HIRURŠKA ANATOMIJA ŠTITASTE I PARAŠTITASTIH …scindeks-clanci.ceon.rs/data/pdf/1452-0923/2012/1452-09231243007P.… · treba ligirati što je moguüe niže, što bliže kapsuli

Prof. dr Ivan Paunovi *1

HIRURŠKA ANATOMIJA ŠTITASTE I PARAŠTITASTIH ŽLEZDI I OSNOVI OPERATIVNE TEHNIKE

Sažetak: Štitasta žlezda je najve i endokrini organ i ima najve u u esta-lost oboljenja u odnosu na druge endokrine organe. Uspešno operativno le enje kako benignih tako i malignih oboljenja štitaste žlezde povezano je s adekvatnom preoperativnom pripremom, preciznom operativnom tehnikom i poznavanjem hirurške anatomije. Komplikacije koje se mogu javiti zbog nepoznavanja hirurške anatomije štitaste i paraštitastih žlezdi trajno ugrožavaju zdravlje operisanog i ine ga doživotnim invalidom. Potrebno je zato da hirurg koji operiše štitastu žlezdu i/ili paraštitaste žlezde poseduje neophodno znanje o hirurškoj anatomiji ovih endokrinih organa bez obzira na sada široku dostupnost aparata koji omogu avaju bolju vizuelizaciju operativnog polja, koagulaciju krvnih sudova, kao i intraoperativni neuromonitoring.

Štitasta žlezda je najve i endokrini organ u odraslog oveka, težina u zdrave osobe iznosi oko 17gr (1), pokriva anterolateralni deo gornjih trahealnih prstenova (od II do IV) i larinksa. Predstavlja bilobarni organ, iji su desni i levi lobus me usobno spojeni trakom istmi nog žlezdanog tkiva. Svaki lobus nalazi se u prostoru izme u traheje i ezofagusa medijalno, karotidne lože pozadi, i sternokleidomastoidnog, ster-nohioidnog i sternotiroidnog miši a napred i lateralno.

Ukoliko se sternotiroidni i sternohioidni miši i moraju prese i i transverzalno tokom tiroidektomije (radi bezbednog pristupa krvnim sudovima gornjeg pola), to treba u initi visoko u nivou krikoidne hrskavice, što obezbe uje prezervaciju njihovog motornog nerva (ansa nervi hypoglossi). Klini ki, nema funkcionalnih posledica zbog presecanja ovih miši a (1).

* Centar za endokrinu hirurgiju, Klinika za endokrinologiju, dijabetes i bolesti metabolizma, 11000 Beograd, Koste Todorovi a br. 8, E mail: [email protected]

8 MEDICINSKI GLASNIK / str. 7-17

Omota i i veze štitaste žlezde

Normalna štitasta žlezda je meke konzistencije, tamnocrvene boje i obavijena je tankom fibroznom kapsulom (tunica propria, anatomska kapsula), koja se teško odvaja s obzirom na to da je intimno srasla sa žlezdanim tkivom. Preko ana-tomske kapsule štitasta žlezda je obavijena spolja drugim fascijalnim omota em (duboki list srednje fascije vrata), koji se naziva hirurška kapsula. Prostor izme u unutrašnje i spoljašnje kapsule štitaste žlezde (spatium praeviscerale), u kome se nalazi rastresito vezivno tkivo, predstavlja upravo onaj hirurški sloj kroz koji se ekstrakapsularno prepariše lobus (2). Štitasta žlezda je lako pri vrš ena za okolne strukture, promene u fiksaciji mogu pobuditi sumnju na postojanje patoloških promena, posebno kada anamnesti ki podaci ukazuju na akutni tiroiditis ili kar-cinom. Normalno, štitasta žlezda je fiksirana prednjim i zadnjim suspenzornim ligamentom. Prednji suspenzorni ligamenti fiksiraju medijalnu ivicu gornjeg pola i gornju ivicu istmusa za krikoidnu hrskavicu. Potrebno ih je prese i radi „otvaranja” krikotiroidnog prostora, što je neophodni elemenat operativne teh-nike za pristup krvnim sudovima gornjeg pola po presecanju istmusa (odvajanje gornje i zadnje strane istmusa od traheje). Zadnji suspenzorni ligament ili Berry-jev ligament izuzetno je zna ajan sa stanovišta hirurške anatomije. Berry-jev ligament predstavlja širu, dosta jaku traku vezivnog tkiva koja vezuje (spaja) unutrašnju stranu gornjeg dela lobusa štitaste žlezde sa zadnjebo nom stranom krikoidne hrskavice i prva dva trahealna prstena. Ispod ovog ligamenta prolazi donji laringealni živac (n. recurrens) na svom putu prema larinksu, koji u 25% slu ajeva (3) prolazi i kroz ligament, pri emu je ovde mogu nost operativne lezije vrlo velika. esto se ispod ligamenta „podvla i” kao „pupoljak” deo tkiva štitaste žlezde, zbog ega je operativna ekstirpacija otežana. Ako imamo u vidu da po donjoj ivici ovog ligamenta prolazi i donja laringealna arterija i da se na toj visini donji laringealni živac esto grana, onda je jasno zašto ovaj predeo predstavlja jednu od visokorizi nih zona za leziju donjeg laringealnog živca pri izvo enju totalne lobektomije.

Krvni sudovi i laringealni nervi

Štitasta žlezda je dobro vaskularizovana, njena vaskularizacija poti e uglavnom od gornje i donje tiroidne arterije. U jednom broju slu ajeva (10%) prisutna je i najdonja tiroidna arterija (a. thyroidea ima) koja se odvaja od luka aorte, ili a.anonymae, i penje se ka štitastoj žlezdi ispred traheje. Ova arterija, kada je ve eg kalibra, može zamenjivati donju tiroidnu arteriju kada kongenitalno nedostaje (1).

9HIRURŠKA ANATOMIJA ŠTITASTE I PARAŠTITASTIH ŽLEZDI I OSNOVI...

Gornja tiroidna arterija (a. thyroidea superior) i gornji laringealni živac (n. laryngeus superior)

Gornja tiroidna je prva grana spoljne karotidne arterije (a. carotis externa) od koje se odvaja neposredno iznad tiroidne hrskavice u nivou hioidne kosti. Nakon odvajanja njene bo ne grane gornje laringealne arterije (a. laryngea superior), ona se spušta napred i naniže na površinu donjeg konstriktora ždrela ispod sternotiroidnog miši a, a pored tireohioidnog miši a, i prilazi prednje-gornjoj strani gornjeg pola lobusa štitaste žlezde, gde se deli na tri završne grane: prednju, spoljašnju i zadnju. Od zadnje grane gornje tiroidne arterije, ili njene anastomoze sa ushodnom granom donje tiroidne arterije, odvaja se paratiroidna arterija za gornju paratiroidnu žlezdu. U neposrednoj blizini gornje tiroidne arterije nalazi se stablo gornjeg grkljanskog živca (n. laryngeus superior), a u završnom delu spoljna grana ovog živca (r. externus), koja je motorni nerv krikotiroidnog miši a.

Ovaj miši je zateza (indirektni) glasne žice, što omogu ava stvaranje visokih tonova. Povreda ovog živca, pogotovu obostrana, lako se može prevideti na posto-perativnoj laringoskopiji. U 6–18% slu ajeva spoljna grana gornjeg grkljanskog živca pruža se zajedno ili ukršta sa gornjom tiroidnom arterijom ili njenim granama i tada je prilikom ligiranja gornje tiroidne arterije izložena riziku povrede (4) i pored toga, rutinska identi kacija ovog nerva tokom tiroidektomije se ne savetuje (5). U stvari, u 20% slu ajeva nerv se ne nalazi oko gornjeg pola štitaste žlezde u hirurški pristupa noj regiji, te se ne može identi kovati bez preparisanja kroz vlakna donjeg konstriktora farinksa, ovaj pristup mnogi autori ne savetuju zbog mogu nosti povrede farinksa (5).

