Effect of Dietary Carbohydrate on the Glucose Tolerance Curve in the Normal and the Carbohydrate-Induced Hyperlipemic Subjectt

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1 fito: AMERICAN JOURNAL OF CLINICAL NuTRITIoN VI. 20, N. 2, I ebruary, 1967, pp I rinted in (.S.:l Effect of Dietary Carbohydrate on the Glucose Tolerance Curve in the Normal and the Carbohydrate-Induced Hyperlipemic Subjectt A. M. COHEN, M.D. -1 JfOST OF THE PREVIOUS PAPERS related.lvi to the effect on the body lipid of i 0 tercha nging the ary carbohydrate from starch to sucrose. The sutbject of the presciit paper is on a different aspect of this ttietary change on the body metabolism, nanielv, the glucose tolerance, which iiiay to niy mind, be the underlying cautse foi the changes observed in the lipid metabolism. in a diabetic survey we found that Yemenite Jews have a very low preyalence of diabetes during the first years aftei their arrival in Israel; however Yemenite Jews residing in the country for 25 years or more have manifested the disease with a considerably higher frequency, comparably as high as among immigrants from Western countries (1). In a ary survey made among the Yemenite Jews (newcomers anti old settlers) the main change in the has been the diminished consuimption of and increased intake of sugal- by die old settlers (2). The glucose tolerance of the organism can be affected by previous states of nittrition (3-5). We have fed rats (6) on fully supplied s of vitamins and proteins bitt changed the type of carbohydrate, starch versus sucrose. After feeding this 1 From the Departments of Medicine B and A and the Isotope Laboratory for Endocrine Research of the 1-1adassah - Hebrew University 1-lospi tal and Medical School, Jerusalem, Israel. we examined the glucose tolerance at (hifferent periods and found that noticeable i Ii1J)dirmen t of glutcose tolerance occurs only after 4-6 is eeks; it becomes statisticall) significant between the 6th to the 8th week. The follos ing (lata show the effect on the glucose tolerance in the noriiial huiiian voltili teers, anti itti one carbohydrate-induiced hyperlipemic sutbject. The experiment involved the intake of bieati or sucrose as the iiiaiii source of carbohydrate in the low fat (tiet. METHODS Sixteen adult hitli1an VoltiliteerS, 6 niates and I 0 females, were the subjects. Their health was ascertained by their history and physical examination. During the control period before the experiment started. OliC male was found to suffer from essential hyperlipemia and his rcstilts are reported separately. The volunteers were first placed on a utniform high fat Western type. After a period of 5 weeks on this, the volunteers were split into two groups: a) A group of 2 males and 6 females switched from the Western thiet to a low in fat in which furnished 60% of the total calories. This was achieved by an intake of g of per day. Sucrose was withheld from the volunteers in this group. h) A group of 3 males and 4 females switched from the Western to a low fat in which IiiO5t of the carbohvtlrate was furnished b sucrose. For this purpose the volunteers had to 126

