ProCite
RefWorks
Reference Manager
BibTeX
Zotero
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1.
Yu XJ et al., 2011. Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 364: 1523–1532.
-
2.
Kim YR, Yun Y, Bae SG, Park D, Kim S, Lee JM, Cho NH, Kim YS, Lee KH, 2018. Severe fever with thrombocytopenia syndrome virus infection, South Korea, 2010. Emerg Infect Dis 24: 2103–2105.
-
3.
Takahashi T et al., 2014. The first identification and retrospective study of severe fever with thrombocytopenia syndrome in Japan. J Infect Dis 209: 816–827.
-
4.
Li H et al., 2018. Epidemiological and clinical features of laboratory-diagnosed severe fever with thrombocytopenia syndrome in China, 2011–17: a prospective observational study. Lancet Infect Dis 18: 1127–1137.
-
5.
Choi SJ et al., 2016. Severe fever with thrombocytopenia syndrome in South Korea, 2013–2015. PLoS Negl Trop Dis 10: e0005264.
-
6.
Kobayashi Y et al., 2020. Severe fever with thrombocytopenia syndrome, Japan, 2013–2017. Emerg Infect Dis 26: 692–699.
-
7.
Liu Q, He B, Huang SY, Wei F, Zhu XQ, 2014. Severe fever with thrombocytopenia syndrome, an emerging tick-borne zoonosis. Lancet Infect Dis 14: 763–772.
-
8.
Casel MA, Park SJ, Choi YK, 2021. Severe fever with thrombocytopenia syndrome virus: emerging novel phlebovirus and their control strategy. Exp Mol Med 53: 713–722.
-
9.
Gai ZT et al., 2012. Clinical progress and risk factors for death in severe fever with thrombocytopenia syndrome patients. J Infect Dis 206: 1095–1102.
-
10.
Li DX, 2015. Severe fever with thrombocytopenia syndrome: a newly discovered emerging infectious disease. Clin Microbiol Infect 21: 614–620.
-
11.
Ding YP et al., 2014. Prognostic value of clinical and immunological markers in acute phase of SFTS virus infection. Clin Microbiol Infect 20: O870–O878.
-
12.
Yoo JR et al., 2021. Neutralizing antibodies to severe fever with thrombocytopenia syndrome virus among survivors, non-survivors and healthy residents in South Korea. Front Cell Infect Microbiol 11: 649570.
-
13.
Li MM et al., 2018. Dynamic changes in the immunological characteristics of T lymphocytes in surviving patients with severe fever with thrombocytopenia syndrome (SFTS). Int J Infect Dis 70: 72–80.
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14.
Lu Q-B, Cui N, Hu J-G, Chen W-W, Xu W, Li H, Zhang X-A, Ly H, Liu W, Cao W-C, 2015. Characterization of immunological responses in patients with severe fever with thrombocytopenia syndrome: a cohort study in China. Vaccine 33: 1250–1255.
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15.
de Jong LC, Crnko S, Ten Broeke T, Bovenschen N, 2021. Noncytotoxic functions of killer cell granzymes in viral infections. PLoS Pathog 17: e1009818.
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Xu W et al., 2017. Association between peripheral γδ T cell subsets and disease progression of severe fever with thrombocytopenia syndrome virus infection. Pathog Dis 75: ftx086.
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Voskoboinik I, Whisstock JC, Trapani JA, 2015. Perforin and granzymes: function, dysfunction and human pathology. Nat Rev Immunol 15: 388–400.
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18.
Korea Disease Control and Prevention Agency , 2016. SFTS Treatment Guideline. Available at: https://www.ksid.or.kr/rang_board/list.html?num=2531&code=notice3. Accessed May 28, 2023.
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Novus Biologicals , 2022. Human Granzyme A ELISA Kit (Colorimetric). Available at: https://www.novusbio.com/products/granzyme-a-elisa-kit_nbp3-11790. Accessed May 28, 2023.
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Novus Biologicals , 2022. Human Perforin ELISA Kit. Available at: https://www.novusbio.com/products/perforin-elisa-kit_nbp3-11726. Accessed May 28, 2023.
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Novus Biologicals Human Granzyme B Quantikine ELISA Kit. Available at: https://www.novusbio.com/products/human-granzyme-b-quantikine-elisa-kit_dgzb00. Accessed May 28, 2023.
