Effect of Absorbable and Nonabsorbable Sugars on Intestinal Calcium Absorption in Humans

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1 GASTROENTEROLOGY 1989;96: Effect f Absrbable and Nnabsrbable Sugars n Intestinal Calcium Absrptin in Humans M. GRIESSEN, P. V. SPEICH, F. INFANTE, P. BARTHOLI, B. COCHET, A. ONATH, B. COURVOISIER, and J-Ph. BONJOUR ivisins f Gastrenterlgy and Nutritin and f Nuclear Medicine. Observatry f Geneva and ivisin f Clinical Pathphysilgy. University f Geneva Hspital and Geneva University. Geneva. Switzerland The effects f glucse, galactse, and lactitl n intestinal calcium absrptin and gastric emptying were studied in 9, 8, and 2 healthy subjects, respectively. Calcium absrptin was measured by using a duble-istpe technique and the kinetic parameters were btained by a decnvlutin methd. The gastric emptying rate was determined with 99mTc_ diethylenetriaminepentaacetic acid and was expressed as the half-time f the emptying curve. Each subject was studied under tw cnditins: (a) with calcium alne and (b) with calcium plus sugar. Glucse and galactse increased the calcium mean transit time and imprved the ttal fractinal calcium absrptin by 3% (p <.2). Lactitl decreased the mean rate f absrptin (p <.1) and reduced the ttal fractinal calcium absrptin by 15% (p <.1). The gastric emptying rate did nt appear t influence directly the kinetic parameters f calcium absrptin. These results shw that bth glucse and galactse exert the same stimulatry effect as lactse n calcium absrptin in subjects with nrmal lactase whereas lactitl mimics the effects f lactse in lactase-deficient patients. Thus the absrbability f sugars determines their effect n calcium absrptin. Calcium supplementatin is ne f the mst cmmn prescriptins recmmended fr the preventin f pstmenpausal and invlutinal steprsis (1-3). It is als prescribed fr lactase-deficient patients wh avid the cnsumptin f dairy prducts (4-6). The absrptin f supplementary calcium can be influenced by varius factrs, particularly by the simultaneus presence f ther dietary cnstituents such as sugars. Studies n the influence f lactse and ther sugars n intestinal calcium absrptin have given cnflicting results (7-1). In a previus paper (11), we have shwn that lactse enhanced calcium absrptin in subjects with nrmal lactase (NL subjects), but decreased it in lactasedeficient (L) patients. We suggested (11) that these ppsite effects were nt lactse specific. Thus, the apparent stimulatry effect f lactse n calcium absrptin in NL subjects culd be ascribed t a prlngatin f the mean transit time resulting frm the slwing dwn f gastric emptying. The inhibitry influence f lactse in L subjects culd be due t a decrease in the absrptin rate brught abut by the intraluminal smtic dilutin arising frm the presence f an unabsrbed sugar. The purpse f the present study was t test these tw hyptheses by cmparing the influence f tw rapidly absrbable sugars, glucse and galactse, and that f a nnabsrbable lactse derivative, lactitl, n intestinal calcium absrptin in healthy yung men. Materials and Methds Subjects Thirty-seven vlunteers were included in the study. Each gave written cnsent after having received a thrugh explanatin f the experimental prcedure. The subjects were white men aged yr and weighing 5-84 kg. All were in gd health. taking n drugs, and withut a histry f milk intlerance. Serum calcium, creatinine, phsphrus, prtein, and alkaline phsphatase values were within the nrmal range. Abbreviatins used in this paper: L, lactase-deficient; NL, nrmal lactase by the American Gastrenterlgical Assciatin /89/$3.5

