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The impact of ischemic preconditioning on hemodynamic, biochemical and inflammatory alterations induced by intra-abdominal hypertension: an experimental study in a porcine model

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Abstract

Purpose

Intra-abdominal hypertension (IAH) has several pathophysiologic implications on human organs and systems. The aim of this experimental study was to investigate whether ischemic preconditioning (IP), namely the application of IAH for a small period of time prior to establish pneumoperitoneum, can attenuate the hemodynamic, biochemical and inflammatory alterations observed during IAH.

Methods

Twenty-four pigs were divided into three groups: group A (control group), group B (pneumoperitoneum of 30 mmHg) and group C (ischemic preconditioning, consisting of pneumoperitoneum of 25 mmHg for 15 min and subsequent pneumoperitoneum of 30 mmHg). Hemodynamic (central venous pressure, cardiac index, mean arterial pressure, heart rate, stroke volume index, systemic vascular resistance index, global end-diastolic index, intrathoracic blood index and extravascular lung water index), biochemical (serum glutamic oxaloacetic transaminase (SGOT), serum glutamic pyruvate transaminase (SGPT), alkaline phosphatase (ALP), γ-glutamyl transpeptidase (γ-GT), urea and creatinine) and inflammatory (tumour necrosis factor-α, interleukin (IL)-6, IL-10 and C-reactive protein) parameters were measured.

Results

(a) Hemodynamics: The increase of central venous pressure monitoring and heart rate and the decrease of cardiac index, mean arterial pressure, stroke volume index, global end-diastolic volume index and intrathoracic blood volume index with the establishment of pneumoperitoneum were attenuated by IP. Systemic vascular resistance index and extravascular lung water were not affected. (b) Urea significantly increased with the pneumoperitoneum. IP, however, attenuated this effect. Οther biochemical parameters (SGOT, SGPT, ALP, γ-GT and creatinine) had a similar upward trend during IAH, which was reversed with IP. (c) Inflammatory parameters: CRP was increased with pneumoperitoneum, an effect that was attenuated with the application of IP. Νo significant differences were observed for interleukins.

Conclusions

Ischemic preconditioning seems to attenuate the pathophysiologic alterations of several hemodynamic, biochemical and inflammatory parameters observed during IAH.

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References

  1. Malbrain ML, De Iaet IE (2009) Intra-abdominal hypertension: evolving concepts. Clin Chest Med 30(1):45–70

    Article  PubMed  Google Scholar 

  2. Malbrain ML, Cheatham ML, Kirkpatrick A et al (2006) Results from the international conference of experts on intra-abdominal hypertension and abdominal compartment syndrome. I. Definitions. Intensive Care Med 32:1722–1732

    Article  PubMed  Google Scholar 

  3. Papavramidis TS, Marinis AD, Pliakos I, Kesisoglou I, Papavramidou N (2011) Abdominal compartment syndrome—intra-abdominal hypertension: defining, diagnosing, and managing. J Emerg Trauma Shock 4(2):279–291

    Article  PubMed  Google Scholar 

  4. Cheatham ML, Malbrain ML, Kirkpatrick A et al (2007) Results from the international conference of experts on intra-abdominal hypertension and abdominal compartment syndrome. II. Recommenations. Intensive Care Med 33:951–962

    Article  PubMed  Google Scholar 

  5. De Waele JJ, Cheatham ML, Malbrain ML, Kirkpatrick AW, Sugrue M, Balogh Z, Ivatury R, De Keulenaer B, Kimball EJ (2009) Recommendations for research from the International Conference of Experts on Intra-abdominal Hypertension and Abdominal Compartment Syndrome. Acta Clin Belg 64(3):203–209 (May–Jun)

    PubMed  Google Scholar 

  6. De Keulenaer BL, De Waele JJ, Malbrain MLNG (2011) Nonoperative management of intra-abdominal hypertension and abdominal compartment syndrome: evolving concepts. Am Surg 77(Suppl 1):s34–s41 (8)

    PubMed  Google Scholar 

  7. Malbrain MLNG, van Mieghem N, Verbrugghe W et al (2003) PiCCO derived parameters versus ‘filling pressures’ in intra-abdominal hypertension. Intensive Care Med 29:S123–S145, Abdominal Compartment Syndrome, chapter 6, p. 99

    Article  Google Scholar 

  8. Schachtrupp A, Graf J, Tons C, Hoer J, Fackeldey V, Schumpelick V (2003) Intravascular volume depletion in a 24-hour porcine model of intra-abdominal hypertension. J Trauma 55(4):734–740

    Article  PubMed  Google Scholar 

  9. Conforto F, Giammaria A, Catoni S, Baragatti E, Brocato G, Tanga I (2006) Pneumoperitoneum influence on the cardiovascular system evaluated by the PiCCO system. Crit Care 10(Suppl 1):P331. doi:10.1186/cc4678

