227
Views
1
CrossRef citations to date
0
Altmetric
Invited Review Articles

Pathological diagnosis of Coronavirus-related nephropathy: insight from postmortem studies

, , , , , , , , , , & show all
Pages 563-575 | Received 01 Apr 2021, Accepted 14 Jun 2021, Published online: 08 Jul 2021

References

  • Zhu N, Zhang D, Wang W, et al. A Novel Coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020;382(8):727–733.
  • Wang C, Horby PW, Hayden FG, et al. A novel Coronavirus outbreak of global health concern. Lancet. 2020;395(10223):470–473.
  • Wang W, Yoneda M. Determination of the optimal penetration factor for evaluating the invasion process of aerosols from a confined source space to an uncontaminated area. Sci Total Environ. 2020;740:140113.
  • Carsana L, Sonzogni A, Nasr A, et al. Pulmonary post-mortem findings in a series of COVID-19 cases from northern Italy: a two-centre descriptive study. Lancet Infect Dis. 2020;20(10):1135–1140.
  • Fotuhi M, Mian A, Meysami S, et al. Neurobiology of COVID-19. J Alzheimers Dis. 2020;76(1):3–19.
  • Bansal M. Cardiovascular disease and COVID-19. Diabetes Metab Syndr. 2020;14(3):247–250.
  • Li Y, Xiao SY. Hepatic involvement in COVID-19 patients: pathology, pathogenesis, and clinical implications. J Med Virol. 2020;92(9):1491–1494.
  • Cheng Y, Luo R, Wang K, et al. Kidney disease is associated with in-hospital death of patients with COVID-19. Kidney Int. 2020;97(5):829–838.
  • Lax SF, Skok K, Zechner P, et al. Pulmonary arterial thrombosis in COVID-19 with fatal outcome: results from a prospective, single-center, clinicopathologic case series. Ann Intern Med. 2020;173(5):350–361.
  • Helms J, Tacquard C, Severac F, et al. High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med. 2020;46(6):1089–1098.
  • Maiese A, Manetti AC, La Russa R, et al. Autopsy findings in COVID-19-related deaths: a literature review. Forensic Sci Med Pathol. 2021;17(2):279–218.
  • WHO. Coronavirus disease (COVID-19) outbreak [Internet]. [cited 2021 May 30]. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019
  • Al Nemer A. Histopathologic and autopsy findings in patients diagnosed with Coronavirus Disease 2019 (COVID-19): what we know so far based on correlation with clinical, morphologic and pathobiological aspects. Adv Anat Pathol. 2020;27(6):363–370.
  • Zizzo M, Bollino R, Castro Ruiz C, et al. Surgical management of suspected or confirmed SARS-CoV-2 (COVID-19)-positive patients: a model stemming from the experience at Level III Hospital in Emilia-Romagna, Italy. Eur J Trauma Emerg Surg. 2020;46(3):513–517.
  • Zizzo M, Bollino R, Annessi V. Pre- and post-operative screening in limited-term elective cancer surgery patients during the COVID-19 pandemic. J Visc Surg. 2020;157(3 Suppl 1):S69–S70.
  • Su H, Yang M, Wan C, et al. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int. 2020;98(1):219–227.
  • Magro C, Mulvey JJ, Berlin D, et al. Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: a report of five cases. Transl Res. 2020;220:1–13.
  • Tian S, Xiong Y, Liu H, et al. Pathological study of the 2019 novel coronavirus disease (COVID-19) through postmortem core biopsies. Mod Pathol. 2020;33(6):1007–1014.
  • Menter T, Haslbauer JD, Nienhold R, et al. Postmortem examination of COVID-19 patients reveals diffuse alveolar damage with severe capillary congestion and variegated findings in lungs and other organs suggesting vascular dysfunction. Histopathology. 2020;77(2):198–209.
  • Barton LM, Duval EJ, Stroberg E, et al. COVID-19 Autopsies, Oklahoma, USA. Am J Clin Pathol. 2020;153(6):725–733.
  • Wichmann D, Sperhake J-P, Lütgehetmann M, et al. Autopsy findings and venous thromboembolism in patients with COVID-19: a prospective cohort study. Ann Intern Med. 2020;173(4):268–277.
