I-1OIIMONF.S
,AYD
Menstrual
Department
RI:HAVIOII,
Cycle:
4, 387-391
Effect
(19731
on Sweetness Preferences
of P.sycholog~~, University
of‘ Edinburgh,
in Women
izdinburgh,
Scotland
and ROSI;MAKY A. CKOW Department
of’ Mrrsing
occur sweet
Variations at different
Stodiq in how stages
University
of‘ Edinburgh,
Edinburgh,
Scotland
pleasant sugza~ solutions of the menstrual cycle.
are. as rated by women. F’ollowing a glucose meal this shift is slower at the time of
solutionsbecomelesspleasant,but ovulation.The signilkancc or thesechangeb is discussed.
Cabanac and Duclaux (1970a) have described shifts in the liking or preference for sweet solutions following the ingestion of a glucose meal in slightly starved people. The interpretation of this effect remains uncertain, (Wooley, Wooley, and Dunham, 1972; Wright, Nayar and Anand, 1972) although Cabanac and Duclaux (1970b) find that obesesubjects do not respond in the sameway as subjectsof normal weight and clearly feel that this shift in affective responseis an important signal in the short-term regulation of food intake (Cabanac, 1971). There is evidence for changes in some sensory thresholds during the course of the menstrual cycle (Le Magnen, 1950; Wynn. 1972). yet to our knowledge the studies of the postingestive effects of glucosewhich have been reported so far make no distinctions within the group of normal (nonobese) subjects. We have asked if affective measuresof taste change over the course of the menstrual cycle, and if such changescan be related 10 appetite or to weight gains. METIIOD We have used the same procedure as Cabanac and Duclaux, with an additional test administcrcd within 10 min of the glucose meal. The subjects were Y4 naive, nonobese women, ranging in age from 16-36 years, and included both students, staff members,and housewives.They were all unpaid 387 Copyright All rights
0 1973 by of reproduction
AcademicPress,Inc. in any
form
rescrved.
388
WRIGHT
AND
CROW
volunteers, and were not using any form of contraceptive pill at the time of testing. The test procedures were conducted in the morning, and subjects were asked not to eat any food after 9 Phi on the previous evening. The subjects were presented with five sugar and five salt solutions of different concentrations in a randomized sequence, and after holding the sample in the mouth for 1.5 see, expectorated, and immediately rated the solution on a scale from +2 (very pleasant) to -2 (very unpleasant). The solutions were rated before, 10 min after, and 1 hr after drinking 200 ml of a 25% glucose solution. The experimenter was in ignorance of the stage of the cycle when testing the subject, as it was not until the end of the testing session that the subjects were asked to complete a questionnaire on food habits, weight, and menstrual history. To allow for individual variations in the length of the menstrual cycle (25-32 days), this was divided into five equal phases, A-E, and each subject was assigned to the appropriate phase according to which ftith of her cycle she was tested within. The first day on which menstrual bleeding occurred was taken as Day 1, and this classification roughly ensured that the period of ovulation fell within phase C, the menses within phase A, and the premenstrual period in phase E.
RESULTS AND DISCUSSION Only the responses to the sucrose solutions will be described here. The results arc expressed as a cumulative measure across the five concentrations of sugar tested (40, 20, 10, 5, and 2.5% sucrose in distilled water). A subject who found all five solutions very pleasant will, therefore, have a cumulative rating of +lO, and one who found all the solutions very unpleasant a rating of -10. Figure 1 shows the initial responses to the sucrose solutions before ingestion of the glucose meal. Means and range within one standard deviation of the mean are plotted for the five phases of the menstrual cycle. It is apparent that the affective response to sugar does vary over the course of the menstrual cycle (F(4,88) = 6.20, p < .Ol), and that this inhomogeneity is due to the distribution of the ratings of subjects in phase D. Subjects tested in this phase find sugar solutions significantly less pleasant than do subjects tested at other phases of the cycle (Sheffe tests for comparision of means, p < .Ol). It is likely that this variation in affective response to sweetness will have some effect on feeding patterns during the cycle, but these will also be affected by factors which determine satiety. One hour after drinking the glucose solution, all subjects find the sugar solutions less pleasant than before the glucose meal, irrespcctivc of the stage of the menstrual cycle (Table 1). This shift in preference has appeared within 10 min of ingestion of the glucose in all subjects except those in phase C;
SWEETNESS PREFERENCE
389
IN WOMEN
Fig. 1. Mean ratings and range within one standard deviation of the mean for all subjects tested at different phases of the menstrual cycle. N refers to the number of Ss tested at that phase of the menstrual cycle. TABLE
1
Shifts in Ratings Following Ingestion of Glucose
After 10 min After 1 hr
Phase A
Phase B
Phase C
Phase D
Phase I<
-2.34** -2.96”*
-2.34** -1.84*
-0.33 -1.80"*
-1.81** -1.77*
-2.jl*" -2.32s
Wilcoxon Matched Pairs Test-** p < .005; * p < .Ol; fp < .025. Negative values indicate shifts toward unpleasantness.
