Soft ripened cheese (SRC) caused over 130 foodborne illnesses in British Columbia (BC), Canada, during two separate listeriosis outbreaks. Multiple agencies investigated the events that lead to cheese contamination with
Several categories of ready-to-eat (RTE) foods have been associated with listeriosis outbreaks including vegetables (corn, celery, coleslaw, sprouts/taco salad) [
Control of
In the province of British Columbia (BC), Canada, cheese manufacture is regulated under the Milk Industry Act and Milk Industry Standard Regulations [
Unlike harder types of cheese, SRC can be more vulnerable to postpasteurization bacterial contamination and subsequent outgrowth due to low acidity and high moisture content. For example, a Camembert would have 70% moisture and pH range of 5.5 to 5.8, whereas a harder Cheddar cheese would have 42% moisture and pH of 5.45 [
Although in theory many critical control points and potential failures in dairy processing have been described during the production of SRC, very few outbreak investigations have successfully identified and described the route of contamination of SRC during postpasteurization processing steps. Previous outbreaks involving pasteurized SRC have shown issues with cross-contamination at retail and by food handlers [
Two listeriosis outbreaks (A and B) occurred in 2002 in BC, one in February 2002 (Plant A) and one in September 2002 (Plant B). Each outbreak was investigated by three means: via epidemiologic methods, laboratory analyses of samples, and plant investigations. Public health responses, in the form of health advisories and recalls, occurred as required by the investigation findings.
A multiagency investigation was required for both outbreaks. The communicable disease department of the BC Centre for Disease Control (BCCDC) coordinated case finding and followup, as well as the necessary restaurant and retail inspections which involved multiple health authorities. In addition to passive identification of cases self-reporting illness to their physician or emergency department, active case identification occurred following release of public health advisories that described the cheese implicated in the outbreaks. The information collected from cases included case demographics (age and gender), symptoms and illness onset, a description of exposure history, and other possible food vehicles. Cases were defined as symptomatic individuals exposed to the implicated SRC in their food history within the exposure period (up to 70 days after ingestion of the SRC). Confirmed invasive cases were identified through isolation of
Clinical (i.e., stool, blood, CSF), food (i.e., cheese and ingredients), water, and environmental samples (i.e., swabs from the plant, soil samples, animal faecal samples, compost, animal bedding, swabs from the farm environment and others) were tested according to standard culture methods. Briefly, any bacterial smears from sterile sites of suspected cases were referred to the provincial diagnostic laboratory for confirmation if they showed growth of
On-site inspections of each implicated dairy processing plant were conducted. Types and quantities of cheese manufactured at the plants from various milk sources were assessed for contamination, processing failure risks, and adherence to HACCP, prerequisite, programs and GMPs. Inspection focused on (1) raw milk quality and handling, (2) pasteurization effectiveness, (3) pasteurization procedures, (4) pasteurization equipment, and the likelihood of postpasteurization contamination from (5) raw milk, (6) the plant environment, (7) ingredients, and (8) personnel. Inspections included owner and operator interviews, review of on-site records and procedures, direct observation of processes involved during SRC production, testing of the dairy environment, testing of dairy ingredients (including water), and finished product sampling at the dairy processing plants. Further site inspections were conducted based on preliminary laboratory findings, and based on hypotheses that arose during the investigation.
In the first of the two outbreaks, two initial cases of bacterial meningitis caused by
Summary of outbreak findings.
