Impact of pneumoperitoneum on intra-abdominal microcirculation blood flow: an experimental randomized controlled study of two insufflator models during transanal total mesorectal excision

An experimental randomized multi-arm trial with parallel treatment design



To compare changes in microcirculation blood flow (MCBF) between pulsatile and continuous flow insufflation.

Summary background data

Transanal total mesorectal excision (TaTME) was developed to improve the quality of the resection in rectal cancer surgery. The AirSeal IFS® insufflator facilitates the pelvic dissection, although evidence on the effects that continuous flow insufflation has on MCBF is scarce.


Thirty-two pigs were randomly assigned to undergo a two-team TaTME procedure with continuous (n = 16) or pulsatile insufflation (n = 16). Each group was stratified according to two different pressure levels in both the abdominal and the transanal fields, 10 mmHg or 14 mmHg. A generalized estimating equations (GEE) model was used.


At an intra-abdominal pressure (IAP) of 10 mmHg, continuous insufflation was associated with a significantly lower MCBF reduction in colon mucosa [13% (IQR 11;14) vs. 21% (IQR 17;24) at 60 min], colon serosa [14% (IQR 9.2;18) vs. 25% (IQR 22;30) at 60 min], jejunal mucosa [13% (IQR 11;14) vs. 20% (IQR 20;22) at 60 min], renal cortex [18% (IQR 15;20) vs. 26% (IQR 26;29) at 60 min], and renal medulla [15% (IQR 11;20) vs. 20% (IQR 19;21) at 90 min]. At an IAP of 14 mmHg, MCBF in colon mucosa decreased 23% (IQR 14;27) in the continuous group and 28% (IQR 26;31) in the pulsatile group (p = 0.034).


TaTME using continuous flow insufflation was associated with a lower MCBF reduction in colon mucosa and serosa, jejunal mucosa, renal cortex, and renal medulla compared to pulsatile insufflation.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. 1.

    Penna M, Hompes R, Arnold S et al (2017) Transanal total mesorectal excision: international registry results of the first 720 cases. Ann Surg 266(1):111–117

    PubMed  Article  Google Scholar 

  2. 2.

    Xu W, Xu Z, Cheng H et al (2016) Comparison of short-term clinical outcomes between transanal and laparoscopic total mesorectal excision for the treatment of mid and low rectal cancer: a meta-analysis. Eur J Surg Oncol 42(12):1841–1850

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Hatipoglu S, Akbulut S, Hatipoglu F, Abdullayev R (2014) Effect of laparoscopic abdominal surgery on splanchnic circulation: historical developments. World J Gastroenterol 20(48):18165–18176

    PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Goitein D, Papasavas P, Yeaney W et al (2005) Microsphere intestinal blood flow analysis during pneumoperitoneum using carbon dioxide and helium. Surg Endosc 19(4):541–545

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Williams MD, Murr PC (1993) Laparoscopic insufflation of the abdomen depresses cardiopulmonary function. Surg Endosc 7(1):12–16

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Galizia G, Prizio G, Lieto E et al (2001) Hemodynamic and pulmonary changes during open, carbon dioxide pneumoperitoneum and abdominal wall-lifting cholecystectomy. A prospective, randomized study. Surg Endosc 15(5):477–483

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Schilling MK, Redaelli C, Krahenbuhl L, Signer C, Buchler MW (1997) Splanchnic microcirculatory changes during CO2 laparoscopy. J Am Coll Surg 184(4):378–382

    CAS  PubMed  Google Scholar 

  8. 8.

    Schafer M, Sagesser H, Reichen J, Krahenbuhl L (2001) Alterations in hemodynamics and hepatic and splanchnic circulation during laparoscopy in rats. Surg Endosc 15(10):1197–1201

    CAS  PubMed  Article  Google Scholar 

  9. 9.

    Sammour T, Mittal A, Loveday BP et al (2009) Systematic review of oxidative stress associated with pneumoperitoneum. Br J Surg 96(8):836–850

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Bickel A, Drobot A, Aviram M, Eitan A (2007) Validation and reduction of the oxidative stress following laparoscopic operations: a prospective randomized controlled study. Ann Surg 246(1):31–35

    PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Bislenghi G, Wolthuis AM, de Buck van Overstraeten A, D’Hoore A (2015) AirSeal system insufflator to maintain a stable pneumorectum during TAMIS. Techn Coloproctol 19(1):43–45

    CAS  Article  Google Scholar 

  12. 12.

    Nepple KG, Kallogjeri D, Bhayani SB (2013) Benchtop evaluation of pressure barrier insufflator and standard insufflator systems. Surg Endosc 27(1):333–338

    PubMed  Article  Google Scholar 

  13. 13.

