High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus glanis)

High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus glanis)

INNFOO-01378; No of Pages 7 Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx Contents lists available at ScienceDirect Innovativ...

474KB Sizes 0 Downloads 36 Views

INNFOO-01378; No of Pages 7 Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx

Contents lists available at ScienceDirect

Innovative Food Science and Emerging Technologies journal homepage: www.elsevier.com/locate/ifset

High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus glanis) Ruth Mengden, Anja Röhner, Nadine Sudhaus, Günter Klein ⁎ Institute of Food Quality and Food Safety, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, D-30173 Hannover, Germany

a r t i c l e

i n f o

Article history: Received 23 June 2015 Received in revised form 24 September 2015 Accepted 1 October 2015 Available online xxxx Keywords: High-pressure processing Listeria monocytogenes Escherichia coli Fish Sensory characteristics

a b s t r a c t In order to determine the effects of high-pressure processing on the microbiological status of mild smoked rainbow trout fillets and fresh European catfish fillets, they were stored under refrigerated conditions for 41 or 7 days, respectively. For inoculation with Listeria monocytogenes or Escherichia coli, the fillets were minced and treated with 200, 400, or 600 MPa for 1 or 5 min at room temperature. HPP reduced L. monocytogenes by N6 log10 CFU/g (P b 0.05) in both fish products, but subsequent growth was detected. Reductions of E. coli were N6 log10 CFU/g (P b 0.05), but during refrigerated storage, no growth was evident in samples. Spoilage microbiota were significantly reduced in the catfish fillets (P b 0.01), whereas the counts in trout fillets was low throughout the storage (around 1–2 log10 CFU/g). In contrast to the nearly unaffected trout fillets, the catfish fillets appeared to be paler and like cooked products. Taking the results of the sensory analyses into account, high-pressure processing seems to be suitable for the treatment of mild smoked rainbow trout fillets, e.g. with a treatment with 600 MPa for 5 min. Industrial relevance: High-pressure processing is an innovative technology in food processing to prolong shelf life. Due to its ability to reduce the overall microbial load and at the same time maintain sensory and nutritional properties, it is especially in use for the treatment of fresh and ready-to-eat foodstuffs. However, it is also known that the range of effects of HPP is dependent on the matrix/food used as well as on the bacteria investigated. Therefore, it is necessary to consider each individual product. Most of the effects analysed in this study, such as microbiological reductions as well as alterations of the sensory characteristics, depended on the intensity of pressure and holding time. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction Fish is of high nutritional value, but is perishable and represents a high microbiological risk for the consumer (Novotny, Dvorska, Lorencova, Beran, & Pavlik, 2004), especially in less processed products like mild smoked fish. A potential risk to human health is the pathogen Listeria monocytogenes, which is ubiquitous in the environment (Magalhães et al., 2014). Contamination or recontamination of seafood with L. monocytogenes may take place at food-processing facilities (Huss, Jørgensen, & Vogel, 2000), since L. monocytogenes is able to survive and grow in a wide range of environmental conditions such as refrigeration temperatures and low pH. Thus, the pathogen is not affected by these food preservation and safety barriers (Gandhi & Chikindas, 2007). According to a study by Domenech, Amorós, Martorell, and Escriche (2012), there is a prevalence of about 2.7% of L. monocytogenes in smoked fish at the industry level and about 25% prevalence at the retail level. Ready-to-eat fishery products represent ⁎ Corresponding author. Tel.: +49 511 953 7256; fax: +49 511 953 7694. E-mail address: [email protected] (G. Klein).

the highest proportion (8.0%) of food samples at processing exceeding the legal safety limits by the European Union (EFSA, 2014). Recalls and alerts concerning contaminations with L. monocytogenes of fish products are issued regularly by food safety agencies (BVL, 2013; Food Standard Agency, 2014). Though recontamination with Listeria is more common in smoked fish products, fresh fish may be affected too (Kuzmanovic et al., 2011), including recontamination with L. monocytogenes (Jallewar, Kalorey, Kurkure, Pande, & Barbuddhe, 2007). The occurrence of Escherichia coli indicates poor hygiene, and may either derive from polluted pond water (Ozer & Demirci, 2006; Suhalim, Huang, & Burtle, 2008) or occur due to inappropriate handling practises after harvest and slaughter. Furthermore, E. coli is a wellknown foodborne pathogen that frequently causes foodborne illness outbreaks (EFSA, 2014; Saldana, Monfort, Condon, Raso, & Alvarez, 2012). Atanassova, Reich, and Klein (2008); Teophilo, dos Fernandes Vieira, dos Prazeres Rodrigues, and Menezes (2002) as well as Shin, Chang, and Kang (2004) also describe E. coli as a potentially pathogenic bacterium associated with seafood or fish. Generally, microorganisms are the main cause of fish spoilage. Innovative ‘nonthermal’ processing based on high hydrostatic pressure, is

http://dx.doi.org/10.1016/j.ifset.2015.10.002 1466-8564/© 2015 Elsevier Ltd. All rights reserved.

