NUTRITION RESEARCH, Vol. 5, pp. 1335-1345, 1985 0271-5317/85 $3.00 + .00 Printed in the USA.

Copyright (c) 1986 Pergamon Press Ltd. All 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 L i l l a n U. Thompson, Ph.D.,l Kah Yun Lam, B.Sc. 2 and David J.A. Jenklns, D.M.I, 2 Department of Nutritional Sciences, Faculty of Medlclne; l Division of Endocrinology and Metabolism, St. Michael's Hospltal; 2 and Women's College Hospital; University of Toronto, Toronto, Ontario, Canada 3 ASRC BTAT To compare the effects of lactose with other carbohydrates on acute blood glucose responses, six diabetic volunteers took breakfast test meals of 38g porridge oats (21g carbohydrate) plus an additional 25g of carbohydrate from either lactose, white bread, sucrose, glucose or fructose. Compared with oats plus bread, the blood glucose responses were increased by 14% (NS) after oats plus glucose, reduced by 1 % 7 (<0.05) after oats plus lactose and decreased by 32% (p < O.Ol) after oats plus fructose. Sucrose and oats gave v i r t u a l l y the same glycemlc response as bread plus oats. The glycemlc indices (GI) of lactose, sucrose, fructose and glucose were calculated to be 69 lO, 91 18, 35 12 and 131 13 respectively with white bread equa111ng l O 0 . The relationship between the GI of the sugars tested here In diabetics with those reported in normal volunteers was significant (r = .g81, p<O.OS). The patients considered sucrose and fructose sweeter than lactose and glucose, but tended to prefer the taste of the less sweet meals. I t is concluded from test meal studies in NIODM that lactose raises the blood glucose level less than an equal amount of bread. The longer term effects remain to be assessed. KEY WORDS: Diabetes, diabetic d i e t , Lactose, Sugars, Blood glucose INTRODUCTION There has been much recent controversy about the place of sugar in the diabetic d i e t (1-9). Thts has resulted tn a statement from the American Diabetes Association that more research is needed on the effects of sugars In the dtabetic d l e t (lO). For many years diabetics have been advised to avoid the consumption of stmple sugars and s u b s t i t u t e complex carbohydrate (1.e. starch) in order to avoid large acute excursions of the blood glucose l e v e l . Thts recommendatlon has extended to foods containing a l l types of sugars, not Just sucrose (11,12). For t h i s reason mtlk has been r e s t r i c t e d because of I t s lactose content (12). Address correspondence to: David J.A. Jenkins, Department of N u t r i t i o n a l Sciences, Faculty of Medicine, U n i v e r s i t y of Toronto, Toronto, Ontario, M5S 1A8 1335

1336

T. W L V R OE E

In view of the desire for lactose containing foods such as ice cream (13) and yoghurt, and the use of high f i b e r breakfast cereals which require m~Ik for p a l a t a b i l i t y , we have compared the blood glucose response of lactose to that of bread and other common sugars In diabetic individuals. W have e also examined the relationship between sweetness and p a l a t a b i l i t y for the sugars, since many diabetic patients desire sweet foods. SUB3ECTS AND M T O S EH D

A group of s i x diabetic volunteers was studied (2 men, 4 women; 63 6 y r ; 145 21% Ideal weight (7); 4 on I n s u l i n , 33 10 units/day; 2 on oral hypoglycemic agents; Table 1). A l l subjects were confirmed as having diabetes by blood glucose concentrations over 11.1 mmol/1 (200 mg/dl) (range 12.1-18.2 mmol/1) 2 hours a f t e r the glucose containing t e s t meal described below. Patients were treated by t h e i r physicians wtth I n s u l i n to control symptoms of diabetes which had persisted a f t e r weight reduction and treatment with d i e t and oral hypoglycemic agents. The patients on I n s u l i n were confirmed as NIDDM on the basis of normal or elevated f a s t i n g l e v e l s (2.4 0.6 pg/ml) and postprandial responses (4.5 0.8 pg/ml: Table 1) of serum C-peptlde (14,15). Fasting and 60 min postprandial s e r u m C-peptide concentrations in a group of 8 normal i n d i v i d u a l s were 1.3 0.1 pg/ml (range 0.62 - 1.g) and 4.8 0.8 pg/ml (range 2.7 - 7.9) r e s p e c t l v e l y . TABLE 1: Patients studied Patient Sex Age ~DW Treatment (See below) 60-62L(a) 25L 5mg Eg. bd 5mgDb. bd 30L 15L
32.8

