TheAnatomic BasisofParathyroid Surgery [622420]

TheAnatomic BasisofParathyroid Surgery
CHIU-AN WANG,M.D.*
Astudyof645normaladultparathyroid glandsin160cadavers
revealed thatthereisadefinite patternofanatomic distribu-
tiononthebasisoftheembryologic development ofthe
parathyroid, thyroid, andthymicglands. Thesitesofpre-
dilection oftheuppergland(Parathyroid IV)are,inorder
offrequency, thecricothyroid junction; thedorsum ofthe
upperpoleofthethyroid; andtheretropharyngeal space.
Thoseofthelowergland(Parathyroid Ill)areatthelower
poleofthethyroidandthethymictongue;rarelyintheupper,
thelateralneck,orthemediastinum. Anunderstanding ofthe
developmental relationship oftheparathyroid glandstothethy-
roidandthethymusisfundamental inthedelineation ofthe
embryologic originoftheparathyroid glands.Theparathyroid
gland,located withinthesurgical capsule ofthethyroid
(subcapsular), whendiseased, remains inplacelocally.Agland
outsideofthecapsule (extracapsular) isoftendisplaced into
theposterior oranterior mediastinum. Acollective assessment
ofthesize,weight,color,shape,andconsistency ofthepara-
thyroidglandismandatory inthedetermination ofitsnormalcy.
Frozensectionexamination forstromal andintracellular fatty
contentisanaddedassurance ofnormalcy. Thatparathyroid
glandssinkinsalinesolution, andfatglobules float,mayaidin
differentiating thetwotypesoftissue.Supernumerary, fused,
andintrathyroidal parathyroids, albeitrare,areofsurgical
importance.
THEFOREMOST TASKforthesurgeon inparathyroid
exploration islocalization ofthediseased para-
thyroidgland.Familiarization withtheanatomic distribu-
tionandcharacteristic features oftheglandundernormal
conditions isthusessential.
Experience gainedfromthedissection of160cadavers
ispresented, withspecialreference toclinicalobserva-
tionsmadeatsurgeryforhyperparathyroidism.
Materials andMethods
Atotalof645parathyroid glandswererecovered
from160postmortem subjects ofwhom156had4,3had5,
and1had6parathyroid glands.Thoseinwhomlessthan4FromtheDepartment ofSurgery,
Massachusetts General Hospital and
Harvard Medical School, Boston, Massachusetts
glandswereidentified wereexcluded. Withinarangeof20
to80years,themeanagewas45.Therewere95
women and61men.Ineachpatient, deathhadre-
sultedfromdiseaseunrelated toparathyroid disorder.
Nonehadhadchronicrenaldiseaseorhadbeentreated
overalongperiodoftimewiththiazides forhyper-
tension.
Theparathyroid glandswereobtained bydissection.t
Eachglandwasmeasured andweighed immediately;
itscolor,shapeandconsistency werenoted;andits
position wassketched onaparathyroid chartinrela-
tiontosuchconstant anatomic landmarks asthecrico-
thyroidjunction, upperpoleofthethyroid, thymic
tongue,andmediastinal thymus.
Findings
Twenty-one ofthe645parathyroid glandsuncovered
werefrom4subjects withsupernumerary glands.
Dataontheseglandswillbepresented separately.
Basedupontheirembryologic derivation, halfofthe
remaining parathyroid glands(312)wereclassified asthe
upper(Parathyroid IV)andhalfasthelowergland
(Parathyroid III).
Position oftheUpperParathyroid Glands
(Parathyroid IV)
Ofthe312upperparathyroid glands,241(77%)were
foundatthecricothyroid junction posteriorly (Fig.la),by
farthemostcommon siteofParathyroid IV.Herethe
tDissection wascarriedoutinsitusystemically. Thetracheo-
esophageal groovewasentered. Searchfortheparathyroid wasbegun
fromtheangleofthejawdowntothemediastinum, including the
thymus.
271Submitted forpublication August15,1975.
*VisitingSurgeon, Massachusetts General Hospital; Associate
ClinicalProfessor ofSurgery, Harvard Medical School.

