An Insulinindex of Foods:The Insulindemand Generatedby

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ABSTRACT The aim of this study was to systematicallycompar e pos tp ra nd ia l in su lin r es pons es to is oe ne rg etic 1000-U(240-kcal) portions of several common foods. C orrelations w ithn ut rie nt c on te nt w er e d et ermi ne d. T hir ty -e ig ht f oo ds s ep ar at ed in tos ix food cat egori es ( fr ui t, bake ry produc ts , snacks , carbohydra ter ic h f oods , p ro te in -ri ch food s, a nd b re ak fa st c er ea ls ) wer e fe d t og ro up s o f 1 1 13 ea lt hy s ub je ct s. F in ge r-p ri ck b lo od s ampl es w er eobtained every 15 m m over 120 m m. A n insulin score w as calculated from the area under the insulin response curve for each foodw ith use of w hite bread as the reference food (score = 100% ).S ig nifica nt d iffe re nce s in in su lin sc ore w ere fou nd b oth w ith in a ndamong the food categories and also among foods containing asim ila r am ou nt o f ca rb oh yd rate. O ve rall, g lu cose an d insu linscores were highly correlated (r = 0.70, P < 0.001, n = 38).Howeve r, p ro te in -r ic h f oods and baker y p roducts ( ric h in f at a ndr ef ined carbohydra te ) e li ci ted i nsul in r esponses t ha t were d isp roportionately higher than their glycemic responses. Total carbohydrate (r = 0.39, P < 0.05, n = 36) and sugar (r = 0.36, P < 0.05,n = 3 6) c on te nt s we re p os itiv el y r ela te d t o th e m e an in su lin s co re s,whereas fat (r 0.27,S, n 36) and protein (r 0.24,S,n = 3 8) c on te nts w ere n eg ative ly re la ted . C on side ra tio n o f in su linscores m ay be relevant to the dietary m anagem ent and pathogene si s o f n on -i ns ul in -d ep endent d ia be te s me ll it us a nd hyp er li pi dem iaan d m ay h elp in crease th e accu racy o f estim atin g prep ran dialin su lin req uirem en ts. Am J C lin N utr l9 97 ;6 6:l2 64 76 .KEY WORDS Insulin, glycem ic index, NIDDM, nonin su lin -d ep endent d ia be te s me ff itu s, d ia be tic d ie t, h yp er lip idem ia , c arbohyd ra te , in su lin s co re , g lu co se s co re , a re a under th ec ur ve , h uman s

INTRODUCTIONThe insulinemic effects of foods may be relevant to thetre atm en t a nd p re ve ntio n o f w eig ht g ain , n on -in su lin -d ep endent d iabet es me ll it us (NIDDM) , and associ at ed compl icat ions.R ec en t stu die s h av e s hown th at c arb oh yd ra te -ric h d ie ts , w hic hresult in high p ostp rand ia l g luc ose an d insu lin resp on ses, area sso cia te d w ith u nd es ira ble lip id p ro file s (1 , 2 ), g re ate r b od yfa t (3 5 ), nd th e d ev elo pm en t o f in su lin re sista nc e in ra ts (6 )and hum ans (7, 8). Both obesity and N JD DM are associatedw ith v ary in g d eg re es o f in su lin re sista nc e a nd fa stin g h yp erins ul in em ia . P ro longed o r h igh deg re es o f pos tp ra nd ia l i ns ulin em ia are thought to contribute to the developm ent of insulinre sis ta nc e an d asso cia te d d ise ase s (9 1 7).T here fore , th e clas

sific atio n o f th e re la tiv e in su lin em ic e ffe cts o f d iffe re nt fo od sis of both theoretical and practical significance.Postprandial blood glucose responses have been the focus ofmuch research because of their im portance for glycem ic control in patients with diabetes. It is now well accepted thatd iffe re nt fo od s c on ta in in g e qu al amoun ts o f c arb oh yd ra te c anproduce a w ide range of blood glucose responses. T he glycem ic index (G I) m ethod w as developed to rank foods accordingto th e ex te nt to w hich th ey in crease b lo od g lu co se co ncen trations (18). Tables of GI values of common carbohydratecontaining foods are a useful guide to help people with diabetesch oo se fo ods that p ro du ce sm aller glycemic resp on ses. H owever, the G I concept does not consider concurrent insulinresponses and few studies have reported GI values and theiraccompanying insu li n r esponses.T he extent to w hich different dietary factors affect postprandial insulinem ia has not been w ell researched becauseinsulin secretion is largely assum ed to be proportional topostprandial glycemia. Furthermore, hyperglycemia isth ou gh t to b e m ore re lev ant to th e se con dary comp lication sof NIDDM because the abnormal insulin secretion or actionin p eo ple w ith d iab etes is co ntro lled w ith ex og eno us in sulinor m edications that counteract insulin resistance. H ow ever,know ledge of factors that influence both postprandial glycemia and insulin secretion in nondiabetic persons is required to devise treatm ent strategies that w ill com pletelynorm alize m eal-related glycem ia (19).T o e xp lo re th e im po rta nc e o f d ie ta ry h ab its a nd p os tp ra nd ia lin sulin em ia in th e etio lo gy an d treatm ent o f N IDDM , w e n eedto be able to systematically rate insulin responses to comm onfoods. If we are to compare insulin responses to foods, what isthe best basis of comparison? Should we compare insulinresponses to portions of food representing a normal servingsize, portions containing an equal amount of carbohydrate, orportions containing an equal amount of energy? 01 tablesrepresent the glycem ic effects of equal-carbohydrate portions

I F rom the Human Nutrition Unit, Department of Biochem istry, TheUni ve rs ity o f S yd ne y; a nd th e S ch oo l o f Ma th em ati ca l S ci en ce s, T heUnivers i ty of Technology, Sydney, Austra l ia .2 S upported by research grants from The University of Sydney andKel logg' s Aus tral ia Pty Ltd.3 Address reprint requests to JC Brand M iller, H uman Nutrition Unit,Depa rtmen t o f B ioc hem is tr y 0 08 , Th e Un iv er si ty o f Sydn ey , NSW 2006,Australia.Re ce iv ed Novembe r 2 1, 1 996.Ac cept ed f or p ub li ca ti on May 22, 1 997.

1264 A m J C lin N utr 1 99 7;6 6:1 26 4 76 .P rin ted in U SA . 1 99 7 A meric an S ocie ty fo r C lin ica l N utr itio n

An insulinindexof foods: the insulindemand generated by1000-kJ portions of common foods13Susanne HA Holt, Janette C Brand M iller, and Peter Petocz


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Food Variety, manufacturer, or place of purchase Preparation

IN SULIN INDEX OF FOODS 1265TABLE!Desc riptionandpreparationof the testfo odsFruitBlack grapesApplesOrangesBananasBakery productsCroissantsChocolate cake withfrostingDoughnuts with cinnamonsugarChocolate chip cookiesWater crackersSnack foods and confectioneryMars BarYogurtIce creamJellybeans (assorted colors)PeanutsPotato chipsPopcorn

Protein-rich foodsCheeseEggsLe n t i l s

Baked beansBeefsteakWhi te f is h

Carbohydrate-rich foodsWhite breadWhole -mea l b readGrain breadWhi te ri ceBrown riceWhite pastaBrown pastaPotatoes

