An insulinindex of foods:the insulindemand generatedby

1000-kJ portions of common foods13

Susanne HA Holt, Janette C Brand Miller, and Peter Petocz

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ABSTRACT The aim of this study was to systematically sification of the relative insulinemic effects of different foods
compare postprandial insulin responses to isoenergetic 1000-U is of both theoretical and practical significance.
(240-kcal) portions of several common foods. Correlations with Postprandial blood glucose responses have been the focus of
nutrient content were determined. Thirty-eight foods separated into much research because of their importance for glycemic con
six food categories (fruit, bakery products, snacks, carbohydrate trol in patients with diabetes. It is now well accepted that
rich foods, protein-rich foods, and breakfast cereals) were fed to different foods containing equal amounts of carbohydrate can
groups of 11—13healthy subjects. Finger-prick blood samples were produce a wide range of blood glucose responses. The glyce
obtained every 15 mm over 120 mm. An insulin score was calcu mic index (GI) method was developed to rank foods according
lated from the area under the insulin response curve for each food to the extent to which they increase blood glucose concentra
with use of white bread as the reference food (score = 100%). tions (18). Tables of GI values of common carbohydrate
Significant differences in insulin score were found both within and containing foods are a useful guide to help people with diabetes
among the food categories and also among foods containing a choose foods that produce smaller glycemic responses. How
similar amount of carbohydrate. Overall, glucose and insulin ever, the GI concept does not consider concurrent insulin
scores were highly correlated (r = 0.70, P < 0.001, n = 38). responses and few studies have reported GI values and their
However, protein-rich foods and bakery products (rich in fat and accompanying insulin responses.
refined carbohydrate) elicited insulin responses that were dispro The extent to which different dietary factors affect post
portionately higher than their glycemic responses. Total carbohy prandial insulinemia has not been well researched because
drate (r = 0.39, P < 0.05, n = 36) and sugar (r = 0.36, P < 0.05, insulin secretion is largely assumed to be proportional to
n = 36) contents were positively related to the mean insulin scores, postprandial glycemia. Furthermore, hyperglycemia is
whereas fat (r —¿0.27,NS, n 36) and protein (r —¿0.24, NS, thought to be more relevant to the secondary complications
n = 38) contents were negatively related. Consideration of insulin of NIDDM because the abnormal insulin secretion or action
scores may be relevant to the dietary management and pathogen in people with diabetes is controlled with exogenous insulin
esis of non-insulin-dependent diabetes mellitus and hyperlipidemia or medications that counteract insulin resistance. However,
and may help increase the accuracy of estimating preprandial knowledge of factors that influence both postprandial gly
insulin requirements. Am J Clin Nutr l997;66:l264—76. cemia and insulin secretion in nondiabetic persons is re
quired to devise treatment strategies that will completely
KEY WORDS Insulin, glycemic index, NIDDM, non normalize meal-related glycemia (19).
insulin-dependent diabetes meffitus, diabetic diet, hyperlipid To explore the importance of dietary habits and postprandial
emia, carbohydrate, insulin score, glucose score, area under the insulinemia in the etiology and treatment of NIDDM, we need
curve, humans to be able to systematically rate insulin responses to common
foods. If we are to compare insulin responses to foods, what is
the best basis of comparison? Should we compare insulin
responses to portions of food representing a normal serving
INTRODUCTION size, portions containing an equal amount of carbohydrate, or
portions containing an equal amount of energy? 01 tables
The insulinemic effects of foods may be relevant to the
represent the glycemic effects of equal-carbohydrate portions
treatment and prevention of weight gain, non-insulin-depen
dent diabetes mellitus (NIDDM), and associated complications.
Recent studies have shown that carbohydrate-rich diets, which I From the Human Nutrition Unit, Department of Biochemistry, The

result in high postprandial glucose and insulin responses, are University of Sydney; and the School of Mathematical Sciences, The
associated with undesirable lipid profiles (1, 2), greater body University of Technology, Sydney, Australia.
2 Supported by research grants from The University of Sydney and
fat (3—5),and the development of insulin resistance in rats (6)
Kellogg's Australia Pty Ltd.
and humans (7, 8). Both obesity and NJDDM are associated 3 Address reprint requests to JC Brand Miller, Human Nutrition Unit,
with varying degrees of insulin resistance and fasting hyperin Department of Biochemistry 008, The University of Sydney, NSW 2006,
sulinemia. Prolonged or high degrees of postprandial insuline Australia.
mia are thought to contribute to the development of insulin Received November 21, 1996.
resistance and associated diseases (9—17).Therefore, the clas Accepted for publication May 22, 1997.

1264 Am J Clin Nutr 1997;66:1264—76. Printed in USA. ©1997 American Society for Clinical Nutrition
 INSULIN INDEX OF FOODS 1265
TABLE!
Descriptionand preparationof the test foods
Food Variety, manufacturer, or place of purchase Preparation
Fruit
Black grapes Waltham cross Fresh, stem removed, served whole
Apples Red delicious Fresh, unpeeled, cut into eight segments
Oranges Navel Fresh, peeled, cut into eight segments
Bananas Cavendish Fresh, peeled, cut into quarters
Bakery products
Croissants Purchased in bulk from supermarket and stored frozen Defrosted, reheated at 180 °Cfor 6 mm, and served warm
Chocolate cake with White Wings Foods, Smithfield, Sydney, Australia Prepared according to manufacturer's directions, stored at
frosting 4 °Cup to 2 d before serving at room temperature

