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Prognostic factors in polymyositisdermatomyositis. A computer-assisted analysis of ninety-two cases

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PROGNOSTIC FACTORS IN
POLYMYOSITIS/DERMATOMYOSITIS
A Computer-Assisted Analysis of Ninety-Two Cases
JOCHANAN BENBASSAT, DOV GEFEL, KEREN LARHOLT, SHAUL SUKENIK,
VLADIMIR MORGENSTERN, and AVlNOAM ZLOTNlCK
An effort was made to identify all patients with
polymyositis/dermatomyositis (PM/DM) admitted to
hospitals in Israel from 1956-1976. The diagnosis of
PM/DM was retrospectively reviewed in 92 (46 definite,
26 probable, and 20 possible) cases. The most common
complaints and physical findings in the course of the
disease were muscle weakness (86 patients), rash (53
patients), arthritis or arthralgia (39 patients), and dysphagia (35 patients). Elevated serum aldolase levels
were found in 64% of the patients for whom data were
available; 92% had abnormal electromyogram results,
and 60.9% had muscle histopathology consistent with
PM/DM. Malignancy was diagnosed in 13 patients.
Malignancy, ischemic heart disease, and pulmonary
complications were the most common causes of death.
The actuarial survival curve was heterogeneous, with an
accelerated mortality during the first year after diagnosis and a slower mortality during the following 7 years.
Independent unfavorable prognostic signs were: failure
to induce remission, leukocytosis, fever, older age, a
shorter disease history, and dysphagia.
___~__
From the Department of Medicine and the Medical Computing Unit, Hadassah University Hospital, Jerusalem: and the
Department of Medicine and Medical Computing Unit, Soroka
Medical Center, Beer Sheva, Israel.
Jochanan Benbassat, MD: Department of Medicine, Hadassah University Hospital; Dov Gefel, MD: Department of Medicine,
Hadassah University Hospital; Keren Larholt, BA: Medical Computing Unit, Soroka Medical Center: S h a d Sukenik, MD: Department of Medicine, Soroka Medical Center; Vladimir Morgenstern:
Medical Computing Unit, Hadassah University Hospital; Avinoam
Zlotnick, MSc, MD: Department of Medicine, Hadassah University
Hospital.
Address reprint requests to J. Benbassat, MD, Department
of Medicine, Hadassah University Hospital, Mt. Scopus, PO Box
24035, Jerusalem, 91240, Israel.
Submitted for publication August 29, 1983; accepted in
revised form September 7, 1984.
Arthritis and Rheumatism, Vol. 28, No. 3 (March 1985)
There are several studies of survival in polymyositis/dermatomyositis (PM/DM) (1-5). Mortality in
this disorder has been reported to be between 13.7%
(6) and 50% (7) within an unspecified length of followup period. Associated autoimmune disease (433) and
malignancy (4,6,8), the length and severity of the
illness ( 5 , 8 ) , age (2,4), and childhood onset of polymyositis (9) have been reported to be predictive of a
reduced length of survival. On the other hand, Bohan
et a1 (6) reported favorable survival statistics for all
groups of patients with PM/DM, with the exception of
those with associated malignancy, and there were no
deaths among the patients with childhood DM reported by Sullivan et a1 (10).
The differences in the reported mortality in PM/
DM, and the conflicting conclusions on the prognostic
significance of the various manifestations of the disease could be because of limited interpretation of
followup data. We know of only one study (3) of the
actuarial survival of patients with PM/DM. This report
is a retrospective computer-assisted analysis of all the
hospital records we were able to collect, between 1956
and 1976, of PMlDM patients in Israel. An attempt is
made to determine the effect of the various manifestations of PM/DM on the actuarial survival of the
patients in order to identify factors of possible prognostic significance.
METHODS
The archives of the general hospitals in Israel, all of
which maintain medical research indexing systems, were
searched for patients discharged between 1956 and 1976 with
diagnoses of polymyositis, dermatomyositis, or myositis.
