Journal of Food Protection 86 (2023) 100131

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Journal of Food Protection

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Research Paper

Investigation of a Salmonella Montevideo Outbreak Related to the

Environmental Contamination of a Restaurant Kitchen Drainage System,
Québec, Canada, 2020–2021
André Paradis 1,†,⇑, Marie-France Beaudet 1,†, Marianne Boisvert Moreau 2,†, Caroline Huot 3,†
1
Infectious Diseases, Direction de Santé Publique, Centre Intégré Universitaire de Santé et de Services Sociaux de la Capitale-Nationale, 2400 Av. D’Estimauville, Québec, QC G1E 7G9, Canada
2
Public Health and Preventive Medicine Resident, Université Laval, 1600 Av. des Sciences-de-la-Vie, Québec, QC G1V 5C3, Canada
3
Unité Évaluation et Soutien à la Gestion des Risques, Direction de la Santé Environnementale, au Travail et de la Toxicologie, Institut National de Santé Publique du Québec, 945 Av.
Wolfe, Québec, QC G1V 5B3, Canada

A R T I C L E I N F O A B S T R A C T

Keywords: In May 2020, the Direction de santé publique du CIUSSS de la Capitale‐Nationale (DSPu) received a report from
Environmental exposure the Laboratoire de santé publique du Québec of a cluster of three cases of Salmonella enterica enterica, serogroup
Food contamination C1, serotype Montevideo. The epidemiological investigation identified a total of 67 cases between January 1,
Outbreak investigation 2020, and August 13, 2021, 66% of which were directly linked to a restaurant in the area. The Salmonella
Restaurant
strains from most of these cases were found to be identical by whole‐genome sequencing (cluster code
Salmonella infections
Salmonella Montevideo
2005MontWGS‐1QC). The initial inspection of the restaurant by the competent authorities (Ministère de l’agri-
culture, des pêcheries et de l’alimentation du Québec) – including the evaluation of hygiene and food safety,
the search for cases of illness among workers and food sampling – was unable to establish the source of the
outbreak. Environmental samples showed that the restaurant’s kitchen drains were contaminated with the
same strain of Salmonella Montevideo as the cases in the outbreak. Several cleaning and disinfection methods
were used repeatedly. When environmental sampling at the restaurant sites was repeatedly and consecutively
negative, cases in the community stopped. The prior occurrence of a fire in the kitchen may have played a role
in the contamination of the restaurant drains. In conclusion, public health professionals should consider drai-
nage systems (plumbing) and possible aerosolization of bacteria as a potential source of a restaurant‐related
salmonellosis outbreak.

Salmonellosis is a mandatory notifiable disease for all laboratories
in the province of Québec, as stipulated in the Minister’s Regulation
under the Public Health Act (chapter S‐2.2, r.2). Regional public health
departments do not, however, investigate every case of salmonellosis
reported in their region. They investigate only when their surveillance
system detects a cluster of cases, which is a significantly higher num-
ber of cases than expected within a given population, location, and
time period.
One hundred and forty cases of salmonellosis were reported on
average per year between 2015 and 2019 in the Capitale‐Nationale
region, for an annual incidence rate of 19 cases per 100,000 inhabi-
tants. This incidence rate is comparable to that of the province of Qué-
bec (17.7 cases per 100,000 inhabitants per year). There is very little
variation from year to year (Institut national de santé publique du
Québec, 2023).
Salmonellosis usually occurs as a result of eating contaminated
food, primarily poultry, pork, and beef (World Health Organization,
2018). Occasionally, human‐to‐human or animal‐to‐human transmis-
sion and environmental contamination may be the cause of infection
(Mair‐Jenkins et al., 2017; Siira et al., 2017).

