veterinary sciences

Review Anomalies of the Portal Venous System in Dogs and Cats as Seen on Multidetector-Row Computed Tomography: An Overview and Systematization Proposal

Giovanna Bertolini San Marco Veterinary Clinic and Laboratory, via dell’Industria 3, 35030 Veggiano, Padova, Italy; [email protected]; Tel.: +39-049-856-1098


Received: 29 November 2018; Accepted: 16 January 2019; Published: 22 January 2019


Abstract: This article offers an overview of congenital and acquired vascular anomalies involving the portal venous system in dogs and cats, as determined by multidetector-row computed tomography angiography. Congenital absence of the portal vein, portal vein hypoplasia, portal vein thrombosis and portal collaterals are described. Portal collaterals are further discussed as high- and low-flow connections and categorized in hepatic arterioportal malformation, arteriovenous fistula, end-to-side and side-to-side congenital portosystemic shunts, acquired portosystemic shunts, cavoportal and porto-portal collaterals. Knowledge of different portal system anomalies helps understand the underlying physiopathological mechanism and is essential for surgical and interventional approaches.

Keywords: portal system; portal vein; portosystemic shunt; portal hypertension; computed tomography

1. Introduction The portal venous system is essential for the maintenance of the liver mass and function in mammals. The portal system collects blood from major abdominal organs (i.e., gastrointestinal tract, pancreas, spleen) delivering nutrients, bacteria and toxins from the intestine to the liver. In addition, the portal blood carries approximately from one-half to two-thirds of the oxygen supply to the liver and specific hepatotrophic factors [1,2]. The portal blood is detoxified by the hepatocytes and then delivered into the systemic circulation via the hepatic veins and caudal vena cava [3]. Gross anatomic connections between the portal system and systemic venous circulation, at any level or other portal system anomalies can have serious clinical consequences [4–8]. Anomalies of the portal vein and portal system in small animals have been increasingly detected in recent years with the growing availability of advanced imaging techniques in veterinary practice [9–13]. A broad spectrum of congenital and acquired disorders may affect the portal venous system in dogs and cats. Congenital disorders of the portal system reflect a variety of embryonic or foetal disturbances, which may be isolated or combined in complex vascular patterns and may be cause of acquired vascular disorders. For example, congenital arterioportal communications are associated with acquired portal collaterals that form in response to the portal hypertension [10,14] (Figure1). Knowledge of the normal anatomy and congenital and acquired patterns and their consequences is of great importance for clinical decision-making for liver surgery and for planning interventional procedures such as transvenous portosystemic shunts or transarterial arterioportal fistulas coil embolization [15,16]. First line imaging evaluation of the portal venous system in small animals is usually performed with colour Doppler ultrasonography. Invasive techniques (e.g., splenoportography) used to obtain more detailed morphological information, are nowadays replaced by computed tomography (CT) or magnetic resonance imaging (MRI) angiography [17–21].

Vet. Sci. 2019, 6, 10; doi:10.3390/vetsci6010010 www.mdpi.com/journal/vetsci Vet. Sci. 2019, 5, 10 2 ultrasonography. Invasive techniques (e.g., splenoportography) used to obtain more detailed morphological information, are nowadays replaced by computed tomography (CT) or magnetic resonance imaging (MRI) angiography [17–21].

Figure 1. Schematization of the anomalies of the portal vein (left) and anomalous connections involving the portal venous system. Arrows indicate possible relationships between various congenital and acquired anomalies. CAPV, congenital absence of portal vein; PVH, portal vein hypoplasia; PPVh, primary portal vein hypoplasia; SPVH, secondary portal vein hypoplasia; PVA, portal vein aneurysm; PVT, portal vein thrombosis; HAVM, hepatic arteriovenous malformation; Vet. Sci. 2019, 6, 10 2 of 17 APF, arterioportal fistula; CPSS; congenital portosystemic shunt; IHPSS, intrahepatic portosystemic shunt; EHPSS, extrahepatic portosystemic shunt; APSS, acquired portosystemic shunt.

Figure 1. Schematization of the anomalies of the portal vein (left) and anomalous connections involving Multidetector-row computed tomography (MDCT) angiography is now widely considered to be the portal venous system. Arrows indicate possible relationships between various congenital and the method of choice for the diagnosis and monitoring of portal vascular anomalies in veterinary acquired anomalies. CAPV, congenital absence of portal vein; PVH, portal vein hypoplasia; PPVh, practice [22–24] MDCT provides excellent visualization of complex vascular anomalies and a primary portal vein hypoplasia; SPVH, secondary portal vein hypoplasia; PVA, portal vein aneurysm; comprehensivePVT, portal overview vein thrombosis; of the HAVM, entire hepaticportal arteriovenoussystem and allows malformation; simultaneous APF, arterioportal evaluation fistula; of other vascularCPSS; and congenital non-vascular portosystemic structures shunt; of the IHPSS, abdomen. intrahepatic portosystemic shunt; EHPSS, extrahepatic Inportosystemic this article, shunt;we present APSS, an acquired overvie portosystemicw of normal shunt. anatomy of the portal system, as seen by MDCT angiography and propose a systematization of congenital and acquired pathological conditions in dogs Multidetector-rowand cats. computed tomography (MDCT) angiography is now widely considered to beAll the collection method procedures of choice forpresented the diagnosis here were and performed monitoring solely of portalfor the vascular dog’s benefit anomalies and for in standardveterinary diagnostic practice [ 22and–24 monitoring] MDCT provides purposes. excellent Previous visualization informed written of complex consent vascular was obtained anomalies from and alla comprehensive dog owners. All overview the procedures of the entire performed portal system complied and allows with the simultaneous European legislation evaluation “on of other the protectionvascular and of non-vascular animals used structures for scientific of the purposes” abdomen. (Directive 2010/63/EU) and with the ethical requirementIn this article, of the Italian we present law (Decreto an overview Legislativo of normal 04/03/2014, anatomy ofn. 26). the portal system, as seen by MDCT angiography and propose a systematization of congenital and acquired pathological conditions in 2.dogs Brief and Anatomy cats. Background All collection procedures presented here were performed solely for the dog’s benefit and for The portal system forms by the confluence of cranial and caudal mesenteric veins, which drain standard diagnostic and monitoring purposes. Previous informed written consent was obtained most of the intestinal tract. From the left side the splenic vein, which accompanies the corresponding from all dog owners. All the procedures performed complied with the European legislation “on artery and receives the left gastric vein, contributes to the portal vein formation. From the right side, the protection of animals used for scientific purposes” (Directive 2010/63/EU) and with the ethical the portal vein receives the gastroduodenal vein, right gastric and gastroepiploic veins before enteringrequirement the ofliver the parenchyma. Italian law (Decreto At the Legislativo hepatic porta, 04/03/2014, the portal n. 26). vein divides into right and left branches2. Brief Anatomy (Figure 2) Background [25]. At this level, the portal vein pattern is almost constant, while the number of the portal branches entering individual liver lobes can vary among subjects [26,27]. In general, the right The branch portal is asystem short forms venous by trunk, the confluence which supplies of cranial the and right caudal portion mesenteric of the liverveins,. One which or drain two dorsolateralmost of the intestinalprimary branches tract. From supply the left for side the thecaudate splenic process vein, whichof the accompaniescaudate lobe theand corresponding one or three ventrolateralartery and receives branches the ran left towards gastric the vein, right contributes lateral lobe to of the the portalliver. The vein left formation. branch of Fromthe portal the rightvein side, the portal vein receives the gastroduodenal vein, right gastric and gastroepiploic veins before entering the liver parenchyma. At the hepatic porta, the portal vein divides into right and left branches (Figure2)[ 25]. At this level, the portal vein pattern is almost constant, while the number of the portal branches entering individual liver lobes can vary among subjects [26,27]. In general, the right branch is a short venous trunk, which supplies the right portion of the liver. One or two dorsolateral primary branches supply for the caudate process of the caudate lobe and one or three ventrolateral branches ran towards the right lateral lobe of the liver. The left branch of the portal vein provides several primary branches supplying the central and left portions of the liver, comprising the right medial, quadrate, left medial and left lateral lobes. In most circumstances, the left portal branch supplies also the dorsal, Vet. Sci. 2019, 5, 10 3 Vet. Sci. 2019, 6, 10 3 of 17 provides several primary branches supplying the central and left portions of the liver, comprising the right medial, quadrate, left medial and left lateral lobes. In most circumstances, the left portal branch right lateral liver lobe. One to three small branches for the papillary process of the caudate lobe arise supplies also the dorsal, right lateral liver lobe. One to three small branches for the papillary process directly from the left branch. The feline portal vein divides into left, central and right portal branches of the caudate lobe arise directly from the left branch. The feline portal vein divides into left, central providing intrahepatic subdivisions to the liver lobes. [28,29]. At all sizes and subdivisions, branches and right portal branches providing intrahepatic subdivisions to the liver lobes. [28,29]. At all sizes of the hepatic artery, portal vein and bile ducts pass in close proximity to one another. Interlobular and subdivisions, branches of the hepatic artery, portal vein and bile ducts pass in close proximity to branches of the hepatic artery and portal vein form hepatic sinusoids, which collect detoxified blood one another. Interlobular branches of the hepatic artery and portal vein form hepatic sinusoids, which into central veins and finally into the vena cava system. collect detoxified blood into central veins and finally into the vena cava system.

