Tissue‐matched analysis of MRI evaluating the tumor infiltrating lymphocytes in hepatocellular carcinoma

Tumor‐infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi‐parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogenei...

Celý popis

Uloženo v:
Podrobná bibliografie
Vydáno v:International journal of cancer Ročník 156; číslo 8; s. 1634 - 1643
Hlavní autoři: Huang, Mengqi, Song, Chenyu, Zhou, Xiaoqi, Wang, Huanjun, Lin, Yingyu, Wang, Jifei, Cai, Huasong, Wang, Meng, Peng, Zhenpeng, Dong, Zhi, Feng, Shi‐Ting
Médium: Journal Article
Jazyk:angličtina
Vydáno: Hoboken, USA John Wiley & Sons, Inc 15.04.2025
Wiley Subscription Services, Inc
Témata:
ISSN:0020-7136, 1097-0215, 1097-0215
On-line přístup:Získat plný text
Tagy: Přidat tag
Žádné tagy, Buďte první, kdo vytvoří štítek k tomuto záznamu!
Abstract Tumor‐infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi‐parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi‐parametric MRI was performed on hepatocellular carcinoma (HCC) mice (N = 28). Three‐dimensional (3D) printing was employed for tissue sampling, to match the multi‐parametric MRI data with tumor tissues, followed by flow cytometry analysis and next‐generation RNA‐sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL‐related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T‐cells, CD4+ T‐cells, CD8+ T‐cells, PD1 + CD8+ T‐cells, B‐cells, macrophages, and regulatory T‐cells (correlation coefficients ranged from −0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non‐inflamed subclasses, with the proportion of T‐cells, CD8+ T‐cells, and PD1 + CD8+ T‐cells significantly higher in the inflamed group compared to the non‐inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z‐score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721–0.910) and a cut‐off value of −0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z‐score was related to the gene expression of T‐cell activation, chemokine production, and cell adhesion. The tissue‐matched analysis of multi‐parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses. What's new? Increasing evidence suggests that the evaluation of tumor‐infiltrating lymphocytes both at baseline and throughout cancer therapy can be valuable for predicting and monitoring treatment responses. Tumor heterogeneity however complicates the assessment of tumor‐infiltrating lymphocytes. In this study, the authors used an animal model and three‐dimensional printing technology to achieve guided tumor spatial segmentation and regional evaluation of tumor‐infiltrating lymphocytes. They present a feasible, non‐invasive magnetic resonance imaging‐based model for evaluating tumor‐infiltrating lymphocytes in hepatocellular carcinoma that takes spatial heterogeneity into account and could potentially inform the immunotherapy response in patients.
AbstractList Tumor-infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi-parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi-parametric MRI was performed on hepatocellular carcinoma (HCC) mice (N = 28). Three-dimensional (3D) printing was employed for tissue sampling, to match the multi-parametric MRI data with tumor tissues, followed by flow cytometry analysis and next-generation RNA-sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL-related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T-cells, CD4+ T-cells, CD8+ T-cells, PD1 + CD8+ T-cells, B-cells, macrophages, and regulatory T-cells (correlation coefficients ranged from -0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non-inflamed subclasses, with the proportion of T-cells, CD8+ T-cells, and PD1 + CD8+ T-cells significantly higher in the inflamed group compared to the non-inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z-score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721-0.910) and a cut-off value of -0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z-score was related to the gene expression of T-cell activation, chemokine production, and cell adhesion. The tissue-matched analysis of multi-parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses.Tumor-infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi-parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi-parametric MRI was performed on hepatocellular carcinoma (HCC) mice (N = 28). Three-dimensional (3D) printing was employed for tissue sampling, to match the multi-parametric MRI data with tumor tissues, followed by flow cytometry analysis and next-generation RNA-sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL-related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T-cells, CD4+ T-cells, CD8+ T-cells, PD1 + CD8+ T-cells, B-cells, macrophages, and regulatory T-cells (correlation coefficients ranged from -0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non-inflamed subclasses, with the proportion of T-cells, CD8+ T-cells, and PD1 + CD8+ T-cells significantly higher in the inflamed group compared to the non-inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z-score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721-0.910) and a cut-off value of -0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z-score was related to the gene expression of T-cell activation, chemokine production, and cell adhesion. The tissue-matched analysis of multi-parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses.
Tumor‐infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi‐parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi‐parametric MRI was performed on hepatocellular carcinoma (HCC) mice (N = 28). Three‐dimensional (3D) printing was employed for tissue sampling, to match the multi‐parametric MRI data with tumor tissues, followed by flow cytometry analysis and next‐generation RNA‐sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL‐related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T‐cells, CD4+ T‐cells, CD8+ T‐cells, PD1 + CD8+ T‐cells, B‐cells, macrophages, and regulatory T‐cells (correlation coefficients ranged from −0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non‐inflamed subclasses, with the proportion of T‐cells, CD8+ T‐cells, and PD1 + CD8+ T‐cells significantly higher in the inflamed group compared to the non‐inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z‐score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721–0.910) and a cut‐off value of −0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z‐score was related to the gene expression of T‐cell activation, chemokine production, and cell adhesion. The tissue‐matched analysis of multi‐parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses.
