determination of histamine in mahi-mahi fillets (coryphaena hippurus) implicated in a foodborne...

DETERMINATION OF HISTAMINE IN MAHI-MAHI FILLETS(CORYPHAENA HIPPURUS) IMPLICATED IN AFOODBORNE POISONINGjfs_303 320..325

H.C. CHEN1,3, Y.C. LEE2, D.F. HWANG3, T.K. CHIOU3 and Y.H. TSAI2,4

1Southern Center for Regional Administration, Food and Drug Administration, Department of Health, Executive Yuan, Taiwan2Department of Seafood Science, National Kaohsiung Marine University, Kaohsiung 811, Taiwan3Department of Food Science, National Taiwan Ocean University, Keelung, Taiwan

4Corresponding author. TEL:+886-7-3617141-3609; FAX:+886-7-3640634; EMAIL:[email protected]

Accepted for Publication January 10, 2011

doi:10.1111/j.1745-4565.2011.00303.x

ABSTRACT

An incident of foodborne poisoning causing illness in 53 victims due to ingestion offish fillets occurred in January, 2009, in Kaohsiung city, southern Taiwan. The twosuspected fish samples contained 11.3 and 37.7 mg/100 g of histamine, which isgreater than the 5.0 mg/100 g allowable limit suggested by the United States Foodand Drug Administration. Given the allergy-like symptoms of the victims and thehigh histamine content in the suspected fish samples, this foodborne poisoning wasstrongly suspected to be caused by histamine intoxication. Five histamine-producing bacterial strains capable of producing 1.23 to 36.48 ppm of histamine intrypticase soy broth (TSB) supplemented with 1.0% L-histidine (TSBH) were iden-tified as Bacillus subtilis (four strains) and Enterobacter aerogenes (one strain) by 16SrDNA sequencing with polymerase chain reaction (PCR) amplification. Moreover,the fish species of suspected samples were identified as mahi-mahi (Coryphaena hip-purus) by using PCR direct sequence analysis.

PRACTICAL APPLICATIONS

Based on the finding that high contents of histamine (>30 mg/100 g) were detectedin the suspected mahi-mahi samples, we speculate the temperature abuse of thefillets before cooking contributed to the presence of high histamine levels in mahi-mahi fillets and resulted in foodborne poisoning. Although histamine-producingstrains, Bacillus subtilis and Enterobacter aerogenes, were isolated from suspected fishsamples, they might not be the main contributors to histamine accumulationbecause of low histamine production. These results re-emphasize proper handlingtemperature for seafoods and offer an important awareness that Coryphaena hippu-rus fillets could become a hazardous food item in causing histamine poisoning eventhough no quality deficiency was observed on the fillets.

INTRODUCTION

Histamine is the causative agent of scombroid poisoning, afoodborne chemical hazard. Scombroid poisoning is usually amild illness with a variety of symptoms including rash, urti-caria, nausea, vomiting, diarrhea, flushing, and tingling anditching of the skin (Taylor 1986). Severity of the symptomscan vary considerably with the amount of histamine ingestedand the individual’s sensitivity to histamine. Scombroid fish

such as tuna, mackerel, bonito and saury that contain highlevels of free histidine in their muscle are often implicated inscombroid poisoning incidents (Taylor 1989). However,several species of nonscombroid fish such as mahi-mahi,bluefish, herring and sardine have often been implicated inincidents of scombroid poisoning. In Taiwan, scombroid poi-soning occurs occasionally (Chen and Malison 1987; Tsaiet al. 2005a; Chen et al. 2008), and the fish implicated in theseoutbreaks are tuna, mackerel and marlin. Recently, due to

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their popularity in Taiwanese people, sailfish, swordfish andmarlin fillets have become the most frequently implicated fishspecies in scombroid outbreaks in Taiwan (Hwang et al. 1995;Hwang et al. 1997; Tsai et al. 2007; Chang et al. 2008; Chenet al. 2010a,b).