2 77 GRIESSEN ET AL. GASTROENTEROLOGY Vl. 96, N.3 Prcedure The fllwing prtcl was accepted by the lcal ethical cmmittee f the University Hspital f Geneva. The study was divided int tw parts. In the first part, a grup f subjects (n = 17) received either glucse (n = 9) r galactse (n = 8); in the secnd part, anther grup f subjects (n = 2) received lactitl. All subjects underwent tw tests f calcium absrptin at 2-3 m intervals. In ne test calcium was given alne (-), whereas in the ther test it was administered tgether with a lad f either 25 g f glucse, 25 g f galactse, r 15 g f lactitl (+). The tests were perfrmed in alternate rder [( - )/( +)] s that the same number f tests f each kind were dne in winter and in summer. The subjects maintained their usual activities and dietary habits during the study perid. T decrease the individual variatin in calcium intake, a.5-g supplement f calcium as glucnlactbinate and carbnate salts (calcium; Sandz Pharmaceuticals, East Hanver, N.J.) was given per s twice daily during the 7 days preceding each absrptin test. The subjects were instructed t eat a meal cntaining n dietary fiber and n pasta the night befre each test in rder nt t interfere with hydrgen breath eliminatin. The absrptin test prcedure was the same as that used in previus studies (11,12). Briefly, after an vernight fast, 2 ~ C(.74 i MBq) f 45Ca (Medipr AG, epartment CIS, Switzerland) with.5 g f calcium carrier (as calcium chlride) in 5 ml f water was administered rally in 3 min. uring the first secnds f the 45Ca ral administratin, a dse f 11 ~ C(.41 i MBq) f sterile 47Ca (The Radichemical Center, Amersham, U.K.) was injected intravenusly. The ttal bdy irradiatin fr each test was < 14 mrem, an amunt crrespnding t the dse received fr bne scintigraphy. N fd was allwed during the 4 h after the administratin f the calcium istpes. Then a lw-calcium lunch was given. After 8 h, subjects were permitted t resume their nrmal eating habits. Heparinized venus bld samples were taken fr measurement f 45Ca and 47Ca frm a temprary catheter, n 26 ccasins during the first 8 h and again at 24 and 32 h. Capillary bld glucse cncentratin was determined at time zer and again after 15, 3, 6, 9, and 12 min. Breath hydrgen cncentratin was measured every 15 min up t an increase f 2:.22 ~ m l then! L every, half hur fr 4 h as previusly described (13). The H2 values were nrmalized as described by Rbb and avidsn (14). Gastric Emptying Measurement Gastric emptying (15) was determined simultaneusly during the calcium absrptin test. Three hundred fifty micrcuries (12.95 MBq) f 99mTc-diethylenetriaminepentaacetic acid was added t the ral slutin and gastric activity was recrded by an Anger camera every 3 s fr the next 9 min. The rate f gastric eliminatin was cnsidered t be a mnexpnential functin and was expressed as its half-time (t 1l2 ). Radiactivity Measurement 47Ca radiactivity in the bld was determined in 2.5-ml plasma samples with a well-type y-cunter. After 8 wk f strage, 1.5 ml f plasma was mixed with 15 ml f Insta-Gel (Packard Instrument Cmpany, wners Grve, Ill.) and 45Ca radiactivity was cunted in a liquid scintillatin spectrmeter. All cunts were crrected fr quenching and fr 45Ca cntaminatin f the intravenus 47Ca preparatin. The ral and intravenus radiactivity cncentratins were expressed as a percentage f the ttal dse per liter f plasma. Mathematical Methds Values fr calcium absrptin and the kinetic parameters were btained by using the SAAM 27 prgram f Berman (16) and by the decnvlutin methd as previusly described (12). Frm the fractinal calcium absrptin A(t), the fllwing tw parameters were derived: Mean transit time = 44 A(t) t dt i f44 J A(t) dt 1 f44 Mean absrptin rate = 44 J