  • Buja LM, Wolf DA, Zhao B, et al. The emerging spectrum of cardiopulmonary pathology of the coronavirus disease 2019 (COVID-19): report of 3 autopsies from Houston, Texas, and review of autopsy findings from other United States cities. Cardiovasc Pathol. 2020;48:107233.
  • Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med. 2020;383(2):120–128.
  • Schaller T, Hirschbühl K, Burkhardt K, et al. Postmortem examination of patients with COVID-19. JAMA. 2020;323(24):2518–2520.
  • Duarte-Neto AN, Monteiro RAA, da Silva LFF, et al. Pulmonary and systemic involvement in COVID-19 patients assessed with ultrasound-guided minimally invasive autopsy. Histopathology. 2020;77(2):186–197.
  • Fox SE, Akmatbekov A, Harbert JL, et al. Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans. Lancet Respir Med. 2020;8(7):681–686.
  • Rapkiewicz AV, Mai X, Carsons SE, et al. Megakaryocytes and platelet-fibrin thrombi characterize multi-organ thrombosis at autopsy in COVID-19: a case series. EClinicalMedicine. 2020;24:100434.
  • Edler C, Schröder AS, Aepfelbacher M, et al. Dying with SARS-CoV-2 infection-an autopsy study of the first consecutive 80 cases in Hamburg, Germany. Int J Legal Med. 2020;134(4):1275–1284.
  • Youd E, Moore L. COVID-19 autopsy in people who died in community settings: the first series. J Clin Pathol. 2020;73(12):840–844.
  • Prieto-Pérez L, Fortes J, Soto C, et al. Histiocytic hyperplasia with hemophagocytosis and acute alveolar damage in COVID-19 infection. Mod Pathol. 2020;33(11):2139–2146.
  • Copin MC, Parmentier E, Duburcq T, et al. Time to consider histologic pattern of lung injury to treat critically ill patients with COVID-19 infection. Intensive Care Med. 2020;46(6):1124–1126.
  • Bradley BT, Maioli H, Johnston R, et al. Histopathology and ultrastructural findings of fatal COVID-19 infections in Washington State: a case series. Lancet. 2020;396(10247):320–332.
  • Borczuk AC, Salvatore SP, Seshan SV, et al. COVID-19 pulmonary pathology: a multi-institutional autopsy cohort from Italy and New York City. Mod Pathol. 2020;33(11):2156–2168.
  • Lagana SM, Kudose S, Iuga AC, et al. Hepatic pathology in patients dying of COVID-19: a series of 40 cases including clinical, histologic, and virologic data. Mod Pathol. 2020;33(11):2147–2155.
  • WHO. SARS (severe acute respiratory syndrome) [Internet]. [cited 2021 Mar 9]. Available from: https://www.who.int/ith/diseases/sars/en/
  • WHO. Middle East respiratory syndrome coronavirus (MERS-CoV) [Internet]. [cited 2021 Mar 9]. Available from: https://www.who.int/emergencies/mers-cov/en/
  • Li W, Shi Z, Yu M, et al. Bats are natural reservoirs of SARS-like Coronaviruses. Science. 2005;310(5748):676–679.
  • Kupferschmidt K. Emerging diseases. researchers scramble to understand camel connection to MERS. Science. 2013;341(6147):702.
  • WHO. A research and development blueprint for action to prevent epidemics [Internet]. [cited 2021 Mar 9]. Available from: https://www.who.int/blueprint/en/
  • Peiris JS, Yuen KY, Osterhaus AD, et al. The severe acute respiratory syndrome. N Engl J Med. 2003;349(25):2431–2441.
  • Zaki AM, van Boheemen S, Bestebroer TM, et al. Isolation of a novel Coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367(19):1814–1820.
  • Hijawi B, Abdallat M, Sayaydeh A, et al. Novel Coronavirus infections in Jordan, April 2012: epidemiological findings from a retrospective investigation. East Mediterr Health J. 2013;19(Supp. 1):S12–S18.
  • Drosten C, Kellam P, Memish ZA. Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med. 2014;371(14):1359–1360.
