Effects of different freezing treatments on the biogenic amine and quality changes of bighead carp (Aristichthys nobilis) heads during ice storage

Food Chemistry 138 (2013) 1476–1482

Contents lists available at SciVerse ScienceDirect

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

Effects of different freezing treatments on the biogenic amine and quality changes of bighead carp (Aristichthys nobilis) heads during ice storage Hui Hong a, Yongkang Luo a,⇑, Zhongyun Zhou a, Yulong Bao a, Han Lu a, Huixing Shen b a

College of Food Science and Nutritional Engineering, China Agricultural University, Beijing Higher Institution Engineering Research Center of Animal Product, P.O. Box 112, Beijing 100083, China b College of Science, China Agricultural University, Beijing 100083, China

a r t i c l e

i n f o

Article history: Received 7 September 2012 Received in revised form 2 November 2012 Accepted 7 November 2012 Available online 16 November 2012 Keywords: Bighead carp Freezing Biogenic amines Physicochemical property Microbial characteristic

a b s t r a c t The effects of different freezing treatments on the quality changes of bighead carp heads were evaluated in terms of pH value, TBARS, TVB-N, K-value, biogenic amine, total aerobic counts (TACs), drip loss, cooking loss and electrical conductivity (EC) during ice storage. Fish heads were stored at 40 °C (T1), 40 °C for 12 h and then 18 °C (T2), 18 °C (T3) for 3 months prior to ice storage. No significant differences were observed among T1, T2 and T3 for drip loss, cooking loss and EC (p > 0.05). T2 showed lower TACs, pH value, TBARS and TVB-N than T3 did. Significant lower value of spermine and spermidine were observed in T1, T2 and T3 than those of control group (fresh) from 9th to 18th day (p < 0.05). Drip loss was significantly correlated with TBARS, pH value, TVB-N, and TACs in groups T1, T2 and T3 (p < 0.05). Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction Fish is highly susceptible to rapid spoilage at ambient temperature. Thus, to preserve the fish, freezing prior to ice storage is a common practise used in food market to extend the shelf life of aquatic products. However, frozen products can undergo excessive quality loss including water loss, lipid oxidation and undesirable texture and flavour of fish during marketing and production (Ozogul et al., 2011). When some of the water freezes out, the concentration of solutes in unfrozen solutions increases. This may lead to a high degree of freezing denaturation and drip loss (Duun & Rustad, 2007). Many studies have reported useful methods to reduce damage to fish quality during frozen storage. Badii and Howell (2002) investigated the role of antioxidants, citrate and cryoprotectants in minimising protein denaturation in frozen cod fillets. Results indicated that protein denaturation and texture changes were minimised in the presence of cryoprotectants. Boonsumrej, Chaiwanichsiri, Tantratian, Suzuki, and Takai (2007) evaluated the quality changes of tiger shrimp (Penaeus monodon) frozen by air-blast and cryogenic freezing, which indicated that freezing the shrimps under the air-blast freezer gave the least freezing loss and same cutting force as the fresh shrimps. In order to evaluate the quality change of fish during storage, many indices could be employed. TBARS, pH value, TVB-N, K-value, total aerobic ⇑ Corresponding author. Tel./fax: +86 10 62737385. E-mail addresses: [email protected], [email protected] (Y. Luo). 0308-8146/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2012.11.031

counts (TACs), drip loss, and cooking loss are commonly used to determine physiochemical and microbial changes of fish products. As an index of the concentration of electrolytes in the muscle tissues, electrical conductivity (EC) could be used to characterise the texture of fish tissue. Biogenic amines (BAs), including tryptamine (TRM), 2-phenylethylamine (2-PHE), tyramine (TYM), histamine (HIM), putrescine (PUT), cadaverine (CAD), spermine (SPM) and spermidine (SPD), are non-volatile organic bases which occur in protein-rich food during storage (Krˇízˇek, Mateˇjková, Vácha, & Dadáková, 2012). In spoiling fish, BAs are produced from free amino acids liberated from proteins and peptides. Bacterial decarboxylases take part in these processes rather than tissue endogenous enzymes (Ten Brink, Damink, & Joosten, 1990). Bighead carp (Aristichthys nobilis) is one of the main commercial freshwater fish species aquacultured in China and its production in China was 2,551,000 tons in 2010 (Fishery Bureau of Ministry of Agriculture of the People’s Republic of China, 2011). Bighead carp head comprises a relatively high proportion of the whole fish (approximately 34%), especially in comparison with that of crucian carp (Carassius carassius) (approximately 19%), grass carp (Ctenopharyngodon idella) (approximately 16.2%) and common carp (Cyprinus carpio) (approximately 26%). Traditionally, bighead carp is sold whole, which is of relatively low economic value. Bighead carp head, being far more expensive than bighead carp fillets, has good culinary value and is widely used in preparation of soup and famous Chinese dishes owing to its high content of healthy fat and delicious taste. In recent years, the demand from

