Three Cases of Non-specific Interstitial Pneumonia Associated with Primary Lung Cancer
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1 CASE REPORT Three Cases of Non-specific Interstitial Pneumonia Associated with Primary Lung Cancer Toshio SATO, Ichiro YAMADORI, Jiro FUJITA*, Noboru HAMADA, Toshiro YONEI, Shuji BANDOH*, Yuji OHTSUKI** and Toshihiko ISHIDA* Abstract NSIP associated with primary lung cancer has been rarely reported. In the present report, three cases of histologically proven non-specific interstitial pneumonia (NSIP) associated with primary lung cancer are described. Importantly, in our 3 cases, interstitial pneumonia which is histologically proven to be NSIP was observed diffusely in both lungs. NSIP in these 3 cases responded to steroid therapy. However, 2 patients died from primary lung cancer and 1 patient died from progression of the interstitial pneumonia. Although the association between lung cancer and NSIP has been rarely documented, this combination was considered to be one of the paraneoplastic phenomena. The possible association between primary lung cancer and NSIP is discussed. (Internal Medicine 43: , 2004) Key words: lung cancer, non-specific interstitial pneumonia Introduction In 1994, Katzenstein and Fiorelli reported the histologic features and clinical significance of non-specific interstitial pneumonia (NSIP) (1). The histologic features of NSIP include a varying degree of interstitial inflammation and fibrosis which appear to develop over a specific time (i.e., the process is temporarily uniform) (1). In addition, they described that 10 of their 64 patients with NSIP had an association with connective tissue diseases, including two patients with polymyositis (1). They also reported that the lesion of cellular interstitial pneumonia associated with dermatomyositis termed by Tazelaar et al (2), corresponds to that of NSIP. This evidence suggests that the pathogenesis of NSIP is closely related to autoimmune disorders. Recently, the clinico-pathological features of NSIP have been well characterized. However, NSIP associated with primary lung cancer has been rarely reported. In the present report, we describe three cases of NSIP associated with primary lung cancer and hypothesize that NSIP can be complicated with primary lung cancer and this may be considered to be one of the paraneoplastic phenomena. Case Report Case 1 A 68-year-old man with a 1-month history of progressive dyspnea on exertion visited the out-patient clinic. He had a dry cough and dyspnea, but no sputum or fever. An abnormal shadow was pointed out on his chest X-ray. He was an office worker, who had not experienced any risk factors for occupational or environmental exposure to toxic materials, nor did he have a hypersensitivity pneumonitis. His medical history revealed he had pleuritis at 38 years old and was diabetic for eight years. He was a previous smoker for 40 packyears. His chest X-ray one year prior to consultation showed no abnormality. Rapid progression of his dyspnea occurred for 2 weeks after attending the out-patient clinic and he was subsequently admitted to the hospital. On physical examination, he was afebrile with a respiratory rate of 25/min, blood pressure of 110/70 mmhg, and a regular pulse rate of 84/min. The chest was symmetric, and bibasilar, coarse crackles were ausculated. Laboratory data showed a normal blood count without eosinophilia. The electrolytes, renal, and liver function tests were normal. Quantitative immunoglobulin assay yielded; IgG 1,867 mg/dl (normal 870 1,700), IgA 486 mg/dl (normal ), and IgM, 104 mg/dl (normal ). Anti-nuclear antibody was negative. Although pro-gastrin releasing peptide (pro-grp), sialyl Lewis x-i antigen (SLX), neuron-specific enolase (NSE) From the National Okayama Medical Center, Okayama, *the First Department of Internal Medicine, Faculty of Medicine, Kagawa University, Kagawa and **the Department of Tumor Pathology, Kochi Medical School, Kochi Received for publication September 11, 2003; Accepted for publication March 2, 2004 Reprint requests should be addressed to Dr. Jiro Fujita, the First Department of Internal Medicine, Faculty of Medicine, Kagawa University, Mikicho, Kita-gun, Kagawa
