olive oil more than just oleic acid
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Olive oil: more than just oleic acid
Dear Sir:
Recent articles in the Journal emphasized the role of olive oil in
cardiovascular protection (1, 2). Many of the healthful effects of olive
oil are usually attributed to olive oils high oleic acid content; how-
ever, comparison of the proportion of oleic acid as a percentage of the
energy intake in the Mediterranean diet with that of other Western
diets (eg, North American and northern European) shows that oleic
acid is present in comparable amounts. In fact, although most of the
dietary lipids in the Mediterranean basin, where consumption of meat
and animal fat is low, come from olive oil, other diets rich in chickenand pork meats provide similar quantities of oleic acid (3, 4). Finally,
other vegetable oils, eg, canola, are high in monounsaturates.
Extra virgin olive oil is a unique dietary lipid in the sense that it
is not extracted from seeds by means of solvents. Rather, it is
obtained from whole fruit (drupe) by using the cold-press tech-
nique, which does not alter the chemical nature of the drupe or that
of the resulting oil. In this way, the compounds that the fruit devel-
ops in response to environmental stress, most of which are pheno-
lic in structure, are transferred to the oil, where they constitute the
polar, minor components fraction. The most abundant phenolic
compound in the drupe is oleuropein, a bitter glycoside that consti-
tutes up to 14% of the fruits dry weight. With the progression of
blooming and maturation, oleuropein undergoes enzymatic and
nonenzymatic hydrolysis and yields several simpler compounds,(eg, hydroxytyrosol, oleuropein aglycone, and ligstroside) that
build up the full fruity taste that connoisseurs of olive oil search for.
Note that these compounds are virtually absent in refined (rectified)
oils (ie, the type of oil simply denominated olive oil), which is
extracted by means of solvents and alkalinized with chemicals to
reduce the excessive acidity (by law, 1% of fatty acids for extra
virgin oils). Finally, the tocopherol content of olive oil is10 times
lower than that of seed oils because of the lack of extraction of
olive seeds, where most of the tocopherols are located.
During the past few years, thanks to the availability of pure com-
pounds, the biological activities of olive oil phenolics, namely
oleuropein and hydroxytyrosol, have been thoroughly investigated
in in vitro studies. These studies included, but were not limited to,
the antioxidant capacity of these phenolics. The results indicatethat olive oil phenolics are potent free radical scavengers, inhibit
chemically induced LDL oxidation, inhibit platelet aggregation and
eicosanoid production by activated human leukocytes [and hence
the potential antithrombotic activity described by Frost Larsen et al
(1)], and potentiate the macrophagic response to endotoxin chal-
lenge by increasing their production of nitric oxide (5). Finally,
recent evidence of a dose-dependent absorption of olive oil pheno-
lics by humans has been obtained (6). In turn, the use of extra vir-
gin olive oil as the principal source of dietary fat and in substitu-
tion of animal fat, in addition to providing a considerable amount
of oleic acid, allows the intake of bioactive compounds whose
potential healthful effects should be taken into consideration.
Francesco Visioli
Claudio Galli
Institute of Pharmacological Sciences
Via Balzaretti 9
20133 Milan
Italy
E-mail: francesco.visioli@unimi.it
REFERENCES
1. Frost Larsen L, Jespersen J,Marckmann P. Are olive oil diets antithrom-
botic? Diets enriched with olive, rapeseed, or sunflower oil affect post-
prandial factor VII differently. Am J Clin Nutr 1999;70:97682.
2. Kris-Etherton PM, Pearson TA, Wan Y, et al. High-monounsaturated
fatty acid diets lower both plasma cholesterol and triacylglycerol
concentrations. Am J Clin Nutr 1999;70:100915.
3. Dougherty RM, Galli C, Ferro-Luzzi A, Iacono JM. Lipid and phos-
pholipid fatty acid composition of plasma red blood cells and platelets
and how they are affected by dietary lipids: a study of normal subjects
from Italy, Finland, and the USA. Am J Clin Nutr 1987;45:44355
4. The British Nutrition Foundation. Unsaturated fatty acids. Nutritional
and physiological significance. London: Chapman & Hall, 1992.5. Visioli F, Galli C. The effect of minor constituent of olive oil on car-
diovascular disease: new findings. Nutr Rev 1998; 56:1427.
6. Visioli F, Galli C, Bornet F, Mattei A, Galli G, Caruso D. Olive oil
phenolics are dose-dependently absorbed in humans. FEBS Lett
2000;468:15960.