Figure 2. Volume rendered images (ventral views) of normal portal venous system in a dog (A) and Figure 2. Volume rendered images (ventral views) of normal portal venous system in a dog (A) and a cat (B). Ao, aorta; CdVC, caudal vena cava; PVBs, portal vein branches; PV, portal vein; ltGV, left a cat (B). Ao, aorta; CdVC, caudal vena cava; PVBs, portal vein branches; PV, portal vein; ltGV, left gastric vein; crPDV cranial pancreatic duodenal vein; SV, splenic vein; MVV, mesenteric veins. gastric vein; crPDV cranial pancreatic duodenal vein; SV, splenic vein; MVV, mesenteric veins. 3. Portal System Venous Anomalies (PVSA) 3. Portal System Venous Anomalies (PVSA) 3.1. Disorder of the Portal Vein System 3.1. Disorder of the Portal Vein System Congenital Absence of the Portal Vein (Aplasia and Atresia) 3.1.1.Congenital Congenital absence Absence of of portal the P veinortal (CAPV)Vein (Aplasia is a rare and condition Atresia) in which the portal blood bypasses the liverCongenital and a splenomesenteric absence of portal vein shunt (CAPV) to the systemicis a rare condition circulation in which is present the portal [30,31 ].blood The bypasses CAPV is attributedthe liver and to excessivea splenomesenteric involution shunt of the to periduodenal the systemic vitelline circulation veins is orpresent failure [ of30,3 the1]. vitellineThe CAPV veins is toattributed establish to anastomosis excessive involution with hepatic of the sinusoids, periduodenal which vitelline leads toveins partial or failure (of the of extrahepatic the vitelline portal veins vein)to establish or complete anastomosis (involving with also hepatic the intrahepaticsinusoids, which portal leads component) to partial absence (of the of extrahepatic the portal system portal (aplasiavein) or orcomplete agenesis). (involving As a result, also the the umbilical intrahepatic flow portal and enterohepatic component) circulationabsence of arethe disturbedportal system and the(aplasi portala or as agenesis) well as placental. As a result venous, the flowumbilical is shunted flow and systemically. enterohepatic There circulation is close relationship are disturbed between and the vitelline portal as veins well and as the placental complex venous development flow is of shunted the systemic system veinsically likely. The explainingre is close the relationship occurrence ofbetween extrahepatic the vitelline portosystemic veins and shunt the complex in case development of CAPVS [32 of,33 th].e Insystemic fact, cases veins of likely CAPVS explaining in dogs arethe alwaysoccurrence described of extrahepatic in association portosystemic to the portal shunt insertion in case into of theCAPVS caudal [32 vena,33]. cavaIn fact, and cases total of diversion CAPVS ofin portaldogs are blood always into described the systemic in association circulation (end-to-sideto the portal portosystemic insertion into shunt)the caudal [34,35 vena]. cava and total diversionImaging of portal alone blood cannot into distinguish the systemic between circulation complete (end or-to incomplete-side portosystemic forms of portalshunt)vein [34,3 aplasia.5]. The definitiveImaging alone diagnosis cannot of distinguish complete agenesis between ofcomplete the portal or incomplete system requires forms additional of portal vein histological aplasia. analysisThe definitive of the hepaticdiagnosis parenchyma of complete that agenesis demonstrates of the theportal absence system of hepaticrequires portal additional venules histological within the portalanalysis triad of the [36 ].hepatic parenchyma that demonstrates the absence of hepatic portal venules within the portalIn dogs, triad CAPV [36]. has been described in association to other developmental anomalies including situsIn inversus, dogs, CAPV congenital has been heart described diseases, venain association cava anomalies to other and developmental polysplenia (Figure anomalies3)[32 including,37]. situs inversus, congenital heart diseases, vena cava anomalies and polysplenia (Figure 3) [32,37]. Vet. Sci. 2019, 6, 10 4 of 17 Vet. Sci. 2019, 5, 10 4 Vet. Sci. 2019, 5, 10 4