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Doughnuts with cinnamon Purchased in bulk from supermarket and stored frozen Prepared by supermarket from standard recipe, defrosted
sugar overnight, reheated at 180 °Cfor 5 mm, and served
warm
Chocolate chip cookies Anion's Biscuits Ltd. Homebush, Sydney, Australia Served crisp at room temperature, stored in airtight
container
Water crackers Grocery Wholesalers Ltd, Yennora, Australia Served crisp at room temperature
Snack foods and confectionery
Mars Bar Mars Confectionary Australia, Ballarat, Australia Cut into four standard pieces and served at room
temperature
Yogurt Strawberry fruit yogurt; Australian Co-operative Stored at 4 °C,served cold
Foods,' Wetherill Park, Sydney, Australia
Ice cream Vanilla ice cream; Dairy Bell, Camperdown, Sydney, Stored frozen and served cold
Australia
Jellybeans (assorted colors) Grocery Wholesalers Ltd Served at room temperature, stored in airtight container
Peanuts Salted roasted peanuts; Grocery Wholesalers Ltd Served at room temperature, stored in airtight container
Potato chips Crinkle cut chips; Smith's Snackfood Company, Served from freshly opened packet
Chatswood, Sydney, Australia
Popcorn Microwave cooked popcorn; Uncle Toby's Company Prepared according to manufacturer's directions
Ltd, Wahgunyah, Australia immediately before serving
Protein-rich foods
Cheese Mature cheddar cheese; Grocery Wholesalers Ltd All servings cut from same large block, stored at 4 °C,
served cold
Eggs Poached hens eggs Poached the day before serving, stored at 4 °Covernight,
reheatedin microwaveoven for 1.5mm immediately
before serving
Lentils Served in tomato sauce2 Prepared in bulk according to recipe, stored at 4 °Cfor up
to 2 d, reheated in a microwave oven for 2 mm
immediatelybeforeserving
Baked beans Canned navy beans in tomato sauce; Franklins, Heated on stove for 5 mm immediately before serving
Chullora, Sydney, Australia
Beef steak Lean topside beef fillets bought in bulk from Grilled the day before serving, cut into standard bite-sized
supermarket, trimmed and stored frozen pieces, and stored at 4 °Covernight; reheated in
microwave oven for 2 mm immediately before serving
White fish Ling fish ifilets bought in bulk from Sydney fish Steamed the day before serving, stored at 4 °Covernight,
markets, trimmed and stored frozen cut into bite-sized pieces, and reheated in microwave
oven for 2 miii immediately before serving
Carbohydrate-rich foods
White bread Fresh sliced wheat-flour bread; Quality Bakers Served fresh and plain at room temperature
Australia Ltd. Eastwood, Sydney, Australia
Whole-meal bread Fresh sliced bread made from whole-meal wheat flour; Served fresh and plain at room temperature
Riga Bakeries, Moorebank, Sydney, Australia
Grain bread Fresh sliced rye bread containing 47% kibbled rye; Tip Served fresh and plain at room temperature
Top Bakeries,Chatswood,Sydney,Australia
White rice Cairose rice (Sunwhite), Ricegrowers' Co-operative Boiled 12 miii and stored overnight at 4 °C,reheated in
Ltd. Leeton, Australia microwave oven for 1.5 mm immediately before serving
Brown rice Calrose rice (Sunbrown), Ricegrowers' Co-operative Boiled 12 mm and stored overnight at 4 °C,reheated in
Ltd microwave oven for 1.5 mm immediately before serving
White pasta Spirals Boiled8 mm and storedovernightat 4 °C
Brown pasta Whole-meal spirals; San Remo Pasta Company, Reheated in microwave oven for 1.5 mm immediately
Auburn, Sydney, Australia before serving
Potatoes Russet potatoes Peeled,boiledfor 20 mm, and storedat 4 °C
overnight;
reheated in a microwave oven for 2 mm immediately
before serving
1266 HOLT ET AL
TABLE 1
Continued

purchasePreparationFrench
FoodVariety, manufacturer, or place of
friesPrefried oven-baked French fries; McCain's Foods frozen, cooked in conventional oven for 15 mm
servingBreakfast (Australia), Castle Hill, Sydney, AustraliaStored immediately before
cereals3CornflakesKellogg's
Australia Pty Ltd, Pagewood, Sydney,
Australia—Special
KToasted flakes made from wheat and rice flour, high in
Ltd—HoneysmacksPuffed protein; Kellogg's Australia Ply
whole-wheat grains with a honey-based coating;
Ltd—SustainA Kellogg's Australia Ply

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mixture of wheat, corn, and rice flakes; rolled oats;
dried fruit; and flaked almonds; Kellogg's Australia
Ltd—All-BranA Pty
high-fiber cereal made from wheat bran; Kellogg's
Ltd—Natural Australia Pty
muesliBased on raw rolled oats, wheat bran, dried fruit, nuts,
and sunflower seeds; Uncle Toby's Company Ltd.
Australia—PorridgeUncle Wahgunyah,
Toby's Company Ltd. Wahgunyah, AustraliaRaw rolled oats cooked in a microwave oven according to
manufacturer's directions and served without sweetener
1 Now Dairy Farmer's.
2 Recipe: 15 mL olive oil, 350 g dried green lentils, 410 g canned tomatoes, 120 g onion, 1 clove garlic, and 1 tsp pepper.

