Anatomia, Histologia, Embryologia
ORIGINAL ARTICLE
Blood Flows in Tributaries of the Portal Vein: Anatomical and Angiographic Studies in Normal Beagle Dogs G. Mogicato1,2*, G. Vautravers1, P. Meynaud-Collard3, A. Deviers1,2 and J. Sautet1 Addresses of authors: 1 Unit e d’Anatomie – Imagerie – Embryologie, Universite de Toulouse, INP, ENVT, F-31076 Toulouse, France; 2 Institut National de la Sant e et de la Recherche M edicale (INSERM), Imagerie Cerebrale et Handicaps Neurologiques UMR 825, CHU Purpan, F-31024, Toulouse, France; 3 Laboratoire de Chirurgie Exp erimentale du Tissu Osseux et Cartilagineux, Unite de Chirurgie, Universite de Toulouse, INP, ENVT, F-31076 Toulouse, France
*Correspondence: Tel.: +33 561193896; fax: +33 561193224; e-mail: [email protected] With 3 figures and 2 tables Received April 2014; accepted for publication October 2014 doi: 10.1111/ahe.12161
Summary Liver anatomy, particularly its vascularization, has been investigated in many studies in dogs. Knowledge of blood flow from the main tributaries of the portal vein (PV) is necessary to explain the preferential sites of secondary lesions within the liver based on the site of the initial malignant lesion. How these flows come together was established in an earlier ex vivo study. Here, we highlight in vivo the blood flows from the main PV tributaries and their distribution in the liver of normal dogs. Portographs of the main PV tributaries were obtained in seven dogs after injection of an angiographic contrast medium. After euthanasia, the livers and their portal vascularization (PV and tributaries) were extracted for a comparative corrosion cast study. Flows were demonstrated in the cranial mesenteric vein, caudal mesenteric vein and splenic vein. However, no proper flow could be distinguished for the gastroduodenal and ileocolic veins. All these tributaries primarily supply the lateral liver lobes (right or left). Most of our observations indicate that the cranial mesenteric, caudal mesenteric and splenic veins primarily supply the right lateral lobe and the caudate process of the caudate lobe and secondarily the left lateral lobe, left medial lobe and the quadrate lobe. The two other tributaries (gastroduodenal and ileocolic veins) primarily supply the right lateral lobe and the caudate process of the caudate lobe.
Introduction The gross anatomy of the blood supply and biliary drainage in the canine liver has been described in many studies (Vitums, 1959; Kalt and Stump, 1993). More recently, details of the main anatomical variations in ramification of the portal vein and hepatic artery and analyses of the course of their major branches have been reported (Ursic et al., 2007). This is of practical importance in liver surgery because, to a large extent, the dissection planes and incisions depend to a large extent, on vessel anatomy (Bismuth, 1982; Bismuth et al., 1982; Covey et al., 2009). Atypical hepatectomies, especially partial or complete lobar resections, require an accurate knowledge of the internal liver structures (Bismuth, 1982; Niza et al.,
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
2004). Liver haemodynamics in the dog, especially regulation of the portal venous blood flow and pressure both to the liver and within the liver, have been investigated in many studies (Colle et al., 2008; Sartor et al., 2010; Dave et al., 2012; Sakamoto et al., 2012). This knowledge is of paramount importance when the blood supply within the liver is modified, for example by portosystemic shunts or liver surgery (Lee et al., 2006; Furneaux, 2011). The portal vein collects venous blood from all unpaired abdominal organs except the terminal rectum (Evans, 1993). Knowledge of the gross anatomy of the portal vein and its tributaries has been based on a study by Vitums, which described the ramification of the portal vein caudal to the hepatic porta (Vitums, 1959). Other authors have
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examined the ramification of the intrahepatic portal vein (Kalt and Stump, 1993; Ursic et al., 2007). Pironcof carried out ex vivo studies by injecting coloured dyes, contrast media and radioactive isotopes to establish how the flow from the main portal vein tributaries came together in the dog (Pironcof, 1971). These experimental studies consisted of injections into the portal tributaries, during laparotomies performed on animals under general anaesthesia and subsequent direct observation of the liver, in an attempt to explain the preferential sites of secondary lesions within the liver, based on the site of the initial malignant lesion. In humans, it has been suggested that the location of secondary hepatic lesions might be determined by the site of the primary tumour (Ridge et al., 1987; Shirai et al., 1996). Thus, one study demonstrated that right colic neoplasia results in significantly more metastases in the right lobe of the liver than in the left one, whereas secondary hepatic metastases from descending colon cancer are reported throughout the whole organ (Shirai et al., 1996). Use of a porto-scanner in an in vivo study in humans demonstrated the presence of laminar flow, as reported by Pironcof (Garcier et al., 2000). To the best of our knowledge, no in vivo studies to confirm Pironcof’s experimental theories have been carried out in dogs. Nevertheless, combining such investigations with the results of studies of liver haemodynamics and gross anatomy might clarify some of the effects of various digestive disorders on the hepatic parenchyma and also the implications of liver surgery on the alimentary canal. Indeed, secondary hepatic metastases for gastric adenocarcinomas – the gastric tumour type most frequently encountered in dogs (Swann and Holt, 2002) – have also been reported in the dog for intestinal adenocarcinomas and visceral mastocytoma. The aim of our study was therefore (1) to describe in vivo the blood flows in the main tributaries of the portal vein and (2) to study the intrahepatic distribution of these flows.
Materials and Methods Dogs The experimental procedure was carried out in accordance with the Guidelines for the Care and Use of Laboratory Animals (National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, 2011). It had been previously reviewed and accepted by our local academic ethical committee. Seven healthy intact beagle dogs (five males and two females), 25.4 (+/ 1.6) months of age with a mean body weight of 15.3 (+/ 1.5) kg and a body condition score of 3–4, were used.
