Gastrointestinal metastasis of primary lung cancer: An analysis of 366 cases

Hu,Yue; Feit,Noah; Huang,Yanqin; Xu,Wenhong; Zheng,Shu; Li,Xiuzhen

doi:10.3892/ol.2018.8575

Gastrointestinal metastasis of primary lung cancer: An analysis of 366 cases

Authors:
- Yue Hu
- Noah Feit
- Yanqin Huang
- Wenhong Xu
- Shu Zheng
- Xiuzhen Li
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Affiliations: Department of Surgical Oncology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, Zhejiang 310009, P.R. China, The Johns Hopkins University, Baltimore, MD 21231, USA, Cancer Institute, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, Zhejiang 310009, P.R. China, Department of Radiation Oncology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, Zhejiang 310009, P.R. China, Department of Pathology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, Zhejiang 310009, P.R. China
Published online on: April 25, 2018 https://doi.org/10.3892/ol.2018.8575
Pages: 9766-9776
Copyright: © Hu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The gastrointestinal (GI) tract is not a common site of metastasis in primary lung cancer. The aim of the present study was to reveal the clinical and prognostic characteristics of gastrointestinal metastases of lung cancer (GMLC). Information on 366 cases of GMLC was collected and factors that affect severe GI complications were analyzed. Univariate and multivariate survival analyses were performed using the Cox proportional hazards model. Of the cases analyzed, the small intestine (59.6%) and colorectum (25.6%) were the two organs where lung cancer was most likely to metastasize in the GI tract. Squamous cell carcinoma (28.5%), adenocarcinoma (27.6%) and large cell carcinoma (20.9%) were the three most common histological types. However, compared with the histological distributions of primary lung cancer, patients with large cell carcinoma exhibited the highest elevated risk of GMLC [relative risk (RR), 4.07; P<0.001] and those with adenocarcinoma exhibited the lowest risk (RR, 0.58; P<0.001). Differences in organ involvement and in histological type led to varying GI complications. It was also indicated that chemotherapy was associated with a decreased risk of hemorrhage (P=0.006), but there was no reduction in the risk of hemorrhage associated with perforation and obstruction (P>0.05). The median overall survival time of GMLC patients was 2.8 months (range, 0‑108 months). The survival analyses revealed that perforation and extra‑GI metastasis were negative prognostic factors but abdominal surgery was identified a positive prognostic factor. In conclusion, the histological distribution of GMLC differed from that of primary lung cancer. Sufficient and careful patient evaluation, targeted surgeries and systemic therapies for specific patients are able to increase patient survival rate and improve the quality of life.

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1	Mao Y, Yang D, He J and Krasna MJ: Epidemiology of Lung Cancer. Surg Oncol Clin N Am. 25:439–445. 2016. View Article : Google Scholar : PubMed/NCBI
2	Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ and He J: Cancer statistics in China, 2015. CA Cancer J Clin. 66:115–132. 2016. View Article : Google Scholar : PubMed/NCBI
3	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2017. CA Cancer J Clin. 67:7–30. 2017. View Article : Google Scholar : PubMed/NCBI
4	Frank CD, Roy HD, Lynn T and Rogerio CL: Non-small Cell Lung CancerDeVita, Hellman and Rosenberg's Cancer: Principles & Practice of Oncology. 10th Edition. Wolters Kluwer Health Corp.; Philadelphia: pp. 495–502. 2015
5	Yoshimoto A, Kasahara K and Kawashima A: Gastrointestinal metastases from primary lung cancer. Eur J Cancer. 42:3157–3160. 2006. View Article : Google Scholar : PubMed/NCBI
6	Antler AS, Ough Y, Pitchumoni CS, Davidian M and Thelmo W: Gastrointestinal metastases from malignant tumors of the lung. Cancer. 49:170–172. 1982. View Article : Google Scholar : PubMed/NCBI
7	Yang CJ, Hwang JJ, Kang WY, Chong IW, Wang TH, Sheu CC, Tsai JR and Huang MS: Gastro-intestinal metastasis of primary lung carcinoma: clinical presentations and outcome. Lung Cancer. 54:319–323. 2006. View Article : Google Scholar : PubMed/NCBI
8	Rossi G, Marchioni A, Romagnani E, Bertolini F, Longo L, Cavazza A and Barbieri F: Primary lung cancer presenting with gastrointestinal tract involvement: Clinicopathologic and immunohistochemical features in a series of 18 consecutive cases. J Thorac Oncol. 2:115–120. 2007. View Article : Google Scholar : PubMed/NCBI
9	Chongbo S and Gaojia Z: A case report of small intestinal metastasis of lung cancer. Chin J Clin Oncol. 20:3191993.(In Chinese).
10	Zhiqiang C and Chenghai Z: Lung cancer with its first symptom of gastrointestinal hemorrhage: a case report. J Jinan Univ (Med Ed). 17:1321996.(In Chinese).
