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Open Access

Kidney Biopsy Findings in Patients with COVID-19

Satoru Kudose, Ibrahim Batal, Dominick Santoriello, Katherine Xu, Jonathan Barasch, Yonatan Peleg, Pietro Canetta, Lloyd E. Ratner, Maddalena Marasa, Ali G. Gharavi, M. Barry Stokes, Glen S. Markowitz and Vivette D. D’Agati
JASN September 2020, 31 (9) 1959-1968; DOI: https://doi.org/10.1681/ASN.2020060802
Satoru Kudose
1Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, New York
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Ibrahim Batal
1Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, New York
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Dominick Santoriello
1Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, New York
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Katherine Xu
2Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, New York
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Jonathan Barasch
2Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, New York
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Yonatan Peleg
2Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, New York
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Pietro Canetta
2Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, New York
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Lloyd E. Ratner
3Department of Surgery, Columbia University Irving Medical Center, New York, New York
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Maddalena Marasa
2Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, New York
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Ali G. Gharavi
2Division of Nephrology, Department of Medicine, Columbia University Irving Medical Center, New York, New York
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M. Barry Stokes
1Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, New York
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Glen S. Markowitz
1Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, New York
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Vivette D. D’Agati
1Department of Pathology and Cell Biology, Columbia University Irving Medical Center, New York, New York
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    Figure 1.

    Kidney biopsy findings in patients with COVID-19. (A) Light microscopy demonstrates a lesion of collapsing glomerulopathy characterized by hyperplasia of glomerular epithelial cells and collapse of the underlying glomerular capillaries. Jones methanamine silver. Magnification, ×600. (B) Diffuse foot process effacement and endothelial TRIs (arrow and inset) in a patient with minimal change disease. Electron micrograph. Magnification, ×8000. (C) Subepithelial electron dense deposits in PLA2R-associated membranous glomerulopathy. Electron micrograph. Magnification, ×15,000. (D) Multiple glomeruli with circumferential cellular crescents (arrows) in a patient with class 4+5 lupus nephritis. Periodic acid–Schiff. Magnification, ×100. (E) A glomerulus compressed by a crescent with global linear GBM staining for IgG in a patient with anti-GBM nephritis. Immunofluorescence for IgG. Magnification, ×400. (F) Tubular simplification and focal shedding of degenerating epithelial cells into the tubular lumina in a patient with isolated ATI. Hematoxylin and eosin. Magnification, ×400. (G) Severe lymphocytic tubulitis in a patient with acute T cell–mediated rejection. Periodic acid–Schiff. Magnification, ×600. (H) ISH for the virus by automated method showing undetectable viral RNA in the kidney (inset shows positive lung control). Automated ISH with hematoxylin counterstain. Magnification, ×400.

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    Table 1.

