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WHOLE GRAINS AND HEALTH
The updated guide to whole grains and their integral role in nutritional health
In an increasingly health-conscious society, the potential benefits of whole grain products are of paramount importance to manufacturers, dieticians, and consumers alike. Whole Grains and Health covers all aspects of this crucial topic, presenting a data-driven study of whole grains’ functional components, associated biomarkers and overall impact upon human health. Now in its second edition, the text has been revised and expanded to include six new chapters and groundbreaking new data. This essential guide features:
- Summaries of large research projects on the health effects of whole grain in Europe and the US
- New data on the associations between whole grain consumption and risk of developing chronic diseases
- Discussions of metabolomics and their use in addressing health effects and finding new biomarkers of both dietary exposure and health effects related to the diet
- Information on the use of genomics in studies of how gene-expression profiles change in response to whole grain intake
- Newly identified bioactive compounds in whole grains and whole grain fractions
- The new EU regulations on health claims that affect whole grain food products
Providing information that will be of interest to food scientists, healthcare specialists and food industry professionals alike, the second edition of Whole Grains and Health is an essential resource for anyone concerned with the impact whole grains may have upon health.
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Table of Contents
Cover
Title Page
Copyright Page
Preface
Editors’ Biographies
Acknowledgments
Contributing Authors
Supplementary Material
1 The Structure of Cereal Grains and Their Products
1.1 Introduction
1.2 Grain structure
1.3 Embryo
1.4 Endosperm
1.5 Bran
1.6 Rolled cereals and porridge
1.7 Protein network‐based products
1.8 Starch network‐based products
1.9 Conclusions
1.10 References
2 Definition of
Whole Grain
and Determination of Content in Cereal Products
2.1 Introduction
2.2 Definition of
whole grain
in different countries
2.3 Definition of
whole grain food
2.4 Recommendations for intake of whole grain foods
2.5 Dietary recommendations for whole grain intake
2.6 Markers for whole grain wheat and rye content in food
2.7 Effects of processing on whole grain
2.8 References
3 Whole grain Fractions and Their Utilization in Foods
3.1 Introduction
3.2 Cereal technologies to obtain fractions from whole grains
3.3 The starchy endosperm fraction – a good source of energy
3.4 The germ fraction – the most unstable of cereal fractions
3.5 Bran fractions – a source of micronutrients to exploit?
3.6 Innovative fractions
3.7 Conclusion
3.8 References
4 Whole grain Carbohydrates
4.1 Introduction
4.2 General composition of whole grain carbohydrates
4.3 Dietary fibre
4.4 Carbohydrate quality of whole grain foods
4.5 Slow digestion property of starch
4.6 Physical form of whole grain foods
4.7 Digestibility of dietary fibre
4.8 Phytochemicals
4.9 Future perspectives
4.10 References
5 Whole grain Content of Cereal Products
5.1 Introduction
5.2 Why is it important to know the whole grain content of food?
5.3 How can we better measure whole grain content and intake in the future?
5.4 References
6 Whole grain consumption and associated lifestyle and sociodemographic factors
6.1 Introduction
6.2 Global whole grain intake
6.3 Whole grain intake according to Mica et al. (2015)
6.4 Single studies of whole grain intake
6.5 Consumers of whole grains
6.6 Recommendations and compliance with recommendations
6.7 Different cereal and product sources of whole grains
6.8 Factors associated with whole grain intake
6.9 Acknowledgements
6.10 References
7 Alkylresorcinols and Their Metabolites as Biomarkers for Whole grain Wheat and Rye
7.1 Introduction
7.2 What is a biomarker?
7.3 Dietary biomarkers
7.4 Discovery and validation of a biomarker
7.5 Biomarkers of whole grain intake and cereal fibre
7.6 Alkylresorcinols as biomarkers of whole grain wheat and rye
7.7 Analytical methods
7.8 Dose‐response
7.9 Reproducibility
7.10 Relative validity
7.11 Applications
7.12 Interventions
7.13 References
8 Body Composition and Weight Management
8.1 Introduction
8.2 Obesity prevalence around the globe
8.3 Abdominal adiposity and cardiometabolic risk
8.4 Studies investigating the link between body weight and whole grain consumption
8.5 Defining grain ingredients and foods in observational studies
8.6 Defining grain ingredients and foods in intervention studies
8.7 Evidence from observational studies
8.8 Intervention studies
8.9 Studies without calorie‐restriction
8.10 Studies with calorie‐restriction
8.11 Proposed mechanism of action by which whole grains influence weight gain
8.12 Conclusion
8.13 Acknowledgements
8.14 References
9 Whole Grains and Type 2 Diabetes
9.1 Introduction
9.2 Evidence from epidemiological studies
9.3 Evidence from randomized controlled trials
9.4 Potential biological mechanisms
9.5 Conclusions and future directions
References
10 Whole Grains and Cardiovascular Disease
10.1 Introduction
10.2 Whole grains and CVD
10.3 Summary
10.4 References
11 Whole Grains and Cancer Risk
11.1 Introduction
11.2 Diet and cancer
11.3 Dietary fibre and colorectal cancer risk
11.4 Possible cancer protective mechanisms
11.5 Colorectal cancer
11.6 Breast cancer
11.7 Other cancers
11.8 Cancer patients and prognosis
11.9 Epidemiological evidence – colorectal cancer
11.10 Epidemiological evidence – breast cancer
11.11 Epidemiological evidence – prostate cancer
11.12 Epidemiological evidence – endometrial cancer
11.13 Epidemiological evidence – stomach cancer
11.14 Epidemiological evidence – whole grains and cancer prognosis
11.15 Conclusion
11.16 Acknowledgments
11.17 References
12 Whole Grain Intake and Mortality
12.1 Introduction
12.2 Epidemiological evidence
12.3 Types of whole grain products and varieties of grain
12.4 Dietary patterns with whole grains and mortality
12.5 Human intervention studies
12.6 Cell and animal studies
12.7 Conclusion
12.8 References
13 Whole Grains and Appetite
13.1 Introduction
13.2 Acute effects of whole grain intake on appetite
13.3 Potential mechanisms of acute effects of whole grain intake on appetite
