Dietary Theodore
fiber B. Van
and
Italbie,3
It has
intake
of food
and
depot
ingestion,
interfering
slightly countries
diet.
intake
Per
of the
effect
has
of caloric or
no
and
the
total
dilttion
with
subjects.
excess
weight
excessive nisms.
an
weight Am.
in even
J. Cbin. Nut,.
that
dietary
the
fiber
Journal
of Clinical
Nutrition
and
the
31: S43-S52,
31: OCTOBER
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
fiber
can of
reduce
has
protect
less
against diet
may
spontaneous
although
obese
agents
obesity
and
than
intake
humans
may
nonobese
deserves
prevent
have
laboratory
their
therefore to
further
overeating in
type
Studies
bulking rats
of but
the
of nonobese
tenacity
energy
nature
decreased,
considerably. inert
tend
rate
of obesity
in the
greatly
Thus,
intake that
with
excessive slowing
prevalence
changes
metabolically
is evidence
the
in the
diminished
energy
diet,
intestinal satiety. and
increased.
have
to prevent
of the
foods
has not
other
dilution
content
tend
marked
starchy
spontaneous there
not
increase with
with may
nutritive
if it does
The
vegetables
quantity
Nevertheless,
During the past century the prevalence of human obesity has increased to the extent that it is now the most common form of malnutrition in the United States and in many other countries (1). The reason for this modern epidemic is not known in any categorical sense, but most authorities agree that it must have resulted from widespread changes in life style, specifically in type of diet and level of physical activity. Such changes have been imposed by a highly industrialized culture that has substituted machines for human labor and supermarkets for farmers’ markets. The relative contribution of a changing diet and diminished physical activity to the increased incidence of obesity can only be conjectured; however, there is little doubt that in sedentary populations the nature of the diet and the way foods are promoted and made available can play a major part in determining the prevalence of obesity. As shown in Figure 1, the most obvious changes that have occurred in the American diet since the turn of the century have been a dramatic decrease in consumption of starchy foods and an increase in sugar and total fat intake (2). Figure 2 illustrates the changes that have taken place in the supplies The American
green
will
density
in eating, promoting
associated
on
caloric
concurrently
cellulose
effect against
hypothesis increase gain
fiber
in the diet
the
absorption. place
fruits
human The
taken
with
and
since
has
inhibitory
fiber
involved
changed,
their
testing
effort
of dietary
animals
sufficient
of energy
1900
defend counterparts.
that
by decreasing
the
efficiency
intake
diet
little
suggested
accumulation
since
associated
in the
disclosed
with
capita
of fiber
of fiber
been fat
increasing
in Western the
2
M.D.
ABSTRACT food
obesity1’
nonobese
and orga-
1978.
per capita of the principal sources of carbohydrates available to retail markets. From 1889 to 1961, total carbohydrates available to consumers decreased by about 28% (from 534 to 385 g/day) while the ratio of complex to simple carbohydrate showed more than a threefold drop (3). During the first half of the 20th century, a 10% decrease occurred in per capita consumption of food energy (Fig. 1), presumably reflecting in part the increasing displacement of human muscular work by machines during the same interval. As pointed out by Cummings (4) and others (5, 6), changes similar to those in the United States have occurred in the British diet. On the basis of these kinds of data, one could surmise that the rising incidence of obesity may have resulted (at least in part) from an increase in fat and/or sugar intake, or simply from an increase in the caloric density of the diet. Recently, however, the proposition has been advanced that the freFrom
the
Department
of Medicine
and
Institute
of
Human Nutrition, College of Physicians and Surgeons, Columbia University, and St. Luke’s Hospital Center, New York, New York 10025. 2Supported in part by a grant from the National Institutes of Health (Obesity Center, AM-17624). Professor of Medicine.
1978,
pp. S43-S52.
Printed
in U.S.A.
S43
VAN
S44
ITALLIE
140
20
too 0/0
80
60
40 909(3
L “5
STARCH
.
‘20
-
‘25
‘30
‘35
‘40
‘45
‘50
‘555658
YEARS
FIG. 1. Changes in the American diet during the first half of the 20th century. Starch consumption fell 50% while the consumption of sugar and fat increased 25 and 16% respectively. (Adapted from Fortune magazine article by F. Bello, December 1959).
quency of obesity in Western countries may be related to the fact that an increasing proportion of our dietary carbohydrate has become refined and therefore fiber depleted. This paper reviews briefly some of the evidence that relates to this proposition and assesses the hypothesis in the light of what we currently know (or think we know) about the pathogenesis of human obesity. The possible role of dietary fiber in prevention of obesity has been discussed in two recent publications. Heaton (7) has called attention to three physiological obstacles to energy intake provided by dietary fiber: 1) it displaces available nutrients from the diet; 2) through increased chewing, it reduces the rate of food ingestion and promotes secretion of saliva and gastric juice that contribute to stomach distension and thereby promote satiety; and 3) it reduces slightly the efficiency with which the small intestine absorbs certain foodstuffs, notably fat and protein. Heaton has also suggested that refined products such as white flour and sugar are inherently liable to cause excess energy intake because they
140 20 and
S7rups
Simple
Sugars
Sugars
Total
CHO
CHO
of Cmez#{231}ftQ Simple CHO
Yeors
FIG. from
2. Percentage
Reference
changes
in supplies
of carbohydrates
3.).
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
from
1889 through
1961 (Reproduced
by permission
DIETARY
FIBER
can be ingested rapidly and absorbed efficiently. Trowell (8) pointed out that obesity is rare among the populations of developing countries where a high proportion of dietary calories is consumed as starchy carbohydrates almost undepleted of fiber. It is also his view that, when taken ad hibitum, high-fiber diets induce a greater satiety effect than do lowfiber diets of comparable energy content. He attributes this increment in satiety value to the fact that a high-fiber diet leaves a larger residue of undigested material in the intestine, with a corresponding increase in sensations of bulk and distension. Some of the arguments that appear to support the hypothesis linking obesity with the ingestion of an excessive proportion of fiberdepleted carbohydrates are summarized below (5, 7, 8): 1) Fiber-depleted food is calorically more concentrated than fiber-intact food. 2) Food fiber promotes chewing, thereby increasing the effort required to eat and retarding the rate of food ingestion. 3) Diets rich in fiber tend to decrease absorptive efficiency. 4) Fiber-depleted food is less satiating than a calorically equivalent amount of the fiberintact original (e.g., white bread is less satiating than whole wheat bread). 5) Obesity is rare in populations that consume high-fiber diets and is common in populations that consume low-fiber diets. 6) Certain animals (e.g., the Egyptian sand rat) that normally eat a high-fiber diet become obese on diets reduced in fiber content. It is incontestable that a sufficient content of fiber in food will decrease energy density and will also promote chewing. In contrast, fiber-depleted foods like sugar, white bread, and polished rice are comparatively more concentrated in calories and can be ingested with little or no masticatory effort. These facts raise two questions: Does the rate at which food is eaten affect the total amount consumed? Can the energy density of the diet chronically influence the amount of food energy ingested and absorbed? The first question confronts an issue about which there has been much speculation but little definitive information. In recent years, human eating behavior has received increasing attention; various parameters of eating,
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AND
OBESITY
S45
including rate of ingestion, have been studied by the use of such devices as closed-circuit television (9), electronically monitored eating utensils (R. D. Moon, unpublished observations), and automated food dispensers (10, 11). Preliminary findings from the studies of Hill and McCutcheon (9) and others (12) indicate that obese persons may eat at a significantly faster rate than nonobese controls. Recent experiments conducted by Kaplan (13), however, fail to support the notion of a more rapid eating rate in the obese; on the other hand, like Meyer and Pudel (14), Kaplan observed that overweight males did not decrease their rate in intake over the duration of a meal to the same extent as normal-weight males. This observation is believed to have implications for satiety. Finally, Jordan and Spiegel (15) have reported that obese subjects appear to be satisfied with less food if they slow their rate of eating by chewing longer, drinking water between mouthfuls, and reducing bite size. The generality of such observations needs to be established by more extensive studies; nevertheless, many behavior therapists are now attempting to teach their obese patients to eat more slowly (16). The principal rationale that is usually advanced to explain why a reduction in rate of eating might be beneficial is based on the supposition that, if food is eaten rapidly, the normal satiety mechanisms in the gastrointestinal tract will not have sufficient time to function properly, resulting in the ingestion of an excessive quantity of food. This explanation has received some support from a study reported by Jordan (17), which suggests that, under single meal conditions, individuals will eat more if they are somehow induced to increase their ingestion rate. Thus, if a person is forced to eat rapidly by a pump that delivers food into his mouth, he will spontaneously eat more than he would under conditions favoring a reduced rate of ingestion. Rapid eating may overwhelm the gastrointestinal satiety mechanism by filling the stomach before a sufficient amount of its contents have been emptied into the small intestine to activate the satiety signals (18) that would normally prevent the ingestion of an excess number of calories. Unfortunately, there is a dearth of experimental work that could tell
