Non-Small Cell Lung Cancer Patients with Skip-N2 Metastases Have Similar Survival to N1 Patients—A Multicenter Analysis

Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20–30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N...

Full description

Saved in:
Bibliographic Details
Published inJournal of personalized medicine Vol. 15; no. 3; p. 113
Main Authors Schlachtenberger, Georg, Schallenberg, Simon, Doerr, Fabian, Menghesha, Hruy, Gaisendrees, Christopher, Amorin, Andres, Lopez-Pastorini, Alberto, Büettner, Reinhard, Quaas, Alexander, Horst, David, Klauschen, Frederick, Frost, Nikolaj, Rueckert, Jens C., Neudecker, Jens, Hekmat, Khosro, Heldwein, Matthias B.
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 14.03.2025
MDPI
Subjects
Online AccessGet full text
ISSN2075-4426
2075-4426
DOI10.3390/jpm15030113

Cover

Loading…
Abstract Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20–30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N2 patients may have comparable long-term survival, considering their similar tumor stages. However, this conclusion remains controversial. Therefore, we carried out this multicenter study to examine the long-term survival and disease-free interval (DFI) of N0N2- and N1 patients. Methods: One-, three-, and five-year survival rates were measured. Kaplan–Meier curves and a Cox proportional hazards model assessed survival and were used to identify prognostic factors for overall survival. Results: Between January 2010 and December 2020, 273 N0N2 and N1 patients were included in our analysis. Of those patients, 77 showed N0N2 and 196 N1. Baseline characteristics did not differ significantly between groups. Between N0N2 and N1 patients, there were no significant differences in one- (p = 0.67), three- (p = 0.20), and five-year (p = 0.27) survival. Furthermore, DFI did not differ between groups (p = 0.45). Conclusions: Our findings indicate that N0N2 patients have a prognosis comparable to that of patients with N1 disease. These results indicate that patients with N0N2 have a similar prognosis to N1 patients. N2-NSCLC is heterogeneous and would benefit from a more precise subdivision and differential treatment in the upcoming UICC 9 classification. The following question remains: are we overtreating N0N2 patients or undertreating N1 patients?
AbstractList Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20-30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N2 patients may have comparable long-term survival, considering their similar tumor stages. However, this conclusion remains controversial. Therefore, we carried out this multicenter study to examine the long-term survival and disease-free interval (DFI) of N0N2- and N1 patients. One-, three-, and five-year survival rates were measured. Kaplan-Meier curves and a Cox proportional hazards model assessed survival and were used to identify prognostic factors for overall survival. Between January 2010 and December 2020, 273 N0N2 and N1 patients were included in our analysis. Of those patients, 77 showed N0N2 and 196 N1. Baseline characteristics did not differ significantly between groups. Between N0N2 and N1 patients, there were no significant differences in one- ( = 0.67), three- ( = 0.20), and five-year ( = 0.27) survival. Furthermore, DFI did not differ between groups ( = 0.45). Our findings indicate that N0N2 patients have a prognosis comparable to that of patients with N1 disease. These results indicate that patients with N0N2 have a similar prognosis to N1 patients. N2-NSCLC is heterogeneous and would benefit from a more precise subdivision and differential treatment in the upcoming UICC 9 classification. The following question remains: are we overtreating N0N2 patients or undertreating N1 patients?
Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20–30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N2 patients may have comparable long-term survival, considering their similar tumor stages. However, this conclusion remains controversial. Therefore, we carried out this multicenter study to examine the long-term survival and disease-free interval (DFI) of N0N2- and N1 patients. Methods: One-, three-, and five-year survival rates were measured. Kaplan–Meier curves and a Cox proportional hazards model assessed survival and were used to identify prognostic factors for overall survival. Results: Between January 2010 and December 2020, 273 N0N2 and N1 patients were included in our analysis. Of those patients, 77 showed N0N2 and 196 N1. Baseline characteristics did not differ significantly between groups. Between N0N2 and N1 patients, there were no significant differences in one- ( p = 0.67), three- ( p = 0.20), and five-year ( p = 0.27) survival. Furthermore, DFI did not differ between groups ( p = 0.45). Conclusions: Our findings indicate that N0N2 patients have a prognosis comparable to that of patients with N1 disease. These results indicate that patients with N0N2 have a similar prognosis to N1 patients. N2-NSCLC is heterogeneous and would benefit from a more precise subdivision and differential treatment in the upcoming UICC 9 classification. The following question remains: are we overtreating N0N2 patients or undertreating N1 patients?
Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20-30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N2 patients may have comparable long-term survival, considering their similar tumor stages. However, this conclusion remains controversial. Therefore, we carried out this multicenter study to examine the long-term survival and disease-free interval (DFI) of N0N2- and N1 patients. Methods: One-, three-, and five-year survival rates were measured. Kaplan-Meier curves and a Cox proportional hazards model assessed survival and were used to identify prognostic factors for overall survival. Results: Between January 2010 and December 2020, 273 N0N2 and N1 patients were included in our analysis. Of those patients, 77 showed N0N2 and 196 N1. Baseline characteristics did not differ significantly between groups. Between N0N2 and N1 patients, there were no significant differences in one- (p = 0.67), three- (p = 0.20), and five-year (p = 0.27) survival. Furthermore, DFI did not differ between groups (p = 0.45). Conclusions: Our findings indicate that N0N2 patients have a prognosis comparable to that of patients with N1 disease. These results indicate that patients with N0N2 have a similar prognosis to N1 patients. N2-NSCLC is heterogeneous and would benefit from a more precise subdivision and differential treatment in the upcoming UICC 9 classification. The following question remains: are we overtreating N0N2 patients or undertreating N1 patients?Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20-30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N2 patients may have comparable long-term survival, considering their similar tumor stages. However, this conclusion remains controversial. Therefore, we carried out this multicenter study to examine the long-term survival and disease-free interval (DFI) of N0N2- and N1 patients. Methods: One-, three-, and five-year survival rates were measured. Kaplan-Meier curves and a Cox proportional hazards model assessed survival and were used to identify prognostic factors for overall survival. Results: Between January 2010 and December 2020, 273 N0N2 and N1 patients were included in our analysis. Of those patients, 77 showed N0N2 and 196 N1. Baseline characteristics did not differ significantly between groups. Between N0N2 and N1 patients, there were no significant differences in one- (p = 0.67), three- (p = 0.20), and five-year (p = 0.27) survival. Furthermore, DFI did not differ between groups (p = 0.45). Conclusions: Our findings indicate that N0N2 patients have a prognosis comparable to that of patients with N1 disease. These results indicate that patients with N0N2 have a similar prognosis to N1 patients. N2-NSCLC is heterogeneous and would benefit from a more precise subdivision and differential treatment in the upcoming UICC 9 classification. The following question remains: are we overtreating N0N2 patients or undertreating N1 patients?
Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis, occurs in approximately 20–30% of patients. According to the International Association for the Study of Lung Cancer, N1 and N0N2 patients may have comparable long-term survival, considering their similar tumor stages. However, this conclusion remains controversial. Therefore, we carried out this multicenter study to examine the long-term survival and disease-free interval (DFI) of N0N2- and N1 patients. Methods: One-, three-, and five-year survival rates were measured. Kaplan–Meier curves and a Cox proportional hazards model assessed survival and were used to identify prognostic factors for overall survival. Results: Between January 2010 and December 2020, 273 N0N2 and N1 patients were included in our analysis. Of those patients, 77 showed N0N2 and 196 N1. Baseline characteristics did not differ significantly between groups. Between N0N2 and N1 patients, there were no significant differences in one- (p = 0.67), three- (p = 0.20), and five-year (p = 0.27) survival. Furthermore, DFI did not differ between groups (p = 0.45). Conclusions: Our findings indicate that N0N2 patients have a prognosis comparable to that of patients with N1 disease. These results indicate that patients with N0N2 have a similar prognosis to N1 patients. N2-NSCLC is heterogeneous and would benefit from a more precise subdivision and differential treatment in the upcoming UICC 9 classification. The following question remains: are we overtreating N0N2 patients or undertreating N1 patients?
Audience Academic
Author Gaisendrees, Christopher
Frost, Nikolaj
Heldwein, Matthias B.
Horst, David
Hekmat, Khosro
Lopez-Pastorini, Alberto
Doerr, Fabian
Rueckert, Jens C.
Quaas, Alexander
Amorin, Andres
Büettner, Reinhard
Klauschen, Frederick
Schlachtenberger, Georg
Menghesha, Hruy
Schallenberg, Simon
Neudecker, Jens
AuthorAffiliation 5 Department of Thoracic Surgery, Helios Clinic Bonn/Rhein-Sieg Bonn, 53123 Bonn, Germany
9 Department of Surgery, Charité—Universitätsmedizin Berlin, 10117 Berlin, Germany; jens-c.rueckert@charite.de (J.C.R.); jens.neudecker@charite.de (J.N.)
7 Department of Pathology, University Hospital of Cologne, 50937 Cologne, Germany; reinhard.buettner@uk-koeln.de (R.B.); alexander.quaas@uk-koeln.de (A.Q.)
8 Department of Infectious Diseases and Respiratory Medicine, Charité—Universitätsmedizin Berlin, 10117 Berlin, Germany; nikolaj.frost@charite.de
2 Department of General, Visceral and Thoracic Surgery, University Hospital of Cologne, 50937 Cologne, Germany; andres.amorin-estremadoyro@uk-koeln.de (A.A.); alberto.lopez-pastorini@uk-koeln.de (A.L.-P.); khosro.hekmat@uk-koeln.de (K.H.); matthias.heldwein@uk-koeln.de (M.B.H.)