    Article  Google Scholar 

  10. Chaney JC, Derdak S (2002) Minimally invasive hemodynamic monitoring for the intenvisist: current and emerging technology. Crit Care Med 7(30):2338–2345

    Article  Google Scholar 

  11. Harrisson SE, Smith JE, Lambert AW, Midwinter MJ (2008) Abdominal compartment syndrome: an emergency department perspective. Emerg Med J 25(3):128–132

    Article  PubMed  CAS  Google Scholar 

  12. Vegar-Brozovic V, Brezak J, Brozovic I (2008) Intra-abdominal hypertension: pulmonary and cerebral complications. Transplant Proc 40(4):1190–1192

    Article  PubMed  CAS  Google Scholar 

  13. Lingegowda V, Ejaz AA, Sood P (2009) Normotensive ischemic acute kidney injury as a manifestation of intra-abdominal hypertension. Int Urol Nephrol 41(4):1043–1045

    Article  PubMed  CAS  Google Scholar 

  14. De Waele JJ, De Laet I (2007) Intra-abdominal hypertension and the effect on renal function. Acta Clin Belg Suppl 2:371–374

    PubMed  Google Scholar 

  15. Marinis A, Argyra E, Lykoudis P, Brestas P, Theodoraki K, Polymeneas G, Boviatsis E, Voros D (2010) Ischemia as a possible effect of increased intra-abdominal pressure on central nervous system cytokines, lactate and perfusion pressures. Crit Care 14(2):R31

    Article  PubMed  Google Scholar 

  16. Diebel LN, Dulchavsky SA, Wilson RF (1992) Effect of increased intra-abdominal pressure on mesenteric arterial and intestinal mucosal blood flow. J Trauma 33:45–49

    Article  PubMed  CAS  Google Scholar 

  17. Bongard F, Pianim N, Dubecz S, Klein SR (1995) Adverse consequences of increased intra-abdominal pressure on bowel tissue oxygen. J Trauma 39:519–525

    Article  PubMed  CAS  Google Scholar 

  18. De Laet IE, Malbrain M (2007) Current insights in intra-abdominal hypertension and abdominal compartment syndrome. Med Intensiva 31:88–99

    Article  PubMed  Google Scholar 

  19. Diebel LN, Wilson RF, Dulchavsky SA et al (1992) Effect of increased intra-abdominal pressure on hepatic arterial, portal venous, and hepatic microcirculatory blood flow. J Trauma 33:279–282

    Article  PubMed  CAS  Google Scholar 

  20. Rezende-Neto JB, Moore EE, Melo de Andrade MV, Teixeira MM, Lisboa FA, Arantes RM, de Souza DG, da Cunha-Melo JR (2002) Systemic inflammatory response secondary to abdominal compartment syndrome: stage for multiple organ failure. J Trauma 53(6):1121–1128

    Article  PubMed  Google Scholar 

  21. Jerome SN, Akimitsu T, Gute DC, Korthuis RJ (1995) Ischemic preconditioning attenuates capillary no-reflow induced by prolonged ischemia and reperfusion. Am J Physiol 268(5pt 2):H2063–H2067

    PubMed  CAS  Google Scholar 

  22. Grisham MB, Granger DN, Lefer DL (1998) Modulation of leukocyte–endothelial interactions by reactive metabolites of oxygen and nitrogen: relevance to ischemic heart disease. Free Rad Biol 25:404–433

    Article  CAS  Google Scholar 

  23. Livingston DH, Mosenthal AC, Deitch EA (1995) Sepsis and multiple organ dysfunction syndrome: a clinical–mechanistic overview. New Horizon 3:257–266

    CAS  Google Scholar 

  24. Xiao F, Eppihimer MJ, Young JA, Nguyen K, Carden DL (1997) Lung neutrophil retention and injury following intestinal ischemia–reperfusion. Microcirculation 4:359–367

    Article  PubMed  CAS  Google Scholar 

  25. Granger DN, Korthuis RJ (1995) Physiologic mechanisms of postischemic tissue injury. Annu Rev Physiol 57:311–332

    Article  PubMed  CAS  Google Scholar 

  26. Granger DN (1988) Role of xanthine oxidase and granulocytes in ischemia–reperfusion injury. Am J Physiol 255:H1269–H1275

    PubMed  CAS  Google Scholar 

  27. Murray JF, Matthay MA, Luce JM, Fick MR (1988) An expanded definition of the adult respiratory distress syndrome. Am Rev Respir Dis 138:720–723

    PubMed  CAS  Google Scholar 

  28. Chun-Fai L, Juergen R, Morella KK, Jurlander J, Hawley TS, Carson WE, Kordula T, Caligiuri MA, Hawley RG, Fey GH, Baumann H (1996) Receptors for interleukin (IL)-10 and IL-6-type cytokines use similar signaling mechanisms for inducing transcription through IL-6 response elements. J Biol Chem 271(24):13968–13975. doi:10.1074/jbc.271.24.13968

