Isolated pulmonary metastases in pancreatic ductal adenocarcinoma: a review of current evidence

ABSTRACT Despite recent advances in cancer therapeutics, pancreatic ductal adenocarcinoma (PDAC) remains a lethal disease with a 5-year overall survival of only 10%. Since either at or within a few months of diagnosis, most patients with PDAC will present with metastatic disease, a more individualized approach to select patients who may benefit from more aggressive therapy has been suggested. Although studies have reported improved survival in PDAC and isolated pulmonary metastasis (ISP) compared to extrapulmonary metastases, such findings remain controversial. Furthermore, the added benefit of pulmonary metastasectomy and other lung-directed therapies remains unclear. In this review, we discuss the metastatic pattern of PDAC, evaluate the available evidence in the literature for improved survival in PDAC and ISP, evaluate the evidence for the added benefit of pulmonary metastasectomy and other lung-directed therapies, identify prognostic factors for survival, discuss the biological basis for the reported improved survival and identify areas for further research.

[1]  A. Jemal,et al.  Cancer statistics, 2022 , 2022, CA: a cancer journal for clinicians.

[2]  Ah-Young Kwon,et al.  The Prognostic Impact of HER2 Genetic and Protein Expression in Pancreatic Carcinoma—HER2 Protein and Gene in Pancreatic Cancer , 2021, Diagnostics.

[3]  J. Feliu,et al.  Liquid Biopsy in Pancreatic Cancer: Are We Ready to Apply It in the Clinical Practice? , 2021, Cancers.

[4]  L. Matrisian,et al.  Estimated Projection of US Cancer Incidence and Death to 2040 , 2021, JAMA network open.

[5]  T. Murakawa Past, present, and future perspectives of pulmonary metastasectomy for patients with advanced colorectal cancer , 2020, Surgery Today.

[6]  E. Aranda,et al.  Circulating Cell-Free DNA-Based Liquid Biopsy Markers for the Non-Invasive Prognosis and Monitoring of Metastatic Pancreatic Cancer , 2020, Cancers.

[7]  C. Vitellius,et al.  Impact of Driver Mutations on the Evolution of Isolated Metachronous Lung Metastasis of Pancreatic Ductal adenocarcinoma , 2020, Molecular Diagnosis & Therapy.

[8]  F. Guerra,et al.  Metastases or primary recurrence to the lung is related to improved survival of pancreatic cancer as compared to other sites of dissemination. Results of a systematic review with meta-analysis. , 2020, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[9]  J. Kleeff,et al.  Surgery for synchronous and metachronous single-organ metastasis of pancreatic cancer: a SEER database analysis and systematic literature review , 2020, Scientific Reports.

[10]  B. Hankey,et al.  Surveillance, Epidemiology, and End Results Program , 2020, Definitions.

[11]  A. Jemal,et al.  Cancer statistics, 2020 , 2020, CA: a cancer journal for clinicians.

[12]  S. Natsugoe,et al.  Lung recurrence and its therapeutic strategy in patients with pancreatic cancer. , 2019, Pancreatology : official journal of the International Association of Pancreatology (IAP) ... [et al.].

[13]  M. Büchler,et al.  Patterns of Recurrence After Resection of Pancreatic Ductal Adenocarcinoma: A Secondary Analysis of the ESPAC-4 Randomized Adjuvant Chemotherapy Trial. , 2019, JAMA surgery.

[14]  J. Dunning,et al.  Pulmonary Metastasectomy versus Continued Active Monitoring in Colorectal Cancer (PulMiCC): a multicentre randomised clinical trial , 2019, Trials.

[15]  C. Pilarsky,et al.  Chemoresistance in Pancreatic Cancer , 2019, International journal of molecular sciences.

[16]  N. Tsang,et al.  Lung Metastases in Patients with Stage IV Pancreatic Cancer: Prevalence, Risk Factors, and Survival Impact , 2019, Journal of clinical medicine.

[17]  J. Cameron,et al.  Isolated pulmonary recurrence after resection of pancreatic cancer: the effect of patient factors and treatment modalities on survival. , 2019, HPB : the official journal of the International Hepato Pancreato Biliary Association.

[18]  Song-Cheol Kim,et al.  Management of isolated recurrence after surgery for pancreatic adenocarcinoma , 2019, The British journal of surgery.

[19]  S. Dabernat,et al.  Liquid Biopsy Approach for Pancreatic Ductal Adenocarcinoma , 2019, Cancers.

[20]  J. Neoptolemos,et al.  Surgical and local therapeutic concepts of oligometastatic pancreatic cancer in the era of effective chemotherapy , 2019, European Surgery.

[21]  D. Jäger,et al.  Chemotherapy for pancreatic cancer. , 2019, Presse medicale.

[22]  M. Maglione,et al.  Progressive Oncological Surgery Is Associated with Increased Curative Resection Rates and Improved Survival in Metastatic Colorectal Cancer , 2019, Cancers.

[23]  A. Maitra,et al.  Circulating Nucleic Acids Are Associated With Outcomes of Patients With Pancreatic Cancer. , 2019, Gastroenterology.

