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The Clinical Utility of the Lupus Band Test.

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382
THE CLINICAL UTILITY OF THE
LUPUS BAND TEST
C . DOUGLAS SMITH, CATHY MARINO. and NAOMI F. ROTHI-JELD
In order to determine the clinical utility of the
lupus band test, the presence of dermal-epidermal
junction (DEJ) deposits of IgG, IgM, IgA, C3, C4, Clq,
and properdin were studied in biopsies of clinically
normal deltoid area skin from 102 patients with systemic
lupus erythematosus (SIX)and 151 patients with other
rheumatic diseases. One or more proteins were detected
at the DEJ in 72.6% (74 of 102) of patients with SLE and
in 36.4% (55 of 151) of the other patients, yielding a
specificity of 64% and a predictive value of 57%. The
predictive value for the diagnosis of SLE was greatest
with C4 (loo%), properdin (91.3%), and IgA (86.2%)
and lowest with IgM (5970). Specificity and predictive
value increased with the number of proteins detected at
the DEJ. The results suggest that more rigid criteria are
required before diagnostic significance is attached to a
positive result on the lupus band test.
~
From the Department of .Medicine. Division of Rheumatic
Diseases. l!niversity of Connecticut School of Medicine, Farmington.
Supported in part by grants from the National Institutes of
Health (NIAMDI)) (Multipurpose Arthritis Center Grant AM20621),
an Arthritis Research Center grant from thc Arthritis Foundation.
the Connecticut Chapter of the Arthritis Foundation. and a grant
from the I ~ ~ p Foundation
us
of America. Connccticut Chapter. Dr.
Smith is a Fellow of the Canadian Arthritis Society.
C. Douglas Smith, MI): Fcllow. Division of Rheumatic
Diseases (currently Assistant Professor of Medicine, University of
Ottowa, Ottowa General Hospital, Department of Khcumatology.
Ottowa. Ontario. Canada): Cathy Marino. RS: Research Assistant
111. Division of Rheumatic Diseases: Naomi F. Kothfield, .MD:
Professor of Medicine and Chief. Division of Rheumatic Diseases.
Address reprint requests to Dr. N . Rothfield. Division of
Rheumatic Diseases, University of Connecticut School of Medicine.
Farmington, C T 06032.
Submitted for publication August 29, 1983; accepted in
revised form November 10. 1983.
Arthritis and Rheumatism, Vol. 27, So. 4 (April 1984)
Deposition of immunoglobulin at thc dcrmalcpidermal junction (DEJ) of lcsional skin from patients
with systemic lupus erythematosus (SLE) was first
dcmonstrated in 1963 by Burnham et a1 ( I ) . In 1964.
Cormanc cxtended this observation by showing similar deposition in clinically normal skin of SIZEpatients
( 2 ) . Many rcports h a w appeared in the literature on
the prcscnce of immunoglobulins and complcmcnt
protcins in the DEJ of paticnts with SLE. and somc
investigators h a w suggcstcd that the presence o f
protcins may be useful in asscssing prognosis and
disease activity (3-7).
Although thc lupus band tcst (LBT) is uscd
primarily as an aid in thc diagnosis of SLE, thc
literaturc is unclear regarding the specificity and predictive value of this tcst. Many authors considcr it to
be highly spccific for SIaE (8-16), while others have
suggestcd that the tcst is nonspecific (17-19).
In ordcr to dctcrminc the clinical utility of thc
LBT in the differential diagnosis of SLE, we rcvicwcd
our results from 151 patients with rheumatic diseases
that might bc considered in the differential diagnosis of
SLE. and comparcd thcm with the results from 102
patients with known SI,E. Our findings suggcst that
when the LBT is uscd in the diffcrcntial diagnosis of
SLE, consideration needs to be given to the number of
proteins found and to the specific protcin(s) dctcctcd
at thc DEJ, in ordcr to intcrprct thc significancc of a
positivc finding on the lupus band tcst.
