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The effects of water temperature on gastric motility and energy intake in healthy young men

The effects of water temperature on gastric motility and energy intake in healthy young men Purpose Although immediate pre-meal water ingestion has been shown to reduce energy intake in healthy young men, no studies are available regarding potential mechanisms underlying the effect of energy intake in response to different tempera - tures of pre-meal water ingestion. This study examined the effects of consuming different temperatures of water on gastric motility and energy intake in healthy young men. Methods Eleven young men were completed three, 1-day trials in a random order. Subjects visited the laboratory after a 10-h overnight fast and consumed 500 mL of water at 2 °C, 37 °C, or 60 °C in 5 min. Then, subjects sat on a chair over 1 h to measure the cross-sectional gastric antral area and gastric contractions using the ultrasound imaging systems. Thereafter, sub- jects consumed a test meal until they felt completely full. Energy intake was calculated from the amount of food consumed. Results Energy intake in the 2 °C (6.7 ± 1.8 MJ) trial was 19% and 26% lower than the 37 °C (7.9 ± 2.3 MJ, p = 0.039) and 60 °C (8.5 ± 3.2 MJ, p = 0.025) trials, respectively. The frequency of the gastric contractions after 1-h consuming water was lowered in the 2 °C trial than the 60 °C trial (trial-time interaction, p = 0.020). The frequency of gastric contractions was positively related to energy intake (r = 0.365, p = 0.037). Conclusions These findings demonstrate that consuming water at 2 °C reduces energy intake and this reduction may be related to the modulation of the gastric motility. Keywords Water ingestion · Water temperature · Gastric motility · Ultrasound imaging · Appetite · Energy intake Introduction and subsequent weight gain in healthy individuals may be important for the long-term weight management. Among Public health research is addressing on the long-term man- available methods for preventing a positive energy balance, agement of weight loss by creating a negative energy bal- water consumption is a simple method and has potentially a ance through increased physical activity and/or decreased key role to play in reducing energy intake [4]. food intake in overweight and obese individuals [1]. How- To date, three laboratory-based studies have examined ever, estimates in many countries suggest that most individu- the effects of pre-meal water ingestion on subsequent energy als do not complete a sufficient amount of physical activ - intake in various individuals [5–7] with disparate effects. ity to meet the guidelines set out by expert panels [2, 3]. These studies vary in protocols including the amount of Thus, while promoting physical activity for all individuals water ingested (i.e., 375–568 mL), and the time interval is important, strategies to prevent a positive energy balance between ingestion of water and the subsequent meal (i.e., immediately before to 30 min before a meal). In addition, only one study has clearly reported the temperature of water * Masashi Miyashita [email protected] used in the study (5–7 °C) [7]. Although the reasons for these discrepant findings among studies are not clearly Graduate School of Sport Sciences, Waseda University, known, Corney et  al. [6] have suggested that the rate of 2-579-15 Mikajima, Tokorozawa, Saitama 359-1192, Japan gastric emptying of liquid meals was slower in older adults Japan Society for the Promotion of Science, 5-3-1 than in younger adults, indicating that gastric distension Koujimachi, Chiyoda-ku, Tokyo 102-0083, Japan may be a factor for influencing subsequent energy intake. Faculty of Sport Sciences, Waseda University, 2-579-15 In addition, the rate of gastric emptying or the magnitude Mikajima, Tokorozawa, Saitama 359-1192, Japan Vol.:(0123456789) 1 3 104 European Journal of Nutrition (2020) 59:103–109 of gastric motility (i.e., measured via cross-sectional antral K.K., Japan). The 500 mL of water was chosen, because area reflecting gastric distention, rate of gastric emptying, this volume has been shown to reduce subsequent energy and frequency of gastric contractions) are known to be influ- intake in a previous study [7]. Subjects then sat on a chair enced by the temperatures of consumed “energy-containing in a fixed position as above in the laboratory until 1005. drinks” [8, 9]. Collectively, to our knowledge, none of pre- Whilst subjects rested until 1005, 2D ultrasound scan was vious studies [5–7] have examined the effects of pre-meal performed to assess the change in the cross-sectional gastric water ingestion on gastric motility and subsequent energy antral area and gastric contractions before and after con- intake in healthy young adults. Furthermore, there is as yet suming a 500 mL of water at 2 °C, 37 °C, or 60 °C. Then, no evidence regarding how different temperatures of “water” subjects were asked to consume the test meal from 1005 and affect energy intake and subjective feelings of appetite in were instructed to eat as much as they satisfied until 1105. healthy young adults. The interval of 60 min between water ingestion and subse- Therefore, the purpose of this study was to investigate the quent meal was chosen, since we thought that this interval effects of different temperatures of water on gastric motility may be long enough to assess gastric motility using ultra- and energy intake in healthy young men. sound imaging as this was the case in the previous study [10]. Subjects also completed a 100-mm visual analogue scale questionnaire [11], assessing the subjective perceptions Methods of appetite, at 0900 (i.e., pre), immediately after consuming water (i.e., post), and 30, 60, 90, and 120 min after consum- Subjects ing water. After approval from the Ethics Committee on Human Subjective appetite perceptions and energy intake Research of Waseda University (approval number: 2017- 260), 11 healthy, lean men gave written informed consent The acceptability of the test meal was ensured by a prior to participate in this study. The physical characteristics of written survey and selected instant noodles as a test meal. the subjects were as follows: age 23.4 ± 1.4 years, height Subjects were provided with a bowl of instant noodles (i.e., 1.71 ± 0.04 m, body mass 64.0 ± 9.8 kg, body mass index 9.7% energy as protein, 20.5% energy as fat, and 69.8% 21.8 ± 2.6  kg/m , and waist circumference 73.1 ± 5.4 cm energy as carbohydrate) at 1005. Subjects were offered with [mean ± standard deviations (SD)]. All subjects were non- repeated small bowls of noodles throughout the meal time. smokers and were not taking any medicine, and their body Warm food was continuously available until the subjects masses had been stable for at least 3 months before the study. finished eating the test meal. Subjects were instructed to eat until they felt “comfortably full and satisfied” and that Experimental protocol additional food