A(t) dt. Maximum absrptin and the crrespnding time were determined after visual inspectin f the cmputer-drawn graphs. Statistical Analysis The results were expressed as mean ± SEM. 1'he paired t-test was used t cmpare the results within the same grup f subjects and the unpaired t-test was used fr cmparisn between grups. The crrelatins were calculated using linear regressins r the rank cefficient f Spearman (17). Results Intestinal Calcium Absrptin Bth glucse and galactse significantly imprved ttal fractinal absrptin by -3%, whereas lactitl had the ppsite effect f reducing the absrptin by -15% (Figure 1). The increase bserved with glucse (+.63 ±.21) was nt significantly different frm that btained with galactse (+.81 ±.17). Kinetic Parameters f Calcium Absrptin The mean transit time f calcium absrptin was significantly prlnged t the same extent by the three sugars (Table 1). The mean rate f calcium absrptin was slightly but nt significantly increased by bth glucse and galactse. In the pres-

3 March 1989 EFFECT OF SUGARS ON CALCIUM ABSORPTION 'ij *.4 Q) >.5; Q) <I> " ".3 13 ~ ~ <.l.2 u. r-.1. L - ~ , ,.---' (-) Glucse (+) (-) Galactse (+) (-) Lactitl Figure 1. Variatin f the ttal fractinal calcium absrptin (TFCaA), expressed in terms f the fractin f the dse administered, in the presence f glucse (25 g), galactse (25 g), and lactitl (15 g). (-), calcium alne; (+), calcium plus sugar. ence f lactitl, hwever, the mean rate f calcium absrptin was significantly reduced. Figure 2 illustrates the effects f glucse, galactse, and lactitl n the decnvlutin curve, which reflects the rate f calcium absrptin per minute as a functin f time after administratin f the calcium istpes. In the presence f glucse r galactse, bth a bradening and a delay in the maximum absrptin rate frm 37 t 59 min (p <.1) were bserved; in the presence f lactitl the maximum absrptin significantly fell frm 2.83 x 1-3 t 2.37 X 1-3 fractin/min (p <.1). The change in ttal fractinal calcium absrptin with either glucse, galactse, r lactitl shwed a weak psitive crrelatin with that f the mean rate f absrptin, but nt with the change in the mean transit time (Figure 3). The median time (time required t absrb 5% f the ttal fractinal calcium absrptin) was significantly increased by either glucse (55.7 ± 3.9 t 7.1 ± 2.8 min, p <.1) r galactse (51.1 ± 6. t 69.2 ± 4.1 min, p <.1), but it was nt influenced by (+).3 Caalne.2.1 Ca with glucse "''',,''''',,... '2 E.3 Caalne Ca with galactse. ~ '=.Q e-.2 '".1.g ~ a: Caalne Ca with lactitl Time (min) Figure 2. Rate f initial calcium entry frm the intestine int the intravascular cmpartment. The tw transit time curves fr each sugar were btained in the same subject. lactitl (59.4 ± 3.4 t 6.3 ± 3.6 min, p = NS). The cumulative absrptin f the dse f absrbed calcium was pltted as a functin f time (Figure 4). Glucse and galactse delayed the first phase f absrptin, prlnging the time required t absrb 5% f the ttal cumulative absrbed dse. In cntrast, lactitl significantly prlnged the secnd Table 1. Effect f Absrbable and Nnabsrbable Sugars n the Ttal Fractinal Calcium Absrptin and the Kinetics ParametersO Mean calcium absrptin rate Mean calcium transit time TFCaA (fractin f dse ingested) (fractin/min x 1-3 ) (min) Sugar n b (_)C (+)d (-) (+) (-) (+) Glucse ± ± ± ± ± ± 3.4 P <.2 e NS p <.1 Galactse ± ± ± ± ± ± 5. P <.1 NS P <.5 Lactitl ± ± ± ± ± ± 4.2 p <.1 P <.1 P <.1 NS, nt Significant; TFCaA, ttal fractinal calcium absrptin. a Results are mean ± SEM. b Number f subjects. C Calcium alne. d Calcium with sugar (glucse and galactse, 25 g; lactitl, 15 g). e Prbability btained by applying Student's t-test fr paired data.

