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Research Article

Enhanced Intestinal Motility during Oral Glucose Tolerance Test after Laparoscopic Sleeve Gastrectomy: Preliminary Results Using Cine Magnetic Resonance Imaging

  • Vo Nguyen Trung,

    Affiliation: Department of Surgery, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Hiroshi Yamamoto mail,

    yhiroshi@belle.shiga-med.ac.jp

    Affiliation: Department of Surgery, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Akira Furukawa,

    Affiliation: Department of Radiology, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Tsuyoshi Yamaguchi,

    Affiliation: Department of Surgery, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Satoshi Murata,

    Affiliation: Department of Surgery, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Masahiro Yoshimura,

    Affiliation: Department of Radiology, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Yoko Murakami,

    Affiliation: Department of Radiology, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Shigetaka Sato,

    Affiliation: Department of Radiology, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Hideji Otani,

    Affiliation: Department of Radiology, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Satoshi Ugi,

    Affiliation: Department of Medicine Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Katsutaro Morino,

    Affiliation: Department of Medicine Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Hiroshi Maegawa,

    Affiliation: Department of Medicine Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Tohru Tani

    Affiliation: Department of Surgery, Shiga University of Medical Science, Seta-Tsukinowa-cho, Otsu, Shiga, Japan

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  • Published: June 18, 2013
  • DOI: 10.1371/journal.pone.0065739

Abstract

Background

Enhanced secretion of glucagon-like peptide-1 (GLP-1) has been suggested as a possible mechanism underlying the improvement in type 2 diabetes mellitus (T2DM) after laparoscopic sleeve gastrectomy (LSG). However, the reason for enhanced GLP-1 secretion during glucose challenge after LSG remains unclear because LSG does not include intestinal bypass. In this study, we focused on the effects of LSG on GLP-1 secretion and intestinal motility during the oral glucose tolerance test (OGTT) using cine magnetic resonance imaging (MRI) before and 3 months after LSG.

Methods

LSG was performed in 12 obese patients with a body mass index >35 kg/m2. Six patients had T2DM. OGTT was performed before and 3 months after the surgery. Body weight, hemoglobin A1c (HbA1c), and GLP-1 levels during OGTT were examined, and intestinal motility during OGTT was assessed using cine MRI.

Results

Body weight was significantly decreased after surgery in all the cases. HbA1c was markedly decreased in all the diabetic subjects. In all cases, GLP-1 secretion during OGTT was enhanced and cine MRI showed markedly increased intestinal motility at 15 and 30 min during OGTT after LSG.

Conclusions

LSG leads to accelerated intestinal motility and reduced intestinal transit time, which may be involved in the mechanism underlying enhanced GLP-1 secretion during OGTT after LSG.

Introduction

Morbid obesity is currently a worldwide health problem because it promotes the development of various diseases, including cardiovascular disease and type 2 diabetes mellitus (T2DM), which considerably increase mortality. However, current therapies, such as diet, exercise, lifestyle modification, and medication, seem to be insufficient for treating morbid obesity.

There is strong evidence that bariatric surgery can cure not only obesity but also its comorbidities. Laparoscopic sleeve gastrectomy (LSG) is typically performed before biliopancreatic diversion in the treatment of morbid obesity for high-risk patients, but LSG has recently been applied as a single-stage procedure because of its technical simplicity, remarkable postoperative weight loss, and T2DM remission [1][3].

However, the mechanism underlying the improvement in T2DM after LSG has not been elucidated until now. Enhanced secretion of glucagon-like peptide-1 (GLP-1) has been suggested to be a mechanism underlying the improvement in T2DM after LSG [4][7]. However, the reason for enhanced GLP-1 release during glucose challenge after LSG remains unclear because LSG does not include intestinal bypass as part of the technique.

A previous study with scintigraphy [8] demonstrated that gastric emptying accelerates after LSG, which may promote GLP-1 release through a neuroendocrine loop to the distal small intestine [9], [10], whereas another study did not demonstrate the same [11]. Because intestinal L cells, which secrete GLP-1, are mainly located in the distal intestine [12], studies investigating the effect of LSG on intestinal motility, including that of the distal intestine, are necessary. However, data on intestinal motility after LSG have been reported only using the scintigraphy method [13], [14]. Cine magnetic resonance imaging (MRI) is a new imaging technology that provides direct visualization of intestinal contraction and peristalsis [15]. We conducted the present study to investigate the effects of LSG on GLP-1 secretion and intestinal motility during the oral glucose tolerance test (OGTT) using cine MRI before and 3 months after LSG.

