Biogenic amines formation in high-pressure processed pike flesh (Esox lucius) during storage

Food Chemistry 151 (2014) 466–471

Contents lists available at ScienceDirect

Food Chemistry

journal homepage: www.elsevier .com/locate / foodchem

Biogenic amines formation in high-pressure processed pike flesh(Esox lucius) during storage

0308-8146/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.foodchem.2013.11.094

⇑ Corresponding author. Tel.: +420 387 772 655; fax: +420 385 310 405.E-mail address: [email protected] (M. Krízek).

Martin Krízek a,⇑, Katerina Matejková a, František Vácha b, Eva Dadáková a

a Faculty of Agriculture, Department of Applied Chemistry, University of South Bohemia, Branišovská 31a, 370 05 Ceské Budejovice, Czech Republicb Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Institute of Aquaculture, University ofSouth Bohemia, Husova 458/102, 370 05 Ceské Budejovice, Czech Republic

a r t i c l e i n f o

Article history:Received 31 July 2013Received in revised form 31 October 2013Accepted 18 November 2013Available online 27 November 2013

Keywords:Biogenic aminesPolyaminesPutrescineHistaminePikeFishHigh pressure processingHigh hydrostatic pressureHHPQuality changes

a b s t r a c t

The effects of vacuum packaging followed by high pressure processing on the shelf-life of fillets of pike(Esox lucius) were examined. Samples were pressure-treated at 300 and 500 MPa and stored at 3.5 and12 �C for up to 70 days. The content of eight biogenic amines (putrescine, cadaverine, spermidine, sperm-ine, histamine, tyramine, tryptamine and phenylethylamine) were determined. Putrescine showed verygood correspondence with the level of applied pressure and organoleptic properties. Polyamines spermi-dine and spermine did not show statistically significant changes with the level of applied pressure andthe time of storage. Increased cadaverine and tyramine contents were found in samples with good sen-sory signs, stored for longer time and/or kept at 12 �C, thus indicating the loss of freshness. Tryptamineand phenylethylamine were not detected in pressure-treated samples kept at 3.5 �C. Histamine was notdetected in samples of good quality.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

The increasing demands on the quality of foodstuffs required byconsumers, and the need for longer shelf-life periods, have lead tothe introduction of new preservation techniques. In high pressureprocessing, foods are subjected to pressures between 100 and1000 MPa – usually for several minutes. The process is capable ofinactivating microorganisms and enzymes to effectively pasteurisefoods with minimal heating while retaining most of their sensorycharacteristics and nutritional value for an extended shelf-life.When high hydrostatic pressures are applied to packages of foodsubmerged in a liquid, the pressure is distributed uniformlythroughout the food, so that all parts receive the same treatment.

Biogenic amines (BAs) – putrescine (PUT), cadaverine (CAD),spermidine (SPD), spermine (SPM), histamine (HIM), tyramine(TYM), tryptamine (TRM) and phenylethylamine (PEA) are basicnitrogenous compounds formed mainly by decarboxylation ofamino acids. In foods BAs are primarily produced by microbialdecarboxylation of amino acids or by enzymes present in the rawmaterial (Karovicova & Kohajdova, 2005). Aromatic amines, HIM

and TYM, are vasoactive. The effects of TYM on healthy individualsare usually limited to headaches or migraines (Til, Falke, Prinsen, &Willems, 1997). HIM is associated with ‘‘scombroid poisoning’’nausea, hypotension, flushing, urticaria (Stratton, Hutkins, &Taylor, 1991). Enzymes that destroy aromatic amines in the digestivetract can be inhibited by medications (antidepressants, tuberculo-statics, mucolytics) (Prester, 2011) or by coincident ingestion ofPUT and CAD (Joosten, 1988). The toxic levels of aromatic aminesare uncertain. HIM levels above 500–1000 mg/kg and TYM levelsabove 100–800 mg/kg are considered potentially dangerous tohuman health (Brink, Damink, Joosten, & Huis int Veld, 1990). Oraltoxicity levels for PUT and CAD have been a subject of discussion.Nevertheless, no tolerable levels in foods have been establishedso far. A large study of the dietary exposure assessment of poly-amines determined the tolerable level of CAD in fish as 510 mg/kg (Rauscher-Gabernig et al., 2012). People having deficient naturalmechanisms for detoxifying BAs resulting from genetic cause orthrough inhibition due to the intake of antidepression medicinesare more susceptible to BA poisoning (Prester, 2011).

