Histamine Food Poisoning Research Articles

The Relationship of Histamine Content in European Pilchard (Sardina pilchardus) with Freshness, Temperature, and Storage Duration

Histamine food poisoning, stemming from the consumption of certain histamine-rich fish species, such as tuna, mackerel, European pilchards, and herring, is one of the major public health issues worldwide. The present study aimed to evaluate the histamine content in fresh European pilchard (Sardina pilchardus Walbaum, 1792) of Mehdia, a coastal city in the north of Morocco. Three randomly selected batches of fresh European pilchards, each weighing 20kg, were obtained from different boats upon landing. The evolution of histamine production was monitored every 8 hours for 6 days, with one batch stored at 0°C and the other at 10°C. The organoleptic characteristics were examined considering sensory evaluation according to the rating system of European Council Regulation No. 2406/96 as common marketing standards for certain fishery products and the quality index method (QIM). The histamine content in European pilchard flesh was determined using the fluorometric method. The results indicated that the average histamine content did not exceed 5 ppm during storage at 0°C. The freshness ratings were highest during the first 3 days, corresponding to QIM values of 0 to 10 at 0°C. On days 4 and 5, the freshness ratings were on quality A, corresponding to QIM values of 11 and 12, and on the last day, they were on quality B, corresponding to a QIM value of 15 with preservation of the organoleptic quality. Statistically, a significant correlation was found between the European pilchard’s freshness and the storage duration. In contrast, this correlation between the histamine content and the storage duration was insignificant. At 10°C, the average histamine content exceeded the regulatory limit in force (100 ppm) after 32 hours of storage, and spoilage occurred on day 3. Statistical analysis revealed a strong correlation between the histamine content, storage temperature, the degree of freshness, and the duration of storage. The extra freshness quality index of European pilchard guarantees a very large margin of safety regarding histamine and can be consumed without risk. Keywords: Degree freshness, European pilchard, Histamine, Sardine, Storage, Temperature

Assessment of Histamine Levels and Histamine-producing Bacteria in <i>Euthynnus affinis</i> Marketed in Tanga and Mtwara Coastal Areas, Tanzania

Histamine (scombrotoxin) food poisoning is a community health risk associated with consumption of some marine fish species and it has been proposed that some anaerobic bacteria contribute to this form of food poisoning. However, histamine levels and histamine producing bacteria in fish marketed in Tanzania have not been appraised. This study was conducted to determine histamine levels and histamine-producing bacteria in the <i>E. affinis</i> (tuna) value chain in Tanga and Mtwara regions. High-performance thin-layer chromatography (HPTLC) was used to determine histamine levels, Bacteriology and biochemical tests were employed to determine histamine-producing bacteria. A total of 64 tuna fish samples were collected from deep sea fish market and Sahare Tanga and ferry market, Mtwara coasts. The mean level of histamine was found to be 86.4±43.9 in Tanga and 64.8±47.5 in Mtwara and the overall mean was 77.1±46.4. All fish 64 samples were positive for histamine; however, the mean level was within the recommended limit for consumed fishery products according to European Union regulation of 200 mg/kg (m) to 400 mg/kg (m) (EC, 2005).<i> Klebsiella spp, pseudomonas spp, </i>and <i>proteus spp</i> were isolated and confirmed as histamine-producing bacteria based on bacteriology and biochemical characteristics. It concluded that although within the recommended levels, all fish samples were positive to histamine and three bacterial species associated with its production isolated. To prevent raising histamine to concern levels, maintenance of hygiene and low temperature along the production chain should be observed.

Evaluation of the Capacity to Produce Histamine by Histamine-Producing Bacteria during Storage at 10℃

