Cited by 1,775COVID-19 Clinical Research StudiesSARS-CoV-2 and COVID-19 ResearchLong-Term Effects of COVID-19

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Multiorgan and Renal Tropism of SARS-CoV-2

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Puelles, Victor G., Lütgehetmann, Marc, Lindenmeyer, Maja T., Sperhake, Jan P., Wong, Milagros N., Allweiss, Lena, Chilla, Silvia, Heinemann, Axel, Wanner, Nicola, Liu, Shuya, Braun, Fabian, Lu, Shun, Pfefferle, Susanne, Schröder, Ann S., Edler, Carolin, Gross, Oliver, Glatzel, Markus, Wichmann, Dominic, Wiech, Thorsten, Kluge, Stefan, Pueschel, Klaus, Aepfelbacher, Martin, Huber, Tobias B.·2020·New England Journal of Medicine

DOI 10.1056/nejmc2011400PMC PMC7240771

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Multiorgan and Renal Tropism of SARS-CoV-2 In this autopsy series, the authors found that SARS-CoV-2 has an organotropism beyond the respiratory tract, including the kidneys, heart, liver, and brai...

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Background
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BackgroundInfluential
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Background
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Background
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Background
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Background
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Betacoronavirus-specific alternate splicing
Karlebach, G., Aronow, B. J., Baylin, S. B., Butler, D., Foox, J., Levy, S. A., Meydan, C., Mozsary, C., Saravia-Butler, A., Taylor, D. M., et al. (2022) · Genomics · doi:10.1016/j.ygeno.2022.110270 · Cited by 20
“…(COVID-19) affects diverse organ systems, including the lungs, digestive tract, kidneys, heart, and brain and is associated with extremely heterogeneous manifestations that range from minimal symptoms to signiﬁcant hypoxia with acute respiratory distress requiring mechanical ventilation [1, 2].”
Signaling Pathway Reporter Screen with SARS-CoV-2 Proteins Identifies nsp5 as a Repressor of p53 Activity
Kumar, A., Grams, T. R., Bloom, D. C., & Tóth, Z. (2022) · Viruses · doi:10.3390/v14051039 · Cited by 19
“Although SARS-CoV-2 preferentially infects cells in the respiratory tract, the virus has been reported to have a broad organotropism and can cause damage not only in the lungs but also, for example, in the heart, kidneys, liver, and brain [5,6].”
Background
Optimized intramuscular immunization with VSV-vectored spike protein triggers a superior immune response to SARS-CoV-2
Taddeo, A., Veiga, I. B., Devisme, C., Boss, R., Plattet, P., Weigang, S., Kochs, G., Thiel, V., Benarafa, C., & Zimmer, G. (2022) · npj Vaccines · doi:10.1038/s41541-022-00508-7 · Cited by 19
Impact of Comorbidities on SARS-CoV-2 Viral Entry-Related Genes
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Glomerular filtration barrier dysfunction in a self-limiting, RNA virus-induced glomerulopathy resembles findings in idiopathic nephrotic syndromes
Nußhag, C., Stütz, A., Hägele, S., Speer, C., Kälble, F., Eckert, C., Brenner, T., Weigand, M. A., Morath, C. P., Reiser, J., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-76050-0 · Cited by 19
Renal transplantation during the SARS‐CoV‐2 pandemic in the UK: Experience from a large‐volume center
Georgiades, F., Summers, D. M., Butler, A. J., Russell, N., Clatworthy, M. R., & Torpey, N. (2020) · Clinical Transplantation · doi:10.1111/ctr.14150 · Cited by 19
SARS‐CoV‐2 RNA detection in stool samples from acute gastroenteritis cases, Brazil
Fumian, T. M., Malta, F. C., dos Santos, D. R. L., Pauvolid‐Corrêa, A., Fialho, A. M., Leite, J. P. G., & Miagostovich, M. P. (2021) · Journal of Medical Virology · doi:10.1002/jmv.26786 · Cited by 19
“SARS‐CoV‐2 has been detected in organs other than the lungs, including the kidneys, liver, heart, brain, and blood.(7) Several studies have demonstrated the presence of the SARS‐CoV‐2 in stool”
Background
Getting to the Heart of the Matter: Myocardial Injury, Coagulopathy, and Other Potential Cardiovascular Implications of COVID-19
Schmid, A., Petrovic, M. T., Akella, K., Pareddy, A. R., & Velavan, S. S. (2021) · International Journal of Vascular Medicine · doi:10.1155/2021/6693895 · Cited by 19
“The presence of SARS CoV-2 RNA was found in the autopsied hearts [96, 98, 101].”
