Clinical Characteristics and Outcomes of Kidney Transplant Recipients With SARS-CoV-2 Reinfections : Transplantation

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Clinical Characteristics and Outcomes of Kidney Transplant Recipients With SARS-CoV-2 Reinfections

Basic-Jukic, Nikolina MD, PhD1; Arnol, Miha MD, PhD2; Maksimovic, Bojana MD, PhD3; Aleckovic-Halilovic, Mirna MD, PhD4; Racki, Sanjin MD, PhD5; Barbic, Jerko MD, PhD6; Babovic, Batric MD, BSc7; Juric, Ivana MD, PhD1; Furic-Cunko, Vesna MD, PhD1; Katalinic, Lea MD1; Radulovic, Goran MD1; Mihaljevic, Dubravka6; Jelakovic, Bojan MD, PhD1; Kastelan, Zeljko MD, PhD1

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doi: 10.1097/TP.0000000000004315
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Data on severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) reinfections in kidney transplant recipients (KTRs) are lacking. We conducted a retrospective observational study between March 2020 and May 2022 to determine the rate of SARS-CoV-2 reinfections and their outcome in 2837 KTRs. Reinfection was defined as positive SARS-CoV-2 reverse transcription–polymerase chain reaction after initial infection and proven eradication. The primary outcomes were the need for hospitalization during the reinfection and mortality. Sixty-two patients developed SARS-CoV-2 reinfection at the median of 11 mo after the first infection (2.2% of the total cohort and 7% of patients who experienced acute coronavirus disease 2019 [COVID-19]). Sixty-six percent of patients received at least 1 dose of the anti–SARS-CoV-2 vaccine before the reinfection. Median age was 51 y, 42% were female, and 42% were asymptomatic. Twenty-two patients required hospitalization during the reinfection for a median of 10 d. Three patients died, all from respiratory insufficiency. Two were fully vaccinated, and 1 received 1 dose of vaccine. The bivariate analysis identified 10 significant predictors for the hospitalization during the reinfection (Table 1). In a multivariate analysis, proteinuria (P = 0.03; OR = 4.99) and rehospitalization after primary acute COVID-19 (P = 0.004; OR = 11.09) significantly contributed to the model. Hospitalization after reinfection was necessary in 11 patients (17.7%). Three patients died after recovery from the reinfection. Two of them were not vaccinated.

TABLE 1. - Predictors of hospitalization during the SARS-CoV-2 reinfection (bivariate logistic regression analysis)
Predictors β P OR 95% CI
 CMV 1.96 0.02 7.13 1.2-39.1
 Steroid dose 0.21 0.04 1.324 1.01-1.52
 Creatinine 0.01 0.03 1.01 1.001-1.02
 CKD-EPI eGFR –0.04 0.003 0.96 0.94-0.98
 Proteinuria (g/24 h) 1.88 0.01 6.57 1.54-27.92
Primary SARS-CoV-2 infection
 Hospitalization during acute covid 1.38 0.02 4.0 1.28-12.5
 Pneumonia 1.42 0.01 4.13 1.35-12.67
 Stop MMF/Aza 1.18 0.04 3.26 1.01-10.59
 Rehospitalization—post-COVID 2.13 <0.001 8.4 2.38-29.6
SARS-CoV-2 reinfection
 Diarrhea 1.96 0.02 7.13 1.30-39.1
CKD-EPI, Chronic Kidney Disease Epidemiology Collaboration; CMV‚ cytomegalovirus; COVID‚ coronavirus disease; eGFR‚ estimated glomerular filtration rate; MMF‚ mycophenolate mofetil; SARS-CoV-2‚ severe acute respiratory syndrome coronavirus 2.

The hospitalization during the initial infection was identified as a risk factor for reinfection.1 In our study, hospitalization during the primary COVID-19 episode was a risk factor for hospitalization during the reinfection. However, hospitalization during the post–COVID-19 was a much stronger risk factor and remained significant in multivariate analysis. This suggests additional clinical problems that may influence the overall immunosuppressive status and increase the risk of reinfection in KTRs. Proteinuria has already been reported as a significant risk factor for hospitalization during the reinfection,2 whereas better renal allograft function had a protective role in this and previous studies.3

In cancer patients, prior vaccination did not affect mortality from reinfection.4 In the study by Morris et al, 2.4% of organ transplant recipients developed reinfection. Two of them were fully vaccinated. However, their study did not include the Omicron variant.5 In our study, vaccination did not affect hospitalization during the reinfection or mortality from reinfection.

The findings in this report are subject to several limitations. The observational nature of the study limits the ability to draw causal conclusions. We had no individual-level viral strain data. Vaccine efficacy was not determined. Strengths of the present study include its multicenter nature with a large number of patients and 100% nationwide coverage of several countries. The results are accurate as our patients have negative reverse transcription–polymerase chain reaction tests after the first SARS-CoV-2 infection, showing the true reinfection incidence. However, very high heterogeneity among patients and variables raises the possibility that the predictions for hospitalization and outcomes may not stand up with the accrual of greater numbers.

In conclusion, COVID-19 reinfection can occur in KTRs and may be severe. Further work is urgently needed to better understand COVID-19 reinfections.


1. Munker D, Osterman A, Stubbe H, et al. Dynamics of SARS-CoV-2 shedding in the respiratory tract depends on the severity of disease in COVID-19 patients. Eur Respir J. 2021;58:2002724.
2. Karras A, Livrozet M, Lazareth H, et al. Proteinuria and clinical outcomes in hospitalized COVID-19 patients: a retrospective single-center study. Clin J Am Soc Nephrol. 2021;16:514–521.
3. Oto OA, Ozturk S, Turgutalp K, et al. Predicting the outcome of COVID-19 infection in kidney transplant recipients. BMC Nephrol. 2021;22:100.
4. Nitipir C, Parosanu AI, Olaru M, et al. Infection and reinfection with SARS-CoV-2 in cancer patients: a cohort study. Exp Ther Med. 2022;23:399.
5. Morris S, Anjan S, Pallikkuth S, et al. Reinfection with SARS-CoV-2 in solid-organ transplant recipients: incidence density and convalescent immunity prior to reinfection. Transpl Infect Dis. 2022;24:e13827.
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