COMPUTED TOMOGRAPHIC CHARACTERISTICS OF COLLATERAL VENOUS PATHWAYS IN DOGS WITH CAUDAL VENA CAVA OBSTRUCTION SWAN SPECCHI, MARC-ANDRE´ D’ANJOU, ERIC NORMAN CARMEL , GIOVANNA BERTOLINI
Collateral venous pathways develop in dogs with obstruction or increased blood flow resistance at any level of the caudal vena cava in order to maintain venous drainage to the right atrium. The purpose of this retrospective study was to describe the sites, causes of obstruction, and configurations of venous collateral pathways for a group of dogs with caudal vena cava obstruction. Computed tomography databases from two veterinary hospitals were searched for dogs with a diagnosis of caudal vena cava obstruction and multidetector row computed tomographic angiographic (CTA) scans that included the entire caudal vena cava. Images for each included dog were retrieved and collateral venous pathways were characterized using image postprocessing and a classification system previously reported for humans. A total of nine dogs met inclusion criteria and four major collateral venous pathways were identified: deep (n = 2), portal (n = 2), intermediate (n = 7), and superficial (n = 5). More than one collateral venous pathway was present in 5 dogs. An alternative pathway consisting of renal subcapsular collateral veins, arising mainly from the caudal pole of both kidneys, was found in three dogs. In conclusion, findings indicated that collateral venous pathway patterns similar to those described in humans are also present in dogs with caudal vena cava obstruction. These collateral pathways need to be distinguished from other vascular anomalies in dogs. Postprocessing of multidetector-row CTA images allowed delineation of the course of these complicated venous pathways and may be a helpful adjunct C 2014 American College of Veterinary Radiology. for treatment planning in future cases. Key words: angiography, caudal vena cava obstruction, collateral vessels, computed tomography.
Introduction
T
blood flow resistance at any level of the caudal vena cava can lead to collateral vein formation to maintain venous drainage to the right atrium. The pattern of collateral venous pathways can also be predicted on the basis of the level of the obstruction.5–7 In dogs, caudal vena cava obstructions or increases in flow resistance have been most commonly described as acquired conditions, typically caused by neoplasia,8–10 trauma,11,12 and thrombosis.13 Congenital obstructive conditions of the caudal vena cava have been rarely reported in humans and dogs. These have included membranous obstructions, segmental dilation, or aneurysm due to congenital wall weakness or other developmental disorders.14,15 Computed tomographic angiography (CTA) has been applied in veterinary medicine for the evaluation of vascular abnormalities,16,17 shunts,18,19 and collateral vessels.20 Volume rendering of CTA datasets has been reported to facilitate comprehension and classification of complex vascular abnormalities. Other imaging modalities used to study vascular anatomy and vascular obstructions have included ultrasound,21,22 MRI,23,24 and scintigraphy.25 The CTA appearance of congenital caudal vena cava anomalies have been previously described in the veterinary literature.16,17 However, there is lack of published information on the CTA
HE CAUDAL VENA cava (vena cava caudalis) is the largest
vein that brings deoxygenated blood from the tissues of the body to the right atrium of the heart. In adult mammals, the caudal vena cava is typically a single right-sided retroperitoneal vessel and is anatomically subdivided into five segments with different developmental origins: prerenal, renal, prehepatic, hepatic, and posthepatic segments.1–3 In dogs, the caudal vena cava begins with the confluence of the caudal iliac veins and lies between the left and right psoas muscles in the retroperitoneal space. More cranially, the vein tunnels through the caudate lobe of the liver and penetrates the diaphragm through the foramen venae cavae. The intrathoracic part of the caudal vena cava lies in the plica venae cavae, before finally converging into the right atrium.4 In humans, chronic obstructions or increases in From the Department of Clinical Sciences, Facult´e de M´edecine V´et´erinaire, Universit´e de Montr´eal, 3200 Rue Sicotte, J2S7C6, Sainte Hyacinthe, Qu´ebec, Canada (Specchi, Carmel, d’Anjou) and the San Marco Veterinary Clinic, Via Sorio 114/c, 35141, Padua, Italy (Bertolini). Portions of this study were presented at the ACVR Annual Scientific Meeting in Savannah, Georgia, 2013. Address correspondence and reprint requests to Swan Specchi at the above address. E-mail: [email protected] Received August 4, 2013; accepted for publication January 17, 2014. doi: 10.1111/vru.12167
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FIG. 1. Illustrations of the appearance of the four major venous collateral pathways in dogs affected by occlusion of the caudal vena cava based on multidetector computed tomographic angiography and three-dimensional volume rendering. CVC, caudal vena cava; CrCV, cranial vena cava; dCIV, deep circumflex iliac vein; PV, portal vein; AV, azygos vein; LVs, lumbar veins; CdMV, caudal mesenteric vein; CrMV, cranial mesenteric vein; ltCV, left colic vein; ltGV, left gonadal vein; dCIL, deep circumflex iliac vein. (A) Schematization of a superficial collateral pathway. Note the dorsal subcutaneous tortuous vessels draining blood from the deep circumflex iliac veins into the 11th intercostal veins and finally the azygos vein. Alternatively, the circumflex iliac vein can anastomose with the caudal epigastric and caudal superficial epigastric veins ending in the internal thoracic veins. (B) Schematization of an intermediate collateral pathway. Note the tortuous vessels around the ureters and uterine horns draining blood from the pre-obstructed caudal vena cava (through the iliac veins) to the renal veins and gonadal veins, respectively, and finally into the postobstructed caudal vena cava (cavo-caval shunt). (C) Schematization of a portal collateral pathway. Note the multiple tortuous vessels around the rectum representing the rectal plexi, which permit communication between the caudal vena cava system (iliac veins) and portal system (left colic vein and cranial mesenteric vein). This pathway could be considered a cavo-portal shunt with a hepatopetal flow. (D) Schematization of a deep collateral pathway. Note the multiple enlarged lumbar veins draining blood from the obstructed caudal vena cava to the internal vertebral venous plexus with blood draining ahead into the azygos vein and finally inside the right atrium of the heart.
appearance of caudal vena cava collateral pathways in dogs. The purpose of this retrospective study was to describe the CTA characteristics of collateral venous pathways in a group of dogs with caudal vena cava obstruction.