HIM, TYM, PUT and CAD are significant both in the safety and inthe quality determination of fish as a human food. These four BAswere used as indicators of the spoilage of sardines (Gokoglu,Yerlikaya, & Cengiz, 2004) or pike-perch (Sander lucioperca) (Ehsani

M. Krízek et al. / Food Chemistry 151 (2014) 466–471 467

& Jasour, 2012). Fresh water species have been studied to a muchsmaller extent compared to marine fish. A large study of marineand fresh water fish species was conducted by Bunka et al.(2013). PUT and TYM were proposed to be good quality evaluationindices for crucian carp (Carassius auratus) (Li, Bao, Luo, Shen, & Shi,2012). For rainbow trout (Oncorhynchus mykiss) PUT, TYM, SPD andSPM were recommended as quality indicators (Chytiri, Paleologos,Savvaidis, & Kontominas, 2004). Other authors recommendusing PUT, CAD and TYM, due to the low content of SPD and SPM(Matejková, Krízek, Vácha, & Dadáková, 2013).

As BAs are formed mainly by the action of bacteria, suppressionof their proliferation is crucial in BAs regulation. Information onthe pressurization of fish or fish products being linked to BAs for-mation is scarce. BAs were determined in samples of smoked cod(Gadus morhua), treated at 400, 500 and 600 MPa (Montiel, DeAlba, Bravo, Gaya, & Medina, 2012). Surprisingly, only TRM andSPM were detected; elevated contents of TRM were found inparticular in high-pressure treated samples. In trout samples(O. mykiss) stored at 3.5 �C, the pressurization to 300 MPa extendedthe shelf life four times to 21–28 days compared to unpressurisedcontrols. Samples of a good quality contained less than 10 mg/kgeach of PUT, CAD and TYM (Matejková et al., 2013). Suppressionof BAs formation can be achieved by eliminating the microorgan-isms. On the other hand sometimes the controlled addition ofselected bacteria is useful. Similarly to preserved vegetable food-stuffs (sauerkraut – fermented shredded cabbage) (Kalac, Špicka,Krízek, & Pelikánová, 2000; Špicka, Kalac, Bover-Cid, & Krízek,2002), experiments with the inoculation of fish flesh with lacticacid bacteria were conducted (Kuley, Ozogul, Ozogul, & Akyol,2011). Contrary to the example of sauerkraut inoculated with lacticacid bacteria, in inoculated fish, the suppression of BAs formationwas not observed.

Pike (E. lucius) belongs to the highly rated freshwater fish. It ispopular for its delicate, non-fat, easily digestible meat ofhigh-nutritional value. Compared with other fish, pike meat islow in energy content. It is marketed in fresh and frozen, wholeand sliced forms of the product. Pike flesh is susceptible to freez-ing, which reduces its quality. Production of pike from fisheryfarms in the Czech Republic is slightly above 100 tons/year. It repre-sents more than half of the production of all predatory fish, producedby fishery farmers in the Czech Republic. This work was undertakento increase the knowledge of the dynamics of BAs formation invacuum-packed fish flesh preserved by less traditional technology.

2. Materials and methods

2.1. Fish samples

2.1.1. Fish productionThe pike samples (E. lucius) were obtained from a fish farm in

Trebon (South Bohemia). In order to ensure the best uniformityof the natural microbial load, all fish were caught in the same fishpond and were treated in the same way. The 45 month old fish ofaverage body mass 3250 g (3190–3350 g) were slaughtered 30 minbefore arrival to the laboratory. The slaughtering method com-bined electrical stunning with cutting off the gill arches, bleedingand decapitation which facilitated further processing. Finally thebody was cut into two halves (fillets). Portions of about 20 g ofmuscles from the chest area served as samples.

2.1.2. Sample packaging and storageSamples were wrapped in PA/PE foil (thickness 80 lm) and

sealed under vacuum, level 10 (99%). This was performed using aprofessional wrapping machine, Speedy 320 (BossVakuum, BadHomburg, Germany). After high-pressure treatment, samples were

placed in two refrigerated boxes with thermostats set at 3.5 �C and12 �C.

2.1.3. High-pressure treatmentPacked samples surrounded with cooling cartridges were

placed in a polystyrene box and transported immediately to theFood Research Institute, Prague. The overall transportation timewas 5 h and the temperature in the box was maintained between0 and 2 �C. The packed samples were HP-treated at 300 and500 MPa for 10 min at 20 �C in a high-pressure processor (CYX 6/0103, made by ZDAS, Zdár n. Sázavou, Czech Republic) using wateras the pressure-transmitting medium. The pressure vessel (diame-ter 90 mm, height 320 mm) had a 2 L capacity and the maximumoperating pressure was 600 MPa. The rate of pressure increasewas 8.3 MPa/s, and the depressurization time was less than 4 s.The control samples were held for 10 min at ambient pressure(0.1 MPa) at 20 �C.

