Small-Cell Lung Carcinoma Produces Salivary-Type Amylase: A Case Report with Review
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1 CASE REPORT Small-Cell Lung Carcinoma Produces Salivary-Type Amylase: A Case Report with Review Seiichi Yamazaki, Shoichiro Ebisawa, Masanori Yasuo, Kazuhisa Urushihata, Tomonobu Koizumi, Keisaku Fujimoto and Keishi Kubo Abstract A 53-year-old woman diagnosed with small-cell lung carcinoma (SCLC) was referred to our hospital because of general malaise and inappetence. Serum amylase levels were drastically elevated at 13,920 IU/l, with the salivary type dominating. She suffered multiple liver metastases and presented with disseminated intravascular coagulation (DIC). She succumbed to progressive malaise one month after admission. The amylase level was increased to 18,630 IU/l just before her death. Necropsy of the right supraclavicular lymph node confirmed SCLC with partial necrosis. Immunohistological analysis revealed that the SCLC produced salivary-type amylase. A rare case of salivary-type amylase-producing SCLC with a futile outcome was reported with review of the previous literature. Key words: small cell lung carcinoma, hyperamylasemia, DIC (DOI: /internalmedicine ) Introduction Reports have occasionally documented hyperamylasemia with ovarian carcinoma, malignant lymphoma, uterine carcinoma and lung carcinoma. Since the first case of bronchogenic carcinoma with elevated serum amylase levels was observed by Weiss et al in 1951 (1), several cases of hyperamylasemia associated with lung carcinoma have been documented. The major histological subtype of these reported cases is adenocarcinoma, whereas small-cell lung carcinoma (SCLC) with hyperamylasemia is extremely uncommon and has never been reviewed to date. In the present study, we encountered a young female smoker who suffered from amylase-producing SCLC with futile outcome, and reviewed this rare case with reference to previous literature. Case Report A 53-year-old woman indicated general malaise and inappetence on a medical examination at a nearby hospital in February Laboratory tests showed markedly elevated serum amylase levels. Chest radiography portrayed massy infiltration of the left upper lung, and abdominal ultrasonography revealed multiple liver masses. Sputum cytology demonstrated the presence of SCLC. She was therefore transferred to our hospital for further evaluation and treatment of the disease in March She had no significant past medical records except for a 40-year cigarette smoking history. Physical examinations revealed emaciation (body height: 150 cm, body weight: 45 kg), left subclavicular lymph node swelling, and liver palpable three finger breadths below the right costal margin. Laboratory findings upon admission (Table 1) indicated slightly elevated leukocyte counts, decreased platelet counts, elevated fibrin degradation product d-dimer (FDP-DD) levels, mild liver dysfunction with diabetes. Serum amylase levels were markedly increased to 13,920 IU/l, with the salivary type dominant. The gastrin-releasing peptide precursor (ProGRP: 5,160 pg/ml) and neuron-specific enolase (NSE: 1,800 ng/ml) were markedly increased. Chest radiography portrayed a massy shadow on the left hilum (Fig. 1). Chest computer tomography revealed a left hilar mm 2 mass with mediastinal lymph node adenopathy being coalescent (Fig. 2). Abdominal ultrasonography (US) showed multiple liver metastases, although abnormalities were not located in the pancreas and ovaries. Although the existence of hyperamylasemia and diabetes suggested First Department of Internal Medicine, Shinshu University School of Medicine, Matsumoto Received for publication August 25, 2006; Accepted for publication February 20, 2007 Correspondence to Dr. Seiichi Yamazaki, se@hsp.md.shinshu-u.ac.jp 883
2 Table1. LaboratoryDataofPatientonAdmision Figure1. ChestX-rayportraysamasyshadowintheleft hilum. apparent pancreatic malignancy, abdominal US indicated negative findings. Bone scintigraphy demonstrated an abnormal massy accumulation in the left hip joint. She was diagnosed as a terminal SCLC case with liver and bone metastases, as well as disseminated intravascular coagulation (DIC). Although she was treated with gabexate mesilate and analgesics for pain relief, her condition deteriorated rapidly and she died on March 31, Serum amylase levels increased to18,630 IU/l just before her death. A necropsy study of the right supraclavicular lymph node was performed, and histopathological findings confirmed the presence of SCLC with neutrophil