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Siemens Healthcare GmbH ADVIA 2400 Chemistry System. Available at: https://www.siemens-healthineers.com/clinical-chemistry/systems/advia-2400-chemistry-system. Accessed May 28, 2023.
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Sysmex , 2023. XE-2100â„¢ Automated Hematology System. Available at: https://www.sysmex.com/la/pt/Products/Documents/English/XE-2100-English.pdf. Accessed May 28, 2023.
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24.
Kogenbiotech PowerChekâ„¢ Tick-Borne Disease Real-time PCR Kit Series. Available at: https://www.kogene.co.kr/kr/sub/product/infectious_disease/tick-borne_disease/qpcr.asp. Accessed May 28, 2023.
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Westmeier J et al., 2020. Impaired cytotoxic CD8+ T cell response in elderly COVID-19 patients. mBio 11: e02243.
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26.
Young JD, Damiano A, DiNome MA, Leong LG, Cohn ZA, 1987. Dissociation of membrane binding and lytic activities of the lymphocyte pore-forming protein (perforin). J Exp Med 165: 1371–1382.
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27.
Praper T, Besenicar MP, Istinic H, Podlesek Z, Metkar SS, Froelich CJ, Anderluh G, 2010. Human perforin permeabilizing activity, but not binding to lipid membranes, is affected by pH. Mol Immunol 47: 2492–2504.
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28.
Zhang Q, Zhao J, Dai Y, Jiang Z, Chen T, Hu N, Jin K, Li J, 2023. A high viral load in urine correlates with acute kidney injury and poor outcomes in hospitalized patients with severe fever with thrombocytopenia syndrome: a noninvasive and convenient prognostic marker. Open Forum Infect Dis 10: ofad085.
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29.
Cook KD, Waggoner SN, Whitmire JK, 2014. NK cells and their ability to modulate T cells during virus infections. Crit Rev Immunol 34: 359–388.
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30.
Ryu S, Chun JY, Lee S, Yoo D, Kim Y, Ali ST, Chun BC, 2022. Epidemiology and transmission dynamics of infectious diseases and control measures. Viruses 14: 2510.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2041 | 1174 | 123 |
| Full Text Views | 293 | 68 | 8 |
| PDF Downloads | 115 | 44 | 4 |
Temporal Dynamics of Serum Perforin and Granzymes in Three Different Clinical Stages of Virus-Induced Severe Fever with Thrombocytopenia Syndrome
Sukhyun Ryu
Sukhyun Ryu
Department of Preventive Medicine, Konyang University College of Medicine, Daejeon, South Korea;
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Jin Kyeong Choi
Jin Kyeong Choi
Department of Immunology, Jeonbuk National University Medical School, Jeonju, South Korea;
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Chiara Achangwa
Chiara Achangwa
Department of Preventive Medicine, Konyang University College of Medicine, Daejeon, South Korea;
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Soojung Cho
Soojung Cho
Department of Preventive Medicine, Konyang University College of Medicine, Daejeon, South Korea;
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Joo-Hee Hwang
Joo-Hee Hwang
Department of Internal Medicine, Jeonbuk National University Medical School, Jeonju, South Korea;
Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea;
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Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea;
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Jeong-Hwan Hwang
Jeong-Hwan Hwang
Department of Internal Medicine, Jeonbuk National University Medical School, Jeonju, South Korea;
Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea;
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Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea;
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Niels Bovenschen
Niels Bovenschen
Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands;
Center for Translational Immunology, University Medical Center Utrecht, Utrecht, The Netherlands;
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Center for Translational Immunology, University Medical Center Utrecht, Utrecht, The Netherlands;
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Chang-Seop Lee
Chang-Seop Lee
Department of Internal Medicine, Jeonbuk National University Medical School, Jeonju, South Korea;
Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea;
Department of Medical Science, Jeonbuk National University Medical School, Jeonju, South Korea
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Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea;
Department of Medical Science, Jeonbuk National University Medical School, Jeonju, South Korea
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ABSTRACT.
