Download Carbohydrates and health—the FAO/WHO consultation

Carbohydrates and health—the FAO/WHO
consultation
Thomas Wolever
Introduction
Carbohydrates are the single most important source of
energy for the world for human nutrition. Over the last 15
or 20 years there has been a lot of research conducted that
has completely changed the way we think about dietary
carbohydrates. For that reason the Food and Agriculture
Organization (FAO) of the United Nations and the World
Health Organization (WHO) convened an expert consultation on carbohydrates in human nutrition that was held in
Rome in 1997, involving scientists from 13 countries (1).
Many people feel that carbohydrates are unhealthy and
we, as health professionals, need to correct that message.
One of the most important recommendations that the consultation made was that the many health benefits of
carbohydrate foods should be recognised and promoted.
The health benefits of carbohydrates are many and
include their roles in weight management and physical
activity, in diabetes prevention and treatment, cardiovascular disease and cancer. One of the FAO/WHO
recommendations was that an optimum diet of at least
55% of energy from carbohydrate is recommended for
everybody over the age of two. For young children fat
restriction may reduce their ability to obtain enough
energy in the diet. Although a high carbohydrate diet is
also appropriate for the elderly in general, this may need
to be individualised because of concomitant medical or
dental conditions or medication use.
Carbohydrates and energy balance
It was recommended that energy balance should be maintained with a diet containing 55% of total energy from
carbohydrate. How is energy balance promoted with a
high carbohydrate diet? There is much evidence that a
high carbohydrate diet promotes weight maintenance. In a
study of healthy subjects who lived in a metabolic chamber for seven days, by the end of the period on a diet with
60% of energy from fat they had consumed over 16 700kJ
(4000 cal) more energy than they had expended. Even on
a typical Western diet containing 40% of energy from fat
and 47% from carbohydrate, they were still in positive
energy balance when given free access to foods. However,
when their fat intake was reduced to 20% of total energy
and carbohydrate intake increased to 67% of energy, they
actually came into negative energy balance, consuming
less than they expended (2) (Figure 1). This is probably
because a high carbohydrate diet is very bulky and is difficult to overeat.
Why then are high carbohydrate diets so unpopular?
Why do the books promoting low carbohydrate diets
become best-sellers (3)? It is because over the first few
days of a high carbohydrate diet people actually gain
weight so the diet does not appear to work. But this is
because people are storing more muscle glycogen and
body water is accumulating. If they persist with these
diets then weight loss will indeed occur.
Figure 1. Effect of varying proportions of dietary
carbohydrate and fat on energy balance in human
subjects (2)
Energy Balance (Kcal)
Abstract Carbohydrates are the single most important source
of food energy in the world and have significant additional
health influences. In April 1997, the Food and Agriculture
Organization of the United Nations and the World Health Organization convened an expert consultation on carbohydrates in
human nutrition in Rome that involved scientists from 13 countries. The consultation considered all aspects of carbohydrate
nutrition and interpreted the current science on the health impact
of dietary carbohydrates, especially where controversy existed.
The ultimate aim was to promote a nutritious and safe food supply globally. Progress in carbohydrate chemistry and our
growing understanding of the diverse physiological roles of carbohydrates in recent decades has led to new dietary approaches
in which carbohydrates play a key role. Diet is one of the major
risk factors in many modern diseases and dietary carbohydrates
can beneficially influence obesity, type 2 diabetes, coronary
heart disease and some cancers. The expert consultation released
22 recommendations to be passed to member countries to assist
them to develop their own dietary guidelines. This paper focuses
on the findings and recommendations related to the role of carbohydrates in the maintenance of health, including
recommendations on the minimum content of carbohydrate in
the diet, the most appropriate sources, the role of carbohydrates
in body weight and endurance exercise, the practical applications of the glycaemic index and implications of carbohydrates
for diabetes, cancer and cardiovascular disease. (Aust J Nutr
Diet 2001;58 Suppl 1:S3–S8)
27:13:60
4000
3000
Carb:Pro:Fat
(%energy)
2000
47:13:40
1000
0
67:13:20
-1000
0
1
2
3
4
5
6
7
Days on Diet
Department of Nutritional Sciences, University of Toronto, Canada
T. Wolever, DM, PhD, Professor of Nutritional Sciences and Medicine
Correspondence: T. Wolever, Department of Nutritional Sciences,
University of Toronto, Toronto, Ontaria, Canada M5S. Email:
[email protected]
Australian Journal of Nutrition and Dietetics (2001) 58 Suppl 1
S3
Carbohydrates and physical activity
The benefits of high carbohydrate intakes for physical
activity have been known for a long time. In classic studies, Bergstrom et al. measured the time to exhaustion for
cycling when subjects were fed three different kinds of
diets (4). On a high carbohydrate diet the subjects cycled
for three times longer than when they were on a high fat
diet. This was related directly to the level of muscle glycogen that was accumulated before the exercise began.