13.4 Impact of whole grain characteristics on appetite and suggested mechanisms
13.5 Second‐meal effects of whole grain intake on appetite
13.6 Influence of whole grain characteristics on appetite and suggested mechanisms
13.7 Long‐term effects of regular whole grain intake on appetite
13.8 Concluding remarks
13.9 References
14 Modulating Glycaemia with Cereal Products
14.1 Introduction
14.2 Postprandial glucose fluxes and hormonal responses determining glycaemia
14.3 Postprandial glucose fluxes – monitoring with the stable isotope technique
14.4 Glycaemia and underlying glucose fluxes – results of isotope studies
14.5 Food factors influencing GIP release
14.6 Food factors influencing GLP‐1 release
14.7 Conclusion
14.8 General implications
14.9 References
15 Whole Grains, Cereal Fibre and the Gut Function
15.1 Introduction
15.2 Whole grains and influence on gut physiology
15.3 The intestinal gut microbiome
15.4 Microbial fermentation end‐products and their impact for gut function
15.5 Microbiome mediated benefits of whole grain consumption
15.6 References
16 Bioactive Compounds in Whole Grains and Their Implications for Health
16.1 Introduction
16.2 Folate
16.3 Glycine betaine, choline and trigonelline
16.4 Tocopherols and tocotrienols
16.5 Carotenoids
16.6 Plant Sterols
16.7 Inositol phosphates
16.8 Lignans
16.9 Phenolic acids
16.10 Avenanthramides
16.11 Benzoxazinoids
16.12 Alkylresorcinols
16.13 References
17 Potential Negative Effects of Whole grain Consumption
17.1 Introduction
17.2 Allergies associated with grain intake
17.3 Non‐allergic conditions associated with wheat, barley and rye intake
17.4 The heavy metal cadmium
17.5 The mineral absorption inhibitor phytate
17.6 Anti‐nutrient properties of phenolic compounds
17.7 The heat‐induced toxicant acrylamide
17.8 Conclusion and future perspectives
17.9 References
18 Application of Metabolomics for the Assessment of Process‐induced Changes in Whole Grain Foods
18.1 Introduction
18.2 Targeted versus untargeted approaches
18.3 Bioactive compounds present in whole grain cereals
18.4 Processing of grains
18.5 Milling
18.6 Germination and malting
18.7 Soaking/hydrothermal processing of grains
18.8 Baking and roasting
18.9 Pasta processing and extrusion cooking
18.10 Fermentation and bioprocessing
18.11 Bioactives in human intervention studies
18.12 Conclusion
18.13 References
19 Application of Metabolomics for the Assessment of Health Effects of Whole grain Foods
19.1 Introduction
19.2 Study designs
19.3 Metabolomics in epidemiological studies on whole grains and health
19.4 Whole grain research on animal models utilizing metabolomics
19.5 Conclusion and future prospects
19.6 References
20 Using Transcriptomics and RNA Sequencing to Assess Health Effects of Whole Grains
20.1 Introduction
20.2 Transcriptomics and RNA sequencing
20.3 Effects of whole grains on gene expression
20.4 Conclusion
20.5 References
21 Whole Grains from an Industry Perspective
21.1 Introduction
21.2 Whole grains in foods
21.3 Whole grain raw materials
21.4 Whole grains in manufactured foods
21.5 Whole grains in extruded products
21.6 Sensory characteristics
21.7 Whole grains and food safety
21.8 Outlook and research needs
21.9 References
22 Global Regulation and Labeling, Claims and Communication with Consumers
22.1 Introduction
22.2 Global regulation on whole grain labelling
22.3 Nutrition and health claims
22.4 Communication with consumers
22.5 Conclusion
22.6 Acknowledgments
22.7 References
Summary
The future of whole grains and health
Index
End User License Agreement
List of Tables
f03
Table 1 Brief description of the content of the sections.
Chapter 4
Table 4.1 Classification of whole grain carbohydrates.
Table 4.2 The composition of whole grain carbohydrates (% dry weight) (Choct ...
Chapter 5
Table 5.1 Flour content and potential contribution to whole grain intake of c...
Chapter 6
Table 6.1 Whole grain intake in different countries, means with standard devi...
Table 6.2 Estimated share of population consuming whole grains. If data were ...
Table 6.3 Whole grain dietary recommendations and compliance with recommendat...
Table 6.4 Whole grain cereal and product sources in different populations. In...
Chapter 7
Table 7.1 Content of AR in cereal grains, bran and WG products of rye, wheat ...
Table 7.2 Analytical methods for quantification of AR and their metabolites i...
Table 7.3 Dose‐response relationship of plasma AR in controlled intervention ...
Table 7.4 Reproducibility of AR and their metabolites.
Table 7.5 Relationships between reported intake of WG or rye products and AR ...
Table 7.6 Relationships between reported intake of cereal fibre and AR or the...
Table 7.7 Observational studies utilizing AR as surrogate measures of whole g...
Chapter 8
Table 8.1 Cross‐sectional evidence: Relationship between higher intakes of wh...
Table 8.2 Cross‐sectional evidence: Relationship between higher intakes of wh...
Table 8.3 Longitudinal cohorts examining the relationship between whole grain...
Table 8.4 Intervention studies investigating the effect of whole grain intake...
Chapter 9
Table 9.1 Prospective studies on the association of whole grains with type 2 ...
Table 9.2 Cross‐sectional studies on the association of whole grain intakes a...
Table 9.3 Randomized controlled trials on the effect of whole grain intake on...
Chapter 10
Table 10.1 Suggested beneficial components and potential mechanisms for benef...
Table 10.2 Whole grain (WG) dietary intervention studies completed since 2010...
Chapter 11
Table 11.1 Percentage of different cancer types worldwide and in Europe and A...
Table 11.2 Cohort studies on whole grains and colorectal cancer (in chronolog...
Chapter 12
Table 12.1 Papers on intake of whole grains and mortality. Results are for co...
Chapter 13
Table 13.1 Randomized, cross‐over studies investigating the effect of whole g...
Table 13.2 Randomized, cross‐over studies investigating the effect of whole g...
Table 13.3 Intervention studies investigating the effect of regular whole gra...
Chapter 14
Table 14.1 Overview location and mode of stimulation of GIP and GLP‐1 (derive...
Chapter 15
Table 15.1 Reported mean retention time (MRT) or mean transit time (MTT) h in...
Chapter 16
Table 16.1 Average contents of folate, tocols, sterols and phenolic acids in ...
Chapter 17
Table 17.1 Classes and examples of components of whole grains with possible a...
