Evidence map›Paper›PMID 38942992›Full record

ArticleNature medicine2024

Multi-parametric atlas of the pre-metastatic liver for prediction of metastatic outcome in early-stage pancreatic cancer.

Linda Bojmar, Constantinos P Zambirinis, Jonathan M Hernandez, Jayasree Chakraborty, Lee Shaashua, Junbum Kim, Kofi Ennu Johnson, Samer Hanna, Gokce Askan, Jonas Burman and 66 more

2 registry-linked trialsAbstract read
In one paragraph

Article in Nature medicine, 2024. The graph could read no effect estimate from its abstract, so it casts no vote on the map. It is linked to 2 registered trials, which are not on this map. Cited by 48 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
48citing papers in PubMed, 1 pooled it
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

NCT07224724 recruitingnot on this map

Exosome-derived Extrahepatic Metastasis Detection By Liquid Biopsy In Colorectal Cancer Liver Metastases

TypeobservationalSponsorCity of Hope Medical CenterRan2024 to 2028Enrolled500ConditionsColorectal Cancer Liver Metastases (CRLM), Metastatic Colorectal Carcinoma (mCRC)ArmsEXELION
NCT07224802 completednot on this map

An Exosome-based Liquid Biopsy Signature for Preoperative Identification of Occult Liver Metastasis in Patients With Pancreatic Ductal Adenocarcinoma

TypeobservationalSponsorCity of Hope Medical CenterRan2024 to 2026Enrolled372ConditionsPDAC - Pancreatic Ductal AdenocarcinomaArmsEXELiM assay (qRT-PCR validation), EXELiM small RNA sequencing
3 · Its place in the literature

Who cites it

48 citing papers in PubMed, 1 synthesis or guideline pooled it.

  1. Pooled it
  2. Article
  3. Observational
  4. Review
  5. Observational
  6. Review
  7. Article
  8. Review
  9. Article
  10. Review
  11. Pancreatic cancer.Nature reviews. Disease primers · 2026
    Review
  12. Article
  13. Review
  14. Article
  15. Review
  16. Neutrophil extracellular traps in cancer.Nature reviews. Cancer · 2026
    Review
  17. Article
  18. Article
  19. Article
  20. Review
4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

76 authors.

