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A BSTRAC T The aim of this study was to system atically
c om p ar e p os tp ra nd ia l in su lin r es po ns es to is oe ne rg etic 1 00 0-U
(240-kcal) portions of several com mon foods. C orrelations w ith
n ut rie nt c on te nt w er e d et er mi ne d. T hir ty -e ig ht f oo ds s ep ar at ed in to
s ix f ood cat egori es ( fr ui t, bake ry produc ts , s nacks , car bohydra te
r ic h f oo ds , p ro te in -ri ch fo od s, a nd b re ak fa st c er ea ls ) w er e fe d t o
g ro up s o f 1 1â €” 13 ea lt hy s ub je ct s. F in ge r-p ri ck b lo od s am pl es w er e
obtained every 15 m m over 120 m m. A n insulin score w as calcu
lated from the area under the insulin response curve for each food
w 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 nd
among the food categories and also among foods containing a
sim ila r am ou nt o f ca rb oh yd rate. O ve rall, g lu cose an d insu lin
scores were highly correlated (r = 0.70, P < 0.001, n = 38).
H o we ve r, p ro te in -r ic h f oo ds a nd b ak er y p ro du cts ( ric h in f at a nd
r ef ined car bohydra te ) e li ci ted i ns ul in r es ponses t ha t w ere d is p ro
portionately higher than their glycemic responses. Total carbohy
drate (r = 0.39, P < 0.05, n = 36) and sugar (r = 0.36, P < 0.05,
n = 36 cont en ts were posi ti ve ly r el at ed t o t he mean insul in s core s
whereas fat (r —¿0.27,S, n 36) a nd 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 lin
scores m ay be relevant to the dietary m anagem ent and pathogen
e si s o f n on -i ns ul in -d ep en de nt d ia be te s m e ll it us a nd h yp er li pi de m ia
an d m ay h elp in crease th e accu racy o f estim atin g prep ran dial
in su lin req uirem en ts. A m J C lin N utr l9 97 ;6 6:l2 64 †”76 .
KEY W ORDS Insulin, glycem ic index, NIDDM , non
in su lin -d ep en de nt d ia be te s m e ff itu s, d ia be tic d ie t, h yp er lip id
e m ia , c arb oh yd ra te , in su lin s co re , g lu co se s co re , a re a u nd er th e
c ur ve , h um an s
INTRODUCTION
The insulinem ic effects of foods m ay be relevant to the
tre atm en t a nd p re ve ntio n o f w eig ht g ain , n on -in su lin -d ep en
dent d iabet es m e ll it us ( N ID D M) , and ass oci at ed com pl icat ions.
R ec en t stu die s h av e s ho wn th at c arb oh yd ra te -ric h d ie ts , w hic h
result in high p ostp rand ia l g luc ose an d insu lin resp on ses, are
a 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 y
fa 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 associated
w 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 erin
s ul in em ia . P ro lo ng ed o r h ig h d eg re es o f p os tp ra nd ia l i ns ulin e
m ia are thought to contribute to the developm ent of insulin
re 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 s
is of both theoretical and practical significance.
Postprandial blood glucose responses have been the focus of
much research because of their im portance for glycem ic con
trol in patients with diabetes. It is now well accepted that
d iffe re nt fo od s c on ta in in g e qu al a mo un ts o f c arb oh yd ra te c an
produce a w ide range of blood glucose responses. T he glyce
m ic index (G I) m ethod w as developed to rank foods according
to th e ex te nt to w hich th ey in crease b lo od g lu co se co ncen tra
tions (18). Tables of GI values of com m on carbohydrate
containing foods are a useful guide to help people with diabetes
ch oo se fo ods that p ro du ce sm aller glyce mic resp on ses. H ow
ever, the G I concept does not consider concurrent insulin
responses and few studies have reported GI values and their
accom panyi ng i ns u li n r es ponses.
T he extent to w hich different dietary factors affect post
prandial insulinem ia has not been w ell researched because
insulin secretion is largely assum ed to be proportional to
postprandial glycem ia. Furtherm ore, hyperglycem ia is
th ou gh t to b e m ore re lev ant to th e se con dary co mp lication s
of NIDDM because the abnormal insulin secretion or action
in p eo ple w ith d iab etes is co ntro lled w ith ex og eno us in sulin
or m edications that counteract insulin resistance. H ow ever,
know ledge of factors that influence both postprandial gly
cem ia and insulin secretion in nondiabetic persons is re
quired to devise treatm ent strategies that w ill com pletely
norm 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 l
in sulin em ia in th e etio lo gy an d treatm ent o f N ID DM , w e n eed
to be able to systematically rate insulin responses to comm on
foods. If we are to compare insulin responses to foods, what is
the best basis of com parison? Should we com pare insulin
responses to portions of food representing a normal serving
size, portions containing an equal amount of carbohydrate, or
portions containing an equal am ount of energy? 01 tables
represent the glycem ic effects of equal-carbohydrate portions
I From the Hum an Nutrition Unit Department of Biochem istry The
U ni ve rs ity o f S yd ne y; a nd th e S ch oo l o f M a th em ati ca l S ci en ce s, T he
Univers i ty of Technology, Sydney, Austra l ia .
Supported by research grants from The University of Sydney and
Kel lo g g' s Au s tral ia Pty Ltd.
3 Address reprint requests to JC Brand Miller Human Nutrition Unit
D e pa rt m en t o f B i oc he m is tr y 0 08 , T h e U n iv er si ty o f S y dn ey , N S W 2 00 6,
Australia.
R e ce iv ed N o ve m be r 2 1, 1 99 6.
A c ce pt ed f or p ub li ca ti on M a y 2 2, 1 99 7.