H. Hong et al. / Food Chemistry 138 (2013) 1476–1482

consumers and restaurants of ready-to-cook bighead carp heads has greatly increased. Although quality control of fish fillets has been extensively studied, very little work has been done on the preservation of freshwater fish heads. In order to evaluate the effects of different freezing treatments on the quality of bighead carp heads and determine whether it is possible to establish an effective freezing method for quality control of bighead carp heads, comparison of the effects of different freezing treatments on the quality of bighead carp heads were studied by evaluating the physiochemical quality and microbial changes as well as determining biogenic amines of heads during storage in ice. 2. Materials and methods 2.1. Sample preparation Cultured bighead carps were purchased from Xiaoyuehe aquatic products wholesale market in Beijing, China, in July, 2011 and were immediately transported to the laboratory alive. The mean weight and length of fish were 1132 ± 84.6 g and 40.2 ± 0.84 cm, respectively. Fish were killed by a blow to the head, scaled, gutted, gilled, and then the heads were chopped off at approximately 5 cm behind the gills. After washing, fish heads were left to drain on a sterile stainless steel wire mesh for 10 min. Then, the heads were packed in polyvinyl chloride bags and were randomly separated into three groups. The first group (T1) was frozen at 40 °C by an ultra-low temperature freezer (model DW-FL270, Zhongke Meiling Co., Ltd., Hefei, China) and kept for up to 3 months. The second group (T2) was frozen at 40 °C in the same way for 12 h and then moved to a freezer at 18 °C and kept for 3 months. The third group (T3) was frozen at 18 °C and kept for up to 3 months. After being stored for 3 months, fish heads were moved to boxes and stored in refrigerated chambers at 4 °C. After that they were surrounded by flake ice at a head-to-ice ratio of 2:1 (w/w). During storage, ice was added to the boxes as required. Control fish heads were obtained from freshly caught bighead carp and then stored in ice. Three lots were taken randomly for analysis at equal intervals. 2.2. Methods 2.2.1. Total aerobic counts (TACs) Determinations of the TACs were according to Hong, Luo, Zhu, and Shen (2012). Ten grams of head meat were aseptically weighed and homogenised with 90 mL sterile 0.9% physiological saline for 1 min. The homogenates and serial 10-fold dilution in sterile 0.9% physiological saline were used for microbial analyses. TACs was performed using enrichment agar, and expressed as log10CFU/g. 2.2.2. Total volatile base nitrogen (TVB-N) The TVB-N content was determined as described by Zhang, Li, Lu, Shen, and Luo (2011) by Kjeldahl distillation mechanism and expressed as mg TVB-N per 100 g muscle. The method was based on water vapour distillation and extraction of volatile base. The distillate was titrated with standard hydrochloric acid. 2.2.3. TBARS The thiobarbituric acid reactive substances (TBARS) were determined according to the method proposed by Erkan and Özden (2008). TBARS values (expressed as milligram malonaldehyde equivalents per kilogram of fish meat) were calculated by multiplying the absorbance readings by a factor of 10.2, which was calculated from a standard curve prepared using 1,1,3,3-tetraethyoxypropane as a precursor of malonaldehyde.

1477

2.2.4. pH value Fish flesh (10 g) was dispersed in 100 ml of distilled water by a lab blender (Jintan Ronghua Instrument Manufacture Co., Changzhou, China) and stirred for 30 min, and then the mixture was filtered. pH value of filtrate was measured using a digital pH meter (FE20/EL20; Mettler Toledo, Shanghai, China). 2.2.5. Drip loss Bighead carp heads were weighed after being drained. The net weight of each head was recorded. After the designated storage period, the heads were taken from polyvinyl chloride bags and left to drain on a stainless steel wire mesh for up to 1 h at 4 °C. Then the heads were blotted with a paper towel and reweighed to determine the drip loss. The drip loss (%) of the heads was expressed as: 100  ((initial weight of head pieces  present weight of head pieces)/initial weight of head pieces). 2.2.6. Cooking loss Cooking loss was determined according to Yu, Li, Xu, and Zhou (2008) with some modifications. 2  2  2 cm3 pieces of head meat prepared for cooking loss measurement were cooked in a boiling water bath to an internal temperature of 85 °C. Samples were weighed before (wb) and after (wa) cooking. After cooking, the samples were cooled to room temperature then blotted dry and reweighed. Cooking loss of the fish flesh cuts was calculated according to the following equation:

