Anatomía de pequeñas venas hepáticas

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    J Hepatobiliary Pancreat Surg (2002) 9:5560

    Basic knowledge of interest

    An anatomical study of short hepatic veins, with special reference todelineation of the caudate lobe for hanging maneuver of the liverwithout the usual mobilization

    Toshio J. Sato1, Ichiro Hirai2, Gen Murakami1, Tetsuhiro Kanamura3, Fumitake Hata4, and Koichi Hirata4

    1 Department of Anatomy, Sapporo Medical University School of Medicine, South 1 West 17, Chuo-ku, Sapporo 060-8556, Japan2 First Department of Surgery, Yamagata University School of Medicine, Yamagata, Japan3 First Department of Surgery, Nara Medical University School of Medicine, Nara, Japan4 First Department of Surgery, Sapporo Medical University School of Medicine, Sapporo, Japan

    only by a finger placed in a pocket-like space between theterminal portions of the middle and right hepatic veins(MHV and RHV). Insertion of the forceps is followed by

    taping, hanging (holding) of the liver, and anterior dis-section alongside the MHV. Because of the lack of mobi-lization, it seems to be a very convenient procedure.

    Although a diffuse distribution of the openings ofveins draining the liver into the IVC was suggestedpreviously (Chang et al.;2 Camargo et al.3), Belghiti etal.1 postulated a longitudinal avascular virtual plane,that would allow the blind insertion of forceps amongthe venous openings in the inside of the IVC. Although,to the best of our knowledge, no anatomical investiga-tions have been carried out since the presentation oftheir methods, some surgeons who have learned of this

    maneuver have started to employ it, especially to pre-pare extended left grafts for living-related liver trans-plantation. Surgeons are expecting that this method willallow them to include the left half of the caudate lobewith its effective drainage veins in the graft, as reportedby Takayama et al.4 with the usual mobilization, butwithout mobilizing the liver. However, if the maneuverof Belghiti et al.1 is employed, the terminal portion ofthe caudate vein, i.e., the thick vein(s) draining Spiegelslobe, should lie on the left side of the forceps, and theopening into the IVC of the inferior right hepatic vein(IRHV) (Makuuchi et al.5), if present, should lie on theright side. Is there really an area free of venous open-

    ings between these veins? Do the openings of otherretrohepatic short hepatic veins lie on the left or theright side of the forceps?

    To answer these questions, we designed this studyto experimentally clarify the topographic relationshipbetween the forceps and various retrohepatic shorthepatic veins, including the IRHV and caudate vein.More specifically, we used anatomical specimens in anattempt to identify the venous openings that lie to theleft and right of the inserted forceps (i.e., the segmentsor subsegments that the veins drain).

    Abstract

    Background/Purpose. The present study was designed to ana-tomically assess a very recently reported hanging maneuver

    of the liver without mobilization, in which forceps areinserted blindly between the inferior vena cava (IVC) andliver parenchyma.Methods. We dissected 56 formalin-fixed livers (1) to deter-mine whether preservation of the caudate vein (the largestvein draining Spiegels lobe) and inferior right hepatic vein(IRHV) was possible and (2) to identify the territories drainedby other, non-preserved short hepatic veins.Results. A potential space for insertion of the forceps wasfound between the openings of the caudate vein and IRHV;however, if preservation of both veins is absolutely necessary,we recommended protecting the IRHV, such as by taping andretracting it. We classified the other short hepatic veins intotwo categories, i.e., those draining the left portal vein territory

    and those draining the right territory. The distributions of theopenings of the veins in these territories overlapped.Conclusions. Clear delineation of the left caudate lobe accord-ing to the drainage veins appeared to be difficult when theliver was divided along a straight line in front of the IVC.