Materials and Methods

Patients

Twelve obese patients with a body mass index (BMI) >35 kg/m2 were recruited into the study. Among these, 6 patients had T2DM and 2 diabetic patients had hemoglobin A1c (HbA1c) levels >7.8%. Patients were eligible to participate in the study if they were between 20 and 65 years of age, and had a BMI between 30 and 35 kg/m2 with T2DM. Candidates were excluded if they had type 1 diabetes, severe diabetic complications, or a contradiction for either surgery. We also excluded subjects with a history of gastrointestinal motility disorders or inflammatory bowel disease. In addition to any assessments required for inclusion, each participant was assessed by a multidisciplinary team. The Ethics Review Committee of Shiga University of Medical Science (Shiga, Japan) approved all protocols described in this study, and all participants provided written informed consent.

Procedure

LSG was performed with the patient in a supine position using a standard 5-port laparoscopic technique with a 45-Fr gastric tube to calibrate the sleeve, and dissection of the greater curvature began approximately 5–6 cm from the pylorus, as described previously [16].

On the first day after surgery, the patient was administered a clear liquid diet, which progressed to a complete liquid diet for 2 weeks, followed by a soft diet for 1 week, eventually advancing to a regular diet.

Measurement of GLP-17–36 during OGTT

OGTT was performed 1 week before and 3 months after the surgery. GLP-17–36 levels during OGTT were measured using commercially available enzyme-linked immunosorbent assay kits (Linco Research Inc., St. Charles, MO, USA).

MRI Protocol

MRI examinations were performed for each patient 1 week before and 3 months after the surgery. After 8 h of fasting, MRI was performed before as well as 15 and 30 min after oral intake of 225 mL of fluid containing 75 g of glucose. Imaging was performed as reported previously [15], using a 1.5T MR scanner (Signa HDxt 1.5T; GE Healthcare, Milwaukee, WI, USA) with an 8-channel body array coil. Before real cine MRI, coronal images of the entire abdomen were obtained to determine the optimal image plane covering the maximum length of the small bowel loops. A serial coronal scan consisting of 50 images was obtained at the selected plane with the patient in a supine position in 25 s during breath holding. The steady-state free precession sequence (FIESTA sequence: TR, 3.4 ms; TE, 1.2 ms; flip angle, 75°; slice thickness, 10 mm; matrix, 256 × 256; field of view, 450 mm) was used for imaging. Intestinal motility was assessed by cine MRI on a monitor using a “cine-loop” display [15].

Based on the cine MRI, 2 bowel segments, one located in the left upper quadrant as representative of the jejunal loops and the other located in the right lower quadrant as representative of the ileal loops, were chosen for assessment of contraction. In this process, bowel loops with a degree of distension similar to the rest of the loops in the same quadrant as well as remaining in the image plane during the sequential imaging without displacement out of the image plane were chosen for assessment. Frequencies of bowel contractions were counted visually on a monitor using cine MRI. Arrival of the orally administered fluid to the jejunum, ileum, and terminal ileum was assessed within each sequence (15 and 30 min after glucose intake) by the presence or absence of bowel distension and high signal fluid. The presence or absence of distension of the jejunal and ileal loops was also judged, and contraction frequencies were compared between distended and collapsed bowel loops after surgery.

Statistical Analysis

We analyzed the data using SPSS version 17.0 software (SPSS Inc., Chicago, IL, USA) and the paired sample t-test. Data are presented as mean ± standard deviation. Area under the curves (AUCs) of GLP-17–36 during OGTT was calculated by trapezoidal integration. A p value <0.05 was considered statistically significant.

Results

Effect on Weight Loss and HbA1c

The percentage of excess weight loss (%EWL) at 3 months after the surgery was 48% ±22% (Table S1). All 6 diabetic patients discontinued all diabetic medications immediately after the surgery, and their HbA1c levels significantly decreased (Table S1).

Effect on GLP-17–36 Secretion during OGTT

In both the nondiabetic and diabetic patients, GLP-17–36 secretion during OGTT was significantly enhanced. AUC of GLP-17–36 was significantly higher after LSG than before LSG (Figure S1).