Tumor‐infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi‐parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi‐parametric MRI was performed on hepatocellular carcinoma (HCC) mice (N = 28). Three‐dimensional (3D) printing was employed for tissue sampling, to match the multi‐parametric MRI data with tumor tissues, followed by flow cytometry analysis and next‐generation RNA‐sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL‐related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T‐cells, CD4+ T‐cells, CD8+ T‐cells, PD1 + CD8+ T‐cells, B‐cells, macrophages, and regulatory T‐cells (correlation coefficients ranged from −0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non‐inflamed subclasses, with the proportion of T‐cells, CD8+ T‐cells, and PD1 + CD8+ T‐cells significantly higher in the inflamed group compared to the non‐inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z‐score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721–0.910) and a cut‐off value of −0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z‐score was related to the gene expression of T‐cell activation, chemokine production, and cell adhesion. The tissue‐matched analysis of multi‐parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses. What's new? Increasing evidence suggests that the evaluation of tumor‐infiltrating lymphocytes both at baseline and throughout cancer therapy can be valuable for predicting and monitoring treatment responses. Tumor heterogeneity however complicates the assessment of tumor‐infiltrating lymphocytes. In this study, the authors used an animal model and three‐dimensional printing technology to achieve guided tumor spatial segmentation and regional evaluation of tumor‐infiltrating lymphocytes. They present a feasible, non‐invasive magnetic resonance imaging‐based model for evaluating tumor‐infiltrating lymphocytes in hepatocellular carcinoma that takes spatial heterogeneity into account and could potentially inform the immunotherapy response in patients.
Tumor-infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi-parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi-parametric MRI was performed on hepatocellular carcinoma (HCC) mice (N = 28). Three-dimensional (3D) printing was employed for tissue sampling, to match the multi-parametric MRI data with tumor tissues, followed by flow cytometry analysis and next-generation RNA-sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL-related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T-cells, CD4+ T-cells, CD8+ T-cells, PD1 + CD8+ T-cells, B-cells, macrophages, and regulatory T-cells (correlation coefficients ranged from -0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non-inflamed subclasses, with the proportion of T-cells, CD8+ T-cells, and PD1 + CD8+ T-cells significantly higher in the inflamed group compared to the non-inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z-score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721-0.910) and a cut-off value of -0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z-score was related to the gene expression of T-cell activation, chemokine production, and cell adhesion. The tissue-matched analysis of multi-parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses.
Tumor‐infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility of multi‐parametric magnetic resonance imaging (MRI) in evaluating TILs and to develop an evaluation model that considers spatial heterogeneity. Multi‐parametric MRI was performed on hepatocellular carcinoma (HCC) mice ( N  = 28). Three‐dimensional (3D) printing was employed for tissue sampling, to match the multi‐parametric MRI data with tumor tissues, followed by flow cytometry analysis and next‐generation RNA‐sequencing. Pearson's correlation, multivariate logistic regression, and receiver operating characteristic (ROC) curve analyses were utilized to model TIL‐related MRI parameters. MRI quantitative parameters, including T1 relaxation times and perfusion, were correlated with the infiltration of leukocytes, T‐cells, CD4+ T‐cells, CD8+ T‐cells, PD1 + CD8+ T‐cells, B‐cells, macrophages, and regulatory T‐cells (correlation coefficients ranged from −0.656 to 0.482, p <.05) in tumor tissues. TILs were clustered into inflamed and non‐inflamed subclasses, with the proportion of T‐cells, CD8+ T‐cells, and PD1 + CD8+ T‐cells significantly higher in the inflamed group compared to the non‐inflamed group (43.37% vs. 25.45%, 50.83% vs. 34.90%, 40.45% vs. 29.47%, respectively; p <.001). The TIL evaluation model, based on the Z‐score combining Kep and T1post, was able to distinguish between these subgroups, yielding an area under the curve of 0.816 (95% confidence interval 0.721–0.910) and a cut‐off value of −0.03 (sensitivity 68.4%, specificity 91.3%). Additionally, the Z‐score was related to the gene expression of T‐cell activation, chemokine production, and cell adhesion. The tissue‐matched analysis of multi‐parametric MRI offers a feasible method of regional evaluation and can distinguish between TIL subclasses.