11	Yuyuan Y: Bowel obstruction caused by colonic metastasis of squamous cell lung cancer: a case report. Chin J Cancer. 18:1431999.(In Chinese).
12	Jianguo S, Xiufeng Z and Qingmei J: A case report of rectal metastasis of small cell lung cancer. Chin J Cancer Prev Treat. 7:3692000.(In Chinese).
13	Jun Q, Wenyong S, Dechuan L, Rongcan L and Guiquan L: A case report of lung cancer with right colonic metastasis. J Coloproctol Surg. 7:492001.(In Chinese).
14	Xiaoqiang L, Delong Z, Yimeng Z and Chunbao Z: Gastric metastasis of primary lung cancer: one case report. Suzhou Med. 24:1602001.(In Chinese).
15	Xiaoning C, Jinlong C and Shilian Z: Bowel obstruction caused by ileum metastasis of lung cancer: a case report. Chin J Prim Med Pharm. 9:7952002.(In Chinese).
16	Xin T, Wang W, Xu Y, Yang Y, Hao W and Li Y: A case report of rectal metastasis of lung cancer. Zhongguo Fei Ai Za Zhi. 5:4572002.(In Chinese).
17	Jinlin L and Xiaoming L: Jejunal metastasis of lung cancer: one case report. J Abdom Surg. 15:592002.
18	Hui C, Yaoguang L and Yin L: A case report of gastric metastasis of lung cancer. J Guangxi Med Univ. 21:7662004.(In Chinese).
19	Huili Z and Hanmeng Y: Bowel idigitation caused by intestinal metastasis of lung cancer: one case report. Med J CASC. 6:352004.
20	Yan L and Chongqin Y: Ileum metastasis of lung adenocarcinoma: a case report. Chin J Geriatr. 24:382–383. 2005.
21	Xiangtao M, Liwei Y, Jing F, Shan W, Ruyi D and Zhirong C: A case report of colonic metastasis of undifferentiated lung cancer. Chin J Clin Oncol. 33:3582006.(In Chinese).
22	Xiangtao M, Liwei Y, Jing F, Shan W, Ruyi D and Zhirong C: Colonic metastasis of squamous cell lung cancer: a case report and review. Cancer Res Prev Treat. 33:6312006.
23	Yong L, Yuguo H, Yongcan L, Hongzhe Y and Fengxia J: A case of colonic metastasis of lung cancer. Chin J Thorac Cardiovasc Surg. 23:1132007.
24	Jianzhong D, Pin Z and Yi W: A case of multiple bowel perforations caused by jejunum metastasis of lung cancer. Chin J Surg. 46:772008.(In Chinese).
25	Lixia L and Weimin Z: Small intestinal metastasis of lung cancer: a case report. J Prac Med. 24:38532008.
26	Xuan W, He H, Muyan C, Liping L, Yuanyuan Z and Li Z: Small intestinal metastasis of non-small cell lung cancer: Case report and literature review. Chin J Cancer. 27:447–448. 2008.(In Chinese).
27	Wei H, Baojin H and Weiru X: A case report of gastric metastasis of primary lung cancer. Chin J Oncol. 30:6982008.(In Chinese).
28	Yingman W, Xiangmin L and Haixia Z: Small intestinal metastasis of lung cancer: case report and literature review. J Fourth Mil Med Univ. 30:962009.
29	Qian L, JIangyang L, Xiaohong W, Yi Y and Lin L: Clinical and pathological analysis of lung giant cell carcinoma with neuroendocrine differentiation metastatic to small intestine. J Diag Pathol. 16:100–103. 2009.
30	Miao Z, Li R and Guangqin Z: A case of gastrointestinal haemorrhage caused by small intestinal metastasis of squamous cell lung cancer. Med J Chin PAPF. 21:605–606. 2010.
31	Fenghui Z and Yunping Z: A case of choroid membrane and rectal metastasis of lung cancer. Chin J Clin Oncol. 37:8782010.(In Chinese).
32	Liu Y, Zhang L, Han X and Zhou T: A case report and literature review of small intestinal metastasis of large cell lung cancer. Zhongguo Fei Ai Za Zhi. 13:655–658. 2010.(In Chinese). PubMed/NCBI
33	Zhidong L, Weijun Z, Funan L, Yimin D and Jixian S: Bowel perforation caused by colonic metastasis of small cell lung cancer: a case report. J Basic Clin Oncol. 23:451–452. 2010.
34	Mo S, Lei D, Wei J, Bin Y and Hongjiang W: Bowel indigitation caused by small intestinal metastasis of lung cancer. J Dalian Med Univ. 32:374–375. 2010.
35	Lei Y, Xishan W, Xinshu D and Li L: Multiple small intestinal metastasis of lung cancer. Chin J Oncol. 32:5252010.(In Chinese).
