Clinical Appearance and Treatment of Adhesive Capsulitis in Diabetes

Appearance
Clinical
andTreatment
of
Adhesive
in Diabetes
Capsulitis
John D. MacGilivray,M.D,,and Mark C, Drakas,B.A,
Diabetes
mellitus
is a diversediseaseaffecting12million
Americans
in
andpresenting
(1).
multiple
organsystems Long{erm
complications
in
of diabetesincludealterations
connective
tissuethatoccuras a resultof
These
changesin glucosehomeostasis.
changesaffecttheextracellular
matrixand
mayleadto significant
in a myrdysfunction
iadof structures,
suchas bloodvesselsand
skin.Although
theetiology
is mostlikelymultifactorial,
several
studieshaveshowninglycosylation
creasednonenzymatic
of
collagen
type-llfibersinthepresence
of
highbloodglucose
levels(2,3) Thisglycoleadsto enhanced
sylation
cross-linking
amongcollagen
molecules,
whichrenders
themmoreresistant
to enzymatic
degradationandmayplaya rolein thecontracture
Dupuytren's
syndromes,
diseaseis an exampleof a contracture
syndrome
of thesofttissuesof theoalmwitha well-established
relation
Inthisarticle,
we present
to diabetes.
adheanother
contracture{ype
syndrome,
whichis a chronic
complicasivecapsulitis,
tionof diabetes.
Definitionand RiskFactors
Adhesive
capsulitis,
alsoknownas frozen
shoulder,
refersto a pathologic
condition
of
inwhich
theshoulder
of unknown
etiology
witha graduallossof
thepatientpresents
joint.Thedecrease
in
motionintheshoulder
is dueto a fibrotic
mobility
thickening
of the
jointcapsule
withadherence
to thehumeral
jointvolume.
head,resulting
in decreased
Tenderness
anddiffuseinflammation
often
Inaddition,
this
accompany
thiscontracture.
mayleadto hyperhidrosis
of the
condition
(4).
handinthe"shoulder-hand
syndrome"
riskfactors,
Adhesive
capsulitis
hasseveral
longduration
of diaincluding
femalegender,
betessymptoms,
ageolderthan40years,
prolonged
immobilization,
thyroiddistrauma,
disease,
andautoimease,cardiovascular
(5-12).
inaddition
munedisease
to diabetes
of 2"/"in
hasa prevalence
Adhesive
capsulitis
population,
or a littlemorethan
thegeneral
IO
fivemillionpeople.The prevalence
of adhesivecapsulitisin diabeteshasbeenreported
at 10 5% Io 29%(5, 7).Approximately
20%Io
30%of patientswithadhesivecapsulitis
will
developthe syndromein the contralateral
shoulder(10),and about70o/"arewomen.Viral initialization
and hormonalchangesduring
the perimenopausalyears
may alsoplaya
rolein itspathogenesis.
HistoricBackground
Theterm"adhesive
capsulitis"
was coinedin
(13)firstdocumented
1945whenNeviaser
changesin the synoviumand subsynovium
in a cohortof his oatientswithshoulder
pathology.lts linkto diabeteswas revealed
in 1972,whenBridgman(7)conducteda
prospectivestudyof 800 diabeticpatients
and 600 nondiabeticpatients.Eighty-six
(10.8%)of the peoplewithdiabetesand 14
(2.3'/.)of the nondiabeticcontrolswere
foundto haveadhesivecapsulitis.
Bridgman
(7) alsodiscoveredthatthe incidenceof adhesivecaosulitiscorrelatedwiththe duration
of diabetessymptoms.In addition,36 patients(4.5%)in the diabeticgrouphad both
shouldersaffectedversus3 (0.5%)in the
nondiabeticgroup.The authoradvocateddiabetesscreeningin patientswho presentto
theirphysicians
withunilateral
and especially
bilateralfrozenshoulder(7).Furthermore,
peoplewithType1 diabeteswerefoundto
havea greaterpredisposition
to adhesive
capsulitisthanthosewithType2 diabetes
(1 4 )
Histologically,
thisdiseaseis characterized
by synovialinflammation
followedby capsular
(15-19).
fibrosisand collagendeposition
(18)showedthe inRodeoand associates
volvementof cytokinesin the pathogenesis
of
adhesivecapsulitis.
higherconSpecifically,
centrationsof transforminggrowthfactorbeta,
platelefderivedgrowthfactor,and hepatic
growthfactorhavebeen isolatedin the synoviumand shouldercapsuleof patientswith
Thesecytokineshave
adhesivecapsulitis.
and
been associatedwith otherinflammatorv
PracticalDiabetology
- :'::: >squelae
in the bodYand arePre: --:t -f navesimilarfunctionsin adhesive
1.