    Key words Caudate lobe Short hepatic vein Inferior venacava Hanging maneuver without mobilization Liver surgery

    Introduction

    Belghiti et al.1 have devised a new maneuver for thesurgical removal of the right lobe of the liver (containinga large hepatocellular carcinoma), with preservation ofthe caudate lobe on the left side. In their procedure,without mobilization of the liver, forceps are insertedinto a potential space between the parenchyma of thecaudate lobe and the retrohepatic inferior vena cava(IVC) from the caudal side, to the cranial side, guided

    Offprint requests to: G. MurakamiReceived: March 22, 2001 / Accepted: August 21, 2001

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    56 T.J. Sato et al.: Anatomy for hanging maneuver without liver mobilization

    Materials and methods

    Fifty-six whole livers, with no evidence of cirrhosis ormacroscopic tumors, were obtained from donated ca-davers after the cadavers had been used for anatomicaldissection by medical or dental students. The liverspecimens did not include any that were too thin or thathad excess upper protrusion of S8 or any in which theleft side of the liver was much smaller than the rightside. After we had opened the IVC on its dorsal side, weconfirmed that all 56 livers were suitable for investiga-tion of the distribution of venous openings.

    The precise course of the forceps inserted ventral tothe IVC by Belghiti et al.1 was not known, because theyinserted the forceps blindly, and because they did notdescribe the course in sufficient detail. We hypothesizedthat there were three possible courses, represented bythree paths of a curved, metal wire (1mm in diameter)placed on the dorsal aspect of the liver (Fig. 1), used

    instead of the forceps ventral to the IVC. The rightcourse extended from the right inferior protrusion ofthe liver (S6a) to a pocket-like space between the MHVand RHV. The left course followed a curved line be-tween the pocket-like space and the deepest point of thegallbladder bed. The third course, the intermediatecourse, lay between the left and right courses.

    After labeling the three hypothetical courses of theforceps on the dorsal aspect of the liver and after depic-tion of the results, we dissected the specimens to iden-tify the drainage territory of the short retrohepatichepatic veins. The territories were identified by the por-

    tal branch supplying them. Spiegels lobe is usually sup-plied by portal vein branches of both left portal vein andhilar bifurcation origin.610 However, we decided that ifwe found a hilar bifurcation branch in this study, wewould consider it to be a left branch, because we believethat, in future it will be possible to include the hilarbifurcation branch in the pedicle for some left-lobe livergrafts. We therefore classified the short veins into sixcategories: (1) caudate veins, one or two veins, over3mm in diameter, draining Spiegels lobe; (2) short he-patic veins from the left caudate lobe (SHV-LC), thindrainage veins (13mm in diameter at their point ofentry into the IVC) arising from the left half of the

    caudate lobe (left portal territory and hilar bifurcationterritory); (3) short hepatic veins from the right caudatelobe (SHV-RC), thin veins (13mm) draining the righthalf of the caudate lobe; (4) IRHV, one or two thickveins over 5mm in diameter at their point of entry intothe IVC and arising from S6; (5) middle right hepaticvein (MRHV) after Couinaud,11 over 5mm in diameter,draining S7, including the dorsolateral paracaval area;12

    (6) SHV-8, vein(s) over 1mm in diameter draining S8,including its most posteromedial territory (the so-calledPV8c territory6,9).

    Results

    General observations

    Examination of the 56 livers revealed 63 thick caudateveins (over 3mm in diameter) draining Spiegels lobe,and 26 IRHVs were identified in 25 of the 56 livers. Thelargest caudate vein was 9.0mm in diameter (average,

    Fig. 1A,B. On which side of the inserted forceps do the ve-nous openings into the inferior vena cava (IVC) lie? An ex-periment in which a metal wire was used instead of forceps

    was performed to determine the answer. Dorsal view of theliver is shown, with A right and B left courses of the wire(the intermediate course is not shown). The right course of thewire lies between the openings of the inferior right hepaticvein (white arrow) and the caudate vein (black arrow),whereas in the left course, the wire crosses the opening of thecaudate vein. Other small venous openings were also identi-fied after this experiment: veins from the portal vein branch ofhilar bifurcation origin (HB), veins of right portal vein origin(R), and veins of S7 and S8 origin (7and 8). The caudal partof Spiegels lobe (asterisks) is supplied by the portal veinbranch of HB origin. Stars, pocket-like spaces between theterminal portions of the right and middle hepatic vein (RHVand MHV); GB, gallbladder; LAL, left anatomical lobe; SP,Spiegels lobe

