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

in healthy subjects1’2
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’

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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.

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in USA.

© 1990

American

Society

forClinical

Nutrition

675

1%. ‘C for process. Scotunits 5. (hourly values only) in eight subjects 20 g fructan (Li) monitored for 12 h. except study 1. Institute t Assessed by an independent nology. In all studies. tap 1-2 mo: 1) 10 g FA in 100 4) 20 g fructose g wheat (D-fructopyranose. eight 16).of all tests and comprised the occurrence of flatucose and fructose in the product revealed that glucose was 1. Standardized symptom scores were completed mination (with kits from Boehringer.9%.ajcn. glucose ingestion of the test meal. in bread or made yeast polysaccharidcs baked at 220 was as above used 3. 2) mL C) starch tional lowing tap water.in All meals were eaten tests were performed before and during all gen). sucrose 14. test 2. The lactulose with 101 5g mL) lactu( SAD.5%. 0). All samples were drawn venous method catheter. five units 7. and fructose.3meals Duplicate samples were taken every 15 mm until orocemL/min. 10 g FA in 100 mL (as 2). as previously described (145. 2. Median incremental breath-hydrogen lose (L. at -20 Serum samples ‘C until analysis for by ppm FA 1 Hours 1 2 3 4 5 6 and 7 8 9 11 10 12 after 10 g lactu- FIG 1. Renfrew. This discrepancy from the HPLC analysis lence. and C-peptide (ICP) were determined before Downloaded from www. Arhus.75 200-300 at 30 *C.4%. lignin made 20 mm.8%. order h. and a total score for each ofthe tests was calculated. abdominal pain. in the g wheat through supplemented the in series (Biorad aminex HPX-42C. 2 h 3%. Other physical symptom properties ofthe product arc shown in Table 1. Copenhagen) solution (SAD) contained meals from ing nase and every 1 5 mm from 0 to 90 mm 90 to 180 mm. mild (1).5 (citric panel acid) (Jutland at 40 ‘C. The frequencies of different chain lengths and resi-wash.0. 5 g fructan concentrations (FA. and three-sugar units 10. 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).002-0. ICP analysis Darmstadt. 3 h 4%. 2012 All subjects were initially challenged lose [4-($-D-galactopyranosyl)-D-fructosej. six units 7. moderate (2). borborygmia. amorphous powder 0. and diarrhea. FRG)glu.8%throughout distension. . Copenhawithin meal with 15 mm.hydrogen land) ( 14). BG was analyzed and every 30 mm from an indwelldehydroge- by a glucose 1 10 g galactose and 60 mg lactose/L. in 100 mL tap water. 400 at 50 C 1/3 x sucrose 130-180 0.676 TABLE Physical Texture Density 1 properties RUMESSEN El generate AL a significant. 10 g FA (i).3%. starch According to the supplier. serum insulin Study design (IRI).1%. #{149}).0%. water.s) Acid stabilityf ‘ White. 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. terminal glucose-fructose glycosidic bond. 4 h 6% lowing 5 g FA in random a single-blind water. seven units 6. concentrations of BG. Enzymatic deter.4%. 0).2%. Hydrogen monitor (Gas Measurements Ltd. four units after concentrations were analyzed on an exhaled10. 20 g fructose (F. All subjects were able to IRI and (Merck. were stored FRG). is due to a slight hydrolytic activity of the column toward the All symptoms were rated as none (0). The breads were baking starch powder. No 6) 50 halfway up salt. by 72 Furthermore. and more than eight units 29. and nonstarch of Tech. Mannheim. :j: Percent hydrolysis at pH 84. Copenhagen) with the fol(% of dry wt): FAs 1 .004 (at 100-300 g/L and at 20 1 h 1%. within on the fol- (gJcm2) Water solubility (gIL) Sweetening power Melting point (C) Viscosity (Pa.5%. Bie & Berntsen. cal transit times were determined and every 30 mm until 12 h dues in the product were as follows: fructose 3.org by guest on April 3. 5) 50 as bread Institute carbohydrate made from of Animal content gluten-containing wheat flour (NaScience. 3) 20 g FA SAD) tap mL water. determinations are considered most accurate.6%. 1%. Denmark).9%. and the enzymatic or severe (3) by the subjects at fixed time intervals.9%.