PATIENTS AND METHODS
Patients. All patients were followed in the Division of
Kheumatic Diseases of the University of Connecticut Health
Center at the time of the study. Thc patient group consisted
of 102 patients with systemic lupus erythematosus fulfilling
383
LUPUS BAND TEST
the American Rheumatism Association (AKA) preliminary
criteria for the classification of SLE (20): 48 patients with
rheumatoid arthritis (RA) fulfilling the ARA criteria for
definite or classic disease (21); 21 patients with progressive
systemic sclerosis (PSS) fulfilling the ARA preliminary criteria for the classification of systemic sclerosis (22) (all with
scleroderma proximal to the metacarpophalangeal joints); 8
patients with the CREST syndrome (calcinosis, Raynaud’s
phenomenon, esophageal dysmotility , sclerodactyly, and
telangiectasiae) based on the presence of Raynaud’s phenomenon as well as at least 2 of the other components of the
syndrome and the absence of scleroderma proximal to the
metacarpophalangeal joints; 17 patients with undifferentiated connective tissue disease (UCTD) who did not meet the
criteria for SLE, RA, PSS, or CREST and who had Raynaud’s phenomenon as well as other clinical evidence of
connective tissue disease (synovitis in 6 patients, telangiectasiae in 4 patients, alopecia in 1 patient, puffy hands in 6
patients, pleurisy in 1 patient, and photosensitive rash in I
patient); 32 patients with Raynaud’s phenomenon which was
triphasic (16 patients), biphasic (13 patients), or monophasic-white (3 patients) without any clinical evidence of a
connective tissue disease as defined above; 9 patients with
dermato/polymyositis (6 dermatomyositis and 3 polymyositis) fulfilling the criteria of Bohan and Peter for probable or
definite disease (23); 16 patients with primary Sjogren’s
syndrome defined as the presence of at least 2 of the 3
clinical features of the sicca complex-xerophthalmia, xerostomia, or salivary gland enlargement-and failure to fulfill
criteria for the diseases described above.
Skin biopsies and immunofluorescence. Punch biopsies (3-5 mm diameter) were obtained from clinically normal
deltoid area skin, snap-frozen in isopentane and dry ice,
transferred to Cryoform (Ames Co., Elkhart, IN), sectioned
at 4~ thickness within 72 hours, and stored at -70°C until
used. Immunofluorescence studies were performed as previously described (24). Antisera to IgG, IgM, IgA, C3, C4, and
Clq conjugated with fluorescein isothiocyanate were obtained from Meloy Laboratories, Inc. (Springfield, VA).
Slides were viewed on an Ortholux I1 microscope (E. Leitz,
Inc., Rockleigh, NJ) equipped with a Ploem vertical illuminator and epi-illumination and filters for ultraviolet ex -itation. The sensitivity and specificity of the above antisera
have been previously described (25). Properdin was detected
using indirect immunofluorescence as previously described
(24). The lupus band test was considered positive if either
granular and continuous, or granular or discontinuous deposits were noted in the DEJ.
Serologic methods. Antinuclear antibodies were detected using indirect immunofluorescence with mouse liver
substrate as previously described (26). Anticentromere antibodies were detected using a commercially available human
epithelial cell line (HEp-2, Antibodies Inc., Davis, CA).
Anti-DNA antibodies were detected using native DNA and a
modified Farr technique as previously described (27).
SLE clinical activity. SLE clinical activity was graded
from 0 to 3+ based on signs and symptoms as previously
described (28).