Years Diabetic 11 2 7 5 20 4
8.2

F.B.G. (mmol/1) 12.8 5.3 6.4 9.3 6.1 8.3

8.0

C-pepttde(pg/ml) Fasting 90min 3.2 1.6 1.1 3.7

2.4

8T KM EH
V8 JH

M F
F

76 61
70

F
M

59
73

AR
Mean SEM

36
63 6

123 116 179 233 120 100

145

3.8 4.6
2.7

6.7
4.5

L = Units Lente Eg. = Euglucon; (a) The changes In carbohydrate

i n s u l i n per day S = Units regular (soluble) i n s u l i n per day; Db. = Dlabeta; tn I n s u l l n dose were not associated with s i g n i f i c a n t changes tolerance: see t e x t .

Volunteers attended the diabetic day care unit of St. Michael's Hospital f a s t i n g one morning a week for the duration of the study (approximately 3 months). After c o l l e c t i n g f a s t i n g f i n g e r - p r i c k c a p i l l a r y blood samples (Autolet lancets, Owen Mumford, Woodstock, England) the patients took t h e i r usual i n s u l i n dose or oral agents and then ate a t e s t meal. Meals were

GY E I RSO S T L CO E L C MC E P N E O A T S

1337

planned to contain 50g carbohydrate, the amount of bread calculated from food tables (16), and the amount of oats from proximate analysts supplied by the manufacturers. The reason that the oats were fed according to the manufacturer's analysis was that these f i g u r e s , even though not including f i b e r , gave more oats per 50g carbohydrate portion (75.4g) than did the figures from the food tables (68.6g) which included a f i g u r e f o r d i e t a r y f i b e r (16). Half the carbohydrate in 5 meals was from hot oatmeal and h a l f was from e i t h e r lactose, white bread, glucose, sucrose, or fructose (Table 2). In a d d i t i o n , the patients took a meal of white bread alone (50g carbohydrate) and a meal of oatmeal alone (50g carbohydrate; Table 2). Test meals were served with a beverage of the p a t i e n t ' s choice (standard for each p a t i e n t ) of one or two cups of water, tea or coffee with or without 30ml of 2 b u t t e r f a t milk per cup. Two patients were given cornflakes (30g per 25g carbohydrate) instead of oatmeal for a l l appropriate meals to t e s t whether the sugar effects were d i f f e r e n t against the background of a higher glycemlc index food. Since no differences were observed, the results were pooled. Duplicate test meals were subsequently analyzed by proximate analysis for carbohydrate, f a t , protein, (17) and d i e t a r y f i b e r by the method of Asp, Furda, and DeVrles (18). Results agreed to w i t h i n l~ of the expected T BE 2 AL Planned composition of test meals Test Meal Uncooked Weight (g) 66.8* 75.4* 37.7* 33.4+ 37.7* 25.0** 37.7* 25.0** 37.7* 25.0** 37.7* 25.0 Protein (g) 7.6 I0.5 9.1 5.3 5.3 5.3 5.3 Fat (g) 0.8 5.4 3.1 2.7 2.7 2.7 2.7 Available Carbohydrate (g) 50.0 50.0 50.0 50.0 50.0 50.0 50.0 Dietary Fiber (g) 2.0 5.3x 3.6x 2.6x 2.6x 2.6x 2.6x

White bread Oats 1/2 Oats plus I/2 White bread 1/2 Oats plus Sucrose I/2 Oats plus Fructose I/2 Oats plus Glucose I/2 Oats plus Lactose

+ Weight of f l o u r . Each loaf of bread containing 334g f l o u r was made with 7g sucrose and 5.5g yeast. * Quaker Quick Oats. Preparation was by the addition of 350ml b o i l i n g water per 37.7g oats, mixing well and allowlng to stand f o r lmin before consumption. ** Sugars were mixed with dry oatmeal before the addition of botltng water. x Dietary f i b e r in oats estimated according to food tables (16).