VAN
S46
us
whether
a
sustained
change
in
rate
ITALLIE
of
eating per se will induce an equally prolonged change in the amount of food eaten. As Heaton (7) has pointed out, increased chewing does more than slow intake: it adds effort to the act of eating. In this regard, several studies have shown that, when animals with various types of experimental obesity are required to exert extra effort to obtain food (usually by a demanding reinforcement schedule), they will reduce energy intake and lose weight (19). It remains to be demonstrated whether the increased effort involved in chewing fiber-rich food will actually be of sufficient magnitude to discourage potentially obese humans from overeating. An experiment described by Schachter and Friedman (20) provides some encouragement for the notion that obese humans will eat less when forced to work to obtain food. In this study, obese and lean subjects were given access to bowls of nuts which on one occasion were without shells and on another occasion retained their shells. The scenario was designed to permit spontaneous eating while the attention of the subject was focused elsewhere. About half the lean subjects ate the nuts regardless of whether they had to remove the shells. In contrast, only one in 20 of the obese subjects ate any nuts when they had to expend the extra effort needed to remove the shells, but virtually all the obese individuals ate the nuts from which the shells had been removed beforehand. In a somewhat similar experiment, Rodin (2!) showed that moderately obese subjects drank significantly smaller amounts of thick milkshake through a straw with a small bore than through a straw with a large bore. In contrast, nonobese subjects drank about the same quantity through the “difficult” straw as they did through the “easy” straw. There are no clear answers to the second question: Can the energy density of the diet chronically influence the amount of food energy ingested and absorbed? This uncertainty exists because the problem becomes increasingly complex as it is given more careful attention. Considered at its face value, the question is deceptively simple; to begin to answer it, however, one would have to know precisely how the caloric dilution or concentration would be accomplished, the nature of
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the species to be tested, and the nutritional status of the subject under investigation. The literature contains several reports that can be used to sustain any one of a number of different points of view concerning the putative effect of changing the caloric density of the diet on spontaneous food intake. For example, in a classic study reported 30 years ago, Adolph (22) demonstrated that, when the diet of rats was diluted with kaolin or cellulose, the animals compensated perfectly by consuming enough extra food to maintain energy intake and body weight at constant levels. This effect was confirmed by Kennedy (23) in 1950. On the other hand, subsequent studies (24) showed that, when certain strains of rats are fed a high-fat diet, they promptly increase total energy intake and become obese. Unfortunately, it is not yet clear whether a diet rich in fat induces such a response because of some unique property possessed by this nutrient or simply because a high-fat diet is also a calorically concentrated diet. To complicate matters further, Kennedy (23) has demonstrated that, in rats with hypothalamic obesity, substantial caloric dilution of the diet can bring about weight loss-at least while marked obesity is still present. Here again there are problems of interpretation, and it remains unclear whether, in such experiments, caloric dilution reduces energy intake by adversely affecting the palatability of the diet, by increasing the physical effort required to ingest the food, or by some other mechanism (25). For example, the presence of obesity could render an animal especially sensitive to the satiating effects of the increased bulk conferred on a diet by the addition of an indigestible dihuent. No discussion of the possible role of dietary fiber in preventing obesity can neglect the information generated by investigators who have attempted to assess the efficacy of methylcellulose and other bulking agents as appetite suppressants. In 1959, Yudkin (26) reported that when 3.3 g of methylceh!ulose was ingested by overweight human volunteers 30 mm before meals, a reduction in food intake and some weight loss ensued. A year later, Duncan et al. (27) found methy!celhuhose to be ineffective as an appetite depressant when the preprandial dose was 1.5 g, less than one-
DIETARY
FIBER
half that used by Yudkin. Subsequently, Evans and Miller (28) studied the effect of methylcellulose and guar gum on the food intakes and body weights of 11 volunteers, of whom three were obese. Each subject received both agents in successive experimental periods lasting 1 week. Each experimental period was preceded or separated by a baseline period of 1 week. The subjects took 10 g of methylcelhulose or 9 g of guar gum with a glass of water 30 mm before luncheon and dinner. At these dosage levels, and with the data averaged on all the subjects, the bulking agents appeared to reduce food intake by about 10%, and some weight loss occurred. Of considerable interest was the observation that the obese subjects lost much more weight (1.7 ± 0.4 kg/week) than did the lean subjects (0.1 ± 0.! kg/week). Indeed, the effect of the two bulking agents on the nonobese subjects, taken as a separate group, appears to have been negligible. Obviously, it is difficult to draw any firm conclusion from such a shortterm study. These preliminary results do suggest, however, that it might be rewarding to conduct a double-blind trial of the effect of buhking agents in a larger group of obese subjects studied for a longer period of time. In our laboratory, Gehiebter (29) has studied the effect of various liquid preloads, nutritive and nonnutritive, on the intake by nonobese individuals of a nutritionally complete test meal, also liquid, offered 70 mm later. The test meal was consumed ad hibitum through a straw from a hidden container. Twelve healthy males of normal weight, with ages ranging from 21 to 36, participated. They fasted for 13 hr before each experiment. The nutritive loads had a volume of 450 ml each and consisted of 283 kcah of either egg albumin, corn starch, corn oil, or a mixture of these. The noncalorie loads consisted of a mixture of kaolin and cellulose (67.4 g in 450 ml of water) and 450 ml of water given alone. Taste and olfactory differences between the loads was minimized by mildly anesthetizing the subjects’ mouths with a topical application of xyhocaine and then by applying nose clips. Indeed, the subjects remained unaware of the nature of the loads, and none realized that one load consisted of water alone. The mean test meal intake is shown in Figure 3. For the purposes of the present
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AND
OBESITY
S47
-%
FIG. 3. Mean test meal intakes after different loads in humans. Note failure of kaolin-cellulose (K/C) load to suppress subsequent food intake as compared with a control of load of water (WAT) alone. Overall, intakes were significantly smaller after caloric loads than after noncaloric loads (29).
discussion, it is necessary only to note that, in this particular experimental setting, 67.4 g of a kaolin and cellulose mixture given as a liquid preload did not inhibit the subsequent intake of a test meal to a greater extent than did a comparable volume of water. Although the data on which they are based are often less than satisfactory, scattered reports (30) indicate that the average weights of the inhabitants of Western countries have increased substantially during the last 50 years. In the United States, three successive surveys (31-33) have provided evidence that the weight of Americans has continued to rise since mid-century, even allowing for a slight concurrent increase in height. Figure 4 contains data on the average body weights of groups of American men (ages 30 to 34 and 5’8” tall) from 1863 to 1962. Although there is no way of knowing how representative the earlier samples were of the overall population, these data (34) suggest that the average weight of American men has increased substantially since the time of the War Between the States; in the case of this particular category, the increment is about 20 pounds. Assuming that such an increase in weight has in fact occurred, can this phenomenon be attributed to a corresponding change in the fiber content of the diet? The reply to this question can only be that too little is known, at the present time, about the effect of dietary fiber on spontaneous energy intake in man to
VAN
S48
ITALLIE
70
CIVILIANS
(6O
OFFICERS
RMY
K (0
CIVIL WAR SOLDIERS
SEPARATEES ARMY
RED IANS
CIVIL
RECRUITS
.1
(863 (850
(924
(900
875
(94346
925
(962
1950
YEARS FIG.
