Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19
Open accessAbstract
BACKGROUND: Progressive respiratory failure is the primary cause of death in the coronavirus disease 2019 (Covid-19) pandemic. Despite widespread interest in the pathophysiology of the disease, relatively little is known about the associated morphologic and molecular changes in the peripheral lung of patients who die from Covid-19. METHODS: We examined 7 lungs obtained during autopsy from patients who died from Covid-19 and compared them with 7 lungs obtained during autopsy from patients who died from acute respiratory distress syndrome (ARDS) secondary to influenza A(H1N1) infection and 10 age-matched, uninfected control lungs. The lungs were studied with the use of seven-color immunohistochemical analysis, micro-computed tomographic imaging, scanning electron microscopy, corrosion casting, and direct multiplexed measurement of gene expression. RESULTS: In patients who died from Covid-19-associated or influenza-associated respiratory failure, the histologic pattern in the peripheral lung was diffuse alveolar damage with perivascular T-cell infiltration. The lungs from patients with Covid-19 also showed distinctive vascular features, consisting of severe endothelial injury associated with the presence of intracellular virus and disrupted cell membranes. Histologic analysis of pulmonary vessels in patients with Covid-19 showed widespread thrombosis with microangiopathy. Alveolar capillary microthrombi were 9 times as prevalent in patients with Covid-19 as in patients with influenza (P<0.001). In lungs from patients with Covid-19, the amount of new vessel growth - predominantly through a mechanism of intussusceptive angiogenesis - was 2.7 times as high as that in the lungs from patients with influenza (P<0.001). CONCLUSIONS: In our small series, vascular angiogenesis distinguished the pulmonary pathobiology of Covid-19 from that of equally severe influenza virus infection. The universality and clinical implications of our observations require further research to define. (Funded by the National Institutes of Health and others.).
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SARS-CoV-2 facilitates release of coagulation factors, secretion of inflammatory cytokines, and formation of leukocyte-platelet aggregates, which might be important mechanisms leading to thromboembolic complications in severe COVID-19.
“Furthermore, the virus facilitates the release of coagulation factors, the secretion of inflammatory cytokines, and the formation of leukocyte-platelet aggregates, which might be important mechanisms leading to thromboembolic complications observed in severe COVID-19 (Ackermann et al., 2020; Gupta et al., 2020; Zhang et al., 2020b).”
From COVID-19 and the human innate immune system (2021) · cites this paper as Ackermann et al., 2020
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A novel coronavirus from patients with pneumonia in China, 2019
Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001017 · Cited by 28,244 · see citing works
Chen, N., Zhou, M., Dong, X., Qu, J., Gong, F., Han, Y., Qiu, Y., Wang, J., Liu, Y., Wei, Y., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30211-7 · Cited by 21,415 · see citing works
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
Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2
Yan, R., Zhang, Y., Li, Y., Xia, L., Guo, Y., & Zhou, Q. (2020) · Science · doi:10.1126/science.abb2762 · Cited by 4,950 · see citing works
Tang, N., Bai, H., Chen, X., Gong, J., Li, D., & Sun, Z. (2020) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14817 · Cited by 3,554 · see citing works
MAGRO, C. M. J., Mulvey, J. J., Berlin, D., Nuovo, G. J., Salvatore, S., HARP, J. L., Baxter-Stoltzfus, A., & Laurence, J. C. (2020) · Translational research · doi:10.1016/j.trsl.2020.04.007 · Cited by 2,185 · see citing works
Acute respiratory distress syndrome
Thompson, B. T., Chambers, R. C., & Liu, K. D. (2017) · New England Journal of Medicine · doi:10.1056/nejmra1608077 · Cited by 1,807 · see citing works
Tian, S., Hu, W., Niu, L., Liu, H., Xu, H., & Xiao, S. (2020) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2020.02.010 · Cited by 1,414 · see citing works
Multiple organ infection and the pathogenesis of SARS
Gu, J., Gong, E., Zhang, B., Zheng, J., Gao, Z., Zhong, Y., Zou, W., Zhan, J., Wang, S., Xie, Z., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050828 · Cited by 1,379 · 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
Self-citationLung pathology of fatal severe acute respiratory syndrome
Nicholls, J. M., Poon, L. L., Lee, K. C., Ng, W. F., Lai, S. T., Leung, C. Y., Chu, C. M., Hui, P. K., Mak, K. L., Lim, W., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13413-7 · Cited by 1,076 · see citing works
COVID-19 Autopsies, Oklahoma, USA
Barton, L. M., Duval, E. J., Stroberg, E., Ghosh, S., & Mukhopadhyay, S. (2020) · American Journal of Clinical Pathology · doi:10.1093/ajcp/aqaa062 · Cited by 832 · see citing works
The Science Underlying COVID-19
Liu, P. P., Blet, A., Smyth, D. R., & Li, H. (2020) · Circulation · doi:10.1161/circulationaha.120.047549 · Cited by 803 · see citing works
Hoffmann, M., Kleine‐Weber, H., Krüger, N., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.31.929042 · Cited by 754 · see citing works
Clinical characteristics of 3062 COVID‐19 patients: A meta‐analysis
Zhu, J., Ji, P., Pang, J., Zhong, Z., Li, H., He, C., Zhang, J., & Zhao, C. (2020) · Journal of Medical Virology · doi:10.1002/jmv.25884 · Cited by 622 · see citing works
Diffuse alveolar damage--the role of oxygen, shock, and related factors. A review.
