KEY WORDSphysiological measures

Stress, relaxation, carbohydrate digestion, starch, cereal, oral cavity, saliva,

AmJClin Nuir 1989:49:97-105. Printed in USA. © 1989 American Society forClinical Nutrition 97

Oral digestion of a complex-carbohydrate cereal: effects ofstress and relaxation on physiological andsalivary measures12

Donald R Morse, George R Schacterle, Lawrence Furst, Mark Zaydenberg, and Robert L Pollack

ABSTRACT A comprehensive study was undertaken with 12 dental hygiene students to

ascertain whether the time ofchewing or the degree ofrelaxation is more important in the oral

digestion of complex carbohydrates. In addition, we studied whether the effects of stress and

relaxation on salivary a-amylase activity was corroborated by physiologic measures. The den-

tal hygiene students chewed an oat cereal for either 20 or 60 s while under two different ordersof stress and relaxation conditions: 1) stress/20 s, stress/60 s, relax/20 s, relax/60 s; and 2)

relax/20 5, relax/60 s, stress/20 s, stress/60 s. Galvanic skin resistance, pulse rate, and bloodpressure (systolic and diastolic) were used to physiologically verify the effects of stress andrelaxation on amylase activity. Amylase activity was judged by spectrophotometric analysisof maltose produced from a specific dilution of expectorated saliva. Results showed that thephysiological measures significantly corroborated the salivary determinations ofstress and re-

laxation and that deep relaxation was significantly more important than thorough chewing inthe oral digestion ofcomplex carbohydrates. Am J C/in Nuir 1989:49:97-105.

Introduction

We have conducted investigations on the effects ofstress and relaxation on saliva, including its volume, vis-cosity, pH, and protein, glycoprotein, bacteria, and a-amylase content ( 1-8). Stress was induced by endodontic(root canal) therapy, college examinations, or mentalarithmetic. Relaxation was induced by transcendentalmeditation (TM) or by simple-word meditation (9). Dur-ing relaxation, contrary to stress, there were statistically

significant decreases in salivary protein, glycoprotein,bacteria, and viscosity and increases in salivary volume,pH, and a-amylasc activity. The salivary determinationsof stress and relaxation were corroborated by question-naire and physiological measures.

The salivary findings are apparently related to the au-tonomic nervous system (ANS) innervation of the sali-vary glands. The sublingual and minor glands are pre-dominantly composed of mucous cells that are activatedby the sympathetic division ofthe ANS to produce large-molecular-weight, glycoprotein-rich, low-volume saliva,which mainly accounts for the increased protein, glyco-protein, and viscosity of the stress-induced saliva. Theparotid glands arc predominantly composed of serouscells that are activated by the parasympathetic division

ofthe ANS to produce an a-amylase-rich, high-volume,free-flowing, high-bicarbonate saliva that mainly ac-

counts for the increased volume, amylase activity, andpH and the decreased bacteria of relaxation-induced sa-liva (10-13). The submaxillary glands have an approxi-

mately equal mixture of mucous and serous cells. The

type of secretion varies depending on the relative condi-tions of stress and relaxation, among other factors suchas food intake.

Salivary a-amylase (primarily produced by the parotidglands) is the principal salivary protein ( 1 1). It catalyzes

the breakdown of large-molecular-weight complex car-bohydrates to produce maltose (principally), maltotri-

ose, a-limit dextrins, and a small amount of D-glucose( 12). Parotid saliva (unlike submaxillary, sublingual, andminor-gland secretions) is greatly augmented by physical

and chemical stimulation (14). We found significantly

higher parotid cx-amylase activity under relaxed chewing

I From the Departments of Endodontology and Biochemistry andNutrition, Temple University School ofDentistry. Philadelphia. PA.

2 Address reprint requests to DR Morse, Department of Endodon-

tology, Temple University School of Dentistry, 3223 North Broad

Street, Philadelphia, PA I 9140.Received October 22. 1987.Accepted for publication February 9. 1988.

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98 MORSE ET AL

conditions than under relaxation alone ( 1 5). In that

study, 4 ofthe 40 subjects were trained in either medita-tion or hypnosis. Their mean a-amylase activity was sig-

nificantly greater than the mean a-amylase activity of the36 other subjects. With this background, we decided toinvestigate amylase activity during the chewing of com-plex carbohydrate foods.

The rationale for the recent series of investigationsinto salivary amylase activity was three-fold. First, thereis currently a widespread interest in complex carbohy-

drates as a major food constituent and energy source forathletic performance, for use in weight-loss diets (16),and as a possible preventive measure for coronary heartdisease, diabetes mellitus, some gastrointestinal diseases,and colon cancer (17-19).

Second, there are conflicting reports on the impor-

tance of oral digestion of complex carbohydrates. Someauthorities contend that food does not remain in themouth long enough for more than a small percentage of

dietary starch to be converted to maltose (20-22). Othersmaintain that if chewing is thorough, a major part ofstarch is converted to maltose (23). Unfortunately, cvi-

dence is not given for either viewpoint. With evolutionsalivary a-amylase has remained intact as a componentofcomplex carbohydrate digestion but there is little cvi-

dence that fat or protein digestion occurs orally. This ap-

pears to emphasize the importance ofthc first stage (oral)ofcomplex carbohydrate digestion. It has also been em-

phasized that saliva is not sufficiently alkaline to havemuch digestive activity because a-amylase works best inan alkaline medium (as is present in the small intestine)(24). However, in three studies we found that saliva isacidic during stress but alkaline during relaxation (2,6,7).