Table 17.2 Cadmium content in different whole grain products.
Table 17.3 Estimated phenolic acid content in selected whole grain cereals (m...
Table 17.4 Acrylamide levels in different food groups and their relative cont...
Chapter 18
Table 18.1 Widely used technologies for metabolomic analysis of whole grains ...
Chapter 19
Table 19.1 Metabolomics applications investigating the impact of a whole grai...
Chapter 21
Table 21.1 Average weekly sales (AWS) of bakery and breakfast cereals new lau...
Table 21.2 Composition of cereal grains (g/100 g, average values).
Table 21.3 Particle size of dry‐milled product produced from wheat.
Chapter 22
Table 22.1 Nutrient criteria required of whole grain products using the Nordi...
Table 22.2 Whole grain ingredient claims that can be used in Australia. (Sour...
Table 22.3 Approved health claims meeting significant scientific agreement am...
Table 22.4 Whole grain content criteria required of products using the Danish...
List of Illustrations
Chapter 1
Figure 1.1 A: General structure of a cereal grain); B: Epifluorescence micro...
Figure 1.2 Schematic representation of a typical endosperm cell (A) and micr...
Figure 1.3 Microstructure of rolled rye grain. A: bright field micrograph wi...
Figure 1.4 CLSM images of untreated (A) and 0.01% protease‐treated (B) brown...
Figure 1.5 Representative cross‐sections of 10‐min cooked spaghetti made of ...
Figure 1.6 Cross‐sectional X‐ray tomography images (10 mm × 10 mm) of extrud...
Figure 1.7 Microstructure of rye crisp bread. A1 and A2: Reconstructed X‐ray...
Chapter 3
Figure 3.1 Main fractionation diagrams according to the cereal‐grain structu...
Figure 3.2 Tissue composition of different bran issues obtained from differe...
Figure 3.3 Processing of wheat fractions leads to changes in their structura...
Chapter 4
Figure 4.1 Depiction of plant cell wall structure consisting of cellulose mi...
Figure 4.2 The endosperm cell wall in oats and barley as it contains starch ...
Figure 4.3 The molecular structure of the major non‐starch polysaccharides f...
Figure 4.4 The general structure of arabinoxylan composed of side chains of ...
Figure 4.5 The general structure of cereal mixed linkage (1→3) (1→4)‐β‐D‐glu...
Chapter 6
Figure 6.1 Global and regional mean whole grains consumed (g products/day) i...
Figure 6.2 Mean whole grain daily intake in children/adolescents (g/day) pre...
Figure 6.3 Mean whole grain intake in adults (g/day) in different population...
Figure 6.4 Dietary and lifestyle factors suggested to be associated with who...
Chapter 7
Figure 7.1 Structures and metabolism of AR. AR homologs (1) containing 17‐25...
Figure 7.2 Suggested absorption, distribution, metabolism and excretion of A...
Chapter 12
Figure 12.1 Whole grain consumption and total mortality and cardiovascular m...
Chapter 13
Figure 13.1 Hypothetical mechanistic links between whole grain intake, appet...
Chapter 14
Figure 14.1 Glucose fluxes after a meal determining total blood glucose resp...
Figure 14.2 Total glucose,
2
H‐ and
13
C‐enrichment of glucose after ingestion...
Chapter 15
Figure 15.1 Interactions among diet, microbiota and host immunity, where a s...
Figure 15.2 Schematic illustration of functions provided by the microbiome....
Chapter 16
Figure 16.1 Chemical structures of representatives of major bioactive (compo...
Chapter 18
Figure 18.1 Overview of integrated metabolomics experiment. WG, Whole grain;...
Figure 18.2 Factors influencing cereal product quality. With kind permission fro...
Chapter 21
Figure 21.1 Growth of food and drink products featuring whole grain benefits...
Figure 21.2 Simplified diagram of the Roller milling process.
Figure 21.3 Mechanical actions in roller milling as functions of roller surf...
Figure 21.4 History of milling technology.
Figure 21.5 Process line for extruded breakfast cereals.
Chapter 22
Figure 22.1 The Nordic Keyhole Label.
Figure 22.2 The Canadian Whole Grain Stamp. The stamp comes in three version...
Figure 22.3 The Danish Whole Grain Logo (“Fuldkornsmærket”). The text says “...
Figure 22.4 The Dutch Whole Grain Logo “100% whole grain.”
Figure 22.5 The Singaporean Healthier Choice Symbol.
Figure 22.6 The American Whole Grain Stamp. The stamp comes in three version...
Guide
Cover Page
Title Page
Copyright Page
Preface
Editors’ Biographies
Acknowledgments
Contributing Authors
Supplementary Material
Table of Contents
Begin Reading
Summary
Index
Wiley End User License Agreement
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Whole Grains and Health
Second Edition
Edited by
Rikard Landberg
Head of Division Food and Nutrition ScienceDepartment of Biology and Biological EngineeringChalmers University of TechnologyGothenburg, Sweden
Nathalie Scheers
Food and Nutrition ScienceDepartment of Biology and Biological EngineeringChalmers University of TechnologyGothenburg, Sweden
This second edition first published 2021© 2021 John Wiley & Sons Ltd
Edition History: Blackwell Publishing (1e, 2007)
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Library of Congress Cataloging‐in‐Publication Data
Names: Landberg, Rikard, editor. | Scheers, Nathalie, editor.Title: Whole grains and health / Rikard Landberg, Nathalie Scheers.Description: Second edition. | Hoboken : Wiley, 2021. | Includes bibliographical references and index.Identifiers: LCCN 2020024775 (print) | LCCN 2020024776 (ebook) | ISBN 9781118939437 (cloth) | ISBN 9781118939413 (adobe pdf) | ISBN 9781118939406 (epub)Subjects: LCSH: Health. | Grain–Therapeutic use. | Grain in human nutrition.Classification: LCC RA776 .W4556 2020 (print) | LCC RA776 (ebook) | DDC 613–dc23LC record available at https://lccn.loc.gov/2020024775LC ebook record available at https://lccn.loc.gov/2020024776
Cover Design: WileyCover Image: © Comaniciu Dan/Shutterstock
Preface
Cereal foods constitute a backbone of the diet worldwide and are the major source of energy and nutrients in many populations. The most common way cereal foods are consumed have detrimental effects on human health. The largest proportion of the intake consists of refined‐cereal products, generally associated with high glycemic index, reduced nutritional density and central in a dietary pattern associated with increased risk for non‐communicable diseases (NCDs). However, shifting the intake towards whole grains is associated with a consistently reduced risk of developing NCDs, specifically cardiovascular disease, type 2 diabetes and certain cancers. In fact, a high whole grain intake is listed as one of the most important modifiable risk factors of NCDs (Global Burden of Disease). Whole grain cereals are rich sources of fibre, many minerals, vitamins and phytochemicals. Public health authorities in the European Union, United States and around the world encourage the increased intake of whole grain cereals based on the health benefits, but recently also for improved sustainability. Most of the evidence for their beneficial effects stem from observational studies, while dietary interventions have shown acute effects on glucose, hormonal and inflammatory responses, and long‐term effects on insulin sensitivity, blood pressure and dyslipidaemia. Such effects have been linked to specific bioactive compounds, fibre components, gut microbiota, processing‐induced changes and the structural features of whole grains and cereal‐grain fractions. The dietary fibre complex, that is, dietary fibre and associated compounds, is believed to have a central role for the health effects of whole grain foods, but the mechanisms are to be elucidated in detail. The development of whole grain cereal foods has a potentially huge positive impact on the health of the global population, but there are important barriers to be torn down to succeed increasing the intake.
