Clinical and immunological features of severe and moderate coronavirus disease 2019
Open accessPublished version of a preprint
Abstract
Abstract Background Since late December, 2019, an outbreak of pneumonia cases caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in Wuhan, and continued to spread throughout China and across the globe. To date, few data on immunologic features of Coronavirus Disease 2019 (COVID-19) have been reported. Methods In this single-centre retrospective study, a total of 21 patients with pneumonia who were laboratory-confirmed to be infected with SARS-CoV-2 in Wuhan Tongji hospital were included from Dec 19, 2019 to Jan 27, 2020. The immunologic characteristics as well as their clinical, laboratory, radiological features were compared between 11 severe cases and 10 moderate cases. Results Of the 21 patients with COVID-19, only 4 (19%) had a history of exposure to the Huanan seafood market. 7 (33.3%) patients had underlying conditions. The average age of severe and moderate cases was 63.9 and 51.4 years, 10 (90.9%) severe cases and 7 (70.0%) moderate cases were male. Common clinical manifestations including fever (100%, 100%), cough (70%, 90%), fatigue (100%, 70%) and myalgia (50%, 30%) in severe cases and moderate cases. PaO2/FiO2 ratio was significantly lower in severe cases (122.9) than moderate cases (366.2). Lymphocyte counts were significantly lower in severe cases (0.7 × 10□/L) than moderate cases (1.1 × 10□/L). Alanine aminotransferase, lactate dehydrogenase levels, high-sensitivity C-reactive protein and ferritin were significantly higher in severe cases (41.4 U/L, 567.2 U/L, 135.2 mg/L and 1734.4 ug/L) than moderate cases (17.6 U/L, 234.4 U/L, 51.4 mg/L and 880.2 ug /L). IL-2R, TNF-α and IL-10 concentrations on admission were significantly higher in severe cases (1202.4 pg/mL, 10.9 pg/mL and 10.9 pg/mL) than moderate cases (441.7 pg/mL, 7.5 pg/mL and 6.6 pg/mL). Absolute number of total T lymphocytes, CD4 + T cells and CD8 + T cells decreased in nearly all the patients, and were significantly lower in severe cases (332.5, 185.6 and 124.3 × 10 6 /L) than moderate cases (676.5, 359.2 and 272.0 × 10 6 /L). The expressions of IFN-γ by CD4 + T cells tended to be lower in severe cases (14.6%) than moderate cases (23.6%). Conclusion The SARS-CoV-2 infection may affect primarily T lymphocytes, particularly CD4 + T cells, resulting in significant decrease in number as well as IFN-γ production, which may be associated with disease severity. Together with clinical characteristics, early immunologic indicators including diminished T lymphocytes and elevated cytokines may serve as potential markers for prognosis in COVID-19.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Human recovery from SARS-CoV-2 infection seems to require both antibody and cell-mediated immune responses.
“Recovery following infection with SARS-CoV-2 in humans appears to involve both humoral and cell-mediated immunity22–24.”
From Immunological mechanisms of vaccine-induced protection against COVID-19 in humans (2021) · cites this paper as [24]
Th1 cells producing interferon-γ arise during acute infection, and a Th1-biased response has been proposed to associate with milder disease.
“Interferon-γ (IFNγ)-producing T helper 1 cells (TH1 cells) are produced during acute infection, and it has been suggested that this TH1 cell-biased phenotype is associated with less severe disease24,49”
From Immunological mechanisms of vaccine-induced protection against COVID-19 in humans (2021) · cites this paper as [24]
Patients infected with SARS-CoV-2 present elevated levels of IL-6, IL-10, IL-1β, INF-γ, CCL2, TNF-α, CXCL10, CCL7, IL-1 receptor antagonist and IL-2 receptor, supposedly associated with disease severity.
“Patients infected with SARS-CoV-2 present elevated levels of IL-6, IL-10, IL-1β, INF-γ, CCL2, TNF-α, CXCL10, CCL7, IL-1 receptor antagonist and IL-2 receptor, supposedly associated with disease severity [9, 98–105].”
