Lower expression level of IL-33 is associated with poor prognosis of pulmonary adenocarcinoma
Lung cancer is one of the deadliest malignancies. The immune checkpoint-blockade (ICB) tumor therapy has led to striking improvement of long-term survival for some lung cancer patients. However, the response rate of immunotherapy is still low for lung cancer. Studying the tumor microenvironment (TME...
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| Veröffentlicht in: | PloS one 2018-03, Vol.13 (3), p.e0193428-e0193428 |
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| creator | Yang, Min Feng, Yuehua Yue, Cuihua Xu, Bin Chen, Lujun Jiang, Jingting Lu, Binfeng Zhu, Yibei |
| description | Lung cancer is one of the deadliest malignancies. The immune checkpoint-blockade (ICB) tumor therapy has led to striking improvement of long-term survival for some lung cancer patients. However, the response rate of immunotherapy is still low for lung cancer. Studying the tumor microenvironment (TME) should shed light on improvement of immunotherapy of lung cancer. Interleukin-33 (IL-33), an "alarmin" cytokine, has been implicated in tumor associated immune responses and inflammatory diseases of the lung. The role of IL-33 in lung cancer progression, however, remains elusive. This study is designed to characterize IL-33 expression in lung tumor tissues and establish the clinical significance of IL-33 in non-small cell lung cancer lung cancer (NSCLC).
Tumor tissue specimens from patients suffering from NSCLC were analyzed for expression of IL-33 protein by immunohistochemistry and expression of IL-33 and ST2 mRNA by RT-quantitative PCR (RT-QPCR). The expression data were analyzed for their association with clinical and pathological parameters of NSCLC. In addition, the association between expression levels of IL-33 mRNA and patient survival was determined using 5 independent expression profiling datasets of human lung cancer.
The expression levels of IL-33 and ST2 were significantly down-regulated in both adenocarcinoma and squamous cell carcinoma of the lung when compared to adjacent normal lung tissues. In addition, the level of IL-33 protein was inversely correlated with tumor grade and size. Moreover, analysis of TCGA and GEO lung cancer expression datasets revealed that higher expression levels of IL-33 mRNA were correlated with longer overall survival of patients suffering from adenocarcinoma of the lung. These data indicate that the expression levels of IL-33 are inversely associated with lung cancer progression, consistent with the hypothesis that IL-33 is involved in immune surveillance of NSCLC. |
| doi_str_mv | 10.1371/journal.pone.0193428 |
| format | Article |
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Tumor tissue specimens from patients suffering from NSCLC were analyzed for expression of IL-33 protein by immunohistochemistry and expression of IL-33 and ST2 mRNA by RT-quantitative PCR (RT-QPCR). The expression data were analyzed for their association with clinical and pathological parameters of NSCLC. In addition, the association between expression levels of IL-33 mRNA and patient survival was determined using 5 independent expression profiling datasets of human lung cancer.
The expression levels of IL-33 and ST2 were significantly down-regulated in both adenocarcinoma and squamous cell carcinoma of the lung when compared to adjacent normal lung tissues. In addition, the level of IL-33 protein was inversely correlated with tumor grade and size. Moreover, analysis of TCGA and GEO lung cancer expression datasets revealed that higher expression levels of IL-33 mRNA were correlated with longer overall survival of patients suffering from adenocarcinoma of the lung. These data indicate that the expression levels of IL-33 are inversely associated with lung cancer progression, consistent with the hypothesis that IL-33 is involved in immune surveillance of NSCLC.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0193428</identifier><identifier>PMID: 29499051</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adenocarcinoma ; Aged ; Antigens ; Biology ; Biology and Life Sciences ; Cancer ; Carcinoma, Non-Small-Cell Lung - metabolism ; Carcinoma, Non-Small-Cell Lung - mortality ; Carcinoma, Non-Small-Cell Lung - pathology ; Carcinoma, Squamous Cell - metabolism ; Carcinoma, Squamous Cell - mortality ; Carcinoma, Squamous Cell - pathology ; Care and treatment ; Colorectal cancer ; Cytokines ; Data processing ; Datasets ; Development and progression ; Down-Regulation ; Female ; Gene expression ; Genetic aspects ; Health aspects ; Hospitals ; Humans ; Immune checkpoint ; Immune response ; Immunohistochemistry ; Immunology ; Immunosurveillance ; Immunotherapy ; Inflammatory diseases ; Interleukin-1 Receptor-Like 1 Protein - genetics ; Interleukin-1 Receptor-Like 1 Protein - metabolism ; Interleukin-33 - genetics ; Interleukin-33 - metabolism ; Interleukins ; Laboratories ; Lung - metabolism ; Lung - pathology ; Lung cancer ; Lung carcinoma ; Lung diseases ; Lung Neoplasms - metabolism ; Lung Neoplasms - mortality ; Lung Neoplasms - pathology ; Male ; Medical prognosis ; Medicine and Health Sciences ; Metastasis ; Middle Aged ; mRNA ; Neoplasm Staging ; Non-small cell lung carcinoma ; Patients ; Prognosis ; Real-Time Polymerase Chain Reaction ; Small cell lung carcinoma ; Squamous cell carcinoma ; Survival ; Survival Rate ; Tissues ; Tumorigenesis</subject><ispartof>PloS one, 2018-03, Vol.13 (3), p.e0193428-e0193428</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Yang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2018 Yang et al 2018 Yang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-885215c1d233e552cb0ee51d33d8edf0b6dcb8b88867cf8ad989b3a3558f66c3</citedby><cites>FETCH-LOGICAL-c692t-885215c1d233e552cb0ee51d33d8edf0b6dcb8b88867cf8ad989b3a3558f66c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834175/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834175/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29499051$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ahmad, Aamir</contributor><creatorcontrib>Yang, Min</creatorcontrib><creatorcontrib>Feng, Yuehua</creatorcontrib><creatorcontrib>Yue, Cuihua</creatorcontrib><creatorcontrib>Xu, Bin</creatorcontrib><creatorcontrib>Chen, Lujun</creatorcontrib><creatorcontrib>Jiang, Jingting</creatorcontrib><creatorcontrib>Lu, Binfeng</creatorcontrib><creatorcontrib>Zhu, Yibei</creatorcontrib><title>Lower expression level of IL-33 is associated with poor prognosis of pulmonary adenocarcinoma</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Lung cancer is one of the deadliest malignancies. The immune checkpoint-blockade (ICB) tumor therapy has led to striking improvement of long-term survival for some lung cancer patients. However, the response rate of immunotherapy is still low for lung cancer. Studying the tumor microenvironment (TME) should shed light on improvement of immunotherapy of lung cancer. Interleukin-33 (IL-33), an "alarmin" cytokine, has been implicated in tumor associated immune responses and inflammatory diseases of the lung. The role of IL-33 in lung cancer progression, however, remains elusive. This study is designed to characterize IL-33 expression in lung tumor tissues and establish the clinical significance of IL-33 in non-small cell lung cancer lung cancer (NSCLC).
Tumor tissue specimens from patients suffering from NSCLC were analyzed for expression of IL-33 protein by immunohistochemistry and expression of IL-33 and ST2 mRNA by RT-quantitative PCR (RT-QPCR). The expression data were analyzed for their association with clinical and pathological parameters of NSCLC. In addition, the association between expression levels of IL-33 mRNA and patient survival was determined using 5 independent expression profiling datasets of human lung cancer.
The expression levels of IL-33 and ST2 were significantly down-regulated in both adenocarcinoma and squamous cell carcinoma of the lung when compared to adjacent normal lung tissues. In addition, the level of IL-33 protein was inversely correlated with tumor grade and size. Moreover, analysis of TCGA and GEO lung cancer expression datasets revealed that higher expression levels of IL-33 mRNA were correlated with longer overall survival of patients suffering from adenocarcinoma of the lung. These data indicate that the expression levels of IL-33 are inversely associated with lung cancer progression, consistent with the hypothesis that IL-33 is involved in immune surveillance of NSCLC.</description><subject>Adenocarcinoma</subject><subject>Aged</subject><subject>Antigens</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cancer</subject><subject>Carcinoma, Non-Small-Cell Lung - metabolism</subject><subject>Carcinoma, Non-Small-Cell Lung - mortality</subject><subject>Carcinoma, Non-Small-Cell Lung - pathology</subject><subject>Carcinoma, Squamous Cell - metabolism</subject><subject>Carcinoma, Squamous Cell - mortality</subject><subject>Carcinoma, Squamous Cell - pathology</subject><subject>Care and treatment</subject><subject>Colorectal cancer</subject><subject>Cytokines</subject><subject>Data processing</subject><subject>Datasets</subject><subject>Development and progression</subject><subject>Down-Regulation</subject><subject>Female</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Immune checkpoint</subject><subject>Immune response</subject><subject>Immunohistochemistry</subject><subject>Immunology</subject><subject>Immunosurveillance</subject><subject>Immunotherapy</subject><subject>Inflammatory diseases</subject><subject>Interleukin-1 Receptor-Like 1 Protein - genetics</subject><subject>Interleukin-1 Receptor-Like 1 Protein - metabolism</subject><subject>Interleukin-33 - genetics</subject><subject>Interleukin-33 - metabolism</subject><subject>Interleukins</subject><subject>Laboratories</subject><subject>Lung - metabolism</subject><subject>Lung - pathology</subject><subject>Lung cancer</subject><subject>Lung carcinoma</subject><subject>Lung diseases</subject><subject>Lung Neoplasms - metabolism</subject><subject>Lung Neoplasms - mortality</subject><subject>Lung Neoplasms - pathology</subject><subject>Male</subject><subject>Medical prognosis</subject><subject>Medicine and Health Sciences</subject><subject>Metastasis</subject><subject>Middle Aged</subject><subject>mRNA</subject><subject>Neoplasm Staging</subject><subject>Non-small cell lung carcinoma</subject><subject>Patients</subject><subject>Prognosis</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Small cell lung carcinoma</subject><subject>Squamous cell carcinoma</subject><subject>Survival</subject><subject>Survival Rate</subject><subject>Tissues</subject><subject>Tumorigenesis</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1uL1DAUgIso7jr6D0QLgujDjLk0afIiLIuXgYEFXXyTkKanM1nSpibt7vrvzTjdZSr7IHnI4eQ715yTZS8xWmFa4g9Xfgyddqved7BCWNKCiEfZaRLIkhNEHx_JJ9mzGK8QYlRw_jQ7IbKQEjF8mv3c-BsIOdz2AWK0vssdXIPLfZOvN0tKcxtzHaM3Vg9Q5zd22OW99yHvg992PqbnhPaja32nw-9c19B5o4OxnW_18-xJo12EF9O9yC4_f7o8_7rcXHxZn59tloZLMiyFYAQzg2tCKTBGTIUAGK4prQXUDap4bSpRCSF4aRqhaylkRTVlTDScG7rIXh_c9s5HNTUmKoKQFGVZcJaI9YGovb5SfbBtSlZ5bdVfhQ9bpcNgjQOlJWkY0KKQvCnKSkoihUgCxQ2nJMVdZB-naGPVQm2gG4J2M6fzl87u1NZfKyZogct9Mu8mB8H_GiEOqrXRgHO6Az_u88aIlowVOKFv_kEfrm6itjoVYLvGp7hm71SdMSJZWRBOErV6gEqnhtaaNEWNTfqZwfuZQWIGuB22eoxRrb9_-3_24secfXvE7kC7YRe9G4c0fnEOFgfQBB9jgOa-yRip_RLcdUPtl0BNS5DMXh1_0L3R3dTTPw1fAVc</recordid><startdate>20180302</startdate><enddate>20180302</enddate><creator>Yang, Min</creator><creator>Feng, Yuehua</creator><creator>Yue, Cuihua</creator><creator>Xu, Bin</creator><creator>Chen, Lujun</creator><creator>Jiang, Jingting</creator><creator>Lu, Binfeng</creator><creator>Zhu, Yibei</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20180302</creationdate><title>Lower expression level of IL-33 is associated with poor prognosis of pulmonary adenocarcinoma</title><author>Yang, Min ; Feng, Yuehua ; Yue, Cuihua ; Xu, Bin ; Chen, Lujun ; Jiang, Jingting ; Lu, Binfeng ; Zhu, Yibei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-885215c1d233e552cb0ee51d33d8edf0b6dcb8b88867cf8ad989b3a3558f66c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adenocarcinoma</topic><topic>Aged</topic><topic>Antigens</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Cancer</topic><topic>Carcinoma, Non-Small-Cell Lung - metabolism</topic><topic>Carcinoma, Non-Small-Cell Lung - mortality</topic><topic>Carcinoma, Non-Small-Cell Lung - pathology</topic><topic>Carcinoma, Squamous Cell - metabolism</topic><topic>Carcinoma, Squamous Cell - mortality</topic><topic>Carcinoma, Squamous Cell - pathology</topic><topic>Care and treatment</topic><topic>Colorectal cancer</topic><topic>Cytokines</topic><topic>Data processing</topic><topic>Datasets</topic><topic>Development and progression</topic><topic>Down-Regulation</topic><topic>Female</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Hospitals</topic><topic>Humans</topic><topic>Immune checkpoint</topic><topic>Immune response</topic><topic>Immunohistochemistry</topic><topic>Immunology</topic><topic>Immunosurveillance</topic><topic>Immunotherapy</topic><topic>Inflammatory diseases</topic><topic>Interleukin-1 Receptor-Like 1 Protein - genetics</topic><topic>Interleukin-1 Receptor-Like 1 Protein - metabolism</topic><topic>Interleukin-33 - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Min</au><au>Feng, Yuehua</au><au>Yue, Cuihua</au><au>Xu, Bin</au><au>Chen, Lujun</au><au>Jiang, Jingting</au><au>Lu, Binfeng</au><au>Zhu, Yibei</au><au>Ahmad, Aamir</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lower expression level of IL-33 is associated with poor prognosis of pulmonary adenocarcinoma</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2018-03-02</date><risdate>2018</risdate><volume>13</volume><issue>3</issue><spage>e0193428</spage><epage>e0193428</epage><pages>e0193428-e0193428</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Lung cancer is one of the deadliest malignancies. The immune checkpoint-blockade (ICB) tumor therapy has led to striking improvement of long-term survival for some lung cancer patients. However, the response rate of immunotherapy is still low for lung cancer. Studying the tumor microenvironment (TME) should shed light on improvement of immunotherapy of lung cancer. Interleukin-33 (IL-33), an "alarmin" cytokine, has been implicated in tumor associated immune responses and inflammatory diseases of the lung. The role of IL-33 in lung cancer progression, however, remains elusive. This study is designed to characterize IL-33 expression in lung tumor tissues and establish the clinical significance of IL-33 in non-small cell lung cancer lung cancer (NSCLC).
