COVID-19 Pathology in the Lung, Kidney, Heart and Brain: The Different Roles of T-Cells, Macrophages, and Microthrombosis
Open accessAbstract
Here, we aim to describe COVID-19 pathology across different tissues to clarify the disease’s pathophysiology. Lungs, kidneys, hearts, and brains from nine COVID-19 autopsies were compared by using antibodies against SARS-CoV-2, macrophages-microglia, T-lymphocytes, B-lymphocytes, and activated platelets. Alzheimer’s Disease pathology was also assessed. PCR techniques were used to verify the presence of viral RNA. COVID-19 cases had a short clinical course (0–32 days) and their mean age was 77.4 y/o. Hypoxic changes and inflammatory infiltrates were present across all tissues. The lymphocytic component in the lungs and kidneys was predominant over that of other tissues (p < 0.001), with a significantly greater presence of T-lymphocytes in the lungs (p = 0.020), which showed the greatest presence of viral antigens. The heart showed scant SARS-CoV-2 traces in the endothelium–endocardium, foci of activated macrophages, and rare lymphocytes. The brain showed scarce SARS-CoV-2 traces, prominent microglial activation, and rare lymphocytes. The pons exhibited the highest microglial activation (p = 0.017). Microthrombosis was significantly higher in COVID-19 lungs (p = 0.023) compared with controls. The most characteristic pathological features of COVID-19 were an abundance of T-lymphocytes and microthrombosis in the lung and relevant microglial hyperactivation in the brainstem. This study suggests that the long-term sequelae of COVID-19 derive from persistent inflammation, rather than persistent viral replication.
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The SARS-CoV-2 genome has been detected by PCR in cardiac tissues from autopsies of patients with COVID-19, suggesting the virus can infect the heart.
“The SARS-CoV-2 genome has been detected by polymerase chain reaction (PCR) in cardiac tissues from autopsies of patients with COVID-19, 20,21 suggesting the virus can infect the heart.”
From COVID-19, Myocarditis and Pericarditis (2023) · cites this paper as [21]
The Results (p. 9) report SARS-CoV-2 traces in heart tissue from one autopsy case, and the Discussion (p. 16) says the virus probably penetrates the heart. But the Methods (p. 4) describe PCR testing of brain tissue, not cardiac tissue; this paper does not establish the claimed PCR detection in the heart and says it found no evidence of viral replication there. (LLM, conf=0.87)
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Endothelial cell infection and endotheliitis in COVID-19
Varga, Z., Flammer, A. J., Steiger, P., Haberecker, M., Andermatt, R., Zinkernagel, A. S., Mehra, M. R., Schuepbach, R. A., Ruschitzka, F., & Moch, H. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30937-5 · Cited by 6,358 · see citing works
Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19
Ackermann, M., Verleden, S. E., Kuehnel, M., Haverich, A., Welte, T., Laenger, F., Vanstapel, A., Werlein, C., Stark, H., Tzankov, A., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2015432 · Cited by 5,613 · see citing works
Characteristics of SARS-CoV-2 and COVID-19
Hu, B., Guo, H., Zhou, P., & Shi, Z.-L. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00459-7 · Cited by 5,291 · 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
Cardiovascular implications of fatal outcomes of patients with Coronavirus Disease 2019 (COVID-19)
Guo, T., Fan, Y., Chen, M., Wu, X., Zhang, L., He, T., Wang, H., Wan, J., Wang, X., & Lu, Z. (2020) · JAMA Cardiology · doi:10.1001/jamacardio.2020.1017 · Cited by 4,194 · see citing works
Montine, T. J., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E., Mirra, S. S., et al. (2012) · Acta Neuropathologica · doi:10.1007/s00401-011-0910-3 · Cited by 2,992 · cited 1× · see citing works