Intestinal Motility

Cine MRI scans before and 3 months after LSG were obtained in 9 of the 12 patients because of 3 patients refused examination, including 2 diabetic patients and 1 nondiabetic patient. Cine MRI was tolerated well in all 9 patients and provided sufficient quality of cine images to analyze bowel contractions and the state of small bowel transit. There was no significant difference in mean frequencies of contractions of the jejunum and ileum prior to glucose intake between before and after LSG. However, their contractions significantly increased at 15 and 30 min after glucose intake after LSG compared with those before LSG (Table S2).

The percentage of patients whose glucose fluid reached the jejunum, ileum, and ileum terminal at 15 and 30 min after fluid intake was markedly increased after LSG (Table S3). Before LSG, 33%, 11%, and 0% of patients showed the presence of fluid in the jejunum, ileum, and ileum terminal at 15 min after fluid intake, respectively. After LSG, 100%, 89%, and 89% of patients showed the presence of fluid in the jejunum, ileum, and ileum terminal, respectively. Moreover, all patients showed the presence of fluid in the jejunum, ileum, and ileum terminal at 30 min after fluid intake following LSG compared with 41%, 33%, and 22% before LSG, respectively (Table S3).

In addition, the mean frequency of contractions of fluid-distended jejunum and ileum loops (6.1/min and 7.4/min, respectively) was significantly higher than that of contractions of collapsed jejunum and ileum loops (0.5/min and 1.4/min, respectively) (Table S4).

We included video clips of 4 representative patients as a demonstration of changes in cine MRI after LSG (Table S5). The results of the remaining patients were the same.

Discussion

Our study offers novel insights into the effects of LSG on intestinal motility using the novel cine MRI method. In summary, we demonstrated that LSG enhances GLP-17–36 secretion and accelerates intestinal motility and propagation of the test fluid during OGTT.

Previous studies have shown that LSG leads to improvement in glucose tolerance, which may be explained by the decrease in insulin resistance due to weight loss [17], [18] and by the increase in insulin secretion due to enhanced GLP-1 secretion [6], [7], [19], [20]. GLP-1 is important for remission of diabetes but may not have a major role in sleeve gastrectomy, since Wilson-Perez HE showed that sleeve gastrectomy is still effective in mice lacking the GLP-1 receptor [21]. In the present study, the changes in GLP-1 secretion and intestinal motility after LSG rather than GLP-1 and its effects on the resolution of diabetes after LSG was the main focus.

To date, the reason for enhanced GLP-1 secretion after LSG still remains unclear because LSG does not include intestinal bypass. Patel RT et al. have recently depicted the role of the duodenum in promoting high levels of GLP-1 following sleeve gastrectomy [20]. In addition, several studies postulated that some implications of the accelerated gastric emptying or intestinal motility could be involved in the mechanism of increased GLP-1 secretion after LSG [8], [13], [14], [22]; however, most studies investigating gastrointestinal motility after LSG employed only scintigraphy.

Our main scope was to evaluate postoperative alterations in small intestinal motility, an area much more obscure than the stomach. There are several ways to monitor and assess small bowel motility function, such as transit time analysis [23][25], manometry [26][28], impedancometry, and tensiometry [29], [30]; however, each method has advantages and limitations, and there is no single established noninvasive method for clinical use [15]. Conventional x-ray methods such as enterography and enteroclysis may also be used to examine the small bowel [31]; however, it is not suitable for long or repetitive examinations because of radiation exposure. With recent advances in technology, MRI has been used for diagnosing various gastrointestinal disorders [32][35], and preliminary trials have reported the potential of MRI to monitor and assess bowel motility [15], [36][41]. Cine MRI using subsecond ultrafast scanning sequences presents a noninvasive method to assess bowel motility function because of the high temporal, spatial, and contrast resolution [15], [38], [41][43]. The present study is the first to investigate the potential of MRI using a steady-state free precession sequence to assess bowel motility function after LSG. The steady-state free precession sequence is a fast imaging sequence providing motion-free images with “T2-like” contrast, which has typically been used in cardiac imaging [15], [44], [45]. With technical development, steady-state free precession sequences can now provide motion-free images with high spatial resolution and temporal resolution slightly less than 0.5 s per image, which is suitable to monitor small bowel motility. Coronal imaging in the prone position is used to separate the bowel loops and to reduce the displacement of the intestinal structures in the imaging section. Consequently, cine-dynamic coronal MRI with a section thickness of 10 mm covers a large portion of the small bowel loops [15].