From Hyperactivation of P2X7 receptors as a culprit of COVID-19 neuropathology (2021) · cites this paper as [101]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A pneumonia outbreak associated with a new coronavirus of probable bat origin
Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., Huang, C.-L., et al. (2020) · Nature · doi:10.1038/s41586-020-2012-7 · Cited by 21,969 · see citing works
Self-citationEarly transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia
Li, Q., Guan, X., Wu, P., Wang, X., Zhou, L., Tong, Y., Ren, R., Leung, K. S. M., Lau, E. H. Y., Wong, J. Y., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001316 · Cited by 16,575 · see citing works
Self-citationPathological findings of COVID-19 associated with acute respiratory distress syndrome
Xu, Z., Shi, L., Wang, Y., Zhang, J., Huang, L., Zhang, C., Liu, S., Zhao, P., Liu, H., Zhu, L., et al. (2020) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(20)30076-x · Cited by 8,545 · see citing works
Self-citationIdentification of a novel coronavirus in patients with severe acute respiratory syndrome
Drosten, C., Günther, S., Preiser, W., van der Werf, S., Brodt, H.-R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., Fouchier, R. A. M., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa030747 · Cited by 4,574 · see citing works
Wan, Y., Shang, J., Graham, R., Baric, R. S., & Li, F. (2020) · Journal of Virology · doi:10.1128/jvi.00127-20 · Cited by 4,341 · see citing works
Chu, H., Zhou, J., Wong, B. H.-Y., Li, C., Chan, J. F.-W., Cheng, Z.-S., Yang, D., Wang, D., Lee, A. C.-Y., Li, C., et al. (2016) · Journal of Infectious Diseases · doi:10.1093/infdis/jiv380 · Cited by 448 · see citing works
Flagged first, then by citations
Research works printed but not linked: 19
- Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367(19):1814-1820. · DOI
- Zhu N, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020;382(8):727-733. · DOI · Paper page
- Gralinski LE, Menachery VD. Return of the coro- navirus: 2019-nCoV. Viruses. 2020;12(2):E135.
- Chan JF, et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indi- cating person-to-person transmission: a study of a family cluster. Lancet. 2020;395(10223):514-523. · DOI
- Huang C, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497-506. · DOI · Paper page
- Chen N, et al. Epidemiological and clinical char- acteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395(10223):507-513. · DOI · Paper page
- Channappanavar R, et al. Dysregulated type I interferon and inflammatory monocyte- macrophage responses cause lethal pneumonia in SARS-CoV-infected Mice. Cell Host Microbe. 2016;19(2):181-193. · DOI
- Venken K, Hellings N, Broekmans T, Hensen K, Rummens JL, Stinissen P. Natural naive CD4 + CD25 + CD127 low regulatory T cell (Treg) development and function are disturbed in mul- tiple sclerosis patients: recovery of memory Treg homeostasis during disease progression. J Immu- nol. 2008;180(9):6411-6420. · DOI
- Xu X, Gao X. Immunological responses against SARS-coronavirus infection in humans. Cell Mol Immunol. 2004;1(2):119-122.
- Frasca L, Piazza C, Piccolella E. CD4 + T cells orchestrate both amplification and deletion of CD8 + T cells. Crit Rev Immunol. 1998;18(6):569-594. · DOI
- Taylor GA, Feng CG, Sher A. p47 GTPases: regu- lators of immunity to intracellular pathogens. Nat Rev Immunol. 2004;4(2):100-109. · DOI
- Arabi YM, et al. Clinical course and outcomes of critically ill patients with Middle East respiratory syndrome coronavirus infection. Ann Intern Med. 2014;160(6):389-397.
- Ying T, Li W, Dimitrov DS. Discovery of T-cell infection and apoptosis by Middle East respi- ratory syndrome coronavirus. J Infect Dis. 2016;213(6):877-879. · DOI
- Chen J, et al. Cellular immune responses to severe acute respiratory syndrome coronavirus (SARS-CoV) infection in senescent BALB/c mice: CD4 + T cells are important in control of SARS- CoV infection. J Virol. 2010;84(3):1289-1301. · DOI
- Zhao JM, et al. [Clinical pathology and patho- genesis of severe acute respiratory syndrome]. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 2003;17(3):217-221.
- Zhao J, et al. Rapid generation of a mouse model for Middle East respiratory syndrome. Proc Natl Acad Sci U S A. 2014;111(13):4970-4975. · DOI
- Li CK, et al. T cell responses to whole SARS coronavirus in humans. J Immunol. 2008;181(8):5490-5500. · DOI
- He Z, et al. Effects of severe acute respiratory syndrome (SARS) coronavirus infection on peripheral blood lymphocytes and their subsets. Int J Infect Dis. 2005;9(6):323-330. · DOI
- Yang M, et al. Hematological findings in SARS patients and possible mechanisms (review). Int J Mol Med. 2004;14(2):311-315.