Ann.Surg.*March1976
®!)CRICOTHYROIDAL and
JUXTACRIOI DAL
241Cases….77%Nr x
BEHIND UPPER POLE
ofTHYROID
68Cases…. 22%
/
0;l
RETROPHARYNGEAL andRETROESOPHAGEAL
3Cases….1%
FIGS.latoc:Anatomic distribution of312upperparathyroid
glands(Parathyroid IV).tributed ratherevenlybetween thelowerpoleofthe
thyroid andthethymus. In131cases(42%),Para-
thyroid IIIwasfoundinananterior oralatero-
posterior surfaceofthelowerpoleofthethyroid(Fig.
2a).Inthesepositions, theglandwasfrequently ob-
scured byvessels orhidden between thethyroid
creases. Thefactthatitwasoftenenclosed inapad
offattytissueprovides thesurgeon withacluetothe
identification ofthegland.
Onehundred andtwenty-two Parathyroid III(39Wo)
werelocated inthelowerneckwithinthethymic
tongue, whichisadistinct structure atthethoracic
inlet,extended fromthelowerthyroid poletothe
mediastinal thymus. Six(2%)werefoundinsidethe
mediastinal thymus, 3to4cmbelowthesternalnotch
(Fig.2b).
Ofthe47(15%)uncovered somedistance lateralto
thelowerthyroidpole,nearlyallweresuspended from
thevascular tributaries. Theseglandswereinvariably
embedded inalobuleoffattytissue(Fig.2c).
Six(2%)occupied anectopicposition(Fig.2d).Three
werehighatthecarotidbifurcation and2to3cmlateral
fromtheupperpoleofthethyroid. Theother3were
locatedinthemidthyroid, nearbutoutsideofthecarotid
sheath.Allwereassociated withasmallpadofthymic
remnant.
glandwasintimately associated withandoccasionally hid-
denbytherecurrent laryngeal nerveandtheadjacent
vascular branches. Mostoftheseglandsweresuspended
byasmallpedicle andenveloped byapadoffatty
tissue.
Sixty-eight (22%)ofthe312parathyroids weretucked
behindtheupperpoleofthethyroid(Fig.lb).Inthis
position, Parathyroid IVwasinvariably subcapsular, ly-
ingunderneath thesurgical capsule ofthethyroid.* It
wasreadilyextruded through theincisedcapsule. Afine
vascular pediclewasnotedascomingfromthethyroid;
nonewasnotedasoriginating fromthecapsule. The
absence ofcapsular fixation permits animpressive
mobility uniquely characteristic oftheparathyroid; a
thyroidnodulenevermovesasfreelywithinthecapsule
astheparathyroid.
ThreeParathyroid IV(lessthan1%)wereuncovered
behindthelowerpharyngeal andupperesophageal
junction inthemidline, encased inalobuleoffatty
tissue(Fig.1c).
Position oftheLowerParathyroid (Parathyroid III)
Thelowerglands(Parathyroid III)weremorewidely
distributed thanParathyroid IV.Theseglandsweredis-()LOWERTHYROID
AaftruirandposteriorsurfoasV3VCm…4.1
©EJUXTATHYROIDAL
47Cow._.OX
*Alsoknown asthepretracheal laminaofthecervical fascial FIGS.2atod:Anatomic distribution of
sheath. glands(Parathyroid III).272 WANG
312lowerparathyroid

PARATHYROID SURGERY
Size,Weight,Color,Consistency andShape
Stripped offat,theaverageparathyroid inthisstudy
measured 5x3x1mm.Thelargestglandwas12x2
x1mmandthesmallest 2x2x1mm.Whenthegland
wasunusually longittendedalsotobenarrowandthin;
conversely, whenitwasshort,itwasinclined tobewide
andthick.
Theaverageweightofaparathyroid inthisserieswas
35to40mg.Itvariedsomewhat withageandsex,
beingheavierinthemanandinpersons between 20and
30yearsofage,andlighterinthewomanandinthose
between 70and80.Thesmallest parathyroid weighed
10mgandthelargest,78mg.
Thecoloroftheglandrangedfromreddishtoyellowish
tan.Incasesofsuddendeath,asinacutecoronary
heartdisease, theglandsweregenerally reddishbrown,
possibly asaresultofvenousstasis.Withchronic ill-
nessandmalnutrition orinthepresence ofinter-
stitialedemafromexcessive infusionoffluid,theglands
werepale,havingaslightlyyellowish tingesimilarto
thecolorofalobuleofordinary fat.
