J Gastrointest Canc DOI 10.1007/s12029-013-9567-6
CASE REPORT
Solitary Metastasis to the Small Bowel from Primary Adenocarcinoma of the Lung Nina Thakkar Rivera & Heather Katz & Geoffrey Weisbaum & Ralph Guarneri & Natasha Bray & Delia Constanza-Guaqueta
# Springer Science+Business Media New York 2013
Introduction
Case Report
More deaths are attributable to lung cancer than any other cancer [1]. At the time of diagnosis, 85 % of patients with lung cancer are found to have metastatic disease [1]. Metastasis from primary adenocarcinoma of the lung is most commonly found in the liver, bones, brain, and adrenal glands [2, 3] (Fig. 1). Adenocarcinoma of the lung with solitary metastasis to the small bowel is rare [4]. Multiple autopsy studies have found a small percentage of small bowel metastasis from primary lung cancer, but these coincided with metastasis to other common sites as well [3, 5–8]. Few case reports have described gastrointestinal metastasis from primary non-small cell lung carcinoma (NSCLC) [9–11]. In this case report, we describe the first known report of primary adenocarcinoma of the lung with solitary metastasis to the small bowel following presentation with gastrointestinal symptoms.
A 61-year-old female presented to the emergency department secondary to worsening epigastric pain over 2 months with associated nausea, vomiting, and reduced appetite of 3-day duration. The patient’s past medical history was significant for hypertension, coronary artery disease, and hyperlipidemia. She had no history of preventative health maintenance exams, including colonoscopy. She was a former smoker with a 15pack-year history, which she quit 2 years prior to presentation. Family history was significant for her father dying in his seventies secondary to liver cancer. Her vital signs, physical exam, and laboratory studies were within normal limits. Chest X-ray on admission uncovered a 3-cm mass in the right upper lobe (Fig. 2a). Subsequent chest computed tomography (CT) revealed a 2.2×2.8-cm right upper lobe lung mass with a 2.7×1.9-cm right paratracheal mass and an 8-cm superior mediastinal node (Fig. 2b, c). Abdomen and pelvis CT demonstrated a 3-cm focal area of moderate wall thickening in the proximal small bowel within the left mid abdomen (Fig. 2d). CT-guided biopsy of the right upper lobe lung mass revealed an infiltrating adenocarcinoma with extensive necrosis and immunostains positive for thyroid transcription factor 1 (TTF1), p63, cytokeratin 7 (CK7), and Napsin A and negative for cytokeratin 20 (CK20) (Fig. 3). Exploratory laparotomy was performed with small bowel resection of three tumor sites. Pathology indicated poorly differentiated adenocarcinoma consistent with metastatic lung adenocarcinoma. Immunostains were positive for TTF-1, CK7, and Napsin A and negative for CK20 (Fig. 3). The patient underwent a brain magnetic resonance imaging (MRI) and whole-body positron emission tomography (PET)/ CT scan as part of the metastatic workup. Brain MRI showed no evidence of metastatic cerebral disease. Follow-up PET/CT scan showed abnormal activity in the known lung mass and
N. T. Rivera (*) : H. Katz : N. Bray Department of Internal Medicine, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA e-mail: [email protected] G. Weisbaum Department of Pathology, Anatomic and Clinical, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA R. Guarneri Department of General Surgery, Trauma, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA D. Constanza-Guaqueta Department of Hematology/Oncology, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA
J Gastrointest Canc
As per recommendations by the National Comprehensive Cancer Network, to aid in the selection of chemotherapy, tissue was sent for staining with EGFR, ALK, and ROS [12]. Treatment with cisplatin, pemetrexed, and bevacizumab was initiated due to the negative stain results. Five months following diagnosis, she is living and still undergoing chemotherapy.
