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68
Review Article
IntroductIon
Theautoimmunemucocutaneousdisordersarethegroupof
diseases,sometimes characterized by acantholysisand in
whichcomponentsoftheepidermisandbasementmembrane
zonearetargetedresultingintheformationofmucosaland
cutaneousblisters.[1]Clinical identicationoftheseblisters
arenecessarytointerpretthepathologyaccurately.Clinical
signsare the well‑known mechanical signs evolved by
cliniciansand are considered animportant part of clinical
examinationinpatientwiththesedisorders.TheNikolsky’s
signisdenedasawell‑describedclinicalsignwhichmanifest
asdislodgementofintactsupercialepidermisbyashearing
force,indicatingaplane of cleavageintheepidermis.The
defectmaybeduetoepidermalantibodiesasinpemphigus
orstaphylococcal toxin asin staphylococcal scalded skin
syndrome.[2]Itischaracteristicallyassociatedwithpemphigus
vulgaris.[3]The presence of Nikolsky’ssign is a signicant
indicatorofactiveacantholysisandalteredstructuralintegrity
withintheepidermis,[4]whichallowsaphysiciantodetermine
thelevelofthesplitintheskinsoastodistinguishbetween
intraepidermaland subepidermal blistering diseasesin the
clinicalsettings.[5,6,7]
Literatureoftencoversclinicalobservationsandindividualcase
reportsinrelationtothesediseasesbutlittleattentionhasbeen
paidtotheimportanceandclinicalutilityofNikolsky’ssignand
otherrelatedsigninthediagnosisofthesedisorders.Thisclinical
paperisanattempttoillustratetheusefulnessofNikolsky’ssign
andotherrelatedsignsalongwiththeirdiagnosticandprognostic
signicanceintheclinicaldiagnosisofvariousmucocutaneous
blisteringdiseasesaffectingtheskinandoralcavity.
Methods
Togetup‑to‑dateinformation,aweb‑basedsearchwasinitiated
usingPubMed/Medlinedatabasesearchingforarticleswritten
Nikolsky’s Sign ‑ A Clinical Method to Evaluate Damage at
Epidermal‑Dermal Junction
Abhishek G. Soni
Department of Oral Medicine and Radiology, Modern Dental College and Research Center, Indore, Madhya Pradesh, India
Softtissuesoftheoralcavityareoftenaffectedbyvariousmucocutaneousdisordersofvariableetiology,affectingboththeskinandmucosae,
withsevereclinicalmanifestationssuchasblistersinvolvingthetissues;andthereforetheirappropriatemanagementreliesontheircorrect
diagnosis.Clinicalsignstoelicitcharacteristicsofblistersareacrucialpartoftheexaminationofpatientswithsuchdisorders.Itistherefore
essentialforclinicianstobefamiliarwith,orratherbeexpertatelicitingthesesignstoframeanaccuratediagnosis,sincepropertreatment
andfollow‑upwilldependonwhichdiseaseisinvolved.TheNikolsky’ssignisonesuchsignthatcanbehelpfulintheclinicaldiagnosisof
pemphigusgroupofdiseaseanddifferentiatingitfromotherblisteringdermatoses.ThisreviewgivesanoverviewofsignofNikolskyandother
relatedsign,itsclinicalpresentationandtheirdiagnosticimplications,usingPubMedandMedlinedatabasessearchingforarticleswrittenin
English.Peer‑reviewedarticlesweretargetedusingthekeywords“Nikolsky’ssign”,“mucocutaneousdisorders”and“pemphigus”.Available
full‑textarticleswereread,andrelatedarticleswerealsoscrutinizedandnallythesearchwassubsequentlyrenedtoarticlesconcerningto
“Nikolsky’ssign”.Itwasconcludedthatearlyrecognitionofthesesignsarenecessarytopreventdelayeddiagnosisandforearlyinstitution
ofappropriatetreatmentofthesepotentiallyseriousmucosalanddermatologicaldiseases.
Keywords:Dermis,epidermis,mucocutaneousdisorders,Nikolsky’ssign,pemphigus
Address for correspondence: Dr. Abhishek G. Soni,
Department of Oral Medicine and Radiology, Modern Dental College
and Research Center, Indore ‑ 453 112, Madhya Pradesh, India.
