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Rheumatol Int (2001) 21: 106111 DOI 10.

1007/s00296-001-0141-3

O R I GI N A L A R T IC L E

Y. Yang J. Fujita M. Tokuda S. Bandoh T. Ishida

Lung cancer associated with several connective tissue diseases: with a review of literature

Received: 19 May 2001 / Accepted: 6 September 2001 / Published online: 10 October 2001 Springer-Verlag 2001

Abstract The association between connective tissue disease (CTD) and malignancy has been an area of debate. Whether this relation is casual or causal, it would seem that the importance of their possible relationship is twofold. The purpose of this study is to describe the clinical features of lung cancer associated with several CTDs. Patients with CTD associated with lung cancer were retrospectively evaluated. A review of the clinical features of 153 reported cases from 1944 to the present was conducted. There were 82 females and 71 males, with a median age of 58. Histological types of lung cancer were as follows, bronchioloalveolar cell carcinoma (39 cases), adenocarcinoma (36), squamous cell carcinoma (28), small cell lung cancer (27), large cell carcinoma (6), others (8), and unknown (10). There was a relationship between smoking and development of lung cancer in patients with rheumatoid arthritis (RA) and polymyositis/dermatomyositis (PM/DM). The majority of patients with progressive systemic sclerosis (PSS) who developed lung cancer were female, with underlying interstitial brosis, and most tumors were of bronchioloalveolar cell or adenocarcinoma cell type. Patient characteristics were signicantly dierent among the various groups of CTD associated with lung cancer.

Keywords Lung cancer Connective tissue disease Smoking Fibrosis Histology

Introduction
Connective tissue disease (CTD) is a group of chronic, multisystem, autoimmune disorders, characterized by inammation of the joints and the surrounding soft tissue, and there are varying degrees of systemic involvement. The etiology is unknown. CTDs include systemic lupus erythematosus (SLE), rheumatoid arthritis (RA), polymyositis/dermatomyositis (PM/DM), progressive systemic sclerosis (PSS), and Sjogren's syn drome (SS). Pulmonary malignancy has become a more commonly recognized feature of CTD, and CTD in association with malignant neoplasm has been the subject of considerable controversy and speculation [1]. Coincident occurrence of CTD and lung cancer has been reported with varying degrees of frequency in PSS, RA, and PM/DM, but rarely in SLE and SS. Mellemkjar et al. [2] have reported that 308 of 20,699 patients (1.49%) identied with RA in the nationwide Danish Hospital Discharge Register were found to have an associated lung cancer. Roumm and Medsger evaluated the association between PSS and malignancy in the Pittsburgh metropolitan area from 1971to 1982 as well data for this geographic area for the Third National Cancer Survey of 19691971. They found an increase in observed lung cancer in patients with PSS after adjusting for age and sex (relative dierence=4.4, P<0.05) [3]. Winkelmann et al. reported 14 cases of lung cancer in patients with a diagnosis of scleroderma [4]. Surprisingly, 9 of the 14 patients in this study had never smoked. Monti pointed out that carcinoma of the lung was the most commonly reported form of malignant disease in female patients with PSS [5]. Certain CTDs are regarded as markers of internal malignancy [6]. This is particularly true of DM [7], and PSS has been similarly considered [8]. Since skepticism still exists concerning pulmonary cancer as a complication

Y. Yang J. Fujita (&) M. Tokuda S. Bandoh T. Ishida First Department of Internal Medicine, Kagawa Medical University, 1750-1, Miki-cho, Kita-gun, Kagawa, 761-0793, Japan E-mail: jiro@kms.ac.jp Tel.: +81-87-891-2147 Fax: +81-87-891-2147 Y. Yang Department of Rheumatology and Immunology, First Clinical College, China Medical University, Shenyang, 110001, China

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of CTD, it is worthwhile to continue to accumulate data from relevant experiences. At present, there are few studies which compare clinical features of CTD associated with lung cancer. Our present study has been designed to compare clinical features of lung cancer associated with PSS, RA, DM/ PM, SLE, and SS.

Literature review
A review of the literature describing cases of lung cancer associated with CTD was carried out (Table 1) [1, 3, 4, 5, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83, 84, 85, 86, 87, 88, 89, 90, 91, 92, 93, 94, 95, 96]. First, we reviewed case reports concerning lung cancer associated with CTD through MEDLINE. Then, articles with good clinical descriptions that were cited in these articles were also included. There were 82 females and 71 males, including 54 smokers, 27 non-smokers, and 72 of unknown smoking status. Pulmonary brosis was detected in 74 cases. Currently, we have reviewed the available literature and found a satisfactory description of many cases of carcinoma of the lung in patients with PSS [1, 3, 4, 5, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56], RA [57, 58, 59.60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71], and PM/DM [71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83, 84, 85, 86, 87, 88, 89. 90]. In contrast, association of lung cancer with SLE [91, 92, 93, 94] and SS [95, 96] was documented to be very rare.

