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Routine vs Extensive Malignancy Search for Adult Dermatomyositis and Polymyositis
A Study of 40 Patients
Agnès Sparsa, MD;
Eric Liozon, MD;
François Herrmann, MD, MPH;
Kim Ly, MD;
Valérie Lebrun, MD;
Pascale Soria, MD;
Véronique Loustaud-Ratti, MD;
Marie-Laure Bouyssou-Gauthier, MD;
Serge Boulinguez, MD;
Christophe Bédane, MD, PhD;
Marie-Odile Jauberteau, MD, PhD;
Elisabeth Vidal, MD;
Jean-Marie Bonnetblanc, MD
Arch Dermatol. 2002;138:885-890.
ABSTRACT
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Objective To identify potential risk factors and the yield of routine screens
for early detection of malignancy associated with dermatomyositis (DM) and
polymyositis (PM).
Design Retrospective study of malignancies in all patients with DM or PM followed
up between the years 1981 and 2000 and a review of the relationship of DM
and PM to malignancy, the usefulness of various tests or examinations for
malignancy search, and the patients' course.
Setting Departments of internal medicine and dermatology in a teaching hospital.
Patients Forty consecutive adult patients with DM (33 cases) or PM (7 cases).
Main Outcome Measures (1) Rate of false-negative results of routine workup and yield (percentage
of positive results) of blind malignancy search and (2) comparison of 16 characteristics
in patients with malignancy vs those without.
Results Malignancy occurred in 16 patients: 13 with DM and 3 with PM. In all
cases, the diagnosis of malignancy was made concurrently with or shortly after
the diagnosis of DM or PM. Factors associated with malignancy were recruitment
in the internal medicine department (P = .02), constitutional
symptoms (P<.01), a rapid onset of DM or PM (P = .02), the lack of Raynaud phenomenon (P< .01), and a higher mean erythrocyte sedimentation rate (P<.01) and creatine kinase level (P<.01). Initial routine search failed to discover 4 malignancies,
3 of which were discovered at an advanced stage by more extensive investigations.
The positive result yield of blind malignancy search was only 13% (11 of 87),
but reached 28% (5 of 18) for blind abdominal-pelvic and thoracic computed
tomographic scans.
Conclusion Extensive search for malignancy, particularly computed tomographic scans,
may be warranted in at least a subset of patients with DM or PM and risk factors
of malignancy.
INTRODUCTION
DERMATOMYOSITIS (DM), a rare inflammatory myopathic disorder characterized
by proximal, symmetric muscle weakness and specific skin lesions, has been
associated with an increased incidence of malignancies, although the exact
risk and incidence in these patients is controversial.1-4
In almost two thirds of all patients, there is a close temporal relationship
between the diagnosis of myositis and the diagnosis of malignancy, suggesting
that the 2 processes are linked.
For Callen et al,5 Callen,6-8
and Richardson and Callen,9 most formerly published
data do not support the usefulness of an extensive malignancy evaluation in
otherwise nonsymptomatic patients with DM or polymyositis (PM). In our opinion,
further studies are warranted to clarify the optimal screening strategies
for malignant neoplasm in patients with DM or PM because (1) there is, to
our knowledge, no published study that has prospectively compared the value
of routine and extensive workup; (2) routine malignancy screening did not
enable all authors to detect malignancies at an early, potentially treatable
stage10-12; (3)
in 2 recent case-control studies, colon and rectal carcinoma were found to
be overrepresented in elderly patients, justifying routine lower digestive
tract investigations in this group of subjects13-14;
(4) pelvic computed tomographic (CT) scans and serum cancer antigen 125 determinations
could be helpful in the evaluation of ovarian cancer,15
an overrepresented tumor in women with DM or PM that is seldom detected prior
to disseminated disease by standard pelvic evaluations11-12,16-18;
(5) recent evidence has been provided that dermatomyositis is strongly associated
with some types of cancers, particularly ovarian and lung19;
and, finally, (6) the risk of developing a specific type of cancer together
with DM or PM may be unequal in different populations. For example, Asian
patients from Hong Kong developing DM seem to be at high risk of underlying
nasopharyngeal carcinoma,20-23
a finding very uncommon in white populations.
