Fructans of Jerusalem artichokes: intestinal transport, absorption, fermentation, and influence on blood glucose, insulin, and C-peptide responses

in healthy subjects12
Jun Johannes Rumessen, Fructans Susan Bode, Ole Hamberg, and Eivind Gudmand-H#{248}yer

are naturally occurring plant oligo- ten incompletely absorbed (5, 6) and which has been promoted properties. Fructans(FAs) isolated as an alternative dietary sweetener (7, 8). Unabsorbable storage from Jerusalem artichokes (He/ianthus tuberosus) were studied and structural polysaccharides may lower BG and insulin rewith respect to intestinal handling and influence on blood glu-sponses to a test meal (9-12) and dietary fiber may increase malabsorption (I 3). We therefore also studied the effects cose (BG), insulin, and C-peptide responses in eight healthy starch subjects. The responses were compared with those for fructose on absorption and metabolic responses of the addition of FAs ingestion. The effect of FAs added to a wheat-starch meal wasto a starch meal. also studied. Standardized breath-hydrogen excretion mdicated that FAs were completely malabsorbed and, after a 20-g Subjects and methods dose, traces of FA were detected in 24-h urine collections in one subject only. Orocecal transit times were longer for FAsSubjects than for lactulose and fructose. The BG and insulin increments Eight healthy subjects (two female, six male) aged 23-33 y were very low after FA ingestion, lower than after fructose inparticipated. The subjects were of ideal body weight 10% gestion, whereas hydrogen production was much higher. Areas (median and interquartile range, 74 kg and 63-76 kg, respecunder BG curves tended to be smaller when 10 g FA was added tively) and had no history of diabetes or of gastrointestinal or to a 50-g wheat-starch meal, but there was no apparent interferpulmonary disease. They were not under any medication, and ence with starch absorption. Am J Clin Nutr l990;52:675blood screening tests were normal. The study protocol apwas 81. proved by the Copenhagen County Medical Ethics Committee. KEY WORDS Breath tests, dietary carbohydrates, dietary Fructans (fructose o/igosaccharides) fiber, fructan, fructose, hydrogen, inulin, oligosaccharidcs, The FAs used in this study were unbranched chains of fructostarch
saccharides with sweetening furanose units in /3-(2l)-glycosidic binding [(2l)-f3-D-fructo-

ABSTRACt

Downloaded from www.ajcn.org by guest on April 3, 2012

Introduction

furanose], pose ofthis

containing a single glucose moiety (2). For the study, FAs were purified from Jerusalem-artichoke

pur-

Fructose polymers containing a single glucose moiety [fruc- tubers in December by means ofa newly developed procedure tans (FAs)] are widespread in various plants, particularly those (Danisco A/S, Danish Sugar Corp, Nakskov, Denmark). of the Compositae and Graminae families Aiium [eg, sp, artiThe cleaned tubers were sliced and extracted in hot water. chokes, asparagus, cereals (wheat and rye), and Dahlia spj (1, The cxtraxt was purified by lime treatment, ion exchange, and 2). Synthetic FAs with sweetening properties and a low degree activated charcoal. The purified juice was concentrated by of polymerization (chain length of three to five sugar units) evaporation, and the final dry, white powder was produced in have been developed through the use ofisolated fructosyltransa vacuum dryer (patent application 1 592/88-K4). ferases (3, 4). We studied naturally occurring fructans of longer The chain lengths of FAs and the sugar residues were deterchain lengths, isolated and purified from the tubers of Jerusa- mined by high-pressure liquid chromatography (HPLC) equip1cm artichokes (He/ianthus tuberosus) by a newly developed ment (Waters Millipore, Inc, Copenhagen) with two columns procedure. Naturally occurring storage polysaccharides from plants, such as FAs, may share properties with resistant starch C From the Laboratory of Gastroenterology and Clinical Nutrition, and easily fermentable dietary fiber. Such polysaccharides Department of Internal Medicine F, and the Department of Clinical could have several potential nutritional advantages as a dietary Chemistry, Gentofte Hospital, University of Copenhagen. supplement and as a sweetening agent for diabetics. 2 Address reprint requests to JJ Rumessen, Department of Medical We studied the absorption, transit, and fermentation of FAs Anatomy C, Panum Institute, University ofCopenhagen, Blegdamsvej as well as their influence on blood glucose (BG), insulin, and3, DK-2200 N, Copenhagen, Denmark. C-peptide responses in healthy subjects. The properties of FAs Received August 4, 1989. were compared with their monomer fructose, which is very of- Accepted for publication October 1 1, 1989.