2.1.4. SamplingSamples were analysed in triplicate after 0 (fresh meat), 7, 14,

21, 28, 42 and 70 of storage. The experiments were designed tobe dynamic. Irregular intervals of sampling were chosen due toprevious experience with various food samples. At the onset ofstorage, the changes in contents of amines are hardly predictable.The control samples were not analysed after the 28th day of stor-age due to their poor sensory properties. For the same reason,HP-treated samples kept at 12 �C were not analysed after the42nd day.

2.2. Analytical method

2.2.1. Sample extraction and derivatisationThe samples were homogenised with an Ultra-Turrax T25

homogeniser (Ika Labortechnik, Staufen, Germany). Biogenicamines were extracted from the homogenised material withdiluted perchloric acid, p.a. (0.6 M) (Acros, Geel, Belgium). Afterfiltration, the volume was made up to 150 ml with perchloric acid(0.6 M). The amines were determined as dansyl derivatives afterderivatisation with dansyl chloride by UPLC (column: Agilent Zor-bax Eclipse XDB C18; 50 mm � 4.6 mm ID, 1.8 lm particle size).The procedure has been described in detail by Dadáková, Krízek,and Pelikánová (2009).

2.2.2. ApparatusUPLC analyses were carried out on an Agilent 1200 Series Rapid

Resolution LC System (Agilent Technologies, Inc., Santa Clara, CA,USA). The system was equipped with binary pumps, a micro-vac-uum degasser, a high performance autosampler and a diode arraydetector. Data processing was performed using a ChemStation forLC 3D systems (Agilent Technologies).

2.3. Statistical evaluation

Samples were prepared in triplicate from one batch of fish andeach sample was analysed twice. The statistical parameters werecalculated using Statistica (data analysis software system) v. 9.0,Stat-Soft Inc. (2009).

2.4. Sensory tests

As 10 trained panellists are needed for fully valid evaluation,our sensory results can be understood only as complementary tothe main objective of this study – the determination of chemicalchanges in the flesh – and were simplified to three levels:

good (1): odour: meaty, neutral; appearance: white, tightlyelastic flesh,

468 M. Krízek et al. / Food Chemistry 151 (2014) 466–471

acceptable (2): odour: neutral, slightly spicy; appearance: grey-ish, solid flesh,

poor (3): odour: fishy, repulsive; appearance: grey, muddyflesh.

A sensory panel consisting of three panellists evaluated themeat samples; each panellist tested all samples twice.

3. Results and discussion

Samples of pike flesh were analysed in triplicate. The initial con-tents of BAs in fresh meat of pike (day 0) were: PUT:0.42 ± 0.36 mg/kg, SPD: 0.88 ± 0.78 mg/kg, SPM: 1.21 ± 0.16 mg/kg, CAD, HIM, TYM, TRM, PEA: ND. The mean amine contents forcontrol and pressure-treated samples at both temperatures aregiven in Tables 1–3.

The level of applied pressure, the temperature and time ofstorage had a decisive influence on the status of samples. The firstsensory signs of deterioration of the control samples (3.5 �C) wererecorded after 14 days of storage (sensory score 2). Samples pres-surised to 300 MPa showed a similar score after 28 days and sam-ples pressurised to 500 MPa after 70 days. At a temperature of12 �C control samples showed the same status of decreased quality(2) already at the first sampling in the 7th day, samples pressurisedto 300 MPa in the 14th day and samples pressurised to 500 MPa inthe 28th day of storage (Table 4). These data reveal the evidentlypositive influence of both reduced temperature and the applicationof high pressure. At 3.5 �C the application of 300 MPa extended theshelf life period from 7 to 21 days (sensory 1), application of500 MPa even as long as 42 days. At 12 �C the positive influenceof high pressure was not so significant. Pressurisation to 300 and500 MPa kept the sample at good quality (sensory 1) only for 7and 21 days respectively.

