Listeria monocytogenes Infection in the Over-60s in England Between 2005 and 2008: A Retrospective Case–Control Study Utilizing Market Research Panel Data

Abstract

A retrospective case–control study of listeriosis in patients in England aged over 60 years is described. The incidence of listeriosis in patients aged ≥60 years in England has doubled since 2001; hence, the investigation of risk factors for infection in this group is important to inform on prevention and control. Standardized epidemiological information has been sought on cases since 2005, but the value of the data accrued is limited without some perception of exposure prevalence in the population at risk of listeriosis. The exposures of listeriosis cases aged ≥60 years reported in England from 2005 to 2008 were compared to those of market research panel members representing the same population (i.e., residents of England aged ≥60 years) and time period. Exposures were grouped to facilitate comparison. Odds ratios and 95% confidence intervals were calculated. Cases were more likely than panel members to report the consumption of cooked meats (beef and ham/pork, but not poultry), cooked fish (specifically smoked salmon) and shellfish (prawns), dairy products (most noticeably milk but also certain cheeses), and mixed salads. They were less likely to report the consumption of other forms of seafood, dairy spread, other forms of dairy, sandwiches, and fresh vegetables. The diversity of high-risk food exposures reflects the ubiquity of the microorganism in the environment and/or the susceptibility of those at risk, and suggests that a wider variety of foods can give rise to listeriosis. Food safety advice on avoiding listeriosis should be adapted accordingly. While not inexpensive, the application of market research data to infectious disease epidemiology can add value to routine surveillance data.

Introduction

L isteriosis is a rare but life-threatening foodborne disease caused by the bacterium Listeria monocytogenes. Affecting pregnant women, unborn or newly delivered infants, the elderly, and those with weakened immune systems, listeriosis has recently been estimated to be the commonest cause of food-related deaths in the United Kingdom (Food Standards Agency, 2007), and therefore the investigation of factors that might alter people's risk of infection is important to inform on prevention and control.

The epidemiology of listeriosis has changed in England and Wales since 2001. Disease incidence has nearly doubled (an average of 109 cases per annum from 1990 to 2000, versus an average of 189 cases from 2001 to 2008), and the clinical presentation has also changed, with more infections in people aged 60 years and over who present with bacteremia in the absence of central nervous system involvement (Gillespie et al., 2006). This increase, which cannot be explained by recognized outbreaks, regional differences, age, gender, or a predominant L. monocytogenes subtype, is not thought to be artifactual (Gillespie et al., 2006). Recent research suggests that the increase relates to patients with cancer and, to a lesser extent, those with other conditions whose treatment leads to stomach acid suppression (Gillespie et al., 2009).

A routine standardized surveillance questionnaire for L. monocytogenes infection was developed for use in England (different public health arrangements exist in Wales) and introduced in 2005. While the data accrued have added to our understanding of the epidemiology of this pathogen, the usefulness of these data for informing on risk is limited without some perception of patients' risk behavior in relation to that observed in the population at risk for listeriosis. To maximize the potential of routine surveillance data and to identify high-risk food exposures for L. monocytogenes infection in people aged ≥60 years in England, a retrospective case–control study of L. monocytogenes infection between 2005 and 2008 was undertaken, utilizing commercial market research panel data to provide estimates of exposure prevalence among the general population of the same age group.

Methods

Active national surveillance for listeriosis in England and Wales is coordinated by the Health Protection Agency Centre for Infections. On the basis of the voluntary referral of putative L. monocytogenes isolates for confirmation and subtyping and/or local electronic reporting of cases, standardized clinical (since 1990) and epidemiological (since 2005) data are subsequently sought from hospital microbiologists and public health practitioners, respectively. Epidemiological data are sought on a standard 12-page questionnaire, which captures information on food exposures in the 30 before illness and is completed on average 18 days after onset. These data are not routinely sought where the patient is deceased but is sometimes received. All data are stored in a bespoke Microsoft Access database. For the purposes of surveillance, a case of listeriosis is defined as a person with a clinically compatible illness from whom L. monocytogenes was isolated from a normally sterile site. Cases are classified further as pregnancy-associated (all maternal–fetal patients and neonatal patients, with a mother–baby pair considered a single case-patient) and nonpregnancy-associated cases (illness in patients >1 month of age).

