FOOD SAFETY PRACTICES IN CATERING DURING THE CORONAVIRUS COVID-19 PANDEMIC
Рубрики: BRIEF COMMUNICATION
Аннотация и ключевые слова
Аннотация (русский):
On January 30, 2020, the Director-General of the World Health Organization declared the outbreak of COVID-19 a Public Health Emergency of International Concern. There is hardly a country in the world that is not currently facing this problem. The number of cases is constantly growing, patients and carriers being the main mode of transmission. The economies of all countries are at stake. However, people need essential goods and food, regardless of the situation. In this respect, agriculture, food industry, food market, and catering have become priority industries. A continuous operation of food service enterprises (FSE) is crucial for the uninterrupted food supply in the period of preventive measures. The paper describes how pathogen makes its way into FSEs, spreads, and infects people. This information makes it possible to assess the probability of coronavirus infection and to reduce its spread, thus ensuring the safe operation of the enterprise. There are three transmission routes the coronavirus can take at a FSE: (1) aerial transmission by droplets and aerosols during the main and secondary technological production processes, (2) person-to-person transmission from clients to staff or from employee to employee via direct or indirect contact, (3) transmission via contaminated surfaces, e.g. packaging, furniture, equipment, etc. FSEs have to follow the recommendations published by the federal and/or local authorities, which may vary depending on the COVID-19 incidence rate in the area. These recommendations are based on the probability of the public health risk associated with person-to-person transmission, rather than on food safety.

Ключевые слова:
Coronavirus COVID-19, containment, food service enterprises, preventive measures, recommendations
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INTRODUCTION
An outbreak of coronavirus infection in Wuhan,
China, has led to a global epidemic declared a Public
Health Emergency of International Concern by the
World Health Organization [1]. The emergence of a new
human coronavirus has become a global public health
problem. The virus has demonstrated a variety of forms,
health effects, and incubation periods. COVID-19 is
resistant to environmental factors, has a high penetration
ability, and may be lethal. The challenge lies in the
new form of the virus and the lack of experience in
combating it, as well as in the absence of an effective
medicine. An infected patient has practically no chance
of recovery without medical intervention. Children
under 14 and 65-plusers are at risk [2]. Since the current
trajectory of the COVID-19 outbreak is unknown,
authorities have to develop public health preventive
measures to curb the spread and gain experience that
could be transformed into treatment recommendations.
The COVID-19 pandemic has affected the whole
world and all spheres of human life. Italy, Spain, France,
Great Britain, USA, and China have suffered the most
damage. The situation in Russia remains noncritical,
which can be explained by its territorial features, longterm
experience in anti-infection preventive measures,
and their timely implementation. Risk awareness
motivates people to adopt preventative behavior.
The growing incidence and fatal outcomes abroad
demonstrated Russians the need to follow official
recommendations, both at home and at work.
COVID-19 is a global problem, and all global
economies are going through hard times. However,
there are vital industries that require priority measures,
food supply being one of them. The US food and
agricultural sector is 100% privately owned. It includes
2.1 million farms, 935 000 restaurants, and more than
200 000 enterprises of food production, processing, and
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Foods and Raw Materials, 2020, vol. 8, no. 2
E-ISSN 2310-9599
ISSN 2308-4057
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Mayurnikova L.A. et al. Foods and Raw Materials, 2020, vol. 8, no. 2, pp. 197–203
storage. This sector accounts for about 20% of economic
activity. The American Food Industry Association
(FMI) promptly issued a Coronavirus Preparedness
Checklist. According to the FMI, a pandemic will
require the mutual efforts of many related spheres,
including health, supply chain, logistics, food safety,
labor, emergency management, and the media.
The food sector is one of the strategic sectors of
Russian economy. It owes its strategic implication to the
fact that every citizen is a consumer of food products.