Since the first edition of the current book, the number of studies on whole grains and health have increased dramatically. In total, 2093 new publications on the search words whole grain AND health appeared in a Scopus search for the period 1 January 2007 to 26 March 2020. There has been a tremendous development of the field during the past decade, including definition and communication of whole grains to consumers, application of techniques to produce whole grain foods and studies of whole grain health effects. Such advancements are covered and discussed in detail in the different chapters of this book. For example, a large number of epidemiological studies have been carried out in different populations on the associations between whole grain consumption and risk of developing chronic diseases such as CVD, type 2 diabetes, some cancers, but also more rare diseases have been studied. Compared to older studies, more recent observational studies have investigated different grains separately and have also managed to estimate the intakes in g/d. Several large controlled human intervention studies have been conducted to investigate different aspects of whole grains on human health, including effects on cardiovascular and diabetes risk factors such as blood pressure, blood lipids, insulin sensitivity, body weight, body fat and inflammation. During the past decade, new biomarkers of whole grain wheat and rye intake has been developed and validated (alkylresorcinols and their metabolites). These biomarkers have been adopted and shown useful to assess compliance in whole grain intervention studies and they have successfully been used as an independent measure of whole grain intake in observational studies in humans. Metabolomics has emerged as a new approach to address health effects and to find new biomarkers of both dietary exposures and health effects related to whole grain intake. Several metabolomics studies have been published recently to achieve better understanding of health effects underlying whole grain consumption. Such studies have recently shown a modest effect on microbial composition after whole grain/high‐fibre cereal intake, which suggested several new mechanisms on why whole grain rye may have particular effects on insulin metabolism. Genomics have been applied in several large‐scale intervention studies and have provided new knowledge on how gene expression profiles cause changes in response to whole grain intake. This will be of importance for the overall understanding of the physiological responses in relation to whole grain intake. Moreover, new bioactive compounds in whole grains and whole grain fractions have been identified and are currently studied. One example of such is the group of benzoxazinoids, which have recently been identified in whole wheat and rye grains and in bakery products of these cereals. These compounds, isolated from other sources or synthesized, have been studied for a number of bioactivities. Their uptake and elimination in animals and humans as well as their effects are currently extensively studied. Untargeted metabolomics approaches have facilitated the process of discovering new compounds. The role of gut microbiota for human health and disease has boomed the last 10 years, and important insights on the role of whole grains and dietary fibre and their interaction with gut microbiota for differential responses in human health outcomes have increased dramatically, although there is still much to improve concerning our understanding in this area. EU‐regulations on health claims have been adopted with consequences for whole grain consumption. No health claim is allowed for whole grains but several specific claims, including grain components (reflecting beneficial physiological effects and disease risk reduction claims related to certain fibres) are allowed. No current worldwide definition of whole grain intake exists, but new definitions of both whole grains and whole grain products have been suggested.
The structure, outline and style of this book is designed to provide a comprehensive treatise on the subject covering the topic from the grains themselves, their components and distribution in different botanical fractions and products to the effect of whole grains on health and the molecular mechanisms/effects on risk factors underlying their health effects. The book also highlights the interest from the food industry and governmental and non‐governmental authorities to develop new food products rich in whole grains as well as to educate consumers about the health benefits of consuming whole grain foods (the whole grain stamp is an example of this communication to the consumer and the whole grain campaigns launched in Denmark and The Netherlands are other examples). The chapters are comprehensive in their coverage with the aim to provide founded knowledge and information for researchers, research students, authority and industry personnel that gives them a multidisciplinary understanding of this important topic.
Recent advances will to a great extent be covered by the update of book chapters of the first edition. As in the previous edition, we divide the book into sections with a slight modification of the suggested sections. More emphasis will be put on the section “whole grains, cereal fibre and chronic disease” and “grain technology and health‐related outcomes,” whereas consumer aspects are given somewhat less attention compared with the first edition. We also provide comprehensive material on the whole grain morphology constituents, fractions and technology as well as products for readers coming from the medical or public‐health sectors. The book comprises 5 sections and concluding remarks and future perspectives. In total, 23 chapters are included (Table 1).
Table 1 Brief description of the content of the sections.
Section
Content
Whole grain basics
Chemical composition and morphological structure of cereal grains and cereal fractions, such as bran, aleurone, germ and the endosperm, are described in detail as this is crucial for the understanding of physiological effects related to health. Differences and similarities among cereals are emphasized here. Important whole grain products are described with emphasis on traits and features that may be of importance for human health. This section also contains a chapter on the different definitions of
whole grain
and
whole grain products
. A chapter on consumption and description of lifestyle factors associated with whole grain intake as well as on tools for objective whole grain intake estimation through dietary biomarkers bridge this section to section two.
Evidences for disease prevention
The current literature on evidence for disease prevention derived from epidemiological – as well as intervention studies in humans and model – and animal studies have been reviewed and the evidence are evaluated in a systematic way focusing on the outcome of largest importance. Hard endpoints such as type 2 diabetes, CVD, cancer and mortality are at main focus in this section.
