Genome-Scale Methylation Analysis Identifies Immune Profiles and Age Acceleration Associations with Bladder Cancer Outcomes

Immune profiles have been associated with bladder cancer outcomes and may have clinical applications for prognosis. However, associations of detailed immune cell subtypes with patient outcomes remain underexplored and may contribute crucial prognostic information for better managing bladder cancer r...

Full description

Saved in:
Bibliographic Details
Published inCancer epidemiology, biomarkers & prevention Vol. 32; no. 10; pp. 1328 - 1337
Main Authors Chen, Ji-Qing, Salas, Lucas A., Wiencke, John K., Koestler, Devin C., Molinaro, Annette M., Andrew, Angeline S., Seigne, John D., Karagas, Margaret R., Kelsey, Karl T., Christensen, Brock C.
Format Journal Article
LanguageEnglish
Published United States American Association for Cancer Research 02.10.2023
Subjects
Online AccessGet full text
ISSN1055-9965
1538-7755
1538-7755
DOI10.1158/1055-9965.EPI-23-0331

Cover

Abstract Immune profiles have been associated with bladder cancer outcomes and may have clinical applications for prognosis. However, associations of detailed immune cell subtypes with patient outcomes remain underexplored and may contribute crucial prognostic information for better managing bladder cancer recurrence and survival. Bladder cancer case peripheral blood DNA methylation was measured using the Illumina HumanMethylationEPIC array. Extended cell-type deconvolution quantified 12 immune cell-type proportions, including memory, naïve T and B cells, and granulocyte subtypes. DNA methylation clocks determined biological age. Cox proportional hazards models tested associations of immune cell profiles and age acceleration with bladder cancer outcomes. The partDSA algorithm discriminated 10-year overall survival groups from clinical variables and immune cell profiles, and a semi-supervised recursively partitioned mixture model (SS-RPMM) with DNA methylation data was applied to identify a classifier for 10-year overall survival. Higher CD8T memory cell proportions were associated with better overall survival [HR = 0.95, 95% confidence interval (CI) = 0.93-0.98], while higher neutrophil-to-lymphocyte ratio (HR = 1.36, 95% CI = 1.23-1.50), CD8T naïve (HR = 1.21, 95% CI = 1.04-1.41), neutrophil (HR = 1.04, 95% CI = 1.03-1.06) proportions, and age acceleration (HR = 1.06, 95% CI = 1.03-1.08) were associated with worse overall survival in patient with bladder cancer. partDSA and SS-RPMM classified five groups of subjects with significant differences in overall survival. We identified associations between immune cell subtypes and age acceleration with bladder cancer outcomes. The findings of this study suggest that bladder cancer outcomes are associated with specific methylation-derived immune cell-type proportions and age acceleration, and these factors could be potential prognostic biomarkers.
AbstractList Immune profiles have been associated with bladder cancer outcomes and may have clinical applications for prognosis. However, associations of detailed immune cell subtypes with patient outcomes remain underexplored and may contribute crucial prognostic information for better managing bladder cancer recurrence and survival.BACKGROUNDImmune profiles have been associated with bladder cancer outcomes and may have clinical applications for prognosis. However, associations of detailed immune cell subtypes with patient outcomes remain underexplored and may contribute crucial prognostic information for better managing bladder cancer recurrence and survival.Bladder cancer case peripheral blood DNA methylation was measured using the Illumina HumanMethylationEPIC array. Extended cell-type deconvolution quantified 12 immune cell-type proportions, including memory, naïve T and B cells, and granulocyte subtypes. DNA methylation clocks determined biological age. Cox proportional hazards models tested associations of immune cell profiles and age acceleration with bladder cancer outcomes. The partDSA algorithm discriminated 10-year overall survival groups from clinical variables and immune cell profiles, and a semi-supervised recursively partitioned mixture model (SS-RPMM) with DNA methylation data was applied to identify a classifier for 10-year overall survival.METHODSBladder cancer case peripheral blood DNA methylation was measured using the Illumina HumanMethylationEPIC array. Extended cell-type deconvolution quantified 12 immune cell-type proportions, including memory, naïve T and B cells, and granulocyte subtypes. DNA methylation clocks determined biological age. Cox proportional hazards models tested associations of immune cell profiles and age acceleration with bladder cancer outcomes. The partDSA algorithm discriminated 10-year overall survival groups from clinical variables and immune cell profiles, and a semi-supervised recursively partitioned mixture model (SS-RPMM) with DNA methylation data was applied to identify a classifier for 10-year overall survival.Higher CD8T memory cell proportions were associated with better overall survival [HR = 0.95, 95% confidence interval (CI) = 0.93-0.98], while higher neutrophil-to-lymphocyte ratio (HR = 1.36, 95% CI = 1.23-1.50), CD8T naïve (HR = 1.21, 95% CI = 1.04-1.41), neutrophil (HR = 1.04, 95% CI = 1.03-1.06) proportions, and age acceleration (HR = 1.06, 95% CI = 1.03-1.08) were associated with worse overall survival in patient with bladder cancer. partDSA and SS-RPMM classified five groups of subjects with significant differences in overall survival.RESULTSHigher CD8T memory cell proportions were associated with better overall survival [HR = 0.95, 95% confidence interval (CI) = 0.93-0.98], while higher neutrophil-to-lymphocyte ratio (HR = 1.36, 95% CI = 1.23-1.50), CD8T naïve (HR = 1.21, 95% CI = 1.04-1.41), neutrophil (HR = 1.04, 95% CI = 1.03-1.06) proportions, and age acceleration (HR = 1.06, 95% CI = 1.03-1.08) were associated with worse overall survival in patient with bladder cancer. partDSA and SS-RPMM classified five groups of subjects with significant differences in overall survival.We identified associations between immune cell subtypes and age acceleration with bladder cancer outcomes.CONCLUSIONSWe identified associations between immune cell subtypes and age acceleration with bladder cancer outcomes.The findings of this study suggest that bladder cancer outcomes are associated with specific methylation-derived immune cell-type proportions and age acceleration, and these factors could be potential prognostic biomarkers.IMPACTThe findings of this study suggest that bladder cancer outcomes are associated with specific methylation-derived immune cell-type proportions and age acceleration, and these factors could be potential prognostic biomarkers.