Da bi se izbegla povreda nerva za vreme ligiranja vaskularne peteljke gornjeg pola, potrebno je prvo uo iti grane gornje tiroidne arterije, ime se onemogu ava ligiranje njenog stabla. Ovakav pristup je posebno preporu ljiv u slu aju operacije jako uve ane štitaste žlezde. Grane gornje tiroidne arterije treba ligirati što je mogu e niže, što bliže kapsuli štitaste žlezde. „Otvaranje” krikotiroidnog prostora presecanjem prednjeg suspenzornog ligamenta omogu a ovakav pristup (4). Pristup kroz ovaj prostor smanjuje rizik od povrede gornjeg grkljanskog živca i/ili njegove spoljne grane, pogotovu ako se preparisanje vrši od medijalne ka lateralnoj strani, što se obezbe uje trakcijom gornjeg pola lobusa štitaste žlezde naniže i spolja. Na ovaj na in mogu e je uo iti nerv kako prolazi, više ili manje, popre no izme u krvnih sudova gornjeg pola a iznad gornjeg pola lobusa, medijalno od donjeg konstriktora farinksa i krikotiroidnog miši a a ispod sternotiroidnog miši a. Navedene anatomske strukture, prema Moosman i De Weeseu (6), ine tzv. sternotiroidno-laringealni trougao i veština prepoznavanja njegovih elemenata jedan je od osnovnih ciljeva u edukaciji endokrinih hirurga. Elektrokoagulacija gran ica gornje tiroidne arterije za donji konstriktor farinksa


i krikotiroidni miši tako e može dovesti do povrede nerva s obzirom na to da se on pruža ispod njih, tako da je bezbednije njihovo ligiranje. Tehniku lobektomije, koja zapo inje preparisanjem gornjeg pola lobusa štitaste žlezde, uveo je Halsted, a usavršili Coller, Boyden i Thomson (7,8,9).

Donja tiroidna arterija (a. thyroideae inferior) i donji laringealni živac (n. recurrens)

Donja tiroidna arterija nastaje ra vanjem tireocervikalnog stabla (truncus thyreocervicalis) grane potklju ne arterije (a. subclavia), na unutrašnjoj ivici prednjeg skalenskog miši a. Penje se spoljnom stranom zajedni ke karotidne arterije preko prednjeg skalenskog miši a do Chassaignacove karotidne kvrge (tuberculum caroticum), u nivou krikoidne hrskavice naglo menja pravac, po-staje horizontalna, skre e unutra i nadole ispred ki mene arterije (a. vertebralis) a ispod zajedni ke karotidne arterije. Horizontalni deo gradi vijugu u obliku položenog slova S, leži na pretki menoj fasciji i ukršta prednju stranu vratnog simpatikusa, koji se na ovom mestu može lako povrediti u slu aju nepažljivog „en masse” podvezivanja arterije. Donja tiroidna arterija se iza donjeg pola ili granice srednje i donje tre ine, na otprilike 1 cm od lobusa štitaste žlezde, deli na tri završne grane: donju, zadnju (ushodnu) i unutrašnju (srednju). Zadnja (ushodna) grana ove arterije pruža se zadnjom stranom lobusa i anastomozira se zadnjom granom gornje tiroidne arterije. Od završnih grana, a ponekad i samog stabla donje tiroidne arterije, odvaja se arterija za donju paratiroidnu žlezdu. Donja laringealna arterija (a. laryngea inferior) je najve a ekstratiroidna grana ove arterije koja prolazi donjom ivicom Berry-jevog ligamenta. Hirurg može donju tiroidnu arteriju identifikovati ispod karotidne arterije tek pošto mobiliše lobus štitaste žlezde medijalno, a jugularnu venu lateralno, što obezbe uje da se arterija „nategne” i tako lakše prepozna i ini osnovu tehnika lobektomije preparisanja lobusa sa lateralne strane ili od donjeg pola. Osnove prve dao je Kocher (10) a kasnije usavršio Lahey (11), dok je drugu inaugurisao Edis sa Mayo klinike (12).

Donja tiroidna arterija je u bliskom odnosu sa donjim laringealnim živcem (n. recurrens), motornim nervom, koji inerviše sve unutrašnje miši e larinksa. Povreda ovog nerva, ili u slu aju grananja povreda njegove motorne grane, dovodi do paralize glasnice na ipsilateralnoj strani. Anatomske varijacije n. recurrensa su brojne, posebno kada je štitasta žlezda patološki izmenjena, tako da u slu aju kada živac nije prepoznat ne postoje „bezbedna” polja u kojima hirurg može da prepariše bez rizika. Izuzetno je važno da hirurg utvrdi ta ku ukrštanja n. recurrensa i donje tiroidne arterije, tj. ta ku neurovaskularne intersekcije (13), ime obezbe uje nizak procenat postoperativne paralize n. recurrensa.


Levi n. recurrens penje se prema larinksu kroz traheoezofagealni žleb ili nešto lateralnije, prednjom stranom jednjaka, naj eš e iza stabla donje tiroidne arterije, ponekad izme u, a re e, i ispred njenih završnih grana. Desni n. recurrens je mnogo više zakošen, tako da je u kaudalnom delu lateralno od traheje za jedan ili više centimetara. Retko prolazi iza stabla donje tiroidne arterije ve mnogo eš e iz-me u njenih grana. Opisane su nebrojene varijacije ovog živca (14). Sa prakti nog stanovišta treba znati da n.recurrens prolazi iza stabla donje tiroidne arterije, ispred ili izme u njenih grana i da je bezbednije tražiti nerv iza arterije. Identi kacijom stabla donje tiroidne arterije i pažljivim ligiranjem njenih grana što bliže kapsu-li, smanjuje se mogu nost povrede nerva i devaskularizacije donje paratiroidne žlezde. Grane donje tiroidne arterije, a posebno njena pobo na grana – donja laringealna arterija, mogu pogrešno biti prepoznate kao n. recurrens iako je ovaj izgledom manje pravilan, zaobljen i rastegljiv. Tako e se mogu uo iti njegovi sinusoidni sudovi (vasa nervorum), njihova izvijuganost smanjuje se kada se me-dijalnom mobilizacijom lobusa nerv „zategne”. Nerv se retko grana u nivou ispod donje tiroidne arterije, a ukoliko grananje postoji, samo je jedna grana motorna. Hirurg mora da ima na umu ovu mogu nost, i da svaku granu n. recurrensa smatra motornom i sve ih po svaku cenu sa uva. Pošto pro e donju tiroidnu arteriju, nerv nastavlja svoj put nagore i medijalno prema zadnje lateralnoj strani srednje tre ine lobusa i blizu je kapsule lobusa. Ponekad n. recurrens može da u ovoj zoni prolazi kroz tkivo štitaste žlezde, što može biti uslovljeno ili patološkim procesom ili re e normalnom anatomskom varijacijom. U nivou gornja dva trahealna prstena nerv prolazi kroz zadnji deo Berry-jevog ligamenta koji se pruža pozadi iza n. recurrensa i labavo vezuje lobus za ezofagus. Pre ulaska u larinks, n. recurrens se grana pozadi krikotiroidnog miši a. Donja laringealna arterija prati nerv, na mestu Berry-jevog ligamenta arterija je obi no pozadi n. recurrensa i daje malu granu koja ga ukršta sa unutrašnje strane pre ulaska u lobus štitaste žlezde. Nerv je u ovom predelu najizloženiji povredi i zato kontrolu hemostaze ligiranjem krvnih sudova ne treba uspostaviti bez njegove prethodne identi kacije. Medijalna mo-bilizacija lobusa, ma koliko neophodna za identi kaciju donje tiroidne arterije, može sa druge strane da ugrozi n. recurrens. Ovim manevrom „zateže” se stablo donje tiroidne arterije, njene grane i Berry-jev ligament i posledica je „istezanje” i dislociranje n. recurrensa napred ka lateralnoj strani traheje. Zadnja vlakna Berry-jevog ligamenta pritiskaju n.recurrens prema lateralnoj strani trahealnih prstenova, što otežava preparisanje. Mobilizacija lobusa nagore, posle osloba anja donjeg pola, omogu ava nežniji pristup identi kaciji i preparisanju nerva do njegovog ulaska u larinks na nivou krikoidne hrskavice (1).

