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Rheological properties of fish actomyosin and pork actomyosin solutions
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Journal of Food Engineering 85 (2008) 173–179 www.elsevier.com/locate/jfoodeng
Rheological properties of fish actomyosin and pork actomyosin solutions Ru Liu 1, Si-ming Zhao, Shan-bai Xiong *, Cheng-guang Qiu, Bi-jun Xie College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei Province 430070, PR China Received 5 February 2007; received in revised form 22 June 2007; accepted 27 June 2007 Available online 2 August 2007
Abstract Rheological properties of actomyosin (AM) solutions from silver carp and pork were investigated by means of rotational rheometer, and described by the power law model. AM solution behaved as pseudoplastic fluid under all test conditions (AM concentration: 4– 25 mg/mL; temperature: 5–45 °C; ionic strength: 0–1.0 M; pH: 6.7–12.3). Systems with higher protein concentration exhibited bigger consistency coefficients and smaller flow indexes than those with lower protein concentration. Compared with pork AM solution, consistency coefficient of fish AM solution was higher at corresponding protein concentration, and its increase with respect to AM concentration was more prominent. Consistency coefficient declined with increasing temperature and pH. The Arrhenius model described successfully the temperature dependence of consistency coefficient (p < 0.001). Activation energy of fish AM solution was lower than that of pork AM solution. With increasing ionic strength, consistency coefficient of fish AM solution showed an increasing trend while that of pork AM increased and then decreased. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Actomyosin; Rheological property; Mathematic model
1. Introduction Meat surimi-based product is an important product from animal muscle, which is chopped, further mixed with water, and grinded with some ingredients, such as neutral salt (NaCl) and so on. Then end products are obtained by heating (Fukushima, Okazaki, Fukuda, & Wataba, 2007). During processing, salt-soluble proteins are dissolved by added salt (Sano, Noguchi, Tsuchiya, & Matsumoto, 1988). This is beneficial for protein molecules extending, entangling (Mitchell & Ledward, 1985), and forming viscous sol called meat paste. The sol turns to a viscoelastic gel upon heating. Actomyosin (AM), which is the major constituent of salt-soluble protein from animal *
Corresponding author. Tel./fax: +86 027 87288375. E-mail addresses: [email protected] (R. Liu), [email protected] (S.-m. Zhao), [email protected] (S.-b. Xiong). 1 Tel./fax: +86 027 87288375. 0260-8774/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jfoodeng.2007.06.031
muscle, plays an important role in the texture and processing characteristics of meat products (Benjakul, Visessanguan, Ishizaki, & Tanaka, 2001; Pe´rez-Juan, Flores, & Toldra´, 2007) owing to its rheological properties. Rheological properties are mainly governed by molecular mass, molecular conformation (Mitchell & Ledward, 1985). The factors are influenced by concentration, temperature, pH, ionic strength and so on. With increasing concentration, the hydrodynamic domains of the protein molecules come into contact, and the interactions between the suspended proteins are of paramount importance (Mitchell & Ledward, 1985). Heating decreases viscosity due to the increase in kinetic energy, and the thermal denaturation contributes to the rheology of the protein system (Mitchell & Ledward, 1985). The pH and ionic strength of macromolecular system affect rheological properties by altering the electrostatic charge (Conway & Dobry-Duclaux, 1960). So adjusting the pH and ionic strength is extensively used to improve the taste, process property and shelf life of several products (Fukushima et al., 2007; Wang & Smith, 1995;
174
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
Nomenclature s d K0 T
shear stress, Pa shear rate, s1 frequency factor, Pa sn Celsius temperature, °C
Yongsawatdigul & Park, 2004). There are considerable variations in functional properties of proteins for variable muscles, such as fish (Fukushima et al., 2007; Ni, Nozawa, & Seki, 2001), chicken (Lan et al., 1995) and pork (Westphalen, Briggs, & Lonergan, 2005, 2006). The differences in their functional properties may derive from inherent factors (protein structure, molecular mass, amino acid composition) (Jime´nez Comenero, Careche, Carballo, & Cofrades, 1994; Asghar, Samejima, & Yasui, 1985). The differences can be reflected by measuring their rheological behavior. For these reasons, in order to control the rheological properties of meat products, it is necessary to have a better knowledge of the rheological behavior of AM solution and the influence of protein concentration, temperature, pH and ionic strength. Fish and pork are the major sources of meat products in China. They exhibit significant variations in process property (Choi, Kang, & Lanier, 2004) which may depend on rheological properties of AM solution. However, there is still little information available on the rheological properties of their AM solution. In this work, AM was prepared from fish (silver carp) and pork. The aim was to study the effect of the factors such as AM concentration, temperature, pH or ionic strength (NaCl levels) on rheological properties of fish and pork AM solutions for comparison. It was anticipated to offer theoretical foundation for improving the quality of meat products.