Cited by
Sorted by citations
Holmes, E. A., O'Connor, R. C., Perry, V. H., Tracey, I., Wessely, S., Arseneault, L., Ballard, C., Christensen, H., Cohen Silver, R., Everall, I., et al. (2020) · The Lancet Psychiatry · doi:10.1016/s2215-0366(20)30168-1 · Cited by 5,715 · see citing works
Nalbandian, A., Sehgal, K., Gupta, A., Madhavan, M. V., McGroder, C., Stevens, J. S., Cook, J. R., Nordvig, A. S., Shalev, D., Sehrawat, T. S., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01283-z · Cited by 4,862 · see citing works
The trinity of COVID-19: immunity, inflammation and intervention
Tay, M. Z., Poh, C. M., Rénia, L., MacAry, P. A., & Ng, L. F. P. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0311-8 · Cited by 4,360 · see citing works
Impaired type I interferon activity and inflammatory responses in severe COVID-19 patients
Hadjadj, J., Yatim, N., Barnabei, L., Corneau, A., Boussier, J., Smith, N., Péré, H., Charbit, B., Bondet, V., Chenevier-Gobeaux, C., et al. (2020) · Science · doi:10.1126/science.abc6027 · Cited by 2,984 · see citing works
Rogers, J. P., Chesney, E., Oliver, D., Pollak, T. A., McGuire, P., Fusar-Poli, P., Zandi, M. S., Lewis, G., & David, A. S. (2020) · The Lancet Psychiatry · doi:10.1016/s2215-0366(20)30203-0 · Cited by 2,407 · see citing works
Pathological inflammation in patients with COVID-19: a key role for monocytes and macrophages
Merad, M., & Martin, J. C. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0331-4 · Cited by 2,472 · see citing works
Longitudinal analyses reveal immunological misfiring in severe COVID-19
Lucas, C., Wong, P., Klein, J., Castro, T. B. R., Silva, J., Sundaram, M., Ellingson, M. K., Mao, T., Oh, J. E., Israelow, B., et al. (2020) · Nature · doi:10.1038/s41586-020-2588-y · Cited by 2,074 · see citing works
Self-citationRydyznski Moderbacher, C., Ramirez, S. I., Dan, J. M., Grifoni, A., Hastie, K. M., Weiskopf, D., Belanger, S., Abbott, R. K., Kim, C., Choi, J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.038 · Cited by 1,790 · see citing works
“001; Figures S5A–S5C) and correlated with disease severity (Figure 5A), consistent with large cohort studies of plasma cytokines (Chen et al., 2020; Laing et al., 2020; Mathew et al., 2020; Yang et al., 2020).”
Cytokine release syndrome in severe COVID-19
Moore, J. B., & June, C. H. (2020) · Science · doi:10.1126/science.abb8925 · Cited by 1,912 · see citing works
McGonagle, D., Sharif, K., O'Regan, A., & Bridgewood, C. (2020) · Autoimmunity Reviews · doi:10.1016/j.autrev.2020.102537 · Cited by 1,654 · see citing works
A single-cell atlas of the peripheral immune response in patients with severe COVID-19
Wilk, A. J., Rustagi, A., Zhao, N. Q., Roque, J., Martínez-Colón, G. J., McKechnie, J. L., Ivison, G. T., Ranganath, T., Vergara, R., Hollis, T., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0944-y · Cited by 1,493 · see citing works
Mathew, D., Giles, J. R., Baxter, A. E., Oldridge, D. A., Greenplate, A. R., Wu, J. E., Alanio, C., Kuri-Cervantes, L., Pampena, M. B., D’Andrea, K., et al. (2020) · Science · doi:10.1126/science.abc8511 · Cited by 1,509 · see citing works
Severe COVID-19 Is Marked by a Dysregulated Myeloid Cell Compartment
Schulte-Schrepping, J., Reusch, N., Paclik, D., Baßler, K., Schlickeiser, S., Zhang, B., Krämer, B., Krammer, T., Brumhard, S., Bonaguro, L., et al. (2020) · Cell · doi:10.1016/j.cell.2020.08.001 · Cited by 1,461 · see citing works
Immunology of COVID-19: Current State of the Science
Vabret, N., Britton, G. J., Gruber, C., Hegde, S., Kim, J., Kuksin, M., Levantovsky, R., Malle, L., Moreira, A., Park, M. D., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.05.002 · Cited by 1,623 · see citing works
Targeting potential drivers of COVID-19: Neutrophil extracellular traps
Barnes, B. J., Adrover, J. M., Baxter-Stoltzfus, A., Borczuk, A., Cools-Lartigue, J., Crawford, J. M., Daßler-Plenker, J., Guerci, P., Huynh, C., Knight, J. S., et al. (2020) · Journal of Experimental Medicine · doi:10.1084/jem.20200652 · Cited by 1,486 · see citing works
Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans
Arunachalam, P. S., Wimmers, F., Mok, C. K. P., Perera, R. A. P. M., Scott, M., Hagan, T., Sigal, N., Feng, Y., Bristow, L., Tak-Yin Tsang, O., et al. (2020) · Science · doi:10.1126/science.abc6261 · Cited by 1,186 · see citing works
Coperchini, F., Chiovato, L., Croce, L., Magri, F., & Rotondi, M. (2020) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2020.05.003 · Cited by 1,288 · see citing works
Popkin, B. M., Du, S., Green, W. D., Beck, M. A., Algaith, T., Herbst, C. H., Alsukait, R. F., Alluhidan, M., Alazemi, N., & Shekar, M. (2020) · Obesity Reviews · doi:10.1111/obr.13128 · Cited by 1,150 · see citing works
Cytokine Storm in COVID-19: The Current Evidence and Treatment Strategies
Tang, Y., Liu, J., Zhang, D., Xu, Z., Ji, J., & Wen, C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01708 · Cited by 1,094 · see citing works
Pedersen, S. F., & Ho, Y.-C. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137647 · Cited by 1,137 · see citing works
Aging in COVID-19: Vulnerability, immunity and intervention
Chen, Y., Klein, S. L., Garibaldi, B. T., Li, H., Wu, C., Osevala, N. M., Li, T., Margolick, J. B., Pawelec, G., & Leng, S. X. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101205 · Cited by 1,007 · see citing works
Elevated Calprotectin and Abnormal Myeloid Cell Subsets Discriminate Severe from Mild COVID-19
Silvin, A., Chapuis, N., Dunsmore, G., Goubet, A.-G., Dubuisson, A., Derosa, L., Almire, C., Hénon, C., Kosmider, O., Droin, N., et al. (2020) · Cell · doi:10.1016/j.cell.2020.08.002 · Cited by 834 · see citing works
Townsend, L., Dyer, A. H., Jones, K., Dunne, J., Mooney, A., Gaffney, F., O'Connor, L., Leavy, D., O'Brien, K., Dowds, J., et al. (2020) · PLOS ONE · doi:10.1371/journal.pone.0240784 · Cited by 911 · see citing works
Winkler, E. S., Bailey, A. L., Kafai, N. M., Nair, S., McCune, B. T., Yu, J., Fox, J. M., Chen, R. E., Earnest, J. T., Keeler, S. P., et al. (2020) · Nature Immunology · doi:10.1038/s41590-020-0778-2 · Cited by 901 · see citing works
Rodrigues, T. S., de Sá, K. S. G., Ishimoto, A. Y., Becerra, A., Oliveira, S., Almeida, L., Gonçalves, A. V., Perucello, D. B., Andrade, W. A., Castro, R., et al. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20201707 · Cited by 839 · see citing works
Weiskopf, D., Schmitz, K. S., Raadsen, M. P., Grifoni, A., Okba, N. M. A., Endeman, H., van den Akker, J. P. C., Molenkamp, R., Koopmans, M. P. G., van Gorp, E. C. M., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abd2071 · Cited by 907 · see citing works
Single-cell multi-omics analysis of the immune response in COVID-19
Cambridge Institute of Therapeutic Immunology and Infectious Disease-National Institute of Health Research (CITIID-NIHR) COVID-19 BioResource Collaboration, Stephenson, E., Reynolds, G., Botting, R. A., Calero-Nieto, F. J., Morgan, M. D., Tuong, Z. K., Bach, K., Sungnak, W., Worlock, K. B., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01329-2 · Cited by 742 · see citing works
De Biasi, S., Meschiari, M., Gibellini, L., Bellinazzi, C., Borella, R., Fidanza, L., Gozzi, L., Iannone, A., Lo Tartaro, D., Mattioli, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17292-4 · Cited by 789 · see citing works
Tan, A. T., Linster, M., Tan, C. W., Le Bert, N., Chia, W. N., Kunasegaran, K., Zhuang, Y., Tham, C. Y. L., Chia, A., Smith, G. J. D., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108728 · Cited by 740 · see citing works
Comprehensive mapping of immune perturbations associated with severe COVID-19
Kuri-Cervantes, L., Pampena, M. B., Meng, W., Rosenfeld, A. M., Ittner, C. A. G., Weisman, A. R., Agyekum, R. S., Mathew, D., Baxter, A. E., Vella, L. A., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abd7114 · Cited by 723 · see citing works
Immune cell profiling of COVID-19 patients in the recovery stage by single-cell sequencing
Wen, W., Su, W., Tang, H., Le, W., Zhang, X., Zheng, Y., Liu, X., Xie, L., Li, J., Ye, J., et al. (2020) · Cell Discovery · doi:10.1038/s41421-020-0168-9 · Cited by 730 · see citing works