After exercise they had depleted their muscle glycogen to
an equivalent extent on each diet.
Importance of dietary fibre
A high carbohydrate diet is recommended, but does it
matter what kinds of foods are consumed? The
FAO/WHO recommended that the bulk of carbohydrates
consumed should be rich in non-starch polysaccharides or
dietary fibre and have a low glycaemic index.
Recent research shows that dietary fibre can have a
potentially positive effect in helping to maintain weight.
Studies from Ludwig et al. of prospective ten-year weight
gain in young adults found that fat intake did not affect
weight gain. However, there was less weight gain for
those with a higher fibre intake (5) (Figure 2). This suggests that having a high intake of dietary fibre may be an
important way of helping to maintain a healthy body
weight.
Glycaemic index
The glycaemic index (GI) was one of the new aspects
which was brought into the FAO/WHO recommendations.
The GI is defined as the blood glucose response of a 50 g
carbohydrate portion of food, expressed as a percentage
for the same amount of carbohydrate from a reference
food taken by the same subject (6). Both bread and glucose
have been used as the reference food but, for international
standardisation, it is recommended that GI values should
be expressed relative to glucose.
There is a large range of blood glucose responses to
foods for the same amount of carbohydrate, both within
and between various food groups (7). Very importantly,
these differences in blood glucose response are reflected
in similar differences in plasma insulin response (8).
Foods with low blood glucose and insulin responses tend
to be digested and absorbed slowly (9,10). Thus, the consultation recommended that for healthy food choices both
Figure 2. Associations of dietary fibre and fat with ten-year
weight gain in young adults (5)(a)
10-Year W eight Gain (lb)
White men and women (n=1602)
Tertiles of Fiber Intake
<6.8g/1000Kcal
6.8-9.0g/1000Kcal
>9.0g/1000Kcal
30
Black men and women (n=1307)
30
20
20
10
10
0
<33.2
33.2-39.1
>39.1
0
<33.2
Tertiles of Fat Intake (% of energy)
Ludwig et al. JAMA 1999;282:1539-46.
(a) 1 lb = 0.4 kg, 1 kcal = 4.2 kJ.
S4
33.2-39.1
>39.1
the chemical composition and the physiological effects of
food carbohydrate should be considered, because food
composition alone does not predict what the physiological
effects will be.
Effects of mixed meals on glucose and insulin
responses
It is often considered that fat and protein have a major
effect on blood glucose and insulin responses. However,
we proposed that variation in source and amount of carbohydrate was the primary determinant of blood glucose and
insulin responses after normal mixed meals. To test this
we fed healthy subjects test meals containing zero to
100 g carbohydrate from each of four single foods varying
in GI so as to derive equations to predict glucose and insulin responses based on the amount and GI of the
carbohydrate consumed (11). We then fed a different group
of healthy subjects five mixed meals that were unmatched
to each other with respect to their contents of energy
[1670–2500 kj (400–600 kcal)], carbohydrate (38–104 g),
protein (12–25 g), fat (8–24 g) and GI (43–99). If fat and
protein were important in determining glucose and insulin
responses, we would have expected that our equations
based on carbohydrate alone would not be very accurate.
However, we found that the predictions based on carbohydrate alone explained over 90% of the variation of the
glucose and the insulin responses of the mixed meals (12).
The large differences in protein and fat content of the
mixed meals had negligible effects on glucose and insulin
responses.
Glycaemic index and physical activity
The kind of carbohydrate one eats also has relevance to
physical activity. Studies done by Brand-Miller et al. demonstrate that if one has a snack of a low GI carbohydrate
before exercise, then the endurance achieved is significantly greater than if one has a high GI carbohydrate
snack (13). On the other hand, Burke et al. have shown that
eating high GI foods aids recovery from strenuous activity. On a high GI diet significantly more muscle glycogen
accumulated than after a low GI diet (14). So both high and
low GI foods may be useful for athletes for various
situations.
