Original Article
Evidence That Histamine Is the Causative Toxin of Scombroid-Fish Poisoning
N Engl J Med 1991; 324:716-720March 14, 1991
- Abstract
- Abstract
Background.
The highest morbidity worldwide from fish poisoning results from the ingestion of spoiled scombroid fish, such as tuna and mackerel, and its cause is not clear. Histamine could be responsible, because spoiled scombroid fish contain large quantities of histamine. Whether histamine is the causative toxin, however, has remained in question. To address this issue, we investigated whether histamine homeostasis is altered in poisoned people.
Methods.
The urinary excretion of histamine and its metabolite, N-methylhistamine, was measured in three persons who had scombroid-fish poisoning (scombrotoxism) after the ingestion of marlin. We measured 9α, 11β-dihydroxy-15–oxo–2,3,18,19-tetranorprost-5-ene-1,20-dioic acid (PGD-M), the principal metabolite of prostaglandin D2, a mast-cell secretory product, to assess whether mast cells had been activated to release histamine.
Results.
The fish contained high levels of histamine (842 to 2503 μmol per 100 g of tissue). Symptoms of scombrotoxism — flushing and headache — began 10 to 30 minutes after the ingestion of fish. In urine samples collected one to four hours after fish ingestion, the levels of histamine and N-methylhistamine were 9 to 20 times and 15 to 20 times the normal mean, respectively. During the subsequent 24 hours, the levels fell to 4 to 15 times and 4 to 11 times the normal values. Levels of both were normal 14 days later. PGD-M excretion was not increased at any time. Two persons treated with diphenhydramine had prompt amelioration of symptoms.
Conclusions.
Scombroid-fish poisoning is associated with urinary excretion of histamine in quantities far exceeding those required to produce toxicity. The histamine is most likely derived from the spoiled fish. These results identify histamine as the toxin responsible for scombroid-fish poisoning. (N Engl J Med 1991; 324:716–20.)
Media in This Article
Figure 1
Urinary Excretion of N-Methylhistamine, Histamine, and PGD-M in Three Persons with Scombrotoxism.Table 1
Urinary Excretion of Histamine and N-Methylhistamine in the Person Who Ate Only a Small Quantity of the Marlin Implicated in the Poisoning and Did Not Have Scombrotoxism.Article Activity
- Article
SCOMBROID-fish poisoning (scombrotoxism) refers to the clinical syndrome that results from the ingestion of spoiled fish, usually of the families Scombridae and Scomberesocidae. This includes tuna, mackerel, skipjack, and bonito.1 However, nonscombroid fish, such as mahi-mahi, bluefish, amberjack, herring, sardines, and anchovies, as well as cheese, have also been implicated as causes of scombrotoxism.2 Scombroid-fish poisoning is the most common cause of ichthyotoxicosis worldwide.3 In the United States, such poisoning represents one of the major chemical food-borne illnesses reported to the Centers for Disease Control (CDC).4
Symptoms of scombroid-fish poisoning usually occur within an hour after the ingestion of spoiled fish and last for several hours.1 The symptoms include flushing, sweating, nausea, vomiting, diarrhea, headache, palpitations, dizziness, rash, and occasionally, swelling of the face and tongue. Respiratory distress can also occur, and vasodilatory shock has been noted on occasion.2
The cause of scombroid-fish poisoning is not clearly understood. The CDC refers to the causative agent as scombrotoxin.4 The toxin is not present when the fish are caught, but it is produced subsequently during spoilage.5 Histamine was first suggested as the causative toxin in the 1940s,6 on the basis of a number of observations. Fish that have caused scombroid poisoning consistently contain large quantities of histamine.6 Scombroid fish contain substantial amounts of free histidine that can be decarboxylated to form histamine by enteric bacteria present in spoiled fish.6 , 7 Furthermore, the symptoms of scombroid-fish poisoning resemble those of histamine toxicity, and improvement in symptoms has been reported after treatment with antihistamines.8
The chief factor that has cast doubt on the role of histamine in scombroid-fish poisoning is that although it has been possible to produce mild symptoms of histamine excess after the oral administration of the substance in massive doses to humans, it has not been possible to reproduce the illness with doses comparable to the quantities ingested in fish that have caused scombrotoxism.9 10 11 This may be because histamine is absorbed very poorly from the gastrointestinal tract and because the liver and intestinal mucosa have a great capacity to inactivate histamine.6 , 11 These results have led to speculation that substances may be present in the spoiled fish that enhance the pharmacologic activity of histamine, facilitate its absorption, or inhibit its inactivation by histamine N-methyltransferase, diamine oxidase, or both.6 , 12
The crucial information required to support or refute the speculation that histamine may be the causative toxin of scombroid-fish poisoning — i.e., a direct assessment of whether levels of histamine sufficient to cause toxicity are present in vivo in humans in association with such poisoning — has never been obtained. A recent outbreak of scombroid poisoning at a local cafeteria provided us with the opportunity to address this question.