AmJC/in

Nuir

1990;52:675-81.

Printed

in USA.

1990

American

Society

forClinical

Nutrition

675

676 TABLE
Physical Texture Density 1 properties

RUMESSEN

El
generate

AL
a significant, air were days A/S) in challenges on different (Danisco sustained of 10 ppm given separated 50 in mL 200 tap in 200 mL rise in hydrogen concentration

ofthe

fructans

studied

in basis

end-expiratory

(14).
by 72

Furthermore,
order h, within on

the

fol-

(gJcm2)

Water

solubility

(gIL)

Sweetening power Melting point (C) Viscosity (Pa.s) Acid stabilityf

White, amorphous powder 0.75 200-300 at 30 *C; 400 at 50 C 1/3 x sucrose 130-180 0.002-0.004 (at 100-300 g/L and at 20 1 h 1%, 2 h 3%, 3 h 4%, 4 h 6%

lowing 5 g FA

in random

a single-blind

water; 2)

mL C) starch tional
lowing

tap

water; 3) 20 g FA
SAD)

tap
mL

water;
tap

1-2 mo: 1) 10 g FA in 100 4) 20 g fructose g wheat

(D-fructopyranose,

water; 5) 50

as bread Institute
carbohydrate

made from of Animal

content

gluten-containing wheat flour (NaScience, Copenhagen) with the fol(% of dry wt): FAs 1 .4%, starch

According

to the supplier. test 2.5 (citric panel acid) (Jutland at 40 C. Institute

t Assessed by an independent nology, Arhus, Denmark). :j: Percent hydrolysis at pH

84.9%, and nonstarch of Tech- 0. 1%. The breads were

baking starch powder, in bread or made yeast

polysaccharidcs baked at 220

was as above used

3.9%; C for
process.

lignin made 20 mm. No

6) 50 halfway

up salt,

in the

g wheat through

supplemented

the
in series (Biorad aminex HPX-42C, Bie & Berntsen, Copenhawithin

meal

with
15 mm.

10 g FA in 100 mL

(as 2).in All meals

were

eaten

tests were performed before and during all gen). Samples were dissolved in deionized water to 5 g/l00 mL Breath-hydrogen after a 12-h overnight fast and a chlorhexidine mouthand analyzed in 15-zL samples at 85 C and a flow rate of 0.3meals Duplicate samples were taken every 15 mm until orocemL/min. The frequencies of different chain lengths and resi-wash. cal transit times were determined and every 30 mm until 12 h dues in the product were as follows: fructose 3.8%; glucose ingestion of the test meal, as previously described (145.1%; sucrose 14.5%; and three-sugar units 10.6%, four units after concentrations were analyzed on an exhaled10.2%, five units 7.5%, six units 7.0%, seven units 6.1%, eight 16). Hydrogen monitor (Gas Measurements Ltd, Renfrew, Scotunits 5.3%, and more than eight units 29.9%. Enzymatic deter- hydrogen land) ( 14). Standardized symptom scores were completed mination (with kits from Boehringer, Mannheim, FRG)glu- of all tests and comprised the occurrence of flatucose and fructose in the product revealed that glucose was 1.8%throughout distension, borborygmia, abdominal pain, and diarrhea. and fructose, 2.4%. This discrepancy from the HPLC analysis lence, is due to a slight hydrolytic activity of the column toward the All symptoms were rated as none (0), mild (1), moderate (2), terminal glucose-fructose glycosidic bond, and the enzymatic or severe (3) by the subjects at fixed time intervals, and a total score for each ofthe tests was calculated. determinations are considered most accurate. Other physical symptom properties ofthe product arc shown in Table 1. In all studies, except study 1, concentrations of BG, serum
insulin Study design (IRI), and C-peptide (ICP) were determined before

Downloaded from www.ajcn.org by guest on April 3, 2012

All subjects were initially challenged lose [4-($-D-galactopyranosyl)-D-fructosej;

in 100 mL tap water. The lactulose

with 101 5g mL) lactu( SAD, Copenhagen)

solution (SAD) contained

meals from
ing nase

and every 1 5 mm from 0 to 90 mm 90 to 180 mm. All samples were drawn

venous method catheter. BG was analyzed

and every 30 mm from an indwelldehydroge-

by a glucose

1 10 g galactose

and

60

mg

lactose/L.