Discussion
Fig. 1 Primary lung cancer: sites of metastasis. Regional lymph node (LN) metastasis ranges from 72 to 84 %. Liver metastasis ranges from 33 to 47 %. Bone metastasis ranges from 21 to 34 %. Brain metastasis ranges from 16 to 32 %. Adrenal metastasis ranges from 20 to 29 %. Heart metastasis ranges from 12 to 29 %. Gastrointestinal metastasis ranges from 0.5 to 2 % [2, 3]
three sites of adenopathy, specifically the left supraclavicular space at 1.5 cm, the precarinal region at 4.5 cm, and the posterior mediastinum at 1.5 cm (not shown). Fig. 2 Chest X-ray and CT of the chest, abdomen, and pelvis. a Chest X-ray demonstrates a 3.5cm mass in the right upper lobe. b CT of the chest with IV contrast shows a 3.18×2.84-cm mass in the right upper lobe. c CT of the chest with IV contrast showed an 8.1-cm superior mediastinal node. A 2.7×1.9-cm right paratracheal mass was also seen (not shown). d CT of the abdomen and pelvis with IV and PO contrast demonstrated a 3-cm focal area of thickening in the proximal small bowel within the left mid abdomen (arrow). Multiple hepatic cysts and a small amount of free fluid in the pelvis were also found (not shown)
Gastrointestinal metastasis from primary NSCLC is rare [4]. Several autopsy studies have been performed to examine the incidence and significance of this finding. Stenbygaard et al. concluded that gastrointestinal metastases were associated with widespread metastatic disease [3]. Similarly, McNeill et al. found that all patients examined with small bowel metastasis had at least one other metastatic site, with an average of 4.8 sites [6]. Further, Berger et al. concluded that surgical resection of gastrointestinal metastatic lesions did not increase survival but was of palliative benefit only [5, 13]. Independent of underlying histology, squamous cell versus
J Gastrointest Canc Table 1 Histopathology
1° Pulmonary adenocarcinoma Metastasis from colorectum Metastasis from thyroid Squamous cell carcinoma Current patient: right upper lobe Current patient: small intestine
TTF-1
CK7
CK20
CDX2
+ − + − + +
+ −
− +
+
p63
Napsin
TG −
+
+ + +
− −
+ +
+ +
Primary adenocarcinoma of the lung is positive for TTF-1, while metastatic adenocarcinoma to the lung is virtually always negative for TTF-1. The exception is metastatic thyroid malignancies in which case thyroglobulin is also positive. Adenocarcinoma metastasis from the gastrointestinal tract is negative for TTF-1 and generally positive for CK20 and CDX2. Napsin is a useful adjunct to TTF-1 as it is commonly found in greater than 80 % of lung adenocarcinomas [12]. The symbol “+” indicates positive staining. The symbol “−” indicates negative staining
adenocarcinoma, primary NSCLC displayed no preference for gastrointestinal metastasis. An extensive literature review using Medline and PubMed confirmed the rarity of this finding. Okazaki et al. described a case report with gastric metastasis from primary lung Fig. 3 Pathology of right upper lung and small bowel tissues. Lung tissue stained with a H & E showing adenocarcinoma, c CK7, and e TTF-1. Small bowel tissue stained with b H & E showing tumor invasion into the submucosa, d CK7, and f TTF-1
adenocarcinoma. Despite resection of the lung mass in combination with chemotherapy, the disease subsequently metastasized to the brain and bone. The patient died within 1 year of diagnosis of gastric metastasis [10]. Katsenos et al. reported a primary lung adenocarcinoma with liver lesion and metastasis
J Gastrointest Canc
