Immune Evasion of Hepatoma Cancer Stem-Like Cells from Natural Killer Cells
Background Poor prognosis in liver cancer is due to its high frequency of intrahepatic metastasis. Cancer stem-like cells (CSLCs), which possess the properties of stemness, tumor initiation capability, and resistance to therapy, also exhibit metastatic potential. Immune surveillance plays an importa...
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| Veröffentlicht in: | Annals of surgical oncology 2022-11, Vol.29 (12), p.7423-7433 |
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| creator | Kimura, Yuta Tsunedomi, Ryouichi Yoshimura, Kiyoshi Matsukuma, Satoshi Shindo, Yoshitaro Matsui, Hiroto Tokumitsu, Yukio Yoshida, Shin Iida, Michihisa Suzuki, Nobuaki Takeda, Shigeru Ioka, Tatsuya Hazama, Shoichi Nagano, Hiroaki |
| description | Background
Poor prognosis in liver cancer is due to its high frequency of intrahepatic metastasis. Cancer stem-like cells (CSLCs), which possess the properties of stemness, tumor initiation capability, and resistance to therapy, also exhibit metastatic potential. Immune surveillance plays an important role in the accomplishment of metastasis. Herein, the property of immune evasion in CSLCs was investigated.
Methods
Sphere cells were induced as CSLCs using a sphere induction medium containing neural survival factor-1. The expression of genes involved in immune evasion was determined using RNA-sequencing for sphere and parental cells followed by validation using flow cytometric analysis and ELISA. Susceptibility to natural killer (NK) cell-mediated cytotoxicity was examined by a chromium release assay. A xenograft model using BALB/c
nu/nu
mice was used to assess tumor growth. Gene set enrichment analysis was performed for interpreting RNA sequencing.
Results
The cell surface expressions of PD-L1, PD-L2, and CEACAM1 were upregulated and those of ULBP1 and MICA/MICB were downregulated in SK-sphere, CSLCs derived from SK-HEP-1, compared with that in parental cells. Levels of soluble MICA were elevated in conditioned medium from SK-sphere. Expression of HLA class I was not downregulated in SK-sphere. The susceptibilities to NK cell-mediated killing and secreted perforin were significantly lower in both CSLCs derived from SK-HEP-1 and HLE than in parental cells. Tumors formed upon inoculation of SK-sphere in immunodeficient mice harboring NK cells were larger than those formed upon inoculation of parental cells.
Conclusion
Human hepatoma cell line-derived CSLCs may possess immune evasion properties, especially from NK cell-mediated immunity. |
| doi_str_mv | 10.1245/s10434-022-12220-w |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2694415627</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2694415627</sourcerecordid><originalsourceid>FETCH-LOGICAL-c418t-270a4a7e468acf9162e2271ba2b9fb534e4cda92159a8585279bf55c28372e33</originalsourceid><addsrcrecordid>eNp9kDFPwzAQhS0EEqXwB5gssbAY7IsdJyOqCq1awUB3ywkXlJLExU6o-PeYBgmJgelOd997enqEXAp-I0Cq2yC4TCTjAEwAAGf7IzIRKp5kmonjuPM0Yzmk6pSchbDlXOiEqwlZLdt26JDOP2yoXUddRRe4s71rLZ3ZrkRPn3ts2bp-QzrDpgm08q6lj7YfvG3oqm6ayBw-5-Sksk3Ai585JZv7-Wa2YOunh-Xsbs1KKbKegeZWWo0xmS2rXKSAAFoUFoq8KmJmlOWLzUGo3GYqU6DzolKqhCzRgEkyJdej7c679wFDb9o6lDGA7dANwUCaSylUCjqiV3_QrRt8F8MZ0JBER1AyUjBSpXcheKzMztet9Z9GcPNdrxnrNbFec6jX7KMoGUUhwt0r-l_rf1Rf2UZ7eg</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2723283254</pqid></control><display><type>article</type><title>Immune