Nephrol Dialysis Transplant (2022) 37: 1140–1151 https://doi.org/10.1093/ndt/gfac008 Advance Access publication date 14 January 2022 Recovery of dialysis patients with COVID-19: health outcomes ORIGINAL ARTICLE 3 months after diagnosis in ERACODA Marc H. Hemmelder1 , Marlies Noordzij2 , Priya Vart2 , Luuk B. Hilbrands 3 , Kitty J. Jager4 , Alferso C. Abrahams5 , David Arroyo6 , Yuri Battaglia7 , Robert Ekart8 , Francesca Mallamaci9 , Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 Sharon-Rose Malloney10 , Joao Oliveira 11 , Andrzej Rydzewski12 , Sivakumar Sridharan 13 , Liffert Vogt14 , Raphaël Duivenvoorden3 , Ron T. Gansevoort2 and Casper F.M. Franssen2 ; ERACODA Collaborators 1 Department of Internal Medicine, Division of Nephrology, Maastricht University Medical Center, CARIM School for Cardiovascular Disease, University of Maastricht, Maastricht, The Netherlands, 2 Department of Internal Medicine, University Medical Center Groningen, Groningen, The Netherlands, 3 Department of Nephrology, Radboud University Medical Center, Nijmegen, The Netherlands, 4 ERA Registry, Department of Medical Informatics, Amsterdam University Medical Center, University of Amsterdam, Amsterdam Public Health Research Institute, Amsterdam, The Netherlands, 5 Department of Nephrology and Hypertension, University Medical Center Utrecht, Utrecht, The Netherlands, 6 Department of Nephrology, Hospital General Universitario Gregorio Marañón, Madrid, Spain, 7 Department of Specialized Medicine, Division of Nephrology and Dialysis, St. Anna University Hospital, Ferrara, Italy, 8 Department of Dialysis, Clinic for Internal Medicine, University Medical Center Maribor, Maribor, Slovenia, 9 Nephrology, Dialysis and Renal Transplantation Unit, Grande Ospedale Metropolitano di Reggio Cal, Italy, 10 Luzerner Kantonsspital, Luzern, Switzerland, 11 Centrodial (Outpatient Dialysis Center), São João da Madeira, Portugal, 12 Department of Internal Medicine, Nephrology and Transplantation Medicine, Centre of Postgraduate Medical Education, Central Clinical Hospital of the Ministry of Internal Affairs, Warsaw, Poland, 13 Department of nephrology, East and North Hertfordshire NHS Trust, Lister Hospital, Hertfordshire, UK and 14 Department of Internal Medicine, Section of Nephrology, Amsterdam University Medical Centers, Amsterdam Cardiovascular Sciences, University of Amsterdam, Amsterdam, The Netherlands Correspondence to: Marc H. Hemmelder; E-mail: marc.hemmelder@mumc.nl ABSTR ACT diagnosis. At 3 months, 87% functioned at their pre-existent Background. Coronavirus disease 2019 (COVID-19)-related functional and 94% at their pre-existent mental level. Only few short-term mortality is high in dialysis patients, but longer- of the surviving patients were still admitted to the hospital (0.8– term outcomes are largely unknown. We therefore assessed 6.3%) or a nursing home (∼5%). A higher age and frailty score patient recovery in a large cohort of dialysis patients 3 months at presentation and ICU admission were associated with worse after their COVID-19 diagnosis. functional outcome. Methods. We analyzed data on dialysis patients diagnosed Conclusions. Mortality between 28 days and 3 months after with COVID-19 from 1 February 2020 to 31 March 2021 COVID-19 diagnosis was low and the majority of patients who from the European Renal Association COVID-19 Database survived COVID-19 recovered to their pre-existent functional (ERACODA). The outcomes studied were patient survival, and mental health level at 3 months after diagnosis. residence and functional and mental health status (estimated Keywords: COVID-19, dialysis, functional health status, men- by their treating physician) 3 months after COVID-19 diagno- tal health status, survival sis. Complete follow-up data were available for 854 surviving patients. Patient characteristics associated with recovery were analyzed using logistic regression. I N T RODU