Cooking loss % ¼

Wb  Wa  100 Wa

2.2.7. Biogenic amines BAs extraction from the samples was carried out according to the procedures developed by Eerola, Hinkkanen, Lindfors, and Hirvi (1993). Briefly, 5.00 g of each sample were weighed into test tubes and homogenised with 10 ml 0.6 M cold perchloric acid using a FLUKO blender (FLUKO, Shanghai, China) for 1 min. The homogenate was centrifuged at 10,000 rpm for 15 min, and supernatant was filtered into a 25-mL volumetric flask. Extraction was repeated with 10 mL 0.6 M perchloric acid solution, mixed with blender and centrifuged as before. Supernatants were then combined and adjusted to 25 mL with 0.6 M perchloric acid. Sample extract (0.2 mL) was made alkaline by adding 40 lL 2 M NaOH and buffered with 60 lL saturated NaHCO3. 0.4 mL of 10 mg/ ml DNS-Cl solution prepared in acetone were added and the reaction mixture was incubated at 40 °C for 45 min in darkness. Residual DNS-Cl was removed by adding 20 lL 25% ammonia. After 30 min mixture was adjusted to 1.0 mL with acetonitrile, centrifuged at 5000 rpm for 5 min. The supernatant was filtered through 0.22-lm filters prior to HPLC analysis. Quantification of the eight BAs was carried out using reversephase HPLC (Shimadzu LC-10A; Shimadzu, Kyoto, Japan) equipped with a COSMOSIL 5C18-PAQ (4.6  250 mm) column and a multiwavelength UV detector (Shimadzu, LC-10A). Ammonium acetate (0.1 M; solvent A) and acetonitrile (solvent B) were used as mobile phases. Elution was carried out using the following gradient: 0 min, 50% B; 25 min, 90% B; 35 min, 90% B; 45 min, 50% B. BAs were identified on the basis of retention time compared with standard solutions. The flow rate was 0.8 mL/min and the temperature was 30 °C. The sample was detected at 254 nm with an injection volume of 10 lL. 2.2.8. Electrical conductivity (EC) The electrical conductivity of bighead carp head was measured using the method described by Ekanem and Achinewhu (2006) with some modifications. Bighead carp head meat (10 g) was homogenised with 100 ml of distilled water and stirred for

1478

H. Hong et al. / Food Chemistry 138 (2013) 1476–1482

30 min. The mixture was filtered and the EC of filtrate was measured using a digital EC metre (FE20/EL20; Mettler Toledo, Shanghai, China). 2.2.9. K-value The bighead carp samples were pre-treated by the way described by Zhang, Li, et al. (2011). Determinations of ATP-related compounds were carried out by HPLC (Shimadzu, LC-10A) with a COSMOSIL 5C18-PAQ (4.6  250 mm) column and a UV detector (Shimadzu, LC-10A). The mobile phase was 0.05 M phosphate buffer (pH 6.8). The sample (20 lL) was injected at a flow rate of 1 mL/ min and the peaks were detected at 254 nm. The individual amounts of ATP and its related compounds were determined and calculated based on ATP, ADP, AMP, IMP, HxR and Hx standards, which were purchased from Sigma Chemical Co. (St. Louis, MO). The K-value was calculated as follows:

K-value % ¼

ð½HxR þ ½HxÞ  100 ð½ATP þ ½ADP þ ½AMP þ ½IMP þ ½HxR þ ½HxÞ

2.2.10. Statistical analysis All measurements were carried out in triplicate (except microbiological analyses were performed in duplicate). Data were subjected to one-way analysis of variance (ANOVA) using the Compare Means Procedure of SPSS 17.0 (SPSS Inc., Chicago, IL). The least significant difference (LSD) procedure was used to test for difference between means (significance was defined at p < 0.05). Pearson’s regression analysis was performed to determine the correlation between physical, microbial and biochemical quality. 3. Results and discussion 3.1. Changes in total aerobic counts (TACs) Microbiological results are shown in Fig. 1. The initial TACs values of bighead carp heads were 2.2, 2.9, 2.8 and 3.8 log10CFU/ g for control, T1, T2 and T3, respectively, indicating good fish quality. Erkan (2010) reported a similar initial microbial load of vacuum-packaged hot smoked rainbow trout (Oncorhynchus mykiss). TACs increased with storage time for all groups except a minor decline at 12th day for T1, T2 and T3, and 15th day for control. The increase of total visible counts in fish flesh during ice storage has also been demonstrated by Bahmani et al. (2011) for golden gray mullet (Liza aurata). TACs for T1, T2 and T3 were significantly higher than those of control except 12th day of stor-

Fig. 1. Changes in TACs of bighead carp heads treated by different freezing methods during ice storage. Control (fresh), T1 (40 °C for 3 months), T2 (40 °C for 12 h and then 18 °C for 3 months) and T3 (18 °C for 3 months).