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002

2

R. Mengden et al. / Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx

able to kill or sublethally injure microorganisms especially through damaging their membrane (Hugas, Garriga, & Monfort, 2002; Kalchayanand, Sikes, Dunne, & Ray, 1998). At the same time, HPP is less destructive for the flavour of compounds or vitamins compared with cooking (Krzikalla, 2008; Smelt, 1998). High-pressure processing (HPP) can operate at low (1.5°C–15°C) or mild (up to 55°C) temperatures and is very effective even for treatments with a short holding time (Chen, 2007; Phuvasate & Su, 2015). HPP has been demonstrated to be capable of inactivating L. monocytogenes or E. coli in seafood (Lakshmanan & Dalgaard, 2004; Ramaswamy, Zaman, & Smith, 2008) and to increase its shelf-life (Hurtado, Montero, & Borderias, 2000; López-Caballero, Perez-Mateos, Borderias, & Montero, 2000). It has been shown that fish products like tuna or salmon may be liable to detrimental alterations (Gómez-Estaca, López-Caballero, Gómez-Guillen, de Lacey, & Montero, 2009; Zare, 2004). However, sensory changes due to protein denaturation are fish species–dependent (Matser, Stegeman, Kals, & Bartels, 2000) and hence each fish product requires specific investigation. Thus, the objective of this study was to investigate the potential of HPP to reduce inoculated L. monocytogenes in minced fresh catfish derived from fillets and minced mild smoked trout derived from fillets. Furthermore, the reduction of inoculated E. coli in the minced mild smoked rainbow trout derived from fillets was investigated. During chilled storage, the microbial status regarding L. monocytogenes, E. coli as well as the mesophilic aerobic count was determined. Another objective was to detect sensory modifications in non-minced samples derived from both kinds of fish fillet. 2. Materials and methods 2.1. Raw material and sample preparation Rainbow trout fillets were hot-smoked, filleted, and then packaged under modified atmosphere packaging by Ternäben Service GmbH, Lembruch, Germany. Afterwards, they were transported under chilled conditions to the laboratory of the Institute of Food Quality and Food Safety. The fresh-filleted catfish were provided by Ahrenhorster Edelfisch GmbH & Co. KG, Badbergen/Vehs, Germany. For sensory evaluation and aerobic plate count determination, the catfish fillets were cut into sections of 100–150 g and vacuum-packed (Henkovac, ML’sHertogenbosch, The Netherlands) at the German Institute of Food Technologies (DIL), Quakenbrück, Germany. Only rainbow trout samples meant for sensory analysis remained in their original wrapping. In order to enable inoculation experiments with L. monocytogenes and E. coli, whole fillets of both kinds of fish were minced (Moulinex®, Krups GmbH, Offenbach, Germany) after reaching the laboratory, portioned to 20 g and vacuum-packed by vacuum device P 500 (ALLPAX, Papenburg, Germany). Before packaging, one-third of the trout samples were inoculated with 4 mL each of the bacterial suspension of L. monocytogenes. Another third was inoculated with 4 mL of the bacterial suspension of E. coli. Hence, a final concentration of 108 CFU/g for L. monocytogenes and 107 CFU/g for E. coli, respectively, could be obtained in the fish samples. The last third remained non-inoculated. The minced catfish derived from fillets were divided into one group inoculated with L. monocytogenes, 8.01 ± 0.14 log10 CFU/g, and another non-inoculated control. 2.2. Bacterial cultures Pure cultures of E. coli (DSM 19754; human faeces) and L. monocytogenes (ATCC 15313; rabbit) were maintained in the frozen stock in the Institute of Food Quality and Food Safety (University of Veterinary Medicine Hannover, Foundation, Hannover, Germany). E. coli was cultured for 24 h at 37°C in a 10-mL sterile brain heart infusion broth (Merck, Darmstadt, Germany) and L. monocytogenes 24 h at

30°C in 10-mL half Fraser broth (OXOID, Wesel, Germany). The enriched microorganisms were then plated on sheep blood agar (OXOID, Wesel, Germany) and incubated for 24 h at 37°C. Inocula were prepared by transferring isolated colonies of E. coli and L. monocytogenes into 500 mL of sterile brain heart infusion broth (Merck, Darmstadt, Germany) and into 500-mL half Fraser broth (OXOID, Wesel, Germany), respectively. E. coli suspension, incubated at 37°C for 24 h, resulted in a suspension containing 7.52 ± 0.43 log10 CFU/mL. L. monocytogenes suspension incubated at 30°C for 24 h, resulted in a suspension containing 8.09 ± 0.27 log10 CFU/mL. This suspension was used for inoculation of mild smoked trout fillets and 8.01 ± 0.14 log10 CFU/ml for the fresh catfish fillets. 2.3. High-pressure treatment Depending on the fish species, different settings were applied. The mild smoked rainbow trout fillets were pressurised for 1 or 5 min at 400 or 600 MPa, respectively, whereas the fresh catfish fillets were pressure-treated for 1 or 5 min at 200, 400 or 600 MPa, respectively. The treatments with 200 MPa were added to the settings, as it was assumed to obtain significant differences regarding HPP effects on the catfish fillets even at lower pressure magnitudes. Untreated samples were used as controls (Table 1). The equipment used for the inoculation experiments as well as for the sensory investigation of the mild smoked rainbow trout fillets consisted of a 2-L capacity chamber for holding the HPP fluid (distilled water) and samples. The isostatic press (Model Isostatic press 6500 bar 2-L, NOVA SWISS®, NOVA-WERKE AG, Effretikon, Switzerland) was rated for operation up to a maximum pressure of 650 MPa and had a pressure rise-up time of maximum 6 min and a decompression period of less than 1 min. The catfish samples for sensory analyses were treated immediately after packaging with the high-pressure device (at the DIL, WAVE 600/ 55, NC Hiperbaric S.A., Spain) possessing a 55-L chamber and a maximum operation level of 600 MPa. Pressure come-up times were about 2.25, 1.30, and 0.52 min to reach 600, 400, and 200 MPa, respectively, while decompression took 25 s or less. Both devices were used at room temperature. Due to adiabatic heating, the temperature inside the vessel reached a maximum of 34°C at the setting 600;5. 2.4. Microbiological examinations Three samples of the different batches were microbiologically analysed before HPP treatment and also during the storage at 5 ± 2°C on days 1, 13, 27, and 41 for rainbow trout samples and on days 1, 4, and 7 for catfish samples after treatment. Additionally, samples without pressure treatment were analysed as a control group on the same storage days. The mesophilic aerobic count (APC) was determined on plate count agar (OXOID, Wesel, Germany) according to the DIN 10161 in the non-inoculated samples. The plates were incubated for 72 h at 30°C. E. coli was enumerated on Tryptone Bile X-glucuronide Agar (TBX, OXOID, Wesel, Germany) and L. monocytogenes on Brilliance™ Listeria Agar (OXOID, Wesel, Germany) in the inoculated samples. The plates