  • El-Kafrawy SA, Corman VM, Tolah AM, et al. Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study. Lancet Planet Health. 2019;3(12):e521–e528.
  • Oh MD, Park WB, Park SW, et al. Middle East respiratory syndrome: what we learned from the 2015 outbreak in the Republic of Korea. Korean J Intern Med. 2018;33(2):233–246.
  • Arabi YM, Arifi AA, Balkhy HH, et al. Clinical course and outcomes of critically ill patients with Middle East respiratory syndrome coronavirus infection. Ann Intern Med. 2014;160(6):389–397.
  • Cui J, Li F, Shi ZL. Origin and evolution of pathogenic Coronaviruses. Nat Rev Microbiol. 2019;17(3):181–192.
  • Su S, Wong G, Shi W, et al. Epidemiology, genetic recombination, and pathogenesis of Coronaviruses. Trends Microbiol. 2016;24(6):490–502.
  • Weiss SR, Leibowitz JL. Coronavirus pathogenesis. Adv Virus Res. 2011;81:85–164.
  • Ren LL, Wang YM, Wu ZQ, et al. Identification of a novel Coronavirus causing severe pneumonia in human: a descriptive study. Chin Med J. 2020;133(9):1015–1024.
  • Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new Coronavirus of probable bat origin. Nature. 2020;579(7798):270–273.
  • Xu X, Chen P, Wang J, et al. Evolution of the Novel Coronavirus from the ongoing Wuhan outbreak and modeling of its spike protein for risk of human transmission. Sci China Life Sci. 2020;63(3):457–460.
  • Chan JFW, Kok KH, Zhu Z, et al. Genomic characterization of the 2019 novel human-pathogenic Coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect. 2020;9(1):221–236.
  • Shi ZL, Guo D, Rottier PJ. Coronavirus: epidemiology, genome replication and the interactions with their hosts. Virol Sin. 2016;31(1):1–2.
  • Chan JFW, Yuan S, Kok KH, et al. A familial cluster of pneumonia associated with the 2019 novel Coronavirus indicating person to person transmission: a study of a family cluster. Lancet. 2020;395(10223):514–523.
  • Liu J, Zheng X, Tong Q, et al. Overlapping and discrete aspects of the pathology and pathogenesis of the emerging human pathogenic Coronaviruses SARS-CoV, MERS-CoV, and 2019-nCoV. J Med Virol. 2020;92(5):491–494.
  • Chu KH, Tsang WK, Tang CS, et al. Acute renal impairment in coronavirus-associated severe acute respiratory syndrome. Kidney Int. 2005;67(2):698–705.
  • Chong PY, Chui P, Ling AE, et al. Analysis of deaths during the severe acute respiratory syndrome (SARS) epidemic in Singapore: challenges in determining a SARS diagnosis. Arch Pathol Lab Med. 2004;128(2):195–204.
  • Wu VC, Hsueh PR, Lin WC, et al. Acute renal failure in SARS patients: more than rhabdomyolysis. Nephrol Dial Transplant. 2004;19(12):3180–3182.
  • Lang ZW, Zhang LJ, Zhang SJ, et al. A clinicopathological study of three cases of severe acute respiratory syndrome (SARS). Pathology. 2003;35(6):526–531.
  • Ding YQ, Wang HJ, Shen H, et al. The clinical pathology of severe acute respiratory syndrome (SARS): a report from China. J Pathol. 2003;200(3):282–289.
  • Gu J, Gong E, Zhang B, et al. Multiple organ infection and the pathogenesis of SARS. J Exp Med. 2005;202(3):415–424.
  • Peiris JS, Chu CM, Cheng VC, et al. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet. 2003;361(9371):1767–1772.
  • Hon KL, Leung CW, Cheng WT, et al. Clinical presentations and outcome of severe acute respiratory syndrome in children. Lancet. 2003;361(9370):1701–1703.
  • Lai KN, Tsang KW, Seto WH, et al. Clinical, laboratory, and radiologic manifestation of SARS. Curr Infect Dis Rep. 2004;6(3):213–219.
  • Peiris JS, Lai ST, Poon LL, et al. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet. 2003;361(9366):1319–1325.