E‑mail: drabhishek_soni@rediffmail.com
Access this article online
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DOI:
10.4103/jiaomr.jiaomr_95_17
Abstract
How to cite this article:SoniAG.Nikolsky'ssign‑Aclinicalmethodto
evaluatedamageat epidermal‑dermal junction.JIndianAcadOral Med
Radiol2018;30:68‑72.
Received: 05‑10‑2017Accepted:04‑03‑2018Published:23‑04‑2018
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Soni: Nikolsky’s sign
Journal of Indian Academy of Oral Medicine & Radiology ¦ Volume 30 ¦ Issue 1 ¦ January‑March 2018 69
inEnglish. Peer‑reviewed articles were targetedusingthe
keyterms “Nikolsky’ssign”, “mucocutaneous disorders”
and“pemphigus” to determine the scope of coveragein
well‑documentedarticles.The search was subsequently
renedtoarticlesconcerningto“Nikolsky’ssign”.Thesites
ofspecialized scientic journals inthe areas of oraland
maxillofacialpathology,dermatology,and other relevant
journalswerealsoused.Thebibliographieswerealsoreviewed
toidentify additional relevant studies.Available full‑text
articleswereread,andrelatedarticleswerealsoscrutinized.
Historical Perspective
Nikolsky’ssignwasrstdescribedbyaRussiandermatologist,
Piotr Vasiliyevich Nikolsky(1858‑1940).[5]Althoughhisname
wasspelt Nikolskiy, the signis better known asNikolsky’s
sign.[8]Herelatedhow,afterrubbingtheskinofpatientswho
hadpemphigusfoliaceus,therewasablisteringordenudation
oftheepidermiswithaglistening,moistsurfaceunderneath.[9]
Accordingtohisexplanation,theskinshowedaweakrelationship
andcontactamongtheepidermallayers(betweenthecorneal
andgranular cell layers) onall surfaces and evenin places
betweenlesions(e.g.,blistersandexcoriations)onseemingly
unaffectedskin.[10]
Thecredit of the finding “Nikolsky’ssign” should also
goto his teacher ProfessorM.I. Stukovenkov [(a Russian
Dermatologist (1847-1897), at the University of Kiev)]who
pointedoutthisobservationinpemphigusfoliaceus.However,
thesignwaswelldescribedbyP.V.Nikolskiyinhisthesisand
popularlycametobeknownasNikolsky’ssign.Nikolsky’s
observationswere later conrmed byLyellin1956, who
describedaNikolsky’ssigninpatientswithtoxicepidermal
necrolysis.[9]
Pathophysiology
Thepathophysiologyassociated withNikolsky’ssignisthe
acantholysis[8]i.e.,lossofcoherencebetweenepidermalcells
duetothebreakdownoftheirintercellularbridges.[11,12,13]In
acantholysis,thecellsremainintactbutarenolongerattached
toeachother;theytendtoacquirethesmallestpossiblesurface
areaand become rounded up, resulting in intra‑epidermal
clefts,vesicles andbullae.[11]Thesigncanbeelicitedinthe
affectedareasaswellasinareaswithintact,normal‑appearing
skinandalso on the oral mucosalsurface.[8,14]However,in
theoralcavityidenticationofintactvesicleandbullareally
posedchallengetotheclinicianbecauseoffriablenatureof
oralmucosa and also due to the constantexposure of oral
mucosato the frictional irritation. Furthermore, rupture of
theselesionsleadstoerosionsorulcerationsonthemucosal
surface,hence making thediagnosis of such lesionseven
moredifficult because the lesionsoften resemble each
otherclinicallyandsometimesitisdifcult to differentiate
betweenthem.Theprimaryhistologicndinginpatientswith
pemphigusisacantholysiswiththeoccurrenceofsuprabasal
epidermal/intraepidermalsplits;[15,16]theseeventspresumably
contributeto the epidermal separation characteristic of a
positiveNikolsky’ssign.[7]Nikolsky’ssignisusuallypositive
indiseases with intraepidermal acantholysisand typically
negativeindiseaseswithdermo‑epidermalseparation,[8]thus
helpingtodistinguishpemphigusfrombullouspemphigoid.[7]
Elicitation of Nikolsky’s sign
Tilltodaythere is no absoluteconsensus available inthe
literatureonastandardmethodtoelicittheNikolsky’ssign.
