Advertisement

Eating Slowly Led to Decreases in Energy Intake within Meals in Healthy Women

      Abstract

      Although reducing eating rate is frequently advocated for control of food intake and thus body weight, empirical evidence is extremely limited and inconsistent. We sought to compare the impact of slow and quick eating rates on development of satiation in healthy women. In a randomized design, 30 healthy women (22.9±7.1 years; body mass index [calculated as kg/m2] 22.1±2.9) were studied on two test visits to compare slow and quick eating rates. Satiation was examined as the main outcome, using the objective measure of energy intake during ad libitum meals. At designated times, subjects also rated perceived hunger, satiety, desire to eat, thirst and meal palatability on visual analogue scales. Slow rates of ingestion led to significant decreases in energy intake (quick: 645.7±155.9 kcal; slow: 579.0±154.7 kcal; P<0.05) and significant increases in water consumption (quick: 289.9±155.1 g; slow: 409.6±205.8 g; P<0.05). Despite higher energy intake upon meal completion under the quick condition, satiety was significantly lower than the slow condition (P<0.05). Accordingly, the quick condition showed a lower Satiating Efficiency Index (quick: 0.1; slow: 0.2; P<0.05). After meal completion, pleasantness ratings tended to be higher under the slow condition (P=0.04; but not significant after Bonferroni adjustment). Ad libitum energy intake was lower when the meal was eaten slowly, and satiety was higher at meal completion. Although more study is needed, these data suggest that eating slowly may help to maximize satiation and reduce energy intake within meals.
      Behavioral and nutritional strategies that can help control appetite and energy intake should be developed and tested for their efficacy in body-weight management (
      • Melanson K.J.
      Food intake regulation in body weight management: A primer.
      ).
      Eating slowly is often advised for weight management because slower eating has been hypothesized to allow satiation to register before too much food is consumed (
      • Stuart R.B.
      • Davis B.
      Slim Chance in a Fat World.
      ). Peripheral biomarkers associated with meal termination include physicochemical measures related to stomach distension and responses of several hormones, including cholecystokinin, glucagon-like peptide 1, and ghrelin (
      • de Graaf C.
      • Blom W.A.
      • Smeets P.A.
      • Stafleu A.
      • Hendriks H.F.
      Biomarkers of satiation and satiety.
      ,
      • Degen L.
      • Matzinger D.
      • Drewe J.
      • Beglinger C.
      The effect of cholecystokinin in controlling appetite and food intake in humans.
      ,
      • Flint A.
      • Raben A.
      • Ersboll A.K.
      • Holst J.J.
      • Astrup A.
      The effect of physiological levels of glucagon-like peptide-1 on appetite, gastric emptying, energy and substrate metabolism in obesity.
      ,
      • Melton P.M.
      • Kissileff H.R.
      • Pi-Sunyer F.X.
      Cholecystokinin (CCK-8) affects gastric pressure and ratings of hunger and fullness in women.
      ,
      • Kissileff H.R.
      • Carretta J.C.
      • Geliebter A.
      • Pi-Sunyer F.X.
      Cholecystokinin and stomach distension combine to reduce food intake in humans.
      ). It has been proposed that slower rates of ingestion allow more time for these processes to take place, lengthen satiety's time course, and reduce total energy intake (
      • Melanson K.J.
      Food intake regulation in body weight management: A primer.
      ,
      • Stuart R.B.
      • Davis B.
      Slim Chance in a Fat World.
      ,
      • Spiegel T.A.
      • Wadden T.A.
      • Foster G.D.
      Objective measurement of eating rate during behavioral treatment of obesity.
      ).
      Although some findings have associated rapid food ingestion with greater energy consumption (
      • Kaplan D.L.
      Eating style of obese and non-obese males.
      ,
      • Chapman I.M.
      • Goble E.A.
      • Wittert G.A.
      • Horowitz M.
      Effects of small-intestinal fat and carbohydrate infusions on appetite and food intake in obese and nonobese men.
      ,
      • Gerace T.A.
      • George V.A.
      Predictors of weight increases over 7 years in fire fighters and paramedics.
      ), data on slow eating are very limited and do not fully substantiate its role in satiation (
      • Spiegel T.A.
      • Kaplan J.M.
      • Tomassini A.
      • Stellar E.
      Bite size, ingestion rate, and meal size in lean and obese women.
      ,
      • Yeomans M.R.
      • Gray R.W.
      • Mitchell C.J.
      • True S.
      Independent effects of palatability and within-meal pauses on intake and appetite ratings in human volunteers.
      ). Animal studies in which eating rate was reduced by increasing time between food items lend support to the hypothesis because increases in meal duration were directly proportional to reductions in food intake (
      • Clifton P.G.
      • Popplewell D.A.
      • Burton M.J.
      Feeding rate and meal patterns in the laboratory rat.
      ,
      • Lucas G.A.
      • Timberlake W.
      Interpellet delay and meal patterns in the rat.
      ,
      • Sclafani A.
      Eating rates in normal and hypothalamic hyperphagic rats.
      ).
      Epidemiological studies in Japanese individuals have shown positive association between self-reported eating rates and body mass index (BMI; calculated as kg/m2), suggesting relevance of this behavior in the prevention of obesity (
      • Takayama S.
      • Akamine Y.
      • Okabe T.
      • Koya Y.
      • Haraguchi M.
      • Miyata Y.
      • Sakai T.
      • Sakura H.
      • Sasaki T.
      Rate of eating and body weight in patients with type 2 diabetes or hyperlipidaemia.
      ,
      • Sasaki S.
      • Katagiri A.
      • Tsuji T.
      • Shimoda T.
      • Amano K.
      Self-reported rate of eating correlates with body mass index in 18-y-old Japanese women.
      ,
      • Otsuka R.
      • Tamakoshi K.
      • Yatsuya H.
      • Murata C.
      • Sekiya A.
      • Wada K.
      • Zhang H.M.
      • Matsushita K.
      • Sugiura K.
      • Takefuji S.
      • OuYang P.
      • Nagasawa N.
      • Kondo T.
      • Sasaki S.
      • Toyoshima H.
      Eating fast leads to obesity: Findings based on self-administered questionnaires among middle-aged Japanese men and women.
      ).
      Studies with children and obese adults have asserted the conventional dieting advice to take smaller bites in order to reduce energy intake (
      • Fisher J.O.
      • Rolls B.J.
      • Birch L.L.
      Children's bite size and intake of an entrée are greater with large portions than with age-appropriate or self-selected portions.
      ,
      • Walden H.M.
      • Martin C.K.
      • Ortego L.E.
      • Ryan D.H.
      • Williamson D.A.
      A new dental approach for reducing food intake.
      ). However, eating rate and satiation were not considered in these studies.
      In other studies, smaller bite sizes and pauses within ad libitum meals were related with longer meal duration but led to no difference in overall consumption, or were, in fact, associated with less satiation (
      • Spiegel T.A.
      • Kaplan J.M.
      • Tomassini A.
      • Stellar E.
      Bite size, ingestion rate, and meal size in lean and obese women.
      ,
      • Yeomans M.R.
      • Gray R.W.
      • Mitchell C.J.
      • True S.
      Independent effects of palatability and within-meal pauses on intake and appetite ratings in human volunteers.
      ). These data appear to contradict the idea that slower eating results in reductions in overall intake.
      The limited evidence and conflicting findings lend support to the need for additional research in this area. To our knowledge, no study to date has examined the combined recommendation of taking small bites, pausing between bites, and chewing thoroughly. Therefore, the present study investigated the impact of these combined techniques to alter eating rate on satiation and energy intake in healthy females.