to the stomach. After 3 months of chemotherapy, metastasis to the brain and bone was found. The patient died within 10 months of diagnosis [9]. Based on the autopsy studies, gastrointestinal metastasis was most commonly found in the presence of widespread metastatic disease [3, 5–8]. The few published case reports further indicated that patients with NSCLC presenting with gastrointestinal involvement should be considered to represent advanced or end-stage disease [14]. One study concluded that the median duration from lung cancer diagnosis to gastrointestinal metastasis was 3 months. Furthermore, the average time from diagnosis of gastrointestinal metastasis to death was 2.8 months. There was no difference in the survival in patients with initial diagnosis of stages I–III versus those with stage IV. Therefore, gastrointestinal metastasis from lung cancer has been shown to indicate a poor prognosis [13, 15]. Currently, as this is the first case to be reported, it is unclear what the effect of solitary metastasis to the gastrointestinal tract entails with regard to both management and prognosis. Many studies, both pre- and postmortem, have indicated gastrointestinal metastasis to be associated with a poorer prognosis. However, this was in the setting of multiple metastatic sites; and therefore, they cannot adequately represent the path of solitary gastrointestinal metastasis from primary lung adenocarcinoma. Because there have been no cases described, this finding of having solitary gastrointestinal metastasis from primary lung adenocarcinoma cannot yet alter the current algorithm of treatment. Still, it provokes the question of both classification and treatment selection. Should this case be treated as stage M1b, guidelines recommend removal of the solitary site of metastasis followed by chemotherapy. This algorithm was based on studies regarding brain and adrenal glands [1]. However, as solitary gastrointestinal metastasis has never been described before, the guidelines cannot necessarily be applied in this case. This case presented the question of whether or not treating solitary gastrointestinal metastasis as M1b and proceeding with surgical removal of the solitary metastatic site followed by chemotherapy can be advantageous and result in a better prognosis versus the alternative option of defining it as stage IV and treating solely with chemotherapy. Furthermore, as this site of solitary metastasis is so rare, can metastectomy be considered independent of the specific site, and will that change the outcome. These questions cannot be answered without adequate case reporting. This is the first reported case; therefore, there is no clear path. In this case, we report the solitary metastasis of primary pulmonary adenocarcinoma to the small bowel. This was discovered incidentally with the presentation of gastrointestinal symptoms. Pathology and the use of
immunostains confirmed that this was in fact a primary adenocarcinoma of the lung found metastasized to the small bowel rather than a second primary adenocarcinoma (Table 1, Fig. 3). Consistent with primary lung adenocarcinoma, the biopsied tissues of both the lung and small bowel tumors stained positive for TTF-1 and CK7, and negative for CK20 (Table 1, Fig. 3). Currently, she is living and undergoing chemotherapy with cisplatin, pemetrexed, and bevacizumab. In summary, this is the first known report of a solitary small bowel metastasis from primary adenocarcinoma of the lung. The course of this patient’s disease and care will be a useful adjunct to the current literature for determining treatment and prognosis in similar cases. Acknowledgments The authors thank the North Broward Hospital District. Conflict of Interest The authors declare that they have no conflict of interest.