Katzenstein, A. L., Bloor, C. M., & Leibow, A. A. (1976) · PubMed · Cited by 519 · see citing works
Buja, L. M., Wolf, D. A., Zhao, B., Akkanti, B. H., McDonald, M. M., Lelenwa, L. C., Reilly, N., Giulia Ottaviani, M., Elghetany, M. T., Trujillo, D. O., et al. (2020) · Cardiovascular Pathology · doi:10.1016/j.carpath.2020.107233 · Cited by 387 · see citing works
Treatment of ARDS With Prone Positioning
Scholten, E. L., Beitler, J. R., Prisk, G. K., & Malhotra, A. (2016) · CHEST Journal · doi:10.1016/j.chest.2016.06.032 · Cited by 365 · see citing works
Alsaad, K. O., Hajeer, A. H., Balwi, M. A. A., Almoaiqel, M., Aloudah, N., Ajlan, A. A., AlJohani, S. M., Alsolamy, S. J., Gmati, G. E. M., Balkhy, H. H., et al. (2017) · Histopathology · doi:10.1111/his.13379 · Cited by 284 · see citing works
Intussusceptive angiogenesis: expansion and remodeling of microvascular networks
Mentzer, S. J., & Konerding, M. A. (2014) · Angiogenesis · doi:10.1007/s10456-014-9428-3 · Cited by 220 · see citing works
Self-citationChest CT and Coronavirus Disease (COVID-19): A Critical Review of the Literature to Date
Raptis, C. A., Hammer, M. M., Short, R. G., Shah, A. B., Bhalla, S., Bierhals, A. J., Filev, P. D., Hope, M. D., Jeudy, J. J., Kligerman, S. J., et al. (2020) · American Journal of Roentgenology · doi:10.2214/ajr.20.23202 · Cited by 214 · see citing works
Venous thromboembolism in COVID‐19 patients
Porfidia, A., & Pola, R. (2020) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14842 · Cited by 102 · see citing works
Morphomolecular motifs of pulmonary neoangiogenesis in interstitial lung diseases
Ackermann, M., Stark, H., Neubert, L., Schubert, S., Borchert, P., Linz, F., Wagner, W. L., Stiller, W., Wielpütz, M. O., Hoefer, A., et al. (2019) · European Respiratory Journal · doi:10.1183/13993003.00933-2019 · Cited by 68 · see citing works
Self-citationVoltersvik, P., Aqrawi, L. A., Dudman, S. G., Hungnes, O., Norwegian Lung Pathology Group, Bostad, L. H., Brokstad, K. A., & Cox, R. J. (2016) · Influenza and Other Respiratory Viruses · doi:10.1111/irv.12410 · Cited by 13 · see citing works
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- [19]O’Donnell JS, Sharif K, Emery P, Bridgewood C. McGonagle D. Why the immune mechanisms of pulmonary intravascular coagulopathy in COVID-19 pneumonia are distinct from macrophage activation syndrome with disseminated intravascular coagulation. 4 2020 (https://www.researchgate.net/publication/340621484_Why_the_Immune_Mechanisms_of_Pulmonary_Intravascular_Coagulopathy_in_COVID-19_Pneumonia_are_Distinct_from_Macrophage_Activation_Syndrome_with_Disseminated_Intravascular_Coagulation). preprint.