      Methods

       Subjects

      It was determined a priori that 30 healthy females would be recruited from the University of Rhode Island and surrounding area by flyers and classroom announcements. Exclusion criteria included allergies to test foods, caffeine or alcohol dependency, type 1 or type 2 diabetes mellitus, adrenal or thyroid disease, any chronic illness that might cause weight change, clinically diagnosed eating disorders, medications that might alter appetite, and BMI >35. The study was approved by the Institutional Review Board of the University of Rhode Island. Informed written consent was obtained from the subjects but the purpose of the study was not disclosed to them. They were paid for their participation in this three-visit comparative protocol.

       Anthropometric Measurements

      During visit 1, body weight was measured once in minimal clothing on a digital scale accurate to 0.1 kg (BodPod, Life Measurements Inc, Concord, CA), height was measured once to the nearest centimeter on a wall-mounted stadiometer (Seca 240, SECA, Hamburg, Germany) accurate to 0.1 cm, and BMI was calculated. Waist circumference (cm) was measured once at the level of the umbilicus with a flexible Tyvek measuring tape (SECA). Body composition was assessed after a minimum 2-hour fast by air displacement plethysmography (BodPod) using standardized techniques (
      • Fields D.A.
      • Goran M.I.
      • McCrory M.A.
      Body composition assessment via air-displacement plethysmography in adults and children: A review.
      ).

       Questionnaires

      Participants completed a personal health history questionnaire. Eating rate was self-reported as “slow,” “medium,” or “fast.” Two validated instruments, the 51-item Three-Factor Eating and 10-item Herman-Polivy Questionnaires, were also administered to assess levels of dietary restraint, disinhibition, and hunger, as well as chronic weight-focused behavior, respectively (
      • Stunkard A.J.
      • Messick S.
      The three-factor eating questionnaire to measure dietary restraint, disinhibition, and hunger.
      ,
      • Herman C.P.
      • Polivy J.
      Anxiety, restraint, and eating behaviour.
      ).

       Study Protocol

      The next two laboratory visits were performed in randomized order to compare experimental conditions 3 to 7 days apart. These second and third visits were conducted during the mid-follicular phase of each subject's menstrual cycle, to control for possible menstrual cycle effects on appetite. Each test visit was conducted with one individual subject at a time.
      On the day prior to each test visit subjects were instructed to avoid strenuous physical activity, to refrain from alcohol and caffeine consumption, and to keep diet as close to normal as possible (no extremes of nutrients and calories) and similar on both days.
      On the morning of test days, subjects' breakfasts were specifically prescribed and matched between the slow and quick eating conditions. At lunch time, subjects reported to the laboratory, following a minimum 4-hour fast. After voiding their bladders, subjects were offered generous preweighed portions (600 g) of a mixed-macronutrient lunch (described here) and water. They were instructed to consume as much of it as they would like, to the point of comfortable satiation. Under the quick condition, subjects used a large spoon (soup spoon) and were told to consume the meal as fast as possible with no pauses between bites. However, they were instructed to not eat so fast that it was uncomfortable for them. During the slow condition they were instructed to take small bites, put down the spoon between each bite and chew each bite 20 to 30 times. A small spoon (teaspoon) was provided with these meals. During both conditions, investigators carefully monitored the subjects, prompting them to eat according to protocol. Exact clock time of meal initiation and completion was recorded. The amount of the meal and water consumed was calculated by weighed differences (to the nearest 0.01 g) on a digital scale (Adventurer; OHAUS Corp, Pine Brook, NJ).

       Assessment of Appetite and Meal Palatability

      For both conditions, hunger, satiety, desire to eat, and thirst were assessed with validated 10-cm visual analogue scales (
      • Flint A.
      • Raben A.
      • Blundell J.E.
      • Astrup A.
      Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. javascript:PopUpMenu2_Set(Menu10702749).
      ) before food intake, during the meal every 5 minutes up to 30 minutes, upon meal completion, and at 45 and 60 minutes. Meal palatability was also assessed with visual analogue scales at 1 minute into each meal and after meal completion. These scales were anchored by statements “not at all” and “extremely.”