Whole grains mechanisms and effects on risk factors for chronic disease
This section bridges the section on whole grain basics and the section on chronic disease by discussing mechanisms and risk factors. This section contains chapters on whole grains and appetite, glycaemia, gut function as well as a chapter on bioactive compounds and effects that may be of relevance to human health. We have also included a chapter on potential negative aspects of whole grain consumption in which risk related to heavy metals, mycotoxins, acrylamide, gluten intolerance and wheat sensitivity are described and discussed.
Searching for new molecular mechanisms underlying health benefits of whole grains
In this section, the possibilities to use – OMICs to generate new hypotheses and to get better insights into new molecular mechanisms of the health effects of whole grains is presented. Metabolomics for discovery of new compounds and to monitor process changes in food products has been covered as well as its implementation in human studies to gain insights into molecular mechanisms and dissect biochemical pathways involved in processes with implication for health. Studies where changes in gene expression in response to interventions with whole grains in humans are also reviewed in a chapter.
Whole grains and the consumer
Barriers for whole grain consumption are at focus here. The industry’s commitment to whole grains has also been discussed by representatives from major enterprises in Europe and the United States. The current regulation and labeling have been covered as well as a chapter describing the current situation on health claims in Europe and the United States, and strategies for consumer communication.
We hope that the current edition of Whole Grains and Health will be of use and great pleasure for researchers, research students, industry personnel, governmental authorities (nutritionists, technologists, product developers, epidemiologists, health professionals) and others with wider interest in foods and health!
Rikard Landberg and Nathalie ScheersGothenburg, Sweden, March 2020.
Editors’ Biographies
Editors’ Biographies
Nathalie ScheersAssociate ProfessorFood and Nutrition ScienceDepartment of Biology and Biological EngineeringChalmers University of TechnologyGothenburg, Sweden
Associate Professor Nathalie Scheers and her research team conduct studies in the area of molecular nutrition with particular focus on metals, specific proteins, bioactive molecules and their physiological effects, on cellular or systemic level.
A core competence of Dr. Scheers includes human cell models. She investigates regulation of intestinal transport proteins, stress response and apoptosis, expression of cancer and inflammation markers, and bioavailability of nutrients. One of her main research topics is within iron nutrition, with a special focus on dietary iron supplements and fortificants. Together with collaborators, she is currently working on the mechanisms of cancer‐promoting and pro‐inflammatory effects of certain types of compounds used to fortify foods with iron. In addition, she is working on detoxification of gluten to celiacs. A few years back, she and her collaborators identified a food additive that can interfere with intestinal transglutaminase processing of gluten in vitro, which has the potential to render gluten non‐immunogenic to celiacs. At present, Dr. Scheers is leading a human intervention trial in healthy volunteers to verify the previous findings in vivo, with the ultimate goal to provide celiac safe gluten products. Dr. Scheers is also active in research about the fish‐protein parvalbumin beta and its association with physiological effects important for neurological diseases, toxicity of insects as human foods, and anti/pro‐inflammatory effects of marine collagen and shellfish processing waste.
Associate Professor Scheers has authored 39 scientific publications including original research, book chapters, proceedings etc. Her main publication area is within molecular iron nutrition and she has an H‐index of 10 according to Google Scholar.
Rikard LandbergProfessorHead of Division Food and Nutrition ScienceDepartment of Biology and Biological EngineeringChalmers University of TechnologyGothenburg, SwedenMember of the Young Academy of Sweden
Affiliated Researcher
Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden
Guest Researcher
Diet, Genes and Environment Group at Danish Cancer Society Research Center, Copenhagen, Denmark
Professor Rikard Landberg is the head of Division of Food and Nutrition Science at Chalmers University of Technology, Sweden. His group studies the preventive role of plant‐based foods using observational and intervention studies as well as various model systems. Professor Landberg is the PI of several RCTs and molecular epidemiological studies on the role of whole grains and dietary fibre in appetite, body weight management, glycaemia, prostate cancer and on cardiometabolic risk. He is particularly interested in the health effects of rye and established the Nordic Rye Forum together with colleagues (https://www.nordicryeforum.info). Professor Landberg also leads studies to test novel OMICs‐based personalized concepts for improved CVD prevention. Metabolomics is a key technique in Professor Landberg’s research program, and it is developed and applied for discovery and validation of exposure and prediction biomarkers, and for molecular phenotyping as the basis for tailored dietary strategies for personalized nutrition. Novel biomarkers, from his lab, such as alkylresorcinolas, are extensively used by researchers all over the world. Professor Landberg has authored more than140 papers and over10 book chapters, and delivered more than 25 invited/keynote lectures. He has an H‐index of 32 according to ISI web of science. Professor Landberg is an elected member of the Young Academy of Sweden and of the National Committee for Nutrition and Food Science at the Swedish Royal Academy of Sciences.
Acknowledgments
We would like to thank all the authors of the chapters in this book for their great contributions. The authors have generously provided their expertise and time to summarize the current knowledge within their respective field(s). We also would like to thank the following external experts for their help to review and provide input to some of the chapters in this book:
Dr. Carl Brunius, Dr. Susanna Larsson, Dr. Matti Marklund, Dr. Rob M. van Dam, and PhD‐student Kia Nöhr‐Iversen.