U retkim slu ajevima (0.63%), desni donji laringealni živac nema rekurentni tok (15). Na levoj strani ova anomalija je vrlo retka, javlja se u 0.04% slu ajeva. Po pravilu, poreklo nerekurentnog laringealnog nerva je cervikalno. Zavisno od


nivoa nastanka, nerv se pruža manje-više nadole duž n.vagus-a i u manjoj ili ve oj meri preko jugulokarotidnog žleba, pri emu zavija nadole. Uvek prolazi ispod zajedni ke karotidne arterije. U jednoj tre ini, on je u bliskom kontaktu sa stablom ili granama donje tiroidne arterije i ulazi u larinks na uobi ajenom nivou. Nerekurentni donji laringealni živac nastaje zbog vaskularne anomalije u toku embrionalnog razvoja luka aorte, gde se desna potklju na arterija direktno odvaja iz luka aorte. Pojava na levoj strani udružena je sa desnim lukom aorte i visceralnim situs inversus-om. Postoji i retka varijanta nerekurentnog donjeg laringealnog živca, zajedno sa ipsilateralnim rekurentnim nervom bez istovremene anomalije u razvoju krvnih sudova. Ukoliko za vreme totalne lobektomije nerv nije na en na uobi ajenom mestu, pre njegovog ukrštanja sa donjom tiroidnom arterijom, potrebno je imati na umu mogu nost da je nerekurentan i potražiti ga popre no, lateralno prema karotidnoj loži i medijalno prema lobusu tiroideje, jer nerv u tom slu aju povezuje ove dve strukture. U slu aju velike retrosternalne strume, posebno u zadnjem medijastinumu, ili ekstratiroidnog širenja karcinoma tiroideje, nerv je teško prepoznati s obzirom na to da tada nije mogu e preparisati ispod donje tiroidne arterije, ve ga treba potražiti više proksimalno na mestu gde ulazi u larinks u nivou krikoidne hrskavice i potom ga preparisati nadole. Ovakav pristup zahteva prethodnu mobilizaciju žlezde ligiranjem vaskularne peteljke gornjeg pola ili medijalnu mobilizaciju lobusa po presecanju istmusa.

Vene štitaste žlezde

Mnogo su eš e varijacije u venskoj drenaži štitaste žlezde nego u njenoj arte-rijskoj vaskularizaciji. Intraglandularne vene su relativno malih dimenzija, usmerene su prema površini gde neposredno ispod anatomske kapsule formiraju vrlo bogat splet koji štitastoj žlezdi daje karakteristi an izgled. U patološki izmenjenoj štitastoj žlezdi kapsularne vene mogu biti izuzetno velikih dimenzija. Prema tome, krvavljenje iz kapsularnih krvnih sudova može biti znatno, zato kod subtotalne resekcije lobusa treba postaviti hvatalice za krvne sudove na kapsularne vene, ime ova procedura postaje relativno beskrvna. Drenaža kapsularne venske mreže odvija se preko tri venska stabla. Gornje tiroidne vene se direktno ili indirektno (preko truncusa thyre-olinguofacialis-a) ulivaju u venu jugularis internu neposredno ispred i lateralno od gornje tiroidne arterije. Lateralne ili srednje vene zna ajno variraju u broju. Polaze od anterolateralne ivice lobusa, relativno su kratke i mogu biti ve eg promera, ulivaju se direktno u jugularnu venu. Njihova identi kacija je zna ajna zbog toga što se mogu pogrešno zameniti za kapsularne vene, a njihovo cepanje je naj eš e na samom uš u u unutrašnju jugularnu venu i doga a se u slu aju mobilizacije lobusa bez prethod-nog ligiranja ovih vena. Potrebno ih je zato identi kovati i podvezati posle pažljive lateralne retrakcije zajedni ke karotidne arterije a pre medijalne mobilizacije lobusa.


Donje tiroidne vene polaze sa donjeg pola i istmusa preko nekoliko stabala, esto formiraju i splet. Ulivaju se u unutrašnju jugularnu venu, a ponekad, kada se spajaju u zajedni ko stablo (v. thyroidea impar), u venu anonimu. Pre podvezivanja najlate-ralnijih donjih tiroidnih vena potrebno je identi kovati rekurentni živac, s obzirom, da može biti zamenjen pogrešno za venu.

Limfna drenaža štitaste žlezde

Limfna drenaža štitaste žlezde je veoma razvijena i pruža se prakti no u svim pravcima (16,17). Folikuli štitaste žlezde su obavijeni intraglandularnim limfnim kapilarima. Postoji obilje intraglandularnih limfnih veza što omogu ava limfnu drenažu iz jednog u drugi lobus preko kompleksa intratiroidnih i perikapsularnih nodusa, ime se objašnjava intraglandularna diseminacija karcinoma štitaste žlezde (18).

Glavni limfni sudovi imaju eferentan tok i prate gran ice tiroidnih arterija i vena u tri glavna pravca: nagore, lateralno i nadole. Gornja oblast tiroidne žlezde se drenira duž gornjih tiroidnih sudova u gornje jugularne noduse. Limfni sudovi iz istmusa upu eni su ka prelaringealnim ili Del jskim nodusima, koji su u vezi s gornjim jugularnim nodusima. Lateralni limfni sudovi prate medijalnu tiroidnu venu do srednjih i donjih jugularnih nodusa. Limfna drenaža iz donjih delova pruža se ka pretrahealnim i paratrahealnim nodusima i lancu donjih jugularnih nodusa. Veze s prednjim medijastinalnim i retrofaringealnim nodusima su este, dok je drenaža u submandibularne i suprahioidne noduse re a. Preko perikapsularnih, pretrahealnih i prelaringealnih nodusa mogu a je kontralateralna drenaža (19).

Sa prakti nog stanovišta, hirurg mora da razmotri postojanje dve zone limfne drenaže. Primarnu zonu limfne drenaže ini paraglandularni prostor ili srednji ili visceralni odeljak vrata (VI i VII grupa limfnih nodusa). Drugu ili sekundarnu zonu limfne drenaže ini lateralni region vrata (II, III, IV i V grupa limfnih nodusa). Veza izme u ove dve zone je karotidna loža.