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The dogs were obtained from an accredited breeder (Avogadro, France). All dogs were considered healthy on the basis of a complete physical examination, and no animal had a clinical history of hepatic disorders or had received any previous treatment. Design of the study The study was carried out in two phases on the same animals: an initial in vivo angiographic study (phase 1) followed by an anatomical approach (phase 2). Phase 1: in vivo angiographic study Extra- and intrahepatic portal vascularization was assessed from intra-operative portal venographs and obtained from the dogs under general anaesthesia. The dogs were pre-anaesthetized/pre-medicated with a combination of morphine (0.1 mg/kg IV) and acepromazine (0.05 mg/kg IV). General anaesthesia was induced with propofol administered to effect before intubation (4–6 mg/kg IV) and thereafter maintained with isoflurane in oxygen. The dogs were placed in dorsal recumbency on the table of fluoroscopy system (Opti 150/30/50C, Siemens, France). The radiographic constants for all the fluoroscopic exams were 64.5 kV and 16 mAs. A median longitudinal laparotomy was performed, the greater omentum was sectioned and the portal vein and its tributaries in the abdominal cavity of the animal were identified. The blood flows in the main portal vein tributaries and their intrahepatic distribution were then investigated. The tributaries examined were the cranial and caudal mesenteric veins, the splenic vein, the gastroduodenal vein and the ileocolic vein so that the results could be compared with those of previous studies (Pironcof, 1971; Garcier et al., 2000). For each portal venogram, a 15 mL bolus of iodine contrast agent (Telebrix 35ND) was injected into different tributaries of the portal vein. Each of the above veins was catheterized with a largebore catheter (10 or 12 gauge). A tributary of the cranial mesenteric vein, the gastroduodenal vein and the ileocolic vein, namely the jejunal vein, the pancreaticoduodenal vein and the right colic vein, respectively, was catheterized. The bolus of contrast agent was injected manually at a flow rate of 2 ml/s. Images were acquired at a rate of 25 per second from the start of the injection until fading of the opacification of the portal vasculature. Two successive injections of contrast agent were administered into each vein, and images were acquired. The injected vessel was then ligated before the next one was catheterized. The catheters were first inserted in the vessel of smallest diameter (jejunal vein) and finally in the vessel of greatest © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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diameter (splenic vein) to ensure that as little modification of the extra and intrahepatic blood flows as possible occurred after vessel ligation. All dynamic portal venograms were recorded on a digital video recorder (DMRE100H, Panasonic). After phase 1, the animals were euthanized with an overdose of pentobarbital (DolethalTM, Vetoquinol, France) (IV). Phase 2: Anatomical approach The portal venograms were then analysed by preparing a corrosion cast of the portal vein for each liver. The caudal vena cava was ligated cranial to the liver after removing the liver from the abdominal cavity. Serous and adipose tissues around the hepatic porta were removed to facilitate visualization and accurate detection of the anatomical structures. The corrosion casting technique has already been described in detail (Tompsett, 1969). First a plastic cannula was inserted in the portal vein after which a mixture consisting of an epoxy resin, a polymerizing agent (AralditeND) and a blue-pigmented polyurethane paste was injected into the portal vein lumen. To slow down the polymerization process during the injection, the livers were placed for 24 h at a temperature of approximately 7°C. The livers were then placed in a hot bath (37°C) with pancreatin (20 g per week) and CO2 bubbling for 6
(a)
Fig. 1. (a) Portovenographic view obtained after injection of contrast medium into the splenic vein. Ventro-dorsal view. 1. Portal vein; 2. Right branch of portal vein; 3. Branch of the right lateral lobe; 4. Branch of the caudate process of the caudate lobe; 5. Left branch of portal vein; 6. Branch of the right medial lobe; 7. Branch of the quadrate lobe; 8. Branch of the left medial lobe; 9. Branches of the left lateral lobe; 10. Branch of the papillar process of the caudate lobe. (b) Portovenographic views obtained after injection of contrast medium into the cranial mesenteric vein. Ventro-dorsal view. b1. immediately after beginning injection; only one part of PV is opacified (blue line). b2. at the end of the injection (yellow line).
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
to 8 weeks and then rinsed with water jets to remove any necrotic liver tissue. Analysis of portal venograms and corrosion casts of the portal vein The portal venograms were assessed by two observers at two non-consecutive times. Both observers were familiar with the portovenography examination procedure described in the section ‘in vivo angiographic study’. All examinations were randomized and blinded. The blood flows in the main portal vein tributaries and the intrahepatic distribution of these flows were determined by performing 56 analyses for each portal vein tributary in the seven healthy intact beagle dogs (2 examinations per dog, 2 injections per dog and 2 examinations per observer). Each observer assessed the blood flows in the main tributaries of the portal vein by answering ‘yes’ or ‘no’ to the question ‘Is the contrast agent in the portal vein fully opaque?’. If the answer was ‘no’, that is, a contrasted blood flow was only apparent in part of the portal vein, the observer was then required to localize the blood flow (right, central or left) in that particular tributary of the portal vein (Fig. 1). To elucidate the intrahepatic distribution of the blood flow in the main tributaries of the portal vein, each observer then compared the extent of opacification brought about the contrast agent in each hepatic lobe.
(b1)
(b2)
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Corrosion casts of the portal vein were used to determine the precise location of this intrahepatic distribution (Fig. 2). All the dynamic portal venograms were examined on videotape, by the two observers at two non-consecutive times, from the start of the injection until fading of the opacification of the portal vasculature. Statistical analysis Normal probability plots were prepared for all the data to see whether the results conformed to a normal distribution. The statistical significance of any differences between the two observers was determined by applying a paired Student’s t-test to the differences obtained between the two observers for the same portal venogram. A probability value of P < 0.05 was taken to indicate statistical significance. For the intrahepatic distribution of blood flow in the main portal vein tributaries, the statistical significance of differences between values was determined by applying a chi-squared test to each portal vein tributary. For this part of our study, the values correspond to the percentages obtained for each lobe per opacification sequence (primary, secondary and tertiary).
Results Blood flows in the main portal vein tributaries Table 1 provides the observations and lateralization of blood flows in the main portal vein tributaries (Table 1).
Fig. 2. Corrosion cast of intrahepatic distribution of portal vein. Visceral surface. 1. terminal bifurcation of portal vein; 2. Right branch of portal vein; 3. Branch of the right lateral lobe; 4. Branch of the caudate process of the caudate lobe; 5. Left branch of portal vein; 6. Branch of the right medial lobe; 7. Branch of the quadrate lobe; 8. Branch of the left medial lobe; 9. Branches of the left lateral lobe; 10. Branch of the papillar process of the caudate lobe.