4 Department of Thoracic Surgery, University Medicine Essen—Ruhrlandklinik, University Duisburg-Essen, 47057 Duisburg, Germany
1 Department of Thoracic Surgery, Hildegardis Hospital
AuthorAffiliation_xml – name: 6 Department of Cardiac Surgery, University Hospital of Cologne, 50937 Cologne, Germany; christopher.gaisendrees@uk-koeln.de
– name: 8 Department of Infectious Diseases and Respiratory Medicine, Charité—Universitätsmedizin Berlin, 10117 Berlin, Germany; nikolaj.frost@charite.de
– name: 1 Department of Thoracic Surgery, Hildegardis Hospital Cologne, Bachemer Strasse 29–33, 50931 Cologne, Germany
– name: 2 Department of General, Visceral and Thoracic Surgery, University Hospital of Cologne, 50937 Cologne, Germany; andres.amorin-estremadoyro@uk-koeln.de (A.A.); alberto.lopez-pastorini@uk-koeln.de (A.L.-P.); khosro.hekmat@uk-koeln.de (K.H.); matthias.heldwein@uk-koeln.de (M.B.H.)
– name: 7 Department of Pathology, University Hospital of Cologne, 50937 Cologne, Germany; reinhard.buettner@uk-koeln.de (R.B.); alexander.quaas@uk-koeln.de (A.Q.)
– name: 3 Department of Pathology, Charité—Universitätsmedizin Berlin, 10117 Berlin, Germany david.horst@charite.de (D.H.); frederick.klauschen@med.uni-muenchen.de (F.K.)
– name: 4 Department of Thoracic Surgery, University Medicine Essen—Ruhrlandklinik, University Duisburg-Essen, 47057 Duisburg, Germany
– name: 5 Department of Thoracic Surgery, Helios Clinic Bonn/Rhein-Sieg Bonn, 53123 Bonn, Germany
– name: 9 Department of Surgery, Charité—Universitätsmedizin Berlin, 10117 Berlin, Germany; jens-c.rueckert@charite.de (J.C.R.); jens.neudecker@charite.de (J.N.)
Author_xml – sequence: 1
  givenname: Georg
  orcidid: 0000-0001-7118-8432
  surname: Schlachtenberger
  fullname: Schlachtenberger, Georg
– sequence: 2
  givenname: Simon
  orcidid: 0000-0002-7897-7116
  surname: Schallenberg
  fullname: Schallenberg, Simon
– sequence: 3
  givenname: Fabian
  orcidid: 0000-0002-0878-0406
  surname: Doerr
  fullname: Doerr, Fabian
– sequence: 4
  givenname: Hruy
  surname: Menghesha
  fullname: Menghesha, Hruy
– sequence: 5
  givenname: Christopher
  surname: Gaisendrees
  fullname: Gaisendrees, Christopher
– sequence: 6
  givenname: Andres
  surname: Amorin
  fullname: Amorin, Andres
– sequence: 7
  givenname: Alberto
  orcidid: 0000-0002-9738-5394
  surname: Lopez-Pastorini
  fullname: Lopez-Pastorini, Alberto
– sequence: 8
  givenname: Reinhard
  orcidid: 0000-0001-8806-4786
  surname: Büettner
  fullname: Büettner, Reinhard
– sequence: 9
  givenname: Alexander
  orcidid: 0000-0002-3537-6011
  surname: Quaas
  fullname: Quaas, Alexander
– sequence: 10
  givenname: David
  surname: Horst
  fullname: Horst, David
– sequence: 11
  givenname: Frederick
  surname: Klauschen
  fullname: Klauschen, Frederick
– sequence: 12
  givenname: Nikolaj
  orcidid: 0000-0001-7452-7129
  surname: Frost
  fullname: Frost, Nikolaj
– sequence: 13
  givenname: Jens C.
  surname: Rueckert
  fullname: Rueckert, Jens C.
– sequence: 14
  givenname: Jens
  surname: Neudecker
  fullname: Neudecker, Jens
– sequence: 15
  givenname: Khosro
  surname: Hekmat
  fullname: Hekmat, Khosro
– sequence: 16
  givenname: Matthias B.