3 All cereals were served fresh with 125 mL fat-reduced (1.5% fat) milk.

of foods.However,carbohydrateis not the only stimulusfor 2) bakery products: croissants, chocolate cake with icing,
insulin secretion. Protein-rich foods or the addition of protein doughnuts with cinnamon sugar, chocolate chip cookies, and
to a carbohydrate-rich meal can stimulate a modest rise in water crackers; 3) snack foods and confectionery: Mars Bar
insulin secretion without increasing blood glucose concentra candy bar (Mars Confectionary Australia, Ballarat, Australia),
tions, particularly in subjects with diabetes (20—22).Similarly, strawberry yogurt, vanilla ice cream, jellybeans, salted roasted
adding a large amount of fat to a carbohydrate-rich meal peanuts, plain potato chips, and plain popcorn; 4) protein-rich
increases insulin secretion even though plasma glucose re foods: cheddar cheese, poached eggs, boiled lentils in a tomato
sponses are reduced (23, 24). sauce, baked beans in a tomato sauce, grilled beef steak, and
Thus, postprandial insulin responses are not always propor steamed white fish; 5) carbohydrate-rich foods: white bread,
tional to blood glucose concentrations or to a meal's total whole-meal bread, rye-grain bread, white rice, brown rice,
carbohydrate content. Several insulinotropic factors are known white pasta, brown pasta, boiled potatoes, and oven-baked
to potentiate the stimulatory effect of glucose and mediate French fries; and 6) breakfast cereals: Cornflakes (Kellogg's
postprandial insulin secretion. These include fructose, certain Australia Pty Ltd. Pagewood, Australia), Special K (Kellogg's
amino acids and fatty acids, and gastrointestinal hormones such Australia Pty Ltd), Honeysmacks (Kellogg's Australia Pty
as gastric inhibitory peptide, glucagon, and cholecystokiin Ltd), Sustain (Kellogg's Australia Pty Ltd), All-Bran
(25, 26). Thus, protein- and fat-rich foods may induce substan (Kellogg's Australia Pty Ltd), natural muesli, and oatmeal
tial insulin secretion despite producing relatively small blood porridge.
glucose responses. We therefore decided that comparing the Each food was served plain as a 1000-U portion with 220
insulinemic effects of foods on an isoenergetic basis was a mL water. White bread was used as the reference food for each
logical and practical approach. food group. The foods were selected to represent a range of
The aim of this study was to systematically compare post natural and processed foods commonly eaten in industrialized
prandial insulin responses to isoenergetic portions of a range of societies. Details of the foods and their preparation methods are
common foods. An insulin score (IS) was calculated for each listed in Table 1. Foods were bought in bulk to minimize
food on the basis of its insulinemic effect relative to a reference variations in composition and were served in standard-sized
food. Thirty-eight foods, categorized into six different food pieces. The nutritional composition ofeach food per 1000 U as
groups, were studied to determine which foods within the same calculated from Australian food tables or manufacturers' data
food group were most insulinogenic. We hypothesized that is shown in Table 2.
postprandial insulin responses are not closely related to the
carbohydrate content or glycemic effects of some foods. Subjects
Separate groups of healthy subjects (n = 11—13)were re
SUBJECTS AND METHODS cruited to test each category of foods. Volunteers were ex
cluded if they were smokers or taking prescription medications,
Test foods had a family history of diabetes or obesity, were dieting, or had
Thirty-eight foods were tested and were grouped into six irregular eating habits. In total, 41 subjects participated. One
food categories: 1) fruit: grapes, bananas, apples, and oranges; subject consumed all of the test foods and 15 other subjects
 INSULIN INDEX OF FOODS 1267
TABLE 2
Nuthtional composition of the test foods per 1000-U serving as calculated from Australian food tables or manufacturers' data'

ServingCarbohydrateEnergyFood
weight FatProtein SugarStarch FiberWater density
k@I/gFruitGrapes3950.43.256.90.03.6317.02.5Bananas2790.34.747.28.46.1210.13.6Apples4350.01.356.52.29.1360.92.3Oranges6250.66.950.60.012.5539.41.6Bakery
g g g g g g

productsCroissants6114.46.13.118.61.813.516.4Cake26411.94.320.110.50.710.715.6Doughnuts6513.44.38.917.01.416.115.4Cookies25110.92.418.716.21.02.119.6Crack

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confectioneryMars
and
Barr549.42.936.71.11.73.518.5Yogurt@2415.311.837.60.00.5187.04.2Ice

cream12013.45.225.80.00.074.28.3Jellybeans880.05.344.611.50.012.211.4Peanuts3820.19.61.73.72.40.626.3Potatochips24416.22.70.222.12.41.122.7Popc

foodsCheese5920.015.00.10.00.020.916.9Eggs15917.919.60.50.00.0119.46.3Lentils2534.619.44.224.91

1.4222.03.9Baked
beans3511.716.116.123.216.8267.12.8Beef
steak1587.742.00.00.00.0104.36.3Fish3331.056.30.00.00.0250.03.0Carbohydrate-rich

foodsWhite
bread2942.18.51.844.13.336.110.6Whole-meal
bread21012.67.61.743.76.640.39.9Grain
bread21085.49.42.437.66.541.49.3White
rice22030.55.00.156.00.4140.04.9Brown
rice21482.15.20.552.61.493.96.8White
pasta2010.87.82.047.13.5134.85.0Brown
pasta22181.611.30.747.810.9132.64.6Potatoes3681.010.03.145.99.2290.82.7French

fries2938.73.91.135.43.533.810.7Breakfast
cerealsCornflakes21702.18.410.236.11.5110.95.9Special

K21722.115.314.027.21.4111.25.8Honeysmacks21722.28.731.117.02.61
15.05.8Sustain21683.19.713.729.13.2119.15.9Muesli21756.110.717.119.86.61

14.15.7Pomdge23836.210.97.529.04.7333.72.6All-Bran21742.911.713.929.414.1111.05.7

I Mars Bar, Mars Confectionary Australia, Ballarat, Australia; Comfiakes, Special K, Honeysmacks, Sustain, and All-Bran: Kellogg's Australia Pty Ltd.
Pagewood, Australia.
2 Nutrient composition calculated from manufacturer's data.

completed two or more food categories. All of the subjects approved by the Medical Ethical Review Committee of the
were university students; relevant characteristics ofthe subjects University of Sydney.
are listed in Table 3. The mean body mass index (BMI, in
kg/m2) of the 41 subjects was 22.7 ±0.4 (range: 19—29).Three P1@Ot(WOl
subjects had a BMI > 25 but two of these were short, stocky Each subject first consumed a 1000-U portion of white bread
males who had excess muscle rather than fat. Female subjects (45.9 g carbohydrate) to confirm normal glucose tolerance.
did not participate during their menstrual period or if they White bread was also used as the reference food (IS = 100%)
experienced adverse premenstrual symptoms. Informed con- against which all other foods were compared, similar to the
sent was obtained from all of the subjects and the study was method used for calculating GI values of foods (18). The use of
1268 HOLT ET AL

