Dietary Proteins and Atherosclerosis, 1st Edition

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Library of Congress Cataloging-in-Publication Data

Debry, Gérard.
Dietary proteins and atherosclerosis / G. Debry.
p. ; cm.
Includes bibliographical references and index.
ISBN 0-8493-2102-6
1. Atherosclerosis—Etiology. 2. Coronary heart disease—Etiology. 3. Proteins in human
nutrition. 4. Proteins in animal nutrition. 5. Proteins—Pathophysiology. I. Title.
[DNLM: 1. Dietary Proteins—adverse effects. 2. Arteriosclerosis—etiology. QU 55
D288d 2003]
RC692.D43 2003
616.1'36071—dc22
2003055434

This book contains information obtained from authentic and highly regarded sources. Reprinted material
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To Annick

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Acknowledgment
I wish to extend very sincere thanks to Moyra Barbier for her help in reviewing the
translation of this work.

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Foreword
To most scientists and to all of the general public, heart disease begins and ends
with fat and cholesterol. Only those scientists who have done research in the field
know that the earliest purely nutritional studies of experimental atherosclerosis were
predicated on finding an atherogenic principle in animal protein. The early experi-
ments did point to a connection between food of animal origin and atherosclerosis,
but the observation that dietary cholesterol induced arterial lesions overwhelmed the
earlier studies. It was assumed that the cholesterol content of the animal protein was
responsible for the observed effects.
The obsession with dietary cholesterol exists to this day and the role(s) of animal
and vegetable proteins have been investigated for brief periods and are rarely cited.
There was a period of interest in the 1920s when Newburgh and Clarkson demon-
strated the atherogenicity of animal protein even in the absence of cholesterol. The
first comparison of the effects of animal and vegetable proteins was carried out by
Meeker and Kesten in 1940, but this observation was not exploited for another two
decades. There has been a steady output of papers in this field since the early 1970s
but it has remained a trickle in comparison to the cholesterol and fat literature. This
situation may change, now that we recognize risk factors such as homocysteine,
C-reactive protein and the role of infection, and we realize that the disease goes
beyond dietary fat.
In this book, Professor Debry has succinctly summarized and discussed the role
that dietary protein may play in the etiology of atherosclerosis and atherosclerotic
heart disease. The book is encyclopedic in scope and, remarkably for its size,
summarizes virtually all aspects of the protein–atherosclerosis connection.
Data are presented on every animal species available for experimental work.
The effects of proteins from different sources and of proteins within each source
category are discussed, as are the additional effects of other dietary components (fat,
fiber, minerals).
The possibility that levels or ratios of specific amino acids may exert special
influences is addressed as well. The possible mechanisms of protein effects (which
have still not been clarified) are also summarized. The effects of the nonprotein
components of plant protein are also mentioned. Finally, there is a discussion of
dietary protein effects in humans. Two of the conditions that play a role in athero-
sclerosis — hypertension and thrombosis — can also be affected by dietary protein
and these, too, are discussed.
In the 1950s when the relationship between dietary fat and atherosclerosis was
becoming established epidemiologically, Yerushalmy and Hilleboe used the same
epidemiologic data to show that there was a protein effect that was as strong as that
of fat. This book provides data that support and expand their observation.

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Professor Debry has provided an invaluable source of data concerning dietary

protein and atherosclerosis. It is not meant to displace the interest in fat and
cholesterol in this disease, but rather to offer another area of interest and investigation
that has been generally neglected. This book should become part of the library of
every person working in atherosclerosis research or in public health. It will expand
the horizons of research workers in the fields of biology and medicine related to
atherosclerosis and heart disease. Combining the many new research tools now
available with the long-neglected data presented in this volume should yield greater
comprehension of the etiology of atherosclerosis and may lead to an earlier solution
of this major health problem.