“Alzheimer’s Disease (AD) severity was assessed on sections immunostained with antibodies against beta-amyloid (4G8, monoclonal antibody, BioLegend San Diego, CA, USA; 1:1000) and phospho-tau (AT8, monoclonal antibody, clone MN1020, Thermo Fisher Scientific Waltham, MA, USA; 1:200) and defined according to Montine’s sc…”
MethodBaig, A. M., Khaleeq, A., Ali, U., & Syeda, H. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00122 · Cited by 2,207 · see citing works
Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China
Su, H., Yang, M., Wan, C., Yi, L.-X., Tang, F., Zhu, H.-Y., Yi, F., Yang, H.-C., Fogo, A. B., Nie, X., et al. (2020) · Kidney International · doi:10.1016/j.kint.2020.04.003 · Cited by 1,763 · see citing works
The COVID-19 Cytokine Storm; What We Know So Far
Ragab, D., Salah-ElDin, H., Taeimah, M., Khattab, R., & Salem, R. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01446 · Cited by 1,624 · see citing works
CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells
Wang, K., Chen, W., Zhang, Z., Deng, Y., Lian, J., Du, P. F., Wei, D., Yang, Z., Sun, X., Gong, L., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00426-x · Cited by 1,592 · see citing works
Fox, S., Akmatbekov, A., Harbert, J. L., Li, G., Brown, J. Q., & Heide, R. S. V. (2020) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(20)30243-5 · Cited by 1,524 · see citing works
Meinhardt, J., Radke, J., Dittmayer, C., Franz, J., Thomas, C., Mothes, R., Laue, M., Schneider, J., Brünink, S., Greuel, S., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-020-00758-5 · Cited by 1,458 · see citing works
The SARS-CoV-2 outbreak: What we know
Wu, D., Wu, T., Liu, Q., & Yang, Z. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.03.004 · Cited by 1,424 · see citing works
Neuropathology of patients with COVID-19 in Germany: a post-mortem case series
Matschke, J., Lütgehetmann, M., Hagel, C., Sperhake, J. P., Schröder, A. S., Edler, C., Mushumba, H., Fitzek, A., Allweiss, L., Dandri, M., et al. (2020) · The Lancet Neurology · doi:10.1016/s1474-4422(20)30308-2 · Cited by 1,300 · see citing works
Menter, T., Haslbauer, J. D., Nienhold, R., Savic, S., Hopfer, H., Deigendesch, N., Frank, S., Turek, D., Willi, N., Pargger, H., et al. (2020) · Histopathology · doi:10.1111/his.14134 · Cited by 1,207 · see citing works
Why does COVID-19 disproportionately affect older people?
Mueller, A. L., McNamara, M. S., & Sinclair, D. A. (2020) · Aging · doi:10.18632/aging.103344 · Cited by 1,128 · see citing works
Hosts and Sources of Endemic Human Coronaviruses
Corman, V. M., Muth, D., Niemeyer, D., & Drosten, C. (2018) · Advances in virus research · doi:10.1016/bs.aivir.2018.01.001 · Cited by 988 · see citing works
Raveendran, A. V., Jayadevan, R., & Sashidharan, S. (2021) · Diabetes & Metabolic Syndrome: Clinical Research & Reviews · doi:10.1016/j.dsx.2021.04.007 · Cited by 921 · see citing works
Beyerstedt, S., Casaro, E. B., & Rangel, É. B. (2021) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-020-04138-6 · Cited by 897 · see citing works
Association of Cardiac Infection With SARS-CoV-2 in Confirmed COVID-19 Autopsy Cases
Lindner, D., Fitzek, A., Bräuninger, H., Aleshcheva, G., Edler, C., Meissner, K., Scherschel, K., Kirchhof, P., Escher, F., Schultheiss, H.-P., et al. (2020) · JAMA Cardiology · doi:10.1001/jamacardio.2020.3551 · Cited by 827 · see citing works
Cytokine storm in COVID-19: pathogenesis and overview of anti-inflammatory agents used in treatment
Soy, M., Keser, G., Atagündüz, P., Tabak, F., Atagündüz, I., & Kayhan, S. (2020) · Clinical Rheumatology · doi:10.1007/s10067-020-05190-5 · Cited by 821 · see citing works
Neuropathological features of Covid-19
Solomon, I. H., Normandin, E., Bhattacharyya, S., Mukerji, S. S., Keller, K., Ali, A. S., Adams, G., Hornick, J. L., Padera, R. F., & Sabeti, P. (2020) · New England Journal of Medicine · doi:10.1056/nejmc2019373 · Cited by 815 · see citing works