  surname: Heldwein
  fullname: Heldwein, Matthias B.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/40137429$$D View this record in MEDLINE/PubMed
BookMark eNptkluPEyEUx4lZ417cJ98NiS8mm1m5DTM8maZR16RbTarPhAGmS52BLszU9M0P4Sf0k0jTtXaNQLj-zh_O4ZyDEx-8BeAFRteUCvRmte5xiSjCmD4BZwRVZcEY4SdH81NwmdIK5VKXhHD0DJwyhGnFiDgD23nwxaJXXQenNnez0S_hVHltI_ysBmf9kOB3N9zBxTe3LuYE3tpBpdxsgjdqY-HC9a5TES7GuHEb1cEhwDk-GP_68XMCb8ducDovs-rEq26bXHoOnraqS_byYbwAX9-_-zK9KWafPnycTmaFpiWhBTdVU6umxI1ABhnWKEJEZY3SBGEjKt2UoiKWYNNQYoigDJda1BTrWrWIN_QCvN3rrsemt2b3iqg6uY6uV3Erg3Ly8Yl3d3IZNhJjwSjndVZ4_aAQw_1o0yB7l3SOlvI2jElSXOdwYs5QRl_9g67CGLPHe6pEjHPxl1qqzkrn25Av1jtROalpVQpRVSRT1_-hcjW2dzqnQevy_iODl8eeHlz889sZuNoDOoaUom0PCEZyl07yKJ3ob_X2u1c
Cites_doi 10.1002/ca.20790
10.1093/ejcts/ezad247
10.1016/S0140-6736(21)02098-5
10.1016/j.annonc.2022.12.009
10.3322/caac.21660
10.6004/jnccn.2204.0023
10.1016/j.cllc.2023.06.007
10.1093/ejcts/ezaa215
10.3389/fsurg.2021.749156
10.1016/S1470-2045(21)00606-9
10.1016/j.chest.2024.05.026
10.1056/NEJMoa2027071
10.3390/cancers13061326
10.21037/jtd.2018.07.125
10.1093/annonc/mdx222
10.1016/j.cllc.2020.02.027
10.1016/j.cllc.2018.12.007
10.1016/j.annonc.2022.12.013
10.1016/j.athoracsur.2004.06.081
10.1056/NEJMoa2202170
10.1016/j.suronc.2020.11.019
10.1016/j.jtcvs.2004.06.016
ContentType Journal Article
Copyright COPYRIGHT 2025 MDPI AG
2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2025 by the authors. 2025
Copyright_xml – notice: COPYRIGHT 2025 MDPI AG
– notice: 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2025 by the authors. 2025
DBID AAYXX
CITATION
NPM
8FE
8FH
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
GNUQQ
HCIFZ
LK8
M7P
PHGZM
PHGZT
PIMPY
PKEHL
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
7X8
5PM
DOI 10.3390/jpm15030113
DatabaseName CrossRef
PubMed
ProQuest SciTech Collection
ProQuest Natural Science Collection
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
ProQuest One
ProQuest Central
ProQuest Central Student
SciTech Premium Collection
Biological Sciences
Biological Science Database
ProQuest Central Premium
ProQuest One Academic
Publicly Available Content Database
ProQuest One Academic Middle East (New)
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
PubMed
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Biological Science Collection
ProQuest Central Essentials
ProQuest One Academic Eastern Edition
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
Biological Science Database
ProQuest SciTech Collection
ProQuest Central China
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Academic UKI Edition
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
ProQuest Central (New)
ProQuest One Academic
ProQuest One Academic (New)
MEDLINE - Academic
DatabaseTitleList PubMed

MEDLINE - Academic
CrossRef
Publicly Available Content Database

Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
EISSN 2075-4426
ExternalDocumentID PMC11943668
A837599772
40137429
10_3390_jpm15030113
Genre Journal Article
GeographicLocations Germany
GeographicLocations_xml – name: Germany
GroupedDBID 53G
5VS
8FE
8FH
AADQD
AAFWJ
AAYXX
ADBBV
AFKRA
AFZYC
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
CCPQU
CITATION
DIK
EMOBN
GX1
HCIFZ
HYE
IAO
IHR
ITC
KQ8
LK8
M48
M7P
MODMG
M~E
OK1
PGMZT
PHGZM
PHGZT
PIMPY
PROAC
RPM
NPM
PMFND
ABUWG
AZQEC
DWQXO
GNUQQ
PKEHL
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
7X8
5PM
ID FETCH-LOGICAL-c3523-6d7b8ab51b90d0d4ba2297edac201d97cb5972e21db32d293415c9831c8af06b3
IEDL.DBID M48
ISSN 2075-4426
IngestDate Thu Aug 21 18:39:40 EDT 2025
Fri Jul 11 18:57:25 EDT 2025
Fri Jul 18 09:40:38 EDT 2025
Tue Jun 17 21:56:54 EDT 2025
Tue Jun 10 20:59:16 EDT 2025
Sat Mar 29 01:29:42 EDT 2025
Tue Jul 01 05:22:03 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 3
Keywords non-small cell lung cancer
lymph nodes
N1 lymph nodes
skip-N2 metastases
Language English
License https://creativecommons.org/licenses/by/4.0
Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c3523-6d7b8ab51b90d0d4ba2297edac201d97cb5972e21db32d293415c9831c8af06b3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
