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Vol. 96. Issue 4.
Pages 184-197 (April 2018)
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Vol. 96. Issue 4.
Pages 184-197 (April 2018)
Review article
DOI: 10.1016/j.cireng.2017.12.010
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Gastrointestinal Metastasis From Primary Lung Cancer. Case Series and Systematic Literature Review
Metástasis gastrointestinales de carcinoma pulmonar primario. Serie de casos y revisión sistemática de la literatura
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Andrea Ballaa,b,
Corresponding author
andrea.balla@gmail.com

Corresponding author.
, José D. Subielaa, Jesús Bolloa, Carmen Martíneza, Carlos Rodriguez Luppia, Pilar Hernándeza, Yuliana Pascual-Gonzálezc, Silvia Quaresimab, Eduard M. Targaronaa
a Unidad de Cirugía General y Digestiva, Hospital de la Santa Creu y Sant Pau, Universidad Autónoma de Barcelona, Barcelona, Spain
b Department of General Surgery and Surgical Specialties Paride Stefanini, Sapienza, University of Rome, Rome, Italy
c Servicio de Neumología, Hospital Universitario de Bellvitge, Universidad de Barcelona, Barcelona, Spain
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Table 1. Patients’ Characteristics.
Abstract

Aim of the present study is to report clinical characteristics and outcomes of patients treated in authors’ hospital for GI metastasis from primary lung cancer, and to report and analyze the same data concerning patients retrieved from a systematic literature review.

We performed a retrospective analysis of prospectively collected data, and a systematic review using the Meta-analysis Of Observational Studies in Epidemiology (MOOSE) guidelines.

Ninety-one patients were included, 5 patients from the authors’ hospital and 86 through PubMed database using the keywords “intestinal metastasis” AND “lung cancer”. The median time between primary lung cancer diagnosis and GI metastasis diagnosis was 2 months and the median overall survival was 4 months.

This group of patients present a poor prognosis and the gold standard treatment is not defined. None of the reported treatments had a significant impact on survival.

Keywords:
Lung cancer
Gastrointestinal metastasis
Surgical management
Systematic literature review
Resumen

El objetivo del presente estudio es describir las características clínicas y el manejo de los pacientes tratados en nuestra institución por metástasis GI de cáncer pulmonar primario; así como realizar una revisión sistemática de casos reportados en la literatura.

Se realizó un análisis retrospectivo de una base de datos prospectiva y revisión sistemática de la literatura utilizando las normas MOOSE (Meta-analysis Of Observational Studies in Epidemiology).

Se incluyeron 91 pacientes, 5 de la base de datos de nuestra institución y 86 de la base de datos PubMed usando las palabras claves «intestinal metastasis» y «lung cancer». La mediana de tiempo entre el diagnóstico de cáncer pulmonar y el diagnóstico de metástasis GI fue 2 meses, la mediana de supervivencia global fue 4 meses.

Este grupo de pacientes presentan mal pronóstico. El tratamiento estándar no se encuentra bien establecido. Ninguno de los tratamientos descritos ha mostrado tener impacto significativo sobre la supervivencia.

Palabras clave:
Cáncer pulmonar
Metástasis gastrointestinales
Manejo quirúrgico
Revisión sistemática de la literatura
Full Text
Introduction

The lung cancer is the neoplasia with the highest known cancer-related death rate ranging from 18% to 23%.1,2 Despite advances in prevention, it has been reported that approximately 50% of cases present metastasis at the time of diagnosis.3 However, due to new technologies in diagnosis and treatment, patients’ survival is increased in the recent years, making it easier to develop metastasis in the long-term period.4

Several studies in literature, report that gastrointestinal (GI) metastasis from primary lung cancer are uncommon, with an incidence that ranges from 0.3% to 1.7%.5 On the other hand, post-mortem studies have estimated that the incidence of this type of metastatic lesions ranges from 4.6% to 14%.5,6 This discrepancy, between the estimated incidence in clinical case studies and autopsies, seems to indicate that, in most cases, there are asymptomatic undiagnosed metastasis.3

Despite the increasing of clinical publications in the literature, there is no still consensus regarding the management of these patients due to their high associated mortality.7 It has been estimated that GI metastasis represent a prognostic sign that occurs late in the lung cancer course.3 In addition, due to the difficulty in its clinical detection, it is complex to develop prospective studies and, due to the poor reported literature, principally case report and retrospective studies,8 until today an adequate diagnostic and therapeutic data to improve patients’ prognosis are missing.

