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Assessment of food business operator training on parasitological risk management in sushi restaurants: a local survey in Florence, Italy.


Over the last few decades, typical Japanese dishes made of raw fish, such as sushi and sashimi, have become more common in the diet of the Western world (Bestor, 2000). The reason for this success is mainly the growing interest of Western consumers for both exotic tastes and "lightly preserved" seafood products, perceived as more wholesome and genuine than processed ones (Bucci et al., 2013).

It has been estimated that the number of sushi restaurants outside of Japan ranged from 14,000-18,000 (Matsumoto, 2007). In the U.S., Japanese cuisine began to spread in the 1970s and between 1988-1998, the number of sushi restaurants quadrupled. Currently in the U.S. there are about 5,000 sushi restaurants (Hsin-I Feng, 2012; Japan External Trade Organization, 2013). In the European Union (EU), the first Japanese restaurant opened in Dusseldorf (Germany) in 1973, but the sushi boom began in the late 1990s and the first sushi chain opened in London in 1997 (Japan External Trade Organization, 2013). Then, the exponential growth of Japanese restaurants was mostly determined by the conversion of other ethnic food business activities in sushi bars or restaurants (Farrer, 2015; Latham & Wu, 2013; Matsumoto, 2007). In fact, some Chinese restauranteurs began to realize as early as in the 1990s that switching to Japanese food business activities, or including Japanese delicacies in their menus, would give their enterprises a greater mass appeal and financial boost (Cwiertka, 2001).

The preparation of sushi and sashimi has always required qualified personnel because these products need continuous and constant attention during all stages of preparation and serving. In Hong Kong for example, sushi and sashimi are classified as restricted foods (Food Business Regulation, 2010) and both producers and vendors have to obtain a specific endorsement (Hsin-I Feng, 2012).

Beyond the microbiological and chemical issues (Atanassova, Reich, & Klein, 2008; Food and Environmental Hygiene Department of Hong Kong, 2000; Hsin-I Feng, 2012), one of the main risks associated with the consumption of raw fish is the presence of infective parasites such as tapeworms (cestodes), flukes (trematodes), and roundworms (nematodes) (Hsin-I Feng, 2012). Although fish-borne zoonotic trematodes are estimated to infect >18 million persons, those at risk equal more than half a billion worldwide; trematodes are a major public health problem in particular in Southeast Asia, where they are found in mainly freshwater and brackish water fish species (Chai, Murrell, & Lymbery, 2005; World Health Organization, 1995).

In Italy, all the confirmed cases of opisthorchiasis were associated with the consumption of raw fillets of tench (Tinca tinca) (Pozio, Armignacco, Ferri, & Gomez Morales, 2013). In regard to cestodes, the most important fishborne zoonosis is diphyllobothriasis, an intestinal infection caused by the fish tapeworm Diphyllobothrium spp. (Chai et al., 2005). Infective larvae (plerocercoid) of Diphyllobothrium latum, the species most often associated with human infections, reside in the muscles of trout, salmon, pike, and sea bass (Nawa, Hatz, & Blum, 2005). Additionally, D. nihonkaiense, the Asian species, has been identified in Japanese patients who had eaten wild salmon sashimi (Ando et al., 2001); it has also been involved in human cases in Switzerland and in France related to consumption of raw Pacific Chum salmon (Oncorhynchus keta) (Wicht, de Marval, & Peduzzi, 2007). Freshwater fish species, however, are not commonly used for the preparation of sushi and sashimi in Europe (Armani et al., 2017).

Roundworms, such as Anisakidae, represent a very high risk for sushi consumers as they are widely distributed in marine aquatic environments and their very small infectious larvae are difficult to visually detect in muscle (Hsin-I Feng, 2012). In humans, Anisakidae are responsible for a zoonotic disease called anisakidosis (Kassai et al., 1988), which may be associated to either noninvasive forms, generally asymptomatic, or invasive forms, characterized by gastrointestinal symptoms (acute or chronic). Moreover, an IgE-mediated allergic reaction can be developed after ingestion of anisakids (alive and dead) (Daschner, Alonso-Gomez, Cabanas, Suarez-de-Parga, & Lopez-Serrano, 2000; Dominguez-Ortega et al., 2001).