    Parraga Ros E, Correa-Martin L, Sanchez-Margallo FM et al (2018) Intestinal histopathological changes in a porcine model of pneumoperitoneum-induced intra-abdominal hypertension. Surg Endosc 32(9):3989–4002

    PubMed  Article  Google Scholar 

  14. 14.

    Hodeige D, de Pauw M, Eechaute W, Weyne J, Heyndrickx GR (1999) On the validity of blood flow measurement using colored microspheres. Am J Physiol 276(4 Pt 2):H1150–H1158

    CAS  PubMed  Google Scholar 

  15. 15.

    Hofer CK, Furrer L, Matter-Ensner S et al (2005) Volumetric preload measurement by thermodilution: a comparison with transoesophageal echocardiography. Br J Anaesth 94(6):748–755

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Strang CM, Hachenberg T, Freden F, Hedenstierna G (2009) Development of atelectasis and arterial to end-tidal PCO2-difference in a porcine model of pneumoperitoneum. Br J Anaesth 103(2):298–303

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Carlson BE, Arciero JC, Secomb TW (2008) Theoretical model of blood flow autoregulation: roles of myogenic, shear-dependent, and metabolic responses. Am J Physiol Heart Circ Physiol 295(4):H1572–H1579

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    de Wit C, Jahrbeck B, Schafer C, Bolz SS, Pohl U (1998) Nitric oxide opposes myogenic pressure responses predominantly in large arterioles in vivo. Hypertension 31(3):787–794

    PubMed  Article  Google Scholar 

  19. 19.

    Demyttenaere S, Feldman LS, Fried GM (2007) Effect of pneumoperitoneum on renal perfusion and function: a systematic review. Surg Endosc 21(2):152–160

    PubMed  Article  Google Scholar 

  20. 20.

    Taura P, Lopez A, Lacy AM et al (1998) Prolonged pneumoperitoneum at 15 mmHg causes lactic acidosis. Surg Endosc 12(3):198–201

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Atkinson TM, Giraud GD, Togioka BM, Jones DB, Cigarroa JE (2017) Cardiovascular and ventilatory consequences of laparoscopic surgery. Circulation 135(7):700–710

    PubMed  Article  Google Scholar 

  22. 22.

    Adelsdorfer C, Taura P, Ibarzabal A et al (2016) Effect of transgastric natural orifice transluminal endoscopic surgery peritoneoscopy on abdominal organ microcirculation: an experimental controlled study. Gastrointest Endosc 83(2):427–433

    PubMed  Article  Google Scholar 

  23. 23.

    Herati AS, Andonian S, Rais-Bahrami S et al (2011) Use of the valveless trocar system reduces carbon dioxide absorption during laparoscopy when compared with standard trocars. Urology 77(5):1126–1132

    PubMed  Article  Google Scholar 

  24. 24.

    Sroussi J, Elies A, Rigouzzo A et al (2017) Low pressure gynecological laparoscopy (7 mmHg) with AirSeal((R)) System versus a standard insufflation (15 mmHg): a pilot study in 60 patients. J Gynecol Obstet Hum Reprod 46(2):155–158

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Annino F, Topazio L, Autieri D, Verdacchi T, De Angelis M, Asimakopoulos AD (2017) Robotic partial nephrectomy performed with Airseal versus a standard CO2 pressure pneumoperitoneum insufflator: a prospective comparative study. Surg Endosc 31(4):1583–1590

    PubMed  Article  Google Scholar 

  26. 26.

    Luketina RR, Knauer M, Kohler G et al (2014) Comparison of a standard CO(2) pressure pneumoperitoneum insufflator versus AirSeal: study protocol of a randomized controlled trial. Trials 15:239

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  27. 27.

    Taura P, Ibarzabal A, Vendrell M et al (2016) Pretreatment with endothelium-derived nitric oxide synthesis modulators on gastrointestinal microcirculation during NOTES: an experimental study. Surg Endosc 30(12):5232–5238

    PubMed  Article  Google Scholar 

  28. 28.

    Sukhotnik I, Mogilner J, Hayari L et al (2008) Effect of elevated intra-abdominal pressure and 100% oxygen on superior mesenteric artery blood flow and enterocyte turnover in a rat. Pediatr Surg Int 24(12):1347–1353

    PubMed  Article  Google Scholar 

  29. 29.

    Tytgat SH, Rijkers GT, van der Zee DC (2012) The influence of the CO(2) pneumoperitoneum on a rat model of intestinal anastomosis healing. Surg Endosc 26(6):1642–1647

    PubMed  Article  Google Scholar 

  30. 30.

    Schafer M, Krahenbuhl L (2001) Effect of laparoscopy on intra-abdominal blood flow. Surgery 129(4):385–389

    CAS  PubMed  Article  Google Scholar 

  31. 31.

    Nguyen NT, Perez RV, Fleming N, Rivers R, Wolfe BM (2002) Effect of prolonged pneumoperitoneum on intraoperative urine output during laparoscopic gastric bypass. J Am Coll Surg 195(4):476–483

    PubMed  Article  Google Scholar 

  32. 32.