ORCID 0000-0001-7118-8432
0000-0002-7897-7116
0000-0001-7452-7129
0000-0001-8806-4786
0000-0002-9738-5394
0000-0002-3537-6011
0000-0002-0878-0406
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.3390/jpm15030113
PMID 40137429
PQID 3181504669
PQPubID 2032376
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_11943668
proquest_miscellaneous_3181371640
proquest_journals_3181504669
gale_infotracmisc_A837599772
gale_infotracacademiconefile_A837599772
pubmed_primary_40137429
crossref_primary_10_3390_jpm15030113
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 20250314
PublicationDateYYYYMMDD 2025-03-14
PublicationDate_xml – month: 3
  year: 2025
  text: 20250314
  day: 14
PublicationDecade 2020
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
– name: Basel
PublicationTitle Journal of personalized medicine
PublicationTitleAlternate J Pers Med
PublicationYear 2025
Publisher MDPI AG
MDPI
Publisher_xml – name: MDPI AG
– name: MDPI
References Topol (ref_12) 2009; 22
Riely (ref_20) 2024; 22
Felip (ref_23) 2021; 398
Detterbeck (ref_28) 2024; 166
Schlachtenberger (ref_6) 2021; 38
ref_19
Seyrek (ref_9) 2021; 27
Asamura (ref_10) 2015; 10
Riquet (ref_13) 2005; 79
ref_16
Morgensztern (ref_3) 2010; 5
Forde (ref_25) 2022; 386
Vicente (ref_24) 2021; 16
Sung (ref_1) 2021; 71
Goldstraw (ref_11) 2016; 11
Kirmani (ref_26) 2018; 10
Chiappetta (ref_15) 2023; 24
Wang (ref_27) 2019; 20
Hendriks (ref_5) 2023; 34
Pourel (ref_21) 2022; 23
Schlachtenberger (ref_7) 2023; 64
Wu (ref_22) 2020; 383
Postmus (ref_2) 2017; 28
Chiappetta (ref_14) 2020; 58
Okada (ref_17) 2005; 129
Wang (ref_8) 2020; 21
ref_4
Hendriks (ref_18) 2023; 34
References_xml – volume: 22
  start-page: 509
  year: 2009
  ident: ref_12
  article-title: The problem of direct lymph drainage of the bronchopulmonary segments into the mediastinal and hilar lymph nodes
  publication-title: Clin. Anat.
  doi: 10.1002/ca.20790
– volume: 10
  start-page: 1675
  year: 2015
  ident: ref_10
  article-title: The International Association for the Study of Lung Cancer Lung Cancer Staging Project: Proposals for the Revision of the N Descriptors in the Forthcoming 8th Edition of the TNM Classification for Lung Cancer
  publication-title: J. Thorac. Oncol. Off. Publ. Int. Assoc. Study Lung Cancer
– volume: 64
  start-page: ezad274
  year: 2023
  ident: ref_7
  article-title: Do skip-N2 metastases significantly impact overall survival and disease-free interval in N2 non-small-cell lung cancer patients? A multicentre analysis
  publication-title: Eur. J. Cardio-Thorac. Surg. Off. J. Eur. Assoc. Cardio-Thorac. Surg.
  doi: 10.1093/ejcts/ezad247
– volume: 398
  start-page: 1344
  year: 2021
  ident: ref_23
  article-title: Adjuvant atezolizumab after adjuvant chemotherapy in resected stage IB-IIIA non-small-cell lung cancer (IMpower010): A randomised, multicentre, open-label, phase 3 trial
  publication-title: Lancet
  doi: 10.1016/S0140-6736(21)02098-5
– volume: 34
  start-page: 339
  year: 2023
  ident: ref_18
  article-title: Oncogene-addicted metastatic non-small-cell lung cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up
  publication-title: Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. Off. J. Eur. Soc. Med.
  doi: 10.1016/j.annonc.2022.12.009
– volume: 11
  start-page: 39
  year: 2016
  ident: ref_11
  article-title: The IASLC Lung Cancer Staging Project: Proposals for Revision of the TNM Stage Groupings in the Forthcoming (Eighth) Edition of the TNM Classification for Lung Cancer
  publication-title: J. Thorac. Oncol. Off. Publ. Int. Assoc. Study Lung Cancer
– volume: 27
  start-page: 304
  year: 2021
  ident: ref_9
  article-title: The Significance of Skip Mediastinal Lymph Node Metastasis in the Prognosis of Patients with Resected Non-Small-Cell Lung Carcinoma: Is It Really a Better N2 Disease Subtype?
  publication-title: Ann. Thorac. Cardiovasc. Surg. Off. J. Assoc. Thorac. Cardiovasc. Surg. Asia
– volume: 71
  start-page: 209
  year: 2021
  ident: ref_1
  article-title: Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries
  publication-title: CA A Cancer J. Clin.
