Pre-transplant donor-specific T-cell alloreactivity is strongly associated with early acute cellular rejection in kidney transplant recipients not receiving T-cell depleting induction therapy
Preformed T-cell immune-sensitization should most likely impact allograft outcome during the initial period after kidney transplantation, since donor-specific memory T-cells may rapidly recognize alloantigens and activate the effector immune response, which leads to allograft rejection. However, the...
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| Veröffentlicht in: | PloS one 2015-02, Vol.10 (2), p.e0117618-e0117618 |
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| creator | Crespo, Elena Lucia, Marc Cruzado, Josep M Luque, Sergio Melilli, Edoardo Manonelles, Anna Lloberas, Nuria Torras, Joan Grinyó, Josep M Bestard, Oriol |
| description | Preformed T-cell immune-sensitization should most likely impact allograft outcome during the initial period after kidney transplantation, since donor-specific memory T-cells may rapidly recognize alloantigens and activate the effector immune response, which leads to allograft rejection. However, the precise time-frame in which acute rejection is fundamentally triggered by preformed donor-specific memory T cells rather than by de novo activated naïve T cells is still to be established. Here, preformed donor-specific alloreactive T-cell responses were evaluated using the IFN-γ ELISPOT assay in a large consecutive cohort of kidney transplant patients (n = 90), to assess the main clinical variables associated with cellular sensitization and its predominant time-frame impact on allograft outcome, and was further validated in an independent new set of kidney transplant recipients (n = 67). We found that most highly T-cell sensitized patients were elderly patients with particularly poor HLA class-I matching, without any clinically recognizable sensitizing events. While one-year incidence of all types of biopsy-proven acute rejection did not differ between T-cell alloreactive and non-alloreactive patients, Receiver Operating Characteristic curve analysis indicated the first two months after transplantation as the highest risk time period for acute cellular rejection associated with baseline T-cell sensitization. This effect was particularly evident in young and highly alloreactive individuals that did not receive T-cell depletion immunosuppression. Multivariate analysis confirmed preformed T-cell sensitization as an independent predictor of early acute cellular rejection. In summary, monitoring anti-donor T-cell sensitization before transplantation may help to identify patients at increased risk of acute cellular rejection, particularly in the early phases after kidney transplantation, and thus guide decision-making regarding the use of induction therapy. |
| doi_str_mv | 10.1371/journal.pone.0117618 |
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However, the precise time-frame in which acute rejection is fundamentally triggered by preformed donor-specific memory T cells rather than by de novo activated naïve T cells is still to be established. Here, preformed donor-specific alloreactive T-cell responses were evaluated using the IFN-γ ELISPOT assay in a large consecutive cohort of kidney transplant patients (n = 90), to assess the main clinical variables associated with cellular sensitization and its predominant time-frame impact on allograft outcome, and was further validated in an independent new set of kidney transplant recipients (n = 67). We found that most highly T-cell sensitized patients were elderly patients with particularly poor HLA class-I matching, without any clinically recognizable sensitizing events. While one-year incidence of all types of biopsy-proven acute rejection did not differ between T-cell alloreactive and non-alloreactive patients, Receiver Operating Characteristic curve analysis indicated the first two months after transplantation as the highest risk time period for acute cellular rejection associated with baseline T-cell sensitization. This effect was particularly evident in young and highly alloreactive individuals that did not receive T-cell depletion immunosuppression. Multivariate analysis confirmed preformed T-cell sensitization as an independent predictor of early acute cellular rejection. In summary, monitoring anti-donor T-cell sensitization before transplantation may help to identify patients at increased risk of acute cellular rejection, particularly in the early phases after kidney transplantation, and thus guide decision-making regarding the use of induction therapy.