TABLE 3 tube radioimmunoassay kit (Coat-A-Count; Diagnostic Prod

Characteristics of each group of subjects' ucts Corporation, Los Angeles). For both plasma glucose and
insulin analysis, all nine plasma samples for a particular sub
groupAgeBMI2yFruit
Food
ject's test were analyzed within the same run to reduce any
error introducedby interassayvariation.When possible,all
(n = 5 F, 6 M)22.9
1.4Bakery ±3.922.9 ± plasma samples for a particular subject were analyzed for
2.7Snacksproducts (n = 6 F, 6 M)22.2 ±3.723.1 ± insulin within the same run. For the insulin analysis, the mean
and confectionery(n = 5 F, 7 M)21.0
3.5Protein-rich ±1.222.9 ±
within-assay CV was 5% and the mean between-assay CV was
foods (n 5 F, 6 M)22.4
3.1Carbohydrate-rich ±2.824.3 ±
7%.
1.9Breakfast foods (n = 5 F, 8 M)21.0 ±1.923.0 ±
cereals (n = 5 F, 6 M)22.8 ±3.922.8 ±1.4
‘¿
I ± SD.
Statistical analysis

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2 In kg/rn2. Cumulative changes in postprandial plasma glucose and
insulin responses for each food were quantified as the incre
a reference food controls for inherent differences between mental area under the 120-mn response curve (AUC), which
individuals that affect insulin sensitivity, such as body weight was calculated by using the trapezoidal rule with fasting con
and activity levels. centrations as the baseline and truncated at zero. Any negative
Subjects were fed 1000-U portions of the test foods in a areas tended to be small and were ignored. For each subject, an
random order on separate mornings after a 10-h overnight IS (%) was calculated for each test food by dividing the insulin
fast. Within each food group, each subject acted as his or her AUC value for the test food by the insulin AUC value for white
own control, being tested at the same time of day and under bread (the reference food), and expressed as a percentage as
as similar conditions as possible. Subjects were asked to follows:
refrain from unusual activity and food intake patterns, to
abstain from alcohol and legumes the day before a test, and IS (%)
to eat a similar meal the night before each test. When
subjects arrived at the lab in the morning, they completed a Area under the 120-mm insulin response
short questionnaire assessing recent food intake and activity curve for 1000 U test food
X100 (1)
patterns. A fasting finger-prick blood sample was collected Area under the 120-mminsulinresponsecurve
and subjects were then given a test food and 220 mL water for 1000 Id white bread
(0 mm). When possible, foods were presented under a large
opaque plastic hood with a hole through which volunteers This equation is similar to that developed by Wolever and
pulled out pieces of the test food one at a time. This was an Jenkins (29) for calculating GI values. A glucose score (GS)
attempt to minimize between-subject variation in cephalic (not the same as a GI score, which is based on a 50-g carbo
phase insulin secretion arising from the sensory stimulation hydrate portion) for each food was also calculated by using the
associated with the anticipation and act of eating (27). same equation with the corresponding plasma glucose results.
However, this was not feasible for the liquid foods (yogurt Analysis of variance (ANOVA) and Fisher's probable least
and ice cream), foods served in a sauce (baked beans and significant-difference test for multiple comparisons were used to
lentils), or with milk (all of the breakfast cereals), which determine statistical differences among the foods within each food
were presented in standard bowls without the hood. group (STATVIEW STUDENT SOFFWARE; Abacus Concepts
Subjects were asked to eat and drink at a comfortable rate. mc, Berkley, CA). Linear-regressionanalysis was used to test
Immediately after finishing the test food, subjects recorded the associations between glucose and insulin responses and nutritional
time taken to eat the food and completed a questionnaire indexes (MINITAB DATA ANALYSIS SOFFWARE, version
assessing various appetite responses and the food's palatability. 7.0; Minitab Inc, State College, PA). Test foods not containing a
[These results are reported in a separate paper (28).] Subjects particular nutrient were excluded from these analyses. Therefore,
remained seated at tables in a quiet environment and were not sample sizes for the correlations between individual nutrients and
permitted to eat or drink until the end of the session (120 mm). the mean GSs and ISs varied from 32 to 36. Mean results for white
Finger-prick blood samples (1.5—2.5mL) were collected bread for each food group were included in some statistical anal
from warmed hands immediately before the meal (0 mm) and yses, so these correlations were made with 43 values. One subject
15, 30, 45, 60, 75, 90, 105, and 120 mm after the start of the from the protein-rich food group did not complete the fish test and
meal (into plastic tubes that had been kept on ice) with use of one subject from the breakfast cereal group did not complete the
an automatic lancet device (Autoclix; Boehringer Mannheim Sustain test. Therefore, in total, 503 indiVidUal tests were fully
Australia, Castle Hill, Australia). Blood samples were centri completed.
fuged immediately after collection (1 miii at 12 500 X g at Stepwise-multiple-regression analysis was used to examine
room temperature) and plasma was pipetted into chilled tubes the extent to which the different macronutrients and GSs ac
and immediately stored at —¿20
°Cuntil analyzed (< 1 mo). counted for the variability of the ISs (MINITAB DATA
Plasma glucose concentrations were analyzed in duplicate with ANALYSIS SOFTWARE). For this analysis, the individual
a Cobas Fara automatic spectrophotometric analyzer (Roche white bread OS and IS results were included for the carbohy
Diagnostica, Basel, Switzerland) and the glucose hexokinase drate-rich food group only; therefore, this analysis was per
enzymatic assay. The mean within-assay and between-assay formed with 446 individual observations for 38 foods. Includ
precisions (CVs) were both < 6%. Plasma insulin concentra ing the white bread results for each food group (n = 503)
tions were measured in duplicate by using an antibody-coated suggests that independent repeat tests were done for white
 INSULIN INDEX OF FOODS 1269
TABLE 4
Areas under the 120-mm plasma glucose and insulin response curves (AUCs), ratio of insulin AUC to glucose AUC, the insulin AUC per g
carbohydrate and per g serving weight, and mean glucose and insulin scores'