Background
Acute Kidney Injury in Pediatric Acute SARS-CoV-2 Infection and Multisystem Inflammatory Syndrome in Children (MIS-C): Is There a Difference?
Grewal, M. K., Gregory, M. J., Jain, A., Mohammad, D., Cashen, K., Ang, J. Y., Thomas, R., & Valentini, R. P. (2021) · Frontiers in Pediatrics · doi:10.3389/fped.2021.692256 · Cited by 19
“The renal tropism of the SARS-CoV-2 has been previously demonstrated in autopsy studies of the renal tissue in adult patients who died secondary to SARS-CoV-2 infection (18, 19).”
Background
Characterization of Virus Replication, Pathogenesis, and Cytokine Responses in Syrian Hamsters Inoculated with SARS-CoV-2
Yang, S.-J., Wei, T.-C., Hsu, C.-H., Ho, S.-N., Lai, C.-Y., Huang, S., Chen, Y.-Y., Liu, S., Yu, G., & Dou, H.-Y. (2021) · Journal of Inflammation Research · doi:10.2147/jir.s323026 · Cited by 19
Self-citation
Activation of STAT3 signaling pathway in the kidney of COVID-19 patients
Salem, F. E., Li, X. Z., Hindi, J., Casablanca, N. N. M., Zhong, F., Jamal, S. M. E., Rasheed, M. R. H. A., Li, L., Lee, K., Chan, L., et al. (2021) · Journal of Nephrology · doi:10.1007/s40620-021-01173-0 · Cited by 18
COVID-19 in pediatric population
Evseeva, G. P., Телепнёва, Р. С., Книжникова, Е. В., Супрун, С. В., Пичугина, С. В., Yakovlev, E. I., Galyant, O. I., Козлов, В. К., & Лебедько, О. А. (2021) · Bulletin physiology and pathology of respiration · doi:10.36604/1998-5029-2021-80-100-114 · Cited by 19
“Это облегчает ассоциированное с SARS-CoV-2 повреждение почек, особенно клубочковых клеток, что ведет к клиническим проявлениям повреждения почек у пациентов с COVID-19 даже с нетяжелыми проявлениями заболевания [38].”
Human Taste Cells Express ACE2: a Portal for SARS-CoV-2 InfectionPreprint
Doyle, M. E., Appleton, A., Liu, Q., Yao, Q., Mazucanti, C. H., & Egan, J. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.21.440680 · Cited by 19
COVID-19, what could sepsis, severe acute pancreatitis, gender differences, and aging teach us?
Gallo, C. G., Fiorino, S., Posabella, G., Antonacci, D., Tropeano, A., Pausini, E., Pausini, C., Guarniero, T., Hong, W., Giampieri, E., et al. (2021) · Cytokine · doi:10.1016/j.cyto.2021.155628 · Cited by 17
Lessons for the clinical nephrologist: recurrence of nephrotic syndrome induced by SARS-CoV-2
Doevelaar, A. A. N., Hölzer, B., Seibert, F. S., Bauer, F., Stervbo, U., Rohn, B., Zgoura, P., Schenker, P., Vonbrunn, E., Amann, K., et al. (2020) · Journal of Nephrology · doi:10.1007/s40620-020-00855-5 · Cited by 18
Acute pericarditis and severe acute respiratory syndrome coronavirus 2: Case report
Blagojevic, N., Bosnjakovic, D., Vukomanovic, V., Srdjan, A., Suzic-Lazić, J., & Tadic, M. V. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.09.1440 · Cited by 18
“Most of the case reports published so far have investigated cardiac involvement in COVID-19 patients with severe respiratory tract infections (Zeng et al., 2020; Chen et al., 2020; Cizgici et al., 2020; Kim et al., 2020; Puelles et al., 2020; Hua et al., 2020; Doyen et al., 2020; Farina et al., 2020; Inciardi et al.,…”
Influential
Neuro-COVID-19 is more than anosmia: clinical presentation, neurodiagnostics, therapies, and prognosis
Schweitzer, F., Kleineberg, N. N., Göreci, Y., Onur, O. A., Franke, C., & Warnke, C. (2021) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000930 · Cited by 18
Transplant of SARS-CoV-2–infected Living Donor Liver: Case Report
Nguyen, M., Lee, E. J., Avery, R. K., Dioverti, M. V., Shoham, S., Tobian, A. A. R., Bloch, E. M., Gurakar, A. O., Rizkalla, N. A., Cameron, A. M., et al. (2021) · Transplantation Direct · doi:10.1097/txd.0000000000001178 · Cited by 18
Proteomic insights into SARS-CoV-2 infection mechanisms, diagnosis, therapies and prognostic monitoring methods
Yu, S., Li, X., Xin, Z., Sun, L., & Shi, J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.923387 · Cited by 18
Kidney injury associated with COVID-19 infection and vaccine: A narrative review
Pacheco, I. C. R., Costa, D. M. D. N., Sousa, D. S., Filho, N. S., Silva, G. E. B., & Neves, P. D. M. D. M. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.956158 · Cited by 18
“This is probably due to the high expression of proteins, such as ACE2, TMPRSS 2, and cathepsin L that enable viral infection (4).”