Abbreviations: CIOSC, Canadian Integrated Outbreak Surveillance Centre; DSPu, Direction de santé publique; DVS, Direction de la vigie sanitaire; INSPQ, Institut national de santé
publique du Québec; LSPQ, Laboratoire de santé publique du Québec; MAPAQ, Ministère de l’agriculture, des pêcheries et de l’alimentation du Québec; MDR‐GNB, Multidrug resistant
Gram‐negative bacilli; MSSS, Ministère de la santé et des services sociaux du Québec; OR, Odds ratio; PCR, Polymerase chain reaction test; QGIS, Quantum Geographic Information
System; WGS, Whole‐genome sequencing.
⇑ Corresponding author.
E-mail address: andre.paradis.med@ssss.gouv.qc.ca (A. Paradis).
†
These four authors have contributed equally to this work and are designated as cofirst authors.

https://doi.org/10.1016/j.jfp.2023.100131
Received 25 May 2023; Accepted 10 July 2023
Available online 18 July 2023
0362-028X/© 2023 The Authors. Published by Elsevier Inc. on behalf of International Association for Food Protection.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
A. Paradis et al. Journal of Food Protection 86 (2023) 100131

Initial situation. On May 22, 2020, the Laboratoire de santé pub-
lique du Québec (LSPQ) detected a cluster of three cases of Salmonella
enterica enterica, serogroup C1, serotype Montevideo, of the same
strain by whole‐genome sequencing (WGS). The cluster code was
given the name 2005MontWGS‐1QC. These three cases had been col-
lected in April and May 2020. The cluster was reported to the Direc-
tion de santé publique (DSPu) of the CIUSSS de la Capitale‐
Nationale for investigation. The following week, three additional cases
of Salmonella Montevideo were reported to the DSPu, which confirmed
the presence of an outbreak.
The objective of this article was to share the experience encoun-
tered in Québec City area related to the investigation and management
of a major Salmonella Montevideo outbreak. The situation described is
uncommon since environmental transmission of salmonellosis is rare
(Kizny Gordon et al., 2017; Mair‐Jenkins et al., 2017).
Methods
On June 17, 2020, the LSPQ asked all local laboratories in the pro-
vince of Québec to send them the Salmonella C1 strains they had
received since January 2020 to be characterized by serotype, pulsovar,
and WGS. Indeed, several Salmonella samples had not been sent to the
LSPQ due to laboratories offloading their activities during the first
wave of the COVID‐19 pandemic. In June 2020, the characterization
of previous Salmonella cases detected an excess of Salmonella ser-
ogroup C1 and Salmonella Montevideo cases in the Capitale‐
Nationale region. On June 21, 2020, the pulsovars in the outbreak
cases were identified by the LSPQ as pulsovar 12 and pulsovar 21, both
of which are very similar.
The DSPu formulated a case definition for this outbreak (Table 1).
The search for subsequent cases was conducted in collaboration with
local laboratories and the LSPQ based on these definitions.

Table 1
Case definitions of the Salmonella Montevideo outbreak, Québec City, 2020

Resident or visitor of Québec City with Salmonella infection, whose symptom onset date or stool sampling date is after January 1, 2020, and having the following characteristics:
Confirmed case Probable case Suspected case Possible case

Serogroup Laboratory confirmation of Salmonella enterica enterica Serogroup C1 (O:7)

Serotype Serotype Montevideo In the absence of serotype
Pulsovar Pulsovar 12 or 21 In the absence of pulsovar
Whole-genome sequencing Aggregate code 2005MontWSG-1QC In the absence of sequencing

Figure 1. Weekly number of reported cases of the Salmonella outbreak meeting the case definitions, by illness onset date, Quebec City, December 30, 2019–July
25, 2020 (as of August 5, 2020). a: Week 1: ending January 4, 2020. b: Week 30: ending July 25, 2020.