The third reason for investigating salivary a-amylaseis that the rate of oral digestion of starches was found to

be related to the blood glucose response (glycemic index)

after ingestion offood (25-27). This is important to dia-betics because it is usually thought that foods that in-

crease the blood glucose level the least for a given carbo-hydrate are most suitable for the diabetic (26).

To help in the resolution of the divergent viewpoints

with regard to oral digestion of starches, the first casestudy was undertaken (28). Two other purposes for thatinvestigation were to evaluate the varying amounts of

maltose found in some common complex carbohydratefoods and to determine how much digestion of thesefoods occurs from the activity ofsalivary a-amylase.

In this and all subsequent studies, we used in vivo cx-pectoration of a chewed food for a-amybase-activity de-termination rather than analyzing a-amylase activity invitro by quantitatively collecting saliva. We used in vivo

expectoration because we wanted to examine the amy-lase activity resulting from chewing a variety of complex-

carbohydrate foods to find one food that could be usedas a model. based on its ability to produce a large mean

amount ofmaltose across conditions. In all ofthe studiesthe percentage of available carbohydrate in the various

foods that was actually digested orally was not deter-mined. Although it would have been of interest to havedetermined the actual percentage of digestion of avail-

able carbohydrate, we could find no practical way toachieve this.

The subject ofthe case study (28), a trained meditator,had his salivary a-amylase activity measured as he

chewed 1 5 different starch foods while he was under theconditions of stress and relaxation. The major findingswere 1) a statistically significant increase in maltose pro-

duction with 60-s chewing as opposed to 20-s chewing; 2)

a statistically significant increase in maltose productionwith relaxation as opposed to stress; 3) no order effect;and 4) certain foods such as an oat cereal accounted forthe largest mean amount ofmaltose under all conditions.

To generalize these findings, a comprehensive studywith 20 dental hygiene student subjects was undertaken

(29). The subjects chewed an oat cereal for the same 20-

and 60-s time periods as in the case study (28). Becausethere was no order effect in the case study, only the first

order was used in this study, ie, under stress while chew-ing for 20 s (stress/20 s), stress while chewing for 60 s

(stress/60 s), relaxation while chewing for 20 s (relax/20s), and relaxation while chewing for 60 s (relax/60 s). Asin the previous study (28), stress was induced by the samemental arithmetic exercise and relaxation was inducedby the simple-word meditation technique (9, 30). The

main findings were a statistically significant increase in

maltose production with 60-s chewing as opposed to 20-s

chewing and a statistically significant increase in maltose

production with relaxation as opposed to stress.

Because no independent measures were used to verify

the conditions of stress and relaxation as determined by

the changes in saliva in the two previous studies (28, 29),another study was undertaken with 25 female dental hy-giene students as subjects (3 1). The main purpose of this

new study was to corroborate the findings concerning

salivary a-amylase relative to stress and relaxation andrapid (20-s) and slow (60-s) chewing. To accomplish this

only the conditions that previously showed the most di-verse findings were evaluated, ie, stress/20 s and relax/60

5. The physiological indices of galvanic skin resistance(GSR), pulse rate, and both systolic and diastolic bloodpressure were used as the corroborative measures of

stress and relaxation (7, 9, 30, 32). The main findingswere a statistically significant greater a-amylase activity

under rclax/60 5 than under stress/20 s, and all the physi-ological measures corroborated the findings concerning

salivary amylase with respect to the determination of

stress and relaxation.

This study was undertaken not merely as a reworking

or replication of the previous studies but rather, to in-

dude all ofthe previous components in one study and todetermine, if possible, which is more important in the

oral digestion of complex carbohydrates: time of chew-

ing or degree of relaxation. Because it required > 3 hI

subject to do all ofthe necessary procedures and the pool

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ORAL DIGESTION OF COMPLEX CARBOHYDRATES 99

of subjects was defined by the dental hygiene curricularequirements, the number ofsubjects had to be limited.

Subjects and methods

Subjects

The subjects were 12 female dental hygiene students with amean age of 20.8 y (range 18-32 y). All subjects were in goodhealth, were not taking any drugs, and had fully functioningsalivary glands. None of the subjects were pregnant (a condi-tion in which salivary rate usually increases [33]) and nonewere evaluated while in the premenstrual or menstrual state(a condition in which salivary rate usually decreases [34]). Tocontrol for other variables that could affect salivary secretion,such as hunger (salivary rate increases with meal anticipationand sight and odor offood [35]) and circadian rhythm (salivary

rate usually increases early in the morning [36]), all ofthe sub-jects were seen on the same day (Thursday) and at the sametime (morning). All subjects gave their informed consent bysigning a form approved by the Human Research Study Re-view Board at the Temple University Health Sciences Center.This organization approved of the experiments performed inthis study.

Measurements and procedures

Each subject sat partially inclined in a comfortable chair.The room was isolated, with moderate temperature and hu-midity. No external distractions were present. The same men-tab arithmetic exercise (with subject verification ofits stressfulnature), simple-word meditation technique, and 5-g portion ofoat cereal (Cheerios#{174},General Mills, Inc, Minneapolis, MN)was used as in the previous studies(28, 29, 31). The same physi-obogical indices were used as in the previous study with dentalhygiene students (31), ie, GSR, pulse rate, and systolic and dia-stolic blood pressure. As in the case study (28), two conditionorders were used, ie, stress/20 s, stress/60 s, relax/20 s, relax/60s; and relax/20 s, relax/60 s, stress/20 s, stress/60 s.

The same measurement procedures and techniques wereused as in the previous study with dental hygiene students (31).However, because some of these methods may not be wellknown, a briefdescription ofthem is now given.