Food Glucose AUCInsulin AUCInsulin AUC: AUC per g AUC per g

scoremol-miniLpmolmin/LpmolminL'g'pmolminL'g'%%
glucose AUCInsulin carbohydrateInsulin serving weightGlucose scoreInsulin

Breakfast
cerealsWhitebread156±2113557±1756108±19295±38144±19100±0100±0All-Bran59

4Porridge80 ±94299 ±61287 ±1599 ±1425 ±340 ±732 ±

±95093 ±49374
4Muesli65±126034±813118±18163±2234±543±746±5Special ±11139 ±1313 ±I60 ±1240 ±

K106 ±148038 ±63595 ±14195 ±1547 ±470

5Honeysmacks91±109102±1506108±12189±3153±960±767±6Sustain93±88938±757102±9209±1853±466±671±6Cornflakes1
±966 ±

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8Groupmean—7183±35792±5169±839±259±357±3Carbohydrate-rich
10 ±118768 ±62388 ±5189 ±1352 ±476 ±1175 ±

foodsWhitebread120±1312882±1901112±15281±41137±20100±0100±0Whitepasta50±114456±453156±4891±922±246±1040±5Brown

5Grainbread68±96659±837106±12166±2162±860±1256±6Brownrice113±136240±61658±5117±1142±4104±1862±11French
pasta74 ±74535 ±57467 ±1093 ±1221 ±368 ±1040 ±

fries70
12Whiterice129±168143±68369±5145±1240±3110±1579±12Whole-meal
±117643 ±713146 ±29209 ±1982 ±871 ±1674 ±

bread106 ±141 1 203 ±1420122 ±20247 ±311 11 ±1497 ±1796

12Potatoes148±2413930±1467120±19284±3038±4141±35121±11Groupmean—8410±461106±8182±1062±588±674±8Protein-rich
±

foodsWhitebread121±1917438±3154177±35387±63185±33100±0100±0Eggs36

6Cheese42 ±114744 ±1017135 ±929340 ±184530 ±642 ±1631 ±

±105994
13Beef18±67910±21931583±939—50±1421±851±16Lentils63
±1590268 ±15364 257 ±15013106 ±2755 ±1845 ±

12Fish29 ±179268 ±2174307 ±103325 ±6837 ±962 ±2258 ±

±149350 ±2055775 ±502—28
18Bakedbeans110±1420106±3776183±44504±8757±11114±18120±19Group ±628 ±1359 ±

mean—9983
7FruitWhite ±1032585 ±6118 607 ±545653 ±654 ±761 ±

bread171 ±1915 563 ±1632105 ±18339 ±36166 ±17100

0Apples83±78919±910118±18152±1520±250±659±4Oranges66±119345±1074166±23185±2115±239±760±3Bananas133
±0100 ±

±1212445 ±1353108 ±22224 ±2445

5Grapes126±1412293±1190113±19216±2131±374±982±6Groupmean—10751±605124±10194±1128±261±571±3Snacks
±579 ±1081 ±

confectioneryWhitebread159±2915592±2376104±24340±52166±25100±0100±0Peanuts20
and

±73047
5Popcorn71±126537±679109±32239±25139±1462±1654±9Potatochips77±158195±1577169±78367±71186±3652±961±14Ice
±828214 ±88564 ±15380 ±2212 ±420 ±

cream93
13Yogurt88±2315611±1808167±33415±4865±762±15115±13MarsBar98±1016682±1896218±65441±50309±3579±13122±15Jellybeans161±
±1712 348 ±1867172 ±38479 ±72103 ±1670 ±1989 ±

productsWhitebread129±1517599±3058188±64383±67187±33100±0100±0Doughnuts78±1412445±2402113±21480±93191±3763±1274±9C

12Crackers139 ±1114 305 ±3472178 ±54467 ±I13223 ±5456 ±1482 ±

12Cookies92±1215223±382200±57436±110298±7574±1192±15Groupmean—12681±1325261±56468±47236±2477±783±5
±2614 673 ±2686331 ±104354 ±65253 ±461 18 ±2487 ±

@ I1 SEM. Mars Bar, Mars Confectionary Australia, Ballarat, Australia; All-Bran, Special K, Honeysmacks, Sustain, and Cornflakes: Kellogg's
Australia Pty Ltd. Pagewood, Australia.
1270 HOLT ET AL

bread, which artificially increases the accuracy of any calcu There were large differences in mean glycemic and insulin
lation involving white bread. responses to the foods, both within and between food groups.
Mean glucose and insulin AUC results, mean GSs and ISs, and
the mean ratios of insulin to glucose AUCs (the amount of
RESULTS insulin secretion in relation to the blood glucose response) are
listed in Table 4. Mean GSs and ISs were calculated for each
Fasting glucose and insulin concentrations
food group by averaging the scores for all test foods within the
Within each food group, the subjects' average fasting food group. On average, the snack food group produced the
plasma glucose and insulin concentrations were not signif highest food group IS (89%), followed by bakery products
icantly different among the foods. Mean fasting plasma (83%), carbohydrate-rich foods (74%), fruit (71%), protein
glucose concentrations did not vary significantly among the rich foods (61%), and breakfast cereals (57%). Average GSs
six food groups, whereas mean fasting insulin concentra for the food groups did not follow the same rank order (Figure

