Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Journal of Complementary and Integrative Medicine

Editor-in-Chief: Lui, Edmund

Ed. by Ko, Robert / Leung, Kelvin Sze-Yin / Saunders, Paul / Suntres, PH. D., Zacharias

CiteScore 2017: 1.41

SCImago Journal Rank (SJR) 2017: 0.472
Source Normalized Impact per Paper (SNIP) 2017: 0.564

See all formats and pricing
More options …

Safer and healthier reduced nitrites turkey meat sausages using lyophilized Cystoseira barbata seaweed extract

Sabrine Sellimi
  • Corresponding author
  • Laboratoire de Génie Enzymatique et de Microbiologie, Ecole Nationale d’Ingénieurs de Sfax, Université de Sfax, BP 1171, Sfax 3000, Tunisia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Abdelkarim Benslima
  • Laboratoire de Génie Enzymatique et de Microbiologie, Ecole Nationale d’Ingénieurs de Sfax, Université de Sfax, BP 1171, Sfax 3000, Tunisia
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Ghada Ksouda
  • Laboratoire de Génie Enzymatique et de Microbiologie, Ecole Nationale d’Ingénieurs de Sfax, Université de Sfax, BP 1171, Sfax 3000, Tunisia
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Veronique Barragan Montero / Mohamed Hajji
  • Laboratoire de Génie Enzymatique et de Microbiologie, Ecole Nationale d’Ingénieurs de Sfax, Université de Sfax, BP 1171, Sfax 3000, Tunisia
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Moncef Nasri
  • Laboratoire de Génie Enzymatique et de Microbiologie, Ecole Nationale d’Ingénieurs de Sfax, Université de Sfax, BP 1171, Sfax 3000, Tunisia
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-10-21 | DOI: https://doi.org/10.1515/jcim-2017-0061



Nitrite salts are still common additives in the meat industry. The present study provides a first approach on the employment of the lyophilized aqueous extract (WE) of the Tunisian seaweed Cystoseira barbata for the quality enhancement of turkey meat sausage.


WE was supplemented as a natural antioxidant agent to investigate its effectiveness in delaying lipid oxidation turkey meat sausages containing reduced amounts of sodium nitrites.


On storage day 5, all concentrations of WE (0.01–0.4 %) reduced the meat lipid oxidation by approximately 36 %, as compared to the negative control containing only 80 mg/kg of meat of sodium nitrites as antioxidant. It was noted that within 15 days of refrigerated storage, a meat system containing 80 mg/kg of meat of sodium nitrites and 0.02 % and 0.04 % of WE had similar Thiobarbituric Acid Reactive Substances (TBARS) levels (19±1.32 and 17±1.12 µmol/kg of meat, respectively), which were comparable to the positive control containing sodium nitrites (150 mg/kg of meat) and 0.045 % vitamin C (18.46±1.27 µmol/kg of meat). In-depth, the metabolomic profiling using gas chromatography–mass spectrometry (GC/MS) and liquid chromatography–quadripole–time–of–flight–mass spectrometry (LC-QTOF-MS) analyses of the Tunisian seaweed C. barbata solvent extracts showed that the main active compounds were phenolic compounds, fatty acids and sterols.


Overall, the cold medium containing C. barbata lyophilized aqueous extrac, with strong antioxidant activity and antihypertensive properties, may open the way to the development of a natural quality enhancement strategy for new functional and ever healthier reduced nitrites meat sausages based on algae.