Table 1 Treatment groups with different pressure–time-combinations Group

Pressure (MPa)

Time (min)

0 200;1 200;5 400;1 400;5 600;1 600;5

– 200 200 400 400 600 600

– 1A 5AB 1 5 1B 5

A B

These settings were not conducted for rainbow trout samples. These settings were not conducted for sensory analysis of catfish samples.

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002

R. Mengden et al. / Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx

were incubated for 24 h at 42°C for E. coli and 48 h at 37°C for L. monocytogenes, according to ISO 16649-2:2001 and DIN EN ISO 11290-2, respectively. For qualitative analyses, L. monocytogenes was enriched in half Fraser broth (OXOID, 24 h at 30°C) followed by Fraser broth (OXOID, 48 h at 37°C) and then plated on Brilliance™ Listeria Agar (OXOID, Wesel, Germany), thus modifying the DIN EN ISO 11290-1. These plates were incubated for 48 h at 37°C. 2.5. Sensory evaluation A trained ten-person panel was asked to differentiate according to ISO 4121:2003(E) in a unipolar comparison between the untreated control and four high-pressure–treated samples of rainbow trout (all settings) or catfish (200;1, 400;1, 400;5, 600;5, see Table 1) on the first or second day after treatment, respectively. The applied scale was defined from 0 (equal to control) to −4 (strongest alteration). Concerning the catfish samples, the panellists should asses the parameters of appearance (raw/cooked; white/glassy) and texture (solid/loose; dry/ juicy), while overall appearance, colour, and texture were to be evaluated for rainbow trout samples only. To compare the results for both species, an overall appearance for the catfish was calculated on the basis of the above-mentioned parameters. Therefore, every single answer of the ten panellists in the six trials was counted and summed for each scale value and parameter. Thus, the more frequently one sample was assessed with one scale value, the higher the overall frequency was (in percent) for this sample. 2.6. Statistical analyses Collecting data and calculating mean values was performed with the programme EXCEL from Microsoft® Office 2003. The obtained data were statistically analysed using the Shapiro–Wilk test to detect normal distribution. If the data showed a normal distribution, the Student's t-test was consulted to determine significance. Whenever the data did not follow a normal distribution, Wilcoxon signed-rank test or Kruskal–Wallis test were conducted. The software used to determine statistical significances was SAS® 9.3. Level of significance was defined as 5%, and thus values with P b 0.05 were considered significant. 3. Results and discussion 3.1. Effects on the mesophilic aerobic count, L. monocytogenes, and E. coli The results of the microbiological analysis of minced mild smoked trout fillets on mesophilic aerobic count (APC) are shown in Fig. 1.