Virus-induced severe fever with thrombocytopenia syndrome (SFTS) induces a cell-mediated immune response that likely contributes to virus control in SFTS patients. To identify the temporal changes of the cell-mediated immune response, we investigated the changes in serum levels of perforin and granzymes at early periods after illness onset in SFTS patients. We analyzed 32 SFTS patients and compared the temporal patterns of serum perforin and granzyme A and B to that of 20 healthy control adults using the Mann-Whitney U test. Compared with healthy controls, the mean level of perforin was significantly reduced by 81% (P < 0.01) during the first week after illness onset, whereas granzyme B significantly increased by 4.6-fold (P = 0.02) in the first week after illness onset and decreased to normal afterward. During the study period, there was no significant difference in serum perforin and granzyme. These findings indicate that perforin and granzyme B in serum can be considered possible serologic markers that reflect the clinical stage of SFTS. Additional study is warranted for tracking circulating perforin and granzyme in different ages and for an extended period after illness onset.
- Supplemental Materials (PDF 641.53 KB)
Author Notes
Financial support: This research was supported by the
The data underlying this article will be shared on reasonable request to the corresponding author. All study participants provided written informed consent, and all study procedures were approved by the Institutional Review Board (IRB) of Jeonbuk National University Hospital (IRB registration number 2019-06-020).
Authors’ addresses: Sukhyun Ryu, Chiara Achangwa, and Soojung Cho, Department of Preventive Medicine, Konyang University College of Medicine, Daejeon, South Korea, E-mails: gentryu@onehealth.or.kr, ciaraacha@gmail.com, and 22531518@konyang.ac.kr. Jin Kyeong Choi, Department of Immunology, Jeonbuk National University Medical School, Jeonju, South Korea, E-mail: jkchoi@jbnu.ac.kr. Joo-Hee Hwang and Jeong-Hwan Hwang, Department of Internal Medicine, Jeonbuk National University Medical School, Jeonju, South Korea, and Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea, E-mails: zany78@naver.com and smilehwang77@hanmail.net. Niels Bovenschen, Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands, and Center for Translational Immunology, University Medical Center Utrecht, Utrecht, The Netherlands, E-mail: n.bovenschen@umcutrecht.nl. Chang-Seop Lee, Department of Internal Medicine, Jeonbuk National University Medical School, Jeonju, South Korea, Research Institute of Clinical Medicine of Jeonbuk National University-Biomedical Research Institute of Jeonbuk National University Hospital, Jeonju, South Korea, and Department of Medical Science, Jeonbuk National University Medical School, Jeonju, South Korea, E-mail: lcsmd@jbnu.ac.kr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Yu XJ et al., 2011. Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 364: 1523–1532.
-
2.
Kim YR, Yun Y, Bae SG, Park D, Kim S, Lee JM, Cho NH, Kim YS, Lee KH, 2018. Severe fever with thrombocytopenia syndrome virus infection, South Korea, 2010. Emerg Infect Dis 24: 2103–2105.
-
3.
Takahashi T et al., 2014. The first identification and retrospective study of severe fever with thrombocytopenia syndrome in Japan. J Infect Dis 209: 816–827.
-
4.
Li H et al., 2018. Epidemiological and clinical features of laboratory-diagnosed severe fever with thrombocytopenia syndrome in China, 2011–17: a prospective observational study. Lancet Infect Dis 18: 1127–1137.
-
5.
Choi SJ et al., 2016. Severe fever with thrombocytopenia syndrome in South Korea, 2013–2015. PLoS Negl Trop Dis 10: e0005264.
-
6.
Kobayashi Y et al., 2020. Severe fever with thrombocytopenia syndrome, Japan, 2013–2017. Emerg Infect Dis 26: 692–699.
-
7.
Liu Q, He B, Huang SY, Wei F, Zhu XQ, 2014. Severe fever with thrombocytopenia syndrome, an emerging tick-borne zoonosis. Lancet Infect Dis 14: 763–772.
-
8.
Casel MA, Park SJ, Choi YK, 2021. Severe fever with thrombocytopenia syndrome virus: emerging novel phlebovirus and their control strategy. Exp Mol Med 53: 713–722.
-
9.
Gai ZT et al., 2012. Clinical progress and risk factors for death in severe fever with thrombocytopenia syndrome patients. J Infect Dis 206: 1095–1102.
-
10.
Li DX, 2015. Severe fever with thrombocytopenia syndrome: a newly discovered emerging infectious disease. Clin Microbiol Infect 21: 614–620.
-
11.
Ding YP et al., 2014. Prognostic value of clinical and immunological markers in acute phase of SFTS virus infection. Clin Microbiol Infect 20: O870–O878.
-
12.
Yoo JR et al., 2021. Neutralizing antibodies to severe fever with thrombocytopenia syndrome virus among survivors, non-survivors and healthy residents in South Korea. Front Cell Infect Microbiol 11: 649570.
