determination of histamine and bacterial isolation in marlin fillets (makaira nigricans) implicated...

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DETERMINATION OF HISTAMINE AND BACTERIAL ISOLATIONIN MARLIN FILLETS (MAKAIRA NIGRICANS) IMPLICATED IN A

FOODBORNE POISONING

H.C. CHEN1,3, Y.C. LEE2, C.M. LIN2, D.F. HWANG3 and Y.H. TSAI2,4

1Southern Region LaboratoryBureau of Foods and Drug Analysis

Department of HealthExecutive Yuan, Taiwan

2Department of Seafood ScienceNational Kaohsiung Marine University

Kaohsiung, 811, Taiwan

3Department of Food ScienceNational Taiwan Ocean University

Keelung, Taiwan

Accepted for Publication November 10, 2009

ABSTRACT

An incident of foodborne poisoning causing illness in seven victims dueto ingestion of marlin fillets occurred in August, 2008, in Kaohsiung City,southern Taiwan. The two suspected marlin samples contained 47.8 and43.5 mg/100 g of histamine, which is greater than the 5.0 mg/100 g allow-able limit suggested by the U.S. Food and Drug Administration. Given theallergy-like symptoms of the victims and the high histamine content in thesuspected marlin samples, this foodborne poisoning was strongly suspectedto be due to histamine intoxication. Two histamine-producing bacterialstrains capable of producing 3.10 ppm and 4.20 ppm of histamine in trypti-case soy broth (TSB) supplemented with 1.0% L-histidine (TSBH) were iden-tified as Bacillus subtilis by 16S rDNA sequencing with polymerase chainreaction amplification. However, major histamine-forming bacteria mighthave been killed during the preparation of fillets before serving and thesetwo B. subtilis isolates might not be the main contributors to histamineaccumulation in suspected fillets.

4 Corresponding author. TEL: +886-7-3617141-3609; FAX: +886 73640634; EMAIL: [email protected]

DOI: 10.1111/j.1745-4565.2010.00234.x

Journal of Food Safety 30 (2010) 699–710.© 2010, Wiley Periodicals, Inc. 699

PRACTICAL APPLICATIONS

Based on the finding that high contents of histamine (>40 mg/100 g) weredetected in the suspected marlin samples, we speculate the temperature abuseof the fillets before cooking contributed to the presence of high histaminelevels in marlin fillets and resulted in foodborne poisoning. Although twohistamine-producing Bacillus subtilis strains were isolated from suspected fishsamples, both might not to be the main contributors to histamine accumulationbecause of low histamine production. These results re-emphasize proper han-dling temperature for seafoods and offer an important awareness whichMakaira nigricans fillets could become a hazardous food item in causinghistamine poisoning even though no quality deficiency was observed on thefillets.

INTRODUCTION

Histamine is the causative agent of scombroid poisoning, a foodbornechemical hazard. Scombroid poisoning is usually a mild illness with a varietyof symptoms, including rash, urticaria, nausea, vomiting, diarrhea, flushingand tingling and itching of the skin (Taylor 1986). Severity of the symptomscan vary considerably with the amount of histamine ingested and the individu-al’s sensitivity to histamine. Scombroid fish such as tuna, mackerel, bonito andsaury that contain high levels of free histidine in their muscle are oftenimplicated in scombroid poisoning incidents (Taylor 1986). However, severalspecies of nonscombroid fish such as mahi-mahi, bluefish, herring and sardinehave often been implicated in incidents of scombroid poisoning. In Taiwan,scombroid poisoning occurs occasionally (Chen and Malison 1987; Tsai et al.2005a; Chen et al. 2008), and the fish implicated in these outbreaks are tuna,mackerel and marlin. Recently, because of their popularity among the Taiwan-ese, sailfish, swordfish and marlin fillets have become the most frequentlyimplicated fish species in scombroid outbreaks in Taiwan (Hwang et al. 1995;Hwang et al. 1997; Tsai et al. 2007; Chang et al. 2008; Chen et al. 2010).