4 772 GRIESSEN ET AL. GASTROENTEROLOGY Vl. 96, N.3 "e.c?.5 r J l ~.. <II,;,. ~ m E. c a ~ m<ll ::E':" -.5 <l "2 I 4 m E i= 'iii 2 <II t= <II m ::E <l.5, , ~ glucse galactse r =.71 p< r i , , r =.23 (NS) r =.57 p<.1.5 r =.1 (NS) r ~ r L\ TFCaA (fractin f dse ingested) Figure 3. Crrelatin between the changes f the ttal fractinal calcium absrptin (TFCaA) and the mean rate f calcium absrptin (upper panels) r the mean transit time (lwer panels). Left: effect f absrbable sugars (glucse and galactse). Right: effect f nnabsrbable sugar (lactitl). phase f the absrptin, i.e., the perid necessary t absrb the secnd half f the absrbed dse (Figure 4). With lactitl the cumulative absrptin curve distinctly flattened beynd 5% as cmp<;lred with the pattern bserved with calcium alne r in the presence f either f the absrbable sugars, glucse r galactse. T quantify these effects n calcium absrptin kinetics, the rati f the slpes frm 8% t 5% and frm 5% t 2% was calculated fr each sugar and cmpared with that btained with calcium alne (Table 2). In the presence f lactitl this rati was significantly higher than with calcium alne, 1, ,...,... d;" ",l"'" /... '.«l... ' *** //,..",..",:1" ~ I " " ' : : / /,,/ *** - Ca alne (n=37)... Ca + galactse (n=8).. 1>....,. Ca + glucse (n=9) --- Ca + lactitl (n=2) Figure 4. Cmparisn f the cumulative calcium absrptin curves with calcium alne and in the presence f sugars. *p <.5; * * *p <.1. O ~ r ~ r r Time (min)

5 March 1989 EFFECT OF SUGARS ON CALCIUM ABSORPTION 773 Table 2. Effect f Absrbable and Nnabsrbable Sugar n the Cumulative Calcium Absrptin Curves Q Rati C Sugar n b (_)d (+)e Glucse ± ±.14 p <.5 f Galactse ± ±.15 NS Lactitl ± ±.12 P <.1 NS, nt significant. a Results are mean ± SEM. b Number f subjects. C Rati f slpe f 8% t 5% and 5% t 2% f the cumulative absrptin curves. d Calcium alne. e Calcium with sugar (glucse and galactse, 25 g; lactitl, 15 g). f Prbability btained by applying Student's t-test fr paired data. prviding evidence that the nnabsrbable sugar extends the duratin f the absrptin prcess. Gastric emptying. Bth glucse and galactse diminished the rate f gastric emptying t the same extent (Table 3). N crrelatin was fund between the increase in gastric emptying half-time and the augmentatin in either the ttal fractinal calcium absrptin r the mean transit time f calcium absrptin. Lactitl, hwever, did nt affect the rate f gastric emptying. Transit time f lactitl frm muth t cecum. The elapsed time frm sugar ingestin t the first detectable rise in breath H2 excretin was determined fr the lactitl grup. This value can be cnsidered as an estimate f the time required fr the head f the lactitl clumn t reach the cln. It averaged 61 ± 5 min (n = 19; range, min). The elapsed time between ingestin and the peak f breath H2 excretin was als determined as it reflects the transit time f the bulk f the lactitl blus. It averaged 144 ± 1 min (n = 19; range, 9-24 min). The maximum H2 cncentratin detectable in the expired air amunted t 3.5 ±.4 pmlll (n = 19). A weak crrelatin between the half-time f gastric emptying and the elapsed time between lactitl Table 3. Effect f Absrbable and Nnabsrbable Sugars n the Rate f Gastric Emptying Expressed as the Emptying Half-Time Q Sugar Glucse Galactse Lactitl (_)C 15 ± 2 16 ± 2 17 ± 2 t1l2 (min) 33 ± 6 3 ± 2 18 ± 2 pe <.2 <.1 NS NS, nt significant; t 1l2, emptying half-time. a Results are mean ± SEM. b Number f subjects. C Calcium alne. d Calcium with sugar (glucse and galactse, 25 g; lactitl, 15 g). e Prbability btained by applying Student's t-test fr paired data. ingestin and the first detectable rise in breath H2 excretin was bserved (rh f Spearman =.51, P <.5). iscussin This study clearly demnstrates that sugars such as glucse r galactse, which are rapidly absrbed in the prximal small intestine, increase the absrptin f calcium as estimated by determining the ttal fractinal calcium absrptin. The stimulatry effect btained with 25 g f either glucse r galactse was abut half that