Each chart was evaluated according to the criteria of Bohan
et a1 (6): (a) symmetric muscle weakness; (b) typical histologic
BENBASSAT ET AL
250
findings on muscle biopsy; (c) increased levels of muscle
enzymes in the serum; (d) compatible electromyographic
(EMG) findings; and (e) characteristic dermatologic manifestations. Patients suspected of having muscular dystrophy,
endocrinopathy, alcoholism, muscle infections, or evidence
of a central or peripheral nervous system disease were
excluded from the study.
One hundred sixty charts were reviewed, and 92
cases partially or completely fulfilled the diagnostic criteria.
PMlDM was considered definite in 46 patients who presented at least 4 manifestations, probable in 26 patients with 3,
and possible in 20 patients with 2 of the 5 manifestations.
‘There were 30 known deaths with 16 autopsies. Classification by diagnostic category (group I: primary idiopathic
polymyositis [PM]; group 11: primary idiopathic dermatomyositis [DM]; group 111: polymyositis with malignancy
IPM/DM-Mall; group IV: polymyositis of childhood onset
IPM/DM-Child]; group V: overlap syndromes [PM/DMOsl) was according to the criteria of Bohan et al (6).
PMBM-Child was defined as PMlDM in a subject age 18 or
less.
The available clinical, laboratory, and followup data
were compiled according to a predesignated format, and a
digital computer was used for their analysis. Followup
information was limited to that found in the patients’ hospital
and outpatient department records. In December 1980, information on additional deaths was obtained from the Ministry
for Internal Affairs, which keeps a central registry of vital
records. The large number of attending physicians and the
heterogeneity of the clinical departments involved precluded
standardization of the assessment of muscle strength and
dysphagia. Therefore, muscle weakness and dysphagia were
assumed to have been present whenever recorded as such in
the patients’ charts. Remission was defined as an increase in
muscle strength, or 2 or more of the following: disappearance of skin rash, normalization of muscle enzyme levels in
serum, and normalization in EMG tracings.
Survival functions were processed by the biomedical
computer program P series of the University of California
Press, 1979 (BMDP 79). The Berkson and Gage (1 1) option
was selected for actuarial survivorship curves. The differences between curves were tested by the analogs of nonparametric rank tests provided by the program, the Breslow
and Mantel-Cox tests (12,L3). Both statistics are asymptotically distributed as chi-square. The Breslow test gives
greater weight to early observations and is less sensitive to
late events which occur when few study patients remain
alive (12,14). Independent risk factors were identified by
stepwise logistic regression using the BMDP-8 I statistical
software of the University of California.
RESULTS
Incidence. Data on the age-adjusted annual incidence rates of PM/DM in Israel derived from the
patients in this series have been presented elsewhere
(15). Briefly, there were 2.18 new cases annually per
1,000,000population. The age distribution was heterogeneous, with modes in the second and seventh de-
cades and with a relatively low incidence among
subjects in their twenties. The male:female ratio
among patients <60 years old was 0.14-0.57, while
that among patients 2-60 was 1.10-1 S O . DeVere and
Bradley (4) have also found the female preponderance
to be restricted to patients aged 55 or less.
Clinical features. Patients with childhood polymyositis comprised 21.7% of our series. Another
31.5% were classified as having primary idiopathic
dermatomyositis, and 19.6% had primary idiopathic
polymyositis. The remaining patients had overlap syndromes (13.0%) and polymyositis with malignancy
(14.1%). The time interval from first manifestation of
the disease to diagnosis was 1 year or less in 69
patients, the average for the whole series being 13.0
months. Patients with PM/DM-Mal, PM/DM-Child,
and PM/DM-0s presented with nonsignificantly
shorter disease histories than did those with PM or DM.
Skin rash was the most common presenting
complaint in DM and PM/DM-Mal, muscle weakness
in PM and PM/DM-Child, and arthralgia in PM/DM0 s . The most common complaints throughout the
duration of the disease were muscle weakness
(93.5%), muscle pain (46.7%), rash (57.6%), and arthralgia (42.4%). By definition, skin rash characterized
DM and was never present in PM. It was observed in
76.9% of the patients with PM/DM-Mal, in half of
those with PM/DM-Child, and in one-third of the
patients with PM/DM-0s. Dysphagia was reported by
38.0% of the patients and it was nonsignificantly more
common in PM/DM-Ma1 and PM/DM-Child. Temperature above 38°C was found in 21.7%, while hepatomegaly , splenomegaly , and lymphadenopathy were
found in 31.5, 20.7, and 10.9% of the patients, respectively.