Cited by
Sorted by citations
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
Extrapulmonary manifestations of COVID-19
Gupta, A., Madhavan, M. V., Sehgal, K., Nair, N., Mahajan, S., Sehrawat, T. S., Bikdeli, B., Ahluwalia, N., Ausiello, J. C., Wan, E. Y., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0968-3 · Cited by 3,185 · see citing works
Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity
Cantuti-Castelvetri, L., Ojha, R., Pedro, L. D., Djannatian, M., Franz, J., Kuivanen, S., van der Meer, F., Kallio, K., Kaya, T., Anastasina, M., et al. (2020) · Science · doi:10.1126/science.abd2985 · Cited by 1,925 · see citing works
Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments
Yong, S. J. (2021) · Infectious Diseases · doi:10.1080/23744235.2021.1924397 · Cited by 1,339 · see citing works
Tomazini, B. M., Maia, I. S., Cavalcanti, A. B., Berwanger, O., Rosa, R. G., Veiga, V. C., Avezum, A., Lopes, R. D., Bueno, F. R., Silva, M. V. A. O., et al. (2020) · JAMA · doi:10.1001/jama.2020.17021 · Cited by 1,241 · see citing works
Neuropilin-1 is a host factor for SARS-CoV-2 infection
Daly, J. L., Simonetti, B., Klein, K., Chen, K.-E., Williamson, M. K., Antón-Plágaro, C., Shoemark, D. K., Simón-Gracia, L., Bauer, M., Hollandi, R., et al. (2020) · Science · doi:10.1126/science.abd3072 · Cited by 1,251 · see citing works
Muñoz-Fontela, C., Dowling, W. E., Funnell, S. G. P., Gsell, P.-S., Riveros-Balta, A. X., Albrecht, R. A., Andersen, H., Baric, R. S., Carroll, M. W., Cavaleri, M., et al. (2020) · Nature · doi:10.1038/s41586-020-2787-6 · Cited by 798 · see citing works
Skendros, P., Mitsios, A., Chrysanthopoulou, A., Mastellos, D. C., Metallidis, S., Rafailidis, P., Ntinopoulou, M., Sertaridou, E., Tsironidou, V., Tsigalou, C., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci141374 · Cited by 786 · see citing works
COVID-19 and the human innate immune system
Schultze, J. L., & Aschenbrenner, A. C. (2021) · Cell · doi:10.1016/j.cell.2021.02.029 · Cited by 714 · 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
Cytokine storms: understanding COVID-19
Mangalmurti, N., & Hunter, C. A. (2020) · Immunity · doi:10.1016/j.immuni.2020.06.017 · Cited by 698 · see citing works
A Mouse-Adapted SARS-CoV-2 Induces Acute Lung Injury and Mortality in Standard Laboratory Mice
Leist, S. R., Dinnon, K. H., Schäfer, A., Tse, L. V., Okuda, K., Hou, Y. J., West, A., Edwards, C. E., Sanders, W., Fritch, E. J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.050 · Cited by 613 · 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
Polak, S. B., Van Gool, I. C., Cohen, D., von der Thüsen, J. H., & van Paassen, J. (2020) · Modern Pathology · doi:10.1038/s41379-020-0603-3 · Cited by 481 · see citing works
Capillary cell-type specialization in the alveolus
Gillich, A., Zhang, F., Farmer, C. G., Travaglini, K. J., Tan, S. Y., Gu, M., Zhou, B., Feinstein, J. A., Krasnow, M. A., & Metzger, R. J. (2020) · Nature · doi:10.1038/s41586-020-2822-7 · Cited by 490 · see citing works
Regional and global contributions of air pollution to risk of death from COVID-19
Pozzer, A., Dominici, F., Haines, A., Witt, C., Münzel, T., & Lelieveld, J. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa288 · Cited by 463 · 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
Virus-induced senescence is a driver and therapeutic target in COVID-19
Lee, S., Yu, Y., Trimpert, J., Benthani, F., Mairhofer, M., Richter-Pechanska, P., Wyler, E., Belenki, D., Kaltenbrunner, S., Pammer, M., et al. (2021) · Nature · doi:10.1038/s41586-021-03995-1 · Cited by 350 · see citing works
Pulmonary pathology of ARDS in COVID-19: A pathological review for clinicians