Biogenic amines are formed mainly through the decar-boxylation of specific free amino acids by exogenous decar-boxylases released by the microbial species associated withseafood. Many different bacterial species are known topossess histidine decarboxylase and have the ability toproduce histamine (Taylor and Speckard 1983). Morganellamorganii, Klebsiella pneumoniae and Hafnia alvei have beenisolated from the fish incriminated in scombroid poisoning(Taylor and Speckard 1983). Many enteric bacteria, includ-ing Proteus vulgaris, Proteus mirabilis, Enterobacter aerogenes,Enterobacter cloacae, Serratia fonticola, Serratia liquefaciensand Citrobacter freundii, capable of producing histaminehave been identified in fish (Yoshinaga and Frank 1982;Taylor and Speckard 1983; Middlebrooks et al. 1988; Kimet al. 2003; Tsai et al. 2005b). In addition to the enteric bac-teria, Clostridium spp., Vibrio alginolyticus, Acinetobacterlowffi, Plesiomonas shigelloides, Pseudomonas putida,Pseudomonas fluorescens, Aeromonas spp. and Photobacte-rium 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 ofhistamine-forming Proteus, Enterobacter, Klebsiella, Rahnellaand Acinetobacter in sailfish fillets in Taiwan (Tsai et al.2004) and identified a weak histamine-forming bacteria Sta-phylococcus spp. from swordfish fillets implicated in foodpoisoning (Chang et al. 2008).

Recently, an incident of foodborne poisoning due to inges-tion of fish fillets occurred in Kaohsiung city, southernTaiwan, in January 2009. The incident caused 53 victims tofall ill. They all suffered from allergy-like symptoms, includ-ing rash, nausea, headache, itching and flushing, but all recov-ered within 12 h. To elucidate the causative agent, twosuspected fish fillets were collected from the suspected restau-rant and analyzed for the levels of biogenic amine, totalcoliform (TC), E. coli, and total volatile basic nitrogen(TVBN), and histamine-forming bacteria. In addition, PCRamplification of mitochondrial (mt) DNA sequence analysiswas used to identify the species of the suspected fish sample.

MATERIALS AND METHODS

Samples

Two fish fillets (114 g and 126 g), which were leftover from thesuspected fish item, were collected from the poisoning associ-ated restaurant in junior high school, Kaohsiung city, January2009. The samples had been stored at 4C for half a day before

collection. The samples were collected with aseptic bags,placed in ice and immediately transported to the laboratoryfor analysis.

pH Value, Water Content and TVBNDetermination

The suspected fish fillet sample (10 g) was homogenized inblenders (Omni International Waterbury, CT) for 5 min at5,000 rpm with 10 mL of distilled water to make thick slurry.The pH of this slurry was then measured using a Corning 145pH meter (Corning Glass Works, Medfield, MA). The watercontent was conducted with the standard gravimetricmethod by drying 1–3 g of a test sample at 102.0 � 2.0Cunder atmospheric pressure for 2 h. Consistency of mass wastested by additional drying until the difference in mass didnot exceed 0.5 mg. The TVBN content of each fish sample wasmeasured by the method of Conway’s dish (Cobb et al. 1973).

Microbiological Analysis and Isolation ofHistamine-Forming Bacteria

A 25-g portion of the fish sample was homogenized at highspeed for 2 min in a sterile blender with 225 mL of sterilepotassium phosphate buffer (0.05 M, pH 7.0). The homoge-nates were serially diluted with a sterile phosphate buffer, and1.0 mL aliquots of the dilutes were placed into a Petri-dish,then mixed with aerobic plate count (APC) agar (Difco,Detroit, MI) containing 0.5% NaCl. Bacterial colonies werecounted after the plates were incubated at 35C for 48 h. Thebacterial numbers in the fillet samples were expressed as log10

colony forming unit (cfu)/g.Analyses of TC and E. coli in bothfillet samples were conducted using the three tubes mostprobable number (MPN) methods (FDA 1998).

To isolate histamine-forming bacteria, a 0.1 mL aliquot ofthe homogenized sample was spread on histamine-formingbacterium isolation agar (HBI agar) fortified with L-histidine(Niven et al. 1981). Following incubation of the differentialagar plates for 4 d at 35C, colonies with blue or purple coloron the plates were picked and further streaked on trypticasesoy agar (TSA) (Difco) to obtain pure cultures. The ability ofeach isolated culture to produce biogenic amines was deter-mined by inoculating the isolates in trypticase soy broth(TSB) (Difco) supplemented with 1% L-histidine (TSBH)and incubated without shaking at 35C for 24 h. The presump-tive histamine-forming isolates were identified on the basis ofmorphology, Gram stain, endospore stain, catalase andoxidase reaction. Cell morphology was examined by phase-contrast microscopy. Gram reaction, the presence of oxidaseand catalase were determined as described by Smibert andKrieg (1981). The identity of histamine-forming isolates wasfurther confirmed with polymerase chain reaction (PCR) by

H.C. CHEN ET AL. HISTAMINE CONTENT IN MAHI-MAHI FILLETS

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amplifying and sequencing approximately 1,400 bp of the16S ribosomal DNA (rDNA) of each isolate (Chen et al.2010a).