1264
A m J C lin N utr 1 99 7;6 6:1 26 4â €” 76 .P rin ted in U SA . Â ©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 by
1 kJ portions of common foods13
Susanne H A H olt Janette C B rand M iller and P eter P etocz
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Food Variety, manufacturer, or place of purchase Preparation
IN SU LIN IN DEX OF FOOD S
1265
TABLE
Desc riptionandpreparationof the testfo ods
Fruit
Black grapes
Apples
Oranges
Bananas
Bakery products
Croissants
Chocolate cake with
frosting
Doughnuts with cinnamon
sugar
Chocolate chip cookies
Water crackers
Snack foods and confectionery
Mars Bar
Yogurt
Ice cream
Jellybeans (assorted colors)
Peanuts
Potato chips
Popcorn
Protein-rich foods
Cheese
Eggs
L e n t i l s
Baked beans
Beefsteak
W hi te f is h
Carbohydrate-rich foods
White bread
W ho le -m ea l b re ad
Grain bread
W hi te ri ce
Brown rice
White pasta
Brown pasta
Potatoes
Waltham cross
Reddelicious
Navel
Cavendish
Fresh, stem removed, served whole
Fresh, unpeeled, cut into eight segments
Fresh, peeled, cut into eight segments
Fresh, peeled, cut into quarters
Defros ted, reheated a t 180°Cor 6 mm, and served warm
Prepared according to manufacturer's directions, stored at
4 °Cup to 2 d before serving at room temperature
Prepared by supermarket from standard recipe, defrosted
overnight, reheated at 180°Cor 5 mm, and served
warm
Served crisp at room temperature, stored in airtight
container
Served crisp at room temperature
Cut into four standard pieces and served at room
temperature
Stored at 4 °C,erved cold
Stored frozen and served cold
Served at room temperature, stored in airtight container
Served at room temperature, stored in airtight container
Served from freshly opened packet
Prepared according to manufacturer's directions
immediately before serving
A ll s erv ing s cut fro m sam e larg e blo ck, s to red at 4 Â °C,
served cold
Poached the day before serving, stored at 4 °Cvernight,
reheatedin microwaveoven for 1.5 mm immediately
before serving
Prepared in bulk according to recipe, stored at 4 °Cor up
to 2 d, re he ate d i n a m ic ro wav e o ve n f or 2 m m
immediatelybeforeserving
Heated on s tove for5 mm immediate ly before serv ing
Gril led the day before serving, cut into standard bite-s ized
pieces, and stored at 4 °Cvernight; reheated in
microwave oven for 2 mm immediately before serving
Steamed the day before serving, stored at 4 °Cvernight,
cut into bite-s ized pieces, and reheated in microwave
oven for 2 miii immediately before serving
Served fresh and plain at room temperature
Served fresh and plain at room temperature
Served fresh and plain at room temperature
Bo iled 12 mii i and s tored overnight a t 4 °C,eheated in
microwave oven for 1.5 mm immediately before serving
Bo iled 12 mm and stored overnight a t 4 °C,eheated in
microwave oven for 1.5 mm immediately before serving
Boiled8 mm and storedovernightat4 °C
Re he ate d i n m ic ro wav e o ve n f or 1 .5 m m im me diate ly
before serving
Peeled,boiledfor 20 mm, andstoredat 4 °Cvernight;
reheated in a microwave oven for2 mm immediate ly
before serving
P urc has ed i n bul k f ro m s upe rm arke t and s to re d f ro ze n
White Wings Foods, Smithfie ld, Sydney, Australia
Purchased in bulk from supermarket and stored frozen
Anion's Biscuits Ltd. Homebush, Sydney, Australia
Grocery Wholesalers Ltd, Yennora, Australia
Mars Confectionary Australia, Ballarat, Australia
Strawberry fruit yogurt; Australian Co-operative
Foods,' Wetherill Park, Sydney, Australia
Vanil la ice cream; Dairy Bell, Camperdown, Sydney,
Australia
Grocery Wholesalers Ltd
Salted roasted peanuts; Grocery Wholesalers Ltd
Crinkle cut chips; Smith's Snackfood Company,
Chatswood, Sydney, Australia
Microwave cooked popcorn; Uncle Toby's Company
Ltd, Wahgunyah, Australia
M ature c he ddar c he es e; G ro ce ry W ho le sa le rs L td
Poached hens eggs
Served in tomato sauce2
Canned navy beans in tomato sauce; Franklins,
Chullora, Sydney, Australia
Le an to ps ide be ef f il le ts bo ug ht i n bulk f ro m
supermarket, trimmed and stored frozen
Ling f ish i fi le ts bought in bulk from Sydney f ish
markets, trimmed and stored frozen
Fresh sliced wheat-flour bread; Quality Bakers
Australia Ltd. Eastwood, Sydney, Australia
Fresh sliced bread made from whole-meal wheat flour;
Riga Bakeries, Moorebank, Sydney, Australia
Fresh sliced rye bread containing 47% kibbled rye; Tip
TopBakeries,Chatswood,Sydney,Australia
Cairose rice (Sunwhite), Ricegrowers' Co-operative
Ltd. Leeton, Australia
Calrose rice (Sunbrown), Ricegrowers' Co-operative
Ltd
Spirals
W ho le -m eal s pi ral s; S an R em o P as ta C om pany ,
Auburn, Sydney, Australia
Russet potatoes
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FoodVariety, manufacturer, or place o furchasePreparationFrench
friesPrefried oven-baked French fries; M cCain's Foods
( A us tra li a) , C as tl e H il l, S y dn ey , A us tra li aS to re d
frozen, cooked in conventional oven for 15 mm
immediately beforeervingBreakfast
cereals3CornflakesKellogg's
Australia Pty Ltd, Pagewood, Sydney,
Australia—Special
KToasted
f lakes made from wheat and rice f lour, high in
protein; Kellogg's Australia Plytd—HoneysmacksPuffed
whole-wheat grains with a honey-based coating;
Kellogg's Australia Plytd—SustainA
mixture of wheat, corn, and rice flakes; rolled oats;
dried fruit; and flaked almonds; Kellogg's Australia
Ptytd—All-BranA
high-fiber cereal made from wheat bran; Kellogg's
Australia Ptytd—Natural
muesliBased on raw rolled oats, wheat b ran, dried fruit, nuts,
and sunflower seeds; Uncle Toby 's Company Ltd.
Wahgunyah,ustralia—PorridgeUncle
Toby's Company Ltd. Wahgunyah, AustraliaRaw
ro lled oats cooked in a microwave oven according to
m anuf ac ture r's di re cti ons and s erv ed w itho ut s w ee te ne r
1266
HOLT ET L
T ABL E 1
Continued
1 N ow Dairy Farmer s.
2 Recipe: 15 m L olive oil 350 g dried green lentils 410 g canned tomatoes 120 g onion 1 clove garlic and 1 tsp pepper
3 Al l cereals were served fr esh wi th 125 mL fat-reduced (1.5 fat) mi lk.
of foods However carbohydrates not the only s timulusfor
i ns ul in s ecre ti on . Prote in -ri ch f oods or the addi ti on of prote in
to a carbohydrate-rich meal can stimulate a modest rise in
i ns ul in s ecre ti on w i thout i ncreas ing blood g lucose concentra
tions , particularly in subjects wi th diabetes (20—22).Similarly,
adding a large amount of fat to a carbohydrate-rich meal
increases insulin secretio n ev en tho ugh plasma g lucose re
spo ns es are re duc ed (2 3, 2 4).
T hus, pos tprandi al i ns ul in responses are not al w ays propor
tional to blood glucose concentrations or to a meal's total
carbohydrate content. Several insul inotropic factors are known
to po tentiate the stimulato ry effec t o f gluco se and mediate
po stprandial insulin se cre tio n. These inc lude fructo se, c ertain
am ino ac ids and fatty acids, and gastro inte stinal ho rmo nes such
as g as tric inhibito ry pe ptide , g luc ag on, and c ho le cy sto ki in
25 , 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 n
ti al i ns ul in s ecre ti on desp ite produci ng re lati ve ly s mall b lood
g luc ose re spo nse s. W e the re fo re de cide d that c om paring the
insulinemic effects of foods on an isoenergetic basis w as a
logical and practical approach.