    Andersson LE, Jogestrand T, Thorne A, Sollevi A, Odeberg-Wernerman S (2005) Are there changes in leg vascular resistance during laparoscopic cholecystectomy with CO2 pneumoperitoneum? Acta Anaesthesiol Scand 49(3):360–365

    CAS  PubMed  Article  Google Scholar 

  33. 33.

    Shin S, Na S, Kim OS, Choi YS, Kim SH, Oh YJ (2016) Effect of pneumoperitoneum on oxidative stress and inflammation via the arginase pathway in rats. Yonsei Med J 57(1):238–246

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Abassi Z, Bishara B, Karram T, Khatib S, Winaver J, Hoffman A (2008) Adverse effects of pneumoperitoneum on renal function: involvement of the endothelin and nitric oxide systems. Am J Physiol Regul Integr Comp Physiol 294(3):R842–R850

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Wang R, Pan Q, Kuebler WM, Li JK, Pries AR, Ning G (2017) Modeling of pulsatile flow-dependent nitric oxide regulation in a realistic microvascular network. Microvasc Res 113:40–49

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Altintas F, Tunali Y, Bozkurt P et al (2001) An experimental study on the relationship of intra-abdominal pressure and renal ischemia. Middle East J Anaesthesiol 16(1):55–66

    CAS  PubMed  Google Scholar 

  37. 37.

    Carmona M, Lopes RI, Borba M et al (2008) Comparison of the effects of carbon dioxide and helium pneumoperitoneum on renal function. J Endourol 22(5):1077–1082

    PubMed  Article  Google Scholar 

  38. 38.

    Chiu AW, Chang LS, Birkett DH, Babayan RK (1996) Changes in urinary output and electrolytes during gaseous and gasless laparoscopy. Urol Res 24(6):361–366

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Nicholson G, Knol J, Houben B, Cunningham C, Ashraf S, Hompes R (2015) Optimal dissection for transanal total mesorectal excision using modified CO2 insufflation and smoke extraction. Colorectal Dis 17(11):O265–O267

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Mosing M, Bohm SH, Rasis A et al (2018) Physiologic factors influencing the arterial-to-end-tidal CO2 difference and the alveolar dead space fraction in spontaneously breathing anesthetised horses. Front Vet Sci 5:58

    PubMed  PubMed Central  Article  Google Scholar 

Download references


The authors acknowledge Conmed Corporation for the partial support of the trial with unrestricted funds, as well as Ms. Anna Escalante, Ms. Elena Ramentol and Dr. Jacqueline van Laarhoven for their collaboration to the achievement of this work.


This trial was partially supported by unrestricted funds from Conmed Corporation, which was used for the purchase of the colored microspheres, the PICCO catheter, several anesthetic fungible material and drugs, the process of the samples and to cover the costs of the animals and incineration. Moreover, it was also used for part-time employment of the person in charge of the tissue blood flow and endothelium-derived mediators’ analysis (Anna Escalante). The design of the study, the statistical analyses and the writing of the manuscript were performed independently of these funds.

Author information




Conception and design: FBL, PT, RD, AML. Administrative support: none. Provision of study material or patients: FBL, PT, RD, AML. Collection and assembly of data: FBL, PT, MCA, JST, RB, AI, RP. Data analysis and interpretation: FBL, PT, JR, AML. Manuscript writing (including critical revising): all authors. Manuscript final approval: all authors.

Corresponding author

Correspondence to F. Borja de Lacy.

Ethics declarations

Conflict of interest

Apart from the funding previously mentioned, Dr. AM Lacy is a consultant for Medtronic, Conmed Corporation, Olympus Medical, Touchstone International Medical Science Co. Ltd., Applied Medical, and Johnson & Johnson. Dr. de Lacy, Dr. Taurà, Dr. Arroyave, Dr. Trépanier, Mr. Ríos, Dr. Bravo, Dr. Ibarzabal, Dr. Pena and Dr. Deulofeu have no other conflicts of interest or financial ties to disclose.

Ethical approval

The Institutional Review Board of the Hospital Clinic approved this trial for the Care and Use of Laboratory Animals. The University of Barcelona Committee on Ethics in Animal Experimentation and the Catalan Department of the Environment Commission on Animal Experimentation granted ethical approval for the study (Reg. 0006S/11367/2015).

Additional information

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Lacy, F.B., Taurà, P., Arroyave, M.C. et al. Impact of pneumoperitoneum on intra-abdominal microcirculation blood flow: an experimental randomized controlled study of two insufflator models during transanal total mesorectal excision. Surg Endosc 34, 4494–4503 (2020).

Download citation


  • Transanal total mesorectal excision
  • Randomized controlled trial
  • Continuous insufflation
  • Colored microspheres