Keywords: antihypertensive potential; antioxidative properties; Cystoseira barbata; food additive; lipid oxidation; turkey meat sausages


  • [1]

    Ngo DH, Wijesekara I, Vo TS, Van Ta Q, Kim SK. Marine food-derived functional ingredients as potential antioxidants in the food industry: An overview. Food Res Int. 2011;44:523–9.CrossrefWeb of ScienceGoogle Scholar

  • [2]

    Alahakoon AU, Jayasena DD, Ramachandra S, Jo C. Alternatives to nitrite in processed meat: Up to date. Trends Food Sci Technol. 2015;45:37–49.Web of ScienceCrossrefGoogle Scholar

  • [3]

    Zanardi E, Ghidini S, Battaglia A, Chizzolini R. Lipolysis and lipid oxidation in fermented sausages depending on different processing conditions and different antioxidants. Meat Sci. 2004;66:415–23.PubMedCrossrefGoogle Scholar

  • [4]

    Bryan NS, Alexander DD, Coughlin JR, Milkowski AL, Boffetta P. Ingested nitrate and nitrite and stomach cancer risk: An updated review. Food Chem Toxicol. 2012;50:3646–65.CrossrefWeb of SciencePubMedGoogle Scholar

  • [5]

    Herrmann SS, Duedahl-Olesen L, Christensen T, Olesen PT, Granby K. Dietary exposure to volatile and non-volatile N-nitrosamines from processed meat products in Denmark. Food Chem Toxicol. 2015;80:137–43.CrossrefWeb of SciencePubMedGoogle Scholar

  • [6]

    Lorenzo JM, González-Rodríguez RM, Sánchez M, Amado IR, Franco D. Effects of natural (grape seed and chestnut extract) and synthetic antioxidants (buthylatedhydroxytoluene, BHT) on the physical, chemical, microbiological and sensory characteristics of dry cured sausage “chorizo”. Food Res Int. 2013;54:611–20.CrossrefWeb of ScienceGoogle Scholar

  • [7]

    Kahl R, Kappus H. Toxicology of the synthetic antioxidants BHA and BHT in comparison with the natural antioxidant vitamin E. Z Lebensm Unters Forsch. 1993;196:329–38.CrossrefPubMedGoogle Scholar

  • [8]

    Mohamed S, Hashim SN, Rahman HA. Seaweeds: A sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol. 2012;23:83–96.CrossrefWeb of ScienceGoogle Scholar

  • [9]

    Bocanegra A, Bastida S, Benedí J, Ródenas S, Sánchez-Muniz FJ. Characteristics and nutritional and cardiovascular-health properties of seaweeds. J Med Food. 2009;12:236–58.PubMedWeb of ScienceCrossrefGoogle Scholar

  • [10]

    Holdt SL, Kraan S. Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol. 2011;23:543–97.CrossrefWeb of ScienceGoogle Scholar

  • [11]

    Stiger-Pouvreau V, Jégou C, Cérantola S, Guérard F, Le LK. Phlorotannins in Sargassaceae species from Brittany (France): : Interesting molecules for ecophysiological and valorisation purposes. Adv Bot Res. 2014;71:379–411.CrossrefGoogle Scholar

  • [12]

    Cicco N, Lanorte MT, Paraggio M, Viggiano M, Lattanzio V. A reproducible, rapid and inexpensive Folin-Ciocalteu micro-method in determining phenolics of plant methanol extracts. Microchem J. 2009;91:107–10.Web of ScienceCrossrefGoogle Scholar

  • [13]

    Zhishen J, Mengcheng T, Jianming W. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem. 1999;64:555–9.CrossrefGoogle Scholar

  • [14]

    Malencić D, Maksimović Z, Popović M, Miladinović J. Polyphenol contents and antioxidant activity of soybean seed extracts. Bioresour Technol. 2008;99:6688–91.PubMedCrossrefWeb of ScienceGoogle Scholar

  • [15]

    Kirby AJ, Schmidt RJ. The antioxidant activity of Chinese herbs for eczema and of placebo herbs — I. J Ethnopharmacol. 1997;56:103–8.CrossrefPubMedGoogle Scholar

  • [16]

    Yildirim A, Mavi A, Kara AA. Determination of antioxidant and antimicrobial activities of Rumex crispus L. extracts. J Agric Food Chem. 2001;49:4083–89.PubMedCrossrefGoogle Scholar

  • [17]