The portion of oat cereal was placed in a sterile, plasticweighing boat immediately before use. The subjects were toldto start chewing immediately on receiving the first portion ofcereal. The subjects kept their eyes open during the stress con-

ditions. In previous studies, it was shown that merely closingthe eyes can increase the frequency of a brain wave patterns onthe electroencephalogram, but other indices of relaxation (eg,GSR, pulse rate)do not necessarily change(30, 32). We showedthat during meditation (when it is standard for the eyes to beclosed) sympathetically induced submaxillary and sublingualsaliva decreased significantly but parasympathetically inducedsubmaxillary and parotid saliva increased significantly (1-8,15, 28, 29, 31). Opposite results occurred during stress (witheyes open). Because a-amylase levels are flow-dependent, it isexpected that some aspect ofthe difference in a-amylase activ-ity that might be found between stress and relaxation is depen-dent on the eyes being closed during relaxation and openduring stress. Nevertheless, in our previous studies of salivawe recorded significantly higher a-amylase activity duringmeditation than during simple eye closure without relaxation(1-8, 15, 28,29,31).

For 5 mm while under stress conditions, the subjects per-formed the mental arithmetic exercise. The mental arithmeticwas continued during the actual chewing periods. The subjectskept their eyes closed during the relaxation conditions. For 5

mm while under these conditions, the subjects performed thesimple-word meditation technique. The eyes were kept closedand the meditation was continued during the actual chewingperiods.

Before each subject performed the mental arithmetic exer-cise and the simple-word meditation technique, the GSR 2#{176}(Thought Technology Ltd, Montreal, Canada) device was at-tached to the index and middle finger of the left hand and theblood pressure cuff(Digiprint 2000 Digital Blood Pressure andPulse Rate Monitor#{176},Labtron Scientific Corp, Hauppauge,NY) was attached to the right arm. Two readings were takenfor each measure during each condition order and the meanwas entered as the value. The first readings were taken immedi-ately before the subjects began to chew the food. The secondreadings were taken immediately after the subjects expecto-

rated the food. The GSR readings were taken and entered byan individual who was not involved in the study. The bloodpressure and pulse rate readings were automatically recordedand printed; they were then placed in the subjects’ records. Be-cause the subjects were not permitted to move their arms be-cause ofthe attached devices, the food was fed to them duringthe allocated time periods.

Immediately after each chewing, each subject completely ex-pectorated the paste into a homogenizer cup. Distilled waterwas then added until it reached a premarked level within thehomogenizer cup. The cup and its contents were then thor-oughly mixed in a liquefier blender (Oster Division, SunbeanCorp. Milwaukee, WI) for exactly 1 mm. The material was thentransferred into two centrifuge tubes and centrifuged (modelHN-S, International Equipment Co. Needham Heights, MA)for exactly 5 mm at 2000 rpm. One milliliter ofthe supernatantfrom one of the two tubes was then added to 19 mL distilledwater to make a 1:20 dilution. (The second tube was kept as aback-up in case of spillage.) The diluted solution was subse-quently thoroughly mixed for 1 mm. Then 1 ml ofthe solutionwas added to I mL maltose reagent (1 g 3,5-dinitrosalicylic acidin 20 mL sodium hydroxide (NaOH, 2 mol/L)(NaOH) and 30g NaK-tartrate and enough water to make 100 mL) in anothertest tube. This tube was then placed in a boiling water bath forexactly 5 mm. It was subsequently withdrawn and run undercold tap water for 1 mm. Ten milliliters of distilled water wasthen added to the test tube. The tube was subsequently placedin the reading tube of the spectrophotometer (Spectronic 20#{176},Bausch and Lomb, Rochester, NY). The absorbency was readat 530 nm. Milligrams of maltose per originally expectoratedsample were calculated with the following formula:

Milligrams of maltose ofsample/l mL = (A ofU/A of 5)

x mg ofmaltose ofstandard X (l/V) (1)

where U = unknown, S = standard, and V = volume of thesupernatant. The standard was prepared from I mL maltosestandard (1 mg/l mL) that was placed in the reading tube andthe absorbency was read at 530 nm. In this study S = 46.0 mgimL and V = 0.05 mL in all cases.

For each ofthe four conditions, milligrams maltose per mil-liliter per sample was obtained in both condition orders. Thenthe two readings per order in each condition were totaled anda mean per condition was obtained. For example, with stress/20 s, ifthe reading was 25 mg/mL in order 1 and 23 mg/mL in

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100 MORSE ET AL

0.99(11 36) = 2.82.t F0��3,331 = 4.41.

TABLE 1Comparison between two orders ofmean values ofmaltose under four experimental conditions (mg/mL)

Stress/20 5 Stress/60 s Relax/20 s Relax/60 s

Order 1 37.9 46.9 57.9 79.9

Order2 37.3 47.1 56.2 81.0

j;� SD 37.6 ± 10.72 47.0 ± 10.05 57.0 ± 17.67 80.4 ± 24.41

Variance 114.92 101.00 312.23 595.85p >0.05 >0.05 >0.05 >0.05

* I test results, NS. n = 12. The mean ofall values is 55.3 mg/mL. The differences between stress/20 s and relax/20 s and between stress/60 s and

relax/60 5 were 19.4 and 33.4 mg/mL, respectively.

order 2, the readings were combined and a mean of24 mg/mLwas obtained and entered as the reading for stress/20 s for thatsubject.