Immune profiles have been associated with bladder cancer outcomes and may have clinical applications for prognosis. However, associations of detailed immune cell subtypes with patient outcomes remain underexplored and may contribute crucial prognostic information for better managing bladder cancer recurrence and survival. Bladder cancer case peripheral blood DNA methylation was measured using the Illumina HumanMethylationEPIC array. Extended cell-type deconvolution quantified 12 immune cell-type proportions, including memory, naïve T and B cells, and granulocyte subtypes. DNA methylation clocks determined biological age. Cox proportional hazards models tested associations of immune cell profiles and age acceleration with bladder cancer outcomes. The partDSA algorithm discriminated 10-year overall survival groups from clinical variables and immune cell profiles, and a semi-supervised recursively partitioned mixture model (SS-RPMM) with DNA methylation data was applied to identify a classifier for 10-year overall survival. Higher CD8T memory cell proportions were associated with better overall survival [HR = 0.95, 95% confidence interval (CI) = 0.93-0.98], while higher neutrophil-to-lymphocyte ratio (HR = 1.36, 95% CI = 1.23-1.50), CD8T naïve (HR = 1.21, 95% CI = 1.04-1.41), neutrophil (HR = 1.04, 95% CI = 1.03-1.06) proportions, and age acceleration (HR = 1.06, 95% CI = 1.03-1.08) were associated with worse overall survival in patient with bladder cancer. partDSA and SS-RPMM classified five groups of subjects with significant differences in overall survival. We identified associations between immune cell subtypes and age acceleration with bladder cancer outcomes. The findings of this study suggest that bladder cancer outcomes are associated with specific methylation-derived immune cell-type proportions and age acceleration, and these factors could be potential prognostic biomarkers.
Author Seigne, John D.
Koestler, Devin C.
Andrew, Angeline S.
Kelsey, Karl T.
Christensen, Brock C.
Molinaro, Annette M.
Karagas, Margaret R.
Chen, Ji-Qing
Salas, Lucas A.
Wiencke, John K.
AuthorAffiliation 4 Department of Neurology, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
6 Departments of Epidemiology and Pathology and Laboratory Medicine, Brown University, Providence, Rhode Island
7 Departments of Molecular and Systems Biology, and Community and Family Medicine, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
3 Department of Biostatistics & Data Science, University of Kansas Medical Center, Kansas City, Kansas
1 Department of Epidemiology, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
5 Department of Surgery, Section of Urology, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
2 Department of Neurological Surgery, University of California San Francisco, San Francisco, California
AuthorAffiliation_xml – name: 3 Department of Biostatistics & Data Science, University of Kansas Medical Center, Kansas City, Kansas
– name: 1 Department of Epidemiology, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
– name: 5 Department of Surgery, Section of Urology, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
– name: 2 Department of Neurological Surgery, University of California San Francisco, San Francisco, California
– name: 6 Departments of Epidemiology and Pathology and Laboratory Medicine, Brown University, Providence, Rhode Island
– name: 4 Department of Neurology, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
– name: 7 Departments of Molecular and Systems Biology, and Community and Family Medicine, Geisel School of Medicine, Dartmouth College, Lebanon, New Hampshire
Author_xml – sequence: 1
  givenname: Ji-Qing
  orcidid: 0000-0002-1598-8811
  surname: Chen
  fullname: Chen, Ji-Qing
– sequence: 2
  givenname: Lucas A.
  orcidid: 0000-0002-2279-4097
  surname: Salas
  fullname: Salas, Lucas A.
– sequence: 3
  givenname: John K.
  orcidid: 0000-0001-7101-6489
  surname: Wiencke
  fullname: Wiencke, John K.
– sequence: 4
  givenname: Devin C.
  orcidid: 0000-0002-0598-0146
  surname: Koestler
  fullname: Koestler, Devin C.
– sequence: 5
  givenname: Annette M.
  orcidid: 0000-0002-9854-7404
  surname: Molinaro
  fullname: Molinaro, Annette M.
– sequence: 6
  givenname: Angeline S.
  orcidid: 0000-0002-3731-5300
  surname: Andrew
  fullname: Andrew, Angeline S.
– sequence: 7
  givenname: John D.
  orcidid: 0000-0002-7057-8727
  surname: Seigne
  fullname: Seigne, John D.
– sequence: 8
  givenname: Margaret R.
  orcidid: 0000-0002-6398-7362
  surname: Karagas
  fullname: Karagas, Margaret R.
– sequence: 9
  givenname: Karl T.
  orcidid: 0000-0002-2302-1600
  surname: Kelsey
  fullname: Kelsey, Karl T.