K n Ea R
consistency coefficient, Pa sn flow index, dimensionless activation energy, J/mol universal gas constant, 8.314 J/(mol K)
Na2HPO4–15.5 mM NaH2PO4 buffer (pH 7.5) and placed for approximate 20 h at 4 °C. Then the suspension was centrifuged at 15,000g for 10 min. The supernatant containing myofibrillar protein was filtered through three-layers of gauze to remove the connective tissue and lipid. The filtrate was stirred in 3 L of deionized water to precipitate myofibrillar protein for 30 min, the supernatant was removed from the pellet. Then the precipitate (AM) was collected at 12,000g for 5 min. AM was dissolved in 0.6 M NaCl for further use. Levels of variables were used to analyse the effect of AM concentration (C, mg/mL), temperature, pH and ionic strength (I; NaCl concentration, M). Six levels of AM concentration were employed: 4, 8, 12, 16, 20, 25 mg/mL (I = 0.6 M). Temperature effects were evaluated from 5 to 45 °C in 5 °C intervals. Ionic strength effects were evaluated at 0, 0.2, 0.4, 0.6, 0.8, 1.0 M. Preparations of different pH (between 6.0 and 12.3) were obtained by addition of 1 M HCl or 1 M NaOH. Four parameters were investigated during which when one parameter is varied, the other three were fixed. Their levels used were 5 mg/mL, 5 °C, 0.6 M and pH 6.7, respectively. 2.3. Protein concentration determination
2. Materials and methods
The protein concentration in each fraction was determined by Lowry method (Lowry, Rosebrough, & Randall, 1951) using bovine serum albumin as standard. The values were the means of three measurements.
2.1. Materials
2.4. Rheological properties determination
Pork Longissiumus dorsi muscle and silver carp were purchased from Huazhong Agricultural University market and taken to our laboratory within 30 min. All chemicals used were of analytical grade.
Rheological evaluations were performed using a rotational viscometer (Haake Model RV12, Haake Mess-Technik, Karlsruhe, Germany) equiped with a NVSP rotor (radius of the rotor, Rri, 17.85 mm; Rro, 20.1 mm; height, h, 60 mm; radius of the cylindrical cup, Rci, 17.5 mm; Rco, 20.5 mm). Samples were loaded into the sample cup and allowed to equilibrate for 5 min at 5 °C except for the experiment of temperature influence. Shear stress (s) was measured from the lowest shear rate (5.41 s1) to the highest (692.48 s1). Most measurements were made in duplicate or triplicate on independently prepared protein dispersions. Mean values of the obtained results were calculated as the consistency coefficient (K) and flow index (n) using the power law model (Turker, 1992):
2.2. Sample preparation AM was extracted using a modified method to that described by Ogawa et al. (1999). Fish or pork mince (100 g) was added 400 mL of 3.38 mM Na2HPO4– 15.5 mM NaH2PO4 buffer (pH 7.5) and homogenized for 2 min at <15 °C. The homogenate was centrifuged at 8000g for 5 min. The supernatant containing sarcoplasmic proteins was discarded. The precipitates were washed twice using the same buffer. Subsequently, the pellet was homogenized with 300 mL of 0.45 M NaCl in 3.38 mM
s ¼ Kdn
ð1Þ
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
K ¼ K 0e
Ea RðT þ273:2Þ
ð2Þ
a
4mg/ml 12mg/ml 20mg/ml
80
Shear stress (Pa)
where s is the shear stress, Pa; K is the consistency coefficient, Pa sn; d is the shear rate, s1; n is the flow index, dimensionless. Temperature effects were performed at 5, 10, 15, 20, 25, 30, 35, 40 and 45 °C. In order to quantify the effect of temperature on K of Newtonian or non-Newtonian food products, an Arrhenius model (Eq. (2)) is frequently used (Ve´lez-Ruiz & Barbosa-Ca´novas, 1998):
175 8mg/ml 16mg/ml 25mg/ml
60
40
20
where K is the consistency coefficient, Pa sn; K0 is the frequency factor, Pa sn; Ea is the activation energy, J/mol; T is the Celsius temperature, °C; R is the universal gas constant, 8.314 J/(mol K).
0 0
200
400
600
Shear rate (s-1)
2.5. Data analysis and calculations
b
3. Results and discussion 3.1. Effect of concentration on rheological properties Fig. 1 shows the rheological curves of fish and pork AM solutions under different concentrations (4, 8, 12, 16, 20, 25 mg/mL) for comparison. At low shear rates (0–22 s1), AM solution exhibited nearly a linear shear stress–shear rate behavior indicating macromolecular chain did not show elastoviscous deformation in the region. At middle shear rates (22–173 s1), AM molecules tended to align in a shear field and presented orientations in flow, so internal friction declined gradually during flowing. Shear stress– shear rate curve departed from beeline and bended downwards. At high shear rates (173–692 s1), it exhibited approximate Newtonian fluid behavior again because it was too late for macromolecular to display elastoviscous deformation or full orientation was reached. Higher shear stress values were observed at higher concentrations, and fish AM solution represented higher shear stress values than pork AM solution. The power law model (Eq. (1)) fit well the shear rate and shear stress data (p < 0.001). The parameters (K and n) are shown in Fig. 2. AM solutions from these species exhibited a pseudoplastic fluid behavior, characterized by n less than 1 at all test conditions. An increase in concentration was accompanied with an increase in pseudoplasticity, shown by a decrease in the n values. In very dilute solution, AM behaved as nearly Newtonian fluid. It was possible that AM molecules hardly interact with each other in this concentration range. With increasing protein concentration, fluid of AM was hindered due to the presence of hydrodynamic interactions and association between the protein molecules (Mitchell & Ledward, 1985; Yasßar, Tog˘rul, & Arslan,
4mg/ml 12mg/ml 20mg/ml
80
Shear stress (Pa)
Statistical analysis of the results was performed using Excel and Statistical Analysis System (SAS Institute Inc., Cary, NC, USA). The regression equations were considered significantly at p < 0.05.
8mg/ml 16mg/ml 25mg/ml
60
40
20
0 0
200
400
Shear rate
600
(s-1)
Fig. 1. Rheological curves of actomyosin solutions under different concentrations (T = 5 °C, I = 0.6 M, pH = 6.7): (a) fish AM solutions; (b) pork AM solutions.
