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Journal of Food Protection, Vol. 61, No.3, 1998, Pages 318-323 Copyright©, International Association of Milk, Food and Environmental Sanitarians

The Incidence of Listeria spp., Salmonella spp., and Clostridium botulinum in Smoked Fish and Shellfish

MAXINE L. HEINITZ1* AND JANELLE M. JOHNSON2

1u.s. Food and Drug Administration, 240 Hennepin Ave., Minneapolis, Minnesota, 55401-1999; and lU.S. Food and Drug Administration, 22201 23rd Drive S.E., Bothell, Washington, 98041-3012, USA

MS 97-81: Received 15 April1997/Accepted 15 July 1997

ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/61/3/318/1658583/0362-028x-61_3_318.pdf by guest on 01 October 2021

The frequency of occurrence of Listeria spp., Salmonella spp., and Clostridium botulinum in samples of smoked finfish and smoked shellfish was analyzed over a 5-year period. Listeria monocytogenes was isolated from 14% of 1,080 samples. For those samples where the smoke process was known, the incidence of L. monocytogenes was higher in cold-smoked than hot-smoked products (51 of 240 cold-smoked compared to 19 of 215 hot-smoked products). Listeria species other than L. monocytogenes were also detected (in 7.2% of cold-smoked and 3.8% of hot-smoked products). The time and temperature smoke processing guidelines are reviewed for a few state authorities. L. monocytogenes was isolated from 15.2% of the 559 samples of foreign origin. There were four countries for which more than 70 samples were analyzed: Canada, Norway, the Philippines, and the United Kingdom. The occurrence of L. monocytogenes in samples from these four countries was 14.3%,23.7%, 0%, and 16.1%, respectively. The 521 samples originating in the United States were processed by 194 plants. Thirty-seven plants in 13 states produced contaminated product. Salmonella species were isolated from 5 (3.2%) of 156 samples tested for this organism. All positive samples were of foreign origin (4 from the Philippines and 1 from the United Kingdom). No C. botulinum spores were detected in any of the 201 vacuum-packed samples tested for this organism.

Smoked fish and shellfish products can be a source of from sewage-polluted waters continues to be a problem. microbial hazards including Listeria monocytogenes, Salmo- Processed seafood products are usually considered to pre- nella species, and Clostridium botulinum. L. monocytogenes sent a lower risk for infections attributed to Salmonella has been identified in several food borne outbreaks, in which species, but outbreaks have occurred. Salmonella paratyphi pasteurized milk (19), coleslaw (46), and soft cheese (29) B infections were associated with consumption of smoked were implicated. This organism has also been isolated from halibut in Germany (33) and a fish-and-chip shop in the a variety of fish and shellfish products (5, 11, 13, 50). An United Kingdom (21). Salmon was the implicated vehicle of epidemic of perinatal listeriosis in New Zealand suggested a infection for Salmonella montevideo food poisoning involv- link to the consumption of raw fish and shellfish (34). Some ing two catered social functions in the United Kingdom (6). sporadic cases have been identified involving undercooked Foodborne C. botulinum intoxication is caused by the fish and mussels (4, 16). Often, however, the source of ingestion of preformed neurotoxin produced by the organ- Listeria outbreaks is never established. ism. The species is divided into seven types, A through G, L. monocytogenes is ubiquitous in nature and able to based on the antigenic specificity of their toxins. C. botuli- grow at low temperatures and in high salt concentrations up num type E is the most prevalent type in marine and to 10% (36). Studies have shown that L. monocytogenes can freshwater environments and has been responsible for most significantly increase in numbers on smoked salmon during of the botulism outbreaks from fishery products (14, 48). storage at 4DC (22, 45). Enhanced virulence of L. monocyto- Outbreaks have usually been due to ethnic preparations of genes has been associated with growth at 4DC (10). Smoked fish involving fermentation or salting, often without removal fish are often packed under vacuum and stored for 3 to 4 of viscera (48). Kapchunka, an uneviscerated salted air-dried weeks under refrigeration. These ready-to-eat food items are whitefish, was responsible for a type E botulism outbreak in potentially high-risk foods. Regulatory agencies in the New York City in 1985 and an international outbreak in United States have adopted a zero-tolerance policy toward 1987 in New York City and Israel (7, 8, 47). Fishborne this organism in ready-to-eat food products. botulism is common in Alaska and Canada in Native Foods commonly involved in transmission of Salmo- American communities, with a seasonal peak from May to nella spp. include eggs, meat and meat products, and milk. October (23). In 1982, a can defect in Alaskan canned Salmonella food poisoning is only occasionally associated salmon was the cause of illness and one death in Belgium with fish other than shellfish (49). Contamination of shellfish from C. botulinum type E toxin (24). This study examines the frequency of Listeria spp., Salmonella spp., and C. botulinum isolation from smoked * Author for correspondence. Tel: 612-334-4100, ext. 126; Fax: 612-334- finfish and shellfish products. The analyses were conducted 4134; E-mail: [email protected] over a 5-year period, 1991 to 1995. J. Food Prot., Vol. 61, No.3 PATHOGENS IN SMOKED FISH AND SHELLFISH 319

