Abstract
Purpose
Palmaria palmata (P. Palmata) is reported to contain anti-inflammatory and antioxidant compounds albeit no study has investigated these effects in humans.
Methods
A randomised parallel placebo-controlled human intervention study was carried out to investigate the effect of consuming P. Palmata (5 g/day) incorporated into a bread on serum markers of inflammation [C-reactive protein (CRP); cytokine analysis] with secondary analysis investigating changes in lipids (cholesterol, triglycerides), thyroid function [thyroid-stimulating hormone (TSH)] and antioxidant status ferric reducing antioxidant power. ANCOVA with baseline values as covariates, controlling for age, BMI, sex and smoking status, was used to compare differences between treatment groups over time . In vitro studies investigated the inflammatory activity of P. Palmata extracts (hot water, cold water and ethanol extract), protein extracts and associated protein hydrolysates using a Caco-2 inflammation cell model.
Results
Consumption of P. Palmata-enriched bread significantly increased serum CRP (+16.1 %, P = 0.011), triglycerides (+31.9 %, P = 0.001) and TSH (+17.2 %, P = 0.017) when compared to the control group. In vitro evaluation of P. palmata extracts and protein hydrolysates identified a significant induction of IL-8 secretion by Caco-2 cells, and the hot water P. palmata extract was shown to increase adipocyte glycerol release (P < 0.05).
Conclusion
Evidence from this human study suggests that P. palmata stimulates inflammation, increases serum triglycerides and alters thyroid function; however, these changes are not likely to impact health as changes remained within the normal clinical range. The data from the in vitro study provided indications that IL-8 may contribute to the apparent immunostimulation noted in the human study.
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References
Yang YJ, Nam SJ, Kong G, Kim MK (2010) A case–control study on seaweed consumption and the risk of breast cancer. Br J Nutr 103(9):1345
Matsumura Y (2001) Nutrition trends in Japan. Asia Pac J Clin Nutr 10:S40–S47
Mouritsen OG, Dawczynski C, Duelund L, Jahreis G, Vetter W, Schröder M (2013) On the human consumption of the red seaweed dulse (Palmaria palmata (L.) Weber & Mohr). J Appl Phycol 25(6):1777–1791
Lordan S, Ross RP, Stanton C (2011) Marine bioactives as functional food ingredients: potential to reduce the incidence of chronic diseases. Marine Drugs 9(6):1056–1100
Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23(3):543–597
Okai Y, Higashi-Okai K (1997) Potent anti-inflammatory activity of pheophytin a derived from edible green alga, Enteromorpha prolifera (Sujiao-nori). Int J Immunopharmacol 19(6):355–358
Kazłowska K, Hsu T, Hou CC, Yang WC, Tsai GJ (2010) Anti-inflammatory properties of phenolic compounds and crude extract from Porphyra dentata. J Ethnopharmacol 128(1):123–130
Cox S, Abu-Ghannam N, Gupta S (2010) An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. Int Food Res J 17:205–220
Brown EM, Allsopp PJ, Magee PJ, Gill CI, Nitecki S, Strain CR, McSorley EM (2014) Seaweed and human health. Nutr Rev 72(3):205–216
Park EJ, Pezzuto JM (2013) Antioxidant marine products in cancer chemoprevention. Antioxid Redox Signal 19(2):115–138
Rhatigan P. (2009). Irish Seaweed Kitchen. The comprehensive guide to healthy everyday cooking with seaweeds. Booklink. Holywood, pp 288
MacArtain P, Gill CI, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65(12):535–543
Jung WK, Choi I, Oh S, Park SG, Seo SK, Lee SW, Choi IW (2009) Anti-asthmatic effect of marine red alga Laurencia undulata polyphenolic extracts in a murine model of asthma. Food Chem Toxicol 47(2):293–297
Gómez-Ordóñez E, Jiménez-Escrig A, Rupérez P (2012) Effect of the red seaweed Mastocarpus stellatus intake on lipid metabolism and antioxidant status in healthy Wistar rats. Food Chem 135(2):806–811
Cian RE, Lopez-Posadas R, Drago SR, De Medina FS, Martinez-Augustin O (2012) A Porphyra columbina hydrolysate upregulates IL-10 production in rat macrophages and lymphocytes through an NF-κB, and p38 and JNK dependent mechanism. Food Chem 134(4):1982–1990