Regional variation in glycaemic index
The FAO/WHO recommended that the published glycaemic response data should be supplemented with tests of
local foods normally prepared because of possible effects
of food variety in cooking. For example, the ripeness of
banana is very important. If a banana is under-ripe
(slightly green at the tips) compared to one that is slightly
over-ripe (yellow with a few brown spots), this makes a
50% difference in the blood glucose response (15). These
are very subtle differences in ripeness.
Another important example is potato. Brand Miller
and colleagues tested several varieties of potatoes in Australia and have found that, regardless of how they are
cooked, potatoes have a very high GI (16). We have found
different results in tests on Canadian potatoes which
tended to have intermediate GI values (17). We recently
exchanged foods with Dr Brand Miller’s unit and when
Australian Journal of Nutrition and Dietetics (2001) 58 Suppl 1
we both tested exactly the same foods we obtained virtually identical results. This suggests that there are real
differences in GI between Australian and Canadian
potatoes.
Clinical use of glycaemic index
The FAO/WHO recommended that the GI should be
employed as a useful indicator of the impact of foods on
blood glucose. It should be used to compare foods of similar macronutrient composition within food groups and for
clinical applications including diabetes and impaired glucose tolerance.
There is much evidence that low GI foods improve
blood glucose control in diabetes. For example, we studied overweight subjects with type 2 diabetes for six weeks
and found a significant improvement in glycosylated
serum proteins with a low GI diet (18). In a recent review
of nine studies in the literature on the use of low GI diets
in the treatment of diabetes, eight of them show a statistically significant improvement in glycated serum
proteins (19). The average improvement in all nine studies,
10%, is of similar magnitude to that achieved in the
United Kingdom prospective diabetes study with oral
hypoglycaemic agents or insulin (20).
Carbohydrates and insulin sensitivity
Many diseases, such as obesity, heart disease and diabetes, are thought to be related to insulin sensitivity (21)
(Figure 3). Insulin sensitivity is a concept that describes
how sensitive the body is to the effects of insulin on whole
body glucose uptake. An insulin-sensitive person needs a
very small amount of insulin to dispose of glucose at a
normal rate. An insulin-resistant person needs much more
insulin to achieve a normal rate of glucose disposal. In
some way we do not understand, the body senses that an
individual is insulin-resistant and compensates by secreting a large amount of insulin. People that are insulinresistant with normal glucose levels have high blood
insulin (22).
Insulin resistance is partly due to genes, and is
strongly inherited (23). However, insulin sensitivity also is
affected by environmental factors. Physical activity promotes insulin sensitivity (24) and obesity promotes insulin
resistance (25). There is now a view that the high blood
insulin concentration related to insulin resistance might
actually cause obesity because the high insulin levels may
alter fat cell metabolism or the morphology of fat cells in
some way.
Hyperinsulinaemia may enhance the insulin resistance
by down-regulating insulin receptors. This results in a
vicious cycle whereby insulin resistance causes a high
plasma insulin concentration which, in turn, promotes
more insulin resistance (26). Insulin resistance is associated with heart disease because high blood insulin and
insulin resistance lead to an increased rate of synthesis of
very low density lipoproteins (VLDL) in the liver and a
low rate of VLDL clearance from the blood (27). This, in
turn, leads to the atherogenic blood lipid profile characterised by increased plasma triglyceride and low high density
lipoprotein (HDL) cholesterol concentrations (28). These
lipid abnormalities also raise plasma free fatty acids (29),
which not only feed-back and make insulin resistance
worse (30) but also impair β-cell function (31). Insulin
resistance is associated with the development of type 2
diabetes because, in the presence of insulin resistance,
blood glucose can be maintained within the normal range
only if the pancreatic β-cells can secrete large amounts of
insulin. If the β-cells begin to fail, and are unable to maintain such high rates of insulin secretion, then blood
glucose begins to rise, leading to type 2 diabetes (32).
Dietary carbohydrates can affect this process in a
number of ways. Although a high carbohydrate, low fat
diet results in higher postprandial insulin responses, it is
also associated with reduced postprandial plasma free
fatty acids (33,34). The reduction in free fatty acids may
help to improve insulin sensitivity and restore β-cell function. Use of low GI carbohydrates may have the added
benefit of putting less strain on the pancreas because less
insulin is required for their metabolism.