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    T.J. Sato et al.: Anatomy for hanging maneuver without liver mobilization 57

    5.1mm), whereas the largest IRHV was 12.0mm indiameter (average, 7.4mm). During dissection from thedorsal and cranial aspects of the liver (Fig. 2) performedafter the experiment described below, we checked tosee whether the caudate vein originated from Spiegelslobe irrespective of whether or not a thin tributary fromthe paracaval portion joined the vein. We also identified

    the territory of the other short hepatic veins, althoughthese veins were removed during the deep dissection.

    Distribution of venous openings into the IVC

    The distribution of the venous openings is shown inFig. 3. The openings of the caudate vein, IRHV, andMRHV were located on either the left side or rightside of the IVC, although some openings convergedrelatively to the left side. The openings of the caudatevein were concentrated in the middle one-third of thecraniocaudal axis of the retrohepatic IVC, whereasthe openings of the IRHVs were concentrated in thecaudal one-third. The openings of the SHV-LC andSHV-RC, especially the former, tended to be dispersed.In some specimens, the SHV-LC even emptied intothe IVC to the right of the SHV-RC. Even in the ab-sence of any IRHVs (31 livers), there were no majordifferences from the other specimens (25 livers with

    IRHVs) in the distribution of the venous openings in-side the IVC.

    Experiment using a metal wire instead of forceps

    We identified the veins located to the left and rightof the path of the wire or along the wire when the wirewas positioned along three routes that corresponded topossible paths of the forceps inserted blindly in theprocedure of Belghiti et al.1 (Fig. 1). The results aresummarized in Tables 13.

    The openings of the caudate veins were consistently

    located to the left of the right course, whereas the termi-nal portions of the IRHV and MRHV were also oftenlocated to the left of the wire (Table 1). Moreover,tracing of the right course revealed that the SHV-RC(right territory) as well as the SHV-LC (left caudatedrainage territory) usually emptied into the IVC on theleft side of the wire. By contrast, tracing of the leftcourse (Table 3) showed that the IRHV and MRHValmost always lay on the right side of the wire, whereasthe caudate vein was almost always on the left side. TheSHV-LC, however, often drained into the IVC on theright side of the wires course.

    Discussion

    The implements used in the actual operations per-formed by Belghiti et al.1 and in our experiment weredifferent: we used a thin metal wire instead of relativelythick forceps. When inserted from the caudal side of theliver toward the pocket-like space between the MHVand RHV, the width of the forceps is about 815mmin the middle one-third and caudal one-third of theretrohepatic IVC. This seems to explain why not only all

    Fig. 2A,B. Deep dissections to identify the drainage territoryof the veins. A Dorso-caudal view and B dorsal view. A and

    B are different specimens. A We first identified the coursesof the caudate vein, inferior right hepatic vein (IRHV), andmiddle right hepatic vein. The inferior vena cava IVC andSpiegels lobe (SP) have been reflected cranially. In thesespecimens, the thick caudate veins (stars) are clearly seen,whereas the other short hepatic veins (arrows) are numerousand thin. Note that the caudate veins run along the IVC alongtheir terminal courses. B The next step was the dissection toidentify the borders between S6, S7, S8, and the three territo-ries of the caudate branches of the portal vein: the left portalterritory (LC), the territory of the branch of hilar bifucationorigin (HB), and the right portal territory (RC). The caudatevein (stars) has been cut and partly removed. This Spiegelslobe contains a notch (a white paper has been inserted in it).LigV, Ligamentum venosum; PT, portal trunk; large asterisk,

    pathological indent; small asterisk, dorsolateral paracavalbranch of the posterior sectorial trunk

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    58 T.J. Sato et al.: Anatomy for hanging maneuver without liver mobilization

    Table 1. Right course of the metal wire on the dorsal aspect of the liver and comparison of the locations of the points of entryof the veins into the IVC

