Journal of the American College of Nutrition, Vol. 21, No. 5, 410-415
(2002)
Published by the American College of Nutrition
Glucose and Insulin Responses to a New Zero-Energy Fiber Source
Judith Hallfrisch, PhD, CNS, FACN,
Daniel J. Scholfield, BS and Kay M. Behall, PhD,
CNS
Diet and Human Performance Laboratory, Beltsville Human
Nutrition Research Center, Agricultural Research Service, United States
Department of Agriculture, Beltsville, Maryland
Address reprint requests to: Judith Hallfrisch, Ph.D., Building
308, Room 126, Beltsville Agricultural Research Center-East, Beltsville, MD
20705. E-mail: [email protected]
|
ABSTRACT |
Objective:
Consumption of a number of soluble fiber sources reduces glucose and
insulin responses in humans. These fibers provide some available
energy. Z-trim, a completely insoluble, noncaloric fiber/fat replacer
produced from grain, was developed by ARS scientist George Inglett
but until this report had not been tested in humans. The objective
was to test the effects of consumption of various doses of this new
fiber on glucose and insulin responses in humans.
Design: Men and women (12 each) matched for age and body mass
index (41 years, BMI 27) were given glucose or glucose with
three levels of fiber in a Latin-square design. Blood samples
were obtained before and 30, 60, 120 and 180 minutes after solutions
containing glucose alone (1 g/kg body weight) and glucose plus
0.08, 0.17 and 0.33 g/kg body weight of Z-trim were consumed.
Plasma glucose, insulin and glucagon were determined by enzyme
or radioimmunoassays. A repeated-measures analysis of variance
was conducted.
Results: Glucose responses were lower for women than for men
(p = 0.02) regardless of the test solution. At 30 minutes,
glucose levels of men were 0.7�1.1 mmol/L lower after the two
higher levels of fiber than after glucose alone. Insulin peak
responses were delayed by high amounts of Z-trim. Fasting and
response levels of glucagon were higher (p < 0.002) in
women than in men. The decline in glucagon usually seen after a
glucose load was moderated by the addition of fiber.
Conclusion: Although high levels of this new fiber may
beneficially affect glucose metabolism of middle-aged people, it is
less effective than soluble fiber.
Key words: glucose, insulin, Z-trim, fiber, glycemic index
|
INTRODUCTION |
Type 2
diabetics compose 90% of the total diabetic population and about 7%
of adult Americans [1]. Half of all
renal dialysis patients are diabetic, and diabetes is a leading cause
of blindness and amputations [2]. Health
professionals agree that control of blood glucose levels prevents or
delays the serious debilitating consequences of diabetes [3]. Numerous studies
have shown that addition of fiber-containing foods can lower glycemic
responses in healthy people and in people with type 2 diabetes [4�10].
Most professional health groups recommend that Americans increase
their consumption of dietary fiber to 20�35 g [11�13].
Unfortunately, it has proven difficult to accomplish this change
by increasing the consumption of foods naturally high in dietary
fiber. Therefore, numerous fiber compounds and extracts have
been developed that both lower fat content of the diet and increase
the amount of dietary fiber, and these products are now being
added to the food supply.
Our laboratory has tested a number of these fiber supplements with
varying success in lowering glucose and insulin responses. Some of
these effective fibers are guar, which lowered glucose responses of
diabetics [14];
high-amylose corn starch, which reduced glucose and insulin responses
in 12 men [15];
whole-wheat bread, which lowered glucose and insulin responses in
both men and women regardless of particle size of the whole-wheat
flour [16]; and Oatrim, an
oat extract high in soluble beta-glucans, which lowered glucose and
insulin responses in men and women both after chronic [17] and acute
feeding [18]
regardless of cooking method. Oatrim was developed by George Inglett
[19]
and was first tested under controlled feeding conditions by our
laboratory.
Z-trim, a new zero-energy insoluble fiber and fat replacer, was
developed by Inglett [20]. It is made
from low-cost agricultural byproducts such as hulls or brans of oats,
corn, rice, wheat, soybean and peas. These byproducts are treated in
a multistage process to disintegrate cellular structures. The
resultant purified substance is an easy-flowing powder which can be
rehydrated to a high viscosity gel with a smooth creamy mouth feel.