– sequence: 10
  givenname: Brock C.
  orcidid: 0000-0003-3022-426X
  surname: Christensen
  fullname: Christensen, Brock C.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37527159$$D View this record in MEDLINE/PubMed
BookMark eNqFUk1v3CAQRVGqfDU_IRXHXpyAMYtRD9VmlSYrpUqk5o4wjLNUGLbGbrTqny_Obtq0h_Y0w_DeG-YNx2g_xAAInVFyTimvLyjhvJByxs-v7pdFyQrCGN1DR5SzuhCC8_2cv2AO0XFKXwkhQnJ-gA6Z4KWgXB6hH9cQYgfFF6M94M8wrDZeDy4GPA_ab5JLeGkhDK51kNOuGwPg-z62zuezDhbPHwHPjQEP_Y6YUjTuOU_4yQ0rfOm1tdDjhQ4mh7txMLlneovetNonON3FE_Tw6ephcVPc3l0vF_PbwlS0HAphCaW2oaySpm3qCqg1VHNScVsabcrGllqA0VbUuWhnBmQLtBVGS9NYyk7QbCs7hrXePGnv1bp3ne43ihI1makmo9RklIK1UyVTk5mZ-HFLXI9NB9ZkG3r9mxy1U3_eBLdSj_H7JFcxORNZ4f1OoY_fRkiD6lzKVnkdII5JlXXFKRGilBn67nWzX11eVpUBfAswfUyph_YfU-Qv8WqKD3_xjBuet5Pf7Px_2D8BdVK-Yw
CitedBy_id crossref_primary_10_1111_acel_14071
crossref_primary_10_1016_j_bbcan_2024_189123
crossref_primary_10_1186_s13148_024_01669_z
crossref_primary_10_1038_s41698_024_00759_8
crossref_primary_10_1016_j_heliyon_2024_e32366
crossref_primary_10_2217_epi_2023_0358
Cites_doi 10.1093/bioinformatics/btu049
10.18632/aging.101414
10.1177/10732748231152322
10.1016/j.eururo.2006.01.017
10.1093/nar/gkv907
10.1016/j.ijrobp.2021.04.002
10.1016/j.ajur.2017.01.004
10.1111/j.1530-0277.2007.00377.x
10.1080/15592294.2020.1861401
10.2337/dc14-3008
10.1371/journal.pone.0041361
10.1038/sj.bjc.6601748
10.1093/bioinformatics/bts680
10.18632/oncotarget.13606
10.1093/jnci/djq497
10.1016/j.cell.2020.05.017
10.1371/journal.pgen.1000602
10.1093/bioinformatics/btq142
10.1016/j.eururo.2016.06.010
10.1007/s00345-019-02754-2
10.1002/cncr.33641
10.1186/1471-2105-13-86
10.1093/jnci/djp361
10.18632/aging.100809
10.1002/ijc.31189
10.1111/j.1541-0420.2012.01756.x
10.1136/jitc-2022-005518
10.1016/j.juro.2007.05.126
10.1371/journal.pone.0204745
10.1016/j.urolonc.2018.05.014
10.1186/s13148-022-01234-6
10.2147/OTT.S143491
10.3322/caac.21708
10.1093/jncics/pkaa109
10.1186/s13059-018-1448-7
10.1016/j.annepidem.2017.05.004
10.2147/OTT.S158275
10.1080/15592294.2019.1603963
10.1016/j.molcel.2012.10.016
10.1016/j.urolonc.2010.08.009
10.1371/journal.pone.0254289
10.1093/bioinformatics/btq470
10.4161/epi.6.6.16158
10.1016/j.eururo.2017.04.015
10.1371/journal.pone.0228633
10.1093/biostatistics/kxj037
10.18632/oncotarget.14179
10.1186/s13059-015-0649-6
10.1111/ijcp.14118
10.3390/ijms18102186
10.1186/s12885-019-5426-6
10.1186/1471-2164-14-293
10.1371/journal.pone.0009651
10.1038/s41467-021-27864-7
10.2147/CMAR.S274058
10.2147/CMAR.S289986
ContentType Journal Article
Copyright 2023 The Authors; Published by the American Association for Cancer Research.
2023 The Authors; Published by the American Association for Cancer Research 2023 American Association for Cancer Research
Copyright_xml – notice: 2023 The Authors; Published by the American Association for Cancer Research.
– notice: 2023 The Authors; Published by the American Association for Cancer Research 2023 American Association for Cancer Research
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
ADTOC
UNPAY
DOI 10.1158/1055-9965.EPI-23-0331
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
Unpaywall for CDI: Periodical Content
Unpaywall
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
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: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 3
  dbid: UNPAY
  name: Unpaywall
  url: https://proxy.k.utb.cz/login?url=https://unpaywall.org/
  sourceTypes: Open Access Repository
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
DocumentTitleAlternate Immune Profiles and Age Acceleration in Bladder Cancer
EISSN 1538-7755
EndPage 1337
ExternalDocumentID oai:escholarship.org:ark:/13030/qt3xb3r5dv
PMC10543967
37527159
10_1158_1055_9965_EPI_23_0331
Genre Research Support, U.S. Gov't, Non-P.H.S
Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NCI NIH HHS
  grantid: R01 CA253976
– fundername: NIGMS NIH HHS
  grantid: P20 GM130423
– fundername: NCI NIH HHS
  grantid: R01 CA207360
– fundername: NCI NIH HHS
  grantid: R01 CA057494
– fundername: NCI NIH HHS
  grantid: P30 CA168524
– fundername: NCI NIH HHS
  grantid: P50 CA097257
– fundername: NCI NIH HHS
  grantid: R01 CA216265
– fundername: NIGMS NIH HHS
  grantid: P20 GM104416
– fundername: ;
  grantid: P30 CA168524
– fundername: ;
  grantid: R01CA253976
– fundername: ;
  grantid: R01CA216265
– fundername: ;
  grantid: P20 GM130423
– fundername: ;
  grantid: R01CA207360
– fundername: ;
  grantid: W81XWH-20-1-0778
– fundername: ;
  grantid: P50CA097257
– fundername: ;
  grantid: P20GM104416
– fundername: ;
  grantid: R01CA057494
GroupedDBID ---
18M
29B
2FS
2WC
34G
39C
53G
5GY
5VS
6J9
AAFWJ
AAYXX
ABOCM
ACPRK
ADBBV
AENEX
AFHIN
AFRAH
ALMA_UNASSIGNED_HOLDINGS
BR6
BTFSW
CITATION
CS3
DIK
DU5
E3Z
EBS
EJD
F5P
FRP
IH2
KQ8
L7B
OK1
P2P
PQQKQ
QTD
RCR
RHI
SJN
W8F
WOQ
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
.55
3O-
ADCOW
ADTOC
AI.