All subjects

were

able

to IRI

and

(Merck, ICP analysis

Darmstadt, were stored

FRG). at -20

Serum samples C until analysis

for by

ppm

FA

Hours
1

6 and

11

10 12 after 10 g lactu-

FIG 1. Median incremental breath-hydrogen lose (L, 0), 20 g fructose (F, 0), 5 g fructan

concentrations (FA, 10 g FA (i), #{149}),

(hourly values only) in eight subjects 20 g fructan (Li) monitored for 12 h.

INTESTINAL TABLE 2
(OCTTs) fructose, and hydrogen and different production doses offructan

HANDLING

OF

FRUCTANS
<

677

Orocecal transit times ingestion oflactulose, eight subjects

after in

Hydrogen OCTT mm 10 g lactulose 20gfructose Sgfructan lOgfructan 20g fructan

production

Total

AUCt

SPeak
ppm 36 (27-47) 21 (10-61) 29(28-32) 51 (38-64) 65 (36-78)

H2

ppm.min.102 74 (54-105) 15(12-57) 48(32-56) 109 (77-138) 177 (124-276) in parentheses.

90 (60- 120) 25(15-225) 270(235-300) 175 (155-270) 145 (85-180) interquartile ranges

significantly slower transit time than 10 g lactuloseP ( Pratts test), and 20 g FA had a significantly faster than 5 g FA (P < 0.0 1, Pratts test) (Table 2). ANOVA ITs of 10 g lactulose, 5 g FA, 10 g FA, and 20 g significant difference (P < 0.01). Multiple-comparison dures showed that there were significant differences g lactulose and 5 g FA < 0.01) and between (P 10 and 1OgFA(P<0.05). Fasting concentrations of BG, IRI, or ICP did nificantly for the different substrates (Table ). The 3
increments in BG were significantly larger for

0.01, transit time ofOCFA showed a procebetween 10 g lactulose not

20

vary

sig-

maximal
g fructose

Medians;

than for 20 g FA(P < 0.02, Pratts test). Similarly, both net areas and positive incremental areas under the BG-vs-time curves were larger for 20 g fructose than for 20 g(PFA 0.04 = and P = 0.08, respectively)(Table 3). Peak incremental IRI was also significantly larger for 20 g fructose than for 20 g FA (P
<

incremental areas under the hydrogen-concentration-vstime curves from OCTTs. :1: aximal incremental M hydrogen concentration from lowest ous values. From the four subjects with detectable fructose malabsorption.

t Total

0.05,

Pratts

test) and 20

although

AUCs

were

not

different

(Table

previ-

4).
20

Peak
g fructose

incremental

ICP
g FA

and
(Table

AUCs
4). There

were
was

the
no

same
detectable

for

difference sponses ANOVA

positive 20 g

between 10 g and 20 g FA for BG, (Tables 3 and 4). With 10 g lactulose showed that both peak incremental
incremental AUCs
<