2 SATO et al Figure 1. Chest CT findings of case 1 on admission. Bilateral interstitial consolidation and a coin lesion are demonstrated. were within the normal limit, carcinoembryonic antigen (CEA, 3.2 ng/ml), carbohydrate antigen 19-9 (CA19-9, 44 U/ml), and cytokeratin 19 fragment (Cyfra 21-1, 2.2 ng/ml) were slightly elevated. Arterial blood gas analysis showed po2 of 78 mmhg, pco2 of 39 mmhg, and ph Lung function studies showed %vital capacity 61.4% and FEV1% 81.3%. Chest CT (Fig. 1) revealed diffuse bilateral interstitial infiltrate as well as a nodule ( cm) in the right upper lobe. Flexible bronchoscopy was non-diagnostic. Therefore, lung biopsy using the video-assisted thoracoscopic surgery (VATS) of the right S 3 (distant from the lung tumor) and needle biopsy of the tumor (right S 2 ) were performed. Pathological evaluation revealed squamous cell lung cancer in the right S 2 as well as NSIP (group II) in the right S 3 (Fig. 2). Clinical staging of the primary lung cancer was stage IIIA. Surgical intervention was offered to the patient, but he refused. Oral prednisolone (1 mg/kg/day) was initiated, and the bilateral infiltrates on chest CT scan disappeared. No exacerbation of the interstitial pneumonia was observed during an oral prednisolone treatment. However, 28 months after Figure 2. (A) Squamous cell carcinoma observed in the needle biopsy specimen from the right S 2 ( 144). (B) NSIP group II observed in the surgical biopsy specimen (right S 3 )bythe VATS ( 72). the first admission, combination chemotherapy was administered because of progression of the primary lung cancer. In spite of combination chemotherapy, lung cancer worsened and the patient s condition deteriorated and he died of respiratory failure 48 months after the first admission. Case 2 A 65-year-old man with a one-month history of progressive dyspnea on exertion visited the out-patient clinic. He had a dry cough and dyspnea, but no sputum or fever. He was diagnosed with cardiac arrhythmia and diabetes mellitus. There were no abnormal findings on his chest X-ray. He was a retired office worker, who had not experienced any risk factors for occupational or environmental exposure to toxic materials, nor did he have a hypersensitivity pneumonitis. He was previously hypertensive and he was a smoker of 10 cigarettes/day for about 45 years. One month after consultation, dyspnea progressed for 2 weeks and chest X-ray demonstrated diffuse interstitial infiltrates and he was subsequently introduced and admitted to the hospital. On physical examination, the chest was symmetric, and 722
3 Lung Cancer and NSIP Figure 3. Chest CT findings of case 2 on admission. Bilateral interstitial consolidation and a coin lesion are demonstrated. Thickened subpleural curvilinear shadow was clearly demonstrated. bibasilar, coarse crackles were ausculated. The abdominal examination was normal. There was no peripheral edema, digital clubbing, or cyanosis. Laboratory examination showed a white blood cell count at 9,400/l with a normal differential. Hemoglobin and hematocrit were normal. C- reactive protein (CRP, 1.79 mg/dl) was slightly increased. Arterial blood gas analysis showed PO2 of 68 mmhg, PCO2 of 35 mmhg and ph Lung function studies showed a vital capacity of 47.5% and percent forced expiratory volume in 1s (FEV1%) was 90.5%. Quantitative immunoglobulin assay yielded; IgG 1,591 mg/dl, IgA 319 mg/dl, and IgM 57 mg/dl. The rheumatoid factor was negative, but antinuclear antibody test was positive ( 80). KL-6 was significantly elevated (2,470 U/ml). Although pro-grp was within the normal limit, CEA (8.5 ng/ml), squamous cell carcinoma antigen (SCC, 6.5 ng/ml), and Cyfra 21-1 (11 ng/ml) were