ActaMed.Okayama,2002 Vol.56,No.5,pp.245-253 Copyright ｃ2002byOkayamaUniversityMedicalSchool.
OriginalArticle http://www.lib.okayama-u.ac.jp/www/acta/
HepatopancreaticArterialRing:BilateralSymmetricTypology inHumanCeliaco-MesentericArterialSystem
MotohiroKosaka ,KanjiHoriuchi ,KeiichiroNishida ,TakehitoTaguchi , TakuroMurakami ,andAijiOhtsuka
DepartmentofHumanMorphology, DepartmentofOrthopaedicSurgery,OkayamaUniversityGraduateSchoolof MedicineandDentistry,and DepartmentofRadiologicalTechnology,FacultyofHealthSciences, OkayamaUniversityMedicalSchool,Okayama700-8558,Japan
Theceliacandmesentericarterialsystem includingtheleftgastric,splenic,commonhepatic,and superiormesentericarteriesshowsvarioustypesoforigins,courses,ramificationsandanastomoses. Inordertoexplainthevariousexpressionsofthissystem,wehaveproposedatypologicalmodel,in which celiacomesentericarteriesdevelopaspairedorbilaterallysymmetricalprimordialvessels originatedfrom theanterioraspectoftheaorta,andthesevesselsanastomoseeachotherwith longitudinalandhorizontalpathways.Here,wereport3unusualcasescharacterizedbyarterial rings, formed by the left gastric, left accessory hepatic, proper hepatic, anterior pan- creaticoduodenal, and dorsalpancreatic arteries. The dorsalpancreatic and anterior pan- creaticoduodenalarteriesarelocatedtotherightandleftoftheembryonicpancreasdevelopingin thedorsalmesentery,respectively.Suchhepatopancreaticarterialringssimultaneouslycontaining rightandleftelementscanonlybeexplainedusingourtypologicalmodel,inwhichtheconceptof pairedarteriesorbilateralsymmetryisintroduced.
Keywords:arterialvariation,celiactrunk,superiormesentericartery,typology,bilateralsymmetry
hreeunpairedarteries theceliactrunkandthe tomoses［1-14］.Theceliactrunkoritsbranchesmay T superiorandinferiormesentericarteries usu- alsogiveo oneorboth(leftandright)theinferior allyoriginatefrom theanterioraspectoftheabdominal phrenic arteries［15］. These variations have been aorta,andsupplytheabdominaldigestiveorgansand classifiedandexplainedusingclassicaltypologicalmodels spleen.Amongthese,theceliactrunk,awideventral［16,17］.Theclassicalmodelsarecharacterizedby4 branchjustbelowtheaortichiatus,passesalmosthori- longitudinallyanastomosedvessels(leftgastric,splenic, zontallyforwardofandslightlyabovethepancreasand commonhepatic,andsuperiormesenteric),whichin- splenicvein,thendividingintothefollowing:theleft dependentlyoriginatefrom theabdominalaorta.Some gastric,commonhepatic,andsplenicarteries.These commonvariations,suchashepatomesenterictrunkor threeandthesuperiormesentericarteriesvaryintermsof independentoriginofleftgastricartery,arewellaccount- patternoforigins,courses,ramifications,andanas- edforusingthisclassicmodel,althoughitdoesnot explaintheformationofsomerarevariationssuchas hepatogastricorsplenomesenterictrunkformation.Previ- ReceivedMarch7,2002;acceptedMay23,2002. Correspondingauthor.Phone:＋81-86-235-7089;Fax:＋81-86-235-7095 ously,wepresentedtypologicaldiagramsofthephrenico- E-mail:aiji＠md.okayama-u.ac.jp(A.Ohtsuka) celiaco-mesentericarterialsystem［8,9,15］.These 246 Kosakaetal. ActaMed.Okayama Vol.56,No.5 diagramswereusefulforintroducingtheconceptof ahumangrossanatomycourseformedicalstudentsatthe left-rightbilateralitytoexplainseveralunpairedorunilat- OkayamaUniversityMedicalSchool. eralvariationsinthisarterialsystem. Inthepresentstudy,wepresentrareanomalouscases Results characterizedbyarterialringformationoftheleftgastric- leftaccessoryhepatic-properhepatic-anteriorpancreati- (Fig.1). Theleftgastricandsplenic