lactose in the diabetic diet a comparison with other carbohydrates

8/2/2019 Lactose in the Diabetic Diet a Comparison With Other Carbohydrates

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NUTRITION RESEARCH, Vol. 5, pp. 1335-1345, 19850271-5317/85 $3.00 + .00 Printed in the USA.Copyright (c) 1986 Pergamon Press Ltd. Al l rights reserved.

Lactose in the Diabetic Diet: A Comparison with other Carbohydrates

Thomas M.S. Wolever, B.M., M.Sc.,1,2 Gerald S. Wong, M.D.,2 Anne Kenshole,M.D., 3 Robert G. ~osse, M.D.,2 Lillan U. Thompson, Ph.D., Kah Yun Lam,B.Sc. 2 and David J.A. Jenklns, D.M.I, 2

Department of Nutritional Sciences, Faculty of Medlclne; Division ofEndocrinology and Metabolism, St. Michael's Hospltal; 2 and Women's CollegeHospital; University of Toronto, Toronto, Ontario, Canada3

ABSTRACTTo compare the effects of lactose with other carbohydrates on acuteblood glucose responses, six diabetic volunteers took breakfast testmeals of 38g porridge oats (21g carbohydrate) plus an additional 25gof carbohydrate from either lactose, white bread, sucrose, glucose orfructose. Compared with oats plus bread, the blood glucose responseswere increased by 14% (NS) after oats plus glucose, reduced by 17%(


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1336 T. WOLEVER

In view of the desire for lactose containing foods such as ice cream(13) and yoghurt, and the use of high fiber breakfast cereals which requirem~Ik for palatabi l i ty, we have compared the blood glucose response of lactoseto that of bread and other common sugars In diabetic individuals. We havealso examined the relationship between sweetness and palatabi l i ty for thesugars, since many diabetic patients desire sweet foods.

SUB3ECTS AND METHODSA group of si x d iab et ic volunteers was stud ied (2 men, 4 women; 63 6 yr ; 145 21% Idea l weight (7) ; 4 on Insu l in , 33 10 un it s/ da y; 2 onora l hypoglycemic agents; Table 1). A l l subjects were confirmed as having

diabetes by blood glucose concent rations over 11 .1 mmol/1 (200 mg/dl) (range12.1-18.2 mmol/1) 2 hours a ft e r the glucose contai ning t es t mea l describedbelow. Patients were treated by th ei r physicians wtth I nsul in to controlsymptoms of diabetes which had per sis ted a f te r weight reduction and treatmentwith diet and ora l hypoglycemic agents. The patien ts on In su li n wereconfirmed as NIDDM on the basis of normal or elevated f as ti ng le ve ls (2.4 0.6 pg/ml) and postprandial responses (4.5 0.8 pg/ml: Table 1) of serumC-peptlde (14,15). Fasting and 60 min postprandial se ru m C-peptideconcentrations in a group of 8 normal individuals were 1.3 0.1 pg/ml(range 0.62 - 1.g) and 4.8 0.8 pg/ml (range 2.7 - 7.9) respectlvely.TABLE 1:

Patients studied

Pa ti en t Sex Age ~DW Treatment Years F.B.G. C-pepttde(pg/ml)(See below) Diabet ic (mmol/1) Fasting 90min

8T M 76 123 60-62L(a) 11 12.8 3.2 3.8KM F 61 116 25L 2 5.3 1.6 4.6EH F 7 0 179 5mg Eg. bd 7 6.4 -V 8 F 59 233 5mgDb. bd 5 9.3 -J H M 7 3 120 30L 20 6.1 1.1 2 . 7AR F 36 100 15L 4 8.3 3.7 6.7

M ea n 6 3 1 4 5 3 2 . 8 8 . 2 8 . 0 2 . 4 4 . 5 S EM 6

L = Units Lente in su li n per day S = Units regu lar (so lub le) in su li n per day;Eg. = Euglucon; Db. = Dlabeta;(a) The changes tn Ins ul ln dose were not associa ted with s ign i f i cant changesIn carbohydrate tole rance: see te xt .Volunteers attended the diabetic day care unit of St. Michael's Hospitalfa st in g one morning a week for the dura tion of the study (approximately 3months). After col lec tin g fasting fin ge r-p ric k cap il la ry blood samples(Autolet lance ts, Owen Mumford, Woodstock, England) the pa tien ts took t he i rusual ins ul in dose or ora l agents and then ate a te st meal. Meals were


