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Intestinal histopathological changes in a porcine model of pneumoperitoneum-induced intra-abdominal hypertension

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Abstract

Background

Low splanchnic perfusion is an immediate effect of pneumoperitoneum-induced intra-abdominal hypertension (IAH). Anatomical structure results in the intestinal mucosa being the area most sensitive to hypoperfusion. The relationship between intestinal injury and clinical parameters of tissue perfusion [abdominal perfusion pressure (APP), gastric intramucosal pH (pHi) and lactic acid (Lc)] has not been previously studied. This study aimed to monitorize intestinal pathogenesis through sequential ileal biopsies and to measure APP, pHi, and Lc levels at different pneumoperitoneum-induced intra-abdominal pressures (20, 30, and 40 mmHg) to evaluate the potential relationships between them.

Materials and methods

Fifty pigs were divided into four groups; a control group (C) and three experimental groups with different pneumoperitoneum-induced levels [20 mmHg (G20), 30 mmHg (G30), and 40 mmHg (G40)], that were maintained for 3 and 5 h. APP, pHi, and Lc were measured and ileal biopsies taken laparoscopically every 30 min. The mucosal damage was graded using the standardized Park’s Score and animals were classified as injured (I+) or uninjured (I−).

Results

Different histopathological lesions were observed in groups G20, G30, and G40 but no damage observed in group C. A 33.3% of animals in G20 and G30 were I+ after 3 h, while 93.3% were injured in G40. After 5 h, histopathological lesions were no longer seen in some animals in G20 and only 10% were I+. Conversely, in G30 I+ pigs increased to 80% while those in G40 remained at 93.3% I+. The I+ animals had significantly lower APP and pHi than those I−. Lc was the clinical parameter that showed the earliest differences, with significantly higher figures in I+ animals.

Conclusions

The evolution of intestinal injuries from pneumoperitoneum-induced IAH depends on the degree of IAP. These damages may be associated with decreases in APP and pHi, and increases in Lc.

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References

  1. Kirkpatrick AW, Roberts DJ, De Waele J, Jaeschke R, Malbrain ML, De Keulenaer B et al (2013) Intra-abdominal hypertension and the abdominal compartment syndrome: updated consensus definitions and clinical practice guidelines from the World Society of the Abdominal Compartment Syndrome. Intensive Care Med 39(7):1190–1206

    Article  PubMed  PubMed Central  Google Scholar 

  2. Holodinsky JK, Roberts DJ, Ball CG, Blaser AR, Starkopf J, Zygun DA et al (2013) Risk factors for intra-abdominal hypertension and abdominal compartment syndrome among adult intensive care unit patients: a systematic review and meta-analysis. Crit Care 17(5):R249

    Article  PubMed  PubMed Central  Google Scholar 

  3. Malbrain M (2009) Abdominal compartment syndrome. F1000 Med Rep 1

  4. Deenichin GP (2008) Abdominal compartment syndrome. Surg Today 38(1):5–19

    Article  PubMed  Google Scholar 

  5. de Laet IE, Malbrain M (2007) Current insights in intra-abdominal hypertension and abdominal compartment syndrome. Med Intensiva 31(2):88–99

    Article  PubMed  Google Scholar 

  6. Cheatham ML, Malbrain ML (2007) Cardiovascular implications of abdominal compartment syndrome. Acta Clin Belg Suppl (1):98–112

  7. 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

    Article  PubMed  PubMed Central  Google Scholar 

  8. Diebel LN, Wilson RF, Dulchavsky SA, Saxe J (1992) Effect of increased intra-abdominal pressure on hepatic arterial, portal venous, and hepatic microcirculatory blood flow. J Trauma 33(2):279–282 (discussion 82–83)

    Article  PubMed  CAS  Google Scholar 

  9. Skoog P, Hörer T, Nilsson KF, Agren G, Norgren L, Jansson K (2015) Intra-abdominal hypertension–an experimental study of early effects on intra-abdominal metabolism. Ann Vasc Surg 29(1):128–137

    Article  PubMed  Google Scholar 

  10. Diebel LN, Dulchavsky SA, Wilson RF (1992) Effect of increased intra-abdominal pressure on mesenteric arterial and intestinal mucosal blood flow. J Trauma 33(1):45–48 (discussion 8–9)

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  12. Narváez-Sánchez R, Chuaire L, Sánchez M, Bonilla J (2004) Circulación intestinal: Su organización, control y papel en el paciente crítico. Colomb Med 35(4):231–244