The national security demands that citizens should have
access to essential food products of domestic origin,
regardless of imports. The food sector is represented
by agriculture, food industry, food processing industry,
and public food service. It is a backbone sphere of
Russian economy. The food sector forms the agri-food
market and ensures food security. Agriculture employs
4.346 million people, food and processing industry
accounts for 2 million jobs, and 1 million people are
engaged in public catering. Together, this is more than
10% of the total number of people employed in the
economy. Russian food industry is represented by more
than 50 000 enterprises, while public catering includes
187 000 enterprises [3]. Therefore, the national food
sector is important, especially in emergency situations.
The Federal Service for Supervision of Consumer
Rights Protection and Human Security responded to
the epidemic as early as in February 2020. It developed
Recommendations for the Prevention and Disinfection
Measures against the Spread of New Coronavirus
Infection in Catering Enterprises and Food Storage of
Educational Organizations [4].
The coronavirus outbreak exposed serious problems
in all sectors of human life, including food security. The
research objective was an analysis and synthesis of the
available information in order to bring it to the scientific
community and the population engaged in the food
sector, thus facilitating the adaptation of food service
enterprises to the extreme conditions and preparing
them for a possible worst-case scenario.
The practical application of the article is that it can
inspire further studies of this urgent problem and set
goals for the future scientific research. This seems to
be the case when the development does not go “from
science to practice” but “from practice to science”.
RESULTS AND DISCUSSION
Canteens and refectories expose staff and clients to
pathogenic microorganisms, e.g. viruses or bacteria.
Workers in the production and service areas should
know the so-called sanitary control points and be able
to control them so as not to endanger the health of
colleagues and clients.
The work of food service enterprises (FSE) during
the COVID-19 pandemic is fraught with extreme
conditions. At a FSE, the pathogen can spread via the
following routes:
– by inhalation of microorganisms that can stay
suspended in the air for a long time;
– by direct contact with oral fluids or other bodily
materials that enter the FSE premises with clients;
– when the mucous membrane of the nose, mouth, and
eyes is exposed to droplets and aerosols that contain
microorganisms formed in the infected person and
spread over short distances with coughing, sneezing, or
talking without a face mask; and
– by indirect contact with contaminated tools and/or
surfaces [5–10].
During the outbreak of COVID-19, the infection
can spread by any of these routes, each of which is
associated with an infected person visiting public places,
including FSEs.
Hotels, catering and tourism incur huge losses.
During the quarantine period, most enterprises were
closed as high COVID-19 incidence is associated with
crowded places. Therefore, it is extremely important to
prevent a further spread of the virus in public places [11,
12]. Social distancing is one of the recommended
preventive measures. Social distancing is most effective
in all scenarios, e.g. airborne contamination when the
microorganism stays viable in the air for a long time, or
in cases of aerial transmission by coughing or sneezing,
as well as in cases of direct or indirect physical contact,
e.g. via contaminated surfaces, etc.
Adequate measures to combat the pandemic in
crowded places are possible only with respect to a full
understanding of the transmission mechanism and
viability of the virus. Given the current global situation,
the mechanism of transmission of the COVID-19 virus
at FSEs requires an urgent and thorough research. Such
research could help analyze and adapt measures aimed at
COVID-19 risk reduction.
Food service employees run into danger of the
COVID-19 infection. They communicate with clients
face to face and have to deal with cutlery and table
surfaces. Moreover, they are exposed to potentially
dangerous biological material, e.g. saliva droplets on
napkins and tableware. Therefore, FSE employees
must know and follow the necessary safety rules,
which may play a great role in preventing the spread
of COVID-19 [5].
There is currently no evidence that COVID-19 can be
transmitted via food or food packaging. Nevertheless, a
person can get COVID-19 by touching a contaminated
surface or object and then touching their mouth, nose,
or eyes. However, this is not the main way the virus
spreads. The US Centers for Disease Control and
Prevention claim that COVID-19 does not live long on
surface areas. Therefore, the risk of virus transmission
via food or packaging is very low. It takes a few days
or weeks to deliver food products and goods to FSEs.
