COVID-19 and the Kidney: From Epidemiology to Clinical Practice

Ida Gagliardi, Gemma Patella, Ashour Michael, Raffaele Serra, Michele Provenzano, Michele Andreucci, Ida Gagliardi, Gemma Patella, Ashour Michael, Raffaele Serra, Michele Provenzano, Michele Andreucci

Abstract

The new respiratory infectious disease coronavirus disease 2019 (COVID-19) that originated in Wuhan, China, in December 2019 and caused by a new strain of zoonotic coronavirus, named severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2), to date has killed over 630,000 people and infected over 15,000,000 worldwide. Most of the deceased patients had pre-existing comorbidities; over 20% had chronic kidney disease (CKD). Furthermore, although SARS-CoV-2 infection is characterized mainly by diffuse alveolar damage and acute respiratory failure, acute kidney injury (AKI) has developed in a high percentage of cases. As AKI has been shown to be associated with worse prognosis, we believe that the impact of SARS-CoV-2 on the kidney should be investigated. This review sets out to describe the main renal aspects of SARS-CoV-2 infection and the role of the virus in the development and progression of kidney damage. In this article, attention is focused on the epidemiology, etiology and pathophysiological mechanisms of kidney damage, histopathology, clinical features in nephropathic patients (CKD, hemodialysis, peritoneal dialysis, AKI, transplantation) and prevention and containment strategies. Although there remains much more to be learned with regards to this disease, nonetheless it is our hope that this review will aid in the understanding and management of SARS-CoV-2 infection.

Keywords: SARS-CoV-2; acute kidney injury; dialysis; pandemic; renal transplantation.

Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Pathophysiological mechanisms of kidney damage associated with coronavirus disease 2019 (COVID-19).
Figure 2
Figure 2
Histological features of kidney from COVID-19 patients.

References

    1. Sun P., Lu X., Xu C., Sun W., Pan B. Understanding of COVID-19 based on current evidence. J. Med. Virol. 2020:10–13. doi: 10.1002/jmv.25722.
    1. Zhu N., Zhang D., Wang W., Li X., Yang B., Song J., Zhao X., Huang B., Shi W., Lu R., et al. A novel coronavirus from patients with pneumonia in China, 2019. N. Engl. J. Med. 2020;382:727–733. doi: 10.1056/NEJMoa2001017.
    1. Numbers S.I.N. Coronavirus disease 2019 (COVID-19) Sci. Total Environ. 2020;2019:200490.
    1. Brazil: WHO Coronavirus Disease (COVID-19) Dashboard. [(accessed on 3 August 2020)]; Available online: .
    1. Shah S.G.S., Farrow A. A commentary on “World Health Organization declares global emergency: A review of the 2019 novel Coronavirus (COVID-19).”. Int. J. Surg. 2020;76:128–129. doi: 10.1016/j.ijsu.2020.03.001.
    1. Bartsch S.M., Ferguson M.C., McKinnell J.A., O’Shea K.J., Wedlock P.T., Siegmund S.S., Lee B.Y. The Potential Health Care Costs and Resource Use Associated with COVID-19 in the United States. Health Aff. 2020;39:927–935. doi: 10.1377/hlthaff.2020.00426.
    1. Chakraborty I., Maity P. COVID-19 outbreak: Migration, effects on society, global environment and prevention. Sci. Total Environ. 2020;728:138882. doi: 10.1016/j.scitotenv.2020.138882.
    1. Cheng Y., Luo R., Wang K., Zhang M., Wang Z., Dong L., Li J., Yao Y. Kidney disease is associated with in-hospital death of patients with COVID-19. Kidney Int. 2020:1–10. doi: 10.1016/j.kint.2020.03.005.
    1. Chen N., Zhou M., Dong X., Qu J., Gong F., Han Y., Qiu Y., Wang J., Liu Y., Wei Y., et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study. Lancet. 2020;395:507–513. doi: 10.1016/S0140-6736(20)30211-7.
    1. Rapezzi C., Ferrari R. The Cardiologist at the time of Coronavirus: A perfect storm. Eur. Heart J. 2020;41:1320–1322. doi: 10.1093/eurheartj/ehaa233.
    1. Boraschi P. COVID-19 Pulmonary Involvement: Is Really an Interstitial Pneumonia? Acad Radiol. 2020;27:900. doi: 10.1016/j.acra.2020.04.010.
    1. Qi F., Qian S., Zhang S., Zhang Z. Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses. Biochem. Biophys. Res. Commun. 2020 doi: 10.1016/j.bbrc.2020.03.044.
    1. 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. Early Transmission Dynamics in Wuhan, China, of Novel Coronavirus-Infected Pneumonia. N. Engl. J. Med. 2020;382:1199–1207. doi: 10.1056/NEJMoa2001316.
    1. Riccardo F., Ajelli M., Andrianou X., Bella A., Del Manso M., Fabiani M., Bellino S., Boros S., Urdiales A.M., Marziano V., et al. Epidemiological characteristics of COVID-19 cases in Italy and estimates of the reproductive numbers one month into the epidemic. medRxiv. 2020 doi: 10.1101/2020.04.08.20056861.
    1. Richardson S., Hirsch J.S., Narasimhan M., Crawford J.M., McGinn T., Davidson K.W., Barnaby D.P., Becker L.B., Chelico J.D., Cohen S.L., et al. Presenting Characteristics, Comorbidities, and Outcomes among 5700 Patients Hospitalized with COVID-19 in the New York City Area. JAMA. 2020 doi: 10.1001/jama.2020.6775.
    1. Onder G., Rezza G., Brusaferro S. Case-Fatality Rate and Characteristics of Patients Dying in Relation to COVID-19 in Italy. JAMA. 2020 doi: 10.1001/jama.2020.4683.