FigureFigure 3. Volume 3. Volume rendered rendered image image (ventral (ventral view) view) of a dog dog with with extrahepatic extrahepatic CAPV, CAPV, portal portal insertion insertion in in Figure 3. Volume rendered image (ventral view) of a dog with extrahepatic CAPV, portal insertion in the renalthe ren segmental segment of the of the CdVC CdVC (arrow). (arrow). This This isis anan example of of end end-to-side-to-side portosystemic portosystemic shunt. shunt. There There the renal segment of the CdVC (arrow). This is an example of end-to-side portosystemic shunt. There is simultaneousis simultaneous azygous azygous continuation continuation of of the the CdVCCdVC due to to congenital congenital absence absence of renal of renal and andprehepatic prehepatic CdVCis simultaneous segments. azygous Moreover, continuation the dog of showedthe CdVC situs due to inversus congenital abdominalis absence of renal (note and the prehepatic left-sided CdVC segments. Moreover, the dog showed situs inversus abdominalis (note the left-sided mesenteric mesentericCdVC segments. and portal Moreover, veins, the the caudal dog right showed kidney situs and inversus cranial left abdominalis one). LK, left (note kidney; the leftRK,- siderightd and portal veins, the caudal right kidney and cranial left one). LK, left kidney; RK, right kidney. kidney.mesenteric and portal veins, the caudal right kidney and cranial left one). LK, left kidney; RK, right kidney. Reduced portal blood flow in the portal vein due to flow diversion through a several types Reduced portal blood flow in the portal vein due to flow diversion through a several types of of congenitalcongenitalReduced extrahepatic extrahepatic portal blood portosystemic portosystemic flow in the shuntportal shunt (CPSS vein (CPSS) )due may to may simulate flow simulate diversion the absence the through absence of the a several portal of the vein.types portal An of vein. An adequateadequatecongenital CT CTextrahepatic portal portal venous venous portosystemic vascular vascular shunt phase phase (CPSS may may ) reveal may reveal simulate a ahypoplastic, hypoplastic, the absence hypoperfused hypoperfused of the portal portal vein. portal vein An vein (portal(portaladequate vein vein atresia) CT atresia) portal and and venous hepatic hepatic vascular portal portal branches,phase branches, may which reveal makes makes a hypoplastic, the the patient patient hypoperfused a candidate a candidate for portal surgical for vein surgical interventionintervention(portal vein of atresia) theof the portosystemic portosystemic and hepatic portalshunt shunt (Figbranches, (Figureure 4). 4Onwhich). contrary, On makes contrary, in the case patient inof portal case a candidate ofvein portal aplasia for vein, surgical aplasia, surgicalattenuationintervention attenuation ofof the the of portosystemic the portosystemic portosystemic shunt connection (Fig connectionure 4 will). On resultwill contrary, result in fatalin in case fatal acute of portal acute portal vein portal hypertension aplasia hypertension, surgical [6]. [6]. attenuation of the portosystemic connection will result in fatal acute portal hypertension [6]. HistopathologyHistopatholog datay data may may be be added added to to CT CT datadata forfor confirmation confirmation of of presence presence or absence or absence of the of portal the portal Histopathology data may be added to CT data for confirmation of presence or absence of the portal venulesvenules within within the portal the portal triad. triad. However, However, smaller smaller or absent or absent portal portal tract tract within within the liver the liver can becan detected be detectedvenules withinin liver thebiopsy portal samples triad. of However, both aplasia smaller and hypoplasia or absent portalportal tractvein conditions within the [ 3 liver8]. can be in liverdetected biopsy in samplesliver biopsy of bothsamples aplasia of both and aplasia hypoplasia and hypoplasia portal vein portal conditions vein conditions [38]. [38].

Figure 4. A. Volume rendered image (ventral view) in a Mongrel dog with extrahepatic portosystemic FigureshuntFigure 4. ( A (PSS).4).. A Volume. V Theolume portal rendered rendered vein image isimage not (ventral visible.(ventral MVV,view) view) in mesenteric in a aMongrel Mongrel veins; dog dog with PSS, with extrahepatic portosystemic extrahepatic portosystemic shunt; portosystemic SV, shuntsplenicshunt (PSS). (PSS). vein; The portal Theha, hepatic portal vein vein isartery; not is visible.ltGV, not visible. left MVV, gastric MVV, mesenteric vein; mesenteric crPDV, veins; veins;cranial PSS, PSS, pancreaticoduodenal portosystemic portosystemic shunt; shunt; vein. SV, SV, splenicB. vein;Transversesplenic ha, hepatic vein; view artery;ha, athepatic the ltGV, porta artery; left hepatis gastric ltGV, of vein;left the gastric same crPDV, dog.vein; cranial An crPDV, hypoplastic pancreaticoduodenal cranial PVpancreaticoduodenal is barely visible. vein. ( BC )..vein. Dorsal Transverse B. viewTransverse at the porta view hepatis at the ofporta the hepatis same dog.of the An same hypoplastic dog. An hypoplastic PV is barely PV visible.is barely (visible.C). Dorsal C. Dorsal thin-MIP (Maximum Intensity Projection) image in the same dog, showing the thin, hypoperfuse portal vein (portal atresia). Vet. Sci. 2019, 5, 10 5

Vet. Sci.thin2019-MIP, 6, 10 (Maximum Intensity Projection) image in the same dog, showing the thin, hypoperfuse5 of 17 portal vein (portal atresia). 3.2. Portal Vein Hypoplasia 3.2. Portal Vein Hypoplasia Portal vein hypoplasia (PVH) refers to a disorder in which microscopic portal veins within the Portal vein hypoplasia (PVH) refers to a disorder in which microscopic portal veins within the liver are underdeveloped. PVH can be morphological (primary portal vein hypoplasia [PPVH]) or liver are underdeveloped. PVH can be morphological (primary portal vein hypoplasia [PPVH]) or functional (secondary PVH or SPVH) due to a reduction of portal blood flow toward the liver [14,36]. functional (secondary PVH or SPVH) due to a reduction of portal blood flow toward the liver [14,36]. These two conditions (morphological or functional) are not distinguishable either by radiology or These two conditions (morphological or functional) are not distinguishable either by radiology or histopathology alone. Integration of imaging and histological information is thus mandatory to the histopathology alone. Integration of imaging and histological information is thus mandatory to the diagnosis of PVH and distinction of morphological or functional conditions. In fact, macroscopic diagnosis of PVH and distinction of morphological or functional conditions. In fact, macroscopic disorders causing chronic hypoperfusion of the liver, such as portosystemic shunting, arterioportal disorders causing chronic hypoperfusion of the liver, such as portosystemic shunting, arterioportal fistula (APF) and portal vein thrombosis (PVT), can lead to the same hepatic histological features as fistula (APF) and portal vein thrombosis (PVT), can lead to the same hepatic histological features as PPVH and should be ruled out with imaging [39–41]. PPVH and should be ruled out with imaging [39–41]. 3.3. Portal Vein Aneurysm 3.3. Portal Vein Aneurysm Portal vein aneurysm (PVA) has a reported prevalence of 0.49% in dogs [42]. PVA can be congenital Portal vein aneurysm (PVA) has a reported prevalence of 0.49% in dogs [42]. PVA can be or acquired. Proposed mechanisms for PVA are an inherent weakness of the vessel wall or incomplete congenital or acquired. Proposed mechanisms for PVA are an inherent weakness of the vessel wall regression of the distal part of the vitelline vein. Larger, male dogs are more frequently affected and or incomplete regression of the distal part of the vitelline vein. Larger, male dogs are more frequently the boxer breed seems to be predisposed to PVA development. On MDCT images, PVA appears as affected and the boxer breed seems to be predisposed to PVA development. On MDCT images, PVA saccular or fusiform dilatation of the portal vein or its branches within the liver. Extrahepatic PVAs appears as saccular or fusiform dilatation of the portal vein or its branches within the liver. are generally located at the insertion of the gastroduodenal vein into the portal vein. Intrahepatic Extrahepatic PVAs are generally located at the insertion of the gastroduodenal vein into the portal PVAs occur at bifurcations (Figure5). Clinical features of PVAs are related to their size and possible vein. Intrahepatic PVAs occur at bifurcations (Figure 5). Clinical features of PVAs are related to their complications, such as thrombosis, rupture of the aneurysm and portal hypertension. Acquired portal size and possible complications, such as thrombosis, rupture of the aneurysm and portal collaterals may coexist with PVA [42,43] Aneurysm of the mesenteric veins can occur in dogs, alone or hypertension. Acquired portal collaterals may coexist with PVA [42,43] Aneurysm of the mesenteric in combination with PVA. Pseudoaneurysmal dilatation of portal branches is also detected in cases of veins can occur in dogs, alone or in combination with PVA. Pseudoaneurysmal dilatation of portal intrahepatic CPSS and hepatic arterioportal malformation [44,45]. branches is also detected in cases of intrahepatic CPSS and hepatic arterioportal malformation [44,45]

