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Effect of remote ischemic preconditioning on postoperative gastrointestinal function in patients undergoing laparoscopic colorectal cancer resection

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International Journal of Colorectal Disease Aims and scope Submit manuscript

Abstract

Purpose

Patients undergoing laparoscopic colorectal cancer resection have a high incidence of postoperative gastrointestinal dysfunction (POGD). Remote ischemic preconditioning (RIPC) is an organ protection measure. The study investigated the effect of RIPC on postoperative gastrointestinal function.

Methods

In this single-center, prospective, double-blinded, randomized, parallel-controlled trial, 100 patients undergoing elective laparoscopic colorectal cancer resection were randomly assigned in a 1:1 ratio to receive RIPC or sham RIPC (control). Three cycles of 5-min ischemia/5-min reperfusion induced by a blood pressure cuff placed on the right upper arm served as RIPC stimulus. Patients were followed up continuously for 7 days after surgery. The I-FEED score was used to evaluate the patient’s gastrointestinal function after the surgery. The primary outcome of the study was the I-FEED score on POD3. Secondary outcomes include the daily I-FEED scores, the highest I-FEED score, the incidence of POGD, the changes in I-FABP and the inflammatory markers (IL-6 and TNF-α), and the time to first postoperative flatus.

Results

A total of 100 patients were enrolled in the study, of which 13 patients were excluded. Finally, 87 patients were included in the analysis, 44 patients in the RIPC group and 43 patients in the sham-RIPC group. Patients assigned to the RIPC group had a lower I-FEED score on POD3 compared with the sham-RIPC group (mean difference 0.86; 95% CI: 0.06 to 1.65; P = 0.035). And patients in the RIPC group were also associated with a lower I-FEED score on POD4 vs the sham-RIPC group (mean difference 0.81; 95% CI: 0.03 to 1.60; P = 0.043). Compared with the sham-RIPC group, the incidence of POGD within 7 days after surgery was lower in the RIPC group (P = 0.040). At T1, T2, and T3 time points, inflammatory factors and I-FABP were considerably less in the RIPC group compared to the sham-RIPC group. The time to the first flatus and the first feces was similar in both groups.

Conclusion

RIPC reduced I-FEED scores, decreased the incidence of postoperative gastrointestinal dysfunction, and lowered concentrations of I-FABP and inflammatory factors.

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Data availability

The data sets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  1. Vather R, Trivedi S, Bissett I (2013) Defining postoperative ileus: results of a systematic review and global survey. J Gastrointest Surg 17(5):962–972

    Article  PubMed  Google Scholar 

  2. Lam D, Jones O (2020) Changes to gastrointestinal function after surgery for colorectal cancer. Best Pract Res Clin Gastroenterol 48–49

  3. Iyer S, Saunders WB, Stemkowski S (2009) Economic burden of postoperative ileus associated with colectomy in the United States. J Manag Care Pharm JMCP 15(6):485–494

    Article  PubMed  Google Scholar 

  4. Alhashemi M, Fiore JF Jr, Safa N, Al Mahroos M, Mata J, Pecorelli N, Baldini G, Dendukuri N, Stein BL, Liberman AS et al (2019) Incidence and predictors of prolonged postoperative ileus after colorectal surgery in the context of an enhanced recovery pathway. Surg Endosc 33(7):2313–2322

    Article  PubMed  Google Scholar 

  5. Gianotti L, Nespoli L, Rocchetti S, Vignali A, Nespoli A, Braga M (2011) Gut oxygenation and oxidative damage during and after laparoscopic and open left-sided colon resection: a prospective, randomized, controlled clinical trial. Surg Endosc 25(6):1835–1843

    Article  PubMed  Google Scholar 

  6. Ishizaki Y, Bandai Y, Shimomura K, Abe H, Ohtomo Y, Idezuki Y (1993) Changes in splanchnic blood flow and cardiovascular effects following peritoneal insufflation of carbon dioxide. Surg Endosc 7(5):420–423