Self-citationT cell responses in patients with COVID-19
Chen, Z., & John Wherry, E. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0402-6 · Cited by 797 · see citing works
Immune response, inflammation, and the clinical spectrum of COVID-19
García, L. F. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01441 · Cited by 739 · see citing works
The hypercoagulable state in COVID-19: Incidence, pathophysiology, and management
Abou-Ismail, M. Y., Diamond, A., Kapoor, S., Arafah, Y., & Nayak, L. (2020) · Thrombosis Research · doi:10.1016/j.thromres.2020.06.029 · Cited by 694 · see citing works
How COVID-19 induces cytokine storm with high mortality
Hojyo, S., Uchida, M., Tanaka, K., Hasebe, R., Tanaka, Y., Murakami, M., & Hirano, T. (2020) · Inflammation and Regeneration · doi:10.1186/s41232-020-00146-3 · Cited by 663 · see citing works
Immunological mechanisms of vaccine-induced protection against COVID-19 in humans
Sadarangani, M., Marchant, A., & Kollmann, T. R. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-021-00578-z · Cited by 560 · see citing works
Heneka, M. T., Golenbock, D., Latz, E., Morgan, D., & Brown, R. (2020) · Alzheimer's Research & Therapy · doi:10.1186/s13195-020-00640-3 · Cited by 555 · see citing works
Impaired immune cell cytotoxicity in severe COVID-19 is IL-6 dependent
Mazzoni, A., Salvati, L., Maggi, L., Capone, M., Vanni, A., Spinicci, M., Mencarini, J., Caporale, R., Peruzzi, B., Antonelli, A., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci138554 · Cited by 502 · see citing works
Galani, I.-E., Rovina, N., Lampropoulou, V., Triantafyllia, V., Manioudaki, M., Pavlos, E., Koukaki, E., Fragkou, P. C., Panou, V., Rapti, V., et al. (2021) · Nature Immunology · doi:10.1038/s41590-020-00840-x · Cited by 503 · see citing works
Immunopathology of Hyperinflammation in COVID-19
Gustine, J. N., & Jones, D. (2021) · The American Journal of Pathology · doi:10.1016/j.ajpath.2020.08.009 · Cited by 516 · see citing works
CD8+ T cells contribute to survival in patients with COVID-19 and hematologic cancer
Bange, E. M., Han, N. A., Wileyto, P., Kim, J. Y., Gouma, S., Robinson, J., Greenplate, A. R., Hwee, M. A., Porterfield, F., Owoyemi, O., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01386-7 · Cited by 519 · see citing works
Bajaj, V., Gadi, N., Spihlman, A. P., Wu, S. C., Choi, C. H., & Moulton, V. R. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2020.571416 · Cited by 476 · see citing works
Self-citationSARS-CoV-2 triggers inflammatory responses and cell death through caspase-8 activation
Li, S., Zhang, Y., Guan, Z., Li, H., Ye, M., Chen, X., Shen, J., Zhou, Y., Shi, Z.-L., Zhou, P., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00334-0 · Cited by 365 · see citing works
Self-citationVeiga, V. C., Prats, J. A. G. G., Farias, D. L. C., Rosa, R. G., Dourado, L. K., Zampieri, F. G., Machado, F. R., Lopes, R. D., Berwanger, O., Azevedo, L. C. P., et al. (2021) · BMJ · doi:10.1136/bmj.n84 · Cited by 388 · see citing works
Local and systemic responses to SARS-CoV-2 infection in children and adults
Yoshida, M., Worlock, K. B., Huang, N., Lindeboom, R. G. H., Butler, C. R., Kumasaka, N., Dominguez Conde, C., Mamanova, L., Bolt, L., Richardson, L., et al. (2022) · Nature · doi:10.1038/s41586-021-04345-x · Cited by 365 · see citing works
Distinct Early Serological Signatures Track with SARS-CoV-2 Survival
Atyeo, C., Fischinger, S., Zohar, T., Slein, M. D., Burke, J., Loos, C., McCulloch, D. J., Newman, K. L., Wolf, C., Yu, J., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.020 · Cited by 349 · see citing works
Recent endemic coronavirus infection is associated with less severe COVID-19
Sagar, M., Reifler, K., Rossi, M., Miller, N. S., Sinha, P., White, L. F., & Mizgerd, J. P. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143380 · Cited by 324 · see citing works
Lessons for COVID-19 immunity from other coronavirus infections
Sariol, A., & Perlman, S. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.005 · Cited by 317 · see citing works
