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Transcript
RESEARCH
Commentary
Fluid Energy—Where’s the Problem?
RICHARD D. MATTES, PhD, MPH, RD
T
he position that energy derived from a fluid may hold
different appetitive and dietary implications than
energy obtained from a solid food is more than a
quarter century old (for examples, see references 1 and 2).
The preponderance of early trials revealed energy-yielding fluids did not elicit strong reductions of hunger or
compensatory dietary responses either in an absolute
sense or relative to solid foods matched on properties,
including energy, macronutrient composition, and palatability. The vehicles used in these studies ranged from
clear beverages to dairy-based formulas to soups (3).
Viewed collectively, the hypothesis emerged that energyyielding fluids may pose a particular problem for energy
balance.
Subsequent research has helped to clarify and refine
understanding of the issue. The original view that different types of fluids elicit comparable appetitive and dietary effects is no longer tenable. Clear distinctions are
emerging, making it useful to classify fluid foods into four
categories based on their effects on satiety and energy
balance. Recognition of these product differences is essential to move understanding forward because negating the
effect of one category of fluids (eg, beverages) by citing
evidence from another (eg, soups) may misdirect attention from real issues.
FLUIDS WITH STRONG SATIETY VALUE THAT MAY NOT
PROMOTE POSITIVE ENERGY BALANCE
Some fluids, such as soups, have high satiety value and
elicit strong dietary compensation. The satiation/satiety
properties of soups are consistently observed in acute
feeding trials (4-8), although the mechanism has not been
firmly established. Attributes such as energy and nutrient composition, chemosensory properties, energy density, temperature, and volume do not appear responsible
because matching soups to solid foods on these properties
does not eliminate differential responses (7,8). One feature that distinguishes soups and beverages is the cognitive impression they impart to consumers (7,9-11). It is
R. D. Mattes is a professor of foods and nutrition, Department of Foods and Nutrition, Purdue University,
West Lafayette, IN.
Address correspondence to: Richard D. Mattes, PhD,
MPH, RD, Professor of Foods and Nutrition, Department of Foods and Nutrition, Purdue University, 212
Stone Hall. 700 W State St, West Lafayette, IN 479072059. E-mail: [email protected]
Copyright © 2006 by the American Dietetic
Association.
0002-8223/06/10612-0016$32.00/0
doi: 10.1016/j.jada.2006.10.026
1956
Journal of the AMERICAN DIETETIC ASSOCIATION
well established that expectations may alter appetite ratings (12,13) and merely labeling a beverage a soup enhances the appetitive response it elicits (8). It is hypothesized that this is due to a belief that soup is nutritive and
augments meal size, rather than serving as a beverage to
satisfy thirst or aid oral clearing. However, additional
mechanisms, such as the timing and mode of ingestion,
still cannot be excluded. Whether due to its satiety property or another mechanism, there is evidence that soup
ingestion reduces energy intake in a subsequent meal
(4,6-8,14,15). Larger servings (15) and chunky soups (14)
exert stronger effects, but all are moderate in size. Soup
may augment weight loss and maintenance of reduced
body weight (16), but these effects must be verified.
FLUIDS DESIGNED FOR STRONG SATIETY VALUE YET MAY
PROMOTE POSITIVE ENERGY BALANCE
Another category of dietary fluids is designed to have
high satiety value, yet these are widely used to promote
weight gain in those challenged to preserve body weight,
such as elderly persons or various clinical populations
(eg, patients with cancer or human immunodeficiency
virus/acquired immunodeficiency syndrome) (17-19).
Meal replacement beverages are an example of fluids
effective in this capacity in part because their satiation/
satiety value is still lower than that of a solid food. More
energy can be consumed in an eating occasion with these
products and their ingestion is less likely to replace another eating occasion. The rationale for maximizing the
satiety value of these products does not stem from this
use, but rather for their application in energy-restricted
diets to promote weight loss or maintenance of lower body
weight. They can be effective for this purpose (20), but it
is not clear that their satiety value is the functional
property. Their incorporation into controlled feeding regimens may be the critical component.