Biogenic Amine Analysis

Each fillet sample was ground in a Waring Blender (Oster Co.,Milwaukee, WI) for 3 min. The ground samples (5 g) weretransferred to 50 mL centrifuge tubes, added 20 mL of 6%trichloroacetic acid (TCA) and homogenized (Omni Interna-tional Waterbury) for 5 min at 5,000 rpm. The homogenateswere centrifuged (10,000 ¥ g, 10 min, 4C) and filteredthrough Whatman no. 2 filter paper (Whatman, Maidstone,England). The filtrates were then placed in volumetric flasks,and TCA was added to bring to a final volume of 50 mL.Samples of standard biogenic amine solutions and 1 mL ali-quots of the fish fillet extracts were derivatized with dansylchloride, and then analyzed with HPLC system according tothe previously described method (Chen et al. 2010a). Onemilliliter of each bacterial TSBH culture broth inoculated iso-lates was also dansylated using the same procedures for fishfillet extracts. The dansyl derivatives were filtrated througha 0.45-mm filter, and 20 mL aliquots were used for HPLCinjection.

DNA Extraction and PCR Amplification ofFish Species

DNA of suspected fish fillets was extracted according to theprotocol described in our previous study (Tsai et al.2007).ThePCR primers CytBL: 5′-CCATCCAACATCTCAGCATGATGAAA-3′ and CytBH: 5′-CCCCTCAGAATGATATTTGTCCTCA-3′ specific for cyt b gene of fish were designed and used toamplify a 348 bp fragment by PCR (Bartlett and Davidson1991). The PCR amplification reactions and sequencing foridentification of fish species were performed according to thepreviouslydescribedmethod(Chenet al.2010a).Inbrief,PCRreaction was carried out in a Gene-Amp PCR system 2400(Perkin Elmer, Foster City, CA) programmed to perform adenaturation step at 95C for 10 min,followed by 40 cycles con-sisting of 1 min at 95C,1 min at 50C and 2 min at 72C.The lastextension step was extended to 10 min at 72C. PCR product(6 mL) was loaded onto a 2% agarose gel containing 1 mg/mLethidium bromide in TBE buffer and electrophoresed at 50 Vfor 120 min. The DNA band was excised under UV light and

melted in 5 volumes of Tris ethylenediaminetetraacetic acid(TE)bufferat65Cfor5 min.PurifiedDNAPCRproductsweresequenced at Mission Biotech (Taipei,Taiwan) using the aboveprimers and theABI Prism BigDye Terminator Cycle Sequenc-ing Ready Reaction Kit (Perkin-Elmer/Applied BiosystemsDivision, Foster City, CA) in a ABI PRISM 377-96 DNAsequencer (Perkin-Elmer/Applied Biosystems Division). Thesequences were analyzed with the BLAST (NCBI) for identifi-cation of fish species.

RESULTS AND DISCUSSION

Values of the pH, water content,APC, TC, E. coli and TVBN inthe suspected fish fillets responsible for histamine poisoningillness are presented in Table 1. The levels of pH and watercontent in two fillet samples ranged from 6.49 to 6.52 and 59.3to 60.4%, respectively. The two fillet samples had 7.81–7.84log cfu/g of APC, which were greater than the level of 6.47 logcfu/g allowed by Taiwanese regulation for cooked frozenfoods. Although, none of both samples contained E. coli, thefillet samples contained 100 and 110 MPN/g of TC (Table 1).The contents of TVBN in both fish samples were below theTaiwanese regulatory level of 25 mg/100 g (Table 1). Based onthe high levels of APC and TC detected in the fish samples, thesuspected fish fillets could been seriously contaminatedduring processing.

The levels of biogenic amines in the suspected fish filletssamples responsible for histamine poisoning illness are sum-marized in Table 2. Although the contents for other eight bio-genic amines in two fish samples were less than 3.0 mg/100 g,the two fish samples had 11.3 and 37.7 mg/100 g of hista-mine, respectively (Table 2). In most scombroid poisoningcases, histamine levels in illness-causing fish have been above20 mg/100 g, often above 50 mg/100 g (FDA) (United StatesFood and Drug Administration [USFDA] 2001, Chap. 7).Similar observation was also reported by the Centers forDisease Control and Prevention (CDC 2000) that histamineat 20 mg/100 g may be sufficient to cause the symptoms ofscombroid poisoning. Thus, the high levels of histamine inboth fish fillet samples along with the allergy-like symptomsdeveloped in the victims supported the conclusion that hista-mine was the causative agent of this food borne poisoningincident. Various types of fish implicated in scombroid poi-soning have been found to contain high levels of histamine.The histamine content of marlin implicated in a poisoning