Waltham crossReddeliciousNavelCavendish

Fresh, stem removed, served wholeFresh, unpeeled, cut into eight segmentsFresh, peeled, cut into eight segmentsFresh, peeled, cut into quartersDefros ted, reheated a t 180Cor 6 mm, and served warmPrepared according to manufacturer's directions, stored at4 Cup to 2 d before serving at room temperaturePrepared by supermarket from standard recipe, defrostedovernight, reheated at 180Cor 5 mm, and servedwarmServed crisp at room temperature, stored in airtightcontainerServed crisp at room temperatureCut into four standard pieces and served at roomtemperatureStored at 4 C,erved coldStored frozen and served coldServed at room temperature, stored in airtight containerServed at room temperature, stored in airtight containerServed from freshly opened packetPrepared according to manufacturer's directionsimmediately before servingA ll s erv ing s cut fro m sam e larg e blo ck, s to red at 4 C,served coldPoached the day before serving, stored at 4 Cvernight,reheatedinmicrowaveoven for 1.5mm immediatelybefore servingPrepared in bulk according to recipe, stored at 4 Cor upto 2 d, re he ate d i n a m ic rowav e o ve n f or 2 mmimmediatelybeforeservingHeated on s tove for5 mm immediate ly before serv ingGril led the day before serving, cut into standard bite-s izedpieces, and stored at 4 Cvernight; reheated inmicrowave oven for 2 mm immediately before servingSteamed the day before serving, stored at 4 Cvernight,cut into bite-s ized pieces, and reheated in microwaveoven for 2 miii immediately before servingServed fresh and plain at room temperatureServed fresh and plain at room temperatureServed fresh and plain at room temperatureBo iled 12 mii i and s tored overnight a t 4 C,eheated inmicrowave oven for 1.5 mm immediately before servingBo iled 12 mm and stored overnight a t 4 C,eheated inmicrowave oven for 1.5 mm immediately before servingBoiled8 mm and storedovernightat4 CRe he ate d i n m ic rowav e o ve n f or 1 .5 mm imme diate lybefore servingPeeled,boiledfor 20 mm, andstoredat 4 Cvernight;reheated in a microwave oven for2 mm immediate lybefore serving

Purc has ed i n bul k f rom supe rmarke t and s to re d f ro ze nWhite Wings Foods, Smithfie ld, Sydney, AustraliaPurchased in bulk from supermarket and stored frozenAnion's Biscuits Ltd. Homebush, Sydney, AustraliaGrocery Wholesalers Ltd, Yennora, AustraliaMars Confectionary Australia, Ballarat, AustraliaStrawberry fruit yogurt; Australian Co-operativeFoods,' Wetherill Park, Sydney, AustraliaVanil la ice cream; Dairy Bell, Camperdown, Sydney,AustraliaGrocery Wholesalers LtdSalted roasted peanuts; Grocery Wholesalers LtdCrinkle cut chips; Smith's Snackfood Company,Chatswood, Sydney, AustraliaMicrowave cooked popcorn; Uncle Toby's CompanyLtd, Wahgunyah, Australia

Mature c he ddar c he es e; G ro ce ry Who le sa le rs L tdPoached hens eggs

Served in tomato sauce2Canned navy beans in tomato sauce; Franklins,Chullora, Sydney, AustraliaLe an to ps ide be ef f il le ts bo ug ht i n bulk f romsupermarket, trimmed and stored frozenLing f ish i fi le ts bought in bulk from Sydney f ishmarkets, trimmed and stored frozenFresh sliced wheat-flour bread; Quality BakersAustralia Ltd. Eastwood, Sydney, AustraliaFresh sliced bread made from whole-meal wheat flour;Riga Bakeries, Moorebank, Sydney, AustraliaFresh sliced rye bread containing 47% kibbled rye; TipTopBakeries,Chatswood,Sydney,AustraliaCairose rice (Sunwhite), Ricegrowers' Co-operativeLtd. Leeton, AustraliaCalrose rice (Sunbrown), Ricegrowers' Co-operativeLtdSpiralsWho le -meal s pi ral s; S an Remo Pas ta Company ,Auburn, Sydney, AustraliaRusset potatoes


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FoodVariety, manufacturer, or place o furchasePreparationFrenchfriesPrefried oven-baked French fries; M cCain's Foods(Aus tra li a) , Cas tl e H il l, S ydney , Aus tra li aS tored frozen, cooked in conventional oven for 15 mmimmediately beforeervingBreakfastcereals3CornflakesKellogg's Australia Pty Ltd, Pagewood, Sydney,

AustraliaSpecialKToasted f lakes made from wheat and rice f lour, high inprotein; Kellogg's Australia PlytdHoneysmacksPuffed whole-wheat grains with a honey-based coating;Kellogg's Australia PlytdSustainA mixture of wheat, corn, and rice flakes; rolled oats;dried fruit; and flaked almonds; Kellogg's AustraliaPtytdAll-BranA high-fiber cereal made from wheat bran; Kellogg'sAustralia PtytdNaturalmuesliBased on raw rolled oats, wheat bran, dried fruit, nuts,and sunflower seeds; Uncle Toby 's Company Ltd.Wahgunyah,ustraliaPorridgeUncle Toby's Company Ltd. Wahgunyah, AustraliaRaw ro lled oats cooked in a microwave oven according tomanuf ac ture r's di re cti ons and s erv ed w ithout sw ee te ne r

1266 HOLT ET ALTABLE 1Continued

1 N ow 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 A ll cereals were served fr esh wi th 125 mL fat-reduced (1.5% fat) mi lk.

of foods.However ,carbohydrates not the only s timulusfori nsul in secre ti on . Prote in -ri ch foods or the addi ti on of prote into a carbohydrate-rich meal can stimulate a modest rise ini nsul in secre ti on wi thout increas ing blood g lucose concentrations , particularly in subjects wi th diabetes (2022).Similarly,adding a large amount of fat to a carbohydrate-rich mealincreases insulin secretio n ev en tho ugh plasma g lucose respons es are re duc ed (2 3, 2 4).Thus, pos tprandial insul in responses are not always proportional to blood glucose concentrations or to a meal's totalcarbohydrate content. Several insul inotropic factors are knownto po tentiate the stimulato ry effec t o f gluco se and mediatepo stprandial insulin se cre tio n. These inc lude fructo se, c ertainam ino ac ids and fatty acids, and gastro inte stinal ho rmo nes suchas gas tric inhibito ry peptide , g lucagon, and cho le cy stoki in(2 5, 2 6). T hu s, p ro te in - a nd fa t-rich fo od s m ay in du ce s ub sta nti al i nsul in secre ti on desp ite producing re lati ve ly small b loodg luc ose re sponse s. We the re fo re de cide d that c omparing theinsulinemic effects of foods on an isoenergetic basis was alogical and practical approach.The aim o f this study w as to sy stematically compare po stprandia l insul in responses to i soenerge ti c porti ons o f a range ofcommon foods. A n insulin score (IS) w as calculated for eachf ood on the bas is o f i ts insul inemic e ff ec t re lati ve to a re ferencefood. Thirty-eight foods, categorized into six different foodgroups, w ere studied to determine w hich foods w ithin the samefood group were most insulinogenic. We hypothesized thatpo stprandial ins ulin re sponse s are no t c lo se ly re late d to thecarbohydrate content or glycemic effects of some foods.SU BJECTS A ND METHOD STest fo odsThirty-eight foods were tested and were grouped into sixfo od cate go ries : 1) fruit: grapes, bananas, apples, and o rang es;

2) bakery products: croissants, chocolate cake w ith icing,doughnuts w ith cinnamon sugar, chocolate chip cookies, andwate r c rac ke rs; 3 ) snac k fo ods and c onfe ctio ne ry : Mars B arc andy bar (Mars Conf ec tio nary Aus tral ia, B al larat, Aus tral ia) ,s trawbe rry y og urt, v ani ll a i ce c re am , je lly be ans , s al te d ro as te dpe anuts , plain po tato c hips, and plain po pco rn; 4) pro tein-ric hf oo ds : c heddar c heese, p oa ched egg s, b oile d le nt ils in a tomat osauce, baked beans in a tomato sauce, grilled beef steak, ands te amed whi te f is h; 5 ) c arbohydrate -rich f oods : white bread,who le -m eal bre ad, ry e-g rain bre ad, white ric e, brown ric e,w hite pasta, brown pas ta, bo ile d po tato es , and o ve n-bake dFre nch frie s; and 6) breakfast ce reals: Cornflakes (Ke llo gg'sA ustralia Pty Ltd. Pag ew oo d, A ustralia), S pec ial K (Ke llo gg'sAustralia Pty Ltd), Honeysmacks (Kellogg's A ustralia PtyLtd), Sustain (Kellogg's Australia Pty Ltd), All-Bran(Kellogg's A ustralia Pty Ltd), natural muesli, and oatmealporridge.Each food was served plain as a 1000-U portion with 220mL w ater. W hite bread w as used as the reference food for eachfo od g ro up. The fo ods w ere selected to represe nt a rang e o fnatural and pro cesse d fo ods commonly e aten in industrializ edso cie ties . D etails o f the fo ods and the ir preparatio n me tho ds arelisted in Table 1. Foods were bought in bulk to minimizevariations in composition and w ere served in standard-sizedpieces. The nutritional composition ofeach food per 1000 U ascal cu lated f rom Aus tra li an food tabl es or manufac turers ' datais shown in Table 2.SubjectsS eparate g ro ups of healthy subje cts (n = 1 113 )w ere recruited to test each category of foods. V olunteers w ere excluded i f they were smokers or taking prescription medications ,had a f am ily his to ry o f di abe te s o r obe si ty , w ere die ting , o r hadi rregular eating habits . In to tal , 41 subjects parti cipated. Onesubject consumed all of the test foods and 15 other subjects