The aim of the present study is to report clinical characteristics and outcomes of patients treated in authors’ hospital for GI metastasis from primary lung cancer, and to report and analyze the same data concerning patients retrieved from a systematic literature review.

Methods

This study is a retrospective analysis of prospectively collected data of patients with GI metastasis from lung primary cancer treated in the authors’ center (Hospital de la Sant Creu i Sant Pau, Barcelona, Spain) between 2012 and 2017. All patients admitted to authors’ center sign an informed consent where they authorize us to use their clinical data for educational purposes. Institutional review board (IRB) approval was obtained.

At the same time, a systematic literature review was conducted according to the Meta-analysis Of Observational Studies in Epidemiology (MOOSE) guidelines.9 It includes only papers about GI metastasis from primary lung cancer.

Search Strategy

The research was carried out on PubMed database using the keywords: “intestinal metastasis” AND “lung cancer”. The search revealed 414 published papers, dating from January 2000 to August 2017.

Studies were included in the review if present the following criteria: (1) studies that included the terms for GI metastasis from primary lung cancer; (2) they were in English or Spanish; and (3) they included adults patients only.

Studies were excluded if (1) involved animals and (2) they were systematic reviews, meta-analysis, image papers, comment papers or correspondence.

Data such as age, gender, smoking habit, lung neoplasia site, TNM, pathological histology, interval time between the lung cancer diagnosis and intestinal metastasis diagnosis, symptoms or diagnosis for hospital admission, diagnostic instrument employed, GI metastasis site, other metastasis site, GI treatment, and survival time were extracted and analyzed.

Search, data extraction and risk of bias analysis were independently performed by two authors to minimize error (A.B. and J.S.).

Statistical Analysis

Quantitative data are presented as mean±Standard Deviation (SD) and percentages. Survival analysis was performed by Kaplan–Meier method. Subgroups analysis was performed stratifying patients according to age, gender, smoking habit, tumor stage, lymph-node stage, pathological histology, synchronous vs diagnosis, clinical presentation, metastasis location and presence of extra-intestinal metastasis. A probability (P) value lower than .05 was considered statistically significant. All computations were carried out with SPSS software 22.0 (SPSS Inc., Chicago, IL, USA).

Results

Of the 414 papers identified in the search, 356 were excluded because did not meet the inclusion criteria (Fig. 1). The remaining 58 studies, published between March 2001 and August 2016, were fully analyzed and all were included in the present review, as shown in the flow diagram (Fig. 1).10–67 All the papers were retrospective analysis, letters to the editor or case reports.10–67

Fig. 1.

Flow diagram.

(0.15MB).

Patients’ characteristics are reported in Table 1. A total of 91 patients were recruited in the present review (86 patients from the literature and 5 form the authors’ series) 77 males (83.7%), 13 females (14.1%), 1 not specified gender patient. Mean age was 64.34±11.08 years, range 41–88.10–67

Table 1.

Patients’ Characteristics.

