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. 2014 Jun 10;3(2):1701. doi: 10.4081/ijfs.2014.1701

Hygienic-Sanitary Evaluation of Sushi and Sashimi Sold in Messina and Catania, Italy

Daniele Muscolino 1, Filippo Giarratana 1, Chiara Beninati 1, Agata Tornambene 1, Antonio Panebianco 1, Graziella Ziino 1,✉
PMCID: PMC5083873  PMID: 27800343

Abstract

Sushi and sashimi are traditional Japanese food, mostly consisting of raw seafood alone or in combination with rice. Eating sushi and sashimi has become popular in many countries even outside Japan. This food is not free from health risks such as ingestion of pathogenic bacteria or parasite. The aim of this study was to investigate on hygienic-sanitary quality of sushi and sashimi sold in the cities of Messina and Catania, Southern Italy. Fifty samples (38 sushi and 12 sashimi) were analysed to determinate the aerobic mesophilic bacteria (AMB), psycrophilic bacteria (PB), Enterobacteriaceae, specific spoilage organisms (SSOs), Pseudomonas spp., coagulase-positive staphylococci, micrococci, Vibrio spp., Bacillus cereus, Salmonella spp. and Listeria monocytogenes. In sushi, AMB ranged from 5.00 to 8.18 log CFU/g, PB from 4.70 to 7.13 log CFU/g, Enterobacteriaceae from 1.41 to 6.67 log CFU/g, while SSOs and Pseudomonas spp. from 3.49 to 7.72 and from 3.36 to 8.00 log CFU/g, respectively. Micrococci ranged from 3.53 to 5.03 log CFU/g and coagulase positive staphylococci were found in 16 samples (2.00 to 3.60 log CFU/g). Bacillus cereus was found in 3 samples (1.70 to 4.00 log CFU/g), while Vibrio spp. was found in 15 of the sushi samples (1.70 to 3.70 log CFU/g). In sashimi, the AMB, PB and SSOs values were higher than 7.00 log CFU/g, Pseudomonas spp. and Enterobacteriaceae were from 6.00 to 8.00 log CFU/g, while Vibrio spp. were found in six samples with means of 2.00 log CFU/g. No Salmonella spp. and Listeria monocytogenes were detected in all sushi and sashimi samples.

Key words: Sushi, Sashimi, Microbiological quality, Food hygiene

Introduction

Sushi and sashimi are traditional Japanese food, though in recent years they attracted a large number of European consumers. Sushi was originally prepared in Southeast Asia as a method to preserve fish. It was formerly used for carps, that were caught, gutted, salted and preserved between two stones, and left to ferment for a period ranged from one to three years. Sushi is prepared with cold cooked rice acidified with vinegar, and it is shaped into bite-sized pieces and topped with raw or cooked fish, or formed into a roll with fish, eggs or vegetables, and wrapped in seaweed (nori) (Atanassova et al., 2008).

The sashimi, instead, is characterised by the use of fish and shellfish, which are cut into thin slices and served with several sauces (e.g. wasabi, soy sauce or ponzu sauce), and accompanied with daikon roots (Food and Environmental Hygiene Department HKSAR, 2000).

Sushi and sashimi are ready-to-eat (RTE) food and regarded as a potentially hazardous. Frequently, indeed, foodborne diseases related to sushi e sashimi consumption have been reported (Adams et al., 1994; Atanassova et al., 2008; Barralet et al., 2004; Food and Environmental Hygiene Department HKSAR, 2000; Masotti et al., 2004; Millard and Rockliff, 2003; NSW Food Authority, 2006). Pathogenic bacteria such as Salmonella spp., Staphylococcus aureus, Vibrio parahaemolyticus, Vibrio cholerae, Listeria monocytogenes, Bacillus cereus can occur in materials used for their preparation such as fish, seafood products, vegetables and rice.

In the light of the significant increase of consumption of traditional Japanese foods in Italy and due to the attention of EC Reg. 2073/05 for RTE foods (European Commission, 2005), the aim of this study was to investigate the microbiological quality of sushi and sashimi sold in Messina and Catania (Southern Sicily, Italy).

Materials and Methods

The study was carried out on 38 samples of sushi and 12 of sashimi collected from restaurants, sushi bar and take-away outlets of Messina and Catania. Different types of sushi were analysed: hosomaki, nigirizushi and uramaki. In addition to rice and nori seaweed, they were made with smoked fish (salmon, tuna and swordfish), canned tuna in oil, surimi, fish eggs, cream cheese, cucumbers, carrots, avocado, sesame or poppy seeds. The sashimi samples were prepared with salmon, tuna or swordfish fillets.