In addition to the two experimental conditions there was acontrol, which was a measurement ofthe milligrams of maltoseper milliliter ofthe oat cereal before it was chewed and digestedby a-amylase. A 5-g sample ofthe cereal was homogenized with

distilled water to the same predetermined level in the homoge-nizer cup. It was then analyzed for maltose content in the sameway as under the experimental conditions.

Statistica/ana/ysis

The t test was used to determine if there was any significantdifference between the milligrams per milliliter maltose read-ings for the two orders per each condition. A two-factor analy-sis of variance (ANOVA) with repeated measures was em-ployed to analyze the results with respect to mean values ofmaltose (mg/mL) produced from the oat cereal under the fourconditions (stress/20 s, stress/60 s, relax/20 s, relax/60 s) (37).A Newman-Keuls procedure was used to determine which ofthe conditions contributed to the overall statistical significance.A correlated t test was employed to analyze the results for thedifferences with each ofthe five measures (maltose, GSR, pulserate, systolic blood pressure, diastolic blood pressure) betweenthe stress/20-s and relax/20-s conditions and the stress/60-sand relax/60-s conditions. Cochran’s relatively simple test (37)was used to test for homogeneity of variance. The level for sig-nificance for all statistics was set at 0.05.

Results

main effects of the four conditions is statistically signifi-cant (F = 23.32, df 3, p < 0.01). Further analysis withthe Newman-Keuls procedure to determine which of theconditions contribute to the overall statistical signifi-

cance is presented in Table 3. The conditions are signifi-cantly different from each other (p < 0.05) and the or-dered conditions (means) from the least to the greatestare as follows: stress/20 s (37.6 mg/mL), stress/60 s (47.0mg/mL), relax/20 s (57.0 mg/mL), and relax/60 s (80.4mg/mL) (Fig 1).

From the data in Table 1, the mean value of2O-s chew-ing is calculated as 47.3 mg maltose/mL whereas themean value of 60-s chewing is 63.7 mg/mL. The meandifference between these averages is 16.4 mg/mL whichis statistically significant (p < 0.01). The mean value ofrelax is 68.7 mg maltose/mL whereas the mean value ofstress is 42.3 mg/mL. The mean difference between theseaverages is 26.4 mg/mL, which is also statistically sig-nificant (p < 0.01). The difference in maltose productionbetween relaxation and stress is greater than the differ-ence between 20- and 60-s chewing (Fig 1).

Corroborative measures

The results ofthe correlated t test for the five measuresunder stress/20 s and relax/20 s are shown in Table 4.The results of the correlated t test for the five measuresunder stress/60 5 and relax/60 s are shown in Table 5. Inrelax/20 5 as opposed to stress/20 s the increased mean

Maltose findings

A comparison between the two orders ofthc mean val-ucs of maltose under the four experimental conditions ispresented in Table 1 . Note that there is no significant

difference between the values for the two orders. A sum-mary of the ANOVA with repeated measures for the 12

subjects under 4 experimental conditions with respect tooat cereal in terms ofmean values ofmaltose is presentedin Table 2. As a reference point it can be noted that themean value of maltose for oat cereal homogenized with

distilled water is 4.3 mg/mL.As shown in Table 2 the main effects between subjects

for all conditions is statistically significant (F = 3.23, df= 1 1 , p < 0.01), which suggests that individual differ-ences are important. More importantly, however, the

TABLE 2Summary ofANOVA with repeated measures ofmean values ofmaltose in mg/mL for oat cereal under four conditions for 12 subjects

Source ofvariation

Squaresofsum

Degreesoffreedom

Meansquares

Varianceratio

Betweensubjects 12208.74 11 1 109.89 3.23Within subjects 12 362.74 36 343.41

Conditions 8 400.6 1 3 2 800.20 23.32tResidual 3962.13 33 120.06

Total 24571.48 47

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TABLE 3Summary ofNewman-Keuls procedure for differences between mean values ofmaltose in mg/mL under four conditions

S/20 S/60 R/20 R/60 S R 20 s 60 s

Conditions

ORAL DIGESTION OF COMPLEX CARBOHYDRATES 101

Condition (Ordered)

Stress/20 5

(37.6 mg/mL)

Stress/60 s

(47.0 mgJmL)

Relax/20 s

(57.0 mgjmL)

Relax/60 s

(80.4 mg/mL)

Stress/20s (37.6 mg/mL) - 9.4 19.4t 42.8t

Stress/60 5 (47.0 mg/mL) - 10.0 33.4t

Relax/20 5 (57.0 mg/mL) - 23.4tRelax/60 5 (80.4 mg/mL) -

* p<0.05. 9.13 11.03 12.13

t p<0.Ol. 12.29 14.06 15.17

maltose is highly statistically significant (corr-t = 5.98, p

< 0.01); the increased GSR (lower values in the arbitraryscale used) is also highly statistically significant (corr-t= -5.26, p < 0.01); the decreased pulse rate is in the mdi-cated direction but it was not statistically significant(corr-t = - 1.70, p > 0.05); the decreased systolic bloodpressure is highly statistically significant (corr-t = -4.68,p < 0.01); and the decreased diastolic blood pressure ishighly statistically significant (corr-t = -4.85, p < 0.01).In relax/60 s as opposed to stress/60 s the increased meanmaltose is highly statistically significant (corr-t = 6.3 1 , p

< 0.01); the increased GSR (lower values in the arbitraryscale used) is highly statistically significant (corr-t= -7.42, p < 0.01); the decreased pulse rate is highly sta-tistically significant (corr-t = -3.33, p < 0.01); the de-creased systolic blood pressure is highly statistically sig-nificant (corr-t = -4.58, p < 0.01); and the decreaseddiastolic blood pressure is highly statistically significant(corr-t = -2.87, p < 0.01). Hence, the four physiologicalmeasures corroborate the a-amylase activity measure asa determinant ofstress and relaxation.