C T ION Results. In 2449 hemodialysis patients (mean ± SD age The COVID-19 pandemic has had a major impact around the 67.5 ± 14.4 years, 62% male), survival probabilities at 3 months world, with dialysis patients being among the patient groups after COVID-19 diagnosis were 90% for nonhospitalized with the highest mortality [1, 2]. If infected with severe acute patients (n = 1087), 73% for patients admitted to the hospital respiratory syndrome coronavirus 2 (SARS-CoV-2), these but not to an intensive care unit (ICU) (n = 1165) and 40% for patients often develop a serious course of COVID-19, which those admitted to an ICU (n = 197). Patient survival hardly requires in-hospital care. The European Renal Association decreased between 28 days and 3 months after COVID-19 COVID-19 Database (ERACODA) Working Group previously © The Author(s) 2022. Published by Oxford University Press on behalf of the ERA. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com KEY LEARNING POINTS What is already known about this subject? • Previous studies have shown that coronavirus disease 2019 (COVID-19)-related short-term mortality is high in dialysis patients. • Data on the longer-term recovery of dialysis patients after COVID-19 are scarce. • We therefore studied different health outcomes, including patient survival, residence (home/hospital/nursing home) and functional and mental health status in a large group of dialysis patients 3 months after a COVID-19 diagnosis. What this study adds? • This study demonstrates that 78% of the dialysis patients survived COVID-19, with the large majority recovering to their pre-existent functional and mental health level at 3 months after diagnosis. Patients who had not yet recovered were mostly those who had been admitted to the intensive care unit (ICU). What impact this may have on practice or policy? Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 • Our findings show that if dialysis patients survive COVID-19, the outcome at 3 months is rather good. This implies that optimal treatment of COVID-19 in this high-risk group is recommended without restrictions. Treating physicians may use this information during consultation with patients, for instance, when in doubt whether to admit them to the hospital and/or an ICU. reported a 28-day mortality of 25% in dialysis patients during of the UMCG, who deemed the collection and analysis of the first pandemic wave [3]. In these patients, age and frailty data exempt from ethics review according to the Medical were the dominant factors independently associated with Research Involving Human Subjects Act (WMO). Data on higher mortality [3]. These findings were confirmed in larger outpatients and hospitalized patients were voluntarily reported cohorts of patients receiving dialysis [4–6]. by physicians responsible for their care. Notwithstanding the high short-term mortality in dialysis A total of 225 physicians from 141 centers in 33 countries, patients, most patients were alive at 28 days after the diagnosis mostly in Europe and bordering the Mediterranean Sea, of COVID-19, but data on longer-term health outcomes in entered data in ERACODA. For the current study, we included dialysis patients who survived COVID-19 are virtually absent. all dialysis patients who presented with COVID-19 between It could well be that a relevant portion of patients experience 1 February 2020 and 31 March 2021 for whom information functional deterioration without recovery or die at a later stage on age, sex, hospitalization, ICU admission and 3-month vital due to the long-term complications of COVID-19 [7]. The aim status were available. The inclusion started at the start of of this study was to assess the recovery of dialysis patients at 3 the COVID-19 pandemic in Europe with the predominant months after COVID-19 diagnosis, in terms of patient survival, original SARS-CoV-2 genotype and ended when the effect of residence