3.1. Putrescine, cadaverine and tyramine

Despite the different chemical structure of TYM, the dynamicsof its formation are similar to PUT and CAD. Concentration increaseof PUT, CAD and TYM corresponds with the deepening decay ofsamples (Tables 1 and 2). The effects of high pressure and temper-ature levels on the dynamics of PUT, CAD and TYM formation areclearly evident. These trends are in good accordance with sensoryparameters (Table 4). In carp flesh (Cyprinus carpio), contents ofPUT at <10 mg/kg were typical for samples of good quality, PUTcontents of 10–20 mg/kg were related to the onset of spoilage,and values exceeding 20 mg/kg were usually found in samples of

Table 1Content of putrescine and cadaverine (mg/kg) in meat of pike (mean ± SD; n = 3) processe

Pressure (MPa) Storage time (days)

7 14 21

Putrescine0 (T1) 0.67 ± 1.16A 7.52 ± 1.97Ba 17.5 ± 4.6300 (T1) ND ND 9.51 ± 6.3500 (T1) ND 1.04 ± 1.79Ab 3.55 ± 3.00 (T2) 22.9 ± 11.0Aa 99.9 ± 19.2Ba 272 ± 22300 (T2) 0.94 ± 1.63Ab 13.5 ± 2.85Bb 32.8 ± 11500 (T2) ND 13.2 ± 5.19Ab 29.3 ± 3.3

Cadaverine0 (T1) ND 6.13 ± 2.29Aa 15.5 ± 3.5300 (T1) ND 2.03 ± 1.77Aa 19.1 ± 4.3500 (T1) ND ND 32.3 ± 190 (T2) 30.3 ± 8.00Aa 118 ± 11.0Ba 158 ± 20300 (T2) 14.1 ± 9.20Aab 21.5 ± 0.66Ab 57.4 ± 26500 (T2) 4.24 ± 1.29Ab 63.4 ± 6.16Bc 78.9 ± 6.2

ND: not detected; means indicated by different capital letters in the same row differ sigMeans indicated by different lowercase letters in the same column differ significantly (

inferior quality (Krízek, Pavlícek, & Vácha, 2002). CAD is formedfrom lysine by the action of bacterial decarboxylases. Unlike PUT,CAD is not a common constituent of cellular tissue (Li et al.,2012). Most likely it was for this reason that it was not detectedeither in fresh pike meat or in stored samples at 3.5 �C (7th day).Similarly to PUT, the CAD contents exceeding 20 mg/kg indicatedthe advanced state of decomposition. The build-up of CAD ingeneral was similar to that of PUT and TYM. The overall trends information of these three BAs were similar to those in carp flesh(Shi, Cui, Lu, Shen, & Luo, 2012). The contents of TYM < 10 mg/kgwere typical for samples of good quality. Good quality of sampleswas seldom observed where higher levels of TYM were recorded.

3.1.1. PutrescineThe formation of PUT corresponded very well with the organo-

leptic properties. Especially at 3.5 �C the positive effect of highpressure is clearly visible. The increasing level of pressurizationmade itself felt in suppressed PUT contents mainly at the begin-ning of storage, approximately up to the 28th day. Subsequentlythe differences between the effect of 300 and 500 MPa were minor.Control samples kept at 12 �C showed elevated PUT contents evenin the first sampling profile (7th day). These samples perished fromthe very start of storage and in spite of their vacuum-packing thedynamics of their decay was very fast. At this temperature the con-tents of PUT in samples pressurised to 300 and 500 MPa did notdiffer substantially. At 12 �C pressurization extended the shelf lifeto 14 days regardless of the level of high pressure applied. There isno telling whether elevated PUT contents precede the worsening ofsensory indices. Increasing PUT concentrations rather follows thedecrease of the sensory quality of the flesh. For these reasonsPUT contents can hardly be used for the prediction of qualitychanges in pike flesh. Generally, samples treated with high pres-sure contained comparable PUT contents regardless of the levelof high pressure applied.

3.1.2. CadaverineThe absence of CAD is typical for samples of very good quality

(Li et al., 2012). CAD was not detected in any sample kept at3.5 �C to the 7th day. Similarly to PUT, the most intensive increasewas observed in control samples especially at 12 �C. Unlike PUT,elevated contents of CAD (>20 mg/kg) were also found in pressur-ised samples at both temperatures in spite of good sensory proper-ties. This is probably related to the type of substrate. In sausagesthe pressurization inhibited CAD formation, while promptingTYM formation (Simon-Sarkadi, Pasztor-Huszar, Istvan, & Kisko,

d under high pressure at T1 = 35 �C and T2 = 12 �C.