TABLE 1. VALUES OF THE PH, WATER CONTENT, TOTAL VOLATILE BASIC NITROGEN (TVBN), AEROBIC PLATE COUNT (APC), TOTAL COLIFORM (TC)AND E. COLI IN THE MAHI-MAHI FILLETS IMPLICATED IN FOOD POISONING

Sample no. pH Water content (%) TVBN (mg/100 g) APC (log cfu/g) TC (MPN/g) E. coli (MPN/g)

1 6.49 60.4 13.5 7.84 110 <32 6.52 59.3 13.2 7.81 100 <3

HISTAMINE CONTENT IN MAHI-MAHI FILLETS H.C. CHEN ET AL.


incident ranged between 93.5 and 276 mg/100 g (Morrowet al. 1991). The hot-smoked mackerel implicated in a scom-brotoxic incident had a histamine content of 270 mg/100 g(Clifford et al. 1989). The histamine content of canned tunaimplicated in a poisoning was 116 mg/100 g, whereas that ofwholesome canned tuna was only 2.74 mg/100 g (Kim andBjeldanes 1979). In Taiwan, scombroid poisoning onlyoccurred occasionally (Chen and Malison 1987; Tsai et al.2005a), and the fish implicated in those occasional outbreakswere tuna, mackerel and marlin. Recently, sailfish, swordfishand marlin fillets have become the most frequently implicatedfish species in scombroid outbreaks in Taiwan (Hwang et al.1995, 1997; Tsai et al. 2007; Chang et al. 2008; Chen et al.2010a,b). However, strong evidence exists that biogenicamines such as putrescine, cadaverine, spermine and spermi-dine in fish tissue can increase the toxic effects of histamine byinhibiting intestinal histamine-metabolizing enzymes such asdiamine oxidase, thereby increasing histamine uptake andliberating endogenous histamine in intestinal fluids (Flicket al. 2001). Quality loss and histamine accumulation oftenoccur after frozen fish of the above mentioned species arethawed and kept for long periods of time at room tempera-ture before further processing. Since histamine is heat resis-tant, it can remain intact in canned or cooked fish products(Lopez-Sabater et al. 1994). In this case, the fish fillets mighthave been stored at an improper temperature before cookingand allowed formation of histamine by histamine producers.

The suspected fillet samples produced 25 purple colonieson the differential HBI agar plates. Only five of them (20%)produced histamine in TSBH medium. The remaining 20 iso-lates were false-positive histamine-formers. Table 3 listed the

identity of the five histamine-forming bacteria as determinedby 16S rDNA sequences, following comparison with referencestrains, using NCBI database analysis. The PCR ampliconsfrom strains A1, A2, A3 and B1 had a 100% homology withBacillus subtilis, while that from strain B2 aligned with Entero-bacer aerogenes at 100% homology (Table 3). The fourhistamine-forming isolates identified as B. subtilis by 16SrDNA sequencing produced small amounts of histamine(1.23 to 2.90 ppm) in TSBH medium (Table 3). Bacillus spp.capable of producing low levels of histamine at 10.5–12.4 ppm have been isolated from salted anchovies(Hernandez-Herrero et al. 1999). Recently, strains of Bacilluscoagulans and Bacillus megaterium were isolated from fer-mented fish products in Taiwan as weak histamine-formingbacteria (Tsai et al. 2006).

The E. aerogenes strain B2 isolated in this study was a weakhistamine former, and it produced only 36.48 ppm of hista-mine in TSBH.Strains of Enterobacter spp.have often been iso-lated from various species of scombroid fish and werefrequently reported as prolific histamine formers in tuna(Lopez-Sabateret al.1996),albacore(Kimet al.2001)andsail-fish (Tsai et al.2004).Recently,E.aerogenes isolated from driedmilkfish was reported to be potent histamine-formers capableof producing >500 ppm of histamine in TSBH (Hsu et al.2009). However, the four B. subtilis and one E. aerogenes iso-lated in this study produced small amounts of histamine inculture broth, indicating that they might not be the main con-tributors to histamine accumulation in the suspected fishfillets. It was possible that the major histamine-forming bacte-ria that contributed to the high levels of histamine in the sus-pected fish fillets might be killed during thawing or re-freezing

TABLE 2. THE LEVELS OF BIOGENIC AMINESIN THE MAHI-MAHI FILLETS IMPLICATED INFOOD POISONING Sample no.

