Skip to main content

Advertisement

SpringerLink
Log in

Probiotic Compounds Enhanced Recovery after Surgery for Patients with Distal Gastric Cancer: A Prospective, Controlled Clinical Trial

  • Gastrointestinal Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Enhanced recovery after surgery (ERAS) for radical distal gastrectomy needs to be improved urgently. We investigated the effects of probiotic compounds (including Lactobacillus plantarum, L. rhamnosus, L. acidophilus, and Bifidobacterium animalis subsp.lactis) on enhance recovery after gastrectomy.

Methods

The patients in this prospective study were divided into probiotic group (PG group, n = 36) and placebo group (CG group, n = 38), taking corresponding capsule according to the protocol during the perioperative period. We compared the trends in perioperative hematologic findings and the postoperative outcomes. Patients’ feces were collected for bacterial 16S rRNA sequencing. Patients were followed up at 1 month postoperatively.

Results

After the application of probiotics, the patients’ postoperative inflammatory response level was reduced, and the trend of postoperative NLR decrease was significantly faster in the patients of the PG group than in the CG group (P = 0.047, partial η2 = 0.054). The trend of postoperative increase in serum albumin concentration in the patients of the PG group was significantly better than that in the CG group (P = 0.016, partial η2 = 0.078). In addition, patients in the PG group met discharge criteria earlier postoperatively and had fewer medical expenses. The quality of life of PG group was improved postoperatively. Postoperative inflammation-related markers, including the ratio of Firmicutes/Bacteroidetes, were increasing in untreated patients. In addition, the postoperative microbial diversity and abundance in the PG group remained stable.

Conclusions

Probiotic compounds can reduce the inflammatory response after gastrectomy and enhance the recovery of the DGC patients by maintaining the stability of the gut microbiota.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The original datasets presented in the study are publicly available. The names of the repository/repositories and accession number can be found below: https://www.ncbi.nlm.nih.gov/, PRJNA673409.

References

  1. Kim AR, Cho J, Hsu YJ, et al. Changes of quality of life in gastric cancer patients after curative resection: a longitudinal cohort study in Korea. Ann Surg. 2012;256:1008–13.

    Article  PubMed  Google Scholar 

  2. Erawijantari PP, Mizutani S, Shiroma H, et al. Influence of gastrectomy for gastric cancer treatment on faecal microbiome and metabolome profiles. Gut. 2020;69:1404–15.

    Article  CAS  PubMed  Google Scholar 

  3. Peng H, Jin L, Zhang Q, et al. Calycosin improves intestinal mucosal barrier function after gastrectomy in rats through alleviating bacterial translocation, inflammation, and oxidative stress. Evid Based Complement Alternat Med. 2022;2022:7412331.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mortensen K, Nilsson M, Slim K, et al. Consensus guidelines for enhanced recovery after gastrectomy: Enhanced Recovery After Surgery (ERAS(R)) Society recommendations. Br J Surg. 2014;101:1209–29.

    Article  CAS  PubMed  Google Scholar 

  5. Bednarski BK, Nickerson TP, You YN, et al. Randomized clinical trial of accelerated enhanced recovery after minimally invasive colorectal cancer surgery (RecoverMI trial). Br J Surg. 2019;106:1311–8.

    Article  CAS  PubMed  Google Scholar 

  6. Yamagata Y, Yoshikawa T, Yura M, et al. Current status of the “enhanced recovery after surgery” program in gastric cancer surgery. Ann Gastroenterol Surg. 2019;3:231–8.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chen Y, Chen H, Ding J, et al. Bifidobacterium longum ameliorates dextran sulfate sodium-induced colitis by producing conjugated linoleic acid, protecting intestinal mechanical barrier, restoring unbalanced gut microbiota, and regulating the toll-like receptor-4/nuclear factor-kappaB signaling pathway. J Agric Food Chem. 2021;69:14593–608.

    Article  CAS  PubMed  Google Scholar 

  8. Liu Y, Yin F, Huang L, Teng H, Shen T, Qin H. Long-term and continuous administration of Bacillus subtilis during remission effectively maintains the remission of inflammatory bowel disease by protecting intestinal integrity, regulating epithelial proliferation, and reshaping microbial structure and function. Food Funct. 2021;12:2201–10.

    Article  CAS  PubMed  Google Scholar 

  9. Davey LE, Malkus PN, Villa M, et al. A genetic system for Akkermansia muciniphila reveals a role for mucin foraging in gut colonization and host sterol biosynthesis gene expression. Nat Microbiol. 2023;8:1450–67.

