Determination of histamine and bacterial isolation in swordfish fillets (Xiphias gladius) implicated in a food borne poisoning Shu-Chen Changa,

Hsien-Feng Kunga, Hwi-Chang Chenb, Chung-Saint Linc, YungHsiang Tsaid, ,

a

Department of Food Science and Technology, Tajen University, Pingtung, Taiwan, ROC Southern Region Laboratory, Bureau of Foods and Drug Analysis, b Department of Health, Executive Yuan, Taiwan, ROC
c

Department of Food Science, Yuanpei University, Hsin-Chu, Taiwan, ROC Department of Seafood Science, National Kaohsiung Marine d University, Kaohsiung 811, Taiwan, ROC Received 22 July 2006; revised 8 January 2007; Accepted 15 January 2007. Available online 13 February 2007.

Abstract
An incident of food borne poisoning causing illness in 43 victims due to ingestion of swordfish fillets occurred in December, 2004, in Taichung Prefecture, central Taiwan. Eight frozen raw swordfish fillets were collected from the suspected restaurant and analyzed for bacterial content and histamine -related quality. The levels of aerobic plate count, total coliform, and total volatile basic nitrogen in all samples ranged from 5.39 to 6.71 log CFU/g, <31360 most probable number (MPN)/g, and 6.4414.56 mg/100 g, respectively. None of these samples contained Escherichia coli. The suspected swordfish fillets contained 85.9 293.7 mg/100 g of histamine greater than the hazard action level of 50 mg/100 g set by the US. Food and Drug Administration (FDA) for tuna fish. Given the allergy-like symptoms of the victims and the high histamine content in the suspected swordfish fillets, this food borne poisoning was strongly suspected to be due to histamine intoxication. In addition, although ten histamine -producing bacteria strains, capable of producing 12.733.0 ppm of histamine in trypticase soy broth supplemented with 1.0% L-histidine, were identified as Staphylococcus sp. (one strain), S. aureus (two strains) and S. aureus subsp. aureus (seven strains), by 16S rDNA sequencing with PCR amplification, they were not determined to be the main contributors to histamine accumulation in suspected swordfish fillets. Keywords: Histamine ; Swordfish; Histamine -forming bacteria; Staphylococcus aureus; Food poisoning

Article Outline

1. Introduction 2. Materials and methods 2.1. Samples 2.2. Microbiological analysis and isolation of histamine-forming bacteria 2.3. Determination of total volatile basic nitrogen (TVBN) 2.4. Identification of histamine-forming isolates 2.5. Biogenic amine analysis 3. Results and discussion
o o o o o

