Abstract
Contents of protein-bound advanced glycation end-products (AGEs) including Nε-carboxymethyl-lysine (CML) and Nε-carboxyethyl-lysine (CEL), as well as total viable counts (TVC), total volatile basic nitrogen (TVB-N) and thiobarbituric acid reactive substances (TBARS) in vacuum-packed dried salted Spanish Mackerel fillets previously brined with 0‒15% NaCl during storage at 25 °C were determined. In freshly dried fish fillets with increased salt concentration, TVB-N decreased from 39.32 ± 5.39 to 22.35 ± 4.55 mg N/100 g and TBARS increased from 0.18 ± 0.01 to 0.50 ± 0.03 mg MDA/kg. No statistical differences were found in the levels of TVC, CML and CEL of dried fish (P = 0.215‒0.645). TVC and TVB-N levels of the dried salted fish fillets increased during 25 d storage (P = 0.000‒0.036), but reduced with increase of NaCl concentration (P = 0.000‒0.002). TBARS levels of the fillets increased until day15 and then slightly declined (P = 0.000‒0.036). Salt promoted the increase in TBARS in dried fish but showed inhibition effect with higher concentrations (P = 0.000‒0.003). Levels of protein-bound CML and CEL in both unsalted and salted fish fillets increased constantly during storage (P = 0.000‒0.050), whereas NaCl of increased content inhibited the formation of protein-bound CML and CEL in fillets (P = 0.000‒0.119). Positive correlations were observed in the contents of protein-bound CML and CEL with TVC, TVB-N and TBARS (r = 0.445‒0.839, P = 0.000‒0.002), indicating the formation of protein-bound AGEs in dried fish fillets is attributable to protein deterioration and lipid oxidation during storage.
Similar content being viewed by others
Change history
07 July 2022
The Figure 1 and Figure 2 captions are revised.
09 July 2022
A Correction to this paper has been published: https://doi.org/10.1007/s11694-022-01504-0
References
T. Nielsen, M. Mihnea, K. Båth, S.C. Cunha, R. Fereira, J.O. Fernandes, A. Gonçalves, M.L. Nunes, H. Oliveira, New formulation for producing salmon pâté with reduced sodium content. Food Chem. Toxicol. 143, 111546 (2020). https://doi.org/10.1016/j.fct.2020.111546
A. Brás, R. Costa, Influence of brine salting prior to pickle salting in the manufacturing of various salted-dried fish species. J Food Eng 100, 490–495 (2010). https://doi.org/10.1016/j.jfoodeng.2010.04.036
E.A. Dinçer, Dried meat products obtained by different methods from past to present. Food Rev. Int. 1–20 (2021). https://doi.org/10.1080/87559129.2021.1956944
S. Koral, B. Tufan, A. Ščavničar, D. Kočar, M. Pompe, S. Köse, Investigation of the contents of biogenic amines and some food safety parameters of various commercially salted fish products. Food Control 32, 597–606 (2013). https://doi.org/10.1016/j.foodcont.2013.01.043
M. Vasconi, F. Bellagamba, C. Bernardi, P.A. Martino, V.M. Moretti, Histamine formation in a dry salted twaite shad (Alosa fallax lacustris) product. J. Food Prot. 80, 127–135 (2017). https://doi.org/10.4315/0362-028X.JFP-16-243
Y. Wu, Y. Chen, L. Li, X. Yang, S. Yang, W. Lin, Y. Zhao, J. Deng, Study on biogenic amines in various dry salted fish consumed in China. J. Ocean. Univ. China 15, 681–689 (2016). https://doi.org/10.1007/s11802-016-2958-0
K.A. Thorarinsdottir1, G. Gudmundsdottir1, S. Arason1, G. Thorkelsson1, K. Kristbergsson1, Effects of added salt, phosphates, and proteins on the chemical and physicochemical characteristics of frozen cod (Gadus morhua) fillets. J. Food Sci. 69, 144–152 (2004). https://doi.org/10.1111/j.13652621.2004.tb06355.x
S. Kose, Evaluation of seafood safety health hazards for traditional fish products: Preventive measures and monitoring issues. Turk. J. Fish. Aquat. Sci. 10, 139–160 (2010). https://doi.org/10.4194/trjfas.2010.0120
J. Kanner, S. Harel, R. Jaffe, Lipid-peroxidation of muscle food as affected by NaCl. J. Agric. Food Chem. 39, 1017–1021 (1991). https://doi.org/10.1021/jf00006a002
C. Qu, Z. He, Z. Wang, S. Li, Z. Wang, H. Li, Effects of NaCl content and drying temperature on lipid oxidation, protein oxidation, and physical properties of dry-cured chicken. J. Food Sci. 85, 1651–1660 (2020). https://doi.org/10.1111/1750-3841.15129
S. Huang, M. Huang, X. Dong, Advanced glycation end products in meat during processing and storage: A review. Food Rev Int, 1–17 (2021). https://doi.org/10.1080/87559129.2021.1936003.