MATERIALS AND METHODS or llltnte levels are insufficient, whereby there is the potential for toxin production. Nitrites are permitted in Smoked fish and shellfish samples. Samples of smoked smoked salmon, sablefish, and shad as long as the level does finfish and shellfish harvested and processed in the United States were obtained from local fish processors or distributors. Smoked not exceed 200 ppm. In smoked chub the nitrite requirement fish and shellfish of foreign manufacturers were collected at the is 100 to 200 ppm (9). Water phase salt guidelines vary consignee of the shipment. In most cases at least 10 units of product depending on smoking process, packaging, and presence of (packages or whole fish) were collected from each lot. nitrites. For vacuum-packaged hot- or cold-smoked fish, water phase salt must be at least 3.5% when no nitrites are Listeria species. The FDA protocol for listeria isolation (26, used and at least 3.0% with at least 100 ppm nitrite. For 37) was used to analyze smoked fish products for Listeria species. Briefly, a 25-g portion was added to 225 ml of enrichment broth, air-packaged hot-smoked product, the water phase salt must tryptic soy broth-yeast extract with acriflavin, nalidixic acid, and be at least 3.0% with or without nitrites. For air-packaged cycloheximide. Broth was streaked onto Oxford agar and lithium cold-smoked product, water phase salt should be at least 3.5% without nitrites and 3.0% with a minimum of 100 ppm chloride-phenylethanol-moxalactam agar after incubation for 24 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/61/3/318/1658583/0362-028x-61_3_318.pdf by guest on 01 October 2021 and 48 hours at 30°C. Typical colonies were characterized biochemi- nitrite (20). cally and serotyped with commercial antisera (Difco Laboratories, Effective 18 December 1997 the Food and Drug Admin- Detroit, MI). istration will initiate hazard analysis critical control point Salmonella species. The conventional FDA culture method (HACCP) regulation of smoked seafood (18). The new for Salmonella spp. was used (1). A 25-g portion of product was regulations will have no specific requirements for each blended with 225 mllactose broth for preenrichment followed by individual factor (nitrite, water phase salt, time, and tempera- selective enrichment in selenite cystine broth and tetrathionate ture) for the control of enteric pathogens in the product. The broth. Broths were streaked onto bismuth sulfite agar, xylose lysine regulations will state that a HACCP plan must control the desoxycholate agar, and Hektoen enteric agar. Typical colonies food safety hazard associated with the toxin of C. botulinum were screened biochemically and serotyped when necessary with for at least as long as the shelf life of the product under commercial or CDC antisera (Difco Laboratories, Detroit, MI; normal conditions and conditions of moderate abuse. Centers for Disease Control, Atlanta, GA). L. monocytogenes was isolated from 14% of the 1,080 Clostridium botulinum. Vacuum-packed smoked fish samples samples. Of those samples for which the smoke process was were tested for C. botulinum type E spores using the method of known, a higher incidence of L. monocytogenes was found Kautter et al. (31, 32). A50- to loo-g portion (depending on the size in cold-smoked fish products (Table 1). There was an of the product units) was placed in a sterile Stomacher bag or sterile association with the smoke process and the presence of L. Whirl Pak bag. The product was covered with freshly steamed and monocytogenes (chi-square = 9.931, P = 0.002). A higher cooled Trypticase-peptone-glucose-yeast extract broth. Bags were occurrence of L. monocytogenes was found in cold-smoked sealed after expelling air and incubated at 26 to 28°C for 7 days. fishery products. United States regulations do not include Smears of broth were Gram stained and examined microscopically smoking time and temperature requirements. The time and for typical rods and spores and a mouse bioassay was performed as temperature guidelines for the smoke processes of some necessary for botulinum toxin. individual state authorities and the Association of Food and Nitrites and water phase salt. When nitrite was declared as Drug Officials are summarized in Table 2. Other studies also an ingredient on the product label, samples were assayed for nitrite linked the prevalence of this pathogen to the smoke process as sodium nitrite using the AOAC colorimetric method (3). (hot or cold). Loncarevic et al. (35) found L. monocytogenes Samples were analyzed gravimetrically for moisture (3) and in 11.5% of cold-smoked and only 1.5% of hot-smoked fish volumetrically for chloride expressed as sodium chloride (3). Water from the retail market in Sweden. Farber (17) isolated L. phase salt was calculated by the formula monocytogenes from 31.2% of cold-smoked salmon. R0rvik