28 42 70

6Ba 28.3 ± 10.7Ba – –1Aab 12.6 ± 3.12ABab 16.3 ± 7.18ABa 23.8 ± 1.67Ba

8Ab 6.04 ± 3.63Ab 17.4 ± 2.20Ba 31.2 ± 3.50Cb

.6Ca 258 ± 91.4BCa – –

.0BCb 21.5 ± 2.82Cb 50.6 ± 4.12Da –5Bb 33.1 ± 8.30Bb 62.0 ± 14.9Ca –

0Ba 30.6 ± 2.23Ca – –9Ba 18.5 ± 12.5ABCa 20.7 ± 8.72Ba 42.6 ± 6.09Ca

.0Aa 39.9 ± 6.45Aa 76.4 ± 6.50Bb 113 ± 11.0Cb

.9Ba 216 ± 62.2Ba – –

.0ABb 58.7 ± 10.3Bb 110 ± 23.3Ca –4Cb 105 ± 15.8Ca 231 ± 50.3Db –

nificantly (P < 0.05).P < 0.05).

Table 2Content of histamine and tyramine (mg/kg) in meat of pike (mean ± SD; n = 3) processed under high pressure at T1 = 35 �C and T2 = 12 �C.

Pressure (MPa) Storage time (days)

7 14 21 28 42 70

Histamine0 (T1) ND ND ND ND – –300 (T1) ND ND ND ND ND ND500 (T1) ND ND ND ND ND ND0 (T2) ND 10.4 ± 2.51A 14.6 ± 2.40Aa 15.9 ± 7.29Aa – –300 (T2) ND ND 1.73 ± 3.00Ab 2.61 ± 4.59Aa ND –500 (T2) ND ND ND 8.44 ± 7.41Aa 13.4 ± 11.8A –

Tyramine0 (T1) 0.43 ± 0.75Aa 12.3 ± 2.25Ba 41.6 ± 6.61Ca 104 ± 33.1Ca – –300 (T1) 0.22 ± 0.39Aa 18.7 ± 1.92Bb 34.6 ± 9.10Ba 55.8 ± 10.1Ca 91.2 ± 28.4Ca 81.1 ± 11.9Ca

500 (T1) ND ND 11.8 ± 5.00Ab 31.7 ± 2.92Bb 40.8 ± 19.4ABa 82.1 ± 14.9Ca

0 (T2) 31.8 ± 11.7Aa 184 ± 15.1Ba 411 ± 50.6Ca 468 ± 131BCa – –300 (T2) 9.99 ± 4.64Aa 51.5 ± 12.4Bb 131 ± 58.2ABCb 123 ± 19.4Cb 372 ± 50.1Da –500 (T2) ND 20.1 ± 5.19Ac 110 ± 16.9Bb 173 ± 56.2Bb 212 ± 54.9Bb –

ND: not detected; means indicated by different capital letters in the same row differ significantly (P < 0.05).Means indicated by different lowercase letters in the same column differ significantly (P < 0.05).

M. Krízek et al. / Food Chemistry 151 (2014) 466–471 469

2012). In our samples CAD formation was prompted, while TYMwas suppressed. It is worth noting, that at 3.5 �C the differencesof CAD contents for the control and pressurised samples werestatistically insignificant up to the 28th day of storage. However,the content of CAD steadily increased with the storage time. At12 �C the increase was most marked in the control samples. Highcontents of CAD, contrasted to a very good sensory score in the14th and 21st day (12 �C, 500 MPa), are surprising. Samples pres-surised to 500 MPa contained usually more CAD compared to thosetreated with 300 MPa. The reason for this is not clear. Higher levelsof pressurization may well lead to changes in the inner structure offlesh, resulting in the more extensive liberation of substratenecessary for CAD formation. The increased contents of CAD mightindicate that the flesh was not fresh and/or it had been stored at aninappropriate temperature.

3.1.3. TyramineSamples of good quality usually contained less than 10 mg/kg of

TYM. Unlike CAD, TYM formation at 3.5 �C was more suppressed bythe application of higher levels of pressurization. The course ofTYM formation was similar to that of PUT and especially of CAD.Similarly to CAD, TYM showed a concentration increase over timein spite of persisting good sensory properties (e.g. 3.5 �C, 300 and500 MPa). The effect of an elevated temperature was similar tothe effect of storage time. For example the TYM content is ten

Table 3Content of spermidine and spermine (mg/kg) in meat of pike (mean ± SD; n = 3) processed

Pressure (MPa) Storage time (days)

7 14 21

Spermidine0 (T1) 2.64 ± 0.31a ND ND300 (T1) 1.60 ± 0.38b ND ND500 (T1) 1.19 ± 0.15Ab 2.54 ± 0.95A 0.73 ± 10 (T2) 0.76 ± 0.66a ND ND300 (T2) ND 0.62 ± 1.07a ND500 (T2) 1.11 ± 1.10Aa 1.47 ± 1.48Aa ND