This renewal of an old controversy compelled us to investigate in our
own series the relationship of DM and PM to malignancy. Also, we reexamined
if some tumors could have been found at an earlier stage had a more extensive
malignancy search been pursued.
PATIENTS AND METHODS
Forty adult patients with DM or PM (age  18 years) seen between 1981
and 2000 in the Departments of Dermatology (19 cases) and Internal Medicine
(21 cases) of Dupuytren Hospital, Limoges, France, were enrolled in a retrospective
study. Diagnosis was based on the criteria of Bohan and Peter24
and of Strongwater.25 Patients with inclusion
body myositis and macrophagic myofascitis were excluded. Dermatomyositis was
considered definite with the presence of 3 or more criteria, probable with
2, and possible with 1. Cutaneous signs were always present. In cases of amyopathic
DM, cutaneous signs were clinically characteristic and were confirmed by a
skin biopsy findings. Polymyositis was considered definite with 4 criteria
and probable with 3. Constitutional symptoms were defined as more than 5%
of body weight loss and/or body temperature above 38°C for at least 1
week or recurring. The onset of DM and PM was considered rapid if the diagnosis
was made within 2 months after the appearance of initial signs and/or symptoms.
Dysphonia, proximal dysphagia, abnormal swallowing, dyspnea, and rhabdomyolysis
were considered signs of severity.
No specific recommendations were made regarding the extent of workup.
All patients without prior cancer underwent at least a routine malignancy
screen, including a careful history review, a complete physical and pelvic
examination, standard biologic tests (including blood cell counts, erythrocyte
sedimentation rate, general chemistry screen and liver function tests, a chest
roentgenogram, a mammogram in women, and any tests or examinations directed
toward abnormal symptoms or results, according to the recommendations of Callen7-8 and Richardson and Callen9).
In addition, 38 patients had 1 to 9 (mean of 4) further blind tests or examinations
(eg, nonjustified by an abnormal finding on routine screening) performed during
the initial course of DM or PM. Tests and examinations that were considered
helpful for the diagnosis of malignancy were those allowing subsequent directed
examinations to establish the diagnosis. Most patients with a negative initial
cancer workup were reinvestigated at least once during the follow-up.
Treatments were not standardized and consisted mainly of systemic glucocorticoids
(26 patients). Resistance to glucocorticoids was defined as persistently elevated
muscle enzyme levels or florid skin lesions after 8 weeks of treatment at
a daily dose of at least 1 mg/kg.
Six patients received high-dose intravenous immunoglobulins, 2 received
antimalaria drugs alone for amyopathic dermatomyositis, and 9 received immunosuppressive
agents (methotrexate, azathioprine, or both). One patient with gastric carcinoma
and true paraneoplastic DM underwent gastrectomy preceded by plasma exchanges.
A cancer of the cervix occurred in a patient who was treated over 4 years
for a refractory PM with a combination of immunosuppressive agents. This case
was initially classified as PM without associated malignancy.
Clinical, biological, and radiological data were recorded and compared
between cases with and without associated malignancy. Given the relatively
small size of our patient sample, only univariate analysis was carried out.
Statistical analyses were evaluated using the  2 method or
the Fisher exact test for qualitative data and the Wilcoxon/Mann-Whitney test
for quantitative data.