AuthorsAge (years)  Gender  Smoker  Lung neoplasia site  TNM  Pathological histology  Interval timea  Symptoms or diagnosis  Diagnostic instrument  GI metastasis site  Other metastasis  GI treatment  Survival 
Ise et al.1041  Male  N.s.  RUL  N.s.  NSCLC  9 months  Bowel perforation  Laparotomy  Jejunum  Adrenal gland, liver  Resection  1 month 
Sakorafas et al.1136  Female  Yes  RL  N.s.  Carcinosarcoma  5 months  Bowel perforation  N.s.  Ileum  Brain  Resection  2 months 
Kim et al.1280  N.s.  N.s.  N.s.  N.s.  NSCLC  N.s.  Bowel perforation  Laparotomy  Ileum  –  Resection  2 days 
Jansen et al.1373  Female  N.s.  RUL  N.s.  NSCLC  8 months  Bleeding  Enteroscopy  Jejunum  –  Resection  Alive at 14 months 
Burnette and Ballard1440  Female  Yes  LUL  N.s.  NSCLC  Synchronous  Bowel perforation  CT scan  Jejunum  –  Resection  9 days 
Garwood et al.1554  Male  N.s.  N.s.  N.s.  Adenocarcinoma  N.s.  Bowel perforation  –  Ileum  –  Resection  21 days 
Habeşoğlu et al.1667  Male  Yes  RLL  T2N1M1  Epidermoid carcinoma  Synchronous  Bowel obstruction  Colonoscopy  Left colon  –  Resection  6 months 
Kanemoto et al.1771  Male  N.s.  RLL  N.s.  SCLC  1 months  Asymptomatic  CT scan  Ileum  Left lung, adrenal gland  Resection  36 months 
Yang et al.18  71  Male  Yes  LLL  N.s.  Epidermoid carcinoma  Synchronous  Melena  Gastroscopy  Stomach  –  N.s.  4.5 months 
  65  Male  Yes  RML  N.s.  Epidermoid carcinoma  Synchronous  Melena  Gastroscopy  Stomach  Bone, pleura  N.s.  3 months 
  62  Male  Yes  RUL  N.s.  Adenocarcinoma  2 months  Melena  Gastroscopy  Stomach  Bone  N.s.  12.5 months 
  50  Male  Yes  RLL  N.s.  Epidermoid carcinoma  14 months  Bowel perforation  Laparotomy  Jejunum  –  N.s.  23 days 
  57  Male  Yes  RUL  N.s.  SCLC  2 months  Intussusception  Laparotomy  Ileum  Brain  N.s.  3 months 
  57  Male  Yes  LUL  N.s.  SCLC  21.5 months  Hematochezia  Colonoscopy  Cecum  Brain, bone  N.s.  2 months 
Kostakou et al.1961  Male  Yes  RLL  N.s.  NSCLC  1 months  Melena  Gastroscopy  Duodenum, jejunum  –  Blood transfusion  7 months 
Yuksel et al.2065  Male  N.s.  N.s.  N.s.  Epidermoid Carcinoma  12 months  Bowel perforation  Laparotomy  Ileum  Brain  Resection  N.s. 
Kagohashi et al.2159  Male  Yes  LUL  N.s.  NSCLC  Synchronous  Intussusception  CT scan  Jejunum  –  Resection  6 months 
Karamercan et al.2263  Male  N.s.  LUL  N.s.  SCLC  11 months  Abdominal pain  CT scan  Ileum  –  Resection  N.s. 
Lau and Leung2359  Male  Yes  LPH  N.s.  SCLC  Synchronous  Abdominal pain  Colonoscopy  Cecum  Brain  Chemotherapy  N.s. 
Kim et al.24  79  Male  Yes  RLL  T2N0M0  N.s.  5.5 months  Abdominal pain  N.s.  Colon  –  Surgery a  1 month 
  56  Male  Yes  LUL  T2N1M0  N.s.  2.5 months  Melena  N.s.  Ileum  –  Surgery a  69 days 
  70  Male  Yes  LLL  T2N0M1  N.s.  1 months  Abdominal pain  N.s.  Ileum  Brain  Surgery a  12 days 
  46  Female  Yes  LLL  T2N2M0  N.s.  30.5 months  Abdominal pain  N.s.  Ileum  Pleural  Surgery a  102 days 
  67  Male  No  LUL  T1N1M1  N.s.  Synchronous  Abdominal pain  N.s.  Stomach  Lung  None  80 days 
  61  Male  Yes  LUL  T3N2M0  N.s.  3.5 months  Abdominal pain  N.s.  Ileum  Adrenal gland  Surgery  Alive at 33 months 
  72  Male  Yes  RUL  T1N0M1  N.s.  Synchronous  Asymptomatic  N.s.  Stomach  Lung, brain, adrenal gland  None  67 days 
  78  Male  Yes  LUL  T1N3M1  N.s.  Synchronous  Hematochezia  N.s.  Colon  Lung, neck, adrenal gland, spleen  None  133 days 
  66  Male  Yes  RLL  N.s.  N.s.  Synchronous  Hematemesis  N.s.  Stomach  Adrenal gland  Elettrocautery  145 days 
  10  62  Male  Yes  RUL  T2N2M1  N.s.  Synchronous  Melena  Laparotomy  Ileum  –  Surgery  Alive at 63 months 
Pollheimer et al.2565  Female  N.s.  N.s.  N.s.  NSCLC  N.s.  Intussusception  CT scan  Ileum, cecum  –  Right hemicolectomy  N.s. 
Chiu et al.2687  Male  N.s.  RUL  N.s.  Adenocarcinoma  Synchronous  Intussusception  CT scan  Jejunum  –  Resection  3 months 