bserved in respnse t 5 g f lactse in NL subjects (11). This quantitative relatinship suggests that the increase in calcium absrptin may be directly prprtinal t the dse f the sugar administered. This culd explain why in an earlier study a lwer (1 g) dse f glucse was nt fund t stimulate calcium absrptin (18). In the present investigatin lactitl, an unabsrbable sugar, exerted an ppsite effect n calcium absrptin t that f either glucse r galactse. These data are cnsistent with ur previus findings n the actin f lactse in NL and L subjects (11). The effects f absrbable and nnabsrbable sugars in bth NL and L subjects, as bserved in ur present and previus studies (11), are summarized in Figure 5. Nte that the inhibitry influence f lactitl was similar t that btained with srbitl, anther prly absrbed sugar (18). The kinetics f calcium absrptin with either glucse r galactse shwed a pattern similar t that previusly btained with lactse in NL subjects: increase in the mean transit time withut a significant alteratin in the absrptin rate. This suggests that absrbable sugars enhance calcium absrptin thrugh a cmmn, nnspecific mechanism. One pssible explanatin was an effect f slvent drag n calcium absrptin due t active sugar uptake (19). Perfusin studies f human jejunum (2) as well as rat jejunum (21) have shwn that the rate f absrptin f water can be varied withut apparent enhancement f calcium absrptin; therefre, slvent drag des nt appear t be the respnsible mechanism. The increase in the mean transit time f calcium absrptin culd be related t the slwing dwn f gastric emptying, an effect generally ascribed t the smlality and energetic (calric) density f the slutins (22,23). The mean transit time, hwever, was nt statistically crrelated with the duratin f gastric emptying. The maximum and mean absrptin rates f calcium were nt significantly mdified by the presence f the tested sugars. The absrptin rate f calcium has been clearly shwn t be related t the intraluminal c n c e n t r a ~ tin f calcium (2). Thus, we may assume that the

6 774 GRIESSEN ET AL. GASTROENTEROLOGY Vl. 96, N.3 Absrbable Sugars W. 4 ~ , U) u " ~.2 () LL r-.1 -' ,.----' (-) (+) Glucse (n=9) W.3-r , (-) (+) Galactse (n=8) Nn Absrbable Sugars.g ~ c " ~.2 :::. ~ () LL r-.1 -'---..-,.---1 (-) (-) Lactitl (n=2) Lactse in L subjects (n= 7) /" (-) (+) Lactse in NL subjects (n= t 2) (+) Figure S. Influence f absrbable and nnabsrbable sugars n the intestinal absrptin f calcium. The effects f lactse in NL subjects, glucse, and galactse (upper panels) are cmpared with the effects f lactse in LO subjects and lactitl (lwer panels). Results are mean ± SEM. See text fr further details. (-). calcium alne; (+). calcium + sugar (glucse, 25 g; galactse, 25 g; lactse, 5 g; lactitl. 15 g); TFCaA, ttal fractinal calcium absrptin. slwer delivery f calcium t the site f intestinal absrptin did nt substantially alter the luminal cncentratin f calcium. The slwer gastric emptying, hwever, wuld prlng the supply f calcium t the intestine, increasing accrdingly the time f cntact between the calcium ins and the intestinal mucsa, and thus the absrptin prcess, as shwn by the increased transit time. One may als speculate that the slwer supply f calcium t the small intestine shuld decrease the luminal cncentratin and thus the absrptin rate f calcium. Hwever, absrbable sugars stimulate water absrptin, which in turn shuld increase the intraluminal cncentratin f calcium (2,24). Therefre, the absence f a visible alteratin in the absrptin rate f calcium might be the result f tw ppsing phenmena. The effect f lactitl in healthy individuals was quite similar t that previusly bserved with lactse in L subjects: a slight increase in the mean transit time assciated with a decrease in the mean rate f calcium absrptin. There is, nevertheless, sme difference between lactse in L subjects and lactitl in healthy individuals. Indeed, a small amunt f lactse is absrbed in L subjects. This leads t a slwing dwn f gastric emptying that