Elsevier

Toxicon

Volume 56, Issue 2, 15 August 2010, Pages 231-243
Toxicon

Scombroid poisoning: A review

https://doi.org/10.1016/j.toxicon.2010.02.006Get rights and content

Abstract

Scombroid poisoning, also called histamine fish poisoning, is an allergy-like form of food poisoning that continues to be a major problem in seafood safety. The exact role of histamine in scombroid poisoning is not straightforward. Deviations from the expected dose-response have led to the advancement of various possible mechanisms of toxicity, none of them proven. Histamine action levels are used in regulation until more is known about the mechanism of scombroid poisoning. Scombroid poisoning and histamine are correlated but complicated. Victims of scombroid poisoning respond well to antihistamines, and chemical analyses of fish implicated in scombroid poisoning generally reveal elevated levels of histamine. Scombroid poisoning is unique among the seafood toxins since it results from product mishandling rather than contamination from other trophic levels. Inadequate cooling following harvest promotes bacterial histamine production, and can result in outbreaks of scombroid poisoning. Fish with high levels of free histidine, the enzyme substrate converted to histamine by bacterial histidine decarboxylase, are those most often implicated in scombroid poisoning. Laboratory methods and screening methods for detecting histamine are available in abundance, but need to be compared and validated to harmonize testing. Successful field testing, including dockside or on-board testing needed to augment HACCP efforts will have to integrate rapid and simplified detection methods with simplified and rapid sampling and extraction. Otherwise, time-consuming sample preparation reduces the impact of gains in detection speed on the overall analysis time.

Introduction

Scombroid poisoning, or histamine fish poisoning, is a type of food poisoning with symptoms and treatment similar to those associated with seafood allergies. Scombroid poisoning results from consumption of mishandled fish. Histamine (2-(1H-imidazol-4-yl) ethanamine) and other decomposition products are generated in time-temperature abused raw fish by bacterial, enzymatic conversion of free histidine (Rawles et al., 1996). Although high levels of histamine are generally found in the implicated fish, neither histamine fish poisoning nor scombroid poisoning fully capture the nature of this intoxication (Lehane and Olley, 2000). The term “scombroid” derives from the type of fish (i.e. Scombridae) first implicated, such as tuna and mackerel. What these (scombrid) fish share in common are high levels of free histidine in their muscle tissues (Suyama and Yoshizawa, 1973, Perez-Martin et al., 1988, Ruiz-Capillas and Moral, 2004). It is now known that other (non-scombroid) fish species are also implicated in scombroid poisoning, such as mahi-mahi (Coryphaena spp.), sardines (Sardinella spp.), pilchards (Sardina pilchardus), anchovies (Engraulis spp.), herring (Clupea spp.), marlin (Makaira spp.) bluefish (Pomatomus spp.) (Taylor, 1986, Hwang et al., 1997), Western Australian salmon (Arripis truttaceus), sockeye salmon (Oncorhynchus nerka), amberjack (Seriola spp.) Cape yellowtail (Seriola lalandii), (Lange, 1988, Muller et al., 1992, Smart, 1992, Gessner et al., 1996) and swordfish (Xiphias gladius) (Chang et al., 2008). Most of these fish species are rich in free histidine (Lukton and Olcott, 1958, Taylor, 1986, Antoine et al., 1999) with salmon and swordfish being exceptions (Lukton and Olcott, 1958, Suzuki et al., 1987).

Scombroid poisoning is clearly associated with elevated histamine levels in the outbreak-associated samples (Taylor, 1986). However, there is not a clear dose-response relationship between oral administration of histamine, and histamine levels ingested in the decomposed fish, with scombrotoxic fish showing higher toxicity than an equivalent oral dose of pure histamine (Taylor et al., 1984, Taylor, 1986, Lehane and Olley, 2000). Thus scombroid poisoning is not uncomplicated histamine poisoning (Taylor et al., 1989, Lehane and Olley, 2000).

