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Parotid sialography for diagnosing Sjogren syndromeWouter W. I.
Kalk, MD, DDS, PhD,a Arjan Vissink, MD, DDS, PhD,aFred K. L.
Spijkervet, DDS, PhD,a Hendrika Bootsma, MD, PhD,bCees G. M.
Kallenberg, MD, PhD,c and Jan L. N. Roodenburg, DDS,
PhD,aGroningen, The NetherlandsUNIVERSITY HOSPITAL GRONINGEN
Objective. Despite the availability of many new imaging
procedures, sialography has, after decades of use, maintainedits
status as the imaging procedure of choice for evaluating the oral
component of Sjogren syndrome (SS). In this study,the clinical
value of sialography as a diagnostic tool in SS was explored by
assessing its diagnostic accuracy, observerbias, and staging
potential.Methods. One hundred parotid sialograms were interpreted
independently in a blinded fashion by 2 trained and 2expert
observers. Sialograms were derived from a group of consecutive
patients referred for diagnostics of SS. Patientswere categorized
as SS and non-SS by the revised European classification
criteria.Results. Trained observers reached a sensitivity of 95 and
a specificity of 33% for SS by sialogram, whereas expertobservers
reached a sensitivity of 87 and a specificity of 84%. There was
only fair interobserver agreement betweentrained and expert
observers, whereas both expert observers showed good agreement with
one another, according toCohens kappa. Intraobserver agreement was
good to very good for all observers. The 4 different gradations
ofsialectasia, ie, punctate, globular, cavitary, and destructive,
showed a weak but significant correlation with theduration of oral
symptoms.Conclusions. This study markedly shows that the diagnostic
value of parotid sialography for diagnosing SS greatlydepends on
the skills of the observer, implying that sialography lacks general
applicability as a diagnostic tool in SSand requires specific
expertise. Nevertheless, given its potentially high sensitivity and
specificity in diagnosing SS aswell as its useful staging
potential, sialography still has its use in the evaluation of the
oral component of SS.(Oral Surg Oral Med Oral Pathol Oral Radiol
Endod 2002;94:131-7)
Sjogren syndrome (SS) is considered a systemic auto-immune
disease with the exocrine glands as main targetorgans. As a result,
the presence of this disease maycause structural damage and
secretory dysfunction ofthe lacrimal and salivary glands. The
lacrimal andsalivary gland involvement with its inherent
morbidityis often addressed as the ocular and the oral compo-nents
of SS, respectively.
The oral component of SS can be evaluated in manyways.
Generally, 2 different procedures are practiced,ie, assessment of
salivary gland function and salivarygland imaging. Salivary gland
function is assessedthrough measurement of salivary secretion rate
(sialom-etry) and analysis of salivary composition
(sialochem-istry).1-3 Salivary gland imaging is currently
performedby several procedures including magnetic resonanceimaging
(MRI), computed tomography (CT) scanning,
ultrasonography, scintigraphy, and sialography.4-9 De-spite the
availability of advanced imaging procedures,the oldest procedure of
all, sialography, has maintainedits status as the method of choice
for exploring theductal system of the salivary gland to diagnose
SS.10
Sialography shows the architecture of the salivaryduct system
radiographically by infusion of a contrastfluid. Radiographic
demonstration of salivary glands invivo was first performed in
1913.11 Four decades agothe sialographic changes seen on sialograms
were ac-curately described and, with regard to chronic
siala-denitis, classified as punctate, globular, cavitary,
anddestructive sialectasia (dilatation) of the acinar sys-tem.12,13
These 4 sialectatic changes are thought torepresent increasing
glandular damage caused bychronic salivary gland inflammation.13 SS
is by far themost frequent cause of such chronic salivary
glandinflammation. Therefore, by observing sialectasia on
asialogram, the presence (and progression) of SS withregard to its
oral component can be determined.
It has been demonstrated that SS-related sialographicfindings
such as sialectasia are more closely related toSS-related clinical
symptoms (stimulated parotid sali-vary flow, incidence of
keratoconjunctivitis sicca) thanis the periductal lymphocytic
infiltration of the labialglands.14 In addition, superior
sensitivity15,16 and/orspecificity for SS have been frequently
ascribed to
aDepartment of Oral and Maxillofacial Surgery, University
HospitalGroningen, The Netherlands.bDivision of Rheumatology,
Department of Internal Medicine, Uni-versity Hospital Groningen,
The Netherlands.cDivision of Clinical Immunology, Department of
Internal Medicine,University Hospital Groningen, The
Netherlands.Received for publication Aug 22, 2001; returned for
revision Dec 9,2001; accepted for publication Apr 4, 2002.Copyright
2002 by Mosby, Inc.1079-2104/2002/$35.00 0
7/16/126017doi:10.1067/moe.2002.126017
131
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sialography as compared to labial gland biopsy.17-20However, the
subjective nature of reading and inter-preting a sialogram causes a
certain observer bias, as isthe case with diagnostic imaging tests
in general. Theamount of observer bias may have a substantial
impacton the clinical value of a particular diagnostic test.
