Pasta cooking time: influence on starch digestion and plasma glucose and insulin responses in healthy subject&3 Francis RJ Bornet, Jean Delort Lava!, ABSTRACI’ digestion

The and

plasma

Denis Cloarec, and Jean-Paul influence glucose

Jean-Luc Galmiche

ofpasta and

c.ooking

insulin

responses

Barry,

time

Paul

Colonna,

Sylvie

Methods

on starch

was studied

in 12 healthy subjects. During 3 consecutive days, one of three pasta test meals (50 g starch) cooked for 1 1, 16.5, and 22 mm was served to each volunteer in a random order. Hydrogen and methane breath excretion was measured after pasta ingestion; plasma responses were compared with those of an equivalent oral glucose-tolerance test. No significant differences were found between cooking times and plasma indices, orocecal transit time, or incremental hydrogen excretion ( peak hydrogen). With one exception, pasta meals that were completely absorbed were ingested by methane producers. Postprandial peak hydrogen was significantly lower in methane than in nonmethane producers (p < 0.02). These results point to a lack of influence ofcooking time on nutritional characteristics of pasta and suggest that starch malabsorption determined by breathhydrogen-test criteria may be underestimated in methane producers. Am J C/in Nuir 1990;5l:421-7.

Subjects

insulinemic

Pasta, cooking time, breath-hydrogen test, methane producer status, glycemic

test, index,

index

Introduction Starchy carbohydrates represent the major source of nutritive energy in humans. Recent investigations in man, with use ofthe breath-hydrogen test, indicated the existence ofa malabsorption by the small bowel of most starchy foods including pasta (1, 2), which may not only modify energy food value but induce abdominal discomfort as well. Other studies showed that the digestion of durum-wheat pasta by diabetics and healthy subjects is characterized by reduced plasma glucose and insulin responses (3-5). Both sets of effects could be explained by a reduced susceptibility of pasta starch to digestion by a-amylase. Digestibility ofstarch in foods by a-amylase can be modified in vitro as well as in vivo by numerous factors inchuding starch origin (6, 7), nonstarchy components such as fibers(8, 9)or glutinous protein (1, 10, 1 1), and food processing (12-16). The aim of this study was to evaluate the effects of pasta cooking time on plasma glucose and insulin responses and on intestinal malabsorption of starch in healthy subjects by using the breath-hydrogen and -methane test methods. Am

J C/in

Nuir

1990;51:42l-7.

Printed

in USA.

© 1990 American

Society

Downloaded from https://academic.oup.com/ajcn/article-abstract/51/3/421/4695053 by Washington University at St Louis user on 23 March 2018

and experimental

design

Twelve young healthy volunteers [six men and six women, aged 22.6 ± 2.5 y, (1± SD) mean body mass index 20.8 ± 2.6 kg/m2] with no history of gastrointestinal disease or diabetes gave their informed written consent to participate in a study approved by the Ethics Committee of the H#{244}pitalGuillaume et Ren#{233} La#{235}nnec. The pasta test meals consisted of spaghetti, industrially produced (Panzani, Marseilles, France) from durum-wheat semolina and dried at a low temperature of 55 #{176}C. The pasta (100 g dry matter) was boiled in 2 L 0.7% salted Evian (BSN Co, Evian, France) water for either 1 1 (Tl), 16.5 (T2), or 22 mm (T3) on the basis of an established reference method ( 17). Immediately after cooking, the water was drained for 1 mm through a colander with 1-mm pores and the pasta meal was served. Each pasta test meal consisted of 50 g starch, 10 g protein, 1.6 ghipids, 275 kcal(1 150 J), and a variable water content comprising

KEY WORDS breath-methane

Gouilloud,

140,

180,

and

220

g for

the

Tl,

T2,

and

T3

test

meals, respectively. To ensure uniformity of water content in the three test meals, an additional drink of water of 1 10, 70, and 30 g accompanied the Tl, T2, and T3 pasta meals, respectively. The chemical and physicochemical characteristics of pasta before and after cooking were reported by Cohonna etal(18). The order ofthe three pasta meals was randomly assigned to each volunteer during a 3-ti consecutive test period by using a Latin-square experimental design; meals were eaten at 0900 h within 6 mm after an overnight fast and immediately preceded by meticulous oral hygiene. Each evening meal preceding the morning test was standardized to contain a low level of mdigestible material and consisted of fish (100 g), white rice (200 I From INRA, Laboratoire de Technologie Apphiqu#{233}e a Ia Nutrition: the Service d’Exploration Fonctionelle Digestive, H#{244}pital Guillaume et Ren#{233} La#{235}nnec;INRA, Laboratoire de Biochimie et de Technologie des Glucides; and the GIS, Nutrition Glucidique de l’Homme Sam, Nantes, France. 2 Supported by a grant from the Minist#{232}re de Ia Recherche et de

l’Enseignement Sup#{233}rieur(MRES), Paris. 3 Address reprint requests to FRi Bornet, INRA, Laboratoire de Technologie Appliqu#{233}ea Ia Nutrition, BP 527 44026, Nantes Cedex 03, France. Received September 14, 1988. Accepted for publication April 12, 1989. for Clinical

Nutrition

421

422

BORNET

g). white

bread

(80

g), a portion

of Camembert

cheese

(30

ET

AL

g), in compressed

and

( 125 g); water

yogurt

Blood

sampling

ingestion

and breath

was permitted

and

a lactulose

smallest a linear

analysis

Baseline testing was done during meals, with volunteers subjected

test

ad hibitum.

test.