L. Yu, C. Gao, M. Zeng, Z. He, L. Wang, S. Zhang, J. Chen, Effects of raw meat and process procedure on Nε-carboxymethyl-lysine and Nε-carboxyethyl-lysine formation in meat products. Food Sci Biotechnol 25, 1163–1168 (2016). https://doi.org/10.1007/s10068-016-0185-5
M.A. Anis, Y.N. Sreerama, Inhibition of protein glycoxidation and advanced glycation end-product formation by barnyard millet (Echinochloa frumentacea) phenolics. Food Chem. 315, 126265 (2020). https://doi.org/10.1016/j.foodchem.2020.126265
X. Sun, X. Li, J. Tang, K. Lai, B.A. Rasco, Y. Huang, Formation of protein-bound Nε-carboxymethyllysine and Nε-carboxyethyllysine in ground pork during commercial sterilization as affected by the type and concentration of sugars. Food Chem. 336, 127706 (2021). https://doi.org/10.1016/j.foodchem.2020.127706
Z. Zhu, J. Yang, X. Zhou, I.A. Khan, A.P. Bassey, M. Huang, Comparison of two kinds of peroxyl radical pretreatment at chicken myofibrillar proteins glycation on the formation of Nε-carboxymethyllysine and Nε-carboxyethyllysine. Food Chem. 353, 129487 (2021). https://doi.org/10.1016/j.foodchem.2021.129487
L. Yu, Q. Li, Y. Li, Y. Yang, C. Guo, M. Li, Impact of frozen storage duration of raw pork on the formation of advanced glycation end-products in meatballs. LWT 146, 111481 (2021). https://doi.org/10.1016/j.lwt.2021.111481
L. Niu, X. Sun, J. Tang, J. Wang, B.A. Rasco, K. Lai, Y. Huang, Free and protein-bound Nε-carboxymethyllysine and Nε-carboxyethyllysine in fish muscle: Biological variation and effects of heat treatment. J. Food Compos. Anal. 57, 56–63 (2017). https://doi.org/10.1016/j.jfca.2016.12.017
D.B. Kul, P. Anlar, Z.F.Y. Oral, M. Kaya, G. Kaban, Furosine and Nε-carboxymethyl-lysine in cooked meat product (kavurma): Effects of salt and fat levels during storage. J. Stored Prod. Res. 93, 101856 (2021). https://doi.org/10.1016/j.jspr.2021.101856
L. Li, S. Kong, Y. Liu, Y. Huang, Y. Li, K. Lai, Effects of acetic acid, ethanol, and sodium chloride on the formation of Nε-carboxymethyllysine, Nε-carboxyethyllysine and their precursors in commercially sterilized pork. J. Food Meas. Charact. 15, 5337–5344 (2021). https://doi.org/10.1007/s11694-021-01102-6
L. Niu, X. Sun, J. Tang, J. Wang, J. Wang, B.A. Rasco, K. Lai, Y. Fan, Y. Huang, Combination effects of salts and cold storage on the formation of protein-bound Nε-(carboxymethyl)lysine and Nε-(carboxyethyl)lysine in raw and subsequently commercially sterilized ground pork. Food Chem. 264, 455–461 (2018). https://doi.org/10.1016/j.foodchem.2018.05.054
Y. Li, C. Xue, W. Quan, F. Qin, Z. Wang, Z. He, M. Zeng, J. Chen, Assessment the influence of salt and polyphosphate on protein oxidation and Nε-(carboxymethyl)lysine and Nε-(carboxyethyl)lysine formation in roasted beef patties. Meat Sci. 177, 108489 (2021). https://doi.org/10.1016/j.meatsci.2021.108489
C.-C. Hwang, C.-M. Lin, H.-F. Kung, Y.-L. Huang, D.-F. Hwang, Y.-C. Su, Y.-H. Tsai, Effect of salt concentrations and drying methods on the quality and formation of histamine in dried milkfish (Chanos chanos). Food Chem. 135, 839–844 (2012). https://doi.org/10.1016/j.foodchem.2012.05.035
