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Anesthesia & Analgesia:
doi: 10.1213/ANE.0b013e3182a9956f
Critical Care, Trauma and Resuscitation: Research Report

The Effects on Gastric Emptying and Carbohydrate Loading of an Oral Nutritional Supplement and an Oral Rehydration Solution: A Crossover Study with Magnetic Resonance Imaging

Nakamura, Makoto MD*; Uchida, Kanji MD, PhD*; Akahane, Masaaki MD, PhD; Watanabe, Yasushi; Ohtomo, Kuni MD, PhD; Yamada, Yoshitsugu MD, PhD*

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From the Departments of *Anesthesiology and Pain Relief Center and Radiology, The University of Tokyo Hospital, Tokyo, Japan.

Accepted for publication August 13, 2013.

Published ahead of print December 31, 2013

Funding: a Grant-in-Aid for Scientific Research A from the Ministry of Education and Science (No. 23249072, YY, KU), and a Grant-in-Aid for Scientific Research B from the Ministry of Education and Science (No. 24390364,KU). A Grant for “Rare Lung Diseases” from the Ministry of Health Labour and Welfare (H24-Nanchitou [Nanchi]-Ippan-035, KU).

Conflict of Interest: See Disclosures at the end of the article.

This report was previously presented, in part, at the 32nd Annual Meeting of the Japan Society of Clinical Anesthesia.

Reprints will not be available from the authors.

Address correspondence to Kanji Uchida, MD, PhD, Department of Anesthesiology and Pain Relief Center, The University of Tokyo Hospital. 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Address e-mail to uchidak-ane@h.u-tokyo.ac.jp.

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BACKGROUND: Preoperative administration of clear fluids by mouth has recently been endorsed as a way to improve postoperative outcomes. A carbohydrate-containing beverage supplemented with electrolytes or proteins may have additional benefits for patients’ satisfaction. However, effects on gastric residual, nausea, and emesis and the effectiveness of these beverages for improving patients’ hydration status have not been well defined.

METHODS: We evaluated changes in gastric volume over time by magnetic resonance imaging, as well as blood glucose levels, before and after administration of 500 mL oral rehydration solution (ORS) containing 1.8% glucose and electrolytes in 10 healthy volunteers. The same volume of an oral nutritional supplement (ONS) containing 18% glucose and supplemental arginine (545 mOsm/kg) was given to the same population using a crossover design.

RESULTS: The mean (median, 95% confidence interval) gastric fluid volume at 1 hour after oral ingestion was 55.0 (55.3, 39.0–70.9) mL in the ORS group, whereas 409.2 (410.9, 371.4–447.0) mL in the ONS group (P = 0.0002). The gastric fluid volume of all participants in the ORS group returned to <1 mL/kg at 90 minutes after ingestion, whereas none reached <1 mL/kg at 120 minutes in the ONS group. The ONS group showed a sustained increase in the blood glucose level after ingestion (P < 0.0001 to baseline at 30, 60, 120 minutes), while the ORS group showed an initial increase (P < 0.0001, P = 0.01, P = 0.205 at each time point).

CONCLUSIONS: ORS supplemented with a small amount of glucose showed faster gastric emptying, which may make it suitable for preoperative administration. In contrast, ONS supplemented with arginine with a relatively low osmolality was associated with a longer time for gastric emptying, although it showed a sustained increase in blood glucose level.

During the past decade, based on the assumption that so-called clear fluids should be cleared from the stomach by 2 to 3 hours, several international guidelines1–4 shortened preoperative fasting periods for clear fluids from overnight (>10 hours) to 2 to 3 hours before induction of anesthesia, though neither a strict formula for clear fluids nor a maximum safe volume for preoperative administration has been determined.

Recently, preoperative administration of fluid supplemented with glucose has even been endorsed to restore dehydration, ameliorate patients’ discomfort, and reduce the incidence of postoperative insulin resistance,5–9 which should improve overall postoperative outcomes. After the announcement of the Enhanced Recovery After Surgery protocol, an additional nutritional supplement in the beverages has been preferred for preoperative use; 400 mL of a 12.5% carbohydrate-containing drink has been shown to be safe in patients undergoing major abdominal surgery.5,10–14

Glucose-supplemented oral rehydration solution (ORS) (OS-1®, Otsuka Pharmaceutical Factory, Tokushima, Japan) contains both salts and glucose, and its osmolality is similar to that of serum; it is advocated for hydration purposes, especially for dehydrated patients. The beverage is assumed to be quickly eliminated from the stomach and is preferable for preoperative hydration for patients undergoing surgery. ORS is reported to be safe for preoperative use in the low-risk Japanese surgical population,15 although the precise performance of ingested beverages in vivo has not been reported.