Commercial denominator data representing the population of England from 2005 to 2008 were obtained from the Worldpanel Usage database from the market research company Taylor Nelson Sofres (London, United Kingdom). Running since 1974 and capturing representative data for the Great Britain population in terms of age and gender, the Taylor Nelson Sofres Worldpanel Usage is a continuous panel of 11,000 individuals in 4200 households. Respondent households complete a 2-week food consumption diary twice a year and the panel is staggered so that each day of the year is represented by approximately 800 individuals. The company was approached to determine the number of fields in the surveillance questionnaire where appropriate panel member data were available, and a grouping procedure was agreed to facilitate comparability and to reduce cost (Table 1). Exposure to each grouped variable for panel members resident in England and aged ≥60 years (N = 18,115) was determined and supplied. It is important to note that these exposure data were not interdependent. Using Table 1 as an example, it was not possible to establish from the data supplied how many of the panel members who consumed processed pork also consumed cold cooked poultry, and so on.

Table 1.

Derivation of the Grouped Exposures from the Health Protection Agency Standard Listeria monocytogenes Surveillance Questionnaire

Grouped exposure	Exposures included
Unheated/ready-to-eat beef	Cold cooked beef, prepacked sliced beef, loose-sold sliced beef, prepacked salt beef, loose-sold salt beef, prepacked pastrami, loose-sold pastrami, potted beef, tongue, brawn, other beef
Unheated/ready-to-eat ham or pork	Cold roast pork, prepacked sliced ham, loose-sold sliced ham, prepacked smoked ham, loose-sold smoked ham, dry cured ham, dry fermented sausages
Processed pork	Frankfurter sausages, sausage rolls, pork pies, Scotch eggs, liver sausage, pork pâté
Other pork	Other pork
Cold cooked poultry	Cold roast chicken, prepacked cooked chicken, prepacked sliced chicken, cold roast turkey, prepacked cooked turkey, prepacked sliced turkey
Processed poultry	Chicken pies, goose liver pate, duck liver pate
Other poultry	Other poultry
Smoked salmon	Smoked salmon
Other cold cooked fish	Mackerel fillets, smoked mackerel, salmon pâté/terrine, smoked trout, fish pate/paste, jellied eels, other cold cooked fish
Prawns	Prawns
Other seafood	Cold seafood, oysters, mussels, squid/calamari, mixed seafood, other seafood
Milk	Pasteurized cows milk, unpasteurized cows milk, sterilized/UHT cows milk, pasteurized goats milk, unpasteurized goats milk, soya milk, powdered milk, flavored milk, other milk
Cream	Cream
Butter	Butter
Dairy spread	Dairy spread
Other dairy	Home-made ice cream, other dairy
Cheddar cheese	Cheddar cheese
Other hard cheese	Other hard cheese
Blue cheese	Blue cheese
Camembert	Camembert
Brie	Brie
Other cheese	Cheese spread, other soft cheese, goats cheese soft goats cheese, other cheese
Top 1 sandwich (cheese)	Hard cheese sandwiches
Top 2 sandwich (ham)	Ham sandwiches
Top 3 sandwich (chicken)	Chicken sandwiches
Top 4 sandwich (bacon)	BLT/other bacon sandwiches
Top 5 sandwich (tuna)	Tuna sandwiches
Other sandwiches	Beef sandwiches, turkey sandwiches, other meat sandwiches, salmon sandwiches, prawn/other seafood sandwiches, egg mayonnaise sandwiches, other egg sandwiches, brie sandwiches, other sandwiches
Fresh vegetables	Bean sprouts, broccoli, cabbage, carrot, cauliflower, courgette, cucumber, lettuce, mush, onion, pepper, radish, spinach, tomato, other fresh vegetables
Mixed salads	Mixed salad, watercress