was available if desired [12]. This ensures that subjects were not able to know how much they had con- The subjects underwent three, 1-day laboratory-based trials sumed while eating. Drinking water was restricted, while in random order: (1) water at 2 °C, (2) water at 37 °C, and the subject was taking the test meal. The upper limit of meal (3) water at 60 °C. The interval between trials was at least intake time was 1 h, and mean time to consume the test 6 days. All subjects were asked to maintain their normal meal in the 2 °C, 37 °C, and 60 °C trials was 18.2 ± 6.5 min, eating habits among the trials and to refrain from vigorous 21.8 ± 9.4 min, and 24.1 ± 11.9 min, respectively. The total exercise and alcohol intake for 24 h before each trial. In the amount of food intake (g) was ascertained by examining the 24 h before the first trial, subjects measured and recorded weighted difference in the test meal remaining compared to all dietary intakes, and then they replicated these dietary that initially presented. The total energy intake from the test intakes in the 24 h preceding the second and third trials. meal was calculated using the manufacture-reported values. Food diaries were analyzed by software to determine energy Subjects completed 100-mm visual analogue scales [11, 13] intake and macronutrient content (Excel Eiyoukun Ver 5.0, before (i.e., pre), immediately after (i.e., post), and at 30, Kenpakusha, Japan). On each trial day, subjects reported to 60, 90, and 120 min after consuming water, to assess the the laboratory at 0850 after a 10-h overnight fast-subjects perceptions of appetite (i.e., hunger, fullness, and desire to were allowed to drink only one glass of water no later than eat sweet, sour, fatty, and salty foods). In addition, subjects 2 h prior to each trial. The subjects were asked to sit on a completed 100-mm visual analogue scales before (i.e., pre), comfortable chair in a fixed position (i.e., the angle between immediately after (i.e., post), and at 30, 60, 90, and 120 min the upper part and lower part of the body was approximately after consuming water, to assess the perceptions of feelings 120°) and to consume a 500 mL of water at 2 °C, 37 °C or of stomach condition (i.e., “Does your stomach feel uncom- 60 °C over a 5-min period at 0900. The water temperature fortable?”, “Do you feel your stomach is expanding?”, and was measured by an electric thermometer (testo 106, Testo “Do you want to eat now?”). Verbal anchors “not at all” 1 3 European Journal of Nutrition (2020) 59:103–109 105 and “extremely” were placed at 0 and 100 mm on the visual Results analogue scales, respectively. Dietary data Assessment of gastric motility Mean self-reported energy intake for the day prior to each Several previous studies suggest that the antrum is the most trial was 7.2 ± 1.5 MJ. Energy intake equated to 30 ± 6% suitable area in which to evaluate the stomach capacity (for (59.9 ± 20.7  g/day) from fat, 54 ± 7% (218.3 ± 30.8  g/day) a review of this, see Ref. [14]). Antral area measurements from carbohydrate, and 16 ± 3% (70.4 ± 20.6 g/day) from were performed using a 2D ultrasound machine (LOGIQ-e, protein. GE Healthcare, USA) and a 5.0 MHz sector transducer. All metals were removed from the surrounding area to avoid the Pre‑trial possibility of interference during acquisition. To optimise precision, the transducer was positioned vertically to obtain There were no significant differences in body mass a parasagittal image of the antrum, with the superior mesen- among the 2 °C, 37 °C, and 60 °C trials (63.8 ± 9.9 kg vs. teric vein and the abdominal aorta in a longitudinal section, 64.3 ± 9.7  kg vs. 63.9 ± 9.9  kg, respectively; p = 0.075) at as described previously [14]. After obtaining these signals pre-trial (i.e., 0900). At pre-trial, subjective appetite per- for measuring antral area for 3 min [15] before (i.e., pre), ceptions (i.e., hunger, fullness, and desire to eat sweet, immediately after (i.e., post), and at 10, 20, 30, 40, 50, and sour, fatty, and salty foods) and perception of the stomach 60 min after consuming water. The gastric antral area (cm ) did not differ across the trials. Cross-sectional antral areas 2 2 2 was determined using an image-editing software (ImageJ (3.1 ± 1.3  cm vs. 3.6 ± 1.3  cm vs. 3.1 ± 1.0  cm for the 1.47, National Institute of Mental Health, USA). The gastric 2 °C, 37 °C, and 60 °C trials, respectively; p = 0.277) and contractions of the antral area were defined as the frequency frequency of gastric contractions (4.5 ± 2.5 times/3 min vs. of contractions per 3 min, and were measured before (i.e., 4.5 ± 2.7 times/3 min vs. 4.5 ± 3.0 times/3 min for the 2 °C, pre), immediately after (i.e., post), and at 10, 20, 30, 40, 50, 37 °C and 60 °C trials, respectively; p = 0.996) were also not and 60 min after consuming water [16]. different at pre-trial (i.e., 0900) among the trials. Statistical analysis Energy intake Data were analyzed using the Predictive Analytics Software Energy intake differed among the trials (6.7 ± 1.8 MJ vs. (PASW) version 23.0 for Windows (IBM SPSS Statistics 7.9 ± 2.3 MJ vs. 8.5 ± 3.2 MJ for the 2 °C, 37 °C and 60 °C 23.0, SPSS Japan Inc., Japan). The Shapiro–Wilk test was trials, respectively; p = 0.009) (Fig. 1). Post hoc tests revealed used to check for normality of distribution—all parameters that energy intake in the 2 °C trial was 19% and 26% lower were found to be normally distributed. Repeated-measures one-factor analysis of variance (ANOVA) was used to assess differences among the three trials in energy intake and the length of meal. Repeated-measures, two-factor ANOVA was used to examine differences over time among the three trials in cross-sectional antral area, frequency of gastric contractions, subjective appetite perceptions (i.e., hunger, fullness and desire to eat sweet, sour, fatty, and salty foods), and subjective perception of the stomach. Where signifi- cant trial–time interactions and trial effects were found, the values were subsequently analyzed using a Bonferroni multiple-comparison test. The correlation coefficients were determined using Pearson’s product-moment tests between the frequency of gastric contractions and energy intake. The 95% confidence intervals (95% CI) for the mean absolute pairwise differences among the three trials were calculated using the t-distribution and degrees of freedom (n − 1). Data Fig. 1 Energy intake at ad libitum test meal: 60 min after consuming water (500 mL) at 2 °C, 37 °C and 60 °C. Data are mean ± SD. Mean were expressed as mean ± standard deviations (SD). Statisti- was compared using one-factor ANOVA for the main effect of trial cal significance was set at p < 0.05. followed by a Bonferroni multiple-comparison test. *Significantly different between the 2  °C and 60  °C trials (p < 0.05). Significantly different between the 2 °C and 37 °C trials (p < 0.05) 1 3 106 European Journal of Nutrition (2020) 59:103–109 than the 37 °C (p = 0.039, 95% CI 15.051–585.749) and compared with the 60 °C