The

the week to an oral

glucose

tolerance

test

(55.5

g

D-glucose diluted in 250 mL water equivaglucose units) was performed at 0900 h after

a 12-h fast.

samples

15 mm

Blood

for 60 mm

sampling

during

were

after

the

drawn

glucose

next

mm before

30

ingestion

and

followed

Norgan

with

1%

chlorhexidine

solution;

Paris)

to reduce

oropharyngeal

to produce

an

increase

20 ppm above baseline values (nadir tration) at one or more breath collections ingestion

(2 1, 22).

as a mean

breath-methane-sample in ambient

Blood

samples hour

during the

2 h thereafter.

9000 glucose

sustained

increase

micro-

hydrogen

status

was

concentration

of

Samples

were

were

of

3 ppm

immediately

assayed

centrifuged

at

for later testing. Plasma by using a glucose-oxidase

The glycemic the ratio response

from

Breath

samples

before

had

one

access

valve.

plastic

in a second

The

and

determined

DP gas chromatograph 60/80

WI) mesh;

to water

was similarly

cal-

intervals meal.

by using Quintron

as the time

to represent

Therefore,

from

the penodjust

orocecal

the beginning

before

hydrogen

the

of car-

the first detectable

(22, 25, 26).

ad hibitum

the end

rubber

end

methane simultaneously (Quintron a molecular Instrument

alveolar

anesthesia

alveolar

plastic usually

Statistica/analysis

Analysis of variance was used to test the effect of subjects, cooking time, and order of pasta meals. Multiple comparisons between the test-meal data were made by using the method of Newman-Keuls (27). Analysis for significance between lactulose

or glucose-tolerance-test

was performed

data

by using

comparison

between

and

Student’s

that

of the

test for paired

t

methane-producer

ducer data was made Results are expressed

after

air

was

syringes analyzed

air was

then

then

fitted within

concentrations

and

by using Student’s as means ± SEM.

test

data

meals

whereas

nonmethane-pro-

test for unpaired

t

data.

indexes

colwith

sam-

areas

responses tolerance

under

after

the

the plasma

observed test

glucose

significantly

pasta

I 80 mm after

are shown

in Figure

test

meals

curves

different with

those

or the glycemic

when

comparing

after

the

glucose

test.

tolerance

test

nificantly. However, meals did not differ

and

after

the

pasta

test

insulin responses significantly.

meals

after

the

differed

sig-

three

pasta

Breath excretion Although

(nadir

Downloaded from https://academic.oup.com/ajcn/article-abstract/51/3/421/4695053 by Washington University at St Louis user on 23 March 2018

glucose glucose

The mean plasma insulin profiles observed within 180 mm ofthe pasta meals and the glucose tolerance test are illustrated in Figure 1 and summarized in Table 2. From 15 to 120 mm after the start of the tests, insulin concentrations after the glu-

gen

as the

carrier gas at a flow rate of 40 mL/min. The chromatograph was calibrated with a hydrogen and methane reference mixture

and

were generally

tolerance

Co).

used

plasma

meals

and

values

cose

with three2 h of collec-

air was

mean

1, with the mean postprandial plasma glucose variations summarized in Table I The mean glycemic i peak value occurred significantly faster (p < 0.05) after the Tl pasta meal (31 ± 2 mm) than after the glucose tolerance test (40 ± 3 mm) but not significantly faster than after the other pasta test meals (T2 and T3). After the pasta meals the mean z plasma glucose responses above baseline fasting concentrations were only halfas high as those after the glucose tolerance test (p < 0.001). The mean z peak plasma glucose under the baseline fasting value was also significantly greater (p < 0.001) after the glucose tolerance test than after the pasta meals. Although there were no significant differences in the plasma glucose responses between pasta meals in the 3-h postprandial test period, plasma glucose varia-

with a MICRO LYZER Instrument Company, Milsieve column ( 12’ Hysep Q, Dry

in plasma

pasta

tions

immediately

in breath

The the

30

the first

bag adapted

Responses

re-

from Subjects

obtained by having into two bags conthe first 500 mL of expira-

When

bag,

bag (l-L

valve).

tion (23). The hydrogen

waukee,

test meal as

Alveolar air samples were exhale through a mouthpiece

air filled

were

index

of a test

and

pasta

curves.

at 1 5-mm

transferred into 50-mL way stopcocks, and was

ples

insulin ingestion

by a three-way

a one-way

insulinemic

collected

period.

lected

for each

method

areas under the 3-h glycemic and to the glucose tolerance test,

were

seated

the subjects

separation

to 9 h after

3-h

test

The

the respective

mained

tory

was calculated

as a percent.