2
A. Paradis et al.
Figure 2. Residence of reported ill persons, Salmonella Montevideo outbreak, Quebec City, 2020 (as of August 5, 2020).
A Canadian Integrated Outbreak Surveillance Centre (CIOSC) Pub-
lic Health Alert was issued on June 22, 2020, to search for cases that
might exist outside the Capitale‐Nationale region. The DSPu also
issued a bulletin on July 17, 2020, to clinicians in the region urging
increased vigilance when investigating patients with a clinical syn-
drome compatible with Salmonella gastroenteritis.
The epidemiological investigation of the cases was conducted using
a hypothesis‐generating questionnaire. Information was collected from
medical records and from the cases themselves, their families, and
their attending physicians. The cases were asked about potential expo-
sures for a period of 6–72 h before the onset of symptoms, which cor-
responds to the recognized incubation period (World Health
Organization, 2018) for salmonellosis cases. To maximize the chances
of identifying a common source and to avoid recall bias, Salmonella
enterica enterica serogroup C1 cases were investigated as early as pos-
sible, without waiting for serotyping confirmation.
Statistical analysis
Descriptive data regarding patients’ characteristics, clinical presen-
tation, infection severity, and exposure were collected through the epi-
demiological investigation of cases and were analyzed to draw a
portrait of the outbreak. Odds ratios (OR) and 95% confidence inter-
vals (CIs) were calculated (Altman, 1991) to compare the eating habits
of the outbreak cases to those of all Quebecers in the Foodbook Report
(used as controls) (Public Health Agency of Canada, 2015) with the
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Journal of Food Protection 86 (2023) 100131
following equation: (Number of exposed cases × Number of nonex-
posed controls)/(Number of exposed controls × Number of nonex-
posed cases). All data analyses were carried out in Excel and
validated with MedCalc. Mapping was carried out in the Quantum
Geographic Information System (QGIS).
Several meetings and information exchanges took place between
members of the DSPu, the Direction de la vigie sanitaire (DVS) of
the Ministère de la santé et des services sociaux (MSSS) du Québec,
the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du
Québec (MAPAQ), and the LSPQ over the course of the outbreak.
Results
As of August 5, 2020, 41 cases were identified and were broken
down by case definition as follows: 15 confirmed, 14 probable, and
12 possible cases.
Descriptive data. Among the 41 cases identified as of August 5,
2020, the mean age was 44 years (ranging from 20 to 81 years old).
Seventeen (41%) were women and 24 (59%) were men. Twelve cases
(29%) required hospitalization. None of the cases died.
Figure 1 shows the epidemic curve as of August 5, 2020, by symp-
tom onset date for the 41 cases identified. The shape of the epidemic
curve suggests a persistent source. Figure 2 shows the geographic dis-
tribution of cases by place of residence. This mapping demonstrated a
geographic link between the cases, with a concentration of cases
within a six‐kilometer radius in an urban area. The cases lived mainly
A. Paradis et al. Journal of Food Protection 86 (2023) 100131

Table 2
Frequency of selected food exposures and estimated odds ratio (compared to Foodbook Report (Public Health Agency of Canada. 2015)) among 33 investigated case-
patients of the Salmonella Montevideo outbreak, Québec City, 2020 (as of August 5, 2020)

Food items Cases (n = 33) Controls (Foodbook) (n = Estimated OR (95%CI)

100)
Exposed Nonexposed Exposed Nonexposed

Meats
Chicken (all types) 24 9 86.9 13.1 0.4 (0.2–1.1)
Chicken (pieces or parts) 19 14 75.0 25.0 0.5 (0.2–1.0)
Chicken (from a restaurant or fast-food establishment) 18 15 18.9 81.1 5.1 (2.2–12)
Chicken (breaded) 7 26 16.8 83.2 1.3 (0.5–3.6)
Beef (all types) 23 10 80.4 19.6 0.6 (0.2–1.4)
Stewing beef 9 24 14.9 85.1 2.1 (0.8–5.5)
Ground beef 3 30 64.5 35.5 0.1 (0–0.2)
Pork (all types) 12 21 56.5 43.5 0.4 (0.2–1.0)
Bacon 10 23 24.4 75.6 1.3 (0.6–3.2)
Ham 8 25 19.4 80.6 1.3 (0.5–3.4)
Deli-meat or cold cuts 12 21 52.7 47.3 0.5 (0.2–1.2)
Fish and shellfish
Fish 11 22 62.5 37.5 0.3 (0.1–0.7)
Shellfish 6 27 15.3 84.7 1.2 (0.4–3.5)
Dairy products
Dairy products (milk, cream, yogurt) 28 5 86.3 13.7 0.9 (0.3–2.7)
Cheese 21 12 93.5 6.5 0.1 (0–0.4)
Eggs 22 11 81.1 18.9 0.5 (0.2–1.1)
Vegetables
Lettuce 17 16 78.4 21.6 0.3 (0.1–0.7)
Prepared salad 11 22 11.6 88.4 3.8 (1.5–9.8)
Tomatoes 20 13 75.8 24.2 0.5 (0.2–1.1)
Fresh herbs 4 29 50.2 49.8 0.1 (0–0.4)
Others
Nuts 15 18 58.9 41.1 0.6 (0.3–1.3)
a
: Odds ratios and confidence intervals were also calculated for confirmed, probable, and possible cases but the results did not change findings and are not shown to
lighten the table.

