the causative toxin of scombroid-fish poisoning. N Engl J Med 1991; 324:716-720. 13. Hughes JM, Potter ME: Scombroid-fish poisoning: From pathogenesis to.
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Articles
Scombroid Fish Poisoning Underreporting and Prevention Among Noncommercial Recreational Fishers GEORGE A. GELLERT, MD, MPH, MPA; JOHN RALLS, REHS; CORWIN BROWN, MS, REHS; JAMES HUSTON, MS, REHS; and ROBERT MERRYMAN, MPH, REHS, Santa Ana, California
Food-borne diseases, including those caused by seafood products, are common and greatly underreported sources of morbidity. In this article we review the epidemiology of scombroid fish poisoning and its possible relationship to the noncommercial and recreational catch and sale of fish. More than 200/o of all fish sold in the United States is caught by sport fishers, and outbreaks of scombroid fish poisoning have involved improperly handled fish from private catches. We report an outbreak of scombroid fish poisoning among recreational fishers in California. The unregulated sale of recreationally caught fish for consumption and the prevention of scombrotoxism are discussed from the perspectives of public health agencies, clinicians, and the fishing public. Scientific and policy issues that require further attention are highlighted. (Gellert GA, Ralls J, Brown C, Huston J, Merryman R: Scombroid fish poisoning-Underreporting and prevention among noncommercial recreational fishers. West J Med 1992 Dec; 157:645-647)
Food-borne diseases are among the most common and underreported sources of morbidity in the United States. Seafood products are implicated in some of these illnesses. In 1987 US consumption of purchased seafood totaled more than 1.6 billion kg (3.5 billion lb), or 7 kg (15.4 lb) per person per year.' An additional 2 kg per person of recreationally caught fish and shellfish was consumed.' Table 1 summarizes several features of naturally occurring seafood toxins and poisons. The highest morbidity worldwide from fish poisoning (ichthyotoxicosis) results from consuming spoiled scombroid fish.2 The resulting acute illness is called scombroid fish poisoning or scombrotoxism. Scombroid fish poisoning is a chemical food-borne illness associated with the consumption of improperly handled dark-meated fish from the family Scombridae (yellowfin tuna, skipjack, bonito, mackerel), although outbreaks are also caused by consuming nonscombroid fish (mahimahi, bluefish). The histamine toxin is not contracted from the marine environment, but is produced directly within the flesh of the fish as a result of enteric bacterial action and decomposition (decarboxylation of histidine). This process occurs when fish are not refrigerated properly following capture. Symptoms can appear ten minutes to several hours after the affected fish has been eaten, may last about four hours and resemble a classic histamine reaction with facial flushing, sweating, a burning sensation of mouth and throat, diarrhea, dizziness, nausea, vomiting, abdominal cramps, palpitations, and headaches.34 A metallic, sharp, or peppery taste may be experienced. In severe cases, tachycardia, blurred vision, bronchospasm, and respiratory distress may develop. Despite often dramatic and alarming symptoms, the illness is generally benign and self-limited with no sequelae.3'4 Treatment has been directed at controlling symptoms.
fornia have the largest number of outbreaks, but 45 states reported outbreaks from 1983 through 1987.1 Scombroid fish poisoning accounted for 4.5% of all cases of food poisoning reported to the Centers for Disease Control between 1978 and 1982.' Between 1973 and 1987, 116 outbreaks (757 cases) of scombroid fish poisoning were reported to the Centers for Disease Control. Of these, 109 (94%) involved mahimahi, tuna, or bluefish.8 No deaths have been reported. In most states, sanitary conditions for fish caught and sold are required after the fish enters a seafood or packaging plant. There is generally low risk of seafood-borne disease due to control failures during processing or at the food service level. Because it is caused by bacterial spoilage, scombroid fish poisoning is entirely preventable. Once the toxin is formed, however, no available method of fish preparation, including cooking, freezing, canning, and smoking, will render the fish toxin-free. The most important preventive measure is to ensure that fish are chilled rapidly, then refrigerated adequately and continuously from time of catch to preparation. Fish flesh temperature must be maintained below 150C. Reported incidence rates are likely to be considerable underestimates because the illness is generally mild, passes rapidly with no aftereffects, and is therefore not usually reported to health authorities. Scombroid fish poisoning is probably much underreported and misdiagnosed as "fish allergy" because scombrotoxism is symptomatically similar to an allergic response. Seafood intolerance, however, is rare. Food-borne diseases are generally acknowledged to be heavily underreported, and because fish has become an increasingly important part of the American diet in recent decades, it follows that the incidence of scombroid fish poisoning is similarly underestimated.