C1A
H13
H~9
UDS
UNPAY
VH1
WHG
X7M
ZXP
ID FETCH-LOGICAL-c412t-7d011db1349cfb84e1dc1a5045d2cac2bd2a7ecad78504d6ce9fe1f7ca9cbd13
IEDL.DBID UNPAY
ISSN 1055-9965
1538-7755
IngestDate Sun Oct 26 03:37:02 EDT 2025
Thu Aug 21 18:36:14 EDT 2025
Thu Oct 02 06:19:59 EDT 2025
Mon Jul 21 05:53:47 EDT 2025
Thu Apr 24 22:55:39 EDT 2025
Tue Jul 01 03:05:11 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 10
Language English
License 2023 The Authors; Published by the American Association for Cancer Research.
This open access article is distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0) license.
cc-by-nc-nd
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c412t-7d011db1349cfb84e1dc1a5045d2cac2bd2a7ecad78504d6ce9fe1f7ca9cbd13
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Cancer Epidemiol Biomarkers Prev 2023;32:1328–37
ORCID 0000-0002-1598-8811
0000-0003-3022-426X
0000-0001-7101-6489
0000-0002-3731-5300
0000-0002-2302-1600
0000-0002-7057-8727
0000-0002-6398-7362
0000-0002-2279-4097
0000-0002-0598-0146
0000-0002-9854-7404
OpenAccessLink https://proxy.k.utb.cz/login?url=https://escholarship.org/uc/item/3xb3r5dv
PMID 37527159
PQID 2845107729
PQPubID 23479
PageCount 10
ParticipantIDs unpaywall_primary_10_1158_1055_9965_epi_23_0331
pubmedcentral_primary_oai_pubmedcentral_nih_gov_10543967
proquest_miscellaneous_2845107729
pubmed_primary_37527159
crossref_primary_10_1158_1055_9965_EPI_23_0331
crossref_citationtrail_10_1158_1055_9965_EPI_23_0331
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2023-10-02
PublicationDateYYYYMMDD 2023-10-02
PublicationDate_xml – month: 10
  year: 2023
  text: 2023-10-02
  day: 02
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Cancer epidemiology, biomarkers & prevention
PublicationTitleAlternate Cancer Epidemiol Biomarkers Prev
PublicationYear 2023
Publisher American Association for Cancer Research
Publisher_xml – name: American Association for Cancer Research
References Suelves (2023100207230412000_bib16) 2016; 15
Dugue (2023100207230412000_bib22) 2021; 5
Dugué (2023100207230412000_bib27) 2018; 142
Johnson (2023100207230412000_bib40) 2007; 8
Reinius (2023100207230412000_bib17) 2012; 7
Akan (2023100207230412000_bib51) 2021; 75
Lostritto (2023100207230412000_bib42) 2012; 68
Oda (2023100207230412000_bib54) 2021; 16
Taylor (2023100207230412000_bib28) 2009; 6
Grossmannm (2023100207230412000_bib63) 2015; 38
Pidsley (2023100207230412000_bib39) 2013; 14
Baris (2023100207230412000_bib31) 2009; 101
Aryee (2023100207230412000_bib36) 2014; 30
Sun (2023100207230412000_bib57) 2018; 11
Horvath (2023100207230412000_bib19) 2015; 16
Poage (2023100207230412000_bib44) 2010; 5
Van Puffelen (2023100207230412000_bib59) 2023; 11
Chung (2023100207230412000_bib24) 2021; 16
Zhang (2023100207230412000_bib49) 2021; 13
Siegel (2023100207230412000_bib1) 2022; 72
Yıldız (2023100207230412000_bib48) 2021; 75
Saginala (2023100207230412000_bib2) 2020; 8
DeGeorge (2023100207230412000_bib5) 2017; 96
Miyake (2023100207230412000_bib52) 2017; 18
Molinaro (2023100207230412000_bib29) 2010; 26
Xiao (2023100207230412000_bib25) 2021; 111
Ferro (2023100207230412000_bib50) 2020; 38
Salas (2023100207230412000_bib15) 2022; 13
Liu (2023100207230412000_bib58) 2020; 12
Murai (2023100207230412000_bib53) 2018; 13
Houseman (2023100207230412000_bib18) 2012; 13
Skopp (2023100207230412000_bib35) 2017; 27
Lv (2023100207230412000_bib55) 2019; 19
Soukup (2023100207230412000_bib8) 2017; 72
Schned (2023100207230412000_bib32) 2007; 178
Levine (2023100207230412000_bib23) 2015; 7
Kang (2023100207230412000_bib11) 2017; 8
Oh (2023100207230412000_bib14) 2020; 181
Xu (2023100207230412000_bib37) 2016; 44
Antoni (2023100207230412000_bib6) 2017; 71
Avissar-Whiting (2023100207230412000_bib45) 2011; 6
Christensen (2023100207230412000_bib46) 2011; 103
Hou (2023100207230412000_bib4) 2017; 8
Witjes (2023100207230412000_bib7) 2006; 49
Vartolomei (2023100207230412000_bib47) 2018; 36
Salas (2023100207230412000_bib13) 2018; 19
Levine (2023100207230412000_bib20) 2018; 10
Lin (2023100207230412000_bib9) 2012; 30
Christensen (2023100207230412000_bib43) 2009; 5
Kelsey (2023100207230412000_bib33) 2004; 90
Lin (2023100207230412000_bib3) 2023; 30
Chen (2023100207230412000_bib12) 2022; 14
Sun (2023100207230412000_bib56) 2017; 10
Laso (2023100207230412000_bib62) 2007; 31
Hannum (2023100207230412000_bib21) 2013; 49
Karagas (2023100207230412000_bib34) 1998; 106
Tan (2023100207230412000_bib10) 2017; 4
Teschendorff (2023100207230412000_bib38) 2013; 29
Koestler (2023100207230412000_bib30) 2010; 26
Elisia (2023100207230412000_bib61) 2020; 15
Xiao (2023100207230412000_bib26) 2021; 127
Zhou (2023100207230412000_bib41) 2017; 45
Das (2023100207230412000_bib60) 2019; 14
References_xml – volume: 106
  start-page: 1047
  year: 1998
  ident: 2023100207230412000_bib34
  article-title: Design of an epidemiologic study of drinking water arsenic exposure and skin and bladder cancer risk in a U.S. population
  publication-title: Environ Health Perspect
– volume: 30
  start-page: 1363
  year: 2014
  ident: 2023100207230412000_bib36
  article-title: Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btu049
– volume: 10
  start-page: 573
  year: 2018
  ident: 2023100207230412000_bib20
  article-title: An epigenetic biomarker of aging for lifespan and healthspan
  publication-title: Aging
  doi: 10.18632/aging.101414
– volume: 30
  start-page: 10732748231152322
  year: 2023
  ident: 2023100207230412000_bib3