Data manipulation and statistical analysis were undertaken using Stata version 10 (StataCorp, College Station, TX) and Microsoft Excel 2007 (Microsoft Corp., Redmond, WA), respectively. New variables were created in Stata to represent the grouped exposures as described in Table 1, and frequency tabulations were performed with the output transposed into Excel. The level of exposure to each grouped variable among cases of L. monocytogenes infection aged ≥60 years reported from laboratories in England was compared with the estimated level in the general population of England for the same age group and time period. Odds ratios with accompanying 95% confidence intervals and p-values were calculated. Finally, to assess the potential for confounding between high-risk exposures, a Spearman's rank correlation coefficient matrix, with the significance level of each correlation coefficient, was constructed.

Results

Study population

Between January 1, 2005, and December 31, 2008, 737 human cases of L. monocytogenes infection were reported to the Health Protection Agency Centre for Infections from laboratories in England. Patient age was available for 734 cases (99.6%), and 492 (67%) of these were aged ≥60 years. Those aged <60 years, which included 95 pregnancy-associated cases, were excluded from the analysis. Questionnaires were received for 218/492 of the older cases (response rate 44%), with the response rate increasing significantly over the surveillance period (χ ² for trend p < 0.001; Table 2). Cases for whom surveillance questionnaires were received were similar to all reported cases in terms of patient age (mean 73 years vs. 74 years; t-test p = 0.51) and gender (χ ² p = 0.63), but fewer questionnaires were received where the patient had died (χ ² p < 0.001). Forty-six partially completed and 13 nonstandard questionnaires were excluded, leaving 159 for analysis.

Table 2.

Characteristics of Listeria monocytogenes Cases Aged ≥60 Years with Surveillance Questionnaires Versus Those Without—England, 2005–2008

	Cases (column percentage [unless stated])
Parameter	Surveillance questionnaire received (n = 218)	Others (n = 274)
Year
2005	22 (19)^a	95 (81)^a
2006	31 (26)^a	89 (74)^a
2007	89 (64)^a	49 (36)^a
2008	76 (65)^a	41 (35)^a
Gender
Male	128 (59)	155 (57)
Female	90 (41)	119 (43)
Age group
60–69 years	77 (35)	95 (35)
70–79 years	83 (38)	89 (32)
80 + years	58 (27)	90 (33)
Mortality
Died	68 (31)	120 (44)
Did not die	143 (66)	86 (31)
Unknown	7 (3)	68 (25)

Row percentages.

Patient exposure in relation to the general population

Cases were more likely than the general population to report the consumption of cooked meats (beef and ham/pork, but not poultry), cooked fish (specifically smoked salmon) and shellfish (prawns), dairy products (most noticeably milk but also butter and certain cheeses (hard cheeses other than Cheddar; blue cheese; Camembert; other cheeses), and mixed salads (Table 3). They were less likely to report the consumption of other forms of seafood, dairy spread, other forms of dairy, sandwiches, and fresh vegetables. There was relatively little correlation between the significant risk exposures identified in this study (Table 4). Where significant correlations were observed, they tended to be within food groups (e.g., within the fish exposures and within the cheese exposures) and were not particularly strong.

Table 3.

Food Risk Profile for Cases of Listeria monocytogenes Infection Aged ≥60 Years Reported in England from 2005 to 2008 in Relation to That Observed in the General Population of the Same Age Group