Linda Bojmar *Departments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0002-2684-5824
Constantinos P Zambirinis *Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.ORCID 0000-0003-2740-3259
Jonathan M Hernandez *Hepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Jayasree ChakrabortyHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Lee ShaashuaDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Junbum KimDepartment of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0001-7344-1593
Kofi Ennu JohnsonDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Samer HannaDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Gokce AskanDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Jonas BurmanDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0002-0325-2321
Hiranmayi RavichandranDepartment of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medicine, New York, NY, USA.
Jian ZhengHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Joshua S JolissaintDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Rami SroujiDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Yi SongHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Ankur ChoubeyHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0001-9930-0609
Han Sang KimDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Michele CioffiDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Elke van BeekHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Carlie SigelDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Jose JessurunDepartment of Pathology and Laboratory Medicine, Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0002-1692-9880
Paulina Velasco RiestraDepartment of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.ORCID 0000-0001-7145-2619
Hakon BlomstrandDepartment of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.ORCID 0000-0002-9845-1410
Carolin JönssonDepartment of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.
Anette JönssonDepartment of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.
Pernille LauritzenDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Weston BuehringDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Yonathan ArarsoDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Dylanne HernandezDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Jessica P Vinagolu-BaurDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Madison FriedmanDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Caroline GliddenDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Laetitia FirmenichDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Grace LiebermanDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Dianna L MejiaDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Naaz NasarHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0009-0004-2232-1590
Anders P MutveiDepartment of Laboratory Medicine, Division of Pathology, Karolinska Institutet, Stockholm, Sweden.
Doru M PaulDivision of Hematology and Medical Oncology, Department of Medicine, Weill Cornell Medicine, New York, NY, USA.
Yaron BramDivision of Gastroenterology & Hepatology, Weill Cornell Medicine, New York, NY, USA.
Bruno Costa-SilvaDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Olca BasturkDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0003-2747-1366
Nancy BoudreauDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Haiying ZhangDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
Irina R MateiDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0002-5712-8430
Ayuko HoshinoDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA.
David KelsenDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Irit SagiDepartment of Biological Regulation, Weizmann Institute of Science, Rehovot, Israel.
Avigdor ScherzDepartment of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel.ORCID 0000-0002-8583-2169
Ruth Scherz-ShouvalDepartment of Biomolecular Sciences, Weizmann Institute of Science, Rehovot, Israel.ORCID 0000-0002-4570-121X
Yosef YardenDepartment of Biological Regulation, Weizmann Institute of Science, Rehovot, Israel.ORCID 0000-0003-4168-7884
Moshe OrenDepartment of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.ORCID 0000-0003-4311-7172
Mikala EgebladCold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
Jason S LewisRadiology and Molecular Pharmacology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0001-7065-4534
Kayvan KeshariDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Paul M GrandgenettEppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, NE, USA.
Michael A HollingsworthEppley Institute for Research in Cancer and Allied Diseases, Fred & Pamela Buffett Cancer Center, University of Nebraska Medical Center, Omaha, NE, USA.ORCID 0000-0002-5255-8888
Vinagolu K RajasekharOrthopedic Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
John H HealeyOrthopedic Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0002-0802-1186
Bergthor BjörnssonDepartment of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.ORCID 0000-0001-9704-1260
Diane M SimeonePerlmutter Cancer Center, New York University Langone Health, New York, NY, USA.ORCID 0000-0001-5142-3087
David A TuvesonCold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
Christine A Iacobuzio-DonahueDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0002-4672-3023
Jaqueline BrombergDepartment of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0002-7957-9339
C Theresa VincentDepartment of Laboratory Medicine, Division of Pathology, Karolinska Institutet, Stockholm, Sweden.
Eileen M O'ReillyDavid M. Rubenstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0002-8076-9199
Ronald P DeMatteoHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Vinod P BalachandranHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0002-2956-223X
Michael I D'AngelicaHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
T Peter KinghamHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Peter J AllenHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Amber L SimpsonHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.ORCID 0000-0002-4387-8417
Olivier ElementoDepartment of Physiology and Biophysics, Institute for Computational Biomedicine, Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0002-8061-9617
Per SandströmDepartment of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.
Robert E SchwartzDivision of Gastroenterology & Hepatology, Weill Cornell Medicine, New York, NY, USA.ORCID 0000-0002-5417-5995
William R JarnaginHepatopancreatobiliary Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
David LydenDepartments of Pediatrics and Cell and Developmental Biology, Children's Cancer and Blood Foundation Laboratories, Drukier Institute for Children's Health, Meyer Cancer Center Weill Cornell Medicine, New York, NY, USA. dcl2001@med.cornell.edu.ORCID 0000-0003-0193-4131