and functional and mental health status. Here we the vaccination campaign in Europe became of influence. For present the first results on these outcomes, as well as their 80 patients (3.3%), the dialysis modality was unknown, and associations with patient and COVID-19 characteristics. we assumed that these patients received in-center hemodialysis (HD), because this was by far the most common dialysis modality in ERACODA and also in general within Europe [10]. M AT E R IA L S A N D M E T HOD S Study population Data collection This study is based on data from ERACODA, which We collected detailed information on patient character- contains granular data on adult patients (>18 years of age) with istics, including age, sex, ethnicity, frailty, comorbidities, kidney failure who were treated with dialysis or living with a hospitalization and medication use and on COVID-19-related functioning kidney allograft and who developed COVID-19 characteristics such as symptoms, vital signs and laboratory [8]. The COVID-19 diagnosis was based on a positive result on test results. Frailty was assessed using the Clinical Frailty a real-time polymerase chain reaction (PCR) assay or a rapid Score [11], which ranges from 1, representing very fit, to 9, antigen test of nasal and/or pharyngeal swab specimens and/or representing terminally ill. Comorbidities were recorded at compatible findings on a computed tomography (CT) scan or presentation from patient charts and obesity was defined as a chest X-ray of the lungs. body mass index (BMI) >30 kg/m2 . The database uses REDCap software, a secure web appli- Information on functional and mental health outcomes cation for building and managing online databases (Research was collected once at 3 months after first presentation with Electronic Data Capture, Vanderbilt University Medical Cen- COVID-19. Due to the study design, we had no options to ter, Nashville, TN, USA) [9] and is hosted at the Univer- invite individual patients to report on their functional and sity Medical Center Groningen (UMCG), Groningen, The mental outcomes. Since nephrologists generally meet their Netherlands. Patient information is stored pseudonymized. HD patients every week and know their patients well, we The study was approved by the institutional review board asked them to report on these outcomes. We composed a Recovery of dialysis patients with COVID-19 1141 standardized questionnaire for this purpose (Appendix 1). on age, sex, hospitalization, ICU admission and 3-month vital If patients had not recovered at 3 months, we asked which status was available for 2617 patients (2449 HD and 168 PD). limiting factors were judged to be responsible for not reaching There were 1087 HD patients (44%) who were not hospitalized, the pre-COVID-19 functional and mental health status and 1165 (48%) who were hospitalized but not admitted to the how long they estimated the interval to reach the pre-COVID- ICU and 197 (8%) who were admitted to the ICU. Table 1 19 status. shows the baseline patient and disease characteristics for these Statistical analysis subgroups and for the total group. For almost all patients (99.8%) the COVID-19 diagnosis was based on a positive PCR All baseline patient and disease characteristics are presented test. Patients who were admitted to the ICU were younger, for the total population and separately for the categories less often Caucasian, less frail and had higher BMI, longer not hospitalized, hospitalized but not ICU admitted and dialysis vintage, fewer previous transplantations and more hospitalized and ICU admitted. Continuous data are presented severe COVID-19 symptoms compared with the two other as mean [standard deviation (SD)] or median [interquartile subgroups. Characteristics of PD patients are presented in range (IQR)] if the data were not normally distributed. Supplementary data, Table S1. Categorical data are presented as percentages. We