4. Conclusion Acknowledgement References

1. Introduction
Histamine is the causative agent of scombroid poisoning, a food borne chemical hazard. Scombroid poisoning is usually a mild illness with a variety of symptoms including rash, urticaria, nausea, vomiting, diarrhea, flushing, and tingling and itching of the skin (Taylor, 1986). Severity of the symptoms can vary considerably with the amount of histamine ingested and the individuals sensitivity to histamine (Russell & Maretic, 1986). Scombroid fish such as tuna, mackerel, bonito, and saury that contain high levels of free histidine in their muscle are often implicated in scombroid poisoning incidents (Taylor, 1986). However, several species of nonscombroid fish such as mahimahi, bluefish, herring, and sardine have often been implicated in incidents of scombroid poisoning (Price & Melvin, 1994). In Taiwan, scombroid poisoning occurs occasionally ( [Chen and Malison, 1987] , [Murray and Hobbs, 1982] and [Tsai et al., 2005] ), and the fish implicated in these outbreaks are tuna, mackerel, and black marlin. Recently, due to their popularity in Taiwanese people, sailfish and marlin fillets have become the most frequently implicated fish species in scombroid outbreaks in Taiwan ( [Hwang et al., 1995] , [Hwang et al., 1997] and [Hwang et al., 1999] ). Biogenic amines are formed mainly through the decarboxylation of specific free amino acids by exogenous decarboxylases released by the microbial species associated with the seafood (Rawles, Flick, & Martin, 1996). Many different bacterial species are known to possess histidine decarboxylase and have the ability to produce histamine (An & Ben-Gigirey, 1998). Although, only Morganella (Proteus) morganii, Klebsiella pneumoniae and Hafnia alvei have been isolated from the fish incriminated in scombroid poisoning (Taylor & Speckard, 1983), a variety of other bacterial species capable of producing histamine have been identified in fish ( [Eitenmiller et al., 1981] , [Middlebrooks et al., 1988] , [Taylor and Speckard, 1983] and [Yoshinaga and Frank, 1982] ). Among them are the enteric bacteria that include P. vulgaris, P. mirabilis, Enterobacter aerogenes, E. cloacae, Serratia fonticola, S. liquefaciens and Citrobacter freundii ( [Ababouch et al., 1991] , [Klausen and Huss, 1987] , [Lopez-Sabater et al., 1996] and [Tsai, Lin et al., 2005] ). In addition to the enteric bacteria, Clostridium spp., Vibrio alginolyticus, Acinetobacter lowffi, Plesiomonas shigelloides, Pseudomonas putida, P. fluorescens, Aeromonas spp. and Photobacterium spp. have also been reported as histamine producers ( [Lopez-Sabater et al., 1994] , [Middlebrooks et al., 1988] , [Okuzumi et al., 1994] , [Ryser et al., 1984] and [Yatsunami and Echigo, 1991] ). Recently, we demonstrated the presence of histamine -forming Proteus, Enterobacter, Klebsiella, Rahnella and Acinetobacter in sailfish fillets in Taiwan, but failed to isolate any of the three above mentioned major histamine formers the H. alvei, M. morganii and K. pneumoniae (Tsai, Kung, Lee, Lin, & Hwang, 2004). In addition, histamine -forming bacteria from marlin fillets implicated in food poisoning have been studied but not isolated (Hwang et al., 1999). An incident of food borne poisoning due to ingestion of swordfish fillets occurred in Taichung Prefecture, central Taiwan, in December 2004. The incident caused 43 victims to fall ill. They all suffered from allergy-like symptoms, including rash, nausea, diarrhea, and flushing, but all recovered within 24 h. To elucidate the causative agent, the suspected swordfish fillet was collected from the suspected restaurant were analyzed for biogenic amine levels. In addition, the levels of total coliform, E. coli, and total volatile basic nitrogen

(TVBN) and histamine -forming bacteria in suspected swordfish samples were also investigated.