       Test Meals

      On the morning of the 2 test days subjects were instructed to consume a standardized breakfast at home containing approximately 400 kcal consisting of 8 oz orange juice, 8 oz 1% or 2% milk, and 1 cup ready-to-eat cereal, except granola or Grape Nuts (Post Cereal, Kraft Foods Inc, Northfield, IL), with 8 oz decaffeinated tea or coffee as optional. Subjects consumed identical breakfasts on the morning before each test, and then fasted for a standard time (minimum 4 hours) during which physical activity was minimized. The test meal contained 870 kcal and consisted of ditalini pasta with diced tomatoes with Italian seasoning, celery, and minced garlic sautéed in olive oil, and Parmesan and Romano cheeses. Ditalini pasta was specially chosen because its small size allowed for slow or quick eating rates with small or large utensils. The percent energy coming from carbohydrate, fat, and protein was 48%, 39%, and 13%, respectively.

       Statistical Analysis

      Main study outcomes were ad libitum energy consumption and ratings of hunger, satiety, desire to eat, thirst, and palatability. All data were entered, double-checked, and managed in Microsoft Excel. Paired t tests were used to compare hypothesis-driven outcomes, including energy intake, total weight consumed, rate of energy consumption, and appetite ratings upon meal completion between quick and slow conditions. For most of these variables comparisons were also conducted between the number of subjects (eg, fast≥slow, slow>fast) using Wilcoxon tests. Additional paired t tests were adjusted for multiple comparisons [Bonferroni adjustment (
      • Hochberg Y.
      A sharper Bonferroni procedure for multiple tests of significance.
      )]. Hunger, satiety, desire to eat, and thirst ratings were compared across time points between conditions as repeated measures analysis of variance, time-by-condition interaction, with post hoc comparisons for each time point. Because of the nonlinear nature of the data, different equations (eg, quadratic, cubic) were explored. The equation maximizing the time-by-condition interaction is reported. Results are expressed as mean±standard deviation, and were considered significant at P<0.05, except for tests using Bonferroni adjustments. Data were analyzed using the software Statistica (version 6.1, 2003, StatSoft Inc, Tulsa, OK) and SPSS (version 15.0, 2006, SPSS Inc, Chicago, IL).