Funding

X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI Nicholas D Socci · 1985 to 2026
$347.4M
Clinical and Translational Science AwardUL1TR001873 · NCATS · COLUMBIA UNIVERSITY HEALTH SCIENCES · PI REILLY, MUREDACH P · 2016 to 2025
$99.0M
Disparities in COVID Disease Severity and Outcomes in New York CityUL1TR002384 · NCATS · WEILL MEDICAL COLL OF CORNELL UNIV · PI JULIANNE L IMPERATO-MCGINLEY · 2017 to 2026
$86.2M
Clinical and Translational Science CenterUL1TR000457 · NCATS · WEILL MEDICAL COLL OF CORNELL UNIV · PI IMPERATO-MCGINLEY, JULIANNE L · 2012 to 2016
$46.0M
Pancreatic Cancer Detection ConsortiumU01CA210240 · NCI · UNIVERSITY OF NEBRASKA MEDICAL CENTER · PI Michael A. Hollingsworth · 2017 to 2026
$12.9M
Principal ProjectU19AI144301 · NIAID · WEILL MEDICAL COLL OF CORNELL UNIV · PI Maria Virginia Pascual · 2019 to 2026
$9.9M
Systemic regulation of metastasisR35CA232093 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI LYDEN, DAVID CHARLES · 2018 to 2024
$7.0M
Tumor-derived extracellular vesicles in the pre-metastatic niche.R01CA207983 · NCI · CHILDREN'S HOSPITAL OF LOS ANGELES · PI Yves A DeClerck · 2017 to 2026
$5.6M
Development and application of asymmetric-flow field-flow (AF4) technology in fractionation and characterization of exosome subpopulations and novel nanoveiscles in pancreatic cancer modelR01CA218513 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI Jacob Geri, DAVID CHARLES LYDEN · 2017 to 2026
$4.3M
Role of N-Cadherin in Pancreatic Tumor MicroenvironmentU54CA163120 · NCI · UNIVERSITY OF NEBRASKA MEDICAL CENTER · PI BATRA, SURINDER K. · 2011 to 2015
$4.2M
Defining neoantigen immunodominance for antigen selection and biomarker discovery in human pancreatic cancer immunotherapyU01CA224175 · NCI · SLOAN-KETTERING INST CAN RESEARCH · PI BALACHANDRAN, VINOD P, LEACH, STEVEN D · 2017 to 2021
$3.1M
Characterization and Functional Analysis of Breast Cancer Secreted Exosomes in MaU01CA169538 · NCI · WEILL MEDICAL COLL OF CORNELL UNIV · PI BISSELL, MINA, LYDEN, DAVID CHARLES · 2012 to 2016
$2.9M
Cancerfonden (Swedish Cancer Society) 21 1824 Pj 01 HNCATS NIH HHS UL1 TR000457NCATS NIH HHS UL1 TR001873NCATS NIH HHS UL1 TR002384NCI NIH HHS P30 CA008748NCI NIH HHS R01 CA169416NCI NIH HHS R01 CA207983NCI NIH HHS R01 CA218513NCI NIH HHS R01 CA234614NCI NIH HHS R35 CA232093NCI NIH HHS R50 CA211462NCI NIH HHS U01 CA169538NCI NIH HHS U01 CA210240NCI NIH HHS U01 CA224175NCI NIH HHS U54 CA163117NCI NIH HHS U54 CA163120NIAID NIH HHS U19 AI144301NIDDK NIH HHS R01 DK121072Svenska Sällskapet för Medicinsk Forskning (Swedish Society for Medical Research) grant no. S21-0079Svenska Sällskapet för Medicinsk Forskning (Swedish Society for Medical Research) TG-23-0306Vetenskapsrådet (Swedish Research Council) 2021-600 02356
6 · The paper itself

Abstract

Metastasis occurs frequently after resection of pancreatic cancer (PaC). In this study, we hypothesized that multi-parametric analysis of pre-metastatic liver biopsies would classify patients according to their metastatic risk, timing and organ site. Liver biopsies obtained during pancreatectomy from 49 patients with localized PaC and 19 control patients with non-cancerous pancreatic lesions were analyzed, combining metabolomic, tissue and single-cell transcriptomics and multiplex imaging approaches. Patients were followed prospectively (median 3 years) and classified into four recurrence groups; early (<6 months after resection) or late (>6 months after resection) liver metastasis (LiM); extrahepatic metastasis (EHM); and disease-free survivors (no evidence of disease (NED)). Overall, PaC livers exhibited signs of augmented inflammation compared to controls. Enrichment of neutrophil extracellular traps (NETs), Ki-67 upregulation and decreased liver creatine significantly distinguished those with future metastasis from NED. Patients with future LiM were characterized by scant T cell lobular infiltration, less steatosis and higher levels of citrullinated H3 compared to patients who developed EHM, who had overexpression of interferon target genes (MX1 and NR1D1) and an increase of CD11B

Indexed as

LiverLiver NeoplasmsPancreatic NeoplasmsAgedBiopsyExtracellular TrapsFemaleHumansMaleMiddle AgedNeoplasm StagingPancreatectomyPrognosis

Identifiers

PMID38942992
PMCPMC11416063

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Registered trials

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.