Results
In patients with PSS, the majority of patients were women, most of them non-smokers. In many cases, the patients had suered from CTD with pulmonary brosis for many years and lung malignancy developed as a terminal event. We can only speculate that the pulmo-

nary brosis, which preceded the cancer in most cases, predisposes the lung to malignant transformation. We did nd that patients over the age of 50 years when CTD was diagnosed were at the greatest risk (Table 1). Frequencies of reported cases of patients with CTD and lung cancer are demonstrated in Fig. 1. There were 96 reported cases of PSS associated with lung cancer, 27 cases of RA, 24 cases of PM/DM, 4 cases of SLE, and 2 cases of SS (Table 1). There were 69 females and 27 males in cases of PSS, 5 females and 22 males in cases of RA, 5 females and 19 males in cases of PM/DM, 2 females and 2 males in cases of SLE, and 1 female and 1 male in SS (Table 1). There was a signicant female predominance in cases of PSS associated with lung cancer in comparison with the other varieties of STD (P<0.0001, v2 test). There were 23 non-smokers and 19 smokers in the 42 reported cases of PSS, in which smoking history was described; 2 non-smokers and 19 smokers in cases of RA; 1 non-smoker and 12 smokers in cases of PM/ DM; 3 smokers in cases of SLE, and 1 non-smoker and 1 smoker in cases of SS (Table 1). There was a significant non-smoker predominance in patients with PSS associated with lung cancer compared with the others STDs (P<0.0001, v2 test). There was a signicant smoker predominance in patients with RA as well as PM/DM associated with lung cancer (P<0.0001, v2 test). There were 44 brosis and 2 non-brosis cases in the 46 cases of PSS in which the status with regard to brosis was described. In those cases so reported with RA, PM/DM, and SLE, there were 20 brosis and 3 non-brosis; 8 brosis and 6 non-brosis; and 2 brosis, 1 non-brosis, respectively.(Table 1). There was a signicant predominance of existing lung brosis in patients with PSS as well as RA associated with lung cancer compared with PM/DM (P<0.0001, v2 test). Dierences of histology of lung cancer in reported cases of patients with CTD are demonstrated in Fig. 2. There were 36 cases with bronchioloalveolar carcinoma (BAC) and 60 cases with non-BAC in reported patients of PSS; 2 with BAC and 26 with non-BAC in cases of RA; 1 with BAC and 23 with non-BAC in cases of PM/ DM (Table 2). There was a signicant predominance of BAC in patients with PSS associated with lung cancer compared with the others (P<0.0001, v2 test, Figure 2).

Table 1 Clinical features of patients with lung cancer associated with several connective tissue diseases. SLE systemic lupus erythematosus, RA rheumatoid arthritis, PM/DM polymyositis/dermatomyositis, PSS progressive systemic sclerosis, Sjogren Sjogren's syndrome Reported case (n) PSS RA PM/DM SLE Sjogren Total 96 27 24 4 2 153 Age (median) (years) 56 63 57 56 73 58 Female/male (n) 69/27 5/22 5/19 2/2 1/1 82/71 Smokers/ non-smoker (n) 19/23 19/2 12/1 3/0 1/1 54/27 Fibrosis (+/)) 44/2 20/3 8/6 2/1 0/0 74/12

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Fig. 1 Frequencies of reported cases of patients with connective tissue disease and lung cancer

Discussion
Since the etiology of CTD is multi-factorial, it can only be speculated that many factors play a role in linking CTD and malignancy. Normal immune mechanisms may constantly be involved in the destruction of abnormal cells that are prototypes of cancer. When abnormal lymphocytes and plasmacytes proliferate and produce defective globulin antibodies, this defense against cancer may break down and a carcinoma may then become manifest clinically. These arguments suggest that immunoproliferative and immunodecient states may provide a bridge between CTD and cancer [32]. In the present study, we demonstrate clinical features of patients with lung cancer associated with CTD. The most important nding of our present study was the striking dierence of frequencies in lung cancer in each
Fig. 2 Dierences of histology of lung cancer in reported cases of patients with connective tissue disease and lung cancer. There is a signicant predominance of bronchioloalveolar cell carcinoma patients without progressive systemic sclerosis associated with lung cancer (P<0.0001, v2 test)