Bélanger and Gagné2760  Male  Yes  RUL, LLL  N.s.  N.s.  Synchronous  Bowel perforation  Laparoscopy  Jejunum, ileum  –  Resection  10 months 
Shi et al.2861  Male  N.s.  N.s.  T2N0M1  Sarcomatoid carcinoma  17 months  Intussusception  CT scan  Jejunum  Adrenal gland, liver, lung, brain  Resection  4 months 
Meneses Grasa et al.2969  Male  Yes  LUL  T3N2M0  Epidermoid carcinoma  6 months  Bowel obstruction  CT scan  Jejunum, ileum mesentery  –  Resection  1.5 months 
Scabini et al.3076  Male  N.s.  N.s.  N.s.  SCLC  N.s.  Bowel obstruction  –  Ileum  –  Resection  N.s. 
Ara3175  Male  Yes  LPH  N.s.  Adenocarcinoma  Synchronous  Bowel obstruction  Laparotomy  Ileum  –  Resection  2.5 months 
Weng et al.3253  Male  Yes  LIL  T4N3M1  Adenocarcinoma  Synchronous  Bowel obstruction  CT scan  Colon  –  Colostomy  6 months 
Kini et al.3378  Male  N.s.  N.s.  N.s.  Adenocarcinoma  7 months  Abdominal pain  CT scan  Jejunum, ileum  –  Resection  Alive at 5 months 
Yildirim et al.3478  Male  N.s.  N.s.  N.s.  Epidermoid carcinoma  3 months  Abdominal pain  Laparotomy  Ileum  –  Resection  21 days 
Okutur et al.3564  Male  N.s.  LUL  N.s.  Epidermoid carcinoma  4 months  Rectal bleeding  Rectal examination  Anal canal  –  Radiotherapy  N.s. 
Otera et al.3663  Male  Yes  N.s.  N.s.  NSCLC  Synchronous  Intussusception  CT scan  Ileum  –  Resection  27 days 
Akamatsu et al.3772  Male  Yes  RUL  N.s.  NSCLC  Synchronous  Asymptomatic  CT scan  Jejunum  –  Chemotherapy  5 months 
Lin et al.3876  Male  No  LUL  N.s.  Adenocarcinoma  0.5 months  Melena  Gastroscopy  Duodenum  Bone  Blood transfusion  2.5 months 
Papaziogas et al.3968  Male  Yes  RLL  N.s.  Epidermoid carcinoma  8 months  Bowel obstruction  CT scan  Ileum  –  Resection  4 months 
Yamada et al.4066  Male  Yes  LUL  T4N3M1  Epidermoid carcinoma  Synchronous  Bowel perforation  CT scan  Duodenum, ileum  –  Resection  4 months 
Nishizawa et al.41  55  Male  N.s.  N.s.  T1N0  Adenocarcinoma  Synchronous  Bowel perforation  Abdominal X-ray  Ileum  Liver, brain  Resection  53 days 
  58  Male  N.s.  N.s.  T4N1  Adenocarcinoma  17.4 months  Bowel perforation  Abdominal X-ray  Jejunum  Colon  Resection  108 days 
  40  Male  N.s.  N.s.  T2N3  Adenocarcinoma  6.7 months  Bowel perforation  Abdominal X-ray  Ileum  Brain  Resection  347 days 
  56  Male  N.s.  N.s.  T2N3  Adenocarcinoma  9.1 months  Abdominal pain  Gastroscopy  Duodenum  Liver  Bypass  25 days 
  78  Male  N.s.  N.s.  T4N2  Epidermoid carcinoma  2.3 months  Bowel perforation  CT scan  Ileum  Lung, liver, bone, adrenal gland  Resection  67 days 
  62  Male  N.s.  RUL  T1N0  Adenocarcinoma  14.7 months  Abdominal pain  Gastroscopy  Jejunum  –  Resection  742 days 
  68  Male  N.s.  N.s.  T4N1  Adenocarcinoma  31.3 months  Abdominal pain  CT scan  Ileum  Brain, bone  Bypass  302 days 
Fujiwara et al.42  66  Female  N.s.  N.s.  N.s.  NSCLC  6.7 months  Melena  N.s.  Colon  –  Resection  40 months 
  68  Male  N.s.  N.s.  N.s.  NSCLC  9.5 months  Anemia  N.s.  Ileum  –  Resection  93.6 months 
  70  Female  N.s.  N.s.  N.s.  NSCLC  19.5 months  Melena  N.s.  Rectum  –  Resection  46.9 months 
  48  Male  N.s.  N.s.  N.s.  NSCLC  9.4 months  Melena  N.s.  Ileum  Adrenal gland  Resection  14.9 months 
  83  Male  N.s.  N.s.  N.s.  NSCLC  6.9 months  Abdominal mass  N.s.  Colon  Liver  Resection  3.7 months 
  51  Male  N.s.  N.s.  N.s.  NSCLC  2.2 months  Anemia  N.s.  Stomach  Skin, brain  N.s.  0.4 months 
  57  Male  N.s.  N.s.  N.s.  NSCLC  1.2 months  Anemia, ileus  N.s.  Ileum, stomach  Liver, kidney  N.s.  1.1 months 
  69  Male  N.s.  N.s.  N.s.  NSCLC  14.3 months  N.s.  N.s.  Colon  Adrenal gland, brain  N.s.  0.2 months 
  70  Male  N.s.  N.s.  N.s.  N.s.  4 months  Melena  N.s.  Ileum  Adrenal gland, pancreas  N.s.  10.8 months 
Tanaka et al.4385  Male  N.s.  N.s.  T4N1M1  Epidermoid carcinoma  120 months  Bowel perforation  CT scan  Jejunum  Bone  Resection  3 months 
Song et al.4458  Male  N.s.  LUL  N.s.  NSCLC  Synchronous  Bowel obstruction  CT scan  Jejunum  Bladder, adrenal gland, brain  Resection  N.s. 