In this study the clinical value of sialography as adiagnostic
tool in SS was explored by assessing itsdiagnostic accuracy,
observer bias, and staging poten-tial in 100 sialograms.
PATIENTS AND METHODSPatients
To study the clinical value of sialography for diag-nosing SS,
100 parotid sialograms were interpretedindependently by 4
observers. Two observers had muchgeneral experience in judging
sialograms, whereas 2observers were especially experienced in the
judging ofsialograms with respect to the diagnosis of SS.
Theobservers with general experience were termed trainedobservers,
and the observers with specific SS expertisewere termed expert
observers. Sialograms were derivedfrom a group of 100 consecutive
patients referred to theoutpatient clinic of the Department of Oral
and Maxil-lofacial Surgery of the University Hospital
Groningenduring the period from December 1997 until August1999.
Patients suspected of SS were referred by rheuma-tologists,
internists, neurologists, ophthalmologists,otolaryngologists,
general practitioners, and dentists.Reasons for referral included
mouth dryness, eye dry-ness, swelling of the salivary glands,
arthralgia, andfatigue. The diagnostic workup for SS, carried out
in allpatients, included the following aspects:
subjectivecomplaints of oral and ocular dryness, sialometry
andsialochemistry, histopathology of salivary gland tissue,serology
(SS-A and SS-B antibodies), and eye tests(rose Bengal staining and
Schirmer tear test). Sialogra-phy was excluded for diagnostic use
in this study toavoid an incorporation bias. In addition to the
diagnos-tic tests, the duration of oral symptoms and the
serumimmunoglobulin G levels were recorded to assess therelation
between the clinical and sialographic stage ofSS. Duration of oral
symptoms was defined as the timefrom first complaints induced by or
related to oraldryness until referral.
In this study the revised European classification cri-teria for
SS were used as reference standard for thediagnosis of SS,
categorizing patients as primary SS,secondary SS, or non-SS
patients.21,22
Exclusion criteriaThe exclusion criteria of the European
classification
for SS were applied. In addition, patients with iodine
allergy were excluded from the study, because iodinewas present
in the contrast fluid used. Psoriatic arthritisand human
immunodeficiency virus infection were ex-cluded because both
diseases may cause sialographicpresentations resembling SS.23-26 No
patients had to beexcluded from the study.
Technical procedure for sialographyAll sialograms were obtained
in the absence of acute
sialadenitis. If present, sialography was postponed
untilclinical signs of inflammation had subsided for at least6
weeks. Parotid sialograms were obtained preferablyof the right
gland in a standardized manner by the sameperson (W.W.I.K.). After
cannulation of the main duct,an oil-based contrast fluid (Lipiodol
UF, Biotek Ltd,Auckland, New Zealand) was injected slowly with
a2-mL Cornwall syringe (Becton and Dickinson, Frank-lin Lakes, NJ),
until the patient reported a suddenincrease of preauricular
pressure. Premature leakage ofcontrast fluid was prevented by
ligating the main ductunder local anesthesia. A General Electric
G1000 and aSiemens Orthopos (Sirona USA, Charlotte, NC) wereused as
x-ray apparatus for lateral and posteroanteriorviews, respectively.
Posteroanterior (6 degrees medio-lateral, focus-film distance 1.10
m) views were madewith an additional filter (2.73 mm aluminum) with
64.5kV/6.3 mA, and lateral (contact) views were made withan
additional filter (4.63 mm aluminum) with 58 kV/15mA during 0.18
second. A Kodak (Rochester, NY)T-MHT G/RA 18 24 film was used in a
Kodak Lanexcassette with medium intensifying screen. After re-moval
of the ligature and massaging the gland, patientswere advised to
stimulate salivary gland secretion withcitric flavored gum or candy
during the first hours toenhance washout of the remaining contrast
fluid. Thewhole procedure was completed within 15 minutes.
Evaluation of the sialogramsFour observers examined
independently 100 sialo-
grams in a random order by using a variable intensityview box
with ambient light dimmed. They were in-formed that the patients
had been referred as suspectedof SS and about the amount of
contrast fluid injected.Twenty-five of the 100 sialograms were
viewed a sec-ond time by all observers without being aware of it
todetermine intraobserver variability. All sialogramswere examined
in the presence of an independent in-vestigator who made sure that
each set of sialogramswas examined within 2 minutes.