elevated. A chest CT showed bilateral ground-glass infiltrates (Fig. 3). A mass, about 4.5 cm in diameter, was present in the area of the ground-glass infiltrates in the left upper lobe. Both Figure 4. (A) Adenocarcinoma observed in TBLB specimen from the left S 1+2 ( 144). (B) NSIP group II observed in the surgical biopsy specimen (left S 8 )bythe VATS ( 72). hilar and mediastinal lymphadenopathies were observed. Bronchoscopic examination revealed no endobronchial lesions. Surgical lung biopsy by the VATS was performed from the left S 8 and it revealed NSIP (group II). The mass lesion was diagnosed as adenocarcinoma by transbronchial lung biopsy (Fig. 4). His treatment with intravenous methyl-prednisolone therapy followed by oral prednisolone, as well as intravenous cyclophosphamide improved his respiratory symptoms. However, the interstitial shadows on chest CT scan showed progression one month later. Three months after the first admission, the patient died of respiratory failure. Specimens obtained by autopsy revealed primary lung cancer and acute exacerbation of the interstitial pneumonia. The pathological pattern of interstitial pneumonia was consistent with usual interstitial pneumonia (UIP). Pathological findings of this case could be interpreted as follows; a lung cancer occurred in a patient who had subclinical UIP changes in bilateral lung bases. Then, NSIP appeared clinically in association with the development of lung cancer. Specimens obtained by VATS were revealed to be NSIP, however, UIP areas were 723
4 SATO et al Figure 5. Chest CT findings of case 3 on admission. Bilateral interstitial consolidation and irregular infiltrates of the lingula (the primary site) are demonstrated. not included in these specimens. Although NSIP had improved by steroid therapy, the patient died from progression of lung cancer. Finally, autopsy revealed extension of lung cancer, diffuse DAD, and subpleural UIP changes. Case 3 A 68-year-old man with a 10-month history of progressive dyspnea on exertion attended the out-patient clinic. He had a dry cough, dyspnea, and slight fever. He was a carpenter, but had not experienced hypersensitivity pneumonitis. His previous medical history revealed chronic sinusitis at 45 years old. He smoked 25 cigarettes daily for about 50 years. Nine months prior to consultation at the out-patient clinic, he experienced gradual progression of his dyspnea and weight loss (7 kg/9 months). He was subsequently admitted. On physical examination, he was febrile (37.1 C) with a respiratory rate of 25/min, blood pressure of 140/72 mmhg, and a regular pulse rate of 78/min. The chest was symmetric, and bibasilar fine crackles were ausculated. Laboratory data showed a normal blood count without eosinophilia. The electrolyte, renal, and liver function tests were normal, except for a slight Figure 6. (A) Adenocarcinoma observed in surgical biopsy specimen (left S 5 )bythe VATS ( 144). (B) NSIP group II observed in the surgical biopsy specimen (left S 5 )bythe VATS ( 72). increase in alkaline phosphatase (ALP, 397 IU/l). Rheumatoid factor was negative, but the antinuclear antibody test was positive ( 40). KL-6 was significantly elevated (1,390 U/ml). Although pro-grp and Cyfra 21-1 were within normal limits, CEA (6.3 ng/ml) and CA19-9 (42.5 ng/ml) were slightly elevated. Arterial blood gas analysis showed po2 of 63 mmhg, pco2 of 36 mmhg, and ph Lung function studies showed %vital capacity 90.4% and FEV1% 79.3%. Chest CT revealed diffuse bilateral interstitial infiltrates with a relatively high density in the lingula of the left lung (Fig. 5). Flexible bronchoscopy was non-diagnostic. Therefore, surgical lung biopsy of the left S 5 and S 8 using VATS was performed. Pathological evaluation revealed adenocarcinoma in the left S 5 and S 8 as well as NSIP (group II) in the same areas (Fig. 6). Intravenous methylprednisolone and oral cyclophosphamide (50 mg/day) were initiated, and bilateral infiltrates on chest CT scan improved. However, the patient deteriorated in spite of combination chemotherapy and he died of respiratory failure 6 months after the first admission. 724