David Kritchevsky
Philadelphia, PA

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Preface
Although food lipids are now recognized as the major nutritional factors in athero-
sclerosis, it is interesting to remember that the first experimental research projects
investigating the possible relationships among nutrition, blood lipids, and athero-
sclerosis studied the effects of animal proteins and meat in particular. Indeed, dietary
meat induces various forms of pathologic damage to hepatic tissues in rabbits
(Garnier and Simon 1907) and dogs, and also liver necrosis and arterial lesions
(D’Amato 1908). The results of these studies on rabbits were confirmed by
Ignatowski (1908a, 1908b) and Fahr (1912). Later, investigators assessed the effects
of different animal proteins: meat (Lubarsch 1909, 1910) or various associations
such as meat, egg yolk, egg white, and milk (Starokadomsky and Ssobolew 1909;
Stuckey 1911, 1912). Anitschkow and Chalatow established the cholesterol-fed
rabbit as a model for atherosclerosis research (Anitschkow and Chalatow 1913;
Finking and Hanke 1997). On the basis of their results, the investigators came to
the conclusion that proteins were not the only factors responsible for arterial injuries
and that the initially suspected effects of cholesterol should be accepted (Chalatow
1912; Wesselkin 1913; Anitschkow and Chalatow 1913; Wacker and Hueck 1913).
The respective roles of animal proteins and cholesterol already studied (Kon
1913, 1914; Steinbiss 1913; Knack 1915; Newburgh 1919; Newburgh and Squier
1920; Newburgh and Clarkson 1922, 1923a, 1923b; Diecke 1926; Clarkson and
Newburgh 1926) are discussed later. A positive correlation has been established
between animal protein consumption and serum cholesterol concentrations and the
extent of atherosclerosis, despite the absence of cholesterol in the diet (Newburgh
and Clarkson 1923a, 1923b). However, according to Diecke, no correlation can be
established between atherosclerosis and hypercholesterolemia (Diecke 1926). The
arterial hypertension observed in rabbits on a diet including meat could also be the
cause of atherosclerotic lesions (Schmidtmann 1926). The prevalence of cardiovas-
cular diseases, as assessed by epidemiologic studies over the same period, is posi-
tively and equally correlated with animal protein or fat consumption (Yerushalmy
and Hilleboe 1957; Yudkin 1957).
Meeker and Kestens (1940, 1941) demonstrated that in contrast to animal pro-
teins, vegetable proteins do not induce an increase in serum cholesterol concentra-
tions. Atherosclerosis is not observed in rabbits fed maize oil and casein or wheat
gluten. Nevertheless, plasma cholesterol concentrations were higher when the rabbits
were fed casein rather than wheat gluten (Enselme et al. 1963).
The experiments by Kritchevsky et al. (1959) and Howard et al. (1965) con-
firmed the results obtained by Meeker and Kestens. When cholesterol was added to
the diet of rabbits, the nonpurified soybean protein provided decreased serum cho-
lesterol concentrations, and not only was harmless but prevented atherosclerosis.
Two general reviews have summarized the effects of dietary proteins on plasma

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cholesterol concentrations and atherosclerosis in animals (Yudkin 1957; Enselme

et al. 1962).
In young women, the capacity of vegetable proteins compared to animal proteins
to lower plasma cholesterol levels was first observed by Walker et al. (1960). In
men, Hodges et al. (1967) showed that vegetable proteins decrease the serum cho-
lesterol concentrations induced by diets containing various proportions of fats and
simple or complex carbohydrates. In spite of these results, investigations on the
relationship between proteins and atherosclerosis have been replaced by others
focusing on the rapid development of the lipidic theory of atherosclerosis.
Nevertheless over the past 30 years, there has been renewed interest in the protein
theory (Connor and Connor 1972; Carroll and Hamilton 1975; Hermus 1975;
Kritchevsky 1976; Hamilton and Carroll 1976; Debry 1976; Carroll 1978a, 1978b;
Kritchevsky 1980a, 1980b; Carroll 1981b; Kritchevsky and Czarnecki 1982, 1983;
Laurent 1983, Terpstra et al. 1983a, 1983b; Kritchevsky 1983a, 1983b; Kritchevsky
et al. 1983, 1984; Debry et al. 1984; Goldberg and Schonfeld 1985; West and Beynen
1986; Forsythe et al. 1986; Kritchevsky et al. 1987; Kritchevsky and Klurfeld 1987;
Debry 1987a, 1987b; Guzman and Strong 1987; Kritchevsky 1987; Foley et al. 1988;
West and Beynen 1988; Barth and Pfeuffer 1988; Kritchevsky 1990; Debry 2001a,
2001b). The history of these relationships was reviewed by Kritchevsky and Czar-
necki (1983) and Terpstra et al. (1983a, 1983b), and more recently by Kritchevsky
(1993, 1995). However, in one general review on diet, plasma cholesterol, and
coronary heart disease by Smith and Pickney (1989), none of the 1700 references
quoted dietary proteins as a possible factor involved in atherosclerosis, and in a
recent review on coronary heart disease risk factors (Ferns and Lamb 2001), the
eventual role of proteins is not mentioned.
The results of experiments with varying diet components have shown that serum
cholesterol concentrations are positively correlated with animal protein content, and
casein in particular. However, according to the authors, these effects could also be
due to other diet components (Carroll and Hamilton 1975; Hamilton and Carroll
1974, 1976; Carroll 1978a), and cannot be generalized since the serum cholesterol
levels induced by certain animal and vegetable proteins are not significantly different.
This is the case, for example, with pork protein or raw egg white, wheat gluten, and
peanut protein (Carroll and Hamilton 1975) or with beef and vegetable proteins
(Kritchevsky et al. 1981). Moreover, since animal growth depends on the biological
value of proteins, this value should be taken into account (Hermus 1975).
Although the results of epidemiologic studies and clinical trials support the
notion of a positive correlation between the consumption of dietary proteins and the
prevalence of atherosclerosis or coronary thrombosis, this theory cannot be attested
with certainty since the collection of data on animal and vegetable protein consump-
tion remains relatively inaccurate in humans. In contrast, the numerous experimental
studies carried out in animals of various species as well as in humans have partly
identified, although only in a limited number of studies, the pathophysiologic mech-
anisms of the effects of proteins on atherosclerosis.
The damage caused by some animal proteins and the protective effects of certain
vegetable proteins have been clearly demonstrated. Although dietary proteins are
considered to be of minor importance in the etiology of hypercholesterolemia and