An arginine-containing oral nutritional supplement (ONS) (Arginaid Water®, Nestle Health Science Company, Tokyo, Japan) is a clear fluid supplemented with 18% glucose, 2% protein including arginine, and 0.008% zinc, and it has an osmolality of 545 mOsm/kg. Its calorie (0.8 kcal/mL) and glucose content (18%) are sufficient to fulfill the Enhanced Recovery After Surgery protocol.16 Arginine facilitates healing from pressure ulcers17 and from surgical wounds,18 and it enhances the immunity of trauma patients.19 Serum zinc decreases after surgery,20 and zinc supplementation has been reported to be protective in an endotoxemic mouse model.21 Therefore, perioperative administration of this beverage may help patients recover faster after surgery. However, the relatively higher glucose content and additives such as arginine in the beverage might compromise gastric emptying. There has been a limited number of papers on the efficacy and safety of this beverage in terms of gastric emptying.22

Magnetic resonance imaging (MRI) creates high-resolution images that distinguish gastric liquid from air and gastric wall, allowing direct measurement of gastric volume to be determined in real time.10,23–25

In the present study, the time course changes in gastric fluid volume (GFV) were evaluated by MRI, and carbohydrate loading efficiency was evaluated by measuring blood glucose levels after the administration of either ORS or ONS to 10 healthy volunteers in a crossover design to validate the efficacy and safety of these 2 beverages for preoperative use.

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Study Design, Setting, and Ethics

The protocol for this randomized, double-blind, crossover study involving healthy volunteers was approved by the Ethics Committee of the Graduate School of Medicine, University of Tokyo (IRB#3476), and it was conducted in accordance with the Declaration of Helsinki-Ethical Principles for Medical Research Involving Human Subjects and with the Ethical Guidelines for Clinical Research issued by the Ministry of Health, Labour, and Welfare in Japan. Written, informed consent was obtained from all participants before enrollment.

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Ten healthy adult men (28–53 years), with no risk factors for delayed gastric emptying (e.g., morbidly obese, diabetes mellitus on medical treatment, past gastrointestinal disorders that required in-hospital treatment) and suitable for MRI scanning (e.g., no metal/implants in the body), were studied. A medical questionnaire was administered before recruitment to confirm the participants’ background.

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Each participant was randomized in a crossover manner to groups ONS (Arginaid Water® Nestle Healthcare Science Company, Tokyo, Japan) or ORS (OS-1®, Otsuka Pharmaceutical Factory, Tokushima, Japan) (Fig. 1). The composition of each test solution is shown in Table 1. Participants were asked to drink 500 mL either OS-1® (ORS group) or Arginaid Water® (ONS group) on 2 separate occasions >5 days apart. Participants were instructed to abstain from alcohol, caffeine, medications, and strenuous exercise after 9:00 PM of the day before examination. They were asked to avoid food after 8:00 AM (>10 hours before ingestion) and beverages after 12 noon on the day of examination (>6 hours before ingestion). The time to ingest test drinks was set at approximately 6:00 PM. Before ingestion, participants’ height, weight, and blood glucose levels were measured, followed by MRI scanning. Participants then consumed either beverage poured in paper cups in a sitting position within 3 minutes. MRI scans were done at 30, 60, 90, and 120 minutes after ingestion. Blood glucose levels were measured with the finger-prick method using Medisafe-mini® (Terumo Corporation, Tokyo, Japan) at 30, 60, and 120 minutes after ingestion.

Table 1
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MRI Studies

All MRI scans were performed on 1.5-Tesla unit (MAGNETOM Avanto, Siemens Medical Solutions, Erlangen, Germany) at the University of Tokyo Hospital by a single professional operator who did not know which beverage was ingested. Each participant was positioned supine in the unit, and a coarse scout scan was taken to locate the position of the abdominal organs. Then, the half-Fourier acquisition single-short turbo spin echo (HASTE) sequence was used to acquire T2-weighed transverse images of the stomach with the following conditions: TE 83 milliseconds, field of view 350 mm, slice width 5 mm, gap width 1.5 mm, image matrix 205 × 256. Twenty-eight slices were taken at each time point under a single breath-hold for 19.6 seconds.

All images were transferred to a personal computer in DICOM format and viewed to locate the gastric lumen and GFV. An example of a series of images throughout the abdomen from 1 participant is shown in Figure 2. The liquid content in the stomach in each slice was manually outlined as the area of interest using Osirix imaging software (Pixmeo SARL, Bernex, Switzerland) (Version 4.0, downloaded from: http://www.osirix-viewer.com) by 1 investigator blinded to the ingested beverages. The volume of gastric content was obtained by summing the volumes calculated from each slice; the area of interest in each slice was multiplied by the thickness of each slice.