Thus, cine MRI can enable visualization of movement of the entire intestine in real time before and after glucose intake. Using this novel method, we showed that intestinal motility was markedly accelerated and small bowel transit time was reduced after glucose intake in all patients following LSG. This acceleration of contraction was concurrently observed with faster arrival of the intake fluid and intestinal distension. The arrival of the glucose fluid might have changed the patterns of bowel contraction from a fasting pattern to a postprandial pattern. As demonstrated by Wakamiya et al. [15], distended loops contract more frequently than collapsed loops, as was also observed in the present study.

Gastrointestinal motility is an integrated process that includes myoelectrical and contractile activities, tone, compliance, and transit [46]. These different aspects of motility are regulated by complex mechanisms involving the central nervous system, local neuronal control, and circulating neurohormonal substances [14]. Theoretically, LSG may affect gastric emptying by several mechanisms, such as removal of the fundus with its receptive and propulsive abilities, altered compliance and contractility of the narrow nondistensible sleeve [47], removal of the gastric pacemaker area from the body of the stomach, and compromise of the action of the antral pump if part of the antrum is resected. However, changes in small bowel motility are even more difficult to explain in relation to known physiological mechanisms [14]. Shortening of gastric emptying time and early arrival of the oral intake fluid to the small bowel may be important factors that stimulate intestine contractions and consequently accelerate bowel propagation, thereby leading to the early arrival of the glucose fluid at the ileum terminal. However, Melissas et al. [14] demonstrated that small bowel transit is accelerated independently after LSG and not just because of faster gastric emptying. In addition, it may seem paradoxical that increased gastrointestinal motility stimulates GLP-1 release, which has been suggested to inhibit gastrointestinal motility [12], [48]; however, this discrepancy can be explained in several ways. For example, Salehi et al. [49] distinguished between GLP-1 actions that are physiological, such as the regulation of islet hormone secretion, and others, such as gastrointestinal motility, which may only be relevant at pharmacological GLP-1 levels. In addition, vagal afferent nerves have been shown to mediate the inhibitory action of GLP-1 on gastrointestinal motility; therefore, partly compromised vagal fibers in the stomach after LSG can attenuate the effects of GLP-1 on gastrointestinal motility [50]. On the other hand, reduction in other hormone levels, including leptin and amylin, which has been observed after LSG, can be associated with enhanced gastrointestinal motility [51][54]. Finally, it is unclear if gastric emptying and intestinal motility would be even higher if not for the increased release of GLP-1 in LSG patients [1]; thus, future studies designed to assess these parameters are needed.

In agreement with previous studies [13], [14], we postulated that the acceleration in intestinal motility after LSG by itself may have enhanced the exposure of ileal L cells to the mixture of glucose fluid and digestive juices and subsequently increased GLP-1 release.

We acknowledged several limitations in the present study. As a first pilot study, we only enrolled 12 patients, and of these, only 9 underwent cine MRI. In addition, our reliance on liquid test meals appears to be the most serious limitation; thus, evaluation of gastrointestinal motility after ingestion of a solid test meal is required before our results can be generalized.

Nevertheless, for the first time, we clearly demonstrated that intestinal motility was markedly accelerated and bowel transit time reduced after LSG using a novel method.

In conclusion, LSG leads to accelerated intestinal motility and reduced intestinal transit time, which may be involved in the mechanism underlying enhanced GLP-1 secretion during OGTT after LSG. However, the exact mechanisms by which LSG affects intestinal motility remain unknown; therefore, further studies are needed to clarify this issue.

Supporting Information

Figure S1.

GLP-1 levels during OGTT before and 3 months after surgery. A: Nondiabetic patients. B: Diabetic patients. Data are presented as mean ± standard deviation. *p<0.05 and **p<0.01. GLP-1: glucagon-like peptide-1; OGTT: oral glucose tolerance test; AUC: area under the curve.

doi:10.1371/journal.pone.0065739.s001

(TIF)

Table S1.

Changes in body weight and HbA1C 3 months after surgery. T2DM: type 2 diabetes mellitus; EWL: excess weight loss; HbA1C: hemoglobin A1C. Data were shown as mean ± standard deviation

doi:10.1371/journal.pone.0065739.s002

(DOC)

Table S2.

Changes in contraction of the jejunum and ileum during OGTT 3 months after surgery. OGTT: oral glucose tolerance test. Data are presented as mean ± standard deviation.

doi:10.1371/journal.pone.0065739.s003

(DOC)

Table S3.

