Parotid sialography for diagnosing Sjogren syndrome

Wouter W. I. Kalk, MD, DDS, PhD,

a
Arjan Vissink, MD, DDS, PhD,
a
Fred K. L. Spijkervet, DDS, PhD,
a
Hendrika Bootsma, MD, PhD,
b
Cees G. M. Kallenberg, MD, PhD,
c
and Jan L. N. Roodenburg, DDS, PhD,
a
Groningen, The Netherlands
UNIVERSITY HOSPITAL GRONINGEN
Objective. Despite the availability of many new imaging procedures, sialography has, after decades of use, maintained
its status as the imaging procedure of choice for evaluating the oral component of Sjo gren syndrome (SS). In this study,
the clinical value of sialography as a diagnostic tool in SS was explored by assessing its diagnostic accuracy, observer
bias, and staging potential.
Methods. One hundred parotid sialograms were interpreted independently in a blinded fashion by 2 trained and 2
expert observers. Sialograms were derived from a group of consecutive patients referred for diagnostics of SS. Patients
were categorized as SS and non-SS by the revised European classication criteria.
Results. Trained observers reached a sensitivity of 95 and a specicity of 33% for SS by sialogram, whereas expert
observers reached a sensitivity of 87 and a specicity of 84%. There was only fair interobserver agreement between
trained and expert observers, whereas both expert observers showed good agreement with one another, according to
Cohens kappa. Intraobserver agreement was good to very good for all observers. The 4 different gradations of
sialectasia, ie, punctate, globular, cavitary, and destructive, showed a weak but signicant correlation with the
duration of oral symptoms.
Conclusions. This study markedly shows that the diagnostic value of parotid sialography for diagnosing SS greatly
depends on the skills of the observer, implying that sialography lacks general applicability as a diagnostic tool in SS
and requires specic expertise. Nevertheless, given its potentially high sensitivity and specicity in diagnosing SS as
well 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 target
organs. As a result, the presence of this disease may
cause structural damage and secretory dysfunction of
the lacrimal and salivary glands. The lacrimal and
salivary gland involvement with its inherent morbidity
is often addressed as the ocular and the oral compo-
nents of SS, respectively.
The oral component of SS can be evaluated in many
ways. Generally, 2 different procedures are practiced,
ie, assessment of salivary gland function and salivary
gland imaging. Salivary gland function is assessed
through measurement of salivary secretion rate (sialom-
etry) and analysis of salivary composition (sialochem-
istry).
1-3
Salivary gland imaging is currently performed
by several procedures including magnetic resonance
imaging (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 maintained
its status as the method of choice for exploring the
ductal system of the salivary gland to diagnose SS.
10
Sialography shows the architecture of the salivary
duct system radiographically by infusion of a contrast
uid. Radiographic demonstration of salivary glands in
vivo was rst performed in 1913.
11
Four decades ago
the sialographic changes seen on sialograms were ac-
curately described and, with regard to chronic siala-
denitis, classied as punctate, globular, cavitary, and
destructive sialectasia (dilatation) of the acinar sys-
tem.
12,13
These 4 sialectatic changes are thought to
represent increasing glandular damage caused by
chronic salivary gland inammation.
13
SS is by far the
most frequent cause of such chronic salivary gland
inammation. Therefore, by observing sialectasia on a
sialogram, the presence (and progression) of SS with
regard to its oral component can be determined.
It has been demonstrated that SS-related sialographic
ndings such as sialectasia are more closely related to
SS-related clinical symptoms (stimulated parotid sali-
vary ow, incidence of keratoconjunctivitis sicca) than
is the periductal lymphocytic inltration of the labial
glands.
14
In addition, superior sensitivity
15,16
and/or
specicity for SS have been frequently ascribed to
a
Department of Oral and Maxillofacial Surgery, University Hospital
Groningen, The Netherlands.
b
Division of Rheumatology, Department of Internal Medicine, Uni-
versity Hospital Groningen, The Netherlands.
c
Division 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 7/16/126017
doi:10.1067/moe.2002.126017
131
sialography as compared to labial gland biopsy.
17-20
However, the subjective nature of reading and inter-
preting a sialogram causes a certain observer bias, as is
the case with diagnostic imaging tests in general. The
amount of observer bias may have a substantial impact
on the clinical value of a particular diagnostic test.
In this study the clinical value of sialography as a
diagnostic tool in SS was explored by assessing its
diagnostic accuracy, observer bias, and staging poten-
tial in 100 sialograms.