36	Wang Y, An T, Yang L, Wang Z, Zhuo M, Duan J, Wang J and Wu M: Primary lung cancer with gastrointestinal metastasis: 2 case report and literature review. Zhongguo Fei Ai Za Zhi. 14:278–280. 2011.(In Chinese). PubMed/NCBI
37	Wu W, Mu J, Tong L and Liu Z: Primary lung squamous cell carcinoma ileocecal metastasis: one case report and literature review. Int J Respir. 31:1225–1227. 2011.
38	Xu L, Zijun L, Yahuan G and Juntao Y: Esophagus metastasis of mucoepidermoid lung carcinoma: case report and literature review. Cancer Res Prev Treat. 38:14622011.
39	Hong Z, Xiaojing L and Honglin W: Duodenal metastases from primary squamous cell carcinoma of the lung: one case report. J Chin Oncol. 18:319–320. 2012.(In Chinese).
40	Junni C, Bo Y, Yanli Z, Jie L and Fen W: Gastric metastasis of primary lung cancer: one case report Guangdong. Med J. 33:13692012.
41	Pezzuto A, Mariotta S, Fioretti F and Uccini S: Metastasis to the colon from lung cancer presenting with severe hyponatremia and dyspnea in a young male: A case report and review of the literature. Oncol Lett. 5:1477–1480. 2013. View Article : Google Scholar : PubMed/NCBI
42	Huang YM, Hsieh TY, Chen JR, Chien HP, Chang PH, Wang CH and Huang JS: Gastric and colonic metastases from primary lung adenocarcinoma: A case report and review of the literature. Oncol Lett. 4:517–520. 2012. View Article : Google Scholar : PubMed/NCBI
43	Sakai H, Egi H, Hinoi T, Tokunaga M, Kawaguchi Y, Shinomura M, Adachi T, Arihiro K and Ohdan H: Primary lung cancer presenting with metastasis to the colon: A case report. World J Surg Oncol. 10:1272012. View Article : Google Scholar : PubMed/NCBI
44	Hsing CT, Kim HY, Lee JH, Han JS, Lee JH, Chang JS, Choi SR and Jeong JS: Gastrointestinal metastasis from a primary adenocarcinoma of the lung presenting with acute abdominal pain. Korean J Gastroenterol. 59:382–385. 2012. View Article : Google Scholar : PubMed/NCBI
45	Pratto D, Resial M, Wulfson A, Gennaro M, Brarda M and Schmidt A: Jejuno-jejunal intussusception as presentation of a primary lung carcinoma: a case report. Acta Gastroenterol Latinoam. 42:50–52. 2012.(In Chinese). PubMed/NCBI
46	Cedres S, Mulet-Margalef N, Montero MA, Martinez P, Martinez A and Felip E: Rectal metastases from squamous cell carcinoma: A case report and review of the literature. Case Rep Med. 2012:9475242012. View Article : Google Scholar : PubMed/NCBI
47	Lee PC, Lo C, Lin MT, Liang JT and Lin BR: Role of surgical intervention in managing gastrointestinal metastases from lung cancer. World J Gastroenterol. 17:4314–4320. 2011. View Article : Google Scholar : PubMed/NCBI
48	Fujiwara A, Okami J, Tokunaga T, Maeda J, Higashiyama M and Kodama K: Surgical treatment for gastrointestinal metastasis of non-small-cell lung cancer after pulmonary resection. Gen Thorac Cardiovasc Surg. 59:748–752. 2011. View Article : Google Scholar : PubMed/NCBI
49	Salemis NS, Nikou E, Liatsos C, Gakis C, Karagkiouzis G and Gourgiotis S: Small bowel perforation secondary to metastatic non-small cell lung cancer. A rare entity with a dismal prognosis. J Gastrointest Cancer. 43:391–395. 2012. View Article : Google Scholar : PubMed/NCBI
50	Yamada H, Akahane T, Horiuchi A, Shimada R, Shibuya H, Hayama T, Nozawa K, Ishihara S, Matsuda K and Watanabe T: A case of lung squamous cell carcinoma with metastases to the duodenum and small intestine. Int Surg. 96:176–181. 2011. View Article : Google Scholar : PubMed/NCBI
51	Ceretti AP, Goi G, Barabino M, De Nicola E, Strada D, Bislenghi G and Opocher E: Colonic metastasis from primary carcinoma of the lung. Case report. Ann Ital Chir. 82:229–232. 2011.(In Italian). PubMed/NCBI
52	Bugiantella W, Cavazzoni E, Graziosi L, Valiani S, Franceschini MS and Donini A: Small bowel metastasis from lung cancer: A possible cause of acute abdomen. Case report and literature review. G Chir. 32:120–122. 2011.PubMed/NCBI