2 1) ietary Carbohydrate and Gluicose Tolerance 127 I Average Composition of the Diets Consumed, g/day Fat Carbohydrates Diet Calories I Mono- Total Pola SFA5 Total saccharide Poly: disac- and charide Protein 1, sugar Polyunsaturated fatty acids. Saturated fatty acids. II Average Composition of the Diets Consumed by the Subject with Essential Hypertriglyceridemia Carbohydrate Fat Period Diet Calories Total PoIysacc. Monoand disacch. Total Pota SFA5 Protein 12/17/63-1/3/64 Western (high fat) 2, /14/64-2/17/64 2, /18/64-3/23/64 sugar 2, /24/64-4/21/64 Western (high fat) 2, #{176}Polyunsaturated fatty acids. ii Saturated fatty acids. eat at least 100 g of sucrose; 50 g of jam or marmalade and 30 g of sweet candy per day. Their intake was limited to a maximum of 150 g per day. The thiets were otherwise made as equal as possible, but because of the high protein content of, compared to sucrose, it was unavoidable that the protein (especially the vegetable protein) intake on A was higher than on B. To compensate on B, lebben (soured skimmed milk) was given as an extra source of protein. After 5 weeks the s of the two groups were interchanged. The volunteers of grout A who had been eating the high now switched over to the high sugar and vice versa. Table I gives the analyses of the experimental s as actually consumed by the normal volunteers and Table II the analysis of the consumed by the hyperlipemic subject. It will be seen that whereas we succeeded in keeping the average amount of calories about the same (about 2,000/24 hr) on both s, the. high sugar contained on the average more carbohydrate and less protein; the fat content was equally low (42 g, 19 cal/loo g) on both s. The blood sugar was measured by the Somogyi-Nelson method (8). RESULTS Table iii shows the average body weight of the s-olunteers at the end of each experimental period. It is apparent that there was no significant change in body weight during the different experimental ing periods. The average fasting blood glucose value of the normal volunteers at the end of the first period on the Western high fat was 88 mg/l00 ml. Table IV gives the averages of the glucose tolerance curves which were obtained at that stage, i.e., before the

3 128 Cohen III Average Body \Veight and Standard Error of the Volunteers During the Different Dieting Periods, in kg Diet Western sugar Group A 62.9 ± ± 2.96l.6 ± 2.8 Group B 68.9 ± 4.l68.7 ± ± 4.1 but there appears to be a marked difference in the individual adaptability of the glucose tolerance to the type of. In the patient with hyperglyceridemia, the glutcose tolerance curve rose on the \\Testern to I 70 mg/ 100 mg after 30 mm, and it did not return to the fasting value after 150 mm. On the the curve became completely normal; on the sugar the abnormality reappeared (Fig. 1). DI5CU55ION Glucose Tolerance Curves in the Two Groups of Volunteers Before they Started on Their Experimental Diets (Blood Glucose, mg/loo Iv trig) Group Fasting 30 mm 60 mm 90 mm 120 mm 130 mm A 87±l44±l24±ll5±l09±99± 3.9#{176} B 88 ±351 ±l30 ±l20 ±113 ± 98 ± #{176}Mean ± SE volunteers split into the groups A and B. There was no significant difference between the glucose tolerance curves in the two groups immediately before they started on their different s. Table v summarizes the averages and standard error of the blood sugar curves of the normal volunteers during the last week of the different ary periods. It will be seen that the average sugar tolerance curve at the end of the high sugar was slightly higher than after 4 weeks on the Western, but the differences were small and not significant. In contrast the average glucose tolerance curve obtained after the volunteers had been eating the high for 4 weeks was consistently lower than that on the \ Vestern and on the sugar and the differences between the last two were statistically significant. The individual sugar tolerance curves show the same tendency, P sugar Difference a Values are means ± SE Difference between the means of the blood glucose values at corresponding points of the tolerance curves on the high sugar and the high In general the blood sugar tolerance curves on the high -low fat were significantly lower in the normal and the hyperlipemic subject than on either the high sugar-low fat or Western, although there was a considerable difference in the individual responses of the volunteers. Himsworth (1) showeti many years ago that previous consumption of a high carbohydrate improves glucose tolerance. However, he did not study the effect of the nature of the carbohydrate on this improvement. In the present experiment the total carbohydrate intake remained. Glucose Tolerance Curves cf the Volutnteel-s at the End of the \Vestern I)iet, the Sugar Diet, and Bread Diet (Blood Glucose, mg/100 mg) Diet Fasting 30 mm 60 mm 90 mm 120 mm 150 mm Western 88 ± 149 ±127 ±ll8 ±1112 ± 99 ± V 4.0#{176} ±l49 ± 134 ±l27 ± 120 ± 98 ± ±126±114±104±1100± 88± NS