Section snippets

Symptoms, reporting, and treatment of scombroid poisoning

The onset of scombroid poisoning is typically from 10 min to 1 h following consumption of poisonous fish (Ansdell, 2008). The symptoms (Arnold and Brown, 1978, Kim, 1979, Gilbert et al., 1980, Taylor, 1986) are variable and include peppery or metallic taste, oral numbness, headache, dizziness, palpitations, rapid and weak pulse (low blood pressure), difficulty in swallowing, and thirst. Noteworthy as allergy-like are symptoms such as hives, rash, flushing and facial swelling (Kim, 1979, Taylor

Histamine physiological role and metabolism

Histamine is a messenger molecule in the human body and thus not a natural toxin per se. It is ubiquitous in its distribution and released from mast cells, enterochromaffin-like cells, and neurons. Histamine targets a range of “histaminergic” receptors and its various actions are mediated by histamine receptors H1, H2, H3 and H4 and histamine has many vital functions in healthy individuals ranging from control of gastric acid secretion to neurotransmission in the central nervous system (

Postulated mechanisms of toxicity in scombroid poisoning

In attempting to explain this dose-response anomaly, any hypothesis for the scombroid poisoning mechanism must be consistent with the previously discussed observations regarding what is known about this intoxication, such as response to antihistamine therapy by victims, presence of the toxicity only in decomposed fish, the presence of histamine and metabolites in the urine of victims, and finally, implication of fish species rich in free histidine.

Potentiation of histamine toxicity by other

Bacterial origins of histamine in fish

Histamine is produced from free histidine due to the action of bacterial histamine decarboxylase (HDC) following time-temperature abuse. Although scombroid poisoning is defined as an illness associated with spoiled fish (López-Sabater et al., 1994a, Satomi et al., 1997, Kim et al., 1999, Kim et al., 2000, Kim et al., 2001b) and fish products (Kimura et al., 2001, Kung et al., 2009) histamine and other biogenic amines are also found in other foods and also in beverages. Histidine is a common

Bacterial histidine decarboxylase as an “independent producer” of histamine

Whether produced by gram-positive or gram-negative bacteria, HDC can be present in fish, and histamine can be produced, even when the HDC positive bacteria are no longer viable. This has now been confirmed in experiments using recombinant HDCs of the histamine-producing bacteria P. phosphoreum, Photobacterium damselae, R. planticola, and M. morganii in which the bacteria themselves were absent (Kanki et al., 2007). These authors studied HDC activities from these sources as a function of pH,

Histamine levels used in regulation

Histamine levels are targeted in regulatory efforts to address the threat of scombroid poisoning (FDA/CFSAN, 2001; EU 2005). Although, as discussed above and in other reviews (Taylor et al., 1989, Lehane and Olley, 2000, Dalgaard et al., 2008, Al Bulushi et al., 2009) scombroid poisoning is not simple histamine poisoning, currently available information suggests that scombroid poisoning is nonetheless caused primarily by histamine in seafood (Dalgaard et al., 2008) and that reducing histamine

Impact of scombroid poisoning and management of susceptible fish

Since it is strictly the result of fish product mishandling, scombroid poisoning can be prevented. It is nonetheless a persistent and global problem (Lehane and Olley, 2000, Dalgaard et al., 2008). Data for worldwide outbreaks of scombroid poisoning were updated recently in project results (BIOCOM, Biogenic amines in seafoods – assessment and management of consumer exposure studies) reported by Dalgaard et al. (2008). Together with ciguatera, scombroid poisoning continues to account for the

Laboratory methods for histamine and related biogenic amines in fish and fish products

The number and variety of methods developed for laboratory histamine testing of fish and fish products is impressive. In contrast to many of the other more potent seafood toxins, the relatively high action levels established for histamine in fish allow for the detection of histamine using a variety of different approaches ranging from simple and inexpensive thin layer chromatography (TLC) procedures to resource-intensive and more powerful LC-MS methods.

Most of the separation methods applied to

Conclusion

Contamination of fish with histamine is due to mishandling and bacterial production of histamine. Although the role of histamine as a seafood “toxin” in scombroid poisoning is not fully understood, detection of histamine and the enforcement of action levels are useful for control purposes. Hypothesized mechanisms for scombroid poisoning remain unproven, and improved prevention of scombroid poisoning can result from investigations of these mechanisms to gain a better understanding of the origins

Acknowledgments

The views and information presented in this article are those of the author and do not necessarily represent those of the U.S. Food and Drug Administration. Mention of brand or firm name does not constitute an endorsement by the U.S. Food and Drug Administration over others of a similar nature not mentioned.

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