Ravindra, N. G., Alfajaro, M. M., Gasque, V., Huston, N. C., Wan, H., Szigeti-Buck, K., Yasumoto, Y., Greaney, A. M., Habet, V., Chow, R. D., et al. (2021) · PLOS Biology · doi:10.1371/journal.pbio.3001143 · Cited by 258 · see citing works
Disease severity-specific neutrophil signatures in blood transcriptomes stratify COVID-19 patients
(DeCOI), G. C.-1. O. I., Aschenbrenner, A. C., Mouktaroudi, M., Krämer, B., Oestreich, M., Antonakos, N., Nuesch-Germano, M., Gkizeli, K., Bonaguro, L., Reusch, N., et al. (2021) · Genome Medicine · doi:10.1186/s13073-020-00823-5 · Cited by 255 · see citing works
Two distinct immunopathological profiles in autopsy lungs of COVID-19
Nienhold, R., Ciani, Y., Koelzer, V. H., Tzankov, A., Haslbauer, J. D., Menter, T., Schwab, N., Henkel, M., Frank, A., Zsikla, V., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18854-2 · Cited by 246 · see citing works
Adverse effects of COVID-19 mRNA vaccines: the spike hypothesis
Trougakos, I. P., Terpos, E., Alexopoulos, H., Politou, M., Paraskevis, D., Scorilas, A., Kastritis, E., Andreakos, E., & Dimopoulos, M. A. (2022) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2022.04.007 · Cited by 273 · see citing works
Ovsyannikova, I. G., Haralambieva, I. H., Crooke, S. N., Poland, G. A., & Kennedy, R. B. (2020) · Immunological Reviews · doi:10.1111/imr.12897 · Cited by 258 · see citing works
Vanderbeke, L., Van Mol, P., Van Herck, Y., De Smet, F., Humblet-Baron, S., Martinod, K., Antoranz, A., Arijs, I., Boeckx, B., Bosisio, F. M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24360-w · Cited by 247 · see citing works
Prospects for a safe COVID-19 vaccine
Haynes, B. F., Corey, L., Fernandes, P., Gilbert, P. B., Hotez, P. J., Rao, S., Santos, M. R., Schuitemaker, H., Watson, M., & Arvin, A. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.abe0948 · Cited by 261 · see citing works
Pathogenesis of COVID-19-induced ARDS: implications for an ageing population
Torres Acosta, M. A., & Singer, B. D. (2020) · European Respiratory Journal · doi:10.1183/13993003.02049-2020 · Cited by 247 · see citing works
Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection
Desai, N., Neyaz, A., Szabolcs, A., Shih, A. R., Chen, J. H., Thapar, V., Nieman, L. T., Solovyov, A., Mehta, A., Lieb, D. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-20139-7 · Cited by 245 · see citing works
Vascular Disease and Thrombosis in SARS-CoV-2-Infected Rhesus Macaques
Aid, M., Busman-Sahay, K., Vidal, S. J., Maliga, Z., Bondoc, S., Starke, C., Terry, M., Jacobson, C. A., Wrijil, L., Ducat, S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.005 · Cited by 215 · see citing works
Dorjee, K., Kim, H., Bonomo, E., & Dolma, R. (2020) · PLOS ONE · doi:10.1371/journal.pone.0243191 · Cited by 216 · see citing works
SARS–CoV-2–specific T cell responses and correlations with COVID-19 patient predisposition
Sattler, A., Angermair, S., Stockmann, H., Heim, K. M., Khadzhynov, D., Treskatsch, S., Halleck, F., Kreis, M. E., & Kotsch, K. (2020) · Journal of Clinical Investigation · doi:10.1172/jci140965 · Cited by 196 · see citing works
Psycho-Neuroendocrine-Immune Interactions in COVID-19: Potential Impacts on Mental Health
Raony, Í., de Figueiredo, C. S., Pandolfo, P., Giestal-de-Araujo, E., Oliveira-Silva Bomfim, P., & Savino, W. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01170 · Cited by 185 · see citing works
Diagnosing COVID-19-associated pulmonary aspergillosis
Verweij, P. E., Gangneux, J.-P., Bassetti, M., Brüggemann, R. J. M., Cornely, O. A., Koehler, P., Lass-Flörl, C., van de Veerdonk, F. L., Chakrabarti, A., & Hoenigl, M. (2020) · The Lancet Microbe · doi:10.1016/s2666-5247(20)30027-6 · Cited by 181 · see citing works
The Effect of the COVID-19 Pandemic on People with Parkinson’s Disease
Brown, E. G., Chahine, L. M., Goldman, S. M., Korell, M., Mann, E., Kinel, D. R., Arnedo, V., Marek, K. L., & Tanner, C. M. (2020) · Journal of Parkinson's Disease · doi:10.3233/jpd-202249 · Cited by 177 · see citing works
SARS-CoV-2 infection, COVID-19 pathogenesis, and exposure to air pollution: What is the connection?
