Impaired Immune Function in Patients With Chronic Postsurgical Hypoparathyroidism: Results of the EMPATHY Study
Abstract Context Despite the pivotal role of calcium signaling in immune response, little is known about immune function in patients affected by hypoparathyroidism. Objective This work aimed to evaluate immune function in hypoparathyroidism. Methods The Evaluation of iMmune function in Postsurgical...
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| Veröffentlicht in: | The journal of clinical endocrinology and metabolism 2021-05, Vol.106 (5), p.e2215-e2227 |
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| creator | Puliani, Giulia Hasenmajer, Valeria Sciarra, Francesca Barbagallo, Federica Sbardella, Emilia Pofi, Riccardo Gianfrilli, Daniele Romagnoli, Elisabetta Venneri, Mary Anna Isidori, Andrea M |
| description | Abstract
Context
Despite the pivotal role of calcium signaling in immune response, little is known about immune function in patients affected by hypoparathyroidism.
Objective
This work aimed to evaluate immune function in hypoparathyroidism.
Methods
The Evaluation of iMmune function in Postsurgical and AuToimmune HYpoparathyroidism (NCT04059380) is a case-control, cross-sectional study set in an Italian referral center. Participants included 20 patients with postsurgical hypoparathyroidism (12 females) and 20 age- and sex-matched controls. Main outcome measures included calcium metabolism assessment, peripheral blood mononuclear cells (PBMC) profiling via flow cytometry, parathyroid hormone receptor 1 (PTHr1) expression analysis using immunofluorescence and PrimeFlow RNA assay, gene expression analysis via real-time polymerase chain reaction, cytokine measurement, and evaluation of infectious disease frequency and severity.
Results
Immune cell profiling revealed decreased monocytes, regulatory, naive, and total CD4+ T lymphocytes, which correlated with total calcium, ionized calcium, and PTH levels, in patients with hypoparathyroidism. Patients with hypoparathyroidism had a higher CD3−CD56+ natural killer (NK) cell count, which inversely correlated with calcium, PTH, and vitamin D levels. Furthermore, they exhibited decreased tumor necrosis factor (TNF) and granulocyte-macrophage colony-stimulating factor gene expression and decreased circulating TNF levels. Gene expression and immunofluorescence analysis confirmed PTHr1 expression in all PBMC lineages; however, the percentage of cells expressing PTHr1 was lower, whereas the intensity of PTHr1 expression in monocytes, total T lymphocytes, CD8+CD4+ and CD4+ T lymphocytes, and total NK cells was higher in patients with hypoparathyroidism.
Conclusions
This study describes for the first time the immune alterations in patients with hypoparathyroidism receiving conventional therapies, supporting the immunoregulatory role of PTH and proposing an explanation for the increased susceptibility to infections observed in epidemiological studies. |
| doi_str_mv | 10.1210/clinem/dgab038 |
| format | Article |
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Context
Despite the pivotal role of calcium signaling in immune response, little is known about immune function in patients affected by hypoparathyroidism.
Objective
This work aimed to evaluate immune function in hypoparathyroidism.
Methods
The Evaluation of iMmune function in Postsurgical and AuToimmune HYpoparathyroidism (NCT04059380) is a case-control, cross-sectional study set in an Italian referral center. Participants included 20 patients with postsurgical hypoparathyroidism (12 females) and 20 age- and sex-matched controls. Main outcome measures included calcium metabolism assessment, peripheral blood mononuclear cells (PBMC) profiling via flow cytometry, parathyroid hormone receptor 1 (PTHr1) expression analysis using immunofluorescence and PrimeFlow RNA assay, gene expression analysis via real-time polymerase chain reaction, cytokine measurement, and evaluation of infectious disease frequency and severity.