    Article  CAS  PubMed  Google Scholar 

  10. Zheng C, Chen T, Wang Y, et al. A randomised trial of probiotics to reduce severity of physiological and microbial disorders induced by partial gastrectomy for patients with gastric cancer. J Cancer. 2019;10:568–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kang SH, Lee Y, Min SH, et al. Multimodal Enhanced Recovery After Surgery (ERAS) program is the optimal perioperative care in patients undergoing totally laparoscopic distal gastrectomy for gastric cancer: a prospective, randomized, clinical trial. Ann Surg Oncol. 2018;25:3231–8. https://doi.org/10.1245/s10434-018-6625-0

    Article  PubMed  Google Scholar 

  12. Fayers P, Bottomley A, Group EQoL, Quality of Life U. Quality of life research within the EORTC-the EORTC QLQ-C30. European Organisation for Research and Treatment of Cancer. Eur J Cancer. 2002;38 Suppl 4:S125–33.

  13. Vickery CW, Blazeby JM, Conroy T, et al. Development of an EORTC disease-specific quality of life module for use in patients with gastric cancer. Eur J Cancer. 2001;37:966–71.

    Article  CAS  PubMed  Google Scholar 

  14. King MT. The interpretation of scores from the EORTC quality of life questionnaire QLQ-C30. Qual Life Res. 1996;5:555–67.

    Article  CAS  PubMed  Google Scholar 

  15. Yao Y, Sun S, Gu J, et al. Roux-en-Y reconstruction alleviates radical gastrectomy-induced colitis via down-regulation of the butyrate/NLRP3 signaling pathway. EBioMedicine. 2022;86:104347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Yan Y, Wang D, Liu Y, et al. Optimal reconstruction after laparoscopic distal gastrectomy: a single-center retrospective study. Cancer Control. 2022;29:10732748221087060.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kuroda H, Saito H, Murakami Y, et al. Duration of postoperative fever as a simple and useful prognostic indicator in gastric cancer patients. Yonago Acta Med. 2021;64:282–91.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Namikawa T, Kitagawa H, Okabayashi T, Sugimoto T, Kobayashi M, Hanazaki K. Double tract reconstruction after distal gastrectomy for gastric cancer is effective in reducing reflux esophagitis and remnant gastritis with duodenal passage preservation. Langenbecks Arch Surg. 2011;396:769–76.

    Article  PubMed  Google Scholar 

  19. Tan S, Zhou F, Zhang Z, et al. Beta-1 blocker reduces inflammation and preserves intestinal barrier function after open abdominal surgery. Surgery. 2021;169:885–93.

    Article  PubMed  Google Scholar 

  20. Kouzu K, Tsujimoto H, Kishi Y, Ueno H, Shinomiya N. Bacterial translocation in gastrointestinal cancers and cancer treatment. Biomedicines. 2022;10:380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Khailova L, Baird CH, Rush AA, Barnes C, Wischmeyer PE. Lactobacillus rhamnosus GG treatment improves intestinal permeability and modulates inflammatory response and homeostasis of spleen and colon in experimental model of Pseudomonas aeruginosa pneumonia. Clin Nutr. 2017;36:1549–57.

    Article  CAS  PubMed  Google Scholar 

  22. Wang WK, Tu CY, Shao CX, et al. Impact of enhanced recovery after surgery on postoperative rehabilitation, inflammation, and immunity in gastric carcinoma patients: a randomized clinical trial. Braz J Med Biol Res. 2019;52:e8265.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Choi Y, Kim JW, Nam KH, et al. Systemic inflammation is associated with the density of immune cells in the tumor microenvironment of gastric cancer. Gastric Cancer. 2017;20:602–11.

    Article  CAS  PubMed  Google Scholar 

  24. Lu J, Xu BB, Zheng ZF, et al. CRP/prealbumin, a novel inflammatory index for predicting recurrence after radical resection in gastric cancer patients: post hoc analysis of a randomized phase III trial. Gastric Cancer. 2019;22:536–45.

    Article  CAS  PubMed  Google Scholar 

  25. Zhang Y, Tao K, Yu J, et al. Evaluation of early liquid drinking after radical gastrectomy in gastric cancer: a Chinese multicenter propensity score matching analysis. Gastroenterol Rep. 2023;11:goad029.

    Article  Google Scholar 

  26. Soeters PB, Wolfe RR, Shenkin A. Hypoalbuminemia: pathogenesis and clinical significance. JPEN J Parenter Enteral Nutr. 2019;43:181–93.