Rikard Landberg and Nathalie Scheers
Contributing Authors
Chapter 1
Maud Langton, Swedish University of Agricultural Sciences, SwedenJosé Luis Vázquez Gutiérrex, Swedish University of Agricultural Sciences, Sweden and Centro Technológico ITENE, Spain
Chapter 2
Wenche Frølich, University of Stavanger, NorwayPer Åman, Swedish University of Agricultural Sciences, Sweden
Chapter 3
Cécile Barron, UMR IATE, CIRAD, INRAE, Université de Montpellier, FranceValérie Micard, UMR IATE, CIRAD, INRAE, Université de Montpellier, FranceValérie Lullien‐Pellerin, UMR IATE, CIRAD, INRAE, Université de Montpellier, France
Chapter 4
Genyi Zhang, Jiangnan University, ChinaBruce R. Hamaker, Purdue University, USA
Chapter 5
Alastair B. Ross, Chalmers University of Technology, Sweden and AgResearch Ltd, New ZealandCynthia Harriman, Oldways Whole Grains Council, USARoberto King, Nestlé Research Center, Switzerland
Chapter 6
Cecilie Kyrø, Danish Cancer Society Research Center, DenmarkAnja Olsen, Danish Cancer Society Research Center, Denmark
Chapter 7
Matti Marklund, Tufts University, USAIzabela Biskup, Chalmers University of Technology, SwedenAfaf Kamal‐Eldin, United Arab Emirates University, UAERikard Landberg, Chalmers University of Technology, Sweden
Chapter 8
Nicola McKeown, Tufts University, USAMette Bredal Kristensen, University of Copenhagen, Denmark
Chapter 9
Shilpa N. Bhupathiraju, Harvard T. Chan School of Public Health, USAFrank B. Hu, Harvard T. Chan School of Public Health, USA
Chapter 10
Chris J. Seal, Newcastle University, UKIain A. Brownlee, Northumbria University, UK
Chapter 11
Anja Olsen, Danish Cancer Society Research Center, DenmarkCecilie Kyrø, Danish Cancer Society Research Center, Denmark
Chapter 12
Guri Skeie, The Arctic University of Norway, NorwayDavid R. Jacobs Jr., University of Minnesota, USA
Chapter 13
Sabine Ibrügger, University of Copenhagen, DenmarkKia Nøhr Iversen, Chalmers University of Technology, SwedenMette Kristensen, University of Copenhagen, DenmarkRikard Landberg, Chalmers University of Technology, Sweden
Chapter 14
Marion G. Priebe, University Medical Center Groningen, The NetherlandsCoby Eelderink, University Medical Center Groningen, The NetherlandsRoel J. Vonk, University Medical Center Groningen, The Netherlands
Chapter 15
Johan Dicksved, Swedish University of Agricultural Sciences, SwedenEmma Ivarsson, Swedish University of Agricultural Sciences, Sweden
Chapter 16
Anne‐Maria Pajari, University of Helsinki, FinlandRiitta Freese, University of Helsinki, FinlandSusanna Kariluoto, University of Helsinki, FinlandAnna‐Maija Lampi, University of Helsinki, FinlandVieno Piironen, University of Helsinki, Finland
Chapter 17
Afaf Kamal‐Eldin, United Arab Emirates University, UAEAgneta Åkesson, Karolinska Institutet, SwedenMaria Kippler, Karolinska Institutet, SwedenKarl‐Erik Hellenäs, National Food Agency, SwedenNathalie Scheers, Chalmers University of Technology, SwedenAnn‐Sofie Sandberg, Chalmers University of Technology, Sweden
Chapter 18
Amanda J. Lloyd, Aberystwyth University, UKKathleen Tailliart, Aberystwyth University, UKManfred Beckmann, Aberystwyth University, UKJohn Draper, Aberystwyth University, UK
Chapter 19
Kati Hanhineva, University of Turku, Finland, University of Eastern Finland, Finland and Chalmers University of Technology, Sweden
Chapter 20
Marjukka Kolehmainen, University of Eastern Finland, Finland
Chapter 21
Frank Thielecke, Thielecke Consulting, SwitzerlandWolfgang Bindzus, Cereal Partners Worldwide S.A., Switzerland
Chapter 22
Heddie Mejborn, Technical University of Denmark, DenmarkCaroline Sluyter, Oldways Whole Grains Council, USA
Supplementary Material
Additional materials, including multiple choice questions and supplementary chapters, can be found under the #8220;Downloads#8221; section online at https://www.wiley.com/en-gb/Whole+Grains+and+Health-p-9781118939437
1The Structure of Cereal Grains and Their Products
Maud Langton1, and José Luis Vázquez Gutiérrex1,2
1Department of Molecular Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden
2Department of Molecular Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden Present address: Centro Technológico ITENE, Valencia, Spain
1.1 Introduction
Through the senses, consumers can subjectively detect properties in food. However, other qualities such as long‐term health benefits of food that cannot be easily detected. A deep knowledge of cereal grain structure and how it is modified by processing is necessary to understand the physical and health properties of the different cereal products. This chapter focuses on the microstructure, at different levels, of cereal grains and their products. The structure of the grain is briefly overviewed and followed by the effect of processing on the structure of different food products. Based on the microstructure of the final product, three groups are distinguished: rolled cereals and porridge, protein network‐based products and starch network‐based products. This different organization is important for food production and technological aspects. The impact on the health‐related aspects of the product is currently investigated.
1.2 Grain structure
Cereals are the most important crops in the world and are destined to become both human food and animal feed. Cereals, which belong to the grass family (Gramineae), produce dry, one‐seeded fruits. These fruits are, botanically speaking, caryopses, but they are commonly referred as “grains” or “kernels.” The cereal grains such as wheat, rice, maize, barley, oats, rye, sorghum and millet provide 50% of the food energy and 50% of the protein consumed on earth. Wheat, rice and corn constitute around 75% of world’s grain production (Ramaswamy and Riahi 2003). In this chapter, wheat is used as reference to explain the structure of cereal grain. Its kernels contain three main parts: embryo, endosperm and their covering layers. The last are, in milling, often separated as the bran fraction (Figure 1.1A). If all the parts of the kernel are retained in processing, one can speak of whole grain. If either the bran or germ is separated from the kernel during milling, then it is a “refined grain.”
Figure 1.1 A: General structure of a cereal grain); B: Epifluorescence micrograph of parts of rye grain. The sections were stained with Acid Fuchsin and Calcofluor: protein appears red, cell walls rich in β‐glucan appear light blue and lignified cell walls of the pericarp appear yellowish‐orange. Structure of cereal foods
(Source: Hemery et al. 2007).
1.3 Embryo
The embryonic axis (rudimentary root and shoot of the next generation) and the scutellum (storage organ) together constitute the embryo, which makes up 2.5% to 3.5% of the weight of the entire kernel in wheat. It is often referred to as germ, although, strictly speaking, the germ is the embryo‐rich fraction of the kernel produced during milling. Wheat germ contains protein (25%), sugar (18%), oil (16% of the embryonic axis and 32% of the scutellum), and it is also rich in vitamins B and E (Delcour and Hoseney 2010a). In the case of rye, the embryo constitutes about 3.8% of the weight of the grain and contains 37.2% of protein, 13.4% of lipids and 43.6% of carbohydrates (Lasztity 1999; Ellis 2007).