. Figure 5. (A). Transverse view in a dog with large saccular aneurysm of the caudal mesenteric vein Figure 5. A. Transverse view in a dog with large saccular aneurysm of the caudal mesenteric vein (CrMV) at the confluence with the splenic vein (not visible here). CDVC, caudal vena cava; Ao, aorta. (CrMV) at the confluence with the splenic vein (not visible here). CDVC, caudal vena cava; Ao, aorta. (B). Volume rendered image (ventral view) of the same dog, showing the large saccular aneurysm of B. Volume rendered image (ventral view) of the same dog, showing the large saccular aneurysm of the cranial mesenteric vein and a fusiform aneurysmal dilatation of the prehepatic portal vein (arrows). the cranial mesenteric vein and a fusiform aneurysmal dilatation of the prehepatic portal vein (arrows). 3.4. Portal Vein Thrombosis 3.4. Portal Vein Thrombosis Portal vein thrombosis (PVT) refers to the partial or total luminal obstruction of the portal vein, withPortal or without vein thrombosis extension to (PVT) its portal refers branches to the partial within or thetotal liver, luminal the splenicobstruction vein of or the the portal mesenteric vein, veinwith [or46 ].without extension to its portal branches within the liver, the splenic vein or the mesenteric vein Local[46]. causes of PVT, such as PVA and vascular invasion from hepatic or pancreatic neoplasia, are easilyLocal identified causes of byPVT, MDCT. such (Figuresas PVA6 and and vascular7)[43]. invasion from hepatic or pancreatic neoplasia, are easily identified by MDCT. (Figure 6 and 7) [43]. Vet. Sci. 2019, 6, 10 6 of 17 Vet. Sci. 2019, 5, 10 6

Vet. Sci. 2019, 5, 10 6

FigureFigureFigure 6 6.. A(A. 6 Transverse).. A Transverse. Transverse image image image of of ofthe thethe liver liverliver at at at the the the portaporta porta hepatishepatis hepatis in in ina acata cat cat with with with pancreatitis pancreatitis pancreatitis and and PV and (portal PV PV (portal (portal vein)vein) vein)thrombosis thrombosis (arrow). (arrow). B (B. ).BVolume. VolumeVolume rendered renderedrendered imageimage image (ventral(ventral (ventral view) view) view) in in the in the thesame same same cat. cat. cat.Note Note Note the largethe the large large fillingfillingfilling defect defect defect due due dueto to the to thethrombosis thrombosis (arrow) (arrow) in in the the prehepatic prehepatic PV. PV.

FigureFigure 7. ( A7.). A Dorsal. Dorsal MPR MPR(multiplanar (multiplanar reformation) reformation) view view of of the the liver liver in a in dog a dog with with suppurative suppurative hepatitis (ln, lymph node). B. Dorsal MPR view in another dog. Note the large filling defect in the Figurehepatitis 7. (ln,A. Dorsallymph node). MPR (multiplanar (B). Dorsal MPR reformation) view in another view of dog. the Note liver the in a large dog filling with suppurativedefect in the portal branches (PB) within the liver. Biliary ducts (bds) are enlarged gallbladder (GB). hepatitisportal branches (ln, lymph (PB) node within). B the. Dorsal liver. BiliaryMPR view ducts in (bds) another are enlargeddog. Note gallbladder the large filling (GB). defect in the portalPVT branches can lead (PB) to within partial the or completeliver. Biliary obstruction ducts (bds) of theare portalenlarged lumen. gallbladder Both, partial (GB). and complete PVT can lead to partial or complete obstruction of the portal lumen. Both, partial and complete PVT, may show peripheral enhancement in post-contrast series [23,42,47]. Partial and complete PVT, may show peripheral enhancement in post-contrast series [23,42,47]. Partial and complete PVTobstruction can lead should to partial be distinguished, or complete because obstruction they can of have the portaldifferent lumen. clinical Both, cons equences.partial and In casescomplete PVT,obstruction of may partial show should occlusion, peripheral be distinguished, some enhancementcontrast because medium in they postpasses can-contrast have around different series the thrombus. [ clinical23,42,4 7 consequences.In]. Partial cases of and complete In complete cases of obstructionpartialobstruction, occlusion, should enhancement some be distinguished, contrast of the medium peripheral because passes rim they around of thecan thrombus thehave thrombus. different is likely Inclinical due cases to dilatation ofcons completeequences. of the obstruction, vasa In cases ofenhancement partialvasorum occlusion, attempting of the peripheral some to recanalize contrast rim the of medium thevesse thrombusl [ 23passes]. is around likely due the to thrombus. dilatation In of cases the vasa of complete vasorum obstruction,attemptingIndirect toenhancement recanalize signs of PVT the of in vesselthe chronic peripheral [23 obstruction]. rim of are the porto thrombus-portal collaterals is likely due (see tobelow), dilatation arterioportal of the vasa vasorumIndirectshunts attempting and signs APSS of to PVT [recanalize10,47 in] chronic Because the obstruction vesse of portall [23 ].arevein porto-portal obstruction, collaterals compensatory (see below),mechanisms arterioportal are immediately activated to re-establish the portal flow to the liver and small arterial–portal connections shuntsIndirect and signs APSS of [ 10PVT,47 in] Becausechronic obstruction of portal are vein porto obstruction,-portal collaterals compensatory (see below), mechanisms arterioportal are may form within the liver. A second mechanism is the formation of portal venous collaterals. In cases shuntsimmediately and APSS activated [10,47 to re-establish] Because the of portal flow vein to obstruction, the liver and compensatory small arterial–portal mechanisms connections are of complete extrahepatic portal vein obstruction, characterized by high pressure in the splanchnic may form within the liver. A second mechanism is the formation of portal venous collaterals. In cases immediatelycirculation activated and normal to re pressure-establish in the the hepatic portal sinusoids, flow to the multiple liver and collateral small hepatopetalarterial–portal vessels connections form of complete extrahepatic portal vein obstruction, characterized by high pressure in the splanchnic may formaround within the thrombotic the liver. segment A second (see mechanism below). is the formation of portal venous collaterals. In cases ofcirculation complete and extrahepatic normal pressure portal invein the obstruction, hepatic sinusoids, characterized multiple by collateral high pressure hepatopetal in the vessels splanchnic form circulationaround3.5. theAnomalous and thrombotic normal Vascula pressure segmentr Connections in (see the below).of hepatic the Portal sinusoids, Vein System multiple collateral hepatopetal vessels form around the thrombotic segment (see below). 3.5. AnomalousThe anomalous Vascular vascular Connections connections of the Portal of the Vein portal System system can be classified broadly as high-flow and low-flow portal connections. 3.5. AThenomalous anomalous Vascula vascularr Connections connections of the Portal of the Vein portal System system can be classified broadly as high-flow and low-flow3.5.1. High portal-Flow A connections.nomalous Portal Connections The anomalous vascular connections of the portal system can be classified broadly as high-flow and low-flowHigh portal-flow po connections.rtal connections are based upon the presence of an arterial component. These High-Flowconditions Anomalous have been Portal rarely Connections described in dogs and cats and different terminology has been used 3.5.1. High-flowinterchangeablyHigh-Flow portalAnomalous causing connections confusion. Portal C are onnectionsHigh based-flow upon anomalous the presence connections of aninvolving arterial the component. portal venous These conditionssystem haveinclude been congenital rarely hepatic described arteriovenous in dogs malformations and cats and (HAVMs) different and terminology congenital or has acquired been used High-flow portal connections are based upon the presence of an arterial component. These interchangeably causing confusion. High-flow anomalous connections involving the portal venous conditions have been rarely described in dogs and cats and different terminology has been used system include congenital hepatic arteriovenous malformations (HAVMs) and congenital or acquired interchangeably causing confusion. High-flow anomalous connections involving the portal venous system include congenital hepatic arteriovenous malformations (HAVMs) and congenital or acquired Vet.Vet. Sci. Sci.2019 201, 69, 5 10, 10 7 of7 17 Vet. Sci. 2019, 5, 10 7 arterioportal fistulas (APFs) (Figure 8 and 9). HAVMs refers to a congenital disorder in which a arterioportalplethoraarterioportal of dysplastic fistulas fistulas (APFs) arteries (APFs) (Figures drain (Figure or 88 shunt andand9 9).directly). HAVMs into refers refersarterialized to to a acongenital congenitalportal vein disorder disorderbranches, in which increating which a a plethoraa vascularplethora of nidus dysplasticof dysplastic (arterialization arteries arteries drain drainof the oror portal shunt system) directly directly [ 4into4 into,4 8,49arterialized arterialized]. Sites of portal communications portal vein vein branches, branches, between creating creating the a vasculararteriala vascular and nidus nidus portal (arterialization (arterialization vessels are often ofof the difficultportal portal system) system) or impossible [44 [,4448,49,48]., 49 toSites]. determine Sitesof communications of communications with non between-selective between the CT theangiography arterialarterial and and [50 portal portal,51]. Recently, vessels are areHAVMs often often difficulthave difficult been or or classified impossible impossible as toright to determine determine divisional with or with nonleft- non-selectivedivisionalselective CT and CT angiographytheangiography left divisional [50 ,[5150 ].,5 were1]. Recently, Recently, subclassified HAVMsHAVMs as have have left medialbeen been classified classified and left as lateral,right as rightdivisional depending divisional or left on divisional or the left site divisional ofand the efferentthe left portal divisional vein drainage were subclassified [50]. Although as left congen medialital, and these left anomalies lateral, depending may be clinically on the site silent of theuntil and the left divisional were subclassified as left medial and left lateral, depending on the site of the hepatoencephalopathyefferent portal vein drainage and portal [50]. hypertension Although congen develop.ital, these Imaging anomalies of these may patients be clinically shows silent direct until and efferent portal vein drainage [50]. Although congenital, these anomalies may be clinically silent until indirecthepatoencephalopathy signs (ascites and and portal acquired hypertension portal collateral develop. Imaging circulation). of these HAVMs patients can shows be direct treated and by hepatoencephalopathy and portal hypertension develop. Imaging of these patients shows direct and transcatheterindirect signs embolization (ascites and alone acquired or in combination portal collateral with circulation).surgery but HAVMsthey may can be bedifficult treated to bytreat indirect signs (ascites and acquired portal collateral circulation). HAVMs can be treated by transcatheter definitivelytranscatheter [51]. embolization alone or in combination with surgery but they may be difficult to treat embolizationdefinitively alone [51].or in combination with surgery but they may be difficult to treat definitively [51].