4.
Average
body
weights
of groups
of American
permit the formulation of a persuasive hypothesis. Indeed, it is not clear whether the total amount of fiber in the diet has decreased substantially during the last century or whether it is only the type of dietary fiber that has changed. In this regard, it may be instructive to consider Trowell’s (35) recent comments about food and fiber in the British diet since 1850. What he says may be applicable to the American experience: In 1970, the average adult British diet contained 4 grams of crude fibre per day: cereals 0.5 grams, potato 1.0 grams, fruit, vegetables and nuts 2.5 grams. In 1850, the average adult British diet also contained about 4 grams of crude fiber per day, but it was derived from different sources: cereals 1.5 grams, potato 1.6 grams, fruit, vegetables and nuts probably about 1 gram. The average adult British crude fibre intake has remained therefore almost stationary during the past 110 years. On
the other
hand,
cereal
crude
fibre
decreased
about
70%
and fibre from vegetables and fruit increased in a corresponding manner. Does this matter? This is one of the fundamental questions in the dietary fibre hypothesis.
Thus far, our attention has been focused on the arguments supporting the hypothesis that food fiber serves as a significant obstacle to energy intake and that foods from whith fiber has been removed promote obesity. Let us now consider this hypothesis in the light of other concepts about the pathogenesis of obesity. In the development of such concepts, a consideration of several animal models of obesity has been helpful. Two such models seem especially relevant to human obesity. They are the genetically obese rat, first de-
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men
ages
30 to 34 and
5’8”
tall
(34).
scribed by Zucker and Zucker (36), and the dietary-obese rat described by Schafani and Springer (19). The adipose tissue of the Zucker obese rat is characterized by both hyperplasia and hypertrophy (37). Unlike normal rats, Zucker rats develop obesity on a stock diet of rat pellets (38). Normal rats can be made obese by adding “snack foods” to their regular diet of rat pellets (19). As shown in Figure 5, food items that induce the rat to overeat and become obese include such items as chocolate candy bars, marshmallows, cookies, bananas, salami, cheese, and sugared breakfast cereal. When rats with snack-food-induced obesity are returned to a diet limited to rat pellets, they spontaneously reduce their food intake and lose weight rapidly. It is not until they return to the weight of their controls that they once more consume sufficient food energy to prevent further weight loss (19). The obesity induced by the snack-food diet appears to be highly resistant to the weight-reducing effect typically seen when caged animals are permitted to exercise voluntarily in activity wheels (19). Even forced exercise is only moderately successful in reversing this form of dietary obesity (S. Gale and T. B. Van Itallie, unpublished observations). However, neither rats given free access to a snack-food diet (19) nor mice fed a fat-enriched diet (39) gain weight in a uniform fashion. That some animals in each population are able to remain relatively lean despite these dietary cha!lenges suggests that genetic factors may be
DIETARY
FIBER
AND
S49
OBESITY
/
A I
I
B FIG. 5. Normal obese on snack-food
rat remaining lean on items (B). (Photographs
diet of standard rat pellets provided by S. K. Gale.)
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
(A),
while
previously
lean
sibling
becomes
S50
VAN
involved in determining tibility to such diets. In recent years, two obesity ogy of
have their
characterized hypertrophy; pocyte
the
level
major
been distinguished adipose tissue
of suscep-
types (40).
of human
by morpholOne type
by adipocyte hyperplasia the other shows principally
hypertrophy.
The
former
ITALLIE
type
is
and adiis more
commonly found in individuals whose obesity began in infancy, childhood, or at some point prior to the cessation of linear growth; the latter type is more often identified among individuals whose obesity started during adult life. As might be expected, hyperplastichypertrophic obesity is generally more severe than hypertrophic obesity; however, the association
of
these
two
morphologic
forms
with any particular age of onset is not clearcut. For example, many patients whose obesity appears to have begun after the age of 21 exhibit adipocyte hyperplasia as well as hypertrophy. Despite these qualifications, it must be apparent that the two morphologic types of human obesity bear more than a casual resemblance to the two animal models described earlier. Indeed, there is a growing belief that there may be two predominant types of obesity in Western countries: one that is constitutionally determined and one that results from the interaction between a psychologically
or
biologically
predisposed
individual and his environment. In the former type, the chief pathogenetic impetus arises in the individual; in the latter type, the environment seems to play a much larger role. The first type may be genetically determined or may result from infant feeding practices that favor fat cell hyperplasia. The second type involves a complex constellation of etiohogic factors, including chronic physical inactivity, the persistent use of food for nonnutritive purposes, and a life style that is especially vulnerable to the manifold opportunities and incentives provided by our culture to overeat. The nature of the diet is an important component of that life style. There is every reason to believe that in many instances the second type of obesity is superimposed on the first type. Also, there must exist many intergrades between the two types, considered as pure forms. How important is food fiber in this overall
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picture? At the present time, it is impossible to say. For example, it is not yet known why the snack-food diet causes rats to become obese. Sclafani and Springer (19) believe that the inherent palatability of this diet, and particularly its novelty and variety, causes rats to overeat and in some instances to become discernibly obese. However, the precise composition of the snack-food diet, as ingested, has yet to be reported; it is certainly calorically concentrated, high in sugar content, and devoid of plant fiber. Would such a diet fail to produce obesity if food fiber were somehow incoporated into the component foods? Questions of this kind deserve further exploration. Finally, there is a growing body of evidence to suggest that animals (4!) and humans (42) with hypertrophic obesity defend their excess weight with less tenacity than animals and people with normal-sized fat cells. Individuals with enlarged adipocytes are more likely than nonobese persons to lose weight when challenged by a change in the palatability of their diet (43) or by an increased level of physical activity (44). Note has already been taken of the preliminary evidence (28) suggesting that obese persons are more responsive than lean subjects to the appetite suppressing effects of bulking agents. Thus, it would not be surprising if subjects with hypertrophic obesity were to exhibit a reduction in food intake and weight loss following a shift from a diet depleted in plant fiber to one rich in fiber. By an extension of this reasoning, it is possible to argue that a fiber-rich diet could also make a contribution to the prevention of obesity. How important such a contribution might be is a question that can only be resolved by future clinical investigation. El References I. OIANCOVA, K., AND S. HEJDA. Epidemiology of obesity. In: Obesity: Its Pathogenesis and Management, edited by J. T. Silverstone. Acton, Mass.: Publishing Sciences Group, 1975, pp. 57-91. 2. Consumption of Food in the United States 1909-52. Supplement for 1961 to Agricultural Handbook No. 62, Washington, D.C.: U.S. Department of Agriculture, 1962. 3. ANTAR, M. A., M. A. OHLSON AND R. E. HODGES. Changes in retail market food supplies in the United States in the last seventy years in relation to the
DIETARY
4. 5.
6. 7. 8. 9.
10.
11.