Statistical analysis. Sensitivity, specificity, predictive
value, and efficiency for the diagnosis of SLE were detcrmined using standard methods (29). These are summarized
as follows:
Sensitivity (%)
=
True-positives
x 100
True-positives + False-negatives
Specificity (%)
=
True-negatives
x 100
True-negatives + False-positives
Predictive value
True-positives
x I00
= True-positives + False-positives
+
test (%)
Predictive value
-
(%)
Efficiency (%)
Table 1. Frequency of positive lupus band test (LBT).defined as 1
or more Droteins at the derrnal-eoidermal iunction
Positive LBT
Disease (n)*
SLE (102)
Total non-SLE (151)
RA (48)
PSS (21)
CREST (8)
Raynaud’s (32)
UCTD (17)
DM/PM (9)
Sjogren‘s ( 16)
n
%
74
55
17
9
72.6
36.4
35.4
42.9
12.5
34.4
41.2
44.4
37.5
1
II
7
4
6
* SLE = systemic lupus erythernatosus;RA = rheumatoid arthritis:
PSS = progressive systemic sclerosis: CREST = calcinosis. Raynaud’s phenomenon, esophageal dysmotility, sclerodactyly, and
telangiectasiae; UCTD = undifferentiated connective tissue disease;
DMlPM
=
derrnatoipolymyositis.
-
=
True-negatives
x 100
True-negatives + False-negatives
True-positives + True-negatives
x 100
All tested
Correlations of various clinical and serologic features were
determined using chi-square analysis and the 2-tailed Fisher’s exact test where indicated.
RESULTS
Incidence of positive biopsies in each disease
group (Table 1). The number of patients in each
disease group having a positive test result (defined as
the presence of at least 1 protein at the DEJ) is shown
in Table 1. A positive test was found in 72.6% of
patients with SLE. A positive test was not uncommon
in the other diseases, occurring in 36.4% of patients in
the overall non-SLE group and varying from 12.5% in
patients with CREST to 44.4% of patients with dcrmato/polymyositis.
SMITH ET AL
384
Table 2. Number of proteins at the dermal-cpiderrnal junction
(DEJ) by disease group
positive test showed a significant increase with increasing disease activity (chi-square 3 df = 15.73, P =
0.00 13).
Of the 48 patients with rheumatoid arthritis, 31
had erosive disease, 13 had nodules, and 37 had 1 or
more swollen joints. No correlation was found between a positive test and any of the following indicators of disease activity: duration of morning stiffness
greater than 30 minutes, presence or absence of swollen joints, or increased erythrocyte sedimentation
rate. There was also no correlation between a positive
test and disease duration or the presence of erosions,
nodules, rheumatoid factor, or antinuclear antibodies.
In all of the other diseases studied, there was a
similar lack of correlation between a positive test and
disease duration or presence or titer of rheumatoid
factor or antinuclear antibodies. In the patients with
PSS and CREST, there was no correlation between a
positive test and the presence of anticentromere antibodies. In the patients with dermato/polymyositis,
there was no correlation between a positive test and
elevation of creatine phosphokinase (>180 unitdliter).
Relationship between individual DEJ proteins
and disease. The number of patients having each
protein at the DEJ, by disease group, is shown in
Table 3. C4 was found only in patients with SLE. IgA
and properdin were uncommon in diseases other than
SLE. Each protein was present significantly more
often in the 102 patients with SLE than in the 151
patients with other diseases (chi-squares for each
protein varied and ranged from 20.72 [IgM] to 56.1
[C3], P < 0.00005). I n patients with rheumatoid arthritis, the presence of IgM at the DEJ did not correlate
with the presence of rheumatoid factor.
Utility of the number of DEJ proteins for diagnosis of SLE. The sensitivity, specificity, predictive
value, and efficiency for increasing numbers of DEJ
No. of proteins at DEJ
Disease (n)*
SLE (102)
Non-SLE (151)
RA (48)
PSS (21)
CREST (8)
Raynaud’s (32)
UCTD (17)
DM/PM (9)
Sioeren’s (16)
0
1
28
14
9 6 2 5 2
3
1
6
1 2 6
7
I
21
6
1 0 3
5
3
1
0
0
2
3
12
1
1
I
0
4
2
0
4
12
8
0
2
4
0
I
2
1
1
5
6
8
I1
13
0
I
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
I
0
7
4
0
0
0
0
0
0
0
0
* See Table 1 for definitions.