Author Song, Chenyu
Wang, Huanjun
Peng, Zhenpeng
Huang, Mengqi
Cai, Huasong
Zhou, Xiaoqi
Wang, Jifei
Feng, Shi‐Ting
Lin, Yingyu
Wang, Meng
Dong, Zhi
AuthorAffiliation 1 Department of Radiology, The First Affiliated Hospital Sun Yat‐sen University Guangzhou China
2 Department of Radiology, Tongji Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan China
AuthorAffiliation_xml – name: 1 Department of Radiology, The First Affiliated Hospital Sun Yat‐sen University Guangzhou China
– name: 2 Department of Radiology, Tongji Hospital, Tongji Medical College Huazhong University of Science and Technology Wuhan China
Author_xml – sequence: 1
  givenname: Mengqi
  surname: Huang
  fullname: Huang, Mengqi
  organization: Huazhong University of Science and Technology
– sequence: 2
  givenname: Chenyu
  surname: Song
  fullname: Song, Chenyu
  organization: Sun Yat‐sen University
– sequence: 3
  givenname: Xiaoqi
  surname: Zhou
  fullname: Zhou, Xiaoqi
  organization: Sun Yat‐sen University
– sequence: 4
  givenname: Huanjun
  surname: Wang
  fullname: Wang, Huanjun
  organization: Sun Yat‐sen University
– sequence: 5
  givenname: Yingyu
  surname: Lin
  fullname: Lin, Yingyu
  organization: Sun Yat‐sen University
– sequence: 6
  givenname: Jifei
  surname: Wang
  fullname: Wang, Jifei
  organization: Sun Yat‐sen University
– sequence: 7
  givenname: Huasong
  surname: Cai
  fullname: Cai, Huasong
  organization: Sun Yat‐sen University
– sequence: 8
  givenname: Meng
  surname: Wang
  fullname: Wang, Meng
  organization: Sun Yat‐sen University
– sequence: 9
  givenname: Zhenpeng
  surname: Peng
  fullname: Peng, Zhenpeng
  organization: Sun Yat‐sen University
– sequence: 10
  givenname: Zhi
  surname: Dong
  fullname: Dong, Zhi
  email: dongzh7@mail.sysu.edu.cn
  organization: Sun Yat‐sen University
– sequence: 11
  givenname: Shi‐Ting
  orcidid: 0000-0002-0869-7290
  surname: Feng
  fullname: Feng, Shi‐Ting
  email: fengsht@mail.sysu.edu.cn
  organization: Sun Yat‐sen University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/39635936$$D View this record in MEDLINE/PubMed
BookMark eNp1kc1u1DAUhS1URKeFBS-ALLEpi7T-iZ3MCqFRoYOKkNDsLY9z03jk2IOdFGXXR-gz8iR4SFsBEitL93w-OveeE3TkgweEXlNyTglhF3ZnzrlgNX2GFpQsq4IwKo7QImukqCiXx-gkpR0hlApSvkDHfCm5WHK5QLuNTWmEn3f3vR5MBw3WXrsp2YRDi798W2O41W7Ug_U3eOgAD2MfIra-tW6I89hN_b4LZhogZQF3sNdDMODc6HTERkdjfej1S_S81S7Bq4f3FG0-Xm5WV8X110_r1YfrwpSkpEXeiIAu620NDZha1kRvTaO3TQ1C5rlgEqqWNS0IMFTQStO2AQayqVrNDT9F72fb_bjtoTHgc06n9tH2Ok4qaKv-Vrzt1E24VZTWTFLGssPZg0MM30dIg-ptOuyjPYQxKU5LKTghosro23_QXRhjvuCBkrKkVS14pt78Gekpy2MNGXg3AyaGlCK0Twgl6lCxyhWr3xVn9mJmf1gH0_9Btf68mn_8Au_sq4M
Cites_doi 10.1002/hep.30889
10.1038/cr.2016.151
10.1186/s12943-021-01428-1
10.1016/j.jhep.2021.06.028
10.1007/s00261-020-02945-1
10.1097/RLI.0000000000000586
10.1158/0008-5472.CAN-19-0213
10.1177/02841851211065935
10.1056/NEJMoa1915745
10.1016/j.ccell.2023.04.010
10.1016/j.mex.2020.100921
10.1186/s40425-017-0243-4
10.1038/s41467-020-18582-7
10.3389/fimmu.2022.952413
10.1001/jamaoncol.2020.4930
10.1007/s11547-022-01569-3
10.1038/nm.3541
10.1097/MD.0000000000013301
10.1016/j.mri.2022.06.003
10.1038/s41572-020-00240-3
10.1016/j.semcdb.2016.10.001
10.1016/j.ccell.2021.10.001
10.1016/j.mri.2022.10.011
10.1186/s40425-019-0814-7
10.1002/jmri.26974
10.3390/ijms22083867
10.1016/j.neo.2019.08.003
10.1002/cncr.32076
10.1016/j.jhep.2012.12.015
ContentType Journal Article
Copyright 2024 The Author(s). published by John Wiley & Sons Ltd on behalf of UICC.
2024 The Author(s). International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.
2024. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2024 The Author(s). published by John Wiley & Sons Ltd on behalf of UICC.
– notice: 2024 The Author(s). International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.
– notice: 2024. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
DBID 24P
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7T5
7TO
7U9
H94
K9.