	Exposed (%)
Exposure	Cases ^a	Controls ^b	OR ^c	95% CI ^d	p-Value
Unheated/ready-to-eat beef	60 (38)	4523 (25)	1.82	1.32–2.51	<0.001
Unheated/ready-to-eat ham or pork	94 (59)	11830 (65)	0.77	0.56–1.06	0.103
Processed pork	71 (45)	5254 (29)	2.00	1.46–2.74	<0.001
Other pork	6 (4)	3293 (18)	0.18	0.08–0.41	<0.001
Cold cooked poultry	61 (38)	5741 (32)	1.34	0.97–1.85	0.072
Processed poultry	16 (10)	2031 (11)	0.89	0.53–1.49	0.647
Other poultry	3 (2)	—	—	—	—
Smoked salmon	20 (13)	529 (3)	4.82	2.99–7.76	<0.001
Other cold cooked fish	54 (34)	408 (2)	22.32	15.85–31.44	<0.001
Prawns	30 (19)	2447 (14)	1.50	1.01–2.24	0.045
Other seafood	17 (11)	4650 (26)	0.35	0.21–0.57	<0.001
Milk	149 (94)	12043 (66)	7.51	3.96–14.26	<0.001
Cream	54 (34)	5004 (28)	1.35	0.97–1.87	0.075
Butter	101 (64)	8959 (49)	1.78	1.29–2.46	<0.001
Dairy spread	66 (42)	13202 (73)	0.26	0.19–0.36	<0.001
Other dairy	55 (35)	12955 (72)	0.21	0.15–0.30	<0.001
Cheddar	112 (71)	13513 (75)	0.85	0.60–1.20	0.351
Other hard cheese	54 (35)	3394 (19)	2.37	1.69–3.30	<0.001
Blue cheese	26 (17)	1482 (8)	2.24	1.47–3.43	<0.001
Camembert	8 (5)	206 (1)	4.80	2.32–9.90	<0.001
Brie	10 (7)	874 (5)	1.38	0.72–2.63	0.326
Other cheese	57 (36)	4659 (26)	1.65	1.19–2.28	0.003
Any sandwich	64 (40)	16172 (89)	0.08	0.06–0.11	<0.001
Top 1 sandwich (cheese)	23 (15)	10194 (56)	0.14	0.09–0.21	<0.001
Top 2 sandwich (ham)	27 (18)	8937 (49)	0.22	0.14–0.33	<0.001
Top 3 sandwich (chicken)	15 (10)	2983 (16)	0.55	0.32–0.94	0.027
Top 4 sandwich (bacon)	7 (5)	4333 (24)	0.15	0.07–0.32	<0.001
Top 5 sandwich (tuna)	15 (10)	2478 (14)	0.68	0.40–1.16	0.156
Other sandwiches	34 (22)	7242 (40)	0.42	0.29–0.61	<0.001
Fresh vegetables	120 (78)	17955 (99)	0.03	0.02–0.05	<0.001
Mixed salads	41 (28)	3306 (18)	1.72	1.20–2.47	0.003

Cases of L. monocytogenes infection.

Panel members.

Odds ratios.

95% confidence intervals.

Table 4.

Correlation Index for Exposures Significantly Associated with an Increased Risk of Listeria monocytogenes Infection

	Correlation coefficient
Exposure	Cold cooked beef	Processed pork	Smoked salmon	Other cold cooked fish	Prawns	Milk	Butter	Other hard cheese	Blue cheese	Camem-bert	Other cheese	Mixed salads
Cold cooked beef	1
Processed pork	0.33^a	1
Smoked salmon	0.07	0.05	1
Other cold cooked fish	0.08	0.12	0.22^b	1
Prawns	−0.03	0.07	0.27^b	0.09	1
Milk	0.15	0.13	0.10	0.02	−0.02	1
Butter	−0.05	−0.08	−0.01	0.05	0.08	−0.01	1
Other hard cheese	0.02	0.02	0.10	0.14	0.08	0.07	0.12	1
Blue cheese	0.02	0.03	0.16	0.08	0.07	0.11	0.04	0.05	1
Camembert	−0.02	0.08	0.14	0.13	−0.01	0.06	0.15	0.07	0.11	1
Other cheese	0.03	0.05	0.09	0.14	0.14	0.01	−0.16^c	0.26^b	−0.05	−0.04	1
Mixed salads	−0.07	−0.02	0.10	0.21^b	0.02	−0.03	0.13	0.17^c	0.06	0.15	0.29^a	1

p < 0.001.

0.001 > p < 0.01.

0.01 > p < 0.05.