age, while T3 was observed to be the highest value (p < 0.05). The significant increase in TACs observed in T1, T2 and T3 samples compared with control can be attributed to possible leakage of internal substances from muscle cell which provided a good medium for microbial growth during frozen storage. According to the proposed limits (7log10CFU/g) for fresh fish by ICMSF (1986), all treatments kept relatively good quality during ice storage as the TACs did not exceed the limit throughout the storage. 3.2. Changes in biochemical quality (pH value, TBARS, TVB-N, K-value and biogenic amines) Fig. 2A shows changes in pH value of the bighead carp heads under different freezing treatments during ice storage of 21 days. The initial pH value in raw bighead carp heads was 7.2. Different freezing treatments did not produce a significant effect on the initial pH value and only a marginal decrease (0.15–0.27) was determined after the treatment process (p > 0.05). Change in pH value of different treatments showed the same trend in which the values decreased initially and then increased. The initial reduction in pH value may be a result of the formation of lactic acid from glycogen in fish meat (Bahmani et al., 2011), whereas, rising pH value later during storage was due to formation of dimethylamine from trimethylamine oxide (Ruiz-Capillas & Moral, 2001). T3 showed a higher pH value than those of control, T1 and T2 after the 12th day, possibly attributed to leakage of intracellular constituents caused by the formation and accretion of ice crystals at 18 °C. At the end of storage, the pH value of all groups reached levels (7.2–8.0) that indicate the production of some alkaline metabolites related with spoilage. Fig. 2B shows TBARS contents in the different treatments during storage. At the beginning of the storage, TBARS values were 0.57, 0.83, 1.1 and 0.65 mg MDA/kg for control, T1, T2 and T3, respectively. TBARS value for T1 increased from 0.83 to 3.3 mg MDA/kg whereas it showed slight fluctuations and kept a comparatively low value in control groups as the storage time increased. After storage for 12 days, significant differences (p < 0.05) were found among control, T1, T2 and T3. Samples previously frozen at 18 °C (T3) showed highest TBARS value in all treatments. Sarkardei and Howell (2008) also reported a sharp increase in this value for horse mackerel (Trachurus trachurus) formulated product during frozen storage at 18 °C. An increase of TBARS concentrations may be due to denaturation of fish muscle during the freezing process. The ice crystals formed during freezing could disrupt cells and release pro-oxidants for lipid oxidation, such as free iron. Levels of 5–8 mg of MDA equivalents per kilogram of flesh are generally regarded as the limit of acceptability for fish stored in ice (Nunes, Batista, & De Campos, 1992). T1, T2 and T3 were all below this limit at which rancid flavours may become evident in fish during storage. This phenomenon might be attributed to the production of other secondary lipid oxidation products from MDA during the 3-month freezing storage. Changes in TVB-N for bighead carp heads are shown in Fig. 2C. The freezing treatments did not produce a significant effect on the initial TVB-N values (8.6, 8.4, 8.3 and 9.1 mg/100 g for control, T1, T2 and T3, respectively). This might be due to limited microorganisms in the fish head at the beginning of storage. TVB-N content increased gradually during storage after a trivial reduction before the 9th day for all treatments. This slight decrease in TVB-N during the first stage of storage may be initiated by degradation of glycogen or production of free amino acids, while the larger increase in TVB-N during the late stage of storage is most likely caused by a combination of microbiological and autolytic activities and the complete microbial reduction of TMAO to TMA (Sallam, Ahmed, Elgazzar, & Eldaly, 2007). TVB-N of T2 and T3 were significantly higher than group T1 and control at the 18th and 21st

1479

H. Hong et al. / Food Chemistry 138 (2013) 1476–1482

Fig. 2. Changes in pH value (A), TBARS (B), TVB-N (C), K-value (D) of bighead carp heads treated by different freezing methods during ice storage. Control (fresh), T1 (40 °C for 3 months), T2 (40 °C for 12 h and then 18 °C for 3 months) and T3 (18 °C for 3 months).

Table 1 Biogenic amines (BAs) concentration (mg/kg) in bighead carp heads treated by different freezing methods during ice storage. BAs

