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Portal Hypertension: the Desperate Search for the Placenta

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Portal Hypertension: the Desperate Search for the Placenta Current Research in Translational Medicine 67 (2019) 56–61 Available online at ScienceDirect www.sciencedirect.com Original article Portal hypertension: The desperate search for the placenta a, b c,d c,d Maria Angeles Aller *, Natalia Arias , Javier Blanco-Rivero , Gloria Balfagón , a Jaime Arias a Department of Surgery. School of Medicine, Complutense University of Madrid, 28040 Madrid, Spain b Upper Third Floor, UCL Medical School, UCL Institute for Liver and Digestive Health, Royal Free Hospital, Rowland Hill Street, London NWÁ 2PF, UK c Department of Physiology, School of Medicine, Autónoma University of Madrid, Spain d Instituto de Investigación Sanitaria del Hospital Universitario La Paz (IdiPAZ), Madrid, Spain A R T I C L E I N F O A B S T R A C T Article history: We propose that the circulatory impairments produced, in both portal hypertension and liver cirrhosis, to Received 26 February 2018 a certain degree resemble those characterizing prenatal life in the fetus. In fact, the left-right circulatory Accepted 30 September 2018 syndrome is common in cirrhotic patients and in the fetus. Thus, in patients with portal hypertension and Available online 30 November 2018 chronic liver failure, the re-expression of a blood circulation comparable to fetal circulation is associated with the development of similar amniotic functions, i.e., ascites production and placenta functions, and Keywords: portal vascular enteropathy. Therefore, these re-expressed embryonic functions are extra-embryonic and Portal hypertension responsible for prenatal trophism and development. Portosystemic shunts Placenta © 2018 Published by Elsevier Masson SAS. Hyperdynamic circulation Left-right shunts 1. Introduction esophagus and upper stomach, the splenorenal veins, the para- rectal veins with haemorrhoids and the paraumbilical veins, which Increased venous pressure in the splanchnic venous system can result in dilated veins in the anterior abdominal wall, thus making reach pathological levels and induce complications, which in turn up a “caput medusa” [1,2]. Furthermore, an intrahepatic collateral cause a higher morbidity and mortality rate in patients with circulation is produced by portal angiogenesis in the hepatic hepatic insufficiency related to cirrhosis. Furthermore, Hyperten- parenchyma, which transports the portal blood to the suprahepatic sion of the splanchnic venous system causes complications veins system [10,11]. associated with an increased morbidity and mortality in the It is obvious that increased pressure in the splanchnic venous cirrhotic patients [1–3]. The splanchnic and systemic failure system increases blood flow and, therefore elevates pressure to the produced by portal hypertension resembles the beginning of systemic venous system [1,7]. In essence, elevated portal pressure, shock. Both splanchnic and systemic hyperdynamic circulation since it is arterialized by the hepatic and mesenteric arterial increase and hence, cardiac output increases. Furthermore, the hyperdynamic circulation, makes portal blood flow carries its high splanchnic hyperdynamic circulation induces dysbiosis. The pressure to the systemic venous system [12]. However, the creation subsequent hypoxia increases the angiogenic factor release, while of an alternative way of draining blood from the portal system to also causing porto-systemic collateral circulation, mesenteric the systemic circulation could be pathophysiological more than the venous vasculopathy and even splenomegaly [4–7]. Vascular transmission itself of high pressure between two venous systems. endothelial growth factor (VEGF) family and placental growth An argument that favors the abovementioned hypothesis could be factor (PIGF) related [8–10] are the most important angiogenic that portal pressure does not become normalized, despite factors causing splanchnic venous impairments. decompression through the porto-systemic collateral circulation. In the vena cava drain, the collateral vessels are created from Another hypothesized objective for the development of porto- the coronary vein, the superior and middle hemorrhoidal veins, the systemic collateral circulation, could be favored by the systemic umbilical vein, and the splenic vein. These first collateral vessels circulatory alterations of the cirrhotic patient, such as decreased are called gastroesophageal veins, with varicose veins of the peripheral vascular resistance, increased cardiac output and the opening of arteriovenous communications inducing the mainte- nance of the splanchnic hyperdynamic circulation and, therefore portal hypertension [13]. Consequently, the systemic and splanch- * Corresponding author at: Department of Surgery School of