Laboratory findings. The EMG results were
abnormal in 72 (92.3%) of the 78 patients examined.
There were no differences in the frequency of EMG
disturbances among the various diagnostic categories.
Muscle biopsies were interpreted as compatible with
polymyositis in 60.9% of the 80 cases that had available data. Abnormal histologic findings were seen in
85% of the muscle biopsies in PMIDM-Child, but only
in 30.8% of those in PM/DM-Ma1 ( P < 0.05).
Serum aspartate aminotransferase (AST), creatine phosphokinase (CPK), aldolase (ALD), and lactic dehydrogenase (LDH) exceeded twice the upper
level of normal in 39 of 83 (47.0%), 33 of 66 (50.0%, 29 of
45 (64.4%), and 34 of 59 (57.6%) cases with available
data, respectively. The highest incidence of muscle
enzyme abnormalities was observed in PM/DM-Child.
25 1
PROGNOSTIC FACTORS IN POLYMYOSITIS
The levels of AST, CPK, ALD, and LDH correlated
significantly ( P < 0.005) with one another, although
product-moment correlations were generally low
(0.290-0.495).
Rheumatoid factor was found in the sera of 6
patients with PM/DM-0s and in 1 patient with PM.
Rheumatoid arthritis was diagnosed in 6 of the patients
with PM/DM-Os, scleroderma was diagnosed in 4, and
Sjogren's syndrome in 2. Antinuclear antibodies
(ANA) were found in the sera of 23.6% of the 55
patients with available data and were evenly distributed among the various diagnostic categories. In most
cases the ANA titers were not recorded in the patients' charts. White blood cell counts exceeded
1 O , O O O / ~ lin 12 (15.6%) of the 77 patients with available
data. There were no marked abnormalities in red blood
cell counts or in liver functions. Blood urea nitrogen
(BUN) levels exceeded 50 mg/dl in 1 1.9%, and proteinuria was found in 14.5% of the patients.
Cardiac and electrocardiographic abnormalities. Electrocardiogram (EKG) results were available
for 73 patients. EKG abnormalities, including nonspecific ST-T changes, supraventricular arrhythmias, Q
waves, and conduction disorders, were detected at the
time of diagnosis in 23 patients (31.5%). In 1 1 of these
23 patients, the EKG abnormalities could be accounted for by an associated hypertensive (4 patients),
ischemic ( 5 patients), or pulmonary (2 patients) heart
disease. In the 4 patients with hypertensive heart
disease, arterial hypertension preceded the diagnosis
of PM/DM by 2, 3 , 5 , and 10 years. In 5 patients,
ischemic and/or hypertensive heart disease was
thought to be the primary cause of death.
The abnormalities on the EKGs of the remaining 12 patients were paroxysmal atrial tachycardia (3
patients), ST-T changes (6 patients), and conduction
disturbances (3 patients). None of the 16 autopsies
revealed edema, lymphocytic infiltration, necrosis, or
other inflammatory myocardial changes which have
been described in PM/DM (16). However, the amount
of effort invested in the search for such changes in the
patients is unknown.
Pulmonary manifestations. Twelve patients had
lung involvement, and in 8 of these 12, pulmonary
disease was thought to be the primary cause of death.
Interstitial lung disease (17) was diagnosed in 2 patients and was confirmed at autopsy in l . Pulmonary
emboli were the suspected cause of sudden death in 3
patients, and this was confirmed at autopsy in 1 . The
most common pulmonary involvement was pneumonia. It was found at autopsy in 7 patient3 and was the
main cause of death in 4 of them. The extent to which
aspiration contributed to the development of pneumonia was not recorded.
