Skip to main content
SpringerLink
Log in

Antioxidant and Anti-hypertensive Activity, and Cytotoxicity of Amino Acids-Enriched Salt Recovered from Codfish (Gadus morhua L.) Salting Wastewater

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Wastewater from codfish (Gadus morhua L.) salting represents an environmental concern and a cost for processors which must address the disposal. Amino acids-enriched liquid salts (NaCl) were recovered from that effluent and were assessed for the antioxidant and anti-hypertensive activity, and for cytotoxicity to evaluate the possibility to be considered as a functional ingredient. Two samples were evaluated: a hypertonic salt at 15 g/L NaCl and 3 g/L amino acids, and an isotonic salt at 9 g/L NaCl and 1.8 g/L amino acids, obtained by diluting the former. Both samples showed moderate antioxidant activity; the values obtained for each assay depended on the mechanism of radical inhibition as well as on amino acids and NaCl concentration. No pro-oxidant effects on DNA were observed. Both salts demonstrated a significant anti-hypertensive activity with IC50 11 µg/mL for the hypertonic and 7.4 µg/mL for the isotonic sample. For the isotonic salt no cytotoxic effects on intestinal cells were noticed over 180 min, and on hepatic cells up to 70 min. The biological activity showed by the amino acids-enriched salt could prompt the application as a functional ingredient and drive the valorisation of the codfish salting wastewater.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Somogyi, A., Rosta, K., Pusztai, P., Tulassay, Z., Nagy, G.: Antioxidant measurements. Physiol. Meas. 28, 41–55 (2007)

    Article  Google Scholar 

  2. Stadtman, E.: Role of antioxidant species in aging. Curr. Med. Chem. 11, 1105–1112 (2004)

    Article  Google Scholar 

  3. Guimarães, C.M., Gião, M.S., Martinez, S.S., Pintado, A.I., Pintado, E.M., Bento, L.S., Malcata, F.X.: Antioxidant activity of sugar molasses, including protective effect against oxidative damage. Food Chem. Toxicol. 72, 39–43 (2007)

    Google Scholar 

  4. Ohishima, H., Sawa, T., Akraike, T.: 8-Nitroguanidine, a product of nitrative DNA damage caused by reactive oxygen species: formation, occurrence, and implication of inflammation and carcinogenesis. Antioxid. Redox Signal. 8, 1033–1045 (2006)

    Article  Google Scholar 

  5. Barzilay, A., Yamamoto, K.: DNA damage response to oxidative stress. DNA Repair (AMST) 3, 1109–1115 (2004)

    Article  Google Scholar 

  6. Sohal, R.S.: Role of oxidative stress and proteins oxidation in the aging process. Free Radical Biol. Med. 33, 37–44 (2002)

    Article  Google Scholar 

  7. Atmaca, G.: Antioxidant effect of sulfur-containing amino acids. Yonsei Med. J. 45, 776–788 (2004)

    Article  Google Scholar 

  8. Wu, H.C., Shiau, C.Y., Chen, H.M., Chiou, T.K.: Antioxidant activity of carnosine, anserine, some free amino acids and their combination. J. Food Drug Anal. 11, 148–153 (2003)

    Google Scholar 

  9. Lawler, J.M., Barnes, W.S., Wu, G., Song, W., Demaree, S.: Direct antioxidant properties of creatine. Biochem. Biophys. Res. Commun. 290, 47–52 (2002)

    Article  Google Scholar 

  10. Oudit, G.Y., Trivieri, M.G., Khaper, N., Husain, T., Wilson, G.J., Liu, P., Sole, M.J., Backx, P.H.: Taurine supplementation reduces oxidative stress and improves cardiovascular function in an iron-overload murine model. Circulation 109, 1877–1885 (2004)