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No significant differences (P = 0.35) were found between the two observers for any of the portal venogram examinations. Blood flow in only a lateralized part of the portal vein was always visualized for the cranial mesenteric vein and splenic vein, and almost always for the caudal mesenteric vein. On the contrary, the blood flows in the gastroduodenal and ileocolic veins systematically involved the whole portal vein (Fig. 3c). Blood flows into the portal vein for the cranial mesenteric and splenic veins were localized, and the observers were able to visualize blood flow into the right and left portions of the portal vein, respectively (Fig. 3a and b). Lateralization for the caudal mesenteric vein was observed to be variable (left for n = 28 and right for n = 28) (Fig. 3d). Intrahepatic distribution of the blood flows in the main tributaries of the portal vein No significant differences (P = 0.21) were found between the two observers for any of the portal venogram examinations. Table 2 and Figure 3 show the intrahepatic distribution of the blood flows for the five portal vein tributaries investigated. The intrahepatic distribution of the blood flows in all seven dogs accorded with the corrosion casts obtained by anatomical approach. In all livers, the portal vein displayed a similar branching pattern, ramifying to a shorter and smaller right portal branch and a longer left portal branch (Fig. 2). Blood flow from the splenic vein primarily irrigates the left lateral and medial lobes and the quadrate lobe, secondarily the right lateral lobe and the caudate process of the caudate lobe and tertiarily the rest of the liver. Blood flow from the cranial mesenteric vein primarily irrigates the right lateral lobe and the caudate process of the caudate lobe, secondarily the left lateral and medial lobes and the quadrate lobe and tertiarily the rest of the liver. No significant differences were apparent between the hepatic lobes in the irrigation of blood flow from the caudal mesenteric vein. Finally, the blood flow from the gastroduodenal and ileocolic veins primarily irrigates the right lateral lobe and the caudate process of the caudate lobe, secondarily the right medial lobe and tertiarily the rest of the liver. Discussion The aim of our study was to describe in vivo the blood flows in the main tributaries of the portal vein and to study the intrahepatic distribution of these flows, to determine valuable implications of various digestive © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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Table 1. Observations and lateralizations of blood flows of main tributaries of the portal vein (PV) for each observer for all examinations of the portal venograms (n = 56) Tributaries of PV
Cran. mes. v.
Caud. mes. v.
Sp. v.
Observers Blood flow
1 x
2 x
1 x
2 x
1 x
2 x
Lateralization
Righta (n = 26) Leftb (n = 2)
Righta (n = 24) Leftb (n = 4)
Righta (n = 16) Lefta (n = 12)
Righta (n = 14) Lefta (n = 14)
Righta (n = 4) Leftb (n = 24)
Righta (n = 2) Leftb (n = 26)
GD. v.
IC. v.
1 o
1 o
2 o
2 o
Cran. mes. v.: cranial mesenteric vein; Caud. mes. v.: caudal mesenteric vein; SP. v.: splenic vein; GD. v.: gastroduodenal vein; IC. V.: ileocolic vein. x represents visualization of a blood flow for only a part of the portal vein, o represents visualization of a blood flow for the entire of portal vein. Different superscript letters for lateralization represent a significant difference (P < 0.001) between left and right for the same tributary of the portal vein.
Fig. 3. Schematic illustration of the blood flows in the main tributaries of the portal vein ((a) cranial mesenteric vein; (b) splenic vein; (c) gastroduodenal and ileocolic vein; (d) caudal mesenteric vein) and of the intrahepatic distribution of these flows. The position of the arrow in the portal vein (1) indicates the lateralization of the blood flow in the main tributaries according to the two observers. The dark colours (blue/red/green/orange) indicate the intrahepatic primary opacification after injection of contrast medium. The light colours (blue/red/green) indicate the intrahepatic secondary opacification after injection of contrast medium. 1. Portal vein; 2. Right branch of portal vein; 3. Branch of the right lateral lobe; 4. Branch of the caudate process of the caudate lobe; 5. Left branch of portal vein; 6. Branch of the right medial lobe; 7. Branch of the quadrate lobe; 8. Branch of the left medial lobe; 9. Branches of the left lateral lobe; 10. Branch of the papillar process of the caudate lobe.
(a)
(b)
(c)
(d)
disorders of the hepatic parenchyma and conversely the effects of certain liver surgery techniques on the alimentary canal. This original study was initially designed to verify Pironcof’s experimental theories in vivo (Pironcof, 1971). To the best of our knowledge, no description of the flows in the main portal vein tributaries in vivo has previously been published for dogs. We therefore first compared the results obtained for blood flows in the main portal vein tributaries in our study with those obtained in earlier studies. We then described the intrahepatic distribution of these flows. © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
Blood flows in the main tributaries of portal vein Many ex vivo studies have reported the existence of separate blood flows in the portal vein. The most recent experimental studies consisted of injecting different markers (Indian ink, a radiopaque substance, radioactive phosphorus, or radioactive microspheres) into the portal tributaries during laparotomies performed on animals under general anaesthesia, followed by direct observation of the liver ex vivo after euthanasia of the animals (Pironcof, 1971; Greenway and Oshiro, 1972). The authors inferred the existence of separated blood flows in the
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Table 2. Intrahepatic distribution of the blood flows in the tributaries of the portal vein (PV) for the two observers for all examinations of the portal venograms (n = 56) expressed in percentages Right branch of PV
Left branch of PV
Hepatic lobes
Tributaries of portal vein Cranial mesenteric vein
Caudal mesenteric vein
Splenic vein
Gastroduodenal vein
Ileocolic vein
Opacification by contrast agent (sequence)
Right lateral lobe Caudate process (%)
Left lateral lobe Left medial lobe (%)
Right medial lobe Quadrate lobe Papillary process (%)
1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
83.33a 14.29a 0.00a 60.00a 16.67a 25.00a 20.00a 50.00a 16.67a 80.00a 0.00a 33.33a 71.43a 0.00a 0.00a
16.67b 57.14b 20.00b 40.00a 50.00b 0.00b 80.00b 33.33a 0.00b 20.00b 28.57b 66.67b 28.57b 25.00b 66.67b
0.00c 28.57b 80.00c 0.00b 33.33b 75.00c 0.00c 16.67b 83.33c 0.00c 71.43c 0.00c 0.00c 75.00c 33.33c
1, 2 and 3 represent the primary, secondary and tertiary opacifications by contrast agent, respectively. Different superscript letters for percentages represent a significant difference (chi-squared>3.84) between hepatic lobes for the same opacification sequence by contrast agent.