coduodenal-dorsalpancreaticarteries.Forexplanationof arteriesformedacommontrunkwiththeleftinferior sucharterialringformation,thebilateralityconceptis phrenicarteryandarosefromtheanterioraspectofthe required;somesegmentsoftheringbelongtotheright abdominalaortabeneaththeaortichiatus.Thisphrenico- system,otherstotheleft. gastro-splenictrunkimmediatelygaveo theleftinferior phrenicartery,anddividedintotheleftgastricandsplenic MaterialsandMethods arteriesbehindtheomentalbursa.Theleftgastricartery ascendedalongtheleftgastropancreaticfoldandreached In1996-2000,weencounteredsignificanthepatopan- theupperendofthelessercurvatureofthestomach.The creaticarterialringsin3Japaneseadultcadavers.Age, leftaccessoryhepaticarteryissuedfrom theleftgastric sex,clinicaldiagnosisatdeath,andabdominalsurgical arteryintheleftgastropancreaticfold,thenranalongthe history ofthesecasesaresummarized in Table1. fissure for the ligamentum venosum in the lesser Cadaverswerefixedconventionallybyarterialperfusion omentum,givingabranchtotheesophagus,andreached with10 formalinthroughtherightorleftradialartery, thehepaticportalregion.Thesplenicarterygaveo the andsubsequentlydehydratedwith50-60 ethanolat anteriorrightaccessoryhepaticartery［11］attheupper 40°C.Untildissection,theywerestored,for6months marginofthepancreaticbody,ranleftalongthepancreas, orlonger, in astainless-steelbody storagesystem and reached the hilum ofthe spleen through the (Katoman,Tokyo,Japan).Dissectionwasperformedin phrenicolienalligament. Theanteriorrightaccessory hepaticarterydescendedontheposterioraspectofthe pancreas,turnedrightatitslowermargintoappearin Table1 Generaldescriptionofthecases frontoftheportalvein,andascendedonthepancreatic anteriorsurface, whereitbranched o theanterior Case Sex Age Diagnosisatdeath Abdominalsurgicalhistory superiorpancreaticoduodenal,rightgastroepiploic,and 1 Male 83y Lungcancer No posterior superior pancreaticoduodenalarteries. The 2 Female 83y Pneumonia No anteriorrightaccessoryhepaticartery,givingo theright 3 Male 73yCerebralinfarction No gastricarterytothelessercurvatureofthestomach, y,yearold. ascendedfurtherinthehepatoduodenalligamentalongthe
Table2 AbbreviationsinFigures1-3,5,and6 a:abdominalaorta m2:leftandrightupperventriculararteries u:umbilicalartery c:intercostal(orlumbar)artery m3:leftandrightmiddleventriculararteries v:portalvein d:dorsalpancreaticartery m4:leftandrightlowerventriculararteries w:gastroduodenalartery e:superioranteriorpancreaticoduodenalartery m5:leftandrightupperintestinal(superiormesenteric) x:accessorygastricartery f:inferioranteriorpancreaticoduodenalartery arteries y:rightgastricartery g:leftgastricartery m6:leftandrightlowerintestinal(inferiormesenteric) B:commonbileduct h:commonhepaticartery arteries D:duodenum i:inferiorphrenicartery n:renalartery G:gallbladder ii:internaliliacartery o:leftaccessoryhepaticartery H:liver k1:anteriorrightaccessoryhepaticartery p:properhepaticartery I:intestine k2:posteriorrightaccessoryhepaticartery r:rightgastroepiploicartery K:kidney k3:leftaccessoryhepaticartery s:splenicartery P:pancreas m:superiormesentericartery t:testicular(ovarian)artery S:stomach m1:leftandrightsubphrenicarteries ti:internalthoracicartery Sp:spleen October2002 HepatopancreaticArterialRing 247