IRI, or ICP reas a reference, BG and net or

Downloaded from www.ajcn.org by guest on April 3, 2012

radioimmunoassay

(RIA-gnost,

Behringswerke,

Marburg,

BG were significantly of
but not for 20 g FA (P
>

larger for

0.10) FRG). After ingestion of2O g FA (study 3) urine was collected (Table 3). for 24 h and the presence ofFA in urine was analyzed by cnzyMalabsorption after ingestion of 50 g wheat starch was dematic determination offructose after perchloric acid hydrolysis tected in six subjects (calculated malabsorbed amounts 2- 1 1 ofFA (Boehringer Mannheim) (17). g). For these subjects OCITs were 6-8 h (Table 5). After 50 g wheat starch with 10 g FA the total hydrogen production Data analysis (AUCs) was not significantly different from that following the starch and 10 g (P > 0. 10, Pratts FA test); For breath-hydrogen tests orocecal transit times (OCIT), sum of 50 g wheat OCTIs for 50 g wheat starch with 10 g FA were shorter compeak incremental hydrogen concentrations (speak ), H2 and pared with the value for wheat starch alone < 0.05, (P Pratts total incremental areas under the hydrogen-concentration-vstime curves (AUC) were calculated as previously described (15,test). the addition of 10 g FA to the starch meal, a trend to1 6). The malabsorbed amounts of fructose and wheat starch After lower BG values, calculated as the positive or net increwere estimated by means of total AUCs of the 10-g lactulose ward areas under the curves, was apparent (Fig 2, Table 6) standards ( 16). In a few instances hydrogen concentration did mental respectively; Pratts test). There was not reach baseline after a 12-h period and the small additional (P = 0. 13 and P = 0.04, no difference between the magnitude or the timing ofthe peak areas were determined by extrapolation. BG values (Fig 2, Table 6). There was no detectFor BG, IRI, and ICP, fasting concentrations (ic, baseline), incremental able difference between peak incremental values or net and peak incremental values, and areas under the concentrationfructose 0.05) vs-time curves were calculated. Areas were calculated both

(P

positive incremental areas above baseline and net incremental areas (total areas minus baseline times 180 mm). Nonparametric statistics [Pratts test (1 8) and Friedmans two-way analysis ofvariance (ANOVA) with multiple-comparison procedures ( 19)] were used and, consequently, all results are expressed as medians and intcrquartile ranges. values P
<

positive incremental as tion curves (Table

areas 7).

under

the

IRI

and

ICP

concentra-

TABLE
Glycemic lactulose

3 responses ofdifferent and fructose in eight doses offructan subjects compared with

0.05

were

considered

significant.

PeakBGt
mmo//L

NetAUC
mmo/. L

Positive
. mm
mmo/.

AUC
L . mm

Results

The AUCs increased in proportion to increasing doses (Fig 1, Table 2). The AUCs of 10 g FA were not significantly different from AUCs of 10 g lactulose. Hydrogen production Medians; interquartile ranges in parentheses. after 20 g fructose was much lower than after 20 g FA 0.01, (P < t Maximal incremental rise ofblood glucose from fasting values. Pratts test). Four subjects had detectable malabsorption of the t Total areas under the blood-glucose-vs-time curves minus [180 20-g-fructose dose (calculated amounts 2-5 g). The OCITs de-mm times fasting values]. creased with increasing doses of FA (Table 2); 10 g FA had a Positive incremental areas above fasting values.

lOglactulose 20 g fructose of FA l0gfructan 20 g fructan

0 (0.OtoO.l) 0.8 (0.6 to 1.0) 0.2(0.1 to0.4) 0.2 (0. 1 to 0.3)

-56(-l l2to -36) -45 (-95 to 34) -14(-52to 18) -38 (-69 to -20)

0(Oto 24 (2 to 9(Oto 2 (0 to

1) 47) 18) 6)

678

RUMESSEN
4 (IRI)

El

AL

TABLE Insulin

and

C-peptide

(ICP)

responses

to fructans

compared

with

fructose

in eight

subjects

IRI SPeak
IRIt Net AUC Positive pmol. AUC L . mm Peak pmo//L 167 ( 100-200) 100(33-133) 133 (67-200) ICPt Net pmo/.

ICP

AUC L . mm

Positive pmo/.

AUC L . mm

pmo//L
20 g fructose lOgfructan 20 g fructan

pmol.

L . mm

29 ( 19-47) 22(11-29) 19 ( 10-24)

646 (-947-1894) -108(-1349-ll33) 624 (222- 101 9)

1040 (502-1894) 330(237-703)

86 1 (4 16- 10 19)

4.3 (-5.3-9.0) 2.0(-3.6-l2.3) -0.3 (-6.6-3.0)

5.7 (2.7-10.3) 4.3(1.0-12.7) 3.3(2.0-4.0)

Medians;

t Maximal

interquartile incremental

ranges in parentheses. rise above fasting values.