Changes in frequency of the presence of glucose fluid in the jejunum, ileum, and ileum terminal during OGTT 3 months after surgery. OGTT: oral glucose tolerance test.

doi:10.1371/journal.pone.0065739.s004

(DOC)

Table S4.

Differences in contraction frequencies between collapsed and fluid-distended bowel loops during OGTT 3 months after surgery. OGTT: oral glucose tolerance test. Data are presented as mean ± standard deviation.

doi:10.1371/journal.pone.0065739.s005

(DOC)

Table S5.

Representative results of intestinal motility during OGTT in 4 patients assessed by cine MRI. T2DM: type 2 diabetes mellitus; OGTT: oral glucose tolerance test; MRI: magnetic resonance imaging.

doi:10.1371/journal.pone.0065739.s006

(DOC)

Video S1.

Assessment of intestinal motility during OGTT before and 3 months after surgery in diabetic patient #1 by cine MRI. Video S1A and video S1B: at 0 and 15 min during OGTT before surgery, respectively. Video S1C and video S1D: at 0 and 15 min during OGTT after surgery, respectively. OGTT: oral glucose tolerance test; MRI: magnetic resonance imaging.

doi:10.1371/journal.pone.0065739.s007

(ZIP)

Video S2.

Assessment of intestinal motility during OGTT before and 3 months after surgery in diabetic patient #2 by cine MRI. Video S2A and video S2B: at 0 and 15 min during OGTT before surgery, respectively. Video S2C and video S2D: at 0 and 15 min during OGTT after surgery, respectively. OGTT: oral glucose tolerance test; MRI: magnetic resonance imaging.

doi:10.1371/journal.pone.0065739.s008

(ZIP)

Video S3.

Assessment of intestinal motility during OGTT before and 3 months after surgery in nondiabetic patient #3 by cine MRI. Video S3A and video S3B: at 0 and 15 min during OGTT before surgery, respectively. Video S3C and video S3D: at 0 and 15 min during OGTT after surgery, respectively. OGTT: oral glucose tolerance test; MRI: magnetic resonance imaging.

doi:10.1371/journal.pone.0065739.s009

(ZIP)

Video S4.

Assessment of intestinal motility during OGTT before and 3 months after surgery in nondiabetic patient #4 by cine MRI. Video S4A and video S4B: at 0 and 15 min during OGTT before surgery, respectively. Video S4C and video S4D: at 0 and 15 min during OGTT after surgery, respectively. OGTT: oral glucose tolerance test; MRI: magnetic resonance imaging.

doi:10.1371/journal.pone.0065739.s010

(ZIP)

Acknowledgments

A part of this work was presented by Hiroshi Yamamoto in International Federation for the Surgery of Obesity and metabolic disorders-Asian Pacific Chapter (IFSO-APC) in Rusutsu, Japan, 2011.

Author Contributions

Conceived and designed the experiments: HY AF SU. Performed the experiments: HY TY SM AF MY YM SS HO SU KM HM TT. Analyzed the data: VNT HY AF MY YM SS HO SU KM. Contributed reagents/materials/analysis tools: VNT HY AF MY YM SS HO SU HM TT. Wrote the paper: VNT HY AF SU HM TT.