Polymyositis with malignancy. Thirteen patients
(14.1%; 3 with PM, 10 with DM) had malignancies,
including Hodgkin's lymphoma, angiosarcoma, and
carcinoma of the bronchus, stomach, colon, breast,
ovary, and prostate. Malignant tumors were found in 6
(18%) of the 34 male patients in this series and in 7
(12%) of the 58 female patients. The diagnoses of
PM/DM and malignancy were made simultaneously at
Table 1. Recorded primary causes of death in 30 patients with polymyositisidermatomyositis,by
diagnostic category*
~ ~ _ _ _ _ _ _ _
~~
______
PM
(n = 18)
Uncontrolled activity
Pulmonary
Cardiac
Cerebrovascular
Malignancy
Uremia
Not given
All causes
Total mortality in
diagnostic category
DM
(n = 29)
PMIDMMa1
(n = 13)
PMIDMChild
(n = 20)
2
2
2
4
4
1
PMIDM0s
(n = 12)
I
I
5
2
1
2
3
16.6
I
12
41.4
22.5
13.3
I
10
1
76.9
3
15.0
2
16.6
79.2
22.7
26.2
10.7
15.2
44.0
11.5
18.6
Total
(n = 92)
3 (10.0%)
8 (26.7%)
5 (16.7%)
I (3.3%')
5 (16.7%)
3 (10.0%')
5 (16.7%')
30 (1007~)
32.6
(96)
Length of followup
(person years)
Mortality per person
years followup
(X
161.3
18.6
100)
~
* PM
~
polymyositis; DM
overlap syndromes.
=
=
dermatomyositis; Ma1
=
malignancy; Child
=
childhood onset; 0 s
=
252
3
aro
BENBASSAT ET AL
presentation in 8 patients. In 2 patients, the malignant
neoplasm was detected 1 month and 8 months prior to
diagnosis of PM/DM. In the remaining 3 patients, the
diagnosis of PM/DM preceded that of malignancy by 6,
18, and 24 months. The frequency of malignancy
increased with age. Malignant tumors were found in 1
(3%) of the 34 patients aged 40 years or less, 5 (16%) of
the 32 patients aged 41-59, and in 7 (27%) of the 26
patients aged 60 or more.
Survival and factors of possible prognostic significance. Malignancy, ischemic heart disease, and
pulmonary complications were the most common
causes of the 30 known deaths. Three patients died of
uremia and 3 died from uncontrolled activity of
PM/DM (Table 1). Actuarial survival depicted a heterogeneous curve, which revealed an accelerated mortality the first year after diagnosis and a slower mortality over the following 7 years. There were no
1
0.0
0
3
6
9
12
Years
Figure 1. Actuarial survival since diagnosis of 92 patients with
polymyositis/dermatornyositis, by sex. After 6 years followup, only
1 man and 7 women remained in the study.
Table 2. Factors affecting actuarial survival of 92 patients since diagnosis of polymyositisi
dermatomvositis
Cumulative proportion
surviving after (months)
Variable*
Sex
Men (34)
Women (58)
Interval from first manifestation
to diagnosis
<7 months (53)
>7 months (37)
Diagnostic category
PM (18)
DM (29)
PMIDM-Ma1 ( 13)
PMiDM-Child (20)
PM/DM-Os (12)
Age at diagnosis (years)
<20 (23)
2 1-60 (46)
>61 (23)
Temperature ("C)
<38 (72)
>38 (20)
Remission achieved
Yes (57)
No (17)
White blood cells
< 10,000/~1(65)
>10,00O/F1'(12)
Dysphagia
N o (57)
Yes (35)
Rash
Yes (53)
N o (39)
9
36
0.72
0.75
72
P
Breslow test
Mantel-Cox test
0.66
0.61
0.8323
0.8802
0.65
0.88
0.49
0.82
0.0308
0.0082
1.00
0.67
0.62
0.86
0.72
0.56
0.66
0.44
0.75
0.72
0.3362
0.2874
0.88
0.79
0.55
0.78
0.64
0.49
0.0855
0.0304
0.86
0.36
0.74
0.24
0.0006
0.0001
0.85
0.34
0.78
0.26
0.0000
0.0000
0.78
0.39
0.68
-
0.0003
0.0000
0.84
0.60
0.81
0.36
0.0072
0.0066
0.64
0.92
0.54
0.77
0.0341
0.1482
0.50
0.22 '
-
* Figures in parentheses indicate the number of patients with available data. See Table 1 for diagnostic
category abbreviation definitions.