Only mild flatulence and borborygmia were reported except diabetes mellitus was observed (22). The interesting dietary and for one subject who complained of moderate flatulence after clinical aspects of FA prompted the production of synthetic 10 g FA (Table 8). The difference between 20 g FA and 20 fructooligosaccharides. g Studies of Neosugar (Meiji Seika Co, fructose or between 50 g wheat starch and 50 g wheat starch Japan), a mixture ofFAs containing two to four fructose moleplus 10 g FA was not significant (P = 0.08 and P = 0. 16, respeccules, suggest that it is not hydrolyzed by digestive enzymes and tively; Pratts test). ANOVA revealed no significant differences increases fecal weight and excretion of volatile fatty acids in rats (4, 23). Studies in humans have suggested that Neosugar is between the symptom scores of all challenges. Diarrhea ab- or dominal pain was not reported. completely malabsorbed (24). It may promote bifidobacteria Urine analyses for FAs in 24-h collections after a 20-g dose in colonic microflora and does ot raise n BG or insulin upon were negative in seven subjects. A concentration ofO.2 corg/L ingestion (25). Yamashita et al (26) found that Neosugar lowresponding to a 24-h excretion of I 32 mg FA (< 1% ofthe load) ered fasting BG concentrations in non-insulin-dependent diawas found in one subject. betics(26). The FAs studied by us occur naturally in Jerusalem artichokes and they have longer chain lengths than Neosugar (50% have more than four fructose units). Discussion The standardized hydrogen production and the urine analyses following a 20-g-FA load, which showed traces ofFA in one FAs arc fructo-oligosaccharides with different degrees of poonly, suggest complete malabsorption of FA. lymerization that occur in varying proportions in different person larger hydrogen response to FA than to fructose plant species and with characteristic seasonal variations (20). The much lower glycemic responses and inThe most well-described FA is inulin, which has -35 fructose and the fact that FA induces sulin peaks than does fructose may indicate thatgastric acid units (2 1). FAs with 50 fructose units have been identified in or small intestinal hydrolysis of FA to fructose monomers is garlic (20). insignificant. This agrees well with in vitro studies of hydrolysis In 1874 inulin was found not to be degraded, hydrolyzed, of cereal FA by human gastric juice (27). The very modest or detected in urine or feces after ingestion in humans (22). A after FA intake seems well acbeneficial effect on urinary glucose excretion in patients with rise in BG seen in our study counted for by the sucrose and monosaccharide contents of the product. FA is transported more slowly in the upper intestine when TABLES compared with fructose or the disaccharide lactulose. upThe Orocecal transit times (OCTTs) and hydrogen responses after 50 g per intestinal transit of FA may be slower than the transit of wheat starch, 10 g fructan, and the combined meal in eight subjects equivalent amounts of nonabsorbable monoor disaccharides
Hydrogen OCTT mm SO g wheat starch l0gfructan 50 g wheat response

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TotaIAUC
ppm.min.102

PeakH2 TABLE
ppm Blood

6
glucose (BC) responses after a starch

meal with

and

without

addition
425(375-475)t 175 (155-270) 29(6-60) 109 (77-138) 24(11-37) 51 (38-64)

of 10 g fructan SPeak

in eight subjects BC Net AUC mmo/. L . mm Positive

mmo/.

AUC
L . mm

starch
+ lOg fructan

mmo//L
SOgwheatstarch 50 g wheat starch + lOgfructan

2.4(1.1-3.7) 2.3(1.4-3.3) ranges

121(37-177) 54(-38-142) in parentheses.

134(37-191) 90 (32-155)

300(300-325) interquartile

141(70-178)

53(48-60)

Medians;

t From

ranges in parentheses. the six subjects with detectable malabsorption.

Medians;

interquartile

INTESTINAL

HANDLING

OF

FRUCTANS glycemic effect than as a sweetening

diabetes because of

679 does fructose, which agent in controlled

its small glycemic

ABG
mmol/1 has

FAs have a smaller been recommended

non-insulin-dependent

1.

effect (7, 8, 22, 29-34). Because of the lack of FA absorption, the possible metabolic disadvantages of fructose ingestion (35) could be avoided. Larger doses of FA are necessary, however, to achieve equal sweetness compared with fructose. Malabsorption of fructose is frequent (6, 36) and it may produce abdominal symptoms in susceptible subjects (37). Chronic intake ofNeosugar may give rise to gas problems (24). Only negligible symptoms were provoked by FA in the present study, but the abdominal symptoms and metabolic consequences of chronic
ingestion of FA with longer chain lengths need further study.