Background
Susceptibility of SARS Coronavirus-2 infection in domestic and wild animals: a systematic review
Rao, S. S., Parthasarathy, K., Sounderrajan, V., Neelagandan, K., Anbazhagan, P., & Chandramouli, V. (2022) · 3 Biotech · doi:10.1007/s13205-022-03416-8 · Cited by 12
SARS-CoV-2 replicates and displays oncolytic properties in clear cell and papillary renal cell carcinoma
Choong, O. K., Jakobsson, R. G., Bergdahl, A. G., Brunet, S., Kärmander, A., Waldenström, J., Arvidsson, Y., Altiparmak, G., Nilsson, J. A., Karlsson, J. W., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0279578 · Cited by 19
SuPAR mediates viral response proteinuria by rapidly changing podocyte function
Wei, C., Datta, P. K., Siegerist, F., Li, J., Sudhini, Y. R., Koh, K. H., Kriho, N., Ismail, A., Luo, S., Fischer, T., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40165-5 · Cited by 18
Integrin αvβ1 facilitates ACE2-mediated entry of SARS-CoV-2
Cai, Z., Bai, H., Ren, D., Xue, B., Liu, Y., Gong, T., Zhang, X., Zhang, P., Zhu, J., Shi, B., et al. (2023) · Virus Research · doi:10.1016/j.virusres.2023.199251 · Cited by 18
“Considering the multi-organ infection in COVID-19 cases (Puelles et al., 2020), a panel of human cell lines derived from different organs were used for pseudotyped-SARS-CoV-2 infection assay, including SW620 (human colon cancer cells), IOSE-80 (human ovarian cancer cells), MDA-MB-231 (human breast…”
Method
SARS-CoV-2 ORF3a Protein as a Therapeutic Target against COVID-19 and Long-Term Post-Infection Effects
Zhang, J., Hom, K., Zhang, C., Nasr, M., Gerzanich, V., Zhang, Y., Tang, Q., Xue, F., Simard, J. M., & Zhao, Y. (2024) · Pathogens · doi:10.3390/pathogens13010075 · Cited by 24
“A similar percentage of kidney complications was also found among those critically ill patients with COVID-19 [99].”
What HIV in the Brain Can Teach Us About SARS-CoV-2 Neurological Complications?
Al‐Harthi, L., Campbell, E. M., Schneider, J. A., & Bennett, D. A. (2020) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2020.0161 · Cited by 18
“The other autopsy studies did not report on brain regions of virus detection, associated pathological changes, or information to inform the route of entry.(62,63) It thus remains unclear if SARS CoV-2 can spread in the brain and undergo productive infection of resident brain cells or alternatively it may infect cells…”
Background
Ultrastructure of cell trafficking pathways and coronavirus: how to recognise the wolf amongst the sheep
Neil, D., Moran, L. B., Horsfield, C. J., Curtis, E., Swann, O. C., Barclay, W., Hanley, B. P., Hollinshead, M. S., & Roufosse, C. A. (2020) · The Journal of Pathology · doi:10.1002/path.5547 · Cited by 18
“In other cases, viral RNA has been found in tissues without data on specific cell types infected: heart [79,82,84,85], skeletal muscle [82], lymph nodes [79], and brain [83].”