RESULTS
DESCRIPTION OF PATIENTS
The main characteristics of the series of patients are shown in Table 1. All 40 patients were adults (mean
age, 57.1 years). Thirty-seven cases met at least 3 criteria of Bohan and
Peter,24 while 3 cases corresponded to amyopathic
DM. One case had overlap syndrome between definite polymyositis and systemic
sclerosis. Sixteen patients (mean ± SD age, 62 ± 16 years) had
DM or PM associated with malignancy, including 3 of 7 patients with PM and
13 of 33 patients with DM. As given in Table 2, 18 malignancies (16 cancers and 2 non-Hodgkin lymphomas)
were discovered, always concurrently with or soon after the DM or PM onset.
Two patients had 2 separate cancers diagnosed simultaneously during the initial
workup. In 3 other patients, recurrence or progression of a previously diagnosed
malignancy was temporally associated with the development of DM or PM. One
true recurrence occurred 15 years after the diagnosis of a cancer of endometrium.
One patient had simultaneously a cancer of the left breast and a squamous
cell cancer of the lung occurring 14 years after a cancer of the right breast.
The diagnosis of malignancy was made before the diagnosis of DM or PM in 2
patients, concurrently with DM or PM in 6, and shortly after DM or PM in 8
(mean [range] time, 5 [1-12] months).
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Table 1. Main Characteristics of the Series*
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Table 2. Characteristics of Malignancies Associated With DM and PM*
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The mean (range) follow-up time from DM or PM onset was 56 (4-216) months
and was respectively 28 (4-160) and 72 (13-216) months in patients with and
without associated malignancy. Sixteen patients (40%) died, including 3 patients
without and 13 patients with associated malignancy (12.5% vs 75%; P<.001). Only 25% of the patients with malignancy compared with
96% of the patients without survived more than 2 years (P<.001). The cause of death was always due to progression of malignancy
in patients with DM or PM with cancer, while it was due to specific complications
of DM or PM or its treatment in patients with idiopathic DM or PM. The mean
time to the cancer death from the diagnosis of myositis was 12.3 months. Only
2 patients with DM or PM associated with neoplasm (malignant lymphoma and
cancer of the breast) recovered from malignancy. In a third patient, microscopic
metastases of a breast cancer were continuously controlled with antihormonal
therapy.
RESULTS OF SCREENING INVESTIGATIONS IN THE DIAGNOSIS OF MALIGNANCY
In patients with previous malignancy, investigations were directed at
least toward the demonstration of recurrence of the same tumor. Results were
positive in 2 cases, including the patient with very late relapse of endometrium
carcinoma. In a third case with a long history of breast cancer, more extensive
investigations were performed, allowing the discovery of 2 separate new tumors.
In the fourth case, pathologic evidence of recurring breast cancer was not
obtained despite multiple thorough workups, but was indirectly confirmed 10
months after the diagnosis of PM, since the patient developed a disseminated
intravascular coagulation, which disappeared within a few weeks with the administration
of antiestrogen therapy.
In patients without a previous malignancy, the diagnosis of an associated
tumor was suspected on clinical and routine screen backgrounds and confirmed
by appropriate investigations in 7 of 12 cases. Initial routine evaluation
failed to discover 4 silent malignancies: an anaplastic lymphoma of the psoas
muscle in a 24-year-old man, a high-grade astrocytoma of the brain in a 72-year-old
man, a recurrence of breast cancer in a 69-year-old woman, and an ovarian
carcinoma in a 46-year-old woman. Further blind workup was only performed
in the patient with breast cancer and was unsuccessful. The malignancies were
diagnosed later at a mean of 7 months after onset of DM, all at an advanced
stage. The 2 patients with astrocytoma and ovarian carcinoma soon died of
cancer, while the other 2 patients with lymphoma and breast carcinoma survived,
despite a poor initial condition. In retrospect, a late diagnosis of neuroendocrine
carcinoma of the mediastinum (suspected only on a blind CT scan) was made
in a fifth patient owing to the failure to recognize a mild enlargement of
the upper mediastinum on the initial chest radiograph.