2007). This leaded to the decrease in n and the increase in K of AM solutions. As it seen in Fig. 2, K increased from 0.0866 Pa sn to 13.5638 Pa sn when protein concentration rose from 4 mg/mL to 25 mg/mL for fish AM solution, while it increased from 0.0895 Pa sn to 6.5510 Pa sn for pork AM solution in the same concentration range. It indicated the increase in K with respect to fish AM concentration was more prominent compared with pork AM concentration. It was also observed that K of fish AM solution was higher compared to that of pork AM solution at corresponding protein concentration. 3.2. Effect of temperature on rheological properties High temperature (>45 °C) commonly resulted in great aggregates in AM solution (Ko, Yu, & Hsu, 2007). This made it hard to measure its rheological properties using rotational viscometer (Haake). Fig. 3 exhibits the parameters (K and n) under different temperatures (5–45 °C) from
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a
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
a
18
0.5
fish AM fish AM
pork AM
15
pork AM
0.4
K (Pa•sn)
K (Pa•sn)
12
9
6
0.3
0.2
3 0.1
0 0
5
10
15
20
25
30 0
Protein concentration (mg/mL)
b
0
20
30
40
50
Temperature (°C)
0.8
b
0.7
0.9 fish AM pork AM
0.8
0.6
0.5
0.7
n
n
10
0.4 0.6
fish AM
0.3
pork AM
0.5
0.2 0
5
10
15
20
25
30
Protein concentration (mg/mL) Fig. 2. Power-law parameters for actomyosin solutions at different concentrations (T = 5 °C, I = 0.6 M, pH = 6.7): (a) consistency coefficient; (b) flow index.
Eq. (1). Rheological properties of AM solutions were strongly temperature dependent. K decreased with increasing temperature. When external energy is supplied by heating, it increases the energy of the molecules, which, in turn, increases the distance between molecules (Mitchell & Ledward, 1985). So heating reduced K of solution. Additionally, protein structure changes or protein interactions induced by heating may contribute to it (Ko et al., 2007). n of fish AM solution showed an increasing trend with the temperature, but that of pork AM solution showed a slight decreasing trend. It indicated that there was a variation in the effect of temperature (<45 °C) on flow capacity of fish and pork AM solution. The Arrhenius model (Eq. (2)) has been successfully used by many researchers (Herceg & Lelas, 2005; Marcotte, Taherian, Trigui, & Ramaswamy, 2001; Telis-Romero, Thomaz, Bernardi, Telis, & Gabas, 2006) to describe the temperature dependency of rheological parameters. In this study, K of AM solution in relation with temperature
0.4
0
10
20
30
40
50
Temperature (°C)
Fig. 3. Power-law parameters for actomyosin solutions under different temperatures (C = 5 mg/mL, I = 0.6 M, pH = 6.7): (a) consistency coefficient; (b) flow index.
obeyed completely the Arrhenius model (p < 0.001). Activation energy (Ea) obtained from Eq. (2) for pork AM (3.2 104 J/mol) was higher than that for fish AM (1.0 104 J/mol), indicating pork AM molecule was more rigid than fish AM molecule. 3.3. Effect of ionic strength on rheological properties Fig. 4 shows the parameters (K and n) under different ionic strengths (0, 0.2, 0.4, 0.6, 0.8, 1.0 M). As seen in Fig. 4, significantly higher K was found for model system with high ionic strength (I P 0.4 M) compared with that with low ionic strength (I 6 0.2 M). This may be mainly because myofibrillar proteins can only solubilized in high ionic strength (I P 0.3 M) (Foegeding, Lanier, & Hultin, 1996). In high ionic strength solution, AM swelled, unfolded, and became flexible upon absorbing solvent (Sherman, 1979), so n declined. Swelling and unfolding in
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
a
have demonstrated that myosin released upon incubation of carp myofibrils with 1.5–2.0 M KCl, which was the result of the selective detachment of F-actin by salt. It could be presumed that the decrease in K be caused by pork myosin detaching from F-actin in high ionic strength (I P 0.8 M). In contrast, the phenomenon in fish AM might take place at higher ionic strength. Takahashi, Yamamoto, Kato, and Konno (2005) reported that myosin in myofibrils at 1.5 M KCl was still present as an AM complex, although the protective effect of F-actin almost completely disappeared.
0.6
fish AM pork AM
0.5
K (Pa•sn)
0.4
0.3
0.2
3.4. Effect of pH on rheological properties
0.1
0.0 0
0.2
0.4
0.6
0.8
1
Ionic strength (M)
b
177
Addition of HCl leaded to turbidity and moreover great sediment in AM solutions. In acidic solution, near to the isoelectric point (5.4–5.6), AM tended to form
0.9
fish AM pork AM
a
0.8
0.5
0.4
K (Pa•sn)
n
0.7
0.6
0.3
0.2
0.5
fish AM pork AM
0.1
0.4 0
0.2
0.4
0.6
0.8
1
Ionic strength (M)
0.0 6.5
7.5
8.5
Fig. 4. Power-law parameters for actomyosin solutions under different ionic strengths (T = 5 °C, C = 5 mg/mL, pH = 6.7): (a) consistency coefficient; (b) flow index.