7X8
5PM
DOI 10.1002/ijc.35281
DatabaseName Wiley Online Library Open Access
CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Immunology Abstracts
Oncogenes and Growth Factors Abstracts
Virology and AIDS Abstracts
AIDS and Cancer Research Abstracts
ProQuest Health & Medical Complete (Alumni)
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
AIDS and Cancer Research Abstracts
ProQuest Health & Medical Complete (Alumni)
Immunology Abstracts
Virology and AIDS Abstracts
Oncogenes and Growth Factors Abstracts
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
AIDS and Cancer Research Abstracts

MEDLINE

CrossRef
Database_xml – sequence: 1
  dbid: 24P
  name: Wiley Online Library Open Access
  url: https://authorservices.wiley.com/open-science/open-access/browse-journals.html
  sourceTypes: Publisher
– sequence: 2
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
DocumentTitleAlternate Huang et al
EISSN 1097-0215
EndPage 1643
ExternalDocumentID PMC11826122
39635936
10_1002_ijc_35281
IJC35281
Genre researchArticle
Journal Article
GrantInformation_xml – fundername: National Natural Science Foundation of China
  funderid: 81771908; 81971684; 82001882; 82271958; 82471948
– fundername: Foundation of Tongji Hospital
  funderid: 2022B14
– fundername: Natural Science Foundation of Guangdong Province
  funderid: 2023A1515011097; 2024A1515012149
– fundername: National Natural Science Foundation of China
  grantid: 81771908
– fundername: Natural Science Foundation of Guangdong Province
  grantid: 2023A1515011097
– fundername: National Natural Science Foundation of China
  grantid: 81971684
– fundername: National Natural Science Foundation of China
  grantid: 82271958
– fundername: Natural Science Foundation of Guangdong Province
  grantid: 2024A1515012149
– fundername: National Natural Science Foundation of China
  grantid: 82471948
– fundername: National Natural Science Foundation of China
  grantid: 82001882
– fundername: Foundation of Tongji Hospital
  grantid: 2022B14
GroupedDBID ---
-~X
.3N
.GA
05W
0R~
10A
1L6
1OB
1OC
1ZS
24P
33P
3SF
3WU
4.4
4ZD
50Y
50Z
51W
51X
52M
52N
52O
52P
52R
52S
52T
52U
52V
52W
52X
5GY
5VS
66C
702
7PT
8-0
8-1
8-3
8-4
8-5
8UM
930
A01
A03
AAESR
AAEVG
AAHHS
AAHQN
AAIPD
AAMNL
AANLZ
AAONW
AAXRX
AAYCA
AAZKR
ABCQN
ABCUV
ABIJN
ABJNI
ABLJU
ABOCM
ABPVW
ABQWH
ABXGK
ACAHQ
ACCFJ
ACCZN
ACFBH
ACGFO
ACGFS
ACGOF
ACIWK
ACMXC
ACPOU
ACPRK
ACXBN
ACXQS
ADBBV
ADBTR
ADEOM
ADIZJ
ADKYN
ADMGS
ADOZA
ADXAS
ADZMN
ADZOD
AEEZP
AEGXH
AEIGN
AEIMD
AENEX
AEQDE
AEUQT
AEUYR
AFBPY
AFFPM
AFGKR
AFPWT
AFRAH
AFWVQ
AFZJQ
AHBTC
AHMBA
AIACR
AIAGR
AITYG
AIURR
AIWBW
AJBDE
ALAGY
ALMA_UNASSIGNED_HOLDINGS
ALUQN
ALVPJ
AMBMR
AMYDB
ATUGU
AZBYB
AZVAB
BAFTC
BFHJK
BHBCM
BMXJE
BROTX
BRXPI
BY8
C45
CS3
D-6
D-7
D-E
D-F
DCZOG
DPXWK
DR2
DRFUL
DRMAN
DRSTM
DU5
EBS
F00
F01
F04
F5P
FUBAC
G-S
G.N
GNP
GODZA
H.X
HBH
HGLYW
HHY
HHZ
HZ~
IH2
IX1
J0M
JPC
KBYEO
KQQ
L7B
LATKE
LAW
LC2
LC3
LEEKS
LH4
LITHE
LOXES
LP6
LP7
LUTES
LYRES
MEWTI
MK4
MRFUL
MRMAN
MRSTM
MSFUL
MSMAN
MSSTM
MXFUL
MXMAN
MXSTM
N04
N05
N9A
NF~
NNB
O66
O9-
OIG
OK1
OVD
P2P
P2W
P2X
P2Z
P4B
P4D
PQQKQ
Q.N
Q11
QB0
QRW
R.K
RIWAO
ROL
RWI
RX1
RYL
SUPJJ
TEORI
UB1
UDS
V2E
V8K
V9Y
W2D
W8V
W99
WBKPD
WHWMO
WIB
WIH
WIJ
WIK
WJL
WOHZO
WQJ
WRC
WUP
WVDHM
WWO
WXI
WXSBR
XG1
XPP
XV2
ZZTAW
~IA
~WT
AAMMB
AAYXX
AEFGJ
AEYWJ
AGHNM
AGXDD
AGYGG
AIDQK
AIDYY
CITATION
O8X
CGR
CUY
CVF
ECM
EIF
NPM
7T5
7TO
7U9
H94
K9.
