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Am J Clin Nutr 89: 431-435, 2009. First published December 3, 2008; doi:10.3945/ajcn.2008.26180
 American Journal of Clinical Nutrition, doi:10.3945/ajcn.2008.26180
Vol. 89, No. 1, 431-435, January 2009
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© 2009 American Society for Clinical Nutrition

ORIGINAL RESEARCH COMMUNICATION

Monosodium L-glutamate added to a high-energy, high-protein liquid diet promotes gastric emptying1,2,3

Hiroaki Zai, Motoyasu Kusano, Hiroko Hosaka, Yasuyuki Shimoyama, Atsuto Nagoshi, Masaki Maeda, Osamu Kawamura and Masatomo Mori

1 From the Department of Medicine and Molecular Science, Gunma University Graduate School of Medicine, Maebashi, Japan (HZ, HH, AN, MM, OK, and MM), and the Department of Endoscopy and Endoscopic Surgery, Gunma University Hospital, Maebashi, Japan (MK and YS).

2 The experimental diets and monosodium L-glutamate used in this study were kind gifts from Ajinomoto Co, Inc.

3 Reprints not available. Address correspondence to M Kusano, Department of Endoscopy and Endoscopic Surgery, Gunma University Hospital, Maebashi 371-8511, Japan. E-mail address: mkusano{at}showa.gunma-u.ac.jp.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Free glutamate activates taste receptors on nerves in the oral cavity to elicit a unique taste known as umami. Recently, umami taste receptors were also found in the gastric mucosa. Although reports suggest that mucosal receptors may respond to free glutamate to modulate gastric function, no evidence of any effect on gastric emptying has been documented.

Objective: We hypothesized that glutamate may act as a modulator of gastric function. We studied the effects of L-glutamate enrichment of a protein-rich liquid meal, and similar enrichment of an equicaloric carbohydrate meal or noncaloric water, on gastric emptying.

Design: Ten healthy men were enrolled. Nine of the 10 subjects included in the study ingested all test meals with and without monosodium L-glutamate (MSG), and the remaining subject ingested only the protein-rich meals with and without MSG. All experimental and control liquid meals included [1-13C]sodium acetate as a tracer. After a test meal or water was ingested, 13C breath tests were performed to estimate gastric emptying.

Results: MSG enrichment not only resulted in a significant decrease in the mathematically simulated half-excretion (emptying) time of a protein-rich meal, but also increased the area under the curve (%dose/h) significantly. In contrast, MSG had no significant effect on the gastric emptying of a carbohydrate meal or a noncaloric water meal.

Conclusions: Enrichment with MSG facilitated gastric emptying of a protein-rich meal exclusively, which suggests that free glutamate is important for protein digestion and may be helpful in the management of delayed gastric emptying.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A wide variety of factors affect rates of gastric emptying. For example, the ingredients and energy density of meals are known to influence gastric emptying significantly. In clinical circumstances, delayed gastric emptying and subsequent prolonged antral distension (1) can reduce hunger, increase satiety, and, in some cases, cause stomach discomfort, all of which pose significant barriers to adequate nutrition (2–4). In such situations, delayed gastric emptying is a focal point of debate about anorexia caused by dyspepsia, and prokinetic agents are administered widely for treatment.

Other methods to improve delayed gastric emptying may involve the chemosensory (gustatory and olfactory) enhancement of meals with flavors and seasonings, which activate the autonomic system that innervates the gastrointestinal (GI) tract. Oral intake of a monosodium salt of L-glutamic acid [monosodium L-glutamate (MSG); a flavor enhancer] is known to stimulate secretions from the exocrine system (saliva and gastric, bile, and pancreatic juices) (5–9) and those from the GI endocrine system (such as insulin) (10). Free L-glutamate binds to receptors on taste cells in the oral cavity, activating taste nerves that elicit the unique taste known as umami (11, 12).

Genes encoding glutamate-sensing receptor molecules were recently identified in the oral cavity (T1R1-T1R3 heterodimers, ionotropic, and different variants of various metabotropic glutamate receptors) (13–18). Interestingly, several recent reports have shown that T1Rs and mGluR1 are also expressed in the upper GI mucosa of humans, rats, and mice (19, 20). Furthermore, intragastric administration of L-glutamate has been shown to increase the firing rate of afferent fibers in the gastric branch of the rat vagus nerve (21). These reports suggest that the stomach is capable of sensing umami substances that help regulate digestion and absorption.