    1. Chow N., Fleming-Dutra K., Gierke R., Hall A., Hughes M., Pilishvili T., Ritchey M., Roguski K., Skoff T., Ussery E. Preliminary Estimates of the Prevalence of Selected Underlying Health Conditions Among Patients with Coronavirus Disease 2019—United States, February 12–March 28, 2020. MMWR. Morb. Mortal. Wkly. Rep. 2020;69:382–386. doi: 10.15585/mmwr.mm6913e2.
    1. Wu Z., McGoogan J.M. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020 doi: 10.1001/jama.2020.2648.
    1. Zimmermann P., Curtis N. COVID-19 in Children, Pregnancy and Neonates: A Review of Epidemiologic and Clinical Features. Pediatr. Infect. Dis. J. 2020;39:469–477. doi: 10.1097/INF.0000000000002700.
    1. Tregoning J.S., Schwarze J. Respiratory viral infections in infants: Causes, clinical symptoms, virology, and immunology. Clin. Microbiol. Rev. 2010;23:74–98. doi: 10.1128/CMR.00032-09.
    1. Michael B., Giuseppe H., Henry B.M. Chronic kidney disease is associated with severe coronavirus disease 2019 (COVID-19) infection. Int. Urol. Nephrol. 2020;2019:9–10. doi: 10.1007/s11255-020-02451-9.
    1. Novel C.P.E.R.E. The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China. Zhonghua Liu Xing Bing Xue Za Zhi. 2020;41:145–151. doi: 10.3760/cma.j.issn.0254-6450.2020.02.003.
    1. Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y., Zhang L., Fan G., Xu J., Gu X., et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497–506. doi: 10.1016/S0140-6736(20)30183-5.
    1. Brienza N., Puntillo F., Romagnoli S., Tritapepe L. Acute Kidney Injury in Coronavirus Disease 2019 Infected Patients: A Meta-Analytic Study. Blood Purif. 2020:1–7. doi: 10.1159/000509274.
    1. Wang D., Hu B., Hu C., Zhu F., Liu X., Zhang J., Wang B., Xiang H., Cheng Z., Xiong Y., et al. Clinical Characteristics of 138 Hospitalized Patients with 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA. 2020;323:1061–1069. doi: 10.1001/jama.2020.1585.
    1. Zhou F., Yu T., Du R., Fan G., Liu Y., Liu Z., Xiang J., Wang Y., Song B., Gu X., et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet. 2020;395:1054–1062. doi: 10.1016/S0140-6736(20)30566-3.
    1. Li Z., Wu M., Yao J., Guo J., Liao X., Song S., Li J., Duan G., Zhou Y., Wu X., et al. Caution on Kidney Dysfunctions of COVID-19 Patients. SSRN Electron. J. 2020:1–25. doi: 10.2139/ssrn.3559601.
    1. Hansrivijit P., Qian C., Boonpheng B., Thongprayoon C., Vallabhajosyula S., Cheungpasitporn W., Ghahramani N. Incidence of acute kidney injury and its association with mortality in patients with COVID-19: A meta-analysis. J. Investig. Med. Off. Publ. Am. Fed. Clin. Res. 2020 doi: 10.1136/jim-2020-001407.
    1. Wang L., Li X., Chen H., Yan S., Li D., Li Y., Gong Z. Coronavirus Disease 19 Infection Does Not Result in Acute Kidney Injury: An Analysis of 116 Hospitalized Patients from Wuhan, China. Am. J. Nephrol. 2020:1–6. doi: 10.1159/000507471.
    1. Zhang J., Litvinova M., Wang W., Wang Y., Deng X., Chen X., Li M., Zheng W., Yi L., Chen X., et al. Articles Evolving epidemiology and transmission dynamics of coronavirus disease 2019 outside Hubei province, China: A descriptive and modelling study. Lancet Infect. Dis. 2020;3099:1–10. doi: 10.1016/S1473-3099(20)30230-9.
    1. Percentuale Pazienti Raggiunti Dati Survey—vs Dati Censimento dic 2018. [(accessed on 3 August 2020)]; Available online: .
    1. Valley A. First considerations on the SARS-CoV-2 epidemic in the Dialysis Units of Piedmont and Aosta Valley, Northern Italy. J. Nephrol. 2020;40:2–4. doi: 10.1007/s40620-020-00732-1.
    1. Ahlquist P., Noueiry A.O., Lee W.-M., Kushner D.B., Dye B.T. Host factors in positive-strand RNA virus genome replication. J. Virol. 2003;77:8181–8186. doi: 10.1128/JVI.77.15.8181-8186.2003.
    1. Corman V.M., Lienau J., Witzenrath M. Coronaviruses as the cause of respiratory infections. Internist (Berl) 2019;60:1136–1145. doi: 10.1007/s00108-019-00671-5.
    1. Perico L., Benigni A., Remuzzi G. Should covid-19 concern nephrologists? Why and to what extent? The emerging impasse of angiotensin blockade. Nephron. 2020;24126 doi: 10.1159/000507305.
    1. Ji W., Wang W., Zhao X., Zai J., Li X. Cross-species transmission of the newly identified coronavirus 2019-nCoV. J. Med. Virol. 2020;92:433–440. doi: 10.1002/jmv.25682.
    1. Lu R., Zhao X., Li J., Niu P., Yang B., Wu H., Wang W., Song H., Huang B., Zhu N., et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: Implications for virus origins and receptor binding. Lancet. 2020;395:565–574. doi: 10.1016/S0140-6736(20)30251-8.
    1. Lam T.T.-Y., Shum M.H.-H., Zhu H.-C., Tong Y.-G., Ni X.-B., Liao Y.-S., Wei W., Cheung W.Y.-M., Li W.-J., Li L.-F., et al. Identification of 2019-nCoV related coronaviruses in Malayan pangolins in southern China. BioRxiv. 2020;583:282–285. doi: 10.1101/2020.02.13.945485.
