Challenges in Listeriosis Cluster and Outbreak Investigations,Province of Quebec,1997

Abstract

Objectives:

Public health authorities place a high priority on investigating listeriosis outbreaks, and these epidemiological investigations remain challenging. Some approaches have been described in the literature to address these challenges. This review of listeriosis clusters and outbreaks investigated in the Province of Quebec (Quebec) highlights investigative approaches that contributed to identifying the source of these outbreaks.

Materials:

The Laboratoire de Santé Publique du Québec (LSPQ) implemented pulsed-field gel electrophoresis (PFGE) molecular subtyping in 1997 to identify Listeria monocytogenes clusters among isolates from invasive listeriosis cases identified throughout Quebec. A cluster was defined as three cases or more with the same or similar PFGE profiles (≤3 band difference) occurring over a 4-month period. An investigation was initiated if the epidemiologic indicators suggested a common source. Listeriosis data from LSPQ's database were reviewed to identify and describe clusters detected from 1997 to 2011, including those that led to an outbreak investigation. Epidemiological reports prepared following each outbreak were also reviewed.

Results:

Eleven clusters were identified in the province by LSPQ between 1997 and 2011. Outbreak investigations were initiated for six clusters, four of which involved more than 10 cases. Factors that contributed to identifying the source for three of these outbreaks highlighted the value of (1) making all stakeholders (food safety and inspection services, public health authorities, and laboratories) aware of any ongoing investigation and sharing relevant information even if the source is not yet identified; (2) promptly collecting food samples identified and considered as possible vehicles of infection identified during the interview of a Listeria case; (3) collecting food items and/or environmental samples in locations reported in common by cases in the same cluster.

Conclusions:

Multiple approaches should be considered when investigating L. monocytogenes clusters. Networks to facilitate continuous exchange of human and food data between public health and food safety partners should be encouraged.

Introduction

L isteria monocytogenes (Lm) infection was recognized as a foodborne illness in the 1980s (Schlech et al., 1983). Older adults, persons with immunocompromising conditions, and pregnant women are at higher risk of Listeria bacteremia and meningitis, which can be fatal (CDC, 2013). Because of the severity of the disease, public health authorities (PHAs) place a high priority on investigating and ending a listeriosis outbreak (Todd et al., 2011). The key to halting a listeriosis outbreak is rapid identification and removal of the contaminated food vehicle from food distribution channels (Cartwright et al., 2013).

Epidemiological investigations of listeriosis clusters are challenging (Cartwright et al., 2013). The long incubation period for invasive listeriosis can compromise a case's ability to remember key information related to their food consumption and purchase history. This is particularly challenging among elderly cases.

This report summarizes listeriosis clusters and outbreaks investigated in Quebec from 1997 to 2011. The findings highlight the importance of employing multiple strategies across epidemiology, food safety, and laboratory disciplines to identify the source of a listeriosis outbreak.

Materials and Methods

A case of invasive listeriosis was defined as isolation of Lm from a normally sterile site (e.g., blood, cerebrospinal fluid) or from products of conception. A case was considered pregnancy-associated when it occurred in a pregnant woman, a fetus, or an infant ≤31 days old: mother–infant pairs were counted as a single case. A cluster was defined as three or more cases of invasive listeriosis with the same or similar pulsed-field gel electrophoresis (PFGE) profiles (≤3 band difference) occurring over a 4-month period.

Cluster detection at the Laboratoire de Santé Publique du Québec (LSPQ)

The LSPQ implemented PFGE molecular subtyping in 1997 using standardized methods (CDC, 2009a). The PFGE profile was designated with BioNumerics (Applied Maths, Sint-Martens-Latern, Belgium) software and then submitted to PulseNet Canada for national comparisons.

Between 1997 and 2003, Lm isolates collected from invasive cases were sent to the LSPQ for standardized PFGE subtyping on a voluntary basis, with all cases recorded in an electronic database. Only clusters were reported to PHAs. In 2003, listeriosis became a reportable disease by law in Quebec, and regional laboratories were requested to send their isolates to LSPQ for subtyping.