Evasion of Hepatoma Cancer Stem-Like Cells from Natural Killer Cells</title><source>SpringerLink Journals - AutoHoldings</source><creator>Kimura, Yuta ; Tsunedomi, Ryouichi ; Yoshimura, Kiyoshi ; Matsukuma, Satoshi ; Shindo, Yoshitaro ; Matsui, Hiroto ; Tokumitsu, Yukio ; Yoshida, Shin ; Iida, Michihisa ; Suzuki, Nobuaki ; Takeda, Shigeru ; Ioka, Tatsuya ; Hazama, Shoichi ; Nagano, Hiroaki</creator><creatorcontrib>Kimura, Yuta ; Tsunedomi, Ryouichi ; Yoshimura, Kiyoshi ; Matsukuma, Satoshi ; Shindo, Yoshitaro ; Matsui, Hiroto ; Tokumitsu, Yukio ; Yoshida, Shin ; Iida, Michihisa ; Suzuki, Nobuaki ; Takeda, Shigeru ; Ioka, Tatsuya ; Hazama, Shoichi ; Nagano, Hiroaki</creatorcontrib><description>Background
Poor prognosis in liver cancer is due to its high frequency of intrahepatic metastasis. Cancer stem-like cells (CSLCs), which possess the properties of stemness, tumor initiation capability, and resistance to therapy, also exhibit metastatic potential. Immune surveillance plays an important role in the accomplishment of metastasis. Herein, the property of immune evasion in CSLCs was investigated.
Methods
Sphere cells were induced as CSLCs using a sphere induction medium containing neural survival factor-1. The expression of genes involved in immune evasion was determined using RNA-sequencing for sphere and parental cells followed by validation using flow cytometric analysis and ELISA. Susceptibility to natural killer (NK) cell-mediated cytotoxicity was examined by a chromium release assay. A xenograft model using BALB/c
nu/nu
mice was used to assess tumor growth. Gene set enrichment analysis was performed for interpreting RNA sequencing.
Results
The cell surface expressions of PD-L1, PD-L2, and CEACAM1 were upregulated and those of ULBP1 and MICA/MICB were downregulated in SK-sphere, CSLCs derived from SK-HEP-1, compared with that in parental cells. Levels of soluble MICA were elevated in conditioned medium from SK-sphere. Expression of HLA class I was not downregulated in SK-sphere. The susceptibilities to NK cell-mediated killing and secreted perforin were significantly lower in both CSLCs derived from SK-HEP-1 and HLE than in parental cells. Tumors formed upon inoculation of SK-sphere in immunodeficient mice harboring NK cells were larger than those formed upon inoculation of parental cells.
Conclusion
Human hepatoma cell line-derived CSLCs may possess immune evasion properties, especially from NK cell-mediated immunity.</description><identifier>ISSN: 1068-9265</identifier><identifier>EISSN: 1534-4681</identifier><identifier>DOI: 10.1245/s10434-022-12220-w</identifier><language>eng</language><publisher>Cham: Springer International Publishing</publisher><subject>Cancer ; CD66 antigen ; CEACAM1 protein ; Cell surface ; Cell-mediated immunity ; Cytotoxicity ; Enzyme-linked immunosorbent assay ; Flow cytometry ; Gene set enrichment analysis ; Hepatoma ; Histocompatibility antigen HLA ; Immune evasion ; Immunodeficiency ; Immunosurveillance ; Inoculation ; Liver cancer ; Major histocompatibility complex ; Medical prognosis ; Medicine ; Medicine & Public Health ; Metastases ; Metastasis ; Natural killer cells ; Oncology ; PD-L1 protein ; Perforin ; Surgery ; Surgical Oncology ; Survival factor ; Translational Research ; Xenografts</subject><ispartof>Annals of surgical oncology, 2022-11, Vol.29 (12), p.7423-7433</ispartof><rights>Society of Surgical Oncology 2022</rights><rights>Society of Surgical Oncology 2022.