FigureFigureFigure 8. 8Acquired. Acquired8. Acquired arterioportal arterioportal arterioportal fistula fistula fistula inin in aa a dog.dog. dog. (AA.. ). TransverseTransverse Transverse viewview view of of the ofthe the liver liver liver obtained obtained obtained during during during early early early arterialarterialarterial phase phase phase (ha, (ha, (ha, hepatic hepatic hepatic artery). artery) artery). NoteNote. Note the the large large hypervascular hypervascular hepatichepatic hepatic lesions lesions lesions (arrow). (arrow). (arrow). B. B. Dorsal B.DorsalDorsal MIP MIP MIP showingshowingshowing the the arterioportalthe arterioportal arterioportal communication. communication. communication. (C C.). .Left Left Left laterallateral lateral view view ofof of volumevolume volume rendered rendered rendered image image image of of the the of same the same same volume (ca, celiac artery). The arrow indicates the focal early enhancement of the liver parenchyma volumevolume (ca, (ca, celiac celiac artery). artery).The The arrowarrow indicatesindicates the focal focal early early en enhancementhancement of of the the liver liver parenchyma parenchyma due to the arterioportal communication. duedue to to the the arterioportal arterioportal communication. communication.

Figure 9. A. HAVM in a young dog with portal hypertension and multiple acquired portal collaterals. Ao, aorta; PB, portal branches; aa, branches of the hepatic artery. B. Angiogram before selective FigureFigure 9. 9(.A A).. HAVM HAVM in in a a young young dog dog with with portal portal hypertension hypertension and and multiple multiple acquired acquired portal portal collaterals. collaterals. transarterial coil embolization through hepatic artery (ha) in the same patient. C. Volume rendered Ao,Ao, aorta; aorta; PB, PB, portal portal branches; branches; aa, aa, branches branches of the hepatic artery. artery. B.B. AngiogramAngiogram before before selective selective image showing the portal venous system dilatation and multiple portal collaterals. PV, portal vein; transarterial coil embolization through hepatic artery (ha) in the same patient. C. Volume rendered transarterialha, hepatic coil artery; embolization SV, splenic through vein; crPDV, hepatic cranial artery pancreaticoduodenal (ha) in the same vein. patient. (C). Volume rendered imageimage showing showing the the portal portal venous venous system system dilatation dilatation and and multiple multiple portal portal collaterals. collaterals. PV,PV, portalportal vein;vein; ha, hepaticha, hepatic artery; artery; SV, splenic SV, splenic vein; vein; crPDV, crPDV, cranial cranial pancreaticoduodenal pancreaticoduodenal vein. vein. Vet. Sci. 2019, 5, 10 8