Bradley, B. T., Maioli, H., Johnston, R., Chaudhry, I., Fink, S. L., Xu, H., Najafian, B., Deutsch, G. H., Lacy, J. M., Williams, T., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)31305-2 · Cited by 814 · see citing works
Cognitive deficits in people who have recovered from COVID-19
Hampshire, A., Trender, W. R., Chamberlain, S. R., Jolly, A., Grant, J. E., Patrick, F., Mazibuko, N., Williams, S., Barnby, J. M., Hellyer, P. J., et al. (2021) · EClinicalMedicine · doi:10.1016/j.eclinm.2021.101044 · Cited by 704 · see citing works
Effects of COVID-19 on the Nervous System
Iadecola, C., Anrather, J., & Kamel, H. (2020) · Cell · doi:10.1016/j.cell.2020.08.028 · Cited by 663 · see citing works
Zhu, Z., Lian, X., Su, X., Wu, W., Marraro, G. A., & Zeng, Y. (2020) · Respiratory Research · doi:10.1186/s12931-020-01479-w · Cited by 614 · see citing works
Iba, T., Levy, J. H., Levi, M. M., & Thachil, J. V. (2020) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14975 · Cited by 594 · see citing works
The Emerging Threat of (Micro)Thrombosis in COVID-19 and Its Therapeutic Implications
McFadyen, J. D., Stevens, H., & Peter, K. (2020) · Circulation Research · doi:10.1161/circresaha.120.317447 · Cited by 592 · see citing works
Microvascular injury in the brains of patients with Covid-19
Lee, M.-H., Perl, D. P., Nair, G., Li, W., Maric, D., Murray, H., Dodd, S. J., Koretsky, A. P., Watts, J. A., Cheung, V., et al. (2021) · New England Journal of Medicine · doi:10.1056/nejmc2033369 · Cited by 562 · see citing works
Pan, X., Xu, D., Zhang, H., Zhou, W., Wang, L., & Cui, X. (2020) · Intensive Care Medicine · doi:10.1007/s00134-020-06026-1 · Cited by 558 · see citing works
Postmortem Examination of Patients With COVID-19
Schaller, T., Hirschbühl, K., Burkhardt, K., Braun, G., Trepel, M., Märkl, B., & Claus, R. (2020) · JAMA · doi:10.1001/jama.2020.8907 · Cited by 557 · see citing works
Hanley, B. P., Naresh, K. N., Roufosse, C. A., Nicholson, A. G., Weir, J., Cooke, G., Thursz, M. R., Manousou, P., Corbett, R., Goldin, R. D., et al. (2020) · The Lancet Microbe · doi:10.1016/s2666-5247(20)30115-4 · Cited by 536 · see citing works
Schurink, B., Roos, E., Radonic, T. R., Barbé, E., Bouman, C. S. C., de Boer, H. H., de Bree, G. J., Bulle, E., Aronica, E., Florquin, S., et al. (2020) · The Lancet Microbe · doi:10.1016/s2666-5247(20)30144-0 · Cited by 505 · see citing works
Zhang, Y., Zheng, L., Liu, L., Zhao, M., Xiao, J., & Zhao, Q. (2020) · Liver International · doi:10.1111/liv.14455 · Cited by 496 · see citing works
Reichard, R. R., Kashani, K. B., Boire, N. A., Constantopoulos, E., Guo, Y., & Lucchinetti, C. F. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02166-2 · Cited by 479 · see citing works
Basso, C., Leone, O., Rizzo, S., De Gaspari, M., van der Wal, A. C., Aubry, M.-C., Bois, M. C., Lin, P. T., Maleszewski, J. J., & Stone, J. R. (2020) · European Heart Journal · doi:10.1093/eurheartj/ehaa664 · Cited by 471 · see citing works
COVID-19 pulmonary pathology: a multi-institutional autopsy cohort from Italy and New York City
Borczuk, A. C., Salvatore, S. P., Seshan, S. V., Patel, S. S., Bussel, J. B., Mostyka, M., Elsoukkary, S., He, B., Del Vecchio, C., Fortarezza, F., et al. (2020) · Modern Pathology · doi:10.1038/s41379-020-00661-1 · Cited by 452 · see citing works
How COVID-19 Affects the Brain
Boldrini, M., Canoll, P., & Klein, R. S. (2021) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2021.0500 · Cited by 433 · see citing works
Edler, C., Schröder, A. S., Aepfelbacher, M., Fitzek, A., Heinemann, A., Heinrich, F., Klein, A., Langenwalder, F., Lütgehetmann, M., Meißner, K., et al. (2020) · International Journal of Legal Medicine · doi:10.1007/s00414-020-02317-w · Cited by 425 · see citing works
Pathophysiology of SARS-CoV-2: the Mount Sinai COVID-19 autopsy experience
Bryce, C., Grimes, Z., Pujadas, E., Ahuja, S., Beasley, M. B., Albrecht, R. A., Hernandez, T., Stock, A., Zhao, Z., AlRasheed, M. R., et al. (2021) · Modern Pathology · doi:10.1038/s41379-021-00793-y · Cited by 412 · see citing works