Number of DEJ proteins in each disease group.
The number of proteins found at the DEJ in each
disease group is shown in Table 2. Four or more DEJ
proteins were found only in SLE patients, with a single
exception. This was a patient with Sjogren’s syndrome, followed for 4 years, with high titer rheumatoid
factor and antinuclear antibodies. She never had antiDNA antibodies or a low level of C3 complement.
However, she was the only non-SLE patient with
antibodies to Sm and has intermittently had a low level
of C4 complement.
Correlations between number of DEJ proteins
and clinical and serologic parameters. Of the 102 SLE
patients, clinical activity was graded as 0 (inactive) in
22, I + active in 34, 2+ active in 34, and 3+ active in
12. A positive test (1 or more proteins) was obtained in
11 of the 22 clinically inactive patients, 21 of the 34
patients with I + disease activity, 31 of the 34 patients
with 2+ disease activity, and in 1 1 of the 12 patients
with 3 + activity. A positive test was significantly more
common in patients with clinically active disease (chisquare 5.791, P = 0.0161), and the incidence of a
Table 3.
Specific proteins present at the derrnal--epidermal junction by disease group
No. (%) positive
c3
Disease (n)*
SLE (102)
Non-SLE (151)
RA (48)
PSS (21)
CREST (8)
Raynaud’s (32)
UCTD (17)
DM/PM (9)
Sjogren’s (16)
* See Table 1 for definitions.
56 ( 5 5 )
39 (26)
13 (27)
7 (33)
0
9 (28)
4 (24)
2 (22)
4 (25)
25 (25)
4 (3)
I (2)
0
c4
CIQ
17 (17)
0
0
0
45 (44)
17 (11)
4 (8)
3 (14)
l(13)
3 (9)
2 (12)
2 (22)
2 (13)
0
0
0
0
0
0
0
1 (6)
0
2 (13)
Properdin
21 (21)
?(I)
0
I (5)
0
1 (3)
0
0
0
385
LUPUS BAND TEST
Table 4. Utility of the number of proteins found at the dermalepidermal junction for the differential diagnosis of systemic lupus
erythernatosus
No. of proteins
Sensitivity (9%)
Specificity
Predictive value
Predictive value
Efficiency (%)
+ test (9%)
-
test (%)
I or
more
2 or
more
3 or
more
4 or
more
72.6
63.6
57.4
77.4
67.2
58.8
80.1
66.6
74.2
71.5
47.1
94.0
84.2
72.5
75.1
35.3
99.3
97.3
69.4
73.5
proteins are shown in Table 4. The presence of I or
more proteins had a sensitivity of 72.6%. However,
the specificity was only 63.6% and the predictive value
(positive test) 57.4%. The predictive value of a positive test increased with the number of proteins present
in the DEJ, reaching 97.3% with 4 or more proteins.
The efficiency was maximal at 75.1% with 3 or more
DEJ proteins.
Utility of the individual proteins at the DEJ for
diagnosis of SLE. The sensitivity, specificity, predictive value, and efficiency of the individual proteins are
shown in Table 5. Specificity and predictive value
were highest for C4 (loo%), properdin (99% and 91%,
respectively), and IgA (97% and 86%, respectively)
and lowest for IgM (74% and 5996, respectively).
Efficiency was greatest with C3 (75.1%), C l q (70.8%).
and IgG (70%) and lowest with IgM and C4 (both
66.4%).
DISCUSSION
Although the lupus band test is generally considered to be highly specific for the diagnosis of SLE
(8-16), the literature supporting this conclusion is
conflicting. Interpretation of some of the studies is
made difficult because of variability in the site of
biopsy, the number of proteins tested, and the relative-
ly small number of patients tested with diseases other
than SLE. In general, IgM has been the most common
immunoglobulin found at the DEJ, particularly in
diseases other than SLE. DEJ deposits have been
found in 0-35% of normal individuals (17-19). They
have been found in 0-50% of rheumatoid arthritis
patients (16,17,30-35) and in about 50% of patients
with mixed connective tissue disease (36). In the few
patients studied with either progressive systemic sclerosis (37) or dermato/polymyositis (38,39), results
have generally been negative.