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c418t-270a4a7e468acf9162e2271ba2b9fb534e4cda92159a8585279bf55c28372e33</citedby><cites>FETCH-LOGICAL-c418t-270a4a7e468acf9162e2271ba2b9fb534e4cda92159a8585279bf55c28372e33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1245/s10434-022-12220-w$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1245/s10434-022-12220-w$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids></links><search><creatorcontrib>Kimura, Yuta</creatorcontrib><creatorcontrib>Tsunedomi, Ryouichi</creatorcontrib><creatorcontrib>Yoshimura, Kiyoshi</creatorcontrib><creatorcontrib>Matsukuma, Satoshi</creatorcontrib><creatorcontrib>Shindo, Yoshitaro</creatorcontrib><creatorcontrib>Matsui, Hiroto</creatorcontrib><creatorcontrib>Tokumitsu, Yukio</creatorcontrib><creatorcontrib>Yoshida, Shin</creatorcontrib><creatorcontrib>Iida, Michihisa</creatorcontrib><creatorcontrib>Suzuki, Nobuaki</creatorcontrib><creatorcontrib>Takeda, Shigeru</creatorcontrib><creatorcontrib>Ioka, Tatsuya</creatorcontrib><creatorcontrib>Hazama, Shoichi</creatorcontrib><creatorcontrib>Nagano, Hiroaki</creatorcontrib><title>Immune Evasion of Hepatoma Cancer Stem-Like Cells from Natural Killer Cells</title><title>Annals of surgical oncology</title><addtitle>Ann Surg Oncol</addtitle><description>Background
Poor prognosis in liver cancer is due to its high frequency of intrahepatic metastasis. Cancer stem-like cells (CSLCs), which possess the properties of stemness, tumor initiation capability, and resistance to therapy, also exhibit metastatic potential. Immune surveillance plays an important role in the accomplishment of metastasis. Herein, the property of immune evasion in CSLCs was investigated.
Methods
Sphere cells were induced as CSLCs using a sphere induction medium containing neural survival factor-1. The expression of genes involved in immune evasion was determined using RNA-sequencing for sphere and parental cells followed by validation using flow cytometric analysis and ELISA. Susceptibility to natural killer (NK) cell-mediated cytotoxicity was examined by a chromium release assay. A xenograft model using BALB/c
nu/nu
mice was used to assess tumor growth. Gene set enrichment analysis was performed for interpreting RNA sequencing.
Results
The cell surface expressions of PD-L1, PD-L2, and CEACAM1 were upregulated and those of ULBP1 and MICA/MICB were downregulated in SK-sphere, CSLCs derived from SK-HEP-1, compared with that in parental cells. Levels of soluble MICA were elevated in conditioned medium from SK-sphere. Expression of HLA class I was not downregulated in SK-sphere. The susceptibilities to NK cell-mediated killing and secreted perforin were significantly lower in both CSLCs derived from SK-HEP-1 and HLE than in parental cells. Tumors formed upon inoculation of SK-sphere in immunodeficient mice harboring NK cells were larger than those formed upon inoculation of parental cells.
