Case Control Study
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jan 7, 2018; 24(1): 46-57
Published online Jan 7, 2018. doi: 10.3748/wjg.v24.i1.46
Increased intestinal mucosal leptin levels in patients with diarrhea-predominant irritable bowel syndrome
De-Rong Liu, Xiao-Juan Xu, Shu-Kun Yao
De-Rong Liu, Graduate School, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing 100730, China
De-Rong Liu, Shu-Kun Yao, Department of Gastroenterology, China-Japan Friendship Hospital, Beijing 100029, China
Xiao-Juan Xu, Department of Gastroenterology, First Hospital of Shanxi Medical University, Taiyuan 030001, Shanxi Province, China
Author contributions: Liu DR performed the study, analyzed the data, and drafted the manuscript; Xu XJ contributed to study design and data interpretation; Yao SK designed the study, revised the manuscript, supervised the study performance, and obtained the funding.
Supported by National Key Technology Support Program during the “12th Five-Year Plan” Period of China, No. 2014BAI08B02.
Institutional review board statement: The study protocol was approved by the China-Japan Friendship Hospital Ethics Committee (No. 2015-33) and Conducted in Accordance with the Declaration of Helsinki.
Informed consent statement: All study participants, or their legal guardian, provided written informed consent prior to study enrollment.
Conflict-of-interest statement: All authors have no conflict of interest related to this manuscript.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Shu-Kun Yao, MD, PhD, Professor, Department of Gastroenterology, China-Japan Friendship Hospital, No. 2, Yinghua East Road, Chaoyang District, Beijing 100029, China. shukunyao@126.com
Telephone: +86-10-84205288 Fax: +86-10-84205288
Received: September 29, 2017
Peer-review started: September 30, 2017
First decision: October 17, 2017
Revised: November 8, 2017
Accepted: November 21, 2017
Article in press: November 21, 2017
Published online: January 7, 2018
Processing time: 100 Days and 15 Hours
Abstract
AIM

To measure the leptin levels in patients with diarrhea-predominant irritable bowel syndrome (IBS-D) and analyze the relationship of leptin with clinical features, visceral sensitivity, mast cells, and nerve fibers.

METHODS

Forty-two patients with IBS-D fulfilling the Rome III criteria and 20 age- and sex-matched healthy controls underwent clinical and psychological evaluations using validated questionnaires (including IBS Symptom Severity Scale, IBS-specific Quality of Life, Hamilton Anxiety Scale, and Hamilton Depression Scale), along with colonoscopy, colonic mucosal biopsy, and visceral sensitivity testing. Serum leptin levels were assayed using enzyme-linked immunosorbent assay. Mucosal leptin expression and localization were evaluated using immunohistochemistry and immunofluorescence. Mucosal leptin mRNA levels were quantified using quantitative real-time reverse transcription polymerase chain reaction. Mast cell counts and activation rates were investigated by toluidine blue staining. Correlation analyses between these parameters were performed.

RESULTS

There were no statistically significant differences in age, gender, or body mass index between the IBS-D group and the control group. The median IBS Symptom Severity Scale score in the IBS-D group was 225.0 (range, 100-475). IBS-D patients had significantly increased anxiety [IBS-D: median, 6.5; interquartile range (IQR), 3.3; control: median, 2.0; IQR, 2.0; P < 0.001] and depression (IBS-D: median, 7.0; IQR, 3.0; control: median, 3.0; IQR, 2.0; P < 0.001) scores. IBS-D patients had significantly lower first sensation threshold (IBS-D: median, 50.6; IQR, 25.9; control: median, 80.5; IQR, 18.6; P < 0.001), defecation sensation threshold (IBS-D: median, 91.5; IQR, 29.3; control: median, 155.0; IQR, 21.1; P < 0.001) and maximum tolerable threshold (IBS-D: median, 163.2; IQR, 71.2; control: median, 226.2; IQR, 39.3; P < 0.001). Mucosal leptin expression, as reflected by integrated optical density (IBS-D: median, 4424.71; IQR, 4533.63; control: median, 933.65; IQR, 888.10; P < 0.001), leptin mRNA expression (IBS-D: median, 1.1226; IQR, 1.6351; control: median, 0.8947; IQR, 0.4595; P = 0.009), and mast cell activation rate (IBS-D: median, 71.2%; IQR, 12.9%; control group: median, 59.4%; IQR, 18.88%; P < 0.001) were significantly increased in IBS-D patients. The colocalization of leptin and leptin receptors was observed on mast cells and PGP9.5-positive nerve fibers in the intestinal mucosa. Also, leptin expression was positively correlated with anxiety, depression, and the mast cell activation rate, but negatively correlated with the defecation sensation threshold and the maximum tolerance threshold during visceral sensitivity testing (adjusted P < 0.0038).

CONCLUSION

Increased levels of mucosal leptin may interact with mast cells and the nervous system to contribute to the pathogenesis of IBS-D.

Keywords: Leptin; Irritable bowel syndrome; Mast cells; Diarrhea; Visceral hypersensitivity

Core tip: Leptin is an important cytokine that exerts significant biological effects on gastrointestinal function and immune system modulation. We found that diarrhea-predominant irritable bowel syndrome (IBS-D) patients had significantly increased psychological symptoms, visceral hypersensitivity, mucosal leptin expression, leptin mRNA expression, and mast cell activation rate. Additionally, leptin expression was positively correlated with anxiety, depression, and the mast cell activation rate, but negatively correlated with the defecation sensation threshold and maximum tolerance threshold during visceral sensitivity testing. Increased levels of mucosal leptin may interact with mast cells and the nervous system to contribute to the pathogenesis of IBS-D.