12.
incidence of coronary heart disease, with special reference to dietary carbohydrates and essential fatty acids. Am. J. CIin. Nutr. 14: 196, 1964. CUMMINGS, J. H. Dietary fibre. Gut 14: 69, 1973. TROWELL, H. C. Dietary changes in modern times. In: Refined Carbohydrate Foods and Disease. Some Implications of Dietary Fibre, edited by D. P. Burkitt and H. C. Trowell. London: Academic Press, 1975. ROBERTSON, J. Changes in the fibre content of the British diet. Nature 238: 290, 1972. HEATON, K. W. Food fibre as an obstacle to energy intake. Lancet 2: 1418, 1973. TROWELL, H. Obesity in the Western world. Plant Foods Man 1: 157, 1975. HILL, S. W., AND N. B. MCCUTCHEON. Eating responses of obese and non-obese humans during dinner meals. Psychosomat. Med. 37: 395, 1975. HASHIM, S. A., AND T. B. VAN ITALLIE. An automatically monitored food dispensing apparatus for the study of food intake in man. Federation Proc. 23: 82, 1964. JORDAN, H. A., W. F. WIELAND, S. P. ZEBLEY, E. STELLAR AND A. J. STUNKARD. Direct measurement of food intake in man: a method for the objective study of eating behavior in man. Psychosomat. Med. 28: 836, 1966. STUNKARD, A., AND D. KAPLAN. Eating in public places:
a review
of eating 13.
FIBER
of
behavior.
reports
of
Internat.
the
direct
J. Obesity
observation
AND
Physiol.
22. 23. 24.
D. L. Eating style of obese and non-obese Doctoral dissertation, University of Penn1977. MEYER, J. E., AND V. PUDEL. Experimental studies of food intake in obese and normal weight subjects. J. Psychosomat. Res. 16: 305, 1972. JORDAN, H. A., AND T. A. SPIEGEL. Palatability and oral factors and their role in obesity. In: The Chemical Senses and Nutrition, edited by M. Kane and 0. Mallen. New York: Academic Press, 1977. JORDAN, H. A., L. S. LEVITZ AND 0. M. KIMBRELL. Eating is Okay! A Radical Approach to Successful Weight Loss. New York: Rawson Associates. 1976, p. 53. JORDAN, H. A. Physiological control of food intake in man. In: Obesity in Perspective, edited by 0. A.
26. 27.
28. 29.
30. 31.
persons. sylvania,
14.
15.
16.
17.
Bray.
DHEW
Publication
No. (NIH)
75-708,
adult
rats:
Similarities
to
hypothalamic
and
human
obesity 20.
21.
syndromes. Physiol. Behav. 17: 461, 1976. SCHACHTER, S., AND L. N. FRIEDMAN. The effects of work and cue prominence on eating behavior. In: Obese Humans and Rats, edited by S. Schachten and J. Rodin. Potomac, Md.: Earlbaum Associates, 1974, pp. 11-14. RODIN, J. Effects of obesity and set point on taste responsiveness and ingestion in humans. J. Comp.
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
high-fat
32.
33.
35.
Statistics,
of adults
ZUCKER,
mutation 37.
57: 541,
1955.
Washington,
D.C.: PHS.
Pub-
18-74
years
of age in the United
States. Washington, D.C.: Advance Data from Vital and Health Statistics, No. 3, pp. 1-8, November 19, 1976. HATHAWAY, M. L., AND E. D. FOARD. Heights and Weights of Adults in the United States. Home Economics Research Report No. 10. Washington, D.C.: U. S. Department of Agriculture, 1960. TROWELL, H. C. Dietary fibre and colonic diseases. In: The Present State of Knowledge, No. 6. London:
Norgine 36.
J. Nutr.
lication No. 1000, Series 11, No. 14, May 1966. U. S. Department of Health, Education, and Welfare. Ten state nutrition survey 1968-1970. DHEW Pub. (HSM) 72-8 134. Atlanta, Ga.: Center for Disease Control, 1972. National Center for Health Statistics. Height and
weight
34.
diets.
A. Appetite and hunger in experimental obesity syndromes. In: Hunger: Basic Mechanisms and Clinical Implications, edited by D. Novin, W. Wyrwicka and 0. A. Bray. New York: Raven Press, 1976, pp. 28 1-295. YIJDKIN, J. The causes and cure of obesity. Lancet 2: 1135, 1959. DUNCAN, L. J. P., K. ROSE AND A. P. MEICKLEJOHN. Phenmetrazine hydrochloride and methylcellulose in the treatment of refractory obesity. Lancet 1: 1662, 1960. EVANS, E., AND D. S. MILLER. Bulking agents in the treatment of obesity. Nutr. Metabol. 18: 199, 1975. GELIEBTER, A. A. The effects of equal caloric loads of protein, fat and carbohydrate, and non-caloric loads on food intake in the rat and man. Doctoral dissertation, Columbia University, 1976 (University Microfilms, 1976, No. 76-29846, Ann Arbor, Michigan). KHOSLA, T., AND C. R. ROWE. Height and weight of British men. Lancet 1: 742, 1968. National Center for Health Statistics. Weight by Height and Age of Adults, United States, 1960-1962. SCLAFANI,
Vital Health
Wash-
ington, D.C.: U.S. Government Printing Office, 1975, pp. 35-47. 18. VAN ITALLIE, T. B., S. K. GALE AND H. R. KISSILEFF. The control of food intake in the regulation of depot fat: An overview. In: Diabetes, Obesity and Vascular Diseases: Molecular and Metabolic Interrelationships. Advances in Modern Nutrition, edited by H. M. Katzen and R. J. Mahlen. New York: John Wiley, vol. 2, 1978, part 2, pp. 427-492. 19. SCLAFANI, A., AND D. SPRINGER. Dietary obesity in
Psychol. 89: 1003, 1975. E. F. Urges to eat and drink in rats. Am. J. Physiol. 151: 110, 1947. KENNEDY, 0. C. The hypothalamic control of food intake in rats. Proc. Roy. Soc. 137: 535, 1950. MICKELSEN, 0., 5. TAKAHASHI AND C. CRAIG. Expenimental obesity I . Production of obesity in rats ADOLPH,
by feeding 25.
1: 89, 1977.
KAPLAN,
S5 1
OBESITY
JOHNSON, HIRSCH.
Ltd.,
1976, pp. 5-6.
L. M., AND T. F. ZUCK.ER. Fatty, in the rat. J. Hered. 52: 275, 1961. P. R., L. M. ZUCKER, J. A. CRUCE Cellularity
of
adipose
depots
in the
a new AND
J.
geneti-
cally obese Zucker rat. J. Lipid Res. 12: 706, 1971. 38. ZUCKER, L. M. Some effects of caloric restriction and deprivation on the obese hyperlipemic rat. J. Nutn. 91: 247, 1967. 39. DE LAEY, P. Hypothalamic and nutritional obesities in mice. A comparative study of growth and body
composition. 388, 1975. 40.
Internat.
Pharmacodynam.
216:
J., AND B. BATCHELOR. Adipose tissue celin human obesity. Clin. Endocrinol. Metab. 1976. SULLIVAN, A. C., J. TRISCARI AND K. COMAI. Caloric HIRSCH,
lularity 5: 299,
41.
Arch.
VAN
S52
compensatory
responses
nonabsorbable
carbohydrate
lean Zucker 42.
rats.
to diets
Am. J. Clin.
containing
on lipid
Nutr.
by
either obese
31: S261,
and
1978.
0. CARLGREN, B. IsAKssoN, M. B. LARSSON AND L. SJ#{246}STR#{246}M. The effect of an energy-reduced dietary regimen in relation to adipose tissue cellularity in obese women.
BJ#{246}RNTORP,
ITALLIE
P.,
KORTKIEWSKI,
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
Am.
43.
J. Clin. Nutr. 28: 445, 1975. S. A., AND T. B. VAN
HASHIM,
normal dispensing
and
obese device.
subjects Ann.
with N.
Y.
ITALLIE.
Studies
a monitored Acad.