Jarmin et al.4575  Male  N.s.  N.s.  N.s.  SCLC  Synchronous  Intussusception  Laparotomy  Duodenum, jejunum  N.s.  Whipple's procedure, resection  N.s. 
Guner et al.4671  Male  N.s.  N.s.  T3N1  Sarcomatoid carcinoma  N.s.  Intussusception  Laparotomy  Ileum  N.s.  Resection  9 months 
Parejo-Sánchez et al.4760  Male  Yes  N.s.  T1N0M0  NSCLC  15  Bleeding  Laparotomy  Jejunum  –  Resection  N.s. 
Li Destri et al.4873  Male  N.s.  N.s.  N.s.  Neuroendocrine carcinoma  Synchronous  Bowel obstruction  CT scan  Ileum  Brain  Resection  277 days 
Lin et al.4978  Male  Yes  RUL  N.s.  NSCLC  Synchronous  Intussusception  CT scan  Jejunum, colon  –  Resection  3 months 
Hara et al.5058  Male  N.s.  RUL  T2N0M0  NSCLC  9 months  Fever  CT scan  Ileum  –  Resection  4 months 
Rivera et al.5161  Female  Yes  RUL  N.s.  Adenocarcinoma  Synchronous  Abdominal pain  CT scan  Ileum  Mediastinum, left supraclavicular space  Resection  Alive at 5 months 
Koh et al.5246  Male  Yes  RUL  N.s.  NSCLC  0.3 moths  Bowel perforation  CT scan  Ileum  Stomach, duodenum, kidneys, pancreas, gallbladder, adrenal gland, thyroid  Resection  14 days 
Khan et al.5360  Male  Yes  RUL  N.s.  SCLC  Synchronous  Anemia  Colonoscopy  Cecum  Brain, liver, spleen  Polypectomy  11 months 
Sifuentes Giraldo et al.5473  Male  Yes  LUL  N.s.  Adenocarcinoma  Synchronous  Bowel perforation  CT scan  Colon  –  Resection  2 months 
de Miguel Valencia et al.5548  Male  Yes  LIL  N.s.  Sarcomatoid carcinoma  Synchronous  Intussusception  CT scan  Ileum  Lung, bone, cerebral, adrenal gland  Resection  5 months 
Guerra et al.5675  Female  Yes  N.s.  N.s.  SCLC  1 months  Perianal pain  Rectal examination  Rectum  Bone  Chemotherapy  Alive at 7 months 
Mandeville et al.5749  Female  N.s.  LUL  T4N0M1b  NSCLC  Synchronous  Intussusception  Laparoscopy  Ileum  Bone, brain  Resection  6 months 
Liu et al.5866  Male  N.s.  RLL  T2N1M0  Epidermoid carcinoma  8 months  Melena  CT scan  Ileum  –  Resection  Alive at 5 months 
Lu et al.5962  Female  N.s.  N.s.  N.s.  Adenocarcinoma  Synchronous  Melena  Colonoscopy  Colon  Skin  Chemotherapy  Alive at 2 months 
Lu et al.6078  Male  Yes  N.s.  TxN1M1  Adenocarcinoma  4 months  Melena  CT scan  Jejunum  Adrenal gland, bone  Resection  2 months 
Chen6161  Male  Yes  RPH  N.s.  Adenocarcinoma  Synchronous  Intussusception  CT scan  Ileum  –  Resection  Alive at 3 months 
Escoda6263  Male  N.s.  LPH  N.s.  Epidermoid carcinoma  Synchronous  Bowel obstruction  CT scan  Ileum  Myocardium, bone  Resection  – 
Romano et al.6360  Male  Yes  LIL  N.s.  Carcinosarcoma  0.5 moths  Intussusception  CT scan  Ileum  Liver, omentum  Resection  8 days 
Nunes et al.6443  Male  Yes  RUL  T2N0M1  Adenosquamous carcinoma  Synchronous  Bowel obstruction  Colonoscopy  Left colon, duodenum  Brain  Resection  Alive at 18 months 
Iwamuro et al.6571  Male  N.s.  RML  T3N2M1  Adenocarcinoma  N.s.  Melena  Gastroscopy  Duodenum  Adrenal gland  Chemotherapy  5 months 
Nakamura et al.6688  Female  N.s.  N.s.  T1N1M0  Epidermoid carcinoma  144 months  Intussusception  CT scan  Ileum  –  Resection  5 months 
Fujii et al.6755  Female  N.s.  LUL  N.s.  NSCLC  Synchronous  Intussusception  CT scan  Jejunum  –  Resection  Alive at 11 months 
Present series  69  Male  Yes  LPH  T4N3M1  Epidermoid carcinoma  6 months  Bowel obstruction  CT scan  Ileum  Liver, bone, peritoneum, mesentery  Resection  1.5 months 
  79  Male  Yes  RML  T4N2M1  Adenocarcinoma  Synchronous  Bowel perforation  CT scan  Jejunum  Peritoneum  Resection  1 months 
  67  Male  Yes  LUL  T4N2M1  Adenocarcinoma  5.5 months  Bowel perforation  CT scan  Ileum  Adrenal gland, abdominal wall  Resection  1 months 
  53  Male  Yes  LIL  T1N2M1  NSCLC  7 months  Abdominal pain  Entero-MRI  Jejunum, ileum  Liver, spleen vertebrae  Conservative  8 months 
  72  Male  Yes  RUL  T3N0M0  Adenocarcinoma  12 months  Asymptomatic  PET-CT  Ileum  Brain  Resection  4 months 
a