Batah, S. S., & Fabro, A. T. (2021) · Respiratory Medicine · doi:10.1016/j.rmed.2020.106239 · Cited by 319 · see citing works
Preeclampsia and COVID-19: results from the INTERCOVID prospective longitudinal study
Papageorghiou, A. T., Deruelle, P., Gunier, R. B., Rauch, S., García-May, P. K., Mhatre, M., Usman, M. A., Abd-Elsalam, S., Etuk, S., Simmons, L. E., et al. (2021) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2021.05.014 · Cited by 311 · 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
Mastellos, D. C., Pires da Silva, B. G. P., Fonseca, B. A. L., Fonseca, N. P., Auxiliadora-Martins, M., Mastaglio, S., Ruggeri, A., Sironi, M., Radermacher, P., Chrysanthopoulou, A., et al. (2020) · Clinical Immunology · doi:10.1016/j.clim.2020.108598 · Cited by 255 · see citing works
Thrombosis in Coronavirus disease 2019 (COVID-19) through the prism of Virchow’s triad
Ahmed, S., Zimba, O., & Gasparyan, A. Y. (2020) · Clinical Rheumatology · doi:10.1007/s10067-020-05275-1 · Cited by 251 · 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
Lamers, M. M., van der Vaart, J., Knoops, K., Riesebosch, S., Breugem, T. I., Mykytyn, A. Z., Beumer, J., Schipper, D., Bezstarosti, K., Koopman, C. D., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020105912 · Cited by 227 · 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
Zhang, M., Wang, P., Luo, R., Wang, Y., Li, Z., Guo, Y., Yao, Y., Li, M., Tao, T., Chen, W., et al. (2021) · Advanced Science · doi:10.1002/advs.202002928 · Cited by 236 · see citing works
COVID-19 vaccine-readiness for anti-CD20-depleting therapy in autoimmune diseases
Baker, D., Roberts, C. A. K., Pryce, G., Kang, A. S., Marta, M., Reyes, S., Schmierer, K., Giovannoni, G., & Amor, S. (2020) · Clinical and Experimental Immunology · doi:10.1111/cei.13495 · Cited by 192 · see citing works
Leukocyte trafficking to the lungs and beyond: lessons from influenza for COVID-19
Alon, R., Sportiello, M., Kozlovski, S., Kumar, A., Reilly, E. C., Zarbock, A., Garbi, N., & Topham, D. J. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-020-00470-2 · Cited by 197 · see citing works
COVID-19 vasculitis and novel vasculitis mimics
McGonagle, D., Bridgewood, C., Ramanan, A. V., Meaney, J. F. M., & Watad, A. (2021) · The Lancet Rheumatology · doi:10.1016/s2665-9913(20)30420-3 · Cited by 192 · see citing works
The pulmonary pathology of COVID-19
Bösmüller, H., Matter, M., Fend, F., & Tzankov, A. (2021) · Virchows Archiv · doi:10.1007/s00428-021-03053-1 · Cited by 180 · see citing works
Self-citationEicosanoid signalling blockade protects middle-aged mice from severe COVID-19
Wong, L.-Y. R., Zheng, J., Wilhelmsen, K., Li, K., Ortiz, M. E., Schnicker, N. J., Thurman, A., Pezzulo, A. A., Szachowicz, P. J., Li, P., et al. (2022) · Nature · doi:10.1038/s41586-022-04630-3 · Cited by 178 · see citing works
Microstructure, pathophysiology, and potential therapeutics of COVID‐19: A comprehensive review
Singh, S. P., Pritam, M., Pandey, B., & Yadav, T. P. (2021) · Journal of Medical Virology · doi:10.1002/jmv.26254 · Cited by 166 · see citing works
COVID-19 and cellular senescence
Schmitt, C. A., Tchkonia, T., Niedernhofer, L. J., Robbins, P. D., Kirkland, J. L., & Lee, S. (2023) · Nature Reviews Immunology · doi:10.1038/s41577-022-00785-2 · Cited by 153 · see citing works
Multi-Organ Involvement in COVID-19: Beyond Pulmonary Manifestations
Thakur, V., Ratho, R. K., Kumar, P., Bhatia, S. K., Bora, I., Mohi, G. K., Saxena, S. K., Devi, M., Yadav, D., & Mehariya, S. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10030446 · Cited by 147 · see citing works
Q493K and Q498H substitutions in Spike promote adaptation of SARS-CoV-2 in mice