References 1. American Cancer Society. Cancer facts and figures. Atlanta: American Cancer Society; 2013. 2. Steinhart AH, Cohen LB, Hegele R, Saibil FG. Upper gastrointestinal bleeding due to superior mesenteric artery to duodenum fistula: rare complication of metastatic lung carcinoma. Am J Gastroenterol. 1991;86(6):771–4. 3. Stenbygaard LE, Sorensen JB, Larsen H, Dombernowsky P. Metastatic pattern in non-resectable non-small cell lung cancer. Acta Oncol. 1999;38(8):993–8. 4. Mosier DM, Bloch RS, Cunningham PL, Dorman SA. Small bowel metastases from primary lung carcinoma: a rarity waiting to be found? Am Surg. 1992;58(11):677–82. 5. Berger A, Cellier C, Daniel C, Kron C, Riquet M, Barbier JP, et al. Small bowel metastases from primary carcinoma of the lung: clinical findings and outcome. Am J Gastroenterol. 1999;94(7):1884–7. doi: 10.1111/j.1572-0241.1999.01224.x. 6. McNeill PM, Wagman LD, Neifeld JP. Small bowel metastases from primary carcinoma of the lung. Cancer. 1987;59(8):1486–9. 7. Yang CJ, Hwang JJ, Kang WY, Chong IW, Wang TH, Sheu CC, et al. Gastro-intestinal metastasis of primary lung carcinoma: clinical presentations and outcome. Lung Cancer. 2006;54(3):319–23. doi:10. 1016/j.lungcan.2006.08.007. 8. Yoshimoto A, Kasahara K, Kawashima A. Gastrointestinal metastases from primary lung cancer. Eur J Cancer. 2006;42(18):3157–60. doi:10.1016/j.ejca.2006.08.030. 9. Katsenos S, Archondakis S. Solitary gastric metastasis from primary lung adenocarcinoma: a rare site of extra-thoracic metastatic disease. J Gastrointest Oncol. 2013;4(2):E11–5. doi:10.3978/j.issn.20786891.2012.057. 10. Okazaki R, Ohtani H, Takeda K, Sumikawa T, Yamasaki A, Matsumoto S, et al. Gastric metastasis by primary lung adenocarcinoma. World J Gastrointest Oncol. 2010;2(10):395–8. doi:10.4251/ wjgo.v2.i10.395. 11. Sileri P, D’Ugo S, Blanco Gdel V, Lolli E, Franceschilli L, Formica V, et al. Solitary metachronous gastric metastasis from pulmonary
J Gastrointest Canc adenocarcinoma: report of a case. Int J Surg Case Rep. 2012;3(8): 385–8. doi:10.1016/j.ijscr.2012.04.017. 12. National Comprehensive Cancer Network. Non-small cell lung cancer. Fort Washington: National Comprehensive Cancer Network; 2013. 13. Goh BK, Yeo AW, Koong HN, Ooi LL, Wong WK. Laparotomy for acute complications of gastrointestinal metastases from lung cancer: is it a worthwhile or futile effort? Surg Today. 2007;37(5):370–4. doi: 10.1007/s00595-006-3419-y.
14. Rossi G, Marchioni A, Romagnani E, Bertolini F, Longo L, Cavazza A, et al. Primary lung cancer presenting with gastrointestinal tract involvement: clinicopathologic and immunohistochemical features in a series of 18 consecutive cases. J Thoracic Oncol: Off Publ Int Assoc Study Lung Cancer. 2007;2(2):115–20. 15. Lee PC, Lo C, Lin MT, Liang JT, Lin BR. Role of surgical intervention in managing gastrointestinal metastases from lung cancer. World J Gastroenterol: WJG. 2011;17(38):4314–20. doi:10.3748/wjg.v17. i38.4314.
CASE REPORT
Solitary Metastasis to the Small Bowel from Primary Adenocarcinoma of the Lung Nina Thakkar Rivera & Heather Katz & Geoffrey Weisbaum & Ralph Guarneri & Natasha Bray & Delia Constanza-Guaqueta
# Springer Science+Business Media New York 2013
Introduction
Case Report
More deaths are attributable to lung cancer than any other cancer [1]. At the time of diagnosis, 85 % of patients with lung cancer are found to have metastatic disease [1]. Metastasis from primary adenocarcinoma of the lung is most commonly found in the liver, bones, brain, and adrenal glands [2, 3] (Fig. 1). Adenocarcinoma of the lung with solitary metastasis to the small bowel is rare [4]. Multiple autopsy studies have found a small percentage of small bowel metastasis from primary lung cancer, but these coincided with metastasis to other common sites as well [3, 5–8]. Few case reports have described gastrointestinal metastasis from primary non-small cell lung carcinoma (NSCLC) [9–11]. In this case report, we describe the first known report of primary adenocarcinoma of the lung with solitary metastasis to the small bowel following presentation with gastrointestinal symptoms.