53	Lin HC, Yu CP, Lin HA and Lee HS: A case of lung cancer metastasized to the gastrointestinal anastomosis site where the primary gastric cancer was resected 17 years ago. Lung Cancer. 72:255–257. 2011. View Article : Google Scholar : PubMed/NCBI
54	Azevedo CR, Cezana L, Moraes ES, Begnami MD, Junior Paiva TF, Dettino AL and Fanelli MF: Synchronous thyroid and colon metastases from epidermoid carcinoma of the lung: Case report. Sao Paulo Med J. 128:371–374. 2010. View Article : Google Scholar : PubMed/NCBI
55	Trouillet N, Robert B, Charfi S, Bartoli E, Joly JP and Chatelain D: Gastric metastases. An endoscopic series of ten cases. Gastroenterol Clin Biol. 34:305–309. 2010. View Article : Google Scholar : PubMed/NCBI
56	Guerin E, Gilbert O and Dequanter D: Acute abdomen: A rare presentation of lung cancer metastasis. Case Rep Med. 2009:9038972009. View Article : Google Scholar : PubMed/NCBI
57	Koch B, Tannapfel A, Vieth M and Grun R: Gastric metastasis from small cell lung cancer. Pneumologie. 63:585–587. 2009.(In German). View Article : Google Scholar : PubMed/NCBI
58	Yun IS, Lee JY, Lee JS, Lee JY, Byun JM, Kim EJ, Park JY and Park JK: Jejunal intussusception with gastrointestinal bleeding caused by metastatic lung cancer. Korean J Gastroenterol. 51:377–380. 2008.(In Koren). PubMed/NCBI
59	Aokage K, Yoshida J, Ishii G, Takahashi S, Sugito M, Nishimura M, Ochiai A and Nagai K: Long-term survival in two cases of resected gastric metastasis of pulmonary pleomorphic carcinoma. J Thorac Oncol. 3:796–799. 2008. View Article : Google Scholar : PubMed/NCBI
60	Kim MS, Kook EH, Ahn SH, Jeon SY, Yoon JH, Han MS, Kim CH and Lee JC: Gastrointestinal metastasis of lung cancer with special emphasis on a long-term survivor after operation. J Cancer Res Clin Oncol. 135:297–301. 2009. View Article : Google Scholar : PubMed/NCBI
61	Goh BK, Yeo AW, Koong HN, Ooi LL and Wong WK: Laparotomy for acute complications of gastrointestinal metastases from lung cancer: Is it a worthwhile or futile effort? Surg Today. 37:370–374. 2007. View Article : Google Scholar : PubMed/NCBI
62	Kostakou C, Khaldi L, Flossos A, Kapsoritakis AN and Potamianos SP: Melena: A rare complication of duodenal metastases from primary carcinoma of the lung. World J Gastroenterol. 13:1282–1285. 2007. View Article : Google Scholar : PubMed/NCBI
63	Ohashi K, Kiura K, Takigawa N, Mizushima T, Ino H, Tabata M, Ueoka H and Tanimoto M: Successful treatment of a patient with gastric and duodenal metastases from large cell carcinoma of the lung with carboplatin and gemcitabine. Anticancer Res. 26:4695–4696. 2006.PubMed/NCBI
64	Karamouzis MV, Linardou H, Papadopoulos G, Bousboukea E, Kanaloupiti D, Bitza M, Spourlis N and Bafaloukos D: Gastrointestinal solitary metastases from squamous cell lung cancer. Lung Cancer. 55:251–252. 2007. View Article : Google Scholar : PubMed/NCBI
65	Kanemoto K, Kurishima K, Ishikawa H, Shiotani S, Satoh H and Ohtsuka M: Small intestinal metastasis from small cell lung cancer. Intern Med. 45:967–970. 2006. View Article : Google Scholar : PubMed/NCBI
66	Casella G, Di Bella C, Cambareri AR, Buda CA, Corti G, Magri F, Crippa S and Baldini V: Gastric metastasis by lung small cell carcinoma. World J Gastroenterol. 12:4096–4097. 2006. View Article : Google Scholar : PubMed/NCBI
67	Altintas E, Sezgin O, Uyar B and Polat A: Acute upper gastrointestinal bleeding due to metastatic lung cancer: An unusual case. Yonsei Med J. 47:276–277. 2006. View Article : Google Scholar : PubMed/NCBI
68	Miyazaki K, Satoh H and Sekizawa K: Metastasis to appendix from lung adenocarcinoma. Int J Gastrointest Cancer. 36:59–60. 2005. View Article : Google Scholar : PubMed/NCBI
69	Garwood RA, Sawyer MD, Ledesma EJ, Foley E and Claridge JA: A case and review of bowel perforation secondary to metastatic lung cancer. Am Surg. 71:110–116. 2005.PubMed/NCBI