Materials and Methods Image databases of the San Marco Veterinary Clinic and Centre Hospitalier V´et´erinaire de l’Universit´e de Montreal were searched from 2005 to 2012 for dogs with caudal vena cava obstruction and contrast-enhanced CT scans. Scans meeting initial inclusion criteria were retrieved and examined. Dogs were included in the study if the entire caudal vena cava was present in postcontrast CT scans (from the common iliac veins confluence to the right atrium), and if obstruction or conditions potentially leading to increased caudal vena cava flow resistance were documented. For each included dog, CT image datasets were transferred from hospital picture archiving and communication systems (PACS) to a dedicated image analysis workstation (ADW 4.0 and 4.6, GE Medical Systems, Mississauga, ON, Canada and Milan, Italy). Both nonvascular contrastenhanced CT and CTA studies were evaluated. Images were analyzed by two board-certified veterinary radiologists (E.N.C. and M.A.D.), a second year resident (S.S.), and a veterinarian with more than 10 years of experience in multidetector row CT imaging (G.B.). Images were first interpreted independently and then interpreted a second
time by all authors together to reach a consensus. The following CT characteristics were recorded for each dog: (i) site of suspected caudal vena cava obstruction: prerenal (from iliac vein confluence to the renal veins), renal (between the renal veins), prehepatic (from the renal veins and the hepatic veins), hepatic, and posthepatic (from the liver to the right atrium); and (ii) presence and configuration of venous collateral pathways (defined based on previously published classification schemes used in humans for inferior vena cava collateral pathways).6 Readers used postprocessing techniques such as multiplanar reformatting, maximum intensity projection, and three-dimensional (3D) volume rendering as aids for visualizing the venous collaterals and characterizing patterns. Automatic and manual segmentation methods were used to enhance the caudal vena cava and its collaterals in the images. Arterial and portal vessels, as well as lymphatic vessels were carefully evaluated in each case. Finally, other nonvascular abnormal CT features were recorded. Medical records were also reviewed and the mechanism of caudal vena cava obstruction or suspected increased resistance was identified. When available, the final diagnosis was recorded.
Results Nine dogs (four males and five females) met inclusion criteria for the study. Four were mixed breed dogs, one Bullmastiff, one Maltese, one Rottweiler, and two American
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FIG. 3. Volume-rendered, left lateral CTA image of a dog with obstruction of the caudal vena cava due to a retroperitoneal peri-aortic lymphoma resulting in a superficial and intermediate (peri-ureteric) collateral pathways and enlarged subcapsular veins. Note the enlarged deep circumflex iliac vein (short white arrow) and the enlarged caudal epigastric vein (long white arrows). The peri-ureteric vein is also visible (white arrow-heads). The asterisk marks tortuous subcapsular veins draining in the deep circumflex iliac vein.
FIG. 2. Volume rendered CTA images, illustrating left lateral (A) and dorsal (B) views of a dog with obstruction of the caudal vena cava due to a retroperitoneal periaortic lymphoma resulting in a superficial collateral pathway. Note the enlarged deep circumflex iliac veins (arrows) and the tortuous superficial subcutaneous vessels (asterisks).
Staffordshire Bull Terriers. Mean (range) age and body weight were 8.4 years (0.75–11.5) and 27.9 kg (3.1–50), respectively. All CT studies were performed with the same 16-row multidetector CT unit (Light Speed 16 slice, General Electric Healthcare, Medical Systems, Milwaukee, WI) with dogs anaesthetized and placed in ventral or dorsal recumbency. Positive pressure ventilation was employed during image acquisition to prevent motion artifacts. In one center (San Marco), images were acquired in helical scan mode, at 120 kV and 200 mAs tube settings, a pitch of 0.562:1 and 1.25 mm slice thickness with 50% overlap with a 0.7 s rotation time and reconstructed with a nonenhancing nonsmoothing algorithm. Contrast-enhanced images were then obtained using a dosage of 640 mgI/kg of iodixanol (Visipaque 320, General Electric Healthcare, Milan, Italy) injected into a cephalic vein through an IV catheter. The contrast medium was injected (3–5 ml/s) in bolus, followed by a saline flush (same injection rate) via a
dual-syringe injector system (Medrad Stellant CT Injection System, Bayer, Milan, Italy). A fixed injection-to-scan delay of 20 s was used for routine nonvascular abdominal contrast-enhanced image assessments. The angiographic studies were performed with the individual transit time determined using a bolus triggering technique, as previously described.19 At the second institution, CT scans were acquired in helical scan mode, at 120 kV and 200 mAs tube settings, at a pitch of 0.938:1 and 1.25 mm slice thickness with 50% overlap at 1 s rotation time and transverse images were reconstructed with a medium-high spatial-frequency soft tissue algorithm. CT-angiography was performed following a previously described protocol26 using a dosage of 600 mgI/kg of iopamidol (Isovue 300, ER Squibb & Sons Company, Princeton, NJ, and Bracco Industria Chimica, Milan, Italy) at 5 ml/s injection rate in the external jugular vein (Medrad EnVision CT, Bayer, ON, Canada). Four main venous collateral pathway patterns were identified with features similar to the human classification scheme proposed by Sonin et al.6 : Pattern 1: Enlargement of the iliac circumflex veins draining blood from the common iliac veins into cranial and caudal superficial branches of the iliac circumflex veins localized in the dorsal abdominal subcutaneous tissues. These branches anastomosed cranially with the 11th intercostal vein ending finally in the azygos vein (Fig. 1A, 2). Alternatively, the deep circumflex iliac vein
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FIG. 4. Three different volume rendered, ventral CTA images of a dog with congenital aneurysm of the caudal vena cava (asterisk) and intermediate pathway (right gonadal vein). Note the enlarged right gonadal (arrow) and right phrenico-abdominal veins ending in the caudal vena cava (arrowheads, in A and B).