CTD. We found that the majority of patients in our clinic had lung cancer combined with SLE and RA; however, our survery revealed that it was PSS that coexisted with lung cancer most frequently. Since our study was designed to evaluate previously reported cases from the literature, accurate incidence of lung cancer in each CTD could not be evaluated. However, reports of lung cancer associated with SLE and SS were extremely rare. The second important nding of the present study was an extraordinarily high frequency of BAC in patients with PSS. Talbott and Barrocas have stated that 77% of the reported lung cancers among patients with PSS were BAC [40]. Montgomery et al. pointed out that over 50% of lung tumors appearing in patients with PSS are of the BAC type, whereas this variety generally accounts for less than 4% of all lung cancers [21]. This type of carcinoma is well known to occur in brotic or scarred lung [43]. In PSS, the atypical proliferation of alveolar epithelium is noted in the vicinity of brotic lung tissue. Therefore, a long-standing immunological imbalance and poor removal of pollutant carcinogens via blocked lymphatic channels by the brotic tissue could be thought of as a trigger mechanism in the neoplastic progression of metaplastic alveolar epithelial cells [46]. Since epithelialization of the cystic spaces is a common nding in this sequence of events, it has been speculated that the terminal bronchiolar epithelium has proliferative potentialities from which bronchiolar neoplastic cells arise as a reaction to the chronic brotic process. Thus, BAC in PSS may be the result either of a metaplasia associated with the brosis or a direct consequence of the systemic sclerotic degeneration [40]. Carcinoma arising in lungs aected by PSS probably diers in its etiological pattern from cancer of an industrial origin where a specic agent such as asbestos, chromate, or hematite is implicated [21].

109 Table 2 Histology of lung cancer associated with several connective tissue diseases. SLE systemic lupus erythematosus, RA rheumatoid arthritis, PM/ DM polymyositis/dermatomyositis, PSS progressive systemic sclerosis, Sjogren Sjogren's syndrome Histology Bronchioloalveolar cell carcinoma Adenocarcinoma Squamous cell carcinoma Small cell carcinoma Large cell carcinoma Others Unknown Total
a

PSS 36 (37.5) 26 13 14 3 1 3 96 (27.1) (13.5) (14.6) (3.1) (1) (3.1)

RA 2 (7.1) 6 (21.4) 7 (25) 6 (21.4) 2 (7.1) 2 (7.1) 3 (10.7) 28a

PM/DM 1 (4.2) 2 5 7 0 5 4 24 (8.3) (20.8) (29.2) (0) (20.8) (16.7)

SLE 0 (0) 1 2 0 1 0 0 4 (25) (50) (0) (25) (0) (0)

Sjogren 0 (0) 1 1 0 0 0 0 2 (50) (50) (0) (0) (0) (0)

One patient had double primary lung cancer

The third nding of our present study was that patients with pulmonary brosis appear prone to develop pulmonary malignancies. Pulmonary brosis associated with CTD may increase the risk of lung cancer. It has been pointed out that chronic pulmonary brosis is the most common pathological nding in the PSS lung. It is found in 7490% of cases autopsied. Several authors suggested that in diuse interstitial brosis, neoplastic proliferation results from atypical epithelial regenerative changes [41]. One possible mechanism is through the eects of cytokines such as transforming growth factorb which may be mitogenic and cause excess cellular division resulting in transformation [97]. Alternatively, changes in the extracellular matrix, which play an important part in growth and dierentiation, may aect the behavior of normal cells [98]. The fourth nding was that since reliable smoking histories were not available for all patients, it is inconclusive whether smoking accounted for the excessive relative risk of lung cancer in this study. Since some patients who developed lung cancer were lifetime nonsmokers, histologic types of cancer which occurred in them are not those chiey associated with smoking. Some researchers have reported that patients with CTD are defective in eliminating inhaled oncogenic factors, and this can be an added stimulus for the malignant transformation of pulmonary regenerating cells [41]. CTD as a paraneoplastic syndrome was frequently the presenting feature of an otherwise occult malignancy. Substances secreted by malignant cells may be directly responsible for the CTD changes as occasionally seen with the carcinoid syndrome [99]. Rarely, CTD and cancer occurred simultaneously, especially in PM/DM, suggesting that the former can be a paraneoplastic manifestation [54]. Awareness of these associations may lead to earlier cancer detection, and hence, potentially may lead to more eective therapy. Chemotherapeutic drugs have been increasingly utilized for their immunosuppressive and anti-inammatory activity in patients with RA, SLE, and PM/DM [100]. Treatment with chronic immunosuppressive agents is believed to be another cause of tumor development in CTD. The potentially oncogenic eect of these agents has recently been reviewed in detail, but with inconclusive results [41]. Because impairment of immune surveillance with subsequent proliferation of

malignant clones may have already occurred in diseases with an altered immune state, immunosuppressive therapy in this setting may be a very serious therapeutic maneuver, potentially further enhancing malignant growth [100]. In the present study, we retrospectively analyzed previously published case reports. Since case reports imply that the co-occurrence represents a real association rather than chance, and since there are potential biases in relation to publication, one needs to be careful in drawing conclusions. In addition, underlying problems of selection bias, publication bias, and missing data in the original publications should be considered. Furthermore, the reported P values have to be regarded as ``descriptive'' because no clear a priori hypothesis had been stated before analyzing the data. Therefore, a suggestion is that the cancer registry of a local area be reviewed in relation to lung cancer to see whether it is possible to link that information to CTD data in relation to histological type. In summary, our present study demonstrates the clinical features of lung cancer associated with CTD. Future studies should be performed to clarify the pathogenesis of the relationship of CTD and lung cancer.

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