The aim o f this study w as to sy stematically c ompare po st
prandia l i ns ul in responses to i soenerge ti c porti ons o f a range of
common foods. A n insulin score (IS) w as calculated for each
f ood on the bas is o f i ts i ns ul inemic e ff ec t re lati ve to a re ference
food. Thirty-eight foods, categorized into six different food
groups, w ere studied to determine w hich foods w ithin the same
food group were most insulinogenic. We hypothesized that
po stprandial ins ulin re spo nse s are no t c lo se ly re late d to the
carbohydrate content or glycemic effects of some foods.
SU BJECTS A ND METHOD S
Test fo ods
Thirty-eight foods were tested and were grouped into six
fo od cate go ries : 1) fruit: grapes, bananas, apples, and o rang es;
2 ba ke ry products: croissants, chocolate cake w ith icing,
doughnuts w ith cinnamon sugar, chocolate chip cookies, and
w ate r c rac ke rs; 3 ) snac k fo ods and c onfe ctio ne ry : M ars B ar
c andy bar ( Mars Co nf ec tio nary A us tral ia, B al larat, A us tral ia) ,
s traw be rry y og urt, v ani ll a i ce c re am , je lly be ans , s al te d ro as te d
pe anuts , plain po tato c hips, and plain po pco rn; 4) pro tein-ric h
f oo ds : c he dd ar c he es e po ac he d e gg s b o ile d le nt ils in a to m at o
sauce, baked beans in a tomato sauce, grilled beef steak, and
s te am ed w hi te f is h; 5 ) c arbo hy drate -ric h f oo ds : w hite bre ad,
w ho le -m eal bre ad, ry e-g rain bre ad, w hite ric e, bro wn ric e,
w hite pasta, bro wn pas ta, bo ile d po tato es , and o ve n-bake d
Fre nch frie s; and 6) breakfast ce reals: Cornflakes (Ke llo gg's
A ustralia Pty Ltd. Pag ew oo d, A ustralia), S pec ial K (Ke llo gg's
Australia Pty Ltd), Honeysmacks (Kellogg's A ustralia Pty
Ltd), Sustain (Kellogg's Australia Pty Ltd), All-Bran
(Kellogg's A ustralia Pty Ltd), natural muesli, and oatmeal
porridge.
Each food was served plain as a 1000-U portion with 220
mL w ater. W hite bread w as used as the reference food for each
fo od g ro up. The fo ods w ere selected to represe nt a rang e o f
natural and pro cesse d fo ods co mm only e aten in industrializ ed
so cie ties . D etails o f the fo ods and the ir preparatio n me tho ds are
listed in Table 1. Foods were bought in bulk to minimize
variations in composition and w ere served in standard-sized
pieces. The nutritional composition ofeach food per 1000 U as
cal cu lated f rom A us tra li an f ood tabl es or manufac turers ' data
is shown in Table 2.
Subjects
S eparate g ro ups of healthy subje cts (n = 1 1—13 )w ere re
cruited to test each category of foods. V olunteers w ere ex
cluded 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 o be si ty , w ere die ting , o r had
i rregul ar eati ng habits . In to tal , 41 s ubjects parti ci pated. O ne
subject consumed all of the test foods and 15 other subjects
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ServingCarbohydrateEnergyFood
weight FatProtein
SugarStarch
FiberWater
density
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'
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.
andonfectioneryMars
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
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 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 the
w ere uni ve rs ity s tude nts ; re le vant c harac te ris tic s o fthe s ubje cts U niv ers ity o f S ydne y.
are listed in Table 3. The mean body mass index (BMI, in
kg/m2) of the 41 subjects w as 22.7  ±0.4 (range: 19—29).Three P1@ Ot(W Ol
subjects had a B MI > 25 but tw o of these w ere short, stocky Each subject first consumed a 1000-U portion of w hite bread
males 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 W hite 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 the
sent 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
 ±.4Bakery
produc ts (n = 6 F, 6 M )2 2.2
±3.7 23 .1  ±.7Snacks
and confectionery(n = 5 F, 7 M)21.0
±1.2 22. 9  ±.5Protein-rich
foods (n 5 F, 6 M)22.4 ±2.824.3
 ±.1Carbohydrate-rich
foods (n = 5 F, 8 M)21.0
±1.923.0 ±.9Breakfast
cereals (n = 5 F, 6 M)22.8
±3.922.8
±1.4
1268
HOLT ET AL
tube radioimmunoassay kit (Coat-A -Count; D iagnostic Prod
ucts Corporation, Los A ngeles). For both plasma glucose and
ins ul in analy si s, all nine plas ma s am ple s f or a partic ular s ub
ject's test w ere analyzed w ithin the same run to reduce any
er ro r in t ro d u ce d b y in t e ra s s a yva r ia t io n . W h e n p o s s i b le , a ll
plasma samples fo r a particular subject w ere analyz ed for
insulin w ithin the same run. For the insulin analysis, the mean
w ithin-assay CV w as 5% and the mean betw een-assay CV w as
7
Stati stical analys is
Cumulativ e chang es in po stprandial plasma g luc ose and
insulin re spo ns es fo r e ac h fo od w ere quantifie d as the inc re
mental area under the 120-mn response curve (A UC), w hich
w as c alc ulate d by us ing the trape zo idal rule w ith fas ti ng c on
centrati ons as the bas el ine and truncated at zero . A ny negati ve
are as te nde d to be s mall and w ere ig no re d. Fo r e ac h s ubje ct, an
IS ( %) w as c alc ulate d f or e ac h te st fo od by div iding the ins uli n
A U C v alue fo r the te st fo od by the ins ulin A U C v alue fo r w hite
bread (the reference food), and expressed as a percentage as
follows:
I S ( )
A re a unde r the 1 20 -m m i ns uli n re spo ns e
c urv e fo r 1 00 0 U te s t fo od
Area underthe 120 -mminsulinresponse curve
f or 1000 Id w hi te bread
TABLE 3
Characteristics of each group of subjects '
â €˜ ¿  ± S D
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 n
indi vi duals that af fe ct ins uli n s ens itiv ity , s uc h as bo dy w eig ht
and ac ti vi ty l eve ls .
Subjects were fed 1000-U portions of the test foods in a
rando m order on separate mo rning s after a 1 0-h o vernig ht
fast. W ithin e ac h fo od g ro up, e ac h subje ct ac te d as his o r he r
o wn contro l, being tested at the same time o f day and under
as similar conditions as possible. S ubjects w ere asked to
refrain fro m unusual ac tiv ity and fo od intake patterns, to
abstain fro m alco ho l and leg umes the day before a te st, and
to eat a similar meal the night before each test. When
subjects arrived at the lab in the mo rning , they co mple ted a
s ho rt que stio nnaire as se ss ing re ce nt f oo d intake and ac tiv ity
patte rns. A fas ting fing er-pric k blo od s am ple w as c olle cte d
and subjects w ere then given a test food and 220 mL water
(0 mm). W hen possible, foo ds w ere prese nted under a larg e
o paque plastic ho od w ith a ho le thro ugh w hich vo lunteers
pulled out pieces of the test food one at a time. This was an
atte mpt to m inim iz e be tw ee n- subje ct v ariatio n in c ephalic
phas e ins ulin s ec re tio n aris ing f ro m the s ens ory s ti mul atio n
associated w ith the anticipation and act of eating (27).