Conclusion
Human hepatoma cell line-derived CSLCs may possess immune evasion properties, especially from NK cell-mediated immunity.</description><subject>Cancer</subject><subject>CD66 antigen</subject><subject>CEACAM1 protein</subject><subject>Cell surface</subject><subject>Cell-mediated immunity</subject><subject>Cytotoxicity</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Flow cytometry</subject><subject>Gene set enrichment analysis</subject><subject>Hepatoma</subject><subject>Histocompatibility antigen HLA</subject><subject>Immune evasion</subject><subject>Immunodeficiency</subject><subject>Immunosurveillance</subject><subject>Inoculation</subject><subject>Liver cancer</subject><subject>Major histocompatibility complex</subject><subject>Medical prognosis</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Natural killer cells</subject><subject>Oncology</subject><subject>PD-L1 protein</subject><subject>Perforin</subject><subject>Surgery</subject><subject>Surgical Oncology</subject><subject>Survival factor</subject><subject>Translational Research</subject><subject>Xenografts</subject><issn>1068-9265</issn><issn>1534-4681</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><recordid>eNp9kDFPwzAQhS0EEqXwB5gssbAY7IsdJyOqCq1awUB3ywkXlJLExU6o-PeYBgmJgelOd997enqEXAp-I0Cq2yC4TCTjAEwAAGf7IzIRKp5kmonjuPM0Yzmk6pSchbDlXOiEqwlZLdt26JDOP2yoXUddRRe4s71rLZ3ZrkRPn3ts2bp-QzrDpgm08q6lj7YfvG3oqm6ayBw-5-Sksk3Ai585JZv7-Wa2YOunh-Xsbs1KKbKegeZWWo0xmS2rXKSAAFoUFoq8KmJmlOWLzUGo3GYqU6DzolKqhCzRgEkyJdej7c679wFDb9o6lDGA7dANwUCaSylUCjqiV3_QrRt8F8MZ0JBER1AyUjBSpXcheKzMztet9Z9GcPNdrxnrNbFec6jX7KMoGUUhwt0r-l_rf1Rf2UZ7eg</recordid><startdate>20221101</startdate><enddate>20221101</enddate><creator>Kimura, Yuta</creator><creator>Tsunedomi, Ryouichi</creator><creator>Yoshimura, Kiyoshi</creator><creator>Matsukuma, Satoshi</creator><creator>Shindo, Yoshitaro</creator><creator>Matsui, Hiroto</creator><creator>Tokumitsu, Yukio</creator><creator>Yoshida, Shin</creator><creator>Iida, Michihisa</creator><creator>Suzuki, Nobuaki</creator><creator>Takeda, Shigeru</creator><creator>Ioka, Tatsuya</creator><creator>Hazama, Shoichi</creator><creator>Nagano, Hiroaki</creator><general>Springer International Publishing</general><general>Springer Nature B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H94</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope></search><sort><creationdate>20221101</creationdate><title>Immune Evasion of Hepatoma Cancer Stem-Like Cells from Natural Killer Cells</title><author>Kimura, Yuta ; Tsunedomi, Ryouichi ; Yoshimura, Kiyoshi ; Matsukuma, Satoshi ; Shindo, Yoshitaro ; Matsui, Hiroto ; Tokumitsu, Yukio ; Yoshida, Shin ; Iida, Michihisa ; Suzuki, Nobuaki ; Takeda, Shigeru ; Ioka, Tatsuya ; Hazama, Shoichi ; Nagano, Hiroaki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c418t-270a4a7e468acf9162e2271ba2b9fb534e4cda92159a8585279bf55c28372e33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Cancer</topic><topic>CD66 antigen</topic><topic>CEACAM1 protein</topic><topic>Cell surface</topic><topic>Cell-mediated immunity</topic><topic>Cytotoxicity</topic><topic>Enzyme-linked immunosorbent assay</topic><topic>Flow cytometry</topic><topic>Gene set enrichment analysis</topic><topic>Hepatoma</topic><topic>Histocompatibility antigen HLA</topic><topic>Immune evasion</topic><topic>Immunodeficiency</topic><topic>Immunosurveillance</topic><topic>Inoculation</topic><topic>Liver cancer</topic><topic>Major histocompatibility complex</topic><topic>Medical prognosis</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Natural killer cells</topic><topic>Oncology</topic><topic>PD-L1 protein</topic><topic>Perforin</topic><topic>Surgery</topic><topic>Surgical Oncology</topic><topic>Survival factor</topic><topic>Translational