Knowing that free L-glutamate coexists naturally with dietary proteins and that L-glutamate activates the autonomic nervous system by both taste and GI luminal stimulation, we investigated whether L-glutamate enrichment could affect the rate of gastric emptying. This study tests the effect of L-glutamate enrichment on gastric emptying in 3 groups of healthy men who consumed protein-rich liquid meals, equicaloric carbohydrate liquid meals, or equivolume noncaloric water meals.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Healthy volunteers
Before the study, Helicobacter pylori infection was assessed by serology (Mitsubishi Kagaku Bio-clinical Laboratories Inc, Tokyo, Japan) at a laboratory in central Japan. Ten healthy male volunteers (mean age: 32.4 y; range: 27–45 y) without H. pylori infection were enrolled. The following exclusion criteria were applied: 1) no previous abdominal surgery (except appendectomy), 2) no regular medication use, and 3) no intake of medications during the previous week that could alter GI motor function.

Experimental protocol
The Institutional Review Board of Gunma University Graduate School of Medicine approved the study protocol, and all subjects gave written informed consent. All examinations were performed after an overnight fast (the subjects could drink water freely until 30 min before examination). When the same subject participated in ≥2 different examinations, the examinations were conducted ≥1 wk apart. The schedule of examinations was set as a double-blind study, and the order of test diets was randomized. The subjects were asked to ingest the test meal in the first 3 min of the examination and were then instructed to lie in supine position during the examination.

Test meals
Three types of liquid test meals (400 kcal/400 mL) labeled with 100 mg [13C]sodium acetate (Cambridge Isotope Laboratories Inc, Cambridge, MA) were prepared: one meal (protein-rich diet) consisted of 12.5% dextrin (TK16; Matsutani Chemical, Itami, Japan) and 12.5% casein-calcium (EN9N; DMV International, Veghel, Netherlands), another (carbohydrate diet) contained 25% dextrin, and the third was a water control to determine whether nutrients influence the glutamate effect. Monosodium L-glutamate (MSG; 0.5% wt:vol; Ajinomoto Inc, Kawasaki, Japan) was either added to or withheld from liquid test meals. To mask the taste of the glutamate, all meals were flavored with the noncaloric sweetener aspartame (Ajinomoto Inc) and plum odor (GIV010790; Givaudan Japan KK, Tokyo, Japan). The dose of MSG to be used in these experiments was chosen based on the fact that 0.5% wt:vol (equivalent to {approx}30 mmol/L glutamate) is a normal habitual concentration (22, 23) and that it is similar to half the effective concentration (EC50) value for taste receptors (15, 17, 18, 23). Nine of the 10 subjects included in the study ingested all test meals with and without MSG, and the remaining subject ingested only the protein-rich meals with and without MSG.

Measurement of gastric emptying
During the 3 h after ingestion of a test meal, a 13C breath test was performed (24–27) on breath samples obtained by using an exclusive nasal cannula connected to an infrared spectrometer (Breath ID System; Exalenz Bioscience Ltd, Modiin, Israel; http://www.exalenz.com) that analyzes the ratio of 13CO2 to 12CO2 in each breath sample. This system, mechanically identical to Microstream capnography for monitoring end-tidal CO2 (Et-CO2), collects each subject's breath automatically under continuous suction, with virtually no subject cooperation (28–31). The Et-CO2 monitoring system is used widely to monitor the respiration of patients receiving critical care or anesthesia. Breath samples were stored in intermediate cells with built-in capnography to regulate carbon dioxide concentrations, which were subsequently passed on continuously and in sequence to an analysis chamber. The total number of breath samples ranged from 60 to 70 per subject. Ratio data obtained from breath tests are expressed as the rate of 13CO2 recovery (ratio of 13CO2 to 12CO2) per hour of each initially administered 13C substrate (%dose/h). In plots of %dose/h values, the slope of the resulting curve corresponds to the velocity of gastric emptying between data time points. Values in %dose/h were determined by calculating the ratio of 13CO2 to 12CO2 in the breath samples. Benefits of stable-isotope techniques that use 13C-labeled test meals for the breath test include ease of performance, noninvasiveness, and high sensitivity for the quantitative assessment of gastric emptying (25, 26, 32–37).

Data analysis
Gastric emptying was evaluated by using 2 parameters: half the gastric excretion (emptying) time (t1/2ex) and total excretion of 13CO2 during 180 min (cumulative %dose/h over 180 min). The t1/2ex indicates the time at which half of the 13CO2 dose, in relation to cumulative 13CO2 excretion when time is infinite, is excreted (29). For the reasons stated above, t1/2ex and scintigraphic half-emptying time are not identical; however, there is a linear correlation between t1/2ex in the 13C breath test and scintigraphic half emptying times (26, 35). Total excretion of 13CO2 during 180 min was calculated by measuring the area under the %dose/h curve.