      Results

      Thirty healthy, nonsmoking, premenopausal females were recruited and all completed the study (Table 1). The majority were college students. Only one woman had a BMI > 30 (31.5) and only three had a BMI between 25 and 30. Because their results did not differ from the rest of the subjects, they were included in the analyses.
      Table 1Age, anthropometric, body composition, and questionnaire results of 30 females participating in the randomized comparative protocol of slow and quick eating
      CharacteristicValues
      mean±standard deviation (range)
      Age (y)22.9±7.1 (18-48)
      Height (m)1.6±0.1 (1.5-1.7)
      Weight (kg)58.1±8.9 (42.7-85.0)
      Body mass index
      Calculated as kg/m2.
      22.1±2.9 (16.0-31.5)
      Waist circumference (cm)74.7±7.0 (60.0-94.5)
      % Body fat26.5±5.2 (17.1-35.5)
      H-P score
      Scores from the Herman-Polivy Questionnaire (H-P). Anchor score: 0-35 (24).
      11.8±4.4 (0-23)
      Dietary restraint score
      Scores from the Three-Factor Eating Questionnaire. Anchor score: restraint: 0-21; disinhibition: 0-16; hunger: 0-14 (23).
      10.2±5.0 (3-20)
      Disinhibition score
      Scores from the Three-Factor Eating Questionnaire. Anchor score: restraint: 0-21; disinhibition: 0-16; hunger: 0-14 (23).
      6.4±2.6 (2-11)
      Hunger score
      Scores from the Three-Factor Eating Questionnaire. Anchor score: restraint: 0-21; disinhibition: 0-16; hunger: 0-14 (23).
      6.1±2.9 (1-12)
      Self-reported eating raten
      Number of subjects.
       Slow4
       Medium14
       Fast12
      a Calculated as kg/m2.
      b Scores from the Herman-Polivy Questionnaire (H-P). Anchor score: 0-35 (
      • Herman C.P.
      • Polivy J.
      Anxiety, restraint, and eating behaviour.
      ).
      c Scores from the Three-Factor Eating Questionnaire. Anchor score: restraint: 0-21; disinhibition: 0-16; hunger: 0-14 (
      • Stunkard A.J.
      • Messick S.
      The three-factor eating questionnaire to measure dietary restraint, disinhibition, and hunger.
      ).
      d Number of subjects.
      Table 2 shows that although meal duration was approximately 21 minutes longer under the slow condition, subjects consumed considerably less energy and weight of food than during the quick condition. No subject consumed the full amount offered under either condition. In contrast, weight of water and total weight consumed were substantially higher in the slow condition than the quick condition. Because of differences in energy and water intakes in both conditions, energy density was considerably lower under the slow condition. The combination of small bites, pauses between bites, and thorough chewing resulted in considerably decreased eating rate, expressed as kcal/min.
      Table 2Meal's duration, intakes, and eating rate in 30 female volunteers who completed the two experimental conditions (quick and slow)
      Eating ConditionNumber of Subjects
      QuickSlowQuick>slow
      Number of subjects in which meal duration and intakes were higher during the quick condition than the slow.
      Slow>quick
      Number of subjects in which meal duration and intakes were higher during the slow condition than the quick.
      mean±standard deviation
      Duration of the meal (min)8.6±3.129.2±8.9
      Statistical differences between conditions were determined by paired t tests.
      P<0.001.
      030
      Statistical differences between the number of subjects were determined by Wilcoxon tests.
      P<0.001.
      Weight of food consumed (g)445.3±107.5399.3±106.7
      Statistical differences between conditions were determined by paired t tests.
      P<0.01.
      255
      Statistical differences between the number of subjects were determined by Wilcoxon tests.
      P<0.01.
      Energy intake (kcal)645.7±155.9579.0±154.7
      Statistical differences between conditions were determined by paired t tests.
      P<0.01.
      255
      Statistical differences between the number of subjects were determined by Wilcoxon tests.
      P<0.01.
      Weight of water consumed (g)289.9±155.1409.6±205.8
      Statistical differences between conditions were determined by paired t tests.
      P<0.001.
      624
      Statistical differences between the number of subjects were determined by Wilcoxon tests.
      P<0.01.
      Total weight consumed (g)735.3±210.5808.9±245.2
      Statistical differences between conditions were determined by paired t tests.
      P<0.05.
      1020
      Energy density (kcal/total g)0.9±0.20.7±0.2
      Statistical differences between conditions were determined by paired t tests.
      P<0.001.
      264
      Statistical differences between the number of subjects were determined by Wilcoxon tests.
      P<0.001.
      Rate of energy consumption (kcal/min)84.8±36.221.0±7.2
      Statistical differences between conditions were determined by paired t tests.
      P<0.001.
      300
      Statistical differences between the number of subjects were determined by Wilcoxon tests.
      P<0.001.
      a Number of subjects in which meal duration and intakes were higher during the quick condition than the slow.
      b Number of subjects in which meal duration and intakes were higher during the slow condition than the quick.
      c Statistical differences between conditions were determined by paired t tests.
      d Statistical differences between the number of subjects were determined by Wilcoxon tests.
      low asterisk P<0.05.
      low asterisklow asterisk P<0.01.
      low asterisklow asterisklow asterisk P<0.001.
      Upon meal completion, despite higher energy intake, satiety ratings were significantly lower under the quick condition than the slow (P=0.02; Figure 1). Accordingly, the quick condition showed a significantly lower Satiating Efficiency Index (satiety ratings/energy intake [kcal]) (
      • Porrini M.
      • Crovetti R.
      • Rizo P.
      • Santangelo A.
      • Testolin G.
      Effects of physical and chemical characteristics of food on specific and general satiety.
      ) of 0.12±0.05 for the quick condition and 0.16±0.07 for the slow condition (P<0.01). Hunger ratings approached significance, being higher upon completion of the meal consumed at a quick pace (P=0.05).
      Figure thumbnail gr1
      Figure 1Visual analogue scale appetite ratings (mean±standard deviation) upon meal completion, from 30 women who consumed the identical meal under quick and slow eating conditions, in randomized order. *Satiety ratings were significantly different between conditions (paired t test; P=0.02).
      No significant differences were observed in palatability ratings between conditions at the meal's beginning (P>0.05; Figure 2). However, after meal completion, subjects rated the slow condition more pleasant than the quick (although P=0.04, this was not statistically significant after Bonferroni adjustment).
      Figure thumbnail gr2
      Figure 2Visual analogue scale palatability ratings (mean±standard deviation), from 30 women who consumed the identical meal under quick and slow eating conditions, in randomized order: (A) 1 minute into the meal; (B) upon meal completion. No significant differences were observed between conditions by paired t test after Bonferroni adjustment.
      The effect of eating rate on ratings of hunger, satiety, desire to eat, and thirst are represented in Figure 3. The time points of 9 and 29 minutes correspond to average meal termination for the quick and slow conditions, respectively. As shown in Figures 3A and 3B, for all time points 5 to 25 minutes, greater hunger and desire to eat were seen in the slow condition when the subjects were still eating (cubic equation; hunger: F=54.38; P<0.001; desire to eat: F=61.06; P<0.001). At 30, 45, and 60 minutes, no significant differences in hunger and desire-to-eat ratings were observed between conditions. While subjects were still eating, satiety ratings were lower at 5, 10, and 15 minutes during the slow condition (Figure 3C; cubic equation; F=22.32; P<0.001). However, from 20 to 60 minutes there were no significant differences in satiety ratings between conditions. Furthermore, the satiety ratings curve for the slow condition showed a gradual steady increase when compared with quick condition's curve, which increased rapidly during meal intake but leveled off after 9 minutes. Greater thirst ratings were observed for the slow condition than the quick (Figure 3D; quadratic equation; F=7.20; P<0.01), with no differences between conditions for any specific time point.
      Figure thumbnail gr3
      Figure 3Visual analogue scale appetite ratings (mean±standard deviation) overtime, from 30 women who consumed the identical meal under quick and slow eating conditions, in randomized order: (A) Hunger; (B) Desire to eat; (C) Satiety; (D) Thirst. Closed and open arrows represent meal completion for the quick (∼9 minutes) and slow (∼29 minutes) conditions, respectively. There were significant time-by-condition interactions with greater hunger (A) and desire to eat (B) in the slow than the quick condition, and greater satiety (C) in the quick than the slow condition, in repeated measures analyses of variance. *Means at a given time point were significantly different between conditions (repeated measures analysis of variance with post-hoc comparisons).