1338

T. W L V R OE E

a v a i l a b l e carbohydrate content of bread. However, our analysis gave a f i g u r e of 42.2g a v a i l a b l e carbohydrate for the oats which were expected to contain 50g. This was due to the higher concentration of f i b e r estimated by our method of analysis (12.5 0.9% for 8 determinations). All six patients completed all seven test meals. Fifty gram carbohydrate portions of white bread were taken at the beginning and end of the series, and the other 6 meals were fed according to a randomized block design. C a p i l l a r y blood samples were obtained f a s t i n g and at h a l f - h o u r l y I n t e r v a l s for 3h a f t e r the s t a r t of the meal for analysis of glucose by a glucose oxidase method (19). Venous samples for C-peptlde analysis (20) were taken f a s t i n g and 90 min a f t e r the consumption of 50g carbohydrate as bread from those patients taking l n s u l l n . A f t e r f i n i s h i n g each t e s t meal the patients rated i t s p a l a t a b i l i t y on a scale of -3 (very unpleasant) to +3 (very pleasant) and sweetness on a scale of 0 (not at a l l sweet) to 10 (extremely sweet). Results are given as means SEN. The glycemic response areas were calculated geometrically as the incremental area under the blood glucose curve above the f a s t i n g l e v e l according to the following formula: Area = (A30 + A60 + Ago + 4120 + 4150 + 4180/2) x 30 where A30, A60, A90 etc represent the p o s i t i v e differences blood glucose concentration f a s t i n g and at 30, 60, go mtn etc (21,22). This formula was used since for every i n d i v i d u a l t e s t , blood glucose concentration was less than the postprandial l e v e l s
calculated as follows:

between the respectively the f a s t i n g (22).

The glycemtc indices (GX) of the sugars f o r each i n d i v i d u a l subject were GX = Sugar qlycemic response area x 100. White bread glycemtc response area

The sugar and white bread glycemic response areas were calculated by subtracting h a l f the glycemic response area f o r the oats alone t e s t meal from the glycemic response areas for the mixed oats plus sugar and oats plus bread meals. This approach was considered J u s t i f i e d because the mean glycemic response area for the mixed bread and oats m e a l (835 mmol.mln/1) was v i r t u a l l y i d e n t i c a l to the mean of the glycemlc responses f o r bread alone (868 mmol.min/1) and oats alone (806 mmol.mtn/1). The GI values given r e p r e s e n t the mean SER of the i n d i v i d u a l r e s u l t s . S t a t i s t i c a l analysis of the meal blood glucose responses was performed by two-way analysts of variance with Ftsher's t e s t to determine the s i g n i f i c a n c e of the difference between I n d i v i d u a l means (23). In a d d i t i o n , f o r comparisons between the 6I of the sugars and the l I of white bread, students t - t e s t for paired data was used. This gave s i g n i f i c a n t levels for the differences between the GI of the sugars and white bread which were the same as those in the analysis of varlance of the differences in glycemtc areas f o r the respective sugar and bread containing meals.