Spermine0 (T1) 1.82 ± 0.13Aa 1.68 ± 0.20Aa 0.40 ± 0300 (T1) 1.36 ± 0.19Ab 1.39 ± 1.32Aa ND500 (T1) 1.31 ± 0.18ABb 2.36 ± 0.44Ca 0.50 ± 00 (T2) 1.85 ± 0.37Aa 1.16 ± 1.06Aa ND300 (T2) ND 1.29 ± 1.12a ND500 (T2) 1.44 ± 0.13Aa 1.53 ± 0.09Aa ND

ND: not detected; means indicated by different capital letters in the same row differ sigMeans indicated by different lowercase letters in the same column differ significantly (

times higher at 12 �C compared to that at 3.5 �C (500 MPa, 21stday), but the sensory score is the same (1) (Tables 2 and 4).Increased contents of TYM, similarly to CAD, may indicate the lossof meat freshness or temperature abuse in spite of persisting goodsensory signs (Hernandez-Jover, Izquierdo-Pulido, Veciana-Nogues, & Vidal-Carou, 1996; Ruiz-Capillas, Carballo, & Colmenero,2007). These phenomena were also observed in pressurisedsausage and may be explained by continuing decarboxylaseactivity in the substrate during storage (Ruiz-Capillas, Colmenero,Carrascosa, & Munoz, 2007).

TYM is toxicologically important substance. In samples of troutflesh (O. mykiss) with sensory score 1, the contents of TYM did notexceed 13 mg/kg (Matejková et al., 2013). The situation in pikeflesh is somewhat different. Contents of TYM in samples with thesame sensory score (1) gradually increased up to 40.8 mg/kg(3 �C, 500 MPa) or up to 110 mg/kg (12 �C, 500 MPa). The TYM con-tent exceeding 100 mg/kg cannot be underestimated.

3.2. Spermidine and spermine

Low concentrations of SPD and SPM were found in fresh pikemeat (day 0) and in most of the samples on the 7th and 14th dayof storage. Similarly to PUT, SPD and SPM are polyamines naturallyoccurring in all cells (Halasz, Barath, Simon-Sarkadi, & Holzapfel,1994). Unlike trout flesh, where SPD and SPM contents showed

under high pressure at T1 = 35 �C and T2 = 12 �C.

28 42 70

ND – –ND ND ND

.26A ND 0.48 ± 0.83A 0.55 ± 0.96A

ND – –ND ND –ND ND –

.68Aa ND – –ND ND 0.47 ± 0.81Aa

.86ABa 0.33 ± 0.57A 0.49 ± 0.85AB 1.84 ± 0.27BCa

ND – –ND ND –ND ND –

nificantly (P < 0.05).P < 0.05).

Table 4Sensory score of samples (1 is the best).

Pressure (MPa) Storage time (days)

7 14 21 28 42 70

0 (T1) 1 2 2 3 – –300 (T1) 1 1 1 2 3 3500 (T1) 1 1 1 1 1 20 (T2) 2 3 3 3 – –300 (T2) 1.5 2 2 2.5 3 –500 (T2) 1 1 1 2 3 –

470 M. Krízek et al. / Food Chemistry 151 (2014) 466–471

minimal fluctuations with no time-trend, in pike flesh bothpolyamines were found mostly at the beginning of storage. Theircontents did not show statistically significant trends over time,but with time they disappeared from most of the samples (Table 3).Due to the limited number of values, it is not possible to make aclear conclusion regarding the influence of high pressure. The ab-sence of both polyamines in samples stored for a longer time mightbe in accordance with the results of other authors, who describedthe decrease of SPD and SPM concentrations over time (Paleologos,Savvaidis, & Kontominas, 2004). With respect to the low concen-trations of polyamines and their insignificant concentrationchanges in pike flesh, the practical importance of their assessmentis little.

3.3. Histamine, tryptamine and phenylethylamine

Histamine can be produced by bacterial decarboxylases inscombroid and other fish that have relatively high free histidinelevels in their muscles (Lehane & Olley, 2000). There are no dataavailable on free histidine content in pike flesh. Histamine wasnot found in any sample of pike flesh stored at 3.5 �C. The contentsof HIM in samples kept at 12 �C were low (<20 mg/kg), not only inthe samples with a good sensory score, but also in the worst(Table 2). The overall sensory status of samples kept at lower tem-perature was better in general, compared to those kept at highertemperature, so this might be the reason for the absence of thoseamines which are typical for deep decay. Compared to trout fleshthe results are similar (Matejková et al., 2013), but contents ofHIM are even lower. HIM does not appear to be a substance thatwould adequately signal or predict the beginning of the degrada-tion processes. In any case, the toxicologically important concen-tration of HIM (>100 mg/kg) (Hungerford, 2010) was not reached,even in samples of inferior quality, so this amine in pike flesh doesnot represent a similar risk for consumers as it does in the case ofscombroid fish. Tryptamine was not found in any sample. Phenyl-ethylamine was found only in two samples (Control, 12 �C) 21stday: 9.40 mg/kg and 28th day: 8.01 mg/kg. Both these sampleswere of inferior quality (sensory score 3).