Banskota AH, Stefanova R, Sperker S, Lall SP, Craigie JS, Hafting JT, Critchley AT (2014) Polar lipids from the marine macroalga Palmaria palmata inhibit lipopolysaccharide-induced nitric oxide production in RAW264. 7 macrophage cells. Phytochemistry 101:101–108
Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85(3):439–444
Courtois A, Simon-Colin C, Boisset C, Berthou C, Deslandes E, Guézennec J, Bordron A (2008) Floridoside extracted from the red alga Mastocarpus stellatus is a potent activator of the classical complement pathway. Marine drugs 6(3):407–417
Yuan YV, Bone DE, Carrington MF (2005) Antioxidant activity of dulse—P. palmata extract evaluated in vitro. Food Chem 91(3):485–494
Yuan YV, Westcott ND, Hu C, Kitts DD (2009) Mycosporine-like amino acid composition of the edible red alga, Palmaria palmata (dulse) harvested from the west and east coasts of Grand Manan Island, New Brunswick. Food Chem 112(2):321–328
Wang T, Jónsdóttir R, Kristinsson HG, Hreggvidsson GO, Jónsson JÓ, Thorkelsson G, Ólafsdóttir G (2010) Enzyme-enhanced extraction of antioxidant ingredients from red algae Palmaria palmata. LWT-Food Sci Technol 43(9):1387–1393
Tsuge K, Okabe M, Yoshimura T, Sumi T, Tachibana H, Yamada K (2004) Dietary effects of porphyran from Porphyra yezoensis on growth and lipid metabolism of Sprague-Dawley rats. Food Sci Technol Res 10(2):147–151
Matanjun P, Mohamed S, Muhammad K, Mustapha NM (2010) Comparison of cardiovascular protective effects of tropical seaweeds, Kappaphycus alvarezii, Caulerpa lentillifera, and Sargassum polycystum on high-cholesterol/high-fat diet in rats. J Med Food 13(4):792–800
EFSA NDA Panel (EFSA Panel on Panel on Dietetic Products Nutrition and Allergies) (2014) Scientific opinion on dietary reference values for iodine. EFSA J 12(5):3660, 57. doi:10.2903/j.efsa.2014.3660
WHO/UNICEF/ICCIDD. Assessment of iodine deficiency disorders and monitoring their elimination: a guide for programme managers, 2nd ed. Geneva: World Health Organization; 2001. http://whqlibdoc.who.int/hq/2001/WHO_NHD_01.1.pdf. Accessed 20 August 2013
Tsitouras PD, Gucciardo F, Salbe AD, Heward C, Harman SM (2008) High omega-3 fat intake improves insulin sensitivity and reduces CRP and IL6, but does not affect other endocrine axes in healthy older adults. Horm Metab Res 40(3):199–205
Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76
Wilms LC, Boots AW, de Boer VC, Maas LM, Pachen DM, Gottschalk RW, Kleinjans J (2007) Impact of multiple genetic polymorphisms on effects of a 4-week blueberry juice intervention on ex vivo induced lymphocytic DNA damage in human volunteers. Carcinogenesis 28(8):1800–1806
Brevik A, Gaivão I, Medin T, Jørgenesen A, Piasek A, Elilasson J, Collins AR (2011) Supplementation of a western diet with golden kiwifruits (Actinidia chinensis var’.Hort 16A) effects on biomarkers of oxidation damage and antioxidant protection. Nutr J 10(1):1–9
Tremblay AJ, Morrissette H, Gagné JM, Bergeron J, Gagné C, Couture P (2004) Validation of the Friedewald formula for the determination of low-density lipoprotein cholesterol compared with β-quantification in a large population. Clin Biochem 37(9):785–790
Harnedy PA, FitzGerald RJ (2013) In vitro assessment of the cardioprotective, anti-diabetic and antioxidant potential of Palmaria palmata protein hydrolysates. J Appl Phycol 25:1793–1806
Bahar B, O’Doherty JV, Sweeney T (2011) A potential role of IL-6 in the chito-oligosaccharide-mediated inhibition of adipogenesis. Br J Nutr 106(08):1142–1153
Price RK, Wallace JM, Hamill LL, Keaveney EM, Strain JJ, Parker MJ, Welch RW (2012) Evaluation of the effect of wheat aleurone-rich foods on markers of antioxidant status, inflammation and endothelial function in apparently healthy men and women. Br J Nutr 108(09):1644–1651
Mishra VK, Temelli F, Ooraikul B, Shacklock PF, Craigie JS (1993) Lipids of the red alga, Palmaria palmata. Botanica Marina 36(2):169–174
Huber GM, Vasantha Rupasinghe HP, Shahidi F (2009) Inhibition of oxidation of omega-3 polyunsaturated fatty acids and fish oil by quercetin glycosides. Food Chem 117(2):290–295
Boekholdt SM, Peters RJ, Hack CE, Day NE, Luben R, Bingham SA, Khaw KT (2004) IL-8 plasma concentrations and the risk of future coronary artery disease in apparently healthy men and women the EPIC-norfolk prospective population study. Arterioscler Thromb Vasc Biol 24(8):1503–1508