Results
Immune cell profiling revealed decreased monocytes, regulatory, naive, and total CD4+ T lymphocytes, which correlated with total calcium, ionized calcium, and PTH levels, in patients with hypoparathyroidism. Patients with hypoparathyroidism had a higher CD3−CD56+ natural killer (NK) cell count, which inversely correlated with calcium, PTH, and vitamin D levels. Furthermore, they exhibited decreased tumor necrosis factor (TNF) and granulocyte-macrophage colony-stimulating factor gene expression and decreased circulating TNF levels. Gene expression and immunofluorescence analysis confirmed PTHr1 expression in all PBMC lineages; however, the percentage of cells expressing PTHr1 was lower, whereas the intensity of PTHr1 expression in monocytes, total T lymphocytes, CD8+CD4+ and CD4+ T lymphocytes, and total NK cells was higher in patients with hypoparathyroidism.
Conclusions
This study describes for the first time the immune alterations in patients with hypoparathyroidism receiving conventional therapies, supporting the immunoregulatory role of PTH and proposing an explanation for the increased susceptibility to infections observed in epidemiological studies.</description><identifier>ISSN: 0021-972X</identifier><identifier>EISSN: 1945-7197</identifier><identifier>DOI: 10.1210/clinem/dgab038</identifier><identifier>PMID: 33484559</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Alfacalcidol ; Calcifediol ; Calcium (blood) ; Calcium metabolism ; Calcium signalling ; Care and treatment ; CD3 antigen ; CD4 antigen ; CD56 antigen ; CD8 antigen ; Colony-stimulating factor ; Communicable diseases ; Disease susceptibility ; Epidemiology ; Flow cytometry ; Gene expression ; Genes ; Granulocyte-macrophage colony-stimulating factor ; Health aspects ; Hypoparathyroidism ; Immune response ; Immunofluorescence ; Immunoregulation ; Infectious diseases ; Leukocytes (mononuclear) ; Lymphocytes ; Lymphocytes T ; Macrophage colony stimulating factor ; Macrophages ; Monocytes ; Natural killer cells ; Parathyroid hormone ; Peripheral blood mononuclear cells ; Physiological aspects ; Risk factors ; Tumor necrosis factor ; Tumor necrosis factor-TNF ; Vitamin D</subject><ispartof>The journal of clinical endocrinology and metabolism, 2021-05, Vol.106 (5), p.e2215-e2227</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Endocrine Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Endocrine Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>COPYRIGHT 2021 Oxford University Press</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Endocrine Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c464t-715b09220a260cc065194976e44fcabac27f3296c8d80b643fe835afeec749b03</citedby><cites>FETCH-LOGICAL-c464t-715b09220a260cc065194976e44fcabac27f3296c8d80b643fe835afeec749b03</cites><orcidid>0000-0002-2220-9783 ; 0000-0002-6298-9235 ; 0000-0001-7808-5735 ; 0000-0002-2682-8266 ; 0000-0002-9037-5417 ; 0000-0003-2899-9146 ; 0000-0002-0687-8135 ; 0000-0003-4301-6662 ; 0000-0002-2972-370X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33484559$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Puliani, Giulia</creatorcontrib><creatorcontrib>Hasenmajer, Valeria</creatorcontrib><creatorcontrib>Sciarra, Francesca</creatorcontrib><creatorcontrib>Barbagallo, Federica</creatorcontrib><creatorcontrib>Sbardella, Emilia</creatorcontrib><creatorcontrib>Pofi, Riccardo</creatorcontrib><creatorcontrib>Gianfrilli, Daniele</creatorcontrib><creatorcontrib>Romagnoli, Elisabetta</creatorcontrib><creatorcontrib>Venneri, Mary Anna</creatorcontrib><creatorcontrib>Isidori, Andrea M</creatorcontrib><title>Impaired Immune Function in Patients With Chronic Postsurgical Hypoparathyroidism: Results of the EMPATHY Study</title><title>The journal of clinical endocrinology and metabolism</title><addtitle>J Clin Endocrinol Metab</addtitle><description>Abstract
Context
Despite the pivotal role of calcium signaling in immune response, little is known about immune function in patients affected by hypoparathyroidism.
Objective
This work aimed to evaluate immune function in hypoparathyroidism.