3

The APC of the minced trout derived from fillets before HPP was below the detection limit (1.0 log10 CFU/g). During storage, there was a moderate increase of the APC to 3.43 ± 1.86 log10 CFU/g in the untreated samples. Kolodziejska, Niecikowska, Januszewska, and Sikorski (2002) showed similar numbers for the initial bacterial count for hotsmoked mackerel. After smoking, the APC in the mackerel meat was 1.5 ± 0.4 log10 CFU/g. During storage for 21 days, they observed no changes in the APC at a storage temperature of 2 ± 1°C, but an increase of up to 4.7 ± 2.0 CFU/g at 8 ± 1°C. The trout samples were stored at 5 ± 2°C. In the present study, no significant effect of HPP on the APC of trout fillets was detectable because of the low initial bacterial count. Nevertheless, the pressure-treated samples had lower values of APC than in the untreated samples at all storage days. Treatment with 600 MPa resulted in APC below the detection limit in almost all trout samples. Yagiz, Kristinsson, Balaban, and Marshall (2007) could determine a reduction of APC in fresh trout with higher initial count by 4 to 6 log10 CFU/g with 400 or 600 MPa, respectively. Also, in our study, the HPP reduction of APC in the catfish fillet samples was higher than in trout because of the higher initial count (see Table 2). The greater the HPP treatment was, the lower the APC was on day 1 as well as the subsequent growth, which is in accordance with the inhibited growth of the total viable counts during storage in pressurised cold-smoked salmon (Erkan et al., 2011). In the present study, even the highest counts of the APC in the catfish groups 600;1 (3.62 ± 0.82 log10 CFU/g) and 600;5 (3.0 ± 1.0 log10 CFU/g) at the end of the storage on day 7 were not as high as the initial counts of the control on day 1 (4.21 ± 0.48 log10 CFU/g). Thus, both treatments at higher pressure extended the shelf-life. The effect of HPP on L. monocytogenes and E. coli was even more obvious (Table 2 as well as Figs. 2 and 3). After inoculation and before pressure treatment, the initial bacterial count of L. monocytogenes was 8.09 ± 0.27 log10 CFU/g and 8.01 ± 0.14 log10 CFU/g for trout samples and catfish samples, respectively. The high-pressure treatment caused a significant (P b 0.01) reduction of L. monocytogenes in both species. On day 1, the bacterial count was lower in the treated samples than in the untreated samples. Even the less intense treatments (200;1, 200;5, and 400;1) used for the catfish samples revealed a significant reduction (P b 0.05). This bacterial count-reducing effect increased with higher pressure and longer holding time. The same effect has been described for L. innocua in cold-smoked salmon (Gudbjornsdottir, Jonsson, Hafsteinsson, & Heinz, 2010). Gudbjornsdottir et al. (2010) had chosen L. innocua as a non-pathogenic model organism because the organism is closely related to L. monocytogenes (Milillo et al., 2011). In the present study, the best reduction rate of 6.46 log10 CFU/g of L. monocytogenes was achieved with 600 MPa for 5 min (P b 0.01) in the minced trout, reducing the bacterial count below the detection limit (2.0 log10 CFU/g) on

9 8

log 10 (CFU/g)

7 6

0

5

400;1 400;5

4

600;1

3

600;5 2 1 0 1

13

27

41

Storage time (days) Fig. 1. Changes of the mesophilic aerobic count in untreated (0) and high-pressure–treated samples (MPa;min) of minced mild smoked rainbow trout derived from fillet during storage at 5 ± 2°C. The error bars indicate the standard deviation out of six trials.

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002

4

R. Mengden et al. / Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx

Table 2 Mesophilic aerobic count and L. monocytogenes (log10 CFU/g ± SD1)) in fresh catfish fillets before (day 0), after HPP (day 1), and during storage at 5 ± 2°C (days 4 and 7) T2)

day 1

day 4

day 7

L. monocytogenes 0 200;1 200;5 400;1 8.01 ± 0.14*) 400;5 600;1 600;5

day 0

8.27 ± 0.12a 8.10 ± 0.11bc 8.13 ± 0.04b 7.90 ± 0.19c 6.85 ± 0.52d 4.55 ± 0.68e 1.81 ± 0.27f

8.34 ± 0.18a 8.09 ± 0.26ab 8.24 ± 0.17a 7.94 ± 0.20b 7.02 ± 0.43c 5.30 ± 0.84d 2.32 ± 0.98e

8.31 ± 0.08a 8.25 ± 0.11ab 8.13 ± 0.08b 7.96 ± 0.10c 7.10 ± 0.57d 5.56 ± 0.65e 3.04 ± 1.26f

Mesophilic aerobic count 0 200;1 200;5 − 400;1 400;5 600;1 600;5

4.21 ± 0.48a 3.72 ± 0.54ab 3.67 ± 0.38b 3.07 ± 0.31c 2.53 ± 0.31d 2.13 ± 0.46de 1.62 ± 0.67e

6.13 ± 1.12a 5.34 ± 0.76ab 5.07 ± 0.62b 3.59 ± 0.49c 3.03 ± 0.39d 2.37 ± 0.42e 2.15 ± 0.64e

7.92 ± 0.18a 7.74 ± 0.39a 7.22 ± 0.21b 5.89 ± 0.65c 4.65 ± 0.71d 3.62 ± 0.82de 3.00 ± 1.0e

*) initial concentration of L. monocytogenes after inoculation. The values on day 0 are equal for every group, because of analysing before splitting in different treatment groups (see Table 1). SD1) = standard deviation, T2) = treatment. a-e Means within a column lacking a common superscript differ significantly (P b 0.05).

day 1. Similarly, the highest reduction in the minced catfish was 6.07 log10 CFU/g. Nevertheless, L. monocytogenes could be qualitatively detected in all samples; hence, the treatment at 600 MPa for 5 min was not able to eliminate the entire microbial population. This indicated that the cells inoculated into the fish samples did not suffer from the rapid temperature change between the growth in half Fraser broth, HPP, and storage. The treatment at 600 MPa for 1 min led to a significant (P b 0.01) reduction of L. monocytogenes in comparison with the untreated group of more than 5.0 log10 CFU/g and 3.0 log10 CFU/g in the trout and in the catfish samples, respectively. Similar results were reported for L. innocua in minced rainbow trout (Basaran-Akgul et al., 2010), where a reduction of about 6.0 log10 units of L. innocua after 5 min with 517 MPa occurred. In contrast to Ritz et al. (2000), who achieved no significant reductions between a 3- and 10-min treatment and therefore treatment time was deemed the least significant setting, there was a significant