The person-to-person route is more likely, e.g. via close
contact with a patient or carrier.
We performed a brief analysis of scientific literature
that revealed the following COVID-19 transmission
routes:
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– a person-to-person direct transmission through
coughing, sneezing, inhalation of droplets, contact
with oral, nasal, or ophthalmic mucous membranes, or
indirect transmission via saliva [5, 11, 13, 14];
– from surfaces to humans;
– from animals to humans; and
– asymptomatic transmission [15].
There is currently no evidence that COVID-19 can
be transmitted through food products. Yet, this fact does
not mean that there is no risk. To assess the chance of
coronavirus infection in FSE conditions, let us describe
the mechanisms by which the pathogen enters a FSE,
how it is transported and transmitted to humans.
Aerial transmission. This mechanism of
COVID-19 transmission has been described in
several studies [5, 7–8, 11, 15–18]. The pathogen
can stay airborne and viable for a long time. It can
spread via direct contact with oral fluids or other
bodily substances. The conjunctiva of nasal or oral
mucosa may contact with droplets and aerosols that
contain microorganisms generated by an infected
person and set in motion by coughing or talking
at a close distance with no face mask on. Finally,
the virus can spread through indirect contact with
contaminated tools, dishes, or surfaces [7–10].
If an infected person is present on the FSE premises, the
infection can follow any of these paths (Fig. 1).
Food production and catering practices show
that many production processes result in droplets or
suspensions that hang in the air, e.g. washing the dishes,
equipment, and tools, or processing raw materials, etc.
These droplets move freely in the air stream. As a result,
there is a chance that they can capture the virus and
carry it on [17].
Community transmission. The waitperson comes
into direct or indirect contact with the bodily liquids
(biological media) of the clients through table surfaces,
dishes, cutlery, napkins, toothpicks, etc. Such exposure
is likely to facilitate the COVID-19 spread [9].
Transmission via contaminated surfaces. The
coronavirus remains viable on such surfaces as glass,
plastic, wood, or metal [7, 18]. Therefore, all surfaces
that food workers have to deal with are potential
sources of COVID-19 transmission. There is a practice
of detecting droplets and aerosols from infected people
who can contaminate surfaces while visiting public
places. At FSEs, the list of potentially contaminated
surfaces includes tables, chairs, furniture, door handles,
etc. The packaging surfaces of products and goods
supplies are another potential source of the coronavirus
infection. At the stage of the incoming goods inspection,
the employees touch the surfaces that may contain traces
of the viral infection. Thus, the virus can enter a FSE via
supply transportation or simply via contact with external
environment and infected people who contaminate the
surfaces around them. Some types of coronavirus are
known to remain viable at room temperature from two
hours to nine days. Several studies showed that the
virus has a better chance of survival at 50% of relative
humidity than at 30%. According to Russian regulatory
documents, the recommended relative air humidity at
FSEs should be 60–40% in the cold season and 40–60%
in the warm season. Therefore, maintaining a clean and
dry environment at FSEs can help reduce the COVID-19
viability [2, 19, 20].
Popova, the Chief Sanitary Doctor of the Russian
Federation, issued a monitoring system and a number
of decrees that control the spread of the coronavirus
infection in Russia. The decrees contain preventive
measures against the COVID-19 infection. As the
threat of importation and spread did not cease, Federal
Law No. 53 On the Sanitary and Epidemiological
Safety of the Population was issued on March 2, 2020.
It introduced some further preventive measures.
Additional recommendations on the COVID-19
prevention were developed for employees and heads
of organizations, regardless of the legal forms of
ownership.
FSEs had to limit public events during the pandemic.