in two boroughs of Québec City, namely Haute‐St‐Charles and Les Riv-
ières, as well as in the city of L’Ancienne‐Lorette.
Clinical presentation. As of August 5, 2020, among the 41 cases
identified, only 33 complete case investigations could be fulfilled.
The eight possible cases that were not surveyed had an episode date
too distant in time to allow adequate collection of information during
the survey. The complete descriptive analysis was therefore performed
with the 33 cases that could be investigated at the time. Among these,
the predominant symptoms were diarrhea (91%), abdominal pain
(75%), fever (50%), nausea (38%), headache (34%), blood in stool
(19%), and vomiting (13%).
Human, animal, and swimming water exposure. Of the 33 cases
surveyed, only two individuals reported exposure to a sick person dur-
ing their incubation period. Almost half (45%) of the cases were
reported to have had contact with animals during the period of inter-
est. Only 30% of cases reported contact with a cat and 21% with a dog.
About a quarter (27%) reported handling animal food. Only 6% of
cases reported swimming in a public area during their exposure
period.
Drinking water exposure. Because the cases were geographically
clustered in a subsection of the region, drinking water was considered
as a potential source of the outbreak. Opinions were sought from the
DSPu’s, INSPQ’s, and Québec City’s environmental health teams. Given
the configuration of the underground water system that supplies the
entire territory of Québec City, it seemed impossible that Salmonella
could be transmitted by potable water and that cases could be concen-
trated in only one part of the city, especially since daily water quality
controls were carried out.
Food exposure. The 33 cases surveyed as of August 5, 2020, were
asked about the grocery stores where they purchased their food. No
grocery store was targeted as a potential source since the cases fre-
quented several different stores.
Table 3
Frequency of restaurant food exposure among 41 investigated case-patients of
the Salmonella Montevideo outbreak, Québec City, 2020 (as of August 5, 2020)
Restaurant N (%)
Restaurant A 18 (44)
Restaurant B 3 (7)
Restaurant C 3 (7)
Restaurant D 3 (7)
Six other restaurants 2 (5)
18 other restaurants 1 (2)
Table 2 shows the food exposures of the 33 cases studied. The most
consumed foods were dairy products, chicken (all types), beef (all
types), eggs, cheese, and tomatoes. Table 2 also shows the results of
the statistical analyses that were performed to compare the eating
habits of the cases in the outbreak to those of all Quebecers in the
Foodbook Report (used as controls) (Public Health Agency of
Canada, 2015).
As chicken is a common carrier of Salmonella, particular attention
was paid to analyzing the frequency of chicken consumption among
the cases and the origin of any chicken consumed. One hypothesis
raised was that of a local chicken producer or distributor who deliv-
ered chicken only in the Capitale‐Nationale region. In the surveys,
73% of the 33 cases reported eating chicken (any form) during the
exposure period. Although this proportion may seem high, chicken is
a food frequently consumed by Quebecers. According to the Foodbook,
86.9% of Quebecers have eaten chicken in the last 7 days (Public
Health Agency of Canada, 2015). A comparison between the frequency
of the cases’ chicken consumption (any form) and that of Quebecers in
general made it possible to estimate a nonsignificant odds ratio (OR) of
0.4 [95%CI: 0.2–1.1] (Table 2). Given this low OR, the hypothesis of a

4
A. Paradis et al. Journal of Food Protection 86 (2023) 100131

Figure 3. Number of confirmed, probable, and possible Salmonella outbreak cases by date of declaration and timeline of key events of the investigation and
interventions, Quebec City, January 27, 2020–March 27, 2021. a: Week 5 (2020): ending February 2, 2020. b: Week 12 (2021): ending March 27, 2021.