Esser D, Vandijk SJ, Oosterink E, Müller M, Afman LA (2013) A High-Fat SFA, MUFA, or n3 PUFA challenge affects the vascular response and initiates an activated state of cellular adherence in lean and obese middle-aged men. J Nutr 143(6):843–851
Elliott P, Chambers JC, Zhang W, Clarke R, Hopewell JC, Peden JF, Kooner JS (2009) Genetic loci associated with C-reactive protein levels and risk of coronary heart disease. JAMA 302(1):37–48
Zhang YQ, Tsai YC, Monie A, Hung CF, Wu TC (2010) Carrageenan as an adjuvant to enhance peptide-based vaccine potency. Vaccine 28(32):5212–5219
Bondu S, Cerantola S, Kervarec N, Deslandes E (2009) Impact of the salt stress on the photosynthetic carbon flux and 13 C-label distribution within floridoside and digeneaside in Solieria chordalis. Phytochemistry 70(2):173–184
Wiencke C, Läuchili A (1981) Inorganic ions and floridoside as osmotic solutes in Porphyra umbilicalis. Zeitschrift für Pflanzenphysiologie 103(3):247–258
Zha XQ, Xiao JJ, Zhang HN, Wang JH, Pan LH, Yang XF, Luo JP (2012) Polysaccharides in Laminaria japonica (LP): extraction, physicochemical properties and their hypolipidemic activities in diet-induced mouse model of atherosclerosis. Food Chem 134(1):244–252
Ara J, Sultana V, Qasim R, Ahmad VU (2002) Hypolipidaemic activity of seaweed from Karachi coast. Phytother Res 16(5):479–483
Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16(4):245–262
Brown L, Rosner B, Willett WW, Sacks FM (1999) Cholesterol-lowering effects of dietary fiber: a meta-analysis. Am J Clin Nutr 69(1):30–42
Kaczmarczyk MM, Miller MJ, Freund GG (2012) The health benefits of dietary fiber: beyond the usual suspects of type 2 diabetes mellitus, cardiovascular disease and colon cancer. Metab, Clin Exp 61(8):1058–1066
Ruxton CHS, Reed SC, Simpson MJA, Millington KJ (2004) The health benefits of omega-3 polyunsaturated fatty acids: a review of the evidence. J Hum Nutr Diet 17(5):449–459
Harris WS (1997) n-3 fatty acids and serum lipoproteins: human studies. Am J Clin Nutr 65(5):1645S–1654S
Kris-Etherton PM, Harris WS, Appel LJ (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106(21):2747–2757
Murad MH, Hazem A, Coto-Yglesias F, Dzyubak S, Gupta S, Bancos I, Montori VM (2012) The association of hypertriglyceridemia with cardiovascular events and pancreatitis: a systematic review and meta-analysis. BMC Endocr Disord 12(1):2
Takeuchi F, Isono M, Katsuya T, Yokota M, Yamamoto K, Nabika T, Kato N (2012) Association of genetic variants influencing lipid levels with coronary artery disease in Japanese individuals. PLoS ONE 7(9):e46385
Chapman MJ, Ginsberg HN, Amarenco P, Andreotti F, Borén J, Catapano AL, Watts GF (2011) Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol in patients at high risk of cardiovascular disease: evidence and guidance for management. Eur Heart J 32(11):1345–1361
Åsvold BO, Vatten LJ, Nilsen TI, Bjøro T (2007) The association between TSH within the reference range and serum lipid concentrations in a population-based study, The HUNT study. Eur J Endocrinol 156(2):181–186
Li M, Eastman CJ (2012) The changing epidemiology of iodine deficiency. Nature reviews. Endocrinology 8(7):434–440
Wigmore SJ, Fearon KC, Maingay JP et al (1997) Interleukin-8 can mediate acute-phase protein production by isolated human hepatocytes. Am J Physiol 273:E720–E726
Acknowledgments
This project (Grant Aid Agreement No. MFFRI/07/01) is carried out under the Sea Change Strategy with the support of the Irish Marine Institute and the Department of Agriculture, Food and the Marine, funded under the National Development Plan 2007–2013.
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Allsopp, P., Crowe, W., Bahar, B. et al. The effect of consuming Palmaria palmata-enriched bread on inflammatory markers, antioxidant status, lipid profile and thyroid function in a randomised placebo-controlled intervention trial in healthy adults. Eur J Nutr 55, 1951–1962 (2016). https://doi.org/10.1007/s00394-015-1011-1
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DOI: https://doi.org/10.1007/s00394-015-1011-1