As for refectories and canteens, they received the
following recommendations, depending on the specific
conditions at the enterprise they serve:
– if the enterprise has a canteen, it is to be provided
with disposable tableware. After using, the utensils are
collected, disinfected, and destroyed in the prescribed
manner. Reusable utensils are to be processed in
specialized dishwashers at ≥ 65°C for 90 min, or
manually at ≥ 65°C with disinfectants, as stated in the
related sanitary standards;
– cooking process should involve high-level heat
treatment technologies;
– sale or consumption of raw or insufficiently thermally
processed products of animal origin is forbidden;
– butchers should observe personal hygiene rules, which
include frequent hand washing after contact with raw
materials and products of animal origin;
– expired raw materials can cause food poisoning;
therefore, feedstock volume should be planned taking
into account the decreasing amount of produced
products;
– canteen and refectories should give preference to foods
with a high nutritional value;
Figure 1 Transmission routes of 2019-nCoV at food service
enterprises
COVID-2019
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– the incoming goods inspection is to ensure a strict
quality control of the incoming raw materials and the
accompanying documents;
– if the enterprise has no canteen, employees are not
allowed to eat at workplaces: they can have their meals
only in a specially designated meal room; and
– should there be no meal room, employees are to be
provided with a specially allocated meal area with a sink
for hand washing and disinfectants.
The above recommendations also determine the
list of food service enterprises that can be potentially
dangerous:
– crowded places, e.g. food courts and canteens, with a
high circulation of people, which increases the risk of
encountering coronavirus patients and virus carriers;
– FSEs that sell finished products in reusable utensils
are to ensure their proper sanitization with the
recommended concentrations of disinfectants;
– self-service enterprises, e.g. self-service buffets, salad
bars, etc.
FSEs that deliver finished culinary products have
certain advantages in the current situation. Disposable
tableware and shipping containers, e.g. thermal bags,
reduce the risk of contamination. However, in this
case, the risk zone shifts towards the person-to-person
transmission route: the infection can be transmitted
via airborne droplets from the delivery person to the
consumer or vice versa. The surfaces the delivery person
contacted with have to undergo additional disinfection,
while both the employee and the client are to wear face
masks and disposable gloves.
FSEs unlicensed to deliver finished products cannot
operate in full during the quarantine. However, they can
sell takeaway meals in disposable packaging, on condition
they follow all recommended preventive measures
concerning the seller – client communication [7].
Recommendations for restaurants offering takeaway
services include the following points:
– FSEs can only accept online or phone orders, without
face-to-face communication on the FSE premises, of
which consumers should be informed via traditional
advertising means;
– the delivery time should be individual for each client,
i.e. they must not enter the premises until their order is
ready;
– spontaneous clients are be advised to leave the
premises to place their order by telephone or online and
return at the appointed time to receive it;
– customers whose orders are ready must enter the site
one at a time to collect their orders and make payments;
and
– employees are to prevent crowding outside by using
queuing systems to maintain the recommended twometer
distance.
In many Russian cities, including Moscow, public
and leisure events consisting of 50 people or more were
banned as early as in mid-March. Cafes, restaurants,
and other FSEs fell under these restrictions, since the
number of personnel and clients combined is likely
to exceed 50 people. An exception was made only
for cafes, restaurants, and FSEs that provide delivery
service. In the Kuzbass, the flow of clients to cafes and
restaurants decreased by an average of 50% in less than
a week. During the quarantine, most consumers prefer
to eat at home or take home-cooked food to work. On
March 17, 2020, all FSEs received Recommendations
for the Prevention of the New Coronavirus COVID-19
Infection and the Protection of Citizens in Trade and
Public Catering Organizations from the Ministry of
Industry and Trade of the Russian Federation. The
recommendations set forth immediate preventive
measures to protect citizens in public catering and trade
organizations.
However, not all FSEs can switch to the takeaway
mode. This type of activity has its own specific features
associated with the quality and safety of remotely sold
products. Food delivery imposes extra obligations on
the businesses, i.e. appropriate permits from regulatory
authorities for the delivery of finished catering products.