local chicken producer was excluded, especially since the grocery break is shown in Figure 3. Most cases occurred before the end of July
stores and restaurants frequented by the cases deal with chicken dis- 2020. A lull occurred in late 2020, and then, new cases occurred until
tributors who have a province‐wide distribution network and this March 2021.
chicken originated from many different farms.
Statistical analyses also revealed that eating chicken in a restaurant
Discussion
was a statistically significant risk factor, with an estimated OR of 5.1
[95%CI: 2.2–12] (Table 2). Data on the cases’ food exposures in restau-
Explanatory hypotheses for the source of the outbreak. As of
rants were collected from all 41 cases and are presented in Table 3. As
August 5, 2020, the investigation of the 33 cases generated several
of August 5, 2020, 18 of the 41 cases (44%) reported frequenting Res-
explanatory hypotheses regarding the source of the outbreak.
taurant A at some point during their exposure period. All other restau-
The survey quickly ruled out certain explanatory hypotheses, such
rants had lower percentages of attendance, ranging from 2% to 7%.
as human, animal, water, and food exposures related to grocery stores,
Statistical analyses also revealed that eating prepared salads was a
since their frequency did not appear to be higher among the cases than
statistically significant risk factor, with an estimated OR of 3.8 [95%
those found in the general population.
CI: 1.5–9.8] (Table 2), although only 33.3% of the cases had eaten pre-
The search for hypotheses that could explain the source of the out-
pared salads.
break identified Restaurant A as the most likely source of the salmonel-
Final review of the outbreak. From the beginning (January 1,
losis outbreak. In fact, 44% of cases reported having visited this
2020) to the end of the outbreak (August 13, 2021), a total of 67 cases
restaurant during their exposure period, which was significantly more
of Salmonella infection were reported, including 56 confirmed cases,
than for all other restaurants (Table 3). In addition, the location of this
one probable case, and 10 possible cases. Indeed, 11 cases could not
restaurant matched well with the mapping of the cases’ home
be confirmed by WGS due to the offloading of several laboratory activ-
addresses. Furthermore, this restaurant primarily serves meals pre-
ities during the COVID‐19 pandemic. Of the 67 cases, 44 (66%) were
pared with chicken, which corresponds to the result of the food con-
related to Restaurant A. None of the cases died. Sixteen cases (24%)
sumption analyses showing that eating chicken in a restaurant is a
were hospitalized. A minority of cases had complications (e.g., spleen
significant risk factor, with an estimated OR of 5.1 [95%CI: 2.2–12]
abscess, septic arthritis). The epidemic curve of cases from the out-
(Table 2). Eating prepared salads also presented a statistically signifi-