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ServingCarbohydrateEnergyFoodweight FatProtein SugarStarch FiberWater density

INSULIN INDEX OF FOODS 1267TABLE 2Nuthtional composition of the test foods per 1000-U serving as calculated from Australian food tables or manufacturers' data'

g g g g g g@I/gFruitGrapes3950.43.256.90.03.6317.02.5Bananas2790.34.747.28.46.1210.13.6Apples4350.01.356.52.29.1360.92.3Oranges6250.66.950.60.012.5539.41.6Bake

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.

andonfectioneryMarsBarr549.42.936.71.11.73.518.5Yogurt@2415.311.837.60.00.5187.04.2Icecream12013.45.225.80.00.074.28.3Jellybeans880.05.344.611.50.012.211.4Peanuts3820.19.61.73.72.40.626.3Potatochips24416.22.70.222.12.41

foodsCheese5920.015.00.10.00.020.916.9Eggs15917.919.60.50.00.0119.46.3Lentils2534.619.44.224.911.4222.03.9Bakedbeans3511.716.116.123.216.8267.12.8Beefsteak1587.742.00.00.00 .0104.36.3Fish3331.056.30.00 .00.0250.03.0Carbohydrate-richfoodsWhitebread2942.18.51.844.13.336.110.6Whole-mealbread21012.67.61.743.76.640.39.9Grainbread21085.49.42.437.66.541.49.3Whiterice22030.55.00.156.00.4140.04.9Brownrice21482.15.20.552.61.493.96.8Whitepasta2010.87.82.047.13.5134.85.0Brownpasta22181.611.30.747.810 .9132.64.6Potatoes3681.010.03.145.99.2290 .82.7French

fries2938.73.91.135.43.533.810.7BreakfastcerealsCornflakes21702.18.410.236.11.5110.95.9SpecialK21722.115.314.027.21.4111.25.8Honeysmacks21722.28.731.117.02.6115.05.8Sustain21683.19.713.729.13.2119.15.9Muesli21756.110.717.119.86.6114.15.7Pomdge23836.210.97.529.04.7333.72.6All-Bran21742.911.713.929.414.1111.05.7

I M ar s Bar , M ars Confectionar y Austral ia, Bal larat, Austral ia; Comf iakes, Special K, H oneysmacks, Sustain, and Al l -Bran: Kel logg' s Austral ia Pty L td.Pagewood, Australia.2 Nutr ient composi tion calculated fr om manufacturer ' s data.

completed two or more food categories. A ll of the subjects approved by the Medical Ethical Review Committee of thewere uni ve rs ity s tudents ; re le vant charac te ris tic s o fthe subje cts Univ ers ity o f Sydney.are listed in Table 3. The mean body mass index (BMI, inkg/m2) of the 41 subjects w as 22.7 0.4 (range: 1929).Three P1@Ot(WOlsubjects had a BMI > 25 but tw o of these w ere short, stocky Each subject first consumed a 1000-U portion of w hite breadmales w ho had ex cess muscle rather than fat. Female subjects (4 5.9 g carbo hy drate) to co nfirm normal g luco se to lerance.did not participate during their menstrual period or if they White bread w as also used as the reference food (IS = 100%)experienced adverse premenstrual symptoms. Informed con- against which all other foods were compared, similar to thesent w as o btained from all o f the subjects and the study w as method used fo r c alculating GI v alues o f fo ods (1 8). The use of


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FoodroupAgeBMI2yFruit(n = 5 F, 6 M)22.9 3.9 22 .9 .4Bakeryproduc ts (n = 6 F, 6 M )2 2.2 3.7 23 .1 .7Snacksand confectionery(n = 5 F, 7 M)21.0 1.222. 9 .5Protein-richfoods (n 5 F, 6 M)22.4 2.824.3 .1Carbohydrate-rich foods (n = 5 F, 8 M)21.0 1.923.0 .9Breakfastcereals (n = 5 F, 6 M)22.8 3.922.8 1.4

1268 HOLT ET ALtube radioimmunoassay kit (Coat-A -Count; D iagnostic Products Corporation, Los A ngeles). For both plasma glucose andins ul in analy si s, all nine plasma sample s f or a particular subject's test w ere analyzed w ithin the same run to reduce anyer ro r in t roduce dby in t e ra s s ayva r ia t ion . W he n pos s i b le , a llplasma samples fo r a particular subject w ere analyz ed forinsulin w ithin the same run. For the insulin analysis, the meanw ithin-assay CV w as 5% and the mean betw een-assay CV w as7%Stati stical analys isCumulativ e chang es in po stprandial plasma g luc ose andinsulin re spons es fo r e ac h fo od w ere quantifie d as the inc remental area under the 120-mn response curve (A UC), w hichwas calculated by us ing the trape zo idal rule w ith fas ti ng concentrati ons as the basel ine and truncated at zero . Any negati veareas tended to be small and were ignored. For each subje ct, anIS (%) was calculated f or each te st food by div iding the insuli nAUC value fo r the te st fo od by the ins ulin AUC value fo r whitebread (the reference food), and expressed as a percentage asfollows:

I S ( %)Are a unde r the 1 20 -mm ins uli n re spo ns e

c urv e fo r 1 00 0 U te s t fo odAreaunderthe 120 -mminsulinresponse curvef or 1000 Id whi te bread

TABLE 3Characteristics of each group of subjects '

SD .2 I n kg/ rn2.

a re fe re nc e fo od c ontro ls fo r inhe re nt diffe re nc es be tw ee nindi vi duals that af fe ct insuli n s ens itiv ity , s uch as body weightand ac ti vi ty l eve ls .Subjects were fed 1000-U portions of the test foods in arandom order on separate mo rning s after a 1 0-h o vernig htfast. W ithin e ac h fo od g roup, e ac h subje ct ac te d as his o r he rown contro l, being tested at the same time o f day and underas similar conditions as possible. S ubjects w ere asked torefrain from unusual ac tiv ity and fo od intake patterns, toabstain from alco ho l and leg umes the day before a te st, andto eat a similar meal the night before each test. Whensubjects arrived at the lab in the mo rning , they comple ted ashort que stionnaire as se ss ing re cent f ood intake and ac tiv itypatte rns. A fas ting fing er-pric k blo od s ample w as c olle cte dand subjects were then given a test food and 220 mL water(0 mm). When possible, foo ds w ere prese nted under a larg eo paque plastic ho od w ith a ho le thro ugh w hich vo lunteerspulled out pieces of the test food one at a time. This was anattempt to m inim iz e be tween- subje ct variation in c ephalicphas e insulin s ec re tion aris ing f rom the s ens ory s timul ationassociated with the anticipation and act of eating (27).How eve r, th is w as n o t fe as ib le fo r th e liq u id fo od s (yo gu rtand ice cream), foods served in a sauce (baked beans andlentils), or w ith milk (all of the breakfast cereals), w hichwere presented in standard bowls w ithout the hood.Subje cts w ere as ke d to e at and drink at a c om fo rtable rate .Imme diate ly afte r finishing the test fo od, subjec ts re co rded thetime taken to eat the food and completed a questionnaireas se ss ing v ari ous appe ti te re spo ns es and the f oo d's palatabil ity .[These results are reported in a separate paper (28).] S ubjectsremained s eated at table s in a qui et env ironment and were no tpermitted to eat or drink until the end of the session (120 mm).Finger- pri ck blood s ample s ( 1.52 .5mL) were colle ctedfrom warmed hands immediately before the meal (0 mm) and15, 30, 45, 60, 75, 90, 105, and 120 mm after the start of themeal (into plastic tubes that had been kept o n ice ) w ith use o fan automatic lanc et devic e (Auto cli x; Boehringer Mannhe imA ustralia, Castle Hill, A ustralia). B lood samples w ere centrifuged immediately after collection (1 miii at 12 500 X g atroom temperature ) and pl asma was pipe tted into chill ed tube sand immediate ly s to re d at 2 0 Cuntil analy ze d (< 1 mo).P lasma glucose concentrati ons were analyzed in dupl icate w itha Cobas Fara automatic s pe ctropho tome tric analy ze r (RocheD iagnostica, B asel, S witzerland) and the glucose hexokinaseenzymatic assay. The mean w ithin-assay and betw een-assaypre cisio ns (CV s) w ere bo th < 6%. Plasma insulin c onc entrati ons were measured in dupli cate by us ing an antibody-coated