70	Morgan MW, Sigel B and Wolcott MW: Perforation of a metastatic carcinoma of the jejunum after cancer chemotherapy. Surgery. 49:687–689. 1961.PubMed/NCBI
71	Tillotson PM and Douglas RG Jr: Metastatic tumor of the small intestine. Three cases presenting unusual clinical and roentgenographic findings. Am J Roentgenol Radium Ther Nucl Med. 88:702–706. 1962.PubMed/NCBI
72	Hayashi K, Masuoka S and Kitade F: A case report of perforation of intestinal metastasis of lung cancer. Nihon Geka Hokan. 34:816–819. 1965.(In Japanese). PubMed/NCBI
73	Wootton DG, Morgan SC and Hughes RK: Perforation of a metastatic bronchogenic carcinoma to the jejunum. Ann Thorac Surg. 3:57–59. 1967. View Article : Google Scholar : PubMed/NCBI
74	Wellmann KF, Chafiian Y and Edelman E: Small bowel perforation from solitary metastasis of clinically undetected pulmonary giant cell carcinoma. Am J Gastroenterol. 51:145–150. 1969.PubMed/NCBI
75	Midell AI and Lochman DJ: An unusual metastatic manifestation of a primary bronchogenic carcinoma. Cancer. 30:806–809. 1972. View Article : Google Scholar : PubMed/NCBI
76	Inalsingh CH, Hazra T and Prempree T: Unusual metastases from carcinoma of the lung. J Can Assoc Radiol. 25:242–244. 1974.PubMed/NCBI
77	Ramanathan T, Skene-Smith H, Singh D and Sivanesan S: Small intestinal perforation due to secondaries from Bronchogenic carcinoma. Br J Dis Chest. 70:121–124. 1976. View Article : Google Scholar : PubMed/NCBI
78	Winchester DP, Merrill JR, Victor TA and Scanlon EF: Small bowel perforation secondary to metastatic carcinoma of the lung. Cancer. 40:410–415. 1977. View Article : Google Scholar : PubMed/NCBI
79	Ejeckam GC, Abele R, Thomas J and Heringer R: Abdominal crisis due to metastasizing lung carcinoma to the small bowel. Can J Surg. 22:351–353. 1979.PubMed/NCBI
80	Sternberg A, Giler S, Segal I, Shmuter Z and Kott I: Small bowel perforation as the presenting symptom of squamous cell carcinoma of the lung. Clin Oncol. 6:181–186. 1980.PubMed/NCBI
81	Leidich RB and Rudolf LE: Small bowel perforation secondary to metastatic lung carcinoma. Ann Surg. 193:67–69. 1981. View Article : Google Scholar : PubMed/NCBI
82	Rosencrans DL: Small bowel perforation caused by metastatic lung carcinoma. Ann Surg. 197:1201983.PubMed/NCBI
83	Quero Hernandez J, Tabernero Zubieta J, Martin Moreno A, Morales Caballero T, de la Higuera Torres-Puchol J, Parra Miras F and de la Higuera Rojas J: Pulmonary large-cell carcinoma with multiple metastases in the small intestine. Rev Clin Esp. 165:285–286. 1982.PubMed/NCBI
84	Catrambone G, Pesce L, Mazza M and Iurilli L: Perforation of the small intestine secondary to metastasis of pulmonary carcinoma. Minerva Chir. 38:55–59. 1983.PubMed/NCBI
85	Nicolosi A, Paderi R, Onnis P and Cafini D: Ileal perforation caused by metastasis of bronchogenic carcinoma. Minerva Chir. 40:567–570. 1985.PubMed/NCBI
86	Quayle AR, Holt S and Clark RG: Jejunal perforation secondary to metastatic bronchogenic carcinoma. Postgrad Med J. 61:163–165. 1985. View Article : Google Scholar : PubMed/NCBI
87	Vesth N, Jensen KH and Karkov J: Perforating small intestinal metastasis from a primary lung tumor. Ugeskr Laeger. 147:34921985.PubMed/NCBI
88	McNeill PM, Wagman LD and Neifeld JP: Small bowel metastases from primary carcinoma of the lung. Cancer. 59:1486–1489. 1987. View Article : Google Scholar : PubMed/NCBI
89	Pang JA and King WK: Bowel haemorrhage and perforation from metastatic lung cancer. Report of three cases and a review of the literature. Aust NZJ Surg. 57:779–783. 1987. View Article : Google Scholar
90	Cavenaile JC, Blairon J and Limbosch JM: Jejunal perforation indicating the metastatic extension of a bronchial neoplasm. Acta Chir Belg. 88:155–157. 1988.PubMed/NCBI
91	Hwang GS, Yeh PF, Lee YC, Perng RP and Li WY: Small bowel perforation secondary to metastatic carcinoma of lung. Zhonghua Yi Xue Za Zhi (Taipei). 41:159–164. 1988.(In Chinese). PubMed/NCBI
