onset, and control interviews followed case interviews by a median of 3 days.

Microbiologic information on isolated STEC
The isolates identified belonged to 34 different serogroups, with O103 being the most frequently identified O antigen, followed by O157 (table 1). Of the 29 STEC of serogroup O157, 16 had the flagellin antigen H7, 12 were nonmotile (H–), of which one was a sorbitol-fermenting strain, and in one STEC O157 the H antigen was not typeable. Among STEC with complete laboratory information (n = 195), the eaeA gene was found in 118 (84 percent) STEC isolated from cases aged 9 years or less, as compared with 12 (23 percent) STEC isolated from cases aged 10 years or more (chi-squared test: p < 0.001). The eaeA gene was also detected in 100 percent of five of the most important STEC serogroups (i.e., O157, O145, O111, O103, and O26) but only in 28 percent of the remaining isolates (chi-squared test: p < 0.001; table 1). Consequently, among STEC with complete laboratory information (n = 195), these serogroups comprised 69 percent (n = 97) of isolates from patients aged 9 years or less, as compared with 15 percent (n = 8) of isolates from patients aged 10 years or more (chi-squared test: p < 0.001).


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  		TABLE 1. Frequencies of different serogroups isolated from cases in a case-control study of Shiga toxin-producing Escherichia coli infection, by age group, Germany, 2001–2003

 
Clinical symptoms
The median duration of (any of the) self-reported symptoms was 10 days. Symptoms ranged from mild, nondiarrheal complaints to reports compatible with hemolytic uremic syndrome. Over all age strata, cases infected by STEC O157 more commonly reported bloody diarrhea (34 percent) or hemolytic uremic syndrome (10 percent) than cases whose stool culture yielded a non-O157 STEC (10 percent and 1 percent, respectively) (table 2).


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  		TABLE 2. Severity of symptoms reported by cases in a case-control study of Shiga toxin-producing Escherichia coli infection, according to the presence of serogroup O157, Germany, 2001–2003

 
Risk factors for sporadic illness associated with STEC infection
Children under 3 years of age (101 case-control pairs).
In the final model (see table 3 for starting set of variables), three variables were significantly associated with illness in children under 3 years of age: having touched a ruminant (odds ratio (OR) = 9.3, 95 percent confidence interval (CI): 2.5, 35.3), having played in a sandbox (OR = 2.6, 95 percent CI: 1.2, 5.3), and having consumed raw milk (OR = 6.9, 95 percent CI: 1.0, 47.9) (table 4). Living with a household member who had had diarrhea preceding disease onset in the case or preceding the control interview was associated with illness in univariate analysis but not after multivariable adjustment.


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  		TABLE 3. Exposure frequencies among cases and controls in a case-control study of Shiga toxin-producing Escherichia coli infection, by age group, Germany, 2001–2003

 

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  		TABLE 4. Results of a risk factor analysis for sporadic Shiga toxin-producing Escherichia coli infection based on an imputed data set, Germany, 2001–2003

 
Children aged 3–9 years (44 case-control pairs).
The age group 3–9 years was the smallest in number, and no robust multivariable model could be built. Thus, only single-variable associations were computed. Cases aged 3–9 years were more likely than matched controls to have played in a sandbox (OR = 9.0, 95 percent CI: 1.1, 71.0) and to have swum in locations other than public swimming pools (OR = 3.8, 95 percent CI: 1.0, 13.9) (table 4).

Persons aged 10 years or older (57 case-control pairs).
In the final model, consumption of lamb meat (OR = 14.1, 95 percent CI: 1.5, 137.1) and consumption of any of the raw fermented spreadable sausages (i.e., teewurst, zwiebelmettwurst, or streichmettwurst) (OR = 3.2, 95 percent CI: 1.1, 9.1) were risk factors for illness. Consumption of fruit juice that was self-produced or purchased from a small-scale producer was inversely associated with illness (OR = 0.3, 95 percent CI: 0.1, 1.1), as was being female (OR = 0.2, 95 percent CI: 0.1, 0.8) (table 4).