Methods
Materials
[2H4] Histamine and [2H3] N-methylhistamine were obtained from MSD Isotopes (Montreal). The principal urinary metabolite of prostaglandin D2 – 9α, 11-β-dihydroxy-15-oxo-2,3,18,19-tetranorprost-5-ene-1,20-dioic acid (PGD-M) — was synthesized and converted to the [18O4]-labeled internal standard, as described elsewhere.13 , 14
Measurement of Histamine, N-Methylhistamine. and PGD-M in Urine
Histamine, N-methylhistamine, and PGD-M were all measured in urine by highly accurate stable-isotope-dilution mass-spectrometric assays.15 16 17 The precision and accuracy of the assays were as follows: for histamine, ±3 percent and 98 percent, respectively; for N-methylhistamine, ±2 percent and 97 percent; and for PGD-M, ±7 percent and 96 percent. The urinary creatinine concentration was measured by the sodium picrate method with an AutoAnalyzer II (Technicon, Tarrytown, N.Y.). The results of the histamine and N-methylhistamine assays were expressed as picomoles per micromole of creatinine, and the results of the PGD-M assay as picomoles per millimole of creatinine. The normal range for each substance was determined by measurements in 20 normal subjects.
Preservation and Handling of the Fish
The marlin implicated in the poisoning incident was caught in Costa Rican waters and flown to Miami. It was shipped to Nashville by refrigerated truck on June 9, 1990. It arrived at the local commercial supplier in Nashville on June 12 and was placed in a walk-in cooler at 1°C. The fish was transported to a local cafeteria on June 14 by refrigerated truck and stored in a walk-in cooler at 7°C. Later that day, the fish was sliced and placed in a reach-in cooler at 9°C. The following morning the fish was cooked and served for lunch. Approximately 50 servings of 100 to 150 g each were prepared, of which 25 were served that day.
In a control study, normal subjects were fed fresh marlin. This fish, obtained on the day of its arrival in Nashville from the same local supplier, was grilled and served immediately after being purchased.
Clinical Study
We studied three persons who had symptoms of scombrotoxism after eating the implicated marlin. Each ate one serving of fish. A fourth person, a chief medical resident at Vanderbilt University, recognized an unusual peppery, metallic taste in the fish. Because he knew that this taste was characteristic of fish implicated in scombroid-fish poisoning,2 , 18 he ate only a small portion and did not swallow portions that tasted peppery. He had no symptoms of scombrotoxism subsequently. The poisoned persons were two men and one woman, 35, 27, and 25 years of age, respectively. All were healthy, and none had any history of allergic reactions to fish nor were they taking any medications. Three separate urine samples were collected from each of the four persons for measurements of histamine, N-methylhistamine, and PGD-M. The first urine sample was obtained one to four hours after the ingestion of fish. The second was a 24-hour collection begun after the collection of the first sample. The third sample was collected for 24 hours 14 days after the poisoning.
The persons studied were all medical personnel at Vanderbilt University. We were made aware of their cases by another physician at the university who recognized that the symptoms were probably due to scombroid-fish poisoning. Subsequently, the cafeteria was informed of the poisoning, and it stopped serving the fish. It was not possible to identify the other persons who had eaten fish at the cafeteria that day to determine whether any of them had had symptoms of poisoning. Unserved portions of fish were seized and sent to the laboratories of the Food and Drug Administration in Atlanta for an analysis of the histamine content by a standard fluorometric method.19
In the control study, we also measured the urinary excretion of histamine and N-methylhistamine in three normal subjects after the ingestion of fresh marlin. Each subject ate 125 g of cooked fish. Urine samples were obtained for analysis from each person during the 24-hour period before the fish was eaten. After the ingestion of the fish, the first urine sample voided (obtained within the first 4 hours) and a subsequent 24-hour collection were obtained from each subject. Three portions of the fresh marlin were also analyzed for their histamine content.