Fatty diets are unhealthyeven those basedon monounsaturates
Dear Sir:
In their recent study, Kris-Etherton et al (1) compared an aver-
age American diet (AAD) rich in saturates (containing 34% total
fat) with the American Heart Association (AHA) Step II diet
(25% total fat) and 3 moderately fatty diets high in monounsatu-
rates and poor in saturates (3436% total fat) that were based on
olive oil, peanut oil, or peanut butter (1). The AHA Step II diet
and the monoene diets were associated with identical reductions
Am J Clin Nutr2000;72:8536. Printed in USA. 2000 American Society for Clinical Nutrition 853
Letters to the Editor
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in LDL cholesterol compared with the AAD. Similar to earlier
studies, the low-fat Step II diet was found to raise triacylglycerol
compared with the higher-fat diets. HDL cholesterol differed
only marginally and insignificantly between diets. The authors
concluded that a high-MUFA, cholesterol-lowering diet may be
preferable to a low-fat diet in prevention of coronary heart dis-
ease. The same opinion was expressed by other authors (2).
We would like to warn people against considering high-fat
monoene diets to be the most healthy diets. There are several rea-sons that high-fat dietseven those based on monoene fats
should be avoided in modern societies in which physical activity
and energy requirements are low. First, any high-fat diet
increases the likelihood of developing obesity, as do most other
highly energy-dense diets (3). Even the olive oilconsuming
Greeks have become more obese during the past decades because
of their increasingly sedentary lifestyle (4, 5).
Second, in the recent study by Kris-Etherton et al and in most
earlier trials comparing diets with various fat contents, energy
intake was fixed and constant (ie, isoenergetic conditions were
maintained) to keep body weight constant. This design is inap-
propriate because spontaneous energy intake would normally dif-
fer if diets with different fat contents were eaten ad libitum (6). It
was shown very elegantly in a meta-analysis by Kris-Ethertonsown group that fat-reduced diets cause a dose-dependent decrease
in energy intake and body weight (7). The spontaneous weight
loss that would be expected with a low-fat Step II diet was thus
inhibited by the design used in the recent study (1). Accordingly,
the blood lipid response was importantly biased. It is well known
that weight loss causes triacylglycerol to decline and that con-
comitant increases in HDL cholesterol are often seen (8). In addi-
tion, earlier long-term trials of healthy and hyperlipemic persons
showed that diets comparable with the Step II diet had no adverse
effects on triacylglycerol if eaten ad libitum (9, 10).
Third, not only blood lipids but also several other cardiovas-
cular risk factors are influenced by diet and therefore need to be
considered in the overall evaluation of the health effect of a diet.
We and other researchers showed that low-fat, high-fiber dietsmay affect blood coagulation and fibrinolysis strongly in an
antithrombotic manner (11, 12). The effects on the hemostatic
system seem to rely heavily on the carbohydrate quality of the
diet, ie, the fiber content and the glycemic index (13). Therefore,
it is unfortunate that Kris-Etherton et al did not report anything
about these aspects of their experimental diets.
Fourth, there is strong epidemiologic evidence that high
intakes of fruit and vegetables are associated with less coronary
heart disease and cancer morbidity. High-fat diets prevent high
intakes of fruit and vegetables because of the low energy ceiling
of modern sedentary societies. Remember that the Greeks of the
1950s and 1960s were very physically active fishermen and farm-
ers and that their high-fat, olive oilbased diets still allowed con-
sumption of a large amount of bread, vegetables, and fruit (5, 14).For these 4 reasons (more could be added), we believe it is
incorrect to consider high-fat monoene diets the most healthy
choice for sedentary people. We can take good care of our body
weight, our blood lipids, our hemostatic system, and our need for
trace elements and unknown nonnutrients present in foods only
if we allow plenty of our energy to be supplied from foods with
low fat contents. Where to set the fat limit is a matter of discus-
sion, but the epidemic of obesity tells us that we still eat more fat
than is appropriate. We consider a population average fat intake
of30% of total energy intake to be a wise recommendation.
Peter Marckmann
Arne Astrup
Research Department of Human Nutrition
Royal Veterinary and Agricultural University
Rolighedsvej 30
DK-1958 Frederiksberg
Denmark
E-mail: pma@kvl.dk
REFERENCES
1. Kris-Etherton PM, Pearson TA, Wan Y, et al. Highmonounsatu-
rated fatty acid diets lower both plasma cholesterol and triacylglyc-
erol concentrations. Am J Clin Nutr 1999;70:100915.
2. Katan MB, Grundy SM, Willett WC. Should a low-fat, high-
carbohydrate diet be recommended for everyone? Beyond low-fat
diets. N Engl J Med 1997;337:5636.
