Effects of prebiotics on immunologic indicators and intestinal microbiota structure in perioperative colorectal cancer patients

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

study design

randomized controlled trial

Citation

PMID PubMed identifier for scientific articles.

30711862

DOI Digital object identifier for electronic documents.

10.1016/j.nut.2018.10.038

URI

Authors

Xie X, He Y, Li H, Yu D, Na L, Sun T, Zhang D, Shi X, Xia Y, Jiang T, Rong S, Yang S, Ma X, Xu G

Journal

Nutrition (Burbank, Los Angeles County, Calif.)

Year

2019

Keywords:

Colorectal cancer, Immune system, Intestinal microbiota, Operation, Prebiotics

OBJECTIVE: The aim of the present study was to investigate the effects of prebiotics (containing fructooligosaccharides, xylooligosaccharides, polydextrose, and resistant dextrin) intake on immune function and intestinal microbiota structure in perioperative patients with colorectal cancer (CRC). METHODS: A randomized, double-blind, no-treatment parallel control clinical trial involving 140 perioperative patients (90 men and 50 women, aged 40-75 y) with CRC was performed. Patients were randomly divided into two groups: an intervention group (prebiotic group, n = 70) that received prebiotic supplementation of 30 g/d for 7 d, and a control group (non-prebiotic group, n = 70) that received no prebiotic supplementation. The nutritional and immunologic indices were evaluated for both groups before and after operation and analyzed against baseline values. Moreover, fecal samples were collected from 40 patients randomly chosen from the two groups to study intestinal microbiota, which was analyzed by sequencing the V3-V4 region of 16S ribosomal DNA using the Illumina (San Diego, CA) MiSeq (PE 2 × 300 bp) platform. RESULTS: Oral intake of prebiotics produced significant effects on immunologic indices in both the preoperative and postoperative periods, but the patterns of effects were different. In the preoperative period, prebiotics increased serum levels of immunoglobulin G (IgG; P = 0.02), IgM (P = 0.00), and transferrin (P = 0.027; all P < 0.05). In the postoperative period, enhanced levels of IgG (P = 0.003), IgA (P = 0.007), suppressor/cytotoxic T cells (CD3+CD8+; P = 0.043), and total B lymphocytes (CD19+; P = 0.012) were identified in the prebiotic group (all P < 0.05). The differences in the intestinal microbiota at the phylum level were not statistically significant between the intervention and control groups (P > 0.05). At the genus level, prebiotics increased the abundance of Bifidobacterium (P = 0.017) and Enterococcus (P = 0.02; both P < 0.05) but decreased the abundance of Bacteroides (P = 0.04) in the preoperative period (all P < 0.05). In the postoperative period, the abundance of Bacteroides (P = 0.04) was decreased, but the abundance of Enterococcus (P = 0.00), Bacillus (P = 0.01), Lactococcus (P = 0.00), and Streptococcus (P = 0.037) increased in the non-prebiotic group (all P < 0.05); however, no significant change was identified in the abundance of Enterococcus (P = 0.56), Lactococcus (P = 0.07), and Streptococcus (P = 0.56) as a result of prebiotic intervention in this period (all P > 0.05). The abundance of Escherichia-Shigella was increased after prebiotic intake in the postoperative period (P = 0.014, P < 0.05). There was a notable trend of decline in the abundance of intestinal microbiota from preoperative to postoperative in the non-prebiotic group. CONCLUSIONS: Prebiotic intake is recommended to improve serum immunologic indicators in patients with CRC 7 d before operation. Prebiotics improved the abundance of four commensal microbiota containing opportunistic pathogens in patients with CRC. Surgical stress decreased the abundance of most intestinal microbiota in the intestinal tract but increased the abundance of some opportunistic pathogens and commensal microbiota. Bacteroides is a relevant bacterial species for further research on the mechanism of prebiotics.

Experiment 1

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Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): WikiWorks, LGeistlinger, Claregrieve1, Mary Bearkland, Peace Sandy, Joiejoie

Subjects

Location of subjects

China

Host species Species from which microbiome was sampled. Contact us to have more species added.