results frm the calric effect f the lactse slutin. Cnsequently, there is a shift f the cumulative absrptin curve f calcium in L subjects. In the case f lactitl, the slutin has n calric effect and thus the gastric emptying half-time was nt significantly mdified. This may explain why in lactitltreated subjects the first part f the cumulative absrptin curve was similar t that btained in the presence f calcium alne. Therefre, althugh the gastric emptying rate influences the mean transit time f calcium absrptin, the tw parameters were nt directly related. The decrease in the absrptin rate bserved with lactitl can easily be ascribed t the smtic effect f the nnabsrbable sugar that dilutes the intraluminal cncentratin f calcium in the small bwel (25). Mre difficult t explain is the prlngatin f the calcium absrptin time in the presence f lactitl in healthy individuals r in the presence f lactse in L subjects (11). One pssible explanatin is that the ileum culd be a reservir that wuld increase the duratin f cntact between the calcium ins and the intestinal mucsa and favr the prlngatin f calcium absrptin. Hwever, nnabsrbable sugars increase the rate f transit thrugh the small intestine and the ileclnic junctin (26-28). Anther pssibility is t implicate the cln in the prcess f calcium absrptin. Indeed, the median absrptin time was attained at abut 6 min fr the lactitl grup. At this time ~ 8 f the % lactitl slutin had left the stmach and H2 began t appear in breath, indicating that the lactitl slutin was entering the cln. In the cln sugars are cnverted t rganic acids. This cnversin tends t decrease ph and thereby increases the availability f calcium fr absrptin. Tw findings suggest that a prlngatin f calcium absrptin culd take place in the cln. First, Hylander et al. (29) shwed that the cln plays a cmpensatry rle in patients wh underg a resectin f the small intestine. Secnd, in patients with untreated celiac disease r intestinal resectin fr besity, we have bserved a prlngatin f the absrptin f calcium f up t 22 min. Althugh there is n way t cnclude definitely abut the perative mechanism, the mst likely explanatin is that the absrptin f calcium was

7 March 1989 EFFECT OF SUGARS ON CALCIUM ABSORPTION 775 cntinued in the cln, pssibly as a result f intraluminal acidificatin due t sugar fermentatin. The fact that absrbable sugars favr the absrptin f calcium, whereas nnabsrbable sugars decrease it, culd have dietary and therapeutic implicatins. Indeed calcium supplementatin shuld be given in the mst absrbable frm, particularly in elderly subjects with lw absrptive capacity. Furthermre, sme prly absrbed sugars are used as laxatives, such as lactitl r lactulse, r are present as srbitl r fructse in sugar-free prducts (3,31). These preparatins culd reduce the intestinal absrptin f calcium and increase the risk f maintaining a negative calcium balance. References 1. Heaney RP, Gallagher JC, Jhnstn CC, Neer R, Parfitt AM, Whedn G. Calcium nutritin and bne health in the elderly. Am J Clin Nutr 1982;36: Nrdin BEC, Plley KJ, Need AG, Mrris HA, Marshall. The prblem f calcium requirement. Am J Clin Nutr 1987;45: Marcus R. The relatinship f dietary calcium t the maintenance f skeletal integrity in man. An interface f endcrinlgy and nutritin. Metablism 1982;31: Birge SJ, Keutmann HT, Cuatrecasas p, Whedn G. Osteprsis, intestinal lactase deficiency and lw dietary calcium intake. N Engl J Med 1967;276: Newcmer A, Hdgsdn SF, McGill B, Thmas PJ. Lactase deficiency: prevalence in steprsis. Ann Intern Med 1978; 89: Finkenstedt G, Skrabal F, Gasser RW. Lactse absrptin, milk cnsumptin, and fasting bld glucse cncentratins in wmen with idipathic steprsis. Br Med J 1986;292: Greenwald E, Samachsn J, Spencer H. Effect f lactse n calcium metablism in man. J Nutr 1963;79: Cndn JR, Nassim JR, Hilbe A, Millard FJC, Stainthrpe FM. Calcium and phsphrus metablism in relatin t lactse tlerance. Lancet 197;i:l Pansu, Chapuy MC. Calcium absrptin enhanced by lactse and xylse. Calcif