Basic Study
Copyright ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Hepatol. May 27, 2020; 12(5): 184-206
Published online May 27, 2020. doi: 10.4254/wjh.v12.i5.184
Pentadecapeptide BPC 157 resolves Pringle maneuver in rats, both ischemia and reperfusion
Marijan Kolovrat, Slaven Gojkovic, Ivan Krezic, Dominik Malekinusic, Borna Vrdoljak, Katarina Kasnik Kovac, Tamara Kralj, Domagoj Drmic, Ivan Barisic, Katarina Horvat Pavlov, Andreja Petrovic, Antonija Duzel, Mario Knezevic, Ivan Mirkovic, Antonio Kokot, Alenka Boban Blagaic, Sven Seiwerth, Predrag Sikiric
Marijan Kolovrat, Slaven Gojkovic, Ivan Krezic, Dominik Malekinusic, Borna Vrdoljak, Katarina Kasnik Kovac, Tamara Kralj, Domagoj Drmic, Ivan Barisic, Katarina Horvat Pavlov, Andreja Petrovic, Antonija Duzel, Mario Knezevic, Ivan Mirkovic, Antonio Kokot, Alenka Boban Blagaic, Sven Seiwerth, Predrag Sikiric, Departments of Pharmacology and Pathology, School of Medicine, University of Zagreb, Zagreb 10000, Croatia
Author contributions: Kolovrat M, Seiwerth S and Sikiric P designed the research; Kolovrat M, Gojkovic S, Krezic I, Malekinusic D, Vrdoljak B, Kasnik Kovac K, Drmic D, Barisic I, Horvat Pavlov K, Duzel A, Mirkovic I, Kokot A, Seiwerth S and Sikiric P performed the research; Seiwerth S and Sikiric P contributed reagents and analytic tools; Kolovrat M, Gojkovic S, Krezic I, Malekinusic D, Vrdoljak B, Kasnik Kovac K, Drmic D, Barisic I, Horvat Pavlov K, Duzel A, Mirkovic I, Kokot A, Seiwerth S and Sikiric P analyzed the data; Kolovrat M, Seiwerth S and Sikiric P wrote the paper.
Institutional animal care and use committee statement: This research was approved by local Ethic Committee (case number 380-59-10106-17-100/290) and by Directorate of Veterinary (UP/I-322-01/15-01/22).
Conflict-of-interest statement: All other authors have nothing to disclose.
Data sharing statement: No additional data are available.
ARRIVE guidelines statement: The authors have read the ARRIVE guidelines, and the manuscript was prepared and revised according to the ARRIVE guidelines.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Predrag Sikiric, MD, PhD, Professor, Departments of Pharmacology and Pathology, School of Medicine, University of Zagreb, POB 916, Salata 11, Zagreb 10000, Croatia. sikiric@mef.hr
Received: October 23, 2019
Peer-review started: October 23, 2019
First decision: November 22, 2019
Revised: March 25, 2020
Accepted: March 30, 2020
Article in press: March 30, 2020
Published online: May 27, 2020
Processing time: 216 Days and 20.4 Hours
ARTICLE HIGHLIGHTS
Research background

The Pringle maneuver (portal triad obstruction) provides huge disturbances during ischemia and even more thereafter in reperfusion. Contrarily, a possible solution may be stable gastric pentadecapeptide BPC 157, with already documented beneficial effects in ischemia/reperfusion conditions. Recently, BPC 157, as a cytoprotective agent, successfully resolved vessel occlusions in rats (ischemic/reperfusion colitis; deep vein thrombosis, superior anterior pancrea-ticoduodenal vein; bile duct cirrhosis) through rapid collateral vessel recruitment to circumvent vessel occlusion. Likely, as a new effect, BPC 157 application may be useful when applied in the ischemia condition much like when given in the reperfusion condition. Thereby, medication BPC 157 regimens were administered as a single challenge before and during ischemia or, alternatively, at various time points during reperfusion.

Research motivation

We focused on the therapy of the Pringle maneuver in rats, so far not described severe preportal hypertension, the temporary portal triad obstruction (PTO), ischemia, the short and prolonged reperfusion, the lack of adequate portocaval shunting as the most detrimental feature that should be counteracted. With stable gastric pentadecapeptide BPC 157, we suggest the resolution of the damages, either those following occlusion or those following re-opening of the hepatic artery, portal vein and bile duct.