[24]  K. Kichikawa,et al.  Prognostic factors for actual long-term survival in the era of multidisciplinary treatment for pancreatic ductal adenocarcinoma , 2018, Langenbeck's Archives of Surgery.

[25]  M. Capanu,et al.  Pancreatic adenocarcinoma: insights into patterns of recurrence and disease behavior , 2018, BMC Cancer.

[26]  Zhiqiang Sun,et al.  Prediction of overall survival for metastatic pancreatic cancer: Development and validation of a prognostic nomogram with data from open clinical trial and real‐world study , 2018, Cancer medicine.

[27]  J. Joo,et al.  Prognostic Implications of Multiplex Detection of KRAS Mutations in Cell-Free DNA from Patients with Pancreatic Ductal Adenocarcinoma. , 2018, Clinical chemistry.

[28]  Jing Guo,et al.  Combined pretreatment serum CA19-9 and neutrophil-to-lymphocyte ratio as a potential prognostic factor in metastatic pancreatic cancer patients , 2018, Medicine.

[29]  T. Ohtsuka,et al.  Primary Recurrence in the Lung is Related to Favorable Prognosis in Patients with Pancreatic Cancer and Postoperative Recurrence , 2017, World Journal of Surgery.

[30]  B. Melichar,et al.  Different clinical presentations of metachronous pulmonary metastases after resection of pancreatic ductal adenocarcinoma: Retrospective study and review of the literature , 2017, World journal of gastroenterology.

[31]  F. Motoi,et al.  Predictive risk factors for peritoneal recurrence after pancreatic cancer resection and strategies for its prevention , 2017, Surgery Today.

[32]  A. Mehrabi,et al.  Prognostic value of site-specific metastases in pancreatic adenocarcinoma: A Surveillance Epidemiology and End Results database analysis , 2017, World journal of gastroenterology.

[33]  Y. Maehara,et al.  Surgical Resection for Pulmonary Metastasis from Pancreatic and Biliary Tract Cancer. , 2017, Anticancer research.

[34]  M. Büchler,et al.  Radical surgery of oligometastatic pancreatic cancer , 2016 .

[35]  Valérie Taly,et al.  Plasma Circulating Tumor DNA in Pancreatic Cancer Patients Is a Prognostic Marker , 2016, Clinical Cancer Research.

[36]  J. Werner,et al.  Isolated pulmonary metastases define a favorable subgroup in metastatic pancreatic cancer. , 2016, Pancreatology : official journal of the International Association of Pancreatology (IAP) ... [et al.].

[37]  J. Fontaine,et al.  Pulmonary metastasectomy for suspected pancreaticobiliary cancer. , 2016, The Journal of thoracic and cardiovascular surgery.

[38]  I. Juan,et al.  Heterogeneity of metastatic pancreatic adenocarcinoma: Lung metastasis show better prognosis than liver metastasis—a case control study , 2016, Oncotarget.

[39]  Taesung Park,et al.  Molecular subtypes of pancreatic cancer based on miRNA expression profiles have independent prognostic value , 2016, Journal of gastroenterology and hepatology.

[40]  A. Maitra,et al.  Minimally invasive genomic and transcriptomic profiling of visceral cancers by next-generation sequencing of circulating exosomes , 2015, Annals of oncology : official journal of the European Society for Medical Oncology.

[41]  H. Zeh,et al.  The indolent nature of pulmonary metastases from ductal adenocarcinoma of the pancreas , 2015, Journal of surgical oncology.

[42]  W. Scheithauer,et al.  nab-Paclitaxel plus gemcitabine for metastatic pancreatic cancer: long-term survival from a phase III trial. , 2015, Journal of the National Cancer Institute.

[43]  R. Weichselbaum,et al.  14q32-encoded microRNAs mediate an oligometastatic phenotype , 2015, Oncotarget.

[44]  V. Brouste,et al.  Combined Ablation and Resection (CARe) as an Effective Parenchymal Sparing Treatment for Extensive Colorectal Liver Metastases , 2014, PloS one.

[45]  T. Treasure Pulmonary Metastasectomy for Colorectal Cancer: Recent Reports Prompt a Review of the Available Evidence , 2014, Current Colorectal Cancer Reports.

[46]  M. Yoshimura,et al.  Radiotherapy for patients with isolated local recurrence of primary resected pancreatic cancer , 2014, Strahlentherapie und Onkologie.

[47]  O. Petrenko,et al.  Analysis of the tumor-initiating and metastatic capacity of PDX1-positive cells from the adult pancreas , 2014, Proceedings of the National Academy of Sciences.

[48]  David Goldstein,et al.  Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. , 2013, The New England journal of medicine.

[49]  J. Pearson,et al.  Clinical and molecular characterization of HER2 amplified-pancreatic cancer , 2013, Genome Medicine.

[50]  J. Gaughan,et al.  Patterns of recurrence and outcomes in pancreatic cancer. , 2013 .