All samples, transported to the laboratory under refrigerated condition, were analysed for the following bacteriological determinations: aerobic mesophilic bacteria (AMB) (ISO 4833:2004; UNI, 2004), psychrophilic bacteria (PB) (ISO 17410:2001; ISO, 2001), specific spoilage organisms (SSOs) (Lyngby Iron Agar at 25°C for 5 days), Enterobacteriaceae (ISO 21528-2:2004; ISO, 2004), Pseudomonas spp. (Pseudomonas agar base with CFC supplement at 30°C for 48 h), quantitative and qualitative determination of Vibrio spp. (Thiosulphate Citrate Bile Salt Sucrose Agar at 37°C for 24 h), coagulase-positive staphylococci and micrococci (ISO 6888-2:1999; ISO, 1999), Bacillus cereus (ISO 7932:2005; UNI, 2005a), Listeria monocytogenes (ISO 11290-1:2005 and ISO 11290-2:2005; UNI, 2005b, 2005c) and Salmonella spp. (ISO 6579:2002; ISO, 2002).

Colonies of Enterobacteriaceae, isolated from tuna sashimi, were identified by API 20 E (bioMérieux, Marcy l’Etoile, France). Then, they were cultured on Niven medium, in order to evaluate their istidino-decarboxylase activity. The pH detection of all samples was made with pH-meter WTW pH330i.

Results

In sushi samples, the AMB ranged from 5.00 to 8.18 log CFU/g, and PB from 4.70 to 7.13 log CFU/g (Table 1). The Enterobacteriaceae showed a wide range from 1.41 to 6.67 log CFU/g. The highest percentage of samples for AMB (44.74%) and PB (47.37%) were from 6.00 to 7.00 log CFU/g, while for Enterobacteriaceae (44.74%) from 4.00 to 5.00 log CFU/g. Specific spoilage organisms and Pseudomonas spp. ranged from 3.49 to 7.72 log CFU/g and from 3.26 to 8.00 log CFU/g respectively. Coagulase-positive staphylococci were isolated in 16 samples (42.11%) with values from 2.00 to 3.60 log CFU/g. Micrococci had values between 3.53 and 5.03 log CFU/g. Bacillus cereus was detected in 3 samples (7.89%), with values between 1.70 and 4.00 log CFU/g and Vibrio spp. were observed in 15 samples (39.47%) ranging from 1.70 to 3.70 log CFU/g. In all sushi samples, no Salmonella spp. and Listeria monocytogenes were found. The pH of the rice ranged from 4.6 to 6.6 (mean 5.6), while the pH of fish from 5.06 to 8.4 (mean 6.06).

Table 1.

Microbiological results of sushi samples.

Value (log CFU/g) Sushi samples distribution (%)
AMB PB SSOs Pseudomonas spp. Enterobacteriaceae
1.00<2.00 - - - - 1 (2.63)
2.00<3.00 - - - - 2 (5.26)
3.00<4.00 - - 2 (5.26) 2 (5.26) 4 (10.53)
4.00<5.00 - 2 (5.26) 1 (2.63) 5 (13.16) 17 (44.74)
5.00<6.00 13 (34.21) 11 (28.95) 16 (42.11) 13 (34.21) 9 (23.68)
6.00<7.00 17 (44.74) 18 (47.37) 11 (28.95) 13 (34.21) 5 (13.16)
7.00<8.00 7 (18.42) 7 (18.42) 8 (21.05) 3 (7.90) -
>8.00 1 (2.63) - - 2 (5.26) -
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CFU, colony forming unit; AMB, aerobic mesophilic bacteria; PB, psychrophilic bacteria; SSOs, specific spoilage organisms.

In sashimi samples, the AMB, PB and SSOs were higher than 7.00 log CFU/g (Table 2). The Enterobacteriaceae and Pseudomonas spp. were from 6.00 to 8.00 log CFU/g. Vibrio spp. were observed in 6 samples (50%) (≥2.00 log CFU/g), while in all 12 samples (100%) no Salmonella spp. and Listeria monocytogenes were found.

Table 2.

Microbiological results of sashimi samples.