253
PROGNOSTIC FACTORS IN POLYMYOSITIS
Table 3. Stepwise logistic regression analysis of the effect of variables on actuarial survival of 92
patients with polymyositisidermatomyositis diagnosed in Israel between 1956 and 1976
Improvement
Global
Step
no.
Variable
entered
Entered
as
XZ
P
X2
P
1
Clinical remission
Leukocyte count
Temperature
Age
Time since first
manifestation
Dvsuhaeia
Yesino
Number
"C
Years
12.674
9.687
9. I08
9.063
0.000
0.002
0.003
0.003
15.307
30.138
39.754
45.620
0.000
0.000
0.000
0.000
Months
Yesino
3.857
3.117
0.050
0.077
45.942
50.484
0.000
0.000
2
3
4
5
6
differences in length of survival time for male and
female patients (Figure 1).
Patients with PM/DM-Ma1 had a higher mortali t y rate than those in the remaining diagnostic categories (Table 1). The mortality of patients with PM/DMMa1 was 44.0 per 100 person years of followup, but it
was only 11.5-18.6 in the remaining diagnostic categories. There were no significant differences in actuarial
survival among the various diagnostic categories,
probably because of the small numbers of patients
(Table 2).
A shorter disease history, rash, dysphagia, temperature above 3 8 T , older age, leukocyte counts
exceeding 1O,OOO/pl at diagnosis, and failure to induce
a clinical remission were associated with a significantly reduced actuarial survival (Table 2). BUN levels
>30 mg/dl, proteinuria, and elevated serum aldolase
levels were associated with a nonsignificantly shorter
actuarial survival. Stepwise logistic regression revealed that failure to induce a clinical remission,
leukocyte counts of 2 10,0001~1at diagnosis, temperature above 38°C at diagnosis, and older age were
independent risk factors. A shorter disease history and
dysphagia contributed to mortality with borderline
significance (Table 3 ) .
Stepwise logistic regression using entry variables only (i.e., excluding clinical remission) showed
that white blood count, temperature, and age remained
independent significant risk indicators ( P = 0.004,
0.002, and 0.01 I , respectively). Repeated analysis
after excluding 12 patients with pulmonary involvement identified only white blood cell count ( P = 0.001)
and age ( P = 0.005) as independent risk factors.
Temperature contributed to mortality with borderline
significance ( P = 0.07).
Survival was not affected by the presence of
arthritis or arthralgia, abnormal histologic findings on
muscle biopsy, increased levels of 1 or more of the
remaining muscle enzymes, erythrocyte sedimentation
rate, abnormalities revealed in the EMG tracing, hemoglobin level, presence of Raynaud's phenomenon,
antinuclear antibodies in the serum, blood pressure at
diagnosis, abnormalities shown in the EKG, splenomegaly, or degree of certainty in the diagnosis.
DISCUSSION
The presented data should be interpreted with
caution. They are based on a retrospective study of a
relatively small number of patients seen over a long
period of time at a large number of institutions. The
degree of evaluation varied, and evaluations of serum
levels of muscle enzymes, EMG, and biopsies were
missing in many cases; hence the relatively high
proportion of probable and possible cases of PM/DM
in the series. However, our study was unique in
employing a stepwise logistic regression. which combined multivariate analytic techniques and actuarial
Table 4. Mortality in published
poly myositisidermatom yosit is
Reference
O'Leary and Waisman (7)
Sheard (19)
Wedgewood et a1 (9)*
Pearson (20)
Logan et al (2)
Winkelman et a1 (8)
Medsger et al (3)
Sullivan et a1 (lo)*
Riddoch and Morgan-Hughes ( 5 )
DeVere and Bradley (4)
Bohan et a1 (6)
Carpenter et a1 (21)t
Henriksson and Sandstedt (18)
This series
series
Number
of
patients
at risk
40
25
26
48
63
289
124
18
20
118
153
62
107
92
of
patients
with
Surveyed
time
interval
Mortality
93
1925-1938
1927-1947
Not given
Not given
1950-1963
Not given
1947-1968
1960-1969
1960-1970
1954-1974
1956-1971
1947-1971
Not given
1956-1976
50.0
52.0
40.0
25.0
41.1
27.6
35.0
0.0
40.0
27.9
13.7
45.1
23.0
32.0
* Including cases of polymyositis/dermatomyositis of childhood
only.