Although the odds ratios for most risk factors differed substantially across age groups, the consumption of doner kebab, a Turkish fast-food product containing ground ruminant meat, and the consumption of raw minced meat had elevated odds ratios for disease in univariate analysis in all three age groups. However, these variables did not reach statistical significance in the multivariable models.

Population attributable fraction
In children under 3 years of age, the (nonadditive) population attributable fractions for the single risk factors "playing in a sandbox," "touching a ruminant," and "consuming raw milk" were 39.1 percent, 19.6 percent, and 7.6 percent, respectively. The overall population attributable fraction for the model was estimated to be 50.1 percent. For persons aged 10 years or older, the population attributable fraction calculated from the final model was 43.9 percent overall; 19.6 percent of cases were attributed to the consumption of lamb meat, and 28.7 percent to consumption of spreadable sausages.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
To our knowledge, this is the first study to report risk factors for sporadic illness associated with STEC infection in which the majority of the case population was infected by strains of serogroups other than O157. Therefore, these results predominantly reflect the epidemiology of non-O157 STEC in Germany. The main findings can be summarized as follows: First, risk factors differed in the different age groups examined. Direct transmission through food appeared to be the predominant route for sporadic infections in persons aged 10 years or older, but not in children under 3 years of age. Second, ruminants—including goats and sheep—were a principal source of sporadic illness associated with STEC infection. Third, the distribution of STEC serogroups differed between cases aged 10 years or older and cases below that age.

Raw milk was the only food significantly associated with illness in children under 3 years of age. Moreover, it accounted for only a small proportion of cases. This suggests that direct transmission through food plays a lesser role in the population that is at greatest risk of both acquiring STEC infection and developing hemolytic uremic syndrome. Similarly, no food was associated with illness in children aged 3–9 years, although any interpretation of findings for this age group must be cautious because of the limitations posed by the small sample size. These findings may not apply to other populations or to specific serogroups (e.g., O157). Our results are in line with those of recent case-control studies, which identified contact with cattle or the farming environment as a major risk factor for sporadic STEC infection (15–17). In this study, direct contact with ruminants conferred the highest risk of disease in children under 3 years of age. Notably, almost 10 percent of cases in this age group (three times as many as their respective controls) were reported to live on a cattle farm, but this did not quite reach significance. We did not explore contact with farming environments further, and therefore it is likely that we underestimated the portion of disease attributable to zoonotic transmission (15, 28). Diarrhea in a household member in the preceding 4 weeks was of borderline significance in univariate analysis for children under 3 years of age. The long time interval was chosen to capture incidents in which transmission may have been facilitated by household members who had recovered from illness but were still excreting STEC. Because interpersonal transmission of STEC more likely occurs while primary cases are symptomatic, a shorter exposure interval may have led to a stronger association with illness.

Overall, four of the five identified risk factors in this study were related to ruminants, pointing to these animal species as primary sources for sporadic STEC-associated illness in Germany. Raw milk consumption (29–31) and contact with cattle (or their feces) are well-known risk factors (15, 32, 33), although in our study the risk also included contact with small ruminants, namely goats and sheep. Likewise, in recent STEC O157 outbreaks in petting zoos in the United States, which have primarily affected young children, contact with animals either encompassed or was limited to small ruminants (34). Consumption of lamb meat and consumption of raw spreadable sausages have not been identified as risk factors in studies examining exposures associated with STEC illness; they are, however, entirely plausible. A prevalence study in Germany detected STEC in 72 percent of lamb carcasses (35). Raw spreadable sausages are a popular element of German cuisine. In a series of investigations carried out from 1997 through 2002, the Federal Research Center for Nutrition and Food in Germany found evidence of STEC contamination in 41 (1.5 percent) of 2,748 raw spreadable sausages investigated (36). Furthermore, a national cross-sectional survey conducted by the Federal Institute for Consumer Health Protection and Veterinary Medicine (since 2002, the Federal Institute for Risk Assessment) in 1995 found a pH exceeding the recommended upper limit of 5.6 in 25 percent of samples of a particular raw spreadable sausage (mettwurst) (37). This also indicates that the fermentation process, used as a safeguard against pathogens, was incomplete. Therefore, the production processes for at least some of these sausages are unlikely to eliminate STEC, particularly considering that the pathogen has been shown to survive under conditions as acidic as pH 4.0 (38). Importantly, the common critical control point for prevention of foodborne STEC infection—thorough cooking—does not apply, because these raw fermented products are purchased ready to eat.