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tions were more variable, ranging from “¿42 to 120 pmol/L. 1). The carbohydrate-rich food group produced the highest
Fasting insulin concentrations were not more variable in average GS (88%), followed by bakery products (77%), snack
females than in males and there were no significant differ foods (65%), fruit (6 1%), breakfast cereals (59%), and protein
ences at various stages of the menstrual cycle. A significant rich foods (54%). Interestingly, the GS rank order is not pro
correlation was found between mean fasting insulin concen portional to the average total carbohydrate content of each food
trations and mean BMI values for the six groups of subjects group, which highlights the influence of other food factors (eg,
(r —¿0.81,P < 0.05,n 6). fiber and processing) in determining the rate of carbohydrate
digestion and absorption.
Postprandial glucoseand insulin responses Overall, among the 38 test foods, jellybeans produced the
As with any biological response, there was between-subject highest mean IS (160 ±16%), eightfold higher than the lowest
variation in the glucose and insulin responses to the same food. IS (for peanuts: 20 ±5%) (Figure 2). White bread, the stan
Two-way ANOVA was used to examine the ranking of each dard food, consistently produced one of the highest glucose and
subject's responses to the different test foods within a food insulin responses (peak and AUC) and had a higher IS than
group (ie, interindividual variation). There were significant most of the other foods (84%). All of the breakfast cereals were
differences among the subjects in the rank order of their glu significantly less insulinogenic than white bread (P < 0.001).
cose AUC responses except within the fruit and protein-rich All-Bran and porridge both produced a significantly lower IS
food groups. There were also significant differences among the than the other cereals (P < 0.001), except muesli. Despite
subjects' rank order of insulin AUC responses within all food containing more carbohydrate than porridge and muesli, All
groups. However, individual subjects within each food group Bran produced the lowest GS. Baked beans, which contain
consistently produced relatively low, medium, or high insulin considerably more carbohydrate than the other protein-rich
responses. Furthermore, subjects produced their lowest insulin foods, produced a significantly higher GS and IS (P < 0.001).
responses for the least insulinogenic foods and their highest On average, fish elicited twice as much insulin secretion as did
insulin responses for the most insulinogenic foods within each the equivalent portion of eggs. Within the fruit group, oranges
food group. and apples produced a significantly lower GS and IS than

100
0 Glucose
score
. Insulin
score
80

4)
0 60J
U
‘¿I)
C
4)
4)
E
0. 40
0
0

20

0
Breakfast Protein Fruit Carbohydrate- Bakery Snacksand
cereals rich foods rich foods products confectionery
FIGURE 1. Mean(±SEM)glucoseand insulinscoresfor each food group.
 INSULIN INDEX OF FOODS 1271

All-Bran I@1
Porridge
Muesli

OUSL4I(J

Eg@
Cheese
Beef . lip

Lentils
Fish
-i
Beans

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.1

Apples 1=1
Oranges
Bananas
Grapes

Brown pasta
White pasta ft
Grain bread
Brown rice
Frenchfries
White rice
...@White
Whole-meal bread
breac.IPrthifr@c.

Doughnuts
Croissants
Cake
Crackers
Cookies

PeanutsI=@lIII―;―t-1@PopcornI=―iiPotato

chipsI='=―iIcecreaml―;lIYogurtI

Jellybeans
100 200

Insulin score (%)

FIGURE 2. Mean (±SEM) insulin scores for 1000-Id portions of the test foods. White bread was the reference food (insulin score = 100%). All-Bran
cereal, Special K cereal, Honeysmacks cereal, Sustain cereal, and Cornflakes, Kellogg's Australia Pty Ltd. Pagewood, Australia; Mars Bar candy bar, Mars
Confectionary Australia, Ballarat, Australia.

grapes and bananas (P < 0.05 to P < 0.001), despite contain both contained large amounts of sugar in combination with
ing a similar amount of carbohydrate. fat or protein, produced relatively high ISs. Popcorn and potato
Potatoes produced significantly higher GSs and ISs than all chips elicited twice as much insulin secretion as peanuts
of the other carbohydrate-rich foods. White bread produced a (P < 0.05 and P < 0.01, respectively).
higher GS and IS than grain bread (P < 0.05 and P < 0.001 Significant differences were found both within and among
respectively), but whole-meal bread and white bread had sim the food groups when the insulin AUC responses were
ilar scores. White and brown rice had similar GSs and ISs, as examined as a function of the food's carbohydrate content
did white and brown pasta. Among the bakery products, crack (Table 4). On average, protein-rich foods produced the
ers produced a significantly higher GS than the other test foods, highest insulin secretion per gram of carbohydrate (food
but there were no significant differences in ISs within this group mean: 18 607 pmol . mm . L' . g@1) (because of
group (all tended to be high). Among the snack foods, jelly their mostly low carbohydrate contents), followed by bakery
beans produced a significantly higher GS and IS than the other products (468 pmol . mm . L@ . g1), snack foods (416
foods in this group. Despite containing similar amounts of pmol . mm . L ‘¿. g 1) fruit (194 pmol . mm . L ‘¿ . g 1),
carbohydrate, jellybeans induced twice as much insulin secre carbohydrate-rich foods (182 pmol . mm . L@ . g'), and
tion as any of the four fruits. The candy bar and yogurt, which breakfast cereals ( 169 pmol . mm . L ‘¿ . g ‘¿).
When the
1272 HOLT ET AL

insulin AUC response was examined in relation to the food's Relations between metabolic responsesand nutrient
serving size (g), the bakery products were the most insuli contents of the foods
nogenic (food group mean: 236 pmol . mm . L ‘¿
. g 1), fol Correlations between the macronutrient compositions of the
lowed by snack foods (163 pmol . mm . L ‘¿
. g 1), carbo test foods and the mean ISs are shown in Figure 5. The portion
hydrate-rich foods (62 pmol . mm . L ‘¿
. g 1), protein-rich size (energy density: kJ/g), water, and fiber contents of the
foods (53 pmol . mm . L ‘¿ . g 1), breakfast cereals (39 foods were not significantly related to the mean ISs. The
pmol . mm . L ‘¿. g ‘¿),
and fruit (28 pmol . mm . L ‘¿. g 1). relation between protein contents and ISs was negative but not
These results reflect the insulinogenic effects of protein and significant (r —¿0.24,n = 38). The mean ISs were positively
fat. related to total carbohydrate content (r = 0.39, P < 0.05, n =
36) and sugar content (r = 0.36, P < 0.05, n = 36), but were
Insulin responses in relation to glucose responses not significantly related to starch content (r = —¿0.09,
n = 30).
Fat content was negatively related to the mean IS (r = —¿0.27,