anastomosed with the caudal epigastric and caudal superficial epigastric veins ending in the thoracic veins (Fig. 3). Most features of this pattern, except for the anastomosis with the 11th intercostal vein, resembled the superficial collateral pathway reported in humans.6 Pattern 2: Enlargement of the gonadal veins and periureteric veins draining blood to the left renal vein and caudal vena cava from some tortuous vessels inside the uterine and urinary bladder (Figs. 1B, 4, and 5). This pattern is similar to the intermediate collateral pathway reported in humans.6 Pattern 3: Enlargement of the left colic vein and cranial mesenteric vein draining blood from numerous tortuous vessels inside the rectal wall and from the jejunal veins into the portal vein (Figs. 1C and 5). This pattern is similar to the portal collateral pathway reported in humans.6 Pattern 4: Enlargement of the lumbar veins and/or vertebral venous system draining blood from the caudal vena cava into an enlarged right azygos vein (Figs. 1D and 6). This pattern resembled the deep collateral pathway reported in humans.6 In addition to these four main patterns, we also identified unique patterns and presentations:
A: In 3/9 dogs, renal subcapsular collateral veins arising mainly from the caudal pole of both kidneys were identified, draining the subcapsular veins and ending caudally in the ipsilateral circumflex iliac vein (Fig. 3). B: In 3/9 patients, abdominal lymphatic vessels draining in the cisterna chili were visible and subjectively dilated (Fig. 7). C: Two patients with obstruction of the hepatic and posthepatic segments of the caudal vena cava showed abdominal fluid and multiple acquired splenogonadal portosystemic shunts (Budd-Chiari like syndrome). D: One of our dogs had dilatation of the caudal vena cava, aneurysm of the renal segment of the caudal vena cava and left renal vein, azygos continuation of the caudal vena cava, and intermediate collateral circulation via the left gonadal (ovarian or testicular) vein (Fig. 4). Eight of nine dogs had a mass invading the caudal vena cava. Six of eight of these dogs had a histological or cytological diagnosis of neoplastic mass. Five dogs presented more than one collateral venous pathway. Abdominal effusion was detected in 5/9 dogs. In two of these, slight to moderate effusion surrounding an abdominal mass was observed, whereas severe diffuse effusion was present in the other
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FIG. 5. Volume-rendered ventral CTA image of a dog with caudal vena cava obstruction due to a right adrenal gland mass resulting in portal and intermediate (peri-ureteric) collateral pathways. Note the enlargement of the left colic vein (lfCV) draining into the caudal mesenteric vein (CdMV) and finally into the portal vein (PV). The caudal vena cava is abruptly interrupted. CrMV, cranial mesenteric vein.
three. Unilateral retroperitoneal effusion was identified in two dogs. Detailed descriptions of the sites and extension of caudal vena cava obstruction, cytological and/or histological diagnoses, and concomitant vascular anomalies are provided for each dog in Appendix 1.
Discussion Similar to those previously reported in humans,5–7,27,28 four main collateral venous pathways were identified in the dogs of the present study. The superficial pathway allows blood to flow from the external iliac veins, through the circumflex iliac veins to the caudal epigastric and caudal superficial epigastric veins. In humans, these subcutaneous vessels terminate inside the subclavian vein bypassing the internal mammary vein or lateral thoracic vein.29 Interestingly, we noted that in some patients the right azygos vein could drain part of the blood coming from the subcutaneous vessels of the superficial pathway. To the authors’ knowledge, this variant has not been reported in humans. The intermediate pathway is most frequently found in humans with occlusion of the renal veins and renal segment of the inferior vena cava.27,29 The intermediate pathway with gonadal veins (ovarian or testicular) is more frequently reported on the left side in humans compared to the right. This is probably because the right go-
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nadal vein empties directly into the prerenal segment of the inferior vena cava, which in these patients could be occluded, whereas the left gonadal vein usually empties into the left renal vein.6 In humans, gonadal and periureteric veins communicate with the internal iliac vein by the vescical and uterine venous plexi. We identified this pathway in 8/9 dogs and in seven of them the occlusion involved the renal segment. In the remaining dog, the occlusion was at the level of the prerenal segment. Even with the few cases reported here, the gonadal and periureteric veins seem to be the preferred collaterals in dogs with occlusion of the renal veins and renal segment of the caudal vena cava as reported in humans. In these patients, the blood flows from caudal to cranial bypassing the site of obstruction through the gonadal and periureteric veins, in particular draining the blood from the pre-occluded segment of the caudal vena cava to the postoccluded segment. The intermediate pathway effectively acts as a cavocaval collateral pathway.7 Portal collateral pathways have been subdivided into five types in humans,28 but only one subtype was found in our patients. In our dogs, collateral vessels were similar to human patients with a cavo-mesenteric-portal collateral pathway. In these patients, the rectal venous plexus allows communication between the caudal vena cava and the portal system.27–29 In humans/dogs, the inferior/caudal and middle rectal plexus are drained by the internal iliac vein, while the superior/cranial venous rectal plexus is drained by the inferior/caudal mesenteric vein. In our dogs, tortuous vessels were identified inside the rectal wall, probably representing an enlargement of the physiologically nonvisible rectal plexus. In human, this pathway is considered a cavoportal connection between the caudal vena cava and the portal vein and may be confused for portosystemic shunting. The hepatopetal flow can help distinguish these cavoportal pathways from portocaval shunts that carry a hepatofugal flow. In CT-angiography series, the level of attenuation of contrast medium in collateral vessels is an important determinant, as it matches one of the venous system draining into these vessels. Therefore, the attenuation of contrast medium in the collateral vessel will match one of the caudal vena cava in case of cavoportal pathway, whereas it will match the portal circulation in the case of portocaval shunts.7,10,29 The left colic and caudal mesenteric veins were concomitantly subjectively enlarged in some dogs, which may have been attributed to the formation of shunts between these veins and the caudal vena cava or gonadal vein, as reported in humans.17 Another subtype of portal collateral pathway described in humans is the cavo-renal-portal pathway with subcapsular veins that anastomose with the splenic vein.28 In 3/9 dogs, enlarged, tortuous subcapsular renal veins were also observed, but these connected to the ipsilateral deep circumflex iliac vein, excluding the portal system as part of this pathway and
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FIG. 6. Computed tomographic angiography images from a dog with obstruction of the caudal vena cava due to a retroperitoneal periaortic neuroendocrine carcinoma and resulting in a deep collateral pathway. (A) Transverse view at the thoracic level. Note the enlarged azygos vein (AV) that has the same size as the aorta (Ao). (B) Parasagittal multiplanar reformatted image of the caudal thoracic vertebral column showing an enlarged AV and internal vertebral venous plexus (arrowheads). (C) Volume-rendered image of the thoracic cavity of the same dog. Note the enlarged AV and some lumbar veins (LVs).