9.5
10.5
11.5
12.5
pH
b
1. 0
fish AM pork AM 0. 9
0. 8
n
turn increased the effective volume or hydrodynamic volume, shortened the distance between the protein molecules. Swelling, unfolding, and flexibility of protein also might increase the axial ratio or axis of rotation (Sherman, 1979), and these could cause the increase in friction force between molecules leading to K increasing. For fish AM solution, increasing ionic strength caused an increase in K and decrease in n. For pork AM solution, K showed an increasing trend up to ionic strength 0.8 M followed by a decrease. The result was similar to that of Cofrades, Carechc, Carballo, and Jime´nez Comenero (1993) who reported that viscosity decreased with higher ionic strength in both chicken and hacke AM. This was possibly due to the fact that an increase in salt concentration was accompanied by an increase in number of AM monomers, so that the smaller molecules resulted in smaller K values (Ogawa et al., 1999). Wakameda and Arai (1986)
0. 7
0. 6
0. 5 6.5
7.5
8.5
9.5
10.5
11.5
12.5
pH Fig. 5. Power-law parameters for actomyosin solutions under different pH (T = 5 °C, C = 5 mg/mL, I = 0.6 M): (a) consistency coefficient; (b) flow index.
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aggregates which include the core not accessible for maximum hydration leading to the unstable state. It was hard to measure its rheological properties using rotational viscometer (Haake). Fig. 5 illustrates the parameters (K and n) at pH 6.7–12.3. K decreased followed by a plateau with increasing pH. n showed an increasing trend up to pH 11.4 followed by a decrease. This may be explained by increase in number of AM monomers or degradation of protein molecules into smaller subunits at the alkaline pH. However, the results were not in good agreement with Cofrades et al. (1993) who reported that a raise in pH increased viscosity of AM from chicken breast, pork L. dorsi muscles and hacke muscles. The reason for it might be the different indexes used. AM solution behaved as non-Newtonian fluid. Its rheological properties are generally strongly shear rate dependent. In other words, it exhibited different rheological behaviors in different shear regions. Apparent viscosity was measured at a special shear rate, while K was obtained by measuring rheological behavior in a wide range of shear rates. 4. Conclusions AM solution behaved as pseudoplastic fluid under all test conditions. Systems with higher protein concentration exhibited bigger K and smaller n than those with lower protein concentration. Compared with pork AM solution, K of fish AM solution was higher at corresponding protein concentration, and its increase with respect to AM concentration was more prominent. K declined with increasing temperature. The correlation between K and temperature was described completely by the Arrhenius equation (p < 0.001). Ea of fish AM was lower than that of pork AM. K at higher ionic strengths (I = 0.4–1.0 M) were higher significantly than them at lower ionic strengths (I = 0–0.2 M). With ionic strength increasing, K of fish AM solution showed an increasing trend while that of pork AM showed increased and then decreased. K of fish and pork AM solutions decreased followed by a plateau with increasing pH. Acknowledgments This research is funded by ‘‘National Key Technology R&D Program in Eleventh-Five-Year Plan”. The accession number is 2006BAD05A18. References Asghar, A., Samejima, K., & Yasui, T. (1985). Functionality of muscle proteins in gelation mechanisms of structured meat products. CRC Critical Reviews in Food Science and Nutrition, 22(1), 27–106. Benjakul, S., Visessanguan, W., Ishizaki, S., & Tanaka, M. (2001). Differences in gelation characteristics of natural actomyosin from two species of bigeye snapper, Priacanthus tayenus and Priacanthus macracanthus. Journal of Food Science, 66(9), 1311–1318.
Choi, Y. J., Kang, I. S., & Lanier, T. C. (2004). Proteolytic enzymes and control in surimi. In J. W. Park (Ed.), Surimi and surimi seafood (2nd ed., pp. 229). New York: Marcel Dekker, Inc.. Cofrades, S., Carechc, M., Carballo, J., & Jime´nez Comenero, C. F. (1993). Protein concentration, pH and ionic strength affect apparent viscosity of actomyosin. Journal of Food Science, 58, 1269–1272. Conway, B. E., & Dobry-Duclaux, A. (1960). In F. Eirich (Ed.). Rheology (Vol. III). London: Academic Press. Foegeding, E. A., Lanier, T. C., & Hultin, H. O. (1996). Characteristics of edible muscle tissue. In O. R. Fennema (Ed.), Food chemistry (pp. 879–942). New York: Marcel Dekker, Inc.. Fukushima, H., Okazaki, E., Fukuda, Y., & Wataba, S. (2007). Rheological properties of selected fish paste at selected temperature pertaining to shaping of surimi-based products. Journal of Food Engineering, 81, 492–499. Herceg, Z., & Lelas, V. (2005). The influence of temperature and solid matter content on the viscosity of whey protein concentrates and skim milk powder before and after tribomechanical treatment. Journal of Food Engineering, 66, 433–438. Jime´nez Comenero, F., Careche, M., Carballo, J., & Cofrades, S. (1994). Influence of thermal treatment on gelation of actomyosin from different myosystems. Journal of Food Science, 59, 211–215. Ko, W. C., Yu, C. C., & Hsu, K. C. (2007). Changes in conformation and sulfhydryl groups of tilapia actomyosin by thermal treatment. LWT – Food Science and Technology, 40(8), 1316–1320. Lan, Y. H., Novakofski, J., McCusker, R. H., Brewer, M. S., Carr, T. R., & McKeith, F. K. (1995). Thermal gelation of myofibrils from pork, beef, fish, chicken and turkey. Journal of Food Science, 60, 941–945. Lowry, O. H., Rosebrough, N. J., & Randall, R. J. (1951). Protein measurement with Folin phenol reagent. Joural of Biological Chemistry, 193, 256–275. Marcotte, M., Taherian, A. R., Trigui, M., & Ramaswamy, H. S. (2001). Evaluation of rheological characteristics of salt-enriched