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Overall, mean glucose and insulin AUC values were posi NS, n = 36). When expressed as a percentage of total energy,
tively correlated (r = 0.67, P < 0.001, n = 43), as were the fat (r = —¿0.27,NS, n = 36) and protein (r = —¿0.24,NS, n =
peak glucose and insulin values (r = 0.57, P < 0.001, n = 43). 38) were negatively associated with the mean IS, whereas total
Hence, the mean GSs and ISs were highly correlated (r = 0.70, carbohydrate was positively related (r = 0.37, P < 0.05, n
P < 0.001, n = 38) (Figure 3). The peak glucose concentration 36).
(change from fasting) correlated positively with glucose AUC Relations between the GSs and the nutrients largely followed
values (r = 0.74, P < 0.001, n = 43) and peak insulin the same directions as the IS correlations. Mean GSs were not
concentrations were proportional to the insulin AUC values significantly related to the foods' serving sizes or water or fiber
(r 0.95, P < 0.001, n 43). In addition, the observed GSs contents. Mean GSs correlated negatively with fat (r = —¿0.38,
for 1000-U portions of the foods correlated with previously P < 0.05, n = 36) and protein (r = —¿0.38,P < 0.05, n = 38)
published GI values based on portions of foods containing 50 g contents, and positively with total carbohydrate content (r =
carbohydrate (r = 0.65, P < 0.001, n = 32). Six test foods 0.32, NS, n = 36). Unlike the ISs, the GSs were significantly
(chocolate chip cookies, eggs, cheese, beef, fish, and Hon related to starch content (r = 0.43, P < 0.05, n = 30) but not
eysmackscereal)werenotincludedin thisanalysisbecauseGI sugar content (r = —¿0.07, NS, n = 36). When expressed as a
values were not available. percentageof total energy, fat (r = —¿0.38,P < 0.05, n = 36)
Insulin AUC values were divided by glucose AUC values to and protein (r = —¿0.39,P < 0.05, n = 38) were negatively
determine which foods were markedly insulinogenic relative to associated with mean GSs, whereas total carbohydrate content
their glycemic effect (Table 4 and Figure 4). On average, the was positively related (r = 0.46, P < 0.01, n = 36).
protein-richfoodsstimulateda large amountof insulinsecre Stepwise-multiple-regression analysis of the 446 individual
tion relative to their glycemic response, followed by the bakery results for the 38 foods was performed to determine the extent
products, snack foods, fruit, carbohydrate-rich foods, and to which the macronutrients and GSs accounted for the van
breakfast cereals. ability of the ISs. Unfortunately, it was not possible to generate
a single multiple-regression equation that included all of the
macronutrients because some pairs of nutrients were highly
correlated (eg, fat and protein, fiber and water, total carbohy
drate and sugar or starch, and sugar and starch). The regression
equation that included all of the macronutrients had unaccept
ably high variance inflation factors. Therefore, two separate
regression equations were generated that were limited to the
. factors that were measured and not interdependent. Equation 2
includes fat but not protein, whereas equation 3 includes pro
tein but not fat:
S S
4)
1@ IS = 72.4 + 0.383 GS —¿
1.88 fat —¿
0.103 water
0
U
4)
C
•¿â€¢ + 0.509 sugar —¿
0.421 starch (2)
S
4)
C
for whichSD = 37.34,R2= 33.1%,andadjustedR2= 32.4%.
P values (significance found in the linear-regression analysis
for the associations between the individual nutrients and the IS)
are as follows: OS and water (P < 0.000), fat (P < 0.001),
sugar (P < 0.005), and starch (P < 0.036).

0 IS = 23.2 + 0.383 05 + 0.785 protein —¿

0.098 water
0 100 200
+ 1.29 sugar + 0.377 starch (3)
Glucose score (%) for which SD = 37.42, R2 = 32.8%, and adjusted R2 = 32.1%.
FIGURE 3. Relationbetweenthe meanglucoseandinsulinscores(r = P values are as follows: GS, water, and sugar (P < 0.000);
0.74, P < 0.001, n = 38). protein (P < 0.003); and starch (P < 0.02).
 INSULIN INDEX OF FOODS 1273

Porridge
All-Bran
Comfiakes
Special K
Sustain
Honeysmacks
Muesli

Brownrice
Brownpasta
White rice
Grain bread
Whitebread

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Potatoes
Whole-meal bread
Frenchfries I..
White pasta I-,
Bananas
Grapes
Apples
Oranges

Popcorn
Jellybeans
Yogurt
Chips
Icecream
Peanuts I-i
MarsBar

Doughnuts
Cake @1
Cooides -I
Crackers
Croissant

Eggs -t
Beans
Cheese
Lentils
Fish
Be@

0 500 1000 1500 2000 2500 3000

InsulinAUC/Giucose
AUC
FIGURE 4. Ratio of insulin area under the curve (AUC) to glucose AUC responses. I ±SEM. All-Bran cereal, Special K cereal, Honeysmacks cereal,
Sustaincereal,and Cornflakes,Kellogg'sAustraliaPty Ltd.Pagewood,Australia;MarsBar candybar, MarsConfectionaryAustralia,Ballarat,Australia.