  article-title: Impact of age at diagnosis of bladder cancer on survival: a surveillance, epidemiology, and end results-based study 2004–2015
  publication-title: Cancer Control
  doi: 10.1177/10732748231152322
– volume: 49
  start-page: 790
  year: 2006
  ident: 2023100207230412000_bib7
  article-title: Management of BCG failures in superficial bladder cancer: a review
  publication-title: Eur Urol
  doi: 10.1016/j.eururo.2006.01.017
– volume: 44
  start-page: e20
  year: 2016
  ident: 2023100207230412000_bib37
  article-title: ENmix: a novel background correction method for Illumina HumanMethylation450 BeadChip
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkv907
– volume: 111
  start-page: 157
  year: 2021
  ident: 2023100207230412000_bib25
  article-title: Association of epigenetic age acceleration with risk factors, survival, and quality of life in patients with head and neck cancer
  publication-title: Int J Radiat Oncol Biol Phys
  doi: 10.1016/j.ijrobp.2021.04.002
– volume: 6
  start-page: 135
  year: 2009
  ident: 2023100207230412000_bib28
  article-title: Bladder cancer in the elderly: clinical outcomes, basic mechanisms, and future research direction
  publication-title: Nat Clin Pract Urol
– volume: 4
  start-page: 239
  year: 2017
  ident: 2023100207230412000_bib10
  article-title: Pretreatment neutrophil-to-lymphocyte ratio predicts worse survival outcomes and advanced tumor staging in patients undergoing radical cystectomy for bladder cancer
  publication-title: Asian J Urol
  doi: 10.1016/j.ajur.2017.01.004
– volume: 31
  start-page: 846
  year: 2007
  ident: 2023100207230412000_bib62
  article-title: Chronic alcohol consumption is associated with changes in the distribution, immunophenotype, and the inflammatory cytokine secretion profile of circulating dendritic cells
  publication-title: Alcohol Clin Exp Res
  doi: 10.1111/j.1530-0277.2007.00377.x
– volume: 75
  start-page: e13813
  year: 2021
  ident: 2023100207230412000_bib51
  article-title: Can the systemic immune inflammation index be a predictor of BCG response in patients with high-risk non-muscle invasive bladder cancer?
  publication-title: Int J Clin Pract
– volume: 16
  start-page: 1306
  year: 2021
  ident: 2023100207230412000_bib24
  article-title: DNA methylation ageing clocks and pancreatic cancer risk: pooled analysis of three prospective nested case-control studies
  publication-title: Epigenetics
  doi: 10.1080/15592294.2020.1861401
– volume: 38
  start-page: 1356
  year: 2015
  ident: 2023100207230412000_bib63
  article-title: Profile of the immune and inflammatory response in individuals with prediabetes and type 2 diabetes
  publication-title: Diabetes Care
  doi: 10.2337/dc14-3008
– volume: 7
  start-page: e41361
  year: 2012
  ident: 2023100207230412000_bib17
  article-title: Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0041361
– volume: 90
  start-page: 1572
  year: 2004
  ident: 2023100207230412000_bib33
  article-title: A population-based study of immunohistochemical detection of p53 alteration in bladder cancer
  publication-title: Br J Cancer
  doi: 10.1038/sj.bjc.6601748
– volume: 29
  start-page: 189
  year: 2013
  ident: 2023100207230412000_bib38
  article-title: A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bts680
– volume: 45
  start-page: e22
  year: 2017
  ident: 2023100207230412000_bib41
  article-title: Comprehensive characterization, annotation and innovative use of Infinium DNA methylation BeadChip probes
  publication-title: Nucleic Acids Res
– volume: 8
  start-page: 1278
  year: 2017
  ident: 2023100207230412000_bib4
  article-title: Association of smoking status with prognosis in bladder cancer: a meta-analysis
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.13606
– volume: 103
  start-page: 143
  year: 2011
  ident: 2023100207230412000_bib46
  article-title: DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma
  publication-title: J Natl Cancer Inst
  doi: 10.1093/jnci/djq497
– volume: 181
  start-page: 1612
  year: 2020
  ident: 2023100207230412000_bib14
  article-title: Intratumoral CD4+ T cells mediate anti-tumor cytotoxicity in human bladder cancer
  publication-title: Cell
  doi: 10.1016/j.cell.2020.05.017
– volume: 8
  start-page: 15
  year: 2020
  ident: 2023100207230412000_bib2
  article-title: Epidemiology of bladder cancer
  publication-title: Med Sci
– volume: 5
  start-page: e1000602
  year: 2009
  ident: 2023100207230412000_bib43
  article-title: Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CPG island context
  publication-title: PLoS Genet
  doi: 10.1371/journal.pgen.1000602
– volume: 26
  start-page: 1357
  year: 2010
  ident: 2023100207230412000_bib29
  article-title: partDSA: deletion/substitution/addition algorithm for partitioning the covariate space in prediction
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btq142
– volume: 71
  start-page: 96
  year: 2017
  ident: 2023100207230412000_bib6
  article-title: Bladder cancer incidence and mortality: a global overview and recent trends
  publication-title: Eur Urol
  doi: 10.1016/j.eururo.2016.06.010
– volume: 38
  start-page: 143
  year: 2020
  ident: 2023100207230412000_bib50
  article-title: Absolute basophil count is associated with time to recurrence in patients with high-grade T1 bladder cancer receiving bacillus Calmette–Guérin after transurethral resection of the bladder tumor