X100 (1)

This equation is similar to that developed by Wolever andJenkins (29) for calculating GI values. A glucose score (GS)(not the same as a GI score, w hich is based on a 50-g carbohydrate portion) for each food w as also calculated by using thesame e quatio n w ith the co rrespo nding plasma g luco se re sults.A nalysis of variance (A NOVA) and Fisher's probable leasts ignif icant-di fference test for multiple comparisons were used todete rm ine s tati sti cal d if fe renc es among the f oods w i th in each foodgroup (S TATV IEW STUDENT SOFFWARE; A bacus Conceptsmc, Berkley, CA). Linear-regressionanalysis was used to testas so ci ati ons betwe en g lucos e and insul in re spons es and nutri ti onalindexes (MINITAB DATA ANALYSIS SOFFWARE, version7.0; M initab Inc, S tate College, PA ). Test foods not containing aparti cu lar nutri en t we re exc luded f rom thes e analys es . The re fo re ,s ample s iz es f or the c orre lati ons be tw ee n i ndi vidual nutrie nts andthe mean GSs and ISs vari ed f rom 32 to 36 . Mean resu lts f or whi tebread for each fo od g ro up w ere inc lude d in some statistical analy se s, so these co rrelations w ere made w ith 4 3 v alues. One subje ctf rom the pro te in- ric h f oo d g ro up di d no t c ompl ete the f is h te st and

one subjec t f rom the breakfas t cereal group did not complete theS ustain tes t. There fore , in to tal, 5 03 indiV idU al te sts w ere fullycompleted.S tepw ise-m ultiple-reg res sio n analy sis w as used to e xaminethe extent to w hich the different macronutrients and GSs accounted for the variability of the ISs (MINITAB DATAANALYSIS SOFTWARE). For this analys is , the indiv idualw hite bread OS and IS results w ere included for the carbohydrate-rich food group only; therefore, this analysis w as perf ormed w ith 446 i ndiv idual obs ervations fo r 38 f oods . Inc luding the white bread results for each food group (n = 503)sug gests that independent repeat tests w ere do ne fo r w hite


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Food Glucose AUCInsulin AUCInsulin AUC:glucose AUCInsulin AUC pe r gcarbohydrateInsulin AUC per gserving weightGlucose scoreInsulincoremol-miniLpmolmin/LpmolminL'g'pmolminL'g'%%

INSULIN INDEX OF FOODS 1269TABLE 4A reas under the 1 20 -mm plas ma g luco se and insulin res po nse curv es (A UCs), ratio o f ins ulin A UC to g luc ose A UC, the ins ulin A UC per gcarbohydrate and perg serving weight, and mean glucose and insulin scores'

BreakfasterealsWhitebread15621135571756108 1929538144191000100 0All-Bran5994299 61287 1599 1425 340 732 Porridge80 95093 49374 11139 1313 I60 1240 Muesli651260348131181816322345437465Special

K1 0 6 1 4 8 0 3 8 6 3 5 9 5 1 4 1 9 5 1 5 4 7 4 7 0 9 6 6 Ho n e y s ma c k s 9 11 0 9 1 0 21 5 0 6 1 0 81 2 1 8 9 3 1 5 39 6 07 6 76Su s t a i n 9 38 8 9 3 87 5 7 1 0 29 2 0 91 8 5 34 6 66 7 16Co r n f l a k e s 1

1 0 1 1 8 7 6 8 62388 5 1 8 9 1 3 5 2 4 7 6 1175 Gr o u pme a n 7 1 8 3 3 5 7 9 2 5 1 6 9 8 3 9 2 5 9 3 5 7 3 Ca r b o h y d r a t e - r i c hfoodsWhitebread1201312882190111215281 41137201000100 0Whitepasta50114456453156 4891922246 10405

p a s t a 7 4 7 4 5 3 5 5 7 4 6 7 1 0 9 3 1 2 2 1 3 6 8 1 0 4 0 Gr a i n b r e a d 6 89 6 6 5 9 8 3 7 1 0 6 1 2 1 6 62 1 6 28 6 01 2 5 66Br own r i c e 1 1 31 3 6 2 4 06 1 6 5 8 5 1 1 71 1 4 24 1 0 41 8 6 21 1 F r e n c h

f r i e s 7 0 1 1 7 6 4 3 713146 29209 1 9 8 2 8 7 1 1 6 7 4 2Wh i t e r i c e 1 2 91 6 8 1 4 36 8 3 6 9 5 1 4 51 2 4 03 1 1 01 5 7 91 2Who l e - me a lb r e a d 1 0 6 1 4 1 1 2 0 3 1 4 2 0 1 2 2 2 0 2 4 7 3 1 1 1 1 1 4 9 7 1 7 9 6 2 P o t a t o e s 1 4 8 2 4 1 3 9 3 0 1 4 6 7 1 2 0 1 9 2 8 4 3 0 3 8 4 1 4 1 3 5 1 2 1 1 1 Gr o u pme a n 8 4 1 0 4 6 1 1 0 6 8 1 8 2 1 0 6 2 5 8 8 6 7 4 8 P r o t e i n - r i c

foodsWhitebread1211917438315417735387 63185331000100 0Eggs361 1 4 7 4 4 1 0 1 7 1 3 5 929340 1 8 4 5 3 0 642 1631 C h e e s e 4 2 1 0 5 9 9 4 1 5 9 0 2 6 8 1 5 3 6 4 2 5 7 1 5 0 1 3 1 0 6 2755 1 8 4 5 3 Be e f 1 8 6 7 9 1 0 2 1 9 3 1 5 8 3 9 3 9 5 0 1 4 2 1 8 5 1 1 6 Le n t i l s 6 31 7 9 2 6 8 2 1 7 4 3 0 7 1 0 3 3 2 5 6 8 3 7 9 6 2 2 2 5 8 2 Fi s h 2 9 1 4 9 3 5 0 2 0 5 5 7 7 5 5 0 2 2 8 6 2 8 1 3 5 9 8Ba k e d b e a n s 1 1 01 4 2 0 1 0 63 7 7 6 1 8 34 4 5 0 48 7 5 71 1 1 1 4 1 8 1 2 01 9Gr o u p

me a n 9 9 8 3 1 0 3 2 5 8 5 6 1 1 8 6 0 7 5 4 5 6 5 3 654 7 6 1 F r u i t Wh i t eb r e a d 1 7 1 1 9 1 5 5 6 3 1 6 3 2 1 0 5 1 8 3 3 9 3 6 1 6 6 1 7 1 0 0 0 1 0 0 Ap p l e s 8 37 8 9 1 99 1 0 1 1 81 8 1 5 2 1 5 2 02 5 06 5 94Or a n g e s 6 61 1 9 3 4 51 0 7 4 1 6 62 3 1 8 52 1 1 52 3 97 6 03Ba n a n a s 1 3 3

1 2 1 2 4 4 5 1 3 5 3 1 0 8 2 2 2 2 4 2 4 4 5 5 7 9 1 0 8 1 Gr a p e s 1 2 61 4 1 2 2 9 31 1 9 0 1 1 31 9 2 1 6 2 1 3 13 7 49 8 26Gr o u pme a n 1 0 7 5 16 0 5 1 2 41 0 1 9 41 1 2 82 6 15 7 13Sn a c k s

andonfectioneryWhitebread1592915592237610424340521662510001000Peanuts2073047 8 2 8 2 1 4 8 8 5 6 4 1 5 3 8 0 2 2 1 2 4 2 0 Po p c o r n 7 11 2 6 5 3 76 7 9 1 0 93 2 2 3 9 2 5 1 3 91 4 6 21 6 5 49Po t a t o c h i p s 7 71 5 8 1 9 5 1 5 7 7 1 6 97 8 3 6 77 1 1 8 63 6 5 29 6 11 4 I c e

c r e a m9 3 1 7 1 2 3 4 8 1 8 6 7 1 7 2 3 8 4 7 9 7 2 1 0 3 1 6 7 0 1 9 8 9 3Yo g u r t 8 82 3 1 5 6 1 11 8 0 8 1 6 73 3 4 1 5 4 8 6 57 6 21 5 1 1 51 3Ma r s B a r 9 81 0 1 6 6 8 21 8 9 6 2 1 86 5 4 4 1 5 0 3 0 9 3 5 7 91 3 1 2 21 5 J e l l y b

productsWhitebread1291517599305818864383 67187331000100 0Doughnuts7814124452402113 21480931913763