    Google Scholar 

  13. Malbrain ML, Cheatham ML, Kirkpatrick A, Sugrue M, Parr M, De Waele J et al (2006) Results from the international conference of experts on intra-abdominal hypertension and abdominal compartment syndrome. I. Definitions. Intensive Care Med 32(11):1722–1732

    Article  PubMed  Google Scholar 

  14. Vollmar B, Menger MD (2011) Intestinal ischemia/reperfusion: microcirculatory pathology and functional consequences. Langenbecks Arch Surg 396(1):13–29

    Article  PubMed  Google Scholar 

  15. Takala J (1997) Determinants of splanchnic blood flow. Br J Anaesth 77:50–58

    Article  Google Scholar 

  16. Sánchez-Miralles A, Castellanos G, Badenes R, Conejero R (2013) Abdominal compartment syndrome and acute intestinal distress syndrome. Med Intensiva 37(2):99–109

    Article  PubMed  Google Scholar 

  17. Gong G, Wang P, Ding W, Zhao Y, Li J (2009) Microscopic and ultrastructural changes of the intestine in abdominal compartment syndrome. J Invest Surg 22(5):362–367

    Article  PubMed  Google Scholar 

  18. Liu D, Zhang HG, Chang MT, Li Y, Zhang LY (2015) Melanocortin-4 receptor agonists alleviate intestinal dysfunction in secondary intra-abdominal hypertension rat model. J Surg Res 195(1):263–270

    Article  PubMed  CAS  Google Scholar 

  19. Unsal MA, Imamoglu M, Kadioglu M, Aydin S, Ulku C, Kesim M et al (2006) The acute alterations in biochemistry, morphology, and contractility of rat-isolated terminal ileum via increased intra-abdominal pressure. Pharmacol Res 53(2):135–141

    Article  PubMed  CAS  Google Scholar 

  20. Correa-Martín L, Castellanos G, García-Lindo M, Díaz-Güemes I, Sánchez-Margallo FM (2013) Tonometry as a predictor of inadequate splanchnic perfusion in an intra-abdominal hypertension animal model. J Surg Res 184(2):1028–1034

    Article  PubMed  Google Scholar 

  21. Ke L, Tong ZH, Ni HB, Ding WW, Sun JK, Li WQ et al (2012) The effect of intra-abdominal hypertension incorporating severe acute pancreatitis in a porcine model. PLoS ONE 7(3):e33125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Toens C, Schachtrupp A, Hoer J, Junge K, Klosterhalfen B, Schumpelick V (2002) A porcine model of the abdominal compartment syndrome. Shock 18(4):316–321

    Article  PubMed  Google Scholar 

  23. Kaussen T, Srinivasan PK, Afify M, Herweg C, Tolba R, Conze J et al (2012) Influence of two different levels of intra-abdominal hypertension on bacterial translocation in a porcine model. Ann Intensive Care 2(Suppl 1):S17

    PubMed  PubMed Central  Google Scholar 

  24. Schachtrupp A, Toens C, 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(1):37–45

    Article  PubMed  CAS  Google Scholar 

  25. Elatroush H, Abed N, Metwaly A, Afify M, Hussien M (2015) The effect of the abdominal perfusion pressure on visceral circulation in critically ill patients with multiorgan dysfunction. Egypt J Crit Care Med 3(2–3):63–67

    Article  Google Scholar 

  26. Cheatham ML, White MW, Sagraves SG, Johnson JL, Block EF (2000) Abdominal perfusion pressure: a superior parameter in the assessment of intra-abdominal hypertension. J Trauma 49(4):621–626 (discussion 6–7)

    Article  PubMed  CAS  Google Scholar 

  27. Malbrain M (2002) Abdominal perfusion pressure as a prognostic marker in intra-abdominal hypertension. Springer, Berlin

    Google Scholar 

  28. Sugrue M, Jones F, Lee A, Buist MD, Deane S, Bauman A et al (1996) Intraabdominal pressure and gastric intramucosal pH: is there an association? World J Surg 20(8):988–991

    Article  PubMed  CAS  Google Scholar 

  29. Mäkinen MJ, Klemola UM, Yli-Hankala A (2000) Gastric air tonometry during laparoscopic cholecystectomy: a comparison of two PaCO2 levels. Can J Anesth 48:121–128