    1. Li X., Zai J., Zhao Q., Nie Q., Li Y., Foley B.T., Chaillon A. Evolutionary history, potential intermediate animal host, and cross-species analyses of SARS-CoV-2. J. Med. Virol. 2020 doi: 10.1002/jmv.25731.
    1. Wu A., Peng Y., Huang B., Ding X., Wang X., Niu P., Meng J., Zhu Z., Zhang Z., Wang J., et al. Genome Composition and Divergence of the Novel Coronavirus (2019-nCoV) Originating in China. Cell Host Microbe. 2020;27:325–328. doi: 10.1016/j.chom.2020.02.001.
    1. Morse J.S., Lalonde T., Xu S., Liu W.R. Learning from the Past: Possible Urgent Prevention and Treatment Options for Severe Acute Respiratory Infections Caused by 2019-nCoV. Chembiochem. 2020;21:730–738. doi: 10.1002/cbic.202000047.
    1. He J., Tao H., Yan Y., Huang S.-Y., Xiao Y. Molecular mechanism of evolution and human infection with the novel coronavirus (2019-nCoV) BioRxiv. 2020;12:428. doi: 10.1101/2020.02.17.952903.
    1. Hoffmann M., Kleine-Weber H., Schroeder S., Kruger N., Herrler T., Erichsen S., Schiergens T.S., Herrler G., Wu N.-H., Nitsche A., et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell. 2020 doi: 10.1016/j.cell.2020.02.052.
    1. Yan R., Zhang Y., Li Y., Xia L., Guo Y., Zhou Q. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science. 2020;367:1444–1448. doi: 10.1126/science.abb2762.
    1. Liu Z., Xiao X., Wei X., Li J., Yang J., Tan H., Zhu J., Zhang Q., Wu J., Liu L. Composition and divergence of coronavirus spike proteins and host ACE2 receptors predict potential intermediate hosts of SARS-CoV-2. J. Med. Virol. 2020 doi: 10.1002/jmv.25726.
    1. Ye M., Wysocki J., William J., Soler M.J., Cokic I., Batlle D. Glomerular localization and expression of Angiotensin-converting enzyme 2 and Angiotensin-converting enzyme: Implications for albuminuria in diabetes. J. Am. Soc. Nephrol. 2006;17:3067–3075. doi: 10.1681/ASN.2006050423.
    1. Zou X., Chen K., Zou J., Han P., Hao J., Han Z. Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection. Front. Med. 2020 doi: 10.1007/s11684-020-0754-0.
    1. Deng Y.-Y., Zheng Y., Cai G.-Y., Chen X.-M., Hong Q. Single-cell RNA sequencing data suggest a role for angiotensin-converting enzyme 2 in kidney impairment in patients infected with 2019-nCoV. Chin. Med. J. 2020 doi: 10.1097/CM9.0000000000000783.
    1. Zhang Z., Zhu Z., Chen W., Cai Z., Xu B., Tan Z., Wu A., Ge X., Guo X., Tan Z., et al. Cell membrane proteins with high N-glycosylation, high expression and multiple interaction partners are preferred by mammalian viruses as receptors. Bioinformatics. 2019;35:723–728. doi: 10.1093/bioinformatics/bty694.
    1. Holmes R.S., Spradling-Reeves K.D., Cox L.A. Mammalian Glutamyl Aminopeptidase Genes (ENPEP) and Proteins: Comparative Studies of a Major Contributor to Arterial Hypertension. J. Data Mining Genomics Proteomics. 2017;8 doi: 10.4172/2153-0602.1000211.
    1. Glowacka I., Bertram S., Herzog P., Pfefferle S., Steffen I., Muench M.O., Simmons G., Hofmann H., Kuri T., Weber F., et al. Differential downregulation of ACE2 by the spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus NL63. J. Virol. 2010;84:1198–1205. doi: 10.1128/JVI.01248-09.
    1. Zou Z., Yan Y., Shu Y., Gao R., Sun Y., Li X., Ju X., Liang Z., Liu Q., Zhao Y., et al. Angiotensin-converting enzyme 2 protects from lethal avian influenza A H5N1 infections. Nat. Commun. 2014;5:3594. doi: 10.1038/ncomms4594.
    1. Ye R., Liu Z. ACE2 exhibits protective effects against LPS-induced acute lung injury in mice by inhibiting the LPS-TLR4 pathway. Exp. Mol. Pathol. 2020;113:104350. doi: 10.1016/j.yexmp.2019.104350.
    1. Guzzi P.H., Mercatelli D., Ceraolo C., Giorgi F.M. Master Regulator Analysis of the SARS-CoV-2/Human Interactome. J. Clin. Med. 2020;9:982. doi: 10.3390/jcm9040982.
    1. Felice C., Nardin C., Di Tanna G.L., Grossi U., Bernardi E., Scaldaferri L., Romagnoli M., Tonon L., Cavasin P., Novello S., et al. Use of RAAS inhibitors and risk of clinical deterioration in COVID-19: Results from an Italian cohort of 133 hypertensives. Am. J. Hypertens. 2020 doi: 10.1093/ajh/hpaa096.
    1. Jessup J.A., Gallagher P.E., Averill D.B., Brosnihan K.B., Tallant E.A., Chappell M.C., Ferrario C.M. Effect of angiotensin II blockade on a new congenic model of hypertension derived from transgenic Ren-2 rats. Am. J. Physiol. Heart Circ. Physiol. 2006;291:H2166–H2172. doi: 10.1152/ajpheart.00061.2006.
    1. Li F. Structure, Function, and Evolution of Coronavirus Spike Proteins. Annu. Rev. Virol. 2016;3:237–261. doi: 10.1146/annurev-virology-110615-042301.