      Discussion

      This study's results showed that the combined techniques of taking small bites, pausing between bites, and chewing thoroughly can decrease the rate of food ingestion, and enhance effects on satiation, decreasing energy intake.
      Several explanations are possible for these observed relationships between slow eating and reduced food intake, all of which need additional investigation, and none of which are mutually exclusive. First, prolonged meal duration can allow more time for physiological satiety signals to develop before too much energy has been consumed. However, empirical evidence must be provided before this reason can be concluded. Secondly, this protocol used combined strategies to slow eating pace, including small bites, thorough chewing, and pausing between bites. Any of these factors, or synergy between them, might have helped the women to consume less and feel more satiated. For example, the process of chewing itself can stimulate physiological satiety signals (
      • Sakata T.
      • Yoshimatsu H.
      • Masaki T.
      • Tsuda K.
      Anti-obesity actions of mastication driven by histamine neurons in rats.
      ,
      • Lavin J.H.
      • French S.J.
      • Ruxton C.H.
      • Read N.W.
      An investigation of the role of oro-sensory stimulation in sugar satiety?.
      ). In addition, eating slowly allows time for consuming water along with the meal. Indeed, the women drank more water under the slow condition. Although it is possible that this may have increased stomach distension, and thus induced satiety (
      • de Graaf C.
      • Blom W.A.
      • Smeets P.A.
      • Stafleu A.
      • Hendriks H.F.
      Biomarkers of satiation and satiety.
      ,
      • Kissileff H.R.
      • Carretta J.C.
      • Geliebter A.
      • Pi-Sunyer F.X.
      Cholecystokinin and stomach distension combine to reduce food intake in humans.
      ), not all studies have shown that water consumed with a meal reduces energy intake (
      • Rolls B.J.
      • Bell E.A.
      • Thorwart M.L.
      Water incorporated into a food but not served with a food decreases energy intake in lean women.
      ). Thus, research is underway in our laboratory to clarify this. Finally, eating slowly allows more time for enjoying food, as supported by the pleasantness ratings in this study. It has been suggested that by slowing down and savoring the sight, smell, taste, flavors, texture, and mouthfeel of food, and sensing hunger being suppressed, more satisfaction can result from fewer calories (
      • Rolls E.T.
      Taste, olfactory, and food texture processing in the brain and the control of food intake.
      ,
      • Albers S.
      Eating Mindfully.
      ). However, Kaplan (
      • Kaplan D.L.
      Eating style of obese and non-obese males.
      ) reported that subjects gave higher taste ratings after meals eaten at faster rates as compared with slower rates.
      Results of the present study seem to support the previously suggested hypothesis that the physiological feedback from ingested food takes at least 20 minutes to develop, and this delay is independent of the amount of food eaten (
      • Stuart R.B.
      • Davis B.
      Slim Chance in a Fat World.
      ). Our data showed that the extension of meal duration by 21 minutes resulted in 67 fewer kilocalories ingested, and 83% of the subjects consumed a greater amount of energy when they were asked to eat fast. More work is needed to ascertain the physiology behind this.
      The present findings expand on a 1980 study (
      • Kaplan D.L.
      Eating style of obese and non-obese males.
      ) that showed a trend toward more food ingestion when subjects decreased pauses between sandwich bites, although it was not clear whether this meant shorter or fewer pauses. In addition, a study in 1991 (
      • Spiegel T.A.
      • Wadden T.A.
      • Foster G.D.
      Objective measurement of eating rate during behavioral treatment of obesity.
      ) associated slower eating rates with greater weight loss in obese women during a behavioral weight-control program. However, the authors indicated that the weight loss may be related to a combination of behaviors. Furthermore, two studies have observed positive associations between self-reported eating rates and energy intake as assessed by diet history questionnaires (
      • Sasaki S.
      • Katagiri A.
      • Tsuji T.
      • Shimoda T.
      • Amano K.
      Self-reported rate of eating correlates with body mass index in 18-y-old Japanese women.
      ,
      • Otsuka R.
      • Tamakoshi K.
      • Yatsuya H.
      • Murata C.
      • Sekiya A.
      • Wada K.
      • Zhang H.M.
      • Matsushita K.
      • Sugiura K.
      • Takefuji S.
      • OuYang P.
      • Nagasawa N.
      • Kondo T.
      • Sasaki S.
      • Toyoshima H.
      Eating fast leads to obesity: Findings based on self-administered questionnaires among middle-aged Japanese men and women.
      ). Moreover, smaller bite sizes were previously associated with reduced energy intake (
      • Fisher J.O.
      • Rolls B.J.
      • Birch L.L.
      Children's bite size and intake of an entrée are greater with large portions than with age-appropriate or self-selected portions.
      ,
      • Walden H.M.
      • Martin C.K.
      • Ortego L.E.
      • Ryan D.H.
      • Williamson D.A.
      A new dental approach for reducing food intake.
      ), as applies to present findings, yet eating rate was not a factor in these studies.
      In contrast to the previously mentioned studies, smaller bite sizes (
      • Spiegel T.A.
      • Kaplan J.M.
      • Tomassini A.
      • Stellar E.
      Bite size, ingestion rate, and meal size in lean and obese women.
      ) or pauses within ad libitum meals (
      • Yeomans M.R.
      • Gray R.W.
      • Mitchell C.J.
      • True S.
      Independent effects of palatability and within-meal pauses on intake and appetite ratings in human volunteers.
      ) led to no differences in general intake and decreased satiation, respectively. The authors suggested that timed pauses during meals are frustrating and that increased intake reflects the subjects' frustration (
      • Yeomans M.R.
      • Gray R.W.
      • Mitchell C.J.
      • True S.
      Independent effects of palatability and within-meal pauses on intake and appetite ratings in human volunteers.
      ). However, food intake was reduced in a preliminary study in which the subjects' eating rate was slowed by having them take mouthfuls upon the beep of a computer (
      • Martin C.
      • Anton S.
      • Walden H.
      • Arnett C.
      • Williamson D.
      Does slower eating rate reduce food intake? Results of an empirical test.
      ). The present study, which tested a more natural situation, showed a preference for the slow condition because declines in pleasantness ratings were expressed when subjects consumed the meal quickly, not slowly. Because most subjects reported themselves as medium or fast eaters, it is likely that our combined technique slowed their habitual eating pace. The capacity of individuals to alter their rates of ingestion and its long-range effectiveness and durability, should be examined further, as enquired in previous studies (
      • Spiegel T.A.
      • Wadden T.A.
      • Foster G.D.
      Objective measurement of eating rate during behavioral treatment of obesity.