3. Bray GA, Popkin BM. Dietary fat intake does affect obesity! Am J
Clin Nutr 1998;68:115773.
4. Mamalakis G, Kafatos A. Prevalence of obesity in Greece. Int J
Obes 1996;20:48892.
5. Voukiklaris GE, Kafatos A, Dontas AS. Changing prevalence of coro-
nary heart disease risk factors and cardiovascular diseases in men of
a rural area of Crete from 1960 to 1991. Angiology 1996;47:439.
6. Siggaard R, Raben A, Astrup A. Weight loss during 12 weeks ad
libitum carbohydrate-rich diet in overweight and normal-weight
subjects at a Danish work site. Obes Res 1996;4:34756.
7. Yu-Poth S, Zhao G, Etherton T, Naglak M, Jonnalagadda S, Kris-
Etherton PM. Effects of the National Cholesterol Education Programs
Step I and Step II dietary intervention programs on cardiovascular dis-
ease risk factors: a meta-analysis. Am J Clin Nutr 1999;69:63246.
8. Marckmann P, Toubro S, Astrup A. Sustained improvement in blood
lipids, coagulation, and fibrinolysis after major weight loss in obese
subjects. Eur J Clin Nutr 1998;52:32933.
9. Schaefer EJ, Lichtenstein AH, Lamon-Fava S, et al. Body weight
and low-density lipoprotein cholesterol changes after consumption
of a low-fat ad libitum diet. JAMA 1995;274:14505.
10. Sandstrm B, Marckmann P, Bindslev N. An eight-month controlled
study of a low-fat/high-fibre diet: effects on blood lipids and bloodpressure in healthy young subjects. Eur J Clin Nutr 1992;46:95109.
11. Marckmann P, Sandstrm B, Jespersen J. Favorable long-term effect
of a low-fat/high-fiber diet on human blood coagulation and fibri-
nolysis. Arterioscler Thromb 1993;13:50511.
12. Avellone G, Di Garbo V, Cordova R, Scaffidi L, Bompiani GD.
Effects of Mediterranean diet on blood lipid, coagulative and fibri-
nolytic parameters in two randomly selected population samples in
western Sicily. Nutr Metab Cardiovasc Dis 1998;8:28796.
13. Jrvi AE, Karlstrm BE, Granfeldt YE, Bjrck IE, Asp NGL,Vessby
BOH. Improved glycemic control and lipid profile and normalized
fibrinolytic activity on a low-glycemic index diet in type 2 diabetic
patients. Diabetes Care 1999;22:108.
14. Kafatos A, Kouroumalis I, Vlachonikolis I, Theodorou C, Labadar-
ios D. Coronary-heart-disease risk-factor status of the Cretan urban
population in the 1980s. Am J Clin Nutr 1991;54:5918.
Reply to P Marckmann
Dear Sir:
Numerous studies, including one we published recently (1),
have shown beneficial effects of a weight-maintenance, high
monounsaturated fatty acid (MUFA), blood cholesterollowering
854 LETTERS TO THE EDITOR
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diet compared with a high-carbohydrate, low-fat diet on impor-
tant cardiovascular disease (CVD) risk factors, notably triacyl-
glycerol, HDL-cholesterol, and plasma glucose and insulin
concentrations (2, 3). It is clear that elevated triacylglycerol and
glucose and insulin concentrations increase the risk of CVD, as
does a low HDL-cholesterol concentration. Lowering plasma tri-
acylglycerol, glucose, and insulin and increasing HDL choles-
terol decrease the risk of CVD. Although not measured in our
recent study, a weight-maintenance, high-carbohydrate, low-fatdiet has also been shown to increase fibrinogen concentrations,
whereas a high-MUFA, blood cholesterollowering diet does not
(4). An elevated fibrinogen concentration was shown to increase
the risk of CVD. Thus, the evidence is convincing that a weight-
maintenance, high-MUFA, blood cholesterollowering diet
beneficially affects CVD risk.
As noted by Marckmann and Astrup, body weight is an impor-
tant factor that must be considered in contemporary dietary rec-
ommendations. The key questions are 1) What is the best diet for
weight loss and weight maintenance? and 2) Will a higher-fat
diet promote weight gain?
In our recent meta-analysis (5), we observed a linear relation
between decreasing percentage of energy from fat and a
decrease in body weight. Although this finding suggests thathigher-fat diets promote weight gain, 3 important limitations of
this study must be noted. First, a higher-fat weight-loss diet was
not tested, so one can question whether weight loss might be
less, the same, or maybe even greater because of better adher-
ence to the higher-fat (ie, high MUFA), energy-reduced diet. It
is generally accepted that a calorie is a calorie regardless of
whether the energy is derived from fat, carbohydrate, or protein.