Before the observers examined the sialograms, acalibration
session took place in which all observersagreed on the criteria to
be applied. Four differentpathologic patterns were agreed on (the
observers hadto determine whether these patterns were present
in
132 Kalk et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGYJuly
2002
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each sialogram). These patterns were sialectasia (sub-divided
into punctate, globular, cavitary, and destruc-tive), thin
appearance of the ducts with or without glandenlargement, irregular
and widened main ducts, andpresence of a space-occupying lesion,
respectively.
If present, sialectasia (dilatations) were graded ac-cording to
the classification of Blatt13: punctate if lessthan 1 mm in size,
globular if uniform and 1 to 2 mmin size, and cavitary if irregular
and more than 2 mm insize (Fig 1). A destructive pattern was
defined as com-plete destruction of the gland architecture,
simulatingan invasive neoplastic process.12 Sialectasia were
con-sidered to be the only patterns consistent with SS.Presence of
thin ducts was regarded as possibly con-sistent with sodium
retention dysfunction syndrome orsialoadenosis.27,28 Irregular and
widened main ductsconsistent with sialodochitis (salivary duct
inflamma-tion) were considered to be the prevalent feature
inchronic recurrent sialadenitis.29,30 A space-occupyinglesion on a
sialogram was considered to be suggestiveof a tumor compressing the
gland.
A consensus judgment of whether a sialogram was inaccordance
with the diagnosis of SS was based on themajority opinion of the
observers.
Statistical analysisData were submitted for statistical analysis
with the
Statistical Package for the Social Sciences (SPSS, Inc,Chicago,
Ill), version 9.0. The following statistical pro-cedures were
applied: Cohens kappa as measure ofinterobserver and intraobserver
agreement (observer bi-as)31,32 and Pearson and Spearman
coefficients as cor-relation tests. In the results section it is
stated which
statistical test was applied in a specific situation. A Pvalue
of less than .05 was considered significant.
RESULTSStudy group
By applying the revised European criteria for SS22on the cohort
studied, 39 patients were categorized asSS (20 primary and 19
secondary SS; male to femaleratio, 1:7; mean age, 54 years;
standard deviation, 15;range, 21 to 84 years) and 61 patients as
nonSS(negative for SS) (male to female ratio, 1:14; mean age,54
years; standard deviation, 15; range, 20 to 81 years).The latter,
on the basis of additional clinical and labo-ratory tests, were
diagnosed as having sialoadenosis(n 18), sodium retention
dysfunction syndrome (n 18), drug-induced xerostomia (n 11), or as
having noalternative disease directly related to salivary gland
Table I. Sensitivity, specificity, positive predictivevalue
(PPV), negative predictive value (NPV), andlikelihood ratio (LR) of
the 4 observers (expert:A,B;trained:C,D) for the diagnosis of SS in
a group of 100patients by presence of sialectasia on the sialogramN
100 A B C D Consensus
Sensitivity 87.2 82.1 94.9 92.3 92.3Specificity 70.5 83.6 32.8
23.3 70.5PPV 65.4 76.2 47.4 43.4 66.7NPV 89.6 87.9 90.9 82.4 93.5LR
3.0 5.0 1.4 1.2 3.1
Consensus judgment was based on the majority of individual
judgments foreach sialogram. Note the large differences between
expert and trainedobservers regarding specificity and LR.
Fig 1. The different stages of sialectasia in SS, as present on
lateral parotid sialograms. From left to right: (A) punctate
sialectasia,less than 1 mm in size; (B) globular sialectasia,
uniform of shape and 1 to 2 mm in size; (C) cavitary sialectasia,
irregular of shapeand more than 2 mm in size; destructive
sialectasia, complete loss of gland architecture (not shown).
Kalk et al 133ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGYVolume
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pathology (n 14). Mean duration of oral symptomsbefore referral
was 35 months for SS and 30 months fornon-SS patients (range, SS 0
to 180 months, non-SS 0to 240 months).
Test accuracy for SSThe sensitivity and specificity differed
greatly be-
tween the trained and expert observers. Trained observ-ers
reached a sensitivity of 95 and a specificity of 33%,whereas with
expert observers it was 87 and 84%,respectively (Table I). The
large difference in specific-ity was mainly due to differences in
deciding betweenno abnormality and punctate sialectasia. Expert
observ-ers chose no abnormality in cases of doubt (observers Aand
B, Table I), whereas trained observers chose punc-tate sialectasia
in the same situations (observers C andD). Examples of sialograms
that gave rise to doubt areillustrated in Figs 2 and 3.