    1. Song W., Gui M., Wang X., Xiang Y. Cryo-EM structure of the SARS coronavirus spike glycoprotein in complex with its host cell receptor ACE2. PLoS Pathog. 2018;14:e1007236. doi: 10.1371/journal.ppat.1007236.
    1. Wan Y., Shang J., Graham R., Baric R.S., Li F. Receptor Recognition by the Novel Coronavirus from Wuhan: An Analysis Based on Decade-Long Structural Studies of SARS Coronavirus. J. Virol. 2020;94 doi: 10.1128/JVI.00127-20.
    1. Zumla A., Chan J.F.W., Azhar E.I., Hui D.S.C., Yuen K.-Y. Coronaviruses—Drug discovery and therapeutic options. Nat. Rev. Drug Discov. 2016;15:327–347. doi: 10.1038/nrd.2015.37.
    1. Bertram S., Heurich A., Lavender H., Gierer S., Danisch S., Perin P., Lucas J.M., Nelson P.S., Pohlmann S., Soilleux E.J. Influenza and SARS-coronavirus activating proteases TMPRSS2 and HAT are expressed at multiple sites in human respiratory and gastrointestinal tracts. PLoS ONE. 2012;7:e35876. doi: 10.1371/journal.pone.0035876.
    1. Hoffmann M., Kleine-Weber H., Krüger N., Müller M., Drosten C., Pöhlmann S. The novel coronavirus 2019 (2019-nCoV) uses the SARS-coronavirus receptor ACE2 and the cellular protease TMPRSS2 for entry into target cells. BioRxiv. 2020 doi: 10.1101/2020.01.31.929042.
    1. Pan X.-W., Xu D., Zhang H., Zhou W., Wang L.-H., Cui X.-G. Identification of a potential mechanism of acute kidney injury during the COVID-19 outbreak: A study based on single-cell transcriptome analysis. Intensive Care Med. 2020 doi: 10.1007/s00134-020-06026-1.
    1. Batlle D., Soler M.J., Sparks M.A., Hiremath S., South A.M., Welling P.A., Swaminathan S. Acute Kidney Injury in COVID-19: Emerging Evidence of a Distinct Pathophysiology. J. Am. Soc. Nephrol. 2020;31:1380–1383. doi: 10.1681/ASN.2020040419.
    1. Diao B., Feng Z., Wang C., Wang H., Liu L., Wang C., Wang R., Liu Y., Liu Y., Wang G., et al. Human Kidney is a Target for Novel Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection. MedRxiv. 2020;2 doi: 10.1101/2020.03.04.20031120.
    1. Su H., Yang M., Wan C., Yi L., Tang F., Zhu H., Yi F., Yang H., Fogo A.B., Nie X., et al. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int. 2020 doi: 10.1016/j.kint.2020.04.003.
    1. Meng X.-M., Nikolic-Paterson D.J., Lan H.Y. Inflammatory processes in renal fibrosis. Nat. Rev. Nephrol. 2014;10:493–503. doi: 10.1038/nrneph.2014.114.
    1. Saffarzadeh M., Juenemann C., Queisser M.A., Lochnit G., Barreto G., Galuska S.P., Lohmeyer J., Preissner K.T. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: A predominant role of histones. PLoS ONE. 2012;7:e32366. doi: 10.1371/journal.pone.0032366.
    1. Pober J.S., Sessa W.C. Inflammation and the blood microvascular system. Cold Spring Harb. Perspect. Biol. 2014;7:a016345. doi: 10.1101/cshperspect.a016345.
    1. Tisoncik J.R., Korth M.J., Simmons C.P., Farrar J., Martin T.R., Katze M.G. Into the eye of the cytokine storm. Microbiol. Mol. Biol. Rev. 2012;76:16–32. doi: 10.1128/MMBR.05015-11.
    1. Kuppalli K., Rasmussen A.L. A glimpse into the eye of the COVID-19 cytokine storm. EBioMedicine. 2020;55:102789. doi: 10.1016/j.ebiom.2020.102789.
    1. Liu J., Li S., Liu J., Liang B., Wang X., Wang H., Li W., Tong Q., Yi J., Zhao L., et al. Longitudinal characteristics of lymphocyte responses and cytokine profiles in the peripheral blood of SARS-CoV-2 infected patients. EBioMedicine. 2020;55 doi: 10.1016/j.ebiom.2020.102763.
    1. Kim K.D., Zhao J., Auh S., Yang X., Du P., Tang H., Fu Y.-X. Adaptive immune cells temper initial innate responses. Nat. Med. 2007;13:1248–1252. doi: 10.1038/nm1633.
    1. Lagunas-Rangel F.A., Chávez-Valencia V. High IL-6/IFN-γ ratio could be associated with severe disease in COVID-19 patients. J. Med. Virol. 2020 doi: 10.1002/jmv.25900.
    1. Fensterl V., Sen G.C. Interferons and viral infections. Biofactors. 2009;35:14–20. doi: 10.1002/biof.6.
    1. McLoughlin R.M., Witowski J., Robson R.L., Wilkinson T.S., Hurst S.M., Williams A.S., Williams J.D., Rose-John S., Jones S.A., Topley N. Interplay between IFN-gamma and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation. J. Clin. Investig. 2003;112:598–607. doi: 10.1172/JCI17129.
    1. Chu K.H., Tsang W.K., Tang C.S., Lam M.F., Lai F.M., To K.F., Fung K.S., Tang H.L., Yan W.W., Chan H.W.H., et al. Acute renal impairment in coronavirus-associated severe acute respiratory syndrome. Kidney Int. 2005;67:698–705. doi: 10.1111/j.1523-1755.2005.67130.x.
    1. Petejova N., Martinek A. Acute kidney injury due to rhabdomyolysis and renal replacement therapy: A critical review. Crit. Care. 2014;18 doi: 10.1186/cc13897.