Methods
The Evaluation of iMmune function in Postsurgical and AuToimmune HYpoparathyroidism (NCT04059380) is a case-control, cross-sectional study set in an Italian referral center. Participants included 20 patients with postsurgical hypoparathyroidism (12 females) and 20 age- and sex-matched controls. Main outcome measures included calcium metabolism assessment, peripheral blood mononuclear cells (PBMC) profiling via flow cytometry, parathyroid hormone receptor 1 (PTHr1) expression analysis using immunofluorescence and PrimeFlow RNA assay, gene expression analysis via real-time polymerase chain reaction, cytokine measurement, and evaluation of infectious disease frequency and severity.
Results
Immune cell profiling revealed decreased monocytes, regulatory, naive, and total CD4+ T lymphocytes, which correlated with total calcium, ionized calcium, and PTH levels, in patients with hypoparathyroidism. Patients with hypoparathyroidism had a higher CD3−CD56+ natural killer (NK) cell count, which inversely correlated with calcium, PTH, and vitamin D levels. Furthermore, they exhibited decreased tumor necrosis factor (TNF) and granulocyte-macrophage colony-stimulating factor gene expression and decreased circulating TNF levels. Gene expression and immunofluorescence analysis confirmed PTHr1 expression in all PBMC lineages; however, the percentage of cells expressing PTHr1 was lower, whereas the intensity of PTHr1 expression in monocytes, total T lymphocytes, CD8+CD4+ and CD4+ T lymphocytes, and total NK cells was higher in patients with hypoparathyroidism.
Conclusions
This study describes for the first time the immune alterations in patients with hypoparathyroidism receiving conventional therapies, supporting the immunoregulatory role of PTH and proposing an explanation for the increased susceptibility to infections observed in epidemiological studies.</description><subject>Alfacalcidol</subject><subject>Calcifediol</subject><subject>Calcium (blood)</subject><subject>Calcium metabolism</subject><subject>Calcium signalling</subject><subject>Care and treatment</subject><subject>CD3 antigen</subject><subject>CD4 antigen</subject><subject>CD56 antigen</subject><subject>CD8 antigen</subject><subject>Colony-stimulating factor</subject><subject>Communicable diseases</subject><subject>Disease susceptibility</subject><subject>Epidemiology</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Granulocyte-macrophage colony-stimulating factor</subject><subject>Health aspects</subject><subject>Hypoparathyroidism</subject><subject>Immune response</subject><subject>Immunofluorescence</subject><subject>Immunoregulation</subject><subject>Infectious diseases</subject><subject>Leukocytes (mononuclear)</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Macrophage colony stimulating factor</subject><subject>Macrophages</subject><subject>Monocytes</subject><subject>Natural killer cells</subject><subject>Parathyroid hormone</subject><subject>Peripheral blood mononuclear cells</subject><subject>Physiological aspects</subject><subject>Risk factors</subject><subject>Tumor necrosis factor</subject><subject>Tumor necrosis factor-TNF</subject><subject>Vitamin D</subject><issn>0021-972X</issn><issn>1945-7197</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkc1rGzEQxUVpady01x6LoJf24ETSSqtVb8YktSGlpkloexJardZW2JU2-jj4v6-C3QRKoMxhYPi9x8w8AN5jdIYJRud6sM6M591WtahqXoAZFpTNORb8JZghRPBccPLrBLyJ8Q4hTCmrXoOTqqINZUzMgF-Pk7LBdHA9jtkZeJmdTtY7aB3cqGSNSxH-tGkHl7vgndVw42OKOWytVgNc7Sc_qaDSbh-87Wwcv8AfJuahqHwP087Ai2-bxc3qN7xOudu_Ba96NUTz7thPwe3lxc1yNb_6_nW9XFzNNa1pKgewFglCkCI10hrVrNwleG0o7bVqlSa8r4ioddM1qK1p1ZumYqo3RnMqyitOwaeD7xT8fTYxydFGbYZBOeNzlIQ2qCKcclbQj_-gdz4HV7aTRLAac464eKK2ajDSut6noPSDqVxwRCrOcF0X6uwZqlRnRqu9M70t8-cEOvgYg-nlFOyowl5iJB8SloeE5THhIvhw3Da3o-ke8b-RFuDzAfB5-p_ZH70ysEc</recordid><startdate>20210501</startdate><enddate>20210501</enddate><creator>Puliani, Giulia</creator><creator>Hasenmajer, Valeria</creator><creator>Sciarra, Francesca</creator><creator>Barbagallo, Federica</creator><creator>Sbardella, Emilia</creator><creator>Pofi, Riccardo</creator><creator>Gianfrilli, Daniele</creator><creator>Romagnoli, Elisabetta</creator><creator>Venneri, Mary