1114 3 0 5 3 4 7 2 1 7 8 5 4 4 6 7 I 1 3 2 2 3 5 4 5 6 1 4 8 2 2 C r a c k e r s 1 3 9 2 6 1 4 6 7 3 2 6 8 6 3 3 1 1 0 4 3 5 4 6 5 2 5 3 4 6 1 1 8 2 4 8 7 2Co o k i e s 9 21 2 1 5 2 2 33 8 2 2 0 0 5 7 4 3 61 1 0 2 9 87 5 7 41 1 9 21 5Gr o u pme a n 1 2 6 8 11 3 2 5 2 6 15 6 4 6 84 7 2 3 62 4 7 77 8 35

I 1 SEM . Mars Bar, M ars Confectionary Australia, Ballarat, Australia; All-Bran, Special K, H oneysmacks, Sustain, and Cornflakes: Kellogg'sAustralia Pty Ltd. Pagewood, Australia.


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1 2 7 0 HOLT ET ALbread, w hich artificially increases the accuracy of any calculation involving w hite bread.

RESULTSFa s tin g g lu co s e a nd in s ulin c on ce n tra tio nsWithin each food group, the subjects' average fastingplasma glucose and insulin concentrations were not significantly different among the foods. Mean fasting plasmaglucose concentrations did not vary significantly among thesix food groups, whereas mean fasting insulin concentrations were more variable, ranging from 4 2o 1 20 pmol/ L.Fasting insulin concentrations were not more variable infemales than in males and there were no significant differences at various stages of the m enstrual cycle. A significantcorrelation was found between m ean fasting insulin concentrations and mean BM I values for the six groups of subjects

( r . 81 , P < 0 . 05 , n 6 ) .Pos tp r and i al g l u c o seand i n s u li n r es ponsesA s w ith any biological response, there w as betw een-subjectvariation in the glucose and insulin responses to the sam e food.Two-way ANOVA was used to examine the ranking of eachsubject's responses to the different test foods within a foodgroup (ie, interindividual variation). There w ere significantdifferences among the subjects in the rank order of their glucose AUC responses except within the fruit and protein-richfood groups. T here w ere also significant differences am ong thesubjects' rank order of insulin AUC responses w ithin all foodgroups. H ow ever, individual subjects w ithin each food groupconsistently produced relatively low , m edium , or high insulinresponses. F urtherm ore, subjects produced their low est insulinresponses for the least insulinogenic foods and their highestinsulin responses for the m ost insulinogenic foods w ithin each

f ood g roup .10 0

There were large differences in mean glycemic and insulinresponses to the foods, both within and between food groups.M ean glucose and insulin AUC results, mean GSs and ISs, andthe mean ratios of insulin to glucose AUCs (the amount ofinsulin secretion in relation to the blood glucose response) arelisted in Table 4. M ean GSs and ISs were calculated for eachfo od g rou p b y av erag in g the sco res fo r all test fo ods w ith in thefood group. On average, the snack food group produced thehighest food group IS (89%), followed by bakery products(8 3% ), carbo hy drate-rich fo od s (74%), fruit (71%), p ro teinrich foods (61%), and breakfast cereals (57%). Average GSsfor the food groups did not follow the same rank order (Figure1 ). T h e c arb o hy dra te -ric h fo od g ro u p p ro d uc e d th e h ig h e s taverage GS (88%), followed by bakery products (77%), snackfoods (65% ), fruit (6 1% ), breakfast cereals (59% ), and proteinric h fo od s (54% ). In te re s tin g ly , th e G S ran k o rd er is n ot p roportional to the average total carbohydrate content of each foodgroup, w hich highlights the influence of other food factors (eg,fiber and processing) in determ ining the rate of carbohydrated ig es tio n a nd a bs or pt io n.Overall, among the 38 test foods, jellybeans produced thehighest m ean IS (160 16% ), eightfold higher than the low estIS (for peanuts: 20 5% ) (F igure 2). W hite bread, the standard food, consistently produced one of the highest glucose andinsulin responses (peak and AUC) and had a higher IS thanm ost of the other foods (84% ). A ll of the breakfast cereals w eresignificantly less insulinogenic than w hite bread (P < 0.001).All-Bran and porridge both produced a significantly lower ISthan the other cereals (P < 0.001), except muesli. Despitecontaining more carbohydrate than porridge and m uesli, A llBran produced the lowest G S. Baked beans, which containconsiderably m ore carbohydrate than the other protein-richfoods, produced a significantly higher GS and IS (P < 0.001).On a ve ra ge , fis h e lic ite d tw ic e a s muc h in su lin se cre tio n a s d idthe equivalent portion of eggs. W ithin the fruit group, orangesand apples produced a significantly lower GS and IS than

0 Glu co seco re. I nsulincore80

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40

20

0

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Break fas tcerea ls C arb oh yd ra te - B ak eryrich fo od s p roduc tsProteinric h fo o ds Fru it S n a c ks a ndcon fec t ioneryFIGURE 1. Mean(SEM)glucoseand insulinscoresforeach food group.


8/13

. . .@White

breac . IPrth ifr@c.

Doughnu t sCroissantsCa k eCrack e r sCook ie s

PeanutsI=@lIII;t-1@PopcornI=iiPotatochipsI='=iIcecream l;lIY ogurtI

. lip

IN SUL IN IN DEX OF FOO DS 1271I@ 1

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All-BranPorridgeMues l i

OUSL4I(J

Eg@CheeseBee fLentilsFishBeans

ApplesO r a n g e sBananasGr a p e sBrown pas taW h i te pas taGrain breadBr o wn r i c e

FrenchfriesWhit e r ic eWho l e -mea l b r e ad

-i.11=1

Je l lybeans1 0 0 2 0 0

In su lin s co re (%)FIGURE 2 . Mean (SEM) insul in s co re s f o r 1000- Id port io ns o f t he t es t f o od s. W h it e b r ead wa s t he re f ere nc e f o od ( in su li n s co re = 100%).A l l-Branc ere al, S p ec ial K c ere al, H on ey sm ac ks c ere al , S u st ain c ere al , an d C orn flak es , K e ll og g's A u strali a Pty L td . Pag ew o od , A u strali a; M a rs B ar c an dy b ar, M a rsConfectionary A ustralia, Ballarat, A ustralia.

grapes and bananas (P < 0.05 to P < 0.001), despite containing a sim ilar am ount of carbohydrate.Potatoes produced signif icantly higher G Ss and IS s than allof the other carbohy drate-rich foods. W hite bread produced ahigher GS and IS than grain bread (P < 0.05 and P < 0.001respectiv ely ), but w hole-m eal bread and w hite bread had similar scores. W hite and brow n rice had sim ilar GS s and IS s, asdid w hite and brow n pasta. A m ong the bak ery products, crackers produced a signif icantly higher G S than the other test f oods,but there w ere no signif icant dif f erences in IS s w ithin thisgroup (all tended to be high). A m ong the snack foods, jellybeans produced a signif icantly higher G S and IS than the otherfoods in this group. Despite containing sim ilar am ounts ofcarbohy drate, jelly beans induced tw ice as m uch insulin secretion as any of the four f ruits. T he candy bar and y ogurt, w hich

both contained large am ounts of sugar in com bination w ithf at or protein, produced relativ ely high IS s. Popcorn and potatochips elicited tw ice as m uch insulin secretion as peanuts( P < 0.05 and P < 0.01, r espectivel y) .S ignif icant dif f erences w ere found both w ithin and am ongthe food groups w hen the insulin A UC responses w ereexam ined as a function of the food's carbohydrate content(T able 4). On av erage, protein-rich foods produced thehighest insulin secretion per gram of carbohydrate (foodgroup m ean: 18 607 pm ol . m m . L ' . g@1) (because oftheir m ostly low carbohy drate contents), follow ed by bak eryproducts (468 pm ol . m m . L @ . g1), snack foods (416pm ol . m m . L g 1) f ruit (194 pm ol . m m . L g 1),carbohydrate-rich foods (182 pm ol . mm . L@ . g'), andbreak fast cereals ( 169 pm ol . m m . L g .W hen the