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GLYCEMCRESPONSETO LACTOSE 1337

planned to contain 50g carbohydrate, the amount of bread ca lculated from foodtab les (16) , and the amount of oats from proximate ana lys ts supplied by themanufacturers. The reason that the oats were fed according to themanufacturer's ana lys is was that these fig ur es , even though not incl udingf iber , gave more oats per 50g carbohydrate por tion (75.4g) than did thefigures from the food tables (68.6g) which included a figure for dietaryf iber (16). Hal f the carbohydrate in 5 meals was from hot oatmeal and ha l fwas from either lactose, white bread, glucose, sucrose, or fructose (Table2). In add it io n, the pat ients took a meal of white bread alone (50gcarbohydrate) and a meal of oatmeal alone (50g carbohydrate; Table 2). Testmeals were served with a beverage of the patient's choice (standard for eachpa ti en t) of one or two cups of water, tea or cof fee with or withou t 30ml of2 bu t te rf a t mi lk per cup. Two patien ts were given corn flakes (30g per 25gcarbohydrate) instead of oatmeal for all appropriate meals to test whetherthe sugar ef fe ct s were d i f fe rent against the background of a higher glycemlcindex food. Since no di fferences were observed, the re su lt s were pooled.Duplicate test meals were subsequently analyzed by proximate analysis forcarbohydrate, fa t , prot ein, (17) and di et ar y f ib er by the method of Asp,Furda, and DeVrles (18) . Resul ts agreed to w i th in l~ of the expectedTABLE 2Planned composition of test meals

Test Meal Uncooked Protein Fat Available DietaryWeight Carbohydrate Fiber(g) (g) (g) (g) (g)White bread 66.8* 7.6 0.8 50.0 2.0Oats 75.4* I0.5 5.4 50.0 5.3x1/2 Oats plus 37.7* 9.1 3.1 50.0 3.6xI/2 White bread 33.4+1/2 Oats plus 37.7* 5.3 2.7 50.0 2.6xSucrose 25.0**I/2 Oats plus 37.7* 5.3 2.7 50.0 2.6xFructose 25.0**I/2 Oats plus 37.7* 5.3 2.7 50.0 2.6xGlucose 25.0**I/2 Oats plus 37.7* 5.3 2.7 50.0 2.6xLactose 25.0

+ Weight of f l our . Each lo af of bread cont ain ing 334g f lour was made with 7gsucrose and 5.5g yeast.* Quaker Quick Oats. Preparation was by the add it ion of 350ml bo il ing waterper 37.7g oats, mixing well and allowlng to stand for lmin beforeconsumption.** Sugars were mixed with dry oatmeal before the addition of botltng water.x Die tary fi be r in oats estimated according to food table s (16).


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1338 T. WOLEVER

av ai lab le carbohydrate content of bread. However, our analys is gave a fi gu reof 42.2g available carbohydrate for the oats which were expected to contain50g. This was due to the higher concent ration of f iber estimated by ourmethod of a nalysi s (12.5 0.9% for 8 determ ina tio ns) .

Al l six patients completed al l seven test meals. F i f t y gramcarbohydrate portions of white bread were taken at the beginning and end ofthe series, and the other 6 meals were fed according to a randomized blockdesign.Capillary blood samples were obtained fasting and at half-hourlyIn te rval s for 3h af te r the st ar t of the meal for a nalys is of glucose by aglucose oxidase method (19) . Venous samples fo r C-peptlde an alys is (20) weretaken f as t ing and 90 min af te r the consumption of 50g carbohydrate as breadfrom those patients taking lnsulln.After f ini shin g each test meal the pat ients rated i t s pa la ta bi l i ty on ascale of -3 (very unpleasant) to +3 (very pleasant) and sweetness on a scaleof 0 (not at all sweet) to 10 (extremely sweet).Results are given as means SEN. The glycemic response areas werecalculated geometrically as the incremental area under the blood glucosecurve above the fasting level according to the following formula:

Area = (A30 + A60 + Ago + 4120 + 4150 + 4180/2) x 30where A30 , A60, A90 etc represent the po si ti ve dif fer ences between theblood glucose concentration fa st in g and at 30, 60, go mtn etc res pe ct iv el y(21,22). This formula was used since for every in div id ual te st , the fas ti ngblood glucose concentration was less than the postprandial levels (22).