Yachou, Y., Idrissi, A. E., Belapasov, V., & BenAli, S. A. (2020) · Neurological Sciences · doi:10.1007/s10072-020-04575-3 · Cited by 374 · see citing works
Ultrastructural Evidence for Direct Renal Infection with SARS-CoV-2
Farkash, E. A., Wilson, A. M., & Jentzen, J. M. (2020) · Journal of the American Society of Nephrology · doi:10.1681/asn.2020040432 · Cited by 350 · see citing works
Duarte‐Neto, A. N., Monteiro, R. A. D. A., da Silva, L. F. F., Malheiros, D. M. A. C., Oliveira, E. P., Filho, J. T., Pinho, J. R. R., Gomes‐Gouvêa, M. S., Salles, A. P. M., de Oliveira, I. R. S., et al. (2020) · Histopathology · doi:10.1111/his.14160 · Cited by 328 · see citing works
Postmortem Kidney Pathology Findings in Patients with COVID-19
Santoriello, D., Khairallah, P., Bomback, A. S., Xu, K. H., Kudose, S., Batal, I., Barasch, J. M., Radhakrishnan, J., D’Agati, V. D., & Markowitz, G. S. (2020) · Journal of the American Society of Nephrology · doi:10.1681/asn.2020050744 · Cited by 314 · see citing works
Neurotropic virus infections as the cause of immediate and delayed neuropathology
Ludlow, M., Kortekaas, J., Herden, C., Hoffmann, B., Tappe, D., Trebst, C., Griffin, D., Brindle, H. E., Solomon, T., Brown, A. S., et al. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1511-3 · Cited by 297 · see citing works
Early evidence of pronounced brain involvement in fatal COVID-19 outcomes
von Weyhern, C. H., Kaufmann, I., Neff, F., & Kremer, M. (2020) · The Lancet · doi:10.1016/s0140-6736(20)31282-4 · Cited by 283 · see citing works
ACE2, TMPRSS2 distribution and extrapulmonary organ injury in patients with COVID-19
Dong, M., Zhang, J., Ma, X., Tan, J., Chen, L., Liu, S., Xin, Y., & Zhuang, L. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110678 · Cited by 259 · see citing works
SARS-CoV-2 cell tropism and multiorgan infection
Liu, J., Li, Y., Liu, Q., Yao, Q., Wang, X., Zhang, H., Chen, R., Ren, L., Min, J., Dèng, F., et al. (2021) · Cell Discovery · doi:10.1038/s41421-021-00249-2 · Cited by 236 · see citing works
Neurovascular injury with complement activation and inflammation in COVID-19
Lee, M. H., Perl, D. P., Steiner, J. P., Pasternack, N., Li, W., Maric, D., Safavi, F., Horkayne‐Szakaly, I., Jones, R., Stram, M. N., et al. (2022) · Brain · doi:10.1093/brain/awac151 · Cited by 225 · see citing works
Aging immunity may exacerbate COVID-19
Akbar, A. N., & Gilroy, D. W. (2020) · Science · doi:10.1126/science.abb0762 · Cited by 209 · see citing works
Falasca, L., Nardacci, R., Colombo, D., Lalle, E., Di, A., Nicastri, E., Antinori, A., Petrosillo, N., Marchioni, L., Biava, G., et al. (2020) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiaa578 · Cited by 195 · see citing works
Neuropathologic features of four autopsied COVID‐19 patients
Kantonen, J., Mahzabin, S., Mäyränpää, M. I., Tynninen, O., Paetau, A. E., Andersson, N., Sajantila, A., Vapalahti, O. P., Carpén, O., Kekäläinen, E., et al. (2020) · Brain Pathology · doi:10.1111/bpa.12889 · Cited by 192 · see citing works
ACE and ACE2 in kidney disease
Mizuiri, S. (2015) · World Journal of Nephrology · doi:10.5527/wjn.v4.i1.74 · Cited by 187 · see citing works
Hariri, L. P., North, C. M., Shih, A. R., Israel, R. A., Maley, J. H., Villalba, J. A., Vinarsky, V., Rubin, J. N., Okin, D. A., Sclafani, A., et al. (2020) · CHEST Journal · doi:10.1016/j.chest.2020.09.259 · Cited by 180 · see citing works
Histopathological observations in COVID-19: a systematic review
Deshmukh, V. R., Motwani, R., Kumar, A., Kumari, C., & Raza, K. (2020) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2020-206995 · Cited by 177 · see citing works
Autopsy Findings in 32 Patients with COVID-19: A Single-Institution Experience
Elsoukkary, S. S., Mostyka, M., Dillard, A., Berman, D. R., Ma, L. X., Chadburn, A., Yantiss, R. K., Jessurun, J., Seshan, S. V., Borczuk, A., et al. (2020) · Pathobiology · doi:10.1159/000511325 · Cited by 162 · see citing works