hydrocolloids in the context of ohmic heating. Journal of Food Engineering, 48(2), 157–167. Mitchell, J. R., & Ledward, D. A. (1985). Functional properties of food macromolecules. London and New York: Elsevier Applied Science Publishers (pp. 64–117). Ni, S., Nozawa, H., & Seki, N. (2001). Effect of pH on the gelation of walleye pollack surimi and carp actomyosin pastes. Fisheries Science, 67, 920–927. Ogawa, M., Nakamura, S., Horimoto, Y., An, H., Tsuchiya, T., & Nakai, S. (1999). Raman spectroscopic study of changes in fish actomyosin during setting. Journal of Agricultural and Food Chemistry, 47, 3309–3318. Pe´rez-Juan, M., Flores, M., & Toldra´, F. (2007). Simultaneous process to isolate actomyosin and actin from post-rigor porcine skeletal muscle. Food Chemistry, 101, 1005–1011. Sano, T., Noguchi, S. F., Tsuchiya, T., & Matsumoto, J. J. (1988). Dynamic viscoelastic behavior of natural actomyosin and myosin during thermal gelation. Journal of Food Science, 53, 924–928. Sherman, P. (1979). Food texture and rheology. London: Academic Press. Takahashi, M., Yamamoto, T., Kato, S., & Konno, K. (2005). Comparative study on thermal denaturation modes of myosin in walleye pollack and carp myofibrils as affected by salt concentration. Fisheries Science, 71, 662–671. Telis-Romero, J., Thomaz, C. E. P., Bernardi, M., Telis, V. R. N., & Gabas, A. L. (2006). Rheological properties and fluid dynamics of egg yolk. Journal of Food Engineering, 74, 191–197. Turker, G. S. (1992). Determining the rhelogical properties of liquid foods containing particulate material during continuous processing. Technical Memorandum 668 (Campden & Choreleywood Food Research Association, Chipping Campden, Glos, GL55 6LD, UK). Ve´lez-Ruiz, J. F., & Barbosa-Ca´novas, G. V. (1998). Rheological properties of concentrated milk as function of concentration, temperature and storage time. Journal of Food Engineering, 35, 177–190.
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179 Wakameda, A., & Arai, K. (1986). Dissociation of carp myosin B into actin and myosin in the presence of a high concentration of NaCl. Nippon Suisan Gakkaishi, 52, 293–300. Wang, S. F., & Smith, D. M. (1995). Gelation of chicken breast muscle actomyosin as influenced by weight ratio of actin to myosin. Journal of Agricultural and Food Chemistry, 43, 331–336. Westphalen, A. D., Briggs, J. L., & Lonergan, S. M. (2005). Influence of pH on rheological properties of porcine myofibrillar protein during heat induced gelation. Meat Science, 70, 293–299.
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Journal of Food Engineering 85 (2008) 173–179 www.elsevier.com/locate/jfoodeng
Rheological properties of fish actomyosin and pork actomyosin solutions Ru Liu 1, Si-ming Zhao, Shan-bai Xiong *, Cheng-guang Qiu, Bi-jun Xie College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei Province 430070, PR China Received 5 February 2007; received in revised form 22 June 2007; accepted 27 June 2007 Available online 2 August 2007
Abstract Rheological properties of actomyosin (AM) solutions from silver carp and pork were investigated by means of rotational rheometer, and described by the power law model. AM solution behaved as pseudoplastic fluid under all test conditions (AM concentration: 4– 25 mg/mL; temperature: 5–45 °C; ionic strength: 0–1.0 M; pH: 6.7–12.3). Systems with higher protein concentration exhibited bigger consistency coefficients and smaller flow indexes than those with lower protein concentration. Compared with pork AM solution, consistency coefficient of fish AM solution was higher at corresponding protein concentration, and its increase with respect to AM concentration was more prominent. Consistency coefficient declined with increasing temperature and pH. The Arrhenius model described successfully the temperature dependence of consistency coefficient (p < 0.001). Activation energy of fish AM solution was lower than that of pork AM solution. With increasing ionic strength, consistency coefficient of fish AM solution showed an increasing trend while that of pork AM increased and then decreased. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Actomyosin; Rheological property; Mathematic model
1. Introduction Meat surimi-based product is an important product from animal muscle, which is chopped, further mixed with water, and grinded with some ingredients, such as neutral salt (NaCl) and so on. Then end products are obtained by heating (Fukushima, Okazaki, Fukuda, & Wataba, 2007). During processing, salt-soluble proteins are dissolved by added salt (Sano, Noguchi, Tsuchiya, & Matsumoto, 1988). This is beneficial for protein molecules extending, entangling (Mitchell & Ledward, 1985), and forming viscous sol called meat paste. The sol turns to a viscoelastic gel upon heating. Actomyosin (AM), which is the major constituent of salt-soluble protein from animal *
Corresponding author. Tel./fax: +86 027 87288375. E-mail addresses: [email protected] (R. Liu), [email protected] (S.-m. Zhao), [email protected] (S.-b. Xiong). 1 Tel./fax: +86 027 87288375. 0260-8774/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jfoodeng.2007.06.031
muscle, plays an important role in the texture and processing characteristics of meat products (Benjakul, Visessanguan, Ishizaki, & Tanaka, 2001; Pe´rez-Juan, Flores, & Toldra´, 2007) owing to its rheological properties. Rheological properties are mainly governed by molecular mass, molecular conformation (Mitchell & Ledward, 1985). The factors are influenced by concentration, temperature, pH, ionic strength and so on. With increasing concentration, the hydrodynamic domains of the protein molecules come into contact, and the interactions between the suspended proteins are of paramount importance (Mitchell & Ledward, 1985). Heating decreases viscosity due to the increase in kinetic energy, and the thermal denaturation contributes to the rheology of the protein system (Mitchell & Ledward, 1985). The pH and ionic strength of macromolecular system affect rheological properties by altering the electrostatic charge (Conway & Dobry-Duclaux, 1960). So adjusting the pH and ionic strength is extensively used to improve the taste, process property and shelf life of several products (Fukushima et al., 2007; Wang & Smith, 1995;