5 Lung Cancer and NSIP Specimens obtained from autopsy revealed lymphangitis caricinomatosa of both lungs. Discussion In this report, we describe 3 cases of NSIP complicated with primary lung cancer. NSIP in these 3 cases responded to steroid therapy. However, 2 patients died from primary lung cancer and 1 patient died from progression of the interstitial pneumonia. Since low dose steroid therapy was continued, recurrence of NSIP was not observed in these 2 cases died from lung cancer. Bronchogenic carcinoma has frequently been associated with paraneoplastic phenomena, ranging from mild systemic or cutaneous disease to neuromyopathic disorders and interstitial pneumonia (3). It has been reported that lung cancer is frequently associated with usual interstitial pneumonia (UIP) and an excess relative risk of lung cancer has been found in patients with UIP compared with the general population (4). This evidence has suggests that UIP may be a precancerous stage before lung cancer. Since clinico-pathological features of NSIP have been recently established (2), there are few reports describing an association between NSIP and primary lung cancer. Recently, Yamadori et al reported a case of primary lung cancer associated with NSIP (5). In contrast, there have been several reports describing focal interstitial pneumonia associated with primary lung cancer. Bandoh et al described a case of focal lymphocytic interstitial pneumonia (LIP) complicated with primary lung cancer (6). In their report, the lung cancer is surrounded by LIP in the same lobe, and infiltrated by CD-8 positive T-cells as well as in the alveolar septa, suggesting that focal LIP is caused by the immunologic reaction against the primary lung cancer (6). In addition, some studies have detailed the immune cell infiltration in lung cancer and the surrounding lung tissue (7 13) and most of the infiltrating lymphocytes consist of T cells, and NK cells which constitute a small portion of the tumor infiltrating lymphocytes (7, 10 13). Watanabe et al have reported that lymphocytic infiltration is marked in adenocarcinoma, particularly in welldifferentiated papillary adenocarcinoma, less in squamous cell carcinoma, and least in small-cell carcinoma (14). Several hypotheses about the pathogenesis of focal interstitial pneumonia associated with primary lung cancer have been suggested. Erickson has reported that the extent of lymphocytic infiltration of tumors and the surrounding lung tissue can reflect the host immune response or tumor antigenicity (15). Bandoh et al also suggested that the occurrence of lymphocyte infiltration in lung cancer (mainly CD8 positive T-cells) is related to the anti-tumor cytotoxic T-cell immunity of the host against the lung cancer (6). Importantly, in the present 3 cases, interstitial pneumonia which is histologically proven to be NSIP was observed diffusely in both lungs. Therefore, the pathogenesis of bilateral NSIP associated with lung cancer should be discussed. Yamadori et al suggested that anti-cytokeratin 8, 18, and 19 antibodies in a patient s serum play a role in the pathogenesis of NSIP associated with primary lung cancer (5). In addition, we have previously demonstrated elevation of anticytokeratin antibodies in sera of patients with NSIP (16 18) as well as patients with radiation pneumonitis (19). Formation of these anti-epithelial antibodies might also play a role in damaging epithelial cells and in developing NSIP in bilateral lungs. In another possibility, since lung cancer produces several growth factors and cytokines, these released products might regulate the development of NSIP. However, the pathogenesis of NSIP complicated with lung cancer still remains unclear, and should be elucidated in future studies. No apparent respiratory disease