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Clinical Research
Open Access

COVID-19 Infection in Kidney Transplant Recipients: Disease Incidence and Clinical Outcomes

Michelle Elias, Daniele Pievani, Christine Randoux, Kevin Louis, Blandine Denis, Alexandra Delion, Océane Le Goff, Corinne Antoine, Clarisse Greze, Evangeline Pillebout, Imad Abboud, Denis Glotz, Eric Daugas and Carmen Lefaucheur
JASN October 2020, 31 (10) 2413-2423; DOI: https://doi.org/10.1681/ASN.2020050639
Michelle Elias
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Daniele Pievani
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Christine Randoux
2Nephrology Department, Bichat Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Kevin Louis
3Paris Translational Research Center for Organ Transplantation, INSERM (Institut National de la Santé et de la Recherche Médicale), UMR-S970, Paris, France
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Blandine Denis
4Infectious Diseases Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Alexandra Delion
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Océane Le Goff
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Corinne Antoine
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Clarisse Greze
2Nephrology Department, Bichat Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Evangeline Pillebout
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Imad Abboud
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Denis Glotz
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
3Paris Translational Research Center for Organ Transplantation, INSERM (Institut National de la Santé et de la Recherche Médicale), UMR-S970, Paris, France
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Eric Daugas
2Nephrology Department, Bichat Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
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Carmen Lefaucheur
1Kidney Transplant Department, Saint Louis Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
3Paris Translational Research Center for Organ Transplantation, INSERM (Institut National de la Santé et de la Recherche Médicale), UMR-S970, Paris, France
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    Figure 1.

    The figure illustates the design of this observational prospective cohort study performed in 1216 kidney transplant recipients with active follow-up in two referral transplant centers. COVIDOM, commercial name of patients' application; ORBIS, commercial name of medical software; PMC, medical hotline platform; pts, patients.

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    Table 1.

    Baseline characteristics of the study population according to the presence of COVID-19 disease after kidney transplantation

    Demographic CharacteristicsAll Patients, n=1216COVID-19–Positive Patients, n=66COVID-19–Negative Patients, n=1150P Valuea
    Age, yr54.1±13.456.4±12.554.0±13.40.14
    Men, no. (%)777 (64)37 (56)740 (64)0.17
    Non-White, no. (%)222 (24)24 (36)198 (17)<0.001
    Blood group, no. (%)0.90
     A463 (38)23 (35)440 (38)
     B194 (16)12 (18)182 (16)
     O489 (40)28 (42)461 (40)
     AB70 (6)3 (5)67 (6)
    Cause of ESKD, no. (%)0.13
     Glomerulopathies254/1206 (21)7/66 (11)247/1140 (22)
     Diabetes195/1206 (16)12/66 (18)183/1140 (16)
     Vascular209/1206 (17)16/66 (24)196/1140 (17)
     Other548/1206 (46)31/66 (47)514/1140 (45)
    Deceased donor, no. (%)1053 (87)64 (97)989 (86)<0.001
    Prior kidney transplant, no. (%)132 (11)8 (12)124 (11)0.69
    Time on dialysis prior to transplantation, mob49.4±4257.8±46.248.8±41.80.09
    Multiorgan recipients, no. (%)96 (8)4 (6)92 (8)0.57
    • Plus-minus values are means ± SD.

    • ↵a P values are for the comparisons between COVID-19–positive and COVID-19–negative patients.

    • ↵b Time on dialysis prior to transplantation was available in 1078 patients.

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    Table 2.

    Clinical features and outcomes of kidney transplant recipients with COVID-19

    Clinical Features and OutcomesAll Patients, n=66Invasive Mechanical Ventilation, n=15No Invasive Mechanical Ventilation, n=51
    Features at diagnosis
     Clinical presentation, no. (%)
      Fever51 (77)12 (80)39 (76)
      Cough38 (58)11 (73)27 (53)
      Dyspnea (exertional or rest)26 (39)12 (80)14 (27)
      Diarrhea17 (26)2 (13)15 (29)
      Anosmia/ageusia7 (11)0 (0)7 (14)
     Laboratory testsa
      White blood cell count, 1000/µl, median (range)a5.9 (1.6–14.2)7.4 (2.6–14.2)5.3 (1.6–13.2)
      Absolute lymphocyte count, /µl528 (80–1300)473 (80–1180)548 (169–1300)
      C-reactive protein, mg/L115 (0–335)159 (18–316)96 (0–335)
     Chest x-ray/pulmonary CT scan,a no. (%)
      Multifocal/bilateral patchy opacities38/56 (68)12/13 (92)26/43 (60)
      Lobar opacities3/56 (5)1/13 (8)2/43 (5)
      No acute findings15/56 (27)0/13 (0)15/43 (35)
     Immunosuppressive treatment, no. (%)
      MMF/MPA/AZA61 (92)13 (87)48 (94)
      CNI57 (86)14 (93)43 (84)
      Belatacept6 (9)1 (7)5 (10)
      Steroids55 (83)13 (87)42 (82)
    Treatment and outcome
     Change in immunosuppression, no. (%)
      Discontinued only MMF/MPA/AZA38/61 (62)13 (100)25/48 (52)
      Discontinued only CNI2/57 (4)2/14 (14)0
      Belatacept infusion postpone1/6 (17)01/5 (20)
      No change24 (36)2 (13)22 (43)
      Discontinued all immunosuppression1 (2)1 (7)0
     Anti–COVID-19 therapies, no. (%)
      Hydroxychloroquine7 (11)4 (27)3 (6)
      Tocilizumab1 (2)0 (l0)1 (2)
      Eculizumab2 (3)0 (0)2 (4)
     Outcomes, no. (%)
      AKI28 (42)13 (87)15 (29)
      RRT required7 (11)7 (47)0 (0)
      Died16 (24)11 (73)5 (10)
      Recovery50 (76)4 (27)46 (90)
    • Data are displayed as n (%) or median (range). CT, computed tomography; MMF, mycophenolate mofetil; MPA, mycophenolic acid; AZA, azathioprine; CNI, calcineurin inhibitor.