difference of counts of L. monocytogenes treated with either 600 MPa for 1 or 5 min in the catfish (P b 0.01) and trout (P b 0.05) samples. During the storage period of 41 days, the bacterial count of L. monocytogenes in the trout samples increased in group 400;5, 600;1, and 600;5 significantly (P b 0.05). Thus, in line with the qualitative analyses of the samples treated with 600 MPa for 5 min on day 1, there was a residual population that was able to grow during storage at 5 ± 2°C. This finding is in agreement with the statement of Gandhi and Chikindas (2007) that L. monocytogenes grows at refrigeration temperatures and Montiel, Bravo, de Alba, Gaya, and Medina (2012a), who also observed a regrowth during storage of cold-smoked salmon at 5°C. The strongest increase was recognisable in the trout samples in group 600;1 and 600;5 from day 1 to day 27 (Fig. 2). In the control and in groups 200;1, 200;5 (catfish), and 400;1 (catfish and trout) no increase was visible. The reason for this could be the maximum level of initial bacterial count in the samples. The bacteriostatic effect seen in group 400;5 (catfish) may be due to the comparatively short storage period, which also led to the only slight regrowth in the catfish groups 600;1 and 600;5. Montero, Gomez-Estaca, and Gomez-Guillen (2007) inhibited growth of L. monocytogenes for 15 days using 300 MPa for 15 min and by addition of salt to cold-smoked dolphin fish, whereas L. monocytogenes in chicken breast fillet remained under the detection limit for 14 days after treatment with 600 MPa for 5 min (Kruk et al., 2011). In contrast, the treated trout samples showed a bacterial regrowth, almost reaching the values of untreated samples during the storage. Thus, the difference between the untreated samples and samples treated with 600 MPa for 5 min was b1 log10 CFU/g on day 41. The ability of sublethally injured L. monocytogenes to recover and regrow after HPP is also a known problem in other food products like milk (Bull, Hayman, Stewart, Szabo, & Knabel, 2005). As previously described for L. monocytogenes, the high-pressure treatment also had an effect on the amount of E. coli in mild smoked trout fillets (Fig. 3). Before pressure treatment, the bacterial count of E. coli, used as a model organism for contamination related to manual handling during processing, was 7.52 ± 0.43 log10 CFU/g in the minced fish derived from fillets. After treatment with 400 MPa for 1 min, the amount of E. coli in the treated sample was 2.37 log10 CFU/g lower than in the untreated samples. With higher pressure and longer holding time, the reduction was much more effective. The treatment at 600 MPa for 5 min achieved a reduction of 6.05 log10 CFU/g for E. coli (P b 0.05) in the trout fillets. Alpas, Kalchayanand, Bozoglu, and Ray (2000) detected

9 8 7

log10 (CFU/g)

6

0 400;1

*1)

5

400;5 4

600;1

3

600;5 *

2 1

**

0 1

13

27

41

Storage time (days) 1)

Only treatments with 600 MPa were still significant.

Fig. 2. Changes of L. monocytogenes in untreated (0) and high-pressure–treated samples (MPa;min) of minced mild smoked rainbow trout derived from fillet during storage at 5 ± 2°C. The error bars indicate the standard deviation out of six trials. Asterisks indicate statistical significance (*P b 0.5, **P b 0.01) between treated samples and controls.

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002

R. Mengden et al. / Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx

5

9 8 7

0

log10 (CFU/g)

6

400;1

5

400;5 4

600;1

3

600;5

2 1 0

** 1)

** 1)

** 1)

** 1)

1

13

27

41

Storage time (days) 1)

Treatment 400;1 was only significant with *P<0.05 throughout the whole storage.

Fig. 3. Changes of E. coli in untreated (0) and high-pressure–treated samples (MPa;min) of minced mild smoked rainbow trout derived from fillet during storage at 5 ± 2°C. The error bars indicate the standard deviation out of six trials. Asterisks indicate statistical significance (*P b 0.5, **P b 0.01) between treated samples and controls.

In conclusion, similar to L. monocytogenes, even the 600 MPa for 5 min did not kill the whole E. coli population. In contrast to L. monocytogenes, the reduction of E. coli on day 41 was nearly identical to the reduction on day 1. This continuity may have been due to the chilled storage.

Frequency of mentioned scale values [%]

a similar effect for two different strains of E. coli in suspensions. With lower pressure (207 MPa) for 5 min, they found a reduction of 0.58 and 0.78 log10 CFU/ml, respectively. With higher pressure, the reduction was more effective (2.52 and 3.66 log10 CFU/ml, respectively). At the beginning of the inoculation and day 1, standard deviations were relatively low but their width increased during storage. This reflects the real conditions during the storage. However, differences between the HPP treatments were detectable. The minimum growth temperature of E. coli is assumed to be ≥7°C (Jones, Gill, & McMullen, 2004). Thus, during storage at 5 ± 2°C, the non-treated samples showed a small decrease of E. coli. The same decreasing effect is described for fish slurry for the untreated control group stored at 4°C in the study of Ramaswamy et al. (2008). All treated samples in our study showed a minor increase from day 1 to day 13, followed by a slight decrease until day 41. In group 600;5, the bacterial count was below the detection limit (1.0 log10 CFU/g) on day 1.

3.2. Effects on the sensory overall appearance In order to compare the sensory appearance of the catfish to the rainbow trout fillets, a value for the overall appearance of catfish samples was calculated using the answers regarding appearance and texture. The high-pressure–treated samples differed from the controls regarding the texture parameters whereas the appearance parameters were similar. In other words, the texture had more influence on the calculated sensory overall appearance of the catfish (data not shown). This generated value was then expressed as the frequency of mentioned

50

40

30

200;1 400;1

20

400;5 600;5

10

0 0

-1

-2

-3

-4

Scale values of sensory evaluation Fig. 4. Effect of high-pressure processing (MPa;min) on the overall sensory appearance of the fresh catfish fillets (scale value range: 0 (equal to control) to −4 (strongest alteration) (n = 6)).