In an attempt to clarify the clinical utility of the
lupus band test, we studied results of biopsies from
clinically normal deltoid area skin of 102 patients with
SLE and compared them with results from 151 patients with diseases which might be considered in the
differential diagnosis of SLE. A positive lupus band
test (defined as the presence of I or more proteins at
the DEJ) was found in 72.6% of patients with SLE and
36.4% of patients with other diseases. In both groups
IgM was the single most common protein found. Of
the individual proteins, specificity and predictive value (positive test) were greatest for C4, properdin, and
IgA, although these proteins were also the least sensitive. The predictive value of finding IgM at the DEJ
was only 59%. The finding of I or more proteins at the
DEJ yielded a specificity of 63.6% and a predictive
value of only 57.4%. Specificity and predictive value
increased with the number of proteins detected.
The efficiency of a diagnostic test may be the
most useful parameter to consider in diseases such as
SLE in which both false-positives and false-negatives
are considered to be equally important (29). Efficiency
was greatest with C3, C l q , and IgG and lowest with
IgM and C4. Peak efficiency (75.1%) was achieved
when 3 or more proteins were detected at the DEJ.
Variability in the sensitivity and specificity of
the lupus band test reported in this and other studies
may occur for several reasons. The major reason for
Table 5. Utility of individual proteins found at the dermakpidermal junction for the differential
diagnosis of systemic lupus erythematosus
Protein
Sensitivity (%)
Specificity (9%)
Predictive value
Predictive value
Efficiency (%)
+ test (9%)
-
test (96)
IgG
IgM
IgA
C3
c4
Clq
Properdin
49.0
84.1
67.6
71.0
70.0
54.9
74.2
59.0
70.9
66.4
24.5
97.4
86.2
65.6
68.0
48.0
93.4
83.1
72.7
75.1
16.7
100.0
100.0
64.0
66.4
44.1
88.7
72.6
70.2
70.8
20.6
98.7
91.3
64.8
67.2
SMITH ET AL
386
the relatively low specificity in this study was the
nature of the control group, which consisted of a
relatively large number of patients with other rheumatic diseases rather than healthy individuals or those
with totally unrelated disease. W e believe this was
justified since these are the types of patients in whom
SLE is considered in t h e differential diagnosis. Another factor which may have had a bearing on t h e
specificity is the site of t h e biopsy. Our biopsies were
taken from clinically normal deltoid area skin. Using
this site, the sensitivity was 72.6%. In patients with
SLE, it is known that the sensitivity of the lupus band
test is increased by using sun-exposed skin as t h e
biopsy site (40). It may b e that this increased sensitivity occurs at the cost of specificity, although studies of
simultaneous biopsies of sun-exposed and sun-protecte d skin in diseases other than SLE are not available.
T h e prevalence o f a disease in the population i s
a very important factor affecting the usefulness of a
test result (29,41). In t h e present study the prevalence
of SLE was 40.3%. If sensitivity a n d specificity are
held constant, predictive value decreases as the prevalence falls. Therefore, while the predictive value of
finding 1 or more proteins at the DEJ in our study was
57.4%, t h e same finding in general populations in
which the prevalence of SLE has been estimated a t
0.4% (42), 1.2% (43), or 10% (43) would yield predictive values of 0.3%, 2.4%, a n d 18.5%, respectively.
In conclusion, we believe more rigorous criteria
are required before diagnostic significance is attached
t o a positive result on t h e lupus band test. T h e nature
of the protein as well as t h e number of proteins found
at the dermal-epidermal junction are important determinants of specificity and predictive value. Finding a
single protein at the DEJ, especially if the protein is
IgM, is of little or no diagnostic value. Based o n our
findings it would appear that this test is of limited
value in establishing a diagnosis of SLE.
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