References

  1. 1. Chambers AP, Jessen L, Ryan KK, Sisley S, Wilson-Perez HE, et al. (2011) Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology 141: 950–958. doi: 10.1053/j.gastro.2011.05.050
  2. 2. Chambers AP, Kirchner H, Wilson-Perez HE, Willency JA, Hale JE, et al.. (2013) The effects of vertical sleeve gastrectomy in rodents are ghrelin independent. Gastroenterology 144: 50–52 e55.
  3. 3. Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, et al. (2012) Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med 366: 1567–1576. doi: 10.1056/nejmoa1200225
  4. 4. Lee WJ, Ser KH, Chong K, Lee YC, Chen SC, et al. (2010) Laparoscopic sleeve gastrectomy for diabetes treatment in nonmorbidly obese patients: efficacy and change of insulin secretion. Surgery 147: 664–669. doi: 10.1016/j.surg.2009.10.059
  5. 5. Mingrone G, Castagneto-Gissey L (2009) Mechanisms of early improvement/resolution of type 2 diabetes after bariatric surgery. Diabetes Metab 35: 518–523. doi: 10.1016/s1262-3636(09)73459-7
  6. 6. Peterli R, Steinert RE, Woelnerhanssen B, Peters T, Christoffel-Courtin C, et al. (2012) Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg 22: 740–748. doi: 10.1007/s11695-012-0622-3
  7. 7. Peterli R, Wolnerhanssen B, Peters T, Devaux N, Kern B, et al. (2009) Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: a prospective randomized trial. Ann Surg 250: 234–241. doi: 10.1097/sla.0b013e3181ae32e3
  8. 8. Braghetto I, Davanzo C, Korn O, Csendes A, Valladares H, et al. (2009) Scintigraphic evaluation of gastric emptying in obese patients submitted to sleeve gastrectomy compared to normal subjects. Obes Surg 19: 1515–1521. doi: 10.1007/s11695-009-9954-z
  9. 9. Pilichiewicz AN, Chaikomin R, Brennan IM, Wishart JM, Rayner CK, et al. (2007) Load-dependent effects of duodenal glucose on glycemia, gastrointestinal hormones, antropyloroduodenal motility, and energy intake in healthy men. Am J Physiol Endocrinol Metab 293: E743–753. doi: 10.1152/ajpendo.00159.2007
  10. 10. Rocca AS, Brubaker PL (1999) Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion. Endocrinology 140: 1687–1694. doi: 10.1210/en.140.4.1687
  11. 11. Bernstine H, Tzioni-Yehoshua R, Groshar D, Beglaibter N, Shikora S, et al. (2009) Gastric emptying is not affected by sleeve gastrectomy–scintigraphic evaluation of gastric emptying after sleeve gastrectomy without removal of the gastric antrum. Obes Surg 19: 293–298. doi: 10.1007/s11695-008-9791-5
  12. 12. Holst JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409–1439. doi: 10.1152/physrev.00034.2006
  13. 13. Shah S, Shah P, Todkar J, Gagner M, Sonar S, et al. (2010) Prospective controlled study of effect of laparoscopic sleeve gastrectomy on small bowel transit time and gastric emptying half-time in morbidly obese patients with type 2 diabetes mellitus. Surg Obes Relat Dis 6: 152–157. doi: 10.1016/j.soard.2009.11.019
  14. 14. Melissas J, Leventi A, Klinaki I, Perisinakis K, Koukouraki S, et al.. (2012) Alterations of Global Gastrointestinal Motility After Sleeve Gastrectomy: A Prospective Study. Ann Surg In press.
  15. 15. Wakamiya M, Furukawa A, Kanasaki S, Murata K (2011) Assessment of small bowel motility function with cine-MRI using balanced steady-state free precession sequence. J Magn Reson Imaging 33: 1235–1240. doi: 10.1002/jmri.22529
  16. 16. Kasama K, Tagaya N, Kanahira E, Umezawa A, Kurosaki T, et al. (2008) Has laparoscopic bariatric surgery been accepted in Japan? The experience of a single surgeon. Obes Surg 18: 1473–1478. doi: 10.1007/s11695-008-9492-0
  17. 17. Gumbs AA, Modlin IM, Ballantyne GH (2005) Changes in insulin resistance following bariatric surgery: role of caloric restriction and weight loss. Obes Surg 15: 462–473. doi: 10.1381/0960892053723367