portal vein from their observations. In our study, we were able to directly observe these separate blood flows using portal venography recorded on videotape. Previous animal studies had shown that blood flow from the cranial and caudal mesenteric veins, which drains most of the splanchnic flow, had to be central in the portal vein, whereas blood flow from the other tributaries had to be peripheral in the portal vein: left for the splenic vein and right for the gastroduodenal and ileocolic veins (Pironcof, 1971). In humans, the blood flow in the main tributaries was visualized using a porto-scanner with an iodine containing contrast medium of low osmolality (Garcier et al., 2000). The results of this study concorded with those obtained in animal studies except for the nature of the cranial mesenteric vein flow, which had to be peripheral and not central. Most previous observations are in agreement with our results. However, the nature of the cranial mesenteric vein flow in our study differs from that reported in previous animal studies but concords with the blood flow into the right portion of the portal vein reported in a human in vivo study. This observation reinforces the results obtained for the intrahepatic distribution of blood flows in the second part of our study. Indeed, we showed that blood flow from the cranial mesenteric vein primarily irrigates the right lateral lobe and the caudate process of
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the caudate lobe, receiving ramifications of the right portal branch. This new information is of paramount importance because it throws light on some of the implications of various digestive disorders on the hepatic parenchyma, especially the preferential localization of secondary hepatic metastasis in the case of aggressive intestinal tumours. Conversely, it would also impact the portal blood flow after certain liver surgery techniques, particularly right lobe liver resection, as demonstrated recently in humans (Wu et al., 2011). Intrahepatic distribution of the blood flows in the mainportal vein tributaries The intrahepatic distribution of the blood flows was further localized by examining the corrosion casts. Detailed descriptions of the portal vein ramification were provided in earlier studies (Vitums, 1959; Kalt and Stump, 1993; Ursic et al., 2007). They showed that the smaller right branch divided into two veins which ramified in the caudate process and right lateral lobe, while the larger transversally coursed left branch gave off vessels for the lobes of the central and left liver segments. Our anatomical findings are to a large extent congruent with these earlier results. Moreover, all our corrosion casts revealed a similar portal system pattern. © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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Previous studies ex vivo elucidated the precise destination of the flows in the main portal vein tributaries to the hepatic parenchyma. They showed that blood from the splenic vein drains mainly towards the left lobe of the liver and blood from the ileocolic vein attains the right lobe, while blood from the gastroduodenal vein attains the central lobe. Finally, their results showed that blood from the cranial mesenteric vein is conveyed to the whole of the liver parenchyma (Griffen et al., 1970; Lifson et al., 1970; Pironcof, 1971; Greenway and Oshiro, 1972). Our findings for the cranial mesenteric vein and the gastroduodenal vein were significantly different. Blood flows in these two vessels attain primarily the right lateral lobe and the caudate process of the caudate lobe. This is consistent with the blood flow from the cranial mesenteric vein into the right portion of the portal vein observed in our study. Our results for blood flow from the caudal mesenteric vein, which had never been reported in previous studies, did not reveal any significant primary drain between the hepatic lobes. Methodology – Perspectives Previous studies indicated that the vascular volume of the liver can change in response to various interventions, including anaesthesia and haemorrhage (Noble et al., 1998a,b). These earlier studies indicated that the liver was likely to have a role in controlling the distribution of blood volume. However, in our study, the portographic evaluation of blood flows was carried out on anaesthetized dogs and each tributary of the portal vein was catheterized and ligated. These methods could therefore have impacted the blood flows and have influenced the results of our study even though the catheterizations were first carried out in the vessel of smaller diameter (jejunal vein) and then the vessel of greater diameter (splenic vein), to change as little as possible the extra and intrahepatic blood flows after vessel ligature. Moreover, the bolus of contrast agent was injected manually at a flow rate of 2 ml/s. This flow rate differs from the physiological flow rate and thus indicates a modification of the intraportal rheological conditions. In our study, seven beagle dogs of similar size and weight were used to obtain reproducible and reliable results. The observations were obtained in duplicate from two observers. It would be interesting to study the blood flows in the portal vein tributaries in a larger population of dogs of different sizes, weights and breeds, and thus be able to refine the results concerning the intrahepatic distribution of these flows. It would also be interesting to use an imaging technique which, unlike portography, is able to visualize these blood flows in three-dimensions. Computed tomography © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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(porto-scanner) improves the spatial characterization of blood flows in the portal vein tributaries (Garcier et al., 2000). Conclusion The in vivo observations here presented are largely in agreement with the ex vivo findings reported in previous studies and provide new information concerning the right segment of the liver. Our results can be used to postulate the site of secondary lesions based on the venous flow draining the territory containing the primary lesion and conversely the implications of liver surgery techniques on the alimentary canal. This work could also have clinical applications in the search for the site of the primary lesion when a hepatic metastasis is discovered.
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Lee, K. C., V. J. Lipscomb, C. R. Lamb, S. P. Gregory, J. Guitian, and D. J. Brockman, 2006: Association of portovenographic findings with outcome in dogs receiving surgical treatment for single congenital portosystemic shunts: 45 cases (2000-2004). J. Am. Vet. Med. Assoc. 229, 1122–1129. Lifson, N., D. G. Levitt, W. O. Jr Griffen, and C. J. Ellis, 1970: Intrahepatic distribution of hepatic blood flow: double-input studies. Am. J. Physiol. 218, 1480–1488. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, 2011: Guide for the Care and Use of Laboratory Animals, 8th edn. Washington (DC): National Academies Press (US). Niza, M. M., A. J. Ferreira, M. C. Peleteiro, and C. L. Vilela, 2004: Bacteriological study of the liver in dogs. J. Small. Anim. Pract. 45, 401–404. Noble, B. J., M. J. Drinkhill, D. S. Myers, and R. Hainsworth, 1998a: Blood mobilization from the liver of the anaesthetized dog. Exp. Physiol. 83, 513–522. Noble, B. J., M. J. Drinkhill, D. S. Myers, and R. Hainsworth, 1998b: Reflex control of splanchnic blood volume in anaesthetized dogs. J. Physiol. 513(Pt 1), 263–272. Pironcof, M., 1971: Considerations on laminar currents in portal circulation. J Chir (Paris) 102, 603–612. Ridge, J. A., J. R. Bading, A. S. Gelbard, R. S. Benua, and J. M. Daly, 1987: Perfusion of colorectal hepatic metastases. Relative distribution of flow from the hepatic artery and portal vein. Cancer 59, 1547–1553.