It can be used to replace fat or some of the glycemic materials
such as starches, sugars and syrups which now replace fat in
many low fat foods. Approximately one gram of Z-trim can replace
90 fat calories in some foods. This report constitutes the first
controlled study in humans using this new fat replacer/fiber
source. Insulin, glucose and glucagon responses to various amounts
of Z-trim added to glucose are reported.
|
METHODS |
Subjects
Twelve
men and 12 women were selected for the study after a preliminary
blood screen and urinalysis and approval by a physician after a
medical evaluation. Subjects were excluded if they had hypertension
(blood pressure >140/90 mmHg), diabetes (fasting glucose > 7.77
mmol/L) or abnormal screening blood or urine values or were taking
medications that would interfere with glucose metabolism. Subject
characteristics are listed in Table 1.
Men and women were matched for age and body mass index (BMI).
The
study was approved by the Johns Hopkins School of Public Health
Institutional Review Board and the United States Department of
Agriculture Human Study Committee. Medical supervision was provided
by Benjamin Caballero, Johns Hopkins School of Public Health,
Baltimore, MD.
Diets
Subjects discontinued vitamin or mineral
supplements for the duration of the experiment. Subjects consumed a
controlled diet for three days during each of four experimental
periods. The amount and content of the menus were identical for each
individual during the four periods. Energy requirements were
determined by using a standard formula or previously recorded
requirements for subjects who had completed other studies at the
center. Menus consisted of standard foods and were prepared in the
Beltsville Human Nutrition Research Center Human Study Facility (Table 2).
The three-day menu contained, on average, 30% of energy from
fat, 55% from carbohydrate and 15% from protein. All foods were
weighed to 0.5 g. Subjects consumed breakfast at the Human Study
Facility and picked up lunch and dinner for consumption at work or
home. Subjects were required to consume all foods presented and no
others except for noncaloric beverages. Intakes of these beverages
were recorded daily.
Glucose
Tolerance Tests
Subjects were weighed daily before consuming
breakfast. Weights were constant throughout the study. On day 3 of
each period, subjects arrived at the center after an overnight fast.
Fasting blood samples were drawn by venipuncture by a licensed
phlebotomist under the supervision of a physician from the Johns
Hopkins School of Public Health. Subjects then consumed either a
glucose solution (1 g/kg body weight) or the glucose solution to
which Z-trim 0.08, 0.17 or 0.33 g/kg body weight had been added.
Subjects consumed the solutions within 10 minutes. Blood samples
were then collected at 0.5, 1, 2 and 3 hours after beginning
consumption of the test solutions. After the last blood sample was
taken, subjects consumed breakfast at the center. Tolerance tests
were given at two week intervals. A makeup period for those
subjects (n = 3) who had missed one of the four regular tests due
to work-related travel or family emergency was given two weeks
after the fourth period. Each period subjects were asked to
record any gastrointestinal symptoms: hunger, too full, diarrhea,
constipation, flatulence, nausea.
Analyses
Blood samples were drawn into evacuated
containers containing EDTA and trasylol. Samples were immediately
mixed and then placed in ice baths. Tubes were centrifuged at 1500
x g at 4�C for 20 minutes and
plasma was divided into aliquots within two hours. Aliquots were then
frozen at -70�C until analysis after all samples were collected.
Plasma glucose was analyzed in duplicate by a double-enzyme method
(Trace-America, Allentown, PA) in an automated system (Centrifichem
System 500, Union Carbide, Trace-America, Miami, FL). Plasma insulin
and glucagon were analyzed by radioimmunoassays (#07-160102, ICN
Biomedicals, Inc., Diagnostic Division, Irvine, CA, and #KGND1,
Diagnostic Products Corporation 5700, Los Angeles, CA). Samples were
counted in a gamma counter (Auto-Gamma 5000 series, Packard
Instrument Company, Downers Grove, IL).