Background
ACE2, the kidney and the emergence of COVID-19 two decades after ACE2 discovery
Lores, E., Wysocki, J. A., & BATLLE, D. C. (2020) · Clinical Science · doi:10.1042/cs20200484 · Cited by 18
MR-proAdrenomedullin as a predictor of renal replacement therapy in a cohort of critically ill patients with COVID-19
Roedl, K., Jarczak, D., Fischer, M., Haddad, M., Boenisch, O., de Heer, G., Burdelski, C. M., Frings, D. P., Sensen, B., Karakas, M., et al. (2021) · Biomarkers · doi:10.1080/1354750x.2021.1905067 · Cited by 18
Self-citation
Postmortale Bildgebung der Lunge bei COVID-19-Todesfällen
Kniep, I., Lutter, M., Ron, A. S. R., Edler, C., Püschel, K., Ittrich, H., Heller, M., & Heinemann, A. W. (2020) · Der Radiologe · doi:10.1007/s00117-020-00733-y · Cited by 16
Self-citation
Case 26-2020: A 60-Year-Old Woman with Altered Mental Status and Weakness on the Left Side
Singhal, A. B., González, R. G., Chwalisz, B. K., & Mukerji, S. S. (2020) · New England Journal of Medicine · doi:10.1056/nejmcpc2004976 · Cited by 17
Characteristics and outcomes of patients with COVID-19 admitted to the ICU in a university hospital in São Paulo, Brazil - study protocol
Ferreira, J. C., Ho, Y.-L., Besen, B. A. M. P., Malbuisson, L. M. S., Taniguchi, L. U., Mendes, P. V., Costa, E. L. V., Park, M., Daltro-Oliveira, R., Roepke, R. M. L., et al. (2020) · Clinics · doi:10.6061/clinics/2020/e2294 · Cited by 17
Renal Morphology in Coronavirus Disease: A Literature Review
de Oliveira, P. V. V., Cunha, K. D. A., Neves, P. D. M. D. M., Muniz, M. P. R., Gatto, G. C., Filho, N. S., Guedes, F. L., & Silva, G. (2021) · Medicina · doi:10.3390/medicina57030258 · Cited by 17
“In another series of autopsies, the viral RNA of SARS-CoV-2 in the kidney was quantified, especially in the glomeruli [4].”
Background
Addressing the ‘hypoxia paradox’ in severe COVID-19: literature review and report of four cases treated with erythropoietin analogues
Begemann, M., Groß, O., Wincewicz, D., Hardeland, R., Gastaldi, V. D., Vieta, E., Weißenborn, K., Miskowiak, K. W., Moerer, O., & Ehrenreich, H. (2021) · Molecular Medicine · doi:10.1186/s10020-021-00381-5 · Cited by 18
“Multitropic by nature, it can in severe cases cause multiorgan failure, in particular of lung, heart, and kidney (Puelles et al. 2020).”
Background
Acute Kidney Injury and Renal Replacement Therapy in COVID-19 Versus Other Respiratory Viruses: A Systematic Review and Meta-Analysis
Cau, A., Cheng, M. P., Lee, T., Levin, A., Lee, T. C., Vinh, D. C., Lamontagne, F., Singer, J., Walley, K. R., Murthy, S., et al. (2021) · Canadian Journal of Kidney Health and Disease · doi:10.1177/20543581211052185 · Cited by 18
MPO-ANCA-positive Microscopic Polyangiitis Following COVID-19 Infection
Kawashima, S., Kishimoto, M., Hibino, T., Lee, H., Sato, Y., Komagata, Y., & Kaname, S. (2021) · Internal Medicine · doi:10.2169/internalmedicine.8615-21 · Cited by 16
“The possibility that the virus directly damages renal tissues has also been reported (5-7), although a consensus has not been reached.”
Background
Comparative pathology of the nasal epithelium in K18-hACE2 Tg mice, hACE2 Tg mice, and hamsters infected with SARS-CoV-2
Yü, P., Deng, W., Bao, L., Qu, Y., Xu, Y., Zhao, W., Han, Y., & Qin, C. (2022) · Veterinary Pathology · doi:10.1177/03009858211071016 · Cited by 15
Cardiorenal Syndrome in COVID-19 Patients: A Systematic Review
Lin, L., Chen, Y., Han, D., Yang, A. Z., Wang, Y., & Qi, W. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.915533 · Cited by 18
“ACE2 is also expressed in the heart and kidney, providing a link between coronavirus infection and potential cardiovascular and renal complications (4).”
Background
Molnupiravir as an Early Treatment for COVID-19: A Real Life Study
Pontolillo, M., Ucciferri, C., Borrelli, P., Nicola, M. D., Vecchiet, J., & Falasca, K. (2022) · Pathogens · doi:10.3390/pathogens11101121 · Cited by 17
“It is known that both basophils and eosinophils can produce IL-4, which is an important cytokine for stimulating the proliferation of activated B and T lymphocytes [52,53].”