Discussion

In a previous study of dental hygiene students (31),correlated t analysis of the physiological measures of

FIG I. Summary ofmean values ofmaltose (mg/mL) for oat cereal

under the conditions stress/20 s, stress/60 s, relax/20 s, relax/60 s, andcombined stress, relax, 20 s, and 60s.

GSR, pulse rate, and systolic and diastolic blood prcs-sure, along with the salivary a-amylase-produced malt-ose, showed that there were statistically significantdifferences between the stress/20-s and relax/60-s condi-tions. In the present study, correlated I analysis of thesame measures showed that there were statistically sig-nificant differences among all four conditions, ie, stress/20 s, relax/20 s, and stress/60 s, and relax/60 s. Hence, itappears that the conditions that were labeled as stressand relaxation in the previous three studies of salivarydigestion (28, 29, 3 1) and the present study were appro-priately designated.

In this study the finding that the differences betweenindividuals was statistically significant (Table 2) was notof major interest to us. In expectation of this result, weused a repeated-measures design to control for individ-ual differences. In fact, the differences between individu-als tended to mask the differences ofinterest, which werethose between stress and relaxation and between rapid

and slow chewing. Differences between rapid and slowchewing are shown in the post hoc test (Table 3).

The variance for the stress conditions was generallylower than the variance for the relaxation conditions(1 14.92 and 10 1.00 vs 3 12.23 and 595.85, respectively;Table 1). It appears that the subjects of this study (andprobably individuals in general) are more alike in how

they react to stress than in how they react to relaxation.Employing Cochran’s relatively simple test, homogene-ity of variance is rejected at the 0.05 level but not at the

0.01 level (C = 0.53, C0.95 0.48, � = 0.55). On thebasis ofthis result, one may question the tenability of thehypothesis of homogeneity of variance with respect tothe stress and relaxation conditions. Recognizing thatthere is a difference between these conditions, we inter-pret the findings ofthe mean differences for the stress andrelaxation conditions with reasonable caution.

It also appears from the findings ofthis and the previ-ous studies of dental hygiene students (29, 3 1) that, ofthose used, the best measures for determining the condi-tions ofstress and relaxation are salivary a-amylase-pro-duced maltose and GSR. In a previous study (3 1) and inthe present one, every one ofthe subjects (25 + 12 = 37)produced a change in the indicated direction with themaltose measure. With GSR, only one subject showedan unexpected response. With the other three measures

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102 MORSE ET AL

TABLE 4Summary of mean values offive measures under the stress/20-s and relax/20-s conditions for 12 subjects

MeanMeasure Stress/20 s� Relax/20 s� difference Corr-tt

Maltose(mg/mL) 37.6 ± 10.72 57.0 ± 17.67 +19.4 +5.98t

Galvanic skin response (arbitrary units) 3.3 ± 0.24 2.0 ± 0.92 -1.3 -5.26fPulse rate(beats/min) 8 1.3 ± 9.36 78.9 ± 8.82 -2.4 -1.70

Systolic blood pressure(mm Hg) 106.5 ± 6.90 101.0 ± 5.62 -5.5 -4.68�Diastolic blood pressure (mm Hg) 73.9 ± 10.03 67.5 ± 8.06 -6.4 -4.85�

1±SD.

t rr511 = 1.80.t rr11 = 2.72.

(pulse rate and systolic and diastolic blood pressure),most but not all of the readings were in the indicateddirections.

In the two previous studies ofdental hygiene students(29, 3 1) the oat cereal had a small amount of maltose (�= 7.0 mg/mL) before digestion and it was readily digest-ible by salivary a-amylase to yield substantial amountsof maltose (mean stress = 6 1 .3 mg/mL; mean relax= 78.5 mg/mL). In the present study similar results werefound. Oat cereal yielded 4.3 mg/mL before digestion,and after digestion a mean of42.3 mg/mL was producedunder stress and 68.7 mg/mL was produced under relax.In the case study with a trained meditator (28), bothstress and relax conditions yielded a substantially greateramount ofmabtose from oat cereal (mean stress = 107.8

mg/mL; mean relax = 1 50.5 mg/mL). Although this wasa report involving only a single individual, it appears thata trained meditator has less stress manifestations (at leastas determined by a salivary measure) and a greater abilityto digest complex carbohydrates orally. The combinedresults ofthe four studies (28, 29, 3 1 , and this one) showthat oat cereal is a complex-carbohydrate cereal contain-ing a small amount of maltose that can be readily di-gested by salivary a-amylase to yield substantialamounts of maltose. Hence, under the proper chewingconditions foods such as oat cereal would be a readilyavailable source ofenergy because the maltose produced

TABLES

orally would require only one additional cleavage toyield two molecules of glucose. Although it is true thatmaltose could also be produced in the small intestine bythe action ofpancreatic amylases, it would appear that itis more efficient if a substantial amount of maltose pro-duction is done earlier in the chain of events (ie, in theoral cavity rather than the small intestine).