Treatment

Storage days 0

3

6

9

12

15

18

TRM

Control T1 T2 T3

ND 0.85 ± 0.14a 2.0 ± 0.45a ND

1.1 ± 0.71a 0.72 ± 0.011a 2.5 ± 0.61a 1.9 ± 0.58a

2.8 ± 0.79a 0.63 ± 0.094a 0.40 ± 0.067a 1.9 ± 0.22a

0.64 ± 0.36a 0.57 ± 0.079a 2.0 ± 0.55a 2.5 ± 0.51ab

1.3 ± 0.63a 1.2 ± 0.30a 0.79 ± 0.33a 2.2 ± 0.31ab

0.75 ± 0.42a 1.2 ± 0.40ab 0.42 ± 0.012a 1.0 ± 0.19a

2-PHE

Control T1 T2 T3

ND ND 0.65 ± 0.17a ND

0.11 ± 0.040a 1.0 ± 0.30a 0.56 ± 0.11a 0.11 ± 0.023a

0.26 ± 0.077a 0.71 ± 0.044a 0.25 ± 0.0058a 0.078 ± 0.0058a

0.080 ± 0.074a 0.60 ± 0.028a 0.36 ± 0.068a 0.92 ± 0.19a

0.41 ± 0.11a 0.63 ± 0.086a 0.49 ± 0.18a 0.12 ± 0.081a

1.5 ± 0.72ab ND 0.20 ± 0.22a 0.061 ± 0.021a

PUT

Control T1 T2 T3

ND 0.20 ± 0.14a 0.19 ± 0.071a ND

0.027 ± 0.047a 0.28 ± 0.016a 0.10 ± 0.17a 0.16 ± 0.029a

0.10 ± 0.019a 0.095 ± 0.057a 0.098 ± 0.061a 0.10 ± 0.071a

0.13 ± 0.020ab 0.17 ± 0.012abc 3.6 ± 0.81bcd 0.35 ± 0.36abc

1.9 ± 0.032ab 2.7 ± 0.31abc 8.3 ± 0.53bcd 4.1 ± 0.68abc

6.1 ± 1.4bc 2.5 ± 0.49ab 2.9 ± 0.32ab 2.34 ± 0.082ab

CAD

Control T1 T2 T3

0.71 ± 0.28a 0.96 ± 0.044a 1.2 ± 0.35a 0.94 ± 0.32a

1.2 ± 0.72a 1.8 ± 0.41a 1.3 ± 0.77a 2.0 ± 0.21a

0.57 ± 0.021a 1.4 ± 0.67a 1.9 ± 0.51a 2.3 ± 0.091a

1.3 ± 0.61a 1.5 ± 0.17abc 1.7 ± 0.77b 2.0 ± 0.43bc

1.4 ± 0.67a 3.0 ± 1.0abc 2.2 ± 0.18ab 3.3 ± 0.80abc

8.5 ± 1.3c 25.3 ± 9.1f 15.7 ± 2.8e 20.9 ± 2.4e

HIM

Control T1 T2 T3

0.89 ± 0.26a 0.62 ± 0.22a 0.13 ± 0.11a 0.52 ± 0.24a

0.47 ± 0.41a 0.43 ± 0.058a 0.43 ± 0.18a 0.53 ± 0.04a

0.91 ± 0.16a 0.46 ± 0.24a 0.67 ± 0.12a 0.37 ± 0.18a

TYM

Control T1 T2 T3

2.4 ± 0.57a 2.6 ± 1.1a 1.5 ± 0.25a 2.2 ± 0.85a

4.5 ± 1.3a 7.4 ± 1.6a 4.5 ± 0.75a 5.5 ± 0.38a

SPD

Control T1 T2 T3

10.6 ± 5.7b 16.0 ± 6.1b 14.5 ± 1.5b 14.7 ± 3.5b

21.8 ± 4.1b 21.1 ± 1.3b 20.2 ± 1.8b 18.6 ± 0.65b

11.1 ± 2.4b 14.2 ± 0.84c 12.9 ± 2.2c 15.5 ± 2.2c

18.7 ± 2.2e 12.7 ± 0.033abcd 13.8 ± 5.4d 11.9 ± 1.3cd

21.9 ± 2.3e 6.2 ± 1.5abcd 12.0 ± 1.5d 8.9 ± 2.9d

18.5 ± 1.3de 8.7 ± 0.37c 9.4 ± 2.4c 8.4 ± 1.4c

11.1 ± 2.7cd 6.9 ± 1.8abc 8.5 ± 2.0bc 6.1 ± 0.56abc

SPM

Control T1 T2 T3

35.1 ± 8.0c 82.2 ± 8.7e 73.3 ± 6.6d 74.1 ± 2.8d

86.6 ± 9.6c 116 ± 12.1e 103 ± 18.4d 101 ± 4.3d

66.8 ± 14.9d 77.7 ± 0.82e 75.6 ± 10.0e 90.0 ± 11.4f

115 ± 17.2h 70.0 ± 1.2f 74.8 ± 4.3g 65.5 ± 6.1f

127 ± 13.1h 52.1 ± 7.8f 76.1 ± 9.3g 51.3 ± 4.5e

108 ± 1.9i 55.4 ± 0.88h 55.6 ± 3.9h 49.6 ± 1.2g

56.9 ± 16.4h 35.8 ± 8.7g 53.5 ± 3.9h 35.2 ± 3.1g

5.2 ± 0.99a 2.0 ± 0.41ab 1.6 ± 0.16a 3.1 ± 0.83a

0.39 ± 0.11a 0.32 ± 0.032a 0.16 ± 0.054a 0.61 ± 0.54a 3.0 ± 0.71abc 1.7 ± 0.11ab 1.8 ± 0.53ab 2.5 ± 0.11ab

0.48 ± 0.54a 0.42 ± 0.28a 1.3 ± 0.10a 1.3 ± 0.53a 3.0 ± 0.51abc 2.5 ± 0.55ab 2.3 ± 0.88ab 2.3 ± 0.98ab

1.2 ± 0.26e 0.76 ± 0.20e 0.53 ± 0.46e 0.49 ± 0.15e 5.1 ± 2.3abc 2.1 ± 0.048ab 1.8 ± 0.54ab 1.3 ± 0.23ab

5.0 ± 0.69a 1.7 ± 0.16a 0.66 ± 0.14a 1.0 ± 0.45a 3.4 ± 0.010abc ND 0.17 ± 0.073a 0.21 ± 0.0045a 2.2 ± 0.27bc 2.3 ± 0.20ab 3.8 ± 1.7abc 1.52 ± 0.10ab 8.6 ± 1.9c 26.1 ± 10.1e 16.69 ± 1.4c 21.9 ± 1.6e 0.75 ± 0.85ab 0.82 ± 0.45ab 0.36 ± 0.076a 1.4 ± 0.80ab 6.3 ± 1.7abc 1.4 ± 0.28ab 0.84 ± 0.18a 0.43 ± 0.036a

Same superscript lowercase letters in a column indicate no significant differences (p > 0.05) among storage days. TRM tryptamine, 2-PHE 2-phenylethylamine, PUT putrescine, CAD cadaverine, HIM histamine, TYM tyramine, SPD spermidine, SPM spermine; ND, not detected.