Linear-regression analysis of the individual OS and IS re and insulinemia. Within each food group, there was a wide
sults had an R2 value of 23%. Therefore, the glycemic response range of insulin responses, despite similarities in nutrient corn
was a significant predictor of the insulin response, but it position. The important Western staples, bread and potato,
accounted for only 23% of the variability in insulinemia. The were among the most insulinogenic foods. Similarly, the highly
macronutrients (protein or fat, water, sugar, and starch) were refined bakery products and snack foods induced substantially
also significant predictors but together accounted for only more insulin secretion per kilojoule or per gram of food than
another 10% of the variability of the insulin responses. Thus, did the other test foods. In contrast, pasta, oatmeal porridge,
we can explain only 33% of the variation of the insulin re and All-Bran cereal produced relatively low insulin responses,
sponses to the 38 foods studied. despite their high carbohydrate contents. Carbohydrate was
quantitatively the major macronutrient for most foods. Thus, it
is not surprising that we observed a strong correlation between
DISCUSSION
GSs and ISs (r = 0.70, P < 0.001). However, some protein
The results of this study confirm and also challenge some of and fat-rich foods (eggs, beef, fish, lentils, cheese, cake, and
our basic assumptions about the relation between food intake doughnuts) induced as much insulin secretion as did some
1274 HOLT ET AL

200
140
S S 5 S

100 S
S S

0 S S 100 S.

•¿t,.. S
U)
C SI•

S
0

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0 10 20 0 20 40 60
Fiber (9/serving) Protein (glservlng)

200W 200

S S

S S
S 100
U)
S
100
C

a, @fS55
C

I @S
S
S
0 0 i I
0 20 40 60 0 20 40 60

Total carbohydrate (9/serving) Sugar (9/serving)

140
S
S

100
S S
S
U)
S 55

C S 0 55
S S S
S
U)
C
60 1@b5 s
S

S S
0 7c1
0 20 40 60 0 10 20 30
Starch (9/serving) Fat (9/serving)
FIGURE 5. Relations between the nutrient contents of the test foods and the mean insulin scores. Fiber: r = —¿0.10,
NS, n = 32; protein: r = —¿0.24,
NS, n = 38; total carbohydrate:r = 0.39, P < 0.05, n = 36; sugar:r = 0.36,P < 0.05,n 36; starch:r = —¿0.09,
NS, n = 30; fat: r = —¿0.27,
P<
0.05, n = 36.

carbohydrate-rich foods (eg, beef was equal to brown rice and whole-meal bread. All of these foods are relatively refined
fish was equal to grain bread). As hypothesized, several foods compared with their traditional counterparts. Collectively, the
with similar GSs had disparate ISs (eg, ice cream and yogurt, fmdings imply that typical Western diets are likely to be
brown rice and baked beans, cake and apples, and doughnuts significantly more insulinogenic than more traditional diets
and brown pasta). Overall, the fiber content did not predict the based on less refined foods.
magnitude of the insulin response. Similar ISs were observed In this study, we chose to test isoenergetic portions of foods
for white and brown pasta, white and brown rice, and white and rather than equal-carbohydrate servings to determine the insu
 INSULIN INDEX OF FOODS 1275

lin response to all of the nutrients in the foods as normally Dietary guidelines for healthy people and persons with
consumed. A standard portion size of 1000 kJ was chosen NIDDM have undergone considerable change and will con
because this resulted in realistic serving sizes for most of the tinue to be modified as our understanding of the relations
foods except apples, oranges, fish, and potatoes. Although between dietary patterns and disease improves. There is con
some of the protein-rich foods may normally be eaten in cern that high-carbohydrate diets may increase triacylglycerol
smaller quantities, fish, beef, cheese, and eggs still had larger concentrations and reduce high-density lipoprotein concentra
insulin responses per gram than did many of the foods consist tions (35, 36). The use of diets high in monounsaturated fat is
ing predominantly of carbohydrate. As observed in previous an attempt to overcome the undesirable effects of some high
studies, consumption of protein or fat with carbohydrate in carbohydrate diets on plasma lipids (37—39).However, diets
creases insulin secretion compared with the insulinogenic ef high in monounsaturated fat are unlikely to facilitate weight
fect of these nutrients alone (22, 30—32). This may partly loss. A low-fat diet based on less-refined, carbohydrate-rich
explain the markedly high insulin response to baked beans. foods with relatively low ISs may help enhance satiety and aid

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Dried hancot beans, which are soaked and boiled, are likely to weight loss as well as improve blood glucose and lipid control
have a lower IS than commercial baked beans, which are more (4).
readily digestible. The results of this study are preliminary but we hope they
The results confirm that increased insulin secretion does not stimulate discussion and further research. Additional studies are
account for the low glycemic responses produced by low-GI needed to determine whether the IS concept is useful, reproducible
foods such as pasta, porridge, and All-Bran cereal (33). Fur around the world, predictable in a mixed-meal context, and cliii
thermore, equal-carbohydrate servings of foods do not neces ically useful in the treatment of diabetes mellitus, hyperlipidemia,
sarily stimulate insulin secretion to the same extent. For exam and overweight. Studies examining the relation between postpran
ple, isoenergetic servings of pasta and potatoes both contained dial insulinemia and the storage and oxidation of fat, protein, and
=,%50g carbohydrate, yet the IS for potatoes was three times carbohydrate may provide further insight into the relation between
greater than that for pasta. Similarly, porridge and yogurt, and fuel metabolism and satiety, and establish whether low-insuline
mic diets can facilitate greater body fat loss than isoenergetic
whole-grain bread and baked beans, produced disparate ISs
high-insWinemic diets.
despite their similar carbohydrate contents. These findings, like
others, challenge the scientific basis of carbohydrate exchange We thank Efi Farmakalidisfor her assistancein the planningof this
tables, which assume that portions of different foods containing study and Natasha Porter for her technical assistance with the experimental
10—15g carbohydrate will have equal physiologic effects and work for the carbohydrate-rich food group.
will require equal amounts of exogenous insulin to be metab
olized. It is possible that preprandial insulin doses for patients
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