The other major disaccharide, sucrose, is much morecariogenic and is therefore bess advantageous than ismaltose (8). In a study on the influence ofvarious dietarycarbohydrates in caries activity in hamsters (38), the fob-lowing carbohydrates were analyzed: starch, dextrin, su-crose, maltose, lactose, fructose, and glucose. The resultsshowed that starch and dextrin did not support caries ac-tivity. Sucrose and fructose supported the highest cariesactivity, glucose and lactose were the next highest, andmaltose was the lowest. With rats, the results were notas clear-cut but generally maltose was significantly besscariogenic than was sucrose (38). Even though maltosemay produce acid that is potentially conductive to initia-tion of dental caries, the results of our stress-relaxationstudies on saliva (2, 6, 7) showed that the saliva becomesalkaline under deep relaxation. Hence, this could coun-

teract the maltose-induced acid production. In addition,in our four studies of sabivary-a-amylase digestion (28,29, 3 1 , and this one), the maltose present in the chewed-up bolus of food did not appear to adhere to tooth sur-

Summary ofmean values offive measures under the stress/60-s and relax/60-s conditions for 12 subjects

MeanMeasure Stress/60 s� Relax/60 s� difference Corr-tt

Maltose(mg/mL) 47.0± 10.05 80.4±24.41 +33.4 +6.31tGalvanic skin response (arbitrary units) 3.3 ± 0.28 1.5 ± 0.91 -1.8 -7.42�

Pulse rate (beats/mm) 83.0 ± 7.35 78.4 ± 8. 10 -4.6 -3.33�Systolic blood pressure (mm Hg) 105.8 ± 8.32 99.8 ± 4.96 -6.0 -4.58�Diastolic blood pressure (mm Hg) 7 1.0 ± 7.68 68.2 ± 7.82 -2.8 -2.87t

t rr9511 = 1.80.

tCorr-to�1111 = 2.72.

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ORAL DIGESTION OF COMPLEX CARBOHYDRATES 103

faces (an important requisite for initiation of dentalcaries). This was evaluated by physical examination; bio-chemical analysis was not done. Therefore, from cur-rently available information we believe that the maltosethat is formed from cereals such as oat cereal is not cario-genic.

As the result of the findings from this study and fromthe previous three studies on salivary digestion (28, 29,3 1), two apparently important chewing variables were

determined. These variables are involved in the oral di-gestion of complex carbohydrates. The first variable isthe amount oftime spent chewing. In the case study witha trained meditator (28), the mean value of2O-s chewingwas 72.8 mg maltose/mL whereas the mean value of 60-S chewing was 185.6 mg/mL. In the first dental hygienestudent study (29), the mean value of 20-s chewing was62.8 mg/mL whereas the mean value of 60-s chewingwas 99.9 mg/mL. In the second dental hygiene studentstudy (3 1), the mean value of2O-s chewing was 5 1 .3 mg/mL whereas the mean value of 60-s chewing was 65.5mg/mL. In the present study, the mean value of 20-schewing was 47.3 mg/mL whereas the mean value of 60-5 chewing was 63.7 mg/mL. The mean differences(1 12.8mg/mL in the case study, 37. 1 mg/mL in the first dentalhygiene student study, 14.2 mg/mL in the second dentalhygiene student study, and 16.4 mg/mL in this study) arestatistically significant (p < 0.01). Hence, it appears thatwith the longer time period there is more salivary a-amy-base present to digest complex carbohydrates, whichwould then result in the production of a larger amountofmaltose. The amount ofmaltose produced by the sub-ject ofthe case report (28) under the two time conditionswas substantially greater than the mean of values fromthe dental hygiene student subjects of the other threestudies (29, 3 1, and this one). In fact, not a single dentalhygiene student subject in any ofthose studies was closeto producing as much maltose as did the case study sub-ject. The probable reason is that the case study subjectis a male who is well-developed (a former weight-liftingchampion) who exerted excessive force while he waschewing. In contrast, the subjects ofthe three dental hy-gienc student studies arc all young females, none ofwhom are involved in weight training or any type ofheavy exercise. Nevertheless it is realized that this ratio-nale is hypothetical because there is no direct evidencethat physical strength is related to biting pressure. Fur-thermore, even if such evidence exists, biting pressurewas not measured in these studies.

Eighty percent of salivary a-amylase is produced bythe parotid glands (1 1 , 1 3). During chewing, contraction

ofthe buccinator muscles occurs and this activity resultsin massage ofthe Stensen (parotid) ducts. This allows formore forceful expulsion ofparotid saliva (14, 39). There-fore, the 60-s chewing should result in the expulsion ofmore amylase than the 20-s chewing. However, becausesalivary a-amylase levels were not measured, it cannotbe definitely stated that longer chewing time results ingreater a-amylase secretion. The rate-limiting step in

maltose production is not known; it could be either a-

amylase or starch levels or, possibly, pH. We did find inprevious studies (2, 6, 7) that saliva has an acidic pH dur-ing stress and an alkaline pH during relaxation. How-ever, that was not related to time ofchewing. It may evenbe that the higher maltose level in 60-s saliva reflects animproved efficacy of a-amylase digestion instead ofhigher levels of amylase.

Our findings apparently contradict the opinion ofSeckurt’s text (22) in which it is stated, “The extent towhich food is chewed has no effect on the processes ofdigestion and absorption; it is not necessary as proposedby some faddists to chew each mouthful of food for pro-longed periods of time.” Our results, in contrast, tendto support the old adage about the benefits of thoroughchewing.