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1272 HOLT ET AL

S

insulin AUC re sponse w as e xam ine d in re latio n to the fo od'sserving size (g), the bakery products were the most insulinogenic (food group mean: 236 pmol . mm . L g 1), followed by snack foods (163 pmol . mm . L g 1), carbohydrate-rich foods (62 pmol . mm . L g 1 ), pro te in- ric hfoods (53 pmol . mm . L g 1), breakfast cereals (39pmol . mm . L g ,nd fruit (28 pmol . mm . L g 1).The se re sults re fle ct the insulino ge nic e ffe cts o f pro te in andfat.In su lin re s po ns e s in re la tio n to g lu co se re s po ns e sOverall, mean glucose and insulin AUC values were positively correlated (r = 0.67, P < 0.001, n = 43), as were thepeak glucose and insulin values (r = 0.57, P < 0.001, n = 43).Henc e, the mean GS s and IS s w ere hig hly c orre late d (r = 0 .7 0,P < 0.001, n = 38) (F igure 3). The peak glucose concentration

(c ha ng e fro m fa s tin g) c orre la te d p os itiv e ly w ith g lu co s e A UCvalues (r = 0.74, P < 0.001, n = 43) and peak insulinc onc entratio ns w ere propo rtio nal to the ins ulin AUC value s(r 0.95, P < 0.001, n 43). In addition, the observed GSsfo r 1 00 0-U po rtio ns o f the fo ods c orre late d w ith pre vio uslypublis hed GI value s bas ed on portions o f foods containing 50 gcarbohydrate (r = 0.65, P < 0.001, n = 32). Six test foods(chocolate chip cookies, eggs, cheese, beef, fish, and Hone y s m a c k sc e r e a l) w e r e n o t in c l u d e din t h is a n a l y s isb e c a u s eG Iv al ue s w ere no t av ail abl e.Insulin AUC values were divided by glucose AUC values todetermine w hich foo ds w ere marke dly insulino genic relativ e toth eir g ly c e m ic e ffe ct (T a ble 4 and Figu re 4 ). O n ave rag e , th ep r o t e in - ric h fo o d s s t im u la t e da la r g e am o u n t o f in s u lin s e c r eti on re lati ve to thei r g lycemic response, f ol lowed by the bakeryproducts, snack foods, fruit, carbohydrate-rich foods, andb re a k f a s t c e r e a ls .

4)1@0U4)C

4)C

20 0

FIGURE 3. Relationbetweenthe meanglucoseandinsulinscores(r =0.74, P < 0.001, n = 38).

R e la t io n s b e t w e e n m e t a b o lic r e s p o n s e sa n d n u t rie n tcontents of the foodsCorre lati ons between the macronutri ent compos iti ons o f thete st fo ods and the mean IS s are s hown in Fig ure 5 . The po rtio nsize (energy density: kJ/g), water, and fiber contents of thefoods were not significantly related to the mean ISs. There lation be tween pro te in contents and IS s was negativ e but no t

significant (r 0.24,n = 38). The mean ISs w ere positivelyrelated to total carbohydrate content (r = 0.39, P < 0.05, n =36) and sugar content (r = 0.36, P < 0.05, n = 36), but wereno t s ignif ic antl y re lated to s tarch content ( r = 0 .09 , = 3 0).Fat c onte nt w as ne gativ ely re late d to the mean IS (r = 0.27,N S, n = 3 6). When e xpressed as a percentag e o f to tal e nerg y,fat (r = 0.27, S , n = 36) and protein (r = 0.24, S, n =38) w ere negatively associated w ith the mean IS , w hereas totalcarbo hydrate w as po sitive ly related (r = 0 .3 7, P < 0.0 5, n36).Relati ons be tween the GSs and the nutri ents l argel y fol lowedthe same dire ctio ns as the IS c orre latio ns. Mean GS s w ere no tsig nific antly related to the fo ods' se rving siz es o r w ater o r fiberc ontents . Mean GSs corre lated negativ ely w ith f at ( r = 0.38,P < 0.05, n = 36) and protein (r = 0.38, < 0.05, n = 38)c ontents , and po siti ve ly w ith to tal c arbohydrate c ontent ( r =0.32, NS, n = 36). Unlike the ISs, the GSs were significantlyrelated to starch content (r = 0.43, P < 0.05, n = 30) but notsug ar c ontent (r = 0.07,NS, n = 36). When expressed as apercentageof total energy, fat (r = 0.38,P < 0.05, n = 36)and protein (r = 0.39, < 0.05, n = 38) were negativelyas soc iated with mean GSs , whereas to tal carbohydrate contentwas positively related (r = 0.46, P < 0.01, n = 36).Stepwise-multipl e- regress ion analys is o f the 446 indiv idualre sults fo r the 38 f oods was pe rf ormed to de te rm ine the extentto whic h the mac ronutrie nts and GSs ac co unte d fo r the v anabil ity o f the ISs . Unfortunate ly , i t was not pos sibl e to generatea s ing le mul tiple -re gre ss ion equati on that inc luded all o f themacronutrients because some pairs of nutrients w ere highlycorre lated ( eg , f at and prote in , f iber and water, to tal carbohydrate and sugar or s tarch, and sugar and s tarch) . The regress ione quatio n that inc luded all o f the m ac ronutrie nts had unac ce ptably high variance inflation factors. Therefore, tw o separateregression equations w ere generated that w ere limited to thefacto rs that w ere me asured and no t inte rde pendent. Equatio n 2inc lude s fat but no t pro te in, whe reas equation 3 i nc lude s prote in but no t f at:IS = 72.4 + 0.383 GS . 88 fat .1 03 wate r

+ 0 .5 09 s u ga r .4 21 s ta rch (2 )

fo r w h ic h S D = 3 7 .3 4 ,R 2 = 3 3 .1% ,a n d a d ju s t e dR 2 = 3 2 .4% .P values (significance found in the linear-regression analysisf or the as soc iati ons be tween the ind iv idual nutri ents 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).IS = 23.2 + 0.383 05 + 0.785 protein . 098 wate r

+ 1.29 s ug a r + 0 .377 s ta rch (3 )for w hich SD = 37.42, R2 = 32.8%, and adjusted R2 = 32.1%.P values are as follows: GS, water, and sugar (P < 0.000);protein (P < 0.003); and starch (P < 0.02).

.

S

S

00 100G lu co s e s c ore (% )


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INSULIN INDEX OF FOODS 1273PorridgeAll-BranComfiakesSpec ia l KS u s t a i nHoneysmacksMues l i

BrownriceBrownpa s t aWhite riceGra in b r e adWhitebreadPotatoesWhole-meal breadFrench r ie sWhite pastaBananasGrapesApplesOrangesPopcornJellybeansYogurtChipsIcecreamPeanutsMarsBar

DoughnutsCak eCoo id e sCrackersCroissantEggsBeansCheeseLentilsFi s hBe@

I. .I- ,

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@1-I

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0 500 1000 1500 2000 2500 3000Insu linAU C/G iuco seUC

FIGURE 4. Ratio of insulin area underthe curve (AUC) to glucose AUC responses.I SEM. All-Brancereal, Special K cereal, Honeysmacks cereal,Sustaincereal,andCornflakes,Kello gg'sAustraliaPty Ltd.Pagewood,Aus tralia;MarsBar candybar,MarsConf ectionaryAus tralia,Ballarat,Australia.Linear-regression analysis of the individual OS and IS res ults had an R2 value of 2 3%. There fore , the g ly cemic respo nse

w as a significant predictor of the insulin response, but itac counted f or only 23% of the variability in insuli nemi a. Themacronutri ents (prote in or fat, water, sugar, and s tarch) werealso significant predictors but together accounted for onlyano the r 10% of the variabil ity o f the i nsulin re spons es . Thus ,we ca n e xp la in on ly 33% o f th e va ria tio n o f th e in s ulin res ponse s to the 3 8 fo ods s tudie d.DISCUSSIONThe re sults o f this s tudy conf irm and als o challe nge s ome o four bas ic as sumptions about the re lati on be tween f ood intake

and insulinemia. W ithin each foo d g roup, there w as a w iderange o f insulin res po nse s, despite similarities in nutrie nt co rnposition. The important Western staples, bread and potato,were among the most insul inogen ic foods . S imil arl y, the h ighlyref ined bakery products and snack foods induced substantial lym ore in su lin s e c re tio n p e r kilo jo u le o r p er g ra m o f fo od th a ndid the o the r te st foods . In contras t, pas ta, oatmeal porridge,and Al l-Bran cereal produced re lati ve ly l ow insul in responses ,de spi te the ir high carbohydrate c ontents . Carbohydrate wasquanti tati ve ly the major macronutri ent for most foods . Thus , i tis no t surpris ing that w e o bs erv ed a stro ng c orre latio n betw ee nGSs and IS s (r = 0 .7 0, P < 0 .0 01 ). However, s ome pro te inand fat-ric h fo ods (e gg s, be ef, fis h, le ntils , c he ese , c ake , anddo ug hnuts) induced as much insulin sec retio n as did some