Sugars
The FAO/WHO consultation concluded that there was no
evidence that sugars or starch are involved in lifestylerelated disorders, but that intakes of carbohydrates and
sugars in excess of energy requirements should be
avoided.
Data from Scotland show that people who eat the largest amount of sugar have the lowest prevalence of obesity.
This is exactly opposite to what most people believe and
in fact, in this study, high fat intakes were related to
obesity (35).
Some people believe that sugar causes a special
increase in insulin, but this is not true. We fed zero to
100 g doses of glucose, sucrose and fructose to healthy
subjects and compared the resulting glucose and insulin
responses to the same doses of starch from bread. In all
cases the plasma insulin responses were directly proportional to the glucose responses elicited by the test meals.
There was no additional secretion of insulin after the sugars in comparison to the starch (36). Another point is that
sucrose (sugar) actually tends to produce lower glucose
and insulin responses than an equal amount of carbohydrate from bread and many other refined starchy foods.
Figure 3. Relationship between lifestyle factors (diet and
exercise), obesity, insulin resistance, pancreatic βcell function, type 2 diabetes and atherosclerosis(a)
ATHEROSCLEROSIS
! Plasma TG, " HDL
Liver: ! VLDL synthesis
Adipose: " VLDL clearance
Hyperinsulinaemia
OBESITY
Insulin Resistance
Physical Inactivity
Diet
Plasma FFA
Hyperglycaemia
Beta-cell Function
Beta-cell Stimulation
Beta-cell Exhaustion
Reduced Insulin Secretion
TYPE 2 DIABETES
(a) TG, triglycerides; HDL, high density lipoprotein; VLDL, very low
density lipoprotein; FFA, free fatty acids.
Australian Journal of Nutrition and Dietetics (2001) 58 Suppl 1
S5
This is counter-intuitive to many health professionals and
people with diabetes who have been taught the opposite
for so many years.
However, it has been shown in normal (37) and
diabetic (17) subjects that sugar-sweetened cereal produces
a significantly lower blood glucose response than a cereal
that is not sugar-sweetened. This does not mean that people with diabetes should eat an unlimited amount of sugar;
but there is no need for undue avoidance of sugar. Sugar
probably has a role in helping to make healthy foods more
palatable and thus promoting their consumption.
Carbohydrates and cancer
In terms of the role of carbohydrates for cancer, the data
are not as strong as other areas. However colon and rectal
cancer and breast and prostate cancers tend to be associated with high intakes of meat, protein and, to a lesser
extent, fat. Low risk for these cancers is associated with
high intakes of fruit and vegetables and, to a lesser extent,
cereals. Butyrate produced by colonic bacterial fermentation of unabsorbed carbohydrates has a number of
potential benefits for cancer prevention including
increased cell differentiation and increased apoptosis or
death of damaged cells. In established tumours, butyrate
reduces cell proliferation rates. It is of interest, then, that
starch fermentation yields a higher proportion of butyrate
than the fermentation of dietary fibre. Finally, many carbohydrate foods are rich in phytochemicals and antioxidants that may have beneficial effects.
Carbohydrates and cardiovascular disease
There is some controversy about the role of carbohydrates
for cardiovascular disease. Few would argue with the contention that if we could reduce obesity this might help to
reduce cardiovascular disease. It also is well established
that a high carbohydrate diet lowers low density lipoprotein cholesterol by displacing saturated fat and that certain
types of soluble fibre may lower serum cholesterol. Blood
pressure is lowered by high intakes of vegetable and fruit,
probably because of their high potassium and low sodium
content. What is more controversial is the effect of carbohydrates on blood triglycerides and HDL-cholesterol.
A number of studies, such as those from Reaven et al.,
have shown that high carbohydrate diets are associated
with increased triglycerides, VLDL triglycerides and
reduced HDL-cholesterol (38). This did not dissuade the
FAO/WHO consultation from recommending a high carbohydrate diet for a number of reasons. Firstly, these were
quite short-term studies—the longest ones being only
about six weeks long. There is some evidence that the rise
in triglycerides is only temporary and returns toward baseline after many months on the diet (39). Secondly, the rise
in triglycerides and reduction in HDL does not occur with
all kinds of carbohydrates. High carbohydrate diets with
high fibre intakes or low GI foods will partly or completely mitigate these deleterious effects (40).