A 61-year-old female presented to the emergency department secondary to worsening epigastric pain over 2 months with associated nausea, vomiting, and reduced appetite of 3-day duration. The patient’s past medical history was significant for hypertension, coronary artery disease, and hyperlipidemia. She had no history of preventative health maintenance exams, including colonoscopy. She was a former smoker with a 15pack-year history, which she quit 2 years prior to presentation. Family history was significant for her father dying in his seventies secondary to liver cancer. Her vital signs, physical exam, and laboratory studies were within normal limits. Chest X-ray on admission uncovered a 3-cm mass in the right upper lobe (Fig. 2a). Subsequent chest computed tomography (CT) revealed a 2.2×2.8-cm right upper lobe lung mass with a 2.7×1.9-cm right paratracheal mass and an 8-cm superior mediastinal node (Fig. 2b, c). Abdomen and pelvis CT demonstrated a 3-cm focal area of moderate wall thickening in the proximal small bowel within the left mid abdomen (Fig. 2d). CT-guided biopsy of the right upper lobe lung mass revealed an infiltrating adenocarcinoma with extensive necrosis and immunostains positive for thyroid transcription factor 1 (TTF1), p63, cytokeratin 7 (CK7), and Napsin A and negative for cytokeratin 20 (CK20) (Fig. 3). Exploratory laparotomy was performed with small bowel resection of three tumor sites. Pathology indicated poorly differentiated adenocarcinoma consistent with metastatic lung adenocarcinoma. Immunostains were positive for TTF-1, CK7, and Napsin A and negative for CK20 (Fig. 3). The patient underwent a brain magnetic resonance imaging (MRI) and whole-body positron emission tomography (PET)/ CT scan as part of the metastatic workup. Brain MRI showed no evidence of metastatic cerebral disease. Follow-up PET/CT scan showed abnormal activity in the known lung mass and
N. T. Rivera (*) : H. Katz : N. Bray Department of Internal Medicine, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA e-mail: [email protected] G. Weisbaum Department of Pathology, Anatomic and Clinical, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA R. Guarneri Department of General Surgery, Trauma, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA D. Constanza-Guaqueta Department of Hematology/Oncology, Broward Health Medical Center, 1600 South Andrews Avenue, Fort Lauderdale, FL 33316, USA
J Gastrointest Canc
As per recommendations by the National Comprehensive Cancer Network, to aid in the selection of chemotherapy, tissue was sent for staining with EGFR, ALK, and ROS [12]. Treatment with cisplatin, pemetrexed, and bevacizumab was initiated due to the negative stain results. Five months following diagnosis, she is living and still undergoing chemotherapy.
Discussion
Fig. 1 Primary lung cancer: sites of metastasis. Regional lymph node (LN) metastasis ranges from 72 to 84 %. Liver metastasis ranges from 33 to 47 %. Bone metastasis ranges from 21 to 34 %. Brain metastasis ranges from 16 to 32 %. Adrenal metastasis ranges from 20 to 29 %. Heart metastasis ranges from 12 to 29 %. Gastrointestinal metastasis ranges from 0.5 to 2 % [2, 3]
three sites of adenopathy, specifically the left supraclavicular space at 1.5 cm, the precarinal region at 4.5 cm, and the posterior mediastinum at 1.5 cm (not shown). Fig. 2 Chest X-ray and CT of the chest, abdomen, and pelvis. a Chest X-ray demonstrates a 3.5cm mass in the right upper lobe. b CT of the chest with IV contrast shows a 3.18×2.84-cm mass in the right upper lobe. c CT of the chest with IV contrast showed an 8.1-cm superior mediastinal node. A 2.7×1.9-cm right paratracheal mass was also seen (not shown). d CT of the abdomen and pelvis with IV and PO contrast demonstrated a 3-cm focal area of thickening in the proximal small bowel within the left mid abdomen (arrow). Multiple hepatic cysts and a small amount of free fluid in the pelvis were also found (not shown)
Gastrointestinal metastasis from primary NSCLC is rare [4]. Several autopsy studies have been performed to examine the incidence and significance of this finding. Stenbygaard et al. concluded that gastrointestinal metastases were associated with widespread metastatic disease [3]. Similarly, McNeill et al. found that all patients examined with small bowel metastasis had at least one other metastatic site, with an average of 4.8 sites [6]. Further, Berger et al. concluded that surgical resection of gastrointestinal metastatic lesions did not increase survival but was of palliative benefit only [5, 13]. Independent of underlying histology, squamous cell versus
J Gastrointest Canc Table 1 Histopathology
1° Pulmonary adenocarcinoma Metastasis from colorectum Metastasis from thyroid Squamous cell carcinoma Current patient: right upper lobe Current patient: small intestine
TTF-1
CK7
CK20
CDX2
+ − + − + +
+ −
− +
+
p63
Napsin
TG −
+
+ + +
− −
+ +
+ +