1480

H. Hong et al. / Food Chemistry 138 (2013) 1476–1482

days (p < 0.05). This can be explained by the development of large ice crystals by slow freezing, which punctures the cells and increases the amount of water in the extracellular space, providing a good culture medium for microorganisms (Lee, Saha, Xiong, Owens, & Meullenet, 2008). The K-values for bighead carp heads during ice storage are shown in Fig. 2D. The initial K-values of control, T1, T2 and T3 were 5.4%, 23.7%, 28.7% and 37.0%, respectively. According to Saito, Arai, and Matsuyoshi (1959) who depicted fish products with K-values lower than 20% as very fresh, with less than 50% as moderately fresh, and higher than 70% as not fresh, the control was very fresh, while groups T1, T2, and T3 were moderately fresh after 3 months. The K-value of the control group rose continuously and showed a slight decrease at the end of storage, which was in accordance with the report of Kamalakanth et al. (2011) for yellowfin tuna (Thunnus albacare) chunks in ethyl vinyl alcohol films during chill storage. Decreasing trends in K-value were noticed for both groups T1 and T2 after 6 days of storage. This is probably because of decomposition of hypoxanthine and hypoxanthine riboside to smaller molecular substances. It can be concluded from these results that K-value is not always a suitable index to determine the shelf life and deterioration of long-time frozen fish. The concentrations of eight biogenic amines (BAs) present in bighead carp heads are shown in Table 1. SPD and SPM were the two major amines found in fish heads under different freezing treatments. This is because SPD and SPM are natural constituents of living cells (Bardóz, 1995). Öogul and Öden (2011) reported that the most accumulated biogenic amines were PUT, CAD and SPM in sea bream (Sparus aurata) stored in ice. SPD in treated groups shows no significant difference (p > 0.05) from control group at the beginning of storage (0–3 days), and then the observed values were significantly lower (p < 0.05) than those of the control group except for at the 6th day. SPM in T1, T2 and T3 increased sharply at the beginning of storage, and then followed steady declines. SPM reached maximum values at the 3rd day of storage (115, 103 and 102 mg/kg for T1, T2 and T3, respectively). The obtained values for SPM in treated groups are higher than the value found in control within first 6 days while SPM in the control began to exceed the value of treated groups in the range of 9–18 days. SPM concentrations in all samples were lower than that of SPD. HIM, CAD and PUT are significant compounds in fish safety and quality determination, since they can be used as indicators of freshness or microbial spoilage in fish. PUT and CAD observed in the present study were quite low at the early stages of storage. PUT determined in fish heads ranged from 0 to 8 mg/kg, showing no significant difference among different treatments (p > 0.05). The concentration of CAD increased throughout storage, reaching maximum levels of 8.6, 26.1, 16.7 and 21.9 mg/kg in control, T1, T2 and T3 after 18 days of storage, respectively. CAD values of T1, T2 and T3 were significantly higher than the control group (p < 0.05) at the end of storage (15th and 18th day). Rabie, Simon-Sarkadi, Siliha, El-seedy, and El Badawy (2009) reported the decarboxylation of lysine leads to the formation of CAD that has been associated with Enterobacteriaceae. The higher CAD value in treated groups may be a result of accumulated free amino acid after the freezing treatments which could be utilised by Enterobacteriaceae. HIM observed in the present study was much lower, ranging from 0.13 to 1.4 mg/kg, compared with the proposed limit of HIM content (50 mg/kg) for tuna and other fish belonging to the Scombridae and Scomberesocidae families (FDA, 2002), possibly owing to the reduced decarboxylation of amino acids to form HIM in freshwater species. The different freezing treatments exerted no significant effect (p > 0.05) on the concentration of HIM in fish heads throughout the whole storage period. Negligible changes were reported in TRM, 2-PHE and TYM content during storage of bighead carp heads. Similar results were also

determined in Atlantic bonito (Sarda sarda) for 2-PHE (Alak, Hisar, Hisar, & Genççelep, 2011). Freezing treatments have no significant effects on TRM, 2-PHE and TYM content during storage. 3.3. Changes in physical quality (drip loss, cooking loss and EC) Drip loss has been reported to be a good indicator for fish quality evaluation because an increment in drip loss has been shown to result in texture loss. Fig. 3A shows the changes of drip loss of bighead carp heads during ice storage after different freezing treatments. The drip loss for all of the studied groups was significantly increased (p < 0.05) as a function of time, except T2 and T3 which had a slight decrease at the 9th day of the storage. The initial drip losses of T1, T2 and T3 were 2.59%, 3.76% and 2.69%, respectively, which were considerably (p < 0.05) higher than that of the control sample. The results agreed with the study from Einen, Guerin, Fjæra, and Skjervold (2002), who found a higher drip loss in Atlantic salmon pre-rigor fillets at 25 °C compared with fresh fillets. The high drip loss in groups T1, T2 and T3 might be due to longer frozen storage periods, which cause mechanical damage of the tissue through ice crystal formation. Cooking loss generally includes a combination of liquid and soluble matter lost from meat during cooking and the main component is water. The loss of water during cooking is caused by the destruction of structures of muscle cells due to the denaturation of myofibrillar proteins by heat. Fig. 3B shows the cooking losses of bighead carp heads. Cooking losses of group T1, T2 and T3 showed fluctuations before the 12th day of storage. Then the cooking loss increased significantly (p < 0.05) with time to the end of storage. There were no significant differences between different treatments on cooking loss. Measured values of electrical conductivities (EC) in minced bighead carp head meat are shown in Fig. 4. The EC of control samples

Fig. 3. Changes in drip loss (A) and cooking loss (B) of bighead carp heads treated by different freezing methods during ice storage. Control (fresh), T1 (40 °C for 3 months), T2 (40 °C for 12 h and then 18 °C for 3 months) and T3 (18 °C for 3 months).