GLYCEMIC RESPONSETO LACTOSE

1339

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1340

T. W L V R OE E

RS LS E UT The test meals were well received and eaten within the requested time of lO m l n . Dosage of insulin and oral hypoglycemlc agents remained constant throughout the course of the study in 5 of the 6 patients. BT added 2 units lente 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). However this difference was not considered significant because i t was well within the range of v a r i a b i l i t y for the patients on standard treatment whose coefficients of variation of blood glucose area after repeated tests of bread ranged from 2 to 43 % ~. There was no change in mean carbohydrate tolerance over the course of the study as Judged by the repeated 50g carbohydrate bread t e s t meals (mean area under the curve at the s t a r t of the study, 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 lactose and fructose containing meals were s l g n | f l c a n t l y less than that for oats plus bread (Table 3). In addition, the mean blood glucose increments after oats plus fructose were s l g n l f l c a n t l y lower than after bread plus oats at 90, 120, 150, and 180 mln (Figure l ) . Oats plus glucose had a higher glycemlc response area than oats plus bread although the difference did not reach s t a t i s t i c a l significance (Table 3). Glycemlc Index The GI of lactose, sucrose, fructose and respectively, were calculated to be 69 lO, 91 13, with white bread being ascribed the value of and fructose (p < O.Ol) had GIs s i g n i f i c a n t l y below sucrose and glucose were not s i g n i f i c a n t l y different P a l a t l b l l l t y and Sweetness Fructose and sucrose were considered s i g n i f i c a n t l y sweeter than lactose and glucose, which in turn were s i g n i f i c a n t l y sweeter than the meals without sugar (Table 3). Although there were no significant differences, the patients tended to prefer the sweetened meals more than the unsweetened ones. However, amongst the meals containing sugar, they tended to prefer those which tasted less sweet ( i . e . those containing glucose and l a c t o s e ) . DISCUSSION The results suggest that in NIDDM the consumption of lactose produces lower glycemtc excursions than sucrose. T h e y also showed that lactose produced a lower blood glucose response than a f t e r the consumption of an equal amount of carbohydrate taken as white bread. The findings for glucose, sucrose and fructose are in agreement wtth other published data In normal (24) and diabetic subjects (3,5,25). I t seems u n l i k e l y that malabsorptlon of lactose could have contributed to the low glycemlc response slncenone of the patients was i n t o l e r a n t to milk; the amount of lactose given was equivalent to that in 500 ml of milk. glucose, (mean SEM) 18, 35 12 and 131 I00. Lactose (p < 0.05) that of bread. The GI of from that of bread.

GLYCEMIC R S O S TO L C O E EP NE AT S

1341

In addltlon, there were no symptoms of flatulence, diarrhea or abdomlnal bloating or discomfort suggestive of carbohydrate malabsorptlon. There are two reasons l i k e l y for the r e l a t i v e l y f l a t blood glucose response following the consumption of lactose: the slower rate of absorption, and the small hyperglycemic effect of galactose. O n l y 50% of the lactose molecule is glucose, 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 of lactose by intestinal brush border 8-glucosldase (lactase) and absorption of the monosaccharlde components occurs at approximately half the rate of sucrose and maltose hydrolysis and absorption (26). Intravenous and oral boluses of galactose ~n normal subjects have produced small blood glucose and insulin responses, presumably due to ~ts Interconverslon to glucose (27,28).

8
r

1 Time (hr)
FIGURE 1

Mean SEN blood glucose increments of 6 NIDDM patients a f t e r consumption of t e s t meals containing oatmeal plus white bread, glucose, lactose, sucrose and fructose. The s i g n i f i c a n c e of the difference of mean values from the oats plus white bread meal are shown by a s t e r i s k s : *p< 0.05, **p< 0.01. Lactose would thus be expected to have a larger acute glycemic e f f e c t than fructose because of I t s glucose content, but less than sucrose due to i t s slower rate of brush border hydrolysis. This picture was seen here where the glycemic index for lactose (69 lO) was midway between that for