Interval time between the lung cancer diagnosis and intestinal metastasis diagnosis. GI: Gastrointestinal. a: surgical procedure not specified. NSCLC: non-small cell lung carcinoma. SCLC: small cell lung carcinoma. N.s.: not specified. CT: computed tomography. MRI: magnetic resonance imaging. PET: positron emission tomography. RL: right lobe. RPH: right pulmonary hilum. RUL: right upper lobe. RML: right middle lobe. RLL: right lower lobe. LPH: left pulmonary hilum. LUL: left upper lobe. LIL: left inferior lobe. LLL: left lingual lobe.

The most common site of primary lung cancer was left upper lobe (17 patients, 18.7%), followed by right upper lobe in (16 patients, 17.6%) and right lower lobe (8 patients, 8.8%) (Table 1). Pathological histology has been reported in 78 patients (non-small cell lung cancer in 69 patients, 75.9%, small cell lung cancer in 9 patients, 9.9%). Non-small cell lung cancer was divided in: 23 adenocarcinomas (25.3%), 16 epidermoid carcinomas (17.6%), 3 sarcomatoid carcinomas (3.3%) and 2 carcinosarcomas (2.2%) (Table 1).

In 33 cases (38.8%), primary lung cancer and GI metastasis were diagnosed at the same time, and in 52 cases (61.2%) delayed. The median time between primary lung cancer diagnosis and GI metastasis diagnosis (reported in 85 cases, 93.4%) was 2 months (95% CI: 0.1–38) (Table 1).

Bowel obstruction was observed in 26 patients (28.6%; 15 intussusceptions, 10 neoplastic stenosis, 1 compression from mesenteric neoplastic infiltration), followed by GI bleeding in 25 patients (27.5%; 15 melena, 5 chronic anemia, 1 hematochezia, 1 hematemesis, 1 rectal bleeding and 2 anemia), bowel perforation in 17 patients (18.7%) and abdominal pain in 14 patients (15.4%). Five patients were asymptomatic (5.5%) and in 3 patients (3.3%) fever, perianal pain and abdominal mass were observed (Table 1).