    1. Mizuiri S., Ohashi Y. ACE and ACE2 in kidney disease. World J. Nephrol. 2015;4:74–82. doi: 10.5527/wjn.v4.i1.74.
    1. Varga Z., Flammer A.J., Steiger P., Haberecker M., Andermatt R., Zinkernagel A.S., Mehra M.R., Schuepbach R.A., Ruschitzka F., Moch H. Endothelial COVID. Lancet. 2020;6736:19–20. doi: 10.1016/S0140-6736(20)30937-5.
    1. Wang K., Chen W., Zhou Y.-S., Lian J.-Q., Zhang Z., Du P., Gong L., Zhang Y., Cui H., Geng J.-J., et al. SARS-CoV-2 invades host cells via a novel route: CD147-spike protein. BioRxiv. 2020 doi: 10.1101/2020.03.14.988345.
    1. Chen G., Wu D., Guo W., Cao Y., Huang D., Wang H., Wang T., Zhang X., Chen H., Yu H., et al. Clinical and immunologic features in severe and moderate Coronavirus Disease 2019. J. Clin. Investig. 2020;130:2620–2629. doi: 10.1172/JCI137244.
    1. Naicker S., Yang C.W., Hwang S.J., Liu B.C., Chen J.H., Jha V. The Novel Coronavirus 2019 epidemic and kidneys. Kidney Int. 2020;97:824–828. doi: 10.1016/j.kint.2020.03.001.
    1. Abbate M., Zoja C., Remuzzi G. How does proteinuria cause progressive renal damage? J. Am. Soc. Nephrol. 2006;17:2974–2984. doi: 10.1681/ASN.2006040377.
    1. Borrelli S., Garofalo C., Mallamaci F., Tripepi G., Stanzione G., Provenzano M., Conte G., De Nicola L., Zoccali C., Minutolo R. Short-term blood pressure variability in nondialysis chronic kidney disease patients: Correlates and prognostic role on the progression of renal disease. J. Hypertens. 2018;36:2398–2405. doi: 10.1097/HJH.0000000000001825.
    1. Luan J., Lu Y., Jin X., Zhang L. Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection. Biochem. Biophys. Res. Commun. 2020 doi: 10.1016/j.bbrc.2020.03.047.
    1. Zhou P., Yang X., Wang X., Hu B., Zhang L., Zhang W., Guo H., Jiang R., Liu M., Chen Y., et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579 doi: 10.1038/s41586-020-2012-7.
    1. Fan C., Li K., Ding Y., Lu W., Wang J. ACE2 Expression in Kidney and Testis May Cause Kidney and Testis Damage After 2019-nCoV Infection. MedRxiv. 2020 doi: 10.1101/2020.02.12.20022418.
    1. Lin W., Hu L., Zhang Y., Ooi J.D., Meng T., Jin P., Ding X. Single-cell Analysis of ACE2 Expression in Human Kidneys and Bladders Reveals a Potential Route of 2019-nCoV Infection. BioRxiv. 2020;14:185–192. doi: 10.1007/s11684-020-0754-0.
    1. Takano T., Elimam H., Cybulsky A. Complement-Mediated Cellular Injury. Semin. Nephrol. 2013;33:586–601. doi: 10.1016/j.semnephrol.2013.08.009.
    1. David S., Biancone L., Caserta C., Bussolati B., Cambi V., Camussi G. Alternative pathway complement activation induces proinflammatory activity in human proximal tubular epithelial cells. Nephrol. Dial. Transplant. 1997;12:51–56. doi: 10.1093/ndt/12.1.51.
    1. Istituto Superiore di Sanità, “Sorveglianza Integrata COVID-19: I Principali Dati Nazionali”. [(accessed on 3 August 2020)]; Available online: .
    1. Goyal P., Choi J.J., Pinheiro L.C., Schenck E.J., Chen R., Jabri A., Satlin M.J., Campion T.R.J., Nahid M., Ringel J.B., et al. Clinical Characteristics of Covid-19 in New York City. N. Engl. J. Med. 2020 doi: 10.1056/NEJMc2010419.
    1. Jin X., Lian J.-S., Hu J.-H., Gao J., Zheng L., Zhang Y.-M., Hao S.-R., Jia H.-Y., Cai H., Zhang X.-L., et al. Epidemiological, clinical and virological characteristics of 74 cases of coronavirus-infected disease 2019 (COVID-19) with gastrointestinal symptoms. Gut. 2020 doi: 10.1136/gutjnl-2020-320926.
    1. City N.Y. Coronavirus Disease 2019 in Children—United States. MMWR Morb. Mortal. Wkly Rep. 2020;69:422–426.
    1. Dong Y., Mo X., Hu Y., Qi X., Jiang F., Jiang Z., Tong S. Epidemiology of COVID-19 among Children in China. Pediatrics. 2020;145:e20200702. doi: 10.1542/peds.2020-0702.
    1. Viner R.M., Whittaker E. Comment Kawasaki-like disease: Emerging complication during the COVID-19 pandemic. Lancet. 2020;6736:19–20. doi: 10.1016/S0140-6736(20)31129-6.
    1. Zhang J., Litvinova M., Liang Y., Wang Y., Wang W., Zhao S., Wu Q., Merler S., Viboud C., Vespignani A., et al. Changes in contact patterns shape the dynamics of the COVID-19 outbreak in China. Science. 2020;368:1481–1486. doi: 10.1126/science.abb8001.
    1. Verdoni L., Mazza A., Gervasoni A., Martelli L., Ruggeri M., Ciuffreda M., Bonanomi E., Antiga L.D. Articles An outbreak of severe Kawasaki-like disease at the Italian epicentre of the SARS-CoV-2 epidemic: An observational cohort study. Lancet. 2020;6736:1–8. doi: 10.1016/S0140-6736(20)31103-X.