    Article  Google Scholar 

  30. Duzgun AP, Gulgez B, Ozmutlu A, Ertorul D, Bugdayci G, Akyurek N et al (2006) The relationship between intestinal hypoperfusion and serum d-lactate levels during experimental intra-abdominal hypertension. Dig Dis Sci 51(12):2400–2403

    Article  PubMed  CAS  Google Scholar 

  31. Nielsen C, Kirkegård J, Erlandsen EJ, Lindholt JS, Mortensen FV (2015) D-lactate is a valid biomarker of intestinal ischemia induced by abdominal compartment syndrome. J Surg Res 194(2):400–404

    Article  PubMed  CAS  Google Scholar 

  32. Malbrain ML, Viaene D, Kortgen A, De Laet I, Dits H, Van Regenmortel N et al (2012) Relationship between intra-abdominal pressure and indocyanine green plasma disappearance rate: hepatic perfusion may be impaired in critically ill patients with intra-abdominal hypertension. Ann Intensive Care 2(Suppl 1):S19

    Article  PubMed  PubMed Central  Google Scholar 

  33. Inal MT, Memis D, Sezer YA, Atalay M, Karakoc A, Sut N (2011) Effects of intra-abdominal pressure on liver function assessed with the LiMON in critically ill patients. Can J Surg 54(3):161–166

    Article  PubMed  PubMed Central  Google Scholar 

  34. Lee RK (2012) Intra-abdominal hypertension and abdominal compartment syndrome: a comprehensive overview. Crit Care Nurse 32(1):19–31

    Article  PubMed  Google Scholar 

  35. Correa-Martín L, Castellanos G, García M, Sánchez-Margallo FM (2013) Renal consequences of intraabdominal hypertension in a porcine model. Search for the choice indirect technique for intraabdominal pressure measurement. Actas Urol Esp 37(5):273–279

    Article  PubMed  Google Scholar 

  36. Malbrain ML (2004) Different techniques to measure intra-abdominal pressure (IAP): time for a critical re-appraisal. Intensive Care Med 30(3):357–371

    Article  PubMed  Google Scholar 

  37. Martín A, Saboya S, Patiño M, Silva JA, Gómez S, Blanco JJ (2008) Hemodynamic monitoring: PiCCO system. Enferm Intensiva 19(3):132–140

    Article  Google Scholar 

  38. de Tomás J, Bardina A, Perea J (2001) Utilidad de la tonometría por aire en el diagnóstico de la isquemia intestinal experimental. Cir Esp 70:129–132

    Article  Google Scholar 

  39. Park PO, Haglund U, Bulkley GB, Fält K (1990) The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery 107(5):574–580

    PubMed  CAS  Google Scholar 

  40. Quaedackers JS, Beuk RJ, Bennet L, Charlton A, oude Egbrink MG, Gunn AJ et al (2000) An evaluation of methods for grading histologic injury following ischemia/reperfusion of the small bowel. Transplant Proc 32(6):1307–1310

    Article  PubMed  CAS  Google Scholar 

  41. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN (1970) Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg 101(4):478–483

    Article  PubMed  CAS  Google Scholar 

  42. Brandt LJ, Boley SJ (2000) AGA technical review on intestinal ischemia. Am Gastrointest Assoc Gastroenterol 118(5):954–968

    CAS  Google Scholar 

  43. Burns BJ, Brandt LJ (2003) Intestinal ischemia. Gastroenterol Clin North Am 32(4):1127–1143

    Article  PubMed  Google Scholar 

  44. American Gastroenterological Association Medical Position Statement (2000) Guidelines on intestinal ischemia. Gastroenterology 118(5):951–953

    Article  Google Scholar 

  45. Oldenburg WA, Lau LL, Rodenberg TJ, Edmonds HJ, Burger CD (2004) Acute mesenteric ischemia: a clinical review. Arch Intern Med 164(10):1054–1062

    Article  PubMed  Google Scholar 

  46. Olofsson PH, Berg S, Ahn HC, Brudin LH, Vikström T, Johansson KJ (2009) Gastrointestinal microcirculation and cardiopulmonary function during experimentally increased intra-abdominal pressure. Crit Care Med 37(1):230–239

    Article  PubMed  Google Scholar 

  47. Gudmundsson FF, Gislason HG, Dicko A, Horn A, Viste A, Grong K et al (2001) Effects of prolonged increased intra-abdominal pressure on gastrointestinal blood flow in pigs. Surg Endosc 15(8):854–860