Thus, weight loss with any energy-reduced diet is due to the
reduction in energy intake relative to expenditure. What is not
clear is whether macronutrient-manipulated weight-loss diets
have any effect on adherence and, hence, on long-term weight
loss and weight maintenance. Second, the weight loss was small
despite a large reduction in energy intake from fat (ie, 2.6-kg
weight loss associated with an 8percentage point decrease inpercentage of energy from fat). A smaller decrease in fat, con-
sistent with current intake recommendations, would be expected
to result in less weight loss (only 1.3 kg for a 4percentage
point decrease in fat intake). Finally, in long-term studies over a
period of 24 y, only small changes in body weight were shown
(0.5-kg weight loss).
Targeting fat reduction as the sole means of affecting the
global epidemic of overweight and obesity is not justified. Obe-
sity is a complex problemits causes are not fully understood.
Although it is clear that an energy imbalance is the root cause,
there is no compelling evidence that this is due to changes in fat
intake. A case in point relates to the ongoing increase in the inci-
dence of overweight and obesity in the United States that is con-
current with little or no change in absolute intake of fat and adecrease in percentage of energy from fat (6). It is clear that an
increase in energy intake in conjunction with a more sedentary
lifestyle (ie, less physical activity) accounts, in part, for the fat-
tening of Americans. Further evidence comes from Sweden,
where a small increase in overweight occurred despite virtually
no change in the diet (8, 9). In addition, there is ample evidence
from other countries that there is no consistent association
between increasing overweight and obesity and fat intake (7, 8).
Energy balance and, if needed, weight loss in individuals
who are following any diet is dependent on energy intake irre-
spective of the macronutrient profile. In the context of a high-
MUFA, blood cholesterollowering diet, it is clear that this diet
has beneficial effects on CVD risk factors in weight-stable indi-
viduals. Although it has not been tested as a weight-loss diet
compared with a high-carbohydrate, low-fat diet in free-living
subjects, such a diet could be planned that would have a low
energy density (ie, high in fruit and vegetables) to provide bulk
and promote satiety. The key issue for controlling energy intake
may not be the macronutrient profile of the diet but rather theenergy density, because the fat content and energy density of
foods are not always perfectly correlated. As argued by Rolls
and Bell (9), energy density is more closely related to factors
such as the water and fiber contents of foods. In that study and
others, subjects ate less when consuming foods of low energy
density compared with foods of high energy density, regardless
of fat content. Thus, focusing solely on the fat content of foods
when designing weight-loss diets may limit the effectiveness of
the diets if the effects of energy density are not considered.
We advocate a reexamination of the effects of the macronutri-
ent content of the diet on risk of CVD. While acknowledging that
the ultimate test of higher-fat diets will be in free-living individ-
uals consuming foods ad libitum, we believe that by promoting
the addition of fruit, vegetables, whole grains, and legumes tothese diets, it may be possible to achieve long-term success in
terms of both weight control and CVD risk reduction.
Penny M Kris-Etherton
Christine L Pelkman
Guixiang Zhao
Thomas A Pearson
Ying Wan
Terry D Etherton
The Pennsylvania State University
Nutrition Department
S-126 Henderson Building
University Park, PA 16802E-mail: pmk3@psu.edu
REFERENCES
1. Kris-Etherton PM, Pearson TA, Wan Y, et al. Highmonounsaturated
fatty acid diets lower both plasma cholesterol and triacylglycerol
concentrations. Am J Clin Nutr 1999;70:100915.
2. Mensink RP, Katan MB. Effect of monounsaturated fatty acids ver-
sus complex carbohydrates on high-density lipoproteins in healthy
men and women. Lancet 1987;1:1225.
3. Lerman-Garber I, Ichazo-Cerro S, Zamora-Gonzalez J, Cardoso-
Saldana G, Posadas-Romero C. Effect of a high-monounsaturated
fat diet enriched with avocado in NIDDM patients. Diabetes Care
1994;17:3115.
4. Kris-Etherton PM, for the DELTA investigators. Effects of replacingsaturated fat (SFA) with monounsaturated fat (MUFA) or carbohy-
drate (CHO) on plasma lipids and lipoproteins in individuals with
markers for insulin resistance. FASEB J 1996;10:2666.