these show an initial shift which is very smaIl and does not reach an acceptable level of significance(Wilcoxon matched pairs test, T = 106, NS). if these shifts are important in determining satiety, then our resultsindicate that the immediate feedback will be less effective at the time of ovulation. If Cabanac and Duclaux are correct, this should lead to small increasesin food intake at this time, and may explain why weight gains of the order of 1% have been rcportcd at midcycle in women, (Russell, 1972). It is of interest that we find no impairment of immediate feedback in the premenstrual period. Weight gains in this period have also been reported, but in this case
390
WRICHI‘ AND CROW
have been associated with the retention of water, although the evidence here is controversial (Greene and Dalton, 1953; Bruce and Russell, 1962). In countries with a high standard of living, the palatability of foodstuffs is an important factor determining intake, and we have shown that the liking for sweet-tasting solutions can vary during the course of the menstrual cycle. The efficiency of mechanisms which may produce satiety also varies with the stage of the cycle. Can these changes be related to underlying hormone levels? Female rats will consume significantly greater quantities of both glucose and very sweet saccharin solutions than do males, (Valenstein, Kakolewski, and Cox, 1967). This sex difference is due to the stimulating effects of ovarian hormones, since gonadectomy produces a marked lowering of saccharin preferences in females, but little change in males, (Zucker, 1969). There is no directly comparable evidence for humans, but Pangborn (1959) has found that women have lower thresholds for detecting sweet stimuli than have men. The depression in sugar preferences, which we find in phase D, corresponds to the broad midluteal peak in progesterone levels revealed by modern immunoassay techniques (Vande Wiele, 1970). The small shift in ratings immediately following the glucose meal which appears in phase C, is similarly likely to be correlated with high levels of oestrogen. It is quite possible that a number of our subjects were experiencing anovulatory cycles, and this would account for the wide variation of response within a single phase. However, despite the grouping of individual data and the assessment of stage of cycle solely in terms of onset of menstrual flow, the phase D depression is very clear and cannot be confused with the general malaise often encountered prcmenstrually in women (Greene and Dalton, 1953). Oestrogen has been found to inhibit food intake in the rat, and decreases bodyweight at the time of oestrus, and there is some suggestion that female baboons and rhesus monkeys consume less food during the follicular phase than during the lueteal phase of their menstrual cycle (Gilbert and Gillman, 1956). While this is contrary to our suggestion for midcycle humans, it is clear that there are numerous species differences in hormonal modulation of ingestive behavior (Wade, 1972). Moreover, other effects of the ovarian hormones, for example on activity (Stcnn and Klinge, 1972) may differ in magnitude between species and make comparison between man and other animals more difficult. To answer these questions in humans, it will be necessary to measure hormone leveb directly and examine variations in taste preferences and weight gains. Such observations will also establish more clearly the direction of the cause-and-effect relationships between food intake and weight, and the menstrual cycle.
SWI’FI‘NESS
PRI
IN WOMEN
391
ACKNOWLFBGME‘NTS We would like to thank the students in Edinburgh University, local housewives, and staff and students of the Department of Physiology in the All India Institute of Medical Sciences, New Delhi, for taking part in these experiments.
RBFERE:NCBS Bruce, J., and Russell, C. R. M. (1962). Premenstrual tension. Lancer 2, 267. Cabanac, \I., and Duclaux, R. (1970a). Specificity of internal signals in producing satiety for taste stimuli. A’ufure 227, 966. Cabanac, M., and Duclaux, R. (1970b). Obesity: Absence of satiety aversion to sucrose. Science 168, 496. Cabanac, M. (1971). Physiological role of pleasure. Science 173, 1103-1107. Grcenc, R., and Dalton, K. (1953). The premenstrual syndrome. &if. !Med. J. 1, 1007. (Gilbert, C., and Gihnan, J. (1956). The changing pattern of food intake and appetite during the menstrual cycle of the baboon @upio ursinus) with a consideration of some of the controlling endocrine factors. S. Afr. J. Med. Sci. 21, 75-88. Le Magnen, J. (1950). Nouvelles don&s sur le phenomene de I’cxaltolide. C. R. H. Acud. Sci. Ser. C 226, 627. Pangborn, R. M. (1959). Influence of hunger on sweetness preferences and taste thresholds. Amer. J. Clin. Xutr. 7, 280-287. Russell, G. 1~. M. (1972). Premenstrual tension and “psychogenic” amenorrhea: Psychophysical interactions. J. Psychosom. Res. 16, 279-287. Scheffe, II. (1959). The analysis of variance, Wiley, New York. Stcnn, P. C;., and Klinge, V. (1972). Relationship between the menstrual cycle and bodily activity in humans. Horm. Rehav. 3, 297-305. Valcnstein, 17. S., Kakolcwski, J. W., and Cox, V. C. (1967). Sex differences in taste preference for gh~cose and saccharin solutions. Science 156, 942-943. Vande Wielc, R. L., Bogumil, J., Dyrenfurth, I., Ferin, X, Jewclcwic/, R., Warren, M., Rizkallah, T., and hlikhail, G. (1970). Mechanisms regulating the menstrual cycle in women. Recent Progr. Hormone Res. 26, 63-103. Wade, C. S. (1972). Gonadal hormones and behavioural regulation of bodywcight. I’hysiol. Behav. 8, 523-534. Wynn, V. T., (1972). Mcasuremcnts of small variations in ‘absolute’ pitch. J. Physiol. 220, 627-637. Woolcy, 0. W., Wooley, S. C., and Dunham, R. B. (1972). Calories and sweet taste: Fffccts on sucrose preference in the obese and nonubcsc. PIzytiol. Behav. 9, 765-768. Wright, P., Nayar, U., and Anand, B. K. (1973). Ingestion of sweet tasting solutions and satiety changes in women. Indian J. Med. Res., in press. Zucker, 1. (1969). Hormonal dctcrminants of sex differences in saccharin preference, food intake and body weight. Physiol. Behav. 4, 595-602.