Histamine is produced from histidine using histidine decarboxylase of histamine-producing bacteria. However, associated histamine food poisoning demands microbiological controls. Furthermore, studies reported that histamine production by histamine-producing bacteria is affected by temperature. Therefore, to prevent histamine food poisoning, it is desirable to store foods below 4℃. However, it is challenging to maintain the storage temperature of food substances in refrigerators constantly below 4℃. Thus, we investigated histamine production capacity using seven histamine-producing bacterial strains under storage at 10℃, a more reasonable cold storage condition. Subsequently, we examined the variation of histamine production in buffers, the correlation between bacterial density and histamine production quantities, and the growth rate in broths. Results showed that similar levels of histamine were produced in buffers even after 5 days of storage under certain conditions in which histamine-producing bacteria did not grow. Moreover, bacterial density was proportional to histamine production, and the coefficient of determination was more than 0.97, and the bacterial density required to produce 200 μg/mL of histamine during storage at 10℃ was calculated to be 4×107-4×108 CFU/mL. When the initial bacterial density was 102-103 CFU/mL, psychrophilic bacteria required 2 or 3 days and mesophilic bacteria required more than 4 days to grow above 107 CFU/mL. The above results suggest that understanding the capacity of histamine-producing bacteria to produce histamine and its growth rate in foods is important for the prevention of histamine food poisoning.

Literature Review on the Type of Fish and Histamine-producing Bacteria Associated with Histamine Poisonings in Japan

Histamine poisoning has been reported worldwide. Improvements in refrigeration technology have led to a reduction in this food poisoning; however, it continues to occur. Misdiagnosis of fish allergies has compounded this problem and the number of patients subjected to histamine poisoning that are transported to the emergency ward because of anaphylactic shock-like symptoms should not be underestimated. We investigated incidents of histamine food poisoning in Japan from 1998 to 2020, and found that there were a mean 9.7 incidents/year and 195.3 cases/year. Facility-wise occurrence of the incidents per year was the highest in restaurants followed by lunch facilities, and these together accounted for approximately 70% of the incidents. Facility-wise total number of cases was the highest in lunch facilities followed by restaurants, and these together accounted for 80% of the cases. Fish associated with histamine poisoning were mainly tuna, marlin, and mackerel. Based on the current literature review, 23 genera of histamine-producing bacteria were isolated from fish purchased in Japan. The most frequently reported bacteria were Morganella morganii and Photobacterium damselae. Psychrophilic bacteria such as Morganella psychrotolerans and Photobacterium phosphoreum were also isolated. To prevent histamine poisoning, freezing or fast handling of fish and the products during processing and consuming is important because only refrigeration of fish is enough.

Microbial production of histamine and the imperatives of processed food consumption

Food processing and storage increase the value chain of food items, both for commercial purposes and for future use by peasant producers. The roles of lactic acid bacteria (LAB) and yeasts in the processing of dairy, brewed, bakery and traditionally fermented foods cannot be over-emphasized. These organisms improve the nutritional contents and organoleptic properties of these foods. However, certain undesired products, especially from protein-rich foods, notably, biogenic amines often characterize the process. This is usually a physiologic response by the organisms to the food environments such as pH, and is often influenced by temperature, time and salt concentration. Histamine production during such a process often results in the accumulation of exogenous histamine in the foods, thereby constituting health hazards to the consumers. Histamine food poisoning affects virtually every system of the body due to the widespread physiological roles of histamine in the body, presenting a wide range of symptoms that make diagnosis difficult. More regulated scientific approaches should be adopted by food processors and handlers especially in the developing countries where technologies may not be available.

Histamine and cholesterol lowering abilities of lactic acid bacteria isolated from artisanal Pico cheese.

This study was designed to select lactic acid bacteria with histamine- and cholesterol-reducing abilities to be used as potential probiotics. Thirty strains of lactic acid bacteria isolated from an artisanal raw milk cheese were screened for their abilities to degrade histamine, reduce cholesterol and hydrolyse bile salts. Strains were also screened for safety and probiotic traits, such as resistance to gastrointestinal conditions, adhesion to Caco-2 cells, resistance to antibiotics and presence of virulence genes. Two Lactobacillus paracasei strains presented high cholesterol- and histamine-lowering abilities, tested negative for the presence of virulence genes and showed susceptibility to most important antibiotics. These strains were also shown to possess desirable in vitro probiotic properties, revealed by tolerance to gastrointestinal conditions and high adhesion to intestinal cells. Among the screened strains, Lb. paracasei L3C21M6 revealed the best cholesterol and histamine reducing abilities together with desirable probiotic and safety features to be used in food applications. The strain L3C21M6 is a good candidate for use as a probiotic with histamine-degrading activity and cholesterol lowering effect. In addition, this strain could be use in dairy foods to prevent histamine food poisoning.

