Immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer: a systematic review and meta-analysis
Purpose This systematic review and meta-analysis aimed to evaluate the immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer. Methods We performed a systematic literature search using PubMed, Embase, and Cochrane Library until 28/09/2021, and conference proceedings from ASCO a...
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Veröffentlicht in: | Journal of cancer research and clinical oncology 2023-07, Vol.149 (7), p.3075-3080 |
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creator | Martins-Branco, Diogo Nader-Marta, Guilherme Tecic Vuger, Ana Debien, Veronique Ameye, Lieveke Brandão, Mariana Punie, Kevin Loizidou, Angela Willard-Gallo, Karen Spilleboudt, Chloe Awada, Ahmad Piccart, Martine de Azambuja, Evandro |
description | Purpose
This systematic review and meta-analysis aimed to evaluate the immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer.
Methods
We performed a systematic literature search using PubMed, Embase, and Cochrane Library until 28/09/2021, and conference proceedings from ASCO and ESMO 2021 annual meetings. We screened for observational or interventional studies including subjects ≥ 16 years old with cancer diagnosis who were vaccinated against SARS-CoV-2. Prime-vaccination was defined as one dose of Ad26.COV2-S vaccine or two doses of BNT162b2, mRNA-1273, ChAdOx1-S or inactivated SARS-CoV-2 vaccine. The outcomes were humoral and adaptive immune responses (proportion of subjects with positive titers of antibody anti-SARS-CoV-2 spike protein and anti-SARS-CoV-2 cellular responses, respectively).
Results
We included 89 records reporting data from 30,183 subjects. The overall seropositive rate within the first month after complete anti-SARS-CoV-2 prime-vaccination was 80% [95% confidence interval (CI), 72–86%], 60% (95%CI, 53–67%) in patients with hematological malignancies (HM) versus 94% (95%CI, 88–97%) in patients with solid malignancies (SM). The diagnosis of HM was significantly associated with a lower seropositive rate on multivariate meta-regression (odds ratio 0.35, 95% CI 0.18–0.69, HM versus both,
p
= 0.002). The overall humoral response was 49% (95% CI, 42–56%) after incomplete prime-vaccination and 79% (95% CI, 70–86%) at 2 months after complete prime-vaccination. These responses were also lower in patients with HM at these time points. The overall cellular response rate at any time after vaccination was 61% (95% CI, 44–76%).
Conclusion
This meta-analysis provides compelling evidence of humoral and adaptive immune responses against SARS-CoV-2 in patients with cancer, which last for at least 2 months following complete prime-vaccination. |
doi_str_mv | 10.1007/s00432-022-04185-w |
format | Article |
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This systematic review and meta-analysis aimed to evaluate the immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer.
Methods
We performed a systematic literature search using PubMed, Embase, and Cochrane Library until 28/09/2021, and conference proceedings from ASCO and ESMO 2021 annual meetings. We screened for observational or interventional studies including subjects ≥ 16 years old with cancer diagnosis who were vaccinated against SARS-CoV-2. Prime-vaccination was defined as one dose of Ad26.COV2-S vaccine or two doses of BNT162b2, mRNA-1273, ChAdOx1-S or inactivated SARS-CoV-2 vaccine. The outcomes were humoral and adaptive immune responses (proportion of subjects with positive titers of antibody anti-SARS-CoV-2 spike protein and anti-SARS-CoV-2 cellular responses, respectively).
Results
We included 89 records reporting data from 30,183 subjects. The overall seropositive rate within the first month after complete anti-SARS-CoV-2 prime-vaccination was 80% [95% confidence interval (CI), 72–86%], 60% (95%CI, 53–67%) in patients with hematological malignancies (HM) versus 94% (95%CI, 88–97%) in patients with solid malignancies (SM). The diagnosis of HM was significantly associated with a lower seropositive rate on multivariate meta-regression (odds ratio 0.35, 95% CI 0.18–0.69, HM versus both,
p
= 0.002). The overall humoral response was 49% (95% CI, 42–56%) after incomplete prime-vaccination and 79% (95% CI, 70–86%) at 2 months after complete prime-vaccination. These responses were also lower in patients with HM at these time points. The overall cellular response rate at any time after vaccination was 61% (95% CI, 44–76%).