Epidemiological investigations conducted by PHAs

Once a cluster (1997 onwards) or a case (2003 onwards) was reported to PHAs, case patients were interviewed as soon as possible using a provincial extended standardized questionnaire that addressed the following topics: demographics, clinical and laboratory data, and food-consumption history over a period of 4 weeks including a large variety of food products (milk and cheese products, deli meat, smoked fish, vegetables, etc.). Data collected from sporadic cases were not entered in a database. If the epidemiologic indicators (e.g., an increase in the number of cases, the rarity of a strain) suggested a common source, an outbreak investigation was initiated.

Since 2001, all listeriosis outbreaks investigated in Quebec have been summarized in a database. For each outbreak, the following information was documented: outbreak size, duration, geographic distribution of cases, and source identified or not. To conclude whether the source or vehicle was identified, reviewers used metrics developed in the Foodborne Diseases Centers for Outbreak Response Enhancement (Foodcore program) (CDC, 2009b). A vehicle was defined as suspect if it was a known risk factor; some errors in food preparation were identified or a large proportion of cluster-associated cases reported consuming the food item. A vehicle was defined as confirmed if the agent was cultured in the vehicle or the vehicle was statistically implicated by an analytic study. In addition, reports completed following each outbreak were reviewed to identify how the source was or was not identified and difficulties encountered during those outbreak investigations.

Food Inspection Services (FIS) at the Ministère de l'Agriculture, des Pêcheries, et de l'Alimentation du Québec (MAPAQ)

Food safety investigations were conducted during outbreak investigations. Food samples were collected using official Food Inspection Branch procedures (Dupont, 2007; DLEAA, 2008; Pagotto et al., 2010; Pagotto et al., 2011; Roy, 2011; Ramsay, 2012; Waburton, 2012). Samples collected were analyzed using standardized methods at either the Laboratoire d'Expertises d'Analyses Alimentaires (LEAA), MAPAQ's food analysis laboratory, or the Laboratoire des Services d'Inspection des Aliments of Montreal, the City of Montreal's food inspection service laboratory, depending on the specimen's origin (Ramsay, 2012). Samples came from case homes, retailers, plants, or dairy herds. Some food samples were collected at the retail level when food items were not available for analysis from case homes. In these instances, food inspectors visited the establishment where the case had purchased or consumed the food suspected of being contaminated, collected samples of the food items reported by the case (i.e., same product and brand), and collected environmental samples as well.

There was also an annual Listeria surveillance program for provincially distributed food items. As part of routine surveillance activities and within the framework of the annual analytical program, many food items including ready-to-eat foods, vegetables, milk products, etc. were sampled and cultured for Lm. When Lm was identified in a food sample, the isolate was sent to LSPQ for molecular subtyping. At the LSPQ, they compared strains found in clinical and food isolates to determine whether the strains were related. LSPQ, FIS, and PHAs shared this information in a timely manner and adopted measures of control that were relevant to the situation.

Results

Listeriosis cases surveillance

Between 1997 and 2011, a total of 575 cases were reported to PHAs: 158 before listeriosis became reportable in 2003 and 417 after that date. Among all the isolates, 267 different PFGE profiles were identified, and 191 of 267 (71.5%) were only found once (Table 1). Since 2003, the number of sporadic cases (not included in any cluster) varied from 28 to 44 per year (averaging 37 cases per year) (Table 2), and the median incidence rate was 5.6 cases per million people (range: 3.7–11.4).

Table 1.

Description of the Pulsed-Field Gel Electrophoresis (PFGE) Diversity of Listeria monocytogenes Clinical Isolates, Québec, 1997–2011

Characteristics	PFGE
Number of L. monocytogenes cases	575
Number of PFGE profiles	267
Number of PFGE profiles found once	191
Range of frequency of each PFGE profile	1–45
Number of clusters^a identified	11

Cluster was defined as three or more cases with the same or similar PFGE profile (<3 band difference assuring over a 4-month-period).