Ho w ev e r, th is w as n o t fe as ib le fo r th e liq u id fo o d s (yo g u rt
and ice cream), foods served in a sauce (baked beans and
lentils), or w ith milk (all of the breakfast cereals), w hich
were presented in standard bowls w ithout the hood.
S ubje cts w ere as ke d to e at and drink at a c om fo rtable rate .
Im me diate ly afte r finishing the test fo od, subjec ts re co rded the
time taken to eat the food and completed a questionnaire
as 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 ubjects
re maine d s eate d at table s in a qui et e nv iro nm ent and w ere no t
permitted to eat or drink until the end of the session (120 mm).
Fi ng er- pri ck blo od s am ple s ( 1.5 †”2 .5m L) w ere c olle cte d
from warmed hands immediately before the meal (0 mm) and
15, 30, 45, 60, 75, 90, 105, and 120 mm after the start of the
meal (into plastic tubes that had been kept o n ice ) w ith use o f
an auto matic lanc et de vic e ( Auto cli x; B oe hring er M annhe im
A ustralia, Castle Hill, A ustralia). B lood samples w ere centri
fuged immediately after collection (1 miii at 12 500 X g at
ro om te mpe rature ) and pl as ma w as pipe tte d into c hill ed tube s
and im me diate ly s to re d at †”¿2 0° Cuntil analy ze d (< 1 m o).
P las ma glucose concentrati ons w ere anal yzed i n dupl icate w ith
a C obas F ara auto matic s pe ctro pho to me tric analy ze r ( Ro che
D iagnostica, B asel, S witzerland) and the glucose hexokinase
enzymatic assay. The mean w ithin-assay and betw een-assay
pre cisio ns (CV s) w ere bo th < 6 %. Plasm a insulin c onc entra
ti ons w ere meas ured i n dupli cate by us ing an anti body-coated
X100 (1)
This equation is similar to that developed by W olever and
Jenkins (29) for calculating GI values. A glucose score (GS)
(not the same as a GI score, w hich is based on a 50-g carbo
hydrate portion) for each food w as also calculated by using the
same e quatio n w ith the co rrespo nding plasma g luco se re sults.
A nalysis of variance (A NOV A) and Fisher's probable least
s ignif icant-di fference test for multiple comparisons were used to
d ete rm in e s tati sti cal d if fe re nc es am on g th e f oo ds w i th in e ac h f oo d
group (S TA TV IEW S TU DEN T S OFFW ARE; A bacus Concepts
mc, Berkley, CA). Linear-regressionanalysis was used to test
as so ci ati on s b etw e en g luc os e and i ns ul in re sp ons es and n utri ti on al
indexes (MINITAB DATA ANALYSIS SOFFWARE, version
7.0; M initab Inc, S tate College, PA ). Test foods not containing a
p arti cu lar n utri en t w e re e xc lu de d f ro m th es e an al ys es . T he re fo re ,
s am ple s iz es f or the c orre lati ons be tw ee n i ndi vidual nutrie nts and
the mean G Ss and ISs vari ed f rom 32 to 36 . Mean resu lts f or w hi te
bread for each fo od g ro up w ere inc lude d in so me statistical anal
y se s, so these co rrelations w ere made w ith 4 3 v alues. One subje ct
f ro m the pro te in- ric h f oo d g ro up di d no t c om pl ete the f is h te st and
one s ubjec t f rom the breakfas t cereal group did not compl ete the
S ustain tes t. There fore , in to tal, 5 03 indiV idU al te sts w ere fully
completed.
S tepw ise-m ultiple-reg res sio n analy sis w as used to e xamine
the extent to w hich the different macronutrients and GSs ac
counted for the variability of the ISs (MINITA B DATA
ANALYSIS SOFTWARE). For this analys is , the indiv idual
w hite bread OS and IS results w ere included for the carbohy
drate-rich food group only; therefore, this analysis w as per
f orm ed w ith 4 46 i ndiv idual o bs erv atio ns fo r 3 8 f oo ds . Inc lud
ing the w hite 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 A UCInsulin
AUCInsulin AUC:
glucose AUCInsulin
A U C pe r g
carbohydrateInsulin
A UC per g
serving weightGlucose scoreInsulincoremol-miniLpmolmin/LpmolminL'g'pmolminL'g'%%
INSULIN INDEX OF FOODS
1269
TA BLE 4
A reas under the 1 20 -m m 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 g
carbohydrate and perg serving weight, and mean glucose and insulin scores'
BreakfasterealsWhitebread156±2113557±1756108± 19295±38144±19100±0100 ±0All-Bran59
±94 299 ±61287 ±1599  ±1425
±340  ±732 ±Porridge80
±95093 ±49374 ±11139
±1313
±I60 ±1240 ±Muesli65±126034±813118±18163±2234±543±746±5Special
K1 6 ±1 4 8 3 8 ±6 3 5 9 5 ±1 4 1 9 5 ± 1 5 4 7 ±4 7
±9 6 6 ±Ho n e y s ma c k s 9 1±1 9 1 2±1 5 6 1 8±1 2 1 8 9 ±3 1 5 3±9 6 ±7 6 7±6Su s t a i n 9 3±8 8 9 3 8±7 5 7 1 2±9 2 9±1 8 5 3±4 6 6±6 7 1±6Co r n f l a k e s 1
1 ±1 1 8 7 6 8
±62388
±5 1 8 9 ± 1 3 5 2 ±4 7 6
±1175
±Gr o u p me a n â € ” 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 h
foodsWhitebread120±1312882±1901112±15281 ±41137±20100±0100± 0Whitepasta50±114456±453156± 4891±922±246± 1040±5
p a s t a 7 4 ±7 4 5 3 5 ±5 7 4 6 7 ± 1 9 3 ± 1 2 2 1 ±3 6 8 ± 1 4 ±Gr a i n b r e a d 6 8±9 6 6 5 9 ±8 3 7 1 6±1 2 1 6 6±2 1 6 2±8 6 ±1 2 5 6±6Br own r i c e 1 1 3±1 3 6 2 4 ±6 1 6 5 8 ±5 1 1 7±1 1 4 2±4 1 4±1 8 6 2±1 1 F r e n c h
f r i e s 7
±1 1 7 6 4 3 ±713146 ±292 9 ± 1 9 8 2 ±8 7 1 ± 1 6 7 4 ±2Wh i t e r i c e 1 2 9±1 6 8 1 4 3±6 8 3 6 9 ±5 1 4 5±1 2 4 ±3 1 1 ±1 5 7 9±1 2Who l e me a l
b r e a d 1 6 ± 1 4 1 1 2 3 ± 1 4 2 1 2 2 ±2 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 ± 1 4 6 7 1 2 ± 1 9 2 8 4 ± 3 3 8 ± 4 1 4 1 ± 3 5 1 2 1 ± 1 1 Gr o u p me a n â € ” 8 4 1 ± 4 6 1 1 6 ± 8 1 8 2 ± 1 6 2 ± 5 8 8 ± 6 7 4 ± 8 P r o t e i n r i c
