Occurrence and Development of Off-Odor Compounds in Farmed Hybrid Catfish (Clarias macrocephalus × Clarias gariepinus) Muscle during Refrigerated Storage: Chemical and Volatilomic Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fish Samples
2.2. Determination of Moisture, pH, and Trichloroacetic Acid (TCA)-Soluble Peptide Contents
2.3. Measurement of FFA Content
2.4. Determination of TVB-N and TMA Contents
2.5. Measurement of Heme and Non-Heme Iron Contents
2.6. Measurement of PV and TBARS
2.7. Determination of Geosmin, 2-MIB, and Volatile Lipid Oxidation Products
2.8. Off-Odor Evaluation
2.9. Statistical Analysis
3. Results and Discussion
3.1. Changes in Moisture Content
3.2. Changes in pH
3.3. Changes in TCA-Soluble Peptide and FFA Contents
3.4. Changes in TVB-N and TMA Contents
3.5. Changes in Heme Iron and Non-Heme Iron Contents
3.6. Changes in PV and TBARS
3.7. Changes in Geosmin and 2-MIB Contents
3.8. Changes in Lipid Oxidation-Derived Volatile Compounds
3.9. Changes in Sensory Scores
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Department of Fisheries. Fisheries Statistics of Thailand; Fishery Statistics Analysis and Research Group, Fisheries Development Policy and Strategy Division, Department of Fisheries: Bangkok, Thailand, 2020. [Google Scholar]
- Casallas, N.E.C.; Casallas, P.E.C.; Mahecha, H.S. Characterization of the nutritional quality of the meat in some species of catfish: A review. Rev. Fac. Nac. Agron. Medellín 2012, 65, 6799–6809. [Google Scholar]
- Jantrarotai, W.; Sitasit, P.; Jantrarotai, P.; Viputhanumas, T.; Srabua, P. Protein and energy levels for maximum growth, diet utilization, yield of edible flesh and protein sparing of hybrid Clarias catfish (Clarias macrocephalus × Clarias gariepinus). J. World. Aquac. Soc. 1998, 29, 281–289. [Google Scholar] [CrossRef]
- Panpipat, W.; Yongsawatdigul, J. Stability of potassium iodide and omega-3 fatty acids in fortified freshwater fish emulsion sausage. LWT Food Sci. Technol. 2008, 41, 483–492. [Google Scholar] [CrossRef]
- Cahu, C.; de Lorgeril, M. Farmed and wild fish in the prevention of cardiovascular diseases: Assessing possible differences in lipid nutritional values. Nutr. Metab. Cardiovasc. Dis. 2004, 14, 34–41. [Google Scholar] [CrossRef]
- Phetsang, H.; Panpipat, W.; Undeland, I.; Panya, A.; Phonsatta, N.; Chaijan, M. Comparative quality and volatilomic characterisation of unwashed mince, surimi, and pH-shift-processed protein isolates from farm-raised hybrid catfish (Clarias macrocephalus × Clarias gariepinus). Food Chem. 2021, 364, 130365. [Google Scholar] [CrossRef]
- Selli, S.; Prost, C.; Serot, T. Odor-active and off-odor components in rainbow trout (Oncorhynchus mykiss) extracts obtained by microwave assisted distillation–solvent extraction. Food Chem. 2009, 114, 317–322. [Google Scholar] [CrossRef]
- Fu, X.; Xu, S.; Wang, Z. Kinetics of lipid oxidation and off-odor formation in silver carp mince: The effect of lipoxygenase and hemoglobin. Food Res. Int. 2009, 42, 85–90. [Google Scholar] [CrossRef]
- Liu, S.; Liao, T.; McCrummen, S.T.; Hanson, T.R.; Wang, Y. Exploration of volatile compounds causing off-flavor in farm-raised channel catfish (Ictalurus punctatus) fillet. Aquac. Int. 2016, 25, 413–422. [Google Scholar] [CrossRef]
