Ann Surg Treat Res.  2019 Jan;96(1):34-40. 10.4174/astr.2019.96.1.34.

Effects of hyperbaric oxygen and iloprost on intestinal ischemia-reperfusion induced acute lung injury

• Yilmaz Y
• Tumkaya L

• KMID: 2429752
• DOI: http://doi.org/10.4174/astr.2019.96.1.34

Abstract

PURPOSE
To research the effects of iloprost (IL) and hyperbaric oxygen (HBO) combination treatment on lung injury and on tumor necrosis factor alpha (TNF-α), myeloperoxidase (MPO), malondialdehyde (MDA), and soluble intercellular adhesion molecule-1 (sICAM-1) levels after tissue or organ ischemia-reperfusion, and on ischemia-reperfusion induced lung neutrophil sequestration.
METHODS
Forty white New Zealand rabbits were assigned randomly into 5 groups: HBO, IL, HBO+IL, control, and sham groups. TNF-α values were checked before ischemia, in the 1st hour of ischemia and in the 1st and 4th hours of reperfusion, also at the end of reperfusion period, plasma and tissue MPO values, MDA values, and sICAM-1 levels were detected. After sacrifice, the degree of lung injury was determined by histopathological examination.
RESULTS
Compared to the control group all therapy groups showed a drastically meaningful reduction in TNF-α increase in 1, 2, and 4 hours. Plasma and lung MDA, MPO, and sICAM-1 levels were significantly lower in IL, HBO, HBO+IL, and sham groups compared with the control group. IL and/or HBO suppressed MDA and MPO increase in the lung tissue and in plasma. Additionally, histopathological score was significantly lower in HBO, IL, HBO+IL, and sham groups than that of the control group.
CONCLUSION
Both HBO and IL therapy have a beneficial effect by causing a meaningful reduction in TNF-α production, MPO, MDA, sICAM-1 levels and pulmonary neutrophil sequestration; which play a role, especially, in ischemia reperfusion induced lung damage.

Keyword

Hyperbaric oxygenation; Iloprost; Tumor necrosis factor-alpha; Reperfusion injury

MeSH Terms

Acute Lung Injury*
Hyperbaric Oxygenation
Iloprost*
Intercellular Adhesion Molecule-1
Ischemia
Lung
Lung Injury
Malondialdehyde
Neutrophils
Oxygen*
Peroxidase
Plasma
Rabbits
Reperfusion
Reperfusion Injury
Tumor Necrosis Factor-alpha
Iloprost
Intercellular Adhesion Molecule-1
Malondialdehyde
Oxygen
Peroxidase
Tumor Necrosis Factor-alpha

Figure

• 

  Fig. 1 Preoperative, serum tumor necrosis factor alpha (TNF-α) levels in first hour of ischemia and first and fourth hours of reperfusion. HBO, hyperbaric oxygenation; IL, iloprost.

• 

  Fig. 2 (A) Lung tissue that does not show ischemic injury (H&E, ×40). (B) Moderate degree of ischemic lung injury characterized by interstitial septal thickening, neutrophil infiltration, mild intra-alveolar edema and bleeding areas (+) (H&E, ×200). (C) Diffuse, severe ischemic lung injury characterized by bleeding, edema, interstitial congestion, and neutrophil infiltration (H&E, ×200).

Reference

1. Bozok S, Kestelli M, Yurekli I, Guzeloglu M, Aksun M, Ortac R, et al. Local angioneogenetic effect of intramuscular interleukin-8 injection. Turkiye Klinikleri J Med Sci. 2012; 32:1273–1277.

2. Firat O, Makay O, Yeniay L, Gokce G, Yenisey C, Coker A. Omega-3 fatty acids inhibit oxidative stress in a rat model of liver regeneration. Ann Surg Treat Res. 2017; 93:1–10.

3. Goldman G, Welbourn R, Klausner JM, Kobzik L, Valeri CR, Shepro D, et al. Mast cells and leukotrienes mediate neutrophil sequestration and lung edema after remote ischemia in rodents. Surgery. 1992; 112:578–586.

4. Ozbek C, Kestelli M, Bozok S, Ilhan G, Yurekli I, Ozpak B, et al. Surgical stimulation of angiogenesis. Asian Cardiovasc Thorac Ann. 2014; 22:36–39.

5. Emrecan B, Tulukoglu E, Bozok S, Aksun M, Yağdi S, Ozcan AV, et al. Iloprost and pentoxifylline attenuate ischemia-reperfusion injury in skeletal muscle in rabbit model. Ulus Travma Acil Cerrahi Derg. 2008; 14:182–187.

6. Bozok S, Ilhan G, Yilmaz Y, Dokumcu Z, Tumkaya L, Karamustafa H, et al. Protective effects of hyperbaric oxygen and iloprost on ischemia/reperfusion-induced lung injury in a rabbit model. Eur J Med Res. 2012; 17:14.

7. Ilhan G, Aksun M, Bozok S, Ozpak HB, Gunes T, Durakoglugil ME, et al. Protective effects of hyperbaric oxygen and iloprost on ischemia-reperfusion injury in rabbit kidneys. Ital J Vasc Endovasc Surg. 2013; 20:89–95.

8. Ilhan G, Aksun M, Ozpak B, Gunes T, Bozok S, Durakoglugil ME, et al. The effect of combined hyperbaric oxygen and iloprost treatment on the prevention of spinal cord ischaemia-reperfusion injury: an experimental study. Eur J Cardiothorac Surg. 2013; 44:e332–e340.