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0C

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0 20 40 60Pro t e i n ( g ls e r v lng )

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0 20 40 60

1274 HOLT ET A L20 0

10 0

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0 10 20F ibe r ( 9 / s e r v i ng )

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0 20 40 60T otal carbo hy drate (9 /se rv in g)

0 i I0 20 40 60Sug a r (9 /s e rv in g )

14 0S

10 0S

S S0S S

S S

60

7c10 0 10 20 30

FIGURE 5 . Re lat io ns b etween the nut ri en t c on te nt s o f t he t es t f o od s and the mean insul in s co re s. F ib er: r = 0 .1 0,S , n = 3 2; p ro te in : r = 0.24,NS , n = 3 8; to tal c arb oh yd rate :r = 0 .3 9, P < 0 .0 5, n = 3 6; s ug ar: r = 0 .3 6, P < 0 .0 5, n 3 6; s tarc h:r = 0.09,S , n = 3 0; f at: r = 0.27,


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INSULIN INDEX OF FOODS 1275lin respo nse to all of the nutrients in the foo ds as normallyconsumed. A standard portion size of 1000 kJ was chosenbecause this resulted in realistic serving sizes for most of thefoods except apples, oranges, fish, and potatoes. A lthoughsome of the protein-rich foods may normally be eaten insmalle r quantiti es , f is h, be ef , c he es e, and egg s s till had larg erinsul in re spons es pe r g ram than did many o f the f oods cons is ting predominantly o f c arbohydrate . A s obs erv ed in previousstudies, consumption of protein or fat w ith carbohydrate increases insulin secretion compared w ith the insulinogenic effect of these nutrients alone (22, 3032). T his may partlye xplain the marke dly hig h ins ulin re spons e to bake d be ans.D ri ed hancot beans , which are s oaked and bo iled, are li ke ly tohave a lower IS than commerc ial baked beans , which are morereadily digestible.The resu lts conf irm that increased insul in secre ti on does notac co unt fo r the low g ly cemic re sponse s pro duc ed by low-G Ifo od s s uch a s p a s ta , p orrid g e , a nd All-Bra n c e re a l (3 3 ). F urthermore, equal-carbohydrate servings of foods do not necessarily stimulate insulin sec retio n to the same ex tent. Fo r ex ample , i soenerge ti c s erv ings o f pas ta and potatoes both contained=,%50g carbohydrate, yet the IS for potatoes w as three timesg reate r than that fo r pasta. S im ilarly , po rridg e and y og urt, andwho le -g rain bre ad and bake d be ans , pro duc ed disparate IS sdespi te their s imilar carbohydrate contents . These f indings , l ikeo thers , chal lenge the sci enti fi c bas is o f carbohydrate exchangetabl es , whi ch as sume that po rti ons o f di ff ere nt f oo ds c ontaini ng1 0 15g carbo hy drate w ill hav e equal phy sio lo gic e ffec ts andw ill re quire e qual amounts o f e xo ge nous insulin to be metabo liz ed. It is po ssible that preprandial insulin dos es fo r patientswith NIDDM could be more scientifically estimated ormatc he d on the basis o f a meal's av erag e ins ulinemic e ffe ct inhealthy indiv iduals, rather than o n the basis o f the meal'scarbohydrate content or 01 . Further research i s required to te stthis hy po the sis. The adve nt of intensive insulin the rapy and theadded risk of hypoglycemia increases the urgency of thisre se arch (34 ).Our study w as undertaken to test the hy po thesis that thepo stprandi al ins ul in re spo ns e was no t ne ce ss ari ly pro po rti onalto the blo od g luco se respo nse and that nutrients o ther thanc arbo hydrate influe nc e the o ve rall le ve l o f insulinem ia. MultipIe -re gre ss io n analy si s o f the i ndi vidual re sul ts s howe d that theg ly cemic re spons e w as a sig nific ant pre dic to r o f the ins ulinrespo nse, but it acco unted fo r o nly 2 3% o f the variability ininsul inemia. The macronutri ents (prote in or fat, water, sugar,and s tarch) were als o s ignif ic ant predic to rs , but toge the r accounted for only another 10% of the variability of the insulinre sponse s. Thus, w e c an e xplain o nly 3 3% o f the v ariatio n o fthe ins ulin re sponse s to the 3 8 fo ods unde r e xaminatio n. Thelow R2 value indic ate s that the macronutrient c omposition o ffo od s h as re la tive ly lim ite d p owe r fo r p re dic tin g th e e xte nt o fpo stprandial ins ulinemia. The rate o f starc h dig estio n, theamount o f rapidly avai lable g lucos e and re sis tant s tarch, thedeg re e ofo sm olality , the v isco sity o fthe g ut's co nte nts , and therate of g as tric em pty ing m ust be o ther im po rtant facto rs influenc ing the degre e o f po stprandial i nsulin s ec re tion. Furthe rresearch i s required to examine the re lati on between pos tprandial insulinemia, food form, and various digestive factors for amuch larg er rang e o f fo ods to produc e a re gre ss io n e quatio nw ith g re ate r pre dic tiv e v al ue .

Dietary guidelines for healthy people and persons withNIDDM have undergone considerable change and will continue to be mo dified as o ur understanding of the relatio nsbe tween di etary patte rns and dis eas e improve s. The re is c onc ern that hig h- carbo hy drate di ets may i nc re as e triac yl gl yc ero lconcentrations and reduce high-density l ipoprote in concentrations (35, 36). The use of diets high in monounsaturated fat isan attempt to o ve rc ome the unde sirable e ffe cts o f s ome hig hcarbohydrate d ie ts on plasma l ip ids (3739).However, d ie tshigh in monounsaturated fat are unlikely to facilitate w eightlo ss . A low -f at die t bas ed on le ss -re fined, c arbohydrate -richfoods w ith relatively low IS s may help enhance satiety and aidw eight loss as w ell as improve blood glucose and lipid control(4).The re sults o f this s tudy are pre lim inary but w e hope the ys timulate dis cus si on and f urthe r re se arc h. Addi tio nal s tudi es areneeded to dete rm ine whe ther the IS concept i s u se fu l, reproduc ib learound the w orld, predictable in a mix ed-me al c ontex t, and cliiii cal ly us eful i n the tre atment o f d iabe te s mel li tu s, hype rl ip idem ia,and overweight. Studies examining the relation between postprandial insul inemia and the storage and oxidation of fat, prote in, andc arbohydrate may provide further ins ight into the re lati on betwe enfu e l m e t a bo lis m a n d s a t ie ty , a n d e s t a b lis h w h e th e r lo w -in s u lin emic diets can facilitate greater body fat loss than isoenergetichigh- insWinemic die ts .We thank Efi Farmakalidisfor her assistancein the planningof thisstudy and NatashaPorter forher technical assistance with the experimentalwork for the carbohydrate-rich food group.

