Case Control Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Nov 28, 2017; 23(44): 7849-7862
Published online Nov 28, 2017. doi: 10.3748/wjg.v23.i44.7849
Intestinal parameters of oxidative imbalance in celiac adults with extraintestinal manifestations
Agnieszka Piatek-Guziewicz, Agata Ptak-Belowska, Magdalena Przybylska-Felus, Pawel Pasko, Pawel Zagrodzki, Tomasz Brzozowski, Tomasz Mach, Malgorzata Zwolinska-Wcislo
Agnieszka Piatek-Guziewicz, Department of Gastroenterology and Hepatology, University Hospital, Cracow 31531, Poland
Agata Ptak-Belowska, Tomasz Brzozowski, Department of Physiology, Jagiellonian University Medical College, Cracow 31531, Poland
Magdalena Przybylska-Felus, Tomasz Mach, Malgorzata Zwolinska-Wcislo, Department of Gastroenterology, Hepatology and Infectious Diseases, Jagiellonian University Medical College, Cracow 31531, Poland
Pawel Pasko, Pawel Zagrodzki, Department of Food Chemistry and Nutrition, Jagiellonian University Medical College, Cracow 30688, Poland
Pawel Zagrodzki, Henryk Niewodniczanski Institute of Nuclear Physics, Cracow 31342, Poland
Author contributions: Piatek-Guziewicz A, Zwolinska-Wcislo M and Ptak-Belowska A designed the research; Piatek-Guziewicz A, Ptak-Belowska A, Przybylska-Felus M, Pasko P and Zagrodzki P performed the research; Ptak-Belowska A analyzed the data; Piatek-Guziewicz A and Zwolinska-Wcislo M wrote the paper; Mach T and Brzozowski T revised and edited the manuscript for final submission.
Supported by Ministry of Science and Higher Education, No. K/ZDS/003811.
Institutional review board statement: The study was reviewed and approved by the Local Ethics Committee at Jagiellonian University Medical College in Cracow, Poland (No. KBET/174/B/2013).
Informed consent statement: All study participants, or their legal guardians, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: The authors of this manuscript have no conflicts of interest to disclose.
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: Tomasz Brzozowski, MD, PhD, Professor, Department of Physiology, Jagiellonian University Medical College, 16 Grzegorzecka Street, Cracow 31-531, Poland. mpbrzozo@cyf-kr.edu.pl
Telephone: +48-12-4211006 Fax:+48-12-4222014
Received: October 11, 2017
Peer-review started: October 11, 2017
First decision: October 18, 2017
Revised: November 3, 2017
Accepted: November 14, 2017
Article in press: November 14, 2017
Published online: November 28, 2017
Processing time: 47 Days and 16.3 Hours
ARTICLE HIGHLIGHTS
Research background

Celiac disease (CD) is a common condition. The only effective treatment available is a strict life-long gluten-free diet (GFD). Untreated CD can have serious complications, such as osteoporosis or malignancy. Some patients do not report symptomatic improvement after starting treatment, and some will still have persisting symptoms after 6 to 12 mo. The literature suggests that complete normalization of duodenal lesions is exceptionally rare in adult celiac patients despite adherence to GFD.

Research motivation

There is an increasing body of evidence suggesting a relationship between oxidative stress and CD. It has been proposed that oxidative stress is one of the mechanisms responsible for gliadin toxicity and persistent oxidative imbalance may be responsible for sustained intestinal damage in CD despite GFD.

Research objectives

The assessment of the severity of oxidative stress, including the evaluation of antioxidant capacity, in patients with CD may have therapeutic implications. The indication of a proper new biomarkers useful in assessing the individual susceptibility to oxidative stress, which may help elucidate the pathogenesis of the disease and implement an appropriate treatment.

Research methods

To determine the involvement of oxidative stress in the mechanism of mucosal injury of the small intestine and to assess the effect of oxidative stress on the course of CD in adult patients with non-classic symptoms and extraintestinal manifestations, we determined the expression of IL-1β, TNF-α, IL-10, HSP-70, HIF-1α, SOD and BAX transcripts in human duodenal samples by reverse transcriptase–polymerase chain reaction.

Research results

The authors found HSP-70, HIF-1α, and BAX to be overexpressed in active CD, with varying degrees of activity in patients on GFD. This overexpression could be triggered by oxidative imbalance linked with an increase in ROS generation. We observed an increased expression of SOD mRNA in active disease, and this increase was attenuated in the treated celiac group. These results suggest that the increased expression of SOD, reflecting the severity of oxidative stress in duodenal mucosa, could be a consequence of either intestinal impairment or of oxidative imbalance.

Our results indicate that oxidative stress persists even in CD patients treated with GFD. Moreover, the results suggest that HSP-70 and HIF-1α may be potential novel biomarkers of this disease. The overexpression of HSP-70 despite dietary compliance may suggest refractory nature of CD. The increased levels of uric acid in patients with CD compared with controls resulting from oxidative stress indicates that uric acid may function as an antioxidant compound.

Further research with a greater number of participants is needed to confirm our results. Further clinical studies are needed to clarify the potential therapeutic role of uric acid as an antioxidant in CD.

Research conclusions

This study deepens the current knowledge on the role of oxidation products on the CD. By its association with intestinal damage, the course of the disease, and perhaps extraintestinal disorders, oxidative imbalance appears to be one of the major factors implicated in the pathogenesis of CD. Our observations may indicate that some markers of oxidative stress persist even in treated CD patients, but GFD partially counteracts the impairment of intestinal mucosa observed in active CD patients. Persistent oxidative imbalance may be responsible for sustained intestinal damage in adult celiac patients despite GFD. Perhaps the expression of HSP-70 could be considered as a more sensitive marker than celiac antibodies in the detection of the trace amounts of gluten in diet. Thus, HSP-70 could be considered a potential novel biomarker of this disease. Additional well-designed clinical studies are needed to clarify the potential use of uric acid (or uric acid precursors) in the diagnosis and prognosis of CD and to examine its role as a marker of oxidative stress and a potential therapeutic utility as an antioxidant. Considering that oxidative stress is involved in the molecular mechanisms of CD, additional measures aimed at reducing oxidative imbalance, such as administration of antioxidants, deserve attention as potential supplementary therapy in the treatment of CD, in addition to the rigorous GFD.

Research perspectives

Studies comparing the different assays for antioxidant capacity measurement in patients with CD are needed to select the method of choice that would best reflect susceptibility to oxidative stress in these patients. These assays might be particularly useful in clinical practice as a tool for therapy monitoring in patients with CD. It should be hypothesized that oral antioxidant supplementation may reduce the toxic effects of peptides contained in gluten on enterocytes and help alleviate histological lesions, thus exerting beneficial effects on the course of the disease. To become aware of the usefulness of nutritional genomics as a tool for targeted medical nutrition therapy, further basic research, epidemiological studies and controlled intervention trials are needed to investigate whether some nutrients such as antioxidant vitamins modulate in vivo predisposition of chronic inflammatory conditions and thus have a role in the therapy of celiac disease, in addition to the rigorous GFD.