trial immediately after consum- 2 2 60 °C (p = 0.025, 95% CI 51.498–793.684) trials, respec- ing water (i.e., post) (10.0 ± 5.0 cm vs. 9.3 ± 1.2  cm vs. tively. The time taken to feel completely full in the 2 °C, 6.8 ± 2.1  cm for the 2 °C, 37 °C and 60 °C trials, respec- 37 °C, and 60 °C trials was 18.2 ± 6.5 min, 21.8 ± 9.4 min, tively; 2 °C vs. 60 °C: p = 0.030, 95% CI 0.379–7.802, 37 °C and 24.1 ± 11.9 min, respectively. The time taken to feel vs. 60 °C: p = 0.0019, 95% CI 0.407–4.556) (Fig. 3). The fre- completely full was 5.9 min shorter in the 2 °C trial than the quency of gastric contractions differed significantly among 60 °C trial (p = 0.046, 95% CI 0.086–11.768). the trials (main effect of trial, p < 0.001, and tr ial–time interaction: p < 0.001). Post hoc analyses indicated differ - Subjective appetite perceptions ences in the frequency of the gastric contractions between trials immediately after (i.e., post) and at 10, 20, 30, 40, For subjective appetite perception of hunger, there was a 50, and 60 min after consuming water—the frequency of significant main effect of time (p < 0.001) and tr ial–time the gastric contractions was lower in the 2 °C trial than the interaction among the three trials (p = 0.027) (Fig. 2). Post 60 °C trial (post: p < 0.001, 95% CI 2.818–5.932, 10 min: hoc analysis revealed that subjective appetite perception of p = 0.001, 95% CI 1.202–3.548, 20  min: p = 0.004, 95% hunger tended to be lower during the 2 °C trial than the CI 1.158–4.592, 30 min: p = 0.002, 95% CI 1.333–4.167, 60 °C trial at 30 and 60 min after consuming water (30 min: 40  min: p = 0.016, 95% CI 0.512–4.238, 50  min: p = 0.074, 95% CI −1.557 to 38.557, 60 min: p = 0.086, and p = 0.026, 95% CI 0.341–4.909, 60 min: p = 0.002, 95% CI 95% CI −2.318 to 40.984). In each trial, subjective appetite 1.608–5.142) (Fig. 4). At immediately after (i.e., post), and perception of hunger peaked 60 min after consuming water at 30, 50, and 60 min after consuming water, the frequency (main effect of time: p < 0.001). There were no significant of the gastric contractions was lower in the 37 °C trial than differences in the other subjective appetite perceptions (i.e., the 60 °C trial (post: p = 0.011, 95% CI 0.605–3.895, 30 min: hunger and desire to eat sweet, sour, fatty, and salty foods) p = 0.034, 95% CI 0.104–2.371, 50 min: p = 0.024, 95% CI or perception of the stomach (i.e., “Dose your stomach feel 0.369–4.656, 60 min: p = 0.005, 95% CI 1.192–5.408). At uncomfortable?”, “Do you feel your stomach is expanding?”, immediately after (i.e., post) and at 10 min after consuming and “Do you want to eat now?”). water, the frequency of the gastric contractions was lower in the 2 °C trial than the 37 °C trial (post: p = 0.003, 95% Gastric antral area and gastric contractions CI 0.880–3.370, 10 min: p < 0.001, 95% CI 1.453–2.872). There were trial–time interactions (p < 0.001). Cross-sec- tional antral areas increased in the 2 °C and 37 °C trials Fig. 3 Cross-sectional gastric antral area before and after consuming water (500 mL) at 2 °C, 37 °C and 60 °C. Data are mean ± SD. Black Fig. 2 Subjective appetite perceptions of hunger before and after rectangle indicates consuming water in 5  min. Data were analyzed consuming water (500  mL) at 2  °C, 37  °C, and 60  °C. Data are mean ± SD. Black rectangle indicates consuming water in 5  min. using two-factor ANOVA followed by a Bonferroni multiple-compar- Data were analyzed using two-factor ANOVA followed by a Bonfer- ison test. There was a significant main effect of time (p < 0.001) and roni multiple-comparison test. There was a significant main effect of trial–time interaction (p = 0.020). *Significantly different between the time (p < 0.001) and trial–time interaction (p = 0.027). (*)Different 2  °C and 60  °C trials (p < 0.05). Significantly different between the between the 2 °C and 60 °C trials (p < 0.10) 37 °C and 60 °C trials (p < 0.05) 1 3 European Journal of Nutrition (2020) 59:103–109 107 water ingestion may provide additional benefits to weight management in healthy individuals as this method can be applied inexpensively and easily on a daily basis. Three laboratory-based studies [5–7] have demonstrated reductions in energy intake after acute water ingestion which were seen in the present study. One study found that pre- meal (i.e., 30 min) water ingestion was effective in reduc- ing subsequent energy intake in overweight and obese older adults [7]. Another study found similar results in response to pre-meal (i.e., 30 min) water ingestion in healthy older adults, but not in healthy young adults [5]. One recent study found that water ingestion immediately before a meal was effective in reducing subsequent energy intake in healthy young adults [6]. Although the precise reasons for the dis- crepant findings observed in the study by Van Walleghen Fig. 4 Frequency of gastric contractions before and after consuming water (500 mL) at 2 °C, 37 °C, and 60 °C. Data are mean ± SD. Black et al. [5] are not known, the timing of ad libitum energy rectangle indicates consuming water in 5  min. Data were analyzed intake in response to water ingestion may affect subsequent using two-factor ANOVA followed by a Bonferroni multiple-com- energy intake [17, 18]. Indeed, a previous study has reported parison test. There was a significant main effect of trial (p < 0.001), that inter-meal interval between drink ingestion and ad libi- main effect of time (p < 0.001), and trial–time interaction (p = 0.020). *Significantly different between the 2 °C and 60 °C trials (p < 0.05). tum meal was associated with gastric antral area and energy Significantly different between the 2  °C and 37  °C trials (p < 0.05). intake, although nutrient drink was used in this study [17, Significantly different between the 37 °C and 60 °C trials (p < 0.05) 18]. Another reason for the discrepant findings is that dif - ferences in the rate of gastric emptying between young and Relationships between energy intake and frequency older individuals might affect subjective energy intake [6 , 19]. Alternatively, given the well-documented slower rate of the gastric contractions of gastric emptying at cold water (i.e., at 5 °C) compared with warm water (i.e., at 37 °C) [20], the temperature of There was a positive relationship between energy intake from the test meal and the frequency of the gastric con- ingested water may be the proposed reason for the discrepant findings among the studies. Indeed, among three available tractions measured immediately after consuming water. The reduction in frequency of the gastric contractions measured studies examined the effect of pre-meal water ingestion on energy intake in humans [5–7], only one study has clearly immediately after consuming water was associated with a reduction in energy intake (r = 0.365, p = 0.037). mentioned the temperature of water used in the study (i.e., at 5–7 °C) [7]. The most plausible explanation for why dier ff ent tempera- tures of water affected ad libitum energy intake