Most human infections are caused by the ingestion of raw fish infected with live third-stage larvae (L3) of Anisakis spp. and Pseudoterranova spp. (Anisakidae family) (Chai et al., 2005; Lymbery & Cheah, 2007), whereas the zoonotic potential of Contracaecum spp. (Anisakidae family) is questionable (Yagi et al., 1996) and Hysterothylacium spp. (Raphidascarididae family) is considered a nonzoonotic nematode (Angelucci et al., 2011). In the last decade, there have been about 20,000 cases of human anisakidosis, with a marked prevalence in Japan (90% of the cases) (Abe, 2008; Bucci et al., 2013).

In Europe, the incidence seems to be, on an average, 20 cases per country per year (Lima dos Santos & Howgate, 2011; Orphanet, 2014). In Italy, where the species most frequently associated with human cases is Anisakis pegreffii (Mattiucci et al. 2013), 54 cases were described between 1996-2011, mainly in the southern regions. This finding is probably related to the frequent consumption of traditional preparations made from raw fish (marinated anchovies) (Griglio et al., 2012; Pozio, 2004). It is not possible, however, to have a precise estimation of the confirmed cases of anisakidosis and of the sources of infection because anisakidosis is still misdiagnosed (Beaudry, 2012; De Liberato et al., 2013; Mattiucci et al., 2011). Moreover, no data on human cases of anisakidosis were reported in the last available EU summary report on trends and sources of zoonoses, zoonotic agents, and foodborne outbreaks (European Food Safety Authority [EFSA], 2015).

To limit as much as possible the risk from foodborne parasitic zoonoses, particularly anisakidosis, a series of regulations aimed at the management of such risk have been issued in EU and the 28 EU member states (D'Amico et al., 2014). According to EU regulations, the FBO has become the main responsible person for food products and--in order to guarantee the health of the consumers--the FBO is required to develop, implement, and maintain procedures based on hazard analysis and critical control points (HACCP) procedures. Regarding the control of parasites, the regulation and its amendments (Specific Hygiene for the Hygiene of Foodstuffs Regulation, 2004) state that fishery products, to be consumed raw or almost raw, and those that undergo a cold smoking process (core temperature <60 [degrees]C), must be previously frozen at a temperature not exceeding -20 [degrees]C (in each part of the mass) for at least 24 hours or at -35 [degrees]C for at least 15 hours. These treatments are effective for the killing of larvae of parasites different from trematodes, such as cestodes and nematodes (Treatment to Kill Viable Parasites in Fishery Products for Human Consumption Regulation, 2011).

Since 2011, according to the regulations, the preventive treatment also can be carried out at the retail and catering level. In this regard, FBOs must be equipped with an appropriate and certified blast chiller, which is a device that quickly lowers the temperature of foodstuffs, and is exclusively used to perform the freezing treatment and not to preserve foods (D'Amico et al., 2014).

Therefore, it is clear that adequate training of FBOs is essential for a proper management of the parasitological risk associated with raw fish products and for an effective implementation of specific procedures (Jones, Anderson, Schulkin, Parise, & Eberhard 2011; Kojima, Usuki, Mizokami, Tanabe, & Machi, 2013; Pekmezci, 2014). It follows that managers of sushi restaurants should thoroughly educate employees on the proper way to prepare and handle raw-fish products (Hsin-I Feng, 2012). In particular, employees should be able to monitor the critical control points (CCPs) and take corrective actions.

The survey performed in this study was made to evaluate the training level of some FBOs operating in the city of Florence who are responsible for the preparation and serving of raw seafood dishes at ethnic restaurants. Through the use of a questionnaire, we tried to understand the level of knowledge of the respondents regarding parasitological risk related to the presence of nematodes and the management measures required by European laws to reduce such risk to an acceptable level. A first survey, carried out in 2012, was subsequently repeated at the same ethnic restaurants in 2014, to assess any improvements.