PATIENTS AND METHODS
Patients
To study the clinical value of sialography for diag-
nosing SS, 100 parotid sialograms were interpreted
independently by 4 observers. Two observers had much
general experience in judging sialograms, whereas 2
observers were especially experienced in the judging of
sialograms with respect to the diagnosis of SS. The
observers with general experience were termed trained
observers, and the observers with specic SS expertise
were termed expert observers. Sialograms were derived
from a group of 100 consecutive patients referred to the
outpatient clinic of the Department of Oral and Maxil-
lofacial Surgery of the University Hospital Groningen
during the period from December 1997 until August
1999.
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, and
fatigue. The diagnostic workup for SS, carried out in all
patients, included the following aspects: subjective
complaints of oral and ocular dryness, sialometry and
sialochemistry, 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 to
avoid an incorporation bias. In addition to the diagnos-
tic tests, the duration of oral symptoms and the serum
immunoglobulin G levels were recorded to assess the
relation between the clinical and sialographic stage of
SS. Duration of oral symptoms was dened as the time
from rst complaints induced by or related to oral
dryness until referral.
In this study the revised European classication cri-
teria for SS were used as reference standard for the
diagnosis of SS, categorizing patients as primary SS,
secondary SS, or non-SS patients.
21,22
Exclusion criteria
The exclusion criteria of the European classication
for SS were applied. In addition, patients with iodine
allergy were excluded from the study, because iodine
was present in the contrast uid used. Psoriatic arthritis
and human immunodeciency virus infection were ex-
cluded because both diseases may cause sialographic
presentations resembling SS.
23-26
No patients had to be
excluded from the study.
Technical procedure for sialography
All sialograms were obtained in the absence of acute
sialadenitis. If present, sialography was postponed until
clinical signs of inammation had subsided for at least
6 weeks. Parotid sialograms were obtained preferably
of the right gland in a standardized manner by the same
person (W.W.I.K.). After cannulation of the main duct,
an oil-based contrast uid (Lipiodol UF, Biotek Ltd,
Auckland, New Zealand) was injected slowly with a
2-mL Cornwall syringe (Becton and Dickinson, Frank-
lin Lakes, NJ), until the patient reported a sudden
increase of preauricular pressure. Premature leakage of
contrast uid was prevented by ligating the main duct
under local anesthesia. A General Electric G1000 and a
Siemens Orthopos (Sirona USA, Charlotte, NC) were
used as x-ray apparatus for lateral and posteroanterior
views, respectively. Posteroanterior (6 degrees medio-
lateral, focus-lm distance 1.10 m) views were made
with an additional lter (2.73 mm aluminum) with 64.5
kV/6.3 mA, and lateral (contact) views were made with
an additional lter (4.63 mm aluminum) with 58 kV/15
mA during 0.18 second. A Kodak (Rochester, NY)
T-MHT G/RA 18 24 lm was used in a Kodak Lanex
cassette with medium intensifying screen. After re-
moval of the ligature and massaging the gland, patients
were advised to stimulate salivary gland secretion with
citric avored gum or candy during the rst hours to
enhance washout of the remaining contrast uid. The
whole procedure was completed within 15 minutes.
Evaluation of the sialograms
Four observers examined independently 100 sialo-
grams in a random order by using a variable intensity
view box with ambient light dimmed. They were in-
formed that the patients had been referred as suspected
of SS and about the amount of contrast uid injected.
Twenty-ve of the 100 sialograms were viewed a sec-
ond time by all observers without being aware of it to
determine intraobserver variability. All sialograms
were examined in the presence of an independent in-
vestigator who made sure that each set of sialograms
was examined within 2 minutes.
Before the observers examined the sialograms, a
calibration session took place in which all observers
agreed on the criteria to be applied. Four different
pathologic patterns were agreed on (the observers had
to determine whether these patterns were present in
132 Kalk et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
July 2002
each sialogram). These patterns were sialectasia (sub-
divided into punctate, globular, cavitary, and destruc-
tive), thin appearance of the ducts with or without gland
enlargement, irregular and widened main ducts, and
presence of a space-occupying lesion, respectively.
If present, sialectasia (dilatations) were graded ac-
cording to the classication of Blatt
13
: punctate if less
than 1 mm in size, globular if uniform and 1 to 2 mm
in size, and cavitary if irregular and more than 2 mm in
size (Fig 1). A destructive pattern was dened as com-
plete destruction of the gland architecture, simulating
an 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 or
sialoadenosis.
27,28
Irregular and widened main ducts
consistent with sialodochitis (salivary duct inamma-
tion) were considered to be the prevalent feature in
chronic recurrent sialadenitis.
29,30
A space-occupying
lesion on a sialogram was considered to be suggestive
of a tumor compressing the gland.
A consensus judgment of whether a sialogram was in
accordance with the diagnosis of SS was based on the
majority opinion of the observers.