has been detected in these 3 cases. However since chest CT was not performed previously in these 3 cases, the existence of subclinical interstitial pneumonia could not be excluded. Therefore, the possibility of acute exacerbation of subclinical interstitial pneumonia in association with the development of lung cancer could not be neglected. In summary, we present 3 cases of NSIP associated with primary lung cancer. The NSIP in these cases probably reflects the local immune response to an antigenic stimulus caused by lung cancer, and this combination is considered to be one of the paraneoplastic phenomena. References 1) Katzenstein AL, Fiorelli RF. Nonspecific interstitial pneumonia/fibrosis Histologic features and clinical significance. Am J Surg Pathol 18: , ) Tazelaar HD, Viggiano RW, Pickersgill J, Colby TV. Interstitial lung disease in polymyositis and dermatomyositis. Clinical features and prognosis as correlated with histologic findings. Am Rev Respir Dis 141: , ) Patel AM, Davila DG, Peters SG. Paraneoplastic syndromes associated with lung cancer. Mayo Clin Proc 68: , ) Turner-Warwick M, Lebowitz M, Burrows B, Johnson A. Cryptogenic fibrosing alveolitis and lung cancer. Thorax 35: , ) Yamadori I, Sato T, Fujita J, Dobashi N, Ohtsuki Y, Takahara J. A case of non-specific interstitial pneumonia associated with primary lung cancer: possible role of antibodies to lung cancer cells in the pathogenesis of non-specific interstitial pneumonia. Respir Med 93: , ) Bandoh S, Fujita J, Haba R, et al. Lung cancer with focal lymphocytic interstitial pneumonia. Intern Med 41: , ) Takanami I, Takeuchi K, Giga M. The prognostic value of natural killer cell infiltration in resected pulmonary adenocarcinoma. J Thorac Cardiovasc Surg 121: , ) Lee TK, Horner RD, Silverman JF, Chen YH, Jenny C, Scarantino CW. Morphometric and morphologic evaluations in stage III non-small cell lung cancers. Prognostic significance of quantitative assessment of infiltrating lymphoid cells. Cancer 63: , ) Lipford EH 3rd, Eggleston JC, Lillemoe KD, Sears DL, Moore GW, Baker RR. Prognostic factors in surgically resected limited-stage, nonsmall cell carcinoma of the lung. Am J Surg Pathol 8: , ) Brittenden J, Heys SD, Ross J, Eremin O. Natural killer cells and cancer. Cancer 77: , ) Johnson SK, Kerr KM, Chapman AD, et al. Immune cell infiltrates and prognosis in primary carcinoma of the lung. Lung Cancer 27: 27 35,
6 SATO et al 12) Tosi P, Sforza V, Santopietro R, et al. Bronchiolo-alveolar carcinoma: an analysis of survival predictors. Eur J Cancer 28A: , ) Mori M, Ohtani H, Naito Y, et al. Infiltration of CD8+ T cells in nonsmall cell lung cancer is associated with dedifferentiation of cancer cells, but not with prognosis. Tohoku J Exp Med 191: , ) Watanabe S, Sato Y, Kodama T, Shimosato Y. Immunohistochemical study with monoclonal antibodies on immune response in human lung cancers. Cancer Res 43: , ) Erickson AD. Assessment of immune responses to tumors using cryostat sections of bronchogenic carcinoma. Cancer Res 40: , ) Dobashi N, Fujita J, Ohtsuki Y, et al. Detection of anti-cytokeratin 8 antibody in the serum of patients with cryptogenic fibrosing alveolitis and pulmonary fibrosis associated with collagen vascular disorders. Thorax 53: , ) Fujita J, Dobashi N, Ohtsuki Y, et al. Elevation of anti-cytokeratin 19 antibody in sera of the patients with idiopathic pulmonary fibrosis and pulmonary fibrosis associated with collagen vascular disorders. Lung 177: , ) Dobashi N, Fujita J, Murota M, et al. Elevation of anti-cytokeratin 18 antibody and circulating cytokeratin 18: anti-cytokeratin 18 antibody immune complexes in sera of patients with idiopathic pulmonary fibrosis. Lung 178: , ) Fujita J, Bandoh S, Ohtsuki Y, et al. The role of anti-epithelial cell antibodies in the pathogenesis of bilateral radiation pneumonitis caused by unilateral thoracic irradiation. Respir Med 94: ,
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