FIGURE
CAPSULITIS
OFADHESIVE
STAGES
can be dividedinto
-:':sive capsulitis
(10,
in and colleagues
:;.:'a stages.Hannaf
of
findings adt, ::'relatedthe arthroscopic
as describedby Neviaser
-e: . e capsulitis,
colorkers(16,21),withthehistologic
".-:
: inicalf indings.Thesestagesare not
-::
: s:rete,but are ratherreferencepointswithin
of thisdisease.Properdiagno:-: continuum
implications
. and staginghavesignificant
"
and prognosisfor
- :ne courseof treatment
-re patient.
STAGE
STAGE1: INITIALIZATION
0 to 3 months
of sYmPtoms:
Duration
PE:Painwithactiveand passiveROM;limitainternalrotationof forwardf lexion,abduction,
rotation
tion,external
lossof ROM
EUA:Normalorminimal
synovitis
glenohumeral
Diffuse
Arthroscopy:
synovlhypervascular
Hypertrophic,
Histology:
unoerlynormal
infiltrates;
lammatory-cell
inf
tis;
ingcapsule
andStaging
Diagnosis
STAGE
2: FREEZING
STAGE
capsulitis
of adhesive
+lthough
theetiology
3 to 9 months
of sYmPtoms:
Duratron
haveelucrrecentstudies
s stillunknown,
PE:Chronicpainwithactiveand passiveROM;
of thiscondition,
datedthepathophysiology
of forwardflexion,abduclimitation
significant
to makemoreconfident
clinicians
enabling
externalrotation
tion,internalrotation,
can be
capsulitis
Adhesive
diagnoses.
ROMwhen
identicalto
primary,
EUA:ROMessentially
groupedintotwomajorcategories:
is
awake
oatient
andseccapsulitis;
adhesive
idiopathic
synovitis
Diffuse,pedunculated
withknownintrin- Arthroscopy:
capsulitis
ondaryadhesive
of
synovlThepathogenesis
hypervascular
origins.
Hypertrophic,
sicor extrinsic
Histology:
scarring;
witha
is progressive,
and subsynovial
capsulitis
adhesive
tiswithperivascular
in the underlying
and scarformation
painfullossof rangeof motion(ROM)inthe
fibroolasia
initialjoint.Therearefourstages:
caosule
shoulder
stage,frozenstage,
izationstage,freezing
STAGE3: FROZENSTAGE
in
andthawingstage.Theseareoutlined
9 to 14 months
of sYmPtoms:
Duration
Figu r 1
e.
Thecourseof
capsulitis.
of ROM,
adhesive
pain
Primary
at extremes
except
PE:Minimal
limits
insidiously.
end point
rigid
capsulitis
with
primary
ROM
adhesive
of
limitation
significant
himfrom
motionand prevents
ihe paiient's
to whenpatientis awake
EUA:ROMidentical
of dailyliving,
activities
normal
performing
fibrotic
No hypervascularity,
Arthroscopy:
withthearmoverhead,
activities
especially
diminwith
capsule
thick
svnovialremnants,
or externally'
or rotatedinternally
abducted,
volume
ishedcapsular
can
intheshoulder
Painandinflammation
withoutsignifisynovitis
Burned-out
Histology:
via
patients
fromdailyactivities
discourage
dense
hypervascularity,
or
hypertrophy
cant
lossof
furtheraccelerating
reflexinhibition,
formation
scar
forcedactivitydespite
motion.Conversely,
canleadto
symptoms
painandinflammatory
STAGE4: THAWINGSTAGE
withintheglenoimpingement
subacromial
15to 24 months
of symptoms:
Duration
joint.Aftera periodof time,thepahumeral
in
progressive
improvement
pain,
PE:Minimal
butthe
painusually
diminishes,
tient's
ROM
stiffwithsevere
extremely
remains
shoulder
in ROM.