    Caudate vein SHV-LC SHV-RC IRHV MRHV SHV-8

    Left side of the wire 63 veins (56 livers) 41 (27) 24 (13) 8 (8) 8 (7) 3 (2)In the path of the wire 0 (0) 3 (2) 0 (0) 13 (13) 9 (8) 1 (1)Right side of the wire 0 (0) 1 (1) 5 (3) 5 (4) 29 (24) 0 (0)

    Total 63 (56) 45 (30) 29 (16) 26 (25) 46 (39) 4 (3)Caudate vein, 1 or 2 thick veins over 3mm in diameter at their junctions with the inferior vena cava (IVC) and originating from Spiegels lobe;SHV-LC, thin drainage vein, 13mm in diameter, arising from the left half of the caudate lobe; SHV-RC, thin drainage vein, 13mm in diameter,from the right half of the caudate lobe; IRHV, 1 or 2 thick veins over 5mm in diameter at their junctions with the IVC and arising from S6;MRHV, drainage veins, over 5mm in diameter, from S7 including the dl-paracaval branch territory; SHV-8, drainage vein(s), over 1mm indiameter, from S8 including the PV8c territory

    Table 2. Intermediate course of the metal wire and comparison of the locations of the points of entry of the veins into the IVC

    Caudate vein SHV-LC SHV-RC IRHV MRHV SHV-8

    Left side of the wire 59 veins (52 livers) 28 (17) 10 (6) 2 (2) 2 (2) 0 (0)In the path of the wire 4 (4) 11 (9) 9 (5) 4 (4) 3 (3) 0 (0)Right side of the wire 0 (0) 6 (4) 10 (5) 20 (19) 41 (34) 4 (3)

    Total 63 (56) 45 (30) 29 (16) 26 (25) 46 (39) 4 (3)

    Abbreviations are same as those in the Table 1

    Table 3. Left course of the wire and comparison of the locations of the points of entry of the veins into the IVC

    Caudate vein SHV-LC SHV-RC IRHV MRHV SHV-8

    Left side of the wire 45 veins (40 livers) 13 (9) 0 (0) 0 (0) 0 (0) 0 (0)In the path of the wire 16 (14) 8 (5) 8 (5) 1 (1) 1 (1) 0 (0)Right side of the wire 2 (2) 24 (16) 21 (11) 25 (24) 45 (38) 4 (3)

    Total 63 (56) 45 (30) 29 (16) 26 (25) 46 (39) 4 (3)

    Abbreviations are same as those in the Table 1

    Fig. 3. Distribution of the openings ofveins, with different drainage territories,into the IVC. The openings of the veinsinto the IVC in the 56 specimens are su-perimposed on a standardized schematicdiagram of the IVC. This is a dorsalview after the dorsal wall of the IVC hasbeen cut and reflected. The caudate veinopenings are concentrated in the middleone-third and on the left side of theretrohepatic IVC, whereas the IRHV joinsthe IVC in its caudal one-third and on theright side. There was no considerable dif-

    ference between the distributions of theopening of the SHV-LC (veins from theleft portal territory) and the SHV-RC(veins from the right portal territory)

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    T.J. Sato et al.: Anatomy for hanging maneuver without liver mobilization 59

    veins along the wire (see Tables 13) but also someveins alongside the wire were damaged during surgery.When the forceps were inserted along the proper course,however, preservation of the caudate vein seemed pos-sible because the openings of the caudate vein was usu-ally localized to the left side of wire. However, theopenings of both the IRHV and the caudate vein weresometimes found to the left of the wires course, possiblybecause of the long extrahepatic course of the IRHV.Moreover, the area of the potential space free of venousopenings, even if such an area existed, was usually nar-rower, i.e., about 515 mm, than the width of the forceps(i.e., 815 mm: see above), making preservation of bothof the caudate vein and the IRHV difficult. Therefore,some pretreatment, such as taping the IRHV beforeinserting the forceps, would seem to be effective if it isnecessary to preserve the IRHV because it drains a largeterritory. Moreover, if care is taken to preserve theIRHV, it would seem that the MRHV would also be

    preserved on the right side of the forceps, because of itslocation further to the right of the openings than theIRHV. Consequently, to preserve the caudate vein dur-ing preparation of extended left-lobe liver grafts by thehanging maneuver without mobilizing the liver, we rec-ommend the right course in our study as the path forinsertion of the forceps, with attention being paid to thequestion of preservation of the IRHV.