[51]  C. Combescure,et al.  Risk Factors for Survival after Lung Metastasectomy in Colorectal Cancer Patients: A Systematic Review and Meta-Analysis , 2013, Annals of Surgical Oncology.

[52]  V. Heinemann,et al.  Prognostic value of CA 19-9, CEA, CRP, LDH and bilirubin levels in locally advanced and metastatic pancreatic cancer: results from a multicenter, pooled analysis of patients receiving palliative chemotherapy , 2013, Journal of Cancer Research and Clinical Oncology.

[53]  Lincoln D. Stein,et al.  Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes , 2012, Nature.

[54]  P. Kozuch,et al.  Case Report: Long-Term Survival in Patients with Initial Lung-Only Metastasis from Pancreatic Adenocarcinoma , 2012, Journal of Gastrointestinal Cancer.

[55]  Jeffrey E. Lee,et al.  Selective Reoperation for Locally Recurrent or Metastatic Pancreatic Ductal Adenocarcinoma Following Primary Pancreatic Resection , 2012, Journal of Gastrointestinal Surgery.

[56]  M. Kage,et al.  Metastatic pulmonary adenocarcinoma 13 years after curative resection for pancreatic cancer: report of a case and review of Japanese literature. , 2012, JOP : Journal of the pancreas.

[57]  R. Weichselbaum,et al.  MicroRNA Expression Characterizes Oligometastasis(es) , 2011, PloS one.

[58]  J. Cameron,et al.  Pulmonary Resection for Isolated Pancreatic Adenocarcinoma Metastasis: an Analysis of Outcomes and Survival , 2011, Journal of Gastrointestinal Surgery.

[59]  Pierre Michel,et al.  FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. , 2011, The New England journal of medicine.

[60]  M. Hashizume,et al.  MicroRNA Expression as a Predictive Marker for Gemcitabine Response after Surgical Resection of Pancreatic Cancer , 2011, Annals of Surgical Oncology.

[61]  M. Nowak,et al.  Distant Metastasis Occurs Late during the Genetic Evolution of Pancreatic Cancer , 2010, Nature.

[62]  V. Jooste,et al.  Epidemiology, management and prognosis of colorectal cancer with lung metastases: a 30-year population-based study , 2010, Gut.

[63]  K. Ohuchida,et al.  MicroRNA, hsa-miR-200c, is an independent prognostic factor in pancreatic cancer and its upregulation inhibits pancreatic cancer invasion but increases cell proliferation , 2010, Molecular Cancer.

[64]  Giovanni Parmigiani,et al.  SMAD4 Gene Mutations Are Associated with Poor Prognosis in Pancreatic Cancer , 2009, Clinical Cancer Research.

[65]  Alison P. Klein,et al.  DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[66]  Sunil Krishnan,et al.  Long-Term Survival After Multidisciplinary Management of Resected Pancreatic Adenocarcinoma , 2009, Annals of Surgical Oncology.

[67]  M. Choti,et al.  Simultaneous Resections of Colorectal Cancer and Synchronous Liver Metastases: A Multi-institutional Analysis , 2007, Annals of Surgical Oncology.

[68]  H. Friess,et al.  Surgery for Recurrent Pancreatic Ductal Adenocarcinoma , 2007, Annals of surgery.

[69]  C. Iacobuzio-Donahue,et al.  Immortalizing the complexity of cancer metastasis: Genetic features of lethal metastatic pancreatic cancer obtained from rapid autopsy , 2005, Cancer biology & therapy.

[70]  Y. Ohno,et al.  Benefits of surgery for patients with pulmonary metastases from colorectal carcinoma. , 2004, The Annals of thoracic surgery.

[71]  B. Eisenberg,et al.  Is Reporting of Recurrence Data Important in Pancreatic Cancer? , 2004, Annals of Surgical Oncology.

[72]  J. Cameron,et al.  The SMAD4 protein and prognosis of pancreatic ductal adenocarcinoma. , 2001, Clinical cancer research : an official journal of the American Association for Cancer Research.

[73]  H. Ueno,et al.  Prognostic Factors in Patients with Metastatic Pancreatic Adenocarcinoma Receiving Systemic Chemotherapy , 2000, Oncology.

[74]  M. Koike,et al.  Hematogenous Metastases of Pancreatic Ductal Carcinoma , 1995, Pancreas.

[75]  Atsushi Fujii,et al.  Patients with Lung Recurrence after Curative Resection forPancreatic Ductal Adenocarcinoma Have a Better Prognosis than Those with Recurrence at Other Sites , 2017 .

[76]  N. Pavlakis,et al.  Patterns and Determinants of Recurrence for Pancreatic Ductal Adenocarcinoma after Resection , 2017 .

[77]  E. Diamandis,et al.  Pancreatic cancer. , 2013, Clinical chemistry.

[78]  H. Taubert,et al.  Elevated expression of microRNAs 155, 203, 210 and 222 in pancreatic tumors is associated with poorer survival , 2010, International journal of cancer.

[79]  W. Leach Carcinoma of the pancreas; a clinical and pathologic analysis of 39 autopsied cases. , 1950, The American journal of pathology.