U visceralnom odeljku nalaze se dve grupe limfnih nodusa: prelaringealni i pre-trahealni limfni nodusi i paratraheoezofagealna grupa limfnih nodusa. Prelaringealni limfni sudovi leže ispred i iznad istmusa i spajaju se gore i lateralno sa limfnim su-dovima gornjeg pola štitaste žlezde i prate krvne sudove vaskularne peteljke gornjeg pola, a zatim dreniraju u lateralne noduse vrata. Pretrahealni limfni sudovi leže ispod istmusa i spajaju se kaudalno sa limfnim sudovima prednjeg gornjeg medijastinuma. Prednja granica visceralnog odeljka je zadnja površina pretiroidnih miši a, ali po-nekada se metastaze u nodusima mogu na i sasvim napred u srednjoj liniji posebno neposredno iznad istmusa (Del jski limfni nodusi). Paratraheoezofagealni limfni sudovi leže duž lateralne i zadnje strane štitaste žlezde i pružaju se duž rekurentnih laringealnih nerava. Lateralno su u vezi sa limfnim sudovima supraklavikularnog


trougla a pozadi sa onima okolo i iza traheje, larinksa, farinksa i ezofagusa. Limfna drenaža istmusa je usmerena naniže, u medijastinalne noduse, i naviše u paralaringe-alne noduse. Normalni tok limfne drenaže je iz centralnih i donjih delova lobusa ka traheoezofagealnim nodusima. Jedino se limfna drenaža gornjih polova lobusa odvija neposredno u lateralne limfne noduse. Ovo može da objasni zašto se u dve tre ine papilarnih karcinoma štitaste žlezde, otkrivenih na osnovu metastaza u laterocervikalne limfne noduse, primarni tumor nalazi u gornjem polu lobusa štitaste žlezde (20), dok je za sve druge karcinome štitaste žlezde centralni ili srednji predeo vrata primarna zona limfne drenaže.

Sekundarnu zonu limfne drenaže ine lateralni predeli vrata (lanac dubokih limfnih nodusa koji se pružaju duž unutrašnje jugularne vene i zadnji trougao vrata). Opstrukcija limfnog toka u centralnoj regiji vrata može dovesti do uve anja limfnih nodusa samo u lateralnoj zoni vrata zbog retrogradnog toka limfe (19). Inicijalno se metastaze u limfnim nodusima obi no zapažaju u centralnom odeljku vrata (medijalno od lože a. carotis comm.) u pretrahealnim i paratrahealnim nodusima, a zatim se šire u lateralni deo u duboke donje i lateralne cervikalne noduse (19). Naj eš e pacijenti s ve im primarnim tiroidnim tumorom imaju ve i broj metastaza u limfnim nodusima (18), mada neki pacijenti mogu imati okultni karcinom tiroidne žlezde i depozite u limfnim nodusima.

Ve ina hirurga se zalaže za pro lakti ku disekciju visceralnog ili centralnog odeljka vrata na primarnoj operaciji kod papilarnog i medularnog karcinoma zato što je ovo primarna zona limfne drenaže. Reoperacija u ovoj regiji, zbog pojave metastaza u limfnim nodusima, povezana je sa zna ajnim rizikom povrede rekurentnog nerva i paratiroidnih žlezdi.

Paratiroidne žlezde

Poznavanje embriologije pomaže hirurgu da razume gde paratiroidne žlezde mogu biti lokalizovane, dok mu njihov makroskopski izgled omogu ava da ih iden-ti kuje i razlikuje od drugih struktura.

Gornji par paratiroidnih žlezdi (PIV) je embriološkog porekla od IV škržnog luka, postavljen je kranijalnije i u bliskom je kontaktu sa štitastom žlezdom. Donji par paratiroidnih žlezdi (PIII) razvija se iz tre eg škržnog luka kao i timus, zato su PIII kaudalnije postavljene, esto pored ili u samom timusu.

Zajedni ko embrionalno poreklo PIII i timusa uslovljava da položaj PIII može biti od ugla mandibule do perikarda.

Paratiroidne žlezde su razli itog oblika (ovalan, jezi ak, list, disk) i kompaktne gra e u 94–98% slu ajeva (21). Boja zavisi od koli ine masnog tkiva i vaskularizacije: svetlobraon ili boje kafe kada je prisutna ve a koli ina masnog tkiva, i tamnija, mrko-žuta ili crvenkasto-braon kada je više celularnija ili ima bolju prokrvljenost. Palpatorno


su meke ali elasti ne konzistencije. U toku razvoja nodusa u štitastoj žlezdi mogu biti spljoštene, me utim, svoj normalan oblik ponovo dobijaju odvajanjem od površine nodusa. Prose na veli ina kre e se oko 5x3x1 mm prema Gilmouru (22) i Wangu (23), dok se prema istim autorima težina kre e u opsegu 10–78 mg, sa prose nom od 40 mg. Paratiroidne žlezde su inkapsulirane, oštrih ivica, glatke i sjajne površine. Naj eš e ih nalazimo potpuno ili delimi no uronjene u masno tkivo tako da zajedno sa njim formiraju „masnu loptu” zbog njihovog posebnog a niteta prema masnom tkivu, od koga se lako mogu odvojiti. Bez obzira na varijacije u veli ini, boji i obliku, paratiroidne žlezde su uvek inkapsulirane, što im daje poseban izgled predominantno žute boje. Masno tkivo je mekše konzistencije, ble e i bez de nitivnog oblika. Limfni nodusi su vrš i, više okrugli, manje homogeni, beli ili prljavo sivi sa crnim ta kama, teško se odvajaju od okolnog masnog tkiva i naj eš e ih ima više. Tkivo štitaste žlezde je vrš e, tamnocrvene boje do svetloplavo-sive na pritisku, dok je tkivo timusa ble e, sivo-žuto ili sivo ruži asto, granulirano i adherentno za masno tkivo.

Arterijska vaskularizacija paratiroidne žlezde je terminalnog tipa, u dve tre ine slu ajeva postoji samo jedna arterija. Dužina arterije kre e se od 1 do 40 mm, o uva-nje ove arterije u toku lobektomije prevashodno zavisi od udaljenosti mesta grananja arterije od kapsule štitaste žlezde.

Vaskularizacija PIII zavisi prevashodno od donje tiroidne arterije, od ijih se završnih grana, a ponekad i samog stabla, odvaja paratiroidna arterija. Paratiroidna arterija za PIV nastaje odvajanjem od zadnje (ushodne) grane donje tiroidne arterije, zadnje grane gornje tiroidne arterije ili njene anastomoze sa ushodnom granom donje tiroidne arterije. Donja tiroidna arterija može da obezbe uje arterijsku vaskularizaciju i gornje i donje paratiroidne žlezde. Hirurg ovu mogu nost uvek treba da ima na umu i da iz tog razloga izbegne ligiranje njenog glavnog stabla. Pojedina no ligiranje grana gornje tiroidne arterije što niže prema kapsuli obezbe uje da se sa uva zadnja grana gornje tiroidne arterije.

Venska drenaža odvija se na tri na ina: preko kapsularnog spleta štitaste žlezde, preko gran ica koje ulaze u štitastu žlezdu ili kombinacijom ova dva na ina. Hemo-stazu paratiroidnih vena treba izbegavati zbog rizika od glandularne infarkcije. Pro-mena boje žlezde i njeno progresivno zatamnjenje predstavlja pouzdan znak ishemije. Incizija kapsule i površnog sloja parenhima može da spre i vensku stazu i omogu i oporavak žlezde i uspostavljanje normalne prebojenosti.

Postoje mnogobrojne varijante u lokalizaciji paratiroidnih žlezdi. Sa prakti nog stanovišta, potrebno je da hirurg zna da je PIII lokalizovana uobi ajeno kaudalno od mesta ukrštanja donje tiroidne arterije i rekurentnog laringealnog nerva. Ukoliko nije na ovom mestu najverovatnije je u timusu. Lokalizacija PIV je konstantnija, postavljene su dublje od PIII u nivou krikoidne hrskavice. Kada se ne na u u uobi-ajenoj lokalizaciji, najverovatnije su se preko ezofagusa spustile nadole u zadnji

medijastinum.