Conclusion
This meta-analysis provides compelling evidence of humoral and adaptive immune responses against SARS-CoV-2 in patients with cancer, which last for at least 2 months following complete prime-vaccination.</description><identifier>ISSN: 0171-5216</identifier><identifier>EISSN: 1432-1335</identifier><identifier>DOI: 10.1007/s00432-022-04185-w</identifier><identifier>PMID: 35867203</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>antibodies ; Cancer ; Cancer Research ; confidence interval ; Diagnosis ; Hematology ; humoral immunity ; immune response ; Immune response (humoral) ; Internal Medicine ; Malignancy ; Medicine ; Medicine & Public Health ; Meta-analysis ; mRNA ; odds ratio ; Oncology ; seroprevalence ; Severe acute respiratory syndrome coronavirus 2 ; Spike protein ; Systematic review ; vaccination ; Vaccines</subject><ispartof>Journal of cancer research and clinical oncology, 2023-07, Vol.149 (7), p.3075-3080</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022</rights><rights>2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.</rights><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c507t-a83a1683b88543d6b060452ed133559d1a12eb9845fee41ce72108a3f2b643a53</citedby><cites>FETCH-LOGICAL-c507t-a83a1683b88543d6b060452ed133559d1a12eb9845fee41ce72108a3f2b643a53</cites><orcidid>0000-0001-9068-8504 ; 0000-0001-9501-4509 ; 0000-0002-1162-7963 ; 0000-0002-1150-1295 ; 0000-0002-1653-3544 ; 0000-0002-7214-4818 ; 0000-0001-5153-1766 ; 0000-0001-7412-9163 ; 0000-0003-2203-161X ; 0000-0002-8009-403X ; 0000-0001-7864-3637 ; 0000-0003-1165-925X ; 0000-0002-2296-9264</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00432-022-04185-w$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00432-022-04185-w$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35867203$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Martins-Branco, Diogo</creatorcontrib><creatorcontrib>Nader-Marta, Guilherme</creatorcontrib><creatorcontrib>Tecic Vuger, Ana</creatorcontrib><creatorcontrib>Debien, Veronique</creatorcontrib><creatorcontrib>Ameye, Lieveke</creatorcontrib><creatorcontrib>Brandão, Mariana</creatorcontrib><creatorcontrib>Punie, Kevin</creatorcontrib><creatorcontrib>Loizidou, Angela</creatorcontrib><creatorcontrib>Willard-Gallo, Karen</creatorcontrib><creatorcontrib>Spilleboudt, Chloe</creatorcontrib><creatorcontrib>Awada, Ahmad</creatorcontrib><creatorcontrib>Piccart, Martine</creatorcontrib><creatorcontrib>de Azambuja, Evandro</creatorcontrib><title>Immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer: a systematic review and meta-analysis</title><title>Journal of cancer research and clinical oncology</title><addtitle>J Cancer Res Clin Oncol</addtitle><addtitle>J Cancer Res Clin Oncol</addtitle><description>Purpose
This systematic review and meta-analysis aimed to evaluate the immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer.
Methods
We performed a systematic literature search using PubMed, Embase, and Cochrane Library until 28/09/2021, and conference proceedings from ASCO and ESMO 2021 annual meetings. We screened for observational or interventional studies including subjects ≥ 16 years old with cancer diagnosis who were vaccinated against SARS-CoV-2. Prime-vaccination was defined as one dose of Ad26.COV2-S vaccine or two doses of BNT162b2, mRNA-1273, ChAdOx1-S or inactivated SARS-CoV-2 vaccine. The outcomes were humoral and adaptive immune responses (proportion of subjects with positive titers of antibody anti-SARS-CoV-2 spike protein and anti-SARS-CoV-2 cellular responses, respectively).