Biogenic amines are formed mainly through the decarboxylation of spe-cific free amino acids by exogenous decarboxylases released by the microbialspecies associated with the seafood. Many different bacterial species areknown to possess histidine decarboxylase and have the ability to producehistamine (Taylor and Speckard 1983). Morganella morganii, Klebsiella pneu-moniae and Hafnia alvei have been isolated from the fish incriminated inscombroid poisoning (Taylor and Speckard 1983). Many enteric bacteria,including Proteus vulgaris, Proteus mirabilis, Enterobacter aerogenes,Enterobacter cloacae, Serratia fonticola, Serratia liquefaciens and Citro-

700 H.C. CHEN ET AL.

bacter freundii, capable of producing histamine, have been identified in fish(Yoshinaga and Frank 1982; Taylor and Speckard 1983; Middlebrooks et al.1988; Kim et al. 2003; Tsai et al. 2005b). In addition to the enteric bacteria,Clostridium spp., Vibrio alginolyticus, Acinetobacter lowffi, Plesiomonasshigelloides, Pseudomonas putida, Pseudomonas fluorescens, Aeromonas spp.and Photobacterium spp. have also been reported as histamine producers(Middlebrooks et al. 1988; Yatsunami and Echigo 1991; Okuzumi et al. 1994).We also demonstrated the presence of histamine-forming Proteus, Entero-bacter, Klebsiella, Rahnella and Acinetobacter in sailfish fillets in Taiwan(Tsai et al. 2004), and identified a weak histamine-forming bacteria Staphylo-coccus spp. from swordfish fillets implicated in food poisoning (Chang et al.2008).

An incident of foodborne poisoning due to ingestion of fish filletsoccurred in Kaohsiung city, southern Taiwan, in August 2008. The incidentcaused seven victims to fall ill. They all suffered from allergy-like symptoms,including rash, nausea, diarrhea and flushing, but all recovered within 24 h. Toelucidate the causative agent, the two suspected marlin fillets were collectedfrom the suspected restaurant and analyzed for the levels of biogenic amine,total coliform, Escherichia coli, total volatile basic nitrogen and histamine-forming bacteria. In addition, polymerase chain reaction (PCR) amplificationof mitochondrial (mt) DNA sequence analysis was used to identify the speciesof the suspected fish sample.

MATERIALS AND METHODS

Samples

Two raw fish fillets (147 g and 165 g) that were left over from thesuspected fish item were collected from the poisoning associated restaurant inKaohsiung city, August 2008. The samples were stored at 4C for half a daybefore collection. The samples were collected with aseptic bags, placed in iceand immediately transported to the laboratory for analysis.

pH Value, Water Content, Salt Content and Total Volatile BasicNitrogen (TVBN) Determination

The suspected fish fillet sample (10 g) was homogenized in blenders with10 mL of distilled water to make thick slurry. The pH of this slurry was thenmeasured using a Corning 145 pH meter (Corning Glass Works, Medfield,MA). The water content was conducted with the standard gravimetric methodby drying 1–3 g of a test sample at 102.0 � 2.0C under atmospheric pressurefor 2 h. Consistency of mass was tested by additional drying until the

701BACTERIAL ISOLATION IN MARLIN FILLETS

difference in mass did not exceed 0.5 mg. The salt content in each sample wasdetermined according to the AOAC procedures (1995). The TVBN content ofeach fish sample was measured by the method of Conway’s dish (Cobb et al.1973).

Microbiological Analysis and Isolation of Histamine-Forming Bacteria

A 25-g portion of the fish sample was homogenized at high speed for2 min in a sterile blender with 225 mL of sterile potassium phosphate buffer(0.05 M, pH 7.0). The homogenates were serially diluted with a sterile phos-phate buffer, and 1.0 mL aliquots of the dilutes were placed onto a Petri-dish,then mixed wtih aerobic plate count (APC) agar (Difco, Detroit, MI) contain-ing 0.5% NaCl. Bacterial colonies were counted after the plates were incu-bated at 35C for 48 h. The bacterial numbers in the fillet samples wereexpressed as log10 colony forming units (cfu)/g. Analyses of total coliform andE. coli in both fillet samples were conducted using the three tubes mostprobable number (MPN) methods (FDA 1998).