A single APF is a congenital or acquired, communication between a high-pressure hepatic arterial branch and a low-pressure portal branch outside or inside the liver [52]. Penetrating abdominal trauma, including liver biopsy and neoplasia are possible causes of APFs that are generallyVet. Sci. 2019 single, 6, 10 and thus easier to treat. Signs of pre-sinusoidal portal hypertension may ensue, such8 of 17 as ascites and acquired portosystemic shunts [14]. Finally, in several hepatic pathological conditions, small or microscopic acquired hepatic peripheral APFs can be identified or suspected in multiphase, thin sectionA single MDCT APF isexamination a congenital of or the acquired, liver. Their communication presence can between causea areas high-pressure of early parenchymal hepatic arterial opacificationbranch and a (hepatic low-pressure perfusion portal disorders) branch outside enhancing or inside in the late liver arterial [52]. phase, Penetrating rather abdominal than in portal trauma, venousincluding phase liver [22,23 biopsy] These and APFs neoplasia do not are require possible treatment, causes ofas APFsthey usually that are resolve generally spontaneously single and thusor diffuseeasier with to treat. the progressi Signs of pre-sinusoidalon of the underlying portal pathology hypertension [53]. may ensue, such as ascites and acquired portosystemic shunts [14]. Finally, in several hepatic pathological conditions, small or microscopic 3.6.acquired Low-flow hepatic Anomalous peripheral Portal C APFsonnections can be identified or suspected in multiphase, thin section MDCT examination of the liver. Their presence can cause areas of early parenchymal opacification (hepatic Low-flow anomalous portal connections are congenital and acquired portosystemic shunts, perfusion disorders) enhancing in late arterial phase, rather than in portal venous phase [22,23] These porto-portal collaterals that develop in case of portal vein obstruction and cavo-portal collaterals that APFs do not require treatment, as they usually resolve spontaneously or diffuse with the progression for chronic increased resistance at any level of the caudal vena cava. of the underlying pathology [53]. 3.6.1. Congenital Portosystemic Shunt 3.6. Low-Flow Anomalous Portal Connections CPSS refers to the presence of abnormal vascular connection between portal system and a Low-flow anomalous portal connections are congenital and acquired portosystemic shunts, systemic vein (of the caudal vena cava or azygous system), due to embryonic errors or foetal vascular porto-portal collaterals that develop in case of portal vein obstruction and cavo-portal collaterals that persistence. Based on its anatomic location, CPSS are customarily divided into two main subtypes: for chronic increased resistance at any level of the caudal vena cava. intrahepatic and extrahepatic. Intrahepatic portosystemic shunt (IHPSS) mostly affects large-size dogs andCongenital generally Portosystemic represents a patent Shunt ductus venosus (foetal vascular persistence) [54–56]. Depending on the side of insertion into the hepatic caudal vena cava, three phenotypes are commonly described in CPSS refers to the presence of abnormal vascular connection between portal system and a systemic the veterinary literature: right-sided, central and the most common left-sided (or -divisional) IHPSS vein (of the caudal vena cava or azygous system), due to embryonic errors or foetal vascular persistence. (Figure 10). In humans, IHPSS are classified into four types based on the location of the shunt within Based on its anatomic location, CPSS are customarily divided into two main subtypes: intrahepatic the liver, number of connections and shunt characteristics [57]. With the widespread use of advanced and extrahepatic. Intrahepatic portosystemic shunt (IHPSS) mostly affects large-size dogs and generally imaging modalities, complex, multiple connections between portal branches and hepatic veins, represents a patent ductus venosus (foetal vascular persistence) [54–56]. Depending on the side of affecting one or more liver lobes within the liver are increasingly described also in dogs (Figure 11, insertion into the hepatic caudal vena cava, three phenotypes are commonly described in the veterinary 12). Therefore, in the author’s opinion, the classification of IHPSS in dogs should be updated (Figure literature: right-sided, central and the most common left-sided (or -divisional) IHPSS (Figure 10). 10). Complex IHPSS are generally accompanied by critical clinical conditions and should be correctly In humans, IHPSS are classified into four types based on the location of the shunt within the liver, identified before treating [58,59]. number of connections and shunt characteristics [57]. With the widespread use of advanced imaging modalities,Figure 10 complex,. On the left, multiple current connections classification between of intrahepatic portal portosystemic branches and shunt hepatic in dogs veins, [54 affecting–56]. On one or morethe liver right, lobes the newwithin classification the liver are proposal. increasingly Four differentdescribed phenotypes also in dogs are (Figures possible. 11 The and persistent 12). Therefore, in theductus author’s venosus opinion, is the most the commonly classification encountered of IHPSS IHPSS. in dogs It can should be anatomically be updated left, (Figure right or 10 central). Complex IHPSSlocated. are Other generally complex accompanied IHPSS are increasingly by critical recognized clinical conditions with CT and and may should involve be one correctly or more liver identified beforelobes, treating as already [45 ,described58]. in children [7,57].

Figure 10. On the left, current classification of intrahepatic portosystemic shunt in dogs [54–56]. On the right, the new classification proposal. Four different phenotypes are possible. The persistent ductus venosus is the most commonly encountered IHPSS. It can be anatomically left, right or central located. Other complex IHPSS are increasingly recognized with CT and may involve one or more liver lobes, as already described in children [7,57]. Vet. Sci. 2019, 6, 10 9 of 17 Vet. Sci. 20120199,, 55,, 1010 99

FigureFigure 1111... A(A.. ). Dorsal Dorsal Dorsal MIP MIP MIP in in in a a a dog dog with with left-sided left left--sidedsided intrahepatic intrahepatic intrahepatic portosystemic portosystemic portosystemic shunt. shunt. shunt. (B.).. Volume Volume Volume renderedrenderedrendered imageimage image (ventral(ventral view)view) inin aa dogdog withwith rightright right-sided--sidedsided intrahepaticintrahepatic portosystemic shunt. shunt.

FigureFigure 1 12.2.. A(A.. ).IntrahepaticIntrahepatic Intrahepatic PSSPSS PSS inin in aa adogdog dog involvinginvolving involving aa a singlesingle single hepatichepatic hepatic lobe.lobe. lobe. PB,PB, PB, portaporta portalll branch;branch; branch; CdVC,CdVC, CdVC, caudalcaudalcaudal venavena vena cava.cava. cava. B (..B IntrahepaticIntrahepatic). Intrahepatic PSSPSS PSS throughthrough through anan ananeurysmalaneurysmal aneurysmal dilatationdilatation dilatation ofof aa of portalportal a portal branchbranch branch (PB).(PB). (PB). C.. Multiple(C). Multiple intrahepaticintrahepatic intrahepatic portosystemicportosystemic portosystemic connectionsconnections connections involvinginvolving involving severalseveral several hepatichepatic hepatic lobes.lobes. lobes.

ExtrahepaticExtrahepatic portosystemic portosystemic shunts shunts (EHPSSs) (EHPSSs)are developmental are developmental anomalies anomalies resulting fromresulting anomalous from anomalousconnections connections between the between vitelline the veins, vitelline which veins, form which the portalform the system portal and system the cardinal and thethe cardinal veins,cardinal forming veins,veins, formingformingthe systemic the the veins. systemic systemic Although veins. veins. the Although Although genetic basisthe the genetic genetic of CPSS basis basis in dogs of of has CPSS CPSS not in in been dogs dogs clearly has has established, not not been been clearly clearly many established,studies have man demonstratedy studies have that demonstrated this condition that occurs this more condition frequently occurs in more purebred frequently dogs andin purebred that it is dogsinherited and that in several it is inherited small and inin toyseveralseveral breeds smallsmall [7, 59andand–61 toytoy] breedsbreeds [[7,60,60–62]] TheThe initial initial description description of of Abernethy Abernethy originally originally reported reported in in people people and and the the following following functional functional classclassificationificationification ofof of MorganMorgan Morgan andand and SuperinaSuperina Superina maymay may bebe be adoptedadopted adopted alsoalso also inin in veterinaryveterinary veterinary patientspatients patients ((Figure (Figure 1)1)[ [[3300,3,3,311].].]. ThisThis classification classification system system is is based based on on whether whether the the portal portal vein, vein, often often hypoplastic, hypoplastic, is is present present and and whetherwhether the the liver liver is is perfused perfused with with blood blood from from the mesenteric v venousenous system. These These different different types types havehave different different clinical clinical impact, impact, treatment treatment options options and and outcome. outcome. In the In the type type I or Iend or end-to-side--toto--side EHPSSEHPSS the connectionthe connection is directly is directly between between the the portal portal vein vein and and a systemic a systemic vein vein due due to to CAPV CAPV and and there there is is no no discerniblediscernible portal portal flow flow to to the the liver liver (Fig (Figureure.. 3 33).).). TheTheThe typetypetype IIIIII ororor sideside-to-side--toto--side shunt,shunt, include include a a number number of of EHPSSEHPSS between between a a portal portal trib tributary,utary, most most commonly commonly emanating emanating from from left left or or right right gastric gastric veins veins and and a a systemicsystemic vein vein (cava (cava or or azygos azygos vein) vein) (Fig (Figuresure.. 1313 13––1166)))... These These connect connectionsionsions mostmost most commonlycommonly commonly areare are emanatingemanating emanating fromfromfrom leftleft left oror or rightright right gastricgastric gastric veinsveins veins... ((Figure (Figure 17)) 17[[62)[–6461]]– The63] Theside- side-to-side-toto--side is the is most the mostcommon common type of type CPSS of describedCPSS described in veterinary in veterinary patients patients [[10–12,62 [10–6–412].]., 61Various–63]. Various repetitive repetitive phenotypes phenotypes of side--toto of--side side-to-side EHPSS, whichEHPSS, reflectreflect which a a reflect common common a common underlying underlying underlying embryological embryological embryological error, error, error, have have have been been been described described described in in in dog dog dog and and and cats. cats. cats.).)).. AnomalousAnomalous portosystemic portosystemic connections connections can can also also involve involve the the mesenteric mesenteric tributaries tributaries of of the the portal portal vein vein system.system. Mesenterico Mesenterico-renal-caval--renalrenal--caval shunt shunt has has been been reported reported in in dogs dogs and and l lefteft colic colic vein vein or or cranial cranial rectal rectal vein toto pelvic systemic vein communications (directly to the caudal vena cava or through common iliaciliac veinvein oror internalinternal iliaciliac vein)vein) hashas beenbeen reportedreported inin both dogs and cats [[64,6,65].]. Vet. Sci. 2019, 6, 10 10 of 17 vein to pelvic systemic vein communications (directly to the caudal vena cava or through common Vet. Sci. 2019, 5, 10 10 iliac vein or internal iliac vein) has been reported in both dogs and cats [63,64]. InIn side side-to-side-to-side EHPSS, there is preservatio preservationn of at least some hepatic portal flow flow [6 [656,6,667]. Many Many of of thesethese patients patients have have extremely extremely hypoplastic hypoplastic portal portal vein vein cranial cranial to to the the shunt shunt that that is is sometimes sometimes difficult difficult toto visualize visualize with with conventional conventional CT CT angiography. angiography. High High quality, quality, thin thin-slices-slices MDCT images may help in detection of a thin portal vein and portal branches. These patients can be treated using partial shunt banding to allow gradual expansion of the intrahepatic portal system while avoiding irreversible portal hypertension. Splenosystemic Splenosystemic shunts shunts with with the the azyg azygousous vein, vein, the the left left phrenic and left gonadal veins have been reported either among acquired or congenital patterns in in dogs and cats and their definitivedefinitive aetiology is still debated [ 10−–12,47,612,47,678,69,68].]. The The presence presence of of other other direct direct or or indirect signs of portal hypertension, such as as ascites ascites or or varices, varices, can can help help the the interpretation interpretation of of these these vascular vascular patterns. patterns. However, those cases without ascites or multiple portosystemic connections connections are are more more difficultdifficult to interpretinterpret [ 6968].

