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Seaweed in Health and Disease Prevention Edited by Joël Fleurence Ira Levine AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, UK 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, USA The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Copyright © 2016 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers may always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN: 978-0-12-802772-1 For information on all Academic Press publications visit our website at https://www.elsevier.com/ Publisher: Nikki Levy Acquisition Editor: Megan Ball Editorial Project Manager: Billie Jean Fernandez Production Project Manager: Jason Mitchell Designer: Mark Rogers Typeset by TNQ Books and Journals www.tnq.co.in Dedication To my sons Julien and Simon for the joy and the happiness that they bring to my life. —Joël Fleurence To Dr. Patricia Bonamo for her faith in playing a hunch. To MILKS for their loving support and to my wife and best friend Laurie. —Ira Levine List of Contributors E. Ar Gall University of Brest, Brest, France J.-M. Bard University of Nantes, Nantes, France P. Baweja University of Delhi, Delhi, India N. Bourgougnon UBS, IUEM, Vannes, France D. Cheney Northeastern University, Nahant, MA, United States L. Coiffard University of Nantes, Nantes, France C. Couteau University of Nantes, Nantes, France A. Couzinet-Mossion University of Nantes, Nantes, France C. Dawes University of South Florida, Tampa, FL, United States A. Delaney Aalborg University, Aalborg, Denmark P. Déléris University of Nantes, Nantes, France E. Deslandes IUEM-UBO, Technopôle Brest-Iroise, Plouzané, France J. Dumay University of Nantes, Nantes, France J. Fleurence University of Nantes, Nantes, France K. Frangoudes Université de Brest, UMR AMURE, Brest, France S.-A. Ii Miyazaki Municipal University, Miyazaki, Japan M. Kendel Bureau d’Etudes et Conseil, Vannes, France S. Kraan Ocean Harvest Technology, Milltown, Ireland xv xvi List of Contributors S. Kumar University of Delhi, Delhi, India I. Levine University of Southern Maine, Lewiston, ME, United States M. Morançais University of Nantes, Nantes, France H. Nazih University of Nantes, Nantes, France D. Sahoo University of Delhi, Delhi, India V. Stiger-Pouvreau IUEM-UBO, Technopôle Brest-Iroise, Plouzané, France C. Vonthron-Sénécheau University of Strasbourg, Strasbourg, France G. Wielgosz-Collin University of Nantes, Nantes, France About the Editors Dr. Ira A. Levine, PhD, is a tenured professor of natural and applied sciences at the University of Southern Maine, Chairperson of the USM Lewiston Auburn College Faculty, and Director of the USM, LAC Aquatic Research Lab (algal genetic engineer- ing, physiological ecology, and new product devel- opment). In addition, Dr. Levine is the President and Board Chair of the Algae Foundation and President and Board Chair of Professors Beyond Borders. Dr. Levine was awarded a 2009–10 US State Department, Fulbright New Century Scholar and in 2007–08 was a visiting professor of biology at Duke University. Dr. Levine combines 30 years of applied and basic research in molecular, physiological ecology, and cultivation of algae, aquatic farming management, and aquaculture engineering. Dr. Levine’s farming experience includes open-ocean and pond cultivation in Canada, China, Indonesia, Japan, Malaysia, the Philippines, and the United States (Hawaii, Florida, and Maine). Current efforts include algal cultivar enhancement for aquaculture and agriculture feed supplementa- tion, human nutraceuticals and cosmaceuticals, fine chemicals, and plant-based biofuels. Dr. Joel Fleurence, PhD, is a professor of marine biology and biochemistry at Nantes University. He is one of two directors of the Research Laboratory “Sea, Molecules, Health.” He has been a member of the University National Council since 2007 and was elected vice-president of the section “Biology of Organisms” in 2011. He is a senior scientist and an international expert on seaweed valorization (100 international publications including patents). In 1985, he began his research career in the pharma- ceutical industry in the French company Roussel- Uclaf. In 1990, he was recruited by the Institute of Valorisation of Seaweeds (CEVA, Brittany, France) to lead research into the chemical composition and nutritional properties of macroalgae. Professor Fleurence has participated in the establishment of the French regula- tion on marine algae used as sea vegetables. In 1994, he was appointed head of the laboratory “Proteins and Quality” at Ifremer (Research French Organism for the Sea Exploitation) and developed research on the nutritional properties of seaweed protein for use in human or animal food. Since 2002, he has been working as a professor at the University of Nantes and leads research on the development of seaweed uses as protein or pigment sources for industry. xvii Acknowledgment The editors thank Mr. O. Barbaroux for the photographs of seaweed factories and markets. xix CHAPTER 1 