2. Materials and methods

2.1. Samples Eight frozen raw swordfish fillets were collected from the suspected restaurant in Taichung Prefecture, where the victims ate the suspected fillets that caused the poisoning. The fish species of swordfish fillets was identified as Xiphias gladius (Tsai et al., in press). After collection, all fillet samples were kept at 4 C and immediately transported to the laboratory for analysis. 2.2. Microbiological analysis and isolation of histamine -forming bacteria A 25-g portion of the fillet sample was homogenized at high speed for 2 min in a sterile blender with 225 ml of sterile potassium phosphate buffer (0.05 M, pH 7.0). The sterile blender was prepared by autoclaving for 15 min at 121 C. The homogenates were serially diluted with a sterile phosphate buffer, and 1.0 ml aliquots of the dilutes were inoculated into aerobic plate count (APC) agar (Difco, Detroit, MI, USA) containing 0.5% NaCl. Bacterial colonies were counted after the plates were incubated at 35 C for 48 h. The bacterial numbers in the fillet samples were expressed as log10 colony forming units (CFU)/g. To isolate histamine -forming bacteria, a 0.1 ml aliquot of the diluted sample was spread on histamine -forming bacterium isolation agar (HBI agar) fortified with L-histidine (Niven, Jeffreg, & Corlett, 1981). Following incubation of the differential agar plates for 4d at 35 C, colonies with blue or purple color on the plates were picked and further streaked on trypticase soy agar (TSA) (Difco) to obtain pure cultures. Their ability to produce biogenic amines was determined by inoculating the isolates in trypticase soy broth (TSB) (Difco) supplemented with 1% L-histidine (TSBH) and incubated without shaking at 35 C for 24 h. Two milliliters of the culture broth were taken for quantitation of biogenic amines. Analyses of total coliform and E. coli in these fillet samples were conducted using the three tube most probable number (MPN) methods (FDA, 1992). Lauryl sulphate tryptose broth (LST broth) and brilliant green lactose bile (2%) broth (BGLB broth) were used for presumptive and confirmed tests for total coliform, respectively. E. coli was determined by using the LST broth and EC broth. Cultures that showed positive production of gas were then confirmed by eosine methylene blue agar (EMBA) and IMViC test. 2.3. Determination of total volatile basic nitrogen (TVBN) The TVBN content of each fillet sample was measured by the method of Conways dish (Cobb, Aoaniz, & Thompson, 1973). The TVBN extract of fillet sample in 6% trichloroacetic acid (TCA, Sigma, St. Louis, MO, USA) was absorbed by boric acid and then titrated with 0.02 N HCl. The TVBN content was calculated and expressed in mg/100 g sample. 2.4. Identification of histamine -forming isolates The presumptive histamine -forming isolates were identified on the basis of morphology, gram stain, endospore stain, catalase and oxidase reaction. The identity of histamine -

forming isolates was further confirmed by amplifying and sequencing approximately 1400 bp of the 16S ribosomal DNA (rDNA) for bacteria ( [Kuhnert et al., 1996] and [Kuhnert et al., 2000] ). Amplification of histamine -forming bacteria was performed using the universal primers UNI-L (5-AGAGTTTGATCATGGCTCAG-3) and UNI-R (5GTGTGACGGGCGGTGTGTAC-3) ( [Kuhnert et al., 1996] and [Kuhnert et al., 2000] ). Bacterial cells were cultured overnight in 2 ml of TSB at 35 C and then centrifuged at 8000 rpm for 10 min. The cell pellet was washed and resuspended in 0.5 ml of TE-buffer (10 mM TrisHCl, 1 mM EDTA; pH 8.0), and then lysed by 20% sodium dodecyl sulfate (SDS). After the solution was boiled for 20 min and the cellular debris was discarded following centrifugation at 13 000g for 3 min, the total DNA in the supernatant was precipitated with 70% ethanol and used as template DNA for PCR. PCR amplification was performed in 20 l reaction mixture containing 10 mM TrisHCl (pH 8.3), 50 mM KCl, 1.5 mM MgCl2, 20 pmol of each primer, a 0.2 mM concentration for each of the four deoxynucleotide triphosphates, 0.5 U of Taq DNA polymerase (Applied Biosystems, Foster City, CA, USA), and template DNA (10 ng). Amplifications were carried out for 35 cycles (94 C for 30 s, 55 C for 30 s, and 72 C for 60 s) in a GeneAmp PCR 2400 Thermal Cycler (Applied Biosystems) with an initial denaturation at 94 C for 4 min and a final extension at 72 C for 7 min ( [Kuhnert et al., 1996] and [Kuhnert et al., 2000] ). Amplicons were detected by electrophoresis on a 1.5% agarose gel staining with ethidium bromide. Amplicons were purified using a QIAquick PCR Purification Kit (Qiagen, Valencia, CA, USA) eluted in TrisHCl (10 mM, pH 8.5) prior to sequencing. The amplified DNA was directly sequenced with the ABI TaqDye Deoxy Terminator Cycle sequencing kit and ABI Model 377 automated DNA sequencer (Applied Biosystems). The sequences were analyzed with the BLAST (NCBI) for identification of histamine -forming bacteria. 2.5. Biogenic amine analysis Each fillet sample was ground in a Waring Blender for 3 min. The ground samples (5 g) were transferred to 50 ml centrifuge tubes and homogenized with 20 ml of 6% trichloroacetic acid (TCA) for 3 min. The homogenates were centrifuged (10 000g, 10 min, 4 C) and filtered through 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 2 ml aliquots of the fillet extracts were derivatized with benzoyl chloride according to the previously described method (Hwang et al., 1997). Two milliliters of each bacterial culture broth were also benzoylated using the same procedures for fillet extracts. The benzoyl derivatives were dissolved in 1 ml of methanol, and 20 l aliquots were used for HPLC injection. The contents of biogenic amines in the fillet samples were determined with a Hitachi liquid chromatograph (Hitachi, Tokyo, Japan) consisting of a Model L-7100 pump, a Rheodyne Model 7125 syringe loading sample injector, a Model L-4000 UVVis detector (set at 254 nm), and a Model D-2500 Chromato-integrator. A LiChrospher 100 RP-18 reversed-phase column (5 m, 125 4.6 mm, E. Merck, Damstadt, Germany) was used for chromatographic separation. The gradient elution program began with 50:50 (v/v) methanol:water at a flow rate of 0.8 ml/min for the first 0.5 min, followed by a linear increase to 85:15 methanol:water (0.8 ml/min) during the next 6.5 min. The methanol:water mix was held constant at 85:15 (0.8 ml/min) for 5 min, and then decreased to 50:50 (0.8 ml/min) during the next 2 min.