Outbreak A | Outbreak B | |
---|---|---|
Illnesses | ||
Total number of illnesses | 49 | 86 |
First reported illness | February 3, 2002 | August 15, 2002 |
Organism identified |
|
|
Serotype | 4b | 4b |
PFGE designations—Apa I | LMAAI.0140 | LMAAI.0017 |
|
LMACI.0023 | LMACI.0082 |
Number of noninvasive (clinical) cases | ||
Febrile gastroenteritis (stool+) | 44 (6) | 86 (14) |
Number of invasive (confirmed) cases | ||
Meningitis | 3 | 0 |
Bacteremia in pregnancy | 2 | 0 |
Demographics | ||
Age range in years (median) | 4 to 85 (49) | 14 to 76 (46) |
% Female | 64 | 72 |
Clinical findings | ||
Incubation period in days (median) | 1 to 33 (7) | 0.5 to 28 (2) |
Symptoms reported (%) | ||
Fatigue | 51 | 62 |
Myalgia | 46 | 55 |
Chills | 38 | 0 |
Night sweats | 24 | 0 |
Bone pain | 19 | 0 |
Abdominal pain | 8 | 54 |
Cheese1 prepared at plant | ||
Number of cheese types produced | 14 | 10+ |
Bacterial smear surface soft ripened cheese |
|
Yes |
Chevre (goat milk soft cheese) |
|
No |
Curds (e.g., cheddar) |
|
Yes |
Feta cheese | Yes | Yes |
Soft cheese (e.g., fromage frais) | Yes | Yes |
Hard cheese (e.g., cheddar cheese) |
|
Yes |
Semihard cheese (e.g., raclette) | No |
|
Soft mould ripened cheese |
|
|
Investigation findings (Acceptable/neutral/unacceptable) | ||
Raw milk quality and handling | Acceptable | Acceptable |
Pasteurization effectiveness/procedures | Acceptable | Acceptable |
Pasteurization equipment | Acceptable | Acceptable |
Postpasteurization—raw milk contamination |
|
Acceptable |
Postpasteurization—interior plant environment | Acceptable | Acceptable |
Postpasteurization—ingredients |
|
|
Postpasteurization—personnel |
|
Acceptable |
External environment |
|
|
Epidemiological curves of weekly illness onsets for confirmed and clinical listeriosis in 2002 outbreaks.
In the second outbreak, cheeses produced by plant B were sold at a farmers’ market on Vancouver Island on September 6, 2002, and linked to a cluster of five illnesses within a family with rapid onset (<24 hrs) of severe febrile diarrhoea requiring hospitalization. An investigation began on September 18, one day following notification and receipt of food and clinical samples, and implicated cheese was recalled on September 19. A total of 86 cases, all with febrile gastroenteritis, were linked to this outbreak, with the earliest case identified one month prior, on August 15, 2002 (Table
Overall, 113 and 104 food and environmental samples were collected and tested for the presence of
Results of lab tests in milk, cheese, and environmental samples.
Outbreak A | Outbreak B | |
---|---|---|
Milk samples | ||
Raw milk SPC (log10 CFU/mL) | ||
(1) Government dairy pool | 3.90 | n/a |
(2) Local farm—cow | n/a | 3.00 |
(3) Local farm—goat | 4.43 | n/a |
Raw cow milk |
Absent | Absent |
Raw cow milk pH | NT | 6.8 |
Pasteurized cow milk phosphatase | Negative | Negative |
Cheese samples | ||
Number of cheese samples |
16 (25) | 22 (29) |
Number of varieties + (number of lots+) | 8 (12) | 3 (3) |
|
2.0 | 2.0 |
|
<2 to 9.4 | <2 to 9.0 |
Environmental samples | ||
In the plant—ingredients | ||
Number of |
2 (33) | 2 (32) |
In the plant—surfaces | ||
FCS number of |
3 (17) | 0 (5) |
NFCS number of |
2 (23) | 0 (17) |
Outside the plant | ||
Number of |
1 (1) | 4 (7) |
On the hobby or dairy farm | ||
Number of |
12 (14) | 6 (14) |
Number of environmental |
17 (88) | 14 (75) |
SPC, standard plate count; NT, not tested; n/a, not applicable;
Overall,
Sample description |
|
Matched to cheese |
---|---|---|
Outbreak A samples | ||
|
|
Yes |
|
|
Yes |
Aging room shelf (where spray bottles stored) |
|
NT1 |
Aging room—inside plastic aging containers (3 samples) |
|
Yes |
Aging room—condensate from blower unit |
|
Yes |
Whey trench outside |
|
NT |
Grass beside walkway |
|
NT |
Pig garden—poo area |
|
NT |
Pig garden—wet bedding |
|
|
Pig garden—compost pile |
|
NT |
Pig garden—whey tank area |
|
|
Dog run |
|
NT |
Pig pen water |
|
|
Pig pen dirt |
|
Yes |
Pig pen bedding |
|
Yes |
Chicken coop floor—dirt |
|
NT |
Chicken run—old flooring |
|
NT |
Chicken run walkway |
|
NT |
Outbreak B samples | ||
Hydrated mould culture |
|
|
Finished water (UV treated/filtered from inside plant) |
|
|
Cistern pipe |
|
Yes |
Pond water |
|
|
Lagoon water |
|
|
Sewage water |
|
NT |
Cow feces |
|
|
Cow feed greens |
|
No |
Water/rag in milk house |
|
Yes |
Swallow nest |
|
Yes |
Chicken feces |
|
|
Pheasant feces |
|
No |
Overall,
A review of the raw milk sources, pasteurization procedures, records, and equipment in both plants A and B did not reveal any obvious food safety hazards that could lead to