Algae: A Way of Life and Health I. Levine University of Southern Maine, Lewiston, ME, United States “Vilor alga” (translated as “more vile or worthless than algae”), wrote Virgil, the Latin Poet, in 30 BC. Civilization was aware of the role of algae in the human condi- tion long before Virgil. The use of macroalgae dates back to Shen Nung, the father of husbandry and medicine, approximately 3000 BC (Doty, 1979). Seaweeds were reported to be utilized in Iceland in 960 BC, the Chinese Book of Poetry (800–600 BC) praised housewives for cooking with algae, and the Chinese Materia Medica (600 BC) refers to algae as follows: “Some algae are a delicacy fit for the most honorable guest, even for the King himself” (Porterfield, 1922; Wood, 1974). Macroalgae (seaweeds) are a diverse group of predominantly marine, multicel- lular, photosynthetic, chlorophyll “a”-containing, eukaryotic organisms, lacking true roots, stems, and leaves with simple reproductive structures and found from the intertidal zone to 300-m deep. The macroalgae or seaweeds are evolutionarily diverse and are found in two kingdoms, Plantae and Chromista, and four phyla, Cha- rophyta (Chara), Chlorophyta (green), Rhodophyta (red), and Ochrophyta (brown). The approximately 10,000 described marine macroalgal species are segregated by photosynthetic pigment content, carbohydrate food reserve, cell wall components, and flagella construction and orientation. This eclectic group has evolved over the last 600–900 million years occupying a variety of ecological niches, ie, attached to hard substrata, unconsolidated sand and mud, other algae, seagrasses, free floating, and, on rare occasions, parasitic. There are many additional groups of algae, known collectively as microalgae, including but not limited to the blue green bacteria (eg, Spirulina sp.), diatoms, and dinoflagellates, which can form biofilms, colonial for- mations, and turfs. Occasionally these formations are considered “macroalgae,” but for the purpose of this text they lie outside of the scope of this book. Early examples of utilization of seaweeds for medicinal purposes include the Chinese use of Sargassum for goiter (16th century, Chinese herbal, “Pen Tsae Kan Mu”), Gelidium for intestinal afflictions, and Laminaria for the dilation of the cervix in difficult child births (Dawson, 1966). The Japanese’s lack of goiter (one case/mil- lion people) is contributed to their large consumption of seaweed and their iodine concentration. Oriental seaweed iodine concentrations range from 18 to 1600 mg/kg dry weight (Chapman and Chapman, 1980). Agar, a phycocolloidal extract from commercial red algae, eg, Gracilaria, has been used since the 17th century as a Seaweed in Health and Disease Prevention. http://dx.doi.org/10.1016/B978-0-12-802772-1.00001-4 1 Copyright © 2016 Elsevier Inc. All rights reserved. 2 CHAPTER 1 Algae: A Way of Life and Health laxative and is perhaps the world’s first diet fad. In addition, during times of war, agar was utilized as a wound dressing because of its antiblood-clotting activity allow- ing wounds to be appropriately disinfected. Subsequently, agar was identified as the ideal substrate for culturing bacteria, assisting with the foundational research into the microbial world. Brown algal phycocolloidal extracts, alginate and algin, have been used in the binding of pills and ointments, cholesterol reduction, as a hemostatic agent (control of bleeding), and have replaced agar as the primary dental mold gel. The ancient Greeks utilized red algae as a vermifuge, thought to be the same alga rediscovered on Corsica in 1775, known as Corsican moss. Finally, a common alga from both North America and Europe, Chondrus crispus, a red alga, has been used as a remedy for urinary tract infections, diarrhea, breast infections, and tuberculosis (Dawson, 1966). Additional traditional algal uses as medicines include: dulse (Palmaria palmata) extract used to assist in breaking of fevers (18th-century England), bull kelp steam extract used to fight headaches (Alaska, USA), Durvillaea as a cure for scabies (New Zealand), and antifungal and antibiotic compounds from the brown, green and red algae (Chapman and Chapman, 1980). The inclusion of large amounts of seaweeds in a balanced diet has been connected to decreased rates of many of the “Western lifestyle” diseases (eg, cancer, cardiovas- cular diseases). Reduced rates of breast cancer in postmenopausal Japanese women are thought to be connected to the ingestion of seaweeds in general and the kelps Kombu and Wakame in particular. Potential mechanisms include: increased fiber influence on fecal bulk and bowel transit time, alteration of posthepatic metabolism of sterols, antibiotic and enzymatic influence on enteric bacterial populations, and increased immune response (Teas, 1983, as reported in Erhart, 2015a). Additional research efforts include (1) a 95% reduction in cancer rates when fed a hot water- extracted kelp powder and (2) apoptosis of stomach, colon, and leukemia cancer cells