92	Koury HI and Kenady D: Perforation of a metastatic lung adenocarcinoma of the jejunum. Am J Gastroenterol. 83:462–463. 1988.PubMed/NCBI
93	Shatikhin VA, Vasil'ev AV and Bychkov MB: Metastasis of lung cancer to the small intestine with its perforation. Klin Med (Mosk). 66:135–136. 1988.PubMed/NCBI
94	Shirani J and Brackett JW: Lung cancer presenting as small bowel perforation. Conn Med. 53:455–456. 1989.PubMed/NCBI
95	Joyce WP, Huddy SP, Corbishley C and Wright NL: Small bowel complications of metastatic lung carcinoma. Ir J Med Sci. 159:149–150. 1990. View Article : Google Scholar : PubMed/NCBI
96	Woods JM IV and Koretz MJ: Emergency abdominal surgery for complications of metastatic lung carcinoma. Arch Surg. 125:583–585. 1990. View Article : Google Scholar : PubMed/NCBI
97	Nakano Y, Kamimori T, Shoji S, Taruya E and Tanaka I: A case of jejunal metastasis from pulmonary adenocarcinoma occurring as perforative peritonitis. Nihon Kyobu Shikkan Gakkai Zasshi. 29:649–653. 1991.(In Japanese). PubMed/NCBI
98	Yasunaga A, Shibata O, Sasaki T, Tohara K, Hadama T, Uchida Y, Yasunaga T and Adachi Y: A case of perforation of the metastatic site of lung carcinoma in the small bowel. Kyobu Geka. 44:596–599. 1991.(In Japanese). PubMed/NCBI
99	Beluffi L, Agostini M, Ruck F, Valenghi D, Morotti L and Marsetti M: Peritonitis caused by jejunal perforation resulting from metastasis of pulmonary carcinoma. Minerva Chir. 47:1023–1026. 1992.(In Italian). PubMed/NCBI
100	Gitt SM, Flint P, Fredell CH and Schmitz GL: Bowel perforation due to metastatic lung cancer. J Surg Oncol. 51:287–291. 1992. View Article : Google Scholar : PubMed/NCBI
101	Ryo H, Sakai H, Ikeda T, Hibino S, Goto I, Yoneda S and Noguchi Y: Gastrointestinal metastasis from lung cancer. Nihon Kyobu Shikkan Gakkai Zasshi. 34:968–972. 1996.(In Japanese). PubMed/NCBI
102	Cossavella D, Paino O, Luc Realis A, Clerico G, Catania S, Pozzo M and Trompetto M: A rare form of intestinal perforation: adenocarcinoma of the ileum. Presentation of a clinical case. Minerva Chir. 53:431–433. 1998.(In Italian). PubMed/NCBI
103	Fischer M, Papp J, Kulka J, Zsiray M, Kempler P and Szalay F: Upper gastrointestinal bleeding and intestinal perforation due to multiple duodenojejunal metastases from a silent bronchogenic adenosquamous carcinoma. Endoscopy. 30:S791998. View Article : Google Scholar : PubMed/NCBI
104	Shiraishi Y, Nakajima Y, Katsuragi N, Hanaoka T, Konno H and Tanaka S: Metastatic lung tumor: report of two cases. Kyobu Geka. 56:47–50. 2003.PubMed/NCBI
105	Yokota T, Yamada Y, Sakata N, Kikuchi S, Kunii Y, Tezuka F, Suzuki H and Yamauchi H: Emergency abdominal surgery for small bowel perforation secondary to metastatic lung cancer. Tohoku J Exp Med. 188:265–270. 1999. View Article : Google Scholar : PubMed/NCBI
106	Ise N, Kotanagi H, Morii M, Yasui O, Ito M, Koyama K and Sageshima M: Small bowel perforation caused by metastasis from an extra-abdominal malignancy: Report of three cases. Surg Today. 31:358–362. 2001. View Article : Google Scholar : PubMed/NCBI
107	Polak M, Kupryjańczyk J and Rell KW: A rare case of colonic perforation in a sole site of latent lung cancer metastasis. Pol Tyg Lek. 45:179–181. 1990.(In Polish). PubMed/NCBI
108	Rahman R, Bernstein Z, Vaickus L, Penetrante R, Arbuck S, Kopec I, Vesper D, Douglass HO Jr and Foon KA: Unusual gastrointestinal complications of interleukin-2 therapy. J Immunother (1991). 10:221–225. 1991. View Article : Google Scholar : PubMed/NCBI
109	Fletcher MS: Gastric perforation secondary to metastatic carcinoma of the lung: a case report. Cancer. 46:1879–1882. 1980. View Article : Google Scholar : PubMed/NCBI
110	Schmidt G, Börsch G, von Liebe S and Böhm E: Gastric perforation secondary to metastatic bronchogenic carcinoma. Hepatogastroenterology. 32:103–105. 1985.PubMed/NCBI