Value (log CFU/g) Sashimi samples distribution (%)
AMB PB SSOs Pseudomonas spp. Enterobacteriaceae
6.00<7.00 - - - 6(50) 6(50)
7.00<8.00 7 (58.33) 8 (66.67) 8 (66.67) 6(50) 6(50)
>8.00 5 (41.67) 4 (33.33) 4 (33.33) - -
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CFU, colony forming unit; AMB, aerobic mesophilic bacteria; PB, psychrophilic bacteria; SSOs, specific spoilage organisms.

Twenty-five colonies of Enterobacteriaceae, isolated from tuna sashimi, were identified as Citrobacter freundii, Klebsiella oxytoxa, Serratia liquefaciens, Rahnella aquatilis and Raoultella ornithinolytica. All these strains showed istidino-decarboxylase activity on Niven medium. The pH of sashimi samples examined ranged from 5.86 to 8.4 (mean 6.98).

Discussion

The microbiological limits for RTE foods such as sushi and sashimi are defined by EC Reg. 2073/2005 (European Commission, 2005). This regulation takes in account two food safety criteria: Salmonella spp. (absence in 25 g of sample) and Listeria monocytogenes. Sushi and sashimi characterised by shelf-life less than five days are RTE foods unable to support the growth of L. monocytogenes. For this reason, L. monocytogenes must be less than 100 CFU/g during the shelf-life of these products.

All samples examined in this study were in accordance with the microbiological criteria of EC Reg. 2073/2005 (European Commission, 2005). On the basis of standards from Gilbert et al. (2000), Hong Kong (Food and Environmental Hygiene Department HKSAR, 2000, 2007) and Food Standards Australia (Food Standards Australia New Zealand, 2001; ANZFA, 2001), 6 sushi samples (21.05%) examined were considered unsatisfactory for AMB criteria (Table 3). Thirty-one samples (81.58%) were unsatisfactory for Enterobacteriaceae and 6 (15.79%) for coagulase-positive staphylococci. Seventeen samples resulted borderline for AMB (44.74%), 6 for Enterobacteriaceae (15.79%), 3 for B. cereus (7.90%) and 11 for coagulase-positive staphylococci (28.95%), as showed in Table 3.

Table 3.

Distribution of results in accordance with international microbiological standards for sushi.

Parameters Acceptable (%) Borderline (%) Unsatisfactory (%)
Aerobic mesophilic bacteria 13 (34.21) 17 (44.74) 8 (21.05)
Enterobacteriaceae 1 (2.63) 6 (15.79) 31 (81.58)
Bacillus cereus 35 (92.10) 3 (7.90) -
Coagulase-positive staphylococci 21 (55.26) 11 (28.95) 6 (15.79)
Salmonella spp. 38(100) - -
Listeria monocytogenes 38(100) - -
Vibrio parahaemolyticus 38(100) - -
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High bacterial charges as well as potentially pathogen microorganisms were observed in sushi and sashimi examined as previously reported by several authors (Adams et al., 1994; Atanassova et al., 2008; Barralet et al., 2004; Millard and Rockliff, 2003). In this regard, Atanassova et al. (2008) described average AMB values of 6.3 log CFU/g in fresh sushi samples. Salmonella spp. and L. monocytogenes were found in 1.6 and 1.2% of samples respectively, while Staphylococcus aureus showed a charge of 2.2 to 4.7 log CFU/g (Atanassova et al., 2008). The microbiological status of sushi and sashimi reflects the microbiology of materials used for their preparation. The detection of Vibrio spp. is indeed related to the fish and shellfish products used (Giuffrida and Panebianco, 2008), while B. cereus has been reported in plant foods (especially rice) (Eglezos et al., 2010). Salmonella spp. and L. monocytogenes can occur in vegetables and dairy products (cheese), while the finding of S. aureus is an evidence of human contact during the preparation of food (Nogara et al., 2004).

Conclusions

This study confirms that the production of sushi and sashimi of good quality obviously depends on the choice of raw materials, as also reported by Atanassova et al. (2008) and Millard and Rockliff (2003). A good rice acidification (pH of the rice must be less than 4.6) and the maintaining of cold chain during preparation and storage are also essential to obtain products of good microbiological status. Finally, a proper training of personnel who manipulates this easily perishable food is desirable.

Further bio-molecular investigations will be necessary to confirm the istidino-decarboxylase activity of Enterobacteriaceae strains isolated from tuna sashimi as suggested by Mancusi et al. (2013). The presence of hista-mine-producing bacteria on sashimi could also represent a potential toxicological hazard.

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