Levels of biogenic amine (mg/100 g)

Put* Cad Try Phe Spd Spm His Tyr Agm

1 2.67 0.15 ND† ND 2.10 ND 11.3 1.07 ND2 0.40 0.48 ND ND ND ND 37.7 3.00 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).

TABLE 3. IDENTIFICATION OF HISTAMINE-FORMING BACTERIA ISOLATED FROM THE MAHI-MAHI FILLETS IMPLICATED IN FOOD POISONING BY 16SRDNA, BASED ON THE OUTPUT RESULTS FROM NCBI DATABASE ANALYSIS, AND THEIR PRODUCTION OF HISTAMINE AND OTHER BIOGENIC AMINES(PPM) IN CULTURE BROTH

Strain Organism identified Percentage identity (%) Gene bank accession number His* Put Try Spd

A1 Bacillus subtilis 100 HQ007937.1 2.90 ND† 7.01 1.11A2 B. subtilis 100 HQ007937.1 2.78 4.57 3.74 0.40A3 B. subtilis 100 HQ007937.1 1.74 21.8 ND 0.40B1 B. subtilis 100 HQ007937.1 1.23 9.0 1.57 11.7B2 Enterobacter aerogenes 100 AB244456.1 36.48 2.20 0.15 0.10

* His, histamine; Put, putrescine; Try, tryptamine; Spd, spermidine.† ND, not detected (amine level less than 0.05 ppm).



process and heating process,or could not grow on the HBI agaror TSBH medium that were used.

The DNA extracts from the suspected fillet samples weretested for PCR amplification with the CytBL and CytBHprimers, which generated a 348-bp fragment. This sequencewas submitted to Genebank for accession number AM265579of Coryphaena hippurus (mahi-mahi) (Fig. 1). Consequently,the fish species of suspected mahi-mahi fillet was identified asC. hippurus. Because the suspected fish samples implicated inhistamine poisoning are usually heavily heated, the proteinsin the fish samples have degraded and almost all proteins weredenatured and damaged. Therefore, protein analysis methodsfor fish species identification, such as sodium dodecyl sulfate-polyacrylamide gel electrophoresis, isoelectric focusing andtwo-dimensional electrophoresis are inappropriate. The PCRtechnique and direct sequence analysis of mitochondrial cyt bgene are successfully for fish species identification. In conclu-sion, scombroid poisoning linked to consumption of mahi-mahi has rarely been reported in Taiwan. Therefore, it is veryimportant for Taiwanese people to be aware that C. hippurusfillets could become a hazardous food item in causing hista-mine poisoning if the fish is contaminated with histamine-forming bacteria and stored at improper temperatures.

ACKNOWLEDGMENTS

The study was supported by the National Science Council,R.O.C. (Contract No. NSC 97-2313-B-022-002 MY3).

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1 50

AM265579 ~~~ACCAGTC TACGAAAATC CCACCCATTA TTAAAAATCG CTAATGACGC

Sample ATGACCAGTC TACGAAAATC CCACCCATTA TTAAAAATCG CTAATGACGC

51 100

AM265579 GCTAATTGCA CTTCCCACAC CATCTAACAT CTCAGCCTGA TGAAATTTCG

Sample GCTAATTGCA CTTCCCACAC CATCTAACAT CTCAGCCTGA TGAAATTTCG

101 150

AM265579 GCTCACTCCT GGGAATTTGA CTTCTCACCC AAATCTTGAC AGGACTCTTC

Sample GCTCACTCCT GGGAATTTGA CTTCTCACCC AAATCTTGAC AGGACTCTTC

151 200

AM265579 CTCGCAATAC ACTACACAGC AGACATTGCC ACGGCTTTCC CCTCCGTCGC

Sample CTCGCAATAC ACTACACAGC AGACATTGCC ACGGCTTTCC CCTCCGTCGC

201 250

AM265579 CCATATTTGC CGGGATGTAA ACTACGGATG ACTAATCCGA AACCTACATG

Sample CCATATTTGC CGGGATGTAA ACTACGGATG ACTAATCCGA AACCTACATG

251 300

AM265579 CTAACGGAGC TTCATTCTTTC TTTATCTGTG TCTACTTCCA CATTGGTCGA

Sample CTAACGGAGC TTCATTCTTTC TTTATCTGTG TCTACT~~~~ ~~~~~~~~~~

FIG. 1. DNA SEQUENCES OF 348-BPREGION OF CYTOCHROME B GENE FROMSUSPECTED FISH SAMPLE AND ACCESSIONNO. AM265579 OF CORYPHAENAHIPPURUS (MAHI-MAHI)

HISTAMINE CONTENT IN MAHI-MAHI FILLETS H.C. CHEN ET AL.


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