    1. Guidance: Paediatric Multisystem Inflammatory Syndrome Temporally Associated with COVID-19. [(accessed on 3 August 2020)]; Available online: .
    1. Klok F.A., Kruip M.J.H.A., van der Meer N.J.M., Arbous M.S., Gommers D.A.M.P.J., Kant K.M., Kaptein F.H.J., van Paassen J., Stals M.A.M., Huisman M.V., et al. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb. Res. 2020 doi: 10.1016/j.thromres.2020.04.013.
    1. Aly M.H., Rahman S.S., Ahmed W.A., Alghamedi M.H., Al Shehri A.A., Alkalkami A.M., Hassan M.H. Indicators of critical illness and predictors of mortality in COVID-19 patients. Infect. Drug Resist. 2020;13:1995–2000. doi: 10.2147/IDR.S261159.
    1. Guan W.J., Liang W.H., Zhao Y., Liang H.R., Chen Z.S., Li Y.M., Liu X.Q., Chen R.C., Tang C.L., Wang T., et al. Comorbidity and its impact on 1,590 patients with Covid-19 in China: A nationwide analysis. Eur. Respir. J. 2020;55 doi: 10.1183/13993003.00547-2020.
    1. Sibbel S., Sato R., Hunt A., Turenne W., Brunelli S.M. The clinical and economic burden of pneumonia in patients enrolled in Medicare receiving dialysis: A retrospective, observational cohort study. BMC Nephrol. 2016;17:1–9. doi: 10.1186/s12882-016-0412-6.
    1. Ielapi N., Licastro N., Provenzano M., Andreucci M., de Franciscis S., Serra R. Cardiovascular disease as a biomarker for an increased risk of COVID-19 infection and related poor prognosis. Biomark. Med. 2020;14:713–716. doi: 10.2217/bmm-2020-0201.
    1. Jung J.Y., Park B.H., Hong S.B., Koh Y., Suh G.Y., Jeon K., Koh S.O., Kim J.Y., Cho J.H., Choi H.S., et al. Acute kidney injury in critically ill patients with pandemic influenza A pneumonia 2009 in Korea: A multicenter study. J. Crit. Care. 2011;26:577–585. doi: 10.1016/j.jcrc.2011.02.012.
    1. Antonio G.E., Wong K.T., Hui D.S.C., Lee N., Yuen E.H.Y., Wu A., Chung S.S.C., Sung J.J.Y., Ahuja A.T. Imaging of severe acute respiratory syndrome in Hong Kong. Am. J. Roentgenol. 2003;181:11–17. doi: 10.2214/ajr.181.1.1810011.
    1. Betjes M.G.H. Immune cell dysfunction and inflammation in end-stage renal disease. Nat. Rev. Nephrol. 2013;9:255–265. doi: 10.1038/nrneph.2013.44.
    1. Wilson J.G., Calfee C.S. ARDS Subphenotypes: Understanding a Heterogeneous Syndrome. Crit. Care. 2020;24 doi: 10.1186/s13054-020-2778-x.
    1. Hirsch J.S., Ng J.H., Ross D.W., Sharma P., Shah H.H., Barnett R.L., Hazzan A.D., Fishbane S., Jhaveri K.D., Abate M., et al. Acute kidney injury in patients hospitalized with COVID-19. Kidney Int. 2020 doi: 10.1016/j.kint.2020.05.006.
    1. Fanelli V., Fiorentino M., Cantaluppi V., Gesualdo L., Stallone G., Ronco C., Castellano G. Acute kidney injury in SARS-CoV-2 infected patients. Crit. Care. 2020;24:155. doi: 10.1186/s13054-020-02872-z.
    1. Zhang F., Liang Y. Potential risk of the kidney vulnerable to novel coronavirus 2019 infection. Am. J. Physiol. Renal. Physiol. 2020;318:F1136–F1137. doi: 10.1152/ajprenal.00085.2020.
    1. Lim J.-H., Park S.-H., Jeon Y., Cho J.-H., Jung H.-Y., Choi J.-Y., Kim C.-D., Lee Y.-H., Seo H., Lee J., et al. Fatal Outcomes of COVID-19 in Patients with Severe Acute Kidney Injury. J. Clin. Med. 2020;9:1718. doi: 10.3390/jcm9061718.
    1. Pei G., Zhang Z., Peng J., Liu L., Zhang C., Yu C., Ma Z., Huang Y., Liu W., Yao Y., et al. Renal Involvement and Early Prognosis in Patients with COVID-19 Pneumonia. J. Am. Soc. Nephrol. 2020;31:1157–1165. doi: 10.1681/ASN.2020030276.
    1. Ronco C., Reis T., Husain-syed F. Viewpoint Management of acute kidney injury in patients with COVID-19. Lancet Respir. 2020;2019:1–5. doi: 10.1016/S2213-2600(20)30229-0.
    1. Nalesso F., Garzotto F., Cattarin L., Gobbi L., Qassim L., Sgarabotto L., Tiberio I., Calò L.A. A Continuous Renal Replacement Therapy Protocol for Patients with Acute Kidney Injury in Intensive Care Unit with COVID-19. J. Clin. Med. 2020;9:1529. doi: 10.3390/jcm9051529.
    1. Grasselli G., Zangrillo A., Zanella A., Antonelli M., Cabrini L., Castelli A., Cereda D., Coluccello A., Foti G., Fumagalli R., et al. Baseline Characteristics and Outcomes of 1591 Patients Infected with SARS-CoV-2 Admitted to ICUs of the Lombardy Region, Italy. JAMA. 2020;323:1574–1581. doi: 10.1001/jama.2020.5394.
    1. Covid-19—Registro ERA-EDTA. [(accessed on 3 August 2020)]; Available online:
    1. Kwan B.C., Leung C., Szeto C., Wong V.W., Cheng Y., Yu A.W., Li P.K. Severe Acute Respiratory Syndrome in Dialysis Patients. J. Am. Soc. Nephrol. 2004:1883–1888. doi: 10.1097/01.ASN.0000131522.16404.1F.