Discussion

We compared the food consumption patterns of older cases of laboratory-confirmed L. monocytogenes infection to members of the general population of the same age group, as estimated from market research panel data, in an attempt to establish which exposures might increase the risk of infection. To our knowledge this is the first time that market research data have been applied to infectious disease epidemiology in this way. Several factors should be considered while interpreting our findings.

First, laboratory surveillance represents the more severe end of the infectious intestinal disease spectrum, and our standardized surveillance dataset includes proportionally fewer data for patients who died. It is possible, therefore, that certain exposures will be underrepresented in our surveillance dataset if those exposures lead to a very mild or severe disease [e.g., foods containing extremely low/high concentrations of L. monocytogenes, or less/more pathogenic subtypes (Jacquet et al., 2004)]. To date, studies of L. monocytogenes mortality (McLauchlin, 1990; Goulet et al., 1996; Gerner-Smidt et al., 2005) have focused on host factors in relation to mortality rather than patients' exposures, and therefore it is not possible to quantify this form of bias.

Second, controls in case–control studies provide an estimate of the exposure prevalence that would be observed in cases if there were no association between that exposure and disease. To ensure the accuracy of these estimates, controls should best represent the population at risk from which the cases arose. The population at risk of listeriosis in England is not the same as the population of England, in that patients with listeriosis are often individuals predisposed to opportunistic infections due to suppression of their T-cell-mediated immunity (Farber and Peterkin, 1991). These conditions and/or their treatments might alter individuals' risk perceptions and consequently their behavior, including their food consumption patterns, especially if patients have received specific food safety advice upon diagnosis of their conditions or the commencement of treatment. Theoretically, therefore, significant exposure differences between cases and panel members in this study cannot be considered risk factors for infection in the classical sense. Alternatively, the aged general population in England will contain large numbers of individuals predisposed to infection with L. monocytogenes due to underlying conditions, and therefore the general population will share some of the host-specific risk characteristics of the aged population at risk of listeriosis. Further, not all predisposing conditions will be perceived by clinicians as increasing the risk of listeriosis and consequently food safety advice may not be given, any advice given might not cover the wide variety of foods known to be contaminated with L. monocytogenes, or the patient might choose to ignore any advice received. In their investigation of a milk-borne outbreak of listeriosis in Massachusetts, Fleming et al. (1985) identified successfully the vehicle of infection in two separate case–control studies utilizing community-matched and underlying condition-matched controls respectively, suggesting that the general population can provide accurate exposure prevalence estimates for the population at risk of listeriosis. In practice, therefore, it is possible that some of the exposure differences between cases and the general population identified in this study will genuinely represent increasing risk.

Third, individuals participating in surveys of any kind will differ systematically from the general population by their willingness to participate. This bias, which might be more profound for market research surveys where participation is often financially motivated, will have a bearing on our findings. Market research data are, however, used extensively by many business sectors and there is economic pressure on market research companies for their study participants to be as representative as possible and considerable resources are committed to ensuring this. The denominator data used in this study match closely the Great Britain population with regard to age and gender; therefore, it is not unreasonable to expect that this group will provide relatively accurate estimates of exposure prevalence for the whole of England. Further, traditional control selection can be problematic and can introduce other forms of bias (McCarthy and Giesecke, 1999).

Fourth, patients were asked retrospectively about food exposures in the 30 days before onset and these data were often captured some time afterward. Conversely, panel members' food consumption patterns were captured prospectively over a 2-week period. These difference in exposure periods and collection methods could enhance recall bias if cases are more likely to recall favorably certain exposures, either because they represented the norm in terms of their consumption patterns or because they occurred closer to the point of illness. It was also possible for more than one panel member to reside in the same household, or for panel members' histories to be included more than once. While it would not be unreasonable to include more than one control from a household in a traditional case–control study, this potential lack of independence in panel members' eating habits could affect our risk estimates. Information on the number of panel members who shared the same residence was unavailable, however.