Consequently, the likelihoodratios also greatly differed between
trained and expertobservers, varying from 1.2 (not very useful as a
test) to5.0 (very useful as a test). Consensus judgment on thebasis
of the majority opinion had an intermediate sen-sitivity and
specificity for SS of 92 and 71%, respec-tively, and a likelihood
ratio of 3.1. Sialectasia waspresent in 18 of the 61 non-SS
patients (Table II).
Observer agreementInterobserver and intraobserver agreement was
cal-
culated for the 4 pathologic conditions. With regard tothe
presence of SS (sialectasia as indicator), there wasonly fair
interobserver agreement between trained andexpert observers,
whereas both expert observersshowed good agreement with one
another. The intraob-server agreement was good to very good (Tables
III andIV). Regarding the diagnosis of other salivary
glanddisorders, the interobserver agreement varied from poorto
moderate (data not shown).
Staging of SSThe 4 different gradations of sialectasia (Fig
1)
showed a weak but significant correlation with theduration of
oral symptoms in SS patients (rPearson, 0.29;P .05). According to
consensus judgment of thesialograms, the observation of punctate
sialectasia cor-responded with an average duration of oral
symptomsof 15 months, whereas globular, cavitary, and destruc-tive
sialectasia corresponded with increasing durationof 39, 44, and 59
months, respectively.
No relation was observed between the serum immu-noglobulin G
level and the presence or grade of sial-ectasia.
Fig 2. An example of a parotid sialogram of an SS patient that
could give cause for doubt. Note the presence of initial
sialectasiaon both projections. All observers judged this sialogram
as positive for SS (sialectasia present).
134 Kalk et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGYJuly
2002
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Ductal changesThe presence of widened or irregular main
ducts,
consistent with sialodochitis, was not diagnostic for
SS(sensitivity 28%, specificity 62%, likelihood ratio 0.7)and was
related neither to salivary flow rates nor toduration of oral
complaints. The observation of thinducts with or without salivary
gland enlargement, re-garded as possibly consistent with
sialoadenosis orsodium retention dysfunction syndrome, did not
relateto any changes of salivary composition (eg, sodium,
potassium, amylase, total protein) or to salivary flowrate.
DISCUSSIONWe have shown that it is possible to achieve both
sensitive and specific test results with parotid
contrastsialography for diagnosing SS (likelihood ratio up to5.0).
This diagnostic accuracy, however, is very muchdependent on the
observer involved, which implies that
Table II. Judgments of 100 sialograms regarding the presence and
grade of sialectasia by 4 individual observers(expert:A,B;
trained:C,D) and by consensusN 100Sialectasia
A B C D Consensus
SS Non-SS SS Non-SS SS Non-SS SS Non-SS SS Non-SS
None 5 43 7 51 2 20 3 14 3 43Punctate 13 5 15 1 11 24 12 36 14
5Globular 11 6 10 3 4 5 15 5 11 7Cavitary 4 3 3 0 15 8 7 5 5
5Destructive 6 4 4 6 7 4 2 1 6 1
For each descriptive category the number of cases accordingly
judged is given. Consensus judgment is based on the majority of
individual judgments for eachsialogram. Note the large variability
between expert and trained observers regarding false positivity,
the trained observers judged many sialograms from non-SSpatients as
punctate.
Fig 3. An example of a parotid sialogram of a non-SS patient
that could give cause for doubt. Note the presence of
smallradiodensities on both projections that could be easily
misinterpreted as initial sialectasia. Both trained observers
judged thissialogram as positive for SS (sialectasia present),
whereas expert observers judged it as negative for SS.
Kalk et al 135ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGYVolume
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the technique lacks general applicability and requiresspecific
expertise.
The 4 different grades of sialectasia showed a weakbut
significant relation to the duration of oral symptomsin SS
patients, suggesting that sialectasia slowly wors-ens as the
disease progresses. Previous studies havealready shown that, in SS
patients, increasing grada-tions of sialectasia correspond with
lower salivary flowrates,3,14,33 as well as that salivary flow
rates deterioratewith increasing duration of oral symptoms.34 We
there-fore suggest that SS can be subdivided into
differentsequential stages according to the type of sialectasia
onthe sialogram, with a corresponding degree of
hyposali-vation.