    Article  Google Scholar 

  11. Meucci, E., Mele, M.C.: Amino acids and plasma antioxidant capacity. Amino Acids 12, 373–377 (1997)

    Article  Google Scholar 

  12. Myliutina, N.P., Ananyan, A.A., Shchugalei, V.S.: Antiradical and antioxidative effects of arginine and its influence on lipid peroxidation activity during hypoxia. Bull. Exp. Biol. Med. 110, 1198–1200 (1991)

    Article  Google Scholar 

  13. Yu, X., Zhao, M., Hu, J., Zeng, S., Bai, X.: Correspondence analysis of antioxidant activity and UV–Vis absorbance of Maillard reaction products as related to reactants. LWT Food Sci. Technol. 46, 1–9 (2012)

    Article  Google Scholar 

  14. Vasdev, S., Stuckless, J.: Antihypertensive effects of dietary protein and its mechanism. Int. J. Angiol. 19, 7–20 (2010)

    Article  Google Scholar 

  15. Elliott, P., Stamler, J., Dyer, A.R., Appel, L., Dennis, B., Kestellot, H., Ueshima, H., Okayama, A., Chan, Q., Garside, D.B., Zhou, B.: Association between protein intake and blood pressure: the INTERMAP study. Arch. Intern. Med. 166, 79–87 (2006)

    Article  Google Scholar 

  16. Stamler, J., Elliott, P., Kesteloot, H., Nichols, R., Claeys, G., Dyer, A.R., Stamler, R.: Inverse relation of dietary protein markers with blood pressure. Findings for 10,020 men and women in the INTERSALT study. Circulation 94, 1629–1634 (1996)

    Article  Google Scholar 

  17. Ferraro, V., Cruz, B.I., Ferreira Jorge, R., Castro, M.L.P., Pintado, E.M.: Recovery of free amino acids and muscle proteins from codfish (Gadus murhua L.) salting wastewater. J. Chem. Technol. Biotechnol. 89, 671–681 (2014)

    Article  Google Scholar 

  18. Ferraro, V., Cruz, B.I., Ferreira Jorge, R., Pintado, E.M., Castro, M.L.P.: Solvent extraction of sodium chloride from codfish (Gadus morhua L.) salting processing wastewater. Desalination 287, 42 (2011)

    Article  Google Scholar 

  19. Benzie, I.F.F., Strain, J.J.: The ferric reducing ability of plasma (FRAP) as a measure of “Antioxidant Power”: the FRAP assay. Anal. Biochem. 239, 70 (1996)

    Article  Google Scholar 

  20. Brand-Williams, W., Cuvelier, M.E., Berset, C.: Use of a free radical method to evaluate antioxidant activity. LWT Food Sci. Technol. 28, 11 (1995)

    Article  Google Scholar 

  21. Ou, B., Hampsch-Woodill, M., Prior, R.L.: Development and validation of an improved oxygen radical oxygen assay using fluorescein as the fluorescent probe. J. Agric. Food Chem. 49, 4619–4626 (2001)

    Article  Google Scholar 

  22. Dávalos, A., Gómez-Cordovés, C., Bartolomé, B.: Extending applicability of the oxygen radical absorbance capacity (ORAC-Fluorescein) assay. J. Agric. Food Chem. 52, 48 (2004)

    Article  Google Scholar 

  23. Schwager, S.L., Carmona, A.K., Sturrock, E.D.: A high-throughput fluorometric assay for angiotensin I-converting enzyme. Nat. Protoc. 1, 1961–1964 (2006)

    Article  Google Scholar 

  24. Berridge, M.V., Tan, A.S., McCoy, K.D., Wang, R.: The biochemical and cellular basis of cell proliferation assays that use tetrazolium salts. Biochemica 4, 14–19 (1996)

    Google Scholar 

  25. Sochor, J., Ryvolova, M., Krystofova, O., Salas, P., Hubalek, J., Adam, V., Trnkova, L., Havel, L., Beklova, M., Zehnalek, J., Provaznik, I., Kizek, R.: Fully automated spectrometric protocols for determination of antioxidant activity: advantages and disadvantages. Molecules 15, 8618–8640 (2010)