4. Conclusions

The application of high hydrostatic pressure can noticeablyreduce the contents of BAs in vacuum-packed pike meat. HIM,the amine of greatest toxicological importance does not representa risk for consumers of pike flesh. HIM was not detected in samplesof good quality. On the other hand, the TYM contents steadilyincreased in samples, even in those with the best sensory score.Samples pressurised at 500 MPa with sensory score 1 reached40.8 and 110 mg/kg of TYM (in samples kept at 3.5 and 12 �Crespectively). When extending the shelf life of pike flesh bypressurization, the increase of TYM contents should be takeninto consideration. Increased TYM and CAD contents werefound in samples stored for a longer time and/or kept at higher

temperatures. TYM, similarly to CAD, may indicate the loss of meatfreshness or temperature abuse in spite of persisting good sensorysigns. Unlike TYM and CAD, PUT rather followed the decrease ofthe sensory quality of flesh. For this reason PUT contents can beless suitable for the prediction of quality changes in pike flesh.The recommended storage time limit for vacuum-packaged pikemeat, specified by producers, is about 5 days at a temperatureof 3.5 �C. The application of high hydrostatic pressure cansubstantially extend this period – by approximately four times(300 MPa) and eight times (500 MPa), to 21 or 42 days respec-tively. High hydrostatic pressure treatment was much less effectiveat 12 �C. Moreover at this temperature the increased formation ofTYM is likely to occur, even in samples with good sensoryproperties.

Acknowledgements

The authors acknowledge the financial support of the projectsP503/11/1417 of the Czech Science Foundation GACR and GAJU058/2013/Z. The study was also supported by the South BohemianResearch Center of Aquaculture and Biodiversity of Hydrocenoses,Grant No. CENAKVA CZ.1.05/2.1.00/01.0024.

References

Brink, B., Damink, C., Joosten, H. M. L. J., & Huis int Veld, J. H. J. (1990). Occurrenceand formation of biologically active amines in foods. International Journal ofFood Microbiology, 11(1), 73–84.

Bunka, F., Budinsky, P., Zimakova, B., Merhaut, M., Flasarova, R., Pachlova, V., et al.(2013). Biogenic amines occurrence in fish meat sampled from restaurants inregion of Czech Republic. Food Control, 31(1), 49–52.

Chytiri, S., Paleologos, E., Savvaidis, I., & Kontominas, M. G. (2004). Relation ofbiogenic amines with microbial and sensory changes of whole and filletedfreshwater rainbow trout (Onchorynchus mykiss) stored on ice. Journal of FoodProtection, 67(5), 960–965.

Dadáková, E., Krízek, M., & Pelikánová, T. (2009). Determination of biogenic aminesin foods using ultra-performance liquid chromatography (UPLC). FoodChemistry, 116(1), 365–370.

Ehsani, A., & Jasour, M. S. (2012). Microbiological properties and biogenic amines ofwhole Pike-Perch (Sander lucioperca, Linnaeus 1758): A perspective on fishsafety during postharvest handling practices and frozen storage. Journal of FoodScience, 77(12), M664–M668.

Gokoglu, N., Yerlikaya, P., & Cengiz, E. (2004). Changes in biogenic amine contentsand sensory quality of sardine (Sardina pilchardus) stored at 4 �C and 20 �C.Journal of Food Quality, 27(3), 221–231.

Halasz, A., Barath, A., Simon-Sarkadi, L., & Holzapfel, W. (1994). Biogenic amines andtheir production by microorganisms in foods. Trends in Food Science &Technology, 5(2), 42–49.

Hernandez-Jover, T., Izquierdo-Pulido, M., Veciana-Nogues, M. T., & Vidal-Carou, M.C. (1996). Biogenic amine sources in cooked cured shoulder pork. Journal ofAgricultural and Food Chemistry, 44(10), 3097–3101.