    Article  PubMed  CAS  Google Scholar 

  48. El-Awady SI, El-Nagar M, El-Dakar M, Ragab M, Elnady G (2009) Bacterial translocation in an experimental intestinal obstruction model. C-reactive protein reliability? Acta Cir Bras 24(2):98–106

    Article  PubMed  Google Scholar 

  49. Leite Junior R, Mello NB, Pereira LeP, Takiya CM, Oliveira CA, Schanaider A (2010) Enterocyte ultrastructural alterations following intestinal obstruction in rats. Acta Cir Bras 25(1):2–8

    Article  PubMed  Google Scholar 

  50. Annecke T, Kubitz JC, Kahr S, Hilberath JM, Langer K, Kemming GI et al (2007) Effects of sevoflurane and propofol on ischaemia-reperfusion injury after thoracic-aortic occlusion in pigs. Br J Anaesth 98(5):581–590

    Article  PubMed  CAS  Google Scholar 

  51. Correa-Martín L, Párraga E, Sánchez-Margallo FM, Latorre R, López-Albors O, Wise R et al (2016) Mechanical intestinal obstruction in a porcine model: effects of intra-abdominal hypertension. A preliminary study. PLoS ONE 11(2):e0148058

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Diebel L, Saxe J, Dulchavsky S (1992) Effect of intra-abdominal pressure on abdominal wall blood flow. Am Surg 58(9):573–575 (discussion 5–6)

    PubMed  CAS  Google Scholar 

  53. Portas M, Garutti I, López J, Ferrando A, Fernández-Quero Bonilla L (2002) Utilidad del pH intramucoso sigmoideo en el diagnóstico precoz de la colitis isquémica postcirugía aórtica. Rev Esp Anestesiol Reanim 49:160–162

    Google Scholar 

  54. Portas M, Garutti I, Fernández-Quero Bonilla L (2003) Tonometría gastrointestinal: una nueva herramienta para el anestesiólogo. Rev Esp Anestesiol Reanim 50:401–408

    Google Scholar 

  55. Kotzampassi K, Paramythiotis D, Eleftheriadis E (2000) Deterioration of visceral perfusion caused by intra-abdominal hypertension in pigs ventilated with positive end-expiratory pressure. Surg Today 30(11):987–992

    Article  PubMed  CAS  Google Scholar 

  56. Pattillo JC, Storaker M, Anastasiadis Z, Llanos O, Urenda J, López F, Castillo L, Bugedo G, Hernández G (2004) Desarrollo de un modelo experimental de hipertensión intra-abdominal. Rev Chil Med Intensiva 19:7–12

    Google Scholar 

  57. Correa-Martín L, Castellanos G, García-Lindo M, Díaz-Güemes I, Piñero A, Sánchez-Margallo FM (2014) Intra-abdominal hypertension: effects on the splanchnic circulation. Preliminary study in a model of ascites. Gastroenterol Hepatol 37(2):51–57

    Article  PubMed  Google Scholar 

  58. van Noord D, Mensink PB, de Knegt RJ, Ouwendijk M, Francke J, van Vuuren AJ et al (2011) Serum markers and intestinal mucosal injury in chronic gastrointestinal ischemia. Dig Dis Sci 56(2):506–512

    Article  PubMed  CAS  Google Scholar 

  59. Chang M, Tang H, Liu D, Li Y, Zhang L (2016) Comparison of melatonin, hypertonic saline, and hydroxyethyl starch for resuscitation of secondary intra-abdominal hypertension in an animal model. PLoS ONE 11(8):e0161688

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

CCMIJU staff of Cáceres (Spain) and department of Veterinary Anatomy and Embryology at the University of Murcia (Spain) for their assistance in conducting this research.

Funding

This work was supported by one grant from Extremadura Regional Government through the Plan Regional de Investigación de Extremadura (PRI09A161 to Minimally Invasive Surgery Center Jesús Usón). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Correspondence to Ester Párraga Ros.

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M.L.N.G. Malbrain is a member of the medical advisory board of Pulsion Medical Systems. Drs. E. Párraga, L. Correa-Martín, F.M. Sánchez-Margallo, I.E. Candanosa, R. Wise, R. Latorre, O. López Albors, and G. Castellanos have no conflicts of interest or financial ties to disclose.

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Párraga Ros, E., Correa-Martín, L., Sánchez-Margallo, F.M. et al. Intestinal histopathological changes in a porcine model of pneumoperitoneum-induced intra-abdominal hypertension. Surg Endosc 32, 3989–4002 (2018). https://doi.org/10.1007/s00464-018-6142-z

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