foodsWhitebread121±1917438±3154177±35387 ±63185±33100±0100 ±0Eggs36
± 1 1 4 7 4 4 ± 1 1 7 1 3 5
±92934
±1 8 4 5 3
±642
±1631
±C h e e s e 4 2
±1 5 9 9 4
± 1 5 9 2 6 8 ± 1 5 3 6 4 2 5 7 ± 1 5 1 3 1 6
±2755
± 1 8 4 5 ±3 Be e f 1 8 ± 6 7 9 1  ±2 1 9 3 1 5 8 3 ± 9 3 9 â € ” 5 ± 1 4 2 1 ± 8 5 1 ± 1 6 Le n t i l s 6 3
±1 7 9 2 6 8
±2 1 7 4 3 7 ± 1 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 ±2 5 5 7 7 5 ±5 2 â € ” 2 8 ±6 2 8 ± 1 3 5 9
±8Ba k e d b e a n s 1 1 ±1 4 2 1 6 ±3 7 7 6 1 8 3±4 4 5 4±8 7 5 7±1 1 1 1 4 ±1 8 1 2 ±1 9Gr o u p
me a n â € ” 9 9 8 3 ± 1 3 2 5 8 5 ±6 1 1 8 6 7 ±5 4 5 6 5 3
±654
±7 6 1 ±F r u i t Wh i t e
b r e a d 1 7 1 ± 1 9 1 5 5 6 3 ± 1 6 3 2 1 5 ± 1 8 3 3 9 ±3 6 1 6 6 ±171 ± 1 ±Ap p l e s 8 3±7 8 9 1 9±9 1 1 1 8±1 8 1 5 2±1 5 2 ±2 5 ±6 5 9±4Or a n g e s 6 6±1 1 9 3 4 5±1 7 4 1 6 6±2 3 1 8 5 ±2 1 1 5±2 3 9±7 6 ±3Ba n a n a s 1 3 3
±1 2 1 2 4 4 5 ± 1 3 5 3 1 8 ±2 2 2 2 4 ±2 4 4 5
±5 7 9 ± 1 8 1 ±Gr a p e s 1 2 6±1 4 1 2 2 9 3±1 1 9 1 1 3±1 9 2 1 6 ±2 1 3 1±3 7 4±9 8 2±6Gr o u pme a n â € ” 1 7 5 1±6 5 1 2 4±1 1 9 4±1 1 2 8±2 6 1±5 7 1±3Sn a c k s
andonfectioneryWhitebread159±2915592±2376104±24340±52166±25100±0100±0Peanuts20
±73 47
±8 2 8 2 1 4 ±8 8 5 6 4 ± 1 5 3 8 ±2 2 1 2 ±4 2 ±Po p c o r n 7 1±1 2 6 5 3 7±6 7 9 1 9±3 2 2 3 9 ±2 5 1 3 9±1 4 6 2±1 6 5 4±9Po t a t o c h i p s 7 7±1 5 8 1 9 5 ±1 5 7 7 1 6 9±7 8 3 6 7±7 1 1 8 6±3 6 5 2±9 6 1±1 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 3 ± 1 6 7 ± 1 9 8 9 ±3Yo g u r t 8 8±2 3 1 5 6 1 1±1 8 8 1 6 7±3 3 4 1 5 ±4 8 6 5±7 6 2±1 5 1 1 5±1 3Ma r s B a r 9 8±1 1 6 6 8 2 ±1 8 9 6 2 1 8±6 5 4 4 1 ±5 3 9±3 5 7 9±1 3 1 2 2±1 5 J e l l y b
productsWhitebread129±1517599±3058188±64383 ±67187±33100±0100 ±0Doughnuts78±1412445±2402113± 21480±93191±3763±
±
3 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 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 2±1 2 1 5 2 2 3±3 8 2 2 ±5 7 4 3 6±1 1 2 9 8±7 5 7 4±1 1 9 2±1 5Gr o u pme a n â € ” 1 2 6 8 1±1 3 2 5 2 6 1±5 6 4 6 8±4 7 2 3 6±2 4 7 7±7 8 3±5
I 1 SE M. M ars Bar M ars Confectionary Australia Ballarat Australia; All-Br an Special K H oneysmacks Sustain and Cornf lakes: Kellogg s
Australia Pty Ltd. Pagewood, Australia.
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2 7
HO LT ET A L
bread, w hich artificially increases the accuracy of any calcu
lation involving w hite bread.
RESULTS
Fa s tin g g lu co s e a nd in s ulin c on ce n tra tio ns
W ithin each food group, the subjects' average fasting
plasma glucose and insulin concentrations were not signif
icantly different am ong the foods. M ean fasting plasma
glucose concentrations did not vary significantly among the
six food groups, w hereas mean fasting insulin concentra
tions were more variable, ranging from “¿42o 120 pm ol/L.
Fasting insulin concentrations were not m ore variable in
fem ales than in males and there were no significant differ
ences at various stages of the m enstrual cycle. A significant
correlation was found between m ean fasting insulin concen
trations and m ean BM I values for the six groups of subjects
r â €” ¿. 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 ponses
A s w ith any biological response, there w as betw een-subject
variation in the glucose and insulin responses to the sam e food.
Two-way ANOVA was used to examine the ranking of each
subject's responses to the different test foods within a food
group (ie, interindividual variation). There w ere significant
differences am ong the subjects in the rank order of their glu
cose AUC responses except within the fruit and protein-rich
food groups. T here w ere also significant differences am ong the
subjects' rank order of insulin AUC responses w ithin all food
groups. H ow ever, individual subjects w ithin each food group
consistently produced relatively low , m edium , or high insulin
responses. F urtherm ore, subjects produced their low est insulin
responses for the least insulinogenic foods and their highest
insulin responses for the m ost insulinogenic foods w ithin each
f oo d g ro up .
10 0
There were large differences in mean glycemic and insulin
responses to the foods, both within and between food groups.
M ean glucose and insulin AUC results, mean GSs and ISs, and
the mean ratios of insulin to glucose AUCs (the amount of
insulin secretion in relation to the blood glucose response) are
listed in Table 4. M ean GSs and ISs were calculated for each
fo od g rou p b y av erag in g the sco res fo r all test fo ods w ith in the
food group. On average, the snack food group produced the
highest food group IS (89 ) , followed by bakery products
(8 3 ), carbo hy drate-rich fo od s (74 ), fruit (71 ), p ro tein
rich foods (61 ), and breakfast cereals (57 ). Average GSs
for the food groups did not follow the same rank order (Figure
1 ). 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 t
average GS (88 ), followed by bakery products (77 ), snack
foods (65 ), fruit (6 1 ), breakfast cereals (59 ), and protein
ric h fo od s (5 4 ). In te re s tin g ly , th e G S ra n k o rd er is n ot p ro
portional to the average total carbohydrate content of each food
group, w hich highlights the influence of other food factors (eg,
fiber and processing) in determ ining the rate of carbohydrate
d ig es tio n a nd a bs or pt io n.