In plant A, temperature records for raw milk receipts ranged from 0.8°C to 5.6°C, with acidity levels within normal range (pH 6.6 to 6.8). Once a week, 400 litres of raw goat’s milk from a licensed dairy farm was used to make ~40 kg of cheese, and once every two weeks, 400 litres of raw cow’s milk from the provincial dairy pool was used to make ~40 kg of cheese. All raw milk was vat pasteurized at 63.3°C for a minimum time of 30 minutes. Phosphatase tests of 11 different cheese types and production dates were negative, confirming that the milk used to make the cheese was properly pasteurized. The pasteurization equipment was tested to verify the accuracy of thermometers and timing clock. The integrity of vat jackets and the integrity of vat pasteurizer outlet protection valves were examined to ensure the absence of leakage. Raw milk cross-contamination into pasteurized milk was assessed during transfer of pasteurized milk to cheese vats. The potential for cross-contamination via operator (hands or clothing), equipment (used for both raw and pasteurized milk), and splashing was also evaluated. The operator demonstrated good understanding of the risks of cross-contamination, and hand/apron sanitizing was frequent. One piece of equipment, the pH meter, was found to be shared by raw and pasteurized milk sources. The probe was rinsed but not sanitized between testing of raw milk and pasteurized cheese curds. Testing of pH probe buffer solutions did not detect
The interior of the dairy processing plant environment appeared clean, sanitary, and well maintained based on a visual inspection. Approved food grade sanitizers designed for use in a food processing environment were correctly employed, verified by a review of the sanitation records. Environmental sampling of the plant interior revealed only five of 40 (12.5%) swabs positive for
In plant B, records for August 16 indicated that the raw milk used to make the implicated batch of cheese was at 2.2°C prior to pasteurization. The pH of the milk was normal (pH = 6.8). SPC tests of the raw milk were performed twice per month, with a previous year annual average of 3.09 log10 CFU/mL. The raw cow’s milk was supplied from the dairy processing plant’s own licensed dairy farm located on the same site, and a daily production yield of 750 L of cow’s milk was processed into several varieties of raw milk and pasteurized milk cheeses three times per week. Similar to the investigation of plant A, no issues were found with the pasteurization equipment or with the pasteurization method. Milk was vat pasteurized above the minimum pasteurization time and temperature to 65°C for 31 minutes. Further, no issues were identified to indicate any postpasteurization contamination of milk from raw milk (splashing or entering). The operator was also aware of potential cross-contamination issues. Raw milk and pasteurized milk cheese were not produced on the same day, and cleaning and sanitizing were performed at the end and beginning of each production. One of two dairy processing plant workers was responsible for milking cows, and the work duties, habits, and sanitary procedures of this worker were assessed as satisfactory. Clothing specific to the milking operation was put on over street clothes in the milk house. When called to work at the plant, the worker first washed hair and hands in the dairy farm milking house, removed clothing, and put on clean street clothes. At the plant office, street clothes were removed, and clean dairy clothes were put on before entering the dairy processing plant. Upon entering, rubber boots, apron, and hair net were worn (all used exclusively in the plant); then hands were washed and sanitized before proceeding into the processing room. A visual inspection of the processing areas did not reveal any deficiencies in the cleaning and sanitation program. These inspection findings were supported by environmental sampling, with none of the 22 swabs of food contact and nonfood contact surfaces within the plant testing positive for
However, the ingredients used to manufacture cheese were not acceptable. Several ingredients were added to milk or cheese postpasteurization including freeze dried starter cultures, vegetable rennet, salt, natamycin, calcium chloride, annatto coloring, and hot water (66°C) to wash curds. During initial testing of 31 ingredients, only one ingredient (3.2%), a hydrated mould culture solution used on September 16 tested positive for
Water for Plant B was supplied by a private deep well located several hundred metres away (Figure
Schematic diagram of water supply system in dairy processing plant B.