Theparathyroid glandwassoftandpliableincon-
sistency. Asaconsequence, itwaseasilyshapedand
moldedbytheadjacent tissue.Thissoftconsistency
wasusefulindifferentiating aparathyroid glandfrom
alymphnodeorathyroidnodule,bothofwhichwere
firmandelasticincontrast. Onsectioning, thecut
surfaceofaparathyroid wasextremely finelygranular
intexture, similartothatofrawchickenliver.
Theinelasticity ofthenormalparathyroid accounts for
itsvarietyofshapeandcontour(Fig.3).Whenthegland
wassubcapsular, asitwaswhenlocated attheupper
poleofthethyroid, itappeared flattened andresembled
apancake oraleaf.Inthecricothyroidal orintra-
thymicposition ontheotherhand,theglandhasan
ovalorspherical shape,suchasateardrop. Occasionally
aglandappears tobebean,sausage, orrod-shaped.
Asubcapsular glandinvariably hasasharpedge;but
inanextracapsular parathyroid gland,whichwasoval
orround,therewasnosharpedge.
Uponfrozensectionexamination, stromalfataswellas
intracellular fattygranules wasinvariably presentina
normalparathyroid. Suchfattycontent wasabsentor
diminished inahyperfunctioning gland.
Withoutexception, apieceofparathyroid tissuesank
innormalsalinesolution, whereas afattyglobulewas
foundtofloat.Thisobservation servestodifferentiate
aglobuleoffatfromaparathyroid gland.
Supernumerary, Fused,andIntrathyroidal Parathyroid
Glands
Foursubjects hadsupernumerary glands.Ofthese,
threehad5andonehad6glands. Inpersons with5
glands,3werelocatedintherightsideand2intheleft.0OVAL
0LEAF273
TEARDROP
SAUSAGE
SCALE:IIef O~
PANCAKE SPHERICAL
ROD BEAN
Variesfrom3-6mm
FIG.3.Variations inshapeofnormalparathyroid glands.
Intheonesubjectwith6glands,3werelocatedineach
side.Alltheseglandswereassociated withalobuleof
thymicremnant. Ingeneraltheyweresmallerthanthe
normalglands,beingmaximally 2mminlengthand1mm
inwidth.Fusedandintrathyroidal parathyroid glands
werenotencountered inthisstudy.
Discussion
Thefindings justpresented areingeneralagreement
withmostoftheauthorscited;butinaddition certain
anatomic features shouldbeemphasized fortheirrele-
vanceatsurgery. Ihave,therefore, correlated these
anatomic findings withclinicalobservations underthe
following headings fordeliberation.
A.Localization andRecognition oftheUpperandLower
Parathyroid Gland
Thisstudyshowsthatdespitethewidedistribution,
theparathyroid glandfallsintoadefinite pattern, and
canbeuncovered intheselocations inagreatmajority of
thecases.
Embryologically theuppergland(Parathyroid IV)
sharesacommon primordium inthefourthbranchial
pouchwiththelateralthyroid whichsubsequently
fuseswiththelateralwingofthemedianthyroid.4'6
Itisnowonder, then,thatupperparathyroid glands
(Parathyroid IV)areinvariably foundincloseproximity
tothedorsum oftheupperthyroidlobe,eitherbehind
theupperpoleoratthecricothyroid junction. Theseare
byfarthemostcommon positions oftheupperpara-
thyroid, although afewoftheglandsmaybelocated
intheretropharyngeal orretroesophageal space.
Similarly, embryologic evidence maybeseeninthe
distribution ofthelowerparathyroid glands(Para-
thyroidIII).Ithasbeenshownthatboththelower
glandandthethymusarisefromthethirdbranchial
complex.4'6 Asthecomplex descends caudally, thelowerVOl.183.NO.3

C.Criteria ofaNormal Gland
Ofalltheparameters ofnormalcy inaparathyroid
gland,sizeandweight areusuallyregarded asthemost
important determinants.1'3 Asourobservations andthose
ofothers attest,46 however, there areoccasional vari-
ations.Theaverage dimension ofanormalglandinour
series was5x3xImm,butonegland wasaslargeas
12mmandoneassmall as2mm.Evenlargerglands
havebeenreported.3 Clearly, sizecannotalwaysbe
usedasthesoledeterminant ofnormalcy inthegland.