174
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
Nomenclature s d K0 T
shear stress, Pa shear rate, s1 frequency factor, Pa sn Celsius temperature, °C
Yongsawatdigul & Park, 2004). There are considerable variations in functional properties of proteins for variable muscles, such as fish (Fukushima et al., 2007; Ni, Nozawa, & Seki, 2001), chicken (Lan et al., 1995) and pork (Westphalen, Briggs, & Lonergan, 2005, 2006). The differences in their functional properties may derive from inherent factors (protein structure, molecular mass, amino acid composition) (Jime´nez Comenero, Careche, Carballo, & Cofrades, 1994; Asghar, Samejima, & Yasui, 1985). The differences can be reflected by measuring their rheological behavior. For these reasons, in order to control the rheological properties of meat products, it is necessary to have a better knowledge of the rheological behavior of AM solution and the influence of protein concentration, temperature, pH and ionic strength. Fish and pork are the major sources of meat products in China. They exhibit significant variations in process property (Choi, Kang, & Lanier, 2004) which may depend on rheological properties of AM solution. However, there is still little information available on the rheological properties of their AM solution. In this work, AM was prepared from fish (silver carp) and pork. The aim was to study the effect of the factors such as AM concentration, temperature, pH or ionic strength (NaCl levels) on rheological properties of fish and pork AM solutions for comparison. It was anticipated to offer theoretical foundation for improving the quality of meat products.
K n Ea R
consistency coefficient, Pa sn flow index, dimensionless activation energy, J/mol universal gas constant, 8.314 J/(mol K)
Na2HPO4–15.5 mM NaH2PO4 buffer (pH 7.5) and placed for approximate 20 h at 4 °C. Then the suspension was centrifuged at 15,000g for 10 min. The supernatant containing myofibrillar protein was filtered through three-layers of gauze to remove the connective tissue and lipid. The filtrate was stirred in 3 L of deionized water to precipitate myofibrillar protein for 30 min, the supernatant was removed from the pellet. Then the precipitate (AM) was collected at 12,000g for 5 min. AM was dissolved in 0.6 M NaCl for further use. Levels of variables were used to analyse the effect of AM concentration (C, mg/mL), temperature, pH and ionic strength (I; NaCl concentration, M). Six levels of AM concentration were employed: 4, 8, 12, 16, 20, 25 mg/mL (I = 0.6 M). Temperature effects were evaluated from 5 to 45 °C in 5 °C intervals. Ionic strength effects were evaluated at 0, 0.2, 0.4, 0.6, 0.8, 1.0 M. Preparations of different pH (between 6.0 and 12.3) were obtained by addition of 1 M HCl or 1 M NaOH. Four parameters were investigated during which when one parameter is varied, the other three were fixed. Their levels used were 5 mg/mL, 5 °C, 0.6 M and pH 6.7, respectively. 2.3. Protein concentration determination
2. Materials and methods
The protein concentration in each fraction was determined by Lowry method (Lowry, Rosebrough, & Randall, 1951) using bovine serum albumin as standard. The values were the means of three measurements.
2.1. Materials
2.4. Rheological properties determination
Pork Longissiumus dorsi muscle and silver carp were purchased from Huazhong Agricultural University market and taken to our laboratory within 30 min. All chemicals used were of analytical grade.
Rheological evaluations were performed using a rotational viscometer (Haake Model RV12, Haake Mess-Technik, Karlsruhe, Germany) equiped with a NVSP rotor (radius of the rotor, Rri, 17.85 mm; Rro, 20.1 mm; height, h, 60 mm; radius of the cylindrical cup, Rci, 17.5 mm; Rco, 20.5 mm). Samples were loaded into the sample cup and allowed to equilibrate for 5 min at 5 °C except for the experiment of temperature influence. Shear stress (s) was measured from the lowest shear rate (5.41 s1) to the highest (692.48 s1). Most measurements were made in duplicate or triplicate on independently prepared protein dispersions. Mean values of the obtained results were calculated as the consistency coefficient (K) and flow index (n) using the power law model (Turker, 1992):
2.2. Sample preparation AM was extracted using a modified method to that described by Ogawa et al. (1999). Fish or pork mince (100 g) was added 400 mL of 3.38 mM Na2HPO4– 15.5 mM NaH2PO4 buffer (pH 7.5) and homogenized for 2 min at <15 °C. The homogenate was centrifuged at 8000g for 5 min. The supernatant containing sarcoplasmic proteins was discarded. The precipitates were washed twice using the same buffer. Subsequently, the pellet was homogenized with 300 mL of 0.45 M NaCl in 3.38 mM
s ¼ Kdn
ð1Þ
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
K ¼ K 0e
Ea RðT þ273:2Þ
ð2Þ
a
4mg/ml 12mg/ml 20mg/ml
80
Shear stress (Pa)
where s is the shear stress, Pa; K is the consistency coefficient, Pa sn; d is the shear rate, s1; n is the flow index, dimensionless. Temperature effects were performed at 5, 10, 15, 20, 25, 30, 35, 40 and 45 °C. In order to quantify the effect of temperature on K of Newtonian or non-Newtonian food products, an Arrhenius model (Eq. (2)) is frequently used (Ve´lez-Ruiz & Barbosa-Ca´novas, 1998):
175 8mg/ml 16mg/ml 25mg/ml
60
40
20
where K is the consistency coefficient, Pa sn; K0 is the frequency factor, Pa sn; Ea is the activation energy, J/mol; T is the Celsius temperature, °C; R is the universal gas constant, 8.314 J/(mol K).