Statistical Analyses
The design of the study was a Latin
square. All subjects consumed glucose and each of the three levels of
Z-trim. Each blood variable was analyzed by using SAS 6.12 Mixed
Procedure [21].
Fixed variables were gender, diet and period; the random variable was
subject (gender). Best fit was selected by using Akaike�s
Information Criteria from three covariance structures: Compound
symmetry, Toeplitz and Unstructured. Insulin and glucagon values
were transformed to logarithmic values before analysis and
converted back to SI units for the purpose of presentation.
Least-squares means and SEM are presented in tables. Mean separation
was conducted by using the Tukey-Kramer adjustment for multiple
comparisons when the F value was significant. Significance level was
set at p < 0.05.
|
RESULTS |
There were
very few reports of gastrointestinal symptoms after consumption of
glucose or fiber tests. The following were reported: For men, there
was one report of hunger after the glucose tolerance; there were
seven reports of feeling too full one of the two days before
consumption of the low level of Z-trim, two for the medium level and
two for the high level, but only one man said he felt too full after
the tolerance (low Z-trim). No women reported hunger either before or
after any of the tolerance tests. One woman reported feeling too full
before the low level of Z-trim, two before the medium level and one
after the medium level of Z-trim. Two women reported feeling too full
after the high level of Z-trim. One man reported slight diarrhea
after the low level of Z-trim, and one woman reported diarrhea
after the high level. Flatulence was the most reported symptom.
For men, there was one report before the glucose tolerance test,
six before the low level, two before the medium level and three
reports of flatulence before the high level of Z-trim. Three
men reported flatulence after the low level of Z-trim. One woman
reported flatulence before the medium level, and two women reported
flatulence before the high level of Z-trim. One woman each reported
flatulence after the low and high levels of Z-trim. One man and
one woman reported nausea after the high level of Z-trim. Since most
of these symptoms were reported before the tolerances, they may be
the result of consumption of a higher amount of fiber than was usual
for the subjects.
Glucose responses of men were higher (p = 0.02) than those of
women (Fig.
1). The significant fiber*time*gender interaction (p =
0.0174) revealed a number of differences at specific times during the
tolerance tests. Fasting levels did not differ, but at 30 minutes
after the test solution was given, as Z-trim increased, the glucose
level declined and was significantly lower after the high level. At
60 minutes after consumption of the solutions, men consuming the
lowest level of Z-trim had the highest level of glucose, indicating a
delay in the absorption of glucose, whereas women�s levels tended to
be lower than men�s regardless of the level of fiber. At 120 minutes
glucose levels of both men and women tended to be higher after
consuming higher fiber than after glucose alone. There were no
differences at 180 minutes.
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Fig. 1. Glucose responses (mmol/L)
of men (___) and women (_ _ _) to glucose alone () 1
g/kg body weight, or with glucose + 0.08 (low �), 0.17 (medium ), and
0.33 g/kg body weight (high ) of Z-trim. Least-squares
means, SEM 0.37. Time: p < 0.0001, gender: p =
0.02, time*fiber p < 0.0001, time*gender*fiber: p =
0.04.
| |
Insulin
responses did not differ between the genders (Fig. 2).
Fasting values were similar. At 30 minutes after the test solutions
were consumed, there was a consistent reduction in insulin response
as the level of Z-trim increased. At 60 minutes peak insulin
levels were reached after the medium and high levels of fiber,
indicating a delay in insulin response. There were no differences
at 120 minutes after the solutions were consumed, but levels
tended to be higher after the medium and high levels of Z-trim.
At 180 minutes insulin was significantly higher after the high
Z-trim than other levels or glucose alone.
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Fig. 2. Insulin responses (pmol/L)
of men and women combined (___) to glucose alone () 1
g/kg body weight) or glucose + (low �) 0.08, (medium ) 0.17,
and (high ) 0.33 g/kg body weight of Z-trim. Least-squares means, SEM
75, n = 24, time p < 0.0001, time*fiber: p <
0.0001.
| |
Glucagon
levels of the women were higher than those of the men (p =
0.0018) (Fig. 3).
Glucagon responses after the medium and high levels of Z-trim tended
to be higher than after the glucose or low level of Z-trim.