  publication-title: World J Urol
  doi: 10.1007/s00345-019-02754-2
– volume: 127
  start-page: 3361
  year: 2021
  ident: 2023100207230412000_bib26
  article-title: Epigenetic age acceleration, fatigue, and inflammation in patients undergoing radiation therapy for head and neck cancer: a longitudinal study
  publication-title: Cancer
  doi: 10.1002/cncr.33641
– volume: 13
  start-page: 86
  year: 2012
  ident: 2023100207230412000_bib18
  article-title: DNA methylation arrays as surrogate measures of cell mixture distribution
  publication-title: BMC Bioinformatics
  doi: 10.1186/1471-2105-13-86
– volume: 101
  start-page: 1553
  year: 2009
  ident: 2023100207230412000_bib31
  article-title: A case-control study of smoking and bladder cancer risk: Emergent patterns over time
  publication-title: J Natl Cancer Inst
  doi: 10.1093/jnci/djp361
– volume: 7
  start-page: 690
  year: 2015
  ident: 2023100207230412000_bib23
  article-title: DNA methylation age of blood predicts future onset of lung cancer in the women's health initiative
  publication-title: Aging
  doi: 10.18632/aging.100809
– volume: 142
  start-page: 1611
  year: 2018
  ident: 2023100207230412000_bib27
  article-title: DNA methylation-based biological aging and cancer risk and survival: pooled analysis of seven prospective studies
  publication-title: Int J Cancer
  doi: 10.1002/ijc.31189
– volume: 68
  start-page: 1146
  year: 2012
  ident: 2023100207230412000_bib42
  article-title: A partitioning deletion/substitution/addition algorithm for creating survival risk groups
  publication-title: Biometrics
  doi: 10.1111/j.1541-0420.2012.01756.x
– volume: 11
  start-page: e005518
  year: 2023
  ident: 2023100207230412000_bib59
  article-title: Intravesical BCG in patients with non-muscle invasive bladder cancer induces trained immunity and decreases respiratory infections
  publication-title: J Immunother Cancer
  doi: 10.1136/jitc-2022-005518
– volume: 178
  start-page: 1196
  year: 2007
  ident: 2023100207230412000_bib32
  article-title: Survival following the diagnosis of noninvasive bladder cancer: WHO/international society of urological pathology versus WHO classification systems
  publication-title: J Urol
  doi: 10.1016/j.juro.2007.05.126
– volume: 96
  start-page: 507
  year: 2017
  ident: 2023100207230412000_bib5
  article-title: Bladder cancer: diagnosis and treatment
  publication-title: Am Fam Physician
– volume: 13
  start-page: e0204745
  year: 2018
  ident: 2023100207230412000_bib53
  article-title: Prediction of intravesical recurrence of nonmuscle-invasive bladder cancer by evaluation of intratumoral Foxp3 + T cells in the primary transurethral resection of bladder tumor specimens
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0204745
– volume: 15
  start-page: 443
  year: 2016
  ident: 2023100207230412000_bib16
  article-title: DNA methylation dynamics in cellular commitment and differentiation
  publication-title: Brief Funct Genomics
– volume: 36
  start-page: 389
  year: 2018
  ident: 2023100207230412000_bib47
  article-title: Prognostic role of pretreatment neutrophil-to-lymphocyte ratio (NLR) in patients with non–muscle-invasive bladder cancer (NMIBC): a systematic review and meta-analysis
  publication-title: Urol Oncol
  doi: 10.1016/j.urolonc.2018.05.014
– volume: 14
  start-page: 14
  year: 2022
  ident: 2023100207230412000_bib12
  article-title: Immune profiles and DNA methylation alterations related with non-muscle-invasive bladder cancer outcomes
  publication-title: Clin Epigenetics
  doi: 10.1186/s13148-022-01234-6
– volume: 10
  start-page: 3949
  year: 2017
  ident: 2023100207230412000_bib56
  article-title: Fibrous sheath interacting protein 1 overexpression is associated with unfavorable prognosis in bladder cancer: a potential therapeutic target
  publication-title: Onco Targets Ther
  doi: 10.2147/OTT.S143491
– volume: 72
  start-page: 7
  year: 2022
  ident: 2023100207230412000_bib1
  article-title: Cancer statistics, 2022
  publication-title: CA Cancer J Clin
  doi: 10.3322/caac.21708
– volume: 5
  start-page: pkaa109
  year: 2021
  ident: 2023100207230412000_bib22
  article-title: Biological aging measures based on blood DNA methylation and risk of cancer: a prospective study
  publication-title: JNCI Cancer Spectr
  doi: 10.1093/jncics/pkaa109
– volume: 19
  start-page: 64
  year: 2018
  ident: 2023100207230412000_bib13
  article-title: An optimized library for reference-based deconvolution of whole-blood biospecimens assayed using the Illumina HumanMethylationEPIC BeadArray
  publication-title: Genome Biol
  doi: 10.1186/s13059-018-1448-7
– volume: 27
  start-page: 397
  year: 2017
  ident: 2023100207230412000_bib35
  article-title: Evaluation of a methodology to validate National Death Index retrieval results among a cohort of U.S. service members
  publication-title: Ann Epidemiol
  doi: 10.1016/j.annepidem.2017.05.004
– volume: 11
  start-page: 1961
  year: 2018
  ident: 2023100207230412000_bib57
  article-title: Knockdown of fibrous sheath interacting protein 1 expression reduces bladder urothelial carcinoma cell proliferation and induces apoptosis via inhibition of the PI3K/AKT pathway
  publication-title: Onco Targets Ther
  doi: 10.2147/OTT.S158275
– volume: 14
  start-page: 589
  year: 2019
  ident: 2023100207230412000_bib60
  article-title: Identification of DNA methylation patterns predisposing for an efficient response to BCG vaccination in healthy BCG-naïve subjects