To isolate histamine-forming bacteria, a 0.1-mL aliquot of the dilutedsample was spread on histamine-forming bacterium isolation agar (HBI agar)fortified with l-histidine (Niven et al. 1981). Following incubation of thedifferential agar plates for 4 days at 35C, colonies with blue or purple color onthe plates were picked and further streaked on trypticase soy agar (Difco) toobtain pure cultures. The ability of each isolated culture to produce biogenicamines was determined by inoculating the isolates in trypticase soy broth(TSB) (Difco) supplemented with 1% l-histidine (TSBH) and incubatedwithout shaking at 35C for 24 h. The presumptive histamine-forming isolateswere identified on the basis of morphology, Gram stain, endospore stain,catalase and oxidase reaction. Cell morphology was examined by phase-contrast microscopy. Gram reaction, the presence of oxidase and catalase,were determined as described by Smibert and Krieg (1981). The identity ofhistamine-forming isolates was further confirmed with PCR by amplifying andsequencing approximately 1,400 bp of the 16S ribosomal DNA (rDNA) ofeach isolate (Chen et al. 2010).

Biogenic Amine Analysis

Each fillet sample was ground in a Waring Blender (Oster Co., Milwau-kee, WI) for 3 min. The ground samples (5 g) were transferred to 50-mLcentrifuge tubes and homogenized with 20 mL of 6% trichloroacetic acid(TCA) for 3 min. The homogenates were centrifuged (10,000 ¥ g, 10 min, 4C)and filtered through Whatman No. 2 filter paper (Whatman, Maidstone, U.K.).The filtrates were then placed in volumetric flasks, and TCA was added tobring to a final volume of 50 mL. Samples of standard biogenic amine


solutions and 1 mL aliquots of the fish fillet extracts were derivatized withdansyl chloride, and then analyzed with high-performance liquid chromatog-raphy (HPLC) system according to the previously described method (Chenet al. 2010). One milliliter of each bacterial TSBH culture broth inoculatedisolates was also dansylated using the same procedures for fish fillet extracts.The dansyl derivatives were filtrated through a 0.45-mm filter, and 20 mLaliquots were used for HPLC injection.

DNA Extraction and PCR Amplification of Fish Species

The DNA of suspected fish fillets was extracted according to the protocoldescribed in our previous study (Tsai et al. 2007). The PCR primersCytBL: 5′-CCATCCAACATCTCAGCATGATGAAA-3′ and CytBH: 5′-CCCCTCAGAATGATATTTGTCCTCA-3′ specific for the cyt b gene of fishwere designed and used to amplify a 348 bp fragment in PCR (Bartlett andDavidson 1991). The PCR amplification reactions and sequencing for identi-fication of fish species were performed according to the previously describedmethod (Chen et al. 2010). In brief, PCR reaction was carried out in a Gene-Amp PCR system 2400 (Perkin Elmer, Foster City, CA) programmed toperform a denaturation step at 95C for 10 min, followed by 40 cycles consist-ing of 1 min at 95C, 1 min at 50C and 2 min at 72C. The last extension stepwas extended to 10 min at 72C. The PCR product (6 mL) was loaded onto a 2%agarose gel containing 1 mg/mL ethidium bromide in TBE buffer and electro-phoresed at 50 V for 120 min. The DNA band was excised under ultravioletlight and melted in five volumes of Tris ethylenediaminetetraacetic acid (TE)buffer at 65C for 5 min. Purified DNA PCR products were sequenced atMission Biotech (Taipei, Taiwan) using the previously mentioned primers andthe ABI Prism BigDye Terminator Cycle Sequencing Ready Reaction Kit(Perkin-Elmer/Applied Biosystems Division, Foster City, CA) in a ABIPRISM 377-96 DNA sequencer (Perkin-Elmer/Applied Biosystems Division).The sequences were analyzed with the BLAST (NCBI) for identification offish species.

RESULTS AND DISCUSSION

Values of the pH, water content, salt content, APC, total coliform (TC),E. coli and TVBN in the suspected fish fillets responsible for histaminepoisoning illness are presented in Table 1. The levels of pH, water content andsalt content in two fillet samples ranged from 6.57 to 6.60, 56.3–56.4% and4.99–5.21%, respectively. In a Taiwanese restaurant, the fish fillet is preparedby smearing the raw fillet with salt and/or vinegar for several minutes to half


an hour and then fried for consumption. The higher salt content and lowerwater content of the suspected fish fillets observed in this work may be relatedto the addition of salt. The two fillet samples had 2.8–2.9 log cfu/g of APC thatwere below the Taiwanese regulatory level of 6.47 log cfu/g. None of bothsamples contained TC and E. coli. The higher salt contents (>4.90%) in bothfish samples apparently had some inhibitory effect on APC and coliformbacterial growth. The contents of TVBN in both fish samples were below theTaiwanese regulatory level of 25 mg/100 g (Table 1).