Source of data: Laboratoire de Santé Publique du Québec.

Table 2.

Listeria monocytogenes, Clusters and Sporadic Cases, Quebec, 2001–2011

	Years
	2001	2002	2003	2004	2005	2006	2007	2008	2009	2010	2011
Characteristics
Number of clusters	1	2	1	0	1	0	1	5	0	1	1
Cluster and associated cases	A (3)	B (17)			D (3)		E (22)^a	E (2)^a		J (3)	K (3)
		C (2)^a	C (5)^a					F (5)^b
								G (3)
								H (3)
								I (36)
Cumulated cluster-associated cases	3	19	5	0	3	0	22	49	0	3	3
% of cases related to a cluster	15%	38%	15%	0	8%	0	37%	58%	0	6%	6%
Sporadic cases	17	31	28	28	32	43	37	36	40	44	44
Total of cases	20	50	33	28	35	43	59	85	40	47	47

Clusters spread out over 2 years.

The Province of Quebec was involved in a national outbreak.

Source of data: Laboratoire de Santé Publique du Québec (LSPQ).

Clusters detected

PFGE subtyping identified 11 clusters from 1997 to 2011 (Table 2). Cases included in each cluster were geographically dispersed. Three clusters involved individuals who resided outside Quebec but for two of the three clusters, these nonresidents were exposed in Quebec. The number of clinical isolates related to clusters overall was 107/575 (18.5%) with variation between years (range by year: 0–58%). Characteristics of each cluster are presented in Table 3. The 11 clusters had 10 different PFGE profiles.

Table 3.

Characteristics of Listeria monocytogenes, Clusters Identified by Pulsed-Field Gel Electrophoresis, Quebec, Canada, 1997–2011 (N=575 Cases)

Clusters	Year of detection	Number of cases included in the cluster	Pregnancy- associated cases	Number of deaths associated with listeriosis	Outbreak investigation	Source or vehicle identified
A	2001	3	0	0	No	Undefined
B	2002	17	5	0	Yes	Unpasteurized cheese
C	2002	7	0	0	Yes	Undefined
D	2005	3	0	0	No	Undefined
E	2007	24	0	7	Yes	Undefined
F	2008	57 (5 in Quebec)	0	23	Yes	Deli meat
G	2008	3	0	0	No	Undefined
H	2008	3	0	0	No	Undefined
I	2008	38 (36 in Quebec)	16	2	Yes	Pasteurized cheese
J	2010	5 (4 in Quebec)	0	0	Yes	Food and environmental samples taken at the restaurant tested positive for the same strain
K	2011	3	0	0	No	Undefined

Five of the 11 clusters involved three cases each (Clusters A, D, G, H, and K). There were no common sources identified for any of these five clusters based on the review of food histories collected from the cases. No other cases were subsequently reported to PHAs for these five clusters and therefore, outbreak investigations were not initiated.

Outbreak investigations

Six of the 11 clusters led to an outbreak investigation (B, C, E, F, I, and J). Four clusters led to major outbreak investigations involving more than 10 cases: one in 2002 (Cluster B), one in 2007 (Cluster E), and two in 2008 (Clusters F and I). These outbreaks are described in the following section.

Cluster B

Cluster B was the first Lm outbreak investigated in Quebec (Gaulin, 2003). The PFGE profile had not been observed prior to this outbreak. Cases clustered in a period of 5 months. There were 17 cases with a mean age of 43 years (range: 0–78 years). Five cases were classified as pregnancy associated. No deaths were associated with this outbreak.

Although investigators used an extended standardized questionnaire including a variety of food exposures, no hypotheses regarding the source were identified. Meanwhile, FIS received complaints from some consumers reporting symptoms of gastroenteritis after eating cheeses from a local producer.