Fig.1 Linedrawingrepresentationofcase1.Threeaberrantaccessoryhepaticarteries(k1,k2,andk3)co-exist,andthecommonhepatic arteryislost.Noteacompletearterialringmadeofanastomosedleftandrightaccessoryhepaticarteries(asterisk).Abbreviations:see Table2. anteriorsideoftheportalvein,andreachedthehepatic (Fig.2). Theleftgastricandsplenic portalregion,wheretheanteriorrightaccessoryhepatic arteriesformedacommontrunk(gastro-splenictrunk), andleftaccessoryhepaticarteriesanastomosedtoforman whicharosefrom theanterioraspectoftheabdominal arterialarch.Thus,theseaccessoryhepaticarteries aorta.Theleftgastricarteryranthroughtheleftgas- formedanarterialringaroundthepancreasandlesser tropancreaticfoldtothelessercurvatureofthestomach. omentum.Therightandlefthepaticbranchesarosefrom Thesplenicartery,afterissuingthedorsalpancreatic thishepaticarterialarch. Additionally, thesuperior artery,ranalongthesuperiorborderofthepancreas,and mesentericarteryissuedtheposteriorrightaccessory reachedthespleen.Thedorsalpancreaticarterydescend- hepaticartery,whichranposteriorlytotheportalveinon edfrom theposterioraspectofthepancreastowardits thebacksideofthepancreas,whereitgaveo branches inferiormargin,whereitbecametheinferiorpancreatic tothepancreasandtheduodenum,thenascendedbehind artery.Thesuperiormesentericarteryoriginatedfrom thecommonbileductandportalveintoreachthegall theaortajustinferiortothegastro-splenictrunk,and bladderandthehepaticrightlobeandtosupplythem. issuedtheposteriorrightaccessoryhepaticartery.This 248 Kosakaetal. ActaMed.Okayama Vol.56,No.5
Fig.2 Linedrawingrepresentationofcase2.Thelackofausualcommonhepaticarteryiscompensatedforbyananomalousposterior rightaccessoryhepaticartery(k2),whichrunsbehindtheportalvein.Noteanarterialringmadeoftheaccessoryhepatic(k2),gastroduodenal (w),pancreaticoduodenal(e),andsuperiormesenteric(m)arteries.Otherabbreviations:seeTable2.
accessoryhepaticarterypassedbehindtheportalveinand thecardiaandfundusofthestomach.Thegastroduodenal ranbetweenthecommonbileductandtheportalveinto arterygaveo thesuperiorposteriorpancreaticoduodenal appearinfrontofthebileduct,wherethisarterybifurcat- artery,whichranontheposteriorsurfaceofthepancreas edintothegastroduodenalandproperhepaticarteries. and anastomosed with the inferior posterior pan- Theproperhepaticartery,afterbranchingo theright creaticoduodenalartery, a branch of the superior gastricartery,ascendedalongtheanterioraspectofthe mesentericartery. Subsequently, the gastroduodenal portalveintoreachtheportahepatis,whereitdivided arterygavethepancreaticheadabranch,whichinturn intorightandleftbranches.Therightbranchpassed anastomosed with theinferiorpancreaticartery (see throughbehindthehepaticduct,issuedabranchtothe above).Thenthegastroduodenalarterydividedintothe gallbladder,andenteredtherightlobeoftheliver.The rightgastroepiploicarteryandthesuperioranteriorpan- leftbranch,runningalongthefissurefortheligamentum creaticoduodenalartery. Thelattermadean arterial venosum,gaveathickbranchtothehepaticleftlobe,and arcadewith theinferioranteriorpancreaticoduodenal finallybecametheaccessorygastricartery,whichcoursed artery,whichwasderivedfromthesuperiormesenteric alongtheuppermarginofthelesseromentumtosupply artery.Thus,arterialringsaroundthepancreaswere October2002 HepatopancreaticArterialRing 249
Fig.3 Linedrawingrepresentationofcase3.Ananomalousartery,theposteriorrightaccessoryhepatic(k2),isoriginated,makinga commontrunkwiththedorsalpancreaticartery,fromthesplenicartery.Notethatanarterialringaroundthepancreasisformedbyathick connectionofthepancreaticoduodenalanddorsalpancreaticarteries(asterisk).Otherabbreviations:seeTable2.