7X8
5PM
ID FETCH-LOGICAL-c4041-1000ea48b8edec8680abcdabd8e56a48526e7f2dfe5ec1517a1fde2e6d7fa3c3
IEDL.DBID 24P
ISICitedReferencesCount 0
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=001371286800001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 0020-7136
1097-0215
IngestDate Tue Nov 04 02:06:24 EST 2025
Thu Jul 10 17:31:26 EDT 2025
Sat Nov 29 14:36:29 EST 2025
Mon Jul 21 06:04:17 EDT 2025
Sat Nov 29 03:46:47 EST 2025
Fri Feb 14 09:50:46 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 8
Keywords magnetic resonance imaging
tumor‐infiltrating lymphocytes
hepatocellular carcinoma
three‐dimensional printing
Language English
License Attribution-NonCommercial-NoDerivs
2024 The Author(s). International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.
This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c4041-1000ea48b8edec8680abcdabd8e56a48526e7f2dfe5ec1517a1fde2e6d7fa3c3
Notes Mengqi Huang and Chenyu Song have contributed equally and considered as co‐first author.
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
ORCID 0000-0002-0869-7290
OpenAccessLink https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fijc.35281
PMID 39635936
PQID 3166417853
PQPubID 105430
PageCount 10
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_11826122
proquest_miscellaneous_3146530057
proquest_journals_3166417853
pubmed_primary_39635936
crossref_primary_10_1002_ijc_35281
wiley_primary_10_1002_ijc_35281_IJC35281
PublicationCentury 2000
PublicationDate 15 April 2025
PublicationDateYYYYMMDD 2025-04-15
PublicationDate_xml – month: 04
  year: 2025
  text: 15 April 2025
  day: 15
PublicationDecade 2020
PublicationPlace Hoboken, USA
PublicationPlace_xml – name: Hoboken, USA
– name: United States
– name: Hoboken
PublicationTitle International journal of cancer
PublicationTitleAlternate Int J Cancer
PublicationYear 2025
Publisher John Wiley & Sons, Inc
Wiley Subscription Services, Inc
Publisher_xml – name: John Wiley & Sons, Inc
– name: Wiley Subscription Services, Inc
References 2017; 5
2021; 46
2019; 7
2021; 7
2017; 64
2023; 96
2021; 20
2021; 22
2022; 92
2020; 382
2019; 54
2017; 27
2019; 79
2019; 125
2020; 11
2014; 20
2023; 64
2020; 7
2020; 6
2023; 41
2021; 75
2013; 58
2020; 51
2019; 21
2020; 71
2021; 39
2022; 13
2018; 97
2022; 127
e_1_2_10_23_1
e_1_2_10_24_1
e_1_2_10_21_1
e_1_2_10_22_1
e_1_2_10_20_1
e_1_2_10_2_1
e_1_2_10_4_1
e_1_2_10_18_1
e_1_2_10_3_1
e_1_2_10_19_1
e_1_2_10_6_1
e_1_2_10_16_1
e_1_2_10_5_1
e_1_2_10_8_1
e_1_2_10_14_1
e_1_2_10_7_1
e_1_2_10_15_1
e_1_2_10_12_1
e_1_2_10_9_1
e_1_2_10_13_1
e_1_2_10_10_1
e_1_2_10_11_1
Magill ST (e_1_2_10_17_1) 2020; 11
e_1_2_10_30_1
e_1_2_10_29_1
e_1_2_10_27_1
e_1_2_10_28_1
e_1_2_10_25_1
e_1_2_10_26_1
References_xml – volume: 54
  start-page: 737
  issue: 12
  year: 2019
  end-page: 743
  article-title: Assessment of hepatic perfusion using GRASP MRI: bringing liver MRI on a new level
  publication-title: Invest Radiol
– volume: 92
  start-page: 33
  year: 2022
  end-page: 44
  article-title: MRI and US imaging reveal evolution of spatial heterogeneity of murine tumor vasculature
  publication-title: Magn Reson Imaging
– volume: 7
  year: 2020
  article-title: A method to establish a c‐Myc transgenic mouse model of hepatocellular carcinoma
  publication-title: MethodsX
– volume: 64
  start-page: 48
  year: 2017
  end-page: 57
  article-title: Cancer heterogeneity and imaging
  publication-title: Semin Cell Dev Biol
– volume: 21
  start-page: 1036
  issue: 10
  year: 2019
  end-page: 1050
  article-title: VCAM‐1 density and tumor perfusion predict T‐cell infiltration and treatment response in preclinical models
  publication-title: Neoplasia
– volume: 5
  start-page: 44
  year: 2017
  article-title: Identifying baseline immune‐related biomarkers to predict clinical outcome of immunotherapy
  publication-title: J Immunother Cancer
– volume: 125
  start-page: 3312
  issue: 19
  year: 2019
  end-page: 3319