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atherosclerosis in humans (Carroll 1978a; Kris-Etherton et al. 1988), their effects

on plasma lipids, various factors of blood coagulation, endocrinologic balance,
arterial hypertension, and arterial wall properties have been demonstrated. The
effects of nonprotein substances associated with vegetable proteins in plants have
been the subjects of numerous studies over recent years. Results have shown that
the direct influence of these proteins on plasma lipid levels and the development of
atherosclerosis remains unclear and further studies are still required to establish the
real effects (Smith 1998).

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The Author
Professor G. Debry is currently Professor Emeritus at the Department of Nutrition
at the University Henri Poincaré in Nancy, France. He achieved the degree of M.D.
in 1956 and has been a professor of human nutrition and metabolic diseases at
University Henri Poincaré since 1967. He founded the Training for Dietitians at
French Technological Universität Institutes in 1968 and was the Director of the
INSERM Unit of Human Nutrition from 1963 to 1983. In 1984 he founded the
Human Nutrition Center of the University Henri Poincaré, which he also managed
until 1996. From 1970 to 1994, Professor Debry held a joint appointment at the
University Hospital as the head of the Diabetes, Nutrition and Metabolic Diseases
and of the Enteral Nutrition Departments.
Professor Debry has served and headed several French ministerial committees,
notably, the Ministries of Health, of Research, and of Agriculture. He was an expert
in nutrition for the World Health Organization from 1970 to 2000, and has been a
corresponding member of the French Academy since 1986 and a member of the
European Academy of Nutritional Science since 1988. He has won several research
awards from the French Academy of Medicine and the French Academy of Sciences,
as well as the Research Prize in Nutrition from the French Nutrition Foundation in
1980 and the André Mayer Award in 1983. He has also received several medals
including Officer of the Legion of Honour in 1991.
Professor Debry has written numerous publications, including 37 contributed
chapters to edited volumes and nine monographs. He has also served as editor for
five International Congresses.

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Contents
Introduction
Epidemiologic Data
Clinical Data

Chapter 1 Protocol Design for Experimental Data on the Effects of Food

Proteins on Plasma Lipids and Lipid Metabolism

1.1 General Conditions for Protocol Design

1.2 Animal Species
1.3 Genetic Factors
1.4 Age
1.5 Sex
1.6 Diet
1.7 Similarities and Contrasts between Animals and Humans
1.8 Conclusion

Chapter 2 Experimental Data on Animals

2.1 Effects of Dietary Protein Level

2.1.1 Birds
2.1.1.1 Chickens and Cockerels
2.1.1.2 Pigeons
2.1.1.3 Quails
2.1.2 Rabbits
2.1.3 Rodents
2.1.3.1 Rats
2.1.3.2 Mice and Hamsters
2.1.4 Dogs
2.1.5 Calves
2.1.6 Pigs
2.1.7 Monkeys
2.1.8 Summary
2.1.9 Effects of Low-Protein Diet on Plasma Lipids, Liver Enzymes,
Lipid Metabolism, and Biliary Flow
2.1.9.1 Plasma Lipids
2.1.9.2 Liver Enzymes and Lipid Metabolism
2.1.9.3 Biliary Flow
2.1.10 Effects of High-Protein Diet on Enzymes and Liver Lipogenesis
2.1.11 Conclusion

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2.2 Effects of the Nature of Proteins