The glycemtc indices (GX) of the sugars f or each in di vi du al subject werecalcul ated as follows:

GX = Sugar qlycemic response area x 100.White bread glycemtc response areaThe sugar and white bread glycemic response areas were calculated bysubt ract ing ha lf the glycemic response area fo r the oats alone te st meal fromthe glycemic response areas for the mixed oats plus sugar and oats plus breadmeals. This approach was considered Jus t i f i ed because the mean glycemicresponse area f or the mixed bread and oats meal (835 mmol.mln/1) wasv i r tu a l l y id en ti ca l to the mean of the glycemlc responses f or bread alone(868 mmol.min/1) and oats alone (806 mmol.mtn/1). The GI values givenre pr es en t the mean SER of the in di vi du al re su lt s.S ta t i s t i ca l analys is of the meal blood glucose responses was performedby two-way analysts of variance with Ftsher's test to determine thesigni fican ce of the differ ence between Indi vidu al means (23). In addi tion ,fo r comparisons between the 6I of the sugars and the l I of whi te bread,students t- t es t for paired data was used. This gave si gn if ic an t l eve ls forthe di ff eren ce s between the GI of the sugars and whi te bread which were thesame as those in the ana lys is of varlance of the dif fer ences in glycemtcareas for the respective sugar and bread containing meals.


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GLYCEMIC RESPONSE TO LACTOSE 1339

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1340 T. WOLEVER

RESULTSThe test meals were well received and eaten within the requested time oflO mln. Dosage of insulin and oral hypoglycemlc agents remained constantthroughout the course of the study in 5 of the 6 patients. BT added 2 unitslente insulin part way through the study. This was associated with a 16%lower area for white bread (660 compared with 787.5 mmol.mln/l). Howeverthis difference was not considered significant because i t was well within therange of variabi l i ty for the patients on standard treatment whosecoefficients of variation of blood glucose area after repeated tests of bread43 ~. There was no change in mean carbohydrate toleranceanged from 2 to %over the course of the study as Judged by the repeated 50g carbohydrate breadtest meals (mean area under the curve at the star t of the s tudy, 855 114

mmol. min/1, compared with 881 69 mmol.min/1 at the end).Blood glucose responses

The areas under the blood glucose response curves for both the lactoseand fructose containing meals were slgn|flcant ly less than that for oats plusbread (Table 3). In addition, the mean blood glucose increments after oatsplus fructose were slgnlflcant ly lower than af ter bread plus oats at 90, 120,150, and 180 mln (Figure l ) . Oats plus glucose had a higher glycemlcresponse area than oats plus bread although the difference did not reachstatistical significance (Table 3).Glycemlc Index

The GI of lactose, sucrose, fructose and glucose, (mean SEM)respectively, were calculated to be 69 lO, 91 18, 35 12 and 131 13, with white bread being ascribed the value of I00. Lactose (p < 0.05)and fructose (p < O.Ol) had GIs significantly below that of bread. The GI ofsucrose and glucose were not significantly di fferent from that of bread.Palat lbl l l ty and Sweetness

Fructose and sucrose were considered significant ly sweeter than lactoseand glucose, which in turn were signi ficant ly sweeter than the meals withoutsugar (Table 3). Although there were no signif icant differences, thepatients tended to prefer the sweetened meals more than the unsweetenedones. However, amongst the meals containing sugar, they tended to preferthose which tasted less sweet ( i . e . those containing glucose and lact os e) .

DISCUSSIONThe re sul ts suggest that in NIDDM the consumption of lactose produceslower glycemtc excursions than sucrose. Th ey also showed that lac toseproduced a lower blood glucose response than af ter the consumption of anequal amount of carbohydrate taken as white bread. The fi nd ings fo r glucose,sucrose and fructose are in agreement wtth other published data In normal(24) and diabetic subjects (3,5,25).I t seems un li ke ly tha t malabsorptlon of lactose could have contr ibute dto the low glycemlc response slncenone of the patients was intolerant tomi lk ; the amount of lactos e given was equi valent to tha t in 500 ml of milk .