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Sakamoto, Y., M. Sakai, and T. Watari, 2012: Three minimally invasive methods of measuring of portal vein pressure in healthy dogs. J. Vet. Med. Sci. 74, 1299–1302. Sartor, R., M. J. Mamprim, R. F. Takahira, and M. F. de Almeida, 2010: Hemodynamic evaluation of the right portal vein in healthy dogs of different body weights. Acta Vet. Scand. 52, 36. Shirai, Y., T. Wakai, T. Ohtani, Y. Sakai, K. Tsukada, and K. Hatakeyama, 1996: Colorectal carcinoma metastases to the liver. Does primary tumor location affect its lobar distribution? Cancer 77, 2213–2216. Swann, H. M., and D. E. Holt, 2002: Canine gastric adenocarcinoma and leiomyosarcoma: a retrospective study of 21 cases (1986-1999) and literature review. J. Am. Anim. Hosp. Assoc. 38, 157–164. Tompsett, D. H., 1969: Anatomical injections. Ann. R. Coll. Surg. Engl. 45, 108–115. Ursic, M., D. Ravnik, M. Hribernik, J. Pecar, J. Butinar, and G. Fazarinc, 2007: Gross anatomy of the portal vein and hepatic artery ramifications in dogs: corrosion cast study. Anat. Histol. Embryol. 36, 83–87. Vitums, A., 1959: Portal vein in the dog. ZBl. Vet. Med 6, 723–741. Wu, T. J., D. Dahiya, C. S. Lee, C. F. Lee, H. S. Chou, K. M. Chan, and W. C. Lee, 2011: Impact of portal venous hemodynamics on indices of liver function and graft regeneration after right lobe living donor liver transplantation. Liver Transpl. 17, 1035–1045.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
ORIGINAL ARTICLE
Blood Flows in Tributaries of the Portal Vein: Anatomical and Angiographic Studies in Normal Beagle Dogs G. Mogicato1,2*, G. Vautravers1, P. Meynaud-Collard3, A. Deviers1,2 and J. Sautet1 Addresses of authors: 1 Unit e d’Anatomie – Imagerie – Embryologie, Universite de Toulouse, INP, ENVT, F-31076 Toulouse, France; 2 Institut National de la Sant e et de la Recherche M edicale (INSERM), Imagerie Cerebrale et Handicaps Neurologiques UMR 825, CHU Purpan, F-31024, Toulouse, France; 3 Laboratoire de Chirurgie Exp erimentale du Tissu Osseux et Cartilagineux, Unite de Chirurgie, Universite de Toulouse, INP, ENVT, F-31076 Toulouse, France
*Correspondence: Tel.: +33 561193896; fax: +33 561193224; e-mail: [email protected] With 3 figures and 2 tables Received April 2014; accepted for publication October 2014 doi: 10.1111/ahe.12161
Summary Liver anatomy, particularly its vascularization, has been investigated in many studies in dogs. Knowledge of blood flow from the main tributaries of the portal vein (PV) is necessary to explain the preferential sites of secondary lesions within the liver based on the site of the initial malignant lesion. How these flows come together was established in an earlier ex vivo study. Here, we highlight in vivo the blood flows from the main PV tributaries and their distribution in the liver of normal dogs. Portographs of the main PV tributaries were obtained in seven dogs after injection of an angiographic contrast medium. After euthanasia, the livers and their portal vascularization (PV and tributaries) were extracted for a comparative corrosion cast study. Flows were demonstrated in the cranial mesenteric vein, caudal mesenteric vein and splenic vein. However, no proper flow could be distinguished for the gastroduodenal and ileocolic veins. All these tributaries primarily supply the lateral liver lobes (right or left). Most of our observations indicate that the cranial mesenteric, caudal mesenteric and splenic veins primarily supply the right lateral lobe and the caudate process of the caudate lobe and secondarily the left lateral lobe, left medial lobe and the quadrate lobe. The two other tributaries (gastroduodenal and ileocolic veins) primarily supply the right lateral lobe and the caudate process of the caudate lobe.
Introduction The gross anatomy of the blood supply and biliary drainage in the canine liver has been described in many studies (Vitums, 1959; Kalt and Stump, 1993). More recently, details of the main anatomical variations in ramification of the portal vein and hepatic artery and analyses of the course of their major branches have been reported (Ursic et al., 2007). This is of practical importance in liver surgery because, to a large extent, the dissection planes and incisions depend to a large extent, on vessel anatomy (Bismuth, 1982; Bismuth et al., 1982; Covey et al., 2009). Atypical hepatectomies, especially partial or complete lobar resections, require an accurate knowledge of the internal liver structures (Bismuth, 1982; Niza et al.,
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
2004). Liver haemodynamics in the dog, especially regulation of the portal venous blood flow and pressure both to the liver and within the liver, have been investigated in many studies (Colle et al., 2008; Sartor et al., 2010; Dave et al., 2012; Sakamoto et al., 2012). This knowledge is of paramount importance when the blood supply within the liver is modified, for example by portosystemic shunts or liver surgery (Lee et al., 2006; Furneaux, 2011). The portal vein collects venous blood from all unpaired abdominal organs except the terminal rectum (Evans, 1993). Knowledge of the gross anatomy of the portal vein and its tributaries has been based on a study by Vitums, which described the ramification of the portal vein caudal to the hepatic porta (Vitums, 1959). Other authors have
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examined the ramification of the intrahepatic portal vein (Kalt and Stump, 1993; Ursic et al., 2007). Pironcof carried out ex vivo studies by injecting coloured dyes, contrast media and radioactive isotopes to establish how the flow from the main portal vein tributaries came together in the dog (Pironcof, 1971). These experimental studies consisted of injections into the portal tributaries, during laparotomies performed on animals under general anaesthesia and subsequent direct observation of the liver, in an attempt to explain the preferential sites of secondary lesions within the liver, based on the site of the initial malignant lesion. In humans, it has been suggested that the location of secondary hepatic lesions might be determined by the site of the primary tumour (Ridge et al., 1987; Shirai et al., 1996). Thus, one study demonstrated that right colic neoplasia results in significantly more metastases in the right lobe of the liver than in the left one, whereas secondary hepatic metastases from descending colon cancer are reported throughout the whole organ (Shirai et al., 1996). Use of a porto-scanner in an in vivo study in humans demonstrated the presence of laminar flow, as reported by Pironcof (Garcier et al., 2000). To the best of our knowledge, no in vivo studies to confirm Pironcof’s experimental theories have been carried out in dogs. Nevertheless, combining such investigations with the results of studies of liver haemodynamics and gross anatomy might clarify some of the effects of various digestive disorders on the hepatic parenchyma and also the implications of liver surgery on the alimentary canal. Indeed, secondary hepatic metastases for gastric adenocarcinomas – the gastric tumour type most frequently encountered in dogs (Swann and Holt, 2002) – have also been reported in the dog for intestinal adenocarcinomas and visceral mastocytoma. The aim of our study was therefore (1) to describe in vivo the blood flows in the main tributaries of the portal vein and (2) to study the intrahepatic distribution of these flows.
Materials and Methods Dogs The experimental procedure was carried out in accordance with the Guidelines for the Care and Use of Laboratory Animals (National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, 2011). It had been previously reviewed and accepted by our local academic ethical committee. Seven healthy intact beagle dogs (five males and two females), 25.4 (+/ 1.6) months of age with a mean body weight of 15.3 (+/ 1.5) kg and a body condition score of 3–4, were used.