FLUIDS WITH LIMITED SATIETY VALUE YET MAY NOT
PROMOTE POSITIVE ENERGY BALANCE
A third type of fluid has low satiety value, but despite this
and its high energy content, exerts limited influence on
body weight. This group is typified by alcohol, when ingested in moderation. Excessive consumption results in
alterations of behavior and physiology that are beyond
the present scope of consideration. When ingested as an
aperitif, alcohol augments hunger (21) and diminishes
satiation (22,23). It also elicits a weak compensatory dietary response (24), so energy intake is increased. The
positive energy balance promoted by alcohol has strong
support in the epidemiologic (25-29) and intervention
(24,30) literatures and occurs in men and women, young
and elderly, as well as light and heavy consumers
© 2006 by the American Dietetic Association
(27,29,31,32). Estimates of energy compensation range
from 0% to 40%. Possible explanations for their limited
satiation/satiety properties include weak effects on intestinal osmoreceptors (33,34) and gut peptide release (35),
rapid gastrointestinal transit time (36), and/or an effect
on ingestion of fat (27,37). The augmentation of hunger
may stem from reduced cognitive inhibition of feeding
due to alcohol’s psychoactive properties and the social
context in which it is often consumed. Despite these effects on appetite and energy balance, there is conflicting
evidence pertaining to the influence of alcohol on body
weight. Studies showing a direct relationship between
alcohol intake and body weight are intuitive. An explanation for the reverse is more problematic. Nevertheless,
a strong case may be made that the energy from alcohol
has little effect on body weight. Observations based on
data from the first and second National Health and Nutrition Examination Surveys (38,39) and the Nurses
Health Study and Health Professionals Follow-up Study
(40), in addition to twin studies (41,42), fail to confirm a
direct relationship. Mechanisms for the latter have been
proposed, but not substantiated (43). If ethanol energy is
not efficiently absorbed or used, and regulatory energy
balance processes are active in human beings, the weak
compensatory dietary response to alcohol may reflect a
limited need for any dietary adjustment.
FLUIDS WITH WEAK SATIETY VALUE THAT MAY PROMOTE
POSITIVE ENERGY BALANCE
The fourth class of energy-yielding fluids would include
those that have low satiety value and promote positive
energy balance. This group includes beverages and, most
notably, energy-containing clear fluids (eg, soda, specialty teas and coffees, sports drinks, and some fruit
juices). It is an especially important grouping because of
their considerable contribution to daily energy intake.
The work by Storey and colleagues (44) reported on p
1992 in this issue of the Journal indicates they account
for approximately 16% to 20% of total energy for individuals aged 6 to 60 years. These new data are important,
not only because of their documentation of high levels of
consumption, but also for identifying variability associated with sex, age, and ethnicity. The weak satiety effects
of clear beverages have been amply documented (9,10,4547). It holds in younger and older populations and different ethnic groups (9,10,46,48-51). Importantly, it occurs
for beverages with different macronutrient compositions.
In particular, the stronger satiety value of protein noted
in solid foods is ameliorated or lost in fluid products (52),
even with substantive loads (53). Higher energy intake
has also been reported among consumers of gourmet teas
and coffees where fat may be a substantive source of
energy (54), as well as dairy products with higher protein
content (11). Whereas soda is the single largest source of
energy in the US diet (55), and its primary source of
energy is carbohydrate, the totality of the literature suggest the amount or particular form of sugars may not be
as important as the fluid medium in determining the
effects of these beverages on energy balance. There is a
direct relationship between viscosity and hunger suppression (56) and a meta-analysis revealed a graded dietary compensation response to ingestion of fluid, semisolid, and solid foods (3) with clear liquids eliciting no
compensation. Moreover, there is limited adaptation with
chronic use (47).
Isolated trials have failed to note a differential effect of
solid and fluid foods matched on energy content, but these
exceptions may stem from methodological issues. For example, they have been noted under atypical conditions
where food was delivered by pump (57). Strong compensation for fluids has also been reported in very young
children (58,59). However, they display more precise compensation generally during their early years and this is
lost by about age 5. Thus, extrapolation of this case to
adolescents, adults, or elderly people is uncertain. Another exception entails designs where appetite is measured following ingestion of large loads (eg, 710 mL), use
of foods not customarily consumed at the time of day
testing was conducted (midmorning snacking is uncommon) (60), testing when participants were not hungry
(thus, potentially creating floor effects), and assessments
at intervals shorter than normal intermeal intervals (eg,
20 minutes or 2 hours) (61). Actually, the failure to note
a differential effect of fluid vs solid foods on appetite
under such conditions also speaks to the lack of sensitivity to fluid loads because they had greater levels of other
attributes associated with satiety such as volume and
weight (almost eightfold).
The nutritionally important question is whether or not
these products exert an effect on energy balance that
differs from comparable solid items. The argument that
they do is based on literature documenting that the relationship between their ingestion and body weight or body
mass index (BMI) is temporarily logical, consistent,
strong, specific, and coherent. Although the BMI of the
population has probably been increasing for over 250
years (62), a sharp rise occurred about three decades ago.
This was associated with a 150 to 300 kcal/day increase of
daily energy intake (63). During this time, the number of
servings and serving sizes of beverages increased (63).