Finally, studies showing the deleterious effects of high
carbohydrate diets are designed with the subjects on both
diets being forced to eat exactly the same amount of
energy. However, it is known that people tend to eat a
little less energy when on high carbohydrate diets. The
S6
point is made very well by a study from Schaefer et al.
which showed that when people on high carbohydrate
diets were forced to maintain weight, their blood lipids
deteriorated. But when they followed an ad libitum high
carbohydrate diet, their weight fell and there was no deterioration of the blood lipids (41).
Carbohydrates and diabetes
Diabetes is a very important condition which is reaching
worldwide epidemic proportions. In virtually every country of the world, it is estimated that within 25 years the
number of people with diabetes will nearly double (42). In
developed countries this increase in diabetes largely will
take place in people over the age of 65 years, reflecting
our aging population and the fact that diabetes is more
prevalent in the older age groups. The tragedy, however, is
that in developing countries the increase largely will occur
in middle-aged subjects at the peak of their productive
lives. This is likely due to the increased Westernisation
and rising rates of obesity in these countries. So the
FAO/WHO consultation recommended that populations in
transition from traditional diets to diets more like those in
developed countries should be provided with dietary recommendations to ensure nutritional adequacy and an
appropriate balance of micronutrients.
What kind of a diet should be recommended for populations at high risk for diabetes? One school of thought is
that a high carbohydrate diet should not be used by people
with insulin resistance because it is associated with an
increase in plasma insulin which not only has deleterious
effects on blood lipids and cardiovascular risk, but also
may make insulin sensitivity worse. Again, the
FAO/WHO was not persuaded by this argument because it
is known from other studies that high carbohydrate diets
are associated with improvements in fasting blood glucose
and improvements in oral glucose tolerance, measures
that are used to define diabetes. A high carbohydrate diet
is also associated with lower plasma insulin response to a
standard carbohydrate challenge (43).
Indeed, it is not just the amount of total carbohydrate
that is important, but also its quality, including the amount
of dietary fibre and its GI. Data from the nurses health (44)
and health professionals (45) studies, conducted at Harvard
University, show that the amount of total carbohydrate in
the diet was not related to the risk of developing diabetes
in either men or women (Figure 4). However, in an almost
identical fashion, higher fibre intakes were associated
with reduced risk of diabetes and a high GI diet with
increased risk of diabetes. This protective effect of low GI
diets potentially could be due to improved insulin sensitivity.There is at least one study showing that there was an
improvement in insulin sensitivity when women with a
family history of cardiovascular disease ate a low GI
diet (46).
Thus, in considering the role of carbohydrates on the
risk of developing diabetes, it is possible to speculate that
a high carbohydrate diet may be beneficial by improving
β-cell function, perhaps by reducing plasma free fatty
acids, and that high fibre, low GI foods may be beneficial
by improving insulin sensitivity.
Australian Journal of Nutrition and Dietetics (2001) 58 Suppl 1
Figure 4. Association of total carbohydrate and dietary fibre intakes and diet glycaemic index (GI) with risk of developing
diabetes in males (45) and females (44)
Total Carbohydrate
Men - ns
Women - ns
1.5
Relative Risk
Cereal Fibre
Glycaemic Index
Men - p=0.007
Women - p=0.001
Men - p=0.03
Women - p=0.005
1.0
0.5
0.0
1
2
3
4
5
1
2
3
4
5
1
2
3
4
5
Quintiles of Intake (adjusted for energy; GI also adjusted for cereal fibre)
Environmental impact of human diets
9.
The health of the individual ultimately is related to the
health of the environment. The world population has
increased rapidly from about one billion after the end of
World War II, to about four billion now, and estimated to
reach six billion in the next 25 years. This increase in population, if not caused by, has certainly been sustained by,
the increased availability of carbohydrate foods as a result
of the green revolution. Some argue that the human diet
should be low in carbohydrate and high in protein, similar
to that consumed by our hunter-gatherer ancestors. However, a hunter-gatherer diet is expensive both from the
economic and ecological points of view; it sustained a
world population of only a few hundred million human
beings. We now have ten times as many mouths to feed,
and perhaps the only sustainable way to do so is with carbohydrate foods. Therefore we must strive to ensure the
best quality of carbohydrates for human health.
Jenkins DJA, Ghafari H, Wolever TMS, Taylor RH, Barker HM,
Fielden H, et al. Relationship between the rate of digestion of foods
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15. Wolever TMS, Jenkins DJA, Jenkins AL, Vuksan V, Wong GS,
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Australian Journal of Nutrition and Dietetics (2001) 58 Suppl 1