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End Points and Sample Size

The primary end point of the study was the remaining GFV at 60 minutes after oral ingestion measured on MRI. Secondary end points included blood glucose at each time point.

Based on the previous report by Lobo et al.,10 the mean difference in GFV 60 minutes after oral ingestion was anticipated to be 80 mL, with a standard deviation (SD) of 50 mL, between groups ONS and ORS. Assuming an α error of 0.05 and a power of 90%, the sample size was calculated to be 10 per beverage.

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Statistical Analysis

All results are expressed as medians (interquartile range; IQR) except where noted. The Wilcoxon rank-sum test was used to compare differences of GFV at 60 minutes after ingestion between groups and blood glucose at each time point. Two-tailed P-value of 0.05 indicated significance for GFV at 60 minutes. Corrected P-value of 0.0125 was applied to indicate statistical significance for blood glucose at each time point to avoid a type I error for multiple comparisons between groups. The time course differences in blood glucose levels were compared using Dunn test with the pre-ingestion value as the control. Statistical analysis was done with JMP Pro v 9 for Macintosh (SAS Institute Inc., Cary, NC).

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All volunteers were men. The median (IQR) age, weight, height, and body mass index of the 10 volunteers were 31.5 (27.8–34.3) years, 64.5 (61–70) kg, 169.5 (166.8–174.5) cm, and 21.9 (21.1–24.9) kg/m2, respectively. No participant had underlying medical problems known to delay gastric emptying. All participants completed serial studies with 2 beverages, and no side effects were observed.

The fasting period and residual gastric volume before entering the study did not differ significantly between the groups: 6.5 (6.50–6.54) hours vs 6.5 (6.4–7.0) hours (P = 0.587), and 15 (8.3–38.2) mL vs 10.4 (6.1–23.3) mL (P = 0.4055) in the ORS and ONS group, respectively.

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After ingestion of the test drinks, the ORS group showed an immediate decrease in GFV, with less intersubject variation (Fig. 3A). GFV of all participants reached <1 mL/kg at 90 minutes (Fig. 4). In contrast, the ONS group showed varied patterns in decreasing GFV among participants (Fig. 3B). GFV did not reach <1 mL/kg at 120 minutes after ingestion in any participant (Fig. 4). The remaining GFV at 60 minutes was significantly higher (P = 0.0002) in the ONS group (410.9, 371.2–451.6 mL, 95% confidence intervals (CIs) of means (95% CI, 371.4–447.0 mL) than in the ORS group (55.3, 34.1–76.6 mL, 95% CI, 39.0–70.9 mL) (Fig. 5).

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Blood Glucose Levels

Baseline blood glucose levels before drink ingestion were 94 (85.8–103.5) mg/dL in the ORS group and 89 (79.3–100.8) in the ONS group, with no significant difference between groups (P = 0.7618). At 30 minutes after ingestion, blood glucose levels increased significantly in both groups compared with baseline (P < 0.0001). Blood glucose levels in the ORS group subsequently decreased and returned to baseline by 120 minutes (P = 0.205), whereas they remained significantly higher during the observation period in the ONS group (P < 0.0001 at 30, 60, 120 minutes). The ONS group showed significantly higher blood glucose levels than the ORS group throughout the observation period (P = 0.0009, 0.0003, 0.0002, at 30, 60, 120 minutes, respectively) (Fig. 6).

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In the present study, precise MRI-based evaluation of remaining gastric fluid contents after oral administration of ORS showed quicker emptying with small variation among participants, while the ONS group showed delayed and variable emptying. Blood glucose levels were significantly increased in both groups, with sustained elevation in the ONS group.

The rate of transfer of fluid-containing nutrients from the stomach to the duodenum is reported to be 1.5–3 kcal/min,26 and the present results of 1.9 kcal/min for the ONS group were within that range. Vist and Maughan27 reported a mean ± SE half gastric emptying time of 600 mL (approximately 8 mL/kg) of a beverage with 18.8% glucose as 64 ± 8 minutes with lower osmolality (237 mOsm/kg) and as 130 ± 18 minutes with higher osmolality (1300 mOsm/kg) for healthy men volunteers. In the present study, 6 of 10 participants cleared half of the ingested 500 mL ONS with 18% glucose and an osmolality 545 mOsm/kg between 90 and 120 minutes (Fig. 4), which indicates that the clearance of ONS used in the present study was close to the high osmolar beverage in Vist and Maughan’s report. Proteins in the ONS should stimulate intraluminal gastrin release28 and increase gastric secretion significantly,29 which may further increase GFV. Seven of 10 participants cleared >250 mL gastric content within 120 minutes, and that coincides with the carbohydrate-containing drink with the same calorie content (200 kcal).10 Therefore, we anticipated that having patients drink 250 mL ONS would be safe for preoperative use. However, 2 of 10 participants could clear up to only 160 mL ONS, and clinicians should therefore be aware of the individual variation in gastric emptying when giving ONS. There are other beverages categorized as clear fluids that have a carbohydrate content and osmolality that are similar to those of ONS used in the present study.30 It is recommended that the gastric emptying time of these beverages be individually evaluated to provide safe preoperative use.