% NaCI = [(g NaCl) X 1oo]/[(g NaCl) + (g H20)]. and Yndestad (44) found the prevalence of L. monocyto- genes to be 9% in cold-smoked salmon from Norway. Ben RESULTS AND DISCUSSION Embarek's review (5) also showed, except for hot-smoked New Zealand mussels (which represented only 14 samples), A total of 1,080 smoked finfish and shellfish products a higher incidence of L. monocytogenes from cold-smoked were analyzed between 1991 and 1995. Two hundred one fish than hot-smoked fish. Jemmi and Keusch (30) demon- (18.6%) and 156 (14.4%) of the samples were analyzed for strated that L. monocytogenes does not survive the hot- C. botulinum and Salmonella spp., respectively. All samples (more than 50% of which were smoked salmon) were TABLE 1. Incidence of L. monocytogenes correlated with smoke analyzed for Listeria spp. Vacuum-packed samples were process tested for C. botulinum type E spores and water phase salt. Nitrite content. was quantified when the product label L. monocytogenes results declared it as an ingredient. Number of samples Food and Drug Administration guidelines consider a smoked seafood product violative if L. monocytogenes, Smoke process Negative Positive % Positive Salmonella species, or preformed C. botulinum toxin is Cold 51 17.5 detected (20). Guidelines also consider a product violative if 240 Hot 215 19 8.1 C. botulinum type E spores are detected and water phase salt 320 HEINITZANDJOHNSON J. FoodProt.,Vol.61, No.3

TABLE 2. Time and temperature guidelines for preparation of TABLE 3. Incidence of L. monocytogenes in smoked fish and smokedfish shellfish from different countries