Sci.
in
food 131:
651,
1965. 44. BJ#{246}RN’rORP, P. Exercise in the treatment Clin. Endocrinol. Metabol. 5: 431, 1976.
of obesity.
fiber B. Van
and
Italbie,3
It has
intake
of food
and
depot
ingestion,
interfering
slightly countries
diet.
intake
Per
of the
effect
has
of caloric or
no
and
the
total
dilttion
with
subjects.
excess
weight
excessive nisms.
an
weight Am.
in even
J. Cbin. Nut,.
that
dietary
the
fiber
Journal
of Clinical
Nutrition
and
the
31: S43-S52,
31: OCTOBER
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
fiber
can of
reduce
has
protect
less
against diet
may
spontaneous
although
obese
agents
obesity
and
than
intake
humans
may
nonobese
deserves
prevent
have
laboratory
their
therefore to
further
overeating in
type
Studies
bulking rats
of but
the
of nonobese
tenacity
energy
nature
decreased,
considerably. inert
tend
rate
of obesity
in the
greatly
Thus,
intake that
with
excessive slowing
prevalence
changes
metabolically
is evidence
the
in the
diminished
energy
diet,
intestinal satiety. and
increased.
have
to prevent
of the
foods
has not
other
dilution
content
tend
marked
starchy
spontaneous there
not
increase with
with may
nutritive
if it does
The
vegetables
quantity
Nevertheless,
During the past century the prevalence of human obesity has increased to the extent that it is now the most common form of malnutrition in the United States and in many other countries (1). The reason for this modern epidemic is not known in any categorical sense, but most authorities agree that it must have resulted from widespread changes in life style, specifically in type of diet and level of physical activity. Such changes have been imposed by a highly industrialized culture that has substituted machines for human labor and supermarkets for farmers’ markets. The relative contribution of a changing diet and diminished physical activity to the increased incidence of obesity can only be conjectured; however, there is little doubt that in sedentary populations the nature of the diet and the way foods are promoted and made available can play a major part in determining the prevalence of obesity. As shown in Figure 1, the most obvious changes that have occurred in the American diet since the turn of the century have been a dramatic decrease in consumption of starchy foods and an increase in sugar and total fat intake (2). Figure 2 illustrates the changes that have taken place in the supplies The American
green
will
density
in eating, promoting
associated
on
caloric
concurrently
cellulose
effect against
hypothesis increase gain
fiber
in the diet
the
absorption. place
fruits
human The
taken
with
and
since
has
inhibitory
fiber
involved
changed,
their
testing
effort
of dietary
animals
sufficient
of energy
1900
defend counterparts.
that
by decreasing
the
efficiency
intake
diet
little
suggested
accumulation
since
associated
in the
disclosed
with
capita
of fiber
of fiber
been fat
increasing
in Western the
2
M.D.
ABSTRACT food
obesity1’
nonobese
and orga-
1978.
per capita of the principal sources of carbohydrates available to retail markets. From 1889 to 1961, total carbohydrates available to consumers decreased by about 28% (from 534 to 385 g/day) while the ratio of complex to simple carbohydrate showed more than a threefold drop (3). During the first half of the 20th century, a 10% decrease occurred in per capita consumption of food energy (Fig. 1), presumably reflecting in part the increasing displacement of human muscular work by machines during the same interval. As pointed out by Cummings (4) and others (5, 6), changes similar to those in the United States have occurred in the British diet. On the basis of these kinds of data, one could surmise that the rising incidence of obesity may have resulted (at least in part) from an increase in fat and/or sugar intake, or simply from an increase in the caloric density of the diet. Recently, however, the proposition has been advanced that the freFrom
the
Department
of Medicine
and
Institute
of
Human Nutrition, College of Physicians and Surgeons, Columbia University, and St. Luke’s Hospital Center, New York, New York 10025. 2Supported in part by a grant from the National Institutes of Health (Obesity Center, AM-17624). Professor of Medicine.
1978,
pp. S43-S52.
Printed
in U.S.A.
S43
VAN
S44
ITALLIE
140
20
too 0/0
80
60
40 909(3
L “5
STARCH
.
‘20
-
‘25
‘30
‘35
‘40
‘45
‘50
‘555658
YEARS
FIG. 1. Changes in the American diet during the first half of the 20th century. Starch consumption fell 50% while the consumption of sugar and fat increased 25 and 16% respectively. (Adapted from Fortune magazine article by F. Bello, December 1959).
quency of obesity in Western countries may be related to the fact that an increasing proportion of our dietary carbohydrate has become refined and therefore fiber depleted. This paper reviews briefly some of the evidence that relates to this proposition and assesses the hypothesis in the light of what we currently know (or think we know) about the pathogenesis of human obesity. The possible role of dietary fiber in prevention of obesity has been discussed in two recent publications. Heaton (7) has called attention to three physiological obstacles to energy intake provided by dietary fiber: 1) it displaces available nutrients from the diet; 2) through increased chewing, it reduces the rate of food ingestion and promotes secretion of saliva and gastric juice that contribute to stomach distension and thereby promote satiety; and 3) it reduces slightly the efficiency with which the small intestine absorbs certain foodstuffs, notably fat and protein. Heaton has also suggested that refined products such as white flour and sugar are inherently liable to cause excess energy intake because they
140 20 and
S7rups
Simple
Sugars
Sugars
Total
CHO
CHO
of Cmez#{231}ftQ Simple CHO
Yeors
FIG. from
2. Percentage
Reference
changes
in supplies
of carbohydrates
3.).
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
from
1889 through
1961 (Reproduced
by permission
DIETARY
FIBER
can be ingested rapidly and absorbed efficiently. Trowell (8) pointed out that obesity is rare among the populations of developing countries where a high proportion of dietary calories is consumed as starchy carbohydrates almost undepleted of fiber. It is also his view that, when taken ad hibitum, high-fiber diets induce a greater satiety effect than do lowfiber diets of comparable energy content. He attributes this increment in satiety value to the fact that a high-fiber diet leaves a larger residue of undigested material in the intestine, with a corresponding increase in sensations of bulk and distension. Some of the arguments that appear to support the hypothesis linking obesity with the ingestion of an excessive proportion of fiberdepleted carbohydrates are summarized below (5, 7, 8): 1) Fiber-depleted food is calorically more concentrated than fiber-intact food. 2) Food fiber promotes chewing, thereby increasing the effort required to eat and retarding the rate of food ingestion. 3) Diets rich in fiber tend to decrease absorptive efficiency. 4) Fiber-depleted food is less satiating than a calorically equivalent amount of the fiberintact original (e.g., white bread is less satiating than whole wheat bread). 5) Obesity is rare in populations that consume high-fiber diets and is common in populations that consume low-fiber diets. 6) Certain animals (e.g., the Egyptian sand rat) that normally eat a high-fiber diet become obese on diets reduced in fiber content. It is incontestable that a sufficient content of fiber in food will decrease energy density and will also promote chewing. In contrast, fiber-depleted foods like sugar, white bread, and polished rice are comparatively more concentrated in calories and can be ingested with little or no masticatory effort. These facts raise two questions: Does the rate at which food is eaten affect the total amount consumed? Can the energy density of the diet chronically influence the amount of food energy ingested and absorbed? The first question confronts an issue about which there has been much speculation but little definitive information. In recent years, human eating behavior has received increasing attention; various parameters of eating,
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AND
OBESITY
S45
including rate of ingestion, have been studied by the use of such devices as closed-circuit television (9), electronically monitored eating utensils (R. D. Moon, unpublished observations), and automated food dispensers (10, 11). Preliminary findings from the studies of Hill and McCutcheon (9) and others (12) indicate that obese persons may eat at a significantly faster rate than nonobese controls. Recent experiments conducted by Kaplan (13), however, fail to support the notion of a more rapid eating rate in the obese; on the other hand, like Meyer and Pudel (14), Kaplan observed that overweight males did not decrease their rate in intake over the duration of a meal to the same extent as normal-weight males. This observation is believed to have implications for satiety. Finally, Jordan and Spiegel (15) have reported that obese subjects appear to be satisfied with less food if they slow their rate of eating by chewing longer, drinking water between mouthfuls, and reducing bite size. The generality of such observations needs to be established by more extensive studies; nevertheless, many behavior therapists are now attempting to teach their obese patients to eat more slowly (16). The principal rationale that is usually advanced to explain why a reduction in rate of eating might be beneficial is based on the supposition that, if food is eaten rapidly, the normal satiety mechanisms in the gastrointestinal tract will not have sufficient time to function properly, resulting in the ingestion of an excessive quantity of food. This explanation has received some support from a study reported by Jordan (17), which suggests that, under single meal conditions, individuals will eat more if they are somehow induced to increase their ingestion rate. Thus, if a person is forced to eat rapidly by a pump that delivers food into his mouth, he will spontaneously eat more than he would under conditions favoring a reduced rate of ingestion. Rapid eating may overwhelm the gastrointestinal satiety mechanism by filling the stomach before a sufficient amount of its contents have been emptied into the small intestine to activate the satiety signals (18) that would normally prevent the ingestion of an excess number of calories. Unfortunately, there is a dearth of experimental work that could tell