However,Nikolskiyoriginallydescribedthree methods to
elicitthesign:[5,15,17]
(1) Hornylayercan be detached for a longdistance,even
onnormal‑appearingskin,by pulling a remnant of the
rupturedwalloftheblister;
(2) Hornylayercanbedislodgedonvisiblynormalskinareas
attheperipheryofexistinglesionsbylateralpressurewith
anger;and
(3) Normal‑appearingskincanbedenudedleavingthemoist
surfaceofthegranularlayerbyrubbingtheepidermis.
Althoughthe classic Nikolsky’s sign is seen on the skin,
therehave been two case reports showing itsappearance
onmucous membranes of othertissues. In one instance, a
Nikolsky’ssignwaselicitedintheesophageal mucosa ofa
patientwithpemphigus vulgaris.[18]Intheother,Nikolsky’s
signwaselicitedinthemucosaoftheuterinecervixin13of
16patientswithpemphigus.[19]However,these occurrences
areexceedinglyrare.
Conditions associated with Nikolsky’s sign
PositiveNikolsky’ssignisthe hallmark of pemphigus
vulgaris,[4]andishelpfulintheclinicaldiagnosisofpemphigus
groupof diseases.[15] Uzun andDurdu[5] in theirstudy on
123consecutive patients withvarious cutaneous diseases
presentingas intact blistersand/or erosions concluded that
Nikolsky’ssign offers a moderately sensitivebut highly
specictoolforthediagnosisofpemphigus.Otherblistering
conditions,which are known toexhibit Nikolsky’ssign
includepemphigus foliaceous, paraneoplastic pemphigus,
Stevens‑Johnsonsyndrome, staphylococcal scalded skin
syndrome(SSSS), toxic epidermalnecrolysis (TEN), oral
lichenplanus, benign mucous membrane pemphigoid,and
epidermolysisbullosa.[20,21]
Variants of Nikolsky’s sign
Clinical Nikolsky’s sign
Whenthe tangential pressure isapplied on apparently
normalskin/mucosa, or on peri‑lesionalskin/mucosa
oron affected skin/mucosa withthe thumb or ngerpad
resultis ashearingforcethat dislodgestheupperlayersof
epidermisfromthelowerepidermisresultinginformation
ofblisters, a phenomenon isknown as Nikolsky’s sign
(Clinical Nikolsky’s sign).[4,6,10,15,17,22]
Microscopic Nikolsky’s sign
MicroscopicNikolsky’ssignis the subclinical counterpart
ofNikolsky’ssign.[11]Whentangentialpressureisexertedon
apparentlynormalskin/mucosa,sameasinelicitingclinical
Nikolsky’ssign, resultin weakening of theintercellular
adhesion.Thismayproduceminimaldamageatthecellular
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Soni: Nikolsky’s sign
Journal of Indian Academy of Oral Medicine & Radiology ¦ Volume 30 ¦ Issue 1 ¦ January‑March 2018
70
levelwhichcan bedemonstratedonlymicroscopically.The
pathologicalchangesthatareinducedafterapplyingtearing
tangentialpressuretoskin/mucosaatthesubclinicallevel,is
denedasmicroscopicNikolsky’ssign.[4,11,16]
Ithasbeen proposed that microscopicNikolsky’ssign may
beabetterandmoresensitivemethodofrapiddiagnosisand
canincreasethesensitivityofthehistopathologicalstudies.[18]
HameedandKhan[16] intheirstudydemonstrated apositive
microscopicNikolsky’ssignin73.9%ofpemphiguspatients
whowerebiopsiedafterapplyingtangentialpressure.There
wereno changes in thebiopsies of healthy controls.They
suggestedthatthistechniquecouldbeofvalueinareaswhere
immunouorescenceisnotreadilyavailable.Inanotherstudy
byBarzegari M et al.,[4] they suggestedthat microscopic
Nikolsky’ssign wassignicantly higher in patientswith
generalizeddisease. Pemphigus vulgaris patients with
mucocutaneousinvolvement have both desmoglein (Dsg3)
andDsg1antibodies.[23,24]Presenceofthegeneralizeddisease
isprobablyduetomuchhigherpemphigus antibodylevels,
makingthedevelopmentofmicroscopicNikolsky’ssignmore
frequent.Thustheyconcluded that microscopic Nikolsky’s
signcan increase thesensitivity of histologic diagnosis of
pemphigusvulgaris.[4]
Marginal and Direct Nikolsky’s sign
“MarginalNikolsky’ssign”canbedescribedastheextension
ofthe erosion on thesurrounding normal‑appearing skin
byrubbing the skin surrounding existing lesions; while
“DirectNikolsky’ssign”is the induction ofan erosion on
normal‑appearingskin,distantfromthelesions.[6,11]Apositive
directNikolsky’ssignindicatessevereactivityofthedisease
inpemphigus.It istherstsign todisappearasthedisease
respondstotherapy;themarginalNikolsky’ssignmaypersist
forsometime.[25]
UzunandDurdu[5]determinetheusefulnessoftheNikolsky’s
signontheclinicaldiagnosisofpemphigusin123consecutive
patientsandfoundthatthesensitivityof“direct”Nikolsky’s
sign(38.4%)waslessthanthatofthe“marginal”form(69.2%),
butthe specicity of “direct”Nikolsky’ssign(100%)was
higherthanthatofthe“marginal”form(93.8%).Basedonthe
resultofthestudytheyconcludedthatapositiveNikolsky’s
sign,whenelicitedespeciallywith‘‘direct’’modication,is
moderatelysensitivebuthighlyspecicforclinicaldiagnosis
ofpemphigus,particularlyforpemphigusvulgaris.