comprisedofthesuperiormesenteric,posteriorright theanterioraspectofthepancreas.Thesplenicartery accessoryhepatic, gastroduodenal, and superiorand gaveo acommontrunkoftheposteriorrightaccessory inferiorpancreaticoduodenalarteries. hepaticanddorsalpancreaticarteries.Thisaccessory (Fig.3). Theceliactrunkaroseasusual hepaticarterypassedbehindtheportalveinandthe (i.e.,asthegastro-spleno-hepatictrunk)fromtheanterior commonbileduct,andrantotherightlobeoftheliver. aspectoftheabdominalaorta.Theleftgastricartery Thedorsalpancreaticarterydescendedontheposterior reachedthecardiacregionofthelessercurvature;the aspectofthepancreaticbody,andappearedonthe commonhepaticarteryemittedtheproperhepaticartery, anterioraspectofthepancreatichead,whereitanas- whichraninfrontoftheportalveintotheportahepatis, tomosedwithabranchoftheanteriorsuperiorpan- whereitprovidedtheaccessorygastricarteryandgave creaticoduodenalartery.Here,achainofthecommon therightgastricarterytothepyloricregionofthelesser hepatic, gastroduodenal, anterior superior pan- curvature,thenbecamethegastroduodenalartery.The creaticoduodenal,dorsalpancreatic,posteriorrightacces- gastroduodenalarterybranchedo theposteriorsuperior soryhepatic,andsplenicarteriesformedanarterialring pancreaticoduodenalarteryattheuppermarginofthe aroundthepancreas.Theinferiorpancreaticoduodenal pancreatichead,andbifurcatedintotherightgastroepi- arteryarosefrom thesuperiormesentericartery,and ploicandanteriorsuperiorpancreaticoduodenalarteriesat dividedintothe2branches,anteriorandposterior,which 250 Kosakaetal. ActaMed.Okayama Vol.56,No.5 inturnanastomosedwiththeanteriorandposterior superiorpancreaticoduodenalarteries,respectively.
Discussion
Thepresentstudyreported3casesofcompleteand incompletearterialringsintheceliaco-mesentericarterial systemaroundthepancreasandliver.Thearterialringin case1consistedofachaincomprisedofthesplenic, anteriorrightaccessoryhepatic,accessorygastric,and leftgastricarteries.Incase2,theringwasformedby connectionofthesuperiormesenteric,posteriorright hepatic, gastroduodenal, anterior superior pan- creaticoduodenal, and anterior inferior pan- creaticoduodenalarteries.Incase3,theringwascom- prisedofthecommonhepatic,gastroduodenal,anterior superiorpancraticoduodenal,dorsalpancreaticandposte- riorrightaccessory hepatic arteries. Ourprevious typologicaldiagrams［8,9］(Fig.4)weremodifiedor revisedinordertoexplaintheformationofthesearterial Fig.4 Atypologicaldiagram previouslydemonstratedbyMura- ringsseeninthepresentcases(Fig.5A).Explanations kamietal.(1998).Thisdiagramisreproducedforcomparisonwith ourdiagram(Fig.5).Thedarklyshadedvascularroutesindicatean ofthepresentcasesaregiven using thismodified ordinarypatternoftheceliacomesentericsystem.Hepatopancreatic typologicalmodel(Fig.5B-D). arterialringsinthepresentcasesarenoteasilyexplainableusingthe Thepresentcasesshowanomaloushepaticarteries, previousmodel.Thearterieslabeled1,2,3,4,5,and6corre- particularlytheanteriorandposteriorrightaccessory spondtom1,m2,m3,m4,m5,andm6inFig.5,respectively. hepaticarteries.Theanteriorrightaccessoryhepatic (Organs)C,gallbladder;D,duodenum;E,esophagus;G,stom- ach;H,liver;L,intestine;M,cloaca;O,allantois;P,pancreas; arteryincase1isconsideredtohavecompensatedwith R,vitellineduct;T,hindgut;V,portalvein.