      ,
      • Kaplan D.L.
      Eating style of obese and non-obese males.
      ,
      • Otsuka R.
      • Tamakoshi K.
      • Yatsuya H.
      • Murata C.
      • Sekiya A.
      • Wada K.
      • Zhang H.M.
      • Matsushita K.
      • Sugiura K.
      • Takefuji S.
      • OuYang P.
      • Nagasawa N.
      • Kondo T.
      • Sasaki S.
      • Toyoshima H.
      Eating fast leads to obesity: Findings based on self-administered questionnaires among middle-aged Japanese men and women.
      ).
      As mentioned previously, greater water consumption under the slow condition led to higher total meal weight, which might have induced more stomach distension, and thus satiation. However, this factor reflects the real-life situation, because eating slowly allows more time for water consumption. Moreover, reductions in energy density observed in the slow condition might have affected intake even when fat content was held constant, as shown in previous work (
      • Kral T.V.
      • Rolls B.J.
      Energy density and portion size: Their independent and combined effects on energy intake.
      ,
      • Rolls B.J.
      • Bell E.A.
      • Castellanos V.H.
      • Chow M.
      • Pelkman C.L.
      • Thorwart M.L.
      Energy density but not fat content of foods affected energy intake in lean and obese women.
      ,
      • Bell E.A.
      • Rolls B.J.
      Energy density of foods affects energy intake across multiple levels of fat content in lean and obese women.
      ). Nevertheless, drinking large quantities of water at a meal might not necessarily decrease energy intake (
      • Rolls B.J.
      • Bell E.A.
      • Thorwart M.L.
      Water incorporated into a food but not served with a food decreases energy intake in lean women.
      ).
      Deprivation-induced hunger and meal palatability have both been associated with increased eating rates, higher energy intake, and body size (
      • Spiegal T.A.
      • Shrager E.E.
      • Stellar E.
      Responses of lean and obese subjects to preloads, deprivation, and palatability.
      ,
      • Hill S.W.
      • McCutcheon N.B.
      Contributions of obesity, gender, hunger, food preference, and body size to bite size, bite speed, and rate of eating.
      ). In the present study, no differences in appetite ratings were seen in the beginning of the meal, hence the variations in hunger, satiety, desire to eat, and thirst ratings observed afterward resulted from the two different test conditions. Subjects were done eating 646 kcal in <9 minutes, but they ingested 579 kcal during 29 minutes.
      In contrast with these findings, greater hunger and lower fullness have been reported at the end of meals with more pauses (
      • Yeomans M.R.
      • Gray R.W.
      • Mitchell C.J.
      • True S.
      Independent effects of palatability and within-meal pauses on intake and appetite ratings in human volunteers.
      ). In another study (
      • Kaplan D.L.
      Eating style of obese and non-obese males.
      ), hunger and fullness ratings before and after the meal revealed no significant differences between two conditions that also differed according to pauses between bites. The present study, which, in addition, slowed eating by smaller bites and more thorough chewing, showed that subjects consumed less energy when they ate more slowly, and rated satiety higher at meal completion.
      Additional research is needed to determine how widely these findings can be generalized to other populations, such as males, as it has been suggested that eating rate and its effects differ by gender (
      • Otsuka R.
      • Tamakoshi K.
      • Yatsuya H.
      • Murata C.
      • Sekiya A.
      • Wada K.
      • Zhang H.M.
      • Matsushita K.
      • Sugiura K.
      • Takefuji S.
      • OuYang P.
      • Nagasawa N.
      • Kondo T.
      • Sasaki S.
      • Toyoshima H.
      Eating fast leads to obesity: Findings based on self-administered questionnaires among middle-aged Japanese men and women.
      ,
      • Martin C.
      • Anton S.
      • Walden H.
      • Arnett C.
      • Williamson D.
      Does slower eating rate reduce food intake? Results of an empirical test.
      ,
      • Hill S.W.
      • McCutcheon N.B.
      Contributions of obesity, gender, hunger, food preference, and body size to bite size, bite speed, and rate of eating.
      ), or obese individuals, because research regarding distinctive eating style has yielded conflicting results. Previous evidence has suggested that obese individuals eat faster than nonobese (
      • Spiegal T.A.
      • Shrager E.E.
      • Stellar E.
      Responses of lean and obese subjects to preloads, deprivation, and palatability.
      ,
      • Hill S.W.
      • McCutcheon N.B.
      Contributions of obesity, gender, hunger, food preference, and body size to bite size, bite speed, and rate of eating.
      ,
      • Gaul D.J.
      • Craighead W.E.
      • Mahoney M.J.
      Relation between eating rates and obesity.
      ,
      • Ortega R.M.
      • Redondo M.R.
      • Lopez-Sobaler A.M.
      • Quintas M.E.
      • Zamora M.J.
      • Andrés P.
      • Encinas-Sotillos A.
      Associations between obesity, breakfast-time, food habits and intake of energy and nutrients in a group of elderly Madrid residents.
      ) or has associated faster self-reported eating rates with greater BMI (
      • Gerace T.A.
      • George V.A.
      Predictors of weight increases over 7 years in fire fighters and paramedics.
      ,
      • Takayama S.
      • Akamine Y.
      • Okabe T.
      • Koya Y.
      • Haraguchi M.
      • Miyata Y.
      • Sakai T.
      • Sakura H.
      • Sasaki T.
      Rate of eating and body weight in patients with type 2 diabetes or hyperlipidaemia.
      ,
      • Sasaki S.
      • Katagiri A.
      • Tsuji T.
      • Shimoda T.
      • Amano K.
      Self-reported rate of eating correlates with body mass index in 18-y-old Japanese women.
      ,
      • Otsuka R.
      • Tamakoshi K.
      • Yatsuya H.
      • Murata C.
      • Sekiya A.
      • Wada K.
      • Zhang H.M.
      • Matsushita K.
      • Sugiura K.
      • Takefuji S.
      • OuYang P.
      • Nagasawa N.
      • Kondo T.
      • Sasaki S.
      • Toyoshima H.
      Eating fast leads to obesity: Findings based on self-administered questionnaires among middle-aged Japanese men and women.
      ), while other studies found no differences in eating rates between obese and nonobese subjects (
      • Kaplan D.L.
      Eating style of obese and non-obese males.
      ,
      • Chapman I.M.
      • Goble E.A.
      • Wittert G.A.
      • Horowitz M.
      Effects of small-intestinal fat and carbohydrate infusions on appetite and food intake in obese and nonobese men.
      ,
      • Spiegel T.A.
      • Kaplan J.M.
      • Tomassini A.
      • Stellar E.
      Bite size, ingestion rate, and meal size in lean and obese women.
      ).
      Limitations of this study include the small sample size and limited range of subject characteristics, so more work is needed in larger more diverse samples. Furthermore, it is unknown if the results seen would hold up under different circumstances than these controlled laboratory conditions, with different foods and beverages, or during longer periods of time, so additional study is required to discern this.