FA may parallel effects of nonabsorbable starch components and certain types ofdietary fiber 13, 38, 39). ( FA does not seem to influence wheat-starch absorption, as we described previously for different types ofdietary fiber (13). Mm. FA may, however, modify the BG responses to ingested starch. BG values seemed to return to baseline earlier with a more attenuated hypoglycemic phase when FA was given. This was not attributable to differences in IRI or ICP responses and was present well before the meal reached the cecum. An effect ofFA on gastric emptying is possible and may also account for some of the shortening ofOCIT. The effect may depend on the dietary -1 formulation, and diabetics may respond differently from nondiabetics. Complete malabsorption of FA reduces the caloric FIG 2. Median incremental blood glucose values(BG) in eight subvalue of the product compared with that of well-absorbed jects after ingestion of 10 g fructan (0), 50 g wheat starch and the (#{149}), combined meal (A) monitored for 180 mm. carbohydrates such as sucrose. This may be relevant for

\N:i

Downloaded from www.ajcn.org by guest on April 3, 2012

non-insulin-dependent tabolic studies energy in may

diabetics humans be available

and suggest from

obese that

individuals. 50-60% malabsorbed of the

Metheocarbohy-

because
osmotic transit

ofthe
effect. times

larger
The ofthe

molecular
OCTTs FA studied

size ofFA
of Neosugar by us (24).

and
seem

a less prominent
shorter than

retical

drate the (40-43).

after

complete
The apparent

colonic

bacterial

fermentation
energy of

processes
Neosugar in

metabolizable

to be two-thirds of the combustion energy Malabsorbed FA is vigorously fermented by the colonic rats was estimated or less (44). flora. Compared with equivalent amounts oflactulose, the hybenefits ofFA as a therapy for diabetes (22, 26) drogen production following FA was ofsimilar magnitude even The potential confirmation. Because of its sweetening properties (although the contents ofactual fructose polymers in the product need though only one-third as sweet as sucrose), FA may be used as was not 100%. The more prolonged OCITs of FA compared additive in sweets, soft drinks, and food. For diabetics, with lactulose is in itself unlikely to influence FA-induced hy-a dietary increase palatability and compliance with insignifidrogen production (1 5). A larger colonic bacterial hydrogen FA could production after ingestion of the FA substrate compared with cant glycemic effect and possibly nutritionally advantageous The properties of FA products with even longer chain lactulose therefore cannot be excluded. Complete or nearly effects. extracted from other plant species need to be investicomplete fermentation of cereal FA and inulin was demon- lengths gated. Long-term studies of FA ingestion are needed to further strated in rat hindgut (28).

TABLE
Insulin

7 (IRI)

and

C-peptide

(ICP)

responses

after

SO g wheat

starch

and

a combined

meal

of 10 g fructan

and

50 g wheat

starch

in eight

subjects

IRI SPeak
pmo//L SOgwheat starch 50 g wheat starch + lOgfructan Medians; 193 (90-274) 201(73-263) ranges

ICP Positive
pmol.

IRI
pmo/.

Net AUC
L . min

AUC
L. mipr

SPeak
pmo//L 800(333-1

ICP
pmo/. 133)

Net AUC
L . mm . iO

Positive
pmo/.

AUC
.

L . mm

io

107 (53-164) 109(46-145) in parentheses.

107 (53-164) 110(49-146)

58.3 (23-89.3) 49 (38-81)

58.3 (23-89.3) 49 (38-81)

867(400-967)

interquartile

680
TABLE 8 Abdominal symptom scores recorded during

RUMESSEN

El

AL

the test periods

Symptoms
Substrate

Median 6
2 2.5 7.5 3.5 0 5.5 as the sum

score

Interquartile 1-9
1-11 0-11 4-14 1-9 0-5 2-9

range

None 2
2 4 0 2 5 1

Mild 6
6 3 8 6 3 7 during the

Moderate 0
0 1 0 0 0 0 12-h tests.