9. Tjarnstrom J, Wikstrom T, Bagge U, Risberg B, Braide M. Effects of hyperbaric oxygen treatment on neutrophil activation and pulmonary sequestration in intestinal ischemia-reperfusion in rats. Eur Surg Res. 1999; 31:147–154.

10. Emrecan B, Tulukoglu E, Bozok S, Kestelli M, Onem G, Kupelioglu A, et al. Effects of Iloprost and pentoxifylline on renal ischemia-reperfusion in rabbit model. Eur J Med Res. 2006; 11:295–299.

11. Pizarro TT, Malinowska K, Kovacs EJ, Clancy J Jr, Robinson JA, Piccinini LA. Induction of TNF alpha and TNF beta gene expression in rat cardiac transplants during allograft rejection. Transplantation. 1993; 56:399–404.

12. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 1978; 86:271–278.

13. Tullis MJ, Brown S, Gewertz BL. Hepatic influence on pulmonary neutrophil sequestration following intestinal ischemia-reperfusion. J Surg Res. 1996; 66:143–146.

14. Calikoglu M, Tamer L, Sucu N, Coskun B, Ercan B, Gul A, et al. The effects of caffeic acid phenethyl ester on tissue damage in lung after hindlimb ischemia-reperfusion. Pharmacol Res. 2003; 48:397–403.

15. Hidiroglu M, Uguz E, Ozerdem G, Yildiz E, Berkan O. The proinflammatory cytokine-mediated protective effects of pentoxifylline, iloprost, and cilostazol on a mitigating lung injury induced by lower limb ischemia and reperfusion in rats. Turk Gogus Kalp Dama. 2014; 22:138–144.

16. Naldan ME, Atalay C, Coskun A, Karaca M, Aydin Y, Dorman E, et al. The efficacy of spironolactone and surfactant treatment on HMGB1, CRP, IL- 1b and TNF-a levels in acute lung injury. Turk Gogus Kalp Dama. 2015; 23:538–543.

17. Okusawa S, Gelfand JA, Ikejima T, Connolly RJ, Dinarello CA. Interleukin 1 induces a shock-like state in rabbits. Synergism with tumor necrosis factor and the effect of cyclooxygenase inhibition. J Clin Invest. 1988; 81:1162–1172.

18. Colletti LM, Remick DG, Burtch GD, Kunkel SL, Strieter RM, Campbell DA Jr. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J Clin Invest. 1990; 85:1936–1943.

19. Mayer AM, Pittner RA, Lipscomb GE, Spitzer JA. Effect of in vivo TNF administration on superoxide production and PKC activity of rat alveolar macrophages. Am J Physiol. 1993; 264(1 Pt 1):L43–L52.

20. Yang ZJ, Bosco G, Montante A, Ou XI, Camporesi EM. Hyperbaric O2 reduces intestinal ischemia-reperfusion-induced TNF-alpha production and lung neutrophil sequestration. Eur J Appl Physiol. 2001; 85:96–103.

21. Yamada T, Taguchi T, Hirata Y, Toyohara T, Hirose R, Suita S, et al. The effect of hyperbaric oxygenation on ischemia-reperfusion injury of the small intestine. Transplant Proc. 1994; 26:1506–1507.

22. Nahum A, Chamberlin W, Sznajder JI. Differential activation of mixed venous and arterial neutrophils in patients with sepsis syndrome and acute lung injury. Am Rev Respir Dis. 1991; 143(5 Pt 1):1083–1087.

23. Kihara M, McManis PG, Schmelzer JD, Kihara Y, Low PA. Experimental ischemic neuropathy: salvage with hyperbaric oxygenation. Ann Neurol. 1995; 37:89–94.

24. Buras JA, Stahl GL, Svoboda KK, Reenstra WR. Hyperbaric oxygen downregulates ICAM-1 expression induced by hypoxia and hypoglycemia: the role of NOS. Am J Physiol Cell Physiol. 2000; 278:C292–C302.

25. Cuzzocrea S, Imperatore F, Costantino G, Luongo C, Mazzon E, Scafuro MA, et al. Role of hyperbaric oxygen exposure in reduction of lipid peroxidation and in multiple organ failure induced by zymosan administration in the rat. Shock. 2000; 13:197–203.

26. Kamada T. Superoxide dismutase and hyperbaric oxygen therapy of the patient with rheumatoid arthritis. Nihon Seikeigeka Gakkai Zasshi. 1985; 59:17–26.

27. Saito K, Tanaka Y, Ota T, Eto S, Yamashita U. Suppressive effect of hyperbaric oxygenation on immune responses of normal and autoimmune mice. Clin Exp Immunol. 1991; 86:322–327.

28. Yamashita M, Yamashita M. Hyperbaric oxygen treatment attenuates cytokine induction after massive hemorrhage. Am J Physiol Endocrinol Metab. 2000; 278:E811–E816.

29. Rossman JE, Caty MG, Zheng S, Karamanoukian HL, Thusu K, Azizkhan RG, et al. Mucosal protection from intestinal ischemia-reperfusion reduces oxidant injury to the lung. J Surg Res. 1997; 73:41–46.

30. Ueno S, Tanabe G, Kihara K, Aoki D, Arikawa K, Dogomori H, et al. Early post-operative hyperbaric oxygen therapy modifies neutrophile activation. Hepatogastroenterology. 1999; 46:1798–1799.