    Clinical findings in patients with COVID-19 who underwent kidney biopsy

    PtAgeSexRaceComorbiditiesISTemperature, °CSpO2 on RABPEdemaCOVID-19 ManifestationsRenal Presentation/Biopsy Indications
    146MBOSA, obesity (BMI=44)N37.194144/100YCough, fever, sore throatAKI, NS
    262MBHTN, prostate carcinomaN37.298126/79YFever, myalgia, weaknessAKI on CKD, NS
    362MBHTN, DM, prostate carcinomaN36.891122/82NFever, hypoxemia, bilateral perihilar and basilar infiltrates on CXRAKI, NRP
    457MBHTN, untreated hepatitis C virusN38.197173/92NFlu-like symptoms with ground glass opacities and patchy consolidation on CXRAKI on CKD, NRP
    561MBHTN, obesity (BMI=31.1)N38.599134/79NCough, feverAKI, NRP
    625MBObesity (BMI=32.2)N38.595117/79YCough, fever, myalgia, infiltrates on CXRAKI, NS
    743FBDM, HLD, streptococcal infection, obesity (BMI=52.5)N37.696107/67NCough, fever, sore throat, weakness, patchy LUL infiltrates on CXRAKI
    828MBNoneN38.696 (on O2)143/62NCough, fever, hypoxemia, bilateral infiltrates on CXR, elevated troponin and CPKAKI
    967MWHTN, gout, history of tobacco use, obesity (BMI=34.9)N36.595135/75NCough, diarrhea, lethargy, multifocal infiltrates on CXRAKI on CKD
    1051MBHTN, DSA+ OHTx for NICM 1 yr ago, atrial fibrillation, CVA, BPH, HLDY36.896117/81NPredominantly nausea, vomiting, abdominal pain, with coughAKI on CKD
    1172MWHTN, DM, HLD, gout, spinal stenosis, atrial fibrillationN36.897 (on O2)125/73YCough, pleural effusion on CTNS
    1270FBHTN, CAD, PVD, cervical carcinoma, GERD, HLD, obesity (BMI=39.4)N38.192118/58YCough, fever, shortness of breathAKI, NRP
    1327FASLE with class 2 lupus nephritisY36.993130/80YCough, fever, shortness of breath, hypoxemia, bilateral infiltrates on CXR, required intubation and ICU admissionAKI, NS
    1448FBGERD, history of tobacco use, obesityN37.698185/80NCough, myalgia, infiltrates on CXRAKI
    1554MWESKD secondary to IgAN s/p DSA+ LURTx 1 mo ago, HTN, obesity (BMI=30.7)Y36.899116/75NAsymptomaticAKI
    1622MBESKD likely secondary to PLA2R+ MGN s/p DDRTx 2 years ago, HTNY37.795178/127NCough, fever, bilateral infiltrates on CXR, required intubation and ICU admissionCKD
    1754FHESKD secondary to PCKD s/p DDRTx 2 months ago, HTNY98.8100104/70NFever, dry throatAKI
    • BP is in millimeters of Hg. Pt, patient; IS, immunosuppression at presentation; SpO2, oxygen saturation (percentage); RA, room air; M, man; B, black; OSA, obstructive sleep apnea; BMI, body mass index; N, no; Y, yes; NS, nephrotic syndrome; HTN, hypertension; AKI on CKD, AKI superimposed on CKD; DM, diabetes mellitus; CXR, chest x-ray; NRP, nephrotic-range proteinuria; F, woman; HLD, hyperlipidemia; LUL, left upper lobe; O2, oxygen; CPK, creatine phosphokinase; W, white; DSA, donor-specific antibody; OHTx, orthotopic heart transplantation; NICM, nonischemic cardiomyopathy; CVA, cerebrovascular accident; BPH, benign prostatic hyperplasia; CT, computed tomography; CAD, coronary artery disease; PVD, peripheral vascular disease; GERD, gastroesophageal reflux disease; A, Asian; ICU, intensive care unit; IgAN, IgA nephropathy; s/p, status post; LURTx, living unrelated renal transplantation; MGN, membranous glomerulopathy; DDRTx, deceased donor renal transplantation; H, Hispanic; PCKD, polycystic kidney disease.

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    Table 2.

    Laboratory findings and follow-up information in patients with COVID-19 who underwent kidney biopsy