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The dogs were obtained from an accredited breeder (Avogadro, France). All dogs were considered healthy on the basis of a complete physical examination, and no animal had a clinical history of hepatic disorders or had received any previous treatment. Design of the study The study was carried out in two phases on the same animals: an initial in vivo angiographic study (phase 1) followed by an anatomical approach (phase 2). Phase 1: in vivo angiographic study Extra- and intrahepatic portal vascularization was assessed from intra-operative portal venographs and obtained from the dogs under general anaesthesia. The dogs were pre-anaesthetized/pre-medicated with a combination of morphine (0.1 mg/kg IV) and acepromazine (0.05 mg/kg IV). General anaesthesia was induced with propofol administered to effect before intubation (4–6 mg/kg IV) and thereafter maintained with isoflurane in oxygen. The dogs were placed in dorsal recumbency on the table of fluoroscopy system (Opti 150/30/50C, Siemens, France). The radiographic constants for all the fluoroscopic exams were 64.5 kV and 16 mAs. A median longitudinal laparotomy was performed, the greater omentum was sectioned and the portal vein and its tributaries in the abdominal cavity of the animal were identified. The blood flows in the main portal vein tributaries and their intrahepatic distribution were then investigated. The tributaries examined were the cranial and caudal mesenteric veins, the splenic vein, the gastroduodenal vein and the ileocolic vein so that the results could be compared with those of previous studies (Pironcof, 1971; Garcier et al., 2000). For each portal venogram, a 15 mL bolus of iodine contrast agent (Telebrix 35ND) was injected into different tributaries of the portal vein. Each of the above veins was catheterized with a largebore catheter (10 or 12 gauge). A tributary of the cranial mesenteric vein, the gastroduodenal vein and the ileocolic vein, namely the jejunal vein, the pancreaticoduodenal vein and the right colic vein, respectively, was catheterized. The bolus of contrast agent was injected manually at a flow rate of 2 ml/s. Images were acquired at a rate of 25 per second from the start of the injection until fading of the opacification of the portal vasculature. Two successive injections of contrast agent were administered into each vein, and images were acquired. The injected vessel was then ligated before the next one was catheterized. The catheters were first inserted in the vessel of smallest diameter (jejunal vein) and finally in the vessel of greatest © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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diameter (splenic vein) to ensure that as little modification of the extra and intrahepatic blood flows as possible occurred after vessel ligation. All dynamic portal venograms were recorded on a digital video recorder (DMRE100H, Panasonic). After phase 1, the animals were euthanized with an overdose of pentobarbital (DolethalTM, Vetoquinol, France) (IV). Phase 2: Anatomical approach The portal venograms were then analysed by preparing a corrosion cast of the portal vein for each liver. The caudal vena cava was ligated cranial to the liver after removing the liver from the abdominal cavity. Serous and adipose tissues around the hepatic porta were removed to facilitate visualization and accurate detection of the anatomical structures. The corrosion casting technique has already been described in detail (Tompsett, 1969). First a plastic cannula was inserted in the portal vein after which a mixture consisting of an epoxy resin, a polymerizing agent (AralditeND) and a blue-pigmented polyurethane paste was injected into the portal vein lumen. To slow down the polymerization process during the injection, the livers were placed for 24 h at a temperature of approximately 7°C. The livers were then placed in a hot bath (37°C) with pancreatin (20 g per week) and CO2 bubbling for 6
(a)
Fig. 1. (a) Portovenographic view obtained after injection of contrast medium into the splenic vein. Ventro-dorsal view. 1. Portal vein; 2. Right branch of portal vein; 3. Branch of the right lateral lobe; 4. Branch of the caudate process of the caudate lobe; 5. Left branch of portal vein; 6. Branch of the right medial lobe; 7. Branch of the quadrate lobe; 8. Branch of the left medial lobe; 9. Branches of the left lateral lobe; 10. Branch of the papillar process of the caudate lobe. (b) Portovenographic views obtained after injection of contrast medium into the cranial mesenteric vein. Ventro-dorsal view. b1. immediately after beginning injection; only one part of PV is opacified (blue line). b2. at the end of the injection (yellow line).
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
to 8 weeks and then rinsed with water jets to remove any necrotic liver tissue. Analysis of portal venograms and corrosion casts of the portal vein The portal venograms were assessed by two observers at two non-consecutive times. Both observers were familiar with the portovenography examination procedure described in the section ‘in vivo angiographic study’. All examinations were randomized and blinded. The blood flows in the main portal vein tributaries and the intrahepatic distribution of these flows were determined by performing 56 analyses for each portal vein tributary in the seven healthy intact beagle dogs (2 examinations per dog, 2 injections per dog and 2 examinations per observer). Each observer assessed the blood flows in the main tributaries of the portal vein by answering ‘yes’ or ‘no’ to the question ‘Is the contrast agent in the portal vein fully opaque?’. If the answer was ‘no’, that is, a contrasted blood flow was only apparent in part of the portal vein, the observer was then required to localize the blood flow (right, central or left) in that particular tributary of the portal vein (Fig. 1). To elucidate the intrahepatic distribution of the blood flow in the main tributaries of the portal vein, each observer then compared the extent of opacification brought about the contrast agent in each hepatic lobe.
(b1)
(b2)
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Corrosion casts of the portal vein were used to determine the precise location of this intrahepatic distribution (Fig. 2). All the dynamic portal venograms were examined on videotape, by the two observers at two non-consecutive times, from the start of the injection until fading of the opacification of the portal vasculature. Statistical analysis Normal probability plots were prepared for all the data to see whether the results conformed to a normal distribution. The statistical significance of any differences between the two observers was determined by applying a paired Student’s t-test to the differences obtained between the two observers for the same portal venogram. A probability value of P < 0.05 was taken to indicate statistical significance. For the intrahepatic distribution of blood flow in the main portal vein tributaries, the statistical significance of differences between values was determined by applying a chi-squared test to each portal vein tributary. For this part of our study, the values correspond to the percentages obtained for each lobe per opacification sequence (primary, secondary and tertiary).
Results Blood flows in the main portal vein tributaries Table 1 provides the observations and lateralization of blood flows in the main portal vein tributaries (Table 1).
Fig. 2. Corrosion cast of intrahepatic distribution of portal vein. Visceral surface. 1. terminal bifurcation of portal vein; 2. Right branch of portal vein; 3. Branch of the right lateral lobe; 4. Branch of the caudate process of the caudate lobe; 5. Left branch of portal vein; 6. Branch of the right medial lobe; 7. Branch of the quadrate lobe; 8. Branch of the left medial lobe; 9. Branches of the left lateral lobe; 10. Branch of the papillar process of the caudate lobe.