    Koleva II, Van Beek TA, Linssen JPH, De Groot A, Evstatieva LN. Screening of plant extracts for antioxidant activity: a comparative study on three testing methods. Phytochem Anal. 2002;13:8–17.CrossrefPubMedGoogle Scholar

  • [18]

    Carter P. Spectrophotometric determination of serum iron at the submicrogram level with a new reagent (ferrozine). Anal Biochem. 1971;40:450–8.PubMedCrossrefGoogle Scholar

  • [19]

    Chung S-K, Osawa T, Kawakishi S. Hydroxyl Radical-scavenging effects of spices and scavengers from brown mustard (Brassica nigra). Biosci Biotechnol Biochem. 1997;61:118–23.CrossrefGoogle Scholar

  • [20]

    Nakamura Y, Yamamoto N, Sakai K, Okubo A, Yamazaki S, Takano T. Purification and characterization of angiotensin I-converting enzyme inhibitors from sour milk. J Dairy Sci. 1995;78:777–83.CrossrefPubMedGoogle Scholar

  • [21]

    Buege J, Aust S. On the solubilization of NADPH-cytochrome c reductase from rat liver microsomes with crude pancreatic lipase. Biochim Biophys Acta Gen Subj. 1972;286:433–6.CrossrefGoogle Scholar

  • [22]

    Kuda T, Tsunekawa M, Goto H, Araki Y. Antioxidant properties of four edible algae harvested in the Noto Peninsula, Japan. J Food Compos Anal. 2005;18:625–33.CrossrefGoogle Scholar

  • [23]

    Leyton A, Pezoa-Conte R, Barriga A, Buschmannad AH, Mäki-Arvel P, Mikkola JP, et al. Identification and efficient extraction method of phlorotannins from the brown seaweed Macrocystis pyrifera using an orthogonal experimental design. Algal Res. 2016;16:201–8.Web of ScienceCrossrefGoogle Scholar

  • [24]

    Machu L, Misurcova L, Ambrozova JV, Orsavova J, Mlcek J, Sochor J, et al. Phenolic content and antioxidant capacity in algal food products. Molecules. 2015;20:1118–33.PubMedWeb of ScienceCrossrefGoogle Scholar

  • [25]

    Miyashita K, Mikami N, Hosokawa M. Chemical and nutritional characteristics of brown seaweed lipids: A review. J Funct Foods. 2013;5:1507–17.Web of ScienceCrossrefGoogle Scholar

  • [26]

    Tkachenko FP, Maslov II. Fatty acids of total lipids of genus Cystoseira C. Agardh species (Phaeophyta) (Black Sea, Crimea). Int J Algae. 2015;17:193–201.CrossrefGoogle Scholar

  • [27]

    Rajauria G, Foley B, Abu-Ghannam N. Identification and characterization of phenolic antioxidant compounds from brown Irish seaweed Himanthalia elongata using LC-DAD-ESI-MS/MS. Innov Food Sci Emerg Technol. 2016;37:261–8.CrossrefWeb of ScienceGoogle Scholar

  • [28]

    Athukorala Y, You-Jin J. Screening for angiotensin 1-converting enzyme inhibitory activity of Ecklonia cava. J Food Sci Nutr. 2005;10:690–756.Google Scholar

  • [29]

    Cha SH, Lee KW, Jeon YJ. Screening of extracts from red algae in Jeju for potentials marine angiotensin-I converting enzyme (ACE) inhibitory activity. Algae. 2006;21:343–8.CrossrefGoogle Scholar

  • [30]

    Wijesinghe WAJP, Ko S-C, Jeon Y-J. Effect of phlorotannins isolated from Ecklonia cava on angiotensin I-converting enzyme (ACE) inhibitory activity. Nutr Res Pract. 2011;5:93.CrossrefPubMedWeb of ScienceGoogle Scholar

  • [31]