Background
Enteric nervous system as a target and source of SARS-CoV-2 and other viral infections
Valdetaro, L., Thomasi, B. B. D. M., Ricciardi, M. C., Santos, K. D. M., Coelho‐Aguiar, J. D. M., & Gomes, A. L. T. (2023) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00229.2022 · Cited by 18
Outcomes of COVID-19 Among Hospitalized Patients With Non-dialysis CKD
Coca, A., Burballa, C., Pérez, F. J. C., Pérez‐Sáez, M. J., Bustamante‐Munguira, E., Cerrato, A. O., Dueñas, C., Arenas, M. D., Pérez‐Martínez, J., Ruíz, G., et al. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.615312 · Cited by 17
“Moreover, indirect factors such as systemic hypoxia or coagulation abnormalities commonly associated to COVID-19 pneumonia may further contribute to AKI progression (43, 44).”
Background
Endotheliitis bei COVID-19
Varga, Z. (2020) · Der Pathologe · doi:10.1007/s00292-020-00875-9 · Cited by 17
Lock, Stock and Barrel: Role of Renin-Angiotensin-Aldosterone System in Coronavirus Disease 2019
Zanza, C., Tassi, M. F., Romenskaya, T., Piccolella, F., Abenavoli, L., Franceschi, F., Piccioni, A., Ojetti, V., Saviano, A., Canonico, B., et al. (2021) · Cells · doi:10.3390/cells10071752 · Cited by 17
“Brains of deceased COVID-19 patients showed evidence of oedema and partial neuronal degeneration [85], white matter lesions [94] and direct presence of the SARS-CoV-2 in the brain has been reported [63,96], although other studies were not able to confirm this finding.”
BackgroundResult
Clinical Characteristics and Early Outcomes of Hospitalized COVID-19 Patients with End-Stage Kidney Disease in Saudi Arabia
Hakami, A., Badedi, M., Elsiddig, M., Nadeem, M., Altherwi, N., Rayani, R., & Alhazmi, A. (2021) · International Journal of General Medicine · doi:10.2147/ijgm.s327186 · Cited by 17

Authors: Puelles, V. G., Lütgehetmann, M., Lindenmeyer, M. T., Sperhake, J. P., Wong, M. N., Allweiss, L., Chilla, S., Heinemann, A., Wanner, N., Liu, S., Braun, F., Lu, S., Pfefferle, S., Schröder, A. S., Edler, C., Gross, O., Glatzel, M., Wichmann, D., Wiech, T., Kluge, S., Pueschel, K., Aepfelbacher, M., & Huber, T. B.
Affiliations: University Medical Center Hamburg-Eppendorf (DE)
Universitätsmedizin Göttingen (DE)
Corresponding author: Huber, Tobias B.
ORCID: Puelles, Victor G.
Lütgehetmann, Marc
Lindenmeyer, Maja T.
Wong, Milagros N.
Allweiss, Lena
Wanner, Nicola
Liu, Shuya
Braun, Fabian
Lu, Shun
Pfefferle, Susanne
Edler, Carolin
Gross, Oliver
Glatzel, Markus
Wichmann, Dominic
Wiech, Thorsten
Kluge, Stefan
Aepfelbacher, Martin
Huber, Tobias B.
Venue: New England Journal of Medicine
Publisher: Massachusetts Medical Society
Published: 2020-08-06
Volume: 383
Issue: 6
Pages: 590-592
ISSN: 0028-4793 (ISSN-L)
1533-4406
DOI: 10.1056/nejmc2011400
PMC: PMC7240771
OpenAlex: W3024126428
Cited by: 1,775
References: 4
Citations by year: 2026: 26 · 2025: 73 · 2024: 138 · 2023: 214 · 2022: 338 · 2021: 595 · 2020: 390
FWCI: 50.56
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: New England Journal of Medicine (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
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 › Clinical Neurology › Long-Term Effects of COVID-19
Keywords: SARS-CoV-2, COVID-19 pandemic, kidney, heart, liver, brain, autopsy findings, viral tissue distribution
MeSH terms: Betacoronavirus, COVID-19, SARS-CoV-2, Aged, Aged, 80 and over, Autopsy, Brain, Female, Heart, Humans, Kidney, Liver, Lung, Male, Middle Aged, Pharynx, Pneumonia, Viral, Coronavirus Infections, Viral Load, Viral Tropism, Pandemics

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Multiorgan and Renal Tropism of SARS-CoV-2

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