      Conclusions

      Slow eating decreased ad libitum energy intake in women, and resulted in more satiety after meal completion. Taking small bites, putting down the utensil, and chewing thoroughly may work together to slow eating pace and help to maximize satiation. Thus, these techniques may be recommended to reduce energy intake within meals and therefore manage body weight. Further research is required to examine eating rate's effects on food intake independent of beverage consumption, the effects of eating rate on inter-meal satiety, and to determine if these findings hold true for other populations, and for longer time frames.
      This study was presented in North American Association for the Study of Obesity's 2006 Annual Scientific Meeting, Boston, MA, October 21, 2006.
      The Luso-American Foundation supported the first author's work on this study. A grant funded by the University of Rhode Island Council for Research supported operating costs for this study.
      We thank all the volunteers for their participation and acknowledge the assistance of Tara Minaker during body composition data collection.
      None of the authors have any conflicts of interest.

      References

        • Melanson K.J.
        Food intake regulation in body weight management: A primer.
        Nutrition Today. 2004; 39: 203-215
        • Stuart R.B.
        • Davis B.
        Slim Chance in a Fat World.
        Research Press, Champaign, IL1972
        • de Graaf C.
        • Blom W.A.
        • Smeets P.A.
        • Stafleu A.
        • Hendriks H.F.
        Biomarkers of satiation and satiety.
        Am J Clin Nutr. 2004; 79: 946-961
        • Degen L.
        • Matzinger D.
        • Drewe J.
        • Beglinger C.
        The effect of cholecystokinin in controlling appetite and food intake in humans.
        Peptides. 2001; 22: 1265-1269
        • Flint A.
        • Raben A.
        • Ersboll A.K.
        • Holst J.J.
        • Astrup A.
        The effect of physiological levels of glucagon-like peptide-1 on appetite, gastric emptying, energy and substrate metabolism in obesity.
        Int J Obes Relat Metab Disord. 2001; 25: 781-792
        • Melton P.M.
        • Kissileff H.R.
        • Pi-Sunyer F.X.
        Cholecystokinin (CCK-8) affects gastric pressure and ratings of hunger and fullness in women.
        Am J Physiol. 1992; 263: R452-R456
        • Kissileff H.R.
        • Carretta J.C.
        • Geliebter A.
        • Pi-Sunyer F.X.
        Cholecystokinin and stomach distension combine to reduce food intake in humans.
        Am J Physiol Regul Integr Comp Physiol. 2003; 285: R992-R998
        • Spiegel T.A.
        • Wadden T.A.
        • Foster G.D.
        Objective measurement of eating rate during behavioral treatment of obesity.
        Behav Ther. 1991; 22: 61-67
        • Kaplan D.L.
        Eating style of obese and non-obese males.
        Psychosom Med. 1980; 42: 529-538
        • Chapman I.M.
        • Goble E.A.
        • Wittert G.A.
        • Horowitz M.
        Effects of small-intestinal fat and carbohydrate infusions on appetite and food intake in obese and nonobese men.
        Am J Clin Nutr. 1999; 69: 6-12
        • Gerace T.A.
        • George V.A.
        Predictors of weight increases over 7 years in fire fighters and paramedics.
        Prev Med. 1996; 25: 593-600
        • Spiegel T.A.
        • Kaplan J.M.
        • Tomassini A.
        • Stellar E.
        Bite size, ingestion rate, and meal size in lean and obese women.
        Appetite. 1993; 21: 131-145
        • Yeomans M.R.
        • Gray R.W.
        • Mitchell C.J.
        • True S.
        Independent effects of palatability and within-meal pauses on intake and appetite ratings in human volunteers.
        Appetite. 1997; 29: 61-76
        • Clifton P.G.
        • Popplewell D.A.
        • Burton M.J.
        Feeding rate and meal patterns in the laboratory rat.
        Physiol Behav. 1984; 32: 369-374
        • Lucas G.A.
        • Timberlake W.
        Interpellet delay and meal patterns in the rat.
        Physiol Behav. 1988; 43: 259-264
        • Sclafani A.
        Eating rates in normal and hypothalamic hyperphagic rats.
        Physiol Behav. 1994; 55: 489-494
        • Takayama S.
        • Akamine Y.
        • Okabe T.
        • Koya Y.
        • Haraguchi M.
        • Miyata Y.
        • Sakai T.
        • Sakura H.
        • Sasaki T.
        Rate of eating and body weight in patients with type 2 diabetes or hyperlipidaemia.
        J Int Med Res. 2002; 30: 442-444
        • Sasaki S.
        • Katagiri A.
        • Tsuji T.
        • Shimoda T.
        • Amano K.
        Self-reported rate of eating correlates with body mass index in 18-y-old Japanese women.
        Int J Obes Relat Metab Disord. 2003; 27: 1405-1410
        • Otsuka R.
        • Tamakoshi K.
        • Yatsuya H.
        • Murata C.