culated

nected

a charcoal of 6%.

between the incremental curve to a pasta meal

expressed

mm

by using reproducibility

index

was considered (24).

in breath

test meal, an increase over baseline (nadir of upon two consecutive

.

method (Beckman Autoanahyzer II, Beckman, Fullerton, CA) with an intraassay reproducibility of 2%. Plasma insulin was tested by radioimmunoassay (Anti-insulin antibody, Novo Industri, Copenhagen) with an intraassay

until

The with

Results

defined

30 mm before and every 15 mm test meal, then every 30 mm for

x g for 10 mm at 4 #{176}C and frozen concentrations

was defined

by 30-mm

air.

were drawn after a pasta

the

time

Co).

was 2 ppm

ofthe hydrogen concenafter a standard lactu-

Methane-producer

above

that

transit

samplings,

malabsorption

intake

Givalex,

in breath

>

lose

breath starch

bohydrate

floral activity (19, 20). Breath samples were collected at 15-mm intervals from 30 mm before lactulose ingestion until 6 h afterwards. During the test, subjects were forbidden to eat, smoke, or exercise. Hydrogen-producer status was defined as the ability of a subject

Instrument

ofboth gases of 2- 150 ppm.

2 h.

a

Laboratories,

1 5-mm-interval significant

every

The lactulose test, consisting of 10 g lactuhose syrup (Duphalac, Duphar Laboratories, Villeurbanne, France) in 100 mL water, was done at 0900 h after suitable oral hygiene (careful mouthwashing

2, Quintron

concentration response range

During the 9-h period after the pasta in hydrogen concentration of 10 ppm the hydrogen concentration), measured

preceding the test glucose-tolerance

monodehydrated lent to 50 g starch

air (Quingas

detectable accuracy

were

all subjects

methane

producers

(

increment

peak

were as well.

hydrogen The

hydrogen)

over

of the hydrogen concentration) was 50.8 ± 8.4 ppm for the nonmethane

M(-)]

and

38

±

8.9

ppm

for

producers, mean

the

basal

ofmaximal

breath

only

half

hydro-

hydrogen

after the lactulose test producergroup [group methane

producer

group

PASTA

COOKING

TIME

AND

STARCH

amylase

susceptibility

and

tion of food starch a more disorganized

(C)

heating nized

423

DIGESTION in vivo

starch

by pancreatic state of the

bioavailability.

or shearing in excess water. state is a function of swelling

This maximally temperature,

pends on the type ofstarch used (28). In agreement with earlier studies in diabetics healthy

subjects

white jects

(4),

our

durum-wheat led

flour

occurred

more

test. The significant test and the Tl pasta

confirmed

in the

form

smaller

and insulin concentrations lution. Mean glycemic meals

study

to a significantly

Diges-

amylase can be increased starch molecule. obtained

and

than after insuhinemic

rapidly

than

disorgawhich de-

of pasta

I 400

time

subglucose

an equivalent glucose peaks after pasta after

carbohydrate,

of

by healthy in plasma

the

difference between the meal in terms of plasma

pasta a slow time and/or

consider peaking

in

ingestion

which

to return

sotest

glucose

tolerance

glucose glucose

tolerance peaking

time may be ascribed to the relatively large time mm) between blood samplings. A shorter sampling val would probably have reduced the differences.

600

5) and

(3,

that

increase

by by

interval (15 time interRather than

supposes

to basal

a delay

in

it may

be

value,

better glucose

defined as a low-effect carbohydrate. Although concentrations decreased below fasting values

second cemic

hour ofthe phenomenon

plasma after the

rI,

z .

200 ri (ns)

100 0 30

0

60

90

120

TIME FIG

vitro

‘

150

180

(mm)

Plasma glucose and insulin responses(i± SENt) in 12 healthy subjects for 180 mm after receiving pasta test meals cooked I 1 (T I , 0). 16.5 (T2, El), and 22 mm (T3, S), or after oral glucose-tolerance test (A). Each carbohydrate test contained 50 g starch or equivalent glucose units. Significance between glucose tolerance test and pasta test meals was as follows: ns, not significant; a, p < 0.05: b. p < 0.02: c, p < 0.01: and d. p < 0.001. [group

M(+)J.

The

was not significant. Figure 2 shows centration given time

difference

between

the variations

the

in mean

9 h after ingestion of the no significant differences

drogen concentrations tions between test

mean

group

three were

pasta found

meals were

or mean peak hydrogen concentrameals (Table 3). The mean estimated oroce-

(of 36), which were apparently ingested by methane-producer

the distribution tions after the their

con-

meals. At any in breath-hy-

cal transit time in subjects with starch mahabsorption 10 subjects after Ti , T2, and T3 meals, respectively) differ significantly. With the exception of one meal,

of mean three pasta

methane-producer

peak meals status.

The

ence, 25 ± 2 ppm for group M(-) M(+), was significantly different (p

mean

vs 15

(7, 9, and did not those 10