used analysis Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 of variance (ANOVA) tests to compare continuous variables between the three subgroups (Kruskal–Wallis test for non- normally distributed data) and Pearson chi-squared tests to Survival at 3 months compare categorical variables. HD and peritoneal dialysis (PD) Overall, 1909 of the 2449 HD patients (78%) survived patients were analyzed separately, but the main focus in this the first 3 months after presentation with COVID-19. Those article is on HD, because of the small sample size of the PD who survived were younger, had a lower frailty score, fewer group. comorbid conditions and fewer symptoms and signs of Unadjusted cumulative survival probability curves by hos- COVID-19 at presentation than those who died in the first 3 pitalization and ICU admission status were created using months (Supplementary data, Table S2). the Kaplan–Meier method and compared using log-rank At day 28, the survival probability of HD patients was tests. Unadjusted and adjusted hazard ratios (HRs) with 95% 90% in the patients who were not hospitalized, 75% in those confidence intervals (CIs) were calculated to compare the risk who were hospitalized but not admitted to the ICU and of mortality in HD and PD patients. 47% in those who were admitted to the ICU. At 3 months We analyzed functional and mental health outcomes in after a COVID-19 diagnosis, survival probabilities were 90%, those who were alive at 3 months after a COVID-19 diagnosis. 73% and 40%, respectively. This indicates that there is a Numbers and proportions are presented for the total group and limited effect on survival between 28 days and 3 months after by hospital and ICU admission status. The Pearson chi-squared diagnosis. Survival was lower in patients admitted to the ICU test was used to compare proportions between patient groups. when compared with those who were not (P-value log-rank Unadjusted and adjusted logistic regression models were test <0.0001). Kaplan–Meier curves for the three groups are applied to calculate odds ratios (ORs) with 95% CIs for the presented in Figure 1. likelihood of reaching the pre-COVID-19 functional or mental Among PD patients, survival probabilities at 3 months were health status. A broad set of variables, including demograph- 86% for patients not hospitalized, 61% for patients hospitalized ics, comorbidities, COVID-19 symptoms and admission to but not admitted to the ICU and 67% for those admitted to the hospital and/or ICU, was included in the crude analysis. ICU (Supplementary data, Figure S1). The survival probability Selection of variables for the multivariable model was based on was lower (P = 0.006) in those who were hospitalized but statistical significance in the crude analysis. The multivariable not admitted to the ICU compared with those admitted to the models included age, sex, frailty score, heart failure, respiration ICU. rate, shortness of breath, hospitalization and ICU admission for functional status and all these variables plus coronary artery disease for mental health status. Missing data in the Residence at 3 months multivariable models were handled by multiple imputations (10 imputed datasets created with 100 interactions) with the Figure 2 presents the residence of survivors at 3 months chained equations method using all variables included in the after the COVID-19 diagnosis. Although this variable was model [12, 13]. unknown for a relatively large proportion of patients (58% All analyses were performed using Stata version 14.0 of patients who were not admitted, 27% of those hospitalized (StataCorp, College Station, TX, USA). A two-sided and 28% of those admitted to the ICU), we observed that in P-value <0.05 indicated statistical significance. cases where residence was known, most patients were at home at 3 months of follow-up (36%, 65% and 61%, respectively). Approximately 5% of the patients (in all three groups) lived R E SU LT S in a nursing home, whereas the proportion of patients who Study population and patient characteristics were in the hospital varied between 0.8% in those who were During the study period, 3331 dialysis patients in the initially not hospitalized and 6.3% in patients who had been ERACODA database presented with COVID-19. Information admitted to the ICU. 1142 M.H. Hemmelder et al. Table 1. Baseline demographic and clinical characteristics of HD patients with COVID-19 by hospitalization and ICU admission status Total* Not hospitalized Hospitalized, no ICU Hospitalized, ICU Variable (n = 2449) (n = 1087) (n = 1165) (n = 197) P-value Patient characteristics Male sex, n(%) 1509 (62) 645 (59) 740 (64) 124 (63) 0.12 Age (years), mean ± SD 67.5 ± 14.4 67.4 ± 15.1 68.0 ± 13.9 65.0 ± 12.5 0.03 BMI (kg/m2 ), mean ± SD 26.6 ± 5.5 26.9 ± 5.8 26.3 ± 5.4 27.0 ± 5.2 0.05 Race, n (%) 0.006 White or Caucasian 1976 (85) 850 (86) 976 (85) 150 (77) Non-white 357 (15) 141 (14) 171 (15) 45 (23) Tobacco use, n(%) <0.001 Current 158 (6.5) 42 (3.9) 100 (8.6) 16 (8.1) Prior 459 (19) 139 (13) 270 (23) 50 (25) Never 879 (36) 269 (25) 519 (45) 91 (46) Unknown 953 (39) 637 (59) 276 (24) 40 (20) Clinical frailty scale (AU), mean ± SD 4.0 ± 1.8 3.9 ± 1.8 4.1 ± 1.9 3.8 ± 1.5 0.04 Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 Reason for screening, n(%) <0.001 Symptoms only 1132 (62) 295 (51) 707 (66) 130 (68) Symptoms and contact 280 (15) 59 (10) 175 (16) 46 (24) Contact only 218 (12) 110 (19) 103 (9.3) 5 (2.6) Routine screening 207 (11) 110 (19) 88 (8.2) 9 (4.7) COVID-19 diagnosis, n(%) Positive PCR 2383 (99.8) 1079 (99.8) 1113 (99.7) 191 (100) 0.94 Abnormal X-raya 562 (60) 39 (80) 434 (64) 89 (78) <0.001 Abnormal CT scanb 475 (81) 23 (47) 353 (82) 99 (88) <0.001 Comorbidities, n(%) Obesity 464 (23) 203 (24) 215 (21) 46 (26) 0.25 Hypertension 1979 (81) 836 (77) 986 (85) 157 (80) <0.001 Diabetes mellitus 1046 (43) 409 (38) 542 (47) 95 (48) <0.001 Coronary artery disease 825 (34) 325 (30) 425 (36) 75 (38) 0.002 Heart failure 571 (23) 200 (18) 321 (28) 50 (25) <0.001 Chronic lung disease 317 (13) 107 (10) 178 (15) 32 (16) <0.001 Active malignancy 136 (5.6) 44 (4.1) 82 (7.0) 10 (5.1) 0.008 Auto-immune disease 88 (3.6) 27 (2.5) 54 (4.6) 7 (3.6) 0.02 Primary kidney disease, n(%) Primary glomerulonephritis 308 (13) 112 (11) 165 (14) 31 (16) 0.06 Pyelonephritis 37 (1.6) 16 (1.6) 20 (1.7) 1 (0.5) 0.44 Interstitial nephritis 69 (3.0) 31 (3.1) 34 (3.0) 4 (2.0) 0.71 Hereditary kidney disease 160 (6.7) 87 (8.8) 63 (5.5) 10 (5.1) 0.006 Congenital diseases 33 (1.4) 18 (1.8) 14 (1.2) 1 (0.5) 0.27 Vascular diseases 420 (18) 214 (22) 174 (15) 32 (16) <0.001 Secondary glomerular diseases 200 (8.6) 131 (13) 60 (5.2) 9 (4.6) <0.001 Diabetic kidney disease 542 (23) 153 (16) 322 (28) 67 (34) <0.001 Other 378 (16) 166 (17) 187 (16) 25 (13) 0.37 Unknown 184 (7.9) 59 (6.0) 109 (9.5) 16 (8.2) 0.01 HD modality, n(%) 0.03 Centre HD 2290 (99) 975 (98) 1122 (99) 193 (99) Home HD 28 (1) 19 (1.9) 8 (0.7) 1 (0.5) Dialysis vintage (years), median (IQR) 4 (2–8) 4 (2–8) 4 (2–8) 5 (3–9) 0.07 Previous kidney transplantation, n (%) 195 (8.6) 105 (10.9) 79 (7.0) 11 (5.7) 0.002 Medication use, n(%) RAAS inhibition 503 (27) 185 (32) 269 (25) 49 (27) 0.01 Immunosuppressive Prednisone 126 (5.1) 37 (3.2) 79 (6.8) 10 (5.1) 0.027 Tacrolimus 33 (1.3) 17 (1.6) 14 (1.2) 2 (1.0) 0.05 Mycophenolate 16 (0.7) 7 (0.6) 8 (0.7) 1 (0.5) 0.66 COVID-19-related characteristics Presenting symptoms, n (%) Sore throat 252 (14) 73 (12) 141 (13) 38 (22) 0.004 Cough 920 (47) 222 (36) 574 (50) 124 (66) <0.001 Shortness of breath 621 (32) 73 (12) 423 (37) 125 (65) <0.001 Fever 1067 (54) 218 (36) 698 (60) 151 (77) <0.001 Headache 193 (10) 51 (8.7) 114 (10) 28 (16) 0.014 Nausea or vomiting 184 (9.5) 39 (6.5) 119 (10) 26 (14) 0.003 Diarrhea 236 (12) 60 (9.9) 146 (13) 30 (16) 0.05 Myalgia or arthralgia 404 (22) 85 (14) 