    Article  CAS  PubMed  Google Scholar 

  27. Carrera PM, Kantarjian HM, Blinder VS. The financial burden and distress of patients with cancer: understanding and stepping-up action on the financial toxicity of cancer treatment. CA Cancer J Clin. 2018;68:153–65.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kwon OK, Yu B, Park KB, Park JY, Lee SS, Chung HY. Advantages of distal subtotal gastrectomy over total gastrectomy in the quality of life of long-term gastric cancer survivors. J Gastric Cancer. 2020;20:176–89.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Zhang S, Liu R, Zhang M, et al. The predictive value of a new inflammatory-nutritional score for quality of life after laparoscopic distal gastrectomy for gastric cancer. Nutr Cancer. 2023;75:1165–76.

    Article  CAS  PubMed  Google Scholar 

  30. Maksimaityte V, Bausys A, Kryzauskas M, et al. Gastrectomy impact on the gut microbiome in patients with gastric cancer: a comprehensive review. World J Gastrointest Surg. 2021;13:678–88.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;33:496–503.

    Article  CAS  PubMed  Google Scholar 

  32. Wang MX, Lin L, Chen YD, et al. Evodiamine has therapeutic efficacy in ulcerative colitis by increasing Lactobacillus acidophilus levels and acetate production. Pharmacol Res. 2020;159:104978.

    Article  CAS  PubMed  Google Scholar 

  33. Wang K, Wang K, Wang J, Yu F, Ye C. Protective effect of Clostridium butyricum on Escherichia coli-induced endometritis in mice via ameliorating endometrial barrier and inhibiting inflammatory response. Microbiol Spectr. 2022;10:e0328622.

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

None.

Funding

This work was supported by the This research was funded by grants from National Natural Science Foundation of China (No. 81960103 to Deng XR), the Natural Science Foundation of Jiangxi province (20202ACBL206010 to Deng XR).

Author information

Author notes

  1. Huan Xiong, Zhipeng He and Yuan Wei have contributed equally to the work.

Authors and Affiliations

  1. Department of Gastrointestinal Surgery, The Second Affiliated Hospital, Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi, People’s Republic of China

    Huan Xiong MD, Zhipeng He MD, Liang Yang MMed, Xi Deng MMed, Kai Wu MMed & Xiaorong Deng MD, PhD

  2. Department of Ophthalmology, Jiangxi Province Hospital of Integrated Chinese and Western Medicine, Nanchang, Jiangxi, People’s Republic of China

    Yuan Wei MMed

  3. Department of Vascular Surgery, Tengzhou Central People’s Hospital, Tengzhou, Shandong, People’s Republic of China

    Qiang Li MMed

  4. Department of Hepatobiliary Surgery, The First Affiliated Hospital of Hunan College of Traditional Chinese Medicine, Zhuzhou, Hunan, People’s Republic of China

    Qun Xiao MMed

  5. Department of General Surgery, Yingtan 184 Hospital, Yingtan, Jiangxi, People’s Republic of China

    Keqiang Wang MMed

Authors
  1. Huan Xiong MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhipeng He MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuan Wei MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiang Li MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qun Xiao MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Liang Yang MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xi Deng MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kai Wu MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Keqiang Wang MMed
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xiaorong Deng MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

HX, KQW, and XRD designed the project. ZPH, YW, and XD participated in patient selection and data collection. LY, QL, QX, and KW performed 16S sequencing, analyzed, and interpreted the data. HX, ZPH, and YW preformed statistical analysis. HX, ZPH, and XRD wrote the manuscript. All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Keqiang Wang MMed or Xiaorong Deng MD, PhD.

Ethics declarations

Disclosure

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical Approval

The ethical approval for this study was granted by the ethics committee of the Second Affiliated Hospital of Nanchang University (No. 201801). The clinical trial was also approved for registration by the China Clinical Trial Registry (ChiCTR1900022506, www.chictr.org.cn). All procedures performed in this study were in accordance with the ethical standards of our hospital and in compliance with the Declaration of Helsinki. The patients/participants provided their written informed consent to participate in this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 192 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiong, H., He, Z., Wei, Y. et al. Probiotic Compounds Enhanced Recovery after Surgery for Patients with Distal Gastric Cancer: A Prospective, Controlled Clinical Trial. Ann Surg Oncol (2024). https://doi.org/10.1245/s10434-024-15394-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1245/s10434-024-15394-7

Search

Navigation