  doi: 10.3322/caac.21660
– volume: 22
  start-page: 249
  year: 2024
  ident: ref_20
  article-title: Non-Small Cell Lung Cancer, Version 4.2024, NCCN Clinical Practice Guidelines in Oncology
  publication-title: J. Natl. Compr. Cancer Netw. JNCCN
  doi: 10.6004/jnccn.2204.0023
– volume: 24
  start-page: e275
  year: 2023
  ident: ref_15
  article-title: Non-Small Cell Lung Cancer With N1 Involvement or Skip Metastases Presents the Same Survival Outcome: Results From a Multicentric Study
  publication-title: Clin. Lung Cancer
  doi: 10.1016/j.cllc.2023.06.007
– volume: 58
  start-page: 1236
  year: 2020
  ident: ref_14
  article-title: External validation of the N descriptor in the proposed tumour-node-metastasis subclassification for lung cancer: The crucial role of histological type, number of resected nodes and adjuvant therapy
  publication-title: Eur. J. Cardio-Thorac. Surg. Off. J. Eur. Assoc. Cardio-Thorac. Surg.
  doi: 10.1093/ejcts/ezaa215
– ident: ref_4
  doi: 10.3389/fsurg.2021.749156
– volume: 23
  start-page: 104
  year: 2022
  ident: ref_21
  article-title: Postoperative radiotherapy versus no postoperative radiotherapy in patients with completely resected non-small-cell lung cancer and proven mediastinal N2 involvement (Lung ART): An open-label, randomised, phase 3 trial
  publication-title: Lancet Oncol.
  doi: 10.1016/S1470-2045(21)00606-9
– volume: 16
  start-page: 860
  year: 2021
  ident: ref_24
  article-title: Four-Year Survival With Durvalumab After Chemoradiotherapy in Stage III NSCLC-an Update From the PACIFIC Trial
  publication-title: J. Thorac. Oncol. Off. Publ. Int. Assoc. Study Lung Cancer
– volume: 166
  start-page: 882
  year: 2024
  ident: ref_28
  article-title: The Proposed Ninth Edition TNM Classification of Lung Cancer
  publication-title: Chest
  doi: 10.1016/j.chest.2024.05.026
– volume: 383
  start-page: 1711
  year: 2020
  ident: ref_22
  article-title: Osimertinib in Resected EGFR-Mutated Non-Small-Cell Lung Cancer
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMoa2027071
– ident: ref_16
  doi: 10.3390/cancers13061326
– volume: 10
  start-page: 4806
  year: 2018
  ident: ref_26
  article-title: Long term and disease-free survival following surgical resection of occult N2 lung cancer
  publication-title: J. Thorac. Dis.
  doi: 10.21037/jtd.2018.07.125
– volume: 5
  start-page: 29
  year: 2010
  ident: ref_3
  article-title: Trends in stage distribution for patients with non-small cell lung cancer: A National Cancer Database survey
  publication-title: J. Thorac. Off. Publ. Int. Assoc. Study Lung Cancer
– volume: 28
  start-page: iv1
  year: 2017
  ident: ref_2
  article-title: Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up
  publication-title: Ann. Oncol. Off. J. Eur. Soc. Med. Oncol.
  doi: 10.1093/annonc/mdx222
– volume: 21
  start-page: e423
  year: 2020
  ident: ref_8
  article-title: Skip N2 Metastasis in Pulmonary Adenocarcinoma: Good Prognosis Similar to N1 Disease
  publication-title: Clin. Lung Cancer
  doi: 10.1016/j.cllc.2020.02.027
– volume: 20
  start-page: e346
  year: 2019
  ident: ref_27
  article-title: Role of Skip Mediastinal Lymph Node Metastasis for Patients With Resectable Non-small-cell Lung Cancer: A Propensity Score Matching Analysis
  publication-title: Clin. Lung Cancer
  doi: 10.1016/j.cllc.2018.12.007
– volume: 34
  start-page: 358
  year: 2023
  ident: ref_5
  article-title: Non-oncogene-addicted metastatic non-small-cell lung cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up
  publication-title: Ann. Oncol. Off. J. Euro-Pean Soc. Med.
  doi: 10.1016/j.annonc.2022.12.013
– ident: ref_19
– volume: 79
  start-page: 225
  year: 2005
  ident: ref_13
  article-title: Skip mediastinal lymph node metastasis and lung cancer: A particular N2 subgroup with a better prognosis
  publication-title: Ann. Thorac. Surg.
  doi: 10.1016/j.athoracsur.2004.06.081
– volume: 386
  start-page: 1973
  year: 2022
  ident: ref_25
  article-title: Neoadjuvant Nivolumab plus Chemotherapy in Resectable Lung Cancer
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMoa2202170
– volume: 38
  start-page: 101505
  year: 2021
  ident: ref_6
  article-title: Postoperative long-term survival of non-small cell lung cancer patients with skip-N2 metastases
  publication-title: Surg. Oncol.
  doi: 10.1016/j.suronc.2020.11.019
– volume: 129
  start-page: 825
  year: 2005
  ident: ref_17
  article-title: Border between N1 and N2 stations in lung carcinoma: Lessons from lymph node metastatic patterns of lower lobe tumors
  publication-title: J. Thorac. Cardiovasc. Surg.
  doi: 10.1016/j.jtcvs.2004.06.016
SSID ssj0000852260
Score 2.2855868
Snippet Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of...
Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of N1 metastasis,...
Introduction: Nodal involvement is one of the most important prognostic factors in NSCLC. Skip-N2 metastasis (N0N2), which is N2 metastasis in the absence of...
SourceID pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Access Repository
Aggregation Database
Index Database
StartPage 113
SubjectTerms Cancer
Cancer therapies
Care and treatment
Lung cancer
Lung cancer, Non-small cell
Lymphatic system
Medical prognosis
Metastases
Metastasis
Mortality
Non-small cell lung carcinoma
Oncology, Experimental
Ostomy
Patient outcomes
Prognosis
Regression analysis
Small cell lung carcinoma
Survival analysis
Thoracic surgery
Tomography
Tumors
SummonAdditionalLinks – databaseName: ProQuest Central
  dbid: BENPR
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwELaglRAXVN6hBRmpEieriZ04zgktq1YrRKOKpVJvkV8rFrrJ0uwiceNH9Bf2lzCz8YYNBy65-BHLM575ZjyeIeRYFVL7VDqmpHEsNXnGVGGRIJnONfeYYwqjLUo5uUw_XmVXweHWhrDKrUzcCGrXWPSRnwDvAXZJpSzeL38wrBqFt6uhhMZ9sg8iWAGH7384LS8-914WABSAL-LuYZ4A-_7k23IB8yBbi4Eq-lcg72ikYbTkjvo5OyCPAm6ko47Qj8k9Xz8hD87DzfhT8qtsajZd6OtrOvbw-QSHmI6RpDf0osud2lJ0utLp9_mSlZye-5UGaNj6lk70T0-n88UczFw6XYP0AP6jq4aWST_47vftiG6e6-IKYdZtOpNn5PLs9Mt4wkJZBWYBbQkmXW6UNlliitjFLjWa8yL3DpM1Jq7IrQEjg3ueOCO4AzgAOt4WSiRW6VksjXhO9uqm9i8J1Wniuc3ymdd5qqXSPPdccyGFtTMnfESOtztcLbvsGRVYHUiIaocQEXmHu1_hmYIttjo8DYCfYHaqagRWdFYAUuURORr0hLNgh81b-lXhLLbVX86JyNu-GUdifFntm3XXR6DpGEfkRUfufsFogeagtiOiBozQd8AM3cOWev51k6k7SYpUSKle_X9dh-Qhx7LCGCaYHpG91c3avwasszJvAkP_AWNkAMk
  priority: 102
  providerName: ProQuest
Title Non-Small Cell Lung Cancer Patients with Skip-N2 Metastases Have Similar Survival to N1 Patients—A Multicenter Analysis
URI https://www.ncbi.nlm.nih.gov/pubmed/40137429
https://www.proquest.com/docview/3181504669
https://www.proquest.com/docview/3181371640
https://pubmed.ncbi.nlm.nih.gov/PMC11943668
Volume 15
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lj9MwEB7tQ0JcEG-yu1RGWolToLETOzkgVKpdKkSjFaVSb5HtuNoubVr6QOyNH8Ev5Jcw0yRVs0JccrEdWzNjz_cl4xmA8ziR2oUy92Npcj80KvLjxJJCIq00d5RjiqItUtkbhp9G0egA6mKclQBX_6R2VE9quJy--fn99j1u-HfEOJGyv71ZzBDWkKWKQzhGl6SohkO_wvk3ZTAWwox2eT_v7piGR7p7Lu85pmbQ5J4XunwIDyr4yDqlvh_BgSsew71-9YP8Cdym88IfzPR0yroOH59xL7MuaXbJrsoUqitG317Z4Ntk4aec9d1aI0JcuRXr6R-ODSazCYqEDTZ4iKAZsvWcpcFu8J9fvztse2uXVohvrbOaPIXh5cXXbs-vqiv4FkGX8GWuTKxNFJiknbfz0GjOE-VyytkY5ImyBrkGdzzIjeA5ogJ09TaJRWBjPW5LI57BUTEv3AtgOgwct5EaO61CLWPNleOaCymsHefCeXBeSzhblEk0MiQfpIhsTxEevCbpZ6RsFLHV1Q0BnISSVGUdJNNRgoCVe3DW6Ilbwjaba_1ltUVleHjhRKGUiQevds00ksLMCjfflH0EMci2B89Lde8WTERUoff2IG4Ywq4DJeputhST623C7iBIQiFlfPL_dZ3CfU7VhSlaMDyDo_Vy414i5FmbFhx_uEivvrTg8OMoaG2N-y8n4QQe
