Brief Article
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World J Gastroenterol. Jul 7, 2012; 18(25): 3310-3316
Published online Jul 7, 2012. doi: 10.3748/wjg.v18.i25.3310
Protective effect of nitric oxide on hepatopulmonary syndrome from ischemia-reperfusion injury
Tong-Jin Diao, Xin Chen, Li-Hua Deng, Han-Xiang Chen, Yan Liang, Xiao-Dong Zhao, Qing-Hua Wang, Wei-Sheng Yuan, Bai-Chun Gao, Yong Ye
Tong-Jin Diao, Qing-Hua Wang, Wei-Sheng Yuan, Bai-Chun Gao, Yong Ye, Department of Hepatobiliary Surgery and Liver Transplant Center, Jinan Military Region, The Chinese PLA 401st Hospital, Qingdao 266071, Shandong Province, China
Xin Chen, Department of Emergency, The People’s Hospital of Chengyang District, Qingdao 266109, Shandong Province, China
Li-Hua Deng, Central Injection Room, Qingdao Municipal Hospital, Qingdao 266011, Shandong Province, China
Han-Xiang Chen, Institute of Pathogenic Biology, School of Medicine, Shandong University, Jinan 250012, Shandong Province, China
Yan Liang, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, Shandong Province, China
Xiao-Dong Zhao, Department of General Surgery, Jinan Military Region, the Chinese PLA 401st Hospital, Qingdao 266071, Shandong Province, China
Author contributions: Diao TJ, Chen X, Deng LH, Chen HX, Liang Y, Zhao XD, Wang QH, Yuan WS, Gao BC and Ye Y performed the experiments, participated in the writing of the paper, and made an important contribution to the conception and design of the study, data acquisition, data analysis, and drafting, interpreting, editing and revising the paper.
Correspondence to: Tong-Jin Diao, PhD, Department of Hepatobiliary Surgery and Liver Transplant Center, Jinan Military Region, the Chinese PLA 401st Hospital, 22 Minjiang Road, Qingdao 266071, Shandong Province, China. diaotongjin@126.com
Telephone: +86-532-51870832 Fax: +86-532-51870563
Received: December 8, 2011
Revised: January 14, 2012
Accepted: May 6, 2012
Published online: July 7, 2012
Abstract

AIM: To evaluate immunological protection of nitric oxide (NO) in hepatopulmonary syndrome and probable mechanisms of ischemia-reperfusion (IR) injury in rat liver transplantation.

METHODS: Sixty-six healthy male Wistar rats were randomly divided into three groups (11 donor/recipient pairs). In group II, organ preservation solution was lactated Ringer’s solution with heparin 10  000/μL at 4 °C. In groups I and III, the preservation solution added, respectively, L-arginine or NG-L-arginine methyl ester (L-NAME) (1 mmol/L) based on group II, and recipients were injected with L-arginine or L-NAME (50 mg/kg) in the anhepatic phase. Grafted livers in each group were stored for 6 h and implanted into recipients. Five rats were used for observation of postoperative survival in each group. The other six rats in each group were used to obtain tissue samples, and executed at 3 h and 24 h after transplantation. The levels of alanine aminotransferase (ALT), tumor necrosis factor (TNF)-α and NO metabolites (NOx) were detected, and expression of NO synthase, TNF-α and intercellular adhesion molecule 1 (ICAM-1) was examined by triphosphopyridine nucleotide diaphorase histochemical and immunohistochemical staining.

RESULTS: By supplementing L-arginine to strengthen the NO pathway, a high survival rate was achieved and hepatic function was improved. One-week survival rate of grafted liver recipients in group I was significantly increased (28.8 ± 36.6 d vs 4 ± 1.7 d, P < 0.01) as compared with groups II and III. Serum levels of ALT in group I were 2-7 times less than those in groups II and III (P < 0.01). The cyclic guanosine monophosphate (cGMP) levels in liver tissue and NOx in group I were 3-4 times higher than those of group II after 3 h and 24 h reperfusion, while in group III, they were significantly reduced as compared with those in group II (P < 0.01). The levels of TNF-α in group I were significantly lower than in group II after 3 h and 24 h reperfusion (P < 0.01), while being significantly higher in group III than group II (P < 0.01). Histopathology revealed more severe tissue damage in graft liver and lung tissues, and a more severe inflammatory response of the recipient after using NO synthase inhibitor, while the pathological damage to grafted liver and the recipient’s lung tissues was significantly reduced in group I after 3 h and 24 h reperfusion. A small amount of constitutive NO synthase (cNOS) was expressed in liver endothelial cells after 6 h cold storage, but there was no expression of inducible NO synthase (iNOS). Expression of cNOS was particularly significant in vascular endothelial cells and liver cells at 3 h and 24 h after reperfusion in group II, but expression of iNOS and ICAM-1 was low in group I. There was diffuse strong expression of ICAM-1 and TNF-α in group III at 3 h after reperfusion.

CONCLUSION: The NO/cGMP pathway may be critical in successful organ transplantation, especially in treating hepatopulmonary syndrome during cold IR injury in rat orthotopic liver transplantation.

Keywords: Nitric oxide; Nitric oxide synthase; Immunoregulatory; Hepatopulmonary syndrome; Ischemia-reperfusion injury; Orthotopic liver transplantation