There was no detectFor BG. There was not reach baseline after a 12-h period and the small additional (P = 0. For breath-hydrogen tests orocecal transit times (OCIT).8 (0.0) 0. mm mmo/. a trend to1 6). (P < t Maximal incremental rise ofblood glucose from fasting values. or ICP reas a reference. PeakBGt mmo//L NetAUC mmo/. Pratt’s test). lOglactulose 20 g fructose of FA l0gfructan 20 g fructan 0 (0. Multiple-comparison dures showed that there were significant differences g lactulose and 5 g FA < 0. mm Results The AUCs increased in proportion to increasing doses (Fig 1.6 to 1. and hydrogen and different production doses offructan HANDLING OF FRUCTANS < 677 Orocecal transit times ingestion oflactulose.0 1. respectively)(Table 3).05.2(0. Pratt’s test). BG were significantly of but not for 20 g FA (P > larger for 0.4) 0. L Positive . g). The OCITs de-mm times fasting values].2 (0. Fasting concentrations of BG. transit time ofOCFA showed a procebetween 10 g lactulose not 20 vary sig- maximal g fructose Medians. After ingestion of2O g FA (study 3) urine was collected (Table 3). all results are expressed as medians and intcrquartile ranges. The malabsorbed amounts of fructose and wheat starch After lower BG values. 2012 radioimmunoassay (RIA-gnost.1 1 ofFA (Boehringer Mannheim) (17). :1: aximal incremental M hydrogen concentration from lowest ous values. The 3 increments in BG were significantly larger for 0. BG values (Fig 2.01) and between (P 10 and 1OgFA(P<0.min. and areas under the concentrationfructose 0.01. Hydrogen production ‘ Medians. Table 2). 10 g FA.05). IRI. and ICP. Pratt’s test) (Table 2). 1 to 0.INTESTINAL TABLE 2 (OCTTs) fructose. Table 6).02. no difference between the magnitude or the timing ofthe peak areas were determined by extrapolation. Pratt’s FA test). With 10 g lactulose showed that both peak incremental incremental AUCs < IRI. H2 and pared with the value for wheat starch alone < 0. Areas were calculated both (P positive incremental areas above baseline and net incremental areas (total areas minus baseline times 180 mm). 10. IRI. 10 g FA had a § Positive incremental areas above fasting values.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) .test). Table 6) standards ( 16).04 = and P = 0. 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. Pratt’s test) and 20 although AUCs were not different (Table previ- 4). (P Pratt’s total incremental areas under the hydrogen-concentration-vstime curves (AUC) were calculated as previously described (15. ANOVA ITs of 10 g lactulose. 20 Peak g fructose incremental ICP g FA and (Table AUCs 4). Marburg. 5 g FA. In a few instances hydrogen concentration did mental respectively.05. t Total 0. Nonparametric statistics [Pratt’s test (1 8) and Friedman’s two-way analysis ofvariance (ANOVA) with multiple-comparison procedures ( 19)] were used and. (Tables 3 and 4).org by guest on April 3. under the IRI and ICP concentra- TABLE Glycemic lactulose 3 responses ofdifferent and fructose in eight doses offructan subjects’ compared with 0. incremental able difference between peak incremental values or net and peak incremental values. baseline).05) vs-time curves were calculated. 90 (60. For these subjects OCITs were 6-8 h (Table 5). The AUCs of 10 g FA were not significantly different from AUCs of 10 g lactulose. AUC L . There were was the no same detectable for difference sponses ANOVA positive 20 g between 10 g and 20 g FA for BG.l) 0.04. 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 2.10) FRG). fasting concentrations (ic. 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. 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). interquartile ranges in parentheses. § From the four subjects with detectable fructose malabsorption. both net areas and positive incremental areas under the BG-vs-time curves were larger for 20 g fructose than for 20 g(PFA 0.102 74 (54-105) 15(12-57) 48(32-56) 109 (77-138) 177 (124-276) in parentheses. than for 20 g FA(P < 0.01).1 to0. BG and net or Downloaded from www. creased with increasing doses of FA (Table 2). sum of 50 g wheat OCTIs for 50 g wheat starch with 10 g FA were shorter compeak incremental hydrogen concentrations (speak ). or ICP did nificantly for the different substrates (Table ). and 20 g significant difference (P < 0. Similarly. 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. was apparent (Fig 2. 13 and P = 0. calculated as the positive or net increwere estimated by means of total AUCs of the 10-g lactulose ward areas under the curves.08. and 20 g FA had a significantly faster than 5 g FA (P < 0. after 20 g fructose was much lower than after 20 g FA 0. Pratt’s test).05 were considered significant.120) 25(15-225) 270(235-300) 175 (155-270) 145 (85-180) interquartile ranges significantly slower transit time than 10 g lactuloseP ( Pratt’s test). Behringswerke. consequently.OtoO. the addition of 10 g FA to the starch meal.ajcn.01. values P < positive incremental as tion curves (Table areas 7).