Literatura

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2. Udelsman R., Thyroidectomy. In: Rob and Smith’s Operative Surgery, eds. Carter DC, Russell RC and Pitt HA, Chapman and Hall, 1996: 1147-1158.

3. Lennquist S., Thyroidectomy. In:Textbook of Endocrine Surgery, eds. Clark OH and Duh QY,Philadelphia,WB Saunders Company, 1997; 147-153.

4. Lennquist S, Cahlin C, Smeds S., The superior laryngeal nerve in thyroid surgery. Surgery, 1987; 102:999-1008.

5. Lennquist S., The Laryngeal Nerves in Thyroid Surgery. In:Jon A. van Heerden(ed), Co-mon Problems in Endocrine Surgery,Chicago,Year Book Medical Publishers. 1989; 123-131.

6. Moosman DA, De Weese MS., The external laryngeal nerve as related to thyroidectomy. Surg Gynecol Obstet. 1968; 127(5): 1011-1016.

7. Brieger HG., A Portrait of Surgery in America, 1875-1889. Surg Clin of North America, 1987; 67(6): 1181-1216.

8. Coller FA, Boyden AM., The development of the technique of thyroidectomy.Surg Gynecol Obstet. 1937; 65: 495-504

9. Thompson NW, Olsen WR, Hoffman GL., The continuing development of the technique of thyroidectomy. Surgery, 1973; 73(6): 913-927.

10. Modlim MI, Kidd M, Sandor A., The In uence of Theodor Kocher on American Surgeons. Dig Surg. 1997; 14: 469-482.

11. Rutkow MI., The Surgical Clinics During the 1920’s. Surg Clin of North America, 1987; 67(6): 1241-328.

12. Edis AJ, Ayala LA, Egdahl RH., Manual of endocrine surgery. New York, Springer Verlag. 1975: 100-108.

13. Paunovi I., Jankovi R., Tomi Lj., Dikli A., Batev N., Laringealni `ivci u hirurgiji štitaste žlezde. Timi ki medicinski glasnik, 1991; 16(1-2): 9-12.

14. Reed AF., Relations of inferior laryngeal nerve to inferior thyroid artery. Anat Rec. 1943; 85: 17-23.

15. Henry JF, Audiffret J, Denizot A., The non recurrent inferior laryngeal nerve: Review of 33 cases, including two on the left side. Surgery, 1988; 104: 977-984

16. Hamming JF, Roukema JA., Management of Regional Lymph Nodes in Papillary,Follicular and Medullary Thyroid Cancer. In:Textbook of Endocrine Surgery, eds. Clark OH and Duh QY,Philadelphia,WB Saunders Company, 1997; 155-166.

17. Ellenhorm JDI, Shah JP, Brennan MF., Impact of therapeutic regional lyph node dissection for medullary carcinoma of the thyroid gland. Surgery, 1993; 114: 1078-1081.

18. Scheumann GFW, Gimm O, Wegener G et al., Prognostic signi cance and surgical ma-nagement of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 1994; 18:559-567.

17SURGICAL ANATOMY OF THYROID AND PARATHYROID GLANDS AND BASIC...

19. Noguchi S, Noguchi A, Murakami N., Papillary carcinoma of thyroid: Developing pattern of metastasis. Cancer 1970; 2: 1053-1060.

20. Henry JF, Denizot A, Bellus JF., Papillary thyroid carcinomas revealed by metastatic cervical lymph nodes. Endocr Surg. 1992; 9: 349-

21. Akerstrom G., Malmaeus J., Bergstrom R., Surgical anathomy of human parathyroid glands. Surgery 1984; 95: 14-21

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Paunovic Ivan*,1Živaljevi Vladan, Gori Zoran, Slijep evi Nikola, Denovi Marija, Dikli Aleksandar

SURGICAL ANATOMY OF THYROID AND PARATHYROID GLANDS AND BASIC PRINCIPLES OF OPERATIVE TECHNIQUE

Abstract: The thyroid gland is the largest endocrine organ with the highest frequency of disorders of all the endocrine organs. A succe-ssful treatment of both benign and malignant diseases of the thyroid is connected with adequate pre-operative evaluation, a precise operative technique and the knowledge of surgical anatomy. Complications that may occur due to the insuf cient knowledge of the surgical anatomy of the thyroid and parathyroid glands permanently damage the health of the patient and cause his lifelong disability. Therefore it is necessary that the surgeon performing a thyroid and/or parathyroid glands operation should have suf cient knowledge of the surgical anatomy of these endocrine organs despite the wide availability of instruments which enable better visualization of the operative eld, coagulation of blood vessels and intraoperative neuromonitoring.

The thyroid gland is the largest endocrine organ in an adult, weighing about 17g (1) in a healthy person and covering the anterolateral area of upper tracheal rings (from II to IV) and larynx. It is a bi-lobed organ, whose left and right lobes are connected by a bridge of isthmic glandular tissue. Each lobe is located in the area between the trachea and oesophagus medially, carotid sheath posteriorly, and sternocleidomastoid and sternohyoid muscles anteriorly and laterally.

If sternocleidomastoid and sternohyoid muscles must also be cut transversely during thyroidectomy (in order to approach the blood vessels of the upper pole), it should be done at the level of the cricoid cartilage, which ensures the preservation of

* Prof.dr Ivan Paunovi , Medical school Belgrade, University of Belgrade, The Centre for En-docrine Surgery, Clinic for Endocrinology, Diabetes and Metabolic Disorders, Clinical Centre of Serbia, 11000 Belgrade, Koste Todorovi a 8, e-mail: [email protected]


their motor nerve (ansa nervi hypoglossi). From a clinical point of view, there are no functional consequences of the cuts of these muscles (1).

Thyroid capsules and connections

A normal thyroid is of soft consistency, dark red colour and surrounded by a thin brous capsule (tunica propria, anatomic capsule) which is very dif cult to separate

since it has grown into the glandular tissue. Via this anatomic capsule, the thyroid is surrounded by another fascial layer (deep layer of the cervical fascia), which is called the surgical capsule. The space between the inner and outer capsules of the thyroid (spatium praeviscerale) with the mealy connective tissue is exactly the surgical layer through which an extracapsular preparation of the lobe is performed (2). The thyroid is loosely attached to the surrounding structures and the changes in xation may arouse suspicion of the existence of pathological changes particularly when anamnestic data indicate acute thyroiditis or carcinoma. Normally, the thyroid is xed with the posterior and anterior suspensory ligaments. Anterior suspensory ligaments xate the medial edge of the upper pole and the upper edge of the isthmus for the cricoid cartilage. They need to be cut in order to ‘open’ the cricothyroid space, which is an essential element of the operating technique to approach the blood vessels of the upper pole upon cutting the isthmus (separating the anterior and posterior parts of the isthmus from the trachea). The posterior suspensory ligament or the ligament of Berry is extremely important in surgical anatomy. The ligament of Berry represents a broader and much stronger connective tissue which connects the inner side of the anterior part of the thyroid lobe with the postelateral part of the cricoid cartilage and the rst two tracheal rings. Beneath this ligament, there is a laryngeal nerve (n.recurrens) on its way to the larynx, which in 25% of all cases (3) also goes through the ligament, thus increasing the possibility of an operative lesion. Beneath the ligament, there is very often a bud-like part of the thyroid tissue, which makes operative extirpation very dif cult. Considering the fact that the inferior laryngeal artery goes along the lower edge of this ligament and that the inferior laryngeal nerve often diverges there, it is clear why this area is one of the high- risk zones for the lesion of the inferior laryngeal nerve when performing total lobectomy.