Wet and Dry Nikolsky’s sign
Nikolsky’ssignis furthercharacterizedas“wet”and“dry”.
Afterapplyingpressureontheskinororalmucosalsurface,
whentheerodedbaseisfoundtobemoistandglistening,the
Nikolsky’ssignisconsideredas“wet”;while“dry”Nikolsky’s
signcan bedescribedas those,inwhichthebaseoferoded
skinororalmucosalsurfaceisdry.[7,11]
Modified Nikolsky’s sign
The“modiedNikolsky’s”signisdescribedastheperipheral
extensionofblistersonapplyingpressuretotheirsurface.This
ishelpfulin patientsinwhomanew vesicleorbullaisnot
availableforbiopsy.Theadvantagehereisthatthearticially
extendedblistercannot show epithelialregeneration,which
issometimesseenintheoorofoldersubepidermalblisters
makingthemappearasintraepidermal.[25,26,27]
Implications of Nikolsky’s sign
Diagnostic implication
• Nikolsky’s sign ispathognomonic of pemphigus
andcanbeusedas a preliminary test for theclinical
diagnosisofpemphigus inclinicalsettings.Although
questionshave been raised aboutits sensitivity and
specificity,[28,29]it appearsto be a highlyspecific
techniqueintheoralsetting(96.3%)andmaybevery
usefulinthe fundamentaldiagnosisoforalblistering
diseases.[30]Although the Nikolsky’ssign is highly
specic,it only offers moderate sensitivityfor the
diagnosisofpemphigusvulgaris[5]
• Nikolsky’ssignisalsousefulindifferentiating various
blisteringdiseases.Itisusuallypositiveinintraepidermal
blisteringdiseasewhileinsubepidermalblisteringdisease
suchasbullouspemphigoid,thesignisusuallyabsent.[7]
Prognostic implication
• Nikolsky’ssignmayalsobeconsideredasasuggestive
signfor the prognosis ofpemphigus by indicating
activediseaseorclinicalexacerbation.[5]TheNikolsky’s
signis positive in the active or progressivestage of
pemphigus.It becomes negative when patientreceives
immunosuppressivetherapyanditindicatestheendof
acutestagedisease.However,itsreappearanceduringthe
courseoftreatmentsignalsaareup.Suchapatientwould
requireanincreaseinthedosageofimmunosuppressant
ortheintroductionofnewdrugs[25]
• Inpatientswith active pemphigus vulgaris,a wet
signis expected, whereasthe dry sign indicates
re‑epithelializationbeneath a pemphigus blisterwhich
wouldsignifyinghealingandthusafavorablending.[21]
Nikolsky’s phenomenon
Theterm “Nikolsky’sphenomenon” is applied whenthe
superciallayer of the epidermisis felt tomove over the
deeperlayer,andinsteadofimmediatelyformingerosionas
inNikolsky’ssign,ablisterdevelopsaftersometime.[25]
Mauserung phenomenon
TheNikolsky’ssignmayalsobeelicitableintherareichthyosis
bullosaof Siemens, where itis termed the “Mauserung
phenomenon”.[31]
False Nikolsky’s sign
FalseNikolsky’ssign,alsoknown as Sheklakov’s sign, is
describedaspullingtheperipheralremnantroofofaruptured
blister,therebyextendingthe erosion on thesurrounding
normalskin.Theerosionsthusinducedarelimitedinsize,lack
thetendencytoextendspontaneously,andhealrapidly.[11,25]Itis
calledthe“falseNikolsky’ssign”becauseitisasubepidermal
cleavageoccurringintheperilesionalskin.[6]
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Soni: Nikolsky’s sign
Journal of Indian Academy of Oral Medicine & Radiology ¦ Volume 30 ¦ Issue 1 ¦ January‑March 2018 71
FalseNikolsky’ssignispositiveinsub‑epidermalblistering
disordersthat includes bullous pemphigoid, cicatricial