being different from the cavo-renal-portal pathway reported in human. We propose that this is a unique feature in canine patients. The other three subtypes of collateral portal pathways described in humans were not recognized in our dogs, but this could be due to the small number of dogs in this study. The deep collateral pathway, the most prevalent in humans, was detected in two of our dogs. Through the lumbar veins and vertebral venous system,29 the blood flows to the right atrium through an enlarged azygos vein. A Budd-Chiari like syndrome was suspected in 2/9 dogs with occlusion of the hepatic and posthepatic segment of the caudal vena cava, peritoneal effusion and acquired splenogonadal portosystemic shunts. Distinction between an intermediate venous collateral pathway involving the gonadal vein and an acquired splenogonadal shunt was based on the difference of origin of the gonadal vein involved. In the first case, the gonadal vein originated caudally from the ovarian and uterine venous plexi, whereas in case of acquired splenogonadal portosystemic shunt the gonadal vein communicated with the splenic vein through an abnormal collateral vessel. In one dog, there was an aneurysm of the renal segment of the caudal vena cava and left renal vein and azygos continuation of the caudal vena cava (Fig. 4). Aneurysm of the caudal vena cava with congenital azygos continuation has been previously reported in one dog.17 In our dog, the combination of ultrasound and CTA findings allowed visualization of engorged abdominal veins with absent/reversed flow into the caudal vena cava, and exclusion of a caval thrombus or other obstructive causes. Due to the absence of hepatomegaly or peritoneal or retroperitoneal
FIG. 7. Computed tomographic angiography images from a dog with congenital aneurism of the caudal vena cava (An). Note the dilated cisterna chyli (asterisk) and the multiples nonenhancing tortuous vessels around it consistent with enlarged lymphatic vessels (arrow heads).
effusion in our dog, a presinusoidal/sinusoidal obliterative cause or a congenital intrinsic weakness of caudal vena cava and renal vein wall was hypothesized. This study was limited by several factors. The retrospective nature of this study prevented us from investigating the potential impact of recumbency on presence and size of collateral venous pathways in dogs. In pregnant women
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lying in supine position, for example, the uterus causes an acute obstruction of the inferior vena cava and the venous return is supplied by the azygos and vertebral veins.30 Dogs in this study were variably positioned in dorsal or ventral recumbency potentially influencing the detection of venous collateral pathways. Moreover, the whole thorax was not imaged in all of our dogs, which may have prevented the detection of additional collaterals. The low number of dogs included in this study prevented a definitive classification of venous collateral pathways for dogs with obstruction of the caudal vena cava. Yet, most features of venous collateral pathways reported in humans were also found in dogs of this study with minor differences.
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In conclusion, findings from the current study indicated that dogs affected by obstruction and/or increased blood flow resistance in the caudal vena cava develop venous collateral pathways that are similar to those previously reported in humans. These venous collaterals should be differentiated from other vascular anomalies. Acquired portosystemic shunts can occur concomitantly with venous collateral pathways in patients affected by a Budd-Chiari like syndrome and this can make interpretation challenging. Multidetector row CTA and postprocessing techniques such as multiplanar reformatting, maximum intensity projection and 3D volume rendering can help more clearly delineate the course and pattern of these complicated collateral venous pathways.
APPENDIX 1. Type of caudal vena cava venous collateral pathway, site of obstruction and presence of acquired portosystemic shunts in nine dogs with caudal vena cava obstruction Pathway Site of obstruction
Dog Superficial Intermediate Portal Deep 1
x
2 3
x x
x
4 5 6 7
x
x x x x
APSS∗
Prerenal
8
x
Prerenal-renal-prehepatic Renal-prehepatic-hepaticposthepatic Prerenal-renal-prehepatic Renal-prehepatic Renal-prehepatic-hepatic Renal-prehepatic-hepaticposthepatic Prerenal
9
x
Renal
∗
x x
x x
x
x
Diagnosis
x
Metastasis from anal sacs adenocarcinoma to the hypogastric and sacral lymph nodes Retroperitoneal periaortic lymphoma Adrenal gland mass
x
Retroperitoneal periaortic histiocytic sarcoma Adrenal gland mass Retroperitoneal periaortic neuroendocrine carcinoma Retroperitoneal periaortic lymphoma Metastasis from ovaric cystoadenocarcinome to the medial iliac lymph nodes Congenital aneurysm of the caudal vena cava
Presence of acquired porto-systemic shunts. REFERENCES
1. Huntington GS, Mcclure CFW. The development of the veins in the domestic cat (Felis domestica) with especial reference, (1) to the share taken by the supracardinal veins in the development of the postcaval and azygos veins and (2) to the interpretation of the variant conditions of the postcava and its tributaries as found in the adult. Anat Rec 1920;20:1–30. 2. Corniellie P and Simoens P. Prenatal development of the caudal vena cava in mammals: review of the different theories with special reference to the dog. Anat Histol Embryol 2005;34:364–372. 3. Hunt GB, Bellenger CR, Borg R, Youmans KR, Tisdall PLC, Malik R. Congenital interruption of the portal vein and caudal vena cava in dogs: six case reports and a review of the literature. Vet Surg 1998;27:203–215. 4. Bezuidenhout AJ. Veins. In: Evans HE (ed): Miller’s Anatomy of the Dog. Saunders MO, 2013;505–534. 5. Pagani JJ, Thomas JL, Bernardino ME. Computed tomographic manifestations of abdominal and pelvic venous collaterals. Radiology 1982;142:415–419. 6. Sonin AH, Mazer MJ, Powers TA. Obstruction of the inferior vena cava: a multiple-modality demonstration of causes, manifestations, and collateral pathways. RadioGraphics 1992;12:309–322. 7. Kapur S, Paik E, Rezaei A, Vu ND. Where there is blood there is a way: unusual collateral vessels in superior and inferior vena cava obstruction. RadioGraphics 2010;30:67–78. 8. Saridomichelakis MN, Koutinas CK, Souftas V, Kaldrymidou H, Koutinas AF. Extensive caudal vena cava thrombosis secondary to unilateral renal tubular cell carcinoma in a dog. J Small Anim Pract 2004;45:108–112.
9. Jaffe MH, Grooters AM, Partington BP, Camus AC, Hosgood G. Extensive venous thrombosis and hind-limb edema associated with adrenocortical carcinoma in a dog. J Am Anim Hosp Assoc 1999;35:306– 310. 10. LeGrange SN, Fossum TW, Lemire T, Storts RW, Thomas JS. Thrombosis of the caudal vena cava presenting as an unusual cause of an abdominal mass and thrombocytopenia in a dog. J Am Anim Hosp Assoc 2000;36:143–151. 11. Lisciandro GR, Harvey HJ, Beck KA. Automobile-induced obstruction of the intrathoracic caudal vena cava in a dog. J Small Anim Pract 1995;36:368–372. 12. Stauthammer C, Tobias A, France M, Olson J. Caudal vena cava obstruction caused by redundant pacemaker lead in a dog. J Vet Cardiol 2009;11:141–145. 13. Font A, Closa JM. Ultrasonographic localization of a caudal vena cava thrombus in a dog with leishmaniasis. Vet Radiol Ultrasound 1997;38:394–6. 14. Malik R, Hunt GB, Chard RB, Allan GS. Congenital obstruction of the caudal vena cava in a dog. J Am Vet Med Assoc 1990;197:880– 882. 15. Mookadam F, Rowley VB, Emani UR, et al. Aneurysmal dilatation of the inferior vena cava. Echocardiography 2011;28:833–842. 16. Zwingenberger AL, Spriet M, Hunt GB. Imaging diagnosis-portal vein aplasia and interruption of the caudal vena cava in three dogs. Vet Radiol Ultrasound, 2011;52:444–447.