VAN
S46
us
whether
a
sustained
change
in
rate
ITALLIE
of
eating per se will induce an equally prolonged change in the amount of food eaten. As Heaton (7) has pointed out, increased chewing does more than slow intake: it adds effort to the act of eating. In this regard, several studies have shown that, when animals with various types of experimental obesity are required to exert extra effort to obtain food (usually by a demanding reinforcement schedule), they will reduce energy intake and lose weight (19). It remains to be demonstrated whether the increased effort involved in chewing fiber-rich food will actually be of sufficient magnitude to discourage potentially obese humans from overeating. An experiment described by Schachter and Friedman (20) provides some encouragement for the notion that obese humans will eat less when forced to work to obtain food. In this study, obese and lean subjects were given access to bowls of nuts which on one occasion were without shells and on another occasion retained their shells. The scenario was designed to permit spontaneous eating while the attention of the subject was focused elsewhere. About half the lean subjects ate the nuts regardless of whether they had to remove the shells. In contrast, only one in 20 of the obese subjects ate any nuts when they had to expend the extra effort needed to remove the shells, but virtually all the obese individuals ate the nuts from which the shells had been removed beforehand. In a somewhat similar experiment, Rodin (2!) showed that moderately obese subjects drank significantly smaller amounts of thick milkshake through a straw with a small bore than through a straw with a large bore. In contrast, nonobese subjects drank about the same quantity through the “difficult” straw as they did through the “easy” straw. There are no clear answers to the second question: Can the energy density of the diet chronically influence the amount of food energy ingested and absorbed? This uncertainty exists because the problem becomes increasingly complex as it is given more careful attention. Considered at its face value, the question is deceptively simple; to begin to answer it, however, one would have to know precisely how the caloric dilution or concentration would be accomplished, the nature of
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the species to be tested, and the nutritional status of the subject under investigation. The literature contains several reports that can be used to sustain any one of a number of different points of view concerning the putative effect of changing the caloric density of the diet on spontaneous food intake. For example, in a classic study reported 30 years ago, Adolph (22) demonstrated that, when the diet of rats was diluted with kaolin or cellulose, the animals compensated perfectly by consuming enough extra food to maintain energy intake and body weight at constant levels. This effect was confirmed by Kennedy (23) in 1950. On the other hand, subsequent studies (24) showed that, when certain strains of rats are fed a high-fat diet, they promptly increase total energy intake and become obese. Unfortunately, it is not yet clear whether a diet rich in fat induces such a response because of some unique property possessed by this nutrient or simply because a high-fat diet is also a calorically concentrated diet. To complicate matters further, Kennedy (23) has demonstrated that, in rats with hypothalamic obesity, substantial caloric dilution of the diet can bring about weight loss-at least while marked obesity is still present. Here again there are problems of interpretation, and it remains unclear whether, in such experiments, caloric dilution reduces energy intake by adversely affecting the palatability of the diet, by increasing the physical effort required to ingest the food, or by some other mechanism (25). For example, the presence of obesity could render an animal especially sensitive to the satiating effects of the increased bulk conferred on a diet by the addition of an indigestible dihuent. No discussion of the possible role of dietary fiber in preventing obesity can neglect the information generated by investigators who have attempted to assess the efficacy of methylcellulose and other bulking agents as appetite suppressants. In 1959, Yudkin (26) reported that when 3.3 g of methylceh!ulose was ingested by overweight human volunteers 30 mm before meals, a reduction in food intake and some weight loss ensued. A year later, Duncan et al. (27) found methy!celhuhose to be ineffective as an appetite depressant when the preprandial dose was 1.5 g, less than one-
DIETARY
FIBER
half that used by Yudkin. Subsequently, Evans and Miller (28) studied the effect of methylcellulose and guar gum on the food intakes and body weights of 11 volunteers, of whom three were obese. Each subject received both agents in successive experimental periods lasting 1 week. Each experimental period was preceded or separated by a baseline period of 1 week. The subjects took 10 g of methylcelhulose or 9 g of guar gum with a glass of water 30 mm before luncheon and dinner. At these dosage levels, and with the data averaged on all the subjects, the bulking agents appeared to reduce food intake by about 10%, and some weight loss occurred. Of considerable interest was the observation that the obese subjects lost much more weight (1.7 ± 0.4 kg/week) than did the lean subjects (0.1 ± 0.! kg/week). Indeed, the effect of the two bulking agents on the nonobese subjects, taken as a separate group, appears to have been negligible. Obviously, it is difficult to draw any firm conclusion from such a shortterm study. These preliminary results do suggest, however, that it might be rewarding to conduct a double-blind trial of the effect of buhking agents in a larger group of obese subjects studied for a longer period of time. In our laboratory, Gehiebter (29) has studied the effect of various liquid preloads, nutritive and nonnutritive, on the intake by nonobese individuals of a nutritionally complete test meal, also liquid, offered 70 mm later. The test meal was consumed ad hibitum through a straw from a hidden container. Twelve healthy males of normal weight, with ages ranging from 21 to 36, participated. They fasted for 13 hr before each experiment. The nutritive loads had a volume of 450 ml each and consisted of 283 kcah of either egg albumin, corn starch, corn oil, or a mixture of these. The noncalorie loads consisted of a mixture of kaolin and cellulose (67.4 g in 450 ml of water) and 450 ml of water given alone. Taste and olfactory differences between the loads was minimized by mildly anesthetizing the subjects’ mouths with a topical application of xyhocaine and then by applying nose clips. Indeed, the subjects remained unaware of the nature of the loads, and none realized that one load consisted of water alone. The mean test meal intake is shown in Figure 3. For the purposes of the present
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AND
OBESITY
S47
-%
FIG. 3. Mean test meal intakes after different loads in humans. Note failure of kaolin-cellulose (K/C) load to suppress subsequent food intake as compared with a control of load of water (WAT) alone. Overall, intakes were significantly smaller after caloric loads than after noncaloric loads (29).
discussion, it is necessary only to note that, in this particular experimental setting, 67.4 g of a kaolin and cellulose mixture given as a liquid preload did not inhibit the subsequent intake of a test meal to a greater extent than did a comparable volume of water. Although the data on which they are based are often less than satisfactory, scattered reports (30) indicate that the average weights of the inhabitants of Western countries have increased substantially during the last 50 years. In the United States, three successive surveys (31-33) have provided evidence that the weight of Americans has continued to rise since mid-century, even allowing for a slight concurrent increase in height. Figure 4 contains data on the average body weights of groups of American men (ages 30 to 34 and 5’8” tall) from 1863 to 1962. Although there is no way of knowing how representative the earlier samples were of the overall population, these data (34) suggest that the average weight of American men has increased substantially since the time of the War Between the States; in the case of this particular category, the increment is about 20 pounds. Assuming that such an increase in weight has in fact occurred, can this phenomenon be attributed to a corresponding change in the fiber content of the diet? The reply to this question can only be that too little is known, at the present time, about the effect of dietary fiber on spontaneous energy intake in man to
VAN
S48
ITALLIE
70
CIVILIANS
(6O
OFFICERS
RMY
K (0
CIVIL WAR SOLDIERS
SEPARATEES ARMY
RED IANS
CIVIL
RECRUITS
.1
(863 (850
(924
(900
875
(94346
925
(962
1950
YEARS FIG.