The second important variable in the oral digestion ofcomplex carbohydrates is the degree ofrelaxation. In thecase study with the trained meditator (28), the meanvalue of relax was 1 50.5 mg maltose/mL whereas themean value ofstress was 107.8 mg/mL. In the first dentalhygiene student study (29), the mean value of relax was9 1 .4 mg/mL whereas the mean value of stress was 71.2mg/mL. In the second dental hygiene student study (31),the mean value of relax was 65.5 mg/mL whereas themean value of stress was 5 1 .3 mg/mL. In the present

study, the mean value ofrelax was 68.7 mg/mL whereasthe mean value of stress was 42.3 mg/mL. The meandifferences (42.7 mg/mL in the case study, 20.2 mg/mLin the first dental hygiene student study, 14.2 mg/mL in

the second dental hygiene student study, and 26.4 mg/mL in this study) are statistically significant (p < 0.01).Hence, it appears that with deep relaxation there is moresalivary a-amylase present in the mouth to digest com-plex carbohydrates, which then yields a higher amountof maltose. A summary of mean maltose in milligramsper milliliter for the four studies is given in Table 6.

With deep relaxation, as with meditation, the para-

sympathetic division of the ANS is activated (40). Stud-ies showed that parasympathetic stimulation yields arapid flow of watery saliva that is rich in a-amylase (20,33, 41). This is apparently what occurred during the relax

conditions.With respect to which factor is more important in oral

digestion of complex carbohydrates, an examination ofthe mean results from the present study shows that of allfour conditions (stress, relax, 20-s chewing, 60-s chew-ing), relax produced the largest amount of maltose (Fig1). Therefore, from the results ofthis study, the most im-portant factor in oral digestion ofcomplex carbohydratesappears to be deep relaxation. However, the best resultsoccur when deep relaxation is coupled with thoroughchewing(Fig 1).

It is understood that people generally do not eat underthe extreme conditions of stress and relaxation as usedin these studies. Nevertheless, it would appear that eating

in a relaxed atmosphere and chewing food thoroughlywould help in subsequent digestion and absorption.

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104 MORSE ET AL

TABLE 6Comparison ofmaltose produced from oat cereal (mg/mL)*

Conditions

Studies Stress/20 s Stress/60 s

iofStress/20 s

and stress/60 s Relax/20 s Relax/60 s

iofRelax/20 s

and relax/60 s

iofStress/20 sand relax/20 s

iofStress/60 sand relax/60 s

1(28) 64.5 151.1 107.8 81.0 220.0 150.5 72.8 185.6

2 (29) 53.3 89.1 71.2 72.2 1 10.6 91.4 62.8 99.9

3(31) 51.3 - 51.3 - 65.5 65.5 51.3 65.54 (present) 37.6 47.0 42.3 57.0 80.4 68.7 47.3 63.7

I Sl.7t 95.7� 68.2 70.1 119.1 94.0� 58.611 103.7

* The mean value for the distilled water homogenate for oat cereal = 6. 1.

t Difference between the mean ofstress/20 s and relax/20 s = I 8.4:tDifference between the mean ofstress/60 s and relax/60 s = 23.4

§Difference between the means ofstress/20 s and stress/60 s means and the means ofrelax/20 s and relax/60 s means = 25.8.

I Difference between the means ofstress/20 s and relax/20 s means and the means ofstress/60 s and relax/60 s means = 45. 1.

The great playwright Oscar Wilde was aware of thebenefits of relaxation during eating. In his 1895 play,“The Importance of Being Earnest (42),” there is a sec-tion in act 2 during which two friends are angry with eachother because of premarital problems. The following isan excerpt:

“Jack: How can you sit there, calmly eating muffins whenwe are in this horrible trouble. I can’t make it out. You seem

to me to be perfectly heartless.Algernon: Well, I can’t eat muffins in an agitated manner.

The butter would probably get on my cuffs. One should alwayseat muffins quite calmly. It is the only way to eat them.” 0

References

1. Morse DR. Schacterle GR, Furst ML, Bose K. Stress, relaxationand saliva: a pilot study involving endodontic patients. Oral SurgOral MedOral Pathol 198 l;52:308-13.

2. Morse DR. Schacterle GR, Furst ML, Esposito JV, Bose K. Stress,relaxation and saliva: a follow-up study involving clinicalendodontic patients. J Human Stress 198 1;7:19-26.

3. Morse DR, Schacterle GR, Furst ML, Brokenshire J, ButterworthM, Cacchio J. Examination-induced stress in meditators and non-meditators as measured by salivary protein changes. Stress198 1;2(3):20-4.

4. Morse DR. Schacterle GR, Furst ML, Mericle M, Mendel G,

Merrian S. Examination-induced stress as measured by changes in

total salivary protein and salivary glycoprotein. Stress l982;3:14-8.

5. Morse DR, Schacterle GR, Furst ML, et al. The effect of stressand meditation on salivary protein and bacteria: a review and pilot

study. J Human Stress 1982; 8:31-9.6. Morse DR, Schacterle GR, Esposito JV, et al. Stress, meditation

and saliva: a study of separate salivary gland secretions inendodontic patients. J Oral Med l983;38: I 50-60.

7. Morse DR, Schacterle GR, Martin JS, et al. Stress and relaxation:

evaluation by questionnaire, salivary changes and physiologicalresponses in a trained meditator. J Oral Med 1984; 39:142-7.

8. Morse DR, Schacterle GR, Furst ML, Esposito JV, Zaydenberg M.

Stress, relaxation and saliva: relationship to dental caries and itsprevention with a literature review. Ann Dent 1983;42:47-54.

9. Morse DR, Furst ML. Meditation: an in-depth study. J Am Soc

Psychosom Dent Med 1982;29(5):3-96.

10. Chauncey HH, Lisanti VF, Winer RA. Human parotid glandsecretions: flow rate and interrelationships of pH and inorganiccomponents. Proc Soc Exp Biol Med 1958;97:539-42.