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17. Schwarz T, Rossi F, Wray JD, et al. Computed tomographic and magnetic resonance imaging features of canine segmental caudal vena cava aplasia. J Small Anim Pract 2009;50:341–349. 18. d’Anjou MA, Huneault L. Imaging diagnosis: complex intrahepatic portosystemic shunt in a dog. Vet Radiol Ultrasound 2008;49: 51–5. 19. Bertolini G, Rolla EC, Zotti A, Caldin M. Three-dimensional multislice helical computed tomography techniques for canine extra-hepatic porto-systemic shunt assessment. Vet Radiol Ultrasound 2006;47:439– 443. 20. Bertolini G. Acquired portal collateral circulation in the dog and cat. Vet Radiol Ultrasound 2010;51:25–33. 21. d’Anjou MA, Penninck D, Cornejo L, Pibarot P. Ultrasonographic diagnosis of portosystemic shunting in dogs and cats. Vet Radiol Ultrasound 2004;45:424–437. 22. Davis MK, Schochet RA, Wrigley R. Ultrasonographic identification of vascular invasion by adrenal tumors in dogs. Vet Radiol Ultrasound 2012;53:442–445. 23. Sharpley J, Thode H, Sestina L, Park R, Monnet E, Kraft SL. Distal abdominal aortica thrombosis diagnosed by three-dimensional
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contrast-enhanced magnetic resonance angiography. Vet Radiol Ultrasound 2009;50:370–375. 24. Mai W. Multiphase time-resolved contrast enhanced portal MRA in normal dogs. Vet Radiol Ultrasound 2009;50:52–57. 25. Morandi F, Cole CR, Echandi RL, Daniel GB. Transplenic portal scintigraphy using 99mTc-mebrofenin in normal dogs. Vet Radiol Ultrasound 2007;48:286–291. 26. Zwingenberger AL, Schwarz T. Dual-phase CT angiography of the normal canine portal and hepatic vasculature. Vet Radiol Ultrasound 2004;45:117–124. 27. Dhekne RD, Moore WH, Long SE. Radionuclide venography in iliac and inferior vena caval obstruction. Radiology 1982;144:597–602. 28. Dahan H, Arriv´e L, Cholley-Monnier L, Le Hir P, Zins M, Tubiana JM. Cavoportal collateral pathways in vena cava obstruction: imaging feature. Am J Roentgenol 1998;171:1405–1411. 29. Shigeaki U, Takashi K, Kaori T, Hisato K, Keizo A. Vascular dilatation in the pelvis: identification with CT and MR imaging. RadioGraphics 2004;24:193–208. 30. Melville GK. The mechanical effects of the gravis uterus in late pregnancy. J Obstet Gynaecol Br 1965;72:513–529.
Collateral venous pathways develop in dogs with obstruction or increased blood flow resistance at any level of the caudal vena cava in order to maintain venous drainage to the right atrium. The purpose of this retrospective study was to describe the sites, causes of obstruction, and configurations of venous collateral pathways for a group of dogs with caudal vena cava obstruction. Computed tomography databases from two veterinary hospitals were searched for dogs with a diagnosis of caudal vena cava obstruction and multidetector row computed tomographic angiographic (CTA) scans that included the entire caudal vena cava. Images for each included dog were retrieved and collateral venous pathways were characterized using image postprocessing and a classification system previously reported for humans. A total of nine dogs met inclusion criteria and four major collateral venous pathways were identified: deep (n = 2), portal (n = 2), intermediate (n = 7), and superficial (n = 5). More than one collateral venous pathway was present in 5 dogs. An alternative pathway consisting of renal subcapsular collateral veins, arising mainly from the caudal pole of both kidneys, was found in three dogs. In conclusion, findings indicated that collateral venous pathway patterns similar to those described in humans are also present in dogs with caudal vena cava obstruction. These collateral pathways need to be distinguished from other vascular anomalies in dogs. Postprocessing of multidetector-row CTA images allowed delineation of the course of these complicated venous pathways and may be a helpful adjunct C 2014 American College of Veterinary Radiology. for treatment planning in future cases. Key words: angiography, caudal vena cava obstruction, collateral vessels, computed tomography.