Woodby, B., Arnold, M. M., & Valacchi, G. (2021) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14512 · Cited by 160 · see citing works
The known unknowns of T cell immunity to COVID-19
Karlsson, A. C., Humbert, M., & Buggert, M. (2020) · Science Immunology · doi:10.1126/sciimmunol.abe8063 · Cited by 165 · see citing works
SARS-CoV-2-specific T cells in infection and vaccination
Bertoletti, A., Le Bert, N., Qui, M., & Tan, A. T. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-021-00743-3 · Cited by 159 · see citing works
Hyperactivation of P2X7 receptors as a culprit of COVID-19 neuropathology
Ribeiro, D. E., Oliveira-Giacomelli, Á., Glaser, T., Arnaud-Sampaio, V. F., Andrejew, R., Dieckmann, L., Baranova, J., Lameu, C., Ratajczak, M. Z., & Ulrich, H. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00965-3 · Cited by 145 · see citing works
Effect of Systemic Glucocorticoids on Mortality or Mechanical Ventilation in Patients With COVID-19
Keller, M. J., Kitsis, E. A., Arora, S., Chen, J.-T., Agarwal, S., Ross, M. J., Tomer, Y., & Southern, W. (2020) · Journal of Hospital Medicine · doi:10.12788/jhm.3497 · Cited by 146 · see citing works
Kadambari, S., Klenerman, P., & Pollard, A. J. (2020) · Reviews in Medical Virology · doi:10.1002/rmv.2144 · Cited by 118 · see citing works
Brough, H. A., Kalayci, O., Sediva, A., Untersmayr, E., Munblit, D., Rodriguez del Rio, P., Vazquez‐Ortiz, M., Arasi, S., Alvaro‐Lozano, M., Tsabouri, S., et al. (2020) · Pediatric Allergy and Immunology · doi:10.1111/pai.13262 · Cited by 111 · see citing works
Magusali, N., Graham, A. C., Piers, T. M., Panichnantakul, P., Yaman, U., Shoai, M., Reynolds, R. H., Botia, J. A., Brookes, K. J., Guetta-Baranes, T., et al. (2021) · Brain · doi:10.1093/brain/awab337 · Cited by 111 · see citing works
COVID-19: Review of a 21st Century Pandemic from Etiology to Neuro-psychiatric Implications
Yamamoto, V., Bolanos, J. F., Fiallos, J., Strand, S. E., Morris, K., Shahrokhinia, S., Cushing, T. R., Hopp, L., Tiwari, A., Hariri, R., et al. (2020) · Journal of Alzheimer's Disease · doi:10.3233/jad-200831 · Cited by 100 · see citing works
Biomarkers of post-covid depression
Lorkiewicz, P., & Waszkiewicz, N. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10184142 · Cited by 102 · see citing works
Chambers, E. S., Vukmanovic-Stejic, M., Shih, B. B., Trahair, H., Subramanian, P., Devine, O. P., Glanville, J., Gilroy, D., Rustin, M. H. A., Freeman, T. C., et al. (2021) · Nature Aging · doi:10.1038/s43587-020-00010-6 · Cited by 96 · see citing works
Costagliola, G., Spada, E., & Consolini, R. (2021) · Immunity, Inflammation and Disease · doi:10.1002/iid3.404 · Cited by 81 · see citing works
Aviv, A. (2020) · The FASEB Journal · doi:10.1096/fj.202001025 · Cited by 73 · see citing works
Wang, Y., Zheng, J., Islam, M. S., Yang, Y., Hu, Y., & Chen, X. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.59534 · Cited by 71 · see citing works
MSC-NTF (NurOwn®) exosomes: a novel therapeutic modality in the mouse LPS-induced ARDS model
Kaspi, H., Semo, J., Abramov, N., Dekel, C., Lindborg, S., Kern, R., Lebovits, C., & Aricha, R. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02143-w · Cited by 68 · see citing works
The dark side of Tregs during aging
Palatella, M., Guillaume, S. M., Linterman, M. A., & Huehn, J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.940705 · Cited by 58 · see citing works
Shinde, T., Hansbro, P. M., Sohal, S. S., Dingle, P., Eri, R., & Stanley, R. (2020) · Microorganisms · doi:10.3390/microorganisms8060921 · Cited by 61 · see citing works
Deficiency of Tfh Cells and Germinal Center in Deceased COVID-19 Patients
Duan, Y.-Q., Xia, M.-H., Ren, L., Zhang, Y.-F., Ao, Q.-L., Xu, S.-P., Kuang, D., Liu, Q., Yan, B., Zhou, Y.-W., et al. (2020) · Current Medical Science · doi:10.1007/s11596-020-2225-x · Cited by 59 · see citing works
COVID-19: more than a cytokine storm