4 Dietary Carbohydrate and Glucose Tolerance 129 hugh during the whole experiment and, therefore, the amoutnt of ary carbohiydrate could not account for the improved glucose tolerance duiring the period and the impairment during the sucrose I)e1i0(I. The animal experiments of Cohen and Teitelbauim (6) point concluisively to the i ole of starch as the factor responsible for the lower blood sugar curve in the, as compared to the sugar,. A completely comparable difference in glucose tolerance in our volunteers (normal and hyperhipemic) was shown to exist in rats fed either sucrose or starch as the main carbohydrate in their. Regarding the metabolic mechanism is hich is responsible for the difference in glucose tolerance on the tlifferent s, it seems most likely that the more rapid inflow of glucose into the circulation on a sutcrose stimulates the glucose storage system acut tely and intermittently, whereas thie slowly digested starch produces less intense and more prolonged stimutlation of that system anti thus produces a better adaptation to a glucose load. Whether this better adaptation consists in a hiigher secretion of insulin or a greatei- sensitivity to the hormone of the glucose storage system has not been decided with certainty. Parallel with the higher sugar tolerance curve on the highi sugar, there was also a higher cholesterol content in the serum. The relation of this impaire(i gillcose tolerance to the higher cholesterol observed during the sucrose feeding pei-iod is not clear. Whether these two phenomena are related or are due to two different and independent mechanisms, bothi resulting from the suicrose feeding, is at present undecided. The improved glucose tolerance during the period, together with the drop of blood cholesterol in the normal volunteers, and more dramatically in the hyperlipemic patients inthicates a close relationship between carbohydrate and lipid metabolism. It suggests EFFECT OF THE DIFFERENT DIETS ON THE Cholesterol mg % o_#{149} Glucose mg% BLOOD CHOLESTEROL, TRIGLYCERIDES AND WESTERN GLUCOSE TOLERANCE BREAD SUGAR mg% Oral Glucose Tolerance at the end of the periods: BREAD SUGAR FIG. 1 Trig Lycerides AVERAGE GLUCOSE TOLERANCE (1gm per 100gm body weight) BY TYPE OF DIET Gse ioof.- i:crease WESTERN 150 j\ / h,0, 100; / 0 o Time in minutes ::L, X:,::::-::::: ::.:::: Minutes Fic. 2 that both may be affected by thie nature of the ingested carbohydrate. In rats on highi sitcrose s fed ad libituim, reducing the ary protein from 18 to 11% (protein replaced by increasing sucrose from 72 to 79%) enhances the impairment of the glucose tolerance caused by sucrose (Fig. 2). On re(lutcing the ary protein from 18 to 11% (with corresponding substitution of the protein by ary carbohydrate) weight gain was more inhibiteti in C

5 130 Cohen animals on high sucrose than on high starch s (7). SUMMARY If sucrose is fed long enough and in appropriate quantities one can produce in either man or rat an impairment to the glucose tolerance. This response may be the background for the change in lipid metabolism observed in the sucrose-fed individuals, normal or hyperlipemic. Changing other ary factors, such as the quantity of ary protein or fat, may influence this impairment. Although this impairment is statistically significant in a group, individual variations are marked, and constitutional factors-enzymatic or hormonal-are to be considered in the response of the individual to this change. REFERENCES I. COHEN, A. M. Metab. Clin. Exptl. 10: 50, COHEN, A. M., S. BAVLY AND R. POSNANSKI. Lancet 2: 1399, BERNARD, C. Le#{231}onstir le diabete Ct la glycogenese animal. Paris: Bailliere, 1877, p Hntswoit rii, N. P. Clin. Sci. 1: 1, URAM, J. A., L. FRIEDMAN AND 0. L. KLINE. Am. I. Physiol. 192: 521, COHEN, A. M., AND A. TEITELBAUM. Am. 1. Physiol. 206: 105, COHEN, A. M., AND A. TEITELBAUM. Metab. Clin. Exptl. 15: 1034, NELSON, N. J. Biol. Chens. 153: 375, 1953.