Search for Substances That Inhibit Histamine Production Using Used Tea Leaves

As food waste has become a major problem in recent years, measures against food loss have become an urgent issue. When manufacturing or making green tea beverages, large quantities of tea leaves are subsequently disposed of, which results in potential food loss. Moreover, because many of the tea components remain in the used tea leaves, these continue to have value, as these leaves exhibit antibacterial action. Furthermore, histamine is produced from histidine via histidine decarboxylase that is produced by microorganisms, with histamine accumulation potentially causing histamine food poisoning. Although we have been trying to develop a simple method for detecting histamine, there has yet to be a quick detection method established. We examined whether a method using a low concentration of bromocresol indicator in the culture medium was capable of rapidly detecting histamine. Our results demonstrated that when using lower indicator concentrations, there was a faster detection of histamine production, within 4 h. Using this method, we also investigated whether used tea leaf components, which have antibacterial effects, could suppress histamine production. In this study, used leaves from green, oolong, and black teas were analyzed according to different extraction processes. Compared with green tea, oolong and black teas were able to suppress histamine production using lower concentrations, 25 and 12.5% extracts, respectively. In contrast, the inhibitory effect on histamine production by used green tea leaves required a high concentration of 50% used tea leaf extracts. Furthermore, our results suggested that used tea leaves suppress histamine production and that the inhibitory effects vary according to different extracts. Based on these findings, we propose that (i) a more rapid detection method for histamine should be established and (ii) used tea leaf extracts may have applications in the storage and processing of foods associated with an undesirable production of histamine.

Modified Enzymatic Assays for the Determination of Histamine in Fermented Foods

Histamine is a biogenic amine, produced in spoiled fish and some fermented products, which causes a foodborne disease similar to an allergic reaction. Because regulatory levels on histamine in food have been set by many countries or organizations, a quick and accurate analysis of histamine is of great interest. An enzymatic histamine determination method on the basis of a colorimetric assay has been used to detect histamine for raw and canned tuna due to its simplicity and rapidity. However, note that some compounds in fermented foods interfere with assay results. In this study, the pretreatments and conditions of the assay for fermented foods were evaluated. Lowering the reaction temperature from 37 to 23°C was considerably effective in reducing the interference. As a result, histamine in salami and sauerkraut (≥5 to 10 mg/kg) could be determined with a 25-fold dilution, as in the manufacturer's instructions. Histamine in soy sauce (≥10 to 20 mg/L) could also be determined with a 100-fold dilution. Removing fat and protein in cheese samples by using perchloric acid with a resultant 25-fold dilution and removing polyphenol with polyvinylpolypyrrolidone for red wine with a fivefold dilution were feasible; the limits of quantification were 5 mg/kg and 1 mg/L, respectively. Good recovery rates, precision repeatability, and correlations with a high-performance liquid chromatography method were confirmed. These protocols are expected to be applicable for histamine determination in various foods and useful for preventing histamine food poisoning.

Histamine Production Behaviors of a Psychrotolerant Histamine-Producer, Morganella psychrotolerans, in Various Environmental Conditions.

Histamine food poisoning is a major safety concern related to seafood consumption worldwide. Morganella psychrotolerans is a novel psychrotolerant histamine-producer. In this study, the histamine production behaviors of M. psychrotolerans and two other major histamine-producers, mesophilic Morganella morganii and psychrotrophic Photobacterium phosphoreum, were compared in seafood products, and histamine accumulation by M. psychrotolerans was characterized at various pH and temperature levels in culture broth. The growth of M. psychrotolerans and P. phosphoreum increased similarly at 4°C in canned tuna, but M. psychrotolerans produced much higher levels of histamine than P. phosphoreum. Histamine accumulation by M. psychrotolerans was induced at lower environmental pH condition at 4 and 20°C. The optimal temperature and pH for producing histamine by crude histidine decarboxylase of M. psychrotolerans were 30°C and pH 7, respectively. The activity of the crude HDC extracted from M. psychrotolerans cells at 10°C retained 45% of the activity at 30°C. Histidine decarboxylase gene expression of M. psychrotolerans was induced by low pH conditions. These results suggest that M. psychrotolerans are also a very important histamine-producer leading to histamine poisoning associated with seafood below the refrigeration temperature.