Following those complaints, food inspectors visited the local cheese plant and examined the production process. The plant was producing four types of unpasteurized cheese. The food inspectors collected 56 samples of cheese from 16 batches representing all four types of cheese produced. All of the cheese samples tested positive for the Lm outbreak strain that caused 17 human cases. This plant was not identified by the 17 cases. Finding the outbreak strain in this plant following consumer complaints from individuals with gastroenteritis was a fortuitous discovery. This information was promptly shared between FIS staff who were aware of the ongoing outbreak investigation and PHAs. PHAs subsequently re-interviewed outbreak cases to determine whether they had eaten cheese from the implicated plant. Only nine of 16 (56%) cases with information available recalled having eaten cheese from this plant. In this outbreak, the source was identified because of timely and thorough follow-up of consumer complaints and information exchange between FIS and PHAs.

Cluster C

There were seven cases in Cluster C with a mean age of 65 years (range: 0–87 years). During this investigation, there were difficulties interviewing three of the cases, limiting the number of valid questionnaires and their interpretation. Review of food histories from cases who were available to answer did not suggest a common source. The outbreak was declared over because no other cases were subsequently reported to PHAs.

Cluster E

Between June 2007 and March 2008, an outbreak of 24 listeriosis cases was identified, with a peak of activity between August and November 2007. The PFGE profile observed in this outbreak was first seen in 2004, following which there were approximately two or three cases reported per year. An outbreak investigation was initiated based on an increase in the number of cases reported between June and September 2007. Cases were geographically dispersed. The majority of cases were older than 65 years (mean age: 70 years, range: 46–86 years), and seven cases died. Some cases were interviewed two or more times, and two cases were interviewed directly at home. None of the cases lived in a long-term care facility. No hypotheses regarding the source of the outbreak were generated based on the case interviews.

During food inspection services' routine surveillance activities and within the framework of the annual analytical program, the outbreak strain of Lm was found at four different retailers in the province and in five different food products (vegetables, sausages, smoked meat, cretons, turkey pastrami, and dried sausage). This finding was unusual because this PFGE profile was isolated from an environmental sample only once prior to this outbreak. None of the 24 cases had purchased food items from the retailers that tested positive, nor had they reported eating any food products that tested positive. FIS tried to identify common food products and brands upstream of the retailers that may have also been distributed to retailers where cases purchased food with no success due to the complexities in the food supply chain. In this outbreak, no link between those positive samples and cases were established. After 7 months of investigation and a period of time during which no new cases were identified, the outbreak was declared over.

Cluster F

Between June and December 2008, there was an outbreak of listeriosis involving 57 cases in seven Canadian provinces, including five cases in Québec. It was the first multiprovincial listeriosis outbreak involving Quebec in Canada. The mean age of cases was 75 years (median: 78 years, range: 29–98 years). Twenty-four (42%) of the cases died as a result of their infection.

The first several cases reported as part of the outbreak and two concurrently identified cases of listeriosis for which molecular subtyping was not conducted were residents of long-term care facilities or hospital inpatients (Weatherhill, 2009; HC, 2010). Local public health inspectors in Ontario collected food samples including deli sandwiches at the institutions where cases resided. These and additional deli meat samples collected by the Canadian Food Inspection Agency subsequently tested positive for the outbreak strain of Lm. Detecting clusters of cases living in the same institution enabled focused food sampling in the early stage of this investigation. This, in combination with epidemiological data and the availability of food purchase records at the institution that traced back to one federally registered meat-processing establishment, contributed to the identification of deli meat as the source of this outbreak.

Cluster I

The contaminated plant was identified following a report from a consumer with gastroenteritis after eating cheese made by this plant and purchased from a local cheese producer. FIS visited the plant and collected cheese samples. FIS identified the Lm outbreak strain in several soft washed rind cheeses made by this plant. In total, 15 of 114 (13.2%) cheese samples made by this plant were contaminated by the outbreak strain. This cheese was determined to be the source of the outbreak and extensive cross-contamination at the retail level. The Lm outbreak strain was found among 22 of 74 (29.7%) retailers known to have received the contaminated cheese from the implicated plant. Retailers were located in 11 regions across Quebec, and more than 25 varieties of cheese tested positive for the outbreak strain.