  • Lee N, Hui D, Wu A, et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med. 2003;348(20):1986–1994.
  • Tang HL, Cheuk A, Chu KH, et al. Severe acute respiratory syndrome in haemodialysis patients: a report of two cases. Nephrol Dial Transplant. 2003;18(10):2178–2181.
  • Wong PN, Mak SK, Lo KY, et al. Clinical presentation and outcome of severe acute respiratory syndrome in dialysis patients. Am J Kidney Dis. 2003;42(5):1075–1081.
  • Pacciarini F, Ghezzi S, Canducci F, et al. Persistent replication of severe acute respiratory syndrome coronavirus in human tubular kidney cells selects for adaptive mutations in the membrane protein. J Virol. 2008;82(11):5137–5144.
  • Eckerle I, Müller MA, Kallies S, et al. In-vitro renal epithelial cell infection reveals a viral kidney tropism as a potential mechanism for acute renal failure during Middle East Respiratory Syndrome (MERS) Coronavirus infection. Virol J. 2013;10:359.
  • Tang JW, To KF, Lo AW, et al. Quantitative temporal-spatial distribution of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) in post-mortem tissues. J Med Virol. 2007;79(9):1245–1253.
  • Kong SL, Chui P, Lim B, et al. Elucidating the molecular physiopathology of acute respiratory distress syndrome in severe acute respiratory syndrome patients. Virus Res. 2009;145(2):260–269.
  • Wong CK, Lam CWK, Wu AKL, et al. Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin Exp Immunol. 2004;136(1):95–103.
  • Huang KJ, Su IJ, Theron M, et al. An interferon-gamma-related cytokine storm in SARS patients. J Med Virol. 2005;75(2):185–194.
  • Damle NK, Doyle LV, Bender JR, et al. Interleukin 2-activated human lymphocytes exhibit enhanced adhesion to normal vascular endothelial cells and cause their lysis. J Immunol. 1987;138(6):1779–1785.
  • Annuk M, Lind L, Linde T, et al. Impaired endothelium-dependent vasodilatation in renal failure in humans. Nephrol Dial Transplant. 2001;16(2):302–306.
  • Menachery VD, Eisfeld AJ, Schäfer A, et al. Pathogenic influenza viruses and coronaviruses utilize similar and contrasting approaches to control interferon-stimulated gene responses. mBio. 2014;5(3):e01174–e01114.
  • Channappanavar R, Fehr AR, Vijay R, et al. Dysregulated type I interferon and inflammatory monocyte-macrophage responses cause lethal pneumonia in SARS-CoV-infected mice. Cell Host Microbe. 2016;19(2):181–193.
  • Tan YJ, Fielding BC, Goh PY, et al. Overexpression of 7a, a protein specifically encoded by the severe acute respiratory syndrome coronavirus, induces apoptosis via a caspase-dependent pathway. J Virol. 2004;78(24):14043–14047.
  • Cha RH, Joh JS, Jeong I, et al. Renal complications and their prognosis in Korean patients with Middle East respiratory syndrome-coronavirus from the central MERS-CoV designated hospital. J Korean Med Sci. 2015;30(12):1807–1814.
  • Guery B, Poissy J, el Mansouf L, et al. Clinical features and viral diagnosis of two cases of infection with Middle East Respiratory Syndrome coronavirus: a report of nosocomial transmission. Lancet. 2013;381(9885):2265–2272.
  • Poissy J, Goffard A, Parmentier-Decrucq E, et al. Kinetics and pattern of viral excretion in biological specimens of two MERS-CoV cases. J Clin Virol. 2014;61(2):275–278.
  • Drosten C, Seilmaier M, Corman VM, et al. Clinical features and virological analysis of a case of Middle East respiratory syndrome Coronavirus infection. Lancet Infect Dis. 2013;13(9):745–751.
  • Yeung ML, Yao Y, Jia L, et al. MERS coronavirus induces apoptosis in kidney and lung by upregulating Smad7 and FGF2. Nat Microbiol. 2016;1(3):16004.
  • Alsaad KO, Hajeer AH, Al Balwi M, et al. Histopathology of Middle East respiratory syndrome Coronovirus (MERS-CoV) infection – clinicopathological and ultrastructural study. Histopathology. 2018;72(3):516–524.