Temperature"andtime Numberof Numberof % Countryoforigin samplescollected samplespositive positive StateororganizationReference Coldsmoking Hotsmoking Belgium 1 0 0.0 Association of 2 :0;32.2°,:0;20h ~62.8°, ~30 min Canada 84 12 14.3 Food and Drug :0;10°, :0;24h Canary Islands 1 1 100.0 Officials Chile 8 3 37.5 :0;48.9°,:0;6h Colombia 1 0 0.0 Maine 38 :0;32.2°,:0;20h ~62.8°, ~30 min Denmark 9 3 33.3 :0;10°, :0;24h Ecuador 4 0 0.0 Minnesota 39 ~82.2°, ~30 minb Faeroe Islands 1 0 0.0 New York 40 :0;32.2°,:0;20h ~62.8°, ~30 min France 2 1 50.0 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/61/3/318/1658583/0362-028x-61_3_318.pdf by guest on 01 October 2021 :0;10°, :0;24h Gambia 1 0 0.0 :0;48.9°,:0;6h Germany 2 0 0.0 Wisconsin 51 :0;32.2°,:0;20h ~62.8°, ~30 min Ghana 4 0 0.0 :0;10°,:0;24h Guyana 1 0 0.0 :0;48.9°,:0;6h Iceland 38 4 10.5 Ireland 18 4 22.2 a Degrees Celsius. Italy 1 1 100.0 b Minnesota regulations allow only one smoke process. Japan 1 0 0.0 Korea, Republic of 10 0 0.0 smoke process (internal temperature 65°C, 20 min, followed Multiple countriesa 3 0 0.0 by 60°C, 45 min). Jemmi and Keusch postulated the L. Netherlands 1 0 0.0 monocytogenes source to be postprocess contamination. New Zealand 28 1 3.6 During storage, growth of the organism may occur, even in a Norway 131 31 23.7 Panama 1 0 0.0 high-salt environment, and pose a potential health hazard Philippines 74 0 0.0 (17,28,41,42,43). Eklund et al. (15) established the source Russia 1 0 0.0 and route of L. monocytogenes contamination in fish pro- Sweden 2 2 100.0 cessed by the cold-smoke method. They recommended Switzerland 3 0 0.0 elimination or reduction of the organism on the surface of Taiwan 2 2 100.0 the fish prior to smoking in order to control the hazard. Thailand 1 0 0.0 Listeria species other than L. monocytogenes were also United Kingdom 124 20 16.1 detected in our study with a prevalence of 7.2% in cold- Vanuata 1 0 0.0 smoked and 3.8% in hot-smoked product (overall 5%). Total 559 85 15.2 Listeria innocua was the most common species isolated, followed by Listeria seeligeri. These findings are similar to a More than one country was indicated on the bill of lading. those reported by other researchers. Dillon et al. (11) found the prevalence of other Listeria species in smoked fish papers indicating that the level of L. monocytogenes varied products to be 11.3%, while Loncarevic et al. (35) isolated from 0% in samples from Iceland to 75% isolation in these organisms from 8.7% of the smoked products tested. A samples from New Zealand. Hudson et al. (27) reported a higher incidence of L. monocytogenes than L. innocua in high incidence of L. monocytogenes in smoked finfish (in 8 samples of smoked fish and shellfish is the opposite of the of 25 samples) and smoked shellfish (in 5 of 25 samples). incidence of these organisms in samples from commercially Mussels accounted for all five of the shellfish samples prepared sandwiches (25), in which L. innocua is more positive for L. monocytogenes in their study. In the present prevalent than L. monocytogenes. Processing environment, study L. monocytogenes was isolated from 1 sample (hot- processing methods, sample matrices, and seasonal sam- smoked mussels) of the 28 samples from New Zealand. (In pling may all contribute to these differences, which warrant the present study half of the samples from New Zealand further study. The incidence of L. monocytogenes in samples were smoked mussels.) We will not speculate about why from products of foreign origin was 15% (Table 3). Al- certain countries have a higher than average incidence of L. though the present study does not have enough samples from monocytogenes because we do not have access to the details anyone country for statistical significance, there are coun- of processing and handling of the products. tries for which 70 or more samples were analyzed. Of those The results of L. monocytogenes analysis results of countries, the highest percentage of L. monocytogenes was smoked fish processed in the United States are summarized found in smoked fish from Norway, followed by the United in Figure 1. The 521 samples tested were collected from 194 Kingdom, and Canada. In comparison, none of the 74 processing plants. The figure shows the states containing the samples analyzed from the Philippines were positive for L. 37 plants in which L. monocytogenes was detected (37 of monocytogenes. L. monocytogenes has routinely been iso- 194 = 19.1%). The locations of141 plants from which no L. lated from smoked fishery products from a variety of monocytogenes was isolated are also shown. Sixteen of the countries (12, 17, 35, 44). Ben Embarek's report (5) cites 521 samples collected carried no indication of the city or J. Food Prot., Vol. 61, No.3 PATHOGENS IN SMOKED FISH AND SHELLFISH 321 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/61/3/318/1658583/0362-028x-61_3_318.pdf by guest on 01 October 2021