Computed tomography (CT) scan was the most useful diagnostic test (35 patients, 38.5%) followed by endoscopy (gastroscopy, colonoscopy or enteroscopy in 15 patients, 16.5%) and laparotomy (11 patients, 12.1%) (Table 1).

The most common site of metastasis was the ileum (40 patients, 44%), followed by colon (18 patients, 19.8%) and jejunum (16 patients, 17.6%). Extra-intestinal metastasis was observed in 50 patients (54.9%) (Table 1).

Regarding treatment options, bowel resection was performed in 67 patients (73.6%), chemotherapy or radiotherapy and conservative treatment in 6 patients (6.6%), respectively, and endoscopic treatment in 2 patients (2.2%) (Table 1).

The median overall survival was 4 months (95% CI: 2.68–5.31) (Fig. 2). Survival stratified analysis revealed statistical significant differences when the patients were compared according to gender (male vs female: 3.7 months, 95% CI: 2.7–4.6 vs 6 months, 95% CI: 0–36.5, Log-rank: P=.01), age (<70 vs ≥70: 4 months, 95% CI: 2.4–5.5 vs 3 months, 95% CI: 2.1–3.8, Log-rank: P=.04), clinical presentation (bowel perforation vs others: 1.8 months. 95% CI: 0.4–3.1 vs 4.8 months, 95% CI: 3.9–5.6, Log-rank: P=.0001) and metastasis location (colon-rectum vs small bowel vs stomach: 6 months, 95% CI: 3.3–86 vs 4 months, 95% CI: 3–4.9 vs 2.6 months, 95% CI: 1.6–3.5, Log-rank: P=.03) (Fig. 3). No statistically significant differences were observed when patients were stratified according smoking habit, pathological histology, tumor stage, lymph-node stage, presence of extra-intestinal metastasis and synchronous vs delay diagnosis.

Fig. 2.

Kaplan–Meier plot of the overall survival curve.

(0.05MB).
Fig. 3.

Kaplan–Meier plot of the survival curve based on gender (A), age (B), clinical presentation (C) and metastasis location (D).

(0.28MB).
Discussion

From March 2001 to August 2017, 86 cases of GI metastasis from primary lung cancer are reported in literature10–67 and between 2012 and 2017, in authors’ hospital, 5 patients were treated for the same reason, for a total of 91 patients included in the present study. The treatment of choice of this type of lesions, is still debated in literature, due to the lack of reported large series and the difficulty to perform Randomized Control Trials (RCTs) due to the patients’ heterogeneous characteristics who experience GI metastasis. Often, the treatment is affected by patients’ urgency conditions, such as bowel perforation or obstruction and bleeding, that do not allow to choose a different treatment than surgery. For these reasons and due to the patients’ poor condition at the time of GI metastasis diagnosis (advanced stage cancer, old age, severe symptoms) the median survival rate is very low.7

We have investigated with the aim to analyze our data and those reporting in literature regarding GI metastasis from primary lung cancer. Anyway, the present study has several biases, such as the relative small number of patients and several missing data from the literature.

The most frequent lung histological subtype cancer related to GI metastasis is still debated in literature3,5,7,8,24 but in the present series, Large cell carcinoma is the most common observed (75.9%).

The majority of patients with GI metastasis from a primary lung cancer are asymptomatic,5 as evidenced by the discrepancy between the estimated incidence in clinical studies and post-mortem studies.24 This clinical under-diagnosis may be due to the fact that the GI discomfort, referred by these patients, is often confused with chemotherapy side effects68 and for this reason requires a greater degree of suspicion by the clinician for early identification. The most frequent uncomplicated symptoms observed are the abdominal pain occurred in 50% of patients and weight loss.7,69 Among complicated symptoms, small bowel perforation is described,7,70 such as the obstruction that can occur as a consequence of an occlusive mass24 or by intussusception of the affected ileal tract.7,33 Finally, acute digestive hemorrhage may be observed as melena in case of stomach, duodenum or small bowel lesions71 and rectal bleeding in case of lower GI tract involvement.68 In the present series, small bowel obstruction is the most frequent complicated symptom observed (28.6%) as well as reported by Di et al. (35%).7

Lung metastasis can be observed in all GI tract such as esophagus (6.3%), small bowel (2.6%), stomach (1.2%) and colon (0.7%).3 Based on the literature, the most frequent small bowel site are the jejunum and ileum,7,24,72 while the duodenum is usually affected in a smaller number of cases.73 In the present series, the most frequent metastasis site is in the ileum (44%).