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0117618</identifier><identifier>PMID: 25689405</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Aged ; Alloantigens ; Analysis ; Antigens ; Biomedical research ; Biopsy ; Clinical decision making ; Cèl·lules T ; Decision making ; Enzyme-linked immunosorbent assay ; Ethnicity ; Female ; Geriatrics ; Graft rejection ; Graft Rejection - immunology ; Health risk assessment ; Hemodialysis ; Histocompatibility antigen HLA ; Humans ; Immune response ; Immune system ; Immunological memory ; Immunosuppression ; Immunosuppression - methods ; Immunosuppressive Agents - therapeutic use ; Immunotherapy ; Induction therapy ; Interferon ; Kidney diseases ; Kidney Transplantation ; Kidney transplants ; Kidneys ; Laboratories ; Lymphocyte Depletion ; Lymphocytes ; Lymphocytes T ; Male ; Memory cells ; Middle Aged ; Multivariate analysis ; Nephrology ; Older people ; Organ transplant recipients ; Patients ; Rebuig (Biologia) ; Rejection ; Retrospective Studies ; Sensitizing ; T cells ; T-Lymphocytes - immunology ; Therapy ; Transplantation ; Transplantation of organs ; Transplants & implants ; Trasplantament d'òrgans ; Trasplantament renal ; γ-Interferon</subject><ispartof>PloS one, 2015-02, Vol.10 (2), p.e0117618-e0117618</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Crespo 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>cc-by (c) Crespo, Elena et al., 2015 info:eu-repo/semantics/openAccess <a href="http://creativecommons.org/licenses/by/3.0/es">http://creativecommons.org/licenses/by/3.0/es</a></rights><rights>2015 Crespo et al 2015 Crespo et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c734t-af86bdcc24a06db620676df5757b66a3cdc20c45f75f929fe2d42f00f40212c23</citedby><cites>FETCH-LOGICAL-c734t-af86bdcc24a06db620676df5757b66a3cdc20c45f75f929fe2d42f00f40212c23</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/PMC4331510/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4331510/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,26951,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25689405$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Crespo, Elena</creatorcontrib><creatorcontrib>Lucia, Marc</creatorcontrib><creatorcontrib>Cruzado, Josep M</creatorcontrib><creatorcontrib>Luque, Sergio</creatorcontrib><creatorcontrib>Melilli, Edoardo</creatorcontrib><creatorcontrib>Manonelles, Anna</creatorcontrib><creatorcontrib>Lloberas, Nuria</creatorcontrib><creatorcontrib>Torras, Joan</creatorcontrib><creatorcontrib>Grinyó, Josep M</creatorcontrib><creatorcontrib>Bestard, Oriol</creatorcontrib><title>Pre-transplant donor-specific T-cell alloreactivity is strongly associated with early acute cellular rejection in kidney transplant recipients not receiving T-cell depleting induction therapy</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Preformed T-cell immune-sensitization should most likely impact allograft outcome during the initial period after kidney transplantation, since donor-specific memory T-cells may rapidly recognize alloantigens and activate the effector immune response, which leads to allograft rejection. However, the precise time-frame in which acute rejection is fundamentally triggered by preformed donor-specific memory T cells rather than by de novo activated naïve T cells is still to be established. Here, preformed donor-specific alloreactive T-cell responses were evaluated using the IFN-γ ELISPOT assay in a large consecutive cohort of kidney transplant patients (n = 90), to assess the main clinical variables associated with cellular sensitization and its predominant time-frame impact on allograft outcome, and was further validated in an independent new set of kidney transplant recipients (n = 67). We found that most highly T-cell sensitized patients were elderly patients with particularly poor HLA class-I matching, without any clinically recognizable sensitizing events. While one-year incidence of all types of biopsy-proven acute rejection did not differ between T-cell alloreactive and non-alloreactive patients, Receiver Operating Characteristic curve analysis indicated the first two months after transplantation as the highest risk time period for acute cellular rejection associated with baseline T-cell sensitization. This effect was particularly evident in young and highly alloreactive individuals that did not receive T-cell depletion immunosuppression. Multivariate analysis confirmed preformed T-cell sensitization as an independent predictor of early acute cellular rejection. In summary, monitoring anti-donor T-cell sensitization before transplantation may help to identify patients at increased risk of acute cellular rejection, particularly in the early phases after kidney transplantation, and thus guide decision-making regarding the use of induction therapy.