Results
Clinical Summary
The three affected persons had symptoms of poisoning that began 10 to 30 minutes after ingestion of the fish and consisted of severe headache, mild nausea, and intense flushing, most notably in the face. One person also had severe diarrhea of sudden onset. One of the three sought care in the Vanderbilt Hospital emergency room and received diphenhydramine (50 mg intramuscularly) that resulted in an amelioration of symptoms within 30 minutes. A second person, a physician, administered diphenhydramine (50 mg intramuscularly) to himself, which also resulted in rapid improvement in symptoms within approximately 30 minutes. The third person did not receive an antihistamine. His symptoms abated after approximately three hours.
In the control study, none of the three subjects who ate fresh marlin had symptoms of scombrotoxism.
Histamine Content of the Ingested Fish
The FDA's analysis of the four random samples of the batch of fish implicated in the poisoning revealed levels of 2495, 1456, 842, and 2503 μmol of histamine per 100 g of fish. Although marlin is a nonscombroid fish and has not previously been reported to cause scombroid poisoning, the histamine content of the fish was very high. The FDA has established a hazard level for poisoning from tuna that contains histamine in concentrations above 450 μmol per 100 g20; fresh tuna contains less than 9 μmol per 100 g.18 The histamine content of the fresh marlin that did not cause symptoms of poisoning was undetectable (<4.5 μmol per 100 g).
Urinary Excretion of Histamine and N-Methylhistamine
Initially, we examined whether the ingestion of the fish resulted in the absorption of substantial amounts of histamine or its metabolites by measuring the urinary excretion of the histamine metabolite N-methylhistamine (Fig. 1Figure 1
Urinary Excretion of N-Methylhistamine, Histamine, and PGD-M in Three Persons with Scombrotoxism.). The urinary levels of N-methylhistamine were normal in the urine samples collected from the three persons 14 days after the poisoning. The levels were much higher, however, in the urine samples collected during the symptomatic phase of scombrotoxism in each of these three persons. The initial samples collected one to four hours after the ingestion of the fish contained levels of N-methylhistamine 15 to 20 times the normal mean. In the samples collected during the subsequent 24 hours, the levels were still elevated but to a lesser extent, ranging from 4 to 11 times the normal mean.Thus, the ingestion of the fish resulted in substantially increased urinary excretion of N-methylhistamine. These results do not prove, however, that systemic concentrations of free histamine were also elevated, since ingested histamine could have been metabolized in the intestinal mucosa and liver before entering the systemic circulation.6 To address this question, we measured the urinary excretion of histamine in the same urine samples. Fourteen days after poisoning, the urinary excretion of histamine in each of the three poisoned persons was normal. However, as we found for the urinary excretion of N-methylhistamine, the levels of histamine were elevated in the urine samples collected immediately after the ingestion of the fish. In the urine samples collected between one and four hours after the ingestion of the fish, the levels of histamine were 9 to 20 times the normal mean. In the samples collected during the subsequent 24-hour period, these levels had fallen to 4 to 15 times the normal mean (Fig. 1).
As previously mentioned, one person recognized the peppery, metallic taste of spoiled scombroid fish and thus ate only a small portion of the serving. This person had no symptoms of scombrotoxism, and the urinary levels of both histamine and N-methylhistamine were normal both in the urine sample collected soon after the meal and in that collected during the subsequent 24 hours (Table 1Table 1
Urinary Excretion of Histamine and N-Methylhistamine in the Person Who Ate Only a Small Quantity of the Marlin Implicated in the Poisoning and Did Not Have Scombrotoxism.). Hence, only those persons in whom scombrotoxism developed had increased circulating concentrations of histamine after ingesting the spoiled fish. In addition, the urinary excretion of both histamine and N-methylhistamine remained normal in the three control subjects who ate fresh marlin that contained undetectable quantities of histamine and that did not produce symptoms of poisoning (Table 2Table 2
Urinary Excretion of Histamine and N-Methylhistamine in Three Control Subjects Who Ate Fresh Marlin Containing No Detectable Histamine.).Assessment of PGD-M Excretion
The increased urinary excretion of histamine in the affected persons could have been due to the ingestion of histamine contained in the fish or the ingestion of other substances present in the fish that evoked the release of endogenous histamine from tissue mast cells. The latter, if it occurs, is unlikely to involve an allergic IgE-dependent mechanism of mast-cell activation, since all persons who eat spoiled scombroid fish have symptoms of poisoning.5 We and others have found that mast cells activated by either IgE-dependent or independent mechanisms in vitro and in vivo release prostaglandin D2 along with histamine.21 22 23 24 25 26 Therefore, we examined whether there was evidence of increased release of prostaglandin D2 in the poisoned persons by measuring the urinary excretion of PGD-M. In contrast to the increased urinary excretion of histamine and N-methylhistamine, the excretion of PGD-M was normal in all three urine samples from each of the three persons (Fig. 1).