    Article  CAS  PubMed  Google Scholar 

  7. Vlug MS, Diepenhorst GM, van Koperen PJ, Renooij W, de Smet MB, Slors JF, Boermeester MA, Bemelman WA (2011) Intestinal barrier function in patients undergoing colectomy. Colorectal Dis 13(12):1432–1437

    Article  CAS  PubMed  Google Scholar 

  8. Watt SK, Hasselbalch HC, Skov V, Kjaer L, Thomassen M, Kruse TA, Burton M, Poulsen HE, Gogenur I (2020) Increased oxidative stress with substantial dysregulation of genes related to oxidative stress and DNA repair after laparoscopic colon cancer surgery. Surg Oncol 35:71–78

    Article  PubMed  Google Scholar 

  9. Li C, Li YS, Xu M, Wen SH, Yao X, Wu Y, Huang CY, Huang WQ, Liu KX (2013) Limb remote ischemic preconditioning for intestinal and pulmonary protection during elective open infrarenal abdominal aortic aneurysm repair: a randomized controlled trial. Anesthesiology 118(4):842–852

    Article  CAS  PubMed  Google Scholar 

  10. Zhou H, Yang L, Wang G, Zhang C, Fang Z, Lei G, Shi S, Li J (2019) Remote ischemic preconditioning prevents postoperative acute kidney injury after open total aortic arch replacement: a double-blind, randomized, sham-controlled trial. Anesth Analg 129(1):287–293

    Article  CAS  PubMed  Google Scholar 

  11. Garcia-de-la-Asuncion J, Bruno L, Perez-Griera J, Galan G, Morcillo A, Wins R, Garcia-Del-Olmo E, Guijarro R, Sarria B, Marti F et al (2017) Remote ischemic preconditioning decreases oxidative lung damage after pulmonary lobectomy: a single-center randomized, double-blind, controlled trial. Anesth Analg 125(2):499–506

    Article  CAS  PubMed  Google Scholar 

  12. Lang JA, Kim J (2022) Remote ischaemic preconditioning - translating cardiovascular benefits to humans. J Physiol 600(13):3053–3067

    Article  CAS  PubMed  Google Scholar 

  13. Tapuria N, Kumar Y, Habib MM, Abu Amara M, Seifalian AM, Davidson BR (2008) Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury–a review. J Surg Res 150(2):304–330

    Article  PubMed  Google Scholar 

  14. Hummitzsch L, Zitta K, Berndt R, Wong YL, Rusch R, Hess K, Wedel T, Gruenewald M, Cremer J, Steinfath M et al (2019) Remote ischemic preconditioning attenuates intestinal mucosal damage: insight from a rat model of ischemia-reperfusion injury. J Transl Med 17(1):136

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zitta K, Meybohm P, Bein B, Heinrich C, Renner J, Cremer J, Steinfath M, Scholz J, Albrecht M (2012) Serum from patients undergoing remote ischemic preconditioning protects cultured human intestinal cells from hypoxia-induced damage: involvement of matrixmetalloproteinase-2 and -9. Mol Med 18:29–37

    Article  CAS  PubMed  Google Scholar 

  16. Filaretova L, Komkova O, Sudalina M, Yarushkina N (2021) Non-invasive remote ischemic preconditioning may protect the gastric mucosa against ischemia-reperfusion-induced injury through involvement of glucocorticoids. Front Pharmacol 12:682643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Colak T, Turkmenoglu O, Dag A, Polat A, Comelekoglu U, Bagdatoglu O, Polat G, Kanik A, Akca T, Aydin S (2007) The effect of remote ischemic preconditioning on healing of colonic anastomoses. J Surg Res 143(2):200–205