    Article  Google Scholar 

  26. Frenkel, E.N., Merkel, A.S.: The problem of using one-dimensional method to evaluate multifunctional food and biological antioxidants. J. Sci. Food Agric. 80, 1925–1940 (2000)

    Article  Google Scholar 

  27. Mishra, M., Mishra, P.K., Kumar, U., Prakash, V.: NaCl phytotoxicity induces oxidative stress and response on antioxidant system in Cicer arietinum L. CV. Abrodhi. Bot. Res. Int. 2, 74–82 (2009)

    Google Scholar 

  28. Ketonen, J., Marvaala, E.: Effects of dietary sodium on reactive oxygen species formation and endothelial dysfunction in low-density lipoprotein receptor-deficiency mice on high-fat diet. Heart Vessels 23, 420–429 (2008)

    Article  Google Scholar 

  29. Zulueta, A., Esteve, M.J., Frígola, A.: ORAC and TEAC assay comparison to measure the antioxidant capacity of food products. Food Chem. 114, 310–316 (2009)

    Article  Google Scholar 

  30. Huang, D., Ou, B., Prior, R.L.: The chemistry behind antioxidant capacity assays. J. Agric. Food Chem. 53, 1841–1856 (2005)

    Article  Google Scholar 

  31. Dmitrieva, N.I., Burg, M.B., Ferraris, J.D.: DNA damage and osmotic regulation in the kidney. Am. J. Physiol. Renal Physiol. 289, 2–7 (2005)

    Article  Google Scholar 

  32. Dmitrieva, N.I., Burg, M.B.: Osmotic stress and DNA damage. Meth. Enzymol. 428, 241–252 (2007)

    Article  Google Scholar 

  33. Anastassopoulou, J.: Metal-DNA interactions. J. Mol. Struct. 651–653, 19–26 (2003)

    Article  Google Scholar 

  34. Schlick, T., Li, B., Olson, W.K.: The influence of salt and on the structure and energetic of supercoiled DNA. Biophys. J. 67, 2146–2166 (1994)

    Article  Google Scholar 

  35. Messina, S., Dawson Jr, R.: Attenuation of oxidative damage to DNA by taurine and taurine analogs. In: Della Corte, G. (ed.) Taurine 4: taurine and excitable tissues, pp. 355–367. Plenum Press, New York (2002)

    Chapter  Google Scholar 

  36. Eppler, B., Dawson Jr, R.: Cytoprotective role of taurine in a renal epithelial cell culture model. Biochem. Pharmacol. 63, 1051–1060 (2002)

    Article  Google Scholar 

  37. Obrosova, I.G., Fathallal, L., Stevens, M.J.: Taurine counteracts oxidative stress and nerve factor deficit in early experimental diabetic neuropathy. Exp. Neurol. 172, 211–219 (2001)

    Article  Google Scholar 

  38. Hwang, D.F., Hour, J.L., Cheng, H.M.: Effects of taurine on toxicity of oxidized fish oil in rats. Food Chem. Toxicol. 38, 585–591 (2000)

    Article  Google Scholar 

  39. Seneviratne, C.K., Khaper, N., Singal, P.K.: Effects of methionine on endogenous antioxidants in the heart. Am. J. Physiol. 227, 2124–2129 (1999)

    Google Scholar 

  40. McKenna, M.J., Morton, J., Selig, S.E., Snow, R.J.: Creatine supplementation increases muscle total creatine but not maximal intermittence exercise performance. J. Appl. Physiol. 87, 2244–2252 (1999)

    Google Scholar 

  41. Reid, M.B.: Redox modulation of skeletal muscle contraction: what we know and what we don’t. J. Appl. Physiol. 90, 724–731 (2001)