Blood vessels and laryngeal nerves

The thyroid gland has a rich blood supply mostly from the superior and inferior thyroid artery. In a number of cases (10%), there is also the lowest thyroid artery (a.thyroidea ima), which diverges from the aorta arch or a.anonymae and moves up towards the thyroid in front of the trachea. This artery when it is of a larger caliber can replace the inferior thyroid artery when it is congenitally missing (1).


Superior thyroid artery (a.thyroidea superior) and superior laryngeal nerve (n.laryngeus superior)

The superior thyroid artery is the rst branch of the external carotid artery (a.carotis externa), from which it diverges directly above the thyroid cartilage at the level of the hyoid bone. After the divergence of its lateral branch of the superior laryngeal artery (a.laryngea superior), it goes forward and downward to the surface of the lower constrictor of the throat beneath the sternothyroid muscle and next to the thyreohyoid muscle and approaches the front posterior side of the upper pole of the thyroid lobe, where it diverges into three nal branches: superior, external and inferior. The parathyroid artery for the superior parathyroid gland diverges from the anterior branch of the superior thyroid artery or its anastomosis with the upward branch of the inferior thyroid artery. Close to the superior thyroid artery, there is the trunk of the superior laryngeal nerve (n.laryngeus superior), and in the ultimate part, there is the external branch of this nerve (r.externus), which is the motor nerve of the cricothyroid muscle.

This muscle is the (indirect) tensioner of the vocal cord, which enables the production of high-pitched tones. The injury of this nerve, especially if it is on both sides, can be easily overlooked during postoperative laryngoscopy. In 6-18% of cases, the external branch of the superior laryngeal nerve goes along with or intersects the superior thyroid artery or its branches, during ligation of the superior thyroid artery it is at risk to be injured (4). However, a routine identi cation of this nerve during thyroidectomy is not recommended (5). Basically, in 20% of cases, this nerve is located around the upper pole of the thyroid in a surgically inaccessible area and it cannot be identi ed through the bers of the lower pharynx constrictor so that this approach is not recommended due to the possibility of damaging the pharynx (5).

In order to avoid injuring the nerve during the ligation of the vascular pedicle of the upper pole, it is necessary to identify the branches of the superior thyroid artery, which enables the ligation of its trunk. This approach is particularly recommended in surgical treatments of an enlarged thyroid. The branches of the superior thyroid artery should be ligated as low as possible and as close to the thyroid capsule as possible. The ‘opening’ of the cricothyroid space by cutting the anterior suspensory ligament makes this procedure possible (4). The approach through this area reduces the risk of injuries of the superior laryngeal nerve and/or its external branch, especially if the dissection is performed from the medial to the lateral side, which is ensured by the traction of the upper pole of the thyroid lobe downward and outward. Thus, it is possible to observe the nerve going more or less cross-sectionally between the blood vessels of the upper pole and above the upper pole of the lobe, medially from the lower pharyngeal constrictor and cricothyroid muscle and below the sternothyroid muscle. According to Moosman and De Weese (6), these anatomic structures make the so-


called sternothyroid-laryngeal triangle and the ability to identify these elements is one of the basic objectives in the education of endocrine surgeons. The electrocoagulation of small branches of the superior thyroid artery for the lower pharyngeal constrictor and the cricothyroid muscle can also lead to the injury of the nerve due to the fact that it goes beneath them, which means that their ligation is a much safer procedure. The lobectomy technique which begins by the preparation of the upper thyroid lobe was introduced by Halsted and improved by Coller, Boyden and Thomson (7,8,9).

Inferior thyroid artery (a.thyroideae inferior) and inferior laryngeal nerve (n.recurrens)

The inferior thyroid artery occurs by bifurcation of thyreocervical trunk (truncus thyreocervicalis) branch of the subclavian artery (a.subclavia), on the inner edge of the anterior scalene muscle. It goes up along the outer edge of the common carotid artery across the anterior scalene muscle to the Chassaignac carotid tubercle (tuber-culum caroticum), then at the level of the cricoid cartilage, it changes the direction abruptly, becomes horizontal, turns inward and downward in front of the spinal artery (a.vertebralis), and beneath the common carotid artery. Its horizontal portion creates a curve in the shape of the lying letter S, it lies on the ante-spinal fascia and it intersects with the front side of the sympathicus, which in this particular point, can be easily hurt in case of an unprofessional “en masse” lygating the artery. Behind the lower pole or the border between the middle and lower third, approximately 1cm far from the thyroid lobe, the inferior thyroid artery is divided into three ultimate branches: inferior, posterior (upward) and internal (middle). The posterior (upward) branch of this artery goes along the posterior side of the lobe and anastomoses with the posterior branch of the superior thyroid artery. The artery for the inferior parathyroid gland diverges from the ultimate branches, and sometimes even from the trunk itself. The inferior laryngeal artery (a.laryngea inferior) is the largest extrathyroid branch of this artery which goes along the lower edge of the Berry ligament. A surgeon can identify the inferior thyroid artery only after medial mobilization of the thyroid lobe, and lateral mobilization of the jugular vein, which ensures the tension of the artery and its easier identi cation and is the basis of the lobectomy technique within which the lobe is prepared laterally or from the lower pole. The basis of this procedure procedure was rst given by Kocher (10) and later improved by Lahey (11), whereas the second one

was inaugurated by Edis at the Mayo clinic (12). The inferior thyroid artery is in close relationship with the inferior laryngeal

nerve (n.recurrens), motor nerve, which innervates all the internal muscles of the larynx. During surgery injury of this nerve, or in case of branching, injury of its motor branch, causes the paralysis of the vocal cord on its ipsilateral side. Anatomic variations of n.recurrensa are numerous, especially when the thyroid is enlarged, so


that when the nerve is not identi ed there are no ‘safe’ areas where a surgeon can operate without any risk. It is extremely important that the surgeon should identify the point of intersection of n.recurrensa and the inferior thyroid artery, i.e. the point of neurovascular intersection (13), which ensures a low percentage of postoperative paralysis of n.recurrensa .

The left n.recurrens goes up towards the larynx through the tracheoesophageal groove or more laterally, along the front side of the oesophagus, usually behind the trunk of the inferior thyroid artery, sometimes between, and rarely in front of its ultimate branches. The right n.recurrens is much more inclined so that in the caudal part it is located one or more centimeters laterally away from the trachea. It rarely goes behind the trunk of the inferior thyroid artery but much more often through its branches. Numerous variations of this nerve have been described (14). From the practical point of view, it should be known that the n.recurrens goes behind the trunk of the inferior thyroid artery, in front of or between its branches and that it is safer to look for the nerve behind the artery. By identifying the trunk of the inferior thyroid artery and by careful ligation of its branches, the possibilities of damaging the nerve and devascularising the inferior parathyroid gland are much reduced. The branches of the inferior thyroid artery and, in particular, its lateral branch – the infe-rior laryngeal artery, may be misidenti ed as n.recurrens although, in its appearance, it is less regular, curved and elastic. Its sinusoidal vessels (vasa nervorum) can also be observed, and their curves are reduced when the nerve becomes ‘tense’ after the medial mobilization of the lobe. The nerve rarely branches below the inferior thyroid artery, and if branches exist, only one of them is a motor branch. A surgeon must bear this possibility in mind, consider each branch of n.recurrens the motor one and try to save all of them at all costs. After passing the inferior thyroid artery, the nerve goes upward and medially towards the posterolateral side of the middle third of the lobe and close to the lobe capsule. Sometimes, in this zone, n.recurrens can go through the thyroid tissue, which may be caused by a pathological process or, rarely, by a normal anatomic variation. At the level of the two upper tracheal rings, the nerve goes through the posterior portion of the Berry ligament and loosely connects the lobe with the oesophagus. Before entering the larynx, n. recurrens branches behind the cricothyroid muscle. The inferior laryngeal artery follows the nerve, and in the area of the Berry ligament, the artery is usually behind n.recurrens producing a small branch which intersects with it on the interior side before entering the thyroid lobe. Here, the nerve is most often subject to injuries and that is why homeostasis control by ligation of blood vessels should not be performed before identifying it rst. Medial mobilization of the lobe, in spite of its importance for the identi cation of the inferior thyroid artery, may, on the other hand, harm n.recurrens. In this procedure, the trunk of the inferior thyroid artery becomes ‘ tense’ as well as its branches and the Berry ligament and, consequently, n.recurrens is ‘tensioned’ and dislocated forward towards


the lateral side of the trachea. Posterior bres of the Berry ligament put pressure on n.recurrens towards the lateral side of the tracheal rings, which makes it dif cult to preparate. The mobilization of the lobe upward, after freeing the lower part, enables a more gentle procedure in identifying and preparating the nerve before it enters the larynx at the level of the cricoid cartilage (1).