Materials and Methods

The survey was developed and conducted by the Department of Veterinary Sciences (Inspection Section) at the University of Pisa, together with the staff of the Local Health Authority (LHA) No. 10 of Florence and the Experimental Zooprophylactic Institute (Section of Pisa). Initially, a census of the ethnic restaurants serving sushi in the city of Florence was done by selecting them both from the registry office of LHA and through an online search using keywords, such as sushi, Florence, restaurants, raw fish, take-away, Japanese food, and sushi bars. Then, FBOs were approached in person for approval to conduct an interview. During the first survey, carried out in the period May-September 2012, 23 FBOs agreed to participate. During the second round of surveys (between May-September 2014), however, only 18 of the 23 FBOs previously interviewed partook in the survey (Table 1).

The 16-question survey was structured in three main sections. Section 1 aimed at collecting the main characteristics of the food business activity such as the category (traditional restaurant, sushi bar, take away, other), the activity carried out (preparation and serving on site, preparation on site and take away, or catering) and the frequency of production (daily, weekly, on demand, other). Section 2 focused on the type of preparations made (raw or almost raw products, marinated and/or salted products, composite products), the seafood species used (fish, mollusks, crustaceans) and the suppliers (fishermen, wholesalers, fishmongers [fish shops], fish markets), as well as whether raw materials were purchased fresh, frozen, or thawed. Lastly, in section number 3, in order to better understand the degree of FBO knowledge, we posed some open questions about the parasitological risks associated with the consumption of raw fish, and the treatments and corrective measures implemented by the FBOs.


With regard to the activities category, in 2012, 13% of FBOs prepared and served sushi on site (i.e., traditional Japanese restaurant); in addition to this, 43.5% also offered take-away service and 26% offered serving on site, in a sushi bar, or take away. In 2014, we interviewed only 18 FBOs because four of them refused to participate again in the survey and one FBO had closed his activity, but the survey responses were quite similar (Table 1).

In both surveys, most of the ethnic restaurants analyzed were managed by FBOs of Chinese origin (68% in 2012 and 78% in 2014), followed by Japanese (45% in 2012 and 11% in 2014), and Italian (27% in 2012 and 11% in 2014).

With regard to the type of product, in 2012, the majority (61%) of FBOs prepared raw or almost raw fishery products, such as sashimi, carpaccio, and sushi, while 26% also prepared marinated or salted products. The remaining 13% prepared only sushi. In 2014, there were no restaurants that prepared only sushi: 50% of FBOs carried out preparations as sushi, sashimi, and carpaccio, while the remaining FBOs also prepared marinated and/ or salted products. The species of fish most commonly used for the preparations of raw dishes were tuna, salmon, sea bass, and sea bream (Figure 1), which, in most of the cases (86.6% in 2012 and 88% in 2014), were purchased as fresh seafood. Among bivalve mollusks, cephalopods, and crustaceans, the most used were octopus, shrimp, and scallop, mainly purchased as frozen (78% in 2012 and 82% in 2014). In much lower percentages, amberjack, turbot, cuttlefish, crab, scampi, and eel were employed (Figure 1). Overall, both in 2012 and 2014, seafood was purchased mostly fresh (87%) and only in a small percentage frozen (3%). The majority of FBOs (89% in 2012 and 91% in 2014) reported they sourced seafood at large-scale retail distributors (wholesalers) and only a small percentage of them (9% in 2012 and 10% in 2014%) from fishmongers.