Anna</creator><creator>Isidori, Andrea M</creator><general>Oxford University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7T5</scope><scope>7TM</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-2220-9783</orcidid><orcidid>https://orcid.org/0000-0002-6298-9235</orcidid><orcidid>https://orcid.org/0000-0001-7808-5735</orcidid><orcidid>https://orcid.org/0000-0002-2682-8266</orcidid><orcidid>https://orcid.org/0000-0002-9037-5417</orcidid><orcidid>https://orcid.org/0000-0003-2899-9146</orcidid><orcidid>https://orcid.org/0000-0002-0687-8135</orcidid><orcidid>https://orcid.org/0000-0003-4301-6662</orcidid><orcidid>https://orcid.org/0000-0002-2972-370X</orcidid></search><sort><creationdate>20210501</creationdate><title>Impaired Immune Function in Patients With Chronic Postsurgical Hypoparathyroidism: Results of the EMPATHY Study</title><author>Puliani, Giulia ; Hasenmajer, Valeria ; Sciarra, Francesca ; Barbagallo, Federica ; Sbardella, Emilia ; Pofi, Riccardo ; Gianfrilli, Daniele ; Romagnoli, Elisabetta ; Venneri, Mary Anna ; Isidori, Andrea M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c464t-715b09220a260cc065194976e44fcabac27f3296c8d80b643fe835afeec749b03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Alfacalcidol</topic><topic>Calcifediol</topic><topic>Calcium (blood)</topic><topic>Calcium metabolism</topic><topic>Calcium signalling</topic><topic>Care and treatment</topic><topic>CD3 antigen</topic><topic>CD4 antigen</topic><topic>CD56 antigen</topic><topic>CD8 antigen</topic><topic>Colony-stimulating factor</topic><topic>Communicable diseases</topic><topic>Disease susceptibility</topic><topic>Epidemiology</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Granulocyte-macrophage colony-stimulating factor</topic><topic>Health aspects</topic><topic>Hypoparathyroidism</topic><topic>Immune response</topic><topic>Immunofluorescence</topic><topic>Immunoregulation</topic><topic>Infectious diseases</topic><topic>Leukocytes (mononuclear)</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Macrophage colony stimulating factor</topic><topic>Macrophages</topic><topic>Monocytes</topic><topic>Natural killer cells</topic><topic>Parathyroid hormone</topic><topic>Peripheral blood mononuclear cells</topic><topic>Physiological aspects</topic><topic>Risk factors</topic><topic>Tumor necrosis factor</topic><topic>Tumor necrosis factor-TNF</topic><topic>Vitamin D</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Puliani, Giulia</creatorcontrib><creatorcontrib>Hasenmajer, Valeria</creatorcontrib><creatorcontrib>Sciarra, Francesca</creatorcontrib><creatorcontrib>Barbagallo, Federica</creatorcontrib><creatorcontrib>Sbardella, Emilia</creatorcontrib><creatorcontrib>Pofi, Riccardo</creatorcontrib><creatorcontrib>Gianfrilli, Daniele</creatorcontrib><creatorcontrib>Romagnoli, Elisabetta</creatorcontrib><creatorcontrib>Venneri, Mary Anna</creatorcontrib><creatorcontrib>Isidori, Andrea M</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>The journal of clinical endocrinology and metabolism</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Puliani, Giulia</au><au>Hasenmajer, Valeria</au><au>Sciarra, Francesca</au><au>Barbagallo, Federica</au><au>Sbardella, Emilia</au><au>Pofi, Riccardo</au><au>Gianfrilli, Daniele</au><au>Romagnoli, Elisabetta</au><au>Venneri, Mary Anna</au><au>Isidori, Andrea M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Impaired Immune Function in Patients With Chronic Postsurgical Hypoparathyroidism: Results of the EMPATHY Study</atitle><jtitle>The journal of clinical endocrinology and metabolism</jtitle><addtitle>J Clin Endocrinol Metab</addtitle><date>2021-05-01</date><risdate>2021</risdate><volume>106</volume><issue>5</issue><spage>e2215</spage><epage>e2227</epage><pages>e2215-e2227</pages><issn>0021-972X</issn><eissn>1945-7197</eissn><abstract>Abstract
Context
Despite the pivotal role of calcium signaling in immune response, little is known about immune function in patients affected by hypoparathyroidism.