Homo sapiens

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology

Nutraceutical , Colorectal carcinoma Dietary Supplement,Food Supplementation,Nutritional supplement,Nutraceutical,nutraceutical

Group 0 name Corresponds to the control (unexposed) group for case-control studies

colorectal cancer patients who didn't take prebiotics (preoperative fecal sample)

Group 1 name Corresponds to the case (exposed) group for case-control studies

colorectal cancer patients who took prebiotics (preoperative fecal sample)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with radiologic and pathologic diagnosis of CRC (preoperatively). Patients in the intervention group (prebiotic group) received a daily oral dose of 30 g prebiotic supplement (Hangzhou Niuqu Biotech Co., Hainengbo, China) containing fructooligosaccharide (25%), xylooligosaccharide (25%), polydextrose (25%), and resistant dextrin (25%) for 7 d from hospitalization to the day before the operation.

Group 0 sample size Number of subjects in the control (unexposed) group

20

Group 1 sample size Number of subjects in the case (exposed) group

18

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)

6 months

Lab analysis

Sequencing type

16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene

V3-V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).

relative abundances

Statistical test

Mann-Whitney (Wilcoxon)

Significance threshold p-value or FDR threshold used for differential abundance testing (if any)

0.05

MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?

No

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

increased

Signature 1

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Source: Table 4; Table 3

Description: Differential microbial abundance between patients who took prebiotics and patients who did not

Abundance in Group 1: decreased abundance in colorectal cancer patients who took prebiotics (preoperative fecal sample)

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Bacteroides
Enterococcus

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Source: Table 4; Table 3

Description: Differential microbial abundance between patients who took prebiotics and patients who did not

Abundance in Group 1: increased abundance in colorectal cancer patients who took prebiotics (preoperative fecal sample)

NCBI	Quality Control	Links
Bifidobacterium

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Experiment 2

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

colorectal cancer patients non-prebiotic (preoperative)

Group 1 name Corresponds to the case (exposed) group for case-control studies

colorectal cancer patients non-prebiotic (postoperative)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with radiologic and pathologic diagnosis of CRC who underwent radical resection (post-operative samples) and did not take prebiotics pre-surgery.

Group 1 sample size Number of subjects in the case (exposed) group

20

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)

no treatment with antibiotics within 6 mo before surgery

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Signature 1

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Source: Table 5

Description: Differential microbial abundance between the pre- and postoperative timepoints in patients who did not take prebiotics

Abundance in Group 1: decreased abundance in colorectal cancer patients non-prebiotic (postoperative)

NCBI	Quality Control	Links
Bacteroides

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Signature 2

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Source: Table 5

Description: Differential microbial abundance between the pre- and postoperative timepoints in patients who did not take prebiotics

Abundance in Group 1: increased abundance in colorectal cancer patients non-prebiotic (postoperative)

NCBI	Quality Control	Links
Bacillus
Enterococcus
Lactococcus
Streptococcus

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Experiment 3

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

colorectal cancer patients who took prebiotics (preoperative fecal sample)

Group 1 name Corresponds to the case (exposed) group for case-control studies

colorectal cancer patients who took prebiotics (postoperative fecal sample)

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Patients with radiologic and pathologic diagnosis of CRC who underwent radical resection (post-operative samples) and took prebiotics pre-surgery.

Group 0 sample size Number of subjects in the control (unexposed) group

18

Group 1 sample size Number of subjects in the case (exposed) group

18

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Signature 1

EditHistoryDelete

Flag for review

Your review change was submitted

Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Source: Table 5; Figure 3

Description: Differential microbial abundance between the pre- and postoperative timepoints in patients who took prebiotics

Abundance in Group 1: increased abundance in

NCBI	Quality Control	Links
Bacillus
Bifidobacterium
Enterococcus
Escherichia/Shigella sp.

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Signature 2

EditHistoryDelete

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Reviewed Marked as Reviewed by Claregrieve1 on 2022/12/22

Curated date: 2022/09/03

Curator: Mary Bearkland

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks

Source: Table 5; Figure 3

Description: Differential microbial abundance between the pre- and postoperative timepoints in patients who took prebiotics

Abundance in Group 1: decreased abundance in

NCBI	Quality Control	Links
Bacteroides

Revision editor(s): Mary Bearkland, Claregrieve1, WikiWorks