Development of the Genus and Species Determination Method for Histamine Producing Bacteria Isolated from Fishery Product with High-Resolution Melting Analysis

Histamine in foods with a high histidine content may be produced by bacteria with histidine decarboxylase activity. Consumption of food enriched in histamine can produce symptoms of histamine poisoning that include flushing, headache, and urticaria. The number of histamine poisoning cases in Japan has decreased with developments in food hygiene management technology. However, approximately 10 cases are still reported each year. In addition, there have been cases where histamine was detected in the end products, prompting large product recalls. To prevent and identify causes of histamine toxicity, manufacturers must identify the bacteria causing the illness. A simple method of identification is needed, since sequence-based identification is complicated to perform and the analysis takes a long time. High-Resolution Melting Analysis (HRMA) is a method that detects differences in the base sequences of PCR products manifested as varied melting temperatures of double-stranded DNA. The present study was intended to develop a rapid identification method for major histamine-producing bacteria using HRMA. Species-specific HRMA primers were designed that specifically targeted the hdcA gene of 20 Gram-negative histamine-producing bacterial strains. The designed primers were used for HRM analysis of the 20 histamine-producing bacterial strains. The strains were divided into three groups (A, B, and C) based on differences in melting temperature values obtained by Tm Calling analysis program. Group A comprised terrestrial bacteria, such as Morganella, Enterobacter, and Raoultella, while Groups B and C comprised marine bacteria, such as those belonging to the genera Vibrio and Photobacterium. The melting profiles obtained in Group A by HRMA were used to identify the aforementioned terrestrial bacteria. The findings indicated that HRMA can easily identify the major gram-negative histamine-producing bacteria. A flow chart was created to identify histamine-producing bacterial species. This method enables the identification of histamine-producing bacterial species more quickly and easily than conventional sequence-based methods. Therefore, the method could be valuable for food companies to screen raw materials and products and track the source of contamination, which will in turn contribute to the prevention of histamine-food poisoning and investigation of its causes.

Scombroid Fish Poisoning and Histamine Food Poisoning

Scombroid fish poisoning (SFP) is a form of histamine food poisoning caused by the ingestion of improperly stored fish. The term "scombroid" derives from the family name of the fish family first implicated, such as tuna and mackerel. On the other hand, non-scombroid fish species, such as sardine and herring, can also cause histamine poisoning. The histamine is converted from histidine by a bacterial enzyme in the causative fish. Because the symptoms of SFP can easily be confused with food allergies, it is believed to have been significantly under-reported. In 2016, an outbreak of SFP occurred among primary school students who had eaten yellowtail steak in Korea. The most common findings consisted of a rapid onset of flushing of the face and trunk, erythematous and urticarial rash, diarrhea, and headache occurring soon after consuming the spoiled fish. Usually, the course is self-limiting and antihistamines can be used successfully to relieve symptoms, but several life-threatening SFP cases have been reported. Clinical toxicologists should be familiar with SFP and have competency to make a differential diagnosis between fish allergy and histamine poisoning. SFP is a histamine-induced reaction caused by the ingestion of histamine-contaminated fish, whereas a fish allergy is an IgE-mediated reaction. This review discusses the epidemiology, pathophysiology, diagnosis, treatment, and preventive measures of SFP.

The presence of biogenic amines in food as a public health concern. An outline focus on histamine food poisoning.

The presence of biogenic amines in food as a public health concern. An outline focus on histamine food poisoning.

Histamine food poisoning: a sudden, large outbreak linked to fresh yellowfin tuna from Reunion Island, France, April 2017.