Overall, am ong the 38 test foods, jellybeans produced the
highest m ean IS (160 Â ±16 ), eightfold higher than the low est
IS (for peanuts: 20 Â ±5 ) (F igure 2). W hite bread, the stan
dard food, consistently produced one of the highest glucose and
insulin responses (peak and AUC) and had a higher IS than
m ost of the other foods (84 ). A ll of the breakfast cereals w ere
significantly less insulinogenic than w hite bread (P < 0.001).
All-Bran and porridge both produced a significantly lower IS
than the other cereals (P < 0.001), except muesli. Despite
containing more carbohydrate than porridge and m uesli, A ll
Bran produced the lowest G S. Baked beans, which contain
considerably m ore carbohydrate than the other protein-rich
foods, produced a significantly higher GS and IS (P < 0.001).
O n a ve ra ge , fis h e lic ite d tw ic e a s m uc h in su lin se cre tio n a s d id
the equivalent portion of eggs. W ithin the fruit group, oranges
and apples produced a significantly lower GS and IS than
lucoseco re
Insulincore
8 0
60 J
40
20
0
4)
U
‘¿ )
C
4)
4)
E
0.
0
B reak fas t
cerea ls
C arb oh yd ra te - B ak ery
ric h fo o d s p ro d uc ts
Protein
ric h fo o ds
Fru it S n a c ks a n d
con fec t ionery
FIGURE 1. Mean(±SEM)glucoseand insulinscoresforeach food group.
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White
breac . IPrth ifr@c.
Doughnu t s
Croissants
Ca k e
Crack e r s
Cook ie s
PeanutsI=@lIII―;―t-1@PopcornI=―iiPotato
chipsI='=―iIcecream l―;lIY ogurtI
lip
IN SUL IN IN DEX OF FOO DS
1271
I@ 1
ft
All-Bran
Porridge
Mues l i
OUSL4I J
Eg @
Cheese
Bee f
Lentils
Fish
e ns
Apples
O r a n g e s
Bananas
Gr a p e s
B r ow n p as ta
W h i te p as ta
Grain bread
r o wn r i c e
Frenchfries
Whit e r ic e
Who l e -mea l b r e ad
-i
.1
1=1
Je l lybeans
1 0 0 2 0 0
In su lin s co re ( )
F IG U R E 2 . M e an ( Â ±S E M ) i ns ul in s co re s f o r 1 00 0- Id p ort io ns o f t he t es t f o od s. W h it e b r ead w a s t he re f ere nc e f o od ( in su li n s co re = 1 00 ) . A l l -B r an
c 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 rs
Confectionary A ustralia, Ballarat, A ustralia.
grapes and bananas (P < 0.05 to P < 0.001), despite contain
ing a sim ilar am ount of carbohy drate.
Potatoes produced signif icantly higher G Ss and IS s than all
of the other carbohy drate-rich foods. W hite bread produced a
higher GS and IS than grain bread (P < 0.05 and P < 0.001
respectiv ely ), but w hole-m eal bread and w hite bread had sim
ilar scores. W hite and brow n rice had sim ilar GS s and IS s, as
did w hite and brow n pasta. A m ong the bak ery products, crack
ers 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 this
group (all tended to be high). A m ong the snack foods, jelly
beans produced a signif icantly higher G S and IS than the other
foods in this group. Despite containing sim ilar am ounts of
carbohy drate, jelly beans induced tw ice as m uch insulin secre
tion 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 ith
f at or protein, produced relativ ely high IS s. Popcorn and potato
chips elicited tw ice as m uch insulin secretion as peanuts
P < 0.05 and P < 0.01, respectively .
S ignif icant dif f erences w ere found both w ithin and am ong
the food groups w hen the insulin A U C responses w ere
ex am ined as a function of the food's carbohydrate content
(T able 4). On av erage, protein-rich foods produced the
highest insulin secretion per gram of carbohy drate (food
group m ean: 18 607 pm ol . m m . L ' . g@ 1) (because of
their m ostly low carbohy drate contents), follow ed by bak ery
products (468 pm ol . m m . L @ . g 1), snack foods (416
pm ol . m m . L ‘¿g 1) f ruit (194 pm ol . m m . L ‘¿g 1),
carbohy drate-rich foods (182 pm ol . m m . L @ . g'), and
break fast cereals ( 169 pm ol . m m . L ‘¿g ‘¿ . hen the
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1272
HOLT ET A L
S
insulin A U C re spo nse w as e xam ine d in re latio n to the fo od's
serving size (g), the bakery products were the most insuli
nogenic (food group mean: 236 pmol . mm . L ‘¿g 1), fol
lowed by snack foods (163 pmol . mm . L ‘¿g 1), carbo
hydrate-rich foods (62 pmol . mm . L ‘¿g 1 ), pro te in- ri ch
foods (53 pmol . m m . L ‘¿g 1), breakfast cereals (39
pmol . 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 and
fat.
In su lin re s po ns e s in re la tio n to g lu co se re s po ns e s
Overall, mean glucose and insulin AUC values were posi
tively correlated (r = 0.67, P < 0.001, n = 43), as were the
peak glucose and insulin values (r = 0.57, P < 0.001, n = 43).
He nc e, the m ean 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 UC
values (r = 0.74, P < 0.001, n = 43) and peak insulin
c onc entratio ns w ere pro po rtio nal to the ins ulin A UC v alue s
r 0.95, P < 0.001, n 43 . In addition, the observed GSs
fo r 1 00 0-U po rtio ns o f the fo ods c orre late d w ith pre vio usly
publis he d G I v alue s bas ed o n po rtio ns o f fo ods c ontaining 5 0 g
carbohydrate (r = 0.65, P < 0.001, n = 32). Six test foods
(chocolate chip cookies, eggs, cheese, beef, fish, and Hon
e y s m a c k sc e r e a l w e r e n o t i n c l u d e d in t h is a n a l y s isb e c a u s eG I
v al ue s w ere no t av ail abl e.
Insulin AUC values were divided by glucose AUC values to
determine w hich foo ds w ere marke dly insulino genic relativ e to
th eir g ly c e m ic e ffe ct (T a ble 4 a n d Fig u re 4 ). O n a v e ra g e , th e
p r o t e in r ic h fo o d s s t im u la t e da la r g e a m o u n t o f in s u lin s e c r e
ti on re lati ve to thei r g lycemic respons e, f ol low ed by the bakery
products, snack foods, fruit, carbohydrate-rich foods, and
b re a k f a s t c e r e a ls .
4)
1 @
0
4)
4)
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 t
contents of the foods
C orre lati ons betw een the macronutri ent compos iti ons o f the
te st fo ods and the m ean IS s are s ho wn in Fig ure 5 . The po rtio n
size (energy density: kJ/g), water, and fiber contents of the
foods were not significantly related to the mean ISs. The
re latio n be tw ee n pro te in c onte nts and IS s w as ne gativ e but no t
significant (r —¿0.24, = 38). The mean IS s w ere positively
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
no t s ig nif ic antl y re late d to s tarc h c onte nt ( r = †”¿0 .0 9, = 3 0).