Epidemiology
Noncommercial and Recreational Catch and Sale of Fish The commercial fishing industry is responsible for few incidents of scombroid fish poisoning, and industry controls
Outbreaks of scombroid fish poisoning involving improperly stored fish from private noncommercial or recreational catches have been reported.356 Hawaii, New York, and Cali-
From the Orange County Health Care Agency, Santa Ana, California. Reprint requests to George Gellert, MD, Orange County Health Care Agency, 515 N Sycamore, Rm 610, Santa Ana, CA 92701.
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for detection are in place. More than 20% of all fish sold in the United States is caught by sport fishers,' and several outbreaks of scombroid fish poisoning have involved improperly handled fish from private catches. No federal or state regulatory agency makes physical examinations of the fish, equipment, or storage conditions on recreational boats. In most states, the fish and game department issues commercial and sport fishing permits. For a higher licensing fee, sport fishers can sell their catches. Fish may pass from noncommercial and recreational boats directly to markets, restaurants, and distributors without being subject to the regulations imposed on the commercial fishing industry (such as inspections or controls before distribution or wholesale and retail sales). Therefore, sport-caught fish present a control problem because they are caught by fishers who either do not enter commercial channels or do so in an unconventional manner.1 Recreational boats that lack adequate refrigeration capability may be chartered by sport fishers. Fish flesh temperatures on such vessels can easily exceed 20°C, and it is not uncommon for fish to be held on deck at even higher temperatures for several hours. Histamine, the causative biochemical agent of the illness, is optimally produced at 30°C. Once a large population of bacteria has been established, residual enzyme activity continues slowly at refrigeration temperatures (0°C to 5°C) even though bacterial growth ceases. Rinsing fish in seawater during handling and cleaning, or for cooling, may contribute to the problem because many of the microorganisms capable of metabolizing elements of fish flesh to histamine are found in the marine environment. Rapid, reliable tests for scombrotoxin are not available.
Report of an Outbreak of Scombroid Fish Poisoning Among Recreational Fishers An outbreak of scombroid fish poisoning occurred among eight persons who had consumed fish caught off the coast of southern California by a recreational fisher in October 1990. Two species of fish were involved, yellowfin and skipjack tuna, with no other foods eaten during the implicated meal. The fish had no foul odor and showed no "honeycombing" of surfaces. Because only yellowfish and skipjack tuna were eaten at the meal, no food-specific attack rates can be calculated. The age range of afflicted persons was 21 to 45 years, with a mean of 33 years. The mean incubation time between the ingestion of fish and the onset ofclinical symptoms was 71 minutes. Of seven persons from whom a history of symptoms was obtained, all had diarrhea, all had headache, four vomited, four had skin flushing or rash, three had dizziness, and two had peculiar oral sensations. No urticaria, pruritus, or bronchospasm was noted. One person sought medical attention. The vessel had been rented commercially at a local dock. The fish were caught at 6 AM by one of the eight people involved on a vessel that had no onboard facilities for refrigerating the catch. The fish were cleaned at about 3:30 PM; the vessel did not dock until 10 PM. The catch was eventually smoked. Six fish specimens were tested for histamine levels. The histamine levels in the specimens ranged from 607 to 840 mg per 100 grams (mean 696 mg, median 667 mg). Because the fish were already smoked when received by the laboratory, it was not possible to differentiate histamine levels by the type of fish. According to the Food and Drug Administration, accept-
THE WESTERN JOURNAL OF MEDICINE
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DECEMBER 1992
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able histamine levels are not to exceed 20 mg per 100 grams, with a hazard action level in tuna defined as 50 mg per 100 grams (fresh fish contains less than 1 mg per 100 grams of histamine).9 The histamine levels identified in fish from this vessel are among the highest recorded in the literature for fish samples obtained in an outbreak setting. Most investigators have reported levels ranging from 10 mg to 250 mg per 100 grams; the highest level reported was 821 mg per 100 grams. 10 The fisher in this incident appeared to be unaware of the potential problems associated with improper refrigeration of scombroid fish. In addition, because these fish were smoked, the persons may have had a false sense of assurance against ill effects from decomposition. Prevention of Scombrotoxism Recreational and subsistence fishers are at risk for scombrotoxism. The food service industry, the public, and health professionals have little understanding of the infrequent but distinct hazards present in seafood. Scombroid fish poisoning is probably highly underreported, and surveillance capabilities must be improved. Disease control will depend on educating sport fishers, especially about the importance of assessing the refrigeration capability of sporting boats as a criterion for chartering a vessel.11 The outbreak reported here is an example of the risk engendered by recreational fishers among those to whom they provide a fish catch. Inspection based on human sensory perception, such as fish appearance and odor, is of no value in detecting and controlling health risks. State health agencies can assume an active role in educating sport fishers on disease prevention. States should provide