N. Sirini, A. Roldán, R. Lucas-González, J. Fernández-López, M. Viuda-Martos, J.A. Pérez-Álvarez, L.S. Frizzo, M.R. Rosmini, Effect of chestnut flour and probiotic microorganism on the functionality of dry-cured meat sausages. LWT 134, 110197 (2020). https://doi.org/10.1016/j.lwt.2020.110197
Y. Li, X. Tang, Z. Shen, J. Dong, Prediction of total volatile basic nitrogen (TVB-N) content of chilled beef for freshness evaluation by using viscoelasticity based on airflow and laser technique. Food Chem. 287, 126–132 (2019). https://doi.org/10.1016/j.foodchem.2019.01.213
T.C. Merlo, JdaC. Antonio, T.V. Savian, C. Villegas, M.D.B. Dargelio, J.S. da Silva Pinto, S.M. d. Alencar, A.L.R. Rodrigues, E. Saldaña, C.J. Contreras-Castillo, Effect of the smoking using Brazilian reforestation woods on volatile organic compounds, lipid oxidation, microbiological and hedonic quality of bacons during shelf life. Meat Sci. 164, 108110 (2020). https://doi.org/10.1016/j.meatsci.2020.108110
X. Sun, J. Tang, J. Wang, B.A. Rasco, K. Lai, Y. Huang, Formation of advanced glycation endproducts in ground beef under pasteurisation conditions. Food Chem. 172, 802–807 (2015). https://doi.org/10.1016/j.foodchem.2014.09.129
L. Niu, X. Sun, J. Tang, J. Wang, B.A. Rasco, K. Lai, Y. Fan, Y. Huang, Formation of advanced glycation end-products in fish muscle during heating: Relationship with fish freshness. J. Food Compost Anal. 63, 133–138 (2017). https://doi.org/10.1016/j.jfca.2017.07.033
Q. Wu, K. Zhao, Y. Chen, J. Xiao, M. Zhou, D. Li, N. Feng, C. Wang, Ethanol as an accelerator for the formation of advanced glycation end products in glucose-lysine solution. LWT 124, 109135 (2020). https://doi.org/10.1016/j.lwt.2020.109135
C. Ruiz-Capillas, A. Moral, Sensory and biochemical aspects of quality of whole bigeye tuna (Thunnus obesus) during bulk storage in controlled atmospheres. Food Chem. 89, 347–354 (2005). https://doi.org/10.1016/j.foodchem.2004.02.041
S. Moini, R. Tahergorabi, S.V. Hosseini, M. Rabbani, Z. Tahergorabi, X. Feás, F. A-flaki, Effect of gamma radiation on the quality and shelf life of refrigerated rainbowtrout (Oncorhynchus mykiss) fillets. J. Food Prot. 72, 1419–1426 (2009). https://doi.org/10.4315/0362-028X-72.7.1419
Z. Ahmed, O.N. Donkor, W.A. Street, T. Vasiljevic, Activity of endogenous muscle proteases from 4 Australian underutilized fish species as affected by ionic strength, pH, and temperature. J. Food Sci. 78(12), C1858–C1864 (2013). https://doi.org/10.1111/1750-3841.12303
K. Suhem, S. Songsamoe, N. Matan, Effects of bamboo sachets containing Litsea cubeba oil on the prevention of mold for extending the shelf life of dried fish, its reusability, and action mechanisms. LWT 154, 112796 (2022). https://doi.org/10.1016/j.lwt.2021.112796
G. Rasul, B.C. Majumdar, F. Afrin, M.A.J. Bapary, A.K.M.A. Shah, Biochemical, microbiological, and sensory properties of dried silver carp (Hypophthalmichthys molitrix) influenced by various drying methods. Fishes 3(3), 25 (2018). https://doi.org/10.3390/fishes3030025
A. Cheng, F. Wan, T. Xu, F. Du, W. Wang, Q. Zhu, Effect of irradiation and storage time on lipid oxidation of chilled pork. Radiat. Phys. Chem. 80, 475–480 (2011). https://doi.org/10.1016/j.radphyschem.2010.10.003