H. Hong et al. / Food Chemistry 138 (2013) 1476–1482

1481

TBARS, pH value, TVB-N, and TACs of bighead carp heads after freezing (p < 0.05). Although freezing at 40 °C maintained better quality of bighead carp heads than freezing at 40 °C for 12 h and then 18 °C storage did in terms of TACs, TBARS and pH value, it is advantageous to use freezing at 40 °C for 12 h and then 18 °C as for preservation of aquatic food products on an energy-saving basis. Further studies should be conducted to investigate the effects of different freezing treatments on myofibrillar proteins changes in fish muscle. Acknowledgement This study was supported by the earmarked fund for China Agriculture Research System (CARS-46) Fig. 4. Changes in EC of bighead carp heads treated by different freezing methods during ice storage. Control (fresh), T1 (40 °C for 3 months), T2 (40 °C for 12 h and then 18 °C for 3 months) and T3 (18 °C for 3 months).

Table 2 Pearson’s correlations (r) between drip loss and TBARS, pH value, TVB-N, and TACs of bighead carp heads during ice storage. Parameters

TBARS pH value TVB-N TACs * **

Drip loss Control

T1

T2

T3

0.29 0.32 0.77* 0.90**

0.89** 0.97** 0.74* 0.82**

0.96** 0.90** 0.68* 0.86**

0.94** 0.94** 0.82** 0.92**

P < 0.05. P < 0.01.

was significantly higher (p < 0.05) than the values of all treatments (T1, T2 and T3) which showed an inverse relationship with drip loss. Drip possibly removed electrolytes from T1, T2 and T3, reducing EC. Slightly enhanced EC values were observed for T1 and T3 before the 15th day which is a consequence of leaky membrane structures, which allow liquids to move between the intracellular and extracellular spaces. 3.4. Relationship between drip loss and TBARS, pH value, TVB-N, and TACs The correlation coefficients between drip loss and TBARS, pH value, TVB-N, and TACs of bighead carp heads during ice storage are shown in Table 2. Drip loss was significantly correlated with TBARS, pH value, TVB-N, and TACs with high Pearson’s correlations (p < 0.05). However, there were no significant correlations between drip loss and TBARS (r = 0.29), and pH value (r = 0.32) of bighead carp head in the control group, indicating that significant correlations between drip loss and TBARS, and pH value can be only observed in bighead carp heads after freezing treatments. A similar result was reported by Zhang, Shen, and Luo (2011), who showed that the Q-value, a physical index determined as impedance change ratio, was significantly correlated with TACs, K-value, TVB-N, and sensory assessment of grass carp. The Q-value can reflect changes in electrical properties of fish. 4. Conclusions Freezing at 40 °C for 12 h and then 18 °C for 3 months prior to ice storage showed lower TACs, TVB-N, pH value and TBARS in bighead carp heads compared to those frozen directly at 18 °C. Significant correlations were observed between drip loss and