In very few cases (0.63%), the right inferior laryngeal nerve does not have a recurrent ow (15). On the left side, this anomaly is very rare and occurs in 0.04% of cases. As a rule, the origins of the non-recurrent laryngeal nerve is cervical. Depen-ding on the level of occurrence, the nerve goes more or less downward along n.vagus and, to a smaller or larger extent, across the jugulocarotid groove, where it curves downward. It always goes beneath the common carotid artery. With a third of its length, it is closely connected with the trunk and the branches of the inferior thyroid artery and enters the larynx at the usual level. The non-recurrent laryngeal nerve occurs due to the vascular anomaly during the embryonic development of the arch of the aorta, where the right subclavian artery directly diverges from the arch of the aorta. The occurrence on the left side is connected with the right arch of the aorta and the visceral situs inversus. There is also a very rare variant of the non-recurrent inferior laryngeal nerve together with the ipsilateral recurrent nerve without a simultaneous anomaly in the development of blood vessels. If, during the total lobectomy, the nerve has not been found in the usual place, before its intersection with the inferior thyroid artery, it should be remembered that it might be non-recurrent and it should be looked for cross-sectionally, laterally towards the carotid space and medially towards the lobe of the thyroidea since the nerve, then, connects these two structures. In the case of a serious retrosternal goiter, particularly in the last mediastinum, or in the case of the extrathyroid spread of the thyroidea carcinoma, the nerve is dif cult to identify and since it is not possible to perform surgery below the inferior thyroid artery, it should be looked for proximally at the point where it enters the larynx at the level of the cri-coid cartilage and then preparated downward. This procedure demands the previous mobilization of the gland by ligating the vascular stem of the upper pole or medial mobilization of the lobe upon cutting the isthmus.

Veins of the thyroid gland

The variations in the vein drainage of the thyroid are much more common than in its arterial vascularisation. Intraglandular veins are of relatively small dimensions, they are directed towards the surface where, just below the anatomic capsule, they form a rich splice which makes the thyroid look very unique. In a pathologically changed thyroid, capsular veins may be of extremely large dimensions. So, bleeding from capsular blood vessels may be substantial and because of that, in the subtotal resection of the lobe, the blood vessel forceps should be placed on the capsular veins, which


makes this procedure almost completely bloodless. The drainage of the network of the capsular veins is done through three vein trunks. The superior thyroid veins, directly or indirectly (via truncus thyreolinguofacialis), ow into the internal jugular vein just in front of and laterally from the superior thyroid artery. The lateral and middle veins vary considerably in terms of their number. They go from the anterolateral edge of the lobe, they are relatively short and may be of a large diameter, and they ow directly into the jugular vein. Their identi cation is important because they can be mistaken for capsular veins, and their splitting most commonly occurs at the very con uence of the internal jugular vein and in cases of lobe mobilization without a previous ligation of these veins. That is why they should be identi ed and tied after a careful lateral retraction of the common carotid artery and before medial mobilization of the lobe. The inferior thyroid veins go from the upper pole and isthmus via several trunks, and very often form a splice. They ow into the internal jugular vein, and sometimes they unite into a common trunk (v.thyroidea impar) into the innonimate vein. Before tying the most lateral inferior thyroid veins, it is necessary to identify the recurrent nerve since it can be mistaken for a vein.

Lymphatic drainage of the thyroid

Lymphatic drainage of the thyroid is highly developed and practically goes to all directions (16,17). The thyroid follicles are surrounded by intraglandular lymphatic capillaries. There is a number of intraglandular lymphatic connections, which ena-bles lymphatic drainage from one to the other lobe via a complex of intrathyroid and pericapsular nodes, and this explains the intraglandular dissemination of the thyroid carcinoma (18).

Main lymphatic vessels have an efferent ow and follow the small branches of thyroid arteries and veins in three major directions: upward, lateral and downward. The upper area of the thyroid is drained along the superior thyroid vessels into the upper jugular nodes. Lymphatic vessels from the isthmus are directed towards pre-laryngeal and delphian nodes which are connected with the upper jugular nodes. Lateral lymphatic vessels follow the medial thyroid vein to the middle and lower jugular nodes. The lymphatic drainage from the lower parts goes towards pretrache-al and paratracheal nodes and the chain of lower jugular nodes. The links with the anterior mediastinal and retropharyngeal nodes are frequent, whereas the drainage into submandibular and suprahyod nodes is rare. Contralateral drainage is possible via pericapsular, pretracheal prelaryngeal nodes (19).

From the practical point of view, a surgeon needs to consider the existence of two zones of lymphatic drainage. The primary zone of lymphatic drainage consists of the paraglandular space or the middle or visceral region of the neck (VI and VII group of lymphatic nodes). The second or secondary zone of lymphatic drainage consists


of the lateral region of the neck (II,III,IV and V group of lymphatic nodes). The link between these two zones is the carotid space.

In the visceral region, there are two groups of lymphatic nodes: prelaryngeal and pretracheal lymphatic nodes and the paratracheoesophageal group of lymp-hatic nodes. Prelaryngeal lymphatic vessels lie in front of and above the isthmus and unite above and laterally with the lymphatic vessels of the upper pole of the thyroid and follow the blood vessels of the vascular stem of the upper pole, nally draining themselves into the lateral nodes of the neck. Pretracheal lymphatic vessels are located below the isthmus and unite caudally with the lymphatic ve-ssels of the anterior upper mediastanum. The anterior edge of the visceral portion is the posterior surface of prethyroid muscles, but sometimes metastases in the nodes can be found in the front and in the middle line immediately above the isthmus (delphian lymphatic nodes). Paratracheoesophageal lymphatic vessels lie along the lateral and posterior sides of the thyroid as well as along the recurrent laryngeal nerves. They are laterally connected with the lymphatic vessels of the supraclavicular triangle, and posteriorly with the ones around and behind the trachea, larynx, pharynx and oesophagus. The lymphatic drainage of the isthmus is directed downwards into mediastinal nodes and upwards into paralaryngeal nodes. The normal ow of the lymphatic drainage is from the central and lower parts of the lobe towards tracheoesophageal nodes. The lymphatic drainage of the upper poles of the lobe is the only one which is performed directly into the lateral lymphatic nodes. This is explained by the fact that in two thirds of papi-llary thyroid carcinoma diagnosed on the basis of the metastases in laterocervical lymphatic nodes, the primary tumor is located in the upper pole of the thyroid (20), whereas in all other thyroid carcinoma, the central and the middle regions of the neck are the primary zone of the lymphatic drainage.