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In addlt lon, there were no symptoms of flatulence, diarrhea or abdomlnalbloating or discomfort suggestive of carbohydrate malabsorptlon. There aretwo reasons l ike ly for the relat ive ly f lat blood glucose response followingthe consumption of lactose: the slower rate of absorption, and the smallhyperglycemic effect of galactose. Only 50% of the lactose molecule isglucose, and when g~ven as lactose, this is absorbed at an approximately 35%slower rate than a l : l mixture of glucose and galactose (26). Hydrolysis oflactose by intestinal brush border 8-glucosldase (lactase) and absorption ofthe monosaccharlde components occurs at approximately half the rate ofsucrose and maltose hydrolysis and absorption (26). Intravenous and oralboluses of galactose ~n normal subjects have produced small blood glucose andinsulin responses, presumably due to ~ts Interconverslon to glucose (27,28).

8r

0 1 2 3T ime (hr )FIGURE 1

Mean SEN blood glucose increments of 6 NIDDM pa ti en ts a f te r consumptionof test meals containing oatmeal plus white bread, glucose, lactose, sucroseand fru cto se. The si gn if icance of the d if fe ren ce of mean values from theoats plus white bread meal are shown by as te ri sk s: *p< 0.05, **p< 0.01.

Lactose would thus be expected to have a larger acute glycemic effectthan fructose because of Its glucose content, but less than sucrose due toi t s slower rate of brush border hyd ro lysi s. This pic tur e was seen here wherethe glycemic index f or lac tose (69 lO) was midway between that fo r


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1342 T. WOLEVER

sucrose (91 18) and fruc tose (35 12). The longer term ef fe ct s of theconsumption of moderate amounts of la ct ose, or of other sugars, on bloodglucose control ~n diabetes remains to be clarified.While there has been conslderable a tt en ti on paid to the short termef fects of sucrose on blood li p i d le ve ls , there has been l i t t l e work donewi th respect to lactose. Fermented mil k has been suggested to behypocholesterolemic possib ly due to it s lactose content (29). Nevertheless,tn a recent study, consumption of 1 l i t e r of 2% mtlk (containing S2g oflactose) per day for 3 weeks had no eff ec t on serum cho les ter ol ortr lg ly ce r~de concentrations in 68 healthy volunteers (30). In an ear lystudy, when lactose replaced glucose In the formula dte ts of mental hospi ta lpa ti en ts , there was no ri se seen In blood 11plds, although a ri se dld occurwhen sucrose replaced glucose (31 ). More work wt l l be needed to determinethe long term effects of lactose on blood 11plds, particularly as comparedwith starchy foods.Sucrose, glucose and fructose are avai la bl e as nu tr i t iv e seeetners.Lactose has not been used for th is purpose because of i ts less sweet tas te ,as was confirmed here where i t had a s i g n i f i ca n t l y lower sweetness ra ti ngthan ei th er sucrose or fructose. Nevertheless i t was considered pal atabl e,while the large amounts of sucrose and fructose in the test meals wereconsidered excessively sweet.In the present series the sugars were given mixed with oats to reducetonlclty and mtnJmlse the possibly nauseating sweetness of the sugars takenalone, factor s which might int er fe re with gas tri c emptying. I f th is hadoccurred, comparison of the results of sugars with bread would have beend i f f i cu l t .The calculation of the glycemic index of the individual sugars in thisstudy depends upon the p ro po rt io na li ty of the glycemic con tri but ion ofindiv idu al foods to the to ta l blood glucose response of a mixed meal. Suchpro port ion a l i ty was seen here where the mixed oat and bread meal had aglycemic response midway between oats alone and bread alone. In ad di ti on , Ina previous study (15), a mixed meal of ha l f bread and ha l f beans taken by 7NIDDM had a glycemlc index of 60, close to halfway between f u l l bread alone,100, and fu l l beans alone, 41. This approach has also been shown to be val id

fo r mixed meals con taining representa ti ve amounts of pro te in and fa t . Inth is si tua ti on the GI of mixed te st meals reported to have been fed to groupsof diabetic subjects were calculated and found to relate significantly to theincremental blood glucose responses derived from the reported data (r = .95,n = 5) (32 ).The G1 of the four sugars ca lculated in th is way were In good agreementwith the glycemtc tndlces In normal in di vi du al s (24) (adjusted so tha t whitebread equals 100) of mi lk, 49; sucrose, 86; fr uc tose , 29; and glucose, 145( r = 0 . 9 8 1 ; p < O . O 5 ) .I t ls concluded tha t lactose raises the blood glucose lev el acute ly

fo ll ow ing a meal to a lesser extent than an equal amount of bread. The longterm effect s of lactose tn the diabetic d iet require furth er study.