In contrast to the ONS group, the ORS group showed faster gastric clearance. Vist and Maughan27 reported the time required to clear half of an isotonic (230 mOsm/kg) glucose solution (4%) as 17 ± 1 minutes, and ORS in the present study showed similar results. Minimal individual variation between groups supports the notion that ORS might be suitable for quick passage from the stomach to the duodenum and ileum.

In Nygren’s5 report, blood glucose increased to 162 ± 7.2 mg/dL 40 minutes after ingestion of 400 mL carbohydrate-rich drink (285 mOsm/kg, 12.0% carbohydrate = 48 g, 0.46 mg/mL sodium). The 48 g carbohydrates led to an increase in insulin sufficient to fully depress hepatic glucose production.31 In the present study, 8 of 10 volunteers in the ONS group had blood glucose levels similar to those of the carbohydrate-rich drink group in Nygren’s report. Therefore, ONS ingestion may be effective for reversing participants’ metabolic status to the fed state.

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Limitations of the Present Study

In the present study, the participants were healthy, relatively young (33 ± 7.6 years), Japanese men. Although the present results duplicate those of previous reports from Western countries, applying the present results to women,10,32,33 children, older patients, and other ethnic groups should be done with caution. Special care should also be taken with patients with other comorbidities related to delayed gastric motility.

It is important to note that one cannot simply extrapolate the present data to patients before surgery, since patients have a certain degree of anxiety that may disturb rapid fluid clearance from the stomach, although that may not affect gastric emptying time.5

Effects of circadian rhythm should also be considered since the present study was done in the evening, whereas most preoperative patients undergo anesthesia in the morning. Although gastric fluid clearance rate is reported to be unchanged between morning and evening,34 the insulin response to orally administered glucose is generally slower and delayed in the evening.35

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In conclusion, glucose-supplemented ORS showed faster gastric emptying, which may make it suitable for preoperative administration without increasing the risk of GFV. In contrast, ONS supplemented with arginine with a relatively low osmolality was associated with a longer time for gastric emptying although it showed a sustained increase in blood glucose level that may reverse patients’ metabolic status to the fed state. The use of preoperative oral fluids supplemented with glucose and protein should be tailored to each patient’s specific needs and based on the safety profile in that patient population.

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Name: Makoto Nakamura, MD.

Contribution: This author helped design and conduct the study, analyze the data, and write the manuscript.

Attestation: Makoto Nakamura has seen the original study data, reviewed the analysis of the data, approved the final manuscript, and is the author responsible for archiving the study files.

Conflicts of Interest: The author has no conflicts of interest to declare.

Name: Kanji Uchida, MD, PhD.

Contribution: This author helped design and conduct the study, analyze the data, and write the manuscript.

Attestation: Kanji Uchida has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.

Conflicts of Interest: The author has no conflicts of interest to declare.

Name: Masaaki Akahane, MD, PhD.

Contribution: This author helped design and conduct the study and write the manuscript.

Attestation: Masaaki Akahane has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.

Conflicts of Interest: The author has no conflicts of interest to declare.

Name: Yasushi Watanabe.

Contribution: This author helped design and conduct the study.

Attestation: Yasushi Watanabe has seen the original study data and approved the final manuscript.

Conflicts of Interest: The author has no conflicts of interest to declare.

Name: Kuni Ohtomo, MD, PhD.

Contribution: This author helped design the study and write the manuscript.

Attestation: Kuni Ohtomo has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.

Conflicts of Interest: Kuni Ohtomo received research funding from Otsuka Pharmaceutical Factory (Tokushima, Japan).

Name: Yoshitsugu Yamada, MD, PhD.

Contribution: This author helped design and conduct the study, analyze the data, and write the manuscript.

Attestation: Yoshitsugu Yamada has seen the original study data, reviewed the analysis of the data, and approved the final manuscript.

Conflicts of Interest: Yoshitsugu Yamada received research funding from Otsuka Pharmaceutical Factory (Tokushima, Japan) and received research funding from Nestle Health Science Company (Tokyo, Japan).

This manuscript was handled by: Steven L. Shafer, MD.

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The authors would like to thank Kenichi Shukuya and Yutaka Yatomi, MD, PhD, for their technical support and sharing their knowledge, and Drs. M. Otsuji, MD, PhD, M. Bougaki, MD, PhD, M. Muroya, MD, PhD, and M. Maekawa, MD, for their help in preparation of the project.

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