  publication-title: Epigenetics
  doi: 10.1080/15592294.2019.1603963
– volume: 49
  start-page: 359
  year: 2013
  ident: 2023100207230412000_bib21
  article-title: Genome-wide methylation profiles reveal quantitative views of human aging rates
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2012.10.016
– volume: 30
  start-page: 680
  year: 2012
  ident: 2023100207230412000_bib9
  article-title: Prognostic relevance of preoperative circulating CD8-positive lymphocytes in the urinary bladder recurrence of urothelial carcinoma
  publication-title: Urol Oncol
  doi: 10.1016/j.urolonc.2010.08.009
– volume: 16
  start-page: e0254289
  year: 2021
  ident: 2023100207230412000_bib54
  article-title: Expression of Spred2 in the urothelial tumorigenesis of the urinary bladder
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0254289
– volume: 26
  start-page: 2578
  year: 2010
  ident: 2023100207230412000_bib30
  article-title: Semi-supervised recursively partitioned mixture models for identifying cancer subtypes
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btq470
– volume: 6
  start-page: 703
  year: 2011
  ident: 2023100207230412000_bib45
  article-title: Polycomb group genes are targets of aberrant DNA methylation in renal cell carcinoma
  publication-title: Epigenetics
  doi: 10.4161/epi.6.6.16158
– volume: 72
  start-page: 801
  year: 2017
  ident: 2023100207230412000_bib8
  article-title: Prognostic performance and reproducibility of the 1973 and 2004/2016 world health organization grading classification systems in non–muscle-invasive bladder cancer: a European association of urology non-muscle invasive bladder cancer guidelines panel syst
  publication-title: Eur Urol
  doi: 10.1016/j.eururo.2017.04.015
– volume: 15
  start-page: e0228633
  year: 2020
  ident: 2023100207230412000_bib61
  article-title: Exploratory examination of inflammation state, immune response and blood cell composition in a human obese cohort to identify potential markers predicting cancer risk
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0228633
– volume: 8
  start-page: 118
  year: 2007
  ident: 2023100207230412000_bib40
  article-title: Adjusting batch effects in microarray expression data using empirical Bayes methods
  publication-title: Biostatistics
  doi: 10.1093/biostatistics/kxj037
– volume: 8
  start-page: 12891
  year: 2017
  ident: 2023100207230412000_bib11
  article-title: Preoperative neutrophil-lymphocyte ratio can significantly predict mortality outcomes in patients with non-muscle invasive bladder cancer undergoing transurethral resection of bladder tumor
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.14179
– volume: 16
  start-page: R115
  year: 2015
  ident: 2023100207230412000_bib19
  article-title: DNA methylation age of human tissues and cell types
  publication-title: Genome Biol
  doi: 10.1186/s13059-015-0649-6
– volume: 75
  start-page: e14118
  year: 2021
  ident: 2023100207230412000_bib48
  article-title: Prognostic value of preoperative inflammation markers in non-muscle invasive bladder cancer
  publication-title: Int J Clin Pract
  doi: 10.1111/ijcp.14118
– volume: 18
  start-page: 2186
  year: 2017
  ident: 2023100207230412000_bib52
  article-title: Regulatory T cells and tumor-associated macrophages in the tumor microenvironment in non-muscle invasive bladder cancer treated with intravesical bacille calmette-guérin: a long-term follow-up study of a Japanese cohort
  publication-title: Int J Mol Sci
  doi: 10.3390/ijms18102186
– volume: 19
  start-page: 204
  year: 2019
  ident: 2023100207230412000_bib55
  article-title: PPARγ activation serves as therapeutic strategy against bladder cancer via inhibiting PI3K-Akt signaling pathway
  publication-title: BMC Cancer
  doi: 10.1186/s12885-019-5426-6
– volume: 14
  start-page: 293
  year: 2013
  ident: 2023100207230412000_bib39
  article-title: A data-driven approach to preprocessing Illumina 450K methylation array data
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-14-293
– volume: 5
  start-page: e9651
  year: 2010
  ident: 2023100207230412000_bib44
  article-title: Genetic and epigenetic somatic alterations in head and neck squamous cell carcinomas are globally coordinated but not locally targeted
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0009651
– volume: 13
  start-page: 761
  year: 2022
  ident: 2023100207230412000_bib15
  article-title: Enhanced cell deconvolution of peripheral blood using DNA methylation for high-resolution immune profiling
  publication-title: Nat Commun
  doi: 10.1038/s41467-021-27864-7
– volume: 12
  start-page: 11371
  year: 2020
  ident: 2023100207230412000_bib58
  article-title: Phosphorylated mapk14 promotes the proliferation and migration of bladder cancer cells by maintaining runx2 protein abundance
  publication-title: Cancer Manag Res
  doi: 10.2147/CMAR.S274058
– volume: 13
  start-page: 849
  year: 2021
  ident: 2023100207230412000_bib49
  article-title: Clinical value of postoperative neutrophil-tolymphocyte ratio change as a detection marker of bladder cancer recurrence
  publication-title: Cancer Manag Res
  doi: 10.2147/CMAR.S289986
SSID ssj0007955
Score 2.488719
Snippet Immune profiles have been associated with bladder cancer outcomes and may have clinical applications for prognosis. However, associations of detailed immune...