Huang, K., Zhang, Y., Hui, X., Zhao, Y., Gong, W., Wang, T., Zhang, S., Yang, Y., Deng, F., Zhang, Q., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103381 · Cited by 119 · see citing works
Thacker, V. V., Sharma, K., Dhar, N., Mancini, G.-F., Sordet-Dessimoz, J., & McKinney, J. D. (2021) · The EMBO Reports · doi:10.15252/embr.202152744 · Cited by 142 · see citing works
Watanabe, A., So, M., Iwagami, M., Fukunaga, K., Takagi, H., Kabata, H., & Kuno, T. (2022) · Respirology · doi:10.1111/resp.14311 · Cited by 139 · see citing works
Manolis, A. S., Manolis, T. A., Manolis, A. A., Papatheou, D., & Melita, H. (2021) · Journal of Cardiovascular Pharmacology and Therapeutics · doi:10.1177/1074248420958973 · Cited by 134 · see citing works
He, L., Mäe, M. A., Muhl, L., Sun, Y., Pietilä, R., Nahar, K., Liébanas, E. V., Fagerlund, M. J., Oldner, A., Liu, J., et al. (2020) · doi:10.1101/2020.05.11.088500 · Cited by 116 · see citing works
COVID-19 pathophysiology may be driven by an imbalance in the renin-angiotensin-aldosterone system
Rysz, S., Al-Saadi, J., Sjöström, A., Farm, M., Campoccia Jalde, F., Plattén, M., Eriksson, H., Klein, M., Vargas-Paris, R., Nyrén, S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22713-z · Cited by 111 · see citing works
Liver injury in COVID-19 and IL-6 trans-signaling-induced endotheliopathy
McConnell, M. J., Kawaguchi, N., Kondo, R., Sonzogni, A., Licini, L., Valle, C., Bonaffini, P. A., Sironi, S., Alessio, M. G., Previtali, G., et al. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.04.050 · Cited by 111 · see citing works
Rosa, B. A., Ahmed, M., Singh, D. K., Choreño-Parra, J. A., Cole, J., Jiménez-Álvarez, L. A., Rodríguez-Reyna, T. S., Singh, B., Gonzalez, O., Carrion, R., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01829-4 · Cited by 106 · see citing works
Targeting senescent cells for a healthier longevity: the roadmap for an era of global aging
Sun, Y., Li, Q., & Kirkland, J. L. (2022) · Life Medicine · doi:10.1093/lifemedi/lnac030 · Cited by 105 · see citing works
Carubbi, F., Salvati, L., Alunno, A., Maggi, F., Borghi, E., Mariani, R., Mai, F., Paoloni, M., Ferri, C., Desideri, G., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-83831-8 · Cited by 104 · see citing works
Stefely, J. A., Christensen, B. B., Gogakos, T., Cone Sullivan, J. K., Montgomery, G. G., Barranco, J. P., & Van Cott, E. M. (2020) · American Journal of Hematology · doi:10.1002/ajh.25979 · Cited by 80 · see citing works
Surfactant therapy for COVID-19 related ARDS: a retrospective case–control pilot study
Piva, S., DiBlasi, R. M., Slee, A. E., Jobe, A. H., Roccaro, A. M., Filippini, M., Latronico, N., Bertoni, M., Marshall, J. C., & Portman, M. A. (2021) · Respiratory Research · doi:10.1186/s12931-020-01603-w · Cited by 70 · see citing works
Exploring the Role of Endothelial Cell Resilience in Cardiovascular Health and Disease
Gao, Y., & Galis, Z. S. (2021) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.120.314346 · Cited by 62 · see citing works
COVID-19 versus HIT hypercoagulability
Warkentin, T. E., & Kaatz, S. (2020) · Thrombosis Research · doi:10.1016/j.thromres.2020.08.017 · Cited by 57 · see citing works
Pathways to Severe COVID‐19 for People with Obesity
O’Rourke, R. W., & Lumeng, C. N. (2021) · Obesity · doi:10.1002/oby.23099 · Cited by 42 · see citing works
Peptide Correlation Analysis (PeCorA) Reveals Differential Proteoform Regulation
Dermit, M., Peters-Clarke, T. M., Shishkova, E., & Meyer, J. G. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00602 · Cited by 40 · see citing works
Nakanishi, T., & Kuragano, T. (2024) · Clinical Kidney Journal · doi:10.1093/ckj/sfae051 · Cited by 39 · see citing works