    Article  Google Scholar 

  42. Morguerza, B., Ramos, M., Sánchez, E., Manso, M.A., Miguel, M., Aleixandre, A., Delgado, M.A., Recio, I.: Antihypertensive activity of milk fermented by Enterococcus faecalis strain isolated from raw milk. Int. Dairy J. 16, 61–69 (2006)

    Article  Google Scholar 

  43. Tsai, H., Deng, H., Tsai, S., Hsu, Y.: Bioactivity comparison of extracts from various parts of common and tartary buckwheats: evaluation of the antioxidant- and angiotensin-converting enzyme inhibitory activities. Chem. Cent. J. 6, 78–82 (2012)

    Article  Google Scholar 

  44. Vasdev, S., Singal, P., Gill, V.: The antihypertensive effect of cysteine. Int. J. Angiol. 18, 7–21 (2009)

    Article  Google Scholar 

  45. Higashi, Y., Oshima, T., Ono, N., Hiraga, H., Yoshimura, M., Watanabe, M., Matsuura, H., Kambe, M., Kajiyama, G.: Intravenous administration of l-arginine inhibits angiotensin-converting enzyme in humans. J. Clin. Endocrinol. Metab. 80, 2198–2202 (1995)

    Google Scholar 

  46. Militante, J.D., Lombardini, J.B.: Treatment of hypertension with oral taurine: experimental and clinical studies. Amino Acids 23, 381–393 (2002)

    Article  Google Scholar 

  47. Fregly, M.J., Sumners, C., Cade, J.R.: Effect of chronic dietary treatment with l-tryptophan on the maintenance of hypertension in spontaneously hypertensive rats. Can. J. Physiol. Pharmacol. 67, 656–662 (1989)

    Article  Google Scholar 

  48. Ferraro, V., Cruz, B.I., Ferreira Jorge, R., Castro, M.L.P., Pintado, E.M.: In-vitro intestinal absorption of free amino acids extracted from codfish salting (Gadus murhua L.) wastewater. Int. J. Food Sci. Technol. 49, 27–33 (2014)

    Article  Google Scholar 

  49. Martín-Venega, R., Rodríguesz-Laguna, M.J., Mercier, Y., Geraert, P.A., Ferrer, R.: Effect of pH on l- and d-methionine uptake across the apical membrane of Caco-2 cells. Am. J. Physiol. Cell Physiol. 269, 632 (2009)

    Google Scholar 

Download references

Acknowledgments

Author Vincenza Ferraro thanks Marie Curie Actions (European Research Area) for a Doctoral Grant (Ref. InSolEx-RTN under FP6). This work was partially supported by National Founds from FCT – Fundação para a Ciência e Tecnologia, through the project PEst-OE/EQB/LA0016/2013.

Author information

Authors and Affiliations

  1. CBQF/Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior de Biotecnologia, Universidade Católica Portuguesa/Centro Regional do Porto, Rua Arquiteto Lobão Vidal, Apartado 2511, 4202-401, Porto, Portugal

    Vincenza Ferraro, Sérgio C. Sousa & Manuela E. Pintado

  2. Department of Biochemistry (U38-FCT), Faculty of Medicine of the University of Porto, Al. Prof. Hernani Monteiro, 4200-319, Porto, Portugal

    Cláudia Marques & Conceição Calhau

Authors
  1. Vincenza Ferraro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sérgio C. Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cláudia Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Conceição Calhau
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuela E. Pintado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuela E. Pintado.

Ethics declarations

Conflict of interest

Authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferraro, V., Sousa, S.C., Marques, C. et al. Antioxidant and Anti-hypertensive Activity, and Cytotoxicity of Amino Acids-Enriched Salt Recovered from Codfish (Gadus morhua L.) Salting Wastewater. Waste Biomass Valor 6, 1115–1124 (2015). https://doi.org/10.1007/s12649-015-9416-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-015-9416-x

Keywords

Search

Navigation