EUA:Sameas stage3
limitations
Secondary
capsulitis'
adhesive
Secondary
Sameas stage3 withsomecelluArthroscopy:
associated
has
been
capsulitis
adhesive
larremodeling
Ina study
treatment.
withorotease-inhibitor
Sameas stage3 withsomecellular
Histology:
treatedwithmatrixmetallopro- remodeling
of 12patients
gastriccanfor inoperable
teinaseinhibitors
or
shoulder
afrozen
6
experienced
cers,
underanesthesia;ROM indicatesrange
examination
(22).
a reSimilarly,
syndrome
Dupuytren-like
ot motion.AdaptedfromClinOrthopMar(372):95-109,
2000.
whodeveloped
centreportof eightpatients
June2001
secof theshoulder
capsulitis
adhesive
imfor
human
treatment
indinavir
ondaryto
implicated
virus
infection
munodeficiency
protease
initiating
as a possible
inhibitors
(23).
mayshift
treatments
Such
mechanism
glenohumeral
synoof
the
theequilibrium
and
of
adhesions
resolution
from
viumaway
fibrotic
and
inflammatory
towardthe
to thiscondition.
inherent
Drocesses
of adhesive
The
Stage1 disease. diagnosis
primarily
thehistory
from
is made
capsulitis
causes
physical
other
after
examination
and
elimibeen
have
of oainandlossof ROM
present
withtennated.Instage'1,patients
Pain
duration.
dernessof lessthan3 months'
the
and
ROM,
of
is elicitedai theendpoints
as achyat rest.Since
is described
shoulder
patients
usuof thesymptoms,
theinitiation
particularly
allyreportgraduallossof motion,
abducforwardflexion,
rotation,
of internal
of the
Palpation
rotation.
tion,andexternal
posterior
capsuleelicitsihese
and
anterior
whichmayradiateto theinpainsymptoms,
sertionof thedeltoid.Painat nightandat rest
witha
Injection
is alsoa commoncomplaint.
improveallowsa significant
localanesthetic
of stage1
mentin ROMandis diagnostic
At thispointinthenatcapsulitis.
adhesive
are
thesymptoms
of thedisease,
uralhistory
of
withinthesynovium
dueto inflammation
synratherthana contracture
theshoulder
andbiopsyreveala hydrome.Arthroscopy
pervascular
withan influxof
synovitis
cells.
inflammatory
of active
anddocumentation
Evaluation
glenoandpassiveROMin theisolated
jointareimportant
forestablishing
humeral
pointsfor laterassessment
of proreference
gression
of thediseaseandefficacyof treatment.Weadvisethatthefollowing
and
be obtainedactively
measurements
internal
passively:
abduction,
forwardflexion,
(highest
spinousprocesson the
rotation
(withtheelbow
rotation
back),andexternal
spineexamination
flexed90").Cervical
Workupshould
shouldalsobe conducted.
x-raysof anteroposterior
includeroutine
axillary
rotation,
andexternal
viewsin internal
views,andoutletviews.
forexcluding
areimportant
Radiographs
processes
suchas glenootherpathologic
fracture,
glenoidor humeral
arthritis,
humeral
Patients
andosteopenia.
calcifictendinitis,
havefilms
capsulitis
withstage1 adhesive
a
reflecting
negative,
thatareessentially
1B
ratherthananosseous
mechanism
soft-tissue
thatmay
one.Othersofttissuepathologies
capsulitis,
of adhesive
mimicthesymptoms
impingement,
acuteor
suchassubacromial
defects,andlabrumtears,
chronicrotator-cuff
canbe ruledoutwithmagneticresonance
(MRl).MRIusually
showsincreased
imaging
capin adhesive
bloodf lowto thesynovium
recomMRIis notroutinely
sulitis.However,
of adhesive
mendedforthediagnosis
caosulitis.
of the aforeStage2 disease.Progression
processleadsto stage2 adhementioned
thesympAt thisjuncture,
sivecapsulitis.
for3 to 9 months,
tomshavebeenpresent
lossof ROM.Whena patient
withcontinued
duringthis
witha localanesthetic
is injected
butROMimproves
stage,painis alleviated
in ROM
Thelackof improvement
minimally.