- Undeland, I. Oxidative stability of seafood. In Oxidative Stability and Shelf Life of Foods Containing Oils and Fats, 1st ed.; Hu, M., Jacobsen, C., Eds.; AOCS Press: San Diego, CA, USA, 2016; pp. 391–460. [Google Scholar]
- Kim, J.H.; Min, D.B. Chemistry of lipid oxidation. In Food Lipids: Chemistry, Nutrition, and Biotechnology, 3rd ed.; Akoh, C.C., Min, D.B., Eds.; CRC Press: New York, NY, USA, 2008; pp. 299–318. [Google Scholar]
- Erickson, C.M. Lipid oxidation of muscle foods. In Food Lipids: Chemistry, Nutrition, and Biotechnology, 3rd ed.; Akoh, C.C., Min, D.B., Eds.; CRC Press: New York, NY, USA, 2008; pp. 322–347. [Google Scholar]
- Chaijan, M.; Panpipat, W. Mechanism of oxidation in foods of animal origin. In Natural Antioxidants, 1st ed.; Banerjee, R., Verma, A.K., Siddiqui, M.W., Eds.; Apple Academic Press: Palm Bay, FL, USA, 2017; pp. 21–58. [Google Scholar]
- Undeland, I.; Ekstrand, B.; Lingnert, H. Lipid oxidation in herring (Clupea harengus) light muscle, dark muscle, and skin, stored separately or as intact fillets. J. Am. Oil Chem. Soc. 1998, 75, 581–590. [Google Scholar] [CrossRef]
- Kunyaboon, S.; Thumanu, K.; Park, J.W.; Khongla, C.; Yongsawatdigul, J. Evaluation of lipid oxidation, volatile compounds and vibrational spectroscopy of silver carp (Hypophthalmichthys molitrix) during ice storage as related to the quality of its washed mince. Foods 2021, 10, 495. [Google Scholar] [CrossRef]
- Prabhakar, P.K.; Vatsa, S.; Srivastav, P.P.; Pathak, S.S. A comprehensive review on freshness of fish and assessment: Analytical methods and recent innovations. Food Res. Int. 2020, 133, 109157. [Google Scholar] [CrossRef]
- Costa, C.; Antonucci, F.; Menesatti, P.; Pallottino, F.; Boglione, C.; Cataudella, S. An advanced colour calibration method for fish freshness assessment: A comparison between standard and passive refrigeration modalities. Food Bioproc. Technol. 2013, 6, 2190–2195. [Google Scholar] [CrossRef] [Green Version]
- Zhang, W.; Cao, A.; Shi, P.; Cai, L. Rapid evaluation of freshness of largemouth bass under different thawing methods using hyperspectral imaging. Food Control 2021, 125, 108023. [Google Scholar] [CrossRef]
- Franceschelli, L.; Berardinelli, A.; Dabbou, S.; Ragni, L.; Tartagni, M. Sensing technology for fish freshness and safety: A review. Sensors 2021, 21, 1373. [Google Scholar] [CrossRef] [PubMed]
- Fogarty, C.; Smyth, C.; Whyte, P.; Brunton, N.; Bolton, D. Sensory and ATP derivative-based indicators for assessing the freshness of Atlantic salmon (Salmo salar) and cod (Gadus morhua). Ir. J. Agric. Food Res. 2019, 58, 71–80. [Google Scholar] [CrossRef] [Green Version]
- Leduc, F.; Tournayre, P.; Kondjoyan, N.; Mercier, F.; Malle, P.; Kol, O.; Berdagué, J.L.; Duflos, G. Evolution of volatile odorous compounds during the storage of European seabass (Dicentrarchus labrax). Food Chem. 2012, 131, 1304–1311. [Google Scholar] [CrossRef]
- Chaijan, M.; Benjakul, S.; Visessanguan, W.; Faustman, C. Changes of lipids in sardine (Sardinella gibbosa) muscle during iced storage. Food Chem. 2006, 99, 83–91. [Google Scholar] [CrossRef]