-
13.
Li MM et al., 2018. Dynamic changes in the immunological characteristics of T lymphocytes in surviving patients with severe fever with thrombocytopenia syndrome (SFTS). Int J Infect Dis 70: 72–80.
-
14.
Lu Q-B, Cui N, Hu J-G, Chen W-W, Xu W, Li H, Zhang X-A, Ly H, Liu W, Cao W-C, 2015. Characterization of immunological responses in patients with severe fever with thrombocytopenia syndrome: a cohort study in China. Vaccine 33: 1250–1255.
-
15.
de Jong LC, Crnko S, Ten Broeke T, Bovenschen N, 2021. Noncytotoxic functions of killer cell granzymes in viral infections. PLoS Pathog 17: e1009818.
-
16.
Xu W et al., 2017. Association between peripheral γδ T cell subsets and disease progression of severe fever with thrombocytopenia syndrome virus infection. Pathog Dis 75: ftx086.
-
17.
Voskoboinik I, Whisstock JC, Trapani JA, 2015. Perforin and granzymes: function, dysfunction and human pathology. Nat Rev Immunol 15: 388–400.
-
18.
Korea Disease Control and Prevention Agency , 2016. SFTS Treatment Guideline. Available at: https://www.ksid.or.kr/rang_board/list.html?num=2531&code=notice3. Accessed May 28, 2023.
-
19.
Novus Biologicals , 2022. Human Granzyme A ELISA Kit (Colorimetric). Available at: https://www.novusbio.com/products/granzyme-a-elisa-kit_nbp3-11790. Accessed May 28, 2023.
-
20.
Novus Biologicals , 2022. Human Perforin ELISA Kit. Available at: https://www.novusbio.com/products/perforin-elisa-kit_nbp3-11726. Accessed May 28, 2023.
-
21.
Novus Biologicals Human Granzyme B Quantikine ELISA Kit. Available at: https://www.novusbio.com/products/human-granzyme-b-quantikine-elisa-kit_dgzb00. Accessed May 28, 2023.
-
22.
Siemens Healthcare GmbH ADVIA 2400 Chemistry System. Available at: https://www.siemens-healthineers.com/clinical-chemistry/systems/advia-2400-chemistry-system. Accessed May 28, 2023.
-
23.
Sysmex , 2023. XE-2100â„¢ Automated Hematology System. Available at: https://www.sysmex.com/la/pt/Products/Documents/English/XE-2100-English.pdf. Accessed May 28, 2023.
-
24.
Kogenbiotech PowerChekâ„¢ Tick-Borne Disease Real-time PCR Kit Series. Available at: https://www.kogene.co.kr/kr/sub/product/infectious_disease/tick-borne_disease/qpcr.asp. Accessed May 28, 2023.
-
25.
Westmeier J et al., 2020. Impaired cytotoxic CD8+ T cell response in elderly COVID-19 patients. mBio 11: e02243.
-
26.
Young JD, Damiano A, DiNome MA, Leong LG, Cohn ZA, 1987. Dissociation of membrane binding and lytic activities of the lymphocyte pore-forming protein (perforin). J Exp Med 165: 1371–1382.
-
27.
Praper T, Besenicar MP, Istinic H, Podlesek Z, Metkar SS, Froelich CJ, Anderluh G, 2010. Human perforin permeabilizing activity, but not binding to lipid membranes, is affected by pH. Mol Immunol 47: 2492–2504.
-
28.
Zhang Q, Zhao J, Dai Y, Jiang Z, Chen T, Hu N, Jin K, Li J, 2023. A high viral load in urine correlates with acute kidney injury and poor outcomes in hospitalized patients with severe fever with thrombocytopenia syndrome: a noninvasive and convenient prognostic marker. Open Forum Infect Dis 10: ofad085.
-
29.
Cook KD, Waggoner SN, Whitmire JK, 2014. NK cells and their ability to modulate T cells during virus infections. Crit Rev Immunol 34: 359–388.
-
30.
Ryu S, Chun JY, Lee S, Yoo D, Kim Y, Ali ST, Chun BC, 2022. Epidemiology and transmission dynamics of infectious diseases and control measures. Viruses 14: 2510.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 2041 | 1174 | 123 |
| Full Text Views | 293 | 68 | 8 |
| PDF Downloads | 115 | 44 | 4 |