1342

T. W L V R OE E

sucrose (91 18) and fructose (35 12). The longer term e f f e c t s of the consumption of moderate amounts of lactose, or of other sugars, on blood glucose control ~n diabetes remains to be c l a r i f i e d . While there has been conslderable a t t e n t i o n paid to the short term effects of sucrose on blood l i p i d l e v e l s , there has been l i t t l e work done with respect to lactose. Fermented milk has b e e n suggested to be hypocholesterolemic possibly due to i t s lactose content (29). Nevertheless, tn a recent study, consumption of 1 l i t e r of 2% mtlk (containing S2g of lactose) per day for 3 weeks had no e f f e c t on serum cholesterol or t r l g l y c e r ~ d e concentrations in 68 healthy volunteers (30). In an early study, when lactose replaced glucose In the formula dtets of mental hospital p a t i e n t s , there was no r i s e seen In blood 11plds, although a r i s e dld occur when sucrose replaced glucose (31). More work w t l l be needed to determine the long term effects of lactose on blood 11plds, p a r t i c u l a r l y as compared with starchy foods. Sucrose, glucose and fructose are a v a i l a b l e as n u t r i t i v e seeetners. Lactose has not been used for t h i s purpose because of i t s less sweet t a s t e , as was confirmed here where i t had a s i g n i f i c a n t l y lower sweetness rating than e i t h e r sucrose or fructose. Nevertheless i t was considered palatable, while the large amounts of sucrose and fructose in the t e s t meals were considered excessively sweet. In the present series the sugars were given mixed with oats to reduce t o n l c l t y and mtnJmlse the possibly nauseating sweetness of the sugars taken alone, factors which might i n t e r f e r e with g a s t r i c emptying. I f t h i s had occurred, comparison of the results of sugars with bread would have been difficult. The c a l c u l a t i o n of the glycemic index of the i n d i v i d u a l sugars in t h i s study depends upon the p r o p o r t i o n a l i t y of the glycemic c o n t r i b u t i o n of i n d i v i d u a l foods to the t o t a l blood glucose response of a mixed meal. Such p r o p o r t i o n a l i t y was seen here where the mixed oat and bread meal had a glycemic response midway between oats alone and bread alone. In a d d i t i o n , In a previous study (15), a mixed meal of h a l f bread and h a l f beans taken by 7 NIDDM had a glycemlc index of 60, close to halfway between f u l l bread alone, 100, and f u l l beans alone, 41. This approach has also been shown to be v a l i d for mixed meals containing representative amounts of protein and f a t . In t h i s s i t u a t i o n the GI of mixed t e s t meals reported to have been fed to groups of diabetic subjects were calculated and found to r e l a t e s i g n i f i c a n t l y to the incremental blood glucose responses derived from the reported data ( r = .95, n = 5) (32). The G1 of the four sugars calculated in t h i s way were In good agreement with the glycemtc tndlces In normal i n d i v i d u a l s (24) (adjusted so that white bread equals 100) of m i l k , 49; sucrose, 86; fructose, 29; and glucose, 145
(r = 0.981; p<O.O5).

I t ls concluded that lactose raises the blood glucose level acutely following a meal to a lesser extent than an equal amount of bread. The long term effects of lactose tn the diabetic d i e t require f u r t h e r study.

GY E I RSO S T L CO E L C HC E P N E O A T S

1343

Acknowledgements: These studies were supported by the Natural Sciences and Engineering Research Council of Canada and by the Quaker Oats Company, Barrlngton, I l l . RFRN E EE E C S

l) 2)

Lenner RA. Speclally designed sweetners and foods for real need Am. 3. Clln. Nutr. 1976;29:726-733. goods HF, Bax NOS. 1982;23:213-215. Sweetness in the diabetic diet.

diabetics

Dlabeto]ogla

3)

Crapo PA, Scarlett 3A, Kolterman OG. Comparison of the metabolic responses to fructose and sucrose sweetened foods. Am. 3. Cltn. Nutr. 1982;36:256-261. Crapo PA, 01efsky JR. 1983;309:44-45. Food f a l l a c i e s and blood sugar. New Eng. 3. Red.

4) 5)

Bantle 3P, Lalne DC, Castle GN, Thomas 3W, Hoogwerf B3, Goetz FC. Postprandial glucose and i n s u l i n responses to meals containing d i f f e r e n t carbohydrates in normal and diabetic subjects. New Engl. 3. Red. 1983;309:7-12. Nuttal FQ. Diet and the diabetic p a t i e n t . Diabetes Care 1983;6:197-207.