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GLYCEHIC RESPONSETOLACTOSE 1343

Acknowledgements:These studies were supported by the Natural Sciences and EngineeringResearch Council of Canada and by the Quaker Oats Company, Barrlngton, I l l .

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1344 T. WOLEVER

14) Block MB, Mako ME, Stelner OF, Rubensteln AH. Circulat ing c-peptldeImmunoreactlvlty: studies in normals and diabetic patients. Diabetes1972;21:I013-1026.15) Jenklns DJA, Wolever TMS, Wong GS, Kenshole A, Josse RG, Thompson LU,Lam KY. Glycemlc responses to foods: possible differences betweenInsulln-dependent and non-lnsulln-dependent diabetics. Am. J. Clln.Nutr. 1984;40:971-781.16) Paul AA, Southgate DAT. McCance and Wlddowson's The Composition ofFoods. Medical Research Council Special Report Series nO. 297. 4thEdition, London: HMSO, 1978.17) AOAC Offi cial Methods of Analysis. Association of Offi ci al Analytical

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the b lood g luco se response to m ixed mea ls . Am. 3 . C l l n . Nu t r . 1985: i np r e s s .23) Snedecor GW, Cochran WG. S ta t i s t i c a l Methods . 7 th E d i t i o n . Iowa S ta teu n i v e r s i t y P r e s s , 1 9 8 0 .24 ) Jen k ins DJ A, Wolever TM S, Ta y lo r RH, ba rke r HM, F te lde n H, Ba ldw in JM,Bow l ing AC, Newman HC, Jen k ins AL, Go f f o r . G lycemic i nde x o f food s : ap h y s i o l o g i c a l b a s i s f o r c a r b o h y d r a t e e x c ha n g e . Am. J . C l l n . N u t r .1981 ; 34 : 362 - 366 .2 5 ) L en n e r RA. S t u d i e s o f gl yc e m t a a nd g l u c o s u r l a i n d i a b e t i c s a f t e r

b r e a k f a s t m e als o f d i f f e r e n t c o m p o s i t io n . Am. J . C l t n . N u t r .1976 ; 29 : 716 - 725 .26) Gray GM, San t iago NA. D lss acc ha r tde ab so rp t i on In normal and d i seas edhum an i n t e s t i n e . G a s t r o e n t e r o l o g y 1 9 6 6 ; 5 1 : 4 8 9 -4 9 7 .


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27) Ganda OP, Soeldner JS, Gleason RE, Cleator IGM, Reynolds C.effects of glucose, mannose, galactose, and fructose %n man.Endocrinol. Metab. 1979;49:616-623.

Metabolic

3. Clin.2B) Ross SA, Dupre J. Effects of %ngestion of tr%glycer%de or galactose onsecretion of gastric %nhibltory polypept%de and on responses tointravenous glucose In normal and diabetic subjects. Diabetes1 9 7 8 ; 2 7 : 3 2 ] - 3 3 3 .29) Ahmed AA, McCarthy RD, Porter GA. Effect of mllk constituents onhepatic cholesterolgenes%s. Atheroscleros%s 197g;32:347-357.30) Thompson LU, Jenkins DJA, V%c Amer MA, Relchert R, Kalmusky J. The

effect of fermented and unfermented milks on serum cholesterol. Am. J.Clin. Nutr. 1982;36:1106-IIII.31) Anderson 3T, Grande F, Matsumoto Y, Keys A. Glucose, sucrose andlactose In the diet and blood llplds in man. 3. Nutr. 1963;79:349-359.32) Wolever TMS, Nuttall FQ, Lee R, Wong GS, Josse RG, Cs~ A, JenklnsDJA. Pred%ctlon of the relative blood glucose response of mixed mealsusing the white bread glycem%c index. Diabetes Care 1985;8:418-428.

Accep ted f o r pu b l i c a t io n Oc tober 29 , 1985 .

lactose in the diabetic diet a comparison with other carbohydrates

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