Primary adenocarcinoma of the lung is positive for TTF-1, while metastatic adenocarcinoma to the lung is virtually always negative for TTF-1. The exception is metastatic thyroid malignancies in which case thyroglobulin is also positive. Adenocarcinoma metastasis from the gastrointestinal tract is negative for TTF-1 and generally positive for CK20 and CDX2. Napsin is a useful adjunct to TTF-1 as it is commonly found in greater than 80 % of lung adenocarcinomas [12]. The symbol “+” indicates positive staining. The symbol “−” indicates negative staining
adenocarcinoma, primary NSCLC displayed no preference for gastrointestinal metastasis. An extensive literature review using Medline and PubMed confirmed the rarity of this finding. Okazaki et al. described a case report with gastric metastasis from primary lung Fig. 3 Pathology of right upper lung and small bowel tissues. Lung tissue stained with a H & E showing adenocarcinoma, c CK7, and e TTF-1. Small bowel tissue stained with b H & E showing tumor invasion into the submucosa, d CK7, and f TTF-1
adenocarcinoma. Despite resection of the lung mass in combination with chemotherapy, the disease subsequently metastasized to the brain and bone. The patient died within 1 year of diagnosis of gastric metastasis [10]. Katsenos et al. reported a primary lung adenocarcinoma with liver lesion and metastasis
J Gastrointest Canc
to the stomach. After 3 months of chemotherapy, metastasis to the brain and bone was found. The patient died within 10 months of diagnosis [9]. Based on the autopsy studies, gastrointestinal metastasis was most commonly found in the presence of widespread metastatic disease [3, 5–8]. The few published case reports further indicated that patients with NSCLC presenting with gastrointestinal involvement should be considered to represent advanced or end-stage disease [14]. One study concluded that the median duration from lung cancer diagnosis to gastrointestinal metastasis was 3 months. Furthermore, the average time from diagnosis of gastrointestinal metastasis to death was 2.8 months. There was no difference in the survival in patients with initial diagnosis of stages I–III versus those with stage IV. Therefore, gastrointestinal metastasis from lung cancer has been shown to indicate a poor prognosis [13, 15]. Currently, as this is the first case to be reported, it is unclear what the effect of solitary metastasis to the gastrointestinal tract entails with regard to both management and prognosis. Many studies, both pre- and postmortem, have indicated gastrointestinal metastasis to be associated with a poorer prognosis. However, this was in the setting of multiple metastatic sites; and therefore, they cannot adequately represent the path of solitary gastrointestinal metastasis from primary lung adenocarcinoma. Because there have been no cases described, this finding of having solitary gastrointestinal metastasis from primary lung adenocarcinoma cannot yet alter the current algorithm of treatment. Still, it provokes the question of both classification and treatment selection. Should this case be treated as stage M1b, guidelines recommend removal of the solitary site of metastasis followed by chemotherapy. This algorithm was based on studies regarding brain and adrenal glands [1]. However, as solitary gastrointestinal metastasis has never been described before, the guidelines cannot necessarily be applied in this case. This case presented the question of whether or not treating solitary gastrointestinal metastasis as M1b and proceeding with surgical removal of the solitary metastatic site followed by chemotherapy can be advantageous and result in a better prognosis versus the alternative option of defining it as stage IV and treating solely with chemotherapy. Furthermore, as this site of solitary metastasis is so rare, can metastectomy be considered independent of the specific site, and will that change the outcome. These questions cannot be answered without adequate case reporting. This is the first reported case; therefore, there is no clear path. In this case, we report the solitary metastasis of primary pulmonary adenocarcinoma to the small bowel. This was discovered incidentally with the presentation of gastrointestinal symptoms. Pathology and the use of
immunostains confirmed that this was in fact a primary adenocarcinoma of the lung found metastasized to the small bowel rather than a second primary adenocarcinoma (Table 1, Fig. 3). Consistent with primary lung adenocarcinoma, the biopsied tissues of both the lung and small bowel tumors stained positive for TTF-1 and CK7, and negative for CK20 (Table 1, Fig. 3). Currently, she is living and undergoing chemotherapy with cisplatin, pemetrexed, and bevacizumab. In summary, this is the first known report of a solitary small bowel metastasis from primary adenocarcinoma of the lung. The course of this patient’s disease and care will be a useful adjunct to the current literature for determining treatment and prognosis in similar cases. Acknowledgments The authors thank the North Broward Hospital District. Conflict of Interest The authors declare that they have no conflict of interest.