Moreover, aparathyroid glandinsituisalwayslarger
because ofitsintensevascularity. Oncetheglandisre-
moveditisnolongerhyperemic andinstantly becomes
smaller. Forthisreason, thediscrepancy insizeoften
arisesbetween thesurgeon attheoperating tableand
thepathologist inthelaboratory.
Theweightofthenormalglandislessvariable than
thesize,averaging 35to40mginourseries.Thelarg-
estglandweighed 78mg,andwasfoundinamanwith
threeothersmallglandsof20,15,and12mgrespectively.
Theoretically, theweightofaglandisabetterindexof
normalcy thansize,butitisimpracticable toweigh a
normalglandatsurgeryunlesstheglandissacrificed.
Thecolorofaparathyroid glanddepends onthe
amount offattytissueandthedegreeofvascularity.1
Anormalcadaveral glandgenerally appears yellowish-
tan,withtheexception ofthoseobtained fromvictimsof
suddendeathwhoseglandsappeared reddish-brown in
color, asaresultofvenousstasis.Inlife,theglandofa
young personhasrelatively fewerfattycellsandiscon-
sequently morereddish-brown thanthatofanelderly per-
sonwhoseglandhasmorefatcellsandgranules,
givingrisetoayellowish-tan color.Itisthepresence
ofstromal fattycellsandintracellular fattygranules,
demonstrated byfrozensectionexamination, thataidsin
confirmation ofthenormalcy ofthegland.
Anormalgland,inthefaceofaparathyroid neoplasm,
frequently appearsyellowish-tan incolor,suchasthatof
acadaveral specimen. Itistheresultofatrophyofdisuse,
aphysiological response totheautonomous diseased
parathyroid. Thus,thecolorofaparathyroid gland may
provide thesurgeon withacluetodifferentiating the
pathologic typeofhyperparathyroidism.2 Forinneo-
plasia,particularly thecommon adenoma, thedisease
process islocalized andonlyonegland orpartofone
glandisinvolved; theremaining threebecome atrophic
andyellowish-tan incolor.Inhyperplasia, ontheother
hand,allfourglands arediseased andhyperemic and,
therefore, allarereddish orbeefy-red incolor.
E.Supernumerary, FusedandIntrathyroidal Glands
Supernumerary glands varyfrom 5to8innumber.3'4'6
Inourstudythere were4subjects (or2.5%)withglanddissociates fromthethymusand,inmostinstances,
islocatedintheanterior orlateroposterior aspectofthe
lowerthyroidpole.Innearlyhalfofthecases,thelower
glandremains withinthethymic tongue atthethoracic
inlet.Afewglands maydescend withthethymus into
themediastinum, ormaybelefthighintheneckasa
resultofearlydevelopmental arrest.Thus,thelower
gland maybefoundanywhere fromtheangleofthe
jawtothepericardium. Thisembryologic variation ac-
countsforthewidedistribution ofthelowergland.
Because ofthisembryologic variation theidentifica-
tionoftheoriginoftheglandisnotalways easy.
Whentheglandisencountered intheseexceptional
locations, itisdifficult tobecertainwhether itisan
upper oralowerparathyroid.
Ithasbeenpresumed thataglandlocatedhighinthe
neckisalways anuppergland(Parathyroid IV)andthat
onelowintheneckisalowergland(Parathyroid III),
apresumption thatisgenerally correct. Asnoted
earlier,however, alowergland(Parathyroid III)may
beleftintheuppernecksecondary tofailureof
descent ofthethirdbranchial complex. Theidentity of
amisplaced lowergland canbemadeonlybythe
presence ofacloselyassociated thymic remnant.
Ontheotherhand, anuppergland(Parathyroid IV)
maybelocated inthelowerpoleofthethyroid.