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002

R. Mengden et al. / Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx

Frequency of mentioned scale values [%]

6

50

400;1 40

400;5 600;1

30

600;5 20

10

0 0

-1

-2

-3

-4

Scale values of sensory evaluation Fig. 5. Effect of high-pressure processing (MPa;min) on the overall sensory appearance of the mild smoked rainbow trout fillets (scale value range: 0 (equal to control) to −4 (strongest alteration) (n = 5)).

scale values (see Fig. 4). Depending on the intensity of the HPP treatment, changes of the sensory appearance could be detected in the catfish samples. The treatment at 200;1 was most mentioned at scale values 0 and −1 (47.92% and 41.67%, respectively) and hence was similar or close to the control, which is in accordance with findings in fresh red mullet fillets (Erkan, Uretener, & Alpas, 2010). Treatment group 600;5 was most often mentioned at − 4, and thus deviated the most. Even treatments 400;1 and 400;5, which solely differed concerning their time setting, revealed differentiating results. In other words, longer pressurisation times affected the sensory quality of the fresh catfish fillets. The panellists predominantly described the treated catfish fillet pieces as “cooked” and “brighter”, as it is reported for other pressurised fish products (Chevalier, Le Bail, & Ghoul, 2001; Lakshmanan, Miskin, & Piggott, 2005; Montiel et al., 2012a; Teixeira et al., 2014). In contrast to the catfish fillets, the overall appearance of the trout fillet samples was more uniform. The panellists merely detected a slight difference between treated samples and controls, which resulted in −1 to be the most mentioned scale value for all the treatments (see Fig. 5). However, the sensory changes due to HPP were less obvious than changes during the smoking process (Montiel, De Alba, Bravo, Gaya, & Medina, 2012b; Unlusayin, Kaleli, & Gulyavuz, 2001). Since sensory appearance plays an important role for the purchase decisions by the costumers (Garber, Hyatt, & Starr, 2003), it is more likely that the pressurised mild smoked rainbow trout fillets will be as well accepted as the original product compared to the substantially altered catfish fillets. On the other hand, there is the possibility to develop new products on the basis of the treated catfish fillets, which would be appreciated by the consumers (Gómez-Estaca et al., 2009; Nielsen et al., 2009). 4. Conclusions The high-pressure treatment was suitable to reduce the amount of inoculated pathogens such as L. monocytogenes and E. coli in mild smoked rainbow trout fillet as well as L. monocytogenes in fresh catfish fillet. This effect increased with higher pressure and longer holding times. Even though 600 MPa for 5 min was able to reduce L. monocytogenes and E. coli by more than 6 log10 CFU/g, the pathogens could not be eliminated completely. Hence, there was a residual population of L. monocytogenes that was able to grow during storage at 5 ± 2°C. Although E. coli could not be eliminated, the pressure treatment

followed by refrigerated storage (5 ± 2°C) prevented its recovery and growth for 41 days (the samples were still sensory acceptable). While the mesophilic aerobic count of the catfish samples was reduced depending on the treatment intensity, no such effect could be seen for the trout fillet due to low initial levels. The sensory investigations revealed strong differences of the highpressure induced changes for the fresh catfish compared to mild smoked rainbow trout fillets, which is assumed to be due to the smoking process.

Acknowledgements This research was supported by the German Federal Ministry of Food and Agriculture (support code: 511-06.01-28-1-63.021-07). The authors thank the involved companies Ternäben Service GmbH, Lembruch, Germany and Ahrenhorster Edelfisch GmbH & Co. KG, Badbergen/Vehs, Germany for providing the sample material.

References Alpas, H., Kalchayanand, N., Bozoglu, F., & Ray, B. (2000). Interactions of high hydrostatic pressure, pressurization temperature and pH on death and injury of pressureresistant and pressure-sensitive strains of foodborne pathogens. International Journal of Food Microbiology, 60(1), 33–42. Atanassova, V., Reich, F., & Klein, G. (2008). Microbiological quality of sushi from sushi bars and retailers. Journal of Food Protection, 71(4), 860–864. Basaran-Akgul, N., Mousavi-Hesary, M., Basaran, P., Shin, J.H., Swanson, B.G., & Rasco, B.A. (2010). High pressure processing inactivation of Listeria innocua in minced trout (Oncorhynchus mykiss). Journal of Food Processing and Preservation, 34, 191–206. Bull, M.K., Hayman, M.M., Stewart, C.M., Szabo, E.A., & Knabel, S.J. (2005). Effect of prior growth temperature, type of enrichment medium, and temperature and time of storage on recovery of Listeria monocytogenes following high pressure processing of milk. International Journal of Food Microbiology, 101(1), 53–61. BVL (2013). Listeria monocytogenes in Forellenfilets. [Retrieved on 27-Aug-2013, from www.lebensmittelwarnung.de]. Chen, H.Q. (2007). Temperature-assisted pressure inactivation of Listeria monocytogenes in Turkey breast meat. International Journal of Food Microbiology, 117, 55–60. Chevalier, D., Le Bail, A., & Ghoul, M. (2001). Effects of high pressure treatment (100– 200 MPa) at low temperature on turbot (Scophthalmus maximus) muscle. Food Research International, 34(5), 425–429. Domenech, E., Amorós, J.A., Martorell, S., & Escriche, I. (2012). Safety assessment of smoked fish related to Listeria monocytogenes prevalence using risk management metrics. Food Control, 25(1), 233–238. EFSA (2014). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA Journal, 12(2), 312.