6)

7)

Nathan DR, Godlne 3E, Ganthler-Kelly C, Kawahara D, Grinvalsky M. Ice cream in the dlet of lnsulln-dependent diabetic patients. 3. Am. Red. Assoc. 1984;251:2825-2827. Jenkins DJA. Dietary carbohydrates and t h e i r Am. Med. Assoc. 1984;251:2829-2831. glycemlc responses. 3.

8)

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3enklns D3A, golever TMS, Jenkins AL, 3osse RG, gong GS. response to carbohydrate foods. Lancet 1984;2:388-391. Glycemlc Effects of Carbohydrates, Policy Association, Diabetes Care 1984;47:607-8.

The glycaemlc

Statement, American Diabetes

The N u t r i t i o n Sub-Committee of the B r i t i s h Diabetic Association's Medical Advisory Committee. Dietary recommendations for diabetics for the 1980's a policy statement by the B r i t i s h Diabetic Association. Hum. Nutr. App. Nutr. 1982;36A:378-394. Special Report Committee: Guidelines for the n u t r i t i o n a l management of diabetes m e l l l t u s : a spectal report from the Canadian Diabetes Association. 3. Can. Oletet. Assoc. 1981;42:110-118. Diem K, Lentner C. Documenta Getgy S c i e n t l f t c Basle, Switzerland, 1790. Tables. 3R Gelgy SA,

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Block MB, Mako ME, Stelner OF, Rubensteln AH. Circulating c-peptlde Immunoreactlvlty: studies in normals and diabetic patients. Diabetes 1972;21:I013-1026. Jenklns DJA, Wolever TMS, Wong GS, Kenshole A, Josse RG, Thompson LU, Lam KY. Glycemlc responses to foods: possible differences between Insulln-dependent and non-lnsulln-dependent diabetics. Am. J. Clln. Nutr. 1984;40:971-781. Paul AA, Southgate DAT. McCance and Wlddowson's The Composition of Foods. Medical Research Council Special Report Series nO. 297. 4th Edition, London: HMSO, 1978. AOAC Official Methods of Analysis. Chemists, Washington DC, 1980. Association of Official Analytical

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Protsky L, Asp N-G, Furda I, DeVrtes JW, Schwelger TF, Harland BF. Determination of t o t a l dietary f i b e r in foods and food products, c o l l a b o r a t i v e study: Presented at 98th Annual International Meeting of the Association of O f f i c i a l A g r i c u l t u r a l Chemists, Oct. 29-Nov.2, 1984, Washington, D.C. Clark LC Jr. A polarographlc enzyme electrode for the measurement of oxidase substrates. In: Kessler M, Bruley DF, Leland CC, Lubbers ON, S i l v e r [A, Strass J. (Eds). Oxygen supply. Urban and Schwarzenberg, Munich, 1977, 120-128. Kuzya T, Matsuda A, Salto T, Yoshtda S. Human c-peptide lmmunoreactlvtty (CPR) in blood and urine: evaluation of a radloimmuno-assay method and l t s c l t n i c a l applications. Dlabetologla 1976;12:511-518. Jenkins DJA, Wolever TMS, Jenkins AL, Thorne MO, Lee R, Kalmusky 3, Relchert R, Wong GS. The glycaemic index of foods tested in diabetic patients: a new basis for carbohydrate exchange favouring the use of legumes. Olabetologia 1983;24:257-264. Wolever TMS, Jenkins DOA. The use of the glycemlc index In predicting the blood glucose response to mixed meals. Am. 3. Clln. Nutr. 1985: in press. Snedecor GW, Cochran WG. u n i v e r s i t y Press, 1980. Statistical Methods. 7th Edition. Iowa State

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Ganda OP, Soeldner JS, Gleason RE, Cleator IGM, Reynolds C. Metabolic effects of glucose, mannose, galactose, and fructose % man. 3. Clin. n Endocrinol. Metab. 1979;49:616-623. Ross SA, Dupre J. Effects of %ngestion of tr%glycer%de or galactose on secretion of gastric %nhibltory polypept%de and on responses to intravenous glucose In normal and diabetic subjects. Diabetes

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31) 32)

Accepted for publication October 29, 1985.