Figure 1 13.3. Extrahepatic PSS emanatingemanating from leftleft gastricgastric veinvein inin aa dog.dog. (A).. Volume Volume rendered rendered ventral view. (BB. ).Frontal Frontal-oblique-oblique view, view, showing showing the the site site of of insertion insertion of of the the PSS PSS in in the the pre pre-hepatic-hepatic segment segment of thethe caudal caudal vena vena cava. cava.

Figure 14 14.. Congenital PSS PSS from from left left gastric vein vein in in a cat. Note Note the the thin, thin, hypoplastic hypoplastic portal portal vein vein (PV). (PV). A.(A ).Maximum Maximum Intensity Intensity Projection. Projection. B. ( BVolume). Volume Rendering Rendering.. Vet. Sci. 2019, 6, 10 11 of 17 Vet.Vet. Sci. Sci. 201 2019, 59,, 105, 10 11 11

FigureFigure 15 .1515. Extrahepatic. ExtrahepaticExtrahepatic congenital congenital congenital PSS PSS from from right right gastric gastric vein vein to theto the pre pre pre-hepatic-hepatic-hepatic segment segment of ofthe the caudal caudal venavena cava cava (CdVC). (CdVC). A .( AAVolume.). Volume Volume rendered rendered rendered image, image, image, ventral ventral ventral view view view (CrPDV, (CrPDV, (CrPDV, cranial cranial pancreatic pancreatic duodenal duodenal vein)vein)vein).. B.. B (DorsalB. ).Dorsal Dorsal view view view showing showing showing the the site the site of site ofthe of the insertion the insertion insertion of ofthe of the PSS the PSS PSSinto into intothe the CdVC the CdVC CdVC.. .

Vet. Sci. 2019, 5, 10 12 FigureFigure 16 .16 16. Congenital. Congenital extrahepatic extrahepatic PSS PSS PSS in ina in dog, a a dog, dog, from from from left left left gastric gastric gastric vein vein vein to tothe to the the right right right azyg azyg azygosos oveins vein vein (Az). (Az). (Az). A. A(VolumeA. ).Volume Volume rendered rendered rendered image, image, image, frontal frontal frontal view. view. view. B. B. (RightB ).Right Right lateral lateral lateral view, view, view, showing showing showing the the thecourse course course and and and termination termination Figure 17. Most common patterns of side-to-side EHPSS reported in the veterinary literature. The of ofthe the shunting shunting vessel vessel into into the the right right azygous azygous vein. vein. black dotted lines represent the normal connections between the portal vein and its tributaries.

FigureThe left 17. orMost right common gastric patterns veins can of side-to-side emanate shunts EHPSS reportedjoining inthe the caudal veterinary vena literature. cava, phrenic The black vein or dotted lines represent the normal connections between the portal vein and its tributaries. the azygos vein directly or can connect with left spleno-gastric veins and then enter the systemic vasculature. Caudal tributaries contributing to the portal venous system, mesenteric and colic veins can connect directly to the caudal vena cava or enter the systemic circulation via renal vein or pelvic veins.

3.7. Acquired Portosystemic Shunts (APSSs) APSSs are characterized by hepatofugal pathways that can be caused by portal hypertension (increased resistance in the portal system) or increased resistance in the cranial vena cava system. In these cases, a combination of hemodynamic, anatomic and angiogenetic factors lead to neo- angiogenesis and the opening of pre-existing vascular connections between the portal and systemic circulations [70]. In normal mammals, no gross connection between these systems is present. However, at least three embryonic connections, with no or minimal perfusion, are present in normal animals that may enlarge in case of portal hypertension: the left colic–pudendal vein, left gastric– cardiac oesophageal branches and phrenic–portal vein connections [4,71]. Several patterns of APSS have been reported in dogs and cats [10,71,72] They can be divided grossly into large shunts (e.g., left splenogonadal or splenophrenic shunt) and small shunts (e.g., oesophageal, gastrophrenic or colic varices). Large and small APSS often coexist in the same patient (Figure 18 and 19). Varices may be subdivided according to their anatomic location and pathways into left gastric vein, gastrophrenic, omental, gallbladder, abdominal wall, duodenal and colic varices [10,73] Importantly, anomalous vascular connections between systemic and portal systems can also occur in case of chronic obstruction of the caudal vena cava (cavo-portal collaterals) allowing blood to return to the right atrium [74]. Special care should be taken to not misinterpret these vascular anomalies. Vet. Sci. 2019, 6, 10 12 of 17

The left or right gastric veins can emanate shunts joining the caudal vena cava, phrenic vein or the azygos vein directly or can connect with left spleno-gastric veins and then enter the systemic vasculature. Caudal tributaries contributing to the portal venous system, mesenteric and colic veins can connect directly to the caudal vena cava or enter the systemic circulation via renal vein or pelvic veins.