1.4 Endosperm
The endosperm is the largest tissue of the grain. It is the primary starch and protein storage site and the source for white flour. It contains protein, carbohydrates, iron and B‐vitamins, such as riboflavin, niacin and thiamine. However, it is nutritionally inferior to the whole grain. The endosperm comprises two different parts: the starchy endosperm and the aleurone layer. The aleurone is botanically part of the endosperm. However, in practice, it is most often part of the bran since it is removed together with the pericarp and testa during the milling process. The main part of the grain constitutes the starchy endosperm, which consists of cells packed with nutrients, mainly starch, to support the growth of the embryonic axis after germination. It is also rich in protein. In all cereals, there is an inverse gradient involving these two components. The protein content increases towards the periphery, while starch is more predominant towards the center of the kernel. Cell size also decreases towards the outside and this is accompanied by increasing cell wall thickness. The endosperm cell walls of wheat are mainly composed of arabinoxylans, while in barley and oats (1‐3)‐ and (1‐4)‐β‐D glucans predominate. The contribution of cellulose to the cereal endosperm cell wall is low except in the case of rice.
1.5 Bran
The bran consists of the hard outer layers of the kernel and, depending on the milling process, constitutes around 14% of the grain. Generally, wheat bran comprises approximately 12% water, 13–18% protein, 3.5% fat and 56% carbohydrates. Wheat bran can be chemically differentiated by the occurrence of complex structures of either C6‐sugars like cellulose or C5‐sugars like xylans. Phenolic compounds and their polymer lignin are found in different concentrations within the bran. It also contains a large quantity of B‐vitamins as well as insoluble dietary fibre (Prückler et al. 2014). From the histological point of view, wheat bran is composed of the pericarp, testa and aleurone layer.
1.5.1 Pericarp
The pericarp consists of several complete and incomplete layers of dry, largely empty cells. During development, it serves to protect and support the growing endosperm and embryo. The outer layers of wheat bran, pericarp and testa are formed by thick cell walls containing cellulose, lignin and complex xylans with high arabinose to xylose ratios and substitution by ferulic acid dehydromers as cross‐linkers between polymer chains (Hemery et al. 2007).
1.5.2 Testa
The testa is a hydrophobic, semipermeable layer under the pericarp, which contains a cuticle rich in lipidic compounds. The testa is the outermost tissue of the seed and may consist of one or two cellular layers. Almost all of the alkylresorcinols in the grain are localized in the testa of wheat, rye, triticale and, at much lower levels, in barley (Ross et al. 2003b; Landberg et al. 2008). Alkylresorcinols are antioxidant compounds whose main function is to protect the membrane against lipid peroxidation. They are commonly used as biomarkers for whole grain intake since they are absorbed and at least partially metabolized in the human intestine (Ross et al. 2003a; Linko et al. 2005).
1.5.3 Aleurone layer
The aleurone layer surrounds the starchy endosperm and part of the embryo, and makes up 5–8% of the kernel. It is usually constituted by a single cell layer except in the case of barley, which contains two to three layers. Aleurone cells do not contain starch but they have high protein content and they are rich in lipids. They release active enzymes that help the cereal grain grow into a plant. The main component of wheat and rye aleurone cell walls is arabinoxylan (Karin 2006). The aleurone cell walls in wheat are relatively thick (3–4 μm) and have been reported to possess high cellulose content and relatively linear arabinoxylans with low arabinose‐xylose ratio (Saulnier et al. 2007). Whole grain wheat contains less than 1% β‐glucan and the majority is located in the aleurone and subaleurone layers, while in whole grain rye (Figure 1.1B), β‐glucan accounts for 1.5% of dry matter and seems to be more evenly distributed throughout the grain (Dornez et al. 2011; Frølich et al. 2013). The content of β‐glucan is higher in other cereals such as oat and barley, which contain 5% and 4.6%, respectively (Frølich et al. 2013). β‐Glucan in oat is more concentrated in the sub‐aleurone layers, while in barley it is evenly distributed across the starchy endosperm (Cui and Wang 2009). The aleurone layer also contains an important amount of minerals like magnesium and phosphorus, vitamins, and phenolic compounds, such as ferulic acid, and p‐coumaric acid. For instance, the aleurone layer contains almost all of the niacin and almost one‐third of the lysine found in wheat (Delcour and Hoseney 2010a).
Cereal grains possess a well‐organized microstructure. The endosperm is rich in starch and storage proteins located in protein bodies, and the cells are compartmentalized by cell wall polysaccharides (Figure 1.2A). Indeed, especially refined cereal foods may be considered at the structural scale as a composite of starch and proteins blended with other ingredients such as fat, sugar and fibre. Processes such as milling, dough mixing, baking, rolling and extrusion cause large changes in the structure of proteins, starch and cell wall components and therefore affect the structure and quality of the end product (Autio and Salmenkallio‐Marttila 2001; Della Valle et al. 2014). The organization of the grain components at different structural levels contributes to the different characteristics among cereal products, as shown in Figure 1.2, and Figure 1.2B shows the microstructure of a rye porridge, where fragments are easily detected. The effect of baking and extrusion on the microstructure is shown in Figures 1.2C and 1.2D, where dough mixing and baking provides a continuous protein network while extrusion provides a continuous starch phase. In both cases, the generation of an aerated structure and the presence of pores are essential for the desired properties of this kind of products. The mechanical properties, which are highly associated with texture and to a great extent consumer acceptance, depend on the morphology of the product. For instance, the structure of porridge is composed of grain fragments in a continuous phase of released amylose from the starch granules and storage proteins (Figure 1.2B). Wheat bread and cakes obtain their solid foam structure due to the continuous gluten network being able to retain air in open or closed cellular network (Figure 1.2C), while many crispbread products and most ready‐to‐eat cereals, which include extruded products, obtain their crunchiness from the multiple air cell layers retained in a continuous starch phase (Figure 1.2D).
Figure 1.2 Schematic representation of a typical endosperm cell (A) and microstructure of different cereal products such as rye porridge (B), wheat bread (C) and extruded rye breakfast cereal (D). Starch and protein can be observed in blue/purple and green, respectively.
Structure is also essential for nutritional properties since it influences the bolus structure before swallowing as well as further gastrointestinal digestion. Most studies have been focused on defining or creating food structures, but knowledge on food structure breakdown during consumption is also needed. In this way, gelatinized starch is more rapidly digested than in its native crystalline form and compact products such as pasta or porridge are more slowly digested than porous ones. At the molecular level, the amylose component of starch is more slowly digested than amylopectin, and the use of high‐amylose raw materials helps lowering the glycaemic response (Alminger and Eklund‐Jonsson 2008; Poutanen et al. 2014). This could be partly due to the lower swelling capacity of high amylose starch granules compared to waxy starch granules (Lii et al. 1996). The presence of sucrose or emulsifiers has also been shown to delay the swelling of starch granules (Richardson et al. 2003). The length of the amylose chains and interactions between starch and other components in the product such as proteins, dietary fibre or lipids can also influence the digestibility of starch (Sajilata et al. 2006).