Statistical analysis
The effects of glutamate enrichment on t1/2ex and total excretion of 13CO2 during 180 min were compared, with serving sequence and subject as variables, in an analysis of variance (ANOVA). A repeated-measures 2-factor ANOVA with interactions was used to analyze treatment and time effects in 10 participants ingesting the protein meal and in 9 participants in each of the other meal groups. If a significant interaction between treatment and time was indicated (P < 0.05), pairwise comparisons were performed after a Bonferroni correction. Analyses comparing liquid test meals were carried out by using a repeated-measures 3-factor ANOVA (time, treatment, and meal) with interactions, with significance defined as a P value <0.05. A Bonferroni correction was applied to 3 pairwise comparisons of meals. Statistical analyses were carried out by using SPSS16.0J for Windows (SPSS Inc, Chicago IL). Results are expressed as mean ± SD, and statistical significance is defined as P values <0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Effect of MSG on gastric emptying after a protein-rich meal
The time courses of 13CO2 excretion (%dose/h curves) for 10 subjects who were used to estimate gastric emptying rate and total excretion of 13CO2 during 180 min (Cum-%dose/h during 180 min) after a protein-rich meal are shown in Figure 1. After the protein-rich meal was ingested, the %dose/h curve ascended rapidly, reaching the plateau of 9.4 ± 1.4%dose/h at 45 min. The %dose/h curve after a protein-rich meal with MSG (0.5% wt:vol) ascended further, with a maximum mean (± SD) of 11.4 ± 2.0%dose/h at 60 min. The %dose/h curve for a protein-rich meal showed a significant interaction between time and treatment (P < 0.001). Partial tests showed a significant difference in %dose/h after protein-rich meals with and without MSG (Figure 1A). Total excretion of 13CO2 (Cum-%dose/h) during 180 min was also significantly higher after a protein meal with MSG than after a meal without MSG (28.6 ± 2.4 compared with 24.7 ± 3.4; P < 0.05) (Table 1). There was a corresponding significant reduction in t1/2ex with the addition of MSG (with MSG: 153.0 ± 34.6 min; without MSG: 212.7 ± 102.6 min). On the basis of these data, we concluded that MSG significantly accelerates gastric emptying of a protein-rich meal (Table 1).


Figure 1
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  		FIGURE 1. Effect of monosodium L-glutamate (MSG) on gastric emptying after a protein-rich meal. A: Curves of 13CO2 excretion (%dose/h) after ingestion of a protein-rich meal with and without MSG (0.5% wt:vol). There was a significant interaction between time and treatment (P < 0.001, ANOVA). Significant differences relative to the ingestion of a protein-rich meal without MSG: aP < 0.05, bP < 0.01, cP < 0.001. B: Cumulative excretion of 13CO2 (Cum.%dose/h) constructed from A. Values are mean ± SD of excretion measured in 10 subjects.

 

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  		TABLE 1. Effect of monosodium L-glutamate (MSG) on gastric emptying1

 
Effect of MSG on gastric emptying after a carbohydrate meal
In contrast, no significant differences attributable to MSG were observed in %dose/h curves (Figure 2A), Cum-%dose/h during 180 min (36.4 ± 2.6 compared with 38.6 ± 3.2), or t1/2ex (197.6 ± 92.8 compared with 172.6 ± 38.2 min) after ingestion of a carbohydrate meal (Table 1). We concluded that MSG had no effect on gastric emptying after a carbohydrate meal.


Figure 2
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  		FIGURE 2. Effect of monosodium L-glutamate (MSG) on gastric emptying after a carbohydrate meal. A: Curves of 13CO2 excretion (%dose/h) after ingestion of a carbohydrate meal with and without MSG (0.5% wt:vol). There was no significant interaction between time and treatment. B: Cumulative excretion of 13CO2 (Cum.%dose/h) constructed from A. Values are mean ± SD of excretion measured in 9 subjects.

 
Effect of MSG on gastric emptying after a water meal
There were no significant differences in t1/2ex (90.8 ± 9.0 compared with 97.4 ± 10.2 min) or in Cum-%dose/h during 180 min (42.7 ± 4.8 compared with 45.6 ± 1.7) in participants who ingested the water meal with or without MSG (Table 1). Although the %dose/h curves for water showed a significant interaction between time and treatment (P < 0.05), partial tests did not show any significant differences at single time points (Figure 3). We concluded that MSG does not significantly enhance gastric emptying after intake of water (Table 1).


Figure 3
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  		FIGURE 3. Effect of monosodium L-glutamate (MSG) on gastric emptying after water intake. A: Curves of 13CO2 excretion (%dose/h) after ingestion of water with and without MSG (0.5% wt:vol). Although a significant interaction was found between time and treatment (P < 0.05), no significant differences were found at single time points. B: Cumulative excretion of 13CO2 (Cum.%dose/h) constructed from A. Values are mean ± SD of excretion measured in 9 subjects.