Postpasteurization contamination of SRC occurred in both outbreaks. Neither pasteurization failure nor contaminated milk supply were likely contributors to the outbreaks. Both dairy processing plants were visually very clean, and inspection observations found acceptable sanitation levels in the interior plant environments. These observations were supported by environmental swab tests of food contact and nonfood contact surfaces in the plants. In plant B, no swab samples were positive for
As
In outbreak B, the findings support a point-source contamination event that affected a single lot of SRC. The intensive investigation of the water source may not have occurred if the operator had not saved the September 16 hydrated culture solution. Following outbreak A and prior to outbreak B, the BCCDC had implemented a new directive to all operators to empty, clean, and sanitize hydrated culture solution bottles after use. However, out of prudence and concern, this solution was purposefully saved for subsequent testing by the operator of plant B upon notification of the recall and illness. A follow-up interview of the operator revealed that plant water normally used to wash curds was used to make the culture solution, instead of the recommended method of preparing the solution with boiled and cooled water.
Through a root cause analysis, it was revealed that the factors contributing to outbreak B included a design failure, a maintenance error, and an operational change (Figure
Although it is not known how long the UV disinfection system was failing, hot water (66°C), normally used to wash the curds would likely have killed any
Another interesting finding from outbreak B was the unusual illness presentation, with only noninvasive listeriosis cases observed.
Immediate recommendations made by BC provincial authorities included a requirement for the two dairy processors involved in the outbreaks to test for
Inspections of dairy processing plants did lead to industry improvements and a reduction in the numbers of listeriosis cases in the years following the 2002 outbreaks. In a 2009 survey of dairy, meat, and fish processors in BC, no dairy products nor processing food contact surfaces in dairy processing plants were found to contain
In summary, investigations of foodborne outbreaks can be complex, requiring multiagency support, and extensive on-site inspection before the root cause of pathogen contamination of manufactured foods can be established. Specifically, in the outbreaks reported here, environmental sampling assisted in focusing on the inspections, generating hypotheses, and formulating the questions asked of plant operators during follow-up inspection interviews.
Inspectors and regulators responsible for oversight of manufacturing processes require detailed systems knowledge to understand where errors can occur. Many regulatory agencies are moving towards outcome based guidance, reliance on inspection of records, and compliance with record keeping. In outbreak B, there should not have been an outbreak when the dairy worker washed the curds with lukewarm water. The issue was that the water should have been potable, and it was not. This dairy had a secondary UV water disinfection system, supported with monitoring records to show that the system had been operating normally and had been maintained as required by the system manufacturer. From a regulatory and records perspective, the dairy was in full compliance. The problem lay in the source water contamination (cistern was open to animals) compounded by a recent improper repair to the water line. The multiple factor failures illustrate how events can lead to illness, despite compliance with regulations and despite good records. A surface examination of records would not have revealed these problems. We are concerned that with regulatory agencies now moving towards a model of records inspection concomitant with a reduced inspection frequency in manufacturing settings could potentially lead to missed opportunities for detecting and correcting errors that are often found during physical and process inspections.
In addition, findings from these listeriosis outbreaks demonstrate the importance of adhering to strict processing procedures to minimize the survival and spread of
The authors declare that there is no conflict of interests regarding the publication of this paper.
The authors thank staff from the BCCDC Public Health Microbiology and Reference Laboratory (Vancouver, BC), Canadian Food Inspection Agency (Burnaby, BC), National Microbiology Laboratory (Winnipeg, Manitoba), and Bureau of Microbial Hazards Health Canada (Ottawa, Ontario) for their assistance with culture and typing. The authors also thank the Environmental Health Officers from the Vancouver Island Health Authority and other regional authorities in BC, assistance from Public Heath Engineers, the staff from the Office of the Provincial Health Officer, Health Canada, and Ministry of Agriculture for their efforts investigating and responding to these outbreaks. The authors also thank Dr. Emily Newhouse, Dr. Jovana Kovačević, and Sion Shyng for critical review of this paper.