by F- and U-fucoidan-sulfated polysaccharides from kelps (Yamamoto et al., 1986 and Anonymous, 1990–1996, as reported in MCSV Cancer Prevention and Treat- ment bulletin). Miller (2008 as reported in Erhart, 2015b) reported an increase in fibrocystic breast disease in American women rose from 3% to 90% in the 1920s and 2000s, respectively. In addition, he infers that 15% of American women experi- ence iodine deficiencies and the same percentage of American women develop breast cancer; however, Japanese women experience the lowest cancer rates by including 200 times as much iodine per day as their American counterparts (45,000 μg/day and 240 μg/day, respectively). Dr. Miller hypothesizes that both fibrocystic disease and breast cancer are iodine deficiency disorders. Kelps provide some of the highest amounts of bioavailable iodine, up to 18,000 times as much as fresh vegetables. As a young man coming from New York City, seaweeds were considered to be just a smelly mess found on the beach but after 10 years of studying algae in Hawaii, the author has embraced his Hawaiian roots and uses the term “limu,” which accord- ing to Pukui and Elbert (1977) as reported by Abbott (1984) is: “a general name for all kinds of plants living under water, both fresh and salt, also algae growing in any damp place in the air, as on the ground, rocks, and on other plants; also mosses, liv- erworts and lichens…” However, for most Hawaiians, limu means edible seaweeds Algae: A Way of Life and Health 3 (Abbott, 1984). Along with fish and poi, limu constituted the troika of the Hawaiian balanced diet, providing vitamins A, B, C, minerals (iodine), and protein. Histori- cal Hawaiian limu usage included the treatment of coral cuts, representing a nearly instant infection, which were historically treated with Sargassum, similar to the traditional use of mosses as a poultice. In addition, seaweeds were used in religious ceremonies (burial cleansing rituals), cultural celebrations (weddings and hula dancing), and family celebrations. “Is Seaweed the New Lobster?” was a headline from the March 2015 edition of Down East: The Magazine of Maine; quite a transformation from the “the stuff washed up on the beach, which tends to be rotting and full of flies” (Sneddon, 2015). Maine, a maritime-based state in the northeastern corner of the United States, has a long history of seaweed utilization dating back to its colonial period and beyond, when marine macroalgae were referred to as “sea manure” (Sneddon, 2015). As algae in general and seaweeds in particular have played an ever-increasing role in the human diet, health, and well-being, its utilization and product development have rapidly expanded our appreciation for its diversity of uses. As with lobsters, which were plentiful and served up as food for the state’s prisoner population, seaweeds have been experiencing a frameshift from the smelly stuff on the beach to a source of valued balanced nutrition. Shep Erhart, the founder of Maine Coast Sea Vegetables, is a pioneer of seaweed utilization in the United States and has dedicated his life to the development and marketing of seaweed products throughout America and beyond. In the 1970s he realized the potential for seaweeds as a complete source of colloidal, chelated miner- als, trace elements, and vitamins to replace the loss of these nutrients from processed food products. “Some people who are mineral deficient get around it and they go crazy…It can kind of buzz you out because it is so energizing” (Shep Erhart, quoted from Sneddon, 2015). “The Road from Science Geek to Being Cool, Algal Physiological Ecology: a Global Economic Development Engine” is the title of a seminar given by the author at Middlebury College, Middlebury, Vermont, USA, in March 2010. How does one become “cool” being a phycologist (someone who studies algae)? Kaitlynn Levine, a Middlebury College molecular biology major, coined the phrase after algae and algal- based biofuels became a research and development priority in the United States during the 21st century. If studying algae, previous to renewed interests, was held in such disregard or benign neglect, then why would anyone dedicate his or her life to algae? Phycology has a long history of remarkable, dedicated scientists and lay practitioners who have advanced our algal-based knowledge through their tireless field and labora- tory efforts. Massive algal collections were assembled and herbarium libraries estab- lished at universities (eg, Harvard University, Cambridge, Massachusetts) and museums (eg, Bishop Museum, Honolulu, Hawaii). Meticulous anatomical, reproductive, and systematic treatises were published expanding our body of knowledge. Biotechnologi- cal methodologies were incorporated into current molecular, genomic, ultrastructural, physiological ecology, and biochemical studies advancing our understanding of the biology, ecology, systematics, and commercial value of algae. Algae represent a field

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