Results c:=:::J None Found E:::J Positive

FIGURE 1. Location of United States smoked fish processors sampled and results ofL. monocytogenes analysis. state in which they were produced. Each of those samples samples were Salmonella groups B, Et. Ez, and E4 (Senften- was considered, in this study, to originate from a separate berg). We are not aware of published surveys of smoked fish processing plant. for contamination with Salmonella species. We postulate the None of the 16 plants in Minnesota produced L. hot-smoke process (Table 2) was sufficient to destroy the monocytogenes-contaminated product whereas 10 of 16 organism and that the source of contamination was postpro- plants in the state of New York produced product in which cess. the pathogen was detected. The smoke process temperature No C. botulinum spores were detected in any of the 201 requirement (Table 2) is higher in Minnesota than in New vacuum-packed samples tested. Growth and toxin produc- York. Jemmi and Keusch (30) found that a temperature of tion of C. botulinum type E is inhibited in these products by 65°C was adequate to destroy L. monocytogenes in hot- a combination of salt or salt plus nitrite, smoke, and smoked fish. We are not prepared on the basis of available refrigerated storage below 38°F (3.3°C) (14). Twenty-five of information to speculate whether the process temperature or the 83 samples in the present study, for which analytical some other critical control factors may contribute to this details were available, had a mean water phase salt concen- difference in incidence. tration less than 3.0% (mean = 3.61; standard devia- Failure to control pathogen contamination in food tion = 1.55). Only a few samples had nitrites declared on production can have serious health and economic conse- the label. The potential for botulinal toxin production exists quences. Dillon et al. (11) expressed great concern about the for such samples, especially over prolonged periods of potential economic impact on the entire industry unless the refrigeration where temperature abuse may occur. problem can be controlled. Five of the 37 U.S. firms This study indicates foodborne pathogen contamination producing smoked fish contaminated with L. monocytogenes of smoked fish and seafood is a consumer health risk went out of business. Six firms also went out of business of because these are ready-to-eat foods. Therefore these prod- the 157 firms which did not have L. monocytogenes- ucts should be routinely tested for presence of L. monocyto- contaminated product. genes and Salmonella spp. and, if packaged by vacuum or Salmonella species were isolated from 5 (3.2%) of the modified atmosphere packaging, analyzed for C. botulinum. 156 smoked fish samples. Four of the five samples were from the Philippines (two were scad, the market name of the ACKNOWLEDGMENTS other two fish was not given). The fifth, salmon, was The authors express their deep appreciation to the microbiologists in packaged in the United Kingdom. Two of the samples FDA's district laboratories throughout the United States who conducted the positive for Salmonella spp. were hot smoked; the smoke analyses and recorded the detailed analytical results into the FDA's Microbiological Information System (Micro-IS). We gratefully acknowl- process for the other three was not provided. The names of edge Albert H. Schwab, Robert Snell, and David Wieneke, FDA, Sita Tatini, the processors were not available. More than two-thirds of Department of Food Science, University of Minnesota, and Douglas M. the 156 samples tested for Salmonella spp. were of foreign Hawkins, Department of Applied Statistics, University of Minnesota, for origin. The smoke process was known for one-third of the their helpful comments on the manuscript, Sue Hakomaki, Academic and Distributed Computing Services, University of Minnesota, for expert samples, equally divided between hot- and cold-smoke assistance on SAS programming language, and Luke Lara, FDA, for processes. The Salmonella serotypes isolated from the five development of the figure. 322 HEINITZ AND JOHNSON J. Food Prot., Vol. 61, No.3

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