completely malabsorbed (24). 16.or dominal pain was not reported. which has ‘-35 fructose and the fact that FA induces sulin peaks than does fructose may indicate thatgastric acid units (2 1).min. mm starch + lOg fructan ‘ mmo//L SOgwheatstarch 50 g wheat starch + lOgfructan ‘ 2.08 and P = 0. of cereal FA by human gastric juice (27). Diarrhea ab. 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). suggest complete malabsorption of FA. A concentration ofO. insignificant. mm pmo//L 20 g fructose lOgfructan 20 g fructan ‘ pmol. betics(26). hydrolyzed.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/. interquartile . AUC L’ .7 (2. mm Positive mmo/. t From ranges in parentheses. 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. 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. 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.0-4.4-3.0(-3. The very modest or detected in urine or feces after ingestion in humans (22). FA is transported more slowly in the upper intestine when TABLES compared with fructose or the disaccharide lactulose.3) ranges 121(37-177) 54(-38-142) in parentheses. 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.3 (-6.0-12. This agrees well with in vitro studies of hydrolysis In 1874 inulin was found not to be degraded.10 19) 4. ANOVA revealed no significant differences increases fecal weight and excretion of volatile fatty acids in rats (4.0) 2.3 (-5. 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 Downloaded from www.1-3.4(1. 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).6-3. L . The difference between 20 g FA and 20 fructooligosaccharides. FAs with 50 fructose units have been identified in or small intestinal hydrolysis of FA to fructose monomers is garlic (20). Medians. 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). AUC L’ .3) -0.3(1. Only mild flatulence and borborygmia were reported except diabetes mellitus was observed (22).0) Medians. suggest that it is not hydrolyzed by digestive enzymes and tively.6-l2.ajcn. L’ . mm 29 ( 19-47) 22(11-29) 19 ( 10-24) 646 (-947-1894) -108(-1349-ll33) 624 (222. respeccules. rise above fasting values.3) 4. Discussion The standardized hydrogen production and the urine analyses following a 20-g-FA load.0) 5. g Studies of Neosugar (Meiji Seika Co.3(2.7-10.7) 2. ICP AUC L’ . 2012 TotaIAUC ppm. mm Peak pmo//L 167 ( 100-200) 100(33-133) 133 (67-200) ICPt Net pmo/. Studies in humans have suggested that Neosugar is between the symptom scores of all challenges. Pratt’s test).2 corg/L ingestion (25). The much lower glycemic responses and inThe most well-described FA is inulin. 10 g fructan. 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 = 0.101 9) 1040 (502-1894) 330(237-703) 86 1 (4 16. 134(37-191) 90 (32-155) 300(300-325) interquartile 141(70-178) 53(48-60) Medians.3(1. which showed traces ofFA in one FAs arc fructo-oligosaccharides with different degrees of poonly. t Maximal interquartile incremental ranges in parentheses.3-9. AUC L ‘ .7) 3. the six subjects with detectable malabsorption. mm Positive pmo/.org by guest on April 3. 23).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.