    Takayama et al.4 preserved the caudate vein duringliving-related liver transplantation, using a left-lobeliver graft that included the caudate lobe, whereasMiyagawa et al.13 sacrificed the caudate vein, and the

    good results obtained by this group cast doubt on roleof the caudate vein in drainage; moreover, accordingto their results, thin short hepatic veins, such as thosedenoted as the SHV-LC and SHV-RC in the presentstudy, were not responsible for venous drainage of thecaudate lobe. Therefore, the problem concerning thesethin veins seems to be limited to bleeding during andafter insertion of the forceps. Nevertheless, Belghiti etal.1 reported no problem with such bleeding along theIVC. Our recent study14 suggested that the high contentof smooth muscle tissue in the adventitia of the IVCstimulated rapid hemostasis in small hepatic veins. Ifthe caudate vein is successfully preserved during inser-

    tion of the forceps, the next question is how to find andreconstruct the vein in the left-lobe liver graft. It may bedifficult to find the caudate vein during anterior dissec-tion without taping the vein and without mobilization ofthe liver. In contrast to the taping of the IRHV, tapingof the caudate vein appeared to be difficult without livermobilization. However, we think that surgeons will beable to locate the caudate vein in the final step of ante-rior dissection if they separate the caudate lobe fromthe IVC, because the terminal course of the caudatevein runs along the IVC (Fig. 2).

    In addition to the caudate vein arising from Spiegelslobe (usually, from a large part of the left half of thecaudate lobe), we found many other veins arising fromthe left half, i.e., the SHV-LC, as has been reportedby Gadzijev et al.15 and Filipponi et al.;16 however, ourstudy revealed intermingling of the openings of theveins from the right half of the lobe (SHV-RC), ratherthan segregation of the distribution of their openings.Moreover, the openings of the SHV-RC also inter-mingled with those of the IRHV, MRHV, and S8 veins(Fig. 3). Therefore, the short hepatic veins do not indi-cate either the right margin of the caudate lobe or theborder between the right and left halves. Our failure toidentify these borders of the caudate lobe according tothe venous openings was in clear contrast to the resultsof previous studies based on portal ramification(Ungvary,17 Yamamoto,18 Kogure et al.19). Our findingssuggest that, regardless of whether the maneuver ofBelghiti et al.1 is used or the usual procedure with mobi-

    lization is performed, not only the SHV-LC but also theSHV-RC (and the S8 veins as well) are likely to be cutor damaged along the IVC during the preparation ofextended left liver grafts.

    In the present study, the hilar bifurcation territory isincluded into the left caudate lobe (see Materials andmethods). However, in conventional method for pre-paration of left-lobe liver grafts, it might be difficultto reconstruct the caudate branch of hilar bifurcationorigin. Moreover, according to our very recent study,whether the hilar bifurcation branch is present or absentis committed to how the right portal territory extends

    into Spiegels lobe (now submitted). Thus recognitionof the hilar bifurcation territory would provide a newimpact on left-lobe liver grafts as well as conventionallobectomy.

    Acknowledgments. We are grateful to the followingprofessors and their laboratory staff for the use oftheir specimens: (in alphabetical order) Professor H.Abe, Akita University School of Medicine; ProfessorY. Dodo, Tohoku University Graduate School ofMedicine; Professor Y. Fukui, Tokushima UniversitySchool of Medicine; Professor M. Kikuchi, TohokuUniversity School of Dentistry; Professor S. Kitamura,

    Tokushima University School of Dentistry; ProfessorJ. Matsumura, Kyorin University School of Medicine;Professor T. Sato, Tokyo Medical and Dental Univer-sity Graduate School; and Professor T. Yajima, HealthScience University of Hokkaido School of Dentistry.

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