On 20 April 2017, an outbreak of histamine food poisoning occurred in a French military unit located near Paris. A total of 40 cases were identified (attack rate: 16.6%). We conducted a case–control study on 31 cases and 63 controls. Multivariate analysis pointed to cooked yellowfin tuna fillet as the very likely source of food poisoning (odds ratio = 156.8; 95% confidence interval: 18.4–1,338.4). The fresh yellowfin tuna was from Reunion Island and was supplied vacuum-sealed and packed with ice at the principal food market of Paris. No cold chain issues could be established in the upstream and downstream supply chains. Histamine concentration was found to be 1,720 mg/kg in leftover raw tuna, and 3,720 mg/kg in control cooked tuna, well above the threshold limit values defined by European regulations (200 mg/kg). The presence of Klebsiella variicola and Pantoea agglomerans, microorganisms of the Enterobacterales order that have been reported to produce histamine, was confirmed in the leftover raw tuna. This type of food poisoning is rarely recognised and confirmed. We describe the outbreak to highlight the specific key points of this type of investigation.

Detection and Characterization of Histamine-Producing Strains of Photobacterium damselae subsp. damselae Isolated from Mullets.

Photobacterium damselae subsp. damselae (Pdd) is considered to be an emerging pathogen of marine fish and has also been implicated in cases of histamine food poisoning. In this study, eight strains isolated from mullets of the genera Mugil and Liza captured in the Ligurian Sea were characterized, and a method to detect histamine-producing Pdd from fish samples was developed. The histamine-producing potential of the strains was evaluated in culture media (TSB+) using a histamine biosensor. Subsequently, two strains were used to contaminate mackerel fillets (4 or 40 CFU/g), simulating a cross-contamination on the selling fish stalls. Sample homogenates were enriched in TSB+. The cultures were then inoculated on thiosulfate-citrate-bile salts-sucrose agar (TCBS) and the dark green colonies were cultured on Niven agar. The violet isolates were characterized using specific biochemical and PCR based tests. All Pdd strains were histamine producers, yielding concentration varying from 167 and 8977 µg/mL in TSB+ cultures incubated at 30 °C for 24 h. Pdd colonies were detected from the inoculated mackerel samples and their histidine decarboxylase gene was amplified using species-specific primer pairs designed for this study. The results indicate that mullets can be source of Pdd and the fish retailers needs to evaluate the risk posed by cross-contamination on the selling fish stalls.

Detection of Histamine in Fish and Fishery Products in Osaka Prefecture (Fiscal 2015 Report).

Histamine food poisoning is caused by ingestion of spoiled fish containing high levels of histamine. This paper reports cases in which histamine was detected in Osaka prefecture in fiscal year 2015 in a survey of fish and fishery products on the market and the food poisoning. A suspected case of histamine food poisoning was also evaluated to investigate the cause and minimize further problems. Histamine in food was separated on SPE cartridge columns, and analyzed after derivatization with fluorescamine by means of HPLC-FL. Histamine was detected in some fishery products on the market and in food that had caused poisoning. The samples in which histamine was detected were semi-dried whole round herring (Urumeiwashi-maruboshi), mackerel (Saba) and sardine dumpling (Iwashi-tsumire). These foods were the main causes of histamine food poisoning according to the report of the Ministry of Health, Labour and Welfare, Government of Japan.

Histamine Food Poisoning.

The consumption of food containing high amounts of histamine and other biogenic amines can cause food poisoning with different symptoms linked to the individual sensitivity and the detoxification activity. Histamine is the only biogenic amine with regulatory limits set by the European Commission in fish and fishery products, because it can lead to a fatal outcome. However, also fermented foods can be involved in outbreaks and sporadic cases of intoxication. The factors affecting the presence of histamine in food are variable and product specific including the availability of the precursor amino acid, the presence of microorganisms producing decarboxylases, and the conditions allowing their growth and enzyme production. Generally, the good quality of raw material and hygienic practices during food processing as well as the use of histidine decarboxylase-negative starter cultures can minimize the occurrence of histamine. Further studies are necessary to estimate the human exposure and the relationship between the total amount of the biogenic amines ingested with food and health effects.