    • ↵a Data recorded in the 60 hospitalized patients, with missing data for two patients in the invasive mechanical ventilation group and two patients in the noninvasive mechanical ventilation group, for patients admitted to other hospitals.

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    Table 3.

    Factors assessed at time of post-transplant risk evaluation associated with COVID-19 disease in patients with kidney transplants: univariate and multivariate analysis

    Factors Associated with COVID-19 Disease in Kidney Transplant PatientsNo. of PatientsNo. of COVID-19–Positive PatientsOdds Ratio (95% CI)P Value
    Factors associated with COVID-19 disease: univariate analysis
     Recipient characteristics
      Age, per 1-yr increment1216661.01 (1.00 to 1.04)0.15
      Sex
       Women439291
       Men777370.71 (0.43 to 1.17)0.17
      Ethnicity
       White994421
       Non-White222242.75 (1.63 to 4.64)<0.001
     Transplant characteristics
      Donor type
       Deceased donor1053641
       Living donor16320.19 (0.05 to 0.79)<0.001
      Prior kidney transplant
       No1084581
       Yes13280.88 (0.41 to 1.88)0.69
      Time on dialysis before graft per 1-mo increment1078661.00 (1.00 to 1.01)0.09
      Multiorgan recipient
       No1120621
       Yes9641.35 (0.48 to 3.79)0.57
     Time of risk evaluation
     Time from transplant to evaluation per 1-mo increment1216660.99 (0.99 to 1.00)0.02
     Functional allograft parameters
      Recent episode of rejection
       No971541
       Yes245120.87 (0.46 to 1.66)0.68
      Serum creatinine per μmol/L increment1185661.00 (1.00 to 1.01)0.11
     Comorbidities
      Smoker
       No1060601
       Yes15660.67 (0.28 to 1.57)0.35
      Obesity (BMI≥30)
       No1043461
       Yes151203.31 (1.90 to 5.77)<0.001
      Diabetes
       No926351
       Yes290313.05 (1.84 to 5.04)<0.001
      Hypertension
       No28781
       Yes929582.32 (1.10 to 4.92)0.02
      Asthma and chronic pulmonary disease
       No1138531
       Yes78134.09 (2.12 to 7.89)<0.001
      Cardiovascular disease
       No1146651
       Yes7010.24 (0.03 to 1.76)0.17
     Maintenance immunosuppressive therapies
      Prednisone
       No368111
       Yes829552.31 (1.19 to 4.46)0.01
      Tacrolimus
       No510291
       Yes691370.94 (0.57 to 1.55)0.80
      Cyclosporin
       No841461
       Yes360201.02 (0.59 to 1.74)0.95
      Mycophenolate mofetil or mycophenolic acid
       No201131
       Yes996530.81 (0.43 to 1.52)0.51
      Belatacept
       No (CNI regimen)a1051570.61 (0.25 to 1.47)0.28
       Yes7061
      Azathioprine
       No1047581
       Yes15080.96 (0.45 to 2.05)0.92
    Factors associated with COVID-19 disease: multivariate model
     Prednisoneb
      No293111
      Yes741551.67 (0.87 to 3.47)0.15
     Ethnicity
      White829421
      Non-White205242.17 (1.23 to 3.78)0.007
     Cardiovascular disease
      No970651
      Yes6410.20 (0.03 to 1.50)0.12
     Obesity (BMI≥30)
      No900461
      Yes134202.19 (1.19 to 4.05)0.01
     Asthma and chronic pulmonary disease
      No964531
      Yes70133.09 (1.49 to 6.41)0.002
     Diabetes
      No785351
      Yes249313.33 (1.92 to 5.77)<0.001
     Time on dialysis before graft per 1-mo increment1034661.01 (0.99 to 1.01)0.07
    • OR, odds ratio; BMI, body mass index; CNI, calcineurin inhibitor (cyclosporin or tacrolimus).

    • ↵a Three patients did not take either CNI or belatacept.

    • ↵b The multivariable analysis was restricted to 1034 patients without any missing data for each of the variables included in the final model by the stepwise backward elimination.

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Journal of the American Society of Nephrology: 31 (10)
Journal of the American Society of Nephrology
Vol. 31, Issue 10
October 2020
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COVID-19 Infection in Kidney Transplant Recipients: Disease Incidence and Clinical Outcomes
Michelle Elias, Daniele Pievani, Christine Randoux, Kevin Louis, Blandine Denis, Alexandra Delion, Océane Le Goff, Corinne Antoine, Clarisse Greze, Evangeline Pillebout, Imad Abboud, Denis Glotz, Eric Daugas, Carmen Lefaucheur
JASN Oct 2020, 31 (10) 2413-2423; DOI: 10.1681/ASN.2020050639

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COVID-19 Infection in Kidney Transplant Recipients: Disease Incidence and Clinical Outcomes
Michelle Elias, Daniele Pievani, Christine Randoux, Kevin Louis, Blandine Denis, Alexandra Delion, Océane Le Goff, Corinne Antoine, Clarisse Greze, Evangeline Pillebout, Imad Abboud, Denis Glotz, Eric Daugas, Carmen Lefaucheur
JASN Oct 2020, 31 (10) 2413-2423; DOI: 10.1681/ASN.2020050639
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