I 1. Kraus FM, Mestecky J. Immunohistological localization of

amylase, lysozyme and immunoglobulins in the human parotid

gland. Arch Oral Biol 1971; 16:781-9.

12. Montgomery R, Dryer RL, Conway TW, et at. Biochemistry: a

case-oriented approach. 4th ed. St Louis, MO: CV Mosby, 1983.

13. Mandel ED, Wotman S. The salivary secretions in health and

disease. In: Melcher AH, Zarb GA, eds. Oral sciences review, Vol8. Scientific approaches to diagnosis in clinical dentistry.Copenhagen: Munksgaard, l976;25-46.

14. Morse DR. Hoffman H. Microbial diseases ofthe salivary glands:with special reference to mumps and acute and chronicsialadenitis. NY State Dent J 1970;36:203-l 3.

15. Morse DR, Schacterle GR, Zaydenberg M, et al. Salivary volume

and amylase activity. 1 : Relaxation versus relaxed chewing. J AmSoc Psychosom Dent Med 1983; 30:85-96.

16. Pollack RL, Hunt G, Rosen M. The pain-free tryptophan diet.New York: Warner Books, 1986.

17. Pritikin N, McGrady PM. The Pritikin program for diet and

exercise. New York: Grosset & Dunlop, 1979.

18. Burkitt D. Dietary fiber. In: Bland J, ed. Medical applications ofclinical nutrition. New Canaan, CT: Keats, 1983;269-86.

19. Greenberger NJ. Gastrointestinal disorders: a pathophysiologic

approach. 3rd ed. Chicago: Year Book Medical Co. 1986.

20. Bell GH, Emslie-Smith D, Paterson CR. Textbook of physiology.10th ed. Edinburgh: Churchill Livingstone, 1980.

21. Jacob SW, Francone CA, Lossow WJ. Structure and function inman. 5th ed. Philadelphia: WB Saunders, 1982.

22. Seckurt EE. Basic physiology for the health sciences. 2nd ed. NewYork: Little Brown, 1982.

23. Ballentine R. Diet and nutrition: a holistic approach. Honesdale,PA: Himalyan Press, 1978.

24. Baum Si. Introduction to organic and biological chemistry. 3rd ed.New York: MacMillan, 1983.

25. O’Dea K, Snow P. Nestal P. Rate ofstarch hydrolysis in vitro as apredictor of metabolic responses to a complex carbohydrate invivo. Am J Clin Nutr 1981;34:1991-3.

26. Jenkins DJA, Wolever TMS, Thorne MJ, et al. The relationship

by on April 10, 2009

ww

w.ajcn.org

Dow

nloaded from

ORAL DIGESTION OF COMPLEX CARBOHYDRATES 105

between glycemic response, digestibility, and factors influencing

the dietary habits ofdiabetics. Am J Clin Nutr 1984;40: 1175-91.27. Brand JC, Nicholson PL, Thoburn AW, Truswell AS. Food

processing and the glycemic index. Am J Clin Nutr 1985;42:

1192-6.

28. Morse DR. Furst ML, Schacterle OR, Zaydenberg M, POllack RL.The effects of stress and relaxation on oral digestion of complexcarbohydrates: a case study. J Oral Med l985;40: 185-90.

29. Morse DR. Schacterle OR, Furst ML, Zaydenberg M, Pollack RL.The effects of stress and relaxation on oral digestion of a complexcarbohydrate food. Int J Psychosom l985;32(3):20-7.

30. Morse DR. Martin JS, Furst ML, Dubin LL. A physiological andsubjective evaluation of meditation, hypnosis, and relaxation.Psychosom Med 1977; 39:304-24.

3 1 . Morse DR. Schacterle OR, Furst ML, Zaydenberg M, Pollack RL.The effects ofstress and relaxation on oral digestion ofa complexcarbohydrate cereal: evaluation by physiological and salivary

measures. J Oral Med l987;42:l6l-5.32. Morse DR. Martin JS, Furst ML, et al. A physiological and

subjective evaluation of neutral and emotionally-charged wordsfor meditation. J Am Soc Psychosom Dent Med l979;26:3l-8,56-62, 106-12.

33. Jenkins ON. The physiology and biochemistry of the mouth. 4thed. Oxford: Blackwell Scientific, 1978:284-359.

34. Morse DR, Furst ML. Women under stress. New York: VanNostrand Reinhold, 1982.

35. SteinerJE, Konijn AM, Ackermann R. Effect offood-related odorstimuli on human salivary response. Isr J Dent Sci 1984; 1:61-5.

36. Dawes C. Circadian rhythms in the flow rate and composition ofunstimulated and stimulated human submandibular saliva. JPhysiol l975;244:535-48.

37. Winer RI. Statistical principles in experimental design. New York:McGraw Hill, 1962.

38. Shaw JH. A summary ofthe relationship ofdietary carbohydratesto experimental dental caries. In: Tanzer JM, ed. Animal modelsin cariology. Washington, DC: Information Retrieval, 1981.

39. Ross SS. A clinical and radiological survey ofl92 cases of recurrentswellings of the salivary glands. Ann R Coll Surg Engl I 954; IS:374-401.

40. Benson H, Beary JF, Carol MP. The relaxation response.Psychiatry 1974; 37:37-46.

41. Brobeck JR. Best and Taylor’s physiological basis of medicalpractice. 8th ed. Baltimore: Williams & Wilkins, 1979.

42. Wilde 0. The importance of being Earnest. New York: WSHeinemanfl Publishing Co. 1970.

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