View larger
version (16K): [in this
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Fig. 3. Glucagon responses (ng/L)
of men (___) and women (_ _ _) to glucose alone () 1
g/kg body weight) or glucose + (low �) 0.08, (medium ) 0.17,
and (high ) 0.33 g/kg body weight of Z-trim. Least-squares means, SEM
3.5. Diet: p = 0.0013, time: p = 0.0018, gender:
p = 0.0018, period*fiber: p = 0.0008, period*gender:
p < 0.0001, period*time*gender: p = 0.0017.
| |
Areas
under the curve of the glucose responses were higher in men than in
women (p = 0.013) but were not affected by level of Z-trim (Table 3). Insulin
areas under the curve did not differ significantly though values for
women were approximately 30% lower than values for men.
View this
table: [in this
window] [in a new window] |
Table 3. Areas under Curve of
Glucose and Insulin Responses of Men and Women after Consuming
Glucose (1 g/kg body weight) and Glucose + 0.08, 0.17 and 0.33 g
Z-Trim/kg1
| |
|
DISCUSSION |
International tables of
glycemic indexes report a wide range of responses to foods containing
complex carbohydrates and fibers [22]. Foods
containing high amounts of soluble fibers have generally been more
effective in controlling glucose and insulin responses than have
those with high amounts of insoluble fiber (e.g., oats and
high-pectin foods compared with whole-wheat foods). Z-trim, a fat
substitute made from seed hulls, was developed by George Inglett [20], the developer
of Oatrim [19].
It is a purified insoluble fiber made of microscopic fragments
of plant cell wall via a multistage process that completely
disintegrates morphological cellular structures. It absorbs water,
which results in a high viscosity and smooth mouth feel, even though
it is a completely insoluble fiber. This report is the first
study in which physiological measurements in response to Z-trim
have been determined in humans. Our goal was to determine the
lowest amount that could be given at one time to effect changes
in glucose and insulin responses. Most of the gastrointestinal
symptoms reported were reported before the tolerance tests.
These may be the consequence of consumption of a step one diet
which contained recommended levels of fat and fiber and may be
bulkier than diets subjects normally consume. The highest level of
Z-trim did provide approximately the daily amount of fiber
recommended for consumption [11�13]. If this
amount was consumed per day as a fat replacer on a 1/1
replacement by a 75-kg person, it would result in a substantial
reduction in energy (25 g x 9
kcal/g = 225 kcal).
Previous similar experiments in our laboratory showed greater
reductions in glucose and insulin responses to an oral carbohydrate
challenge than were found in the present study [14�18].
Oatrim, which contains a high concentration of soluble beta-glucans,
reduced glucose response to an acute dose comparable with the
high amount of Z-trim in the present study whether it was consumed
in an instant, baked or boiled pudding and chronically after
five weeks [17,18]. Insulin
responses were also reduced after acute or chronic consumption of
Oatrim. In a comparison of glucose, white bread and bread made with
standard or ultra-fine ground whole-wheat flour, consumption of both
whole-grain breads resulted in lower glucose and insulin responses
than did consumption of glucose or white bread [16]. Although whole
wheat contains predominantly insoluble fiber, other components of the
flour, such as resistant starch, may have moderated the glucose
responses. In the present study all subjects were given the same
amount of glucose solution each time with various amounts of
Z-trim. Consumption of four refined fibers (cellulose,
carboxymethyl cellulose, karaya gum and locust bean gum) for four
weeks each did not result in significant changes in glucose or
insulin responses in 12 healthy men [7]. Consumption of
an acute meal of high-amylose starch, though, did reduce insulin
response, but not glucose response, as compared with a
high-amylopectin starch meal.
Glucagon levels normally decline in response to a rise in insulin;
however, in our subjects glucagon levels are fairly consistent
throughout the tolerance tests. The higher levels in women and
the lack of decline in response to the glucose-containing solutions
may indicate a relative insensitivity such as is seen in obesity
and in type 2 diabetes [23]. Numerous
researchers have found excessive glucagon secretion and lack of
suppression of glucagon after a glucose challenge in subjects who are
obese [24],
have impaired glucose tolerance [25] or are type 2
diabetics [26].