- Gallart-Jornet, L.; Rustad, T.; Barat, J.M.; Fito, P.; Escriche, I. Effect of superchilled storage on the freshness and salting behavior of Atlantic salmon (Salmo salar) fillets. Food Chem. 2007, 103, 1268–1281. [Google Scholar] [CrossRef]
- AOAC. Offcial Methods of Analysis, 16th ed.; Association of Offcial Analytical Chemists: Washington, DC, USA, 2000. [Google Scholar]
- Benjakul, S.; Seymour, T.A.; Morrissey, M.T.; An, H. Physicochemical changes in Pacific whiting muscle proteins during iced storage. J. Food Sci. 1997, 62, 729–733. [Google Scholar] [CrossRef]
- Panpipat, W.; Chaijan, M. Biochemical and physicochemical characteristics of protein isolates from bigeye snapper (Priacanthus tayenus) head by-product using pH shift method. Turk. J. Fish. Aquat. Sci. 2016, 16, 41–50. [Google Scholar]
- Bligh, E.G.; Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37, 911–917. [Google Scholar] [CrossRef] [Green Version]
- Lowry, R.R.; Tinsley, I.J. Rapid colorimetric determination of free fatty acids. J. Am. Oil Chem. Soc. 1976, 53, 470–472. [Google Scholar] [CrossRef] [PubMed]
- Benjakul, S.; Bauer, F. Biochemical and physicochemical changes in catfish (Silurus glanis Linne) muscle as influenced by different freeze-thaw cycles. Food Chem. 2001, 72, 207–217. [Google Scholar] [CrossRef]
- Schricker, B.R.; Miller, D.D.; Stouffer, J.R. Measurement and content of nonheme and total iron in muscle. J. Food Sci. 1982, 47, 740–743. [Google Scholar] [CrossRef]
- Panpipat, W.; Cheong, L.Z.; Chaijan, M. Impact of lecithin incorporation on gel properties of bigeye snapper (Priacanthus tayenus) surimi. Int. J. Food Sci. Technol. 2021, 56, 2481–2491. [Google Scholar] [CrossRef]
- NIH. The Belmont Report. Ethical Principles and Guidelines for the Protection of Human Subjects of Research. 1979. Available online: http://ohsr.od.nih.gov/guidelines/belmont.html (accessed on 1 March 2020).
- Chaijan, M.; Klomklao, S.; Benjakul, S. Characterization of muscles from Frigate mackerel (Auxis thazard) and catfish (Clarias macrocephalus). Food Chem. 2013, 139, 414–419. [Google Scholar] [CrossRef]
- Testi, S.; Bonaldo, A.; Gatta, P.P.; Badiani, A. Nutritional traits of dorsal and ventral fillets from three farmed fish species. Food Chem. 2006, 98, 104–111. [Google Scholar] [CrossRef]
- Sun, Y.; Ma, L.; Ma, M.; Zheng, H.; Zhang, X.; Cai, L.; Li, J.; Zhang, Y. Texture characteristics of chilled prepared Mandarin fish (Siniperca chuatsi) during storage. Int. J. Food Prop. 2018, 21, 242–254. [Google Scholar] [CrossRef] [Green Version]
- Foegeding, E.A.; Lanier, T.C.; Hultin, H.O. Characteristics of edible muscle tissues. In Food Chemistry, 3rd ed.; Fennema, O.R., Ed.; Marcel Dekker: New York, NY, USA, 1996; pp. 880–942. [Google Scholar]
- Sikorski, Z.E.; Kołakowska, A.; Burt, J.R. Postharvest biochemical and microbial changes. In Seafood: Resources, Nutritional Composition, and Preservation, 1st ed.; Sikorski, Z.E., Ed.; CRC Press: New York, NY, USA, 1990; pp. 55–75. [Google Scholar]