During both surveys, all the interviewed FBOs claimed to have a self-monitoring plan including the management of food made of raw or almost raw fish. In 2012, 69.5% of FBOs reported being aware that parasites dangerous to consumer health can be present in raw fish. In 2014, the situation was slightly improved: 83% of FBOs asserted to being aware of the risks associated with the presence of anisakids during the preparing and serving of raw or almost raw fish. In 2012, 69.5% of them reported to being aware of the recommended preventive treatment to be applied to fishery products before being served raw. In 2014, this percentage increased to 89%. The majority of FBOs reported that their food business was equipped with a blast chiller and that they applied a freezing treatment on fresh products at their business, while the rest declared that they did not accomplish any type of treatment (Table 2). Only 40% in 2012 and 54.5% in 2014, however, made a proper use of it, according to the parameters set by EU Regulations No. 853/2004 and No. 1276/2011. In both surveys, approximately 20% of FBOs used completely inappropriate temperatures (-5 or -12 [degrees]C), while 80% applied adequate temperatures but for too a short time (15 min-12 hr).


The lack of a proper preparation found in several Japanese restaurants and sushi bars analyzed in this study, which were newly opened and frequently managed by staff of Asian origin, brings to the fore the inadequate application of good practices in the preparation of raw fish. A similar survey conducted by Kwon and coauthors (2011) highlighted the need for training in food safety for staff working in ethnic restaurants, especially with regard to risk behaviors related to the parameters of temperature/time. Although our survey brought to light a slight improvement (2014 compared with 2012) in the knowledge of FBOs on the requirements relating to the freezing treatment (Table 2), there remains a lack of awareness regarding the proper management of parasitological risk. In fact, a good percentage of FBOs interviewed (60% in 2012 and 45.5% in 2014) applied combi nations of time/temperature that were noncompliant and poorly effective in killing the live larvae of anisakids.

Within a sushi foodservice, when raw materials are purchased as fresh, the preventive freezing treatment is the key (and only) CCP of the whole production process for controlling and lowering to an acceptable level the parasitological risk. In addition to strict compliance with EU time/temperature parameters, it is of fundamental importance that FBOs constantly check the correct working temperature of the blast chiller (e.g., through physical measurements such as temperature readings) and that they ensure regular maintenance.

In the catering sector, a proper knowledge of the etiologic agents responsible for foodborne illness and their contributing factors are of pivotal importance, and food handlers must adopt and implement the most effective management practices for preventing outbreaks (Green & Selman, 2005). In fact, improper food handler practices contribute to approximately 97% of foodborne illnesses (Howes, McEwen, Griffiths, & Harris, 1996; Lambrechts, Human, Doughari, & Lues, 2014; Prabhu & Shah, 2014). Therefore, the education of food handlers and managers represent a key element for achieving high quality standards (McIntyre, Vallaster, Wilcott, Henderson, & Kosatsky, 2013; Mortlock, Peters, & Griffith, 1999). Moreover, trained and qualified staff contributes to better inspection scores during official controls (Averett, Nazir, & Neuberger, 2011; Cates et al., 2009). For the aforementioned reasons, the training of FBOs should be relevant to the tasks and activities they hold and must be supervised by the food business managers, who must ensure that staff receive adequate training in food hygiene and in the application of HACCP principles.

It should be noted, however, that shortcomings in ethnic food services are largely due to the language difficulties of foreign-born FBOs, which hamper a proper acquisition of the food safety principles and interfere in communication with local control authorities (Armani, Castigliego, Gianfaldoni, & Guidi, 2011; D'Amico et al., 2014; Green & Selman, 2005; Guidi et al., 2010; Pham, Jones, Sargeant, Marshall, & Dewey, 2010; Rudder, 2006). During the survey, we encountered that many FBOs have a difficult time understanding specific technical terms related to food safety. For those who deal with and are in charge of training courses for foreign-born FBOs, the language barriers should not be underestimated. In fact, worldwide, ethnic workers represent a driving force in the restaurant industry and, to properly communicate the nuances of food safety to them, it becomes indispensable to meet their language needs and therefore adopt language-specific training in the classroom (Niode, Bruhn, & Simonne, 2011). It is pointless to subject operators to educational programs if language barriers are not addressed--ignoring this problem risks ineffective promotion of correct operating procedures. Moreover, the adoption of practical and interactive activities and role-playing to support the theoretical teaching could probably result in a better understanding of the basic principles of food safety and improve retention of safety knowledge by ethnic operators (Clayton, Griffith, Price, & Peters, 2002; Niode et al., 2011).