5
A. Paradis et al.
cant OR of 3.8 [95%CI: 1.5–9.8] (Table 2), which could be explained
by the fact that a prepared coleslaw salad was served with most meals
at Restaurant A.
It should be noted that several cases did not consume food at Res-
taurant A. However, it is possible that some of them acquired the dis-
ease through secondary human‐to‐human transmission from someone
who consumed food at Restaurant A and became an asymptomatic car-
rier of Salmonella.
Investigation and intervention by the MAPAQ. In Québec, the
MAPAQ has the legal responsibility (P‐29 – Food Products Act) of inves-
tigating the source of contamination in a food establishment, including
restaurants. An initial visit by MAPAQ inspectors to Restaurant A took
place on July 8, 2020, which revealed that none of the restaurant’s
employees had experienced gastrointestinal symptoms in the preced-
ing weeks. No hygiene or food safety deficiencies were noted by
MAPAQ inspectors at Restaurant A. In fact, several additional preven-
tive health measures had been put in place by employees since the
beginning of the COVID‐19 pandemic. The chicken‐cooking process
was adequate according to temperature measurements. At the time
of this first visit, food samples taken from ready‐to‐eat chicken and
raw chicken were negative for Salmonella.
During a second visit on July 20, 2020, food samples taken from
coleslaw salad were negative for Salmonella. On the same day, the
MAPAQ collected environmental samples from work surfaces, knives,
door handles, sinks, and drains. Salmonella bacteria was detected by
polymerase chain reaction test (PCR) at several locations. On July
31, 2020, the MAPAQ received confirmation that the strains detected
in the environment matched those of the human cases. The presence of
the Salmonella Montevideo strain 2005MontWGS‐1QC in both the
cases and the environment of Restaurant A confirmed that the restau-
rant was the source of the outbreak. In the weeks that followed, the
MAPAQ intervened on several occasions to disinfect the site and repeat
environmental samples.
Explanatory hypotheses for the origin of the outbreak at Res-
taurant A. There were two main hypotheses as to the origin of the out-
break at Restaurant A: persistent environmental contamination and the
presence of an asymptomatic food handler infected with Salmonella.
It is known that environmental contamination can lead to
salmonellosis not only through direct food contamination but also
through indirect contamination, such as by aerosols. For example, in
2015, a prolonged outbreak of Salmonella Typhimurium in England
was linked to contaminated drains in a restaurant (Mair‐Jenkins
et al., 2017). Furthermore, it is known that hospital plumbing systems
can be a reservoir for Enterobacteriaceae, including multidrug resistant
Gram‐negative bacilli (MDR‐GNB), which cause infections in humans.
A literature review showed that 32 studies reported colonization of
hospital plumbing systems by MDR‐GNB and 27 of these studies
involved outbreaks in patients. The most contaminated plumbing
items in this literature review were drains, sinks, and taps (Kizny
Gordon et al., 2017). Moreover, several scientific articles report situa-
tions of drain contamination in Québec hospitals (Bédard et al., 2015;
Hota et al., 2009).
In order to explore the hypothesis of persistent environmental con-
tamination, environmental samples were taken by the MAPAQ and pri-
vate laboratories hired by Restaurant A’s management team. At the
same time, the DSPu’s requested the expertise of the Institut national
de santé publique (INSPQ)’s environmental health team and the
Polytechnique of Montréal’s expert team to discuss the various envi-
ronmental hypotheses and the appropriate sampling and disinfection
techniques for this type of contamination.
Several sample sites tested positive for Salmonella Montevideo in
Restaurant A’s kitchen, repeatedly but variably throughout the epi-
demiological investigation. The positive results were mainly from sites
such as the underside of a shelf, sink drains, and the floor drain. Sev-
eral rounds of cleaning and disinfection were carried out by the restau-
rant’s management team. Private decontamination contractors were
6
Journal of Food Protection 86 (2023) 100131
hired by Restaurant A’s owner. Several different methods were used
to decontaminate the environment.
Environmental samples were taken before and after each disinfec-
tion procedure to verify its effectiveness. Several sample sites that
were initially positive turned out to be negative after a cleaning and
disinfection operation. Other sites were more difficult to decontami-
nate, testing positive again in postintervention control samples. On
several occasions, contamination was detected in areas where it had
not previously been present.
The restaurant’s main sink was replaced on September 10, 2020,
due to its age and to the impossibility to decontaminate it. Unfortu-
nately, new cases of salmonellosis occurred even after this sink was
replaced (Figure 3). Then, one particular sampling site—the drain in
the dishwashing sink—repeatedly tested positive between January
and March 2021.
All environmental samples collected after March 25, 2021, were
found to be negative. The last sample was taken on July 8, 2021.
The hypothesis of an asymptomatic food handler carrying Sal-
monella was also investigated. As of July 14, 2020, the DSPu de la
Capitale‐Nationale sent a questionnaire to all Restaurant A employees.
Eighty‐three percent (83%) of them completed the questionnaire. It
indicated that no employees had been sick with gastroenteritis since