In Russia, regulatory documents that control
food safety issues include Sanitary Regulations and
Standards, Technical Regulations of Customs Union,
etc. For instance, the On Food Safety Technical
Regulation of Customs Union 021/2011 indicates the
mandatory presence of a safety management system in
the food industryI. According to Article 10 (Clause 2),
food production processes must be based on the
principles of Hazard Analysis and Critical Control
Points. Otherwise, FSEs cannot fully ensure the
production and sale safety, especially during the
coronavirus pandemic. The basic systems for ensuring
the quality and safety of food products in industrial
practice include Good Manufacture Practice (GMP)
and Good Hygiene Practice (GHP). Maintaining
these systems can minimize the possibility of surface
contamination and eliminate it, should it occur. This
factor is important for the safe operation of FSEs, both
in the current situation and in the future.
Infection control at FSEs. Catering personnel and
managers should be aware of coronavirus transmission
routes, symptoms, and preventive measures.
Identification of potentially infected clients. All
catering staff should be prepared to identify and report
a client suspected to be infected. Ideally, COVID-19
patients are not allowed to visit public places. However,
FSE employees ought to maintain COVID-19 alert and
refuse to provide service to any client with symptoms.
They must immediately inform the manager of possible
infection, as well as appropriate authorities as instructed.
Protocol for assessment of FSE staff. The
epidemiological safety of a FSE is the responsibility
I TR TS 021/2011. Tekhnicheskiy reglament Tamozhennogo soyuza
“O bezopasnosti pishchevoy produktsii” [TR CU 021/2011. Technical
regulations of the Customs Union “On food safety”]. 2011.
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of its managers. They are to monitor the possible
incidence among the employees every day. Managers
must keep their staff updated on the situation and make
sure that they take the situation seriously. Managers are
to collect data that can be used as the primary method
for identifying potential COVID-19 carriers. In other
words, they are to measure the body temperature of their
employees with a non-contact forehead thermometer.
A simple survey is another useful precaution. The list
of questions may include the following: Have you been
abroad in the past 14 days? If yes, what country did you
visit? Have you had a fever in the past 14 days? Have
you participated in gatherings, meetings, or had contact
with large groups of strangers? Have you had contact
with a patient with confirmed coronavirus infection? Do
you have breathing problems? etc. If the employee gives
a positive answer to any of the questions, he/her must
be self-isolated and quarantined, and the management
must inform the appropriate authorities as instructed
[5, 22]. If an employee proved COVID-19-positive,
employers should inform the staff about the possibility
of COVID-19 infection without revealing the identity of
the infected employee. The latter is to be denied access
to the premises until officially reported safe to return to
work by health authorities.
Hand hygiene. F oreign s ources r eported c ases o f
fecal-oral route of COVID-19 transmission, which makes
the issue of hand hygiene even more important for FSE
staff. Despite the fact that hand hygiene is mandatory
in food production as part of sanitary and hygienic
requirements, the level of compliance still leaves much
to be desired. During the coronavirus pandemic, hand
hygiene should be the golden safety rule and an essential
element of personal hygiene. Hand washing is obligatory
before commencing work; whenever your hands become
dirty; after every trip to the toilet; after touching raw
materials or packaging; between process operations,
e.g. when proceeding from raw materials to finished
products; after touching your hair, nose, ears, and
eyes; after smoking or eating; after handling garbage,
chemicals, or cleaning tools, etc. Proper hand washing is
of particular importance for waitpersons, administrators,
and cashiers, i.e. those who touch banknotes or various
surfaces in the retail space. Any unprotected contact with
environment and equipment without proper disinfection
afterwards can be dangerous if one subsequently touches
one’s oral, nasal, or ophthalmic mucous membrane
or damaged skin. Visitor service area staff should be
especially careful [24].
Personal protective equipment for employees.
There are currently no specific COVID-19 infection
protection measures for catering staff. Taking into
account the transmission route by airborne droplets,
all employees are to wear goggles, face masks, gloves,
protective clothing, and mop caps. Disposable protective
equipment should be changed every 2–3 h [22, 23].