    Article  PubMed  Google Scholar 

  18. Hausenloy DJ, Candilio L, Evans R, Ariti C, Jenkins DP, Kolvekar S, Knight R, Kunst G, Laing C, Nicholas J et al (2015) Remote ischemic preconditioning and outcomes of cardiac surgery. N Engl J Med 373(15):1408–1417

    Article  CAS  PubMed  Google Scholar 

  19. Struck R, Wittmann M, Muller S, Meybohm P, Muller A, Bagci S (2018) Effect of remote ischemic preconditioning on intestinal ischemia-reperfusion injury in adults undergoing on-pump CABG surgery: a randomized controlled pilot trial. J Cardiothorac Vasc Anesth 32(3):1243–1247

    Article  PubMed  Google Scholar 

  20. Hedrick TL, McEvoy MD, Mythen MMG, Bergamaschi R, Gupta R, Holubar SD, Senagore AJ, Gan TJ, Shaw AD, Thacker JKM et al (2018) American society for enhanced recovery and perioperative quality initiative joint consensus statement on postoperative gastrointestinal dysfunction within an enhanced recovery pathway for elective colorectal surgery. Anesth Analg 126(6):1896–1907

    Article  PubMed  Google Scholar 

  21. Alsharqawi N, Alhashemi M, Kaneva P, Baldini G, Fiore JF Jr, Feldman LS, Lee L (2020) Validity of the I-FEED score for postoperative gastrointestinal function in patients undergoing colorectal surgery. Surg Endosc 34(5):2219–2226

    Article  PubMed  Google Scholar 

  22. Peng LH, Wang WJ, Chen J, Jin JY, Min S, Qin PP (2021) Implementation of the pre-operative rehabilitation recovery protocol and its effect on the quality of recovery after colorectal surgeries. Chin Med J (Engl) 134(23):2865–2873

    Article  PubMed  Google Scholar 

  23. Schietroma M, Pessia B, Carlei F, Cecilia EM, Amicucci G (2013) Intestinal permeability, systemic endotoxemia, and bacterial translocation after open or laparoscopic resection for colon cancer: a prospective randomized study. Int J Colorectal Dis 28(12):1651–1660

    Article  PubMed  Google Scholar 

  24. Reddy BS, Gatt M, Sowdi R, MacFie J (2006) Surgical manipulation of the large intestine increases bacterial translocation in patients undergoing elective colorectal surgery. Colorectal Dis 8(7):596–600

    Article  CAS  PubMed  Google Scholar 

  25. Braga M, Vignali A, Gianotti L, Zuliani W, Radaelli G, Gruarin P, Dellabona P, Di Carlo V (2002) Laparoscopic versus open colorectal surgery: a randomized trial on short-term outcome. Ann Surg 236(6):759–766

  26. Leventi A, Argyra E, Avraamidou A, Marinis A, Asonitis S, Perrea D, Voros D, Theodoraki K (2015) Attenuation of oxidative stress by ischemic preconditioning in an experimental model of intraabdominal hypertension. J Invest Surg 28(5):253–260

    Article  PubMed  Google Scholar 

  27. Wu MY, Yiang GT, Liao WT, Tsai AP, Cheng YL, Cheng PW, Li CY, Li CJ (2018) Current mechanistic concepts in ischemia and reperfusion injury. Cell Physiol Biochem 46(4):1650–1667

    Article  CAS  PubMed  Google Scholar 

  28. Deitch EA (2012) Gut-origin sepsis: evolution of a concept. Surgeon 10(6):350–356

    Article  PubMed  PubMed Central  Google Scholar 

  29. Lenaerts K, Ceulemans LJ, Hundscheid IH, Grootjans J, Dejong CH, Olde Damink SW (2013) New insights in intestinal ischemia-reperfusion injury: implications for intestinal transplantation. Curr Opin Organ Transplant 18(3):298–303

    Article  PubMed  Google Scholar 

  30. Li G, Zhang Y, Fan Z (2021) Cellular signal transduction pathways involved in acute lung injury induced by intestinal ischemia-reperfusion. Oxid Med Cell Longev 2021:9985701