    1. Xiong F., Tang H., Liu L., Tu C., Tian J., Lei C., Liu J., Dong J., Chen W., Wang X., et al. Clinical Characteristics of and Medical Interventions for COVID-19 in Hemodialysis Patients in Wuhan, China. J. Am. Soc. Nephrol. 2020;31:1387–1397. doi: 10.1681/ASN.2020030354.
    1. Ferrey A.J., Choi G., Hanna R.M. Nephrology A Case of Novel Coronavirus Disease 19 in a Chronic Hemodialysis Patient Presenting with Gastroenteritis and Developing Severe Pulmonary Disease. Am. J. Nephrol. 2020;92868:337–342. doi: 10.1159/000507417.
    1. Rubens G., Freitas R., Fernandes L., Agena F., Jaluul O., Silva C., Brambate F., Lemos C., David- E., Galante N.Z. Aging and End Stage Renal Disease Cause a Decrease in Absolute Circulating Lymphocyte Counts with a Shift to a Memory Profile and Diverge in Treg Population. Aging Dis. 2019;10:49–61.
    1. Tang B., Li S., Xiong Y., Tian M., Yu J., Xu L., Zhang L., Li Z., Ma J. Coronavirus Disease 2019 (COVID-19) Pneumonia in a Hemodialysis Patient. Kidney Med. 2020;2:354–358. doi: 10.1016/j.xkme.2020.03.001.
    1. Second SIN Survey on COVID-19 and Impact on Dialysis and Transplant Patients, Dialysis Centers and Nephrology Staff. [(accessed on 3 August 2020)]; Available online: .
    1. Gao Y., Xi H., Chen L. Emergency Surgery in Suspected COVID-19 Patients With Acute Abdomen: Case Series and Perspectives. Ann. Surg. 2020;272:38–39. doi: 10.1097/SLA.0000000000003961.
    1. Vischini G., Alonzo S.D., Grandaliano G., Ascenzo F.M.D. SARS-CoV-2 in the peritoneal waste in a patient treated with peritoneal dialysis. Kidney Int. 2020:2093. doi: 10.1016/j.kint.2020.05.005.
    1. Precautionary Measures for PD Patients. [(accessed on 3 August 2020)]; Available online: .
    1. Fishman J.A., Grossi P.A. Novel Coronavirus-19 (COVID-19) in the immunocompromised transplant recipient: #Flatteningthecurve. Am. J. Transplant. 2020 doi: 10.1111/ajt.15890.
    1. Zhu L., Xu X., Ma K., Yang J., Guan H., Chen S., Chen Z., Chen G. Successful recovery of COVID-19 pneumonia in a renal transplant recipient with long-term immunosuppression. Am. J. Transplant. 2020:1–5. doi: 10.1111/ajt.15869.
    1. Alberici F., Delbarba E., Manenti C., Econimo L., Valerio F., Pola A., Maffei C., Possenti S., Zambetti N., Moscato M., et al. A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia. Kidney Int. 2020:1–6. doi: 10.1016/j.kint.2020.04.002.
    1. Akalin E., Azzi Y., Bartash R., Seethamraju H., Parides M., Hemmige V., Ross M., Forest S., Goldstein Y.D., Ajaimy M., et al. Covid-19 and Kidney Transplantation. N. Engl. J. Med. 2020 doi: 10.1056/NEJMc2011117.
    1. Early Description of Coronavirus 2019 Disease in Kidney Transplant Recipients in New York. J. Am. Soc. Nephrol. 2020;31:1150–1156. doi: 10.1681/ASN.2020030375.
    1. Husain S.A., Dube G., Morris H., Fernandez H., Chang J., Paget K., Sritharan S., Patel S., Pawliczak O., Boehler M., et al. Article Early Outcomes of Outpatient Management of Kidney Transplant Recipients with Coronavirus Disease 2019. Clin. J. Am. Soc. Nephrol. 2020:1–5. doi: 10.2215/CJN.05170420.
    1. Kumar D., Michaels M.G., Morris M.I., Green M., Avery R.K., Liu C., Danziger-isakov L., Stosor V., Estabrook M., Gantt S., et al. Recipients of Solid-Organ Transplants: A Multicentre Cohort Study. Lancet. 2011;10:521–526. doi: 10.1016/S1473-3099(10)70133-X.
    1. Syed-Ahmed M., Narayanan M. Immune Dysfunction and Risk of Infection in Chronic Kidney Disease. Adv. Chronic Kidney Dis. 2019;26:8–15. doi: 10.1053/j.ackd.2019.01.004.
    1. Glst R. Raccomandazioni per la Gestione Dell’ Emergenza da SARS-CoV-2 nei Reparti e Ambulatori Nefrologici, nei Centri Dialisi e Negli Ambulatori Trapianti. [(accessed on 3 August 2020)]; Available online: .
    1. Basile C., Combe C., Pizzarelli F., Covic A., Davenport A., Kanbay M., Kirmizis D., Schneditz D., van der Sande F., Mitra S. Recommendations for the prevention, mitigation and containment of the emerging SARS-CoV-2 (COVID-19) pandemic in haemodialysis centres. Nephrol. Dial. Transplant. 2020;35:737–741. doi: 10.1093/ndt/gfaa069.
    1. Zeuschner P., Sester U., Stöckle M., Saar M., Zompolas I., El-Bandar N., Liefeldt L., Budde K., Öllinger R., Ritschl P., et al. Should We Perform Old-for-Old Kidney Transplantation during the COVID-19 Pandemic? The Risk for Post-Operative Intensive Stay. J. Clin. Med. 2020;9:1835. doi: 10.3390/jcm9061835.