Fat c onte nt w as ne gativ ely re late d to the m ean IS (r = †”¿0.27,
N S, n = 3 6). W hen e xpressed as a percentag e o f to tal e nerg y,
fat (r = —¿0.27,S, n = 36) and protein (r = —¿0 .2 4,S , n =
38) w ere negatively associated w ith the mean IS , w hereas total
carbo hydrate w as po sitive ly related (r = 0 .3 7, P < 0.0 5, n
36).
R el ati ons be tw een the G Ss and the nutri ents l argel y f ol low ed
the sam e dire ctio ns as the IS c orre latio ns. M ean GS s w ere no t
sig nific antly related to the fo ods' se rving siz es o r w ater o r fiber
c onte nts . M ean G Ss c orre late d ne gativ ely w ith f at ( r = †”¿0.38,
P < 0.05, n = 36) and protein r = — ¿0.38,< 0.05, n = 38)
c onte nts , and po siti ve ly w ith to tal c arbo hy drate c onte nt ( r =
0.32, NS, n = 36). Unlike the ISs, the GSs were significantly
related to starch content (r = 0.43, P < 0.05, n = 30) but not
sug ar c ontent (r = —¿0.07,S , n = 36). When expressed as a
percentageof total energy, fat (r = —¿0.38, < 0.05, n = 36)
and protein (r = —¿0.39, < 0.05, n = 38) w ere negatively
as soc iated w ith mean G Ss , w hereas to tal carbohydrate content
was positively related (r = 0.46, P < 0.01, n = 36).
Stepw is e- multi pl e- regress ion anal ys is o f the 446 i ndiv idual
re sults fo r the 3 8 f oo ds w as pe rf orm ed to de te rm ine the e xte nt
to w hic h the m ac ro nutrie nts and G Ss ac co unte d fo r the v an
abil ity o f the ISs . U nf ortunate ly , i t w as not pos si bl e to generate
a s ing le m ul tiple -re gre ss io n e quati on that inc lude d all o f the
macronutrients because some pairs of nutrients w ere highly
corre lated ( eg , f at and prote in , f iber and w ater, to tal carbohy
drate and s ugar or s tarch, and s ugar and s tarch) . T he regress ion
e quatio n that inc luded all o f the m ac ronutrie nts had unac ce pt
ably high variance inflation factors. Therefore, tw o separate
regression equations w ere generated that w ere limited to the
facto rs that w ere me asured and no t inte rde pendent. Equatio n 2
inc lude s fat but no t pro te in, w he re as e quatio n 3 i nc lude s pro
te in but no t f at:
IS = 72.4 + 0.383 GS —¿.88 f at —¿.1 03 w ate r
+ 0 .5 09 s u ga r â €”¿.4 2 1 s ta rc h (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 analysis
f or the as soc iati ons be tw een the i nd 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 —¿.0 98 w ate r
+ 1.2 9 s ug a r + 0 .3 7 7 s ta rc h (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
â € ¢ ¿ â € ¢
S
0
0
G lu co s e s c ore ( )
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INSULIN INDEX OF FOODS
1273
Porridge
All-Bran
Comfiakes
S pe c ia l K
S u s t a i n
Honeysmacks
Mues l i
Brownrice
Brownpa s t a
White rice
Gra in b r e ad
Whitebread
Potatoes
Whole-meal bread
Frenchries
White pasta
Bananas
Grapes
Apples
Oranges
Popcorn
Jellybeans
Yogurt
Chips
Icecream
Peanuts
MarsBar
Doughnuts
C a k e
Coo id e s
Crackers
Croissant
Eggs
Beans
Cheese
Lentils
Fi s h
Be@
I. .
I-
I- i
@ 1
-I
-t
500 1000 1500 2000 2500
3000
Insu 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,and Cornflakes,Kello gg'sAustraliaPty Ltd.Pag ew oo d,Aus tralia;MarsBar candybar, MarsConf ectionaryAus tralia,Ballarat,Australia.
Linear-regression analysis of the individual OS and IS re
s ults had an R2 value of 2 3%. There fore , the g ly ce mic respo nse
w as a significant predictor of the insulin response, but it
ac co unte d f or o nly 2 3% o f the v ariability in ins uli ne mi a. The
macronutri ents ( prote in or f at, w ater, s ugar, and s tarch) w ere
also significant predictors but together accounted for only
ano the r 1 0% o f the v ariabil ity o f the i ns ulin re spo ns 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 re
s po nse s to the 3 8 fo ods s tudie d.
DISCUSSION
The re sults o f this s tudy c onf irm and als o c halle ng e s om e o f
o ur bas ic as sum ptio ns abo ut the re lati on be tw ee n f oo d intake
and insuline mia. W ithin each foo d g roup, there w as a w ide
range o f insulin res po nse s, despite similarities in nutrie nt co rn
position. The important Western staples, bread and potato,
w ere among the most i ns ul inogen ic f oods . S imil arl y, the h ighl y
ref ined bakery products and snack foods induced substantial ly
m 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 n
did the o the r te st fo ods . In c ontras t, pas ta, o atm eal po rridg e,
and A l l- Bran cereal produced re lati ve ly l ow i ns ul in respons es ,
de spi te the ir hig h c arbo hy drate c onte nts . C arbo hy drate w as
quanti tati ve ly the major macronutri ent f or most f oods . T hus , i t
is no t surpris ing that w e o bs erv ed a stro ng c orre latio n betw ee n
G Ss and IS s (r = 0 .7 0, P < 0 .0 01 ). H ow ev er, s om e pro te in
and fat-ric h fo ods (e gg s, be ef, fis h, le ntils , c he ese , c ake , and
do ug hnuts) induced as much insulin sec retio n as did so me
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0
U)
0 20 40 60
P ro t e i n g l s e rv l n g )
10 0
S S
0 20 40
60
1274
H OL T ET A L
20 0
10 0
0
14 0
S
S 5
S
S
S
S
S .
â € ¢ ¿ ,.. S
S I•
S
0 10 20
F ib e r 9 / s e r v in g )
20 0
10 0
S
S
S
U)
C
a
S
U)
U)
C
S
@ f S 5 5
I
S t a rc h 9 /s e rv in g )
S S
200W
10 0
0
@ S
S
S 55
55
S S
1@ b5 s
S
F a t 9 /s e rv in g )
S
0 20 40 60
T otal carbo hy drate (9 /se rv in g)
0 i I
0 20 40 60
S u g a r 9 / s e r v i n g )
14 0
S
10 0
S
S
S
S
S
S S
60
7c1
0
0 10 20 30
F IG U R E 5 . R e lat io ns b et w ee n t he n ut ri en t c on te nt s o f t he t es t f o od s an d t he m e an i ns ul in s co re s. F ib er: r = †”¿0.10,S , n = 32; p rotein: r = —¿0.24,
N S , 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,<
0.05, n = 36.
c arb oh yd rate -ric h f oo ds (e g, b ee f w as e qu al to b ro w n ric e an d
f ish w as e qu al to g rain b read ). A s h yp othesiz ed , sev eral f oo ds
w ith sim ilar G S s h ad disp arate IS s (eg , ice cre am an d y og urt,
b ro w n ric e an d b ak ed be ans, cak e an d ap ples, an d do ug hnu ts
an d b ro w n p as ta). O v erall, th e f ib er c on te nt d id n ot p re dic t th e
m ag nitu de o f th e in su lin re sp onse. S im ilar IS s w e re o bserv ed
f or w h ite an d b ro w n p asta, w h ite an d b ro w n rice, an d w h ite and
w hole-m eal bread. A ll of these foods are relatively ref ined
c om p are d w i th th eir t rad itio nal c ou nte rp arts . C o lle ct iv e ly , th e
fm dings im ply that ty pical W estern diets are lik ely to be
sig nif ican tly m o re in sulin og en ic th an m o re trad itio nal d iets
based on less ref in ed f ood s.