3.7. Acquired Portosystemic Shunts (APSSs) APSSs are characterized by hepatofugal pathways that can be caused by portal hypertension (increased resistance in the portal system) or increased resistance in the cranial vena cava system. In these cases, a combination of hemodynamic, anatomic and angiogenetic factors lead to neo-angiogenesis and the opening of pre-existing vascular connections between the portal and systemic circulations [69]. In normal mammals, no gross connection between these systems is present. However, at least three embryonic connections, with no or minimal perfusion, are present in normal animals that may enlarge in case of portal hypertension: the left colic–pudendal vein, left gastric–cardiac oesophageal branches and phrenic–portal vein connections [4,70]. Several patterns of APSS have been reported in dogs and cats [10,70,71] They can be divided grossly into large shunts (e.g., left splenogonadal or splenophrenic shunt) and small shunts (e.g., oesophageal, gastrophrenic or colic varices). Large and small APSS often coexist in the same patient (Figures 18 and 19). Varices may be subdivided according to their anatomic location and pathways into left gastric vein, gastrophrenic, omental, gallbladder, abdominal wall, duodenal and colic varices [10,72] Importantly, anomalous vascular connections between systemic and portal systems can also occur in case of chronic obstruction of the caudal vena cava (cavo-portal collaterals) allowing blood to return Vet.to theSci. right2019, 5 atrium, 10 [73]. Special care should be taken to not misinterpret these vascular anomalies. 13

FigureFigure 18.18. A(A. ).Dorsal Dorsal thin thin-MIP-MIP showing showing small small varices varices in in left left retroperitoneal retroperitoneal region (gastrophrenic varices) and splenogonadal shunt in a a dog dog with with portal portal hypertension. hypertension. (B.). Transverse Transverse view view at at the the diaphragmaticdiaphragmatic level in a dog with portalportal hypertensionhypertension andand oesophagealoesophageal varices.varices. (C.). Transverse Transverse view view ofof the cranial abdomen in in a dog with portal hypertension due due to to HAVM. HAVM. Arrow indicates gastric submucosalsubmucosal varices. varices. Ao, Ao, aorta; aorta; CdVC, CdVC, caudal caudal vena vena cava; cava; PV, PV, portal portal vein; vein; crMV, crMV, cranial cranial mesenteric mesenteric vein. vein.

Figure 19. A. Splenogonadal shunt in a cat with portal hypertension. B. Splenophrenic shunt in another cat with portal hypertension.

3.8. Porto-Portal Collaterals or Cavernous Transformation of the Portal Vein The gradual thrombosis or extrinsic compression of the portal vein stem may lead to obstruction of the portal vein that will result partially absent on MDCT images. Portal vein obstruction causes portal hypertension and can be accompanied by portal cavernous transformation and acquired portosystemic shunts (APSSs) [10,47]. Cavernous transformation of the portal vein (CTPV) refers to the radiological appearance of porto-portal collaterals around a thrombosed portal vein [47]. Two main types of porto-portal collaterals are described in dogs and cats: short tortuous collaterals developing around/inside the thrombus and long collaterals, forming a network to overcome the obstructed portal vein (Figure 20). These collaterals course the hepatoduodenal ligament, around the gallbladder and common biliary and cystic ducts and terminating in portal branches within the liver. When complete portal vein obstruction persists for some time, portal hypertension can ensue and hepatofugal portosystemic Vet. Sci. 2019, 5, 10 13

Figure 18. A. Dorsal thin-MIP showing small varices in left retroperitoneal region (gastrophrenic varices) and splenogonadal shunt in a dog with portal hypertension. B. Transverse view at the diaphragmatic level in a dog with portal hypertension and oesophageal varices. C. Transverse view Vet. Sci. 2019, 6of, 10the cranial abdomen in a dog with portal hypertension due to HAVM. Arrow indicates gastric 13 of 17 submucosal varices. Ao, aorta; CdVC, caudal vena cava; PV, portal vein; crMV, cranial mesenteric vein.

Figure 19.Figure(A ). 19 Splenogonadal. A. Splenogonadal shunt shunt in in a a cat cat with with portal portal hypertension. hypertension. B. Splenophrenic (B). Splenophrenic shunt in shunt in anotheranother cat with cat portalwith portal hypertension. hypertension.

3.8. Porto-Portal3.8. Porto-P Collateralsortal Collaterals or Cavernous or Cavernous Transformation Transformation of of the the Portal Portal Vein Vein The gradual thrombosis or extrinsic compression of the portal vein stem may lead to obstruction Theof gradualthe portal thrombosis vein that will or result extrinsic partially compression absent on ofMDCT the portalimages. vein Portal stem vein may obstruction lead to obstructioncauses of the portalportal vein hypertension that will result and can partially be accompanied absent on by MDCT portal images. cavernous Portal transformation vein obstruction and acquired causes portal hypertensionportosystemic and can shunts be accompanied (APSSs) [10,47 by]. portal cavernous transformation and acquired portosystemic shunts (APSSs)Caverno [10us,47 transformation]. of the portal vein (CTPV) refers to the radiological appearance of Cavernousporto-portal transformation collaterals around of athe thrombosed portal vein portal (CTPV) vein [ refers47]. Two to main the radiological types of porto appearance-portal of collaterals are described in dogs and cats: short tortuous collaterals developing around/inside the porto-portal collaterals around a thrombosed portal vein [47]. Two main types of porto-portal thrombus and long collaterals, forming a network to overcome the obstructed portal vein (Figure 20). collateralsThese are collaterals described course in dogsthe hepatoduodenal and cats: short ligament, tortuous around collaterals the gallbladder developing and common around/inside biliary the thrombusand and cystic long ducts collaterals, and terminating forming in portal a network branches to overcome within the the liver. obstructed When complete portal portal vein vein (Figure 20). These collateralsobstruction coursepersists thefor some hepatoduodenal time, portal hypertension ligament, aroundcan ensue the and gallbladder hepatofugal andportosystemic common biliary and cystic ducts and terminating in portal branches within the liver. When complete portal vein obstructionVet. Sci. persists2019, 5, 10 for some time, portal hypertension can ensue and hepatofugal portosystemic14 collateral pathways will develop. Portal obstruction and indirect signs of portal hypertension must be distinguishedcollateral from pathways the congenitalwill develop. absence Portal obstruction of the portal and indirect vein eventually signs of portal associated hypertension with must congenital be distinguished from the congenital absence of the portal vein eventually associated with congenital portosystemic shunts (CPSS) [33]. The closure of acquired portal collaterals in patients with portal portosystemic shunts (CPSS) [33]. The closure of acquired portal collaterals in patients with portal hypertensionhypertension may bemay fatal. be fatal.

Figure 20.FigurePorto-portal 20. Porto-portal collaterals collaterals (cavernous (cavernous transformation of PV) of PV) in a indog a due dog to due PV thrombosis. to PV thrombosis. A. Transverse view at the porta hepatis, showing multiple tortuous vessels surrounding the (A). Transverse view at the porta hepatis, showing multiple tortuous vessels surrounding the thrombosed PV (arrows). B. Volume rendered image (ventral view) in another dog with extrahepatic thrombosed PV (arrows). (B). Volume rendered image (ventral view) in another dog with extrahepatic PV thrombosis. Arrow indicates a porto-portal collateral bypassing the site of obstruction. PV thrombosis. Arrow indicates a porto-portal collateral bypassing the site of obstruction. 4. Conclusion Portal vein system anomalies are numerous and often related to each other. Correct identification of these vascular anomalies is important because they have different clinical and prognostic significance and is essential for selecting appropriate treatment options.

Funding: None of the author of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper.

Conflicts of Interest: The author declare no conflict of interest.

References

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4. Conclusions Portal vein system anomalies are numerous and often related to each other. Correct identification of these vascular anomalies is important because they have different clinical and prognostic significance and is essential for selecting appropriate treatment options.

Funding: None of the author of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. Conflicts of Interest: The author declares no conflict of interest.

References

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