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No significant differences (P = 0.35) were found between the two observers for any of the portal venogram examinations. Blood flow in only a lateralized part of the portal vein was always visualized for the cranial mesenteric vein and splenic vein, and almost always for the caudal mesenteric vein. On the contrary, the blood flows in the gastroduodenal and ileocolic veins systematically involved the whole portal vein (Fig. 3c). Blood flows into the portal vein for the cranial mesenteric and splenic veins were localized, and the observers were able to visualize blood flow into the right and left portions of the portal vein, respectively (Fig. 3a and b). Lateralization for the caudal mesenteric vein was observed to be variable (left for n = 28 and right for n = 28) (Fig. 3d). Intrahepatic distribution of the blood flows in the main tributaries of the portal vein No significant differences (P = 0.21) were found between the two observers for any of the portal venogram examinations. Table 2 and Figure 3 show the intrahepatic distribution of the blood flows for the five portal vein tributaries investigated. The intrahepatic distribution of the blood flows in all seven dogs accorded with the corrosion casts obtained by anatomical approach. In all livers, the portal vein displayed a similar branching pattern, ramifying to a shorter and smaller right portal branch and a longer left portal branch (Fig. 2). Blood flow from the splenic vein primarily irrigates the left lateral and medial lobes and the quadrate lobe, secondarily the right lateral lobe and the caudate process of the caudate lobe and tertiarily the rest of the liver. Blood flow from the cranial mesenteric vein primarily irrigates the right lateral lobe and the caudate process of the caudate lobe, secondarily the left lateral and medial lobes and the quadrate lobe and tertiarily the rest of the liver. No significant differences were apparent between the hepatic lobes in the irrigation of blood flow from the caudal mesenteric vein. Finally, the blood flow from the gastroduodenal and ileocolic veins primarily irrigates the right lateral lobe and the caudate process of the caudate lobe, secondarily the right medial lobe and tertiarily the rest of the liver. Discussion The aim of our study was to describe in vivo the blood flows in the main tributaries of the portal vein and to study the intrahepatic distribution of these flows, to determine valuable implications of various digestive © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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Table 1. Observations and lateralizations of blood flows of main tributaries of the portal vein (PV) for each observer for all examinations of the portal venograms (n = 56) Tributaries of PV
Cran. mes. v.
Caud. mes. v.
Sp. v.
Observers Blood flow
1 x
2 x
1 x
2 x
1 x
2 x
Lateralization
Righta (n = 26) Leftb (n = 2)
Righta (n = 24) Leftb (n = 4)
Righta (n = 16) Lefta (n = 12)
Righta (n = 14) Lefta (n = 14)
Righta (n = 4) Leftb (n = 24)
Righta (n = 2) Leftb (n = 26)
GD. v.
IC. v.
1 o
1 o
2 o
2 o
Cran. mes. v.: cranial mesenteric vein; Caud. mes. v.: caudal mesenteric vein; SP. v.: splenic vein; GD. v.: gastroduodenal vein; IC. V.: ileocolic vein. x represents visualization of a blood flow for only a part of the portal vein, o represents visualization of a blood flow for the entire of portal vein. Different superscript letters for lateralization represent a significant difference (P < 0.001) between left and right for the same tributary of the portal vein.
Fig. 3. Schematic illustration of the blood flows in the main tributaries of the portal vein ((a) cranial mesenteric vein; (b) splenic vein; (c) gastroduodenal and ileocolic vein; (d) caudal mesenteric vein) and of the intrahepatic distribution of these flows. The position of the arrow in the portal vein (1) indicates the lateralization of the blood flow in the main tributaries according to the two observers. The dark colours (blue/red/green/orange) indicate the intrahepatic primary opacification after injection of contrast medium. The light colours (blue/red/green) indicate the intrahepatic secondary opacification after injection of contrast medium. 1. Portal vein; 2. Right branch of portal vein; 3. Branch of the right lateral lobe; 4. Branch of the caudate process of the caudate lobe; 5. Left branch of portal vein; 6. Branch of the right medial lobe; 7. Branch of the quadrate lobe; 8. Branch of the left medial lobe; 9. Branches of the left lateral lobe; 10. Branch of the papillar process of the caudate lobe.
(a)
(b)
(c)
(d)
disorders of the hepatic parenchyma and conversely the effects of certain liver surgery techniques on the alimentary canal. This original study was initially designed to verify Pironcof’s experimental theories in vivo (Pironcof, 1971). To the best of our knowledge, no description of the flows in the main portal vein tributaries in vivo has previously been published for dogs. We therefore first compared the results obtained for blood flows in the main portal vein tributaries in our study with those obtained in earlier studies. We then described the intrahepatic distribution of these flows. © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
Blood flows in the main tributaries of portal vein Many ex vivo studies have reported the existence of separate blood flows in the portal vein. The most recent experimental studies consisted of injecting different markers (Indian ink, a radiopaque substance, radioactive phosphorus, or radioactive microspheres) into the portal tributaries during laparotomies performed on animals under general anaesthesia, followed by direct observation of the liver ex vivo after euthanasia of the animals (Pironcof, 1971; Greenway and Oshiro, 1972). The authors inferred the existence of separated blood flows in the
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Table 2. Intrahepatic distribution of the blood flows in the tributaries of the portal vein (PV) for the two observers for all examinations of the portal venograms (n = 56) expressed in percentages Right branch of PV
Left branch of PV
Hepatic lobes
Tributaries of portal vein Cranial mesenteric vein
Caudal mesenteric vein
Splenic vein
Gastroduodenal vein
Ileocolic vein
Opacification by contrast agent (sequence)
Right lateral lobe Caudate process (%)
Left lateral lobe Left medial lobe (%)
Right medial lobe Quadrate lobe Papillary process (%)
1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
83.33a 14.29a 0.00a 60.00a 16.67a 25.00a 20.00a 50.00a 16.67a 80.00a 0.00a 33.33a 71.43a 0.00a 0.00a
16.67b 57.14b 20.00b 40.00a 50.00b 0.00b 80.00b 33.33a 0.00b 20.00b 28.57b 66.67b 28.57b 25.00b 66.67b
0.00c 28.57b 80.00c 0.00b 33.33b 75.00c 0.00c 16.67b 83.33c 0.00c 71.43c 0.00c 0.00c 75.00c 33.33c
1, 2 and 3 represent the primary, secondary and tertiary opacifications by contrast agent, respectively. Different superscript letters for percentages represent a significant difference (chi-squared>3.84) between hepatic lobes for the same opacification sequence by contrast agent.