  18. 18. Sumithran P, Prendergast LA, Delbridge E, Purcell K, Shulkes A, et al. (2011) Long-term persistence of hormonal adaptations to weight loss. N Engl J Med 365: 1597–1604. doi: 10.1056/nejmoa1105816
  19. 19. Lee WJ, Chong K, Ser KH, Lee YC, Chen SC, et al. (2011) Gastric bypass vs sleeve gastrectomy for type 2 diabetes mellitus: a randomized controlled trial. Arch Surg 146: 143–148. doi: 10.1001/archsurg.2010.326
  20. 20. Patel RT, Shukla AP, Ahn SM, Moreira M, Rubino F (2013) Surgical control of obesity and diabetes: The role of intestinal vs gastric mechanisms in the regulation of body weight and glucose homeostasis. Obesity (Silver Spring) In press.
  21. 21. Wilson-Perez HE, Chambers AP, Ryan KK, Li B, Sandoval DA, et al.. (2013) Vertical Sleeve Gastrectomy is Effective in Two Genetic Mouse Models of Glucagon-like Peptide-1 Receptor Deficiency. Diabetes In press.
  22. 22. Michalsky D, Dvorak P, Belacek J, Kasalicky M (2013) Radical resection of the pyloric antrum and its effect on gastric emptying after sleeve gastrectomy. Obes Surg 23: 567–573. doi: 10.1007/s11695-012-0850-6
  23. 23. Cremonini F, Mullan BP, Camilleri M, Burton DD, Rank MR (2002) Performance characteristics of scintigraphic transit measurements for studies of experimental therapies. Aliment Pharmacol Ther 16: 1781–1790. doi: 10.1046/j.1365-2036.2002.01344.x
  24. 24. Iida M, Ikeda M, Kishimoto M, Tsujino T, Kaneto H, et al. (2000) Evaluation of gut motility in type II diabetes by the radiopaque marker method. J Gastroenterol Hepatol 15: 381–385. doi: 10.1046/j.1440-1746.2000.02076.x
  25. 25. Madsen JL, Larsen NE, Hilsted J, Worning H (1991) Scintigraphic determination of gastrointestinal transit times. A comparison with breath hydrogen and radiologic methods. Scand J Gastroenterol 26: 1263–1271. doi: 10.3109/00365529108998623
  26. 26. Hansen MB (2002) Small intestinal manometry. Physiol Res 51: 541–556.
  27. 27. Husebye E (1999) The patterns of small bowel motility: physiology and implications in organic disease and functional disorders. Neurogastroenterol Motil 11: 141–161. doi: 10.1046/j.1365-2982.1999.00147.x
  28. 28. Simren M, Castedal M, Svedlund J, Abrahamsson H, Bjornsson E (2000) Abnormal propagation pattern of duodenal pressure waves in the irritable bowel syndrome (IBS) [correction of (IBD)]. Dig Dis Sci 45: 2151–2161. doi: 10.1023/a:1010770302403
  29. 29. Gao C, Petersen P, Liu W, Arendt-Nielsen L, Drewes AM, et al. (2002) Sensory-motor responses to volume-controlled duodenal distension. Neurogastroenterol Motil 14: 365–374. doi: 10.1046/j.1365-2982.2002.00341.x
  30. 30. Schnoor J, Bartz S, Klosterhalfen B, Kuepper W, Rossaint R, et al. (2003) A long-term porcine model for measurement of gastrointestinal motility. Lab Anim 37: 145–154. doi: 10.1258/00236770360563796
  31. 31. Thoeni RF, Gould RG (1991) Enteroclysis and small bowel series: comparison of radiation dose and examination time. Radiology 178: 659–662.
  32. 32. Fidler JL, Guimaraes L, Einstein DM (2009) MR imaging of the small bowel. Radiographics 29: 1811–1825. doi: 10.1148/rg.296095507
  33. 33. Furukawa A, Saotome T, Yamasaki M, Maeda K, Nitta N, et al. (2004) Cross-sectional imaging in Crohn disease. Radiographics 24: 689–702. doi: 10.1148/rg.243035120
  34. 34. Savoye-Collet C, Thoumas D, Savoye G, Ducrotte P, Dacher JN (2002) Colonic transit time and MR colonography. AJR Am J Roentgenol 179: 435–436. doi: 10.2214/ajr.179.2.1790435
  35. 35. Wiarda BM, Kuipers EJ, Heitbrink MA, van Oijen A, Stoker J (2006) MR Enteroclysis of inflammatory small-bowel diseases. AJR Am J Roentgenol 187: 522–531. doi: 10.2214/ajr.05.0511
  36. 36. de Zwart IM, Mearadji B, Lamb HJ, Eilers PH, Masclee AA, et al. (2002) Gastric motility: comparison of assessment with real-time MR imaging or barostat measurement initial experience. Radiology 224: 592–597. doi: 10.1148/radiol.2242011412