    PtBaseline sCrRenal Function at PresentationComplete Blood CountsOther Laboratory TestsFollow-Up Information
    sCrDialysisUrine ProtsAlbUrine RBCHgbWBCPltDuration, dTherapyOutcome
    11.112.5Y5.83.1216.67.7242LDH 1504 U/L, ESR>130 mm/h, hsCRP 49.4 mg/L ferritin 1147 ng/ml, IL-6 12 pg/ml, IL-2R 1530 pg/ml24Tocilizumab, steroidsDialysis dependent with sCr 14.2 mg/dl, UPCR 10.2 g/g, repeat COVID-19 negative
    2210.7N12.13.10–514.27.1 (with lymphopenia)235ESR 125 mm/h, ferritin 340.3 ng/ml30NonesCr 3.8 mg/dl, UACR 5.5 g/g, repeat COVID-19 negative
    3111.6N192.411.714.4 (with lymphopenia)355ESR 130 mm/h, CRP 232 mg/L, ferritin 5000 ng/ml12Steroids, hydroxychloroquine, ceftriaxone, doxycyclinesCr 2.3 mg/dl, UPCR 4 g/g, decreased ferritin, ESR, IL-6
    41.14.9N6.22.509.87257elevated ESR, CRP 11.1 mg/L, ferritin 907 ng/ml, elevated IL-6 and d-dimer, CK 3200 U/L, +HCV Ab11Azithromycin, ceftriaxonesCr 4.9 mg/dl, UPCR 4.1 g/g, repeat COVID-19 negative
    5Normal15Y92.58.321368ESR 41 mm/h, CRP 229 mg/L, ferritin 2542 ng/ml5Dialysis dependent, repeat COVID-19 negative
    6Normal2.2N21<1.53–513.98.5408LDH 590 U/L, CRP 33.4 mg/L, ferritin 374 ng/ml27Azithromycin, hydroxychloroquine, steroidssCr 0.8 mg/dl, UPCR 4.3 g/g, decreased CRP
    73.5 (at adm)6.7Y1+ on UA21–5011.414250None
    82 (at adm)9Y100 mg/dl on UA2.6010.613.1 (with lymphopenia)320LDH 3075 U/L, CRP 4.7 mg/L, ferritin >7500 ng/ml, CK 3309 U/L<30Tocilizumab, hydroxychloroquine, ceftriaxone, azithromycinsCr 1.2 mg/dl
    95.7Y300 mg/dl on UA2.7>512.89.2 (with lymphopenia)454LDH 309 U/L, CRP 13 mg/L, ESR>100 mm/h, ferritin 924 ng/ml, CK 128 U/L30Tocilizumab, hydroxychloroquine, ceftriaxone, azithromycinDialysis dependent
    101.5–1.84.8N0.54.2311.53.2107LDH 524 U/L, CRP 50.8 mg/L, ESR 33 mm/h, ferritin 2282 ng/ml, IL-6 21.4 pg/ml, +ANA1HydroxychloroquinesCr 2.5 mg/dl, urine prot 100 mg/dl on UA, repeat COVID-19 positive
    11Normal0.8N8.81.76–1512.314.8283LDH 300 U/L, CRP 153 mg/L, ferritin 397 ng/ml18TacrolimussCr 1.3 mg/dl, repeat COVID-19 positive
    122.9N6.83.0Present96.1183LDH 1019 U/L, ESR 127 mm/h, ferritin 635 ng/ml, +ANA, +anti-dsDNA Ab35NonesCr 2.4 mg/dl, UPCR 5–6 g/g, improved edema
    130.92.5N9.22.020–5086.8182IL-6 79 pg/ml6SteroidsDied from multiorgan failure secondary to COVID-19
    140.920Y>300 mg/dl on UA3.1>182, with RBC casts9.59.1167CRP 143 mg/L, CK 1460 U/L, +anti-GBM Ab16PLEX, steroids, cyclophosphamideDialysis dependent with sCr 6.7 mg/dl, repeat COVID-19 negative
    151.72.6N0.24.5608.13.9211IL-6 6.6 pg/ml55Tocilizumab, IVIG, steroids, thymoglobulinsCr 2 mg/dl, UPCR 0.1 g/g, repeat COVID-19 negative
    16Dialysis dependent9.4Y3.44.46.1202LDH 333 U/L, ESR 79 mm/h, CRP 195.6 mg/L, ferritin 1630 ng/ml4Tocilizumab, hydroxychloroquine, piperacillin-tazobactam, azithromycinDialysis dependent with sCr 6.7 mg/dl
    172.52.9N0.24.4310.13.3286CRP 0.49 ng/ml, ferritin 1677 ng/ml (previously)7NonesCr 2.2 mg/dl
    • Pt, patient; sCr, serum creatinine (milligrams per deciliter); urine prot, urine protein-creatinine ratio or 24-h urine protein; sAlb, serum albumin (grams per deciliter); RBC, red blood cell (per high-power field); Hgb, hemoglobin (grams per deciliter); WBC, white blood cell count (103 per microliter); Plt, platelet (103 per microliter); Y, yes; LDH, lactate dehydrogenase; ESR, erythrocyte sedimentation rate; hsCRP, high-sensitivity C-reactive protein; IL-2R, IL-2 receptor; UPCR, urine protein-creatinine ratio; repeat COVID-19, repeat PCR testing for severe acute respiratory syndrome coronavirus 2; N, no; UACR, urine microalbumin-creatinine ratio; CRP, C-reactive protein; CK, creatine kinase; +, positive; HCV Ab, Ab for hepatitis C virus; adm, admission; UA, urinalysis; ANA, antinuclear antibody; dsDNA, double-stranded DNA; PLEX, plasmapheresis; IVIG, intravenous Ig.