G. Jin, J. Zhang, X. Yu, Y. Lei, J. Wang, Crude lipoxygenase from pig muscle: Partial characterization and interactions of temperature, NaCl and pH on its activity. Meat Sci. 87, 257–263 (2011). https://doi.org/10.1016/j.meatsci.2010.09.012
L. Yu, M. Chai, M. Zeng, Z. He, J. Chen, Effect of lipid oxidation on the formation of Nε-carboxymethyl-lysine and Nε-carboxyethyl-lysine in Chinese-style sausage during storage. Food Chem. 269, 466–472 (2018). https://doi.org/10.1016/j.foodchem.2018.07.051
E.J. Kwak, S.I. Lim, The effect of sugar, amino acid, metal ion, and NaCl on model Maillard reaction under pH control. Amino Acids 27, 85–90 (2004). https://doi.org/10.1007/s00726-004-0067-7
C. Thongraung, S. Kangsanan, Influence of pH, NaCl and pre-incubation on utilisation of surimi wash water in generation of antioxidative material by using the Maillard reaction. Int. J. Food Sci. Technol. 45, 1696–1702 (2010). https://doi.org/10.1111/j.1365-2621.2010.02318.x
S. Zhuang, Y. Tan, H. Hong, D. Li, L. Zhang, Y. Luo, Exploration of the roles of spoilage bacteria in degrading grass carp proteins during chilled storage: A combined metagenomic and metabolomic approach. Food Res. Int. 152, 110926 (2021). https://doi.org/10.1016/j.foodres.2021.110926
V.A.S. Vidal, J.M. Lorenzo, P.E.S. Munekata, M.A.R. Pollonio, Challenges to reduce or replace NaCl by chloride salts in meat products made from whole pieces – A review. Crit. Rev. Food Sci. Nutr. 61, 2194–2206 (2020). https://doi.org/10.1080/10408398.2020.1774495
H. Cui, J. Yu, Y. Zhai, L. Feng, P. Chen, K. Hayat, Y. Xu, X. Zhang, C. Ho, Formation and fate of Amadori rearrangement products in Maiilard reaction. Trends Food Sci Tech 115, 391–408 (2021). https://doi.org/10.1016/j.tifs.2021.06.055
M.W. Poulsen, R.V. Hedegaard, J.M. Andersen, B. de Courten, S. Bugel, J. Nielsen, L.H. Skibsted, L.O. Dragsted, Advanced glycation endproducts in food and their effects on health. Food Chem. Toxicol. 60, 10–37 (2013). https://doi.org/10.1016/j.fct.2013.06.052
Z. Zhu, Y. Cheng, S. Huang, M. Yao, Y. Lei, I.A. Khen, M. Huang, X. Zhou, Formation of Nε-Carboxymethyllysine and Nε-Carboxyethyllysine in Prepared Chicken Breast by Pan Frying. J. Food Prot. 82, 2154–2160 (2019). https://doi.org/10.4315/0362-028X.JFP-19-319
Acknowledgements
This paper was financially supported by the Natural Science Foundation of Shandong Province (ZR2019PC058).
Author information
Authors and Affiliations
Contributions
Conceptualization: Yiqun Huang, Lihong Niu, Keqiang Lai; Methodology: Lihong Niu, Keqiang Lai, Shanshan Kong; Formal analysis and investigation: Shanshan Kong, Fuyu Chu; Writing – original draft preparation: Shanshan Kong; Writing – review and editing: Lihong Niu, Keqiang Lai; Funding acquisition: Lihong Niu, Keqiang Lai; Resources: Lihong Niu, Keqiang Lai; Supervision: Lihong Niu, Keqiang Lai.
Corresponding authors
Ethics declarations
The authors declare no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kong, S., Chu, F., Huang, Y. et al. Effects of salt concentrations on the advanced glycation end-products in dried salted spanish mackerel fillets during storage. Food Measure 16, 3469–3476 (2022). https://doi.org/10.1007/s11694-022-01440-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11694-022-01440-z