infiltration. Immunohistological examination of the malignant cells located neural celladhesion molecules (N-CAM) (+), chromogranin A (CGA) (+), synaptophysin (-), salivary-type amylase (+: cytoplasmic, focal), thus confirming the laboratory/clinical finding of the abnormal cells as the salivary-type amylase-producing SCLC (Fig. 3). Discussion The present case of salivary-type amylase-producing SCLC had a poor outcome, although the salivary gland and pancreas were clinically unaffected. Macroamylasemia was excluded because of elevated urine amylase levels. Apparently, excessive amylase in the present case was produced by the SCLC, because immunohistochemical staining of the carcinoma tissue indicated positive signs for anti-salivary type amylase antibodies. N-CAM, CGA, synaptophysin may be the precursors of other biologically active proteins, and Figure2. ChestcontrastedCTrevealsamasinthelefthi lum andmediastinum lymphnodeadenopathy. such carcinoma-positive neuroendocrine markers indicate either SCLC or large-cell neuroendocrine carcinoma (LCNEC). Identification of the carcinoma subtype may be sometimes difficult based on these morphological features; however, smaller cell size, high nuclear/cytoplasmic ratio and prevalence in the central lung indicated our case to be SCLC (2). Carcinoma tissues in the present case histologically coincided with pure SCLC. Hyperamylasemia associated with lung carcinoma is unusual, accounting for only 1-3% of all lung carcinoma cases (3). Hitherto, there have been approximately 80 cases of amylase-producing lung carcinoma reported (4). Minami et al (5) and Ozawa (6) have reported 47 and 14 cases of amylase-producing lung carcinoma, respectively. Both reports showed histological prevalence of adenocarcinoma 884
3 Figure3. Stainingoftherightsupraclavicularlymphnodewiththehematoxylin-eosin(HE)reagent(A),salivaryamylaseimmunostain(B),chromograninA(CGA)immunostain(C),orneural celadhesionmolecule(n-cam)immunostain(d).histpathologicalfindingsoftherightsupraclavicularlymphnodewereconsistentwithstainingofamylase-producingsclc(smal-cellung carcinoma),yieldingsalivary-amylase(+),cga (+)andn-cam (+).(Originalmagnification: 400). (>80% cases of adenocarcinoma and a small percentage of SCLC), with slight male domination (60% males) and complicated distant metastasis with poor prognosis in all cases. The authors showed an early onset of mean ages of 58 (age range: 26-83) and 53 (age range: 37-71) years in their cases of amylase-producing lung carcinoma, respectively. With reference to the estimated mean onset-age for whole-lung carcinoma as years (7-9), the onset of amylaseproducing lung carcinoma might have occurred at a relatively young age. Elevation of the serum amylase implied that the carcinoma cells were distributed adjacent to blood vessels and were thus strategically well facilitated to eventuate remote metastasis. To our knowledge, among the hitherto reported 11 amylase-producing SCLC cases (Table 2), 6 (including the present case) are originated from Japan (5, 10-18). Some authors have previously confirmed and advocated the approach of monitoring amylase production by measuring the amylase activity of extract from carcinoma tissues, and/or exclusion of other internal organ involvement. Alternatively, use of the immunohistochemical method is certain to confirm amylase production from SCLC; viz., even findings of a patient sample of as few as 5 cases (including the present case) have been able to afford immunohistochemical monitoring. Findings of a poor prognosis and a mean age of 56.5 (age range: 26-79) years for all eleven amylase-producing SCLC cases closely resemble those of adenocarcinoma cases. Several explanations for the occurrence of hyperamylasemia with lung carcinomas have been suggested. Amylase immunoreactivity was observed in normal ciliated epithelial cells of the bronchus and in normal serous cells of the bronchial glands (19). Neutrophic inflammation in or adjacent to the carcinoma, or direct invasion of carcinoma cells into the submucosal bronchial glands may give rise to increased amylase activity (20). That might be related to the fact that the prevalence of adenocarcinoma in many amylaseproducing lung carcinomas is a common finding (4-6). In addition, various secretion-related features of SCLC might be involved. SCLC is supposedly derived from neural crest origin cells with multidirectional differentiation in the womb period, and it does not only relate to endocrine neuropeptides but may also involve certain exocrine enzymes (13, 18). Yoshida et al found that ultrastructurally focal and clustered amylase-producing cells specifically contained large zymogen-like granules with excretory ducts and small 885