Previous studies reported declines in glucagon responses after
soluble fibers, including Oatrim [17] and guar [23], but with
the high amount of fiber, glucagon response was somewhat higher
than after the glucose solution. While the women in our study
had higher glucagon levels, their glucose response levels were
lower and insulin levels were not different from those of the
men, nor were they any more obese or older than the men. All
values are within normal ranges, and these small dietary differences
in response may not be of physiological significance.
Obesity is an international epidemic [27] and is
particularly prevalent in the United States. International
comparisons of intake demonstrate that carbohydrate consumption (in
g/day) in the United States is among the lowest in the world [28]. The
most important use of this new zero-energy fiber may be in its use as
a fiber supplement and fat replacer, thus increasing carbohydrate and
fiber intake and reducing both total energy and fat intake. These
dietary changes would promote weight loss and reduction in coronary
and diabetic risk factors.
|
CONCLUSION |
In
summary, higher levels of this insoluble fiber extract (Z-trim)
elicited small but significant declines in glucose and insulin
responses. Peak responses were delayed and moderated to result
in a slower decline. The highest amount (0.33 g/kg body weight)
was tolerated well by subjects with minimal adverse effects.
This initial dose-response test opens the way for research to
determine effects of chronic consumption on these responses and
on risk factors for cardiovascular disease and diabetes
mellitus.
|
ACKNOWLEDGMENTS |
The
authors wish to thank all the volunteer subjects; Willa Mae Clark,
Demetria Fletcher, and Razia Hussain for technical assistance in
conducting the study and analysis of samples; gentle and unfailingly
accurate phlebotomist Elisa Armero; and Human Study Facility Director
Evelyn Lashley and research cooks Sue Burns, Linda Lynch and Joe
Hall, whose excellent meal preparation, cheerful interaction with
subjects and delivery of the test menus made these studies
possible.
|
FOOTNOTES |
Z-trim was provided by George Inglett, Lead Scientist,
NCAUR, ARS, USDA, 1815 North University Street, Peoria, Illinois
61604.
Received December 21, 2001. Accepted May 24, 2002.
|
REFERENCES |
- National Center for Health Statistics: Births, marriages, divorces
and deaths for 1986.Vital Stat Rep32(Suppl 2) :1 �20,1989 .
- Brownlee M: Nonenzymatic glycosylation of macromolecules and the
pathogenesis of diabetic complications.Ann Intern Med101 :527 �537,1984 .[Medline]
- Bloomgarten ZT: New and traditional treatment of glycemia in
NIDDM.Diabetes Care19 :295 �299,1996 .[Medline]
- Leclere CJ, Champ M, Boillot J, Guille G, Lecannu G, Molis C,
Bornet F, Krempf M, Delort-Laval J, Galmiche JP: Role of viscous guar gums in
lowering the glycemic response after a solid meal.Am J Clin Nutr59 :914
�921,1994 .[Abstract]
- Osilesi O, Trout DL, Glover EE, Harper SM, Koh ET, Behall KM,
O�Dorisio TM, Tartt J: Use of xanthan gum in dietary management of diabetes
mellitus.Am J Clin Nutr42 :597 �603,1985 .[Abstract]
- Behall KM, Scholfield DJ, Canary J: Effect of starch structure on
glucose and insulin responses in adults.Am J Clin Nutr47 :428 �432,1988 .[Abstract]
- Behall KM, Scholfield DJ, Lee KH, Moser PB: Blood glucose and
hormone levels in adult males fed four refined fibers.Nutr Rep Int30 :537
�543,1984 .
- Behall KM, Howe JC: Effect of long-term consumption of amylose vs
amylopectin starch on metabolic variables in human subjects.Am J Clin Nutr61
:334 �340,1995 .[Abstract]
- Wolever TMS, Katzman-Relle L, Jenkins AL, Vuksan V, Josse RG,
Jenkins DJA: Glycemic index of 102 complex carbohydrate foods in patients with
diabetes.Nutr Res14 :651 �669,1994 .