A typical chromatographic profile of nine standard biogenic amines bythe gradient elution system was developed (Fig. 1). All nine amines were wellseparated in 22 min total run time with good peak resolution, sharpness andsymmetry. The levels of biogenic amines in the suspected fish fillets samplesresponsible for histamine poisoning illness are summarized in Table 2.Although the contents for other eight biogenic amines in two fish samples wereless than 5.0 mg/100 g, the two fish samples had 47.8 and 43.5 mg/100 g ofhistamine, respectively (Table 2). In most cases, histamine levels in illness-causing fish have been above 20 mg/100 g, often above 50 mg/100 g (FDA)(USFDA 2001, chap. 7). A similar observation was also reported by theCenters for Disease Control and Prevention (CDC 2000): histamine at 20 mg/100 g may be sufficient to cause the symptoms of scombroid poisoning. Thus,the high levels of histamine in both fish fillet samples, along with the allergy-like symptoms developed in the victims, supported the conclusion that hista-mine was the causative agent of this foodborne poisoning incident. Varioustypes of fish implicated in scombroid poisoning have been found to containhigh levels of histamine. The histamine content of marlin implicated in apoisoning incident ranged between 93.5 and 276 mg/100 g (Morrow et al.1991). The hot-smoked mackerel implicated in a scombrotoxic incident had ahistamine content of 270 mg/100 g (Clifford et al. 1989). The histaminecontent of canned tuna implicated in a poisoning was 116 mg/100 g, while thatof wholesome canned tuna was only 2.74 mg/100 g (Kim and Bjeldanes1979). In Taiwan, scombroid poisoning only occurred occasionally (Chen andMalison 1987; Tsai et al. 2005a), and the fish implicated in those occasional

TABLE 1.VALUES OF THE pH, WATER CONTENT, SALT CONTENT, TOTAL VOLATILE BASICNITROGEN (TVBN), AEROBIC PLATE COUNT (APC), TOTAL COLIFORM (TC) ANDESCHERICHIA COLI IN THE MARLIN FILLETS IMPLICATED IN FOOD POISONING

Sample no. pH Watercontent (%)

Saltcontent (%)

TVBN(mg/100 g)

APC(log cfu/g)

TC(MPN/g)

E. coli(MPN/g)

1 6.57 56.4 4.99 24.6 2.8 <3 <32 6.60 56.3 5.21 23.5 2.9 <3 <3


FIG. 1. THE HIGH-PERFORMANCE LIQUID CHROMATOGRAPHY PROFILES OFBIOGENIC AMINES IN ONE SUSPECTED MARLIN SAMPLE THAT CONTAINS 47.8 mgHISTAMINE/100 g (UPPER), ALONG WITH AUTHENTIC BIOGENIC AMINES (LOWER)


outbreaks were tuna, mackerel and marlin. Recently, sailfish, swordfish andmarlin fillets have become the most frequently implicated fish species inscombroid outbreaks in Taiwan (Hwang et al. 1995, 1997; Tsai et al. 2007;Chang et al. 2008; Chen et al. 2010). However, strong evidence exists thatbiogenic amines such as putrescine, cadaverine, spermine and spermidine infish tissue can increase the toxic effects of histamine by inhibiting intestinalhistamine-metabolizing enzymes such as diamine oxidase, thereby increasinghistamine uptake and liberating endogenous histamine in intestinal fluids(Flick et al. 2001). Quality loss and histamine accumulation often occur afterfrozen fish of the previously mentioned species are thawed and kept for longperiods of time at room temperature before further processing. Because his-tamine is heat-resistant, it can remain intact in canned or cooked fish products(Lopez-sabater et al. 1994). In this study, the temperature abuse of the filletsbefore cooking could be the reason for the presence of toxic levels of histaminein the fish fillets.