The risk of infection with anisakid larvae, mainly Anisakis spp., by eating sushi and sashimi is higher in countries where regulations on preventive treatment have not been implemented. Therefore, sushi and sashimi served in Japanese restaurants in the EU can be considered safer and the risk of infection is not as significant as is generally feared (Nawa et al., 2005). Many factors, however, can influence the overall probability of contracting an infection. In fact, because of the culinary tradition, most cases of infection have been reported in Japan (Abe, 2008; Bucci et al., 2013), where the consumption of raw fish is common. Also, the familiarity with raw fish preparation can be crucial for good management and safety of these products. The risk of infection seems to be lower when sushi and sashimi are prepared by professional chefs, who are experts in identifying larval infestation (Chai et al., 2005; Lymbery & Cheah, 2007; Nawa et al., 2005).

In Western countries, in contrast, parasitic infections can be favored by the non-application of freezing treatment, which can be intentionally avoided by FBOs so as not to alter the flavor of sushi and other raw fish delicacies (Nieuwenhuizen & Lopata, 2013). Moreover, as our investigation and other studies have showed (Cwiertka, 2001; Farrer, 2015; Matsumoto, 2007), sushi food services outside of Japan are frequently run by people who are Chinese, Korean, or Vietnamese.

Consumption of raw fish is a more recent trend in China, where many traditional fishery products are salted, dried, and fermented. For this reason, Chinese cooks are less accustomed to the handling and management of raw foods. This failure of proper handling might not be intentional, but rather is often due to the involvement in restaurant operations of family members who are not formally employed (and therefore not formally trained). In these circumstances, food safety and health codes might not be understood or followed (Kwon, Roberts, Shanklin, Liu, & Yen, 2011; Ram, Sanghera, Abbas, Barlow, & Jones, 2000).

The increasing popularity of sushi and sashimi worldwide is one of the factors contributing to the growing incidence of anisakidosis globally over the past 20 years (De Liberato et al., 2013; Mattiucci et al., 2013). The only positive finding of our survey is that almost all respondents seem to have never experienced an infected fish by parasite larvae. This finding is probably because the majority of FBOs buy raw materials at large fishing platforms, which are subject to stringent control systems.

Considering the species mostly commonly used (sea bream, sea bass, and salmon) and also the modest selling price of the finished products, it is plausible that in the majority of cases the seafood came from aquaculture and thus is at a lower risk to contain parasitic larvae. According to the European Food Safety Authority (EFSA) panel report, Scientific Opinion on Risk Assessment of Parasites in Fishery Products, while all wild-caught seafood must be considered at risk of containing any viable parasites, fishery products from aquaculture, such as Atlantic salmon, are raised in floating cages or onshore tanks within free marine areas and fed on compound feedstuffs, and therefore can be considered "Anisakis-free" (EFSA Panel on Biological Hazards, 2010). A research project of the Spanish Asociacion Empresarial de Productores de Cultivos Marinos showed that aquacultured sea bass and sea bream reared in floating cages or onshore tanks have a negligible risk of infection from Anisakis spp. larvae (Asociacion Empresarial de Productores de Cultivos Marinos de Espana, 2012; Penalver, Dolores, & Munoz, 2010). These findings notwithstanding, FBOs operating in Japanese restaurants should be aware that Anisakis spp. can induce severe allergic reactions in sensitive individuals not only after ingestion (the preventive treatment is not able to prevent hypersensitivity reactions), but also during manipulation and handling of infected fish, representing for FBOs an occupational health hazard (Nieuwenhuizen & Lopata, 2013).


The results of this survey, also supported by the findings of inspection controls carried out by LHA of Florence, reveal a worrying situation about the training of FBOs who work in the food businesses under investigation. Participants lacked management practices, knowledge, and science-based resources for dealing with raw-fish products. Despite the undeniable lack of knowledge of FBOs interviewed, the low selling price of the products allows for the assumption that the raw materials were mostly from aquaculture, and therefore naturally less infected by parasitic larvae, which could result in the reduction of the parasitological risk of gastrointestinal anisakidosis associated with sushi consumption.