Finally, by using grouped market research data in this study it is possible that true risk factors for infection could have been obscured if grouped with protective factors, although the likelihood of this occurring was reduced by the grouping employed (all the meat exposures together, all the fish exposures together, etc.). Similarly, we were unable to perform simple stratified analysis to examine confounding between variables, let alone complex multiple variable analysis, and therefore some high-risk exposures may represent uncontrolled confounding. For a factor to be considered a confounder, however, it must be associated with the exposure under investigation and be independently associated with the outcome of interest, and there were relatively few correlations between the high-risk exposures identified in this study. Future work could address the issue of confounding by making use of individual-level market research denominator data matched to cases by age, gender, geography, and season, but this was prohibitively expensive for the current unfunded study.

The diversity of high-risk exposures identified in this study reflects the ubiquity of the bacterium in the environment, the susceptibility of those at risk (Gillespie et al., 2009), both, or uncontrolled confounding as described above. Several of the foods identified have been implicated in outbreaks of human listeriosis or are known to be intermittently contaminated with this bacterium (Table 5), although normally at levels within legal limits (i.e., ≤100 cfu/g) (EC, 2005). U.K. food safety advice on avoiding listeriosis, which is delivered passively and targeted preferentially at pregnant women (Food Standards Agency, 2009a), recommends the avoidance of mold-ripened soft cheeses, soft blue cheeses, all types of pâté (including vegetable pâté), undercooked ready meals, and raw/cold cooked shellfish. The recommendation that hard cheeses, cold meats, and smoked fish are safe (Food Standards Agency, 2009b) may need to be reviewed in light of this study, which adds to the epidemiological and microbiological evidence described above.

Table 5.

Evidence from the Peer-Reviewed Literature in Support of the High-Risk Foods Identified in This Study

High-risk exposure	Implicated in outbreaks of human listeriosis	Intermittent contamination with L. monocytogenes
Cooked beef	Sim et al. (2002)	Little et al. (2009)
Processed pork	De Valk et al. (2001), Goulet et al. (1998), Sim et al. (2002)	Little et al. (2009)
Smoked fish	Ericsson et al. (1997), Miettinen et al. (1999)	Food Standards Agency (2008)
Prawns	Riedo et al. (1994)	Valdimarsson et al. (1998)
Milk	CDC (2008), Dalton et al. (1997), Fleming et al. (1985)	Greenwood et al. (1991)
Butter	Lyytikainen et al. (2000)	Lewis et al. (2006)
Cheese	Bille (1990), Bille et al. (2006), Bula et al. (1995), Carrique-Mas et al. (2003), Gaulin et al. (2003), Goulet et al. (1995), Linnan et al. (1988), MacDonald et al. (2005), Makino et al. (2005)	Little et al. (2008), Little et al. (2009)
Mixed salads	Aureli et al. (2000)	Little et al. (2007)

Conclusions

The incidence of listeriosis in England and Wales is highest in older age groups and listeria-associated mortality increases with age (Gillespie et al., 2006). There is therefore a clear public health imperative to provide elderly people with the information and advice they require to reduce their risk of becoming infected. To do this, it is vital to utilize all relevant data sources and develop epidemiological approaches that can help identify high-risk exposures that might contribute to the burden of listeriosis in the elderly. Such information can provide important evidence to inform research priorities and the development of interventions and policy. It is within this context that we have sought to explore the potential for using market research data, in conjunction with surveillance data, to produce information for action. Our findings clearly suggest that a wide range of foods give rise to listeriosis in older people, highlighting the need for specific food safety advice for this growing sector of society and questioning whether the current EC legislative limits for L. monocytogenes in ready-to-eat foods (EC, 2005) provide an appropriate level of protection to this group of consumers. The potential benefits of acquiring and using commercially available market research panel data are also highlighted. While not inexpensive, these are important resources that can add value to routine surveillance data.

Footnotes

Acknowledgements

We gratefully acknowledge the continued contribution of local public health, environmental health, and hospital microbiology staff to this surveillance system.

Disclosure Statement

No competing financial interests exist.

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