5. Yu-Poth S, Zhao G, Etherton T, Naglak M, Jonnalagadda S, Kris-
Etherton PM. Effects of the National Cholesterol Education Pro-
grams Step I and Step II dietary intervention programs on cardiovas-
cular disease risk factors: a meta-analysis. Am J Clin Nutr 1999;69:
63246.
6. Ernst ND, Obarzanek E, Clark MB, Briefel RR, Brown CD, Donato
K. Cardiovascular health risks related to overweight. J Am Diet
Assoc 1997;97(suppl):S4751.
LETTERS TO THE EDITOR 855
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7. Seidell JC. Obesity in Europe: scaling an epidemic. Int J Obes Relat
Metab Disord 1995;19(suppl):S14.
8. Epstein FH. The relationship of lifestyle to international trends in
CHD. Int J Epidemiol 1989;18(suppl):S2039.
9. Rolls BJ, Bell EA. Intake of fat and carbohydrate: role of energy
density. Eur J Clin Nutr 1999;53(suppl 1):S6673.
All cereals may not be equal
Dear Sir:
I wish to comment on the article by Liu et al in your September
1999 issue (1), which found an inverse relation between the prevalence
of coronary heart disease and whole-grain consumption in a large
prospective study of nurses. In 1988, I carried out a statistical study (2)
in which the consumption of60 food items in 21 countries belong-
ing to the Organization of Economic Cooperation and Development
(OECD) was correlated with mortality from coronary disease. My
results, regarding cereal consumption, were as follows in Table 1:
As far as correlation with coronary disease is concerned, all cere-als appear to be different. A negative correlation was found only with
rice consumption, and even this could be due to an indirect linkage.
Coronary mortality in eastern Asia could be low on account of low fat
and milk consumption but give the appearance of a negative correla-
tion with high rice consumption. Similarly, the high positive correla-
tion with oats consumption could be indirect. Appreciable quantities
of oats are consumed only in a few countries of northern Europe. The
true correlation could be between coronary disease mortality and
environmental temperature. The world leaders in coronary disease
mortality are Russia and its neighbors, which all have cold climates.
In warmer countries, coronary mortality tends to be lower, and very
low in the tropics. In my opinion, the connection between coronary
disease and grain consumption must be treated with caution.
Stephen Seely
3 Truro Drive
Sale, Cheshire M33 5DF
United Kingdom
REFERENCES
1. Liu S, Stampfer MJ, Hu FB, et al. Whole-grain consumption and
risk of coronary heart disease: results from the Nurses Health
Study. Am J Clin Nutr 1999;70:4129.
2. Seely S. Diet and coronary arterial disease: a statistical study. Int J
Cardiol 1988;20:18392.
Reply to S Seely
Dear Sir:
We appreciate Seelys proposition that all cereals my not be
equal in affecting risk of coronary heart disease mortality. We
would like to emphasize 2 main points. First, in a prospective
cohort study, we reported an inverse relation between whole-
grain consumption and the incidence, not prevalence, of coro-
nary heart disease (1). The difference between prevalence and
incidence is subtle but important. Prevalence includes people
with coronary heart disease at baseline who may have changedtheir diet after disease diagnosis.Incidence studies can provide a
direct assessment of the association between diet and disease
that would not be confounded by factors modified after disease
diagnosis (2). Second, the study by Seely can at best suggest a
hypothesis to be explored because of important limitations inher-
ent in any such international correlation or ecologic study,
including the crude assessment of diet, lack of information on
individual diets, and the lack of adjustment for confounding fac-
tors including genetic predisposition, environment, and lifestyle
practices (3). Seely noted only a few of the many differences
between these countries. Large prospective cohort studies with
detailed dietary assessment, long-term follow-up, and careful
control of multiple confounding factors are better suited to
examine diet-disease associations.
Simin Liu
JoAnn E Manson
Walter C Willett
Brigham and Womens Hospital
Division of Preventive Medicine
900 Commonwealth Avenue East
Boston, MA 02215-1204
REFERENCES
1. Liu S, Stampfer M, Hu F, et al. Whole-grain consumption and risk
of coronary heart disease: results from the Nurses Health Study.Am J Clin Nutr 1999;70:4129.
2. Rothman KJ, Greenland S. Modern epidemiology. 2nd ed. Philadel-
phia: Lippincott-Raven Publishers, 1998.
3. Willett WC. Nutritional epidemiology. 2nd ed. New York: Oxford
University Press, 1998.
856 LETTERS TO THE EDITOR
TABLE 1
Correlation between cereal consumption and mortality from coronary
disease
Food item
Wheat 0.03
Rye 0.33
Barley 0.20
Oats 0.95
Maize 0.27
Rice 0.55
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