Although this study was limited to a small geographical area and a small number of samples, it definitely highlights the main problems that many foreign operators and environmental health food safety practitioners face every day around the world. The findings of this study should encourage other more rigorous research to address these issues regarding the safe handling of seafood to be served raw, as it is evident that there is an immediate need to raise the training quality level and make FBOs more aware of the risks related to the products they handle. In this regard, the development of food safety resources, such as written material, flyers, or booklets, in different languages and the use of native speakers during training events, can provide enhanced support to foreign-born FBOs.

Acknowledgement: This study was supported by the Italian Ministry of Health, Projects Code: Current Research Grant IZSLT13/12RC "Valutazione della qualita igienico-sanitaria e commerciale dei prodotti ittici destinati alla ristorazione scolastiche, ospedaliere ed etniche."

Corresponding Author: Andrea Armani, FishLab, Department of Veterinary Sciences, University of Pisa, Via delle Piagge 2, 56124, Pisa, Italy. E-mail:


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Andrea Armani, DVM, PhD

Priscilla D'Amico, DVM

FishLab, Department of Veterinary Sciences, University of Pisa

Luca Cianti, DVM

Local Health Authority of Florence

Marco Pistolesi

FishLab, Department of Veterinary Sciences, University of Pisa

Francesca Susini, DVM

Experimental Zooprophylactic Institute of Lazio and Tuscany

Lorenzo Castigliego, PhD

FishLab, Department of Veterinary Sciences, University of Pisa

Marcella Guarducci, DVM

Experimental Zooprophylactic Institute of Lazio and Tuscany

Daniela Gianfaldoni, PhD

Guidi Alessandra, DVM

FishLab, Department of Veterinary Sciences, University of Pisa
Type of Ethnic Food Activity Analyzed

Ethnic Food Activity                      2012        2014
                                          # (%)       # (%)

Traditional restaurant                  3 (13.0)     1 (5.5)
Sushi bar                                1 (4.4)     1 (5.5)
Traditional restaurant and take away    10 (43.5)   10 (55.8)
Traditional restaurant and sushi bar        0        1 (5.5)
Sushi bar and take away                  2 (8.7)    3 (16.6)
Traditional restaurant, sushi bar,      6 (26.0)    2 (11.1)
  and take away
Food business activity with weekly       1 (4.4)        0
  production of sushi

Questions Asked for the Evaluation of Parasitic Risk Management

Question                                                 Yes
                                                  2012        2014
                                                  # (%)       # (%)

Does your self-monitoring plan include the      23 (100)    18 (100)
preparation of raw/almost raw fish products?

Are you aware of the existence of parasites     16 (69.5)   15 (83.0)
that might be found in the flesh of fish and
that can be harmful for the consumer?

Are you aware of the preventive treatment for   16 (69.5)   16 (89.0)
parasites in fishery products?

Are you equipped with a blast chiller?          17 (73.9)   15 (83.0)

Do you apply the freezing treatment at your
food business activity?

Seafood Species Used for the Preparation of Raw Dishes


Octopus     13%
Sea Bream   9%
Crabs       3%
Eel         2%
Others      5%
Tuna        18%
Salmon      17%
Shrimps     17%
Sea Bass    16%

Scallops         1%
Norway Lobster   1%
Amberjack        1%
Cuttlefish       1%
Turbot           1%


Octopus     11%
Shrimps     15%
Scallops    5%
Others      10%
Salmon      19%   2014
Tuna        17%
Sea Bass    16%
Sea Bream   7%

Grouper      1%
Squid        3%
Eel          3%
Yellowtail   3%

Note: Table made from pie chart.
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Author:Armani, Andrea; Cianti, Luca; Pistolesi, Marco; Susini, Francesca; Castigliego, Lorenzo; Guarducci,
Publication:Journal of Environmental Health
Date:Sep 1, 2017
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