3. Results and discussion

Values of the APC, total coliform, E. coli and TVBN in the suspected swordfish fillets responsible for histamine poisoning illness are presented in Table 1. The fillet samples had 5.396.71 log CFU/g of APC. Based on the Taiwanese regulatory standard of 6.47 log CFU/g for APC, 25% (2/8) of the fillet samples were unacceptable. Although, none of these samples contained E. coli, two of the 8 fillet samples (25%) contained 730 and 1360 MPN/g of total coliform, which are more than the 10 MPN/g Taiwan allowable limit (Table 1). The contents of TVBN in all fillet samples were below the Taiwanese regulatory level of 25 mg/100 g (Table 1). Table 1. Values of the aerobic plate count (APC), total coliform (TC), E. coli, and total volatile basic nitrogen (TVBN) in the swordfish fillets implicated in food poisoning Sample no. APC (log CFU/g) TC (MPN/g) E. coli (MPN/g) TVBN (mg/100 g) 1 5.56 <3 <3 9.24 2 3 4 5 6 7 8 5.39 6.71 6.41 5.58 5.45 6.66 6.42 <3 1360 <3 <3 <3 730 <3 <3 <3 <3 <3 <3 <3 <3 6.44 14.56 11.76 8.96 10.36 6.72 10.08

The levels of biogenic amines in the suspected swordfish fillets responsible for histamine poisoning illness are summarized in Table 2. The histamine contents of the swordfish fillet samples ranged from 85.9 to 293.7 mg/100 g. These eight swordfish fillet samples contained less than 12 mg/100 g of the other biogenic amines. The US Food and Drug Administration (FDA) has established a hazard action level of 50 mg histamine /100 g (500 ppm) for tuna fish based on data collected from numerous outbreaks (Taylor, 1989). Bartholomev, Berry, Rodhouse, and Gilhouse (1987) demonstrated that histamine at greater than 100 mg/100 g in fish would be toxic and unsafe for consumption. Thus, the high level of histamine in all swordfish fillet samples along with the allergy-like symptoms developed in the victims supported the conclusion that histamine was the causative agent of this food borne poisoning incident. Table 2. The levels of biogenic amines in the swordfish fillets implicated in food poisoning Sample no. Levels of biogenic amine (mg/100 g) Puta Cad Try Phe Spd Spm His 1 2 3 4 5 6 7
b

Tyr Agm

ND 6.6 7.8 ND ND ND 202.5 0.3 ND ND 11.9 ND ND ND ND 193.1 ND ND 1.2 10.6 ND ND ND 7.2 1.6 5.7 ND ND ND 4.9 293.7 1.9 ND 269.5 4.3 ND