Daily energy derived from beverages increased from 2.8%
to 7.0% and they are estimated to have contributed energy equal to about 50% of the total increment in energy
intake (63). Thus, the temporal trends support an association. The consistency of an association between beverage consumption and BMI is supported by evidence that
it holds in adults and children, males and females, and
different ethnic groups (50,51,64-70). Furthermore, an
analysis of data from the 1994 Continuing Study of Food
Intakes by Individuals revealed a dose–response relationship between beverage and energy intake in adolescents
(49). The strength of association is supported by multiple
controlled animal model studies (for examples, see references 71 and 72) as well as observational and intervention trials with human beings documenting a weaker
compensatory dietary response to fluids compared to solids and/or a direct relationship between clear beverage
consumption and BMI (3,9,51,65,66,68,70,71,73,74). Evidence indicating the relationship is specific stems from
findings that adding caloric beverages to the diet leads to
elevations of energy intake and weight gain (65,75) while
their reduction or elimination from the diet results in
lower energy intake and BMI (67,76,77). A within-subject
intervention trial directly contrasting responses to fluid
and solid foods showed weight gain only with the fluid
load (65). Furthermore, a controlled trial with humans
December 2006 ● Journal of the AMERICAN DIETETIC ASSOCIATION
1957
has demonstrated non– energy-containing fluid ingestion
is not associated with increased energy intake or body
weight, but both increase with the addition of an energy
source to the beverage (78). This is expanded in the study
by Flood and colleagues (79) reported in this issue of the
Journal (p 1984) who observed the inclusion of larger
portions of energy-yielding beverages in a meal led to
increased energy intake due to a lack of adjustment in
food intake. A weak compensatory dietary response to
beverages has been reported within meals (11) and over
days (69,70).
Collectively, these points lead to a coherent argument
that beverages may be contributing to positive energy
balance and the increasing incidence and prevalence of
overweight/obesity. However, another important element
is identification of plausible mechanisms. Why might energy-yielding fluids exert different effects on energy balance than solid foods? To date, much of the work on this
topic has focused on establishing the phenomenon with
limited exploration of mechanisms. Feeding is guided by
environmental and physiological (eg, cognitive, orosensory, digestive, metabolic, endocrine, and neural) influences. Differential responses may be posited at each level.
Environmentally, portion sizes of beverages have increased markedly (80,81), they are among the least expensive sources of energy, and are a meal component that
is provided in unlimited quantity in most commercial
restaurants. Beverages have lower expected satiety
value, lower demand for oral processing, shorter gastrointestinal transit times, and the energy they contain has
greater bioaccessibility and bioavailability. Each of these
attributes has been associated with weaker effects on
appetite and dietary compensation (65,82-89). The absolute and relative importance of these properties, and others, has not been established, but warrants exploration.
An additional possibility is that clear beverages alter diet
composition and may displace components that help regulate intake. A popularly cited example is milk. However,
milk also seems to elicit a weak compensatory dietary
response (11).
IMPLICATIONS FOR FUTURE RESEARCH AND CLINICAL
PRACTICE
Recognition of the differences in the appetitive and dietary effects of various energy-yielding fluids should help
clarify their health implications and guide future research. To isolate the effects of the medium (ie, fluid)
rather than some other physical (eg, solid form) or chemical (ie, macronutrient) property on appetite and or diet,
it is essential that the identical foods be used. Studies
comparing the appetitive responses to fruit juice and the
same whole food (45,90) approach this standard and have
noted weaker satiety effects for the fluid form. Still, better-controlled studies are required because these contrasts do not account for dietary fiber, a known satiety
factor. It will also be important to explore and control the
effects of thirst on appetite. Although the physiological
systems controlling these sensations are distinct, fluids
are increasingly ingested as food/meal replacements. The
acute and long-term dietary consequences of this substitution are unknown, but based on the literature cited
here, may be expected to increase energy intake.
Taken together, it appears that clear beverages are
1958
December 2006 Volume 106 Number 12
especially problematic for energy balance. They are
widely consumed, elicit weak compensatory dietary responses, promote positive energy balance, and increase
body weight. Some have recommended their use be restricted, especially by children and adolescents. This has
prompted the exploration or passage of regulations on the
availability of sweetened carbonated beverages and sport
drinks in schools (eg, California bill SB965). Currently,
more than 60% of states are considering or have enacted
legislation limiting sales of such products in schools or
during school hours (91). It is often proposed that these
products be replaced with more healthful beverages such
as fruit juice (for an example see reference 92); however,
the literature indicates these products are also problematic with respect to energy balance. So, the efficacy of this
approach, with respect to weight management, is questionable. An alternative is to replace the energy-rich versions with non– energy-containing substitutes. This
would permit continued consumption with limited affect
on energy intake. Whether such an approach has negative implications for overall diet quality is a separate but
meritorious issue. Alternatively, clear beverages can continue to be ingested at their current level if a conscious
effort is made to offset the energy contributed by this
source through reductions of food intake. The practicality, efficacy, and nutritional implications of this approach
are also not known. Clearly there is a need for objective
study of these options. The two articles in this issue of the
Journal provide useful insights toward this end. They
document levels of consumption by different subgroups of
the population (44) and the effects on energy balance of
incorporating different serving sizes of energy-containing
beverages into meals (79).
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