SourceID unpaywall
pubmedcentral
proquest
pubmed
crossref
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage 1328
SubjectTerms DNA Methylation
Humans
Lymphocytes
Neoplasm Recurrence, Local - genetics
Prognosis
Proportional Hazards Models
Urinary Bladder Neoplasms
Title Genome-Scale Methylation Analysis Identifies Immune Profiles and Age Acceleration Associations with Bladder Cancer Outcomes
URI https://www.ncbi.nlm.nih.gov/pubmed/37527159
https://www.proquest.com/docview/2845107729
https://pubmed.ncbi.nlm.nih.gov/PMC10543967
https://escholarship.org/uc/item/3xb3r5dv
UnpaywallVersion submittedVersion
Volume 32
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVAFT
  databaseName: Open Access Digital Library
  customDbUrl:
  eissn: 1538-7755
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0007955
  issn: 1055-9965
  databaseCode: KQ8
  dateStart: 19911101
  isFulltext: true
  titleUrlDefault: http://grweb.coalliance.org/oadl/oadl.html
  providerName: Colorado Alliance of Research Libraries
– providerCode: PRVBFR
  databaseName: Free Medical Journals - Free Access to All
  customDbUrl:
  eissn: 1538-7755
  dateEnd: 20241101
  omitProxy: true
  ssIdentifier: ssj0007955
  issn: 1055-9965
  databaseCode: DIK
  dateStart: 19910101
  isFulltext: true
  titleUrlDefault: http://www.freemedicaljournals.com
  providerName: Flying Publisher
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1Zb9NAEB5BKgEv3IcpVIvEq5N47Y3tx7RqaUApkWil8rTayzQiOJEPrv75znpt01KJ49X2WmvNt7PfeGa_AXg91lmWsVT7NBRWVFsKP5G48BRyhUBGTJhGjmF-NDk8id6estNWLNqehTFdTHe23DSJ_Nr1JBuF32VYMP31JmxNGNLuAWydHC2mH5tsJmM-8nbmtFETZIyMtad1ApaM-vvo4Zc4KX_sespd2oeukcvrNZK363wjfnwTq9WlDejgnivdKhvdQlt38nlYV3Kofv6m6vhP33Yf7rY0lEwdbh7ADZM_hFvzNtH-CM7fmHz9xfgf0ISGzA2a0xXNkU7FhLgjvhlG2mRmD5kYsnD9v0sick2mnwyZKoW7WtEO_AWEktjfv2R3Zd1eQfYs8gryvq4Q_qZ8DMcH-8d7h37bp8FXUUArP9boJLS0Qocqk0lkAq0CwZAsaqqEolJTERsldJzgRT1RJs1MkMVKpErqIHwCg3ydm2dAlLR8lcVRKsdRloYpup9URAp5TCIUCz2IOqNx1WqY21YaK97EMizh1tbc2prvL2achtza2oNhP2zjRDz-NuBVhwiOy83mUERu1nXJcTdHL2ZDEg-eOoT0rwxjRmOkhx4kV7DTP2ClvK_eyZdnjaQ3zgKZ4ST2YNTD7A9TRRx3U33-3yO24Q5FptZUJNIXMKiK2rxEZlXJHYwpZu922pV1AfUXI4Q
linkProvider Unpaywall
linkToUnpaywall http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1Lb9QwEB7BVgIulPJMKchIXLO7ceJNclyqlhZp25VopXKy_ApdsWRXefAof55xnISWStBek0zkaD7PfI7H3wC8Hessy1iqfRoKK6othZ9InHgKuUIgIyZMI8cwO5ocnEYfzthZKxZtz8KYbk13vlg3G_m160k2Cn_IsGD6213YmDCk3QPYOD2aTz81u5mM-cjbmdNGTZAxMtae1glYMurvY4Rf4KD8sespdykPXSOX12sk79f5Wvz8LpbLSwlof9OVbpWNbqGtO_kyrCs5VBd_qTre6NsewcOWhpKpw80W3DH5Y7g3azfan8Cv9yZffTX-R3ShITOD7nRFc6RTMSHuiG-GK21yaA-ZGDJ3_b9LInJNpp8NmSqFWa1oDf8AoST29y95t7RhryC7FnkFOa4rhL8pn8LJ_t7J7oHf9mnwVRTQyo81BgktrdChymQSmUCrQDAki5oqoajUVMRGCR0neFFPlEkzE2SxEqmSOgifwSBf5eYFECUtX2VxlMpxlKVhiuEnFZFCHpMIxUIPos5pXLUa5raVxpI3axmWcOtrbn3N9-aHnIbc-tqDYW-2diIe_zN40yGC43SzeygiN6u65JjNMYrZJYkHzx1C-leGMaMx0kMPkivY6R-wUt5X7-SL80bSG0eBzHASezDqYfaPoSKOu6Fu39riJTygyNSaikS6A4OqqM0rZFaVfN3Oqd8lxCKL
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=Genome-Scale+Methylation+Analysis+Identifies+Immune+Profiles+and+Age+Acceleration+Associations+with+Bladder+Cancer+Outcomes&rft.jtitle=Cancer+epidemiology%2C+biomarkers+%26+prevention&rft.au=Chen%2C+Ji-Qing&rft.au=Salas%2C+Lucas+A.&rft.au=Wiencke%2C+John+K.&rft.au=Koestler%2C+Devin+C.&rft.date=2023-10-02&rft.issn=1055-9965&rft.eissn=1538-7755&rft.volume=32&rft.issue=10&rft.spage=1328&rft.epage=1337&rft_id=info:doi/10.1158%2F1055-9965.EPI-23-0331&rft.externalDBID=n%2Fa&rft.externalDocID=10_1158_1055_9965_EPI_23_0331
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1055-9965&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1055-9965&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1055-9965&client=summon