Research</topic><topic>Xenografts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kimura, Yuta</creatorcontrib><creatorcontrib>Tsunedomi, Ryouichi</creatorcontrib><creatorcontrib>Yoshimura, Kiyoshi</creatorcontrib><creatorcontrib>Matsukuma, Satoshi</creatorcontrib><creatorcontrib>Shindo, Yoshitaro</creatorcontrib><creatorcontrib>Matsui, Hiroto</creatorcontrib><creatorcontrib>Tokumitsu, Yukio</creatorcontrib><creatorcontrib>Yoshida, Shin</creatorcontrib><creatorcontrib>Iida, Michihisa</creatorcontrib><creatorcontrib>Suzuki, Nobuaki</creatorcontrib><creatorcontrib>Takeda, Shigeru</creatorcontrib><creatorcontrib>Ioka, Tatsuya</creatorcontrib><creatorcontrib>Hazama, Shoichi</creatorcontrib><creatorcontrib>Nagano, Hiroaki</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><jtitle>Annals of surgical oncology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kimura, Yuta</au><au>Tsunedomi, Ryouichi</au><au>Yoshimura, Kiyoshi</au><au>Matsukuma, Satoshi</au><au>Shindo, Yoshitaro</au><au>Matsui, Hiroto</au><au>Tokumitsu, Yukio</au><au>Yoshida, Shin</au><au>Iida, Michihisa</au><au>Suzuki, Nobuaki</au><au>Takeda, Shigeru</au><au>Ioka, Tatsuya</au><au>Hazama, Shoichi</au><au>Nagano, Hiroaki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Immune Evasion of Hepatoma Cancer Stem-Like Cells from Natural Killer Cells</atitle><jtitle>Annals of surgical oncology</jtitle><stitle>Ann Surg Oncol</stitle><date>2022-11-01</date><risdate>2022</risdate><volume>29</volume><issue>12</issue><spage>7423</spage><epage>7433</epage><pages>7423-7433</pages><issn>1068-9265</issn><eissn>1534-4681</eissn><abstract>Background
Poor prognosis in liver cancer is due to its high frequency of intrahepatic metastasis. Cancer stem-like cells (CSLCs), which possess the properties of stemness, tumor initiation capability, and resistance to therapy, also exhibit metastatic potential. Immune surveillance plays an important role in the accomplishment of metastasis. Herein, the property of immune evasion in CSLCs was investigated.
Methods
Sphere cells were induced as CSLCs using a sphere induction medium containing neural survival factor-1. The expression of genes involved in immune evasion was determined using RNA-sequencing for sphere and parental cells followed by validation using flow cytometric analysis and ELISA. Susceptibility to natural killer (NK) cell-mediated cytotoxicity was examined by a chromium release assay. A xenograft model using BALB/c
nu/nu
mice was used to assess tumor growth. Gene set enrichment analysis was performed for interpreting RNA sequencing.
Results
The cell surface expressions of PD-L1, PD-L2, and CEACAM1 were upregulated and those of ULBP1 and MICA/MICB were downregulated in SK-sphere, CSLCs derived from SK-HEP-1, compared with that in parental cells. Levels of soluble MICA were elevated in conditioned medium from SK-sphere. Expression of HLA class I was not downregulated in SK-sphere. The susceptibilities to NK cell-mediated killing and secreted perforin were significantly lower in both CSLCs derived from SK-HEP-1 and HLE than in parental cells. Tumors formed upon inoculation of SK-sphere in immunodeficient mice harboring NK cells were larger than those formed upon inoculation of parental cells.
Conclusion
Human hepatoma cell line-derived CSLCs may possess immune evasion properties, especially from NK cell-mediated immunity.</abstract><cop>Cham</cop><pub>Springer International Publishing</pub><doi>10.1245/s10434-022-12220-w</doi><tpages>11</tpages></addata></record> |
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| subjects | Cancer CD66 antigen CEACAM1 protein Cell surface Cell-mediated immunity Cytotoxicity Enzyme-linked immunosorbent assay Flow cytometry Gene set enrichment analysis Hepatoma Histocompatibility antigen HLA Immune evasion Immunodeficiency Immunosurveillance Inoculation Liver cancer Major histocompatibility complex Medical prognosis Medicine Medicine & Public Health Metastases Metastasis Natural killer cells Oncology PD-L1 protein Perforin Surgery Surgical Oncology Survival factor Translational Research Xenografts |
| title | Immune Evasion of Hepatoma Cancer Stem-Like Cells from Natural Killer Cells |
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