I n t hi s s tu dy , we c ho se t o t es t i so en erg et ic p ort io n s o f f o od s
rat he r t han e qu al- carb oh y drate s erv in gs to d ete rm i ne th e in su
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INSULIN INDEX OF FOODS
1275
lin respo nse to all of the nutrients in the foo ds as normally
consumed. A standard portion size of 1000 kJ was chosen
because this resulted in realistic serving sizes for most of the
foods except apples, oranges, fish, and potatoes. A lthough
some of the protein-rich foods may normally be eaten in
s malle r quantiti es , f is h, be ef , c he es e, and e gg s s till had larg er
ins ul in re spo ns es pe r g ram than did m any o f the f oo ds c ons is t
ing pre do minantly o f c arbo hy drate . A s o bs erv ed in pre vio us
studies, consumption of protein or fat w ith carbohydrate in
creases insulin secretion compared w ith the insulinogenic ef
fect of these nutrients alone (22, 30—32). T his may partly
e xplain the m arke dly hig h ins ulin re spo ns e to bake d be ans.
D ri ed hanc ot be ans , w hic h are s oake d and bo ile d, are li ke ly to
hav e a lo w er IS than c om me rc ial bake d be ans , w hic h are m ore
readily digestible.
T he resu lts conf irm that i ncreas ed i ns ul in s ecre ti on does not
ac co unt fo r the lo w g ly ce mic re spo nse s pro duc ed by lo w-G I
fo od s s uch a s p a s ta , p orrid g e , a nd All-Bra n c e re a l 33 ). F u r
thermore, equal-carbohydrate servings of foods do not neces
sarily stimulate insulin sec retio n to the same ex tent. Fo r ex am
ple , i soenerge ti c s erv ings o f pas ta and potatoes both contai ned
=,%50g carbohydrate, yet the IS for potatoes w as three times
g reate r than that fo r pasta. S im ilarly , po rridg e and y og urt, and
w ho le -g rain bre ad and bake d be ans , pro duc ed disparate IS s
despi te their s imilar carbohydrate contents . These f indings , l ike
o thers , chal lenge the s ci enti fi c bas is o f carbohydrate exchange
tabl es , w hi ch as sum e that po rti ons o f di ff ere nt f oo ds c ontaini ng
1 0†”15g carbo hy drate w ill hav e equal phy sio lo gic e ffec ts and
w ill re quire e qual am ounts o f e xo ge no us insulin to be m etab
o liz ed. It is po ssible that preprandial insulin dos es fo r patients
with NID DM could be more scientifically estimated or
m atc he d o n the basis o f a m eal's av erag e ins uline mic e ffe ct in
healthy indiv iduals, rather than o n the basis o f the meal's
carbohydrate content or 01 . Further research i s required to te st
this hy po the sis. The adve nt of intensive insulin the rapy and the
added risk of hypoglycemia increases the urgency of this
re se arc h ( 34 ).
Our study w as undertaken to test the hy po thesis that the
po stprandi al ins ul in re spo ns e w as no t ne ce ss ari ly pro po rti onal
to the blo od g luco se respo nse and that nutrients o ther than
c arbo hydrate influe nc e the o ve rall le ve l o f insulinem ia. M ulti
pIe -re gre ss io n analy si s o f the i ndi vidual re sul ts s ho we d that the
g ly ce mic re spo ns e w as a sig nific ant pre dic to r o f the ins ulin
respo nse, but it acco unted fo r o nly 2 3% o f the variability in
i ns ul inemia. T he macronutri ents ( prote in or f at, w ater, s ugar,
and s tarc h) w e re als o s ig nif ic ant pre dic to rs , but to ge the r ac
counted for only another 10% of the variability of the insulin
re spo nse s. Thus, w e c an e xplain o nly 3 3% o f the v ariatio n o f
the ins ulin re spo nse s to the 3 8 fo ods unde r e xaminatio n. The
lo w R 2 v alue indic ate s that the m ac ro nutrie nt c om po sitio n o f
fo 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 f
po stprandial ins uline mia. The rate o f starc h dig estio n, the
am ount o f rapidly av ai lable g luc os e and re sis tant s tarc h, the
deg re e ofo sm olality , the v isco sity o fthe g ut's co nte nts , and the
rate of g as tric em pty ing m ust be o ther im po rtant facto rs influ
e nc ing the de gre e o f po stprandial i ns ulin s ec re tio n. F urthe r
research i s required to examine the re lati on betw een pos tpran
dial insulinemia, food form, and various digestive factors for a
m uc h larg er rang e o f fo ods to pro duc e a re gre ss io n e quatio n
w ith g re ate r pre dic tiv e v al ue .
Dietary guidelines for healthy people and persons with
NIDDM have undergone considerable change and will con
tinue to be mo dified as o ur understanding of the relatio ns
be tw ee n di etary patte rns and dis eas e im pro ve s. The re is c on
c ern that hig h- carbo hy drate di ets m ay i nc re as e triac yl gl yc ero l
concentrations and reduce high-density l ipoprote in concentra
tions (35, 36). The use of diets high in monounsaturated fat is
an atte mpt to o ve rc om e the unde sirable e ffe cts o f s om e hig h
carbohydrate d ie ts on plas ma l ip ids ( 37—39).H ow ever, d ie ts
high in monounsaturated fat are unlikely to facilitate w eight
lo ss . A lo w -f at die t bas ed o n le ss -re fine d, c arbo hy drate -ric h
foods w ith relatively low IS s may help enhance satiety and aid
w 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 ho pe the y
s tim ulate dis cus si on and f urthe r re se arc h. A ddi tio nal s tudi es are
n ee de d to d ete rm in e w he th er th e IS c on ce pt i s u se fu l, re pro duc ib le
around the w orld, predictable in a mix ed-me al c ontex t, and cliii
i cal ly us ef ul i n th e tre atm ent o f d iabe te s m el li tu s, h ype rl ip id em ia,
and overweight. Studies examining the relation between postpran
dial insul inemia and the storage and oxidation of fat, prote in, and
c arb oh yd rate m ay p ro vi de f urth er i ns ig ht i nto th e re lati on b etw e en
fu 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 e
mic diets can facilitate greater body fat loss than isoenergetic
high- insWinemic die ts .
We thank Efi Farmakalidisfor her assistancein the planningof this
study and NatashaPorter forher technical assistance with the experimental
work for the carbohydrate-rich food group.
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Recommended