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002

R. Mengden et al. / Innovative Food Science and Emerging Technologies xxx (2015) xxx–xxx Erkan, N., Uretener, G., & Alpas, H. (2010). Effects of high pressure treatment on physicochemical characteristics of fresh sea bass (Dicentrarchus labrax). Journal of Consumer Protection and Food Safety, 5(1), 83–89. Erkan, N., Üretener, G., Alpas, H., Selçuk, A., Özden, Ö., & Buzrul, S. (2011). The effect of different high pressure conditions on the quality and shelf life of cold smoked fish. Innovative Food Science & Emerging Technologies, 12(2), 104–110. Food Standard Agency (2014). The Fine Seafood Company recalls packs of smoked salmon. [Retrieved on 26-Jul-2014, from http://www.food.gov.uk/news-updates/news/ 2014/6069/salmon#.U6vjB0Dl6Wc]. Gandhi, M., & Chikindas, M.L. (2007). Listeria: a foodborne pathogen that knows how to survive. International Journal of Food Microbiology, 113(1), 1–15. Garber, L.L., Jr., Hyatt, E.M., & Starr, R.G., Jr. (2003). Measuring consumer response to food products. Food Quality and Preference, 14(1), 3–15. Gómez-Estaca, J., López-Caballero, M.E., Gómez-Guillen, M.C., de Lacey, A.L., & Montero, R. (2009). High pressure technology as a tool to obtain high quality Carpaccio and Carpaccio-like products from fish. Innovative Food Science & Emerging Technologies, 10(2), 148–154. Gudbjornsdottir, B., Jonsson, A., Hafsteinsson, H., & Heinz, V. (2010). Effect of highpressure processing on Listeria spp. and on the textural and microstructural properties of cold smoked salmon. LWT - Food Science and Technology, 43(2), 366–374. Hugas, M., Garriga, M., & Monfort, J.M. (2002). New mild technologies in meat processing: high pressure as a model technology. Meat Science, 62(3), 359–371. Hurtado, J.L., Montero, P., & Borderias, A.J. (2000). Extension of shelf life of chilled hake (Merluccius capensis) by high pressure. Food Science and Technology International, 6(3), 243–249. Huss, H.H., Jørgensen, L.V., & Vogel, B.F. (2000). Control options for Listeria monocytogenes in seafoods. International Journal of Food Microbiology, 62(3), 267–274. Jallewar, P.K., Kalorey, D.R., Kurkure, N.V., Pande, V.V., & Barbuddhe, S.B. (2007). Genotypic characterization of Listeria spp. isolated from fresh water fish. International Journal of Food Microbiology, 114(1), 120–123. Jones, T., Gill, C.O., & McMullen, L.M. (2004). The behaviour of log phase Escherichia coli at temperatures that fluctuate about the minimum for growth. Letters in Applied Microbiology, 39(3), 296–300. Kalchayanand, N., Sikes, A., Dunne, C.P., & Ray, B. (1998). Factors influencing death and injury of foodborne pathogens by hydrostatic pressure-pasteurization. Food Microbiology, 15(2), 207–214. Kolodziejska, I., Niecikowska, C., Januszewska, E., & Sikorski, Z.E. (2002). The microbial and sensory quality of mackerel hot smoked in mild conditions. Food Science and Technology, 35(1), 87–92. Kruk, Z.A., Yun, H., Rutley, D.L., Lee, E.J., Kim, Y.J., & Jo, C. (2011). The effect of high pressure on microbial population, meat quality and sensory characteristics of chicken breast fillet. Food Control, 22(1), 6–12. Krzikalla, K.I. (2008). Hochdruckinduzierte Veränderungen von Lebensmittelinhaltsstoffen. Diss. Berlin: Technische Universität Berlin. Kuzmanovic, J., Asanin, R., Baltic, M., Misic, D., Dimitrijevic, M., Stojanovic, M., ... Kovacevic, I. (2011). Presence of Listeria spp. in fish samples, fish products and sea products. Acta Veterinaria-Beograd, 61(2–3), 193–203. Lakshmanan, R., & Dalgaard, P. (2004). Effects of high-pressure processing on Listeria monocytogenes, spoilage microflora and multiple compound quality indices in chilled cold-smoked salmon. Journal of Applied Microbiology, 96(2), 398–408. Lakshmanan, R., Miskin, D., & Piggott, J.R. (2005). Quality of vacuum packed cold-smoked salmon during refrigerated storage as affected by high-pressure processing. Journal of the Science of Food and Agriculture, 85(4), 655–661. López-Caballero, M.E., Perez-Mateos, M., Borderias, J.A., & Montero, P. (2000). Extension of the shelf life of prawns (Penaeus japonicus) by vacuum packaging and highpressure treatment. Journal of Food Protection, 63(10), 1381–1388. Magalhães, R., Mena, C., Ferreira, V., Silva, J., Almeida, G., Gibbs, P., & Teixeira, P. (2014). Bacteria: Listeria monocytogenes. In Y. Motarjemi (Ed.), Encyclopedia of food safety (pp. 450–461). Waltham: Academic Press. Matser, A.M., Stegeman, D., Kals, J., & Bartels, P.V. (2000). Effects of high pressure on colour and texture of fish. High Pressure Research, 19(1–6), 499–505. Milillo, S.R., Friedly, E.C., Saldivar, J.C., Muthaiyan, A., O'Bryan, C., Crandall, P.G., ... Ricke, S.C. (2011). A review of the ecology, genomics, and stress response of Listeria innocua