Invited Review: The spectrum of neuropathology in COVID‐19
Al‐Sarraj, S., Troakes, C., Hanley, B. P., Osborn, M., Richardson, M. P., Hotopf, M. H., Bullmore, E. T., & Everall, I. (2020) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12667 · Cited by 148 · see citing works
Thrombotic complications of COVID-19
Avila, J., Long, B., Holladay, D., & Gottlieb, M. (2021) · The American Journal of Emergency Medicine · doi:10.1016/j.ajem.2020.09.065 · Cited by 143 · see citing works
Correlates of critical illness-related encephalopathy predominate postmortem COVID-19 neuropathology
Deigendesch, N., Sironi, L., Kutza, M., Wischnewski, S., Fuchs, V., Hench, J., Frank, A., Nienhold, R., Mertz, K. D., Cathomas, G., et al. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02213-y · Cited by 140 · see citing works
A review of the main histopathological findings in coronavirus disease 2019
Vasquez-Bonilla, W. O., Orozco, R., Argueta, V., Sierra, M., Zambrano, L. I., Muñoz‐Lara, F., Molina, D. S. L., Arteaga‐Livias, K., Grimes, Z., Bryce, C., et al. (2020) · Human Pathology · doi:10.1016/j.humpath.2020.07.023 · Cited by 137 · see citing works
Neuronophagia and microglial nodules in a SARS-CoV-2 patient with cerebellar hemorrhage
Al‐Dalahmah, O., Thakur, K. T., Nordvig, A. S., Prust, M., Roth, W., Lignelli, A., Uhlemann, A., Miller, E. H., Kunnath-Velayudhan, S., Portillo, A. D., et al. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01024-2 · Cited by 136 · see citing works
Große, C., Große, A., Salzer, H. J. F., Dünser, M. W., Motz, R., & Langer, R. (2020) · Cardiovascular Pathology · doi:10.1016/j.carpath.2020.107263 · Cited by 125 · see citing works
Poloni, T. E., Carlos, A. F., Cairati, M., Cutaia, C., Medici, V., Marelli, E., Ferrari, D., Galli, A., Bognetti, P., Davin, A., et al. (2020) · EClinicalMedicine · doi:10.1016/j.eclinm.2020.100490 · Cited by 124 · see citing works
Self-citationCOVID‐19‐related neuropathology and microglial activation in elderly with and without dementia
Poloni, T. E., Medici, V., Moretti, M., Visoná, S. D., Cirrincione, A., Carlos, A. F., Davin, A., Gagliardi, S., Pansarasa, O., Cereda, C., et al. (2021) · Brain Pathology · doi:10.1111/bpa.12997 · Cited by 123 · see citing works
Self-citationMyocarditis revealing COVID-19 infection in a young patient
Paul, J., Charles, P., Richaud, C., Caussin, C., & Diakov, C. (2020) · European Heart Journal - Cardiovascular Imaging · doi:10.1093/ehjci/jeaa107 · Cited by 122 · see citing works
Intracerebral endotheliitis and microbleeds are neuropathological features of COVID‐19
Kirschenbaum, D. S., Imbach, L., Rushing, E. J., Frauenknecht, K. B. M., Gascho, D., Ineichen, B. V., Keller, E., Köhler, S., Lichtblau, M., Reimann, R., et al. (2020) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12677 · Cited by 116 · see citing works
Histopathological findings and clinicopathologic correlation in COVID-19: a systematic review
Caramaschi, S., Kapp, M., Miller, S., Eisenberg, R., Johnson, J. E., Epperly, G., Maiorana, A., Silvestri, G., & Giannico, G. A. (2021) · Modern Pathology · doi:10.1038/s41379-021-00814-w · Cited by 111 · see citing works
Myocarditis in COVID-19 patients: current problems
Mele, D., Flamigni, F., Rapezzi, C., & Ferrari, R. (2021) · Internal and Emergency Medicine · doi:10.1007/s11739-021-02635-w · Cited by 108 · see citing works
Self-citationFullard, J. F., Lee, H.-C., Voloudakis, G., Suo, S., Javidfar, B., Shao, Z., Peter, C. J., Zhang, W., Jiang, S., Corvelo, A., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00933-8 · Cited by 108 · see citing works
Microvascular injury and hypoxic damage: emerging neuropathological signatures in COVID-19
Jaunmuktane, Z., Mahadeva, U., Green, A. C., Sekhawat, V., Barrett, N. A., Childs, L., Shankar‐Hari, M., Thom, M., Jäger, H. R., & Brandner, S. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02190-2 · Cited by 101 · see citing works