Severe 0
0 0 0 0 0 0

10 g lactulose
SOgfructan l0gfructan 2Ogfructan 20 g fructose 50 g wheat starch SOgwheatstarch+

lOgfructan were calculated

Total

scores

ofall

registered

symptoms

in well-defined

intervals

assess the physiological and nutritional effects jects and in patients with diabetes mellitus.

in healthy

sub-

ofbreath hydrogen (H2) analysis Evaluation ofa H2-monitor and interpretation ofthe H2 breath test. Scand J Clin Invest Lab
aspects l987;47:555-60. E. Influence of oro-

We are grateful to G Bischoff, E Borresen, B Fallesen, 0 Hansen, L Krogh, and I Staack for technical assistance. Peters and JO Rumessen for comments on the manuscript.

LM Hansen, 15. Rumessen ii, Hamberg 0, Gudmand-Heyer We thank S caecal transit time on hydrogen excretion absorption. Gut 1989;3O:8l 1-4.
16.

after carbohydrate

mal-

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References
1. Archbold HK. Fructosans in the monocotyledons.
The mechanisms offructosan

A review.

Phytol l940;39: 18-219. 2. Edelman J, Jefford TG.

Rumessen JJ, Hamberg 0, Gudmand-Hyer E. Interval sampling ofend-expiratory hydrogen (H,) concentrations to quantitate carbohydrate malabsorption by means of lactulose standards. Gut l990;3l:37-42. New 17. Beutler H-O. Inulin. In: Bergmeyer HU, ed. Methods of enzymatic

analysis. 3rd ed. Basel: VerlagChemie, Weinheim, 1984:41-5. 18. Rahe AJ. Tables ofcritical values for the Pratt matched pair signed in higher plants as exemplified He/ianihus in tuberosus. New Phyrank statistic. J Am StatAssoc l974;69:368-73. tol l968;67:5l7-3l. NJ Jr. Nonparametric statistics for the behav3. Shiomi N, Izawa M. Purification and characterization of sucrose: 19. Siegel S, Castellan ioral sciences. 2nd ed. New York: McGraw-Hill, 1988. sucrose- 1-frutosyltransferase from the roots of asparagus Aspara( 20. Darbyshire B, Henry Ri. Differences in fructan content and syngus officinalis L.). Agric Biol Chem I980;44:603-l4. thesis in some allium species. New Phytol 198 l;87:249-56. 4. Oku T, Tokunaga T, Hosoya N. Nondigestibility of a new sweet21. Bacon JSD, Edelman J. The carbohydrates ofthe Jerusalem artiener, Neosugar, in therat. J Nutr 1984; 1 14:1574-81. choke and other Compositae. Biochem J 1951;48:l 14-26. 5. Ravich Wi, Bayless TM, Thomas M. Fructose: incomplete intesti22. K#{252}lz On the pathology and therapy E. of diabetes mellitus. Marnal absorption in humans. Gastroenterology l983;84:26-9. burg: NG Elwerts Verlag, 1874 (in German). 6. Rumessen ii, Gudmand-H#{248}yer E. Absorption capacity of fructose
metabolism in healthy adults. Comparison with sucrose and its constituent monosaccharides. Gut 1986;27:1161-8. 7. Crapo PA, Koltermann 00, Olefsky JM. Effects oforal fructose normal, diabetic and impaired glucose tolerance subjects. Diabetes Care 1980;3:575-82. 23. in 24. Tokunaga T, Oku T, Hosoya N. Influence ofchronic intake of new

sweetener

testinal Stone-Dorshow poorly absorbed

fructooligosacchaiide (Neosugar) on growth and gastroinfunction ofthe rat. Nutr Sd Vitaminol J l986;32:l 1 1-2 1.
T, Levitt MD. Gaseous response to ingestion fructo-oligosaccharide sweetener. Am J Clin Nutr of a

8. Crapo PA, Koltermann 00, of two-week fructose feeding l986;9:1 11-9. 9. Jenkins DJA, Leeds AR, Gassull
Decrease in postprandial

Henry RR. Metabolic consequence in diabetic subjects. Diabetes Care 25.

l987;46:6

1-5.
of

MA, Cochet B, Alberti KGMM. insulin and glucose concentrations

by26.

Hidaka H, Eida T, Takizawa T, Tokunaga T, Tashiro Y. Effects fructooligosaccharides on intestinal flora and human health. Bifidobact Micro l986;5:37-50. Yamashita K, Kawai K, Itakura M. Effects of fructo-oligosaccha-

guarand
10.

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