2.2.1 Casein versus Soybean Protein: Effects on Serum Cholesterol
Concentrations
2.2.1.1 Birds
2.2.1.2 Rabbits
2.2.1.3 Rats
2.2.1.4 Mice
2.2.1.5 Guinea Pigs and Hamsters
2.2.1.6 Pigs
2.2.1.7 Monkeys
2.2.2 Casein versus Soybean Protein: Effects on Lipid and
Cholesterol Metabolisms
2.2.2.1 Rabbits
2.2.2.2 Rats
2.2.3 Casein versus Soybean Protein: Effects on Lipoproteins
2.2.3.1 Birds
2.2.3.2 Rabbits
2.2.3.3 Rats
2.2.3.4 Monkeys
2.2.4 Casein versus Soybean Protein: Effects on Apoproteins
2.2.5 Casein versus Soybean Protein: Effects on Polyunsaturated
Fatty Acids
2.2.6 Summary
2.3 Effects of Various Types of Soybean Protein and Casein Products
2.3.1 Soybean Protein Isolates
2.3.1.1 Gerbils
2.3.1.2 Rabbits
2.3.1.3 Rats and Mice
2.3.1.4 Hamsters
2.3.1.5 Pigs
2.3.1.6 Monkeys
2.3.2 Soybean Protein Extracts of High or Low Molecular Weight
and Undigested Fractions of Soybean Protein
2.3.3 Germinated or Fermented Soybean
2.3.4 Soybean Protein Hydrolysates
2.3.5 Casein and Soybean Protein Treated with Formaldehyde
2.3.6 Sodium Caseinate
2.3.7 Summary
2.4 Influence of Dietary Food Environments on Effects of Soybean Protein
and Casein
2.4.1 Balance
2.4.2 Fatty Acid Content
2.4.3 Choline and Lecithin Content
2.4.4 Cholesterol Content
2.4.5 Carbohydrate Content
2.4.6 Dietary Fiber Content

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2.4.7 Mineral and Vitamin Content

2.4.7.1 Calcium Content
2.4.7.2 Zinc, Copper, and Magnesium Content
2.4.7.3 Vitamin A and Vitamin E Content
2.4.8 Conclusion
2.5 Effects of Other Food Proteins
2.5.1 Vegetable Proteins
2.5.1.1 Wheat and Corn Gluten
2.5.1.2 Rice and Rice-Protein Concentrates
2.5.1.3 Other Vegetable Proteins
2.5.1.4 Summary
2.5.2 Animal Proteins
2.5.2.1 Fish Protein
2.5.2.2 Milk Protein
2.5.2.3 Egg Protein
2.5.2.4 Beef Protein
2.5.2.5 Carnitine
2.5.3 Animal and Vegetable Proteins
2.5.4 Summary
2.6 Effects of Amino Acid Mixtures and Amino Acids
2.6.1 Amino Acid Mixtures
2.6.1.1 Rabbits
2.6.1.2 Rats
2.6.1.3 Monkeys
2.6.1.4 Summary
2.6.2 Amino Acids
2.6.2.1 Alanine
2.6.2.2 Cysteine
2.6.2.3 Ethionine
2.6.2.4 Glutamic Acid
2.6.2.5 Glycine
2.6.2.6 Histidine
2.6.2.7 Isoleucine
2.6.2.8 Leucine
2.6.2.9 Methionine
2.6.2.10 Phenylalanine
2.6.2.11 Taurine
2.6.2.12 Threonine
2.6.2.13 Tryptophan
2.6.2.14 Tyrosine
2.6.2.15 Valine
2.6.2.16 Summary and Conclusion
2.7 Action Mechanisms of Soybean Protein, Casein, and Amino Acids
2.7.1 Effects on Digestive Absorption of Lipids, Cholesterol, and
Steroids and Fecal Excretion of Steroids

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2.7.1.1 Digestive Absorption of Lipids, Cholesterol,

and Steroids
2.7.1.2 Fecal Excretion of Steroids and Bile Acids
2.7.2 Effects on Serum Lipids, Liver Cholesterol, and Liver Enzymes
2.7.3 Effects of Amino Acids and Lysine/Arginine Ratio
2.7.3.1 Amino Acids
2.7.3.2 Lysine/Arginine Ratio
2.7.3.3 Action Mechanism of Amino Acids
2.7.4 Effects of Nonprotein Components
2.7.4.1 Dietary Fibers
2.7.4.2 Phytates
2.7.4.3 Saponins
2.7.4.4 Isoflavones
2.7.4.5 Soybean Globulins
2.7.5 Effects on Endocrine Responses
2.7.5.1 Insulin and Glucagon
2.7.5.2 Growth Hormone
2.7.5.3 Thyroid Hormones
2.7.5.4 Cortisol and Corticosterone
2.7.6 Conclusion