portal vein from their observations. In our study, we were able to directly observe these separate blood flows using portal venography recorded on videotape. Previous animal studies had shown that blood flow from the cranial and caudal mesenteric veins, which drains most of the splanchnic flow, had to be central in the portal vein, whereas blood flow from the other tributaries had to be peripheral in the portal vein: left for the splenic vein and right for the gastroduodenal and ileocolic veins (Pironcof, 1971). In humans, the blood flow in the main tributaries was visualized using a porto-scanner with an iodine containing contrast medium of low osmolality (Garcier et al., 2000). The results of this study concorded with those obtained in animal studies except for the nature of the cranial mesenteric vein flow, which had to be peripheral and not central. Most previous observations are in agreement with our results. However, the nature of the cranial mesenteric vein flow in our study differs from that reported in previous animal studies but concords with the blood flow into the right portion of the portal vein reported in a human in vivo study. This observation reinforces the results obtained for the intrahepatic distribution of blood flows in the second part of our study. Indeed, we showed that blood flow from the cranial mesenteric vein primarily irrigates the right lateral lobe and the caudate process of
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the caudate lobe, receiving ramifications of the right portal branch. This new information is of paramount importance because it throws light on some of the implications of various digestive disorders on the hepatic parenchyma, especially the preferential localization of secondary hepatic metastasis in the case of aggressive intestinal tumours. Conversely, it would also impact the portal blood flow after certain liver surgery techniques, particularly right lobe liver resection, as demonstrated recently in humans (Wu et al., 2011). Intrahepatic distribution of the blood flows in the mainportal vein tributaries The intrahepatic distribution of the blood flows was further localized by examining the corrosion casts. Detailed descriptions of the portal vein ramification were provided in earlier studies (Vitums, 1959; Kalt and Stump, 1993; Ursic et al., 2007). They showed that the smaller right branch divided into two veins which ramified in the caudate process and right lateral lobe, while the larger transversally coursed left branch gave off vessels for the lobes of the central and left liver segments. Our anatomical findings are to a large extent congruent with these earlier results. Moreover, all our corrosion casts revealed a similar portal system pattern. © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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Previous studies ex vivo elucidated the precise destination of the flows in the main portal vein tributaries to the hepatic parenchyma. They showed that blood from the splenic vein drains mainly towards the left lobe of the liver and blood from the ileocolic vein attains the right lobe, while blood from the gastroduodenal vein attains the central lobe. Finally, their results showed that blood from the cranial mesenteric vein is conveyed to the whole of the liver parenchyma (Griffen et al., 1970; Lifson et al., 1970; Pironcof, 1971; Greenway and Oshiro, 1972). Our findings for the cranial mesenteric vein and the gastroduodenal vein were significantly different. Blood flows in these two vessels attain primarily the right lateral lobe and the caudate process of the caudate lobe. This is consistent with the blood flow from the cranial mesenteric vein into the right portion of the portal vein observed in our study. Our results for blood flow from the caudal mesenteric vein, which had never been reported in previous studies, did not reveal any significant primary drain between the hepatic lobes. Methodology – Perspectives Previous studies indicated that the vascular volume of the liver can change in response to various interventions, including anaesthesia and haemorrhage (Noble et al., 1998a,b). These earlier studies indicated that the liver was likely to have a role in controlling the distribution of blood volume. However, in our study, the portographic evaluation of blood flows was carried out on anaesthetized dogs and each tributary of the portal vein was catheterized and ligated. These methods could therefore have impacted the blood flows and have influenced the results of our study even though the catheterizations were first carried out in the vessel of smaller diameter (jejunal vein) and then the vessel of greater diameter (splenic vein), to change as little as possible the extra and intrahepatic blood flows after vessel ligature. Moreover, the bolus of contrast agent was injected manually at a flow rate of 2 ml/s. This flow rate differs from the physiological flow rate and thus indicates a modification of the intraportal rheological conditions. In our study, seven beagle dogs of similar size and weight were used to obtain reproducible and reliable results. The observations were obtained in duplicate from two observers. It would be interesting to study the blood flows in the portal vein tributaries in a larger population of dogs of different sizes, weights and breeds, and thus be able to refine the results concerning the intrahepatic distribution of these flows. It would also be interesting to use an imaging technique which, unlike portography, is able to visualize these blood flows in three-dimensions. Computed tomography © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol.
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(porto-scanner) improves the spatial characterization of blood flows in the portal vein tributaries (Garcier et al., 2000). Conclusion The in vivo observations here presented are largely in agreement with the ex vivo findings reported in previous studies and provide new information concerning the right segment of the liver. Our results can be used to postulate the site of secondary lesions based on the venous flow draining the territory containing the primary lesion and conversely the implications of liver surgery techniques on the alimentary canal. This work could also have clinical applications in the search for the site of the primary lesion when a hepatic metastasis is discovered.
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Lee, K. C., V. J. Lipscomb, C. R. Lamb, S. P. Gregory, J. Guitian, and D. J. Brockman, 2006: Association of portovenographic findings with outcome in dogs receiving surgical treatment for single congenital portosystemic shunts: 45 cases (2000-2004). J. Am. Vet. Med. Assoc. 229, 1122–1129. Lifson, N., D. G. Levitt, W. O. Jr Griffen, and C. J. Ellis, 1970: Intrahepatic distribution of hepatic blood flow: double-input studies. Am. J. Physiol. 218, 1480–1488. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals, 2011: Guide for the Care and Use of Laboratory Animals, 8th edn. Washington (DC): National Academies Press (US). Niza, M. M., A. J. Ferreira, M. C. Peleteiro, and C. L. Vilela, 2004: Bacteriological study of the liver in dogs. J. Small. Anim. Pract. 45, 401–404. Noble, B. J., M. J. Drinkhill, D. S. Myers, and R. Hainsworth, 1998a: Blood mobilization from the liver of the anaesthetized dog. Exp. Physiol. 83, 513–522. Noble, B. J., M. J. Drinkhill, D. S. Myers, and R. Hainsworth, 1998b: Reflex control of splanchnic blood volume in anaesthetized dogs. J. Physiol. 513(Pt 1), 263–272. Pironcof, M., 1971: Considerations on laminar currents in portal circulation. J Chir (Paris) 102, 603–612. Ridge, J. A., J. R. Bading, A. S. Gelbard, R. S. Benua, and J. M. Daly, 1987: Perfusion of colorectal hepatic metastases. Relative distribution of flow from the hepatic artery and portal vein. Cancer 59, 1547–1553.
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