111	Opanasenko NS: Gastric perforation into the left pleural cavity after pleuropulmonectomy for pulmonary cancer. Klin Khir. 56–57. 2000.(In Russian). PubMed/NCBI
112	Suzaki N, Hiraki A, Ueoka H, Aoe M, Takigawa N, Kishino T, Kiura K, Kanehiro A, Tanimoto M and Harada M: Gastric perforation due to metastasis from adenocarcinoma of the lung. Anticancer Res. 22:1209–1212. 2002.PubMed/NCBI
113	Sanli Y, Adalet I, Turkmen C, Kapran Y, Tamam M and Cantez S: Small bowel metastases from primary carcinoma of the lung: Presenting with gastrointestinal hemorrhage. Ann Nucl Med. 19:161–163. 2005. View Article : Google Scholar : PubMed/NCBI
114	Tomas D, Ledinsky M, Belicza M and Kruslin B: Multiple metastases to the small bowel from large cell bronchial carcinomas. World J Gastroenterol. 11:1399–1402. 2005. View Article : Google Scholar : PubMed/NCBI
115	Misra SP, Dwivedi M, Misra V, Dharmani S and Gupta M: Duodenal metastases from squamous cell carcinoma of the lung: Endoscopic management of bleeding and biliary and duodenal obstruction. Indian J Gastroenterol. 23:185–186. 2004.PubMed/NCBI
116	Katsinelos P, Paroutoglou G, Beltsis A, Pilpilidis I, Papaziogas B, Mimidis K and Tsolkas P: Hematemesis as a presenting symptom of lung cancer with synchronous metastases to the esophagus and stomach. A case report. Rom J Gastroenterol. 13:251–253. 2004.PubMed/NCBI
117	Kobayashi O, Murakami H, Yoshida T, Cho H, Yoshikawa T, Tsuburaya A, Sairenji M, Motohashi H, Sugiyama Y and Kameda Y: Clinical diagnosis of metastatic gastric tumors: Clinicopathologic findings and prognosis of nine patients in a single cancer center. World J Surg. 28:548–551. 2004. View Article : Google Scholar : PubMed/NCBI
118	Capasso L, Iarrobino G, D'Ambrosio R, Carfora E, Ventriglia R and Borsi E: Surgical complications for gastric and small bowel metastases due to primary lung carcinoma. Minerva Chir. 59:397–403. 2004.PubMed/NCBI
119	Renault PA, Arotçarena R, Calès V, Lippa A, Benichou M, Laurent P and Laborde Y: Metastatic obstruction of the small bowel revealing or complicating squamous-cell lung cancer. Two cases and a review of the literature. Rev Pneumol Clin. 59:161–165. 2003.PubMed/NCBI
120	Yamamoto M, Matsuzaki K, Kusumoto H, Uchida H, Mine H, Kabashima A, Maehara Y and Sugimachi K: Gastric metastasis from lung carcinoma. Case report. Hepatogastroenterology. 49:363–365. 2002.PubMed/NCBI
121	Ito Y, Suzuki M, Oyamada Y, Kou H, Takeshita K, Asano K and Yamaguchi K: A case of relapsed small cell lung cancer recognized by simple metastasis to the duodenum. Nihon Kokyuki Gakkai Zasshi. 39:30–34. 2001.(In Japanese). PubMed/NCBI
122	Fukata T, Fukino S, Hayashi E, Okada K, Tamai N and Nakashima H: A case of G-CSF-producing large cell carcinoma of the lung with gastric metastasis. Kyobu Geka. 53:798–803. 2000.(In Japanese). PubMed/NCBI
123	Berger A, Cellier C, Daniel C, Kron C, Riquet M, Barbier JP, Cugnenc PH and Landi B: Small bowel metastases from primary carcinoma of the lung: clinical findings and outcome. Am J Gastroenterol. 94:1884–1887. 1999. View Article : Google Scholar : PubMed/NCBI
124	Centeno Cortés C, Clavero Borau MJ, Rubiales Sanz A and Martín López-Lara F: Intestinal bleeding in disseminated non-small cell lung cancer. Lung Cancer. 18:101–105. 1997. View Article : Google Scholar : PubMed/NCBI
125	Akahoshi K, Chijiiwa Y, Hirota I, Ohogushi O, Motomatsu T, Nawata H and Sasaki I: Metastatic large-cell lung carcinoma presenting as gastrointestinal hemorrhage. Acta Gastroenterol Belg. 59:217–219. 1996.PubMed/NCBI
126	Raijman I: Duodenal metastases from lung cancer. Endoscopy. 26:752–753. 1994. View Article : Google Scholar : PubMed/NCBI
127	Gateley CA, Lewis WG and Sturdy DE: Massive lower gastrointestinal haemorrhage secondary to metastatic squamous cell carcinoma of the lung. Br J Clin Pract. 47:276–277. 1993.PubMed/NCBI