ND 8.0 1.4 ND ND ND 189.2 ND ND 2.1 4.8 ND ND ND ND 157.0 ND ND 1.9 2.7 ND ND ND ND 85.9 ND ND

Sample no. Levels of biogenic amine (mg/100 g) Puta Cad Try Phe Spd Spm His 8
a

Tyr Agm

ND 1.3 ND ND ND 0.8 124.0 1.2 ND Put, putrescine; Cad, cadaverine; Try, tryptamine; Phe, 2-phenylethylamine; Spd, spermidine; Spm, spermine; His, histamine ; Tyr, tyramine; and Agm, agmatine. b ND, not detected (amine level less than 0.1 mg/100 g). Various types of fish implicated in scombroid poisoning have been found to contain high levels of histamine . The histamine content of marlin implicated in a poisoning incident ranged between 93.5 and 276 mg/100 g (Morrow, Margolies, Rowland, & Robert, 1991). The hot-smoked mackerel implicated in a scombrotoxic incident had a histamine content of 270 mg/100 g (Clifford, Walker, & Wright, 1989). The histamine content of canned tuna implicated in a poisoning was 116 mg/100 g, while that of wholesome canned tuna was only 2.74 mg/100 g (Kim & Bjeldanes, 1979). In Taiwan, scombroid poisoning only occurred occasionally ( [Chen and Malison, 1987] , [Murray and Hobbs, 1982] and [Tsai et al., 2005] ), and the fish implicated in those occasional outbreaks are tuna, mackerel, and black marlin. Recently, sailfish and marlin fillets have become the most frequently implicated fish species in scombroid outbreaks in Taiwan ( [Hwang et al., 1995] , [Hwang et al., 1997] and [Hwang et al., 1999] ). Quality loss and histamine accumulation often occur after frozen fish of the above mentioned species are thawed and kept for long periods of time at room temperature before further processing. Since histamine is heat resistant, it can remain intact in canned or cooked fish products (Lopez-Sabater, Rodriguez-Jerez, Roig-Sagues, & Mora-Ventura, 1994). In this study, the use of poor quality fish as raw material for cooking results in the presence of toxic levels of histamine in the swordfish fillets. The suspected swordfish fillets produced 27 purple colonies on the differential HBI agar plates. Only 10 of them (37.0%) produced histamine in TSBH medium. The remaining 17 isolates were false-positive histamine -formers. Lopez-Sabater et al. (1996) also found that 63.1% of the presumptive histamine -producers that they isolated from Nivens medium were actually false-positives when grown in a histidine-supplemented culture broth. Thus, our results confirm the previous observations that Nivens medium may yield false-positive isolates of histamine -producers, because other alkaline products of bacterial origin can also cause color changes of the colonies on the agar plates ( [Ababouch et al., 1991] , [Tsai et al., 2004] and [Tsai, Lin et al., 2005] ). Table 3 listed the identity of these ten histamine -forming bacteria as determined by 16S rDNA sequences, following comparison to reference strains, using NCBI database analysis. The PCR amplicons from strains F1-1 and F2-2 had a 100% homology with Staphylococcus sp. and S. aureus, respectively, while those from strains F3-1, F3-2, F4-2, F4-3, F5-2 and F62 aligned with S. aureus subsp. aureus at 100%. The PCR amplicons from strains F7-3 had a 100% homology with S. aureus subsp. aureus, whereas those from strain F8-1 had a homology with S. aureus at 100% (Table 3). These ten histamine -forming isolates as Staphylococcus sp. (one strain), S. aureus (two strains) and S. aureus subsp. aureus (seven strains) by 16S rDNA sequencing produced substantial amounts of histamine (12.733.0 ppm) in TSBH medium. Some of them also produced different amounts of cadaverine, 2phenylethylamine and tyramine (Table 3). However, these isolates produced small amounts of histamine in culture broth, indicating that they are not the main contributors to histamine accumulation in the suspected swordfish fillets. It was possible that the major