January 2020. However, this questionnaire could not rule out the
hypothesis of an asymptomatic food handler and chronic carrier at Res-
taurant A. In the fall of 2020, after several months of cleaning and dis-
infection of the environment, and given the persistence of cases of
Salmonella Montevideo in the population, the hypothesis of an asymp-
tomatic chronic carrier was discussed more intensively. A screening of
restaurant employees was organized in collaboration with the Centre
hospitalier universitaire de Québec. Stool samples for culture were
ordered for all Restaurant A employees, both food handlers and non-
food handlers. Unfortunately, the participation rate in this voluntary
screening was low (10%). Only four employees were tested, and their
results were negative. No food handlers agreed to the screening. This
low participation rate limited the collection of important information
and could be explained by the workers’ fear of being removed from
work in case of positive stool cultures.
An order from the medical health officer was issued in January
2021 for Restaurant A food handlers to be screened. The order was
directed at the restaurant owner and required him to provide evidence
that all of his food handlers had tested negative on two stool cultures
taken more than 24 h apart. This order gave the owner the leverage he
needed to convince his employees to get tested. The screening partic-
ipation rate was 94% this time around. Indeed, 17 of the 18 food han-
dlers currently on the job were tested. The only one who refused the
test quit his job.
This second employee screening found that two food handlers were
colonized with Salmonella Montevideo strain 2005MontWGS‐1QC.
They were removed from work starting on February 5, 2021. One of
the two employees was able to return to work after a few weeks fol-
lowing negative control samples, while the second employee was on
extended leave due to persistent Salmonella colonization. Unfortu-
nately, additional cases of Salmonella Montevideo occurred in the pop-
ulation despite the removal of colonized employees and extensive
disinfection of Restaurant A.
It is unlikely that the presence of two food handlers colonized with
Salmonella Montevideo can explain the cases in the community and the
persistence of cases over time. First, because these two employees reg-
ularly ate meals from Restaurant A while on the job, they were poten-
tially the victims of Salmonella contamination from meals prepared in
Restaurant A, rather than the potential sources of that contamination.
Second, the surfaces of the environmental samples that tested positive
in Restaurant A were not those frequently touched by food handlers. In
fact, no utensils, work surfaces, or door handles tested positive for Sal-
monella. Third, hygiene measures had been heightened throughout the
outbreak, due particularly to salmonellosis, but also because of the
A. Paradis et al.
COVID‐19 pandemic. In sum, the environmental source remained the
main hypothesis for explaining the persistence of the outbreak.
Explanatory hypothesis adopted. The most plausible explanation
for the origin of this outbreak remains the contamination of the drains
in Restaurant A. Indeed, most of the environmental samples positive for
Salmonella were found in sinks or near them (sink sprayers, drains).
The presence of contaminated biofilm (Mair‐Jenkins et al., 2017) in
the restaurant’s kitchen drainage system may have had a role to play
in the extended duration of this outbreak.
Over the course of the epidemiologic investigation, public health
responders learned that Restaurant A had experienced an accidental
fire in its kitchen before the Salmonella Montevideo outbreak began.
According to the Québec City fire department’s incident report, the fire
started in–and was limited to–the oven used for cooking chicken. A fire
department response was necessary. The firefighters used a powder
extinguisher first, then a water jet to contain and extinguish the
flames. Unfortunately, it was not clear how much damage was caused
by the firefighters’ use of extinguishers and water jets. Information
regarding the kitchen cleaning processes and products used after the
fire was not available. The investigation has not determined whether
this fire was the source of the introduction of Salmonella into the
plumbing at Restaurant A, but this remains plausible. The kitchen
drains could have been contaminated with food products when fire-
fighters used their water jets on the oven used for cooking chicken.
This hypothesis raises questions about the need to recommend a rou-
tine drain cleaning operation following a restaurant kitchen fire when
fire suppression requires the use of water that comes into contact with
food.
Limitations. There are some limitations to this outbreak manage-
ment. First, the number of cases related to this outbreak is most likely
underestimated and the hospitalization rate is probably overestimated
since many infected individuals may not have sought medical atten-
tion. Indeed, salmonellosis can be asymptomatic or minimally symp-
tomatic. In addition, those who sought help may not have received a
stool culture prescription or may not have taken the stool samples rec-
ommended by their physician. Despite the limited number of cases, it
was possible for the DSPu’s team to carry out an appropriate investiga-
tion and to identify the source of the outbreak.
Second, recall bias may have affected the quality and accuracy of
the data obtained from the food surveys, especially during the first
weeks of the outbreak. Indeed, cases of Salmonella Montevideo and