pemphigoid,pemphigoidgestationis,dermatitisherpetiformis,
linearimmunoglobulinA(IgA) bullous dermatosis,
epidermolysisbullosa acquisita, junctional and dystrophic
epidermolysisbullosa,porphyriasandbulloussystemiclupus
erythematosus(SLE).[25]
Pseudo Nikolsky’s sign
PseudoNikolsky’ssignor epidermal peeling signcan be
elicitedinthesamewayasfortrueNikolsky’ssign,butthis
couldbeelicitedonlyintheinvolvederythematousareas.Here,
theunderlyingmechanismisnecrosisofepidermalcellsin
contrasttoacantholysisintrueNikolsky’ssign.[11,14,25]
PseudoNikolsky’ssignis positive in Stevens‑Johnson
syndrome,toxicepidermalnecrolysis,insomecasesofburns
andbullousichthyosiformerythroderma.[25]
Other related signs
Bulla spread sign
The“bullaspreadsign”,alsoknownasLutzsign,[14,25]refers
totheextensionofablistertoadjacentunblisteredskinwhen
pressureisputonthetopofthebulla.[32]
Inthetraditional“bullaspread”sign,themarginofanintact
bullaisrstmarkedbyapen.Slowandcarefulunidirectional
pressureapplied by a ngerto the bulla causesperipheral
extensionofthebullabeyondthemarkedmargin.Thebulla
thusextendedhasanirregularangulatedborderinpemphigus
vulgaris,whilearegularroundedborderisobservedinbullous
pemphigoidorother subepidermal blistering disorders.The
signmay also be elicited on a burstblister if an adequate
portionoftheroofisintact.[14,25]
Thebullaspreadsignispositiveinallvarietiesofblistering
diseaseslike the pemphigusgroupof diseases and many
casesofsubepidermalblisters,includingbullouspemphigoid,
dermatitisherpetiformis, epidermolysis bullosaacquisita,
cicatricialpemphigoid, dystrophic epidermolysis bullosa,
bullousdrugeruptions,Stevens‑Johnsonsyndromeandtoxic
epidermalnecrolysis.[14,25]
Asboe-Hansen sign
TheAsboe‑Hansensign,namedbyaDanishphysician,Gustav
Asboe‑Hansen(1917‑1989),[14,33]isconsideredasavariationof
thebullaspreadsign.However,itappliestosmaller,intact,tense
bullaewherethepressureisappliedtothecentreoftheblister.[34]
BothAsboe Hansen and Nikolsky’s sign have been
demonstratedinacutebullouslichenplanus.[35]Duetofragility
oftheroofoftheblisterAsboeHansensignisusuallynegative
inHailey‑Hailey disease andstaphylococcal scalded skin
syndrome.[25]
conclusIon
Despitethenumerousinvestigationmethodsthatareusedinthe
diagnosisofautoimmuneblisteringdiseases,Nikolsky’ssign,
ifperformedcorrectlyandinterpretedproperly,canstillserve
asausefulandrapiddiagnostictooltoassistinpreliminary
chairsidediagnosisofthepemphigusgroupofdiseaseandalso
differentiatingitfromotherblisteringdiseases.Also,inthose
areaswherefacilitiesforimmunouorescencearelimitedand
appropriatelesionsforobtainingmeaningfulresultsbyroutine
histopathologyarenotreadilyavailable,theseclinicalsigns
couldbeusedasanadjunctivediagnosticmeasure.Insummary,
itappearsreasonabletoconcludethateveryclinicianshould
beawareabout theseclinicalsignswhichare imperativein
earlydiagnosisandprompttreatmentofthesepotentiallyfatal
mucocutaneousdiseasesinclinicalsettings.Althoughthelack
ofstandardizationregardinghowexactlytoelicitthesignhas
limitedits usefulness, but it remains an interestingsign to
observeandinterpret.
Financial support and sponsorship
Nil.
Conflicts of interest
Therearenoconictsofinterest.
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