is likely to Discussion be the changes in gastric motility. In the present study, the cross-sectional gastric antral areas measured immediately The present study is, to our knowledge, the first to investigate how different water temperatures influence gastric motil- after consuming water (i.e., post) increased significantly in the 2 °C and 37 °C trials compared with the 60 °C trial. ity and energy intake using ultrasound imaging systems. The main findings of the present study are that consuming On the other hand, the frequency of the gastric contractions measured over 1 h after consuming water was lowered in the 500 mL of water at 2 °C suppressed gastric contractions and ad libitum energy intake compared with consuming 500 mL 2 °C trial than the 60 °C trial. The temperature of a drink is known to be one of the major factors affecting the gastric of water at 37 °C and 60 °C. Furthermore, subjective appe- tite perception of hunger tended to be lower after consuming motility [8, 9, 21, 22]. Although no studies have addressed the effects of different water temperatures on the cross-sec- 500 mL of water at 2 °C than after consuming 500 mL of water at 60 °C. In addition, reduced energy intake after con- tional antral area, Mishima et al. [9] reported that the val- ues of the lag-phase time, as an index of gastric emptying, suming cold water (i.e., at 2 °C) ingestion was accompanied by a change in gastric contractions. These findings add new were shorter after consuming nutrient drinks at 60 °C than consuming the same drinks at 37 °C. Several studies have knowledge to the existing literature that water temperature may play an important role in modulating gastric motility suggested that gastric distention is one of the key factors in the regulation of energy intake [23–25]. The previous study and energy intake. Although these findings need to be con- firmed in larger and more diverse populations, the present has reported that subjective appetite perception of fullness was linearly related to the total gastric volumes [23]. Other study is of value in showing that pre-meal cold (vs. warm) 1 3 108 European Journal of Nutrition (2020) 59:103–109 studies have also reported that gastric distension prior to and older adults [31], and obese middle-aged adults [32], a meal is related with energy intake [10, 17]. In addition, it would be interesting for future studies to examine the there was a relationship between the frequency of the gastric effects of long-term pre-meal water ingestion at different contractions measured at immediately after consuming water temperatures on weight management in various populations. and energy intake as demonstrated in the present study. One In addition, since the present study did not ask or objectively possible mechanism for these changes in gastric contrac- measure daily fluid intake for each subject, this habitual fluid tions associated with subjective energy intake is changes in intake and hydration status might play a role in subjective gut hormones including motilin, a hormone that stimulates appetite [33] and energy intake. Thus, further studies should proximal stomach tone and enhances meal-induced satiety examine the effects of daily fluid intake and hydration status [26]. Future studies are required to address a more mechani- on gastric motility and energy intake. cal understanding of water temperature-induced modulation In conclusion, this study demonstrates that gastric con- of gastric motility and energy intake. Furthermore, internal tractions and ad libitum energy intake were dependent on and external changes in temperature affect the physiological the temperatures of pre-meal water in healthy young men— response in humans. Boschmann et al. have reported that consuming 500 mL of water at 2 °C 1 h before a meal was consuming water induced thermogenesis with the stimula- more effective in reducing gastric contractions and ad libi- tion of the sympathetic nervous system and the temperature tum energy intake than consuming the same amount of water of water in healthy adults [27]. In addition, the previous at 37 °C and/or 60 °C. The present findings also show that studies have addressed that exercising in a cold environ- cold water-induced reduction in energy intake appears to be ment (2 °C) increased energy intake compared with a neutral related to the modulation of the gastric motility. condition (20 °C) in overweight adults [28], and fluid tem- Acknowledgements This study was part of research activities of the perature affected gastric emptying rate in healthy adults [9 ]. Human Performance Laboratory, Organization for University Research Nonetheless, no studies are available to compare directly the Initiatives, Waseda University. effects of water-induced thermogenesis on gastric motility and appetite. Thus, further studies are warranted to examine Author contributions KF designed the study, supervised the data col- these issues. lection, and performed the data analysis. YH, TY, RY, and KS assisted the data collection. MM supervised all the aspects of the study. KF This study has several strengths. We examined the effects and MM conceived the study and wrote the manuscript. All authors of different temperatures of water on both gastric motil- approved the final version of the manuscript. ity and energy intake. The physical characteristics of the subjects, the amount of water drunk, and the time interval Compliance with ethical standards between ingestion of water and the subsequent meal were often used to address the factors for the influence of pre- Ethical standard This study was approved by the Ethics Committee on Human Research of Waseda University (approval number: 2017-260). meal water ingestion on energy intake [5–7]. To our knowl- edge, the present study is the first to examine the effects of Informed consent A written informed consent was obtained from all different temperatures of water on subsequent energy intake. subjects prior to the study. Moreover, we have tried to address the role of gastric motil- ity, a potential mechanism underpinning the modulation Conflict of interest All authors declare that there is no conflict of in- of energy intake [23], on subsequent energy intake. The terest. findings of the present study may help to support appetite adjustment in healthy young individuals as an inexpensive Open Access This article is distributed under the terms of the Crea- tive Commons Attribution 4.0 International License (http://creat iveco and easy method of weight management. The limitations of mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- the present study include measuring gastric distention and tion, and reproduction in any medium, provided you give appropriate contractions as the only indices of gastric motility. 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The effects of water temperature on gastric motility and energy intake in healthy young men

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Springer Journals