  • Hocke AC, Becher A, Knepper J, et al. Emerging human middle East respiratory syndrome Coronavirus causes widespread infection and alveolar damage in human lungs. Am J Respir Crit Care Med. 2013;188(7):882–886.
  • Raj VS, Mou H, Smits SL, et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human Coronavirus-EMC. Nature. 2013;495(7440):251–254.
  • Hong WJ, Petell JK, Swank D, et al. Expression of dipeptidyl peptidase IV in rat tissues is mainly regulated at the mRNA levels. Exp Cell Res. 1989;182(1):256–266.
  • Kenny AJ, Booth AG, George SG, et al. Dipeptidyl peptidase IV, a kidney brush-border serine peptidase. Biochem J. 1976;157(1):169–182.
  • Lambeir A-M, Durinx C, Scharpé S, et al. Dipeptidyl-peptidase IV from bench to bedside: an update on structural properties, functions, and clinical aspects of the enzyme DPP IV. Crit Rev Clin Lab Sci. 2003;40(3):209–294.
  • Chan JF, Chan KH, Choi GK, et al. Differential cell line susceptibility to the emerging novel human betacoronavirus 2c EMC/2012: implications for disease pathogenesis and clinical manifestation. J Infect Dis. 2013;207(11):1743–1752.
  • Cha RH, Yang SH, Moon KC, et al. A case report of a middle east respiratory syndrome survivor with kidney biopsy results. J Korean Med Sci. 2016;31(4):635–640.
  • Ng DL, Al Hosani F, Keating MK, et al. Clinicopathologic, immunohistochemical, and ultrastructural findings of a fatal case of middle east respiratory syndrome Coronavirus Infection in the United Arab Emirates, April 2014. Am J Pathol. 2016;186(3):652–658.
  • Walker DH. Value of autopsy emphasized in the case report of a single patient with middle east respiratory syndrome. Am J Pathol. 2016;186(3):507–510.
  • Gupta A, Madhavan MV, Sehgal K, et al. Extrapulmonary manifestations of COVID-19. Nat Med. 2020;26(7):1017–1032.
  • Remmelink M, De Mendonça R, D’Haene N, et al. Unspecific post-mortem findings despite multiorgan viral spread in COVID-19 patients. Crit Care. 2020;24(1):495.
  • Deshmukh V, Motwani R, Kumar A, et al. Histopathological observations in COVID-19: a systematic review. J Clin Pathol. 2021;74(2):76–83.
  • Yan L, Mir M, Sanchez P, et al. COVID-19 in a hispanic woman. Arch Pathol Lab Med. 2020;144(9):1041–1047.
  • Puelles VG, Lütgehetmann M, Lindenmeyer MT, et al. Multiorgan and renal tropism of SARS-CoV-2. N Engl J Med. 2020;383(6):590–592.
  • Werion A, Belkhir L, Perrot M, et al. SARS-CoV-2 causes a specific dysfunction of the kidney proximal tubule. Kidney Int. 2020;98(5):1296–1307.
  • Lacy JM, Brooks EG, Akers J, et al. COVID-19: postmortem diagnostic and biosafety considerations. Am J Forensic Med Pathol. 2020;41(3):143–151.
  • Nasr SH, Kopp JB. COVID-19-associated collapsing glomerulopathy: an emerging entity. Kidney Int Rep. 2020;5(6):759–761.
  • Larsen CP, Bourne TD, Wilson JD, et al. Collapsing glomerulopathy in a patient with COVID-19. Kidney Int Rep. 2020;5(6):935–939.
  • Kissling S, Rotman S, Gerber C, et al. Collapsing glomerulopathy in a COVID-19 patient. Kidney Int. 2020;98(1):228–231.
  • Peleg Y, Kudose S, D’Agati V, et al. Acute kidney injury due to collapsing glomerulopathy following COVID-19 infection. Kidney Int Rep. 2020;5(6):940–945.
  • Chen W, Pan JY. Anatomical and pathological observation and analysis of SARS and COVID-19: microthrombosis is the main cause of death. Biol Proced Online. 2021;23(1):4.