4.
Average
body
weights
of groups
of American
permit the formulation of a persuasive hypothesis. Indeed, it is not clear whether the total amount of fiber in the diet has decreased substantially during the last century or whether it is only the type of dietary fiber that has changed. In this regard, it may be instructive to consider Trowell’s (35) recent comments about food and fiber in the British diet since 1850. What he says may be applicable to the American experience: In 1970, the average adult British diet contained 4 grams of crude fibre per day: cereals 0.5 grams, potato 1.0 grams, fruit, vegetables and nuts 2.5 grams. In 1850, the average adult British diet also contained about 4 grams of crude fiber per day, but it was derived from different sources: cereals 1.5 grams, potato 1.6 grams, fruit, vegetables and nuts probably about 1 gram. The average adult British crude fibre intake has remained therefore almost stationary during the past 110 years. On
the other
hand,
cereal
crude
fibre
decreased
about
70%
and fibre from vegetables and fruit increased in a corresponding manner. Does this matter? This is one of the fundamental questions in the dietary fibre hypothesis.
Thus far, our attention has been focused on the arguments supporting the hypothesis that food fiber serves as a significant obstacle to energy intake and that foods from whith fiber has been removed promote obesity. Let us now consider this hypothesis in the light of other concepts about the pathogenesis of obesity. In the development of such concepts, a consideration of several animal models of obesity has been helpful. Two such models seem especially relevant to human obesity. They are the genetically obese rat, first de-
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men
ages
30 to 34 and
5’8”
tall
(34).
scribed by Zucker and Zucker (36), and the dietary-obese rat described by Schafani and Springer (19). The adipose tissue of the Zucker obese rat is characterized by both hyperplasia and hypertrophy (37). Unlike normal rats, Zucker rats develop obesity on a stock diet of rat pellets (38). Normal rats can be made obese by adding “snack foods” to their regular diet of rat pellets (19). As shown in Figure 5, food items that induce the rat to overeat and become obese include such items as chocolate candy bars, marshmallows, cookies, bananas, salami, cheese, and sugared breakfast cereal. When rats with snack-food-induced obesity are returned to a diet limited to rat pellets, they spontaneously reduce their food intake and lose weight rapidly. It is not until they return to the weight of their controls that they once more consume sufficient food energy to prevent further weight loss (19). The obesity induced by the snack-food diet appears to be highly resistant to the weight-reducing effect typically seen when caged animals are permitted to exercise voluntarily in activity wheels (19). Even forced exercise is only moderately successful in reversing this form of dietary obesity (S. Gale and T. B. Van Itallie, unpublished observations). However, neither rats given free access to a snack-food diet (19) nor mice fed a fat-enriched diet (39) gain weight in a uniform fashion. That some animals in each population are able to remain relatively lean despite these dietary cha!lenges suggests that genetic factors may be
DIETARY
FIBER
AND
S49
OBESITY
/
A I
I
B FIG. 5. Normal obese on snack-food
rat remaining lean on items (B). (Photographs
diet of standard rat pellets provided by S. K. Gale.)
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
(A),
while
previously
lean
sibling
becomes
S50
VAN
involved in determining tibility to such diets. In recent years, two obesity ogy of
have their
characterized hypertrophy; pocyte
the
level
major
been distinguished adipose tissue
of suscep-
types (40).
of human
by morpholOne type
by adipocyte hyperplasia the other shows principally
hypertrophy.
The
former
ITALLIE
type
is
and adiis more
commonly found in individuals whose obesity began in infancy, childhood, or at some point prior to the cessation of linear growth; the latter type is more often identified among individuals whose obesity started during adult life. As might be expected, hyperplastichypertrophic obesity is generally more severe than hypertrophic obesity; however, the association
of
these
two
morphologic
forms
with any particular age of onset is not clearcut. For example, many patients whose obesity appears to have begun after the age of 21 exhibit adipocyte hyperplasia as well as hypertrophy. Despite these qualifications, it must be apparent that the two morphologic types of human obesity bear more than a casual resemblance to the two animal models described earlier. Indeed, there is a growing belief that there may be two predominant types of obesity in Western countries: one that is constitutionally determined and one that results from the interaction between a psychologically
or
biologically
predisposed
individual and his environment. In the former type, the chief pathogenetic impetus arises in the individual; in the latter type, the environment seems to play a much larger role. The first type may be genetically determined or may result from infant feeding practices that favor fat cell hyperplasia. The second type involves a complex constellation of etiohogic factors, including chronic physical inactivity, the persistent use of food for nonnutritive purposes, and a life style that is especially vulnerable to the manifold opportunities and incentives provided by our culture to overeat. The nature of the diet is an important component of that life style. There is every reason to believe that in many instances the second type of obesity is superimposed on the first type. Also, there must exist many intergrades between the two types, considered as pure forms. How important is food fiber in this overall
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picture? At the present time, it is impossible to say. For example, it is not yet known why the snack-food diet causes rats to become obese. Sclafani and Springer (19) believe that the inherent palatability of this diet, and particularly its novelty and variety, causes rats to overeat and in some instances to become discernibly obese. However, the precise composition of the snack-food diet, as ingested, has yet to be reported; it is certainly calorically concentrated, high in sugar content, and devoid of plant fiber. Would such a diet fail to produce obesity if food fiber were somehow incoporated into the component foods? Questions of this kind deserve further exploration. Finally, there is a growing body of evidence to suggest that animals (4!) and humans (42) with hypertrophic obesity defend their excess weight with less tenacity than animals and people with normal-sized fat cells. Individuals with enlarged adipocytes are more likely than nonobese persons to lose weight when challenged by a change in the palatability of their diet (43) or by an increased level of physical activity (44). Note has already been taken of the preliminary evidence (28) suggesting that obese persons are more responsive than lean subjects to the appetite suppressing effects of bulking agents. Thus, it would not be surprising if subjects with hypertrophic obesity were to exhibit a reduction in food intake and weight loss following a shift from a diet depleted in plant fiber to one rich in fiber. By an extension of this reasoning, it is possible to argue that a fiber-rich diet could also make a contribution to the prevention of obesity. How important such a contribution might be is a question that can only be resolved by future clinical investigation. El References I. OIANCOVA, K., AND S. HEJDA. Epidemiology of obesity. In: Obesity: Its Pathogenesis and Management, edited by J. T. Silverstone. Acton, Mass.: Publishing Sciences Group, 1975, pp. 57-91. 2. Consumption of Food in the United States 1909-52. Supplement for 1961 to Agricultural Handbook No. 62, Washington, D.C.: U.S. Department of Agriculture, 1962. 3. ANTAR, M. A., M. A. OHLSON AND R. E. HODGES. Changes in retail market food supplies in the United States in the last seventy years in relation to the
DIETARY
4. 5.
6. 7. 8. 9.
10.
11.