Inthissituation, theglandisfrequently suspended bya
longbuttenuous vascular pediclefromtheinferiorthyroid
arteryandlateralthyroid veinatthecricothyroid
junction. Theoriginofthevascular pedicle mayserve
asaguideintheidentification ofalow-lying upper
parathyroid gland(Parathyroid IV).Byknowing which
glanditis,thesurgeon maysavemanyhoursinsearchof
themissingparathyroid.5
B.Subcapsular andExtracapsular Parathyroid Glands
Itiswellknownthatthethyroidglandissheathed ina
transparent fibrouscapsule whichisthickandstrongin
theupperandmiddleportions ofthethyroidandthin
andfriableinthelowerthyroid pole.When apara-
thyroidglandislocated behindthiscapsule, itisdes-
ignated assubcapsular; andonelyingoutsideofthecap-
suleisknown asextracapsular. Thisanatomic feature
isofsurgicalimportance because, whendiseased, asub-
capsular parathyroid usually remains initsplaceand
expands locally withintheconfines ofthesurgical
capsule ofthethyroid. Anextracapsular parathyroid,
ontheotherhand,tendstobedisplaced intoanarea
whereitmeetslittleifanyresistance. Thus, anen-
largedsubcapsular parathyroid gland,locatedbehindthe
upper orlowerpoleofthethyroidisseldomdisplaced
toanydegree, andanextracapsular glandatthecrico-
thyroidjunction orwithinthethymus invariably falls
intoeithertheposterior oranterior mediastinum.274 WANG Ann.Surg. 9March1976

Vol.183.No.3 PARATHYROID SURGERY 275
supernumerary glands,with5glandsin3,and6glands
in1subject. Supernumerary glandsarefrequently
associated withinalobuleofthymictissuewhichsug-
gestsitsderivation fromthesameprimordium withthe
thymus,havingundergone multipledivisions inthecourse
ofembryologic descent. Theclinical significance of
supernumerary glandsliesinthefactthatitcanbethe
causeofcontinuing hyperparathyroidism.
Whentwoparathyroid glandsareintimately approxi-
matedtoeachother,andappearfused,theyareknownas
"kissing pairs."Atrue"kissing pair"israreandwas
notencountered inthisstudy.Akissing-paired para-
thyroidmaybedifferentiated fromabilobular glandby
thepresence ofacleavage planewhichisabsentina
bilobular gland.Further, abilobular glandoftenhasan
intactcapsule. Itisimportant nottoconfuse thetwoat
thetimeofsurgicalexploration.
Anintrathyroid parathyroid isadistinct possibility,
thoughararity.Nonewasuncovered inthisstudy.Itis
generally theuppergland(Parathyroid IV).Inthis
instance, theprimordium oftheParathyroid IVinthe
4thbranchial pouchistrapped between thelateralandthemedianthyroidpriortotheirembryologic fusion.
Thus,itisfrequently locatedwithintheupperthyroid
lobe.Atrueintrathyroidal glandissurrounded withthy-
roidtissueonallfoursides.Onethatisburiedinthe
creaseofthethyroid orlocated withinthesurgical
capsule ofthethyroid maynotbedefined asintra-
thyroidal.
References
1.Castleman, B.andMallory, T.B.:ThePathology ofthePara-
thyroidGlandinHyperparathyroidism. Am.J.Pathol11:1,1935.
2.Cope,0.:TheStoryofHyperparathyroidism attheMassa-
chusetts GeneralHospital. N.Engl.J.Med.,274:1174, 1966.
3.Gilmour, J.R.:TheGrossAnatomy oftheParathyroid Glands.
J.Pathol.Bacteriol., 46:133,1938.
4.Norris, E.H.:TheParathyroid GlandsandtheLateralThyroid
inMan:TheirMorphogenesis, Histogenesis, Topographic
Anatomy andPrenatal Growth. Carnegie Inst.,Washington,
Pub.No.479,Contrib. Embryol., 159:247, 1937.
5.Wang,C.A.:Surgery oftheParathyroid Glands. Advances in
Surgery, Vol.5,EditedbyC.E.WelchandJ.D.Hardy.
Chicago, YearBookMedicalPublishers, Inc.,1966,pp.109-127.
6.Weller, G.L.:Development oftheThyroid, Parathyroid and
Thymus GlandsinMan.Carnegie Inst.,Washington, Pub.No.
443,Contrib. Embryol., 141,Vol.24,1933.