  37. 37. Evans DF, Lamont G, Stehling MK, Blamire AM, Gibbs P, et al. (1993) Prolonged monitoring of the upper gastrointestinal tract using echo planar magnetic resonance imaging. Gut 34: 848–852. doi: 10.1136/gut.34.6.848
  38. 38. Froehlich JM, Patak MA, von Weymarn C, Juli CF, Zollikofer CL, et al. (2005) Small bowel motility assessment with magnetic resonance imaging. J Magn Reson Imaging 21: 370–375. doi: 10.1002/jmri.20284
  39. 39. Lauenstein TC, Vogt FM, Herborn CU, DeGreiff A, Debatin JF, et al. (2003) Time-resolved three-dimensional MR imaging of gastric emptying modified by IV administration of erythromycin. AJR Am J Roentgenol 180: 1305–1310. doi: 10.2214/ajr.180.5.1801305
  40. 40. Nishino M, Iwata S, Hayakawa K, Kanao S, Morimoto T, et al. (2005) Functional evaluation of the postoperative gastrointestinal tract using kinematic MR imaging: Quantitative assessment of peristaltic activity. Eur J Radiol 53: 263–267. doi: 10.1016/j.ejrad.2004.04.002
  41. 41. Shen SH, Guo WY, Hung JH (2007) Two-dimensional fast imaging employing steady-state acquisition (FIESTA) cine acquisition of fetal non-central nervous system abnormalities. J Magn Reson Imaging 26: 672–677. doi: 10.1002/jmri.21054
  42. 42. Ailiani AC, Neuberger T, Brasseur JG, Banco G, Wang Y, et al. (2009) Quantitative analysis of peristaltic and segmental motion in vivo in the rat small intestine using dynamic MRI. Magn Reson Med 62: 116–126. doi: 10.1002/mrm.21982
  43. 43. Froehlich JM, Daenzer M, von Weymarn C, Erturk SM, Zollikofer CL, et al. (2009) Aperistaltic effect of hyoscine N-butylbromide versus glucagon on the small bowel assessed by magnetic resonance imaging. Eur Radiol 19: 1387–1393. doi: 10.1007/s00330-008-1293-2
  44. 44. Ichikawa Y, Sakuma H, Kitagawa K, Ishida N, Takeda K, et al. (2003) Evaluation of left ventricular volumes and ejection fraction using fast steady-state cine MR imaging: comparison with left ventricular angiography. J Cardiovasc Magn Reson 5: 333–342. doi: 10.1081/jcmr-120019422
  45. 45. Slavin GS, Saranathan M (2002) FIESTA-ET: high-resolution cardiac imaging using echo-planar steady-state free precession. Magn Reson Med 48: 934–941. doi: 10.1002/mrm.10321
  46. 46. Hansen MB (2003) Neurohumoral control of gastrointestinal motility. Physiol Res 52: 1–30.
  47. 47. Yehoshua RT, Eidelman LA, Stein M, Fichman S, Mazor A, et al. (2008) Laparoscopic sleeve gastrectomy–volume and pressure assessment. Obes Surg 18: 1083–1088. doi: 10.1007/s11695-008-9576-x
  48. 48. Hellstrom PM (2010) Glucagon-like peptide-1 gastrointestinal regulatory role in metabolism and motility. Vitam Horm 84: 319–329.
  49. 49. Salehi M, Vahl TP, D’Alessio DA (2008) Regulation of islet hormone release and gastric emptying by endogenous glucagon-like peptide 1 after glucose ingestion. J Clin Endocrinol Metab 93: 4909–4916. doi: 10.1210/jc.2008-0605
  50. 50. Imeryuz N, Yegen BC, Bozkurt A, Coskun T, Villanueva-Penacarrillo ML, et al. (1997) Glucagon-like peptide-1 inhibits gastric emptying via vagal afferent-mediated central mechanisms. Am J Physiol 273: G920–927.
  51. 51. Kiely JM, Noh JH, Graewin SJ, Pitt HA, Swartz-Basile DA (2005) Altered intestinal motility in leptin-deficient obese mice. J Surg Res 124: 98–103. doi: 10.1016/j.jss.2004.10.005
  52. 52. Stefater MA, Perez-Tilve D, Chambers AP, Wilson-Perez HE, Sandoval DA, et al.. (2010) Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 138: 2426–2436, 2436 e2421–2423.
  53. 53. Dimitriadis E, Daskalakis M, Kampa M, Peppe A, Papadakis JA, et al. (2013) Alterations in gut hormones after laparoscopic sleeve gastrectomy: a prospective clinical and laboratory investigational study. Ann Surg 257: 647–654. doi: 10.1097/sla.0b013e31826e1846
  54. 54. Mayer AP, Durward A, Turner C, Skellett S, Dalton N, et al. (2002) Amylin is associated with delayed gastric emptying in critically ill children. Intensive Care Med 28: 336–340. doi: 10.1007/s00134-002-1224-7