References 1. American Cancer Society. Cancer facts and figures. Atlanta: American Cancer Society; 2013. 2. Steinhart AH, Cohen LB, Hegele R, Saibil FG. Upper gastrointestinal bleeding due to superior mesenteric artery to duodenum fistula: rare complication of metastatic lung carcinoma. Am J Gastroenterol. 1991;86(6):771–4. 3. Stenbygaard LE, Sorensen JB, Larsen H, Dombernowsky P. Metastatic pattern in non-resectable non-small cell lung cancer. Acta Oncol. 1999;38(8):993–8. 4. Mosier DM, Bloch RS, Cunningham PL, Dorman SA. Small bowel metastases from primary lung carcinoma: a rarity waiting to be found? Am Surg. 1992;58(11):677–82. 5. Berger A, Cellier C, Daniel C, Kron C, Riquet M, Barbier JP, et al. Small bowel metastases from primary carcinoma of the lung: clinical findings and outcome. Am J Gastroenterol. 1999;94(7):1884–7. doi: 10.1111/j.1572-0241.1999.01224.x. 6. McNeill PM, Wagman LD, Neifeld JP. Small bowel metastases from primary carcinoma of the lung. Cancer. 1987;59(8):1486–9. 7. Yang CJ, Hwang JJ, Kang WY, Chong IW, Wang TH, Sheu CC, et al. Gastro-intestinal metastasis of primary lung carcinoma: clinical presentations and outcome. Lung Cancer. 2006;54(3):319–23. doi:10. 1016/j.lungcan.2006.08.007. 8. Yoshimoto A, Kasahara K, Kawashima A. Gastrointestinal metastases from primary lung cancer. Eur J Cancer. 2006;42(18):3157–60. doi:10.1016/j.ejca.2006.08.030. 9. Katsenos S, Archondakis S. Solitary gastric metastasis from primary lung adenocarcinoma: a rare site of extra-thoracic metastatic disease. J Gastrointest Oncol. 2013;4(2):E11–5. doi:10.3978/j.issn.20786891.2012.057. 10. Okazaki R, Ohtani H, Takeda K, Sumikawa T, Yamasaki A, Matsumoto S, et al. Gastric metastasis by primary lung adenocarcinoma. World J Gastrointest Oncol. 2010;2(10):395–8. doi:10.4251/ wjgo.v2.i10.395. 11. Sileri P, D’Ugo S, Blanco Gdel V, Lolli E, Franceschilli L, Formica V, et al. Solitary metachronous gastric metastasis from pulmonary
J Gastrointest Canc adenocarcinoma: report of a case. Int J Surg Case Rep. 2012;3(8): 385–8. doi:10.1016/j.ijscr.2012.04.017. 12. National Comprehensive Cancer Network. Non-small cell lung cancer. Fort Washington: National Comprehensive Cancer Network; 2013. 13. Goh BK, Yeo AW, Koong HN, Ooi LL, Wong WK. Laparotomy for acute complications of gastrointestinal metastases from lung cancer: is it a worthwhile or futile effort? Surg Today. 2007;37(5):370–4. doi: 10.1007/s00595-006-3419-y.
14. Rossi G, Marchioni A, Romagnani E, Bertolini F, Longo L, Cavazza A, et al. Primary lung cancer presenting with gastrointestinal tract involvement: clinicopathologic and immunohistochemical features in a series of 18 consecutive cases. J Thoracic Oncol: Off Publ Int Assoc Study Lung Cancer. 2007;2(2):115–20. 15. Lee PC, Lo C, Lin MT, Liang JT, Lin BR. Role of surgical intervention in managing gastrointestinal metastases from lung cancer. World J Gastroenterol: WJG. 2011;17(38):4314–20. doi:10.3748/wjg.v17. i38.4314.