  • Sekhawat V, Green A, Mahadeva U. COVID-19 autopsies: conclusions from international studies. Diagn Histopathol. 2021;27(3):103–107.
  • Adachi T, Chong JM, Nakajima N, et al. Clinicopathologic and immunohistochemical findings from autopsy of patient with COVID-19. Emerg Infect Dis. 2020;26(9):2157–2161.
  • Hooper JE, Padera RF, Dolhnikoff M, et al. A postmortem portrait of the Coronavirus Disease 2019 (COVID-19) pandemic: a large multiinstitutional autopsy survey study. Arch Pathol Lab Med. 2021;145(5):529–535.
  • Varga Z, Flammer AJ, Steiger P, et al. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020;395(10234):1417–1418.
  • Luan J, Lu Y, Jin X, et al. Spike protein recognition of mammalian ACE2 predicts the host range and an optimized ACE2 for SARS-CoV-2 infection. Biochem Biophys Res Commun. 2020;526(1):165–169.
  • Wrapp D, Wang N, Corbett KS, et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science. 2020;367(6483):1260–1263.
  • Wang K, Chen W, Zhang Z, et al. CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells. Signal Transduct Target Ther. 2020;5(1):283.
  • Spuntarelli V, Luciani M, Bentivegna E, et al. COVID-19: is it just a lung disease? A case-based review. SN Compr Clin Med. 2020;2:1401–1406.
  • Delsante M, Rossi GM, Gandolfini I, et al. Kidney involvement in COVID-19: need for better definitions. J Am Soc Nephrol. 2020;31(9):2224–2225.
  • Ding Y, He L, Zhang Q, et al. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol. 2004;203(2):622–630.
  • Farcas GA, Poutanen SM, Mazzulli T, et al. Fatal severe acute respiratory syndrome is associated with multiorgan involvement by Coronavirus. J Infect Dis. 2005;191(2):193–197.
  • To KF, Tong JH, Chan PK, et al. Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J Pathol. 2004;202(2):157–163.
  • Diao B, Feng Z, Wang C, et al. Human kidney is a target for novel severe acute respiratory syndrome Coronavirus 2 (SARS-CoV-2) infection. medRxiv. 2020.
  • Rossi GM, Delsante M, Pilato FP, et al. Kidney biopsy findings in a critically ill COVID-19 patient with dialysis-dependent acute kidney injury: a case against “SARS-CoV-2 nephropathy”. Kidney Int Rep. 2020;5(7):1100–1105.
  • Zhu H, Zhang H, Xu Y, et al. PCR past, present and future. Biotechniques. 2020;69(4):317–325.
  • van der Linden A, Blokker BM, Kap M, et al. Post-mortem tissue biopsies obtained at minimally invasive autopsy: an RNA-quality analysis. PLoS One. 2014;9(12):e115675.
  • Bijol V, Farag YMK, Harris DCH, et al. Renal pathology practice globally: identifying needs and meeting the challenge. Kidney Int. 2019;96(2):258–261.
  • Xu Z, Shi L, Wang Y, et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8(4):420–422.
  • Wang W, Xu Y, Gao R, et al. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 2020;323(18):1843–1844.
  • Miller SE, Brealey JK. Visualization of putative coronavirus in kidney. Kidney Int. 2020;98(1):231–232.
  • Goldsmith CS, Miller SE, Martines RB, et al. Electron microscopy of SARS-CoV-2: a challenging task. Lancet. 2020;395(10238):e99.
  • Hopfer H, Herzig MC, Gosert R, et al. Hunting coronavirus by transmission electron microscopy – a guide to SARS-CoV-2-associated ultrastructural pathology in COVID-19 tissues. Histopathology. 2021;78(3):358–370.
  • Sanguedolce F, Zanelli M, Ascani S, et al. SARS-CoV-2-related lung pathology: macroscopic and histologic features and their clinical implications. Panminerva Med. 2020. DOI:https://doi.org/10.23736/S0031-0808.20.04157-9
  • Farkash EA, Wilson AM, Jentzen JM. Ultrastructural evidence for direct renal infection with SARS-CoV-2. J Am Soc Nephrol. 2020;31(8):1683–1687.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.