Introduction
T
blood flow resistance at any level of the caudal vena cava can lead to collateral vein formation to maintain venous drainage to the right atrium. The pattern of collateral venous pathways can also be predicted on the basis of the level of the obstruction.5–7 In dogs, caudal vena cava obstructions or increases in flow resistance have been most commonly described as acquired conditions, typically caused by neoplasia,8–10 trauma,11,12 and thrombosis.13 Congenital obstructive conditions of the caudal vena cava have been rarely reported in humans and dogs. These have included membranous obstructions, segmental dilation, or aneurysm due to congenital wall weakness or other developmental disorders.14,15 Computed tomographic angiography (CTA) has been applied in veterinary medicine for the evaluation of vascular abnormalities,16,17 shunts,18,19 and collateral vessels.20 Volume rendering of CTA datasets has been reported to facilitate comprehension and classification of complex vascular abnormalities. Other imaging modalities used to study vascular anatomy and vascular obstructions have included ultrasound,21,22 MRI,23,24 and scintigraphy.25 The CTA appearance of congenital caudal vena cava anomalies have been previously described in the veterinary literature.16,17 However, there is lack of published information on the CTA
HE CAUDAL VENA cava (vena cava caudalis) is the largest
vein that brings deoxygenated blood from the tissues of the body to the right atrium of the heart. In adult mammals, the caudal vena cava is typically a single right-sided retroperitoneal vessel and is anatomically subdivided into five segments with different developmental origins: prerenal, renal, prehepatic, hepatic, and posthepatic segments.1–3 In dogs, the caudal vena cava begins with the confluence of the caudal iliac veins and lies between the left and right psoas muscles in the retroperitoneal space. More cranially, the vein tunnels through the caudate lobe of the liver and penetrates the diaphragm through the foramen venae cavae. The intrathoracic part of the caudal vena cava lies in the plica venae cavae, before finally converging into the right atrium.4 In humans, chronic obstructions or increases in From the Department of Clinical Sciences, Facult´e de M´edecine V´et´erinaire, Universit´e de Montr´eal, 3200 Rue Sicotte, J2S7C6, Sainte Hyacinthe, Qu´ebec, Canada (Specchi, Carmel, d’Anjou) and the San Marco Veterinary Clinic, Via Sorio 114/c, 35141, Padua, Italy (Bertolini). Portions of this study were presented at the ACVR Annual Scientific Meeting in Savannah, Georgia, 2013. Address correspondence and reprint requests to Swan Specchi at the above address. E-mail: [email protected] Received August 4, 2013; accepted for publication January 17, 2014. doi: 10.1111/vru.12167
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FIG. 1. Illustrations of the appearance of the four major venous collateral pathways in dogs affected by occlusion of the caudal vena cava based on multidetector computed tomographic angiography and three-dimensional volume rendering. CVC, caudal vena cava; CrCV, cranial vena cava; dCIV, deep circumflex iliac vein; PV, portal vein; AV, azygos vein; LVs, lumbar veins; CdMV, caudal mesenteric vein; CrMV, cranial mesenteric vein; ltCV, left colic vein; ltGV, left gonadal vein; dCIL, deep circumflex iliac vein. (A) Schematization of a superficial collateral pathway. Note the dorsal subcutaneous tortuous vessels draining blood from the deep circumflex iliac veins into the 11th intercostal veins and finally the azygos vein. Alternatively, the circumflex iliac vein can anastomose with the caudal epigastric and caudal superficial epigastric veins ending in the internal thoracic veins. (B) Schematization of an intermediate collateral pathway. Note the tortuous vessels around the ureters and uterine horns draining blood from the pre-obstructed caudal vena cava (through the iliac veins) to the renal veins and gonadal veins, respectively, and finally into the postobstructed caudal vena cava (cavo-caval shunt). (C) Schematization of a portal collateral pathway. Note the multiple tortuous vessels around the rectum representing the rectal plexi, which permit communication between the caudal vena cava system (iliac veins) and portal system (left colic vein and cranial mesenteric vein). This pathway could be considered a cavo-portal shunt with a hepatopetal flow. (D) Schematization of a deep collateral pathway. Note the multiple enlarged lumbar veins draining blood from the obstructed caudal vena cava to the internal vertebral venous plexus with blood draining ahead into the azygos vein and finally inside the right atrium of the heart.
appearance of caudal vena cava collateral pathways in dogs. The purpose of this retrospective study was to describe the CTA characteristics of collateral venous pathways in a group of dogs with caudal vena cava obstruction.
Materials and Methods Image databases of the San Marco Veterinary Clinic and Centre Hospitalier V´et´erinaire de l’Universit´e de Montreal were searched from 2005 to 2012 for dogs with caudal vena cava obstruction and contrast-enhanced CT scans. Scans meeting initial inclusion criteria were retrieved and examined. Dogs were included in the study if the entire caudal vena cava was present in postcontrast CT scans (from the common iliac veins confluence to the right atrium), and if obstruction or conditions potentially leading to increased caudal vena cava flow resistance were documented. For each included dog, CT image datasets were transferred from hospital picture archiving and communication systems (PACS) to a dedicated image analysis workstation (ADW 4.0 and 4.6, GE Medical Systems, Mississauga, ON, Canada and Milan, Italy). Both nonvascular contrastenhanced CT and CTA studies were evaluated. Images were analyzed by two board-certified veterinary radiologists (E.N.C. and M.A.D.), a second year resident (S.S.), and a veterinarian with more than 10 years of experience in multidetector row CT imaging (G.B.). Images were first interpreted independently and then interpreted a second
time by all authors together to reach a consensus. The following CT characteristics were recorded for each dog: (i) site of suspected caudal vena cava obstruction: prerenal (from iliac vein confluence to the renal veins), renal (between the renal veins), prehepatic (from the renal veins and the hepatic veins), hepatic, and posthepatic (from the liver to the right atrium); and (ii) presence and configuration of venous collateral pathways (defined based on previously published classification schemes used in humans for inferior vena cava collateral pathways).6 Readers used postprocessing techniques such as multiplanar reformatting, maximum intensity projection, and three-dimensional (3D) volume rendering as aids for visualizing the venous collaterals and characterizing patterns. Automatic and manual segmentation methods were used to enhance the caudal vena cava and its collaterals in the images. Arterial and portal vessels, as well as lymphatic vessels were carefully evaluated in each case. Finally, other nonvascular abnormal CT features were recorded. Medical records were also reviewed and the mechanism of caudal vena cava obstruction or suspected increased resistance was identified. When available, the final diagnosis was recorded.
Results Nine dogs (four males and five females) met inclusion criteria for the study. Four were mixed breed dogs, one Bullmastiff, one Maltese, one Rottweiler, and two American
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FIG. 3. Volume-rendered, left lateral CTA image of a dog with obstruction of the caudal vena cava due to a retroperitoneal peri-aortic lymphoma resulting in a superficial and intermediate (peri-ureteric) collateral pathways and enlarged subcapsular veins. Note the enlarged deep circumflex iliac vein (short white arrow) and the enlarged caudal epigastric vein (long white arrows). The peri-ureteric vein is also visible (white arrow-heads). The asterisk marks tortuous subcapsular veins draining in the deep circumflex iliac vein.
FIG. 2. Volume rendered CTA images, illustrating left lateral (A) and dorsal (B) views of a dog with obstruction of the caudal vena cava due to a retroperitoneal periaortic lymphoma resulting in a superficial collateral pathway. Note the enlarged deep circumflex iliac veins (arrows) and the tortuous superficial subcutaneous vessels (asterisks).