</description><subject>Adult</subject><subject>Aged</subject><subject>Alloantigens</subject><subject>Analysis</subject><subject>Antigens</subject><subject>Biomedical research</subject><subject>Biopsy</subject><subject>Clinical decision making</subject><subject>Cèl·lules T</subject><subject>Decision making</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Ethnicity</subject><subject>Female</subject><subject>Geriatrics</subject><subject>Graft rejection</subject><subject>Graft Rejection - immunology</subject><subject>Health risk assessment</subject><subject>Hemodialysis</subject><subject>Histocompatibility antigen HLA</subject><subject>Humans</subject><subject>Immune 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Edoardo</au><au>Manonelles, Anna</au><au>Lloberas, Nuria</au><au>Torras, Joan</au><au>Grinyó, Josep M</au><au>Bestard, Oriol</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pre-transplant donor-specific T-cell alloreactivity is strongly associated with early acute cellular rejection in kidney transplant recipients not receiving T-cell depleting induction therapy</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-02-17</date><risdate>2015</risdate><volume>10</volume><issue>2</issue><spage>e0117618</spage><epage>e0117618</epage><pages>e0117618-e0117618</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Preformed T-cell immune-sensitization should most likely impact allograft outcome during the initial period after kidney transplantation, since donor-specific memory T-cells may rapidly recognize alloantigens and activate the effector immune response, which leads to allograft rejection. However, the precise time-frame in which acute rejection is fundamentally triggered by preformed donor-specific memory T cells rather than by de novo activated naïve T cells is still to be established. Here, preformed donor-specific alloreactive T-cell responses were evaluated using the IFN-γ ELISPOT assay in a large consecutive cohort of kidney transplant patients (n = 90), to assess the main clinical variables associated with cellular sensitization and its predominant time-frame impact on allograft outcome, and was further validated in an independent new set of kidney transplant recipients (n = 67). We found that most highly T-cell sensitized patients were elderly patients with particularly poor HLA class-I matching, without any clinically recognizable sensitizing events. While one-year incidence of all types of biopsy-proven acute rejection did not differ between T-cell alloreactive and non-alloreactive patients, Receiver Operating Characteristic curve analysis indicated the first two months after transplantation as the highest risk time period for acute cellular rejection associated with baseline T-cell sensitization. This effect was particularly evident in young and highly alloreactive individuals that did not receive T-cell depletion immunosuppression. Multivariate analysis confirmed preformed T-cell sensitization as an independent predictor of early acute cellular rejection. In summary, monitoring anti-donor T-cell sensitization before transplantation may help to identify patients at increased risk of acute cellular rejection, particularly in the early phases after kidney transplantation, and thus guide decision-making regarding the use of induction therapy.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25689405</pmid><doi>10.1371/journal.pone.0117618</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-02, Vol.10 (2), p.e0117618-e0117618 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1655740416 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; Recercat; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adult Aged Alloantigens Analysis Antigens Biomedical research Biopsy Clinical decision making Cèl·lules T Decision making Enzyme-linked immunosorbent assay Ethnicity Female Geriatrics Graft rejection Graft Rejection - immunology Health risk assessment Hemodialysis Histocompatibility antigen HLA Humans Immune response Immune system Immunological memory Immunosuppression Immunosuppression - methods Immunosuppressive Agents - therapeutic use Immunotherapy Induction therapy Interferon Kidney diseases Kidney Transplantation Kidney transplants Kidneys Laboratories Lymphocyte Depletion Lymphocytes Lymphocytes T Male Memory cells Middle Aged Multivariate analysis Nephrology Older people Organ transplant recipients Patients Rebuig (Biologia) Rejection Retrospective Studies Sensitizing T cells T-Lymphocytes - immunology Therapy Transplantation Transplantation of organs Transplants & implants Trasplantament d'òrgans Trasplantament renal γ-Interferon |
| title | Pre-transplant donor-specific T-cell alloreactivity is strongly associated with early acute cellular rejection in kidney transplant recipients not receiving T-cell depleting induction therapy |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-11T07%3A52%3A14IST&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=Pre-transplant%20donor-specific%20T-cell%20alloreactivity%20is%20strongly%20associated%20with%20early%20acute%20cellular%20rejection%20in%20kidney%20transplant%20recipients%20not%20receiving%20T-cell%20depleting%20induction%20therapy&rft.jtitle=PloS%20one&rft.au=Crespo,%20Elena&rft.date=2015-02-17&rft.volume=10&rft.issue=2&rft.spage=e0117618&rft.epage=e0117618&rft.pages=e0117618-e0117618&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0117618&rft_dat=%3Cgale_plos_%3EA425367916%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=1655740416&rft_id=info:pmid/25689405&rft_galeid=A425367916&rft_doaj_id=oai_doaj_org_article_27d01757638645c5a419df5994dd4a55&rfr_iscdi=true |