Research objectives

The first objective in the PTO-syndrome in rats is the rapidly activated way, portal vein-superior mesenteric, vein-inferior mesenteric vein-rectal vein-left iliac vein-inferior caval vein, supposed to appear as a specific activation of the collateral circulation, as the bypassing loop that can rapidly circumvent occlusions and decompress PTO-rats upon BPC 157 administration. The additional objective is verification that that solution in Pringle-rats with ischemia and reperfusion goes with resolution of the whole syndrome. In this, there are the resolution of oxidative stress, hemodynamic disturbances, severe portal and caval hypertension, aortic hypotension, rapid cloth formation in the portal vein, superior mesenteric vein, lienal vein, inferior caval vein, hepatic artery, ascites, peaked P waves, tachycardia; increased serum values; gross intestine, liver, lung, spleen and heart lesions. The final objective is demonstration that it goes also with the agent application during reperfusion.

Research methods

In the Pringle-rats with the PTO occluded or reopen, assessment includes gross (USB camera) and microscopic observations, venography, blood pressure and electrocardiogram assessment, bilirubin and enzyme activity, levels of nitric oxide, malondialdehyde in the liver. With the mentioned methods, assessed was the activated pathway, portal vein-superior mesenteric, vein-inferior mesenteric vein-rectal vein-left iliac vein-inferior caval vein. Then, we assessed the resolution of the oxidative stress, hemodynamic disturbances, severe portal and caval hypertension, aortic hypotension, rapid cloth formation in the portal vein, superior mesenteric vein, lienal vein, inferior caval vein, hepatic artery, ascites, peaked P waves, tachycardia; increased enzymes serum values; gross intestine, liver, lung, spleen and heart lesions.

Research results

BPC 157 counteracts electrocardiogram disturbances (increased P wave amplitude, S1Q3T3 QRS pattern and tachycardia). BPC 157 administration rapidly presented portal vein-superior mesenteric vein-inferior mesenteric vein-rectal veins-left ileal vein-inferior caval vein vascular pathway as the adequate shunting. As evidenced, this vascular pathway recovery means the immediately recovered disturbed hemodynamic. Portal hypertension and severe aortal hypotension during PTO, as well as portal and caval hypertension and mild aortal hypotension in reperfusion and refractory ascites formation were markedly attenuated (during PTO) or completely abrogated (reperfusion); thrombosis in portal vein tributaries and inferior caval vein or hepatic artery was counteracted during PTO. Likewise, the whole vicious injurious circle was counteracted [i.e., lung pathology (severe capillary congestion), liver (dilated central veins and terminal portal venules), intestine (substantial capillary congestion, submucosal edema, loss of villous architecture), splenomegaly, right heart (picked P wave values)], otherwise regularly perpetuated in ischemia and progressed by reperfusion in Pringle rats.

Research conclusions

BPC 157 resolves Pringle maneuver in rats, both for ischemia and reperfusion.

Research perspectives

The reported evidence that the administration of BPC 157 resolves the adverse effects of the Pringle maneuver means the immediate recovery of collaterals, which results in the bypassing of the obstruction, even in the worst conditions of PTO disturbances. The key importance of this therapy effect verifies the reversal of the signs of the right heart failure much like the severe portal hypertension and severe aortal hypotension during PTO as well as the severe portal and caval hypertension and mild aortal hypotension in reperfusion, along with refractory ascites formation, thrombosis and ischemia markedly decreased and completely disappeared. The rapid reestablishment of blood flow in both the ischemic and reperfusion conditions accompanied the reduction of the increased malondialdehyde values in liver tissues to the normal values. Likely, this combined effect resolves the further circle of injuries (i.e., the specific pathology in the liver, intestine, spleen, lung and heart). Thus, these new insights into Pringle maneuver and related disturbances, and into portal hypertension, suggest the effective BPC 157 use in future therapy. Otherwise, the abrupt PTO and severe portal hypertension (> 60 mmHg) [and in reperfusion, caval hypertension (> 70 mmHg)] makes spontaneous decompression of the portal system by a portocaval shunt hardly possible as well as severe aortal hypotension in the ischemia not compensated in the reperfusion.