(Celiaco-mesenteric thickening of the anterior superior-inferior pan- arteries)1,leftandrightsubphrenicarteries;2,leftandrightupper creaticoduodenalarteriesforthelackofatypicalcommon ventriculararteries;3,leftandrightmiddleventriculararteries;4, hepaticartery［11］.Theposteriorrighthepaticarteryin leftandrightlowerventriculararteries;5,leftandrightupper case2isconsideredtobeanunusuallydevelopedvessel intestinalarteries;6,leftandrightlowerintestinalarteries;ca, accessorymiddlecolicartery;ch,commonhepaticartery,cm, from theposteriorsuperior-inferiorpancreaticoduodenal middlecolicartery;cy,cysticartery;ic,ileocolicartery;id,inferior arteriesandnutrientarteriesofthebileduct.Theposte- pancreaticoduodenalartery;le,leftgastroepiploicartery;lg,left riorrightaccessoryhepaticarteryincase2seemstohave gastricartery;lh,leftaccessoryhepaticartery;1i,leftinferior derived from pancreatic branches of the superior phrenic artery;mi, inferior mesenteric artery;ms, superior mesentericartery［12］.Incase3,anunusuallydevel- mesentericartery;ph,properhepaticartery;pm,pancreaticbranch (arteria pancreatica magna);re, rightgastroepiploicartery;rg, opedbranchofthedorsalpancreaticarterymighthave rightgastricartery;rh,rightaccessoryhepaticartery;ri,right becomethisanomaloushepaticartery［6］. inferiorphrenicartery;sd,superiorpancreaticoduodenalartery;sp, Generally,itiswellknownthattheceliaco-mesenteric splenicartery;tc,celiactrunk.(Otherarteries)A,abdominalaorta; system showsnumerousvariationsinitsbranchingand c,intercostalorlumbararteries;k,leftrenalartery;I,common originatingpattern.Adachi［1］exhaustivelyinvestigated iliacarteries;m,leftmiddleadrenalartery;p,inneriliacarteries; t,lefttesticularorovarianartery;u,umbilicalorsupravesical 252casesandclassifiedthevariationalpatternsinto5 arteries;v,vitellinearteries.Reproducedwithpermissionfrom［9］. typesbasedonthecombinationoforiginsandtrunk formationoftheleftgastric,splenic,commonhepatic, andsuperiormesentericarteries.Accordingtohissys- tem,thepresentcase1,case2,andcase3areclassified classifiedasoneofAdachi’stypes,andconsideredtheo- asAdachi’sTypeVI,TypeVI,andTypeI,respective- reticallyatypologicalmodeloftheceliaco-mesenteric ly.Morita［16］encounteredacasethatcouldnotbe arterialsystem.Hismodelexplainedvariationalpatterns October2002 HepatopancreaticArterialRing 251
Fig.5 Atypologicalpatternoftheceliaco-mesentericarteriesatanearlystageofthefetalperiod(viewedfromtheleftside),modified afterMurakamietal.(1998)(A),andtypologicaldemonstrationsofcase1(B),case2(C),andcase3(D)usingthisdiagram.The gastrointestinalloop(I),liver(H),gallbladder(G),pancreas(P),andspleen(Sp)aresuppliedbythe6setsofpairedvessels:leftandright subphrenicarteries(m1),leftandrightupperventriculararteries(m2),leftandrightmiddleventriculararteries(m3),leftandrightlower ventriculararteries(m4),leftandrightupperintestinal(superiormesenteric)arteries(m5),andleftandrightlowerintestinal(inferior mesenteric)arteries(m6).Thesepairedvesselsareconnectedbyhorizontalandlongitudinalanastomoses.Otherabbreviations:seeTable2. 252 Kosakaetal. ActaMed.Okayama Vol.56,No.5 byfourunpairedvessels(leftgastric,splenic,hepatic, andsuperiormesentericarteries)thatoriginatedfromthe anterioraspectoftheabdominalaortaandwereconnected bylongitudinalanastomosingvessels.Thislongitudinal anastomosisisbasedonTandler’sobservationofthe humanembryo［17］.Morita’smodelwellexplained commonvariationssuchasindependentoriginoftheleft gastricarteryortrunkformationofgastro-splenicand hepato-mesenteric trunk. Furthermore, his model predictedtheindependentoriginsofthe4vessels,which rareanomalyhasbeenreportedbyseveralgroups,includ- ingours［9］.However,hismodelcannotexplainsome