The effect may depend on the dietary -1 formulation. Chronic intake ofNeosugar may give rise to gas problems (24). 22.ajcn. mm . BG values seemed to return to baseline earlier with a more attenuated hypoglycemic phase when FA was given. 26) drogen production following FA was ofsimilar magnitude even The potential confirmation. but the abdominal symptoms and metabolic consequences of chronic ingestion of FA with longer chain lengths need further study. 36) and it may produce abdominal symptoms in susceptible subjects (37). 39).lengths gated. 2012 non-insulin-dependent tabolic studies energy in may diabetics humans be available and suggest from obese that individuals.3 (23-89. soft drinks. Mm. 8. which agent in controlled its small glycemic ABG mmol/1 has FAs have a smaller been recommended non-insulin-dependent 1. and food. FA may. min’ AUC L’. however. Compared with equivalent amounts oflactulose. 50 g wheat starch and the (#{149}). 50-60% malabsorbed of the Metheocarbohy- because osmotic transit ofthe effect. flora. the possible metabolic disadvantages of fructose ingestion (35) could be avoided.3 (23-89. carbohydrates such as sucrose. as we described previously for different types ofdietary fiber (13). 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).3) 49 (38-81) 58. FA may be used as was not 100%. This was not attributable to differences in IRI or ICP responses and was present well before the meal reached the cecum. 193 (90-274) 201(73-263) ranges ICP Positive pmol. Complete malabsorption of FA reduces the caloric FIG 2. IRI pmo/. combined meal (A) monitored for 180 mm. The more prolonged OCITs of FA compared additive in sweets. to achieve equal sweetness compared with fructose. 29-34). iO Positive pmo/. An effect ofFA on gastric emptying is possible and may also account for some of the shortening ofOCIT. mm io 107 (53-164) 109(46-145) in parentheses. Only negligible symptoms were provoked by FA in the present study. Larger doses of FA are necessary. extracted from other plant species need to be investicomplete fermentation of cereal FA and inulin was demon. the hybenefits ofFA as a therapy for diabetes (22. effect (7. Because of its sweetening properties (although the contents ofactual fructose polymers in the product need though only one-third as sweet as sucrose).org by guest on April 3. Because of the lack of FA absorption. times larger The ofthe molecular OCTTs FA studied size ofFA of Neosugar by us (24). and diabetics may respond differently from nondiabetics. mipr’ SPeak pmo//L 800(333-1 ICP pmo/. 38. This may be relevant for \N:i Downloaded from www.INTESTINAL HANDLING OF FRUCTANS glycemic effect than as a sweetening diabetes because of 679 does fructose. L’ . Long-term studies of FA ingestion are needed to further strated in rat hindgut (28). ( FA does not seem to influence wheat-starch absorption. 107 (53-164) 110(49-146) 58. Malabsorption of fructose is frequent (6. FA may parallel effects of nonabsorbable starch components and certain types ofdietary fiber 13. 133) Net AUC L’ . 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. modify the BG responses to ingested starch. with lactulose is in itself unlikely to influence FA-induced hy-a dietary increase palatability and compliance with insignifidrogen production (1 5).3) 49 (38-81) 867(400-967) ‘ interquartile . however. 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). Complete or nearly effects. For diabetics. and seem a less prominent shorter than retical drate the (40-43). Net AUC L’ . 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. AUC .