    PubMed  PubMed Central  Google Scholar 

  31. Koike Y, Li B, Ganji N, Zhu H, Miyake H, Chen Y, Lee C, Janssen Lok M, Zozaya C, Lau E et al (2020) Remote ischemic conditioning counteracts the intestinal damage of necrotizing enterocolitis by improving intestinal microcirculation. Nat Commun 11(1):4950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Evennett NJ, Petrov MS, Mittal A, Windsor JA (2009) Systematic review and pooled estimates for the diagnostic accuracy of serological markers for intestinal ischemia. World J Surg 33(7):1374–1383

    Article  PubMed  Google Scholar 

  33. Khadaroo RG, Fortis S, Salim SY, Streutker C, Churchill TA, Zhang H (2014) I-FABP as biomarker for the early diagnosis of acute mesenteric ischemia and resultant lung injury. PLoS ONE 9(12):e115242

    Article  PubMed  PubMed Central  Google Scholar 

  34. Memet O, Zhang L, Shen J (2019) Serological biomarkers for acute mesenteric ischemia. Ann Transl Med 7(16):394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kuhn KA, Manieri NA, Liu TC, Stappenbeck TS (2014) IL-6 stimulates intestinal epithelial proliferation and repair after injury. PLoS ONE 9(12):e114195

    Article  PubMed  PubMed Central  Google Scholar 

  36. Jeffery V, Goldson AJ, Dainty JR, Chieppa M, Sobolewski A (2017) IL-6 signaling regulates small intestinal crypt homeostasis. J Immunol 199(1):304–311

    Article  CAS  PubMed  Google Scholar 

  37. Li A, Xiong J, Chen Z (2012) IL-6, TNF-α, and iNOS is associated with decreased colonic contraction in rats with multiple organ dysfunction syndrome. J Surg Res 178(2):e51–e57

    Article  CAS  PubMed  Google Scholar 

  38. Wehner S, Schwarz NT, Hundsdoerfer R, Hierholzer C, Tweardy DJ, Billiar TR, Bauer AJ, Kalff JC (2005) Induction of IL-6 within the rodent intestinal muscularis after intestinal surgical stress. Surgery 137(4):436–446

    Article  PubMed  Google Scholar 

  39. Zhu P, Jiang H, Fu J, Chen W, Wang Z, Cui L (2013) Cytokine levels in abdominal exudate predict prolonged postoperative ileus following surgery for colorectal carcinoma. Oncol Lett 6(3):835–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hampson A, Raj N, Lingamanaicker V et al (2021) Serum cytokine levels as markers of paralytic ileus following robotic radical prostatectomy at different pneumoperitoneum pressures. Curr Urol 15(2):91–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Anesthesiology, The Affiliated Lianyungang Hospital of Xuzhou Medical University, No. 182 Tongguan North Road, Lianyungang , Jiangsu, 222002, China

    Mengyao Yi, Yong Wu, Meng Li, Tianyu Zhang & Ying Chen

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  1. Mengyao Yi
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  2. Yong Wu
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  3. Meng Li
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  4. Tianyu Zhang
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  5. Ying Chen
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All authors contributed to data analysis, drafting or revising the article, gave final approval of the version to be published, and agreed to be accountable for all aspects of the work.

Corresponding author

Correspondence to Ying Chen.

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Approval for this study was obtained from the ethics committee of the Affiliated Lianyungang Hospital of Xuzhou Medical University, and each patient provided written informed consent.

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The authors declare no competing interests.

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Yi, M., Wu, Y., Li, M. et al. Effect of remote ischemic preconditioning on postoperative gastrointestinal function in patients undergoing laparoscopic colorectal cancer resection. Int J Colorectal Dis 38, 68 (2023). https://doi.org/10.1007/s00384-023-04346-4

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