Aoki, R., Iwasawa, T., Hagiwara, E., Komatsu, S., Utsunomiya, D., & Ogura, T. (2021) · Japanese Journal of Radiology · doi:10.1007/s11604-020-01085-2 · Cited by 26 · see citing works
Lai, A., Chang, M. L., O'Donnell, R. P., Zhou, C., Sumner, J. A., & Hsiai, T. K. (2021) · Science of The Total Environment · doi:10.1016/j.scitotenv.2021.146464 · Cited by 25 · see citing works
Poloni, T. E., Moretti, M., Medici, V., Turturici, E., Belli, G., Cavriani, E., Visonà, S. D., Rossi, M., Fantini, V., Ferrari, R. R., et al. (2022) · Cells · doi:10.3390/cells11193124 · Cited by 24 · see citing works
Mesenteric ischemia in COVID-19 patients: A review of current literature
Kerawala, A. A., Das, B., & Solangi, A. (2021) · World Journal of Clinical Cases · doi:10.12998/wjcc.v9.i18.4700 · Cited by 23 · see citing works
Devaux, C. A., & Camoin-Jau, L. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1042200 · Cited by 20 · see citing works
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de Lima Beltrão, F. E., de Almeida Beltrão, D. C., Carvalhal, G., de Lima Beltrão, F. E., de Souza Braga Filho, J., de Brito Oliveira, J., de Jesus, J. D. S., Machado, G. J. R., dos Santos Silva, H., Teixeira, H. M. P., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac075 · Cited by 12 · see citing works
Pneumatosis Intestinalis in the Setting of COVID-19: A Single Center Case Series From New York
Miyara, S. J., Becker, L. B., Guevara, S., Kirsch, C., Metz, C. N., Shoaib, M., Grodstein, E., Nair, V. V., Jandovitz, N., McCann-Molmenti, A., et al. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.638075 · Cited by 9 · see citing works
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Kreidieh, F., & Temraz, S. (2020) · Mediterranean Journal of Hematology and Infectious Diseases · doi:10.4084/mjhid.2020.078 · Cited by 7 · see citing works
- Authors
- Ackermann, M., Verleden, S. E., Kuehnel, M., Haverich, A., Welte, T., Laenger, F., Vanstapel, A., Werlein, C., Stark, H., Tzankov, A., Li, W. W., Li, V. W., Mentzer, S. J., & Jonigk, D.
- Affiliations
- Witten/Herdecke University (DE)
- From the Institute of Pathology and Department of Molecular Pathology, Helios University Clinic Wuppertal, University of Witten–Herdecke, Wuppertal (M.A.), the Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg University Mainz, Mainz (M.A.), the Institute of Pathology (M.K., F.L., C.W., H.S., D.J.), the Department of Cardiothoracic, Transplantation, and Vascular Surgery (A.H.), and the Clinic of Pneumology (T.W.), Hannover Medical School, and the...
- ORCID
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2020-07-09
- Volume
- 383
- Issue
- 2
- Pages
- 120-128
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC7412750
- OpenAlex
- W3027918021
- Cited by
- 5,613
- References
- 24
- Citations by year
- 2026: 205 · 2025: 272 · 2024: 435 · 2023: 650 · 2022: 1144 · 2021: 1739 · 2020: 1160 · 2013: 1 · 2012: 1
- FWCI
- 153.14
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- Funders
- H2020 European Research Council (771883)
- National Heart, Lung, and Blood Institute (HL134229, HL94567)
- 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, pulmonary thrombosis, intussusceptive angiogenesis, endothelial injury, H1N1 influenza, acute respiratory distress syndrome, diffuse alveolar damage, T cell infiltration, respiratory failure, lung histopathology
- MeSH terms
- Betacoronavirus, COVID-19, SARS-CoV-2, Aged, Aged, 80 and over, Autopsy, Endothelium, Vascular, Female, Humans, Influenza, Human, Lung, Male, Middle Aged, Neovascularization, Pathologic, Pneumonia, Viral, Respiratory Distress Syndrome, Respiratory Insufficiency, Thrombosis, Coronavirus Infections, Influenza A Virus, H1N1 Subtype, Pandemics
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