veryrareanomalies,suchasgastro-hepaticandspleno- mesenterictrunkformationthatavoidscrossoverofthe vessels［5］.Incontrast,ourbilateraltypologicalmodel, Fig.6 Schematicdiagramrepresentingbilateralsymmetryofthe candemonstratesuchraretrunkformation. mesenterialarterialsystemandotherparietalandvisceralarteries. Ourtypologicalmodelofthemesentericarterialsys- Longitudinalanastomosesareindicatedbyopencircles( ).Abbrevi- tem ischaracterizedbythe5pairsofintestinalarteries ations:seeTable2. originatingfrom theaortaandtheirlongitudinaland horizontalanastomoses(Figs.5A,6).Felix［18］inves- tigatedthedevelopmentoftheabdominalarteriesinthe andbranching［19］.Intheceliacomesentericarterial humanembryo.Intheearlystage,paireddorsalaortae system, variationalpatternsoftrunk formation and developandemitbrancheslaterallytotheprimitiveintes- branchingarewellexplained using longitudinalanas- tineoryolksac.Thesebranchesbilaterallycreatethe tomoticvesselsbetweensegmentalmesentericarteries. intestinalarterialnet.Themesentericarteries,orceliaco- Thus,longitudinalanastomoticvesselsplayanimportant mesentericarterialsystem,whichisderivedfrom the roleinthemorphogenesisoftheparietalandvisceral omphalomesentericarteries,originallydevelopfrom the vascularsystems. bilaterallysymmetricalintestinalarterialnet. Thearterialringformationinthepresentcasesstrong- Acknowledgements. WewouldliketothankMr.HisaoMizoguchi, Mr.MasahiroNarasakiandMr.HiroyukiOsugifortheirtechnicalhelp. ly suggestsapaired bilateralarterialsystem in the And,wespeciallyappreciatehonestworksofMr.HiromichiKusano,who mesentery.Thepancreaswasdevelopedintheposterior waskilledinanaccident. mesentery,andthestomachwasrotated,withitsright aspectfacingbehind.Thearterialsegmentthatruns References behindthepancreasderivesfrom therightsystem;the 1. AdachiB:Aortaabdominalis;inDasArteriensystem derJapanerII, segmentthatrunsinfrontofthepancreasderivesfrom MaruzenCo.,Kyoto(1928)pp11-129. theleftsystem;andthesegmentoftheleftgastricartery 2. FeiglW,FirbasW,SinzingerHandWickeL:Variabilit atdesTruncus tothehepaticportalbelongstotherightsystem.Thus, coeliacusundseinerAnastomosenmitderArteriamesentericasupe- rior.ActaAnat(1975) ,272-284. thesecasesofarterialringsaroundthepancreasare 3. OkadaS,OhtaY,ShimizuT,NakamuraM andYasoK:Arare explainedasthecontinuationoftherightandleftarterial anomalouscaseofabsenceoftheceliactrunk theleftgastric,the system.Itisnoteworthythatlongitudinalanastomosis splenicandthecommonhepaticarteriesarosefrom theabdominal commonlyappearedinothersitesofthebodyinthese aortaindependently.OkajimasFoliaAnatJpn(1983) ,65-71. 4. YamakiK,TanakaN,MatsushimaT,MiyazakiKandYoshizukaM:A cases.Forexample,thelongitudinalanastomosisatthe rarecaseofabsenceoftheceliactrunk:Theleftgastric,thesplenic, anteriorthoracicandabdominalwall(anteriorparietal) thecommonhepaticandthesuperiormesentericarteriesarising remainsastheinternalthoracicandsuperiorandinferior independentlyfromtheabdominalaorta.AnatAnz(1995) ,97- 100. epigastricarterialaxis(Fig.6).Inthearterialsystemof 5. KitamuraS,NishiguchiT,SakaiAandKumamotoK:Rarecaseofthe thescalenusregion,atypologicaldiagram introducing inferiormesentericarteryarisingfromthesuperiormesentericartery. precostallongitudinalanastomoses between interseg- AnatRec(1987) ,99-102. mentalarteriescanexplainvariouspatternsoforigination 6. MatsumuraH:Thesignificanceofthemorphologyofthedorsal October2002 HepatopancreaticArterialRing 253
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