        • Sekiya A.
        • Wada K.
        • Zhang H.M.
        • Matsushita K.
        • Sugiura K.
        • Takefuji S.
        • OuYang P.
        • Nagasawa N.
        • Kondo T.
        • Sasaki S.
        • Toyoshima H.
        Eating fast leads to obesity: Findings based on self-administered questionnaires among middle-aged Japanese men and women.
        J Epidemiol. 2006; 16: 117-124
        • Fisher J.O.
        • Rolls B.J.
        • Birch L.L.
        Children's bite size and intake of an entrée are greater with large portions than with age-appropriate or self-selected portions.
        Am J Clin Nutr. 2003; 77: 1164-1170
        • Walden H.M.
        • Martin C.K.
        • Ortego L.E.
        • Ryan D.H.
        • Williamson D.A.
        A new dental approach for reducing food intake.
        Obes Res. 2004; 12: 1773-1780
        • Fields D.A.
        • Goran M.I.
        • McCrory M.A.
        Body composition assessment via air-displacement plethysmography in adults and children: A review.
        Am J Clin Nutr. 2002; 75: 453
        • Stunkard A.J.
        • Messick S.
        The three-factor eating questionnaire to measure dietary restraint, disinhibition, and hunger.
        J Psychosom Res. 1985; 29: 71-83
        • Herman C.P.
        • Polivy J.
        Anxiety, restraint, and eating behaviour.
        J Abnorm Psychol. 1975; 84: 666-672
        • Flint A.
        • Raben A.
        • Blundell J.E.
        • Astrup A.
        Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. javascript:PopUpMenu2_Set(Menu10702749).
        Int J Obes Relat Metab Disord. 2000; 24: 38-48
        • Hochberg Y.
        A sharper Bonferroni procedure for multiple tests of significance.
        Biometrika. 1988; 75: 800-803
        • Porrini M.
        • Crovetti R.
        • Rizo P.
        • Santangelo A.
        • Testolin G.
        Effects of physical and chemical characteristics of food on specific and general satiety.
        Physiol Behav. 1995; 57: 461-468
        • Sakata T.
        • Yoshimatsu H.
        • Masaki T.
        • Tsuda K.
        Anti-obesity actions of mastication driven by histamine neurons in rats.
        Exp Biol Med. 2003; 228: 1106-1110
        • Lavin J.H.
        • French S.J.
        • Ruxton C.H.
        • Read N.W.
        An investigation of the role of oro-sensory stimulation in sugar satiety?.
        Int J Obes Relat Metab Disord. 2002; 26: 384-388
        • Rolls B.J.
        • Bell E.A.
        • Thorwart M.L.
        Water incorporated into a food but not served with a food decreases energy intake in lean women.
        Am J Clin Nutr. 1999; 70: 448-455
        • Rolls E.T.
        Taste, olfactory, and food texture processing in the brain and the control of food intake.
        Physiol Behav. 2005; 85: 45-56
        • Albers S.
        Eating Mindfully.
        New Harbinger Publications, Inc, Oakland, CA2003
        • Martin C.
        • Anton S.
        • Walden H.
        • Arnett C.
        • Williamson D.
        Does slower eating rate reduce food intake?.
        Obes Res. 2004; 12 (22-OR): A6
        • Kral T.V.
        • Rolls B.J.
        Energy density and portion size: Their independent and combined effects on energy intake.
        Physiol Behav. 2004; 82: 131-138
        • Rolls B.J.
        • Bell E.A.
        • Castellanos V.H.
        • Chow M.
        • Pelkman C.L.
        • Thorwart M.L.
        Energy density but not fat content of foods affected energy intake in lean and obese women.
        Am J Clin Nutr. 1999; 69: 863-871
        • Bell E.A.
        • Rolls B.J.
        Energy density of foods affects energy intake across multiple levels of fat content in lean and obese women.
        Am J Clin Nutr. 2001; 73: 1010-1018
        • Spiegal T.A.
        • Shrager E.E.
        • Stellar E.
        Responses of lean and obese subjects to preloads, deprivation, and palatability.
        Appetite. 1989; 13: 45-69
        • Hill S.W.
        • McCutcheon N.B.
        Contributions of obesity, gender, hunger, food preference, and body size to bite size, bite speed, and rate of eating.
        Appetite. 1984; 5: 73-83
        • Gaul D.J.
        • Craighead W.E.
        • Mahoney M.J.
        Relation between eating rates and obesity.
        J Consult Clin Psychol. 1975; 43: 123-125
        • Ortega R.M.
        • Redondo M.R.
        • Lopez-Sobaler A.M.
        • Quintas M.E.
        • Zamora M.J.
        • Andrés P.
        • Encinas-Sotillos A.
        Associations between obesity, breakfast-time, food habits and intake of energy and nutrients in a group of elderly Madrid residents.
        J Am Coll Nutr. 1996; 15: 65-72

      Biography

      A. M. Andrade is a doctoral student, G. W. Greene is a professor, and K. J. Melanson is an associate professor, Department of Nutrition and Food Sciences, University of Rhode Island, Kingston, RI.