CT scan is the most used diagnostic test, both in authors’ experience and in the literature.5 This test has been widely described5 due to its versatility and easy access in the context of urgency, with an estimated sensitivity rate of 72%,74 however, it has been shown difficulty in detecting small lesions.74 Positron emission tomography-CT (PET-CT) scan shown to be useful in the diagnosis of metastasis from primary lung cancer also in case of asymptomatic GI metastasis.75,76 Although, in the present study is employed only in one patient, and, at now, no sufficient data about sensitivity and specificity of this test are available.77 The use of endoscopic approach has been described in several series as a diagnostic test in patients who present digestive bleeding or anemia.68,69,76,77 A recent study reports the use of endoscopic capsule such as feasible diagnostic test for small bowel lesions and as a non-invasive diagnostic method that could reduce the metastasis under-diagnosis.78 Magnetic resonance imaging (MRI) is a less common diagnostic test proposed in the literature,47 and has been employed in only one patient of the present series.

The treatment of choice of the lung GI metastasis is still debated in literature, between authors that support conservative approach8,79 and authors in favor of surgical approach.3,24 Anyway, in case of bowel perforation or obstruction or in case of massive bleeding, the surgical approach is often the only possible treatment.3 A perioperative mortality rate between 20% and 100%, is reported in literature, in patients who underwent surgery8,79 but it should be noted that most of these deaths were not due to immediate surgical complications.7 Goh et al. suggest that an adequate selection of patients who underwent surgery could increase the survival rate,3 considering multiple extra-intestinal metastasis and bowel perforation the most important factors that affected the postoperative outcomes.3 In the present series perioperative mortality was observed in one case. The most common surgical technique performed, in the literature such as in the present series, is the bowel resection with primary anastomosis by laparotomy,3,8 but a recent study shows the feasibility of laparoscopic approach.80

The median survival ranges between 1 and 6 months.3,7,8,24 The largest series published in literature, that reports a retrospective analysis of 100 previously published cases (including autopsies), shows a median survival of 2.3 months7 and reports that the risk factors mostly associated with mortality are: age greater than 70 years, bowel perforation and presence of extra-intestinal metastasis,7 as well as confirmed in this series. In the present study, the survival rate is similar to that published in literature (4 months, 95% CI: 2.68–5.31), and stratifying the patients, the statistical significant differences were observed only for gender, age, clinical presentations and metastasis site.

The gold standard treatment is not still available based on the published data, and none of the reported treatments had a significant impact on survival. Anyway, surgical treatment cannot defer in case of bowel perforation but also in some case of massive bleeding or bowel obstruction. For this reason, in patients with acute abdomen and history of lung cancer, GI metastasis should be considered such as differential diagnosis. At the time of primary lung cancer diagnosis, after CT scan, PET-CT scan could be helpful to diagnose eventual synchronous metastasis.

To the best of the authors’ knowledge, this is the first systematic review, concerning GI metastasis from primary lung cancer, reported in literature.

Randomized clinical trials are difficult to perform due to the rarity and the heterogeneity of these lesions, however a wider sample size of patients, and further studies are required to confirm these data.

Authors’ Contribution

Andrea Balla: study designs, acquisition of data, analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

José D. Subiela: study designs, acquisition of data, analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Jesús Bollo: study designs, acquisition of data, analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Carmen Martinez: analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Carlos Rodriguez Luppi: analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Pilar Hernández: analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Yuliana Pascual: analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Silvia Quaresima: analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Eduard M. Targarona: study designs, acquisition of data, analysis and interpretation of results, manuscript preparation, critical revision and approval of the final version of the manuscript.

Conflict of Interest

Dr. Andrea Balla, Dr. José D. Subiela, Dr. Jesús Bollo, Dr. Carmen Martinez, Dr. Carlos Rodriguez Luppi, Dr. Pilar Hernández, Dr. Yuliana Pascual, Dr. Silvia Quaresima and Professor Eduard M. Targarona have no conflicts of interest or financial ties to disclose.

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Please cite this article as: Balla A, Subiela JD, Bollo J, Martinez C, Rodriguez Luppi C, Hernández P, et al. Metástasis gastrointestinales de carcinoma pulmonar primario. Serie de casos y revisión sistemática de la literatura. Cir Esp. 2018;96:184–197.

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