The suspected fillet samples produced eight purple colonies on the dif-ferential HBI agar plates. Only two of them (25%) produced histamine inTSBH medium. The remaining six isolates were false-positive histamineformers. Table 3 listed the identity of the two histamine-forming bacteria asdetermined by 16S rDNA sequences, following comparison to referencestrains, using NCBI database analysis. The PCR amplicons from strains MnB4and MnB5 had a 100% homology with Bacillus subtilis (Table 3). The twohistamine-forming isolates as B. subtilis by 16S rDNA sequencing producedsmall amounts of histamine (4.20 and 3.10 ppm) in TSBH medium. Bothstrains also produced different amounts of putrescine, tryptamine and spermi-dine (Table 3). Bacillus spp. capable of producing low levels of histamine at10.5–12.4 ppm have been isolated from salted anchovies (Hernandez-Herreroet al. 1999). The recently isolated B. coagulans and B. megateriumfrom fermented fish products in Taiwan were also identified as weak

TABLE 2.THE LEVELS OF BIOGENIC AMINES IN THE MARLIN FILLETS IMPLICATED IN

FOOD POISONING

Sampleno.

Levels of biogenic amine (mg/100 g)

Put* Cad Try Phe Spd Spm His Tyr Agm

1 2.70 ND‡ ND 0.20 ND ND 47.8 0.17 ND2 2.10 4.70 ND 0.27 ND ND 43.5 0.16 ND

* Put, putrescine; Cad, cadaverine; Try, tryptamine; Phe, 2-phenylethylamine; Spd, spermidine; Spm,spermine; His, histamine; Tyr, tyramine; and Agm, agmatine.

‡ ND, not detected (amine level less than 0.05 mg/100 g).


histamine-forming bacteria (Tsai et al. 2006). Two B. subtilis isolates in thisstudy produced small amounts of histamine in culture broth, indicating thatthey were not the main contributors to histamine accumulation in the suspectedmarlin fillets. It was possible that the major histamine-forming bacteria thatcontributed to the higher levels of histamine in the suspected fish fillets mightbe killed or inhibited during thawing or re-freezing and heating processes, orcould not grow on the HBI agar or TSBH medium that were used.

The DNA extracts from the suspected fillet samples were tested for PCRamplification with the CytBL and CytBH primers, which generated a 348 bpfragment. This sequence was submitted to Genebank for accession numberDQ080246 of Makaira nigricans (blue marlin) (data not shown). Conse-quently, the fish species of suspected marlin fillet was identified as M. nigri-cans. Because the suspected fish samples implicated in histamine poisoningare usually heavily heated, the proteins in the fish samples have degraded andalmost all proteins were denatured and damaged. Therefore, protein analysismethods for fish species identification, such as sodium dodecyl sulfate-polyacrylamide gel electrophoresis, isoelectric focusing and two-dimensionalelectrophoresis are inappropriate. The PCR technique and direct sequenceanalysis of the mitochondrial cyt b gene are successful for fish species iden-tification. Recently, M. nigricans was identified as a vehicle for in histaminefoodborne poisonings in Taiwan (Tsai et al. 2007). Therefore, it is also veryimportant for the Taiwanese people to be aware that M. nigricans fillets couldbecome a hazardous food item in causing histamine poisoning if the fish iscontaminated with histamine-forming bacteria and stored at improper holdingtemperatures.

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AOAC 1995. Official Methods of Analysis of AOAC International, 16th Ed.,AOAC International, Arlington, VA.

TABLE 3.IDENTIFICATION OF HISTAMINE-FORMING BACTERIA ISOLATED FROM THE MARLIN

FILLETS IMPLICATED IN FOOD POISONING BY 16S RDNA, BASED ON THE OUTPUTRESULTS FROM NCBI DATABASE ANALYSIS, AND THEIR PRODUCTION OF HISTAMINE

AND OTHER BIOGENIC AMINES (ppm) IN CULTURE BROTH

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MnB4 Bacillus subtilis 100 EF488088 4.20 0.06 0.11 1.79MnB5 Bacillus subtilis 100 AY787000 3.10 0.05 0.14 0.81

* His, histamine; Put, putrescine; Try, tryptamine; Spd, spermidine.


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determination of histamine and bacterial isolation in marlin fillets (makaira nigricans) implicated...

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