    Article  Google Scholar 

  29. Müller C, Drüge G, Eichelbrönner O, Roewer N (2000) Are IL-6, IL-10 and PCT plasma concentrations more reliable than APACHE-III or SAPS-II for the individual mortality risk prediction in severe sepsis? Crit Care 4(Suppl 1):64

    Article  Google Scholar 

  30. Sahin DA, Haliloglu B, Sahin FK, Akbulut G, Fidan H, Koken G, Buyukbas S, Aktepe F, Arikan Y, Dilek ON (2007) Stepwise rising CO2 insufflation as an ischemic preconditioning method. J Laparoendosc Adv Surg Tech A 17(6):723–729

    Article  PubMed  Google Scholar 

  31. Altindis M, Yilmaz S, Polat C, Serteser M (2004) Sequential periods of preconditioning decrease laparoscopy-related elevations in hepatic TNF-alpha and IL-6 levels in rats. J Laparoendosc Adv Surg Tech A 14(6):380–383

    PubMed  Google Scholar 

  32. Yilmaz S, Koken T, Tokyol C, Kahraman A, Akbulut G, Serteser M, Polat C, Gokce C, Gokce O (2003) Can preconditioning reduce laparoscopy-induced tissue injury? Surg Endosc 17(5):819–824

    Article  PubMed  CAS  Google Scholar 

  33. Cevrioglu AS, Yilmaz S, Koken T, Tokyol C, Yilmazer M, Fenjci IV (2004) Comparison of the effects of low intra-abdominal pressure and ischemic preconditioning on the generation of oxidative stress markers and inflammatory cytokines during laparoscopy in rats. Hum Reprod 19(9):2144–2151

    Article  PubMed  Google Scholar 

  34. Eleftheriadis E, Kotzampassi K, Botsios D, Tzartinoglou E, Farmakis H, Dadoukis J (1996) Splanchnic ischaemia during laparoscopic cholecystectomy. Surg Endosc 10:324–326

    Article  PubMed  CAS  Google Scholar 

  35. Kirsch AJ, Hensle TW, Chang DT (1994) Renal effects of CO2 insufflation: oliguria and acute renal dysfunction in a rat model. Urology 43:453–459

    Article  PubMed  CAS  Google Scholar 

  36. Richter S, Olinger A, Hildebrandt U, Menger MD, Vollmar B (2001) Loss of physiologic hepatic blood flow (hepatic arterial buffer response) during CO2-pneumoperitoneum in the rat. Anesth Analg 93:872–877

    Article  PubMed  CAS  Google Scholar 

  37. Schachtrupp A, Toens Ch, Hoer J, Klosterhalfen B, Lawong AG, Schumpelick V (2002) A 24-h pneumoperitoneum leads to multiple organ impairment in a porcine model. J Surg Res 106:37–45

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  39. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124–1136

    Article  PubMed  CAS  Google Scholar 

  40. Peralta C, Hotter G, Closa D et al (1997) Protective effect of preconditioning on the injury associated to hepatic ischemia-reperfusion in the rat: role of nitric oxide and adenosine. Hepatology 25:934–937

    Article  PubMed  CAS  Google Scholar 

  41. Bonventre JV (2002) Kidney ischemic preconditioning. Curr Opin Nephrol Hypertens 1:43–48

    Article  Google Scholar 

  42. Ogawa T, Mimura Y, Hiki N, Kanauchi H, Kaminishi M (2000) Ischaemic preconditioning ameliorates functional disturbance and impaired renal perfusion in rat ischaemia-reperfused kidneys. Clin Exp Pharmacol Physiol 27:997–1001

    Article  PubMed  CAS  Google Scholar 

  43. Mannick JA, Rodrick ML, Lederer JA (2001) The immunologic response to injury. J Am Coll Surg 193:237–244

    Article  PubMed  CAS  Google Scholar 

  44. Oberholzer A, Oberholzer C, Moldawer LL (2000) Cytokine signaling-regulation of the immune response in normal and critically ill states. Crit Care Med 28:N3–N12

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Special Account for Research of the National and Kapodistrian University of Athens.

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Correspondence to Alexandra Avraamidou.

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This study conforms to our institutional standards and is under the appropriate license of the veterinary authorities and in adherence to National and European regulations for animal studies.

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Avraamidou, A., Marinis, A., Asonitis, S. et al. The impact of ischemic preconditioning on hemodynamic, biochemical and inflammatory alterations induced by intra-abdominal hypertension: an experimental study in a porcine model. Langenbecks Arch Surg 397, 1333–1341 (2012). https://doi.org/10.1007/s00423-012-0977-x

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  • DOI: https://doi.org/10.1007/s00423-012-0977-x

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