Staffordshire Bull Terriers. Mean (range) age and body weight were 8.4 years (0.75–11.5) and 27.9 kg (3.1–50), respectively. All CT studies were performed with the same 16-row multidetector CT unit (Light Speed 16 slice, General Electric Healthcare, Medical Systems, Milwaukee, WI) with dogs anaesthetized and placed in ventral or dorsal recumbency. Positive pressure ventilation was employed during image acquisition to prevent motion artifacts. In one center (San Marco), images were acquired in helical scan mode, at 120 kV and 200 mAs tube settings, a pitch of 0.562:1 and 1.25 mm slice thickness with 50% overlap with a 0.7 s rotation time and reconstructed with a nonenhancing nonsmoothing algorithm. Contrast-enhanced images were then obtained using a dosage of 640 mgI/kg of iodixanol (Visipaque 320, General Electric Healthcare, Milan, Italy) injected into a cephalic vein through an IV catheter. The contrast medium was injected (3–5 ml/s) in bolus, followed by a saline flush (same injection rate) via a
dual-syringe injector system (Medrad Stellant CT Injection System, Bayer, Milan, Italy). A fixed injection-to-scan delay of 20 s was used for routine nonvascular abdominal contrast-enhanced image assessments. The angiographic studies were performed with the individual transit time determined using a bolus triggering technique, as previously described.19 At the second institution, CT scans were acquired in helical scan mode, at 120 kV and 200 mAs tube settings, at a pitch of 0.938:1 and 1.25 mm slice thickness with 50% overlap at 1 s rotation time and transverse images were reconstructed with a medium-high spatial-frequency soft tissue algorithm. CT-angiography was performed following a previously described protocol26 using a dosage of 600 mgI/kg of iopamidol (Isovue 300, ER Squibb & Sons Company, Princeton, NJ, and Bracco Industria Chimica, Milan, Italy) at 5 ml/s injection rate in the external jugular vein (Medrad EnVision CT, Bayer, ON, Canada). Four main venous collateral pathway patterns were identified with features similar to the human classification scheme proposed by Sonin et al.6 : Pattern 1: Enlargement of the iliac circumflex veins draining blood from the common iliac veins into cranial and caudal superficial branches of the iliac circumflex veins localized in the dorsal abdominal subcutaneous tissues. These branches anastomosed cranially with the 11th intercostal vein ending finally in the azygos vein (Fig. 1A, 2). Alternatively, the deep circumflex iliac vein
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FIG. 4. Three different volume rendered, ventral CTA images of a dog with congenital aneurysm of the caudal vena cava (asterisk) and intermediate pathway (right gonadal vein). Note the enlarged right gonadal (arrow) and right phrenico-abdominal veins ending in the caudal vena cava (arrowheads, in A and B).
anastomosed with the caudal epigastric and caudal superficial epigastric veins ending in the thoracic veins (Fig. 3). Most features of this pattern, except for the anastomosis with the 11th intercostal vein, resembled the superficial collateral pathway reported in humans.6 Pattern 2: Enlargement of the gonadal veins and periureteric veins draining blood to the left renal vein and caudal vena cava from some tortuous vessels inside the uterine and urinary bladder (Figs. 1B, 4, and 5). This pattern is similar to the intermediate collateral pathway reported in humans.6 Pattern 3: Enlargement of the left colic vein and cranial mesenteric vein draining blood from numerous tortuous vessels inside the rectal wall and from the jejunal veins into the portal vein (Figs. 1C and 5). This pattern is similar to the portal collateral pathway reported in humans.6 Pattern 4: Enlargement of the lumbar veins and/or vertebral venous system draining blood from the caudal vena cava into an enlarged right azygos vein (Figs. 1D and 6). This pattern resembled the deep collateral pathway reported in humans.6 In addition to these four main patterns, we also identified unique patterns and presentations:
A: In 3/9 dogs, renal subcapsular collateral veins arising mainly from the caudal pole of both kidneys were identified, draining the subcapsular veins and ending caudally in the ipsilateral circumflex iliac vein (Fig. 3). B: In 3/9 patients, abdominal lymphatic vessels draining in the cisterna chili were visible and subjectively dilated (Fig. 7). C: Two patients with obstruction of the hepatic and posthepatic segments of the caudal vena cava showed abdominal fluid and multiple acquired splenogonadal portosystemic shunts (Budd-Chiari like syndrome). D: One of our dogs had dilatation of the caudal vena cava, aneurysm of the renal segment of the caudal vena cava and left renal vein, azygos continuation of the caudal vena cava, and intermediate collateral circulation via the left gonadal (ovarian or testicular) vein (Fig. 4). Eight of nine dogs had a mass invading the caudal vena cava. Six of eight of these dogs had a histological or cytological diagnosis of neoplastic mass. Five dogs presented more than one collateral venous pathway. Abdominal effusion was detected in 5/9 dogs. In two of these, slight to moderate effusion surrounding an abdominal mass was observed, whereas severe diffuse effusion was present in the other
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FIG. 5. Volume-rendered ventral CTA image of a dog with caudal vena cava obstruction due to a right adrenal gland mass resulting in portal and intermediate (peri-ureteric) collateral pathways. Note the enlargement of the left colic vein (lfCV) draining into the caudal mesenteric vein (CdMV) and finally into the portal vein (PV). The caudal vena cava is abruptly interrupted. CrMV, cranial mesenteric vein.
three. Unilateral retroperitoneal effusion was identified in two dogs. Detailed descriptions of the sites and extension of caudal vena cava obstruction, cytological and/or histological diagnoses, and concomitant vascular anomalies are provided for each dog in Appendix 1.