Chapter 3 Experimental Data on Humans

3.1 Healthy Humans
3.1.1 Amount of Proteins
3.1.2 Nature of Proteins
3.1.2.1 Casein and Soybean Protein
3.1.2.2 Fish, Pork, Beef, Soybean Protein Analogues, and
Poultry Proteins
3.1.2.3 Milk and Whey Proteins
3.1.2.4 Egg Protein
3.1.2.5 Amino Acids
3.1.2.6 Carnitine
3.1.2.7 Food Environments
3.2 Hyperlipidemic Humans
3.2.1 Soybean Protein, Animal Protein, and Amino Acids
3.2.2 Wheat Gluten
3.2.3 Garlic Protein
3.2.4 Food Environments
3.2.5 Summary
3.3 Mechanisms Involved in Soybean Protein, Casein, and Amino Acid
Effects
3.3.1 Effects on Digestive Absorption of Lipids and Fecal Excretion
of Steroids
3.3.2 Effects on Hepatic and Lipoprotein Cholesterol
3.3.3 Effects of Nonprotein Components

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3.3.3.1 Lecithin
3.3.3.2 Dietary Fibers
3.3.3.3 Saponins
3.3.3.4 Isoflavones
3.3.3.5 Summary
3.3.4 Effects on Endocrine Response
3.3.4.1 Insulin and Glucagon
3.3.4.2 Growth Hormone
3.3.4.3 Thyroid Hormones
3.3.4.4 Cortisol and Corticosterone
3.4 Conclusion

Chapter 4 Data on Atherosclerosis

4.1 Experimental Data in Animals
4.1.1 Low-Protein Diet
4.1.2 High-Protein Diet
4.1.3 Nature of Proteins
4.1.4 Amino Acids
4.1.4.1 Arginine
4.1.4.2 Lysine
4.1.4.3 Lysine/L-Arginine and L-Arginine/Aspartic Acid
Ratios
4.1.4.4 Methionine
4.1.4.5 Taurine
4.1.4.6 Summary
4.1.5 Immunologic Effects of Proteins
4.1.6 Glutathione
4.1.7 Influence of Food Environments on Diets
4.1.7.1 Copper and Zinc
4.1.7.2 Choline and Lecithin
4.1.7.3 Dietary Fibers
4.1.7.4 Isoflavones
4.1.8 Conclusion
4.2 Data on Humans
4.2.1 Epidemiologic Data
4.2.1.1 Animal Proteins
4.2.1.2 Taurine
4.2.1.3 Biological Parameters
4.2.2 Experimental Data
4.2.2.1 Dairy Proteins
4.2.2.2 Amino Acids
4.2.2.3 Immunologic Effects of Proteins
4.2.2.4 Dietary Fibers
4.2.2.5 Isoflavones
4.2.3 Conclusion

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Chapter 5 Data on Hypertension

5.1 Data on Animals
5.1.1 Summary
5.2 Data on Humans
5.2.1 Epidemiologic Data
5.2.2 Experimental Data
5.2.2.1 Nature of Proteins
5.2.2.2 Amino Acids
5.2.2.3 Isoflavones
5.3 Mechanisms
5.3.1 Effects of Sympathetic Nervous System
5.3.2 Dietary Protein and Natriuresis
5.3.3 Effects of Amino Acids
5.3.3.1 Arginine
5.3.3.2 Lysine
5.3.3.3 Methionine
5.3.3.4 Taurine
5.3.3.5 Tyrosine and Tryptophan
5.4 Effects of Casein Peptides
5.5 Conclusion

Chapter 6 Data on Thrombosis in Animals and Humans

6.1 Effects of Proteins
6.1.1 Milk Peptides from Casein, Soybean Protein, Lactalbumin,
Lactotransferrin, and Other Proteins
6.1.2 Immunoglobulins
6.1.3 Amino Acids
6.1.3.1 Arginine
6.1.3.2 Methionine and Homocysteine
6.1.3.3 Taurine
6.1.3.4 Tryptophan
6.2 Effects of Isoflavones
6.3 Conclusion

Chapter 7 General Conclusions

References

Amino Acid Index

Alanine
Arginine
Cysteine and Cystine
Ethionine

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Glutamic Acid
Glycine
L-Histidine
Isoleucine
Leucine
Lysine
Lysine/Arginine Ratio
Methionine
Phenylalanine
Serine
Taurine
Threonine
Tryptophan
Tyrosine
Valine

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