References Alak, G., Hisar, S., Hisar, O., & Genççelep, H. (2011). Biogenic amines formation in Atlantic bonito (Sarda sarda) fillets packaged with modified atmosphere and vacuum, wrapped in chitosan and cling film at 4 °C. European Food Research and Technology, 232(1), 23–28. Badii, F., & Howell, N. K. (2002). Effect of antioxidants, citrate, and cryoprotectants on protein denaturation and texture of frozen cod (Gadus morhua). Journal of Agricultural and Food Chemistry, 50(7), 2053–2061. Bahmani, Z. A., Rezai, M., Hosseini, S. V., Regenstein, J. M., Böhme, K., Alishahi, A., et al. (2011). Chilled storage of golden gray mullet (Liza aurata). LWT – Food Science and Technology, 44(9), 1894–1900. Bardóz, S. (1995). Polyamines in food and their consequences for food quality and human health. Trends in Food Science & Technology, 6(10), 341–346. Boonsumrej, S., Chaiwanichsiri, S., Tantratian, S., Suzuki, T., & Takai, R. (2007). Effects of freezing and thawing on the quality changes of tiger shrimp (Penaeus monodon) frozen by air-blast and cryogenic freezing. Journal of Food Engineering, 80(1), 292–299. Duun, A. S., & Rustad, T. (2007). Quality changes during superchilled storage of cod (Gadus morhua) fillets. Food Chemistry, 105(3), 1067–1075. Eerola, S., Hinkkanen, R., Lindfors, E., & Hirvi, T. (1993). Liquid chromatographic determination of biogenic amines in dry sausages. Journal of AOAC International, 76(3), 575–577. Einen, O., Guerin, T., Fjæra, S. O., & Skjervold, P. O. (2002). Freezing of pre-rigor fillets of Atlantic salmon. Aquaculture, 212(1–4), 129–140. Ekanem, E. O., & Achinewhu, S. C. (2006). Mortality and quality indices of live West African hard-shell clam (Galatea paradoxa born) during wet and dry postharvest storage. Journal of Food Processing and Preservation, 30(3), 247–257. Erkan, N. (2010). The effect of thyme and garlic oil on the preservation of vacuumpackaged hot smoked rainbow trout (Oncorhynchus mykiss). Food and Bioprocess Technology, 5(4), 1246–1254. Erkan, N., & Özden, Ö. (2008). Quality assessment of whole and gutted sardines (Sardina pilchardus) stored in ice. International Journal of Food Science & Technology, 43(9), 1549–1559. FDA (Food and Drug Administration) (2002). Scombrotoxin (histamine) formation, fish and fishery products hazards and controls guide (3rd ed., pp. 73–93). Washington, DC: Department of Health and Human Services, Public Health Service, Food and Drug Administration, Center for Food Safety and Applied Nutrition, Office of Seafood. Fishery Bureau of Ministry of Agriculture of the People’s Republic of China (2011). China fishery statistical yearbook. Beijing, China: China Agriculture Press. in Chinese. Hong, H., Luo, Y., Zhu, S., & Shen, H. (2012). Application of the general stability index method to predict quality deterioration in bighead carp (Aristichthys nobilis) heads during storage at different temperatures. Journal of Food Engineering, 113(4), 554–558. ICMSF (1986). Microorganisms in foods. The international commission on microbiological specifications for foods of the international union of biological societies. Oxford: Blackwell Scientific Publications. Kamalakanth, C. K., Ginson, J., Bindu, J., Venkateswarlu, R., Das, S., Chauhan, O. P., et al. (2011). Effect of high pressure on K-value, microbial and sensory characteristics of yellowfin tuna (Thunnus albacares) chunks in EVOH films during chill storage. Innovative Food Science & Emerging Technologies, 12(4), 451–455. Krˇízˇek, M., Mateˇjková, K., Vácha, F., & Dadáková, E. (2012). Effect of low-dose irradiation on biogenic amines formation in vacuum-packed trout flesh (Oncorhynchus mykiss). Food Chemistry, 132(1), 367–372. Lee, Y. S., Saha, A., Xiong, R., Owens, C. M., & Meullenet, J. F. (2008). Changes in broiler breast fillet tenderness, water-holding capacity, and color attributes during long-term frozen storage. Journal of Food Science, 73(4), E162–E168. Nunes, M. L., Batista, I., & De Campos, R. M. O. (1992). Physical, chemical and sensory analysis of sardine (Sardina pilchardus) stored in ice. Journal of the Science of Food and Agriculture, 59(1), 37–43. Öogul, F., & Öden, Ö. (2011). The Effects of gamma irradiation on the biogenic amine formation in sea bream (Sparus aurata) stored in ice. Food and Bioprocess Technology.

1482

H. Hong et al. / Food Chemistry 138 (2013) 1476–1482

Ozogul, Y., Durmusß, M., Balıkcı, E., Ozogul, F., Ayas, D., & Yazgan, H. (2011). The effects of the combination of freezing and the use of natural antioxidant technology on the quality of frozen sardine fillets (Sardinella aurita). International Journal of Food Science & Technology, 46(2), 236–242. Rabie, M., Simon-Sarkadi, L., Siliha, H., El-seedy, S., & El Badawy, A. (2009). Changes in free amino acids and biogenic amines of Egyptian salted-fermented fish (Feseekh) during ripening and storage. Food Chemistry, 115(2), 635–638. Ruiz-Capillas, C., & Moral, A. (2001). Correlation between biochemical and sensory quality indices in hake stored in ice. Food Research International, 34(5), 441–447. Saito, T., Arai, K., & Matsuyoshi, M. (1959). A new method for estimating the freshness of fish. Bulletin of the Japanese Society of Scientific Fisheries, 24(9), 749–750. Sallam, K. I., Ahmed, A. M., Elgazzar, M. M., & Eldaly, E. A. (2007). Chemical quality and sensory attributes of marinated Pacific saury (Cololabis saira) during vacuum-packaged storage at 4 °C. Food Chemistry, 102(4), 1061–1070.

Sarkardei, S., & Howell, N. K. (2008). Effect of natural antioxidants on stored freezedried food product formulated using horse mackerel (Trachurus trachurus). International Journal of Food Science & Technology, 43(2), 309–315. Ten Brink, B., Damink, C., & Joosten, H. (1990). Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, 11(1), 73–84. Yu, X. L., Li, X. B., Xu, X. L., & Zhou, G. H. (2008). Coating with sodium alginate and its effects on the functional properties and structure of frozen pork. Journal of Muscle Foods, 19(4), 333–351. Zhang, L., Li, X., Lu, W., Shen, H., & Luo, Y. (2011). Quality predictive models of grass carp (Ctenopharyngodon idellus) at different temperatures during storage. Food Control, 22(8), 1197–1202. Zhang, L., Shen, H., & Luo, Y. (2011). A nondestructive method for estimating freshness of freshwater fish. European Food Research and Technology, 232(6), 979–984.