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Copyright © The Author(s) 2019
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Chemistry; Nutrition
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1436-6207
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1436-6215
DOI
10.1007/s00394-018-1888-6
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Abstract

Purpose Although immediate pre-meal water ingestion has been shown to reduce energy intake in healthy young men, no studies are available regarding potential mechanisms underlying the effect of energy intake in response to different tempera - tures of pre-meal water ingestion. This study examined the effects of consuming different temperatures of water on gastric motility and energy intake in healthy young men. Methods Eleven young men were completed three, 1-day trials in a random order. Subjects visited the laboratory after a 10-h overnight fast and consumed 500 mL of water at 2 °C, 37 °C, or 60 °C in 5 min. Then, subjects sat on a chair over 1 h to measure the cross-sectional gastric antral area and gastric contractions using the ultrasound imaging systems. Thereafter, sub- jects consumed a test meal until they felt completely full. Energy intake was calculated from the amount of food consumed. Results Energy intake in the 2 °C (6.7 ± 1.8 MJ) trial was 19% and 26% lower than the 37 °C (7.9 ± 2.3 MJ, p = 0.039) and 60 °C (8.5 ± 3.2 MJ, p = 0.025) trials, respectively. The frequency of the gastric contractions after 1-h consuming water was lowered in the 2 °C trial than the 60 °C trial (trial-time interaction, p = 0.020). The frequency of gastric contractions was positively related to energy intake (r = 0.365, p = 0.037). Conclusions These findings demonstrate that consuming water at 2 °C reduces energy intake and this reduction may be related to the modulation of the gastric motility. Keywords Water ingestion · Water temperature · Gastric motility · Ultrasound imaging · Appetite · Energy intake Introduction and subsequent weight gain in healthy individuals may be important for the long-term weight management. Among Public health research is addressing on the long-term man- available methods for preventing a positive energy balance, agement of weight loss by creating a negative energy bal- water consumption is a simple method and has potentially a ance through increased physical activity and/or decreased key role to play in reducing energy intake [4]. food intake in overweight and obese individuals [1]. How- To date, three laboratory-based studies have examined ever, estimates in many countries suggest that most individu- the effects of pre-meal water ingestion on subsequent energy als do not complete a sufficient amount of physical activ - intake in various individuals [5–7] with disparate effects. ity to meet the guidelines set out by expert panels [2, 3]. These studies vary in protocols including the amount of Thus, while promoting physical activity for all individuals water ingested (i.e., 375–568 mL), and the time interval is important, strategies to prevent a positive energy balance between ingestion of water and the subsequent meal (i.e., immediately before to 30 min before a meal). In addition, only one study has clearly reported the temperature of water * Masashi Miyashita [email protected] used in the study (5–7 °C) [7]. Although the reasons for these discrepant findings among studies are not clearly Graduate School of Sport Sciences, Waseda University, known, Corney et  al. [6] have suggested that the rate of 2-579-15 Mikajima, Tokorozawa, Saitama 359-1192, Japan gastric emptying of liquid meals was slower in older adults Japan Society for the Promotion of Science, 5-3-1 than in younger adults, indicating that gastric distension Koujimachi, Chiyoda-ku, Tokyo 102-0083, Japan may be a factor for influencing subsequent energy intake. Faculty of Sport Sciences, Waseda University, 2-579-15 In addition, the rate of gastric emptying or the magnitude Mikajima, Tokorozawa, Saitama 359-1192, Japan Vol.:(0123456789) 1 3 104 European Journal of Nutrition (2020) 59:103–109 of gastric motility (i.e., measured via cross-sectional antral K.K., Japan). The 500 mL of water was chosen, because area reflecting gastric distention, rate of gastric emptying, this volume has been shown to reduce subsequent energy and frequency of gastric contractions) are known to be influ- intake in a previous study [7]. Subjects then sat on a chair enced by the temperatures of consumed “energy-containing in a fixed position as above in the laboratory until 1005. drinks” [8, 9]. Collectively, to our knowledge, none of pre- Whilst subjects rested until 1005, 2D ultrasound scan was vious studies [5–7] have examined the effects of pre-meal performed to assess the change in the cross-sectional gastric water ingestion on gastric motility and subsequent energy antral area and gastric contractions before and after con- intake in healthy young adults. Furthermore, there is as yet suming a 500 mL of water at 2 °C, 37 °C, or 60 °C. Then, no evidence regarding how different temperatures of “water” subjects were asked to consume the test meal from 1005 and affect energy intake and subjective feelings of appetite in were instructed to eat as much as they satisfied until 1105. healthy young adults. The interval of 60 min between water ingestion and subse- Therefore, the purpose of this study was to investigate the quent meal was chosen, since we thought that this interval effects of different temperatures of water on gastric motility may be long enough to assess gastric motility using ultra- and energy intake in healthy young men. sound imaging as this was the case in the previous study [10]. Subjects also completed a 100-mm visual analogue scale questionnaire [11], assessing the subjective perceptions Methods of appetite, at 0900 (i.e., pre), immediately after consuming water (i.e., post), and 30, 60, 90, and 120 min after consum- Subjects ing water. After approval from the Ethics Committee on Human Subjective appetite perceptions and energy intake Research of Waseda University (approval number: 2017- 260), 11 healthy, lean men gave written informed consent The acceptability of the test meal was ensured by a prior to participate in this study. The physical characteristics of written survey and selected instant noodles as a test meal. the subjects were as follows: age 23.4 ± 1.4 years, height Subjects were provided with a bowl of instant noodles (i.e., 1.71 ± 0.04 m, body mass 64.0 ± 9.8 kg, body mass index 9.7% energy as protein, 20.5% energy as fat, and 69.8% 21.8 ± 2.6  kg/m , and waist circumference 73.1 ± 5.4 cm energy as carbohydrate) at 1005. Subjects were offered with [mean ± standard deviations (SD)]. All subjects were non- repeated small bowls of noodles throughout the meal time. smokers and were not taking any medicine, and their body Warm food was continuously available until the subjects masses had been stable for at least 3 months before the study. finished eating the test meal. Subjects were