Tumor tissue specimens from patients suffering from NSCLC were analyzed for expression of IL-33 protein by immunohistochemistry and expression of IL-33 and ST2 mRNA by RT-quantitative PCR (RT-QPCR). The expression data were analyzed for their association with clinical and pathological parameters of NSCLC. In addition, the association between expression levels of IL-33 mRNA and patient survival was determined using 5 independent expression profiling datasets of human lung cancer.
The expression levels of IL-33 and ST2 were significantly down-regulated in both adenocarcinoma and squamous cell carcinoma of the lung when compared to adjacent normal lung tissues. In addition, the level of IL-33 protein was inversely correlated with tumor grade and size. Moreover, analysis of TCGA and GEO lung cancer expression datasets revealed that higher expression levels of IL-33 mRNA were correlated with longer overall survival of patients suffering from adenocarcinoma of the lung. These data indicate that the expression levels of IL-33 are inversely associated with lung cancer progression, consistent with the hypothesis that IL-33 is involved in immune surveillance of NSCLC.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29499051</pmid><doi>10.1371/journal.pone.0193428</doi><tpages>e0193428</tpages><oa>free_for_read</oa></addata></record> |
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| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2009877465 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adenocarcinoma Aged Antigens Biology Biology and Life Sciences Cancer Carcinoma, Non-Small-Cell Lung - metabolism Carcinoma, Non-Small-Cell Lung - mortality Carcinoma, Non-Small-Cell Lung - pathology Carcinoma, Squamous Cell - metabolism Carcinoma, Squamous Cell - mortality Carcinoma, Squamous Cell - pathology Care and treatment Colorectal cancer Cytokines Data processing Datasets Development and progression Down-Regulation Female Gene expression Genetic aspects Health aspects Hospitals Humans Immune checkpoint Immune response Immunohistochemistry Immunology Immunosurveillance Immunotherapy Inflammatory diseases Interleukin-1 Receptor-Like 1 Protein - genetics Interleukin-1 Receptor-Like 1 Protein - metabolism Interleukin-33 - genetics Interleukin-33 - metabolism Interleukins Laboratories Lung - metabolism Lung - pathology Lung cancer Lung carcinoma Lung diseases Lung Neoplasms - metabolism Lung Neoplasms - mortality Lung Neoplasms - pathology Male Medical prognosis Medicine and Health Sciences Metastasis Middle Aged mRNA Neoplasm Staging Non-small cell lung carcinoma Patients Prognosis Real-Time Polymerase Chain Reaction Small cell lung carcinoma Squamous cell carcinoma Survival Survival Rate Tissues Tumorigenesis |
| title | Lower expression level of IL-33 is associated with poor prognosis of pulmonary adenocarcinoma |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-07T08%3A08%3A13IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Lower%20expression%20level%20of%20IL-33%20is%20associated%20with%20poor%20prognosis%20of%20pulmonary%20adenocarcinoma&rft.jtitle=PloS%20one&rft.au=Yang,%20Min&rft.date=2018-03-02&rft.volume=13&rft.issue=3&rft.spage=e0193428&rft.epage=e0193428&rft.pages=e0193428-e0193428&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0193428&rft_dat=%3Cgale_plos_%3EA529574262%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2009877465&rft_id=info:pmid/29499051&rft_galeid=A529574262&rft_doaj_id=oai_doaj_org_article_a92f5e34496f47b99298847b31f6329b&rfr_iscdi=true |