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

doi:10.1681/ASN.2020050639

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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 Characteristics	All Patients, n=1216	COVID-19–Positive Patients, n=66	COVID-19–Negative Patients, n=1150	P Value^a
Age, yr	54.1±13.4	56.4±12.5	54.0±13.4	0.14
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
A	463 (38)	23 (35)	440 (38)
B	194 (16)	12 (18)	182 (16)
O	489 (40)	28 (42)	461 (40)
AB	70 (6)	3 (5)	67 (6)
Cause of ESKD, no. (%)				0.13
Glomerulopathies	254/1206 (21)	7/66 (11)	247/1140 (22)
Diabetes	195/1206 (16)	12/66 (18)	183/1140 (16)
Vascular	209/1206 (17)	16/66 (24)	196/1140 (17)
Other	548/1206 (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, mo^b	49.4±42	57.8±46.2	48.8±41.8	0.09
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 Outcomes	All Patients, n=66	Invasive Mechanical Ventilation, n=15	No Invasive Mechanical Ventilation, n=51
Features at diagnosis
Clinical presentation, no. (%)
Fever	51 (77)	12 (80)	39 (76)
Cough	38 (58)	11 (73)	27 (53)
Dyspnea (exertional or rest)	26 (39)	12 (80)	14 (27)
Diarrhea	17 (26)	2 (13)	15 (29)
Anosmia/ageusia	7 (11)	0 (0)	7 (14)
Laboratory tests^a
White blood cell count, 1000/µl, median (range)^a	5.9 (1.6–14.2)	7.4 (2.6–14.2)	5.3 (1.6–13.2)
Absolute lymphocyte count, /µl	528 (80–1300)	473 (80–1180)	548 (169–1300)
C-reactive protein, mg/L	115 (0–335)	159 (18–316)	96 (0–335)
Chest x-ray/pulmonary CT scan,^a no. (%)
Multifocal/bilateral patchy opacities	38/56 (68)	12/13 (92)	26/43 (60)
Lobar opacities	3/56 (5)	1/13 (8)	2/43 (5)
No acute findings	15/56 (27)	0/13 (0)	15/43 (35)
Immunosuppressive treatment, no. (%)
MMF/MPA/AZA	61 (92)	13 (87)	48 (94)
CNI	57 (86)	14 (93)	43 (84)
Belatacept	6 (9)	1 (7)	5 (10)
Steroids	55 (83)	13 (87)	42 (82)
Treatment and outcome
Change in immunosuppression, no. (%)
Discontinued only MMF/MPA/AZA	38/61 (62)	13 (100)	25/48 (52)
Discontinued only CNI	2/57 (4)	2/14 (14)	0
Belatacept infusion postpone	1/6 (17)	0	1/5 (20)
No change	24 (36)	2 (13)	22 (43)
Discontinued all immunosuppression	1 (2)	1 (7)	0
Anti–COVID-19 therapies, no. (%)
Hydroxychloroquine	7 (11)	4 (27)	3 (6)
Tocilizumab	1 (2)	0 (l0)	1 (2)
Eculizumab	2 (3)	0 (0)	2 (4)
Outcomes, no. (%)
AKI	28 (42)	13 (87)	15 (29)
RRT required	7 (11)	7 (47)	0 (0)
Died	16 (24)	11 (73)	5 (10)
Recovery	50 (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 Patients	No. of Patients	No. of COVID-19–Positive Patients	Odds Ratio (95% CI)	P Value
Factors associated with COVID-19 disease: univariate analysis
Recipient characteristics
Age, per 1-yr increment	1216	66	1.01 (1.00 to 1.04)	0.15
Sex
Women	439	29	1
Men	777	37	0.71 (0.43 to 1.17)	0.17
Ethnicity
White	994	42	1
Non-White	222	24	2.75 (1.63 to 4.64)	<0.001
Transplant characteristics
Donor type
Deceased donor	1053	64	1
Living donor	163	2	0.19 (0.05 to 0.79)	<0.001
Prior kidney transplant
No	1084	58	1
Yes	132	8	0.88 (0.41 to 1.88)	0.69
Time on dialysis before graft per 1-mo increment	1078	66	1.00 (1.00 to 1.01)	0.09
Multiorgan recipient
No	1120	62	1
Yes	96	4	1.35 (0.48 to 3.79)	0.57
Time of risk evaluation
Time from transplant to evaluation per 1-mo increment	1216	66	0.99 (0.99 to 1.00)	0.02
Functional allograft parameters
Recent episode of rejection
No	971	54	1
Yes	245	12	0.87 (0.46 to 1.66)	0.68
Serum creatinine per μmol/L increment	1185	66	1.00 (1.00 to 1.01)	0.11
Comorbidities
Smoker
No	1060	60	1
Yes	156	6	0.67 (0.28 to 1.57)	0.35
Obesity (BMI≥30)
No	1043	46	1
Yes	151	20	3.31 (1.90 to 5.77)	<0.001
Diabetes
No	926	35	1
Yes	290	31	3.05 (1.84 to 5.04)	<0.001
Hypertension
No	287	8	1
Yes	929	58	2.32 (1.10 to 4.92)	0.02
Asthma and chronic pulmonary disease
No	1138	53	1
Yes	78	13	4.09 (2.12 to 7.89)	<0.001
Cardiovascular disease
No	1146	65	1
Yes	70	1	0.24 (0.03 to 1.76)	0.17
Maintenance immunosuppressive therapies
Prednisone
No	368	11	1
Yes	829	55	2.31 (1.19 to 4.46)	0.01
Tacrolimus
No	510	29	1
Yes	691	37	0.94 (0.57 to 1.55)	0.80
Cyclosporin
No	841	46	1
Yes	360	20	1.02 (0.59 to 1.74)	0.95
Mycophenolate mofetil or mycophenolic acid
No	201	13	1
Yes	996	53	0.81 (0.43 to 1.52)	0.51
Belatacept
No (CNI regimen)^a	1051	57	0.61 (0.25 to 1.47)	0.28
Yes	70	6	1
Azathioprine
No	1047	58	1
Yes	150	8	0.96 (0.45 to 2.05)	0.92
Factors associated with COVID-19 disease: multivariate model
Prednisone^b
No	293	11	1
Yes	741	55	1.67 (0.87 to 3.47)	0.15
Ethnicity
White	829	42	1
Non-White	205	24	2.17 (1.23 to 3.78)	0.007
Cardiovascular disease
No	970	65	1
Yes	64	1	0.20 (0.03 to 1.50)	0.12
Obesity (BMI≥30)
No	900	46	1
Yes	134	20	2.19 (1.19 to 4.05)	0.01
Asthma and chronic pulmonary disease
No	964	53	1
Yes	70	13	3.09 (1.49 to 6.41)	0.002
Diabetes
No	785	35	1
Yes	249	31	3.33 (1.92 to 5.77)	<0.001
Time on dialysis before graft per 1-mo increment	1034	66	1.01 (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.