COVID-19 and Crosstalk With the Hallmarks of Aging
Salimi, S., & Hamlyn, J. M. (2020) · The Journals of Gerontology Series A · doi:10.1093/gerona/glaa149 · Cited by 95 · see citing works
Yende, S. P., & Parikh, C. R. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-021-00487-3 · Cited by 94 · see citing works
Erratum to “Long COVID: An overview” [Diabetes Metabol. Syndr. Clin. Res. Rev. (2021) 869–875]
Raveendran, A. V., Jayadevan, R., & Sashidharan, S. (2022) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2022.102660 · Cited by 87 · see citing works
Hassanein, M., Radhakrishnan, Y., Sedor, J. R., Vachharajani, T. J., Vachharajani, V., Augustine, J. J., Demirjian, S. G., & Thomas, G. (2020) · Cleveland Clinic Journal of Medicine · doi:10.3949/ccjm.87a.20072 · Cited by 81 · see citing works
COVID-19 pandemic: Its impact on liver disease and liver transplantation
Şahin, T. T., Akbulut, S., & Yılmaz, S. (2020) · World Journal of Gastroenterology · doi:10.3748/wjg.v26.i22.2987 · Cited by 77 · see citing works
Multisystemic Cellular Tropism of SARS-CoV-2 in Autopsies of COVID-19 Patients
Wong, D. W. L., Klinkhammer, B. M., Djudjaj, S., Villwock, S., Timm, M. C., Buhl, E. M., Wucherpfennig, S., Cacchi, C., Braunschweig, T. A., Knüchel, R., et al. (2021) · Cells · doi:10.3390/cells10081900 · Cited by 74 · see citing works
Gagliardi, S., Poloni, T. E., Pandini, C., Garofalo, M., Dragoni, F., Medici, V., Davin, A., Visoná, S. D., Moretti, M., Sproviero, D., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.05.012 · Cited by 55 · see citing works
Self-citationAcute pericarditis as a primary presentation of COVID-19
Kumar, R., Kumar, J., Daly, C., & Edroos, S. A. (2020) · BMJ Case Reports · doi:10.1136/bcr-2020-237617 · Cited by 52 · see citing works
Ahmad, M. S., Shaik, R. A., Ahmad, R. K., Yusuf, M., Khan, M., Almutairi, A. B., Alghuyaythat, W. K. Z., & Almutairi, S. B. (2021) · PubMed · doi:10.26355/eurrev_202109_26669 · Cited by 48 · see citing works
Overview of Targets and Potential Drugs of SARS-CoV-2 According to the Viral Replication
Zhang, Y., & Tang, L. V. (2020) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00526 · Cited by 46 · see citing works
The roles of medical examiners in the COVID-19 era: a comparison between the United States and Italy
Moretti, M., Malhotra, A., Visoná, S. D., Finley, S. J., Osculati, A. M. M., & Javan, G. T. (2021) · Forensic Science Medicine and Pathology · doi:10.1007/s12024-021-00358-0 · Cited by 44 · see citing works
Self-citationSARS-CoV-2, myocardial injury and inflammation: insights from a large clinical and autopsy study
Ferro, M. D., Bussani, R., Paldino, A., Nuzzi, V., Collesi, C., Zentilin, L., Schneider, E., Correa, R., Silvestri, F., Zacchigna, S., et al. (2021) · Clinical Research in Cardiology · doi:10.1007/s00392-021-01910-2 · Cited by 41 · see citing works
Romanova, E. S., Vasilyev, V. V., Startseva, G. Y., Karev, V. E., Mg, R., & Platonov, P. G. (2021) · Journal of Internal Medicine · doi:10.1111/joim.13300 · Cited by 31 · see citing works
Abbiategrasso Brain Bank Protocol for Collecting, Processing and Characterizing Aging Brains
Poloni, T. E., Medici, V., Carlos, A. F., Davin, A., Ceretti, A., Mangieri, M., Cassini, P., Vaccaro, R., Zaccaria, D., Abbondanza, S., et al. (2020) · Journal of Visualized Experiments · doi:10.3791/60296 · Cited by 26 · see citing works
Self-citationCardiac pathology in COVID-19: a single center autopsy experience
Sang, C. J., Burkett, A. E., Heindl, B. F., Litovsky, S. H., Prabhu, S. D., Benson, P. V., & Rajapreyar, I. N. (2021) · Cardiovascular Pathology · doi:10.1016/j.carpath.2021.107370 · Cited by 26 · see citing works
Pisano, T. J., Hakkinen, I., & Rybinnik, I. (2020) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2020.105307 · Cited by 25 · see citing works
Drug Abuse-Related Neuroinflammation in Human Postmortem Brains: An Immunohistochemical Approach