    Shibata T, Yamaguchi K, Nagayama K, Kawaguchi S, Nakamura T. Inhibitory activity of brown algal phlorotannins against glycosidases from the viscera of the turban shell Turbo cornutus. Eur J Phycol. 2002;37:493–500.CrossrefGoogle Scholar

  • [32]

    Hidalgo M, Martin-Santamaria S, Recio I, Sanchez–Moreno C, de Pascual–Teresa B, Rimbach G, et al. Potential anti-inflammatory, anti-adhesive, anti/estrogenic, and angiotensin-converting enzyme inhibitory activities of anthocyanins and their gut metabolites. Genes Nutr. 2012;7:295–306.Web of ScienceCrossrefPubMedGoogle Scholar

  • [33]

    Jassbi AR, Mohabati M, Eslami S, Sohrabipour J, Miri R. Biological activity and chemical constituents of red and brown algae from the Persian Gulf. Iran J Pharm Res IJPR. 2013;12:339–48.Google Scholar

  • [34]

    Abdullah NS, Muhamad S, Omar IC, Abdullah H Radical scavenging activity and total phenolic content of Gracilaria manilaensis extracts. In: Technology, Science, Social Sciences and Humanities International Conference 2012; 2012.Google Scholar

  • [35]

    Chew YL, Lim YY, Omar M, Khoo KS. Antioxidant activity of three edible seaweeds from two areas in South East Asia. Lwt-Food Sci Technol. 2008;41:1067–72.Web of ScienceCrossrefGoogle Scholar

  • [36]

    O’Sullivan AM, O’Callaghan YC, O’Grady MN, Queguineur B, Hanniffy D, Troy DJ, et al. In vitro and cellular antioxidant activities of seaweed extracts prepared from five brown seaweeds harvested in spring from the west coast of Ireland. Food Chem. 2011;126:1064–70.Web of ScienceCrossrefGoogle Scholar

  • [37]

    Ahn GN, Kim KN, Cha SH, Song CB, Lee J, Heo MS, et al. Antioxidant activities of phlorotannins purified from Ecklonia cava on free radical scavenging using ESR and H2O2-mediated DNA damage. Eur Food Res Technol. 2006;226:71–9.Web of ScienceGoogle Scholar

  • [38]

    Ye D, Jiang Z, Zheng F, Wang H, Zhang Y, Gao F, et al. Optimized extraction of polysaccharides from Grateloupia livida (Harv.) Yamada and biological activities. Molecules. 2015;20:16817–32.CrossrefWeb of ScienceGoogle Scholar

  • [39]

    Yuan YV, Bone DE, Carrington MF. Antioxidant activity of dulse (Palmaria palmata) extract evaluated in vitro. Food Chem. 2005;91:485–94.CrossrefGoogle Scholar

  • [40]

    Wang T, Jónsdóttir R, Ólafsdóttir G. Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem. 2009;116:240–48.Web of ScienceCrossrefGoogle Scholar

  • [41]

    Berardo A, De Maere H, Stavropoulou DA, Rysman T, Leroy F, De Smet S. Effect of sodium ascorbate and sodium nitrite on protein and lipid oxidation in dry fermented sausages. Meat Sci. 2016;121:359–364.PubMedWeb of ScienceCrossrefGoogle Scholar

  • [42]

    Fernández J, Pérez-Álvarez JA, Fernández-López JA. Thiobarbituric acid test for monitoring lipid oxidation in meat. Food Chem. 1997;59:345–53.CrossrefGoogle Scholar

About the article

Published Online: 2017-10-21

Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

Research funding: None declared.

Employment or leadership: None declared.

Honorarium: None declared.

Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

Citation Information: Journal of Complementary and Integrative Medicine, Volume 15, Issue 1, 20170061, ISSN (Online) 1553-3840, DOI: https://doi.org/10.1515/jcim-2017-0061.

Export Citation

© 2018 Walter de Gruyter GmbH, Berlin/Boston.Get Permission

Comments (0)

Please log in or register to comment.
Log in