Cluster J

The major Lm outbreak in Quebec in terms of magnitude and public health impact included 38 cases between August and December (Gaulin et al., 2012). The PFGE profile observed in this outbreak was first seen in 2002 and only five cases were reported from 2002 to 2007. In 2008, several cases were reported to PHAs that were tightly clustered in time and geographically dispersed. Sixteen cases were classified as pregnancy-associated cases, with a mean age of 31 years old. The mean age of the remaining 22 cases was 65 years. Each Lm case was reported to PHAs and to the FIS as well. After these notifications, three different cheese brands, identified and consumed by the first three Lm cases, were collected at case homes or from retailers where cases purchased the cheese. All cheese samples tested positive for the Lm outbreak strain. Two of the brands were made with raw milk and were produced by the same cheese producer in Quebec and the remaining brand was made with pasteurized milk by another producer in Quebec. Isolation of the Lm outbreak strain from three different brands and two different producers of cheese and sold by three different retailers made PHAs suspect broad contamination. Information gathered from subsequent Lm cases and by the FIS revealed that many more varieties of cheese were contaminated by the outbreak strain and contaminated cheese had been sold by many retailers throughout Quebec.

Cluster J included five cases. A single restaurant was identified as a common exposure among all cases. FIS visited the restaurant and collected food and environmental samples. Some environmental samples tested positive for the same PFGE profile involved in the cluster. Food handling errors were identified by FIS. The exact source of the contamination was not identified but was suspected to be a food prepared by the restaurant. Investigators hypothesized that the contamination was introduced via a combination of a contaminated ingredient or product used to prepare meals and food handling errors as previously observed (Todd et al., 2011).

To summarize, among the six outbreaks investigated, the source of the contamination was confirmed for three (B, E, and I) and suspected for one (J). Sources were all confirmed or suspected based on microbiological detection of the outbreak strain in food and/or environmental samples.

Discussion

The number of Lm cases in Quebec was relatively stable over the years reviewed and comparable to North American and European countries (Farber et al., 1991; WHO, 2004; Goulet et al., 2008; HC, 2010; Silk et al., 2012). Most of the cases were considered sporadic as observed elsewhere (Ryser et al., 2007). In years when clusters were detected, the proportion of cluster-associated cases rose as high as 58%. The number of cluster-associated cases might be due to the popularity and distribution of implicated food items.

It is important for investigators to record and review details of outbreak investigations to identify risk factors for infection and to devise strategies that facilitate source identification (Luber et al., 2011). Although relatively few outbreaks have been reported in Quebec since 1997, this review demonstrated both challenges in applying some methodological approaches as well as strategies that contributed to identifying outbreak sources.

There were several challenges encountered during the outbreak investigations reviewed. Although sporadic cases of Lm were promptly interviewed using an extended standardized questionnaire, the information obtained was often limited for reasons that are already known: the exposure window is long, compromising cases' ability to recall foods eaten, particularly if the source product is not listed in the questionnaire (Yde et al., 2012); some cases were not available for the interview because they were severely affected or died (Tauxe, 2002; Goulet et al., 2007; Swaminathan et al., 2007; Cartwright et al., 2013). A recent study concluded that the median incubation period of invasive listeriosis differs significantly by the clinical form of the disease. The incubation period for cases involving the central nervous system and bacteremia was shorter (<15 days) than previous estimates for listeriosis in general (Goulet et al., 2013). Consideration should be given to decreasing the window for assessing case exposures from 4 weeks to 15 days for these forms of listeriosis and may improve hypothesis generating based on case interviews.