The description of blind screening investigations and the contribution
of each to the diagnosis of malignancy associated with DM or PM are given
in Table 3. Of 122 investigations,
30 (25%) were considered positive. The rate of positive results was 54% (19
of 35) for directed screens and 13% (11 of 87) for blind screens. Abdominal-pelvic
and thoracic CT scans were the most useful blind examinations, with 28% (5
of 18) of the positive results.
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Table 3. Description and Results of Nonroutine Screening Tests and
Examinations Performed in Patients With DM or PM*
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RISK FACTORS OF MALIGNANCY
The prevalences of risk factors of malignancy are listed in Table 4. Men with cancer were older (mean
of 56.2 years vs 33.2 years) but this difference did not reach significance
(P = .1) and was not observed in women (mean of 60
years vs 57.4 years). The variables significantly associated with the occurrence
of malignancy were the presence of constitutional symptoms (P = .009), the lack of Raynaud phenomenon (P
= .003), and a higher mean erythrocyte sedimentation rate (P = .008) and creatine kinase level (P = .01).
Both cases of DM presenting with cutaneous necrosis had associated cancer
(P = .16). Recruitment in the internal medicine department,
as opposed to the dermatology department, was also associated with a higher
risk to discover a malignancy (P = .02). No interdepartmental
differences were found between patients with respect to age, sex, and rapid
onset of symptoms and signs of severity. Patients recruited by internists
more often presented with constitutional symptoms (P
= .07).
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Table 4. Factors Associated With Malignancy in 40 Patients With DM
or PM*
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COMMENT
In an unselected sample of 40 adult patients with DM or PM, we found
in retrospect a malignancy temporally associated with the disease onset in
16 cases (40%). The reported rate of malignancies in unselected series of
patients with DM or PM has widely ranged from 11% to 43%,2-3,13-14,26-39
with a large population cohort and case-control studies reporting a rate of
13% to 25%.2-3,31, 39
This high frequency of malignant diseases closely related to DM and PM in
our series may be explained in part by a large number of patients with DM,
which has been more closely associated than PM with malignancy in large population-based
studies.3, 19, 39 It
is worthy to note that most malignancies were diagnosed in patients observed
by internists and that the risk of disclosing a neoplasm temporally linked
to DM or PM was significantly higher in this population than in patients observed
by dermatologists (52% vs 26%; P = .02). Such a difference
is unlikely to result from a more aggressive cancer-screening policy by internists,
because patients observed by internists did not undergo much more blind investigations
(mean, 4.2) than did patients followed up by dermatologists (mean, 3.6). Most
probably, patients referred to internists are sicker than those referred to
dermatologists and are more likely to have a malignancy.
Cancers encountered in our patients were similar in type and location
to those previously described,1, 6, 13, 17, 30, 32-34,40-41
except for a case of primary brain neoplasm, which to our knowledge has been
reported only once.42 Lymphoma represented
13% of all malignancies. In other studies, this rate has ranged from 0% to
22%.2, 17, 31-33,37, 40, 43
In our study, several clinical observations and laboratory variables
were associated with the risk of concurrent or subsequent malignancy. Cancer
was twice more frequent in women than in men with DM or PM, a figure that
has already been reported,32 but not by all
authors.1-5,13, 31
In our series, the difference, however, was not statistically significant.