Hungerford, J. M. (2010). Scombroid poisoning: A review. Toxicon, 56(2), 231–243.Joosten, H. M. L. J. (1988). The biogenic amine contents of Dutch cheese and their

toxicological significance. Netherlands Milk and Dairy Journal, 42(1), 25–42.Kalac, P., Špicka, J., Krízek, M., & Pelikánová, T. (2000). Changes in biogenic amine

concentrations during sauerkraut storage. Food Chemistry, 69(3), 309–314.Karovicova, J., & Kohajdova, Z. (2005). Biogenic amines in food. Chemical Papers-

Chemicke Zvesti, 59(1), 70–79.Krízek, M., Pavlícek, T., & Vácha, F. (2002). Formation of selected biogenic amines in

carp meat. Journal of the Science of Food and Agriculture, 82(9), 1088–1093.Kuley, E., Ozogul, F., Ozogul, Y., & Akyol, I. (2011). The function of lactic acid bacteria

and brine solutions on biogenic amine formation by foodborne pathogens introut fillets. Food Chemistry, 129(3), 1211–1216.

Lehane, L., & Olley, J. (2000). Histamine fish poisoning revisited. International Journalof Food Microbiology, 58(1–2), 1–37.

Li, K. F., Bao, Y. L., Luo, Y. K., Shen, H. X., & Shi, C. (2012). Formation of biogenicamines in crucian carp (Carassius auratus) during storage in ice and at 4 �C.Journal of Food Protection, 75(12), 2228–2233.

Matejková, K., Krízek, M., Vácha, F., & Dadáková, E. (2013). Effect of high-pressuretreatment on biogenic amines formation in vacuum-packed trout flesh(Oncorhynchus mykiss). Food Chemistry, 137(1–4), 31–36.

Montiel, R., De Alba, M., Bravo, D., Gaya, P., & Medina, M. (2012). Effect of highpressure treatments on smoked cod quality during refrigerated storage. FoodControl, 23(2), 429–436.

Paleologos, E. K., Savvaidis, I. N., & Kontominas, M. G. (2004). Biogenic aminesformation and its relation to microbiological and sensory attributes in ice-stored whole, gutted and filleted Mediterranean sea bass (Dicentrarchus labrax).Food Microbiology, 21(5), 549–557.

M. Krízek et al. / Food Chemistry 151 (2014) 466–471 471

Prester, L. (2011). Biogenic amines in fish, fish products and shellfish: A review. FoodAdditives and Contaminants Part A – Chemistry Analysis Control Exposure & RiskAssessment, 28(11), 1547–1560.

Rauscher-Gabernig, E., Gabernig, R., Brueller, W., Grossgut, R., Bauer, F., & Paulsen, P.(2012). Dietary exposure assessment of putrescine and cadaverine andderivation of tolerable levels in selected foods consumed in Austria. EuropeanFood Research and Technology, 235(2), 209–220.

Ruiz-Capillas, C., Carballo, J., & Colmenero, F. J. (2007). Biogenic amines inpressurized vacuum-packaged cooked sliced ham under different chilledstorage conditions. Meat Science, 75(3), 397–405.

Ruiz-Capillas, C., Colmenero, F. J., Carrascosa, A. V., & Munoz, R. (2007). Biogenicamine production in Spanish dry-cured ‘‘chorizo’’ sausage treated with high-pressure and kept in chilled storage. Meat Science, 77(3), 365–371.

Shi, C., Cui, J. Y., Lu, H., Shen, H. X., & Luo, Y. K. (2012). Changes in biogenic amines ofsilver carp (Hypophthalmichthys molitrix) fillets stored at different temperatures

and their relation to total volatile base nitrogen, microbiological andsensory score. Journal of the Science of Food and Agriculture, 92(15), 3079–3084.

Simon-Sarkadi, L., Pasztor-Huszar, K., Istvan, D., & Kisko, G. (2012). Effect of highhydrostatic pressure processing on biogenic amine content of sausage duringstorage. Food Research International, 47(2), 380–384.

Špicka, J., Kalac, P., Bover-Cid, S., & Krízek, M. (2002). Application of lactic acidbacteria starter cultures for decreasing the biogenic amine levels in sauerkraut.European Food Research and Technology, 215(6), 509–514.

Stratton, J. E., Hutkins, R. W., & Taylor, S. L. (1991). Biogenic amines in cheeseand other fermented foods – A review. Journal of Food Protection, 54(6),460–470.

Til, H. P., Falke, H. E., Prinsen, M. K., & Willems, M. I. (1997). Acute and subacutetoxicity of tyramine, spermidine, spermine, putrescine and cadaverine in rats.Food and Chemical Toxicology, 35(3–4), 337–348.