Jefford TG. Rumessen ii. Fructose: incomplete intesti22. Oku T. 50:324-8.44:603-l4. Koltermann 00.84:26-9. J Nutr and 1988. LM Hansen. Bifidobact Micro l986. Influence of oro- We are grateful to G Bischoff. Thomas M. Izawa M. Scarlett JA.8:279-83. Rumessen ii. 1 18:1482-6.). Shiomi N. Ravich Wi. Bj#{246}rck Availability I. 12. Bayless TM. 30. Phytol l940. J Am StatAssoc l974.9:1 11-9. sucrose. rides on blood glucose Res 1984. 15. of cereal fructans and of pan- the rat intestinal Akg#{252}n Ertel S.39: 18-219. E Borresen. sorbitol. Darbyshire B. Fructosans in the monocotyledons. Hidaka H. Takizawa T. Gudmand-Heyer We thank S caecal transit time on hydrogen excretion absorption. Diabetes 1980. Crapo PA. Edelman J.5:37-50. Agric Biol Chem I980. and pea fibre. Scand J Gastroenterol l989. meals in normal and diabetic subjects. NH. 1988. Rumessen ii. Gudmand-H#{248}yer E. Nilsson U. Nutr Sd Vitaminol J l986. New York: McGraw-Hill. The effects ofsucrose.l:l392-4. Effects fructooligosaccharides on intestinal flora and human health. Comparisons with sugar-beet fiber and wheat bran. Nilsson U. and serum lipids in diabetic subjects. Marnal absorption in humans. ed. 2nd ed. 4.24: 103-9. insulin and glucose concentrations by26. Differences in fructan content and syngus officinalis L. Gut l990. Itakura M. Henry Ri. J#{228}gerstadM. diabetic and impaired glucose tolerance subjects. 36:256-61. Rumessen ii. Crapo PA. Gudmand-H#{248}yer E.46:6 1-5. In: Bergmeyer HU. Am J Clin Nutr of a 8. Am J Clin Nutr 1989. K#{252}lz On the pathology and therapy E. Nondigestibility of a new sweet21. “Neosugar. tract. 2. thesis in some allium species. Akg#{252}n Ertel NH. Olefsky JM. Care fructose 3:582-5. Cereal vitro and in vivo studies on availability rats and humans. Castellan ioral sciences.1-frutosyltransferase from the roots of asparagus Aspara( 20. after carbohydrate mal- Downloaded from www. 1874 (in German). Hagander B. Eida T.) concentrations to quantitate carbohydrate malabsorption by means of lactulose standards. Leeds AR. 1 14:1574-81. of diabetes mellitus. sugar-beet fibre.69:368-73. Absorption capacity of fructose metabolism in healthy adults. 1988. Inhibition starch absorption by dietary fibre. 23. 28. fructose and high-fructose corn syrup meals on plasma glucose and insulin in noninsulindependent diabetic subjects. J Nutr 1984. Peters and JO Rumessen for comments on the manuscript.4:96l-6.67:5l7-3l. 0 Hansen. Tokunaga T. Oku T. New Phytol 198 l. fibre Br Med 27. TMS. Rahe AJ.48:l 14-26. of carbohydrate metabolism creatic and gastrointestinal hormones. of MA.5 0 5. Alberti KGMM. Diabetes Care 25. Comparison with sucrose and its constituent monosaccharides. A comparative study of wheat bran. in J Nutr inulin in 1 1. 9. pectin. 29. Weinheim. Gut 1986. Hosoya N. Lundquist beet fibre meal in nonto plasma levels I. Interval sampling ofend-expiratory hydrogen (H.3l:37-42. tol l968. Beutler H-O. 3:91-6. Diabetes Care l985.5 7. 16. Comparison ofthe metsbolic responses to fructose and sucrose sweetened foods. Leeds AR. in 24. Hamberg 0. fructans: Nutr in ofviscosity. Gut 1989. Reduced blood glucose response to pea fiber. Metabolic consequence in diabetic subjects. 2012 References 1. Diabetes Res 1986. 31. l987.3O:8l 1-4. Scand J Clin Invest Lab aspects l987. Tokunaga T. Oste R. 1984:41-5. Wolever analogues. Koltermann 00. New 17. burg: NG Elwerts Verlag. NJ Jr. Am J Clin of Nutr 1982. and glucose J l978. Nonparametric statistics for the behav3. B Fallesen. . Effects oforal fructose normal. Purification and characterization of sucrose: 19. Hosoya N. Kokholm G. The mechanisms offructosan A review. E. L Krogh. Tashiro Y. Scherst#{233}n .5 3. Reduced B glycemic responsesto insulin-dependent diabetics and its relation Efendi#{233} Nilsson-Ehle S. Biochem J 1951. New Phyrank statistic. and I Staack for technical assistance. Cochet B. Influence ofchronic intake of new sweetener testinal Stone-Dorshow poorly absorbed fructooligosacchaiide (Neosugar) on growth and gastroinfunction ofthe rat. 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- B ofbreath hydrogen (H2) analysis Evaluation ofa H2-monitor and interpretation ofthe H2 breath test.87:249-56. Rumessen JJ. Effects of fructo-oligosaccha- guarand 10.47:555-60. Bacon JSD. P. Hamberg 0.32:l 1 1-2 1. The carbohydrates ofthe Jerusalem artiener.” in therat. Koltermann 00. of two-week fructose feeding l986. Inulin. Gudmand-Hyer E. T. Levitt MD. Dietary importance fibres. 18. Jenkins DJA. Birkhed D.3:575-82. 6. Tokunaga T. et al.org by guest on April 3. 7. Methodological A comparison after sucrose. Hamberg 0. choke and other Compositae. Crapo PA. 5. Kawai K. 3rd ed. Yamashita K. Hamberg 0. 13. Gudmand-Hyer E. Edelman J. Siegel S. Gudmand-H#{248}yer E.86:20-3.680 TABLE 8 Abdominal symptom scores recorded during RUMESSEN El AL the test periods’ Symptoms Substrate Median 6 2 2. 118:132S-30. Methods of enzymatic analysis. Gastroenterology l983. 14. 5. Tables ofcritical values for the Pratt matched pair signed in higher plants as exemplified He/ianihus in tuberosus. Gassull Decrease in postprandial Henry RR. tolerance: l977. Ann Intern Med Jenkins DJA.27:1161-8. Basel: VerlagChemie. Archbold HK. Rumessen ii. Asp N-G.ajcn. Diabetes Care 1980. Gaseous response to ingestion fructo-oligosaccharide sweetener.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.