  article-title: Immune checkpoint inhibitors for hepatocellular carcinoma
  publication-title: Cancer
– volume: 11
  start-page: 4803
  issue: 1
  year: 2020
  article-title: Multiplatform genomic profiling and magnetic resonance imaging identify mechanisms underlying intratumor heterogeneity in meningioma
  publication-title: Nat Commun
– volume: 41
  start-page: 1134
  issue: 6
  year: 2023
  end-page: 1151
  article-title: Tailoring vascular phenotype through AAV therapy promotes anti‐tumor immunity in glioma
  publication-title: Cancer Cell
– volume: 75
  start-page: 1397
  issue: 6
  year: 2021
  end-page: 1408
  article-title: Single‐cell atlas of tumor cell evolution in response to therapy in hepatocellular carcinoma and intrahepatic cholangiocarcinoma
  publication-title: J Hepatol
– volume: 127
  start-page: 1342
  issue: 12
  year: 2022
  end-page: 1354
  article-title: Radiomics for prediction of response to EGFR‐TKI based on metastasis/brain parenchyma (M/BP)‐interface
  publication-title: Radiol Med
– volume: 27
  start-page: 109
  issue: 1
  year: 2017
  end-page: 118
  article-title: Regulatory T cells in cancer immunotherapy
  publication-title: Cell Res
– volume: 39
  start-page: 1497
  issue: 11
  year: 2021
  end-page: 1518
  article-title: Determinants of anti‐PD‐1 response and resistance in clear cell renal cell carcinoma
  publication-title: Cancer Cell
– volume: 46
  start-page: 2575
  issue: 6
  year: 2021
  end-page: 2583
  article-title: Comparative study of evaluating the microcirculatory function status of primary small HCC between the CE (DCE‐MRI) and non‐CE (IVIM‐DWI) MR perfusion imaging
  publication-title: Abdom Radiol
– volume: 64
  start-page: 32
  issue: 1
  year: 2023
  end-page: 41
  article-title: Evaluation of response in patients with hepatocellular carcinoma treated with intratumoral dendritic cell vaccination using intravoxel incoherent motion (IVIM) MRI and histogram analysis
  publication-title: Acta Radiol
– volume: 13
  year: 2022
  article-title: Construction and validation of an epigenetic regulator signature as a novel biomarker for prognosis, immunotherapy, and chemotherapy in hepatocellular carcinoma
  publication-title: Front Immunol
– volume: 97
  issue: 50
  year: 2018
  article-title: Prognostic value of tumor‐infiltrating lymphocytes in hepatocellular carcinoma: a meta‐analysis
  publication-title: Medicine
– volume: 20
  start-page: 131
  issue: 1
  year: 2021
  article-title: Crosstalk between cancer‐associated fibroblasts and immune cells in the tumor microenvironment: new findings and future perspectives
  publication-title: Mol Cancer
– volume: 7
  start-page: 331
  issue: 1
  year: 2019
  article-title: PD1 CD8 T cells correlate with exhausted signature and poor clinical outcome in hepatocellular carcinoma
  publication-title: J Immunother Cancer
– volume: 96
  start-page: 1
  year: 2023
  end-page: 7
  article-title: Prediction of therapeutic response of advanced hepatocellular carcinoma to combined targeted immunotherapy by MRI
  publication-title: Magn Reson Imaging
– volume: 22
  start-page: 3867
  issue: 8
  year: 2021
  article-title: Physiological imaging methods for evaluating response to immunotherapies in glioblastomas
  publication-title: Int J Mol Sci
– volume: 71
  start-page: 1247
  issue: 4
  year: 2020
  end-page: 1261
  article-title: Dual programmed death receptor‐1 and vascular endothelial growth factor receptor‐2 blockade promotes vascular normalization and enhances antitumor immune responses in hepatocellular carcinoma
  publication-title: Hepatology
– volume: 7
  start-page: 6
  issue: 1
  year: 2021
  article-title: Hepatocellular carcinoma
  publication-title: Nat Rev Dis Primers
– volume: 58
  start-page: 977
  issue: 5
  year: 2013
  end-page: 983
  article-title: The functional impairment of HCC‐infiltrating γδ T cells, partially mediated by regulatory T cells in a TGFβ‐ and IL‐10‐dependent manner
  publication-title: J Hepatol