Results
We included 89 records reporting data from 30,183 subjects. The overall seropositive rate within the first month after complete anti-SARS-CoV-2 prime-vaccination was 80% [95% confidence interval (CI), 72–86%], 60% (95%CI, 53–67%) in patients with hematological malignancies (HM) versus 94% (95%CI, 88–97%) in patients with solid malignancies (SM). The diagnosis of HM was significantly associated with a lower seropositive rate on multivariate meta-regression (odds ratio 0.35, 95% CI 0.18–0.69, HM versus both,
p
= 0.002). The overall humoral response was 49% (95% CI, 42–56%) after incomplete prime-vaccination and 79% (95% CI, 70–86%) at 2 months after complete prime-vaccination. These responses were also lower in patients with HM at these time points. The overall cellular response rate at any time after vaccination was 61% (95% CI, 44–76%).
Conclusion
This meta-analysis provides compelling evidence of humoral and adaptive immune responses against SARS-CoV-2 in patients with cancer, which last for at least 2 months following complete prime-vaccination.</description><subject>antibodies</subject><subject>Cancer</subject><subject>Cancer Research</subject><subject>confidence interval</subject><subject>Diagnosis</subject><subject>Hematology</subject><subject>humoral immunity</subject><subject>immune response</subject><subject>Immune response (humoral)</subject><subject>Internal Medicine</subject><subject>Malignancy</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Meta-analysis</subject><subject>mRNA</subject><subject>odds ratio</subject><subject>Oncology</subject><subject>seroprevalence</subject><subject>Severe acute respiratory syndrome coronavirus 2</subject><subject>Spike protein</subject><subject>Systematic review</subject><subject>vaccination</subject><subject>Vaccines</subject><issn>0171-5216</issn><issn>1432-1335</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqFkU1v1DAQhi1ERbcLf4ADssSFi8EfceJwQKpWUCpVQqLA1XKc2dZVYi-2s6v99zjdfgAHOFj-mGfemfGL0EtG3zJKm3eJ0kpwQnlZFVOS7J6gBZufmBDyKVpQ1jAiOauP0UlKN7TcZcOfoWMhVd1wKhYonY_j5AFHSJvgE-AcsPHZkcvTr5dkFX4QjjfRjUC2xlrnTXbBY-fxppzA54R3Ll9ja7yF-B4bnPYpw1iCtmhuHeyKXI9HyIYYb4Z9cuk5OlqbIcGLu32Jvn_6-G31mVx8OTtfnV4QK2mTiVHCsFqJTilZib7uaE0ryaGfp5Ntzwzj0LWqkmuAilloOKPKiDXv6koYKZbow0F3M3Uj9La0G82g53FM3OtgnP4z4t21vgpb3YpSqKJF4M2dQAw_J0hZjy5ZGAbjIUxJF6w4UDeK_RfldSuaRtF2buv1X-hNmGL5m0IpwZRqWdmXiB8oG0NKEdYPfTOqZ_v1wX5d7Ne39utdSXr1-8QPKfd-F0AcgFRC_griY-1_yP4CBwi7Vw</recordid><startdate>20230701</startdate><enddate>20230701</enddate><creator>Martins-Branco, Diogo</creator><creator>Nader-Marta, Guilherme</creator><creator>Tecic Vuger, Ana</creator><creator>Debien, Veronique</creator><creator>Ameye, Lieveke</creator><creator>Brandão, Mariana</creator><creator>Punie, Kevin</creator><creator>Loizidou, Angela</creator><creator>Willard-Gallo, Karen</creator><creator>Spilleboudt, Chloe</creator><creator>Awada, Ahmad</creator><creator>Piccart, Martine</creator><creator>de Azambuja, Evandro</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>NPM</scope><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>8C1</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9068-8504</orcidid><orcidid>https://orcid.org/0000-0001-9501-4509</orcidid><orcidid>https://orcid.org/0000-0002-1162-7963</orcidid><orcidid>https://orcid.org/0000-0002-1150-1295</orcidid><orcidid>https://orcid.org/0000-0002-1653-3544</orcidid><orcidid>https://orcid.org/0000-0002-7214-4818</orcidid><orcidid>https://orcid.org/0000-0001-5153-1766</orcidid><orcidid>https://orcid.org/0000-0001-7412-9163</orcidid><orcidid>https://orcid.org/0000-0003-2203-161X</orcidid><orcidid>https://orcid.org/0000-0002-8009-403X</orcidid><orcidid>https://orcid.org/0000-0001-7864-3637</orcidid><orcidid>https://orcid.org/0000-0003-1165-925X</orcidid><orcidid>https://orcid.org/0000-0002-2296-9264</orcidid></search><sort><creationdate>20230701</creationdate><title>Immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer: a systematic review and meta-analysis</title><author>Martins-Branco, Diogo ; Nader-Marta, Guilherme ; Tecic Vuger, Ana ; Debien, Veronique ; Ameye, Lieveke ; Brandão, Mariana ; Punie, Kevin ; Loizidou, Angela ; Willard-Gallo, Karen ; Spilleboudt, Chloe ; Awada, Ahmad ; Piccart, Martine ; de Azambuja, Evandro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c507t-a83a1683b88543d6b060452ed133559d1a12eb9845fee41ce72108a3f2b643a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>antibodies</topic><topic>Cancer</topic><topic>Cancer Research</topic><topic>confidence interval</topic><topic>Diagnosis</topic><topic>Hematology</topic><topic>humoral immunity</topic><topic>immune response</topic><topic>Immune response (humoral)</topic><topic>Internal Medicine</topic><topic>Malignancy</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Meta-analysis</topic><topic>mRNA</topic><topic>odds ratio</topic><topic>Oncology</topic><topic>seroprevalence</topic><topic>Severe acute respiratory syndrome coronavirus 2</topic><topic>Spike protein</topic><topic>Systematic review</topic><topic>vaccination</topic><topic>Vaccines</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martins-Branco, Diogo</creatorcontrib><creatorcontrib>Nader-Marta, Guilherme</creatorcontrib><creatorcontrib>Tecic Vuger, Ana</creatorcontrib><creatorcontrib>Debien, Veronique</creatorcontrib><creatorcontrib>Ameye, Lieveke</creatorcontrib><creatorcontrib>Brandão, Mariana</creatorcontrib><creatorcontrib>Punie, Kevin</creatorcontrib><creatorcontrib>Loizidou, Angela</creatorcontrib><creatorcontrib>Willard-Gallo, Karen</creatorcontrib><creatorcontrib>Spilleboudt, Chloe</creatorcontrib><creatorcontrib>Awada, Ahmad</creatorcontrib><creatorcontrib>Piccart, Martine</creatorcontrib><creatorcontrib>de Azambuja, Evandro</creatorcontrib><collection>PubMed</collection><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>Public Health Database</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</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>Research Library</collection><collection>Research Library (Corporate)</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 Basic</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cancer research and clinical oncology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Martins-Branco, Diogo</au><au>Nader-Marta, Guilherme</au><au>Tecic Vuger, Ana</au><au>Debien, Veronique</au><au>Ameye, Lieveke</au><au>Brandão, Mariana</au><au>Punie, Kevin</au><au>Loizidou, Angela</au><au>Willard-Gallo, Karen</au><au>Spilleboudt, Chloe</au><au>Awada, Ahmad</au><au>Piccart, Martine</au><au>de Azambuja, Evandro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer: a systematic review and meta-analysis</atitle><jtitle>Journal of cancer research and clinical oncology</jtitle><stitle>J Cancer Res Clin Oncol</stitle><addtitle>J Cancer Res Clin Oncol</addtitle><date>2023-07-01</date><risdate>2023</risdate><volume>149</volume><issue>7</issue><spage>3075</spage><epage>3080</epage><pages>3075-3080</pages><issn>0171-5216</issn><eissn>1432-1335</eissn><abstract>Purpose
This systematic review and meta-analysis aimed to evaluate the immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer.