REFERENCES1 . Jenkins DJA, Wolever TMS, Kalmusky J, e t a l. Low g lycemic indexcarbohydrate foods in the management of hyperlipidemia. Am J Clin

Nu t r 1 9 8 5; 4 2 : 6 0 4 1 7 .2 . Jenk ins DJA , Wo le ve r TMS, Vuksan V . e t al . N ibb ling v s gorg ing :metabolic advantages of increased meal frequency . N EngI J Med1989;32l:92934.3. Bymes SE, Brand Miller JC, Denyer GS. D evelopment of insulinre si sta nc e i n rats af te r l ow - v s hi gh- amyl os e di ets . B ac he lo r o f S ci enc eHonours The si s, Department o f B io chem is try , The Unive rs ity o fSydney , 1993 .4 . S labber M , B arnard HC, Kuy l JM , D annhaus er A , S chall R. Effects o flow-insulin-response,energy-restricted dieton weight loss and plasmainsulin concentrations in hyperinsulinemic obese females . Am J ClinNutr l994;60:4853.5. Lerer-MetzgerM, Rizkalla SW, Luo J, et a l. Effects of long-termlow-g lycaemic index s tarchy food on plasma g lucose and l ipid concentrations and adipose tissue cellularity in normal and diabetic rats .Br J Nutr 1996;75:72332.6. Bymes SE, Brand MillerJC, DenyerGS. Amylopectinstarch promotes the development of insulin resistance in rats. J N utr1995;125:14307.7 . S a lmr on,As che r ioA, Rimin EB, e t a l .Die ta ry f ibe r , g lycem ic load ,and risk o f N!DDM in men. Diabete s Care l997 ;20 :545-50.8 . S almronJ, Mans on JE , Mei r J, e t al . D ie tary f ibe r, g ly cemi c l oad, a ndri sk o f non-insul in-dependent diabe te s me ll itus in women. JAMAl 9 9 7; l 2 : 4 7 2 7 .9. Modan M, Halkin H, Almog 5, et al. Hyperinsutinemia:a link betweenhy pertensio n, o be sity and gluco se into le ranc e. J Clin Inve stl985;75:80917.1 0. Zavaroni I, Bono ra E , Pag li ara M, e t a! . R isk f ac to rs f or c oronaryartely disease in healthy persons with hyperinsulinaemia and normalglucose tolerance. N Engi J Med l989;320:7026.


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1276 HOLT ET AL11 . DeFronzo RA, Ferrannim E. Insulin resi stance . A multi face ted syndrome responsible for NIDDM, obesity , hypertension, dyslipidemia,and atherosc lero ti c card iovascu lar di sease. D iabe te s Care199l;14:17394.1 2. D eFro nzo RA , B onado nna RC, Fe rrannini E. Patho gene sis ofNIDDMabalanced overview. Diabetes Care 1992;15:3l868.13 . Coldi tz GA, Manson JE, StampferMi , RosnerB, Willett WC, SpeizerFE. D iet and risk of clinical diabetes in women. Am J Clin Nutr

1992;55:lOl823.14. HaffnerSM, Valdez BA, Hazuda HP,et al. Prospective analysis of theinsulin-resistance syndrome (syndrome X). Diabetes l992;41:715-22.1 5. L il li oja 5 , Mo ft DM, Sprau l M, Ctal . In su lin re si stance and insul insecretory dysfunction as precursors of non-insulin-dependentdiabetesme ll itus. N Eng l J Med 1993;329:198892 .16. StoutR.Hypennsulinaemiaas a riskfactorforcardiovasculardisease.hi t D iabe te s F ed Bul l 1 99 4;3 9:l 8 9 .17 . Zavaroni I, Bonini L, Fantuzz i M, e t al . Hyperinsul inaemia, obes ity ,and syndrome X. J Intern Med l994;235:516.1 8. Wo le ve r TMS, Jenk ins DJA , Jenk ins AL , Jo ss e RG. The g ly cemicindex : me tho do lo gy and c linic al implic atio ns. Am J Clin N utrl99l;54:846-54.19. ServiceFJ, Pizza PA, HallLD,Ctal.Prandialrequirementsn insulindependent d iabeti cs : e ff ec ts o f s iz e, time o f day , and s equenc e o fmeal s. J C li ii E ndo cri no l Metab 1 98 3;5 7:9 31 -. 6.2 0. S imps on RW, McDonald J, Wahl qv is t ML, A lte y L, Outc h K . Mac ronutri ents hav e di ff ere nt metabo li c e ff ec ts i n nondi abe ti cs and di nbetics. Am J Clii i Nutr 1985;42:44953.2 1. Nuttal l FQ , Moo radi an AD , Ganno n MC, e t al . E ff ec t o f pro te iningestion on the g lucose and insul in response to a s tandardized oralglucose load. Diabetes Care l984;7:46570.22. Krezowski P, Nuttall FQ, Gannon MC, Bartosh NH. The effect ofprotein ingestion on the metabolic response to oral glucose in normalindividuals . Am J Clin Nutr l986;44:84756.2 3. C oll ie r G , McLe an A , O 'D ea K . E ffe ct o f c o- ing es ti on o f f at o n themetabolic responses to slowly and rapidly absorbed carbohydrates .Diabetologia 1984;26:50-.4.2 4. Ganno n MC, N uttall FQ, W es tphal S A, S eaquist ER. The effect o f fatand carbohydrate on plasma glucose, insulin, C-peptide, and triglycerides in normal male subjec ts . J Am Coll Nutr l993 ;12 :36 -41 .25. Nuttall FQ, Gannon MC. Plasma glucose and insulin response tomacronutrients in nondiabetic and NIDDM subjects . Diabetes Carel991;l4:82438.2 6. M org an L Insulin sec retio n and the entero -insular ax is . In: Rau PR,

e d. N utrie nt re gulatio n o f ins uli n s ec re tio n. Lo ndo n: Po rtl and Pre ssLtd. 1992:122.2 7. Teff K. Cephalic phase insulin release in humans: mechanism andfunction. In: Fernstrom J, Miller G, eds . Appeti te and body we ightregulation. Sugar, fat and macronutrient substitutes . London: CRCPress, 1993:3749.28. Holt SHA, Brand MillerJC, Petocz P. Farmakalidis E. A satiety indexo f common foods. Eur J Clin Nutr 1995 ;49 :67590 .2 9. Wol ev er TMS , Je nki ns DJA . The us e o f the g ly cemi c i nde x i n predicting the blood glucose response to mixed meals. A m J Clin N utrl986;43:16772.3 0. Es tri ch D , Rav ni k A , S chli ef G , Fukay ama 0 , K ins el l L E ff ec ts o fc o- ing es ti on o f f at and pro te in upon c arbohydrate -i nduc ed hype rg lycemia. Diabetes 1967;16:2327.3 1. Rasmuss en 0 , Whi ther E , Arnfred J, Hermansen K . Compari son o fblood glucose and insulin responses in non-insulin dependent diabeticpatients . EurJ Clin Nutr l988;42:95361.32. Peters AL, Davidson MB. Protein and fat effects on glucose responsesand insulin requirements in subjects with insulin-dependent diabetesme ll itus. Am J Clin Nutr 1993 ;58 :555-60 .33 . Wolever TMS, Katzman-Rel le L, Jenkins AL, e t al . Glycaemic indexof 102complex carbohydrate foods in patients with diabetes . NutrResl994;l4:65169.3 4. The D iabe tes Co ntro l and Complicatio ns Trial Res earch Gro up. Thee ff ec t o f intens iv e tre atment o f d iabete s on the dev el opment andprogression of long-term complications in insulin-dependent diabetesmellitus . N EngI J Med 1993;329:97786.35 . Coulston AM, Hollenbeck CB, Swislocki ALM, Reaven GM. Pers istence of hypertrig lyceridaemic effect of low-fat, high-carbohydratediets in NIDDM patients. Diabetes Care 1989;l2:94lOl.36 . Rive llese A, Giacco R, Genovese 5 , e t al . Effec ts o f changing amountof carbohydrate in diet on plasma lipoproteins and apolipoproteins in

ty pe II diabetic patients. D iabe tes Care 1 99 0;1 3:4 46 -8 .37. Garg A , Grundy SM, Unger RH. Compari son o f e ff ec ts o f h igh andlow carbohydrate diets on plasma lipoproteins and insulin sensitivity inpatients with mild NIDDM. Diabetes l992;4l:127885.38 . Garg A, Bantle JP, Henry RR, e t al . Effec ts o f vary ing carbohydratecontent of diet in patients with non-insulin-dependent diabetes. JAMA1994;271:14218.39. Campbe ll LV , Marmot PE, Dyer JA , Borkman M, Sto rl ie n LH. Thehi gh-monouns aturate d f at di et as a pra cti cal al te rnati ve f or N IDDM.Diabetes Care 1994;17:17782.

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