128	Maeda J, Miyake M, Tokita K, Iwahashi N, Nakano T, Tamura S, Hada T and Higashino K: Small cell lung cancer with extensive cutaneous and gastric metastases. Intern Med. 31:1325–1328. 1992. View Article : Google Scholar : PubMed/NCBI
129	Mosier DM, Bloch RS, Cunningham PL and Dorman SA: Small bowel metastases from primary lung carcinoma: A rarity waiting to be found? Am Surg. 58:677–682. 1992.PubMed/NCBI
130	Park SW, Cho HJ, Choo WS, Chung KS, Kim HY, Yoo JY, Kim JS and Shin HS: A case of intestinal hemorrhage due to small intestinal metastases from primary lung cancer. Korean J Intern Med. 6:79–84. 1991. View Article : Google Scholar : PubMed/NCBI
131	Spedini C, Lombardi C and Buffoli F: Multiple mucosal gastrointestinal metastases from primary asymptomatic bronchogenic carcinoma. Recenti Prog Med. 81:442–444. 1990.PubMed/NCBI
132	Ono H, Okabe M, Kimura T, Kawakami M, Nakamura K, Danjo Y, Takasugi H and Nishihara H: Colonic metastasis from primary carcinoma of the lung: Report of a case and review of Japanese literature. Clin J Gastroenterol. 2:89–95. 2009. View Article : Google Scholar : PubMed/NCBI
133	Stinchcombe TE, Socinski MA, Gangarosa LM and Khandani AH: Lung cancer presenting with a solitary colon metastasis detected on positron emission tomography scan. J Clin Oncol. 24:4939–4940. 2006. View Article : Google Scholar : PubMed/NCBI
134	Travis WD, Brambilla E, Nicholson AG, Yatabe Y, Austin JH, Beasley MB, Chirieac LR, Dacic S, Duhig E, Flieder DB, et al: The 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol. 10:1243–1260. 2015. View Article : Google Scholar : PubMed/NCBI
135	Edge S, Byrd D, Compton C, Fritz A, Greene F and Trotti A: AJCC Cancer Stageing Manual. Springer; New York: 2010
136	Kim CH, Lee YC, Hung RJ, McNallan SR, Cote ML, Lim WY, Chang SC, Kim JH, Ugolini D, Chen Y, et al: Exposure to secondhand tobacco smoke and lung cancer by histological type: A pooled analysis of the International Lung Cancer Consortium (ILCCO). Int J Cancer. 135:1918–1930. 2014. View Article : Google Scholar : PubMed/NCBI
137	Cox D and Oakes N: Analysis of Survival Data. Chapman and Hall; New York: 1984
138	Guo Z, Han B and Wang Y: The status of diagnosis and therapy for gastrointestinal metastasis from primary lung cancer. Zhongguo Fei Ai Za Zhi. 14:69–71. 2011.(In Chinese). PubMed/NCBI
139	Hillenbrand A, Sträter J and Henne-Bruns D: Frequency, symptoms and outcome of intestinal metastases of bronchopulmonary cancer. Case report and review of the literature. Int Semin Surg Oncol. 2:132005. View Article : Google Scholar : PubMed/NCBI
140	Yuen JS, Chow PK and Ahmed Q: Metastatic lung cancer causing bowel perforations: Spontaneous or chemotherapy-related? ANZ J Surg. 72:245–246. 2002. View Article : Google Scholar : PubMed/NCBI
141	Kim SY, Ha HK, Park SW, Kang J, Kim KW, Lee SS, Park SH and Kim AY: Gastrointestinal metastasis from primary lung cancer: CT findings and clinicopathologic features. AJR Am J Roentgenol. 193:W197–W201. 2009. View Article : Google Scholar : PubMed/NCBI
142	Di JZ, Peng JY and Wang ZG: Prevalence, clinicopathological characteristics, treatment, and prognosis of intestinal metastasis of primary lung cancer: A comprehensive review. Surg Oncol. 23:72–80. 2014. View Article : Google Scholar : PubMed/NCBI
143	Israel O, Yefremov N, Bar-Shalom R, Kagana O, Frenkel A, Keidar Z and Fischer D: PET/CT detection of unexpected gastrointestinal foci of 18F-FDG uptake: Incidence, localization patterns and clinical significance. J Nucl Med. 46:758–762. 2005.PubMed/NCBI
144	Kim MS, Cheon GJ, Lim SM, Kim CH and Lee JC: F-18 FDG PET-CT imaging of intestinal metastasis from primary lung cancer. Clin Nucl Med. 33:870–871. 2008. View Article : Google Scholar : PubMed/NCBI
145	Kini S, Kapadia RM and Amarapurkar A: Intussusception due to intestinal metastasis from lung cancer. Indian J Pathol Microbiol. 53:141–143. 2010. View Article : Google Scholar : PubMed/NCBI