Methods
We performed a systematic literature search using PubMed, Embase, and Cochrane Library until 28/09/2021, and conference proceedings from ASCO and ESMO 2021 annual meetings. We screened for observational or interventional studies including subjects ≥ 16 years old with cancer diagnosis who were vaccinated against SARS-CoV-2. Prime-vaccination was defined as one dose of Ad26.COV2-S vaccine or two doses of BNT162b2, mRNA-1273, ChAdOx1-S or inactivated SARS-CoV-2 vaccine. The outcomes were humoral and adaptive immune responses (proportion of subjects with positive titers of antibody anti-SARS-CoV-2 spike protein and anti-SARS-CoV-2 cellular responses, respectively).
Results
We included 89 records reporting data from 30,183 subjects. The overall seropositive rate within the first month after complete anti-SARS-CoV-2 prime-vaccination was 80% [95% confidence interval (CI), 72–86%], 60% (95%CI, 53–67%) in patients with hematological malignancies (HM) versus 94% (95%CI, 88–97%) in patients with solid malignancies (SM). The diagnosis of HM was significantly associated with a lower seropositive rate on multivariate meta-regression (odds ratio 0.35, 95% CI 0.18–0.69, HM versus both,
p
= 0.002). The overall humoral response was 49% (95% CI, 42–56%) after incomplete prime-vaccination and 79% (95% CI, 70–86%) at 2 months after complete prime-vaccination. These responses were also lower in patients with HM at these time points. The overall cellular response rate at any time after vaccination was 61% (95% CI, 44–76%).
Conclusion
This meta-analysis provides compelling evidence of humoral and adaptive immune responses against SARS-CoV-2 in patients with cancer, which last for at least 2 months following complete prime-vaccination.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>35867203</pmid><doi>10.1007/s00432-022-04185-w</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0001-9068-8504</orcidid><orcidid>https://orcid.org/0000-0001-9501-4509</orcidid><orcidid>https://orcid.org/0000-0002-1162-7963</orcidid><orcidid>https://orcid.org/0000-0002-1150-1295</orcidid><orcidid>https://orcid.org/0000-0002-1653-3544</orcidid><orcidid>https://orcid.org/0000-0002-7214-4818</orcidid><orcidid>https://orcid.org/0000-0001-5153-1766</orcidid><orcidid>https://orcid.org/0000-0001-7412-9163</orcidid><orcidid>https://orcid.org/0000-0003-2203-161X</orcidid><orcidid>https://orcid.org/0000-0002-8009-403X</orcidid><orcidid>https://orcid.org/0000-0001-7864-3637</orcidid><orcidid>https://orcid.org/0000-0003-1165-925X</orcidid><orcidid>https://orcid.org/0000-0002-2296-9264</orcidid><oa>free_for_read</oa></addata></record> |
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source | SpringerLink Journals - AutoHoldings |
subjects | antibodies Cancer Cancer Research confidence interval Diagnosis Hematology humoral immunity immune response Immune response (humoral) Internal Medicine Malignancy Medicine Medicine & Public Health Meta-analysis mRNA odds ratio Oncology seroprevalence Severe acute respiratory syndrome coronavirus 2 Spike protein Systematic review vaccination Vaccines |
title | Immune response to anti-SARS-CoV-2 prime-vaccination in patients with cancer: a systematic review and meta-analysis |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T03%3A59%3A06IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Immune%20response%20to%20anti-SARS-CoV-2%20prime-vaccination%20in%20patients%20with%20cancer:%20a%20systematic%20review%20and%20meta-analysis&rft.jtitle=Journal%20of%20cancer%20research%20and%20clinical%20oncology&rft.au=Martins-Branco,%20Diogo&rft.date=2023-07-01&rft.volume=149&rft.issue=7&rft.spage=3075&rft.epage=3080&rft.pages=3075-3080&rft.issn=0171-5216&rft.eissn=1432-1335&rft_id=info:doi/10.1007/s00432-022-04185-w&rft_dat=%3Cproquest_pubme%3E2693778095%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2831889128&rft_id=info:pmid/35867203&rfr_iscdi=true |