Disinfection. FSEs must take strict and effective
disinfection measures according to the current sanitary
standards. Public, industrial, storage, and utility areas
should be washed and disinfected on a regular basis,
including door handles, chairs, and tables. The same
procedure holds for elevators. Employees that have to
deal with cash and plastic cards, e.g. managers, cashiers,
accountants, couriers, etc., should avoid touching any
objects of shared use, e.g. terminals, cash desks, etc.,
after direct contact with the specified items [25, 26].
The list of scientifically approved anti-coronavirus
surface disinfectants includes a 62–71% ethanol solution
and a 0.1% sodium hypochlorite solution [23, 24, 27,
28]. Disinfectants that contain even small doses of these
substances in the required concentration proved most
effective. The Research Institute of Disinfectology of
the Federal Service for Supervision of Consumer Rights
Protection and Human Welfare published a longer list of
registered disinfectants.
Every FSE should have a sufficient supply of
disinfectants. Disinfection procedures require protection
of skin, eyes, and breathing organs. The personnel
responsible for disinfection should wear protective
equipment, i.e. face masks or respirators, goggles, and
gloves, according to the specific application instructions.
All in all, FSE personnel should constantly monitor
the existing risk assessments and safe working systems.
Managers are to update the personnel responsible for
human safety on any relevant official information.
Managers should follow updates on the epidemic in
other countries to be aware of possible new transmission
routes. For instance, FSEs purchase raw materials of
animal and fish origin to produce catering products. The
World Health Organization published recommendations
that are aimed at transmission risk reduction from
animals to humans at the market. Visitors of live animal
markets, seafood markets, or animal products markets
should practice general hygiene measures. They include
regular hand washing with soap and water after touching
animals and animal products, avoiding touching eyes,
nose, or mouth, and avoiding contact with sick animals
or spoiled animal products. Buyers should also avoid
contact with potentially contaminated livestock wastes
or spilt liquids in stores and market facilities. Raw
or undercooked animal products can be dangerous
for consumption. According to food safety practices,
raw meat, milk, and animal organs should be handled
carefully to avoid cross-contamination.
CONCLUSION
The outbreak of COVID-19 has become a clinical
threat to people around the world. The World Health
Organization declared COVID-19 a global pandemic.
The situation crippled healthcare, production of first
priority goods, and service industry. Their employees
cannot avoid face-to-face contact with clients while
having to perform their professional duties even
during epidemics. In spite of the fact that all countries
are doing their best to solve the problem, our current
knowledge about the new virus remains limited.
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Scenarios for antiviral therapy and vaccination are still
being developed. As a result, preventive and infection
control measures remain the most effective instrument
to combat the current spread of COVID-19. Scientists
and pandemic experts are studying epidemics of the past
to find options for urgent prevention and treatment of
severe acute respiratory infections caused by COVID-19.
The rapidly growing number of person-to-person
transmission cases delivered a hard blow to the
catering industry. In conditions when self-isolation
has become the main preventive measure, most food
service enterprises switched to delivery or takeaway
sales. However, a complete isolation of food service
enterprises does not seem possible. A significant part
of the population needs food service while at home
or at work. By learning the mechanism of COVID-19
transmission, managers of food service enterprises can
develop measures to reduce the risks. A further analysis
and synthesis of methods should take into account the
national, cultural, economic, and climatic features of
specific countries. Many catering establishments will
draw a lesson from their pandemic experience. On the
one hand, they will understand that failure to comply
with the Hazard Analysis and Critical Control Points
system ruins production safety and increases the risk
of infection. On the other hand, the negative experience
can become a new growth point for the food service
enterprises when they emerge from the crisis.
CONTRIBUTION
The authors were equally involved in writing the
manuscript and are equally responsible.
CONFLICT OF INTEREST
The authors declare that there is no conflict of
interests related to the publication of this article.

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