- Rawdkuen, S.; Jongjareonrak, A.; Benjakul, S.; Chaijan, M. Discoloration and lipid deterioration of farmed giant catfish (Pangasianodon gigas) muscle during refrigerated storage. J. Food Sci. 2008, 73, C179–C184. [Google Scholar] [CrossRef] [PubMed]
- Rawdkuen, S.; Jongjareonrak, A.; Phatcharat, S.; Benjakul, S. Assessment of protein changes in farmed giant catfish (Pangasianodon gigas) muscles during refrigerated storage. Int. J. Food Sci. Technol. 2010, 45, 985–994. [Google Scholar] [CrossRef]
- Delbarre-Ladrat, C.; Chéret, R.; Taylor, R.; Verrez-Bagnis, V. Trends in postmortem aging in fish: Understanding of proteolysis and disorganization of the myofibrillar structure. Crit. Rev. Food Sci. Nutr. 2006, 46, 409–421. [Google Scholar] [CrossRef]
- Ueki, N.; Matsuoka, Y.; Wan, J.; Watabe, S. The effects of endogenous proteases within abdominal muscle parts on the rheological properties of thermally induced gels from white croaker (Pennahia argentata). Food Chem. 2018, 268, 498–503. [Google Scholar] [CrossRef] [PubMed]
- Hwang, K.T.; Regenstein, J.M. Characteristics of mackerel mince lipid hydrolysis. J. Food Sci. 1993, 58, 79–83. [Google Scholar] [CrossRef]
- Nayak, J.; Viswanathan Nair, P.G.; Ammu, K.; Mathew, S. Lipase activity in different tissues of four species of fish: Rohu (Labeo rohita Hamilton), oil sardine (Sardinella longiceps Linnaeus), mullet (Liza subviridis Valenciennes) and Indian mackerel (Rastrelliger kanagurta Cuvier). J. Sci. Food Agric. 2003, 83, 1139–1142. [Google Scholar] [CrossRef]
- Benjakul, S.; Visessanguan, W.; Tueksuban, J. Changes in physico-chemical properties and gel-forming ability of lizardfish (Saurida tumbil) during post-mortem storage in ice. Food Chem. 2003, 80, 535–544. [Google Scholar] [CrossRef]
- Clark, G.J.; Ward, F.B. Purification and properties of trimethylamine N-oxide reductase from Shewanella sp. NCMB 400. Microbioloy 1988, 134, 379–386. [Google Scholar] [CrossRef] [Green Version]
- Gram, L.; Huss, H.H. Microbiological spoilage of fish and fish products. Int. J. Food Microbiol. 1996, 33, 121–137. [Google Scholar] [CrossRef]
- Niizeki, N.; Daikoku, T.; Hirata, T.; El-Shourbagy, I.; Song, X.; Sakaguchi, M. Mechanism of biosynthesis of trimethylamine oxide from choline in the teleost tilapia, Oreochromis niloticus, under freshwater conditions. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2002, 131, 371–386. [Google Scholar] [CrossRef]
- Baixas-Nogueras, S.; Bover-Cid, S.; Veciana-Nogués, M.T.; Vidal-Carou, M.C. Suitability of volatile amines as freshness indexes for iced Mediterranean hake. J. Food Sci. 2003, 68, 1607–1610. [Google Scholar] [CrossRef]
- Chaijan, M.; Benjakul, S.; Visessanguan, W.; Faustman, C. Changes of pigments and color in sardine (Sardinella gibbosa) and mackerel (Rastrelliger kanagurta) muscle during iced storage. Food Chem. 2005, 93, 607–617. [Google Scholar] [CrossRef]
- Dulavik, B.; Sørensen, N.K.; Barstad, H.; Horvli, O.; Olsen, R.L. Oxidative stability of frozen light and dark muscles of saithe (Pollachius virens L.). J. Food Lipids 1998, 5, 233–245. [Google Scholar] [CrossRef]
- Chaijan, M.; Undeland, I. Development of a new method for determination of total haem protein in fish muscle. Food Chem. 2015, 173, 1133–1141. [Google Scholar] [CrossRef]