'IIncluding cases of polymyositis and dermatomyositis only.
BENBASSAT ET AL
254
Table 5. Prognostic factors in published series of patients with polymyositis/dermatomyositis
(PM/DM)*
Reference
Riddoch and Morgan-Hughes
(5 )
Winkelman et al (8)
Logan et al (2)
Number
of cases
20
289
63
DeVere and Bradley (4)
I I8
Medsger et al ( 3 )
124
Bohan et a1 ( 6 )
Carpenter et a1 (21)
Henriksson and Sandstedt
(18)
This series
I53
62
107
92
Unfavorable prognostic
signs
Prolonged disease history,
low serum CPK levels
Raynaud’s phenomenon,
severity of activity,
malignancy,
scleroderma,
pharyngeal and chest
muscle weakness
Older age, “fulminating”
type of PMiDM
Prolonged duration prior
to Rx, overlap syndrome, malignancy,
older age
Older age, degree
of muscle weakness,
dysphagia, pneumonitis
Malignancy, older age,
prolonged duration
prior to Rx
Dysphagia, severe
proximal muscle
weakness
Older age, prolonged
duration prior to Rx,
cardiac manifestations,
malignancy, no
response to Rx
Independent risk factors
Older age
Fever
Leukocytosis
Failure to induce remission
Comorbid factors
Malignancy
Skin rash
Dysphagia
Shorter disease historv
Signs with no prognostic
significance
Skin rash, “routine” test
results, sex, duration of
disease, age
Severity of activity,
ESR
Sex, skin rash,
ESR, EMG abnormalities, hematocrit
abnormal muscle histopathology
.
Severity of activity,
scleroderma,
Raynaud’s phenomenon
Corticosteroid Rx,
degree of inflammation
on muscle biopsy
Arthritis, ESR, abnormal muscle histopathology, EMG abnormalities, Raynaud’s
phenomenon, hemoglobin level, blood pressure, EKG abnormalities, splenomegaly, sex,
ANF, level of muscle
enzymes
*CPK = creatine phosphokinase; Rx = treatment: ESR = erythrocyte sedimentation rate: EMG
electromyogram; EKG = electrocardiogram; ANF = antinuclear factor.
survival rates. Using these methods, failure to induce
remission, leukocytosis of lO,OOO/pIor more, temperature above 38”C, and older age, and to a lesser degree,
a shorter history and dysphagia, were identified as
independent risk factors for mortality. Pneumonia was
the main reason fever was identified as a risk. After
exclusion of the remission variable and of pneumonia
patients, the significant risk indicators identified were
white blood cell count and age.
Our findings are similar to those in other series
with regard to the overall proportion of patients with
=
PM/DM who died during followup (2-5,8,9) (Table 41,
main causes of death (3-6,8,18) (Table I), and shape of
the actuarial survival curve ( 3 ) (Figure 1). Similarly to
other series of patients with PM/DM, older age (2,4,6),
dysphagia (3,8), and acute progressive onset of the
disease (2,s) with fever and leukocytosis predicted
poorer survival. Surprisingly, malignancy, which has
been reported to be associated with reduced survival
in PM/DM (4,6,8,18), was not independently found to
affect survival in our subjects (Table 5 ) .
We could not confirm that the overlap syn-
PROGNOSTIC FACTORS IN POLYMYOSITIS
dromes (4,8), a prolonged disease history ( 5 , 6 ) , the
degree of elevation of serum CPK (3,cardiac manifestations (18), or Raynaud’s phenomenon (8) had any
effect on survival. In agreement with other studies, sex
(3,6,8), sedimentation rate (3,4), hemoglobin level (31,
a n d EMG abnormalities (3) had no prognostic significance. Additional parameters which did not affect
survival were arthritis, splenomegaly, high blood pressure levels at diagnosis, antinuclear antibodies in the
serum, or abnormal histologic findings on muscle
biopsy (Table 5).
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