Tissue Res 197;4(Suppl): Kcian J, Skala I, Baks K. Calcium absrptin enhanced frm milk and lactse free milk in healthy subjects and patients with lactse intlerance. igestin 1973;9: Cchet B, Jung A, Griessen M, Barthldi p, Schaller P, nath A. Effect f lactse n intestinal calcium absrptin in nrmal and lactase-deficient subjects. Gastrenterlgy 1983;84: Griessen M, Jung A, Cchet B, et al. A simple methd fr measurement f intestinal calcium absrptin in humans by duble-istpe technique. J Lab Clin Med 1985;15: Cchet B, Griessen M, Balant L, Infante F, Vallttn MC, Bergz R. Valeur du test de I'hydrgene expire dans Ie diagnstic des deficits en lactse. I. Analyse methdlgique et statistique. Gastrenterl Clin Bii 1981;5: Rbb TA, avidsn GP. Advances in breath hydrgen quantitatin in paediatrics: sample cllectin and nrmalizatin t cnstant xygen and nitrgen levels. Clin Chim Acta 1981; 111: Gulsrud PO, Taylr IL, Watts H, Chen MB, Elashff J, Meyer JH. Hw gastric emptying f carbhydrate affects glucse tlerance and symptms after truncal vagtmy with pylrplasty. Gastrenterlgy 198;78: Berman M. Cmpartmental analysis in kinetics. In: Stracey R, Waxman B, eds. Cmputer in bimedical research. Vlume 2. New Yrk: Academic, 1965: Snedecr GW, Cchran WG. Statistical methds. 7th ed. Ames, Iwa: Iwa State University Press, Francis RM, Peacck M, Barkwrth SA, Marshall H. A cmparisn f the effect f srbitl and glucse n calcium absrptin in pstmenpausal wmen. Am J Clin Nutr 1986;43: Pappenheimer JR, Reiss KZ. Cntributin f slvent drag thrugh intercellular junctins t absrptin f nutrients by the small intestine f the rat. J Membr Bii 1987;1: Nrman A, Mrawski SG, Frdtran JS. Influence f glucse, fructse and water mvement n calcium absrptin in the jejunum. Gastrenterlgy 198;78: Yunszai MK, Nathan R, Ykyama L. Intestinal calcium absrptin is enhanced by -glucse in diabetic and cntrl rats. Gastrenterlgy 1985;88: Hunt IN. A pssible relatin between the regulatin f gastric emptying and fd intake. Am J Physil 198;239:Gl McHugh PR The cntrl f gastric emptying. J Autn Nerv Syst 1983;9: Ck GC. Rates and mechanisms f glucse, galactse, and xylse absrptin in man in viv. Scand J Gastrenterl 1977;12: ebngnie JC, Newcmer A, McGill B, Phillips SF. Absrptin f nutrients in lactase deficiency. ig is Sci 1979; 24: Read NW, Miles CA, Fisher, et al. Transit f a meal thrugh the stmach, small intestine, and cln in nrmal subjects and its rle in the pathgenesis f diarrhea. Gastrenterlgy 198;79: Griessen M, Bergz R, Balant L, Lizeau E. Effet du lactitl sur la prductin d'hydrgene expire chez l'hmme nrmal. Schweiz Med Wchenschr 1986;116: Spiller RC, Brwn ML, Phillips SF. Emptying f the terminal ileum in intact humans. Influence f meal residue and ileal mtility. Gastrenterlgy 1987;92: Hylander E, Ladefged K, Jarnum S. The imprtance f the cln in calcium absrptin fllwing small-intestinal resectin. Scand J GastrenterI198;15: Hyams JS. Srbitl intlerance: an unappreciated cause f functinal gastrintestinal cmplaints. Gastrenterlgy 1983;84: Ravich WJ, Bayless TM, Thmas M. Fructse: incmplete intestinal absrptin in humans. Gastrenterlgy 1983;84:26-9. Received April 2, Accepted September 27, Address requests fr reprints t: r. Marthe Griessen, Ph.., Labratire Central de Chimie Clinique, H6pital Cantnal Universitaire de Geneve, CH-1211 Geneve 4, Switzerland. This wrk was supprted in part by the Fnds Natinal Suisse de la Recherche Scientifique (grant ), the Sandz Fundatin (Bale), and Zyma SA (Nyn). The SAAM 27 cmputer prgram was kindly prvided by the U.S. Public Health Service/ Natinal Institutes f HealthlNatinal Heart, Lung, and Bld Institute-Natinal Cancer Institute jint develpment prject. A part f this wrk was presented at the XIXth Eurpean Sympsium n Calcified Tissues, Stckhlm, Sweden, June 15-19, The authrs thank Mrs. E. Bachmann and E. Martin fr helpful technical assistance, Mrs. M-C. Brandt fr secretarial assistance, and r. J.R. Green fr reviewing the manuscript.

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