- Abdollahi, M.; Marmon, S.; Chaijan, M.; Undeland, I. Tuning the pH-shift protein-isolation method for maximum hemoglobin-removal from blood rich fish muscle. Food Chem. 2016, 212, 213–224. [Google Scholar] [CrossRef]
- Boselli, E.; Caboni, M.F.; Rodriguez-Estrada, M.T.; Toschi, T.G.; Daniel, M.; Lercker, G. Photoxidation of cholesterol and lipids of turkey meat during storage under commercial retail conditions. Food Chem. 2005, 91, 705–713. [Google Scholar] [CrossRef]
- Mei, J.; Ma, X.; Xie, J. Review on natural preservatives for extending fish shelf life. Foods 2019, 8, 490. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Hui, T.; Wang, F.; Li, S.; Cui, B.; Cui, Y.; Peng, Z. Chinese red pepper (Zanthoxylum bungeanum Maxim.) leaf extract as natural antioxidants in salted silver carp (Hypophthalmichthys molitrix) in dorsal and ventral muscles during processing. Food Control 2015, 56, 9–17. [Google Scholar] [CrossRef]
- Kolakowska, A.; Deutry, J. Some comments on the usefulness of 2-thiobarbituric acid (TBA) test for the evaluation of rancidity in frozen fish. Food/Nahrung 1983, 27, 513–518. [Google Scholar] [CrossRef] [PubMed]
- Tironi, V.A.; Tomás, M.C.; Añón, M. Structural and functional changes in myofibrillar proteins of sea salmon (Pseudopercis semifasciata) by interaction with malonaldehyde (RI). J. Food Sci. 2002, 67, 929–935. [Google Scholar] [CrossRef]
- Wu, H.; Xiao, S.; Yin, J.; Zhang, J.; Richards, M.P. Mechanisms involved in the inhibitory effects of free fatty acids on lipid peroxidation in turkey muscle. Food Chem. 2021, 342, 128333. [Google Scholar] [CrossRef]
- Howgate, P. Tainting of farmed fish by geosmin and 2-methyl-iso-borneol: A review of sensory aspects and of uptake/depuration. Aquaculture 2004, 234, 155–181. [Google Scholar] [CrossRef]
- Grimm, C.C.; Lloyd, S.W.; Zimba, P.V. Instrumental versus sensory detection of off-flavors in farm-raised channel catfish. Aquaculture 2004, 236, 309–319. [Google Scholar] [CrossRef]
- DeWitt, C.A.M.; Kleinholz, C.W.; Vann, D.G.; Bilby, C.A.; Thomas, S.; Schrader, K.K. Evaluation of acid and alkaline processing to remove muddy off-flavors in channel catfish (Ictalurus punctatus). J. Aquat. Food Prod. Technol. 2007, 16, 77–90. [Google Scholar] [CrossRef]
- Yarnpakdee, S.; Benjakul, S.; Penjamras, P.; Kristinsson, H.G. Chemical compositions and muddy flavour/odor of protein hydrolysate from Nile tilapia and broadhead catfish mince and protein isolate. Food Chem. 2014, 142, 210–216. [Google Scholar] [CrossRef]
- Pignoli, G.; Bou, R.; Rodriguez-Estrada, M.T.; Decker, E.A. Suitability of saturated aldehydes as lipid oxidation markers in washed turkey meat. Meat Sci. 2009, 83, 412–416. [Google Scholar] [CrossRef]
- Chaijan, M.; Benjakul, S.; Visessanguan, W.; Lee, S.; Faustman, C. The effect of freezing and aldehydes on the interaction between fish myoglobin and myofibrillar proteins. J. Agric. Food Chem. 2007, 55, 4562–4568. [Google Scholar] [CrossRef]
- Frankel, E.N. Volatile lipid oxidation products. Prog. Lipid Res. 1983, 22, 1–33. [Google Scholar] [CrossRef]
- Frankel, E.N. Lipid oxidation: Mechanisms, products and biological significance. J. Am. Oil Chem. Soc. 1984, 61, 1908–1917. [Google Scholar] [CrossRef]