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3NbtNAEB6VVAIuiH8MBRapiJNVe9de2weEQmiV0sSqSCv1Zta7GxFo7NAkoN54CJ6Dh-JJmIntEHPg1osv--PVzjc73-zOzgLsxolUNpDGjWVu3CCPQjdONAkkVJHilnJMUbRFKvunwfuz8GwLfjV3YSisslkTVwu1KTXtke8h9pC7BFImb2ZfXXo1ik5Xmyc0Klgc2cvv6LLNXx--Q_m-5Pxg_6TXd-tXBVyNZEO40kR5rPLQzxPPeCbIFedJZA3lKvRNEukcOTa33De54AatIZo4ncTC17EaezIX2O812A4EUoUObL_dT48_rHd1kMAgn_Gqi4BCJN7e59kUx01qJFqm718DsGEB29GZG-bu4Dbcqnkq61bAugNbtrgL14f1Sfw9uEzLwh1N1fk561n8DHDRYD2C0AU7rnK1zhlt8rLRl8nMTTkb2oVCKjq3c9ZX3ywbTaYTdKvZaImrFeKdLUqW-uvGv3_87LLV9WAaIfbapE-5D6dXMuEPoFOUhX0ETAW-5TqMxlZFgZKx4pHligsptB4bYR3YbWY4m1XZOjL0ckgQ2YYgHHhFs5-RDuMUa1VfRcCfUDasrItee5ggM-YO7LRqou7pdnEjv6zW_Xn2F6kOvFgXU0uKZytsuazqCHJVPQceVuJeD5g83ghpggNxCwjrCpQRvF1STD6tMoP7foK4lPHj_4_rOdzonwwH2eAwPXoCNzk9aUwhisEOdBYXS_sUedYif1aDm8HHq9anP-iQPSI
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Pb9MwFH8anTRxQfwnY4CRhjhFTezESQ4IlW5Vx7aookzaLTi2K8rWtKwtaDc-BJ-Gj8Mn4b0mKQ0HbrvkYjtx_P79nv3eM8B-nEhlA2ncWObGDfIodONEE0FCFSluqcYURVuksn8WvD8Pz7fgV50LQ2GVtU5cKWoz1bRH3kbeQ-wSSJm0R1VYxOCg93b21aUbpOiktb5Oo2SRY3v9Hd23-ZujA6T1K857hx-7fbe6YcDVCDyEK02UxyoP_TzxjGeCXHGeRNZQ3ULfJJHOEW9zy32TC27QMqK500ksfB2rkSdzge-9BdsRpY-2YPvdYTr4sN7hQTCD2MYrkwKFSLz2l9kE_4FESjTM4L_GYMMaNiM1N0xf7y7cqTAr65RMdg-2bHEfdk6rU_kHcJ1OC3c4UZeXrGvxcYIKhHWJna7YoKzbOme04cuGF-OZm3J2ahcKYenczllffbNsOJ6M0cVmwyVqLuR9tpiy1F8P_v3jZ4etUoVphvjWupTKQzi7kQV_BK1iWtgnwFTgW67DaGRVFCgZKx5ZrriQQuuREdaB_XqFs1lZuSNDj4cIkW0QwoHXtPoZyTMusVZVWgJ-hCpjZR304MMEUTJ3YK_RE-VQN5tr-mWVHphnf7nWgZfrZhpJsW2FnS7LPoLcVs-BxyW51xMm7zdCyOBA3GCEdQeqDt5sKcafV1XCfT8JhJTx7v_n9QJ2UI6yk6P0-Cnc5nS7MUUrBnvQWlwt7TOEXIv8ecXbDD7dtDj9AZTLQWA
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Non-Small+Cell+Lung+Cancer+Patients+with+Skip-N2+Metastases+Have+Similar+Survival+to+N1+Patients%E2%80%94A+Multicenter+Analysis&rft.jtitle=Journal+of+personalized+medicine&rft.au=Schlachtenberger%2C+Georg&rft.au=Schallenberg%2C+Simon&rft.au=Doerr%2C+Fabian&rft.au=Menghesha%2C+Hruy&rft.date=2025-03-14&rft.pub=MDPI+AG&rft.eissn=2075-4426&rft.volume=15&rft.issue=3&rft.spage=113&rft_id=info:doi/10.3390%2Fjpm15030113&rft.externalDBID=HAS_PDF_LINK
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2075-4426&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2075-4426&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2075-4426&client=summon