advisory bulletins on scombrotoxism as an integral component of the licensing process for recreational fishers. Local health agencies should post educational messages about the need for adequate refrigeration at docks and other locations where vessels are chartered, along with information on how to report occurrences of scombroid fish poisoning. If surveillance confirms substantial underreporting, the incidence of scombrotoxic disease may warrant a regulatory role for local health agencies in ensuring that chartered vessels have adequate refrigeration capability to engage in commercial recreational fishing. Remaining Scientific and Policy Issues Several basic scientific and policy issues should be addressed with respect to scombroid fish poisoning. Important questions concern what are accurate incidence estimates of scombrotoxic disease and how best to model estimates. Levels of surveillance must be increased. A recent report of the National Academy of Science, Institute of Medicine, recognized the need for an improved national surveillance system to provide more reliable and comprehensive information on the incidence of seafood-borne disease.1 To reduce confusion, we need to better assess the actual incidence of fish allergy and determine what percentage of cases diagnosed as fish allergy represent misdiagnosis and misclassification of scombroid fish poisoning. The symptoms of the two conditions may overlap because both share a rapid onset and transience, and both may cause such symptoms as vomiting, headache, and nausea. The biochemical and immunologic characteristics of seafood allergies should be investigated further to achieve this objective. Scombroid fish poisoning may be differentiated from allergy by the oc-
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currence of clusters of affected persons. A history of several cases of illness resulting from a common meal, as well as identifying the specific species of fish as one typically associated with scombroid fish poisoning, should raise the suspicion of scombrotoxism. Public health practitioners need to identify the prospective regulatory roles and potential of state and local health departments in helping prevent scombroid fish poisoning. Intergovernmental responsibilities and roles in public education and regulation should be clearly delineated. The possibility of an interjurisdictional regulatory collaboration among selected coastal cities and counties should be explored. Determining what data are available on the number and annual catch weight of recreational fishing vessels for charter will help to direct regulatory activities. The knowledge level of recreational fishers on this public health problem must be heightened. In view of the recent confirmation of histamine as the causative agent of scombrotoxism, 2 physicians and the public should be educated on the use of antihistamines in clinical and self-treatment. This breakthrough in comprehending the basic pathogenesis of scombroid fish poisoning should not, however, obscure the inherent public health nature of this problem and of the most effective control measures. 1' To recommend that physicians counsel patients who fish about the need to chill their catch rapidly and to maintain refrigeration until the fish is prepared for eating is an incomplete solution to this problem."3 State and local health agencies, not clinicians, have the primary responsibility for addressing the prevention of food-borne disease. Maintaining the temperature of fish flesh below 15°C should become routine practice in all types of fishing. Physicians most frequently manage illness when such prevention efforts fail. Health providers nonetheless should be educated on the identification and treatment of scombroid fish poisoning so that they can conduct office-based preventive education among their clients who are known to be sport fishers. Finally, from the environmental health perspective, it is imperative that a rapid assay for detecting scombrotoxin be developed for use in subsequent regulatory activities. If inexpensive and relatively simple, such rapid assays could be made available to the public and, in particular, to recreational fishers. REFERENCES 1. National Academy of Sciences, Institute of Medicine, Food and Nutrition Board: Seafood Safety. Washington, DC, National Academy Press, 1991 2. Bagnis R, Berglund F, Elias PS, et al: Problems of toxicants in marine food products-I. Marine biotoxins. Bull WHO 1970; 42:69-88 3. Bartholomew BA, Berry PR, Rodhouse JC, Gilbert RJ, Murray CK: Scombrotoxic fish poisoning in Britain: Features of over 250 suspected incidents from 1976 to 1986. Epidemiol Infect 1987; 99:775-782 4. Taylor SL: Histamine food poisoning: Toxicology and clinical aspects. CRC Crit Rev Toxicol 1986; 17:91-128 5. Centers for Disease Control (CDC): Scombroid poisoning-New Jersey. MMWR 1980; 29:106-107 6. California Department of Health Services: Scombroid poisoning-San Jose. Calif Morbid 1980; 12:1 7. Foodborne Disease Surveillance, Annual Summary Reports. 1978 to 1982. Atlanta, Ga, CDC, 1978 to 1982 8. Bean NH, Griffin PM: Foodborne disease outbreaks in the United States, 197387: Pathogens, vehicles, and trends. J Food Protection 1990; 53:804-817 9. Food and Drug Administration: Defect action levels for histamine in tuna: Availability of guide. Federal Register 1982; 47:40487 10. Lerke PA, Werner SB, Taylor SL, Guthertz LS: Scombroid poisoning-Report of an outbreak. West J Med 1978; 129:381-386 11. Gellert GA, Ralls J, Merryman R, Brown C, Huston J, Ehling LR: Scombroidfish poisoyuing (Letter). N Engl J Med 1991; 325:516 12. Morrow JD, Margolies GR, Rowland J, Roberts U: Evidence that histamine is the causative toxin of scombroid-fish poisoning. N Engl J Med 1991; 324:716-720 13. Hughes JM, Potter ME: Scombroid-fish poisoning: From pathogenesis to prevention. N Engl J Med 1991; 324:766-768