Statistical analysis
Data 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 of
interobserver and intraobserver agreement (observer bi-
as)
31,32
and Pearson and Spearman coefcients as cor-
relation tests. In the results section it is stated which
statistical test was applied in a specic situation. A P
value of less than .05 was considered signicant.
RESULTS
Study group
By applying the revised European criteria for SS
22
on the cohort studied, 39 patients were categorized as
SS (20 primary and 19 secondary SS; male to female
ratio, 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 no
alternative disease directly related to salivary gland
Table I. Sensitivity, specicity, positive predictive
value (PPV), negative predictive value (NPV), and
likelihood ratio (LR) of the 4 observers (expert:A,B;
trained:C,D) for the diagnosis of SS in a group of 100
patients by presence of sialectasia on the sialogram
N 100 A B C D Consensus
Sensitivity 87.2 82.1 94.9 92.3 92.3
Specicity 70.5 83.6 32.8 23.3 70.5
PPV 65.4 76.2 47.4 43.4 66.7
NPV 89.6 87.9 90.9 82.4 93.5
LR 3.0 5.0 1.4 1.2 3.1
Consensus judgment was based on the majority of individual judgments for
each sialogram. Note the large differences between expert and trained
observers regarding specicity 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 shape
and more than 2 mm in size; destructive sialectasia, complete loss of gland architecture (not shown).
Kalk et al 133 ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
Volume 94, Number 1
pathology (n 14). Mean duration of oral symptoms
before referral was 35 months for SS and 30 months for
non-SS patients (range, SS 0 to 180 months, non-SS 0
to 240 months).
Test accuracy for SS
The sensitivity and specicity differed greatly be-
tween the trained and expert observers. Trained observ-
ers reached a sensitivity of 95 and a specicity of 33%,
whereas with expert observers it was 87 and 84%,
respectively (Table I). The large difference in specic-
ity was mainly due to differences in deciding between
no abnormality and punctate sialectasia. Expert observ-
ers chose no abnormality in cases of doubt (observers A
and B, Table I), whereas trained observers chose punc-
tate sialectasia in the same situations (observers C and
D). Examples of sialograms that gave rise to doubt are
illustrated in Figs 2 and 3. Consequently, the likelihood
ratios also greatly differed between trained and expert
observers, varying from 1.2 (not very useful as a test) to
5.0 (very useful as a test). Consensus judgment on the
basis of the majority opinion had an intermediate sen-
sitivity and specicity for SS of 92 and 71%, respec-
tively, and a likelihood ratio of 3.1. Sialectasia was
present in 18 of the 61 non-SS patients (Table II).
Observer agreement
Interobserver and intraobserver agreement was cal-
culated for the 4 pathologic conditions. With regard to
the presence of SS (sialectasia as indicator), there was
only fair interobserver agreement between trained and
expert observers, whereas both expert observers
showed good agreement with one another. The intraob-
server agreement was good to very good (Tables III and
IV). Regarding the diagnosis of other salivary gland
disorders, the interobserver agreement varied from poor
to moderate (data not shown).
Staging of SS
The 4 different gradations of sialectasia (Fig 1)
showed a weak but signicant correlation with the
duration of oral symptoms in SS patients (r
Pearson
, 0.29;
P .05). According to consensus judgment of the
sialograms, the observation of punctate sialectasia cor-
responded with an average duration of oral symptoms
of 15 months, whereas globular, cavitary, and destruc-
tive sialectasia corresponded with increasing duration
of 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 sialectasia
on both projections. All observers judged this sialogram as positive for SS (sialectasia present).
134 Kalk et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
July 2002
Ductal changes
The presence of widened or irregular main ducts,
consistent with sialodochitis, was not diagnostic for SS
(sensitivity 28%, specicity 62%, likelihood ratio 0.7)
and was related neither to salivary ow rates nor to
duration of oral complaints. The observation of thin
ducts with or without salivary gland enlargement, re-
garded as possibly consistent with sialoadenosis or
sodium retention dysfunction syndrome, did not relate
to any changes of salivary composition (eg, sodium,
potassium, amylase, total protein) or to salivary ow
rate.
DISCUSSION
We have shown that it is possible to achieve both
sensitive and specic test results with parotid contrast
sialography for diagnosing SS (likelihood ratio up to
5.0). This diagnostic accuracy, however, is very much
dependent 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 consensus
N 100
Sialectasia
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 43
Punctate 13 5 15 1 11 24 12 36 14 5
Globular 11 6 10 3 4 5 15 5 11 7
Cavitary 4 3 3 0 15 8 7 5 5 5
Destructive 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 each
sialogram. Note the large variability between expert and trained observers regarding false positivity, the trained observers judged many sialograms from non-SS
patients 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 small
radiodensities on both projections that could be easily misinterpreted as initial sialectasia. Both trained observers judged this
sialogram as positive for SS (sialectasia present), whereas expert observers judged it as negative for SS.