Although the use of oil-based contrast fluid has oftenbeen
associated in the literature with high rates ofcomplications, we
have experienced none of the com-plications associated with
oil-based contrast fluids dur-ing or after the 100 sialograms
performed. The use ofoil-based contrast fluid in our hands results
in superiorimage quality. In case of iodine allergy,
sialographyshould not be performed to prevent local and
systemicallergic reactions. Alternative positive contrast
materi-als other than iodine that are currently in use are
notsuitable for sialography. Therefore, in cases of iodineallergy
other imaging techniques such as scintigraphyor ultrasonography
should be used instead to visualize
salivary gland involvement in SS. Regarding the use ofCT and MRI
techniques in diagnosing SS, conflictingresults have been reported
in the literature.4,5,8
Although some studies have reported abnormal pa-rotid
sialographic findings as a fairly common findingin control subjects
(up to 40%),8,35,36 sialography isgenerally considered to be a very
specific diagnostictest for SS.18-20 However, sialectasia may also
occur asa result of chronic recurrent parotitis, a condition
un-related to SS. The latter may perhaps account for atleast some
of the sialectasia we observed in 30% of thenon-SS patients.
Furthermore, some of the observedsialectasia in non-SS patients
probably has to be attrib-uted to observer error, because the
number of falsepositive cases varied markedly between trained
andexpert observers. The observers decision, especiallywhen in
doubt about recognizing initial sialectasia atthe beginning of SS,
reflects crucially on the test spec-ificity, ie, the number of
false positive cases (Tables Iand II, Figs 2 and 3). Other imaging
procedures, how-ever, may well suffer from the same human factor,
ie,subjectivity and varying expertise with interpreting
theimage.
Because diagnostic testing for SS is performed in thesecondary
health care, there is an increased priorchance for SS compared with
the general population.Furthermore, the diagnosis of SS is based on
severaldiagnostic tests. Both the increased prior chance for SSand
the combined test approach require diagnostic testswith emphasis on
specificity. For this reason it is rec-ommended that one chooses
negatively when in doubtabout the presence of sialectasia on a
sialogram (asillustrated in Figs 2 and 3), thereby increasing
thespecificity of the test result. The diagnostic accuracy
ofsialography might be further improved with
subtractionradiography.10,19 Such enhancement of image qualitymight
not only reduce the number of false positive testresults but also
significantly improve interobserveragreement. Disadvantages of this
procedure are its sen-sitivity to patient movement (swallowing,
tonguemovement) during contrast injection and the need
forsophisticated x-ray equipment.
In conclusion, reading and interpreting a sialogramrequire
certain expertise with regard to the recognitionand correct
interpretation of first stage sialectasia, re-stricting its use as
a diagnostic tool for incipient SS toexpert observers. In cases of
doubt, one should there-fore consider sending the digitized
sialogram to anexpert center. Despite limited general
applicability, sia-lography still has its unique value in the
evaluation ofSS. Its costs are low and, if interpreted properly, it
ishighly diagnostic. Furthermore, it has a relatively lowdegree of
invasiveness, and it is a relatively simple andquick procedure.37
The time relation of the progression
Table III. Interobserver agreement between the 4 ob-servers
(expert:A,B: trained:C,D) regarding the judg-ment of presence of
sialectasia on a sialogramN 100 A B C D
A B 0.762 C 0.386 0.339 D 0.322 0.258 0.588
Interobserver agreement is expressed by Cohens kappa. A kappa
valuebelow 0.200 is considered as poor agreement, between
0.200-0.400 as fair,between 0.400-0.600 as moderate, and between
0.600-0.800 as goodagreement (according to Landis & Koch32).
Note there is fair agreementbetween trained and expert observers,
moderate agreement between bothtrained observers, and good
agreement between both expert observers.
Table IV. Intraobserver agreement for the 4 observers(A-D) with
regard to repeated judgment of presenceand type of sialectasia in
25 sialograms, expressed byCohens kappaN 25 A B C D
0.824 0.874 0.839 0.762
A kappa value between 0.600-0.800 is considered as good
agreement,whereas values above 0.800 are very good agreement.
136 Kalk et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGYJuly
2002
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of sialectasia renders sialography an especially valuabletool in
SS to monitor disease progression.
The advice and support of Dr B. Stegenga (Oral and
Maxil-lofacial Surgeon, Epidemiologist, University Hospital
Gro-ningen) and Dr J. Schortinghuis (Research Associate,
Depart-ment Of Oral and Maxillofacial Surgery, University
HospitalGroningen) are gratefully acknowledged.
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Reprint requests:W. W. I. Kalk, MD, DDS, PhDDepartment of Oral
and Maxillofacial SurgeryUniversity Hospital GroningenHanzeplein
19713 GZ GroningenThe [email protected]
Kalk et al 137ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGYVolume
94, Number 1