12.
incidence of coronary heart disease, with special reference to dietary carbohydrates and essential fatty acids. Am. J. CIin. Nutr. 14: 196, 1964. CUMMINGS, J. H. Dietary fibre. Gut 14: 69, 1973. TROWELL, H. C. Dietary changes in modern times. In: Refined Carbohydrate Foods and Disease. Some Implications of Dietary Fibre, edited by D. P. Burkitt and H. C. Trowell. London: Academic Press, 1975. ROBERTSON, J. Changes in the fibre content of the British diet. Nature 238: 290, 1972. HEATON, K. W. Food fibre as an obstacle to energy intake. Lancet 2: 1418, 1973. TROWELL, H. Obesity in the Western world. Plant Foods Man 1: 157, 1975. HILL, S. W., AND N. B. MCCUTCHEON. Eating responses of obese and non-obese humans during dinner meals. Psychosomat. Med. 37: 395, 1975. HASHIM, S. A., AND T. B. VAN ITALLIE. An automatically monitored food dispensing apparatus for the study of food intake in man. Federation Proc. 23: 82, 1964. JORDAN, H. A., W. F. WIELAND, S. P. ZEBLEY, E. STELLAR AND A. J. STUNKARD. Direct measurement of food intake in man: a method for the objective study of eating behavior in man. Psychosomat. Med. 28: 836, 1966. STUNKARD, A., AND D. KAPLAN. Eating in public places:
a review
of eating 13.
FIBER
of
behavior.
reports
of
Internat.
the
direct
J. Obesity
observation
AND
Physiol.
22. 23. 24.
D. L. Eating style of obese and non-obese Doctoral dissertation, University of Penn1977. MEYER, J. E., AND V. PUDEL. Experimental studies of food intake in obese and normal weight subjects. J. Psychosomat. Res. 16: 305, 1972. JORDAN, H. A., AND T. A. SPIEGEL. Palatability and oral factors and their role in obesity. In: The Chemical Senses and Nutrition, edited by M. Kane and 0. Mallen. New York: Academic Press, 1977. JORDAN, H. A., L. S. LEVITZ AND 0. M. KIMBRELL. Eating is Okay! A Radical Approach to Successful Weight Loss. New York: Rawson Associates. 1976, p. 53. JORDAN, H. A. Physiological control of food intake in man. In: Obesity in Perspective, edited by 0. A.
26. 27.
28. 29.
30. 31.
persons. sylvania,
14.
15.
16.
17.
Bray.
DHEW
Publication
No. (NIH)
75-708,
adult
rats:
Similarities
to
hypothalamic
and
human
obesity 20.
21.
syndromes. Physiol. Behav. 17: 461, 1976. SCHACHTER, S., AND L. N. FRIEDMAN. The effects of work and cue prominence on eating behavior. In: Obese Humans and Rats, edited by S. Schachten and J. Rodin. Potomac, Md.: Earlbaum Associates, 1974, pp. 11-14. RODIN, J. Effects of obesity and set point on taste responsiveness and ingestion in humans. J. Comp.
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
high-fat
32.
33.
35.
Statistics,
of adults
ZUCKER,
mutation 37.
57: 541,
1955.
Washington,
D.C.: PHS.
Pub-
18-74
years
of age in the United
States. Washington, D.C.: Advance Data from Vital and Health Statistics, No. 3, pp. 1-8, November 19, 1976. HATHAWAY, M. L., AND E. D. FOARD. Heights and Weights of Adults in the United States. Home Economics Research Report No. 10. Washington, D.C.: U. S. Department of Agriculture, 1960. TROWELL, H. C. Dietary fibre and colonic diseases. In: The Present State of Knowledge, No. 6. London:
Norgine 36.
J. Nutr.
lication No. 1000, Series 11, No. 14, May 1966. U. S. Department of Health, Education, and Welfare. Ten state nutrition survey 1968-1970. DHEW Pub. (HSM) 72-8 134. Atlanta, Ga.: Center for Disease Control, 1972. National Center for Health Statistics. Height and
weight
34.
diets.
A. Appetite and hunger in experimental obesity syndromes. In: Hunger: Basic Mechanisms and Clinical Implications, edited by D. Novin, W. Wyrwicka and 0. A. Bray. New York: Raven Press, 1976, pp. 28 1-295. YIJDKIN, J. The causes and cure of obesity. Lancet 2: 1135, 1959. DUNCAN, L. J. P., K. ROSE AND A. P. MEICKLEJOHN. Phenmetrazine hydrochloride and methylcellulose in the treatment of refractory obesity. Lancet 1: 1662, 1960. EVANS, E., AND D. S. MILLER. Bulking agents in the treatment of obesity. Nutr. Metabol. 18: 199, 1975. GELIEBTER, A. A. The effects of equal caloric loads of protein, fat and carbohydrate, and non-caloric loads on food intake in the rat and man. Doctoral dissertation, Columbia University, 1976 (University Microfilms, 1976, No. 76-29846, Ann Arbor, Michigan). KHOSLA, T., AND C. R. ROWE. Height and weight of British men. Lancet 1: 742, 1968. National Center for Health Statistics. Weight by Height and Age of Adults, United States, 1960-1962. SCLAFANI,
Vital Health
Wash-
ington, D.C.: U.S. Government Printing Office, 1975, pp. 35-47. 18. VAN ITALLIE, T. B., S. K. GALE AND H. R. KISSILEFF. The control of food intake in the regulation of depot fat: An overview. In: Diabetes, Obesity and Vascular Diseases: Molecular and Metabolic Interrelationships. Advances in Modern Nutrition, edited by H. M. Katzen and R. J. Mahlen. New York: John Wiley, vol. 2, 1978, part 2, pp. 427-492. 19. SCLAFANI, A., AND D. SPRINGER. Dietary obesity in
Psychol. 89: 1003, 1975. E. F. Urges to eat and drink in rats. Am. J. Physiol. 151: 110, 1947. KENNEDY, 0. C. The hypothalamic control of food intake in rats. Proc. Roy. Soc. 137: 535, 1950. MICKELSEN, 0., 5. TAKAHASHI AND C. CRAIG. Expenimental obesity I . Production of obesity in rats ADOLPH,
by feeding 25.
1: 89, 1977.
KAPLAN,
S5 1
OBESITY
JOHNSON, HIRSCH.
Ltd.,
1976, pp. 5-6.
L. M., AND T. F. ZUCK.ER. Fatty, in the rat. J. Hered. 52: 275, 1961. P. R., L. M. ZUCKER, J. A. CRUCE Cellularity
of
adipose
depots
in the
a new AND
J.
geneti-
cally obese Zucker rat. J. Lipid Res. 12: 706, 1971. 38. ZUCKER, L. M. Some effects of caloric restriction and deprivation on the obese hyperlipemic rat. J. Nutn. 91: 247, 1967. 39. DE LAEY, P. Hypothalamic and nutritional obesities in mice. A comparative study of growth and body
composition. 388, 1975. 40.
Internat.
Pharmacodynam.
216:
J., AND B. BATCHELOR. Adipose tissue celin human obesity. Clin. Endocrinol. Metab. 1976. SULLIVAN, A. C., J. TRISCARI AND K. COMAI. Caloric HIRSCH,
lularity 5: 299,
41.
Arch.
VAN
S52
compensatory
responses
nonabsorbable
carbohydrate
lean Zucker 42.
rats.
to diets
Am. J. Clin.
containing
on lipid
Nutr.
by
either obese
31: S261,
and
1978.
0. CARLGREN, B. IsAKssoN, M. B. LARSSON AND L. SJ#{246}STR#{246}M. The effect of an energy-reduced dietary regimen in relation to adipose tissue cellularity in obese women.
BJ#{246}RNTORP,
ITALLIE
P.,
KORTKIEWSKI,
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S43/4656120 by Washington University School of Medicine Library user on 09 April 2018
Am.
43.
J. Clin. Nutr. 28: 445, 1975. S. A., AND T. B. VAN
HASHIM,
normal dispensing
and
obese device.
subjects Ann.
with N.
Y.
ITALLIE.
Studies
a monitored Acad.
Sci.
in
food 131:
651,
1965. 44. BJ#{246}RN’rORP, P. Exercise in the treatment Clin. Endocrinol. Metabol. 5: 431, 1976.
of obesity.