instructed to eat until they felt “comfortably full and satisfied” and that Experimental protocol additional food was available if desired [12]. This ensures that subjects were not able to know how much they had con- The subjects underwent three, 1-day laboratory-based trials sumed while eating. Drinking water was restricted, while in random order: (1) water at 2 °C, (2) water at 37 °C, and the subject was taking the test meal. The upper limit of meal (3) water at 60 °C. The interval between trials was at least intake time was 1 h, and mean time to consume the test 6 days. All subjects were asked to maintain their normal meal in the 2 °C, 37 °C, and 60 °C trials was 18.2 ± 6.5 min, eating habits among the trials and to refrain from vigorous 21.8 ± 9.4 min, and 24.1 ± 11.9 min, respectively. The total exercise and alcohol intake for 24 h before each trial. In the amount of food intake (g) was ascertained by examining the 24 h before the first trial, subjects measured and recorded weighted difference in the test meal remaining compared to all dietary intakes, and then they replicated these dietary that initially presented. The total energy intake from the test intakes in the 24 h preceding the second and third trials. meal was calculated using the manufacture-reported values. Food diaries were analyzed by software to determine energy Subjects completed 100-mm visual analogue scales [11, 13] intake and macronutrient content (Excel Eiyoukun Ver 5.0, before (i.e., pre), immediately after (i.e., post), and at 30, Kenpakusha, Japan). On each trial day, subjects reported to 60, 90, and 120 min after consuming water, to assess the the laboratory at 0850 after a 10-h overnight fast-subjects perceptions of appetite (i.e., hunger, fullness, and desire to were allowed to drink only one glass of water no later than eat sweet, sour, fatty, and salty foods). In addition, subjects 2 h prior to each trial. The subjects were asked to sit on a completed 100-mm visual analogue scales before (i.e., pre), comfortable chair in a fixed position (i.e., the angle between immediately after (i.e., post), and at 30, 60, 90, and 120 min the upper part and lower part of the body was approximately after consuming water, to assess the perceptions of feelings 120°) and to consume a 500 mL of water at 2 °C, 37 °C or of stomach condition (i.e., “Does your stomach feel uncom- 60 °C over a 5-min period at 0900. The water temperature fortable?”, “Do you feel your stomach is expanding?”, and was measured by an electric thermometer (testo 106, Testo “Do you want to eat now?”). Verbal anchors “not at all” 1 3 European Journal of Nutrition (2020) 59:103–109 105 and “extremely” were placed at 0 and 100 mm on the visual Results analogue scales, respectively. Dietary data Assessment of gastric motility Mean self-reported energy intake for the day prior to each Several previous studies suggest that the antrum is the most trial was 7.2 ± 1.5 MJ. Energy intake equated to 30 ± 6% suitable area in which to evaluate the stomach capacity (for (59.9 ± 20.7  g/day) from fat, 54 ± 7% (218.3 ± 30.8  g/day) a review of this, see Ref. [14]). Antral area measurements from carbohydrate, and 16 ± 3% (70.4 ± 20.6 g/day) from were performed using a 2D ultrasound machine (LOGIQ-e, protein. GE Healthcare, USA) and a 5.0 MHz sector transducer. All metals were removed from the surrounding area to avoid the Pre‑trial possibility of interference during acquisition. To optimise precision, the transducer was positioned vertically to obtain There were no significant differences in body mass a parasagittal image of the antrum, with the superior mesen- among the 2 °C, 37 °C, and 60 °C trials (63.8 ± 9.9 kg vs. teric vein and the abdominal aorta in a longitudinal section, 64.3 ± 9.7  kg vs. 63.9 ± 9.9  kg, respectively; p = 0.075) at as described previously [14]. After obtaining these signals pre-trial (i.e., 0900). At pre-trial, subjective appetite per- for measuring antral area for 3 min [15] before (i.e., pre), ceptions (i.e., hunger, fullness, and desire to eat sweet, immediately after (i.e., post), and at 10, 20, 30, 40, 50, and sour, fatty, and salty foods) and perception of the stomach 60 min after consuming water. The gastric antral area (cm ) did not differ across the trials. Cross-sectional antral areas 2 2 2 was determined using an image-editing software (ImageJ (3.1 ± 1.3  cm vs. 3.6 ± 1.3  cm vs. 3.1 ± 1.0  cm for the 1.47, National Institute of Mental Health, USA). The gastric 2 °C, 37 °C, and 60 °C trials, respectively; p = 0.277) and contractions of the antral area were defined as the frequency frequency of gastric contractions (4.5 ± 2.5 times/3 min vs. of contractions per 3 min, and were measured before (i.e., 4.5 ± 2.7 times/3 min vs. 4.5 ± 3.0 times/3 min for the 2 °C, pre), immediately after (i.e., post), and at 10, 20, 30, 40, 50, 37 °C and 60 °C trials, respectively; p = 0.996) were also not and 60 min after consuming water [16]. different at pre-trial (i.e., 0900) among the trials. Statistical analysis Energy intake Data were analyzed using the Predictive Analytics Software Energy intake differed among the trials (6.7 ± 1.8 MJ vs. (PASW) version 23.0 for Windows (IBM SPSS Statistics 7.9 ± 2.3 MJ vs. 8.5 ± 3.2 MJ for the 2 °C, 37 °C and 60 °C 23.0, SPSS Japan Inc., Japan). The Shapiro–Wilk test was trials, respectively; p = 0.009) (Fig. 1). Post hoc tests revealed used to check for normality of distribution—all parameters that energy intake in the 2 °C trial was 19% and 26% lower were found to be normally distributed. Repeated-measures one-factor analysis of variance (ANOVA) was used to assess differences among the three trials in energy intake and the length of meal. Repeated-measures, two-factor ANOVA was used to examine differences over time among the three trials in cross-sectional antral area, frequency of gastric contractions, subjective appetite perceptions (i.e., hunger, fullness and desire to eat sweet, sour, fatty, and salty foods), and subjective perception of the stomach. Where signifi- cant trial–time interactions and trial effects were found, the values were subsequently analyzed using a Bonferroni multiple-comparison test. The correlation coefficients were determined using Pearson’s product-moment tests between the frequency of gastric contractions and energy intake. The 95% confidence intervals (95% CI) for the mean absolute pairwise differences among the three trials were calculated using the t-distribution and degrees of freedom (n − 1). Data Fig. 1 Energy intake at ad libitum test meal: 60 min after consuming water (500 mL) at 2 °C, 37 °C and 60 °C. Data are mean ± SD. Mean were expressed as mean ± standard deviations (SD). Statisti- was compared using one-factor ANOVA for the main effect of trial cal significance was set at p < 0.05. followed by a Bonferroni multiple-comparison test. *Significantly different between the 2  °C and 60  °C trials (p < 0.05). Significantly different between the 2 °C and 37 °C trials (p < 0.05) 1 3 106 European Journal