volumedue
capsular
is a resultof decreased
inthe
condition
to thechronicinflammatory
jointspace.Arthroscopic
evalandhistologic
synouationsreveala dense,hypervascular
scarformation,
vitiswithperivascular
without
andfibroplasia
collagendeposition,
Thismarkstheconinfiltrates.
inflammatory
fromitsinflamcapsulitis
versionof adhesive
matorystageto a fibroticprocess.X-raysof
the patientin thisstagerevealdecreased
jointspace,particularly
recess.
in theaxillary
Thesesequelaecontinuein
Stage3 disease.
stage3, whenpatientspresentwithmarked
aswellas substanof theshoulder
stiffening
tiallossof ROM.At thisstage,painhasbeen
withsomevaripresent
for9 to 14months,
an exIngeneral,
abilityinthesymptoms.
tremelypainfulphasetypicallyresolves
and lossof ROM
butstiffness
spontaneously,
and
persist.
withlocalanesthetics
Injection
no
reveal
anesthesia
under
examination
an intra-articular
changein ROM,indicating
of the
lossofjointspaceas a consequence
histologic
and
Arthroscopic
fibrosis.
capsular
unreat thisstagearerelatively
evaluations
but
synovialthickening
with
some
markable,
i
ltrates.
i
nf
lammatory
i
nf
or
larity
hypervascu
no
Stage4 disease.In stage4, thereis a gradof ROMbecauseof cellularreualrecovery
withincreased
capsule,
of
the
modeling
thepainand
stage,
At
this
motion.
shoulder
jointhave
shoulder
in
the
fibroplasia
active
thepaConsequently,
subsided.
completely
via
in
the
shoulder
ROM
tientmustrecover
exercises.
andconditioning
strength
Severalstudieshave
diseases.
Associated
PracticalDiabetologY
withother
capsulitis
adhesive
associated
ratesof Dupuytren's
Increased
syndromes.
carpaltunnelsyntenosynovitis,
disease,
have
syndrome"
drome,and "shoulder-hand
of adhesive
inthepresence
beenreported
in
andmayreveala predisposition
capsulitis
to othercontracturetype
certainindividuals
(4,6,7, 15,24).Otherstudies
conditions
capthatadhesive
evidence
haveprovided
butnot
withretinopathy,
sulitisis associated
(5,7,
or macroproteinemia
withneuropathy
14).Webelievethatwhena patientpresents
heor sheshouldbe
capsulitis,
withadhesive
syndromes,
forothercontracture
screened
earlysigns
particularly
of thehand.Similarly,
shouldbe evaluated.
of retinopathy
2.
FIGURE
OF
REHABILITATION
CAPSULITIS
ADHESIVE
STAGE
STAGE1: INITIALIZATION
and paincycle
inflammation
lnterrupt
Goal:
postural
position,
(resting
Education
Treatment:
cortiNSA|Ds,
modification,
activity
correction),
(joint
mobiROM
exercises
injection,
costeroid
movement,
gentlephysiologic
lization,
passivemovement,
continuous
continuous
closed-chain
passivemotion,hydrotherapy),
program
home-exercise
scaoularstabilization,
STAGE
STAGE2: FREEZING
painand inflammation,
miniGoal:Decrease
of
and restriction
mizecapsularadhesions
ROM
injection,
NSA|Ds,corticosteroid
Treatment:
diand posterior
in the inferior
ROMexercises
activeexercisein the planeof the
rections,
scapula,trainingof scapularmuscles,homeprogram
exercrse
Treatment
include
capsulitis
foradhesive
Treatments
intrabenignneglect,physicalrehabilitation,
distention
injections,
corticosteroid
articular
jointmanipulation,
andsurgical
arthrography,
of thecapsuleof theglenohumeral
release
joint.Therehasbeena widespectrum
of
STAGE3: FROZENSTAGE&
of thisdisease,
treatment
regarding
opinions
STAGE
4:THAWING
STAGE
conservative
favoring
withsomeclinicians
Goal:IncreaseROM
moreaggresandothersfavoring
treatments
and
surgicalintervention
Possible
Treatment:
(10,24).Although
treatsiveinterventions
(propriopulation,
stretching
aggressive
mani
mentof thisdiseaseis stillcontroversial
softtissue
facilitation;
ceotiveneuromuscular
of eachof theinterbecauseof drawbacks
prolongedstretch),
low-load,
mobilization;
we believe
thatproperstagingof
ventions,
and tissueexto promoterelaxation
modalities
forestablishing
efthisdiseaseis paramount
strengthendiscomfort,
and reduce
tensibility
guidelines,
whichareoutfectivetreatment
force
couples,
scapula
ingto reestablish
2.
