Histamine fish poisoning revisited

Abstract

Histamine (or scombroid) fish poisoning (HFP) is reviewed in a risk-assessment framework in an attempt to arrive at an informed characterisation of risk. Histamine is the main toxin involved in HFP, but the disease is not uncomplicated histamine poisoning. Although it is generally associated with high levels of histamine (≥50 mg/100 g) in bacterially contaminated fish of particular species, the pathogenesis of HFP has not been clearly elucidated. Various hypotheses have been put forward to explain why histamine consumed in spoiled fish is more toxic than pure histamine taken orally, but none has proved totally satisfactory. Urocanic acid, like histamine, an imidazole compound derived from histidine in spoiling fish, may be the “missing factor” in HFP. cis-Urocanic acid has recently been recognised as a mast cell degranulator, and endogenous histamine from mast cell degranulation may augment the exogenous histamine consumed in spoiled fish. HFP is a mild disease, but is important in relation to food safety and international trade. Consumers are becoming more demanding, and litigation following food poisoning incidents is becoming more common. Producers, distributors and restaurants are increasingly held liable for the quality of the products they handle and sell. Many countries have set guidelines for maximum permitted levels of histamine in fish. However, histamine concentrations within a spoiled fish are extremely variable, as is the threshold toxic dose. Until the identity, levels and potency of possible potentiators and/or mast-cell-degranulating factors are elucidated, it is difficult to establish regulatory limits for histamine in foods on the basis of potential health hazard. Histidine decarboxylating bacteria produce histamine from free histidine in spoiling fish. Although some are present in the normal microbial flora of live fish, most seem to be derived from post-catching contamination on board fishing vessels, at the processing plant or in the distribution system, or in restaurants or homes. The key to keeping bacterial numbers and histamine levels low is the rapid cooling of fish after catching and the maintenance of adequate refrigeration during handling and storage. Despite the huge expansion in trade in recent years, great progress has been made in ensuring the quality and safety of fish products. This is largely the result of the introduction of international standards of food hygiene and the application of risk analysis and hazard analysis and critical control point (HACCP) principles.

Introduction

Histamine (or scombroid) fish poisoning (HFP) is a foodborne chemical intoxication caused by eating spoiled, or bacterially contaminated, fish. The fish are harmless when fresh, and after they have become toxic they may still have a normal appearance and odour (Sapin-Jaloustre and Sapin-Jaloustre, 1957). No available method of preparation, including freezing, canning and smoking, will destroy the causative toxin(s) (Etkind et al., 1987). The disease is not uncomplicated histamine poisoning, but is generally associated with high levels of histamine (≥50 mg/100 g) in the spoiled fish.

Histamine is a naturally occurring substance in mammalian physiology. It is contained in mast cells and basophils, and its biological effects are usually seen only when it is released in large amounts in the course of allergic and other reactions. Histamine exerts its effects by binding to receptors on cellular membranes in the respiratory, cardiovascular, gastrointestinal and haematological/immunological systems and the skin (Cavanah and Casale, 1993).

HFP is a common form of fish poisoning, but many incidents go unreported because of the mildness of the disease, lack of required reporting, and misdiagnosis. Symptoms can be confused with those of “Salmonella infection” (Russell and Maretic, 1986) and food allergy (Taylor, 1985). While the syndrome is that of histamine toxicity, there is individual variation in susceptibility, and clinical signs are more severe in people taking medications such as isoniazid, which inhibit enzymes that normally detoxify histamine in the intestine (Stratton et al., 1991).

HFP is a significant public health and safety concern (Sánchez-Guerrero et al., 1997, Wu et al., 1997) and a trade issue (Anonymous, 1998a). The earliest record of the disease was in 1828 (Henderson, 1830). Since then, it has been described in many countries, and is now the most prevalent form of seafood-borne disease in the United States (Lipp and Rose, 1997). The worldwide network for harvesting, processing and distributing fish products has made HFP a global problem. However, because it is a consequence of improper handling or storage of fish and there are effective testing methods to identify likely toxic fish, control and prevention are possible (Institute of Medicine, 1991).

Scientific information on HFP is reviewed here in a risk-assessment framework (Kindred, 1996, Buchanan, 1998). An attempt has been made to address, as accurately as possible, the questions: “What causes outbreaks of HFP?”, “What are the underlying factors contributing to outbreaks?” and “What are the consequences of outbreaks?”