Playing in a sandbox was identified as a risk factor. Since the variable was associated with illness in both groups that consisted only of children, a spurious association seems unlikely. Recently, a study from the Netherlands found an association between playing in a sandbox and sporadic Salmonella Typhimurium infection in children aged 4–12 years (39). It is conceivable that playing in a sandbox may, at least in part, be a surrogate for unmeasured exposures (e.g., outdoor/environmental contact). This warrants further investigation, particularly since this exposure accounted for the largest proportion of illness among the identified risk factors.

As in another German study (40), isolates carrying the eaeA gene, and thus the serogroups most commonly carrying these genes, were more frequently found in young patients. Provided that the epidemiology differs among serogroups, this serves as a plausible explanation for the identification of different sets of risk factors across age groups. However, similar risk factors (e.g., consumption of raw or undercooked meat products, contact with ruminants) suggesting principally the same source (ruminants) were identified in this study, which encompassed all STEC regardless of serogroup as compared with studies focusing on O157 exclusively. Furthermore, differences in risk factors related to cattle and farm exposure between children and older persons have also been found in a study focusing on a single serogroup—O157 (17). This may suggest that age-related differences do not primarily depend on the serogroup.

In addition to potential biases inherent in case-control methodology (e.g., cases or controls do not represent the source population), this study had limited statistical power. Sample size calculations were largely based on experiences from a small laboratory sentinel study carried out in 1997 (unpublished data). At the time, STEC was not notifiable, and diagnosis for this pathogen was not routinely established in Germany. We attempted to enroll a case population substantially larger in size than the study population. In this light, it may seem contradictory to compromise statistical power by splitting the data set and conducting only age-specific analyses. However, we found substantial heterogeneity with regard to both the estimated odds ratios for the identified risk factors and their exposure frequencies among the examined age groups. This precluded our merging the data into one stratum to analyze risk factors for the entire case population. Considering that controls were closely matched to the cases on age, a risk factor analysis of the whole data set including interaction terms with age would not have enabled us to reveal the effect-measure modification by age. The rather small sample size per group, however, may have prevented us from identifying some of the risk factors. For example, the consumption of doner kebab was associated with elevated risk in all age groups, yet this variable was rejected, albeit late in the selection process, from both models. Furthermore, the sample size did not allow for serogroup-specific analyses. Hence, it remains to be elucidated whether some important serogroups, such as O157, are associated with a different set of risk factors in Germany. Serogroup-specific differences could be described, however, with respect to self-reported symptoms. Persons infected by STEC O157 more frequently reported severe symptoms (i.e., bloody diarrhea or hemolytic uremic syndrome) than persons whose stool cultures yielded a non-O157 STEC. Although this finding was unadjusted for age, this adds to the notion that non-O157 STEC are, on average, less virulent but much more commonly isolated from patients with diarrhea.

We estimate that the three risk factors identified for children under 3 years of age account for 50 percent of sporadic STEC cases occurring in this age group in Germany, indicating a high potential for prevention. Likewise, 44 percent of sporadic cases in persons aged 10 years or older may be attributed to the consumption of lamb meat and raw spreadable sausages. Considering the high incidence of STEC infection and hemolytic uremic syndrome in young children, prevention efforts should prioritize this age group and should emphasize measures intended to minimize the risk of zoonotic transmission (e.g., controlled and supervised contact with animals, the use of hand-washing (41)) and possibly person-to-person spread. In addition, educating the public about sausages containing raw meat and the risks associated with eating them may contribute to illness prevention in Germany.

In this study, risk factors for sporadic STEC-associated illness differed by age group. Assuming that risk behavior, consumption habits, and host susceptibility vary with age, risk factors for other zoonotic enteric pathogens might be age-specific as well.


   ACKNOWLEDGMENTS
 
Financial support was provided by the German Ministry of Education and Research ("Emerging Foodborne Pathogens in Germany" project; grant 01K10202).

The authors are grateful for the insightful comments of Arnold Bosman, Alain Moren, and Roland Salmon.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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