of Nutrition (2020) 59:103–109 than the 37 °C (p = 0.039, 95% CI 15.051–585.749) and compared with the 60 °C trial immediately after consum- 2 2 60 °C (p = 0.025, 95% CI 51.498–793.684) trials, respec- ing water (i.e., post) (10.0 ± 5.0 cm vs. 9.3 ± 1.2  cm vs. tively. The time taken to feel completely full in the 2 °C, 6.8 ± 2.1  cm for the 2 °C, 37 °C and 60 °C trials, respec- 37 °C, and 60 °C trials was 18.2 ± 6.5 min, 21.8 ± 9.4 min, tively; 2 °C vs. 60 °C: p = 0.030, 95% CI 0.379–7.802, 37 °C and 24.1 ± 11.9 min, respectively. The time taken to feel vs. 60 °C: p = 0.0019, 95% CI 0.407–4.556) (Fig. 3). The fre- completely full was 5.9 min shorter in the 2 °C trial than the quency of gastric contractions differed significantly among 60 °C trial (p = 0.046, 95% CI 0.086–11.768). the trials (main effect of trial, p < 0.001, and tr ial–time interaction: p < 0.001). Post hoc analyses indicated differ - Subjective appetite perceptions ences in the frequency of the gastric contractions between trials immediately after (i.e., post) and at 10, 20, 30, 40, For subjective appetite perception of hunger, there was a 50, and 60 min after consuming water—the frequency of significant main effect of time (p < 0.001) and tr ial–time the gastric contractions was lower in the 2 °C trial than the interaction among the three trials (p = 0.027) (Fig. 2). Post 60 °C trial (post: p < 0.001, 95% CI 2.818–5.932, 10 min: hoc analysis revealed that subjective appetite perception of p = 0.001, 95% CI 1.202–3.548, 20  min: p = 0.004, 95% hunger tended to be lower during the 2 °C trial than the CI 1.158–4.592, 30 min: p = 0.002, 95% CI 1.333–4.167, 60 °C trial at 30 and 60 min after consuming water (30 min: 40  min: p = 0.016, 95% CI 0.512–4.238, 50  min: p = 0.074, 95% CI −1.557 to 38.557, 60 min: p = 0.086, and p = 0.026, 95% CI 0.341–4.909, 60 min: p = 0.002, 95% CI 95% CI −2.318 to 40.984). In each trial, subjective appetite 1.608–5.142) (Fig. 4). At immediately after (i.e., post), and perception of hunger peaked 60 min after consuming water at 30, 50, and 60 min after consuming water, the frequency (main effect of time: p < 0.001). There were no significant of the gastric contractions was lower in the 37 °C trial than differences in the other subjective appetite perceptions (i.e., the 60 °C trial (post: p = 0.011, 95% CI 0.605–3.895, 30 min: hunger and desire to eat sweet, sour, fatty, and salty foods) p = 0.034, 95% CI 0.104–2.371, 50 min: p = 0.024, 95% CI or perception of the stomach (i.e., “Dose your stomach feel 0.369–4.656, 60 min: p = 0.005, 95% CI 1.192–5.408). At uncomfortable?”, “Do you feel your stomach is expanding?”, immediately after (i.e., post) and at 10 min after consuming and “Do you want to eat now?”). water, the frequency of the gastric contractions was lower in the 2 °C trial than the 37 °C trial (post: p = 0.003, 95% Gastric antral area and gastric contractions CI 0.880–3.370, 10 min: p < 0.001, 95% CI 1.453–2.872). There were trial–time interactions (p < 0.001). Cross-sec- tional antral areas increased in the 2 °C and 37 °C trials Fig. 3 Cross-sectional gastric antral area before and after consuming water (500 mL) at 2 °C, 37 °C and 60 °C. Data are mean ± SD. Black Fig. 2 Subjective appetite perceptions of hunger before and after rectangle indicates consuming water in 5  min. Data were analyzed consuming water (500  mL) at 2  °C, 37  °C, and 60  °C. Data are mean ± SD. Black rectangle indicates consuming water in 5  min. using two-factor ANOVA followed by a Bonferroni multiple-compar- Data were analyzed using two-factor ANOVA followed by a Bonfer- ison test. There was a significant main effect of time (p < 0.001) and roni multiple-comparison test. There was a significant main effect of trial–time interaction (p = 0.020). *Significantly different between the time (p < 0.001) and trial–time interaction (p = 0.027). (*)Different 2  °C and 60  °C trials (p < 0.05). Significantly different between the between the 2 °C and 60 °C trials (p < 0.10) 37 °C and 60 °C trials (p < 0.05) 1 3 European Journal of Nutrition (2020) 59:103–109 107 water ingestion may provide additional benefits to weight management in healthy individuals as this method can be applied inexpensively and easily on a daily basis. Three laboratory-based studies [5–7] have demonstrated reductions in energy intake after acute water ingestion which were seen in the present study. One study found that pre- meal (i.e., 30 min) water ingestion was effective in reduc- ing subsequent energy intake in overweight and obese older adults [7]. Another study found similar results in response to pre-meal (i.e., 30 min) water ingestion in healthy older adults, but not in healthy young adults [5]. One recent study found that water ingestion immediately before a meal was effective in reducing subsequent energy intake in healthy young adults [6]. Although the precise reasons for the dis- crepant findings observed in the study by Van Walleghen Fig. 4 Frequency of gastric contractions before and after consuming water (500 mL) at 2 °C, 37 °C, and 60 °C. Data are mean ± SD. Black et al. [5] are not known, the timing of ad libitum energy rectangle indicates consuming water in 5  min. Data were analyzed intake in response to water ingestion may affect subsequent using two-factor ANOVA followed by a Bonferroni multiple-com- energy intake [17, 18]. Indeed, a previous study has reported parison test. There was a significant main effect of trial (p < 0.001), that inter-meal interval between drink ingestion and ad libi- main effect of time (p < 0.001), and trial–time interaction (p = 0.020). *Significantly different between the 2 °C and 60 °C trials (p < 0.05). tum meal was associated with gastric antral area and energy Significantly different between the 2  °C and 37  °C trials (p < 0.05). intake, although nutrient drink was used in this study [17, Significantly different between the 37 °C and 60 °C trials (p < 0.05) 18]. Another reason for the discrepant findings is that dif - ferences in the rate of gastric emptying between young and Relationships between energy intake and frequency older individuals might affect subjective energy intake [6 , 19]. Alternatively, given the well-documented slower rate of the gastric contractions of gastric emptying at cold water (i.e., at 5 °C) compared with warm water (i.e., at 37 °C) [20], the temperature of There was a positive relationship between energy intake from the test meal and the frequency of the gastric con- ingested water may be the proposed reason for the discrepant findings among the studies. Indeed, among three available tractions measured immediately after consuming water. The reduction in frequency of the gastric contractions measured studies examined the effect of pre-meal water ingestion on energy intake in humans [5–7], only one study has clearly immediately after consuming water was associated with a reduction in energy intake (r = 0.365, p = 0.037). mentioned the temperature of water used in the study (i.e., at 5–7 °C) [7]. The most plausible explanation for why dier ff ent tempera- tures of water affected ad libitum energy intake is likely to Discussion be the changes in gastric motility. In the present study, the cross-sectional gastric antral areas measured immediately The present study is, to our knowledge, the first to investigate how different water temperatures influence gastric motil- after consuming water (i.e., post) increased significantly in the 2 °C and 37 °C trials compared with the 60 °C trial. ity and energy intake using ultrasound imaging systems. The main findings of the present study are that consuming On the other hand, the frequency of the gastric contractions measured over 1 h after consuming water was lowered in the 500 mL of water at 2 °C suppressed gastric contractions and ad libitum energy intake compared with consuming 500 mL 2 °C trial than the 60 °C trial. The temperature of a drink is known to be one of the major factors affecting the gastric of water at 37 °C and 60 °C. Furthermore, subjective appe- tite perception of hunger tended to be lower after consuming motility [8, 9, 21, 22]. Although no studies have addressed the effects of different water temperatures on the cross-sec- 500 mL of water at 2 °C than after consuming 500 mL of water at 60 °C. In addition, reduced energy intake after con- tional antral area, Mishima et al. [9] reported that the val- ues of the lag-phase time, as an index of gastric emptying, suming cold water (i.e., at 2 °C) ingestion was accompanied by a change in gastric contractions. These findings add new were shorter after consuming nutrient drinks at 60 °C than consuming the same drinks at 37 °C. Several studies have knowledge to the existing literature that water temperature may play an important role in modulating gastric motility suggested that gastric distention is one of the key factors in the regulation of energy intake [23–25]. The previous study and energy intake. Although these findings need to be con- firmed in larger and more diverse populations, the present has reported that subjective appetite perception of fullness was linearly related to the total gastric volumes [23]. Other study is of value in showing that pre-meal cold (vs. warm) 1 3 108 European Journal of Nutrition (2020) 59:103–109 studies have also reported that gastric distension prior to and older adults [31], and obese middle-aged adults [32], a meal is related with energy intake [10, 17]. In addition, it would be interesting for future studies to examine the there was a relationship between the frequency of the gastric effects of long-term pre-meal water ingestion at different contractions measured at immediately after consuming water temperatures on weight management in various populations. and energy intake as demonstrated in the present study. One In addition, since the present study did not ask or objectively possible mechanism for these changes in gastric contrac- measure daily fluid intake for each subject, this habitual fluid tions associated with subjective energy intake is changes in intake and hydration status might play a role in subjective gut hormones including motilin, a hormone that stimulates appetite [33] and energy intake. Thus, further studies should proximal stomach tone and enhances meal-induced satiety examine the effects of daily fluid intake and hydration status [26]. Future studies are required to address a more mechani- on gastric motility and energy intake. cal understanding of water temperature-induced modulation In conclusion, this study demonstrates that gastric con- of gastric motility and energy intake. Furthermore, internal tractions and ad libitum energy intake were dependent on and external changes in temperature affect the physiological the temperatures of pre-meal water in healthy young men— response in humans. Boschmann et al. have reported that consuming 500 mL of water at 2 °C 1 h before a meal was consuming water induced thermogenesis with the stimula- more effective in reducing gastric contractions and ad libi- tion of the sympathetic nervous system and the temperature tum energy intake than consuming the same amount of water of water in healthy adults [27]. In addition, the previous at 37 °C and/or 60 °C. The present findings also show that studies have addressed that exercising in a cold environ- cold water-induced reduction in energy intake appears to be ment (2 °C) increased energy intake compared with a neutral related to the modulation of the gastric motility. condition (20 °C) in overweight adults [28], and fluid tem- Acknowledgements This study was part of research activities of the perature affected gastric emptying rate in healthy adults [9 ]. Human Performance Laboratory, Organization for University Research Nonetheless, no studies are available to compare directly the Initiatives, Waseda University. effects of water-induced thermogenesis on gastric motility and appetite. Thus, further studies are warranted to examine Author contributions KF designed the study, supervised the data col- these issues. lection, and performed the data analysis. YH, TY, RY, and KS assisted the data collection. MM supervised all the aspects of the study. KF This study has several strengths. We examined the effects and MM conceived the study and wrote the manuscript. All authors of different temperatures of water on both gastric motil- approved the final version of the manuscript. ity and energy intake. The physical characteristics of the subjects, the amount of water drunk, and the time interval Compliance with ethical standards between ingestion of water and the subsequent meal were often used to address the factors for the influence of pre- Ethical standard This study was approved by the Ethics Committee on Human Research of Waseda University (approval number: 2017-260). meal water ingestion on energy intake [5–7]. To our knowl- edge, the present study is the first to examine the effects of Informed consent A written informed consent was obtained from all different temperatures of water on subsequent energy intake. subjects prior to the study. Moreover, we have tried to address the role of gastric motil- ity, a potential mechanism underpinning the modulation Conflict of interest All authors declare that there is no conflict of in- of energy intake [23], on subsequent energy intake. The terest. findings of the present study may help to support appetite adjustment in healthy young individuals as an inexpensive Open Access This article is distributed under the terms of the Crea- tive Commons Attribution 4.0 International License (http://creat iveco and easy method of weight management. The limitations of mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- the present study include measuring gastric distention and tion, and reproduction in any medium, provided you give appropriate contractions as the only indices of gastric motility. 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Published: Feb 7, 2020

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