Analytical approaches such as case–control studies are often used to validate hypotheses in outbreak investigations but were not employed in the outbreaks investigated in Quebec (Gregg, 2008). In two of the outbreaks (Clusters B and E), there were no hypotheses generated during the case interviews because cases had difficulties in remembering food items eaten during the 4-week period prior to illness. Other challenges may be associated with broad contamination. Analytical approaches such as case–control studies are useful when a unique or few sources are suspected. Multiples vehicles of infection may be identified during a listeriosis outbreak as observed in Clusters I, J, and probably in cluster E. Retail environments or restaurants may play an important role in the contamination of foods with Lm (Luber et al., 2011). Food handling errors may lead to a high level of contamination in one or more lots of food (Todd et al., 2011). This phenomenon may not be rare and complicates the use of analytical studies for listeriosis.

There are also some challenges associated with appropriate control selection for listeriosis case–control studies, and case–case studies have been proposed to overcome these. To be comparable to cases, controls need to match cases based on age, pregnancy status, or underlying conditions. Case–case study methodology involves selecting controls from sporadic cases who are diagnosed with listeriosis due to an unrelated strain and who are typically well matched to cases of the outbreak strain on these factors. These methods have been applied with success in previous outbreaks involving other pathogens (McCarthy et al., 1999; Gillespie et al., 2002; Krumkamp et al., 2008; Wilson et al., 2008). The United States Centers for Disease Control and Prevention (CDC) implemented a Listeria initiative in 2004 (CSTE, 2003) followed by Canada in 2010 to facilitate case–case methodology (Morton et al., 2013). This methodology has proven efficient in some recent Lm outbreaks (CDC, 2011a, 2011b). As in case–control studies, case–case studies are used to test hypotheses that are generated during the descriptive phase of the investigation. The absence of a hypothesis may limit its use.

In Quebec, other strategies contributed to identifying outbreak sources. In four of the outbreaks, the suspect or confirmed source was identified by promptly sharing information between PHAs and food safety authorities. The proactive role of food inspectors collecting food samples was critical to identify and confirm the source of some outbreaks and highlights the value of (1) making stakeholders (FIS, PHAs, and laboratory) aware of any ongoing investigation and sharing all information that might be relevant during an investigation (Cluster B); (2) promptly collecting samples of foods identified and considered at risk of Lm contamination during the interview of a listeriosis case (Clusters F and I); and (3) collecting food items and/or environmental samples from locations reported in common by cases in the same cluster (Clusters F and J). The creation of provincial and national networks linking human disease laboratories, food laboratories, and animal laboratories should be encouraged to facilitate the exchange of information about circulating Lm strains in a timely manner (Luber et al., 2011).

Conclusions

Sharing information about Lm surveillance and outbreak investigation between FIS, PHAs, and laboratories in a timely manner is essential for successful outbreak response. Considering the challenges associated with investigating Lm outbreaks, multiple investigative approaches should be considered. Chief among these should be the creation of networks to facilitate continuous exchange of human and food data between main stakeholders.

Footnotes

Acknowledgments

We would like thank Dr. Dean Middleton and Yvonne Withfield from Enteric, Zoonotic and Vectorborne Diseases Unit, Public Health Ontario.

Disclosure Statement

No competing financial interests exist.

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Challenges in Listeriosis Cluster and Outbreak Investigations,Province of Quebec,1997–2011

Abstract

Objectives:

Materials:

Results:

Conclusions:

Introduction

Materials and Methods

Cluster detection at the Laboratoire de Santé Publique du Québec (LSPQ)

Epidemiological investigations conducted by PHAs

Food Inspection Services (FIS) at the Ministère de l'Agriculture, des Pêcheries, et de l'Alimentation du Québec (MAPAQ)

Results

Listeriosis cases surveillance

Clusters detected

Outbreak investigations

Cluster B

Cluster C

Cluster E

Cluster F

Cluster I

Cluster J

Discussion

Conclusions

Footnotes

Acknowledgments

Disclosure Statement

References