7

and Listeria monocytogenes. Critical Reviews in Food Science and Nutrition, 52(8), 712–725. Montero, P., Gomez-Estaca, J., & Gomez-Guillen, M.C. (2007). Influence of salt, smoke, and high pressure on growth of Listeria monocytogenes and spoilage microflora in coldsmoked dolphinfish (Coryphaena hippurus). Journal of Food Protection, 70(2), 399–404. Montiel, R., Bravo, D., de Alba, M., Gaya, P., & Medina, M. (2012a). Combined effect of high pressure treatments and the lactoperoxidase system on the inactivation of Listeria monocytogenes in cold-smoked salmon. Innovative Food Science & Emerging Technologies, 16(0), 26–32. Montiel, R., De Alba, M., Bravo, D., Gaya, P., & Medina, M. (2012b). Effect of high pressure treatments on smoked cod quality during refrigerated storage. Food Control, 23(2), 429–436. Nielsen, H.B., Sonne, A.M., Grunert, K.G., Banati, D., Pollak-Toth, A., Lakner, Z., ... Peterman, M. (2009). Consumer perception of the use of high-pressure processing and pulsed electric field technologies in food production. Appetite, 52(1), 115–126. Novotny, L., Dvorska, L., Lorencova, A., Beran, V., & Pavlik, I. (2004). Fish: a potential source of bacterial pathogens for human beings. Veterinarni Medicina, 49(9), 343–358. Ozer, N.P., & Demirci, A. (2006). Electrolyzed oxidizing water treatment for decontamination of raw salmon inoculated with Escherichia coli O157:H7 and Listeria monocytogenes Scott a and response surface modeling. Journal of Food Engineering, 72(3), 234–241. Phuvasate, S., & Su, Y. -C. (2015). Efficacy of low-temperature high hydrostatic pressure processing in inactivating Vibrio parahaemolyticus in culture suspension and oyster homogenate. International Journal of Food Microbiology, 196, 11–15. Ramaswamy, H.S., Zaman, S.U., & Smith, J.P. (2008). High pressure destruction kinetics of Escherichia coli (O157:H7) and Listeria monocytogenes (Scott A) in a fish slurry. Journal of Food Engineering, 87(1), 99–106. Ritz, M., Jugiau, F., Rama, F., Courcoux, P., Semenou, M., & Federighi, M. (2000). Inactivation of Listeria monocytogenes by high hydrostatic pressure: effects and interactions of treatment variables studied by analysis of variance. Food Microbiology, 17(4), 375–382. Saldana, G., Monfort, S., Condon, S., Raso, J., & Alvarez, I. (2012). Effect of temperature, pH and presence of nisin on inactivation of Salmonella Typhimurium and Escherichia coli O157:H7 by pulsed electric fields. Food Research International, 45(2), 1080–1086. Shin, J.H., Chang, S., & Kang, D.H. (2004). Application of antimicrobial ice for reduction of foodborne pathogens (Escherichia coli O157:H7, Salmonella Typhimurium, Listeria monocytogenes) on the surface of fish. Journal of Applied Microbiology, 97(5), 916–922. Smelt, J.P.P.M. (1998). Recent advances in the microbiology of high pressure processing. Trends in Food Science & Technology, 9(4), 152–158. Suhalim, R., Huang, Y. -W., & Burtle, G.J. (2008). Survival of Escherichia coli O157:H7 in channel catfish pond and holding tank water. LWT - Food Science and Technology, 41(6), 1116–1121. Teixeira, B., Fidalgo, L., Mendes, R., Costa, G., Cordeiro, C., Marques, A., ... Nunes, M.L. (2014). Effect of high pressure processing in the quality of sea bass (Dicentrarchus labrax) fillets: pressurization rate, pressure level and holding time. Innovative Food Science & Emerging Technologies, 22(0), 31–39. Teophilo, G., dos Fernandes Vieira, R., dos Prazeres Rodrigues, D., & Menezes, F. (2002). Escherichia coli isolated from seafood: toxicity and plasmid profiles. International Microbiology, 5(1), 11–14. Unlusayin, M., Kaleli, S., & Gulyavuz, H. (2001). The determination of flesh productivity and protein components of some fish species after hot smoking. Journal of the Science of Food and Agriculture, 81(7), 661–664. Yagiz, Y., Kristinsson, H.G., Balaban, M.O., & Marshall, M.R. (2007). Effect of high pressure treatment on the quality of rainbow trout (Oncorhynchus mykiss) and mahi mahi (Coryphaena hippurus). Journal of Food Science, 72(9), C509–C515. Zare, Z. (2004). High pressure processing of fresh tuna fish and its effects on shelf life. Diss. Montreal, Quebec, Canada: Macdonald Campus of McGill University.

Please cite this article as: Mengden, R., et al., High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus gl..., Innovative Food Science and Emerging Technologies (2015), http://dx.doi.org/10.1016/j.ifset.2015.10.002