Objective
This work aimed to evaluate immune function in hypoparathyroidism.
Methods
The Evaluation of iMmune function in Postsurgical and AuToimmune HYpoparathyroidism (NCT04059380) is a case-control, cross-sectional study set in an Italian referral center. Participants included 20 patients with postsurgical hypoparathyroidism (12 females) and 20 age- and sex-matched controls. Main outcome measures included calcium metabolism assessment, peripheral blood mononuclear cells (PBMC) profiling via flow cytometry, parathyroid hormone receptor 1 (PTHr1) expression analysis using immunofluorescence and PrimeFlow RNA assay, gene expression analysis via real-time polymerase chain reaction, cytokine measurement, and evaluation of infectious disease frequency and severity.
Results
Immune cell profiling revealed decreased monocytes, regulatory, naive, and total CD4+ T lymphocytes, which correlated with total calcium, ionized calcium, and PTH levels, in patients with hypoparathyroidism. Patients with hypoparathyroidism had a higher CD3−CD56+ natural killer (NK) cell count, which inversely correlated with calcium, PTH, and vitamin D levels. Furthermore, they exhibited decreased tumor necrosis factor (TNF) and granulocyte-macrophage colony-stimulating factor gene expression and decreased circulating TNF levels. Gene expression and immunofluorescence analysis confirmed PTHr1 expression in all PBMC lineages; however, the percentage of cells expressing PTHr1 was lower, whereas the intensity of PTHr1 expression in monocytes, total T lymphocytes, CD8+CD4+ and CD4+ T lymphocytes, and total NK cells was higher in patients with hypoparathyroidism.
Conclusions
This study describes for the first time the immune alterations in patients with hypoparathyroidism receiving conventional therapies, supporting the immunoregulatory role of PTH and proposing an explanation for the increased susceptibility to infections observed in epidemiological studies.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>33484559</pmid><doi>10.1210/clinem/dgab038</doi><orcidid>https://orcid.org/0000-0002-2220-9783</orcidid><orcidid>https://orcid.org/0000-0002-6298-9235</orcidid><orcidid>https://orcid.org/0000-0001-7808-5735</orcidid><orcidid>https://orcid.org/0000-0002-2682-8266</orcidid><orcidid>https://orcid.org/0000-0002-9037-5417</orcidid><orcidid>https://orcid.org/0000-0003-2899-9146</orcidid><orcidid>https://orcid.org/0000-0002-0687-8135</orcidid><orcidid>https://orcid.org/0000-0003-4301-6662</orcidid><orcidid>https://orcid.org/0000-0002-2972-370X</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The journal of clinical endocrinology and metabolism, 2021-05, Vol.106 (5), p.e2215-e2227 |
| issn | 0021-972X 1945-7197 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_2480327475 |
| source | Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Alfacalcidol Calcifediol Calcium (blood) Calcium metabolism Calcium signalling Care and treatment CD3 antigen CD4 antigen CD56 antigen CD8 antigen Colony-stimulating factor Communicable diseases Disease susceptibility Epidemiology Flow cytometry Gene expression Genes Granulocyte-macrophage colony-stimulating factor Health aspects Hypoparathyroidism Immune response Immunofluorescence Immunoregulation Infectious diseases Leukocytes (mononuclear) Lymphocytes Lymphocytes T Macrophage colony stimulating factor Macrophages Monocytes Natural killer cells Parathyroid hormone Peripheral blood mononuclear cells Physiological aspects Risk factors Tumor necrosis factor Tumor necrosis factor-TNF Vitamin D |
| title | Impaired Immune Function in Patients With Chronic Postsurgical Hypoparathyroidism: Results of the EMPATHY Study |
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