Discussion Similar to those previously reported in humans,5–7,27,28 four main collateral venous pathways were identified in the dogs of the present study. The superficial pathway allows blood to flow from the external iliac veins, through the circumflex iliac veins to the caudal epigastric and caudal superficial epigastric veins. In humans, these subcutaneous vessels terminate inside the subclavian vein bypassing the internal mammary vein or lateral thoracic vein.29 Interestingly, we noted that in some patients the right azygos vein could drain part of the blood coming from the subcutaneous vessels of the superficial pathway. To the authors’ knowledge, this variant has not been reported in humans. The intermediate pathway is most frequently found in humans with occlusion of the renal veins and renal segment of the inferior vena cava.27,29 The intermediate pathway with gonadal veins (ovarian or testicular) is more frequently reported on the left side in humans compared to the right. This is probably because the right go-
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nadal vein empties directly into the prerenal segment of the inferior vena cava, which in these patients could be occluded, whereas the left gonadal vein usually empties into the left renal vein.6 In humans, gonadal and periureteric veins communicate with the internal iliac vein by the vescical and uterine venous plexi. We identified this pathway in 8/9 dogs and in seven of them the occlusion involved the renal segment. In the remaining dog, the occlusion was at the level of the prerenal segment. Even with the few cases reported here, the gonadal and periureteric veins seem to be the preferred collaterals in dogs with occlusion of the renal veins and renal segment of the caudal vena cava as reported in humans. In these patients, the blood flows from caudal to cranial bypassing the site of obstruction through the gonadal and periureteric veins, in particular draining the blood from the pre-occluded segment of the caudal vena cava to the postoccluded segment. The intermediate pathway effectively acts as a cavocaval collateral pathway.7 Portal collateral pathways have been subdivided into five types in humans,28 but only one subtype was found in our patients. In our dogs, collateral vessels were similar to human patients with a cavo-mesenteric-portal collateral pathway. In these patients, the rectal venous plexus allows communication between the caudal vena cava and the portal system.27–29 In humans/dogs, the inferior/caudal and middle rectal plexus are drained by the internal iliac vein, while the superior/cranial venous rectal plexus is drained by the inferior/caudal mesenteric vein. In our dogs, tortuous vessels were identified inside the rectal wall, probably representing an enlargement of the physiologically nonvisible rectal plexus. In human, this pathway is considered a cavoportal connection between the caudal vena cava and the portal vein and may be confused for portosystemic shunting. The hepatopetal flow can help distinguish these cavoportal pathways from portocaval shunts that carry a hepatofugal flow. In CT-angiography series, the level of attenuation of contrast medium in collateral vessels is an important determinant, as it matches one of the venous system draining into these vessels. Therefore, the attenuation of contrast medium in the collateral vessel will match one of the caudal vena cava in case of cavoportal pathway, whereas it will match the portal circulation in the case of portocaval shunts.7,10,29 The left colic and caudal mesenteric veins were concomitantly subjectively enlarged in some dogs, which may have been attributed to the formation of shunts between these veins and the caudal vena cava or gonadal vein, as reported in humans.17 Another subtype of portal collateral pathway described in humans is the cavo-renal-portal pathway with subcapsular veins that anastomose with the splenic vein.28 In 3/9 dogs, enlarged, tortuous subcapsular renal veins were also observed, but these connected to the ipsilateral deep circumflex iliac vein, excluding the portal system as part of this pathway and
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FIG. 6. Computed tomographic angiography images from a dog with obstruction of the caudal vena cava due to a retroperitoneal periaortic neuroendocrine carcinoma and resulting in a deep collateral pathway. (A) Transverse view at the thoracic level. Note the enlarged azygos vein (AV) that has the same size as the aorta (Ao). (B) Parasagittal multiplanar reformatted image of the caudal thoracic vertebral column showing an enlarged AV and internal vertebral venous plexus (arrowheads). (C) Volume-rendered image of the thoracic cavity of the same dog. Note the enlarged AV and some lumbar veins (LVs).
being different from the cavo-renal-portal pathway reported in human. We propose that this is a unique feature in canine patients. The other three subtypes of collateral portal pathways described in humans were not recognized in our dogs, but this could be due to the small number of dogs in this study. The deep collateral pathway, the most prevalent in humans, was detected in two of our dogs. Through the lumbar veins and vertebral venous system,29 the blood flows to the right atrium through an enlarged azygos vein. A Budd-Chiari like syndrome was suspected in 2/9 dogs with occlusion of the hepatic and posthepatic segment of the caudal vena cava, peritoneal effusion and acquired splenogonadal portosystemic shunts. Distinction between an intermediate venous collateral pathway involving the gonadal vein and an acquired splenogonadal shunt was based on the difference of origin of the gonadal vein involved. In the first case, the gonadal vein originated caudally from the ovarian and uterine venous plexi, whereas in case of acquired splenogonadal portosystemic shunt the gonadal vein communicated with the splenic vein through an abnormal collateral vessel. In one dog, there was an aneurysm of the renal segment of the caudal vena cava and left renal vein and azygos continuation of the caudal vena cava (Fig. 4). Aneurysm of the caudal vena cava with congenital azygos continuation has been previously reported in one dog.17 In our dog, the combination of ultrasound and CTA findings allowed visualization of engorged abdominal veins with absent/reversed flow into the caudal vena cava, and exclusion of a caval thrombus or other obstructive causes. Due to the absence of hepatomegaly or peritoneal or retroperitoneal
FIG. 7. Computed tomographic angiography images from a dog with congenital aneurism of the caudal vena cava (An). Note the dilated cisterna chyli (asterisk) and the multiples nonenhancing tortuous vessels around it consistent with enlarged lymphatic vessels (arrow heads).
effusion in our dog, a presinusoidal/sinusoidal obliterative cause or a congenital intrinsic weakness of caudal vena cava and renal vein wall was hypothesized. This study was limited by several factors. The retrospective nature of this study prevented us from investigating the potential impact of recumbency on presence and size of collateral venous pathways in dogs. In pregnant women
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lying in supine position, for example, the uterus causes an acute obstruction of the inferior vena cava and the venous return is supplied by the azygos and vertebral veins.30 Dogs in this study were variably positioned in dorsal or ventral recumbency potentially influencing the detection of venous collateral pathways. Moreover, the whole thorax was not imaged in all of our dogs, which may have prevented the detection of additional collaterals. The low number of dogs included in this study prevented a definitive classification of venous collateral pathways for dogs with obstruction of the caudal vena cava. Yet, most features of venous collateral pathways reported in humans were also found in dogs of this study with minor differences.
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In conclusion, findings from the current study indicated that dogs affected by obstruction and/or increased blood flow resistance in the caudal vena cava develop venous collateral pathways that are similar to those previously reported in humans. These venous collaterals should be differentiated from other vascular anomalies. Acquired portosystemic shunts can occur concomitantly with venous collateral pathways in patients affected by a Budd-Chiari like syndrome and this can make interpretation challenging. Multidetector row CTA and postprocessing techniques such as multiplanar reformatting, maximum intensity projection and 3D volume rendering can help more clearly delineate the course and pattern of these complicated collateral venous pathways.
APPENDIX 1. Type of caudal vena cava venous collateral pathway, site of obstruction and presence of acquired portosystemic shunts in nine dogs with caudal vena cava obstruction Pathway Site of obstruction
Dog Superficial Intermediate Portal Deep 1
x
2 3
x x
x
4 5 6 7
x
x x x x
APSS∗
Prerenal
8
x
Prerenal-renal-prehepatic Renal-prehepatic-hepaticposthepatic Prerenal-renal-prehepatic Renal-prehepatic Renal-prehepatic-hepatic Renal-prehepatic-hepaticposthepatic Prerenal
9
x
Renal
∗
x x
x x
x
x
Diagnosis
x
Metastasis from anal sacs adenocarcinoma to the hypogastric and sacral lymph nodes Retroperitoneal periaortic lymphoma Adrenal gland mass
x
Retroperitoneal periaortic histiocytic sarcoma Adrenal gland mass Retroperitoneal periaortic neuroendocrine carcinoma Retroperitoneal periaortic lymphoma Metastasis from ovaric cystoadenocarcinome to the medial iliac lymph nodes Congenital aneurysm of the caudal vena cava
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