The secondary zone of the lymphatic drainage consists of the lateral regions of the neck (a chain of deep lymphatic nodes which go along the internal jugular vein and the posterior triangle of the neck). The obstruction of the lymphatic ow in the central region of the neck may lead to the enlargement of the lymphatic nodes only in the lateral region of the neck due to the retrograde ow of the lymph (19). Initially, the metastases in the lymphatic nodes are usually observed in the central region of the neck (medially from the space a. carotis comm.) in the pretracheal and paratracheal nodes, and then they spread to the lateral region into the deep upper and lateral cervi-cal nodes (19). Most often, patients with larger primary thyroid tumors have a larger number of metastases in the lymphatic nodes (18), although some patients may have an occult thyroid carcinoma and deposits in the lymphatic nodes.

Most surgeons are in favour of the pro lactic dissection of the visceral and central region of the neck during the primary operation of papillary and medular carcinoma since this is the primary zone of lymphatic drainage. Reoperation in this region, due


to the appearance of metastases in the lymphatic nodes, is connected with an increased risk of damaging the recurrent nerve and parathyroid glands.

Parathyroid glands

Knowing embryology helps a surgeon to understand where parathyroid glands can be located whereas their macroscopic appearance enables him to identify them and differ from other structures

The upper pair of parathyroid glands (PIV) is of embryological origin of the fourth pharyngeal pouch, it is located more cranially and in close contact with the thyroid. The lower pair of parathyroid glands (PIII) is developed from the third pharyngeal pouch just like the thymus, and that is why PIII are located more caudally and very often near or inside the thymus itself.

The common embryological origin of PIII and thymus causes the position of PIII to be from the corner of the mandibule to the pericardium.

Parathyroid glands are of various shapes (oval, tongue-shaped, leaf-shaped, discus-shaped) and of compact structure in 94-98% cases (21). The colour depends on the amount of fat tissue and vascularisation: lightbrown or the colour of coffee is present when the amount of fat tissue is larger and they are dark, yellowish-brown or reddish-brown when they are more cellular and with a better blood ow. In terms of palpation, they are soft and of elastic consistency. During the development of the nodes, they can be attened in the thyroid, but they regain their normal shape by se-parating themselves from the surface of the nodes. The average size is around 5x3x1 mm according to Gilmour (22) and Wang (23), whereas according to the same authors, the weight ranges from 10 to 78 mg, with the average weight being 40 mg. parathyroid glands are incapsular, with sharp edges and with a smooth and glossy surface. They are usually completely or partially immersed in the fat tissue and together with it they form a ‘greasy ball’ because of their special af nity towards the fat tissue, from which they can be easily separated. Regardless of the variations in size, colour and shape, parathyroid glands are always incapsular, which gives them a special, mainly yellow appearance. The fat tissue is of softer consistency, paler and without a de nite shape. The lymphatic nodes are harder, more rounded, less homogenous, white or dark grey with black spots, they are dif cult to separate from the surrounding fat tissue and there are usually more of them. The thyroid tissue is harder, from dark red to light bluish-grey in colour when under pressure, whereas the thymus tissue is paler, yellowish-grey or pinkish-grey, granulated and adherent to the fat tissue.

Arterial vascularisation of the parathyroid is of terminal type, and in two-thirds of all cases there is only one artery. The length of the artery is between 1 and 40 mm, so that the preservation of this artery during lobectomy mainly depends on the distance between the point of divergence of the artery and the thyroid capsule.


PIII vascularisation mainly depends on the inferior thyroid artery, from whose ultimate branches, and sometimes even from the trunk itself, the parathyroid artery diverges. The parathyroid artery for PIV appears by diverging from the posterior (upward) branch of the inferior thyroid artery, the posterior branch of the superior thyroid artery or its anastamoses with the upward branch of the inferior thyroid artery. The inferior thyroid artery can ensure arterial vascularisation of both superior and inferior parathyroid glands. A surgeon must always bear this in mind and avoid the ligation of its main trunk. Individual ligation of the branches of the superior thyroid artery as low towards the capsule as possible ensures the preservation of the posterior branch of the superior thyroid artery.

Vein drainage is performed in three ways: via the capsular splice of the thyroid, via the small branches entering the thyroid or using the combination of these two methods. The hemostasis of the parathyroid veins should be avoided due to the risk of glandular infection. The change of colour of the thyroid and its progressive dar-kening is a certain sign of ischemia. The incision of the capsule and the surface of the parenchyma may stop a venous stasis and enable the recovery of the gland and its normal colour.

There are numerous variants in the localization of the parathyroid glands. From the practical point of view, it is necessary for a surgeon to know that PIII is localized in a usual way, caudally from the intersection with the inferior thyroid artery and the recurrent laryngeal nerve. If it is not in this place, it is probably in the thymus. The localization of PIV is more constant, they are located deeper than PIII at the level of the cricoid cartilage. When they are not typically localized, they have most probably gone downward across the oesophagus into the posterior mediastinum.

LITERATURE

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2. Udelsman R: Thyroidectomy. In: Rob and Smith’s Operative Surgery, eds. Carter DC, Russell RC and Pitt HA, Chapman and Hall. 1996: 1147-1158.

3. Lennquist S: Thyroidectomy. In:Textbook of Endocrine Surgery, eds Clark OH and Duh QY,Philadelphia,WB Saunders Company, 1997; 147-153.

4. Lennquist S, Cahlin C, Smeds S: The superior laryngeal nerve in thyroid surgery. Surgery, 1987; 102:999-1008.

5. Lennquist S: The Laryngeal Nerves in Thyroid Surgery. In:Jon A. van Heerden(ed):Comon Problems in Endocrine Surgery,Chicago,Year Book Medical Publishers. 1989; 123-131.

6. Moosman DA, De Weese MS: The external laryngeal nerve as related to thyroidectomy. Surg Gynecol Obstet. 1968; 127(5): 1011-1016.


7. Brieger HG: A Portrait of Surgery in America, 1875-1889. Surg Clin of North America, 1987; 67(6): 1181-1216.

8. Coller FA, Boyden AM: The development of the technique of thyroidectomy. Surg Gynecol Obstet. 1937; 65: 495-504

9. Thompson NW, Olsen WR, Hoffman GL: The continuing development of the technique of thyroidectomy. Surgery, 1973; 73(6): 913-927.

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16. Hamming JF, Roukema JA: Management of Regional Lymph Nodes in Papillary,Follicular and Medullary Thyroid Cancer. In:Textbook of Endocrine Surgery, eds Clark OH and Duh QY,Philadelphia,WB Saunders Company, 1997; 155-166.

17. Ellenhorm JDI, Shah JP, Brennan MF: Impact of therapeutic regional lyph node dissection for medullary carcinoma of the thyroid gland.Surgery, 1993; 114: 1078-1081.

18. Scheumann GFW, Gimm O, Wegener G et al.: Prognostic signi cance and surgical ma-nagement of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 1994; 18:559-567.

19. Noguchi S, Noguchi A, Murakami N: Papillary carcinoma of thyroid: Developing pattern of metastasis. Cancer 1970; 2: 1053-1060.

20. Henry JF, Denizot A, Bellus JF: Papillary thyroid carcinomas revealed by metastatic cervical lymph nodes. Endocr Surg. 1992; 9: 349-

21. Akerstrom G, Malmaeus J, Bergstrom R: Surgical anathomy of human parathyroid glands. Surgery 1984; 95: 14-21

22. Gilmour JR, Martin WJ: The wight of the parathyroid glands. J Pathol Bact. 1987; 34: 431-

23.Wang CA: The anatomic basis of parathyroid surgery. Ann Surg. 1976; 183: 271-275.

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