We did not find any association between malignancy and increasing age, contrary
to many studies.2, 13-14,17, 28, 30, 32, 37, 39, 43
This difference may be due to the small size of our sample. One third of our
patients with DM or PM and malignancy were younger than 50 years, suggesting,
in agreement with the study of Schulman et al,10
that age alone should not dissuade clinicians from a careful cancer assessment.41, 44 We found a consistent association
between a rapid onset of the disease and malignancy, confirming the findings
in a previous report.43 In our patients there
was also a striking negative association between Raynaud phenomenon and cancer,
a sign that has been previously reported.34
Skin necrosis, which appears as a potential marker of underlying cancer,27, 33, 35 was a presenting
sign in 2 patients in our series, both with concurrent cancer. We could not
confirm previous observations that normal creatine kinase levels in DM and
PM carry a high risk of malignancy,21, 45-46
but we found a significant association between malignancy and high creatine
kinase levels (P = .009). Constitutional symptoms
and a higher mean erythrocyte sedimentation rate were also associated with
cancer in our study. Finally, as shown in Table 5, studies on malignancy in DM and PM do not demonstrate any
universal risk factor. The search of such risk factors seems, therefore, of
limited value in clinical practice.4 We agree
with Callen's recent propositions41, 47
that patients with a history of cancer should be more carefully evaluated
because we found in all 4 such patients either recurrence of a prior malignancy
or a new cancer synchronously with the DM or PM onset.
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Table 5. Risk Factors of Malignancy in the Series of Patients With
DM or PM*
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Finally, our experience is at variance with the classic recommendations
of Callen and others. Strikingly, we found that in all cases the tumor onset
coincided closely with the onset of DM or PM. Other studies have shown that
malignancies occur concurrently with or within 1 year after the diagnosis
of myositis in 26% to 70% of the cases.2-3,6, 17, 43
These data support the performance of a meticulous malignancy screen in patients
with DM or PM. It is widely accepted that the presence of an associated malignancy
represent a major indicator of poor prognosis in DM and PM.4, 24, 27-28,34, 48-49
Likewise, in our series the rate of deaths was impressively higher in cases
of DM and PM associated with malignancy than in idiopathic DM and PM (75%
vs 12.5%; P<.001). This distressing figure, together
with the observation that death always occurred as the result of progression
of malignant disease, even in cases where DM or PM was only partially or poorly
controlled, underscores the potential harmful effects of delayed diagnosis
of malignancy in patients with DM or PM, as exemplified in at least 3 personal
patients' stories. Delaying the diagnosis of malignancy might therefore be
dangerously misleading in some patients.
The main limitations of our study are the retrospective nature of the
work, the relatively small sample size (which did not allow us to determine
unquestionable risk factors of cancer using logistic regression analysis),
and the extremely protean locations and presentations of the tumors encountered,
which prevented us from providing precise guidelines for blind investigations.
Nevertheless, as nondirected abdominal-thoracic (in men) and pelvic-abdominal-thoracic
(in women) CT scans yielded a fairly good rate of positive results in our
patients, we always include it in the workup. Our attitude is in agreement
with that of Hill et al,19 who recommend that
patients with DM undergo body CT scans, in view of the notably increased risk
of non-Hodgkin lymphoma and ovarian, lung, and pancreatic cancer. As suggested
by our results and other studies,13-14
endoscopic studies of the upper and lower gastrointestinal tract should be
done according to the patient's age. Whether new imaging techniques (such
as positron emission tomography) would help uncover some tumors and expedite
the malignancy workup in patients with DM or PM deserves prospective studies.
AUTHOR INFORMATION
Accepted for publication August 20, 2001.
Corresponding author: Eric Liozon, MD, Service de Médecine
Intenre A, CHRU Dupuytren, 87042, Limoges, France (e-mail: eric.liozon{at}unilim.fr).
From the Departments of Dermatology (Drs Sparsa, Lebrun, Bouyssou-Gauthier,
Boulinguez, Bédane, and Bonnetblanc) and Internal Medicine (Drs Liozon,
Ly, Soria, Loustaud-Ratti, and Vidal), and the Immunology Laboratories (Dr
Jauberteau), University Hospital of Limoges, Limoges, France; and the Department
of Geriatrics, University Hospitals of Geneva, Geneva, Switzerland (Dr Herrmann).
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When and How Should the Patient With Dermatomyositis or Amyopathic Dermatomyositis Be Assessed for Possible Cancer?
Callen
Arch Dermatol 2002;138:969-971.
FULL TEXT
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