Dietary Oat Bran Reduces Systemic Inflammation in Mice Subjected to Pelvic Irradiation

Piyush Patel, Dilip Kumar Malipatlolla, Sravani Devarakonda, Cecilia Bull, Ana Rascón, Margareta Nyman, Andrea Stringer, Valentina Tremaroli, Gunnar Steineck, Fei Sjöberg, Piyush Patel, Dilip Kumar Malipatlolla, Sravani Devarakonda, Cecilia Bull, Ana Rascón, Margareta Nyman, Andrea Stringer, Valentina Tremaroli, Gunnar Steineck, Fei Sjöberg

Abstract

Patients undergoing radiotherapy to treat pelvic-organ cancer are commonly advised to follow a restricted fiber diet. However, reducing dietary fiber may promote gastrointestinal inflammation, eventually leading to deteriorated intestinal health. The goal of this study was to evaluate the influence of dietary fiber on radiation-induced inflammation. C57BL/6J male mice were fed a High-oat bran diet (15% fiber) or a No-fiber diet (0% fiber) and were either irradiated (32 Gy delivered in four fractions) to the colorectal region or only sedated (controls). The dietary intervention started at 2 weeks before irradiation and lasted for 1, 6, and 18 weeks after irradiation, at which time points mice were sacrificed and their serum samples were assayed for 23 cytokines and chemokines. Our analyses show that irradiation increased the serum cytokine levels at all the time points analyzed. The No-fiber irradiated mice had significantly higher levels of pro-inflammatory cytokines than the High-oat irradiated mice at all time points. The results indicate that a fiber-rich oat bran diet reduces the intensity of radiation-induced inflammation, both at an early and late stage. Based on the results, it seems that the advice to follow a low-fiber diet during radiotherapy may increase the risk of decreased intestinal health in cancer survivors.

Keywords: dietary fiber; oat bran; pelvic radiotherapy; radiation-induced inflammation; serum cytokines.

Conflict of interest statement

Ana Rascón is a part-time employee of Glucanova, the provider of the bioprocessed oat bran. She is also the author of the patent for its preparation.

Figures

Figure 1
Figure 1
Experimental design. (A) Mice were fed the High-oat or No-fiber diet starting at 2 weeks before irradiation until 1, 6, and 18, weeks post-irradiation. Mice were sacrificed at 1, 6, and 18 weeks post-irradiation followed by blood sample collection. (B) Compositions of the High-oat and the No-fiber diets.
Figure 2
Figure 2
Serum cytokine and chemokine levels in mice at 1 week post-irradiation. A two-tailed Mann–Whitney test was used to compare the cytokine and chemokine levels in High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups. Data shown are average concentrations and the error bars represent SEM. * p ≤ 0.05; and ** p ≤ 0.01.
Figure 2
Figure 2
Serum cytokine and chemokine levels in mice at 1 week post-irradiation. A two-tailed Mann–Whitney test was used to compare the cytokine and chemokine levels in High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups. Data shown are average concentrations and the error bars represent SEM. * p ≤ 0.05; and ** p ≤ 0.01.
Figure 3
Figure 3
Principal component analysis (PCA), a multivariate dimensionality reduction analysis was performed on serum cytokines and chemokines levels in mice at 1 week post-irradiation. (A) PCA score scatter plot of cytokine profiles, showing discrimination between the groups. (B) PCA loading scatter plot showing the associations between the cytokines and different groups.
Figure 3
Figure 3
Principal component analysis (PCA), a multivariate dimensionality reduction analysis was performed on serum cytokines and chemokines levels in mice at 1 week post-irradiation. (A) PCA score scatter plot of cytokine profiles, showing discrimination between the groups. (B) PCA loading scatter plot showing the associations between the cytokines and different groups.
Figure 4
Figure 4
Serum cytokine and chemokine levels in mice at 6 weeks post-irradiation. A two-tailed Student’s t-test was used to compare the cytokine levels in the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups. Data shown are average concentrations and the error bars represent SEM. * p ≤ 0.05.
Figure 5
Figure 5
PCA analysis of serum cytokines and chemokines levels in mice at 6 weeks post-irradiation. (A) PCA score scatter plot of cytokine profiles, showing discrimination between the groups. (B) PCA loading scatter plot showing the associations between the cytokines and different groups.
Figure 6
Figure 6
Serum cytokine and chemokine levels in mice at 18 weeks post-irradiation. A two-tailed Mann–Whitney test was used to compare the cytokine and chemokine levels in High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups. Data shown are average concentrations and the error bars represent SEM. * p ≤ 0.05; and ** p ≤ 0.01.
Figure 6
Figure 6
Serum cytokine and chemokine levels in mice at 18 weeks post-irradiation. A two-tailed Mann–Whitney test was used to compare the cytokine and chemokine levels in High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups. Data shown are average concentrations and the error bars represent SEM. * p ≤ 0.05; and ** p ≤ 0.01.
Figure 7
Figure 7
PCA analysis of serum cytokines and chemokines levels in mice at 18 weeks post-irradiation. (A) PCA score scatter plot of cytokine profiles, showing discrimination between the groups. (B) PCA loading scatter plot showing the associations between the cytokines and different groups.
Figure 8
Figure 8
Pathway enrichment analysis. The comparison analysis was used to compare the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups, to observe the top 15 canonical pathways associated with the cytokine profiles at (A) 1, (B) 6, and (C) 18 weeks post-irradiation, ordered according to the highest activation z-score. The orange colorations indicate upregulation of the pathway and the blue colorations indicate downregulation of the pathway.
Figure 8
Figure 8
Pathway enrichment analysis. The comparison analysis was used to compare the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups, to observe the top 15 canonical pathways associated with the cytokine profiles at (A) 1, (B) 6, and (C) 18 weeks post-irradiation, ordered according to the highest activation z-score. The orange colorations indicate upregulation of the pathway and the blue colorations indicate downregulation of the pathway.
Figure 8
Figure 8
Pathway enrichment analysis. The comparison analysis was used to compare the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups, to observe the top 15 canonical pathways associated with the cytokine profiles at (A) 1, (B) 6, and (C) 18 weeks post-irradiation, ordered according to the highest activation z-score. The orange colorations indicate upregulation of the pathway and the blue colorations indicate downregulation of the pathway.
Figure 9
Figure 9
Biological function and disease enrichment analysis. The comparison analysis was used to compare the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups, to observe the top 15 biological functions or diseases associated with the cytokine profiles at (A) 1, (B) 6, and (C) 18 weeks post-irradiation, ordered according to the highest activation z-score. The orange colorations indicate activation of the functions or diseases and the blue colorations indicate inhibition of the functions or diseases.
Figure 9
Figure 9
Biological function and disease enrichment analysis. The comparison analysis was used to compare the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups, to observe the top 15 biological functions or diseases associated with the cytokine profiles at (A) 1, (B) 6, and (C) 18 weeks post-irradiation, ordered according to the highest activation z-score. The orange colorations indicate activation of the functions or diseases and the blue colorations indicate inhibition of the functions or diseases.
Figure 9
Figure 9
Biological function and disease enrichment analysis. The comparison analysis was used to compare the High-oat irr vs. High-oat cntl, No-fiber irr vs. No-fiber cntl, High-oat irr vs. No-fiber irr, and High-oat cntl vs. No-fiber cntl groups, to observe the top 15 biological functions or diseases associated with the cytokine profiles at (A) 1, (B) 6, and (C) 18 weeks post-irradiation, ordered according to the highest activation z-score. The orange colorations indicate activation of the functions or diseases and the blue colorations indicate inhibition of the functions or diseases.

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Source: PubMed

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