Structural characteristics of cells and tissues influence grain quality and performance in food processes. These microstructural changes can be studied using a variety of microscopy techniques such as light microscopy, confocal laser scanning microscopy (CLSM) and electron microscopy. Light microscopy provides lower magnification than, for instance electron microscopy but it allows specific staining of different chemical components. This is particularly useful in cereal products, which are complicated multicomponent multiphase materials. For instance, amylose and amylopectin can be identified under the light microscopy by staining with iodine (Langton and Hermansson 1989; Autio and Salmenkallio‐Marttila 2001). Iodine staining also allows subsequent image analyses and obtaining quantitative results (Srikaeo et al. 2006). Some staining systems can also be used in CSLM, which requires a lower degree of sample preparation compared to other microscopy techniques (Autio and Salmenkallio‐Marttila 2001). Moreover, the use of fluorescently labelled antibodies has high potential due to the combination of immunological specificity with the sensitivity of fluorescence (Vázquez‐Gutiérrez and Langton 2015). Scanning electron microscopy (SEM) permits three‐dimensional observation of a wide spectrum of food structures. Since this technique does not require sectioning, it is appropriate for visualization of porous structures and sample preparation is easier compared to light microscopy (Sanchez‐Pardo et al. 2008). SEM has been used to observe cooking‐induced changes in starch granules and protein matrix (Srikaeo et al. 2006; Sanchez et al. 2008).
1.6 Rolled cereals and porridge
The structure of cereal products such as muesli and porridge, just before their consumption, is composed of rolled whole grains or grain fragments in a continuous aqueous phase. The confinement of a great part of the starch inside the cellular structure of the grain fragments (which are semi‐intact inside the cells) is an efficient way of slowing down starch digestion, compared to other products with higher proportion of gelatinized starch such as bread (Poutanen et al. 2014). However, it has also been suggested that porridge, due to its semisolid nature, could be emptied faster from the gastric compartment. In cases where porridge is made from flour rather than flakes, this could result in faster intestinal hydrolysis of starch and release of glucose (Johansson et al. 2018).
Rolled cereal, such as oat, rye or wheat, is one of the main components of muesli. The elaboration of rolled cereal involves steaming, pressing between rollers and drying of the grains. Light microscopy images of rolled rye show that cell walls are partially disrupted after the rolling process, gluten bodies are deformed developing a more network‐like structure within the particulate fragments, and starch is partially gelatinized after the drying (Figure 1.3). In this way, the resulting rolled grains absorb water more quickly and, in the case of those consumed as porridge, the cooking time decreases as the thickness of the rolled grains decreases. There is also a relationship between the rolled grain size and its subsidiary effects on digestion and colonic microbiota fermentation. The thickness would determine the availability and types of dietary fibre that are able to avoid digestion, and this would in turn have a consequence in the fermentation profile (Connolly et al. 2010).
Porridge is a dish made by boiling rolled or crushed cereal, usually oats, in water, milk or both, usually served hot in a bowl or dish. From the structural point of view, porridge is a compact cereal product where insoluble fragments of grain are dispersed in viscous grain extract. The boiling process favors the partial release of amylose from the starch granules and their swelling which, together with the amounts of β‐glucan solubilized from the cell walls, directly affect the viscosity and the texture of the product (Source: Yiu et al. 1987; Vázquez‐Gutiérrez et al. 2015) (Figure 1.2B).
Figure 1.3 Microstructure of rolled rye grain. A: bright field micrograph with iodine and light green staining for observation of starch (purple) and protein (green), respectively; B: epifluorescence micrograph with Calcofluor and Acid Fuchsin staining for observation of cell walls (blue) and protein (red), respectively.
1.7 Protein network‐based products
The formation of gluten is essential for the structure and texture of bread, cakes and pasta.
1.7.1 Bread
With the addition of water to wheat flour and subsequent mixing, the storage proteins of the wheat endosperm (glutenin and gliadin) hydrate and interact to develop the gluten matrix, which provides viscoelastic properties to the dough and allows the incorporation of air (Autio and Salmenkallio‐Marttila 2003; Boitte et al. 2013). The gluten forms the continuous phase in which starch granules, lipid, added yeast cells, and cell wall fragments are dispersed (Figure 1.2C). The aggregation of gliadins and glutenins are greatly determined by noncovalent bonds and define the structural and physical properties of the dough. The quantity and quality of gluten proteins largely determine dough mixing requirements and the rheological properties, which influences the gas retention properties and the volume and crumb structure of the resulting bread (Chavan and Chavan 2011). Apart from gluten, the other components affecting the distribution of water in the dough, such as starch and cell walls, have a direct influence on the final texture of bread, too (Flander 2012).
During yeast fermentation, carbon dioxide is generated and the dough expands. At the beginning of the fermentation process, the gas cells are embedded in the starch‐protein matrix. At a later stage of expansion, the matrix fails to enclose the gas cells and areas containing only liquid film are formed between adjacent gas cells. The end of dough expansion is marked by the rupture of the film, and not that of the starch–protein matrix (Gan et al. 1995). The major structural changes at the microscopic level during baking are starch gelatinization, denaturation of protein, melting of fat crystals and their incorporation into the surface of air cells and, sometimes, fragmentation of the cell walls (Autio and Salmenkallio‐Marttila 2001). Therefore, the final crumb structure is dependent not only on the shape, number and size of gas bubbles, but also on the structural properties of gluten‐starch matrix and probably on liquid film composed of surface‐active material (Autio and Salmenkallio‐Marttila 2003). The addition of shortenings stabilizes the gas cells. The fat crystals from the shortenings migrate towards the gas‐liquid interface and they melt during baking, allowing the bubbles to grow without rupture (Brooker 1996). Light microscopy is the most commonly used technique to determine bread structure (Jakubczyk et al. 2008). Scanning and transmission electron microscopy have also been used to study the effect of baking on starch granule structure (Bechtel 1985).