0 0
200
400
600
Shear rate (s-1)
2.5. Data analysis and calculations
b
3. Results and discussion 3.1. Effect of concentration on rheological properties Fig. 1 shows the rheological curves of fish and pork AM solutions under different concentrations (4, 8, 12, 16, 20, 25 mg/mL) for comparison. At low shear rates (0–22 s1), AM solution exhibited nearly a linear shear stress–shear rate behavior indicating macromolecular chain did not show elastoviscous deformation in the region. At middle shear rates (22–173 s1), AM molecules tended to align in a shear field and presented orientations in flow, so internal friction declined gradually during flowing. Shear stress– shear rate curve departed from beeline and bended downwards. At high shear rates (173–692 s1), it exhibited approximate Newtonian fluid behavior again because it was too late for macromolecular to display elastoviscous deformation or full orientation was reached. Higher shear stress values were observed at higher concentrations, and fish AM solution represented higher shear stress values than pork AM solution. The power law model (Eq. (1)) fit well the shear rate and shear stress data (p < 0.001). The parameters (K and n) are shown in Fig. 2. AM solutions from these species exhibited a pseudoplastic fluid behavior, characterized by n less than 1 at all test conditions. An increase in concentration was accompanied with an increase in pseudoplasticity, shown by a decrease in the n values. In very dilute solution, AM behaved as nearly Newtonian fluid. It was possible that AM molecules hardly interact with each other in this concentration range. With increasing protein concentration, fluid of AM was hindered due to the presence of hydrodynamic interactions and association between the protein molecules (Mitchell & Ledward, 1985; Yasßar, Tog˘rul, & Arslan,
4mg/ml 12mg/ml 20mg/ml
80
Shear stress (Pa)
Statistical analysis of the results was performed using Excel and Statistical Analysis System (SAS Institute Inc., Cary, NC, USA). The regression equations were considered significantly at p < 0.05.
8mg/ml 16mg/ml 25mg/ml
60
40
20
0 0
200
400
Shear rate
600
(s-1)
Fig. 1. Rheological curves of actomyosin solutions under different concentrations (T = 5 °C, I = 0.6 M, pH = 6.7): (a) fish AM solutions; (b) pork AM solutions.
2007). This leaded to the decrease in n and the increase in K of AM solutions. As it seen in Fig. 2, K increased from 0.0866 Pa sn to 13.5638 Pa sn when protein concentration rose from 4 mg/mL to 25 mg/mL for fish AM solution, while it increased from 0.0895 Pa sn to 6.5510 Pa sn for pork AM solution in the same concentration range. It indicated the increase in K with respect to fish AM concentration was more prominent compared with pork AM concentration. It was also observed that K of fish AM solution was higher compared to that of pork AM solution at corresponding protein concentration. 3.2. Effect of temperature on rheological properties High temperature (>45 °C) commonly resulted in great aggregates in AM solution (Ko, Yu, & Hsu, 2007). This made it hard to measure its rheological properties using rotational viscometer (Haake). Fig. 3 exhibits the parameters (K and n) under different temperatures (5–45 °C) from
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a
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a
18
0.5
fish AM fish AM
pork AM
15
pork AM
0.4
K (Pa•sn)
K (Pa•sn)
12
9
6
0.3
0.2
3 0.1
0 0
5
10
15
20
25
30 0
Protein concentration (mg/mL)
b
0
20
30
40
50
Temperature (°C)
0.8
b
0.7
0.9 fish AM pork AM
0.8
0.6
0.5
0.7
n
n
10
0.4 0.6
fish AM
0.3
pork AM
0.5
0.2 0
5
10
15
20
25
30
Protein concentration (mg/mL) Fig. 2. Power-law parameters for actomyosin solutions at different concentrations (T = 5 °C, I = 0.6 M, pH = 6.7): (a) consistency coefficient; (b) flow index.
Eq. (1). Rheological properties of AM solutions were strongly temperature dependent. K decreased with increasing temperature. When external energy is supplied by heating, it increases the energy of the molecules, which, in turn, increases the distance between molecules (Mitchell & Ledward, 1985). So heating reduced K of solution. Additionally, protein structure changes or protein interactions induced by heating may contribute to it (Ko et al., 2007). n of fish AM solution showed an increasing trend with the temperature, but that of pork AM solution showed a slight decreasing trend. It indicated that there was a variation in the effect of temperature (<45 °C) on flow capacity of fish and pork AM solution. The Arrhenius model (Eq. (2)) has been successfully used by many researchers (Herceg & Lelas, 2005; Marcotte, Taherian, Trigui, & Ramaswamy, 2001; Telis-Romero, Thomaz, Bernardi, Telis, & Gabas, 2006) to describe the temperature dependency of rheological parameters. In this study, K of AM solution in relation with temperature
0.4
0
10
20
30
40
50
Temperature (°C)
Fig. 3. Power-law parameters for actomyosin solutions under different temperatures (C = 5 mg/mL, I = 0.6 M, pH = 6.7): (a) consistency coefficient; (b) flow index.