Medicine, Complutense University of Madrid, Ramón y Cajal s.n., 28040 Madrid, Spain. nic response of the vascular bed to hemodynamic disturbances in E-mail address: [email protected] (M.A. Aller). portal hypertension is maladaptive. Nevertheless, beyond this http://dx.doi.org/10.1016/j.retram.2018.09.001 2452-3186/© 2018 Published by Elsevier Masson SAS. M.A. Aller et al. / Current Research in Translational Medicine 67 (2019) 56–61 57 mechanical explanation, the development of a porto-systemic This aggravation of the portal inflammatory response involves collateral circulation in portal hypertension could be biological, the return to their initial stages with a hemodynamic decompen- which would allow for a pathophysiological integration of the sation secondary to acute-on-chronic splanchnic ischemia-reper- cardiocirculatory alterations produced in this severe and very fusion injury, which would result in excessive interstitial edema, common condition. overwhelmed lymphatic drainage and excess of lymph collected in the peritoneal cavity with ascites formation [17,19]. 2. The portal hypertensive inflammatory response In embryonic development, metabolic needs slowly increase, therefore the initial phases could predominate the ischemia- The successive impairments of the ischemia-reperfusion, reperfusion phenotype metabolism. The hyperexpression of the immunological activation and worsening of angiogenesis phe- ischemia-reperfusion phenotype in the inflammatory response of nomena could be integrated as successive phenotypes when portal acute-on-chronic portal hypertension could represent the estab- hypertension exists. Since these phenotypes characterize the lishment of those metabolic characteristic alterations of the first inflammatory response, portal hypertension is expressed by the phases of embryonic development. If so, the body’s objective when body, either as splanchnic or systemic, with a low-grade faced with a situation that threatens its survival is to try to rebuild inflammatory response [14,15]. The basic pathophysiological itself through primitive embryonic mechanisms. However, this mechanisms that control the abovementioned phenotypes, are clever survival mechanism takes place without the invaluable typical of inflammation and are like those expressed during normal metabolic and functional support of a gestating body through the embryonic development. This is why we could suspect that these placenta, which a developing embryo has. [20]. mechanisms originated long ago [16–19]. A survival mechanism for cirrhotic patients with portal Furthermore, we could correlate the phenotypes that character- hypertension could be based on the re-expression of embryonic ize inflammation in portal hypertension with the extra- and intra- mechanisms with anaerobic metabolism. Aerobic glycolysis embryonic functions. Hence, the amniotic functions could be like associated with this metabolism will allow patients with chronic those produced during portal hypertension after ischemia-reperfu- hepatic insufficiency to survive when the hepatic metabolism is sion phenotype expression. In turn, different functions of the innate insufficient because oxidative phosphorylation is severely inhib- and acquired immune responses in portal hypertension would ited. However, this embryonic survival mechanism is insufficient reflect typical vitelline sac functions.Lastly, the connective and because post-natal life does not have the complementary functions angiogenic remodelation in portal hypertension seem to represent that the placenta gives the embryo [20]. the embryonic phenomena that occurs after gastrulation is Notably, in the production of edema after isquemia-reperfusion produced. Therefore, the metabolic impairments that are developed in organ transplantation, mediators released by the mast cells, like in portal hypertension associated with chronic liver injury, which histamine and serotonin, participate. Thus, amines whose pre- also characterize these three phenomena, would be similar to those cursors are effectively used in preservation solutions, like histidine of extra-amniotic and vitellin and intra-embryonic development and tryptophan, are both components of the preservation solution [17,18]. If it is considered that portal hypertension secondary to histidine-tryptophan-ketoglutarate (HTK; Custodiol1 [21]. It chronic hepatic insufficiency induces a low-grade inflammatory could be considered that our own body has defensive cellular response during its compensated phase, then it could be deduced mechanisms against complications related to ischemia-reperfu- that its worsening could provoke an acute-on-chronic inflammatory sion. However, its effectiveness could be reduced in physiological response when there is hemorrhage, infection or hepatic insuffi- situations, since they would be expressed when an injury, like the ciency worsening.
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