 
Effects of liquid test meals
A repeated-measures 3-factor ANOVA (time, treatment, and meal) with interaction detected significant differences in %dose/h curves between the 3 types of meals (P < 0.001). Post hoc paired comparisons of each meal showed that gastric emptying was significantly faster after ingestion of water (P < 0.01), but that there were no significant differences in emptying after a protein-rich meal or a carbohydrate meal.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study, enrichment of a high-energy liquid diet rich in casein (a major dairy protein in liquid meals) with MSG promoted gastric emptying in healthy men. We anticipate that the results of this study will be useful in designing treatments for the elderly, patients with dyspepsia and anorexia, and others for whom delayed gastric emptying is a significant problem. Delayed gastric emptying and subsequently prolonged antral distension result in reduced hunger, increased satiety, and, in some cases, stomach discomfort, which often prevents elders and patients from continuing proper nutrition intake (1).

Free L-glutamate binds to taste receptors on taste cells in the oral cavity and activates taste nerves to elicit the unique taste umami (11, 12)—a pleasant taste sensation that differs qualitatively from sweet, salty, sour, and bitter. Glutamate monosodium salt is used widely as a flavor enhancer in Asian cuisine. Because typical dietary proteins are tasteless by themselves (with the exception of particularly sweet proteins such as monellin) (38), it has been suggested that the umami taste presented by free L-glutamate guides protein intake, similar to the way that sweet taste guides carbohydrate intake and salt taste guides mineral intake (12). The concentration of free L-glutamate used for this study was 30 mmol/L, similar to its concentration in meat broth and within the range of recognition by human adults as the umami taste in aqueous solution (39). Our finding that a daily-use dose of MSG promotes gastric emptying after consumption of a protein-rich liquid meal suggests that we should direct our attention to the amino acid composition of foodstuffs to understand a meals' effect on digestion.

Although glutamate enrichment of the high-protein meal promoted gastric emptying, it did not result in any significant changes in gastric emptying time for either the equicaloric carbohydrate meal or the noncaloric water. This inconsistency suggests that the action of L-glutamate on the GI system differs from that of prokinetic agents that facilitate motility uniformly via direct activation of the myenteric plexus neurons (40–43). In general, noncaloric water leaves the stomach most quickly, carbohydrates and proteins leave the stomach at a similar intermediate speed, and lipids clear most slowly. Our findings in post hoc paired comparisons of the gastric emptying curves for 3 types of meals after repeated-measures 3-factor ANOVA support this generalization. The acceleration of gastric emptying observed only with the high-protein diet suggests that glutamate's effects may vary depending on other nutritional factors or ingredients in ingested food.

According to several reports, oral intake of monosodium L-glutamate stimulates exocrine secretion (saliva and gastric, bile, and pancreatic juices) (5–9). Thus, the mechanism involved in the promotion of gastric emptying of a high-protein meal is likely to involve the digestive juice secretion. Several recent reports also suggest involvement of the gastric phase of digestion: mucosal receptors for L-glutamate (umami substances) have recently been identified in mice, rats, and the human GI tract (19, 20), and it has been suggested that luminal L-glutamate may activate these mucosal receptors or vagal nerve afferents (21). However, the primary mechanism of L-glutamate's effect on gastric emptying remains to be determined.

This report provides evidence that enrichment of dietary free L-glutamate promotes gastric emptying of a high-energy, high-protein liquid diet in humans. Although further studies of gastric emptying, as well as postprandial sensations, are necessary, our findings suggest the potential for improvements in GI dysfunction involving delayed gastric emptying. The physiologic action promoted by various amino acids must be clarified further to apply this knowledge specifically in a clinical setting.


   ACKNOWLEDGMENTS
 
We gratefully acknowledge the contributions of all of the volunteers who participated in this study. We especially thank Zen Itoh (Professor Emeritus of Gunma University) for his general supervision, technical help, and writing assistance. We are also grateful to the Ajinomoto Co, Inc (Kawasaki, Japan), for supplying us with the experimental diets and monosodium L-glutamate (MSG).

The authors' responsibilities were as follows—HZ: study design, subject recruitment, study setup, data collection, sample and data analysis, and manuscript writing; MK: study design, interpretation of data, and critical revision of the manuscript; HH, YS, AN, and MM: study setup and data collection; and OK and MM: interpretation of data and critical revision. None of the authors had any conflicts of interest.


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 SUBJECTS AND METHODS
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 DISCUSSION
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Received for publication March 19, 2008. Accepted for publication October 8, 2008.




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S. Yamamoto, M. Tomoe, K. Toyama, M. Kawai, and H. Uneyama
Can dietary supplementation of monosodium glutamate improve the health of the elderly?
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