Moretti, M., Belli, G., Morini, L., Monti, M. C., Osculati, A. M. M., & Visoná, S. D. (2019) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlz084 · Cited by 24 · see citing works
Self-citationLarge vessel thrombosis in patient with COVID-19, a case series
Baram, A., Kakamad, F. H., Abdullah, H. M., Mohammed-Saeed, D. H.-B., Hussein, D. A., Mohammed, S. H., Abdulrahman, B. B., Mirza, A. J., Abdullah, H. O., Rahim, H. M.-A., et al. (2020) · Annals of Medicine and Surgery · doi:10.1016/j.amsu.2020.11.030 · Cited by 22 · see citing works
Coronavirus Precautions: Experience of High Volume Liver Transplant Institute
Başkıran, A., Akbulut, S., Şahin, T. T., Tunçer, A., Kaplan, K., Bayındır, Y., & Yılmaz, S. (2022) · The Turkish Journal of Gastroenterology · doi:10.5152/tjg.2022.21748 · Cited by 16 · see citing works
Abbiategrasso Brain Bank Protocol for Collecting, Processing and Characterizing Aging Brains
Poloni, T. E., Medici, V., Carlos, A. F., Davin, A., Ceretti, A., Mangieri, M., Cassini, P., Vaccaro, R., Zaccaria, D., Abbondanza, S., et al. (2020) · Journal of Visualized Experiments · doi:10.3791/60296-v · Cited by 11 · see citing works
Self-citationLynch, M. R., & Tang, J. (2020) · PubMed · Cited by 10 · see citing works
Flagged first, then by citations
1 of the 92 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
COVID-19, Myocarditis and Pericarditis
Fairweather, D., Beetler, D. J., Di Florio, D. N., Musigk, N., Heidecker, B., & Cooper, L. T. (2023) · Circulation Research · doi:10.1161/circresaha.123.321878 · Cited by 181 · see citing works
Theoharides, T. C., & Kempuraj, D. (2023) · Cells · doi:10.3390/cells12050688 · Cited by 81 · see citing works
Li, W., Sun, L., Yue, L., & Xiao, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1120495 · Cited by 29 · see citing works
Cerebromicrovascular mechanisms contributing to long COVID: implications for neurocognitive health
Fekete, M., Lehoczki, A., Szappanos, Á., Tóth, A., Mahdi, M., Sótonyi, P., Benyó, Z., Yabluchanskiy, A., Tarantini, S., & Ungvari, Z. I. (2025) · GeroScience · doi:10.1007/s11357-024-01487-4 · Cited by 25 · see citing works
Stein, J. A., Kaes, M., Smola, S., & Schulz‐Schaeffer, W. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1229641 · Cited by 18 · see citing works
Ciszewski, W. M., Woźniak, L. A., & Sobierajska, K. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01665-z · Cited by 10 · see citing works
Babkina, A. S., Yadgarov, M. Y., Lyubomudrov, M. A., Ostrova, I. V., Volkov, A. V., Kuzovlev, A. N., Grechko, A. V., & Golubev, A. M. (2023) · Biomedicines · doi:10.3390/biomedicines11051407 · Cited by 8 · see citing works
Cellular Immune Profiling of Lung and Blood Compartments in Patients with SARS-CoV-2 Infection
Santinelli, L., Lazzaro, A., Sciarra, F., Maddaloni, L., Frasca, F., Fracella, M., Moretti, S., Borsetti, A., Bugani, G., Alessandri, F., et al. (2023) · Pathogens · doi:10.3390/pathogens12030442 · Cited by 7 · see citing works
Cui, Y., Chen, Z., Kong, Y., Wang, Y., Wang, Y., Zhang, J., Wang, L., Zhang, J., Sun, W., & Wu, L. (2024) · Neurological Sciences · doi:10.1007/s10072-024-07587-5 · Cited by 5 · see citing works
Postmortem neuropathology in COVID ‐19: An update
Younger, D. S. (2023) · Brain Pathology · doi:10.1111/bpa.13204 · Cited by 4 · see citing works
The Intersection of SARS-CoV-2 and Diabetes
Nichols, J. H., Smith, A. M., & Jonsson, C. B. (2025) · Microorganisms · doi:10.3390/microorganisms13061390 · Cited by 6 · see citing works
Long Coronavirus Disease and the Brain
Guedj, É., Cionca, A., Péron, J., Ayubcha, C., Assal, F., Horowitz, T., & Alavi, A. (2024) · PET Clinics · doi:10.1016/j.cpet.2024.09.013 · Cited by 2 · see citing works
Suwanai, H., Kanda, M., Harada, K., Ishii, K., Iwasaki, H., Hara, N., Kobayashi, Y., Matsumura, H., Inoue, T., & Suzuki, R. (2025) · PLoS ONE · doi:10.1371/journal.pone.0319801 · Cited by 1 · see citing works
The roles of GABA and NMDA receptors in viral infections: based on current literature