Jenkins DJA. mellitus. sor. 42.INTESTINAL 32. Levitt MD. 694-700. Assimilation of Lactitol. 36. and abdominal distress after ingestion of fructose.44. 34. bitol and l988. Gastroenterology I988. McBurney MI. fructooligosaccharide (Neosugar). Gudmand-H#{248}yer E. Thi#{233}baud Jacot E. Holland GC. 17:1-3. Functional bowel disease: malman. Falko J. 2012 .92:383-9. Tokunaga T.22:43 1-6. De Groot L. Silk DBA. Rumessen JJ. Vogt JE. Scand Gastroenterol l987. Shetty PS. Bantle dietary JP.95: sweetener. Thompson LU. Patil DH. Gut 37. Osei K.29: 1666-7 1. Rumessen absorption 1987. Lame RD. 1 19:553-9. Spengler M. dde41. effects OF FRUCTANS 681 JAMA 33. Hosoya N. Energy balances ofeight volunfor teers fed on diets supplemented with either lactitol or saccharose. Halfon P.org by guest on April 3. Lack ofdetectable ofdailyfructose ingestion Care 1988. Kurpad AV. “unabsorbed” disaccharide in the normal human colon. J Nutr in 1989. Hirsch P. H. Schwitz D. Comparative study of isomalt and sucrose by means ofcontinuous indirect calorimetry. et al. as a natural sweetener in the physiologic meals of ambulaobese patients with type II diabetes. Colonic fermentstion of some breads andits implication for energy availability in JJ. l986. rats. Oku T.256:324l-6. Metabolism l984.43:2l0-2. Utilization and excretion ofa new fructose-sorbitol mixtures. BrJ Nutr I986. Malabsorption of fructose-sorbitol mixtures. Rizkall SW. Increasing starch intake in the human diet increases fecal bulking. Interactions causing abdominal distress. Gastroenterology of tion after ingestion fructose tory 55.7:l229-4l. Dawn C. Bossetti BM. NutrRes l987. fructose and sucrose in types I and Metabolic II diabetic Metabolic HANDLING effects of 38. Downloaded from www. Felber JP.33:808-l 3. Van Es AJH. 39. subjects.83:249C. 1 1:546-50. Grigoresco terious 35. Levine AS. Am J Med l987. Sheahan M. H2 excreof complex carbohydrates. effects on metabolic patients. Grimble GH. J 43. an 40.ajcn. Am J Clin Nutr l986.56:545-54. control Diabetes 2 mo in NIDDM Sestoft L. Gudmand-Hyer E. Thomas JW. Fructose and the dietary therapy of diabetes Diabetologia 1979. Fetzer CA.