    1. Ahmed O., Brockmeier D., Lee K., Chapman W.C., Doyle M.B. Organ Donation during the Covid-19 pandemic. Am. J. Transplant. 2020 doi: 10.1111/ajt.16199.
    1. Guan W.J., Ni Z.Y., Hu Y., Liang W.H., Ou C.Q., He J.X., Liu L., Shan H., Lei C.L., Hui D.S.C., et al. Clinical Characteristics of Coronavirus Disease 2019 in China. N. Engl. J. Med. 2020 doi: 10.1056/NEJMoa2002032.
    1. Coppolino G., Presta P., Nicotera R., Placida G., Vita C., Carullo N., Andreucci M., Bolignano D., Castagna A., Ruotolo G. COVID-19 and renal disease in elderly patients. Geriatr. Care. 2020;6 doi: 10.4081/gc.2020.9029.
    1. Ikizler T.A. COVID-19 and Dialysis Units: What Do We Know Now and What Should We Do? Am. J. Kidney Dis. 2020 doi: 10.1053/j.ajkd.2020.03.008.
    1. Chinese Society of Nephrology Recommendations for prevention and control of novel coronavirus infection in blood purification center (room) from the Chinese Medical Association Nephrology Branch. Chin. J. Nephrol. 2020;36:82–84.
    1. Castagnoli R., Votto M., Licari A., Brambilla I., Bruno R., Perlini S., Rovida F., Baldanti F., Marseglia G.L. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Infection in Children and Adolescents: A Systematic Review. JAMA Pediatr. 2020 doi: 10.1001/jamapediatrics.2020.1467.
    1. Rombolà G., Heidempergher M., Pedrini L., Farina M., Aucella F., Messa P., Brunori G. Practical indications for the prevention and management of SARS-CoV-2 in ambulatory dialysis patients: Lessons from the first phase of the epidemics in Lombardy. J. Nephrol. 2020;33:193–196. doi: 10.1007/s40620-020-00727-y.
    1. Kliger A.S., Cozzolino M., Jha V. Managing the COVID-19 Pandemic: International Comparisons in Dialysis Patients. Kidney Int. 2020 doi: 10.1016/j.kint.2020.04.007.
    1. SARS-COV2—COVID19 Raccomandazioni per L’Assistenza Infermieristica al Paziente Dializzato e Trapiantato. [(accessed on 3 August 2020)]; Available online: .
    1. Yang L., Tian D., Liu W. Strategies for vaccine development of COVID-19. Sheng Wu Gong Cheng Xue Bao. 2020;36:593–604. doi: 10.13345/j.cjb.200094.
    1. Thanh Le T., Andreadakis Z., Kumar A., Gómez Román R., Tollefsen S., Saville M., Mayhew S. The COVID-19 vaccine development landscape. Nat. Rev. Drug Discov. 2020;19:305–306. doi: 10.1038/d41573-020-00073-5.
    1. Alberici F., Del Barba E., Manenti C., Econimo L., Pola A., Maffei C., Possenti S., Gaggia P., Bove S., Malberti F., et al. Gestione del paziente in dialisi e con trapianto di rene in corso di infezione da coronavirus Covid-19. GIN. 2020;2:1–6.
    1. Martinez M.A. Compounds with Therapeutic Potential against Novel Respiratory 2019 Coronavirus. Antimicrob. Agents Chemother. 2020;64 doi: 10.1128/AAC.00399-20.
    1. Jie Z., He H., Xi H., Zhi Z. Expert consensus on chloroquine phosphate for the treatment of novel coronavirus pneumonia. Zhonghua Jie He He Hu Xi Za Zhi. 2020;43:E019. doi: 10.3760/cma.j.issn.1001-0939.2020.0019.
    1. Tomcsányi J., Tomcsányi K. Hazard of acquired long QT syndrome during coronavirus pandemic. Focus on hydroxychloroquine. Orv. Hetil. 2020;161:689–691. doi: 10.1556/650.2020.31817.
    1. Zhang C., Wu Z., Li J.-W., Zhao H., Wang G.-Q. Cytokine release syndrome in severe COVID-19: Interleukin-6 receptor antagonist tocilizumab may be the key to reduce mortality. Int. J. Antimicrob. Agents. 2020;55:105954. doi: 10.1016/j.ijantimicag.2020.105954.
    1. Toniati P., Piva S., Cattalini M., Garrafa E., Regola F., Castelli F., Franceschini F., Airò P., Bazzani C., Beindorf E.-A., et al. Tocilizumab for the treatment of severe COVID-19 pneumonia with hyperinflammatory syndrome and acute respiratory failure: A single center study of 100 patients in Brescia, Italy. Autoimmun. Rev. 2020;19:102568. doi: 10.1016/j.autrev.2020.102568.
    1. Kow C.S., Hasan S.S. Use of low-molecular-weight heparin in COVID-19 patients. J. Vasc. Surgery. Venous Lymphat. Disord. 2020 doi: 10.1016/j.jvsv.2020.06.006.
    1. Pérez-Sáez M.J., Blasco M., Redondo-Pachón D., Ventura Aguilar P., Bada-Bosch T., Pérez-Flores I., Melilli E., Sánchez-Cámara L.A., López-Oliva M.O., Canal C., et al. Use of tocilizumab in kidney transplant recipients with COVID-19. Am. J. Transplant. 2020 doi: 10.1111/ajt.16192.
    1. Wadman M. Can interferons stop COVID-19 before it takes hold? Science. 2020;369:125–126. doi: 10.1126/science.369.6500.125.
    1. Bouhaddou M., Memon D., Meyer B., White K.M., Rezelj V.V., Marrero M.C., Polacco B.J., Melnyk J.E., Ulferts S., Kaake R.M., et al. The Global Phosphorylation Landscape of SARS-CoV-2 Infection. Cell. 2020:1–28. doi: 10.1016/j.cell.2020.06.034.

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