Discussion
Histamine was suggested approximately 50 years ago as the causative agent of scombrotoxism, but its role has remained in question. One reason for the lingering doubt is that it has been impossible to reproduce the illness in normal subjects by administering histamine orally in doses comparable to those ingested when spoiled fish is eaten.10 , 11 The crucial information required to resolve this question has not been obtained — namely, whether scombroid-fish poisoning is associated with sufficient increases in circulating histamine to cause toxicity. Our results document clearly that this does indeed occur. The urinary levels of histamine in the affected persons far exceeded those associated with symptoms of histamine excess. Kaliner and colleagues found that the urinary excretion of histamine during intravenous infusions of histamine in doses that resulted in flushing, headache, and tachycardia was approximately 34 nmol per hour, or 92 pmol per micromole of creatinine on the basis of an hourly rate of excretion of creatinine of 370 μmol.27 When first measured, the urinary histamine levels in the three poisoned persons were all higher than 200 pmol per micromole of creatinine (Fig. 1).
Whether potentiators of histamine toxicity were present in the spoiled scombroid fish is unknown.6 , 12 It is noteworthy, however, that the increases in the urinary excretion of both histamine and N-methylhistamine in the poisoned persons were of similar magnitude. Thus, it is probably valid to conclude that the spoiled fish did not contain substances that potentiated histamine toxicity by inhibiting its inactivation by histamine N-methyltransferase.
The failure to find increased endogenous release of prostaglandin D2 in association with increased levels of histamine suggests that the source of the excess histamine was the fish rather than the release of histamine from mast cells. This is further supported by the finding that the ingestion of fresh marlin containing undetectable quantities of histamine did not result in increased urinary excretion of histamine. Although it is unlikely, we cannot exclude the possibility that other unknown substances may be present in spoiled fish that selectively release histamine but not prostaglandin D2 from mast cells or that selectively activate basophils, which do not produce prostaglandin D2, to release histamine.28 29 30 31 Whether histamine is derived from exogenous or endogenous sources, however, does not influence the conclusion that it is the causative toxin of scombroid-fish poisoning.
The identification of histamine as the causative agent of scombrotoxism should serve as the basis for a general public health policy recommendation that persons with scombroid poisoning receive treatment with an antihistamine. Symptoms usually improve with the administration of H1-receptor—antagonist drugs.8 The two persons in our study who took diphenhydramine also had rapid amelioration of symptoms. A single report has also described symptomatic improvement after the administration of an H2-antagonist drug.32 We and others have demonstrated previously that blood vessels in humans have H2 receptors and that blocking the vascular effects of histamine requires the blockade of both H1 and H2 receptors.27 , 33 Thus, there is a rational basis for recommending that persons with scombroid poisoning be treated with antagonists to both H1 and H2 receptors in combination.
We conclude that histamine is the toxin responsible for scombroid-fish poisoning. Such poisoning can be prevented effectively by handling and refrigerating fish appropriately.2 If warming occurs at any point from the time the fish is caught until it is consumed, bacterial proliferation can lead to the production of histamine in quantities sufficient to cause poisoning in the absence of obvious putrefaction.5 For these reasons, scombroid-fish poisoning will probably continue to be one of the most common causes of ichthyotoxicosis.
Supported by grants (GM–15431, GM–33040, and HL–02499) from the National Institutes of Health. Dr. Morrow is a Boehringer Ingelheim Centennial Fellow in Clinical Pharmacology.
We are indebted to Dr. Barney S. Graham for alerting us to the poisoning incident; to Ms. Tanya Duckworth and Mr. William Zackert for expert technical assistance; and to Ms. Amanda Simpson for assistance in the preparation of the manuscript.
Source Information
From the Departments of Pharmacology and Medicine (J.D.M., G.R.M., L.J.R.), Vanderbilt University, and the Food Inspection Division, Nashville-Davidson County Metropolitan Board of Health (J.R.), both in Nashville. Address reprint requests to Dr. Roberts at the Department of Pharmacology, Vanderbilt University, Nashville, TN 37232–6602.
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