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    Table 3.

    Pathologic findings in patients with COVID-19 who underwent kidney biopsy

    PtDiagnosisLight MicroscopyElectron Microscopy
    DiagnosisOther FindingsNo. GlomNo. GSNo. CollapseNo. Noncollapsed FSGSHypercellularityMicrocystsIIIFTAVSFPETRIViral Particles
    1Collapsing FSGSATI200140NYFocalMildMildNAaNAaN
    2Collapsing FSGSATI8320NYFocalModerateModerate to severe100YN
    3Collapsing FSGSATI18441NYNoneModerateModerate30NN
    4Collapsing FSGSATI10150NNFocalSevereMildNANANA
    5Collapsing FSGSATI11370NYFocalSevereModerate to severe90NN
    6MCDATI17000NYNoneNoneNone100YN
    7ATI15000NNFocalNoneMild15YN
    8ATIPigment casts22000NNNoneNoneMild10YN
    9ATI2100NNNoneMildModerateNAaNAaN
    10ATI8000NNNoneNoneModerate5NN
    11MGNPLA2R stain positiveb15304NNFocalMildMild to moderate100NN
    12MGNPLA2R stain negativeb3200NYFocalModerateModerate to severe30YN
    13LN class 4+535900Mes, Endo, CrescentsNDiffuseMildMild90YN
    14Anti-GBM GNATI, RBC casts32100CrescentsYDiffuseMildModerateNAaNAaN
    15TCMR grade 2A11100NNFocalNoneMildNANANA
    16InfarctioncNANANANANANFocalSevereNANANANA
    17ATI20100NNNoneNoneMildNANANA
    • Pt, patient; glom, No., number; glomerulus or glomeruli; GS, global sclerosis; II, interstitial inflammation; IFTA, tubular atrophy and interstitial fibrosis; VS, vascular sclerosis; FPE, foot process effacement (percentage); N, no; Y, yes; NA, not available; MCD, minimal change disease; LN, lupus nephritis; Mes, mesangial hypercellularity; Endo, endocapillary hypercellularity; RBC, red blood cell; TCMR, T cell–mediated rejection.

    • ↵a All glomeruli were involved by crescents in the patient with anti-GBM GN, and no glomeruli were available for ultrastructural examination in two patients with native kidney biopsies.

    • ↵b Performed by tissue staining.

    • ↵c Nephrectomy specimen.

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Journal of the American Society of Nephrology
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September 2020
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Kidney Biopsy Findings in Patients with COVID-19
Satoru Kudose, Ibrahim Batal, Dominick Santoriello, Katherine Xu, Jonathan Barasch, Yonatan Peleg, Pietro Canetta, Lloyd E. Ratner, Maddalena Marasa, Ali G. Gharavi, M. Barry Stokes, Glen S. Markowitz, Vivette D. D’Agati
JASN Sep 2020, 31 (9) 1959-1968; DOI: 10.1681/ASN.2020060802

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Kidney Biopsy Findings in Patients with COVID-19
Satoru Kudose, Ibrahim Batal, Dominick Santoriello, Katherine Xu, Jonathan Barasch, Yonatan Peleg, Pietro Canetta, Lloyd E. Ratner, Maddalena Marasa, Ali G. Gharavi, M. Barry Stokes, Glen S. Markowitz, Vivette D. D’Agati
JASN Sep 2020, 31 (9) 1959-1968; DOI: 10.1681/ASN.2020060802
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