obeyed completely the Arrhenius model (p < 0.001). Activation energy (Ea) obtained from Eq. (2) for pork AM (3.2 104 J/mol) was higher than that for fish AM (1.0 104 J/mol), indicating pork AM molecule was more rigid than fish AM molecule. 3.3. Effect of ionic strength on rheological properties Fig. 4 shows the parameters (K and n) under different ionic strengths (0, 0.2, 0.4, 0.6, 0.8, 1.0 M). As seen in Fig. 4, significantly higher K was found for model system with high ionic strength (I P 0.4 M) compared with that with low ionic strength (I 6 0.2 M). This may be mainly because myofibrillar proteins can only solubilized in high ionic strength (I P 0.3 M) (Foegeding, Lanier, & Hultin, 1996). In high ionic strength solution, AM swelled, unfolded, and became flexible upon absorbing solvent (Sherman, 1979), so n declined. Swelling and unfolding in
R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
a
have demonstrated that myosin released upon incubation of carp myofibrils with 1.5–2.0 M KCl, which was the result of the selective detachment of F-actin by salt. It could be presumed that the decrease in K be caused by pork myosin detaching from F-actin in high ionic strength (I P 0.8 M). In contrast, the phenomenon in fish AM might take place at higher ionic strength. Takahashi, Yamamoto, Kato, and Konno (2005) reported that myosin in myofibrils at 1.5 M KCl was still present as an AM complex, although the protective effect of F-actin almost completely disappeared.
0.6
fish AM pork AM
0.5
K (Pa•sn)
0.4
0.3
0.2
3.4. Effect of pH on rheological properties
0.1
0.0 0
0.2
0.4
0.6
0.8
1
Ionic strength (M)
b
177
Addition of HCl leaded to turbidity and moreover great sediment in AM solutions. In acidic solution, near to the isoelectric point (5.4–5.6), AM tended to form
0.9
fish AM pork AM
a
0.8
0.5
0.4
K (Pa•sn)
n
0.7
0.6
0.3
0.2
0.5
fish AM pork AM
0.1
0.4 0
0.2
0.4
0.6
0.8
1
Ionic strength (M)
0.0 6.5
7.5
8.5
Fig. 4. Power-law parameters for actomyosin solutions under different ionic strengths (T = 5 °C, C = 5 mg/mL, pH = 6.7): (a) consistency coefficient; (b) flow index.
9.5
10.5
11.5
12.5
pH
b
1. 0
fish AM pork AM 0. 9
0. 8
n
turn increased the effective volume or hydrodynamic volume, shortened the distance between the protein molecules. Swelling, unfolding, and flexibility of protein also might increase the axial ratio or axis of rotation (Sherman, 1979), and these could cause the increase in friction force between molecules leading to K increasing. For fish AM solution, increasing ionic strength caused an increase in K and decrease in n. For pork AM solution, K showed an increasing trend up to ionic strength 0.8 M followed by a decrease. The result was similar to that of Cofrades, Carechc, Carballo, and Jime´nez Comenero (1993) who reported that viscosity decreased with higher ionic strength in both chicken and hacke AM. This was possibly due to the fact that an increase in salt concentration was accompanied by an increase in number of AM monomers, so that the smaller molecules resulted in smaller K values (Ogawa et al., 1999). Wakameda and Arai (1986)
0. 7
0. 6
0. 5 6.5
7.5
8.5
9.5
10.5
11.5
12.5
pH Fig. 5. Power-law parameters for actomyosin solutions under different pH (T = 5 °C, C = 5 mg/mL, I = 0.6 M): (a) consistency coefficient; (b) flow index.
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R. Liu et al. / Journal of Food Engineering 85 (2008) 173–179
aggregates which include the core not accessible for maximum hydration leading to the unstable state. It was hard to measure its rheological properties using rotational viscometer (Haake). Fig. 5 illustrates the parameters (K and n) at pH 6.7–12.3. K decreased followed by a plateau with increasing pH. n showed an increasing trend up to pH 11.4 followed by a decrease. This may be explained by increase in number of AM monomers or degradation of protein molecules into smaller subunits at the alkaline pH. However, the results were not in good agreement with Cofrades et al. (1993) who reported that a raise in pH increased viscosity of AM from chicken breast, pork L. dorsi muscles and hacke muscles. The reason for it might be the different indexes used. AM solution behaved as non-Newtonian fluid. Its rheological properties are generally strongly shear rate dependent. In other words, it exhibited different rheological behaviors in different shear regions. Apparent viscosity was measured at a special shear rate, while K was obtained by measuring rheological behavior in a wide range of shear rates. 4. Conclusions AM solution behaved as pseudoplastic fluid under all test conditions. Systems with higher protein concentration exhibited bigger K and smaller n than those with lower protein concentration. Compared with pork AM solution, K of fish AM solution was higher at corresponding protein concentration, and its increase with respect to AM concentration was more prominent. K declined with increasing temperature. The correlation between K and temperature was described completely by the Arrhenius equation (p < 0.001). Ea of fish AM was lower than that of pork AM. K at higher ionic strengths (I = 0.4–1.0 M) were higher significantly than them at lower ionic strengths (I = 0–0.2 M). With ionic strength increasing, K of fish AM solution showed an increasing trend while that of pork AM showed increased and then decreased. K of fish and pork AM solutions decreased followed by a plateau with increasing pH. Acknowledgments This research is funded by ‘‘National Key Technology R&D Program in Eleventh-Five-Year Plan”. The accession number is 2006BAD05A18. References Asghar, A., Samejima, K., & Yasui, T. (1985). Functionality of muscle proteins in gelation mechanisms of structured meat products. CRC Critical Reviews in Food Science and Nutrition, 22(1), 27–106. Benjakul, S., Visessanguan, W., Ishizaki, S., & Tanaka, M. (2001). Differences in gelation characteristics of natural actomyosin from two species of bigeye snapper, Priacanthus tayenus and Priacanthus macracanthus. Journal of Food Science, 66(9), 1311–1318.
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