Emerging Approach: Reduce Histamine Poisoning with Diamine Oxidase

Rihaakuru is a cooked fish paste from the Maldives, consumed as a condiment with rice and other food. One of our studies confirmed that Rihaakuru contained up to 10 different biogenic amines, with histamine in excess of 500 ppm (n = 28). This may cause histamine poisoning, with symptoms such as skin rashes, vomiting and fever, thus making it a food security issue in the Maldives. Another study by us developed a regression model that predicted the rate and amount of histamine removal by diamine oxidase (DAO) under varied pH and salt concentrations in the tuna soup used to manufacture Rihaakuru. Based on the results of these studies, a conceptual design in producing histamine-free Rihaakuru is described in this paper. This conceptual design could be used as a guideline in the actual production of histamine-free Rihaakuru. Histamine-free Rihaakuru could be a potential export containing high protein and omega-3. Practical Applications Rihaakuru is a fish paste that is rich in protein, minerals and contains omega 3. However, Rihaakuru can contain more than 500 ppm histamine that may cause food poisoning. This histamine originates from poor quality raw fish used to manufacture this product. The manufacture of Rihaakuru is seen as a way of using poor quality fish. Rihaakuru is generally stable in terms of bacterial deterioration and the only issue is the high histamine level. This research demonstrated on a novel method to prevent histamine food poisoning using diamine oxidase, to degrade the histamine in the fish soup during the manufacture of Rihaakuru. This enables the manufacture of histamine free-Rihaakuru and has the potential to be applied to other foods containing histamine.

Control of Halophilic Histamine-Producing Bacteria by Using Natural Antimicrobials and Other Agents

We have investigated the control of halophilic histamine-producing bacteria, Photobacterium phosphoerum and Photobacterium damselae by using vapor of essential oils and other agents. Three of fourteen essential oils showed high antibacterial activity against histamine-producing bacteria. Among food additives and detergents, ten of twenty-one food additives and seven of nine detergents also showed antibacterial activity. Low concentrations of sodium chloride suppressed the growth of both species. We examined the resistance of these bacteria to dryness on food contact surfaces. After 0.5 hours, no viable cells were detected. So, the bacteria were sensitive to dry conditions. These results should contribute to development of the techniques to prevent histamine food poisoning.

An unusual cause of hypotension and abnormal electrocardiogram (ECG) — scombroid poisoning

Abstract Scombroid fish or histamine food poisoning is an illness typically associated with fish consumption, rarely encountered and reported in Europe. Symptoms develop quickly and resemble an allergic reaction. This paper reports three cases of severe scombroid poisoning in previously healthy patients, which presented diffuse macular erythema, hypotension, palpitations, and abnormal electrocardiogram (ECG). All patients required intensive care, with a complete resolution of symptoms and ECG changes within 24 hours. This is the first Romanian report of scombroid poisoning, emphasizing that medical personnel should be aware of this condition, because symptoms and ECG changes often lead to confusion with other diseases.

Differential characterization of biogenic amine‐producing bacteria involved in food poisoning using MALDI‐TOF mass fingerprinting

Histamine poisoning is caused by the consumption of fish and other foods that harbor bacteria possessing histidine decarboxylase activity. With the aim of preventing histamine formation, highly specific mass spectral fingerprints were obtained from the 16 major biogenic amine-producing enteric and marine bacteria by means of MALDI-TOF MS analysis. All bacterial strains analyzed exhibited specific spectral fingerprints that enabled its unambiguous differentiation. This technique also identified peaks common to certain bacterial groups. Thus, two protein peaks at m/z 4182+/-1 and 8363+/-6 were found to be present in all Enterobacteriaceae species analyzed except for Morganella morganii. Peaks at m/z 3635+/-1 and 7267+/-2 were specific to both M. morganii and Proteus spp. Biogenic amine-forming Proteus spp. exhibited three genus-specific peaks at m/z 3980, 7960+/-1 and 9584+/-2. The genus Photobacterium also showed three genus-specific peaks at m/z 2980+/-1, 4275+/-1 and 6578+/-1. The two histamine-producing Gram-positive bacteria Lactobacillus sp. 30A and Staphylococcus xylosus exhibited a few protein peaks in the 2000-7000 m/z range and could be easily distinguished from biogenic amine-forming Gram-negative bacteria. Clustering based on MALDI-TOF MS also exhibited a good correlation with phylogenetic analysis based on the 16S rRNA gene sequence, validating the ability of the MALDI-TOF technique to establish relationships between microbial strains and species. The approach described in this study leads the way toward the rapid and specific identification of major biogenic amine-forming bacteria based on molecular protein markers with a goal to the timely prevention of histamine food poisoning.