- Barriuso, B.; Astiasarán, I.; Ansorena, D. A review of analytical methods measuring lipid oxidation status in foods: A challenging task. Eur. Food Res. Technol. 2013, 236, 1–15. [Google Scholar] [CrossRef]
- Chaijan, S.; Panpipat, W.; Panya, A.; Cheong, L.Z.; Chaijan, M. Preservation of chilled Asian sea bass (Lates calcarifer) steak by whey protein isolate coating containing polyphenol extract from ginger, lemongrass, or green tea. Food Control 2020, 118, 107400. [Google Scholar] [CrossRef]
- Ross, C.F.; Smith, D.M. Use of volatiles as indicators of lipid oxidation in muscle foods. Compr. Rev. Food Sci. Food Saf. 2006, 5, 18–25. [Google Scholar] [CrossRef] [PubMed]
- Shahidi, F.; Pegg, R.B. Hexanal as an indicator of meat flavor deterioration. J. Food Lipids 1994, 1, 177–186. [Google Scholar] [CrossRef]
- Maqsood, S.; Benjakul, S. Effect of bleeding on lipid oxidation and quality changes of Asian seabass (Lates calcarifer) muscle during iced storage. Food Chem. 2011, 124, 459–467. [Google Scholar] [CrossRef]
- Jónsdóttir, R.; Bragadóttir, M.; Olafsdottir, G. The role of volatile compounds in odor development during hemoglobin-mediated oxidation of cod muscle membrane lipids. J. Aquat. Food Prod. Technol. 2007, 16, 67–86. [Google Scholar] [CrossRef]
Volatile Compound | Retention Time (min) | Retention Index | Selected Ion [m/z] c | Confirmation d | |
---|---|---|---|---|---|
Libraries a | Calculation b | ||||
propanal | 2.672 | 798 | 789 | 58 *, 29 | MS, STD |
hexanal | 6.237 | 1083 | 1085 | 44 *, 56, 82 | MS, STD |
cis-4-heptenal | 8.774 | 1240 | 1247 | 84 *, 94 | MS, STD |
octanal | 9.495 | 1289 | 1295 | 67 *, 41, 81 | MS, STD |
trans-2-heptenal | 10.047 | 1323 | 1334 | 83 *, 69 | MS, STD |
1-hexanol | 10.396 | 1355 | 1359 | 56 *, 69 | MS, STD |
nonanal | 10.975 | 1391 | 1400 | 58 *, 95, 81 | MS, STD |
1-octen-3-ol | 11.699 | 1450 | 1454 | 72 *, 57 | MS, STD |
2,4-heptadienal | 12.367 | 1495 | 1505 | 81 * | MS, STD |
2-MIB | 13.694 | 1592 | 1612 | 95 *, 108, 135, 150 | MS, STD |
geosmin | 16.480 | 1810 | 1860 | 112 *, 97, 125 | MS, STD |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Phetsang, H.; Panpipat, W.; Panya, A.; Phonsatta, N.; Chaijan, M. Occurrence and Development of Off-Odor Compounds in Farmed Hybrid Catfish (Clarias macrocephalus × Clarias gariepinus) Muscle during Refrigerated Storage: Chemical and Volatilomic Analysis. Foods 2021, 10, 1841. https://doi.org/10.3390/foods10081841
Phetsang H, Panpipat W, Panya A, Phonsatta N, Chaijan M. Occurrence and Development of Off-Odor Compounds in Farmed Hybrid Catfish (Clarias macrocephalus × Clarias gariepinus) Muscle during Refrigerated Storage: Chemical and Volatilomic Analysis. Foods. 2021; 10(8):1841. https://doi.org/10.3390/foods10081841
Chicago/Turabian StylePhetsang, Hatairad, Worawan Panpipat, Atikorn Panya, Natthaporn Phonsatta, and Manat Chaijan. 2021. "Occurrence and Development of Off-Odor Compounds in Farmed Hybrid Catfish (Clarias macrocephalus × Clarias gariepinus) Muscle during Refrigerated Storage: Chemical and Volatilomic Analysis" Foods 10, no. 8: 1841. https://doi.org/10.3390/foods10081841