- Pastors JG, Blaisdell PW, Balm TK, Asplin CM, Pohl SL: Psyllium
fiber reduces rise in postprandial glucose and insulin concentrations in
patients with non-insulin-dependent diabetes.Am J Clin Nutr53 :1431 �1435,1991
.[Abstract]
- USDA, USDHHS:"Nutrition and Your Health. Year 2000 Dietary
Guidelines for Americans," 5th ed. Washington, DC: US Government Printing
Office,2000 .
- Gorman MA, Bowman C, American Dietetic Association: Position of
the American Dietetic Association. Health implications of dietary fiber.J Am
Diet Assoc93 :1446 �1447,1993 .[Medline]
- US Department of Health and Human Services:"Healthy People 2010:
National Health Promotion and Disease Prevention Objectives." Washington, DC:
US Public Health Service,2000 .
- McIvor ME, Cummings CC, van Duyn MA, Leo TA, Margolis S, Behall
KM, Michnowski JE, Mendeloff AI: Long-term effects of guar gum on blood
lipids.Atherosclerosis60 :7 �13,1986 .[Medline]
- Behall KM, Scholfield DJ, Yuhaniak I, Canary J: Diets containing
high amylose vs amylopectin starch: effects on metabolic variables in human
subjects.Am J Clin Nutr49 :337 �344,1989 .[Abstract]
- Behall KM, Scholfield DJ, Hallfrisch J: The effect of particle
size of whole-grain flour on plasma glucose, insulin, glucagon and
thyroid-stimulating hormone in humans.J Am Coll Nutr18 :591 �597,1999 .[Abstract/Full
Text]
- Hallfrisch J, Scholfield D, Behall KM: Diets containing Oatrim
improve glucose and insulin responses of moderately hypercholesterolemic men
and women.Am J Clin Nutr61 :379 �384,1995
.[Abstract]
- van der Sluijs AMC, Behall KM, Scholfield DJ, Hallfrisch J: The
effect of cooking Oatrim containing beneficial soluble beta-glucans on
glucose, insulin, and glucagon in human subjects.Cereal Foods World40 :662
�663,1995 .
- Inglett GE: Method for making a soluble dietary fiber composition
from oats. US Patent number 4,996,063, February,1991 .
- Inglett GE: New grain products and their beneficial
components.Nutr Today36 :66 �68,2001 .
- SAS Institute, Inc: SAS Version 6.12, Cary, NC,1995 .
- Foster-Powell K, Miller JB: International tables of glycemic
index.Am J Clin Nutr62 :871S �893S, 1995.
- Gee JM, Lee-Finglas W, Wortley GW, Johnson IT: Fermentable
carbohydrates elevate plasma enteroglucagon but high viscosity is also
necessary to stimulate small bowel mucosal cell proliferation in rats.J
Nutr126 :373 �379,1996 .[Medline]
- Iannello S, Campione R, Belfiore F: Response of insulin,
glucagon, lactate, and nonesterified fatty acids to glucose in visceral
obesity with and without NIDDM: relationship to hypertension.Mol Genet Metab63
:214 �223,1998 .[Medline]
- Borghi VC, Wajchenberg BL, Cesar FP: Plasma glucagon
suppressibility after oral glucose in obese subjects with normal and impaired
glucose tolerance.Metabolism33 :1068 �1074,1984 .[Medline]
- Reaven GM, Chen YD, Golay A, Swislocki AL, Jaspan JB:
Documentation of hyperglucagonemia throughout the day in nonobese and obese
patients with noninsulin-dependent diabetes mellitus.J Clin Endocrinol Metab64
:106 �110,1987 .[Abstract]
- Popkin BM, Doak CM: The obesity epidemic is a worldwide
phenomenon.Nutr Rev56 :106 �114,1998 .[Medline]
- Stephen AM, Sieber GM, Gerster YA, Morgan DR: Intake of
carbohydrate and its components�international comparisons, trends over time,
and effects of changing to low-fat diets.Am J Clin Nutr62 :851S �867S,1995 .[Abstract]