Ning, K., Xu, W., Wang, Y., Lei, L., Shen, W.-S.-J., & Liu, Z. (2025) · Clinical & Experimental Immunology · doi:10.1093/cei/uxaf052 · Cited by 1 · see citing works
Immune dysregulation in coronavirus infection COVID-19
Evdokimova, A. E., Саубанович, Х. Х., Алексеевич, А. В., & Рагинов, И. С. (2025) · Journal Infectology · doi:10.22625/2072-6732-2025-17-3-24-32 · Cited by 1 · see citing works
Human brain matters: Navigating the neuropathology of COVID ‐19
Nieuwland, J. M., Scaramuzza, A., Bugiani, M., van de Berg, W. D. J., & Middeldorp, J. (2026) · Brain Pathology · doi:10.1111/bpa.70101 · Cited by 1 · see citing works
Pathogenesis of neuropsychic complications of new coronavirus infection
Klimov, N. A., & Валерьевна, Ш. О. (2023) · Medical academic journal · doi:10.17816/maj624867
RT-qPCR investigation of post-mortem tissues during COVID-19
Berdygulova, Z. A., Maltseva, E. R., Perfilyeva, Y. V., Nizkorodova, A. S., Zhigailov, A. V., Naizabayeva, D. A., Ostapchuk, Y. O., Kuatbekova, S. A., Dosmagambet, Z. M., Kuatbek, M. M., et al. (2024) · Journal of Applied Biomedicine · doi:10.32725/jab.2024.013
Чернов, А. С., Kazakov, V. A., Gogleva, I. S., Вадимович, С. С., Николаевна, Щ. В., Loginova, S. Y., Borisevich, S. V., Smirnov, I. V., Telegin, G. B., & Belogurov, A. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.12.623177
IMPACT OF COVID-19 ON DIAGNOSTIC ANALYSIS OF MYOCARDITIS
Hysenaj, K., Qyra, S., Stena, R., & Bani, B. (2024) · International Ayurvedic Medical Journal · doi:10.46607/iamj06p9012024
A perspective on pathogenesis of post-COVID syndrome
Klimov, N. A., & Simbirtsev, A. S. (2024) · Cytokines and inflammation · doi:10.17816/ci636474
Beduleva, L., Fomina, K., Khramova, T., Terentiev, A., Menshikova, D., Terentievа, O. S., Menshikov, I., Sidorov, A., Makhankova, P., & Николаевна, А. Н. (2025) · Scientific Reports · doi:10.1038/s41598-025-21304-y · Cited by 1 · see citing works
Causes of Lymphopenia in Patients Died from COVID-19
Evdokimova, A., Рагинов, И. С., Саубанович, Х. Х., Алексеевич, А. В., & Ovchinnikova, A. G. (2026) · Ural Medical Journal · doi:10.52420/umj.25.4.35
Wolabaugh, A., Agashe, V. V., Wang, Z., Danzl, N. M., Parks, C. A., Maharlooei, M. K., Ding, X., Li, H. W., Castagna, C., Zanetti, G., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1951246
- Authors
- Poloni, T. E., Moretti, M., Medici, V., Turturici, E., Belli, G., Cavriani, E., Visonà, S. D., Rossi, M., Fantini, V., Ferrari, R. R., Carlos, A. F., Gagliardi, S., Tronconi, L., Guaita, A., & Ceroni, M.
- Affiliations
- Fondazione Golgi Cenci (IT)
- University of Pavia (IT)
- Department of Public Health, Experimental and Forensic Medicine, University of Pavia, 27100 Pavia, Italy
- Unit of Molecular Biology and Transcriptomics IRCCS Mondino Foundation, 27100 Pavia, Italy
- Corresponding author
- Poloni, Tino Emanuele
- ORCID
- Venue
- Cells
- Publisher
- MDPI AG
- Published
- 2022-10-04
- Volume
- 11
- Issue
- 19
- Pages
- 3124
- ISSN
- 2073-4409 (ISSN-L)
- PMC
- PMC9563269
- OpenAlex
- W4303628086
- Cited by
- 24
- References
- 92
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 7 · 2023: 8
- FWCI
- 2.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cells (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Fondo di Beneficenza Intesa Sanpaolo (Italy) (B/2020/0045)
- Topics
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Neurology › Long-Term Effects of COVID-19
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Keywords
- SARS-CoV-2, T cells, macrophages, microglial activation, microvascular thrombosis, lung, kidney, heart, brain, Alzheimer's disease pathology, chronic inflammation, hypoxia, lymphocyte infiltration, autopsy findings, long-term sequelae
- MeSH terms
- COVID-19, SARS-CoV-2, Aged, Antigens, Viral, Brain, Humans, Kidney, Lung, Macrophages, RNA, Viral, T-Lymphocytes, Thrombosis
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.
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