Salmonella C1 that had been reported several weeks before the start
of the epidemiological investigation were investigated at a later date.
Thus, it is possible that recall bias may have underestimated the num-
ber of cases related to Restaurant A. To avoid recall bias, Salmonella
enterica enterica serogroup C1 cases were investigated as early as pos-
sible, without waiting for serotyping confirmation.
Third, as recommended in the medical literature (World Health
Organization, 2018), the survey questionnaire used for salmonellosis
cases inquires about food exposures within 3 days before the onset
of symptoms. However, the Salmonella incubation period can be longer
than 72 h when the cause is environmental. In fact, in 2017, a pro-
longed outbreak of Salmonella Typhimurium was investigated in Nor-
way and was linked to environmental contamination of a restaurant
kitchen at the Oslo Airport (Siira et al., 2017). Extended incubation
periods, ranging from 4.5 to 9 days on average, were noted. Thus, it
was only after the link to Restaurant A was discovered and an environ-
mental source was suspected that the exposure period questioned in
the investigations was extended to 7 days. Consequently, it is likely
that for several of the Salmonella Montevideo cases initially investi-
gated, consumption of a meal at Restaurant A could not be identified
because the search period was limited to only 72 h before the onset
of symptoms.
Fourth, it should be noted that the ORs for individual foods calcu-
lated in Table 2 are most likely underestimated since the period of
exposure questioned in the surveys for salmonellosis is 3 days before
7
Journal of Food Protection 86 (2023) 100131
the onset of symptoms, whereas the Foodbook Report with which
the comparisons were made is based on a telephone survey that tracks
food consumption over the last 7 days. Moreover, the food categories
of the Foodbook did not always exactly correspond to those of the
hypothesis‐generating questionnaire. Nevertheless, the Foodbook
Report remains a relevant tool to help with foodborne illness outbreak
investigations and response in Canada. It allowed us to compare case
and control groups and to estimate ORs that pointed in the direction
of chicken from a restaurant or fast‐food establishment as the source.
Fifth, the unique context of the COVID‐19 pandemic certainly
affected the handling of this outbreak on several levels. Salmonella
cases might have been underreported from mid‐March to early May
2020 because of the lockdown, which explains why no cases were
reported for a 4‐week period. The reduction of in‐person medical visits
during the pandemic may have reduced the number of prescriptions
for stool samples. Diagnostic bias may also have occurred, as many
gastrointestinal symptoms were investigated solely to rule out a diag-
nosis of COVID‐19. Furthermore, in order to meet the high demand for
laboratory tests for COVID‐19 diagnoses, several laboratory activities
were offloaded, which resulted in the suspension of shipments of Sal-
monella strains to the LSPQ by local laboratories for characterization
analyses. Thus, the initial identification of the cluster may have been
complicated by the offloading of clinical, public health, and laboratory
activities during the COVID‐19 pandemic. Of course, as soon as the
cluster was identified, appropriate resources were dedicated to the
investigation of this outbreak.
The public health investigation showed environmental contamina-
tion of Restaurant A, particularly its drainage system. WGS of Sal-
monella strains from cases’ stool cultures with those from
environmental samples was a cornerstone of the investigation. Human
or food contamination from the drains may have been direct or indi-
rect (e.g., aerosolization). This environmental contamination was very
difficult to eradicate. Extensive and repeated cleaning and disinfection
of the drains using different processes finally controlled the contami-
nation. The last case of salmonellosis related to this outbreak occurred
on March 19, 2021, and the outbreak was declared over on August 13,
2021. Enhanced surveillance for salmonellosis continued after the out-
break was declared over. In conclusion, public health professionals
should consider restaurant drainage systems as a potential source of
salmonellosis outbreaks.
Funding source
The Direction de santé publique du CIUSSS de la Capitale‐Nationale
and the Institut national de santé publique du Québec provided finan-
cial support for the conduct of the research and the preparation of the
article.
Contributors
All authors have materially participated in the research and article
preparation. The four authors have contributed equally to this work
and are designated as cofirst authors. AP, MFB, and MBM contributed
to the outbreak investigation and management. CH contributed to the
outbreak investigation as an environmental expert. AP and MBM
drafted the manuscript. MFB and CH contributed major revisions to
the manuscript. All authors have read and approved the final article.
CRediT authorship contribution statement
André Paradis: Investigation. Marie‐France Beaudet: Investiga-
tion. Marianne Boisvert Moreau: Investigation. Caroline Huot:
Investigation.
A. Paradis et al.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgments
The authors of this article wish to thank all those who contributed
to this epidemiological investigation. They also wish to thank Julie
Ducrocq from the INSPQ for her precious help with statistical analysis
and table presentation.
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