– volume: 382
  start-page: 1894
  issue: 20
  year: 2020
  end-page: 1905
  article-title: Atezolizumab plus Bevacizumab in unresectable hepatocellular carcinoma
  publication-title: N Engl J Med
– volume: 6
  issue: 12
  year: 2020
  article-title: Systemic therapy and sequencing options in advanced hepatocellular carcinoma: a systematic review and network meta‐analysis
  publication-title: JAMA Oncol
– volume: 79
  start-page: 3952
  issue: 15
  year: 2019
  end-page: 3964
  article-title: Multiparametric MRI and coregistered histology identify tumor habitats in breast cancer mouse models
  publication-title: Cancer Res
– volume: 20
  start-page: 607
  issue: 6
  year: 2014
  end-page: 615
  article-title: Tumor endothelium FasL establishes a selective immune barrier promoting tolerance in tumors
  publication-title: Nat Med
– volume: 51
  start-page: 1755
  issue: 6
  year: 2020
  end-page: 1763
  article-title: Diagnostic value of Gd‐EOB‐DTPA‐enhanced MRI for the expression of Ki67 and microvascular density in hepatocellular carcinoma
  publication-title: J Magn Reson Imaging
– ident: e_1_2_10_24_1
  doi: 10.1002/hep.30889
– ident: e_1_2_10_23_1
  doi: 10.1038/cr.2016.151
– ident: e_1_2_10_9_1
  doi: 10.1186/s12943-021-01428-1
– ident: e_1_2_10_14_1
  doi: 10.1016/j.jhep.2021.06.028
– ident: e_1_2_10_12_1
  doi: 10.1007/s00261-020-02945-1
– ident: e_1_2_10_13_1
  doi: 10.1097/RLI.0000000000000586
– ident: e_1_2_10_18_1
  doi: 10.1158/0008-5472.CAN-19-0213
– ident: e_1_2_10_11_1
  doi: 10.1177/02841851211065935
– ident: e_1_2_10_3_1
  doi: 10.1056/NEJMoa1915745
– ident: e_1_2_10_8_1
  doi: 10.1016/j.ccell.2023.04.010
– ident: e_1_2_10_20_1
  doi: 10.1016/j.mex.2020.100921
– ident: e_1_2_10_6_1
  doi: 10.1186/s40425-017-0243-4
– volume: 11
  start-page: 4803
  issue: 1
  year: 2020
  ident: e_1_2_10_17_1
  article-title: Multiplatform genomic profiling and magnetic resonance imaging identify mechanisms underlying intratumor heterogeneity in meningioma
  publication-title: Nat Commun
  doi: 10.1038/s41467-020-18582-7
– ident: e_1_2_10_30_1
  doi: 10.3389/fimmu.2022.952413
– ident: e_1_2_10_4_1
  doi: 10.1001/jamaoncol.2020.4930
– ident: e_1_2_10_19_1
  doi: 10.1007/s11547-022-01569-3
– ident: e_1_2_10_21_1
  doi: 10.1038/nm.3541
– ident: e_1_2_10_28_1
  doi: 10.1097/MD.0000000000013301
– ident: e_1_2_10_16_1
  doi: 10.1016/j.mri.2022.06.003
– ident: e_1_2_10_2_1
  doi: 10.1038/s41572-020-00240-3
– ident: e_1_2_10_15_1
  doi: 10.1016/j.semcdb.2016.10.001
– ident: e_1_2_10_7_1
  doi: 10.1016/j.ccell.2021.10.001
– ident: e_1_2_10_10_1
  doi: 10.1016/j.mri.2022.10.011
– ident: e_1_2_10_29_1
  doi: 10.1186/s40425-019-0814-7
– ident: e_1_2_10_25_1
  doi: 10.1002/jmri.26974
– ident: e_1_2_10_26_1
  doi: 10.3390/ijms22083867
– ident: e_1_2_10_27_1
  doi: 10.1016/j.neo.2019.08.003
– ident: e_1_2_10_5_1
  doi: 10.1002/cncr.32076
– ident: e_1_2_10_22_1
  doi: 10.1016/j.jhep.2012.12.015
SSID ssj0011504
Score 2.474611
Snippet Tumor‐infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility...
Tumor-infiltrating lymphocytes (TILs) play critical roles in the tumor microenvironment and immunotherapy response. This study aims to explore the feasibility...
SourceID pubmedcentral
proquest
pubmed
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 1634
SubjectTerms Animals
Carcinoma, Hepatocellular - diagnostic imaging
Carcinoma, Hepatocellular - immunology
Carcinoma, Hepatocellular - pathology
CD4 antigen
CD8 antigen
Cell activation
Cell adhesion
Chemokines
Feasibility studies
Flow cytometry
Gene expression
Hepatocellular carcinoma
Humans
Immunotherapy
Inflammation
Leukocytes
Liver cancer
Liver Neoplasms - diagnostic imaging
Liver Neoplasms - immunology
Liver Neoplasms - pathology
Lymphocytes
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - pathology
Macrophages
Magnetic resonance imaging
Magnetic Resonance Imaging - methods
Male
Metastases
Mice
Multiparametric Magnetic Resonance Imaging - methods