Kalk et al 135 ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
Volume 94, Number 1
the technique lacks general applicability and requires
specic expertise.
The 4 different grades of sialectasia showed a weak
but signicant relation to the duration of oral symptoms
in SS patients, suggesting that sialectasia slowly wors-
ens as the disease progresses. Previous studies have
already shown that, in SS patients, increasing grada-
tions of sialectasia correspond with lower salivary ow
rates,
3,14,33
as well as that salivary ow rates deteriorate
with increasing duration of oral symptoms.
34
We there-
fore suggest that SS can be subdivided into different
sequential stages according to the type of sialectasia on
the sialogram, with a corresponding degree of hyposali-
vation.
Although the use of oil-based contrast uid has often
been associated in the literature with high rates of
complications, we have experienced none of the com-
plications associated with oil-based contrast uids dur-
ing or after the 100 sialograms performed. The use of
oil-based contrast uid in our hands results in superior
image quality. In case of iodine allergy, sialography
should not be performed to prevent local and systemic
allergic reactions. Alternative positive contrast materi-
als other than iodine that are currently in use are not
suitable for sialography. Therefore, in cases of iodine
allergy other imaging techniques such as scintigraphy
or ultrasonography should be used instead to visualize
salivary gland involvement in SS. Regarding the use of
CT and MRI techniques in diagnosing SS, conicting
results have been reported in the literature.
4,5,8
Although some studies have reported abnormal pa-
rotid sialographic ndings as a fairly common nding
in control subjects (up to 40%),
8,35,36
sialography is
generally considered to be a very specic diagnostic
test for SS.
18-20
However, sialectasia may also occur as
a result of chronic recurrent parotitis, a condition un-
related to SS. The latter may perhaps account for at
least some of the sialectasia we observed in 30% of the
non-SS patients. Furthermore, some of the observed
sialectasia in non-SS patients probably has to be attrib-
uted to observer error, because the number of false
positive cases varied markedly between trained and
expert observers. The observers decision, especially
when in doubt about recognizing initial sialectasia at
the beginning of SS, reects crucially on the test spec-
icity, ie, the number of false positive cases (Tables I
and 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 the
image.
Because diagnostic testing for SS is performed in the
secondary health care, there is an increased prior
chance for SS compared with the general population.
Furthermore, the diagnosis of SS is based on several
diagnostic tests. Both the increased prior chance for SS
and the combined test approach require diagnostic tests
with emphasis on specicity. For this reason it is rec-
ommended that one chooses negatively when in doubt
about the presence of sialectasia on a sialogram (as
illustrated in Figs 2 and 3), thereby increasing the
specicity of the test result. The diagnostic accuracy of
sialography might be further improved with subtraction
radiography.
10,19
Such enhancement of image quality
might not only reduce the number of false positive test
results but also signicantly improve interobserver
agreement. Disadvantages of this procedure are its sen-
sitivity to patient movement (swallowing, tongue
movement) during contrast injection and the need for
sophisticated x-ray equipment.
In conclusion, reading and interpreting a sialogram
require certain expertise with regard to the recognition
and correct interpretation of rst stage sialectasia, re-
stricting its use as a diagnostic tool for incipient SS to
expert observers. In cases of doubt, one should there-
fore consider sending the digitized sialogram to an
expert center. Despite limited general applicability, sia-
lography still has its unique value in the evaluation of
SS. Its costs are low and, if interpreted properly, it is
highly diagnostic. Furthermore, it has a relatively low
degree of invasiveness, and it is a relatively simple and
quick 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 sialogram
N 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 value
below 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 good
agreement (according to Landis & Koch
32
). Note there is fair agreement
between trained and expert observers, moderate agreement between both
trained observers, and good agreement between both expert observers.
Table IV. Intraobserver agreement for the 4 observers
(A-D) with regard to repeated judgment of presence
and type of sialectasia in 25 sialograms, expressed by
Cohens kappa
N 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 PATHOLOGY
July 2002
of sialectasia renders sialography an especially valuable
tool 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 Hospital
Groningen) are gratefully acknowledged.
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Reprint requests:
W. W. I. Kalk, MD, DDS, PhD
Department of Oral and Maxillofacial Surgery
University Hospital Groningen
Hanzeplein 1
9713 GZ Groningen
The Netherlands
w.w.i.kalk@kchir.azg.nl
Kalk et al 137 ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
Volume 94, Number 1