histamine -forming bacteria that contributed to the higher levels of histamine in the suspected swordfish fillet were killed or inhibited during thawing or re-freezing process and storage condition, or could not grow on the HBI agar or TSBH medium that were used. Table 3. Identification of histamine -forming bacteria isolated from the swordfish fillets implicated in food poisoning by 16S rDNA, basing on the output results from NCBI database analysis, and their production of histamine and other biogenic amines (ppm) in culture broth Strain Organism Percentage Gene bank accession Hisa Cad 2Tyr identified identity (%) number Phe F1-1 Staphylococcus sp. 100 AY940424.1 21.4 NDb ND ND F2-2 F3-1 F3-2 F4-2 F4-3 F5-2 F6-2 F7-3 S. aureus S. aureus subsp. aureus S. aureus subsp. aureus S. aureus subsp. aureus S. aureus subsp. aureus S. aureus subsp. aureus S. aureus subsp. aureus S. aureus subsp. aureus 100 100 100 100 100 100 100 100 BX571857.1 CP000046.1 CP000046.1 CP000046.1 CP000046.1 CP000046.1 CP000046.1 L37599.1 22.6 1.9 4.1 12.7 ND ND 20.5 ND ND 13.5 1.4 ND 22.0 1.6 ND 33.0 2.0 ND 22.7 2.2 4.8 20.4 1.8 3.4 ND 6.9 8.9 6.9 11.7 ND 8.2 8.3 7.5

F8-1 S. aureus 100 BX571857.1 19.3 ND ND a His, histamine , Cad, cadaverine, 2-Phe, 2-Phenylethylamine, Tyr, tyramine. b ND, not detected (amine level less than 1 ppm).

Staphylococcus spp. were the most frequently reported histamine -formers in fermented salted fish, accounting for nearly 50% of histamine -forming microorganisms. They were usually shown to have powerful histamine -forming activity ( [Yatsunami and Echigo, 1991] and [Yatsunami and Echigo, 1992] ). For example, S. epidermidis and S. capitis isolated from salted Spanish anchovies produced more than 1000 ppm and 400 ppm of histamine , respectively (Hernandez-Herrero, Roig-Sagues, Rodriguez-Jerez, & Mora-Ventura, 1999). The S. capitis recently isolated from mustard pickle products in Taiwan was a potent histamine -former capable of producing more than 1000 ppm of histamine (Kung et al., 2006). However, the recently isolated S. pasteuri from miso and natto products in Taiwan were identified as weak histamine -forming bacteria ( [Kung et al., 2007] and [35] ). Similarly, all of the histamine -forming bacteria strains as Staphylococcus spp. that were isolated in this study were also weak histamine -formers and produced only between 12.7 ppm and 33.0 ppm of histamine in TSBH (Table 3). Since Staphylococci are one of the major microbial groups inhabiting human skin, it is reasonable to expect that they would be found as part of the microflora of food products, which require considerable human contact during preparation and processing. In addition, S. aureus is the most important food pathogen

among the staphylococci (Jay, 1986). Based on the finding that S. aureus was isolated from the suspected swordfish fillets implicated food poisoning, we postulate that the swordfish had been seriously contaminated during capture and subsequent unhygienic handling.

4. Conclusion
This study showed that two of eight suspected swordfish fillets (25%) had APC and total coliform levels greater than Taiwanese regulatory limit of 6.47 log CFU/g and 10 MPN/g, respectively. Based on the finding that high contents of histamine (>85 mg/100 g) were detected in the suspected fillet samples, we believe the use of poor quality raw fish for cooking contributed to the presence of high histamine levels in swordfish fillets and resulting in food borne poisoning. Staphylococcus sp. (one strain), S. aureus (two strains) and S. aureus subsp. aureus (seven strains) were the ten weak histamine formers isolated from these fillet samples.

Acknowledgement
The study was partly supported by the National Science Council, ROC. (Contract No. NSC 95-2313-B-022-005).

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