PD-1 protein
RESEARCH ARTICLE
Spatial heterogeneity
three‐dimensional printing
Tumor microenvironment
Tumor Microenvironment - immunology
Tumors
tumor‐infiltrating lymphocytes
Title Tissue‐matched analysis of MRI evaluating the tumor infiltrating lymphocytes in hepatocellular carcinoma
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fijc.35281
https://www.ncbi.nlm.nih.gov/pubmed/39635936
https://www.proquest.com/docview/3166417853
https://www.proquest.com/docview/3146530057
https://pubmed.ncbi.nlm.nih.gov/PMC11826122
Volume 156
WOSCitedRecordID wos001371286800001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVWIB
  databaseName: Wiley Online Library - Journals
  customDbUrl:
  eissn: 1097-0215
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0011504
  issn: 0020-7136
  databaseCode: DRFUL
  dateStart: 19960101
  isFulltext: true
  titleUrlDefault: https://onlinelibrary.wiley.com
  providerName: Wiley-Blackwell
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpZ3LbtQwFIaPqhYhNtwvgVIZxIJNqGM7jkesUGFEUVtV1YBmFzmO007VJmguSN3xCDwjT8I5zgVGFRISmyiyHcXx8eV3bH8H4FXCpc2scLGV1ShWxvK4QFkUezfKrNReu8Dp_nKQHR2Z6XR0vAFv-7MwLR9i-OFGLSP019TAbbHY_Q0NnZ27N4QmwanPVpJIQ34bhDoelhBQ6XQIZh7jTEz3WCEudodH1wejawrz-kbJPwVsGIHGd_4r73fhdic82bu2ptyDDV_fh5uH3dL6AzifBBP8_P4DNSxasmS245WwpmKHJ_usB4PXpwxVI1uuLps5wwo6uwjoXQy-uMK60bgrlK8Ywc5wqFs2tDRAe12ZI7dFdXNpH8Jk_GGy9zHuHDHETnFFW94491aZwvjSO6MNt4UrbVEan2oMT4X2WSXKyqfeoYTIbFKVXnhdZpWVTj6Czbqp_RNgUtuUyxJ1XiWULNTISGmV5g5VBoHfI3jZGyT_2uI28hasLHIstDwUWgTbvanyrsUtcplorZIM1UcEL4ZobCv0lbb2zYrSEE2Ozt9G8Li17PAWiT0ReTeMwKzZfEhAHO71mHp2FnjcYY6WCBHB62D0v-c83_-0F26e_nvSZ3BLkM9h4kum27C5nK_8c7jhvi1ni_lOqPN4zaZmB7ben4w_H_wC5gkKBA
linkProvider Wiley-Blackwell
linkToHtml http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpZ3LbtQwFIaPqoKADfdLoIBBLNiEOrbjeCQ2qKLqwMyoQiPUXeQ4Dp2qTdB0Bqk7HoFn5Ek4x7nAqEJCYhfZjuL4-Ni_b58BXiVc2swKF1tZjWJlLI8LlEWxd6PMSu21C5zuz5NsNjNHR6PDLXjbn4Vp-RDDhBt5RmivycFpQnr3NzV0ceLeEJsExz5XFPYyVMuFOhzWEFDqdAxmHuNQTPdcIS52h1c3e6NLEvPyTsk_FWzogvZv_V_mb8PNTnqyd21duQNbvr4L16bd4vo9OJkHI_z8_gNVLNqyZLYjlrCmYtNPY9ajwesvDHUjW63PmiXDKro4DfBdDD69wNrRuAsUsBjBjrGzWzW0OEC7XZmji4vq5szeh_n--_neQdxdxRA7xRVteuPcW2UK40vvjDbcFq60RWl8qjE8FdpnlSgrn3qHIiKzSVV64XWZVVY6-QC266b2j4BJbVMuS1R6lVCyUCMjpVWaO9QZhH6P4GVvkfxrC9zIW7SyyLHQ8lBoEez0tso7nzvPZaK1SjLUHxG8GKLRW-gvbe2bNaUhnhydwI3gYWva4SsS2yK63zACs2H0IQGRuDdj6sVxIHKHUVoiRASvg9X_nvN8_GEvPDz-96TP4frBfDrJJ-PZxydwQ9ANxESbTHdge7Vc-6dw1X1bLc6Xz4ID_AIVpAtn
linkToPdf http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpZ3NbtQwEMdH1RZVXPimBAoYxIFLqGM7jlfiglpWLGxXVbWg3iLHduhWbVJtd5F64xF4Rp6EsfMBqwoJiVtkO0ri8dh_x_ZvAF4llOtMMxNrXg5joTSNC5RFsTPDTHPppAmc7i-TbDpVx8fDww14252FafgQ_Q837xmhv_YO7i5sufubGjo_NW88mwTnPpvCB5EZwOb-0ejzpF9FQLHTUphpjJMx2ZGFKNvtb14fj66JzOt7Jf_UsGEQGt3-v9e_A7da8UneNa3lLmy46h5sHbTL6_fhdBbM8PP7D9SxaE1LdMssIXVJDo7GpIODV18JKkeyXJ3XC4KNdH4W8LuYfHaF7aM2VyhhMYOc4HC3rP3ygN_vSowPXVTV5_oBzEbvZ3sf4jYYQ2wEFX7bG6VOC1UoZ51RUlFdGKsLq1wqMT1l0mUls6VLnUEZkemktI45abNSc8MfwqCqK_cICJc6pdyi1iuZ4IUYKs61kNSg0vDw9whedhbJLxrkRt7AlVmOlZaHSotgp7NV3nrdZc4TKUWSoQKJ4EWfjf7iv1JXrl75Mp4o58_gRrDdmLZ_CsfeyEc4jECtGb0v4Fnc6znV_CQwucM8LWEsgtfB6n9_83z8cS9cPP73os9h63B_lE_G009P4CbzIYg9bjLdgcFysXJP4Yb5tpxfLp61HvALaUsMfQ
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=Tissue%E2%80%90matched+analysis+of+MRI+evaluating+the+tumor+infiltrating+lymphocytes+in+hepatocellular+carcinoma&rft.jtitle=International+journal+of+cancer&rft.au=Huang%2C+Mengqi&rft.au=Song%2C+Chenyu&rft.au=Zhou%2C+Xiaoqi&rft.au=Wang%2C+Huanjun&rft.date=2025-04-15&rft.pub=John+Wiley+%26+Sons%2C+Inc&rft.issn=0020-7136&rft.eissn=1097-0215&rft.volume=156&rft.issue=8&rft.spage=1634&rft.epage=1643&rft_id=info:doi/10.1002%2Fijc.35281&rft_id=info%3Apmid%2F39635936&rft.externalDocID=PMC11826122
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0020-7136&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0020-7136&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0020-7136&client=summon