Riva, G., Nasillo, V., Tagliafico, E., Trenti, T., Comoli, P., & Luppi, M. (2020) · Critical Care · doi:10.1186/s13054-020-03267-w · Cited by 46 · see citing works
COVID-19 e Estado de Hipercoagulabilidade: Uma Nova Perspectiva Terapêutica
Nascimento, J. H. P., Gomes, B. F. D. O., Carmo, P. R. D., Petriz, J. L. F., Rizk, S. I., Costa, I. B. S. D. S., Lacerda, M. V. G., Bacal, F., Hajjar, L. A., & Oliveira, G. M. M. D. (2020) · Arquivos Brasileiros de Cardiologia · doi:10.36660/abc.20200308 · Cited by 47 · see citing works
Excess cerebrovascular mortality in the united states during the COVID-19 pandemic
Sharma, R., Kuohn, L. R., Weinberger, D. M., Warren, J. L., Sansing, L. H., Jasne, A., Falcone, G., Dhand, A., & Sheth, K. N. (2021) · Stroke · doi:10.1161/strokeaha.120.031975 · Cited by 46 · see citing works
Lafon, E., Diem, G., Witting, C., Zaderer, V., Bellmann-Weiler, R. M., Reindl, M., Bauer, A., Griesmacher, A., Fux, V., Hoermann, G., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.684014 · Cited by 46 · see citing works
Excess body weight is an independent risk factor for severe forms of COVID-19
Pietri, L., Giorgi, R., Bégu, A., Lojou, M., Koubi, M., Cauchois, R., Grangeot, R., Dubois, N., Kaplanski, G., Valéro, R., et al. (2021) · Metabolism · doi:10.1016/j.metabol.2021.154703 · Cited by 35 · see citing works
Nouveau, L., Buatois, V., Cons, L., Chatel, L., Pontini, G., Pleche, N., & Ferlin, W. G. (2021) · European Journal of Immunology · doi:10.1002/eji.202149181 · Cited by 25 · see citing works
Dysfunctional purinergic signaling correlates with disease severity in COVID-19 patients
Pietrobon, A. J., Andrejew, R., Custódio, R. W. A., Oliveira, L. D. M., Scholl, J. N., Teixeira, F. M. E., de Brito, C. A., Glaser, T., Kazmierski, J., Goffinet, C., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1012027 · Cited by 23 · see citing works
SARS-CoV-2 INFECTED PATIENTS: FROM A HEMATOLOGIST PERSPECTIVE: COVID-19 and Hematology
Kreidieh, F., & Temraz, S. (2020) · Mediterranean Journal of Hematology and Infectious Diseases · doi:10.4084/mjhid.2020.078 · Cited by 7 · see citing works
Mansour, H. M. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102195 · Cited by 3 · see citing works
- Authors
- Chen, G., Wu, D., Guo, W., Cao, Y., Huang, D., Wang, H., Wang, T., Zhang, X., Chen, H., Yu, H., Zhang, X., Zhang, M., Wu, S., Song, J., Chen, T., Han, M., Li, S., Luo, X., Zhao, J., & Ning, Q.
- Affiliations
- Tongji Hospital (CN)
- Corresponding author
- Ning, Qin
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2020-04-13
- Volume
- 130
- Issue
- 5
- Pages
- 2620-2629
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC7190990
- OpenAlex
- W3014003872
- Cited by
- 4,750
- References
- 6
- Citations by year
- 2026: 63 · 2025: 159 · 2024: 317 · 2023: 531 · 2022: 869 · 2021: 1402 · 2020: 1398 · 2019: 2 · 2018: 1 · 2017: 1 · 2015: 1 · 2013: 3 · 2012: 1
- FWCI
- 138.43
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- medRxiv (acceptedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Tongji Hospital for Pilot Scheme Project (Tongji Hospital for Pilot Scheme Project)
- the Chinese National Thirteenth Five Years Project in Science and Technology (2017ZX10202201)
- Topics
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Neurology › Long-Term Effects of COVID-19
- Keywords
- COVID-19 pandemic, SARS-CoV-2, disease severity, T cells, CD4+ T cells, CD8+ T cells, interferon-gamma, cytokines, lymphopenia, hypoalbuminemia, immunological markers, clinical features, D-dimer, ferritin, C-reactive protein, lactate dehydrogenase, alanine aminotransferase
- MeSH terms
- COVID-19, Adult, Aged, Cell Count, China, Female, Gene Expression Regulation, Humans, Male, Middle Aged, Pneumonia, Viral, Retrospective Studies, Severity of Illness Index, T-Lymphocytes, Cytokines, Coronavirus Infections, Gene Expression Profiling, Pandemics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review