linedin Figure
program
home-exercise
thecourseof
Throughout
measures.
General
drug; ROM
anti-inflammatory
NSAIDindicatednonsteroidal
patients
withpainand limited
treatment,
indicatesrangeof motion.AdaptedfromClinOrthopMar
anti-inflammatory (372):9G-109,2000.
ROMaregivennonsteroidal
an intraFurthermore,
drugs(NSAIDs).
the patienthasadopted
because
anteriorly
mayhave
injection
of an analgesic
articular
in rerotatedposition
internally
an adducted,
Early
benefits.
andtherapeutic
diagnostic
sympsponseto thepainandinflammatory
injection
is adwitha corticosteroid
treatment
IOMS.
thesynovivocatedbecauseit can obliterate
f ibrosis
Stage1 disease.In patientswithstage1 adthesubsequent
tis,circumventing
is to
thegoalof treatment
hesivecapsulitis,
Theuseof specific
to thisdisease.
inherent
of thediseasecausedby
retardprogression
eninhibitors
to slowthechemical
cytokine
is
Activitymodification
thepainfulsynovitis.
gineof thisdiseaseis another
areaunder
that
to limitthetenderness
recommended
currentinvestigation.
with
thecycle.Painis attenuated
caninitiate
shouldalsobe placedin a superPatients
transcryotherapy,
otheranalgesics,
NSA|Ds,
program
ROM,
to restore
visedrehabilitation
and
painandinflammation,
nervestimulation,
electrical
cutaneous
andreattenuate
Therapies
to reduceingalvanic
stimulation.
function.
The
normalglenohumeral
establish
cryotherapy,
includeNSAlDs,
flammation
perceived
by thepatientoften
tenderness
phonophoresis,
andlocalcorprevents
iontophoresis,
fromreaching
an end
theclinician
Relaxwhenappropriate.
injection
pointto ROMpositions.
ticosteroid
therestFrequently,
jointis
ationof themusclesandshoulder
headhasmoved
of thehumeral
ingposition
June2001
19
achieved
withmoistheatandultrasound
Thebenefitsof physical
therapyarevaritherapies.
Hydrotherapy
is alsoadvocated
to
able.Mostpatients
reporta significant
improvideresistive
promote
goodbioexercise,
provement
by 3-4 months,
butothershave
mechanics,
andcreatea biofeedback
effect.
symptoms
thatmayevenprogress.
ApproxiHelpful
exercises
includeclosed-chain
momately10%of patients
havelongtermprobtions,wherethedistalaspectofthelimbrs
Iemswithadhesive
(26).Treatcapsulitis
fixed.Muscles
thatstabilize
thescapula
mentsin patients
refractory
to physical
thershouldbe strengthened
to promote
a stable
apyinclude
physical
continued
rehabilitation,
basefordistalmobility.
ROMcanbe improved closedmanipulation,
arthroscopy,
or capsupendulum
through
andpassive
exercises.
larrelease
andmanipulation.
MoreaggresStage2 disease.
ln stage2 adhesive
capsiveintervention
is warranted
in oatients
with
painis usually
sulitis,
elicited
attheextremes persistent
pain,stiffness,
andlossof function
of ROM.At thisjuncture,
limitation
in external forat least1 yearwithoutimprovement
derotation
is mostnotable,
witha rigidend
spiteconventional
conservative
treatments.
pointasa resultofthefibroplasia.
As in
Closedmanipulation
andarthroscopic
restage1,thegoalof therapyis to reducethe
leaseconstitute
thecurrentsurgical
treatcycleof painand inflammation.
Passive
mentoptions
foradhesive
capsulitis.