4 Table2. Case-reportsofHyperamylasemiaAsociatedwithSmalCelLungCarcinoma endocrine-like granules in an SCLC case with hyperamylasemia (13). Thus, amylase-producing SCLC may manifest histopathological features that resemble those of adenocarcinoma. As SCLC is a relatively poorly differentiated carcinoma, the limited diversity of carcinoma cell differentiation might be related to amylase secretions. In patients with amylase-producing malignancies, hyperamylasemia may serve as a useful tumor marker (16, 17, 21). Compared to amylase levels in other reported cases, the present case indicated an extremely high serum amylase level with DIC that yielded no possibility of survival. Several reports have suggested that a proportional relationship exists between the serum amylase level and the progressive stage of disease in lung adenocarcinomas. Because of the limited number of reported SCLC cases, the relationship between the incidence of hyperamylasemia and the clinical outcome and/or chemosensitivity remains unclear to date. In summary, we encountered a rare case of salivary type amylase-producing SCLC with extremely poor prognosis. In addition to the susceptibility of SCLC to smoking, endocrine factors and histopathological diversity may be related with the onset of amylase-producing SCLC. A more detailed pathogenesis of amylase secretion is warranted to clarify the relationship of amylase-producing SCLC with amylase production. Based on the present and other previous findings, amylase-production may be considered as one of the paraneoplastic syndromes in SCLC. References 1. Weiss MJ, Edmondson HA, Wertman M. Elevated serum amylase associated with bronchogenic carcinoma; report of case. Am J Clin Pathol 21: , Matsuno Y, Asanuma H, Nagai K. Clinicopathologic aspects of neuroendocrine tumors of the lung. Haigan (Jpn J Lung Cancer) 46: , 2006 (in Japanese). 3. Takeuchi T, Kametani T. Tumor-associated amylase isozymes. Metabolism 16: 41-49, 1979 (in Japanese). 4. Watanabe M. An autopsy case of amylase-producing lung cancer. Jpn J Cancer Clin 43: , Minami S, Komuta K, Asai M. A case of amylase-producing lung cancer. Nihon Kokyuki Gakkai Zasshi 41: , 2003 (in Japanese). 6. Ozawa S. A case of ectopic amylase producing lung cancer. Jpn J Chest Dis 45: , 1986 (in Japanese). 7. Yang P, Allen MS, Aubry MC, et al. Clinical features of 5,628 primary lung cancer patients: experience at Mayo Clinic from 1997 to Chest 128: , Kimura B, Kidokoro T, Hashizume M. 403 Patients with Lung Cancer Admitted to the 7 Local Community Hospitals in Tokyo. Haigan (Jpn J Lung Cancer) 37: 13-21, 1997 (in Japanese). 9. Kojima T, Yamazaki K, Okamoto Y. Clinical Features of Primary Lung Cancer According to Age. Haigan (Jpn J Lung Cancer) 40: , 2000 (in Japanese). 10. Handler S. Amylase production by bronchogenic small cell carcinoma. Minn Med 58: , Ueda M, Fujii M, Nakashima Y, et al. Hyperamylasemia of unknown etiology. Nippon Shokakibyo Gakkai Zasshi 72: , 1975 (in Japanese). 12. Roberts I, Chopra S, Warshaw AL. Carcinoma of the lung with marked hyperamylasemia and elevated serum calcitonin. Am J Gastroenterol 77: 43-44, Yoshida Y, Mori M, Sonoda T. Ultrastructural,immunohistochemical and biochemical studies on amylase and ACTH producing lung cancer. Virchows Arch 408: , Tsukawaki M, Izawa M, Yoshida M, et al. A case of amylaseproducing lung cancer. Intern Med 31: 60-63, Galus M, Schiffman R, Olkowska D. Massive liver necrosis associated with hyperamylasemia. Liver 18: , Minami S, Yamamoto S, Atagi S. A case of amylase producing lung cancer. Haigan (Jpn J Lung Cancer) 44: 37-41, 2004 (in Japanese). 886
5 17. Benedetti G, Rastelli F, Damiani S, et al. Challenging problems in malignancy: case 1. Presentation of small-cell lung cancer with marked hyperamylasemia. J Clin Oncol 22: , Flood JG, Schuerch C, Dorazio RC, et al. Marked hyperamylasemia associated with carcinoma of the lung. Clin Chem 24: , Hayashi Y, Fukayama M, Koike M, et al. Amylase in human lungs and the female genital tract. Histochemical and immunohistochemical localization. Histochemistry 85: , Lenler-Peterson P. Alpha-amylase in resectable lung cancer(review). Eur Resp J 7: , Uno T, Mochizuki H, Okada T. A case of Amylase-producing lung cancer diagnosed by transbronchial curettage. Haigan (Jpn J Lung Cancer) 43: , 2003 (in Japanese) The Japanese Society of Internal Medicine 887
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