During
shoulder
movements
areadvocated
to rethisprocess,
therestricting
softtissueis
storenormalmotion
of theglenohumeraljoint physically
stretched
andtornas motionrsrejointspace,Frequent
andreestablish
ROM
storedin theentireROM.
pendulums,
exercises
including
caneexerArthroscopy
shouldbe performed
before
cises,and"end-ROM
mobilization
techmanipulation
to ruleoutpersistent
synovitis,
niques"(25)areadvisedto improveinternal
whichcouldbe excised
performing
without
andexternal
rotation,
themanipulation.
Inaddition,
we advocate
Stages3 and4 disease.
Patients
withstages
arthroscopy
f irstto ruleoutintra-articular
3 and4 adhesive
pathology
capsulitis
oftenreporta
andavoidfluidextravasation
into
resolution
of theirpainfulsymptoms,
butare
thetissues
asa resultof manipulation.
leftwithan extremely
stiffshoulder
withabArthroscopy
is alsousefulin detecting
connormalbiomechanics.
Intra-articular
corticomitantpathologies,
suchas rotator-cuff
or
costeroid
injection
is contraindicated
labraldefectsor subacromial
at this
impingement,
pointbecausetheinflammatory
stageof the
andin inspecting
thejointspaceandsyndisease,
inwhichsuchtreatment
wouldoe
ovium.Onceotherpathologies
havebeen
mostefficacious,
haspassed.Weadvisethat
excluded,
arthroscopy,
capsular
release,
and
treatment
optionsbe customized
to individmanipulation
areperformed.
ualpatients
andtheirparticular
degreeof
Thesequence
of manipulation
is asforglenohumeral
dysfunction.
lows:forwardflexion,
extension,
abduction,
Therisksandbenefitsof surgical
intervenand internal
andexternal
rotation.
Following
physical
tionversuscontinued
rehabilitation
manipulation,
an arthroscopic
capsularremustbeweighed.
goalat this
Theprimary
leaseis performed
withtheuseof an electrostageof thediseaseis to restoreROM
cauterydeviceanda motorized
shaver.
The
through
aggressive
stretching
beyondthepacapsular
scarcausedby thefibroplasia
is ditientsactiveROM.An activewarmuoencourvided,removing
themostprominent
restricagesbloodflowto theareaof interest.
protocol
A
tionto ROM.Thepostoperative
protracted,
low-load
stressmayincrease
the
entailsaggressive
ROMandstretching
exerplasticdeformation
passivemotion,
of thesofttissueof the
cises,continuous
treatment
capsule
andencourage
an increase
in ROM.
for painand inflammation,
andhydrotherapy.
quickandlargeforceslendto
Conversely,
Several
studieshaveshownthatarthroelasticdeformation
anda returnto theorescopicrelease
forrefractory
adhesive
capprostretch
state.Techniques
mayincludeproprio- sulitisis an appropriate
intervention,
particularly ducingsignificant
ceptiveneuromuscular
faciIitation,
increases
in ROMcomparedwiththe preoperative
mobilization
of thesubscapularis
andpecstate(27-29).
toralisminor;heat(intheformof ultrasound
Thesestudiesshowedthatoatients
or
withdiahot,moistcloths)topromote
musclerelaxbetesdid worseinitially,
buttheultimate
outation;andcryotherapy
to reducetenderness
comeswerecomparable
in patients
withand
Iitationexercises.
withoutdiabetes.
afterrehabi
20
PracticalDiabetology
Discussion
is a self-limited
adhesivecapsulitis
In general,
a
involving
with a clinicalhistory
dis-ease
several
of
oainfullossof ROMin the shoulder
months'durationand a physicalexamination
motion.Upon
painful,restricted
confirming
ROMshouldbe evaluated
initialexamination,
and documented,and x-raysshouldbe obsuch as
tainedto excludeotherpathologies
and fracture.In
olenohumeral
iointarthritis
iact. the hallmarkof this diseaseis lossof externalrotationwithoutevidenceof glenohumeralarthritison x-ray.
shouldbe treatedwithNSAIDS'
Patients
a supervisedphysicalinjection,
corticosteroid
to
program,and, if refractory
rehabilitation
and
closedmanipulation
thesetreatments,
References
patients
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29