267 (24) 52 (30) <0.001 Recovery of dialysis patients with COVID-19 1143 Table 1. Continued Total* Not hospitalized Hospitalized, no ICU Hospitalized, ICU Variable (n = 2449) (n = 1087) (n = 1165) (n = 197) P-value Vital signs, mean ± SD Temperature (°C) 37.4 ± 1.0 37.0 ± 1.0 37.5 ± 1.0 37.8 ± 1.0 <0.001 Respiration rate/min 18.4 ± 4.9 15.9 ± 3.7 19.1 ± 4.8 21.3 ± 5.3 <0.001 O2 saturation room air (%) 93.9 ± 5.4 96.6 ± 2.7 93.5 ± 5.2 90.0 ± 7.8 <0.001 Systolic BP (mmHg) 136.4 ± 25.4 139.4 ± 24.9 136.0 ± 25.5 130.8 ± 25.2 <0.001 Diastolic BP (mmHg) 73.6 ± 15.1 72.5 ± 14.9 73.9 ± 15.5 75.4 ± 13.6 0.08 Pulse rate (BPM) 81.1 ± 15.0 75.8 ± 13.0 82.6 ± 15.3 86.9 ± 14.0 <0.001 Laboratory test results, median (IQR) Lymphocytes (×1000/μL) 0.9 (0.6–1.3) 0.9 (0.7–1.2) 0.9 (0.6–1.4) 0.7 (0.5–1.1) 0.0013 CRP (mg/L) 41 (9.9–94) 5 (3–30) 43 (12–95) 71 (24–124) <0.001 Hospitalization duration (days) 14 (8–23) – 14 (8–21) 24 (18–40) <0.001 ICU admission duration (days) 6 (2–11) – – 6 (2–11) – * Numbers may not add up to total because of missing values. Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 a X-rays were performed for 933 of 2449 patients (38%), including 138 in the non-hospitalized group, 681 in the group admitted to the hospital (not ICU) and 114 in patients admitted to the ICU. b CT scans were performed for 589 of 2449 patients (24%), including 49 in the non-hospitalized group, 428 in the group admitted to the hospital (not ICU) and 112 in patients admitted to the ICU. Groups were compared using one-way ANOVA, Kruskal–Wallis test or chi-squared test, as appropriate. Obesity is defined as BMI >30 kg/m2 . RAAS, renin-angiotensin-aldosterone system; BP, blood pressure; CRP, C-reactive protein; O2 , oxygen. of patients who did not recover was higher in the subgroup 1.00 admitted to the ICU compared with the other two subgroups. Among those who had not yet recovered, the most important 0.75 limiting factors were reduced muscle strength (48%), reduced mobility (41%) and tiredness (37%). For 58% of these patients, 0.50 their nephrologist estimated that they would reach their pre- 0.25 P Log rank test <.0001 COVID-19 functional status within 1 year after diagnosis, while they estimated that this would never happen in 28%. 0.00 Patients for whom a late (>1 year) or no functional recovery 0 7 14 21 28 35 42 49 56 63 70 77 84 91 analysis time was expected, were older, had a higher frailty score, more often Number at risk hosp_icu_cat Not hospitalized = 1 108710541011 992 979 543 543 543 543 543 543 543 543 543 had coronary artery disease as a comorbidity and had a lower hosp_icu_cat Hospitalized, no ICU = 2 11651072 959 894 870 642 636 635 632 632 632 631 631 630 Hospitalized, hosp_icu_cat ICU = 3 197 168 124 100 92 67 64 62 62 60 59 59 59 59 oxygen saturation (data not shown). There were no statistically Not hospitalized Hospitalized, no ICU significant differences in limiting factors for recovery between Hospitalized, ICU patients who were not hospitalized, those hospitalized but not admitted to the ICU and those admitted to the ICU (Table 2). FIGURE 1: Kaplan–Meier curves presenting cumulative 3-month In a multivariable logistic regression analysis, older age [OR survival probability (in days) among HD patients with COVID-19. 0.98/year (95% CI 0.97–1.0)], higher frailty score [OR 0.79/unit (95% CI 0.70–0.90)] and ICU admission [OR 0.43 (95% CI 0.18–0.99)] were associated with a lower likelihood to reach Functional and mental health status pre-COVID-19 functional status (Table 4). Data on functional and mental health status were collected Treating nephrologists indicated that 94% of their patients at 3 months after a COVID-19 diagnosis and were available for had reached their pre-COVID-19 mental health status at 3 854 of the 1014 HD patients (84%) who were alive at this time months after COVID-19 diagnosis (Figure 3B). Although point and had follow-up data available (Supplementary data, mental health tended to be more often impaired in the sub- Figure S2). The residence status of these patients is presented group of patients admitted to the ICU, this was not statistically in Supplementary data, Figure S3. Characteristics of patients different compared with the other two subgroups. Among the who were excluded from this analysis because of missing values 51 patients (6%) who had not reached their pre-COVID-19 did not differ from those of the included patients, except for mental health status, the most commonly mentioned limiting active malignancy as a comorbidity, which was more frequent factors were memory loss (35%), depression (31%) and anxiety in patients with missing data, and respiration rate, which (18%). For 56% of these patients, their nephrologist expected was lower in those with missing data (Supplementary data, that the pre-COVID-19 mental status would be reached Table S3). within the upcoming year, whereas 27% were expected to At 3 months after a COVID-19 diagnosis, according to never fully recover their mental health state. There were their nephrologist, functional status had recovered to the pre- no statistically significant differences between the subgroups COVID-19 level in 87% of the patients (Figure 3A), whereas based on hospital admission (Table 3). For mental health status, this was not the case in 111 patients (13%). The proportion only a higher frailty score [OR 0.75/unit (95% CI 0.63–0.90)] 1144 M.H. Hemmelder et al. Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 FIGURE 2: Flow diagram of hospitalization, ICU admission, vital status and residence at 3 months after a COVID-19 diagnosis. was associated with a lower likelihood of reaching the pre- after a COVID-19 diagnosis. Impaired functional outcome COVID-19 status (Table 4). was associated with older age, higher frailty score and ICU There was considerable overlap in the recovery of functional admission, whereas impaired mental outcome was associated and mental status. Among the 743 patients in whom the only with higher frailty score. Among those who had not fully functional status had recovered within 3 months, there were recovered at 3 months after a COVID-19 diagnosis, 58% of only 5 patients (0.67%) in whom the mental status had not patients were expected to recover functionally and 56% to yet recovered. Conversely, almost half [46 (41.4%)] of the 111 recover mentally within 1 year. Together, our results show patients who had not yet recovered functionally also had not that although the short-term mortality of COVID-19 in HD recovered mentally after 3 months. patients is high, surviving patients have a good prognosis to Finally, the residence status differed between patients who recover from COVID-19, both functionally and mentally. had and those who had not yet recovered. Among those whose We demonstrated that in dialysis patients who were alive at functional status had not recovered, 17.2% lived in a nursing 3 months after a COVID-19 diagnosis, only 13% still had an home and 11.8% were still hospitalized after 3 months versus impaired functional status compared with their pre-COVID- 9.6% and 1.8%, respectively, in those who had recovered. For 19 status. Not unexpectedly, nonrecovery to pre-COVID-19 mental status, 24% of those not recovered lived in a nursing functional status was more frequent in patients who were home and 20% were still hospitalized, whereas this was 9.7% admitted to the ICU. The most prevalent limiting factors and 2%, respectively, for those who had reached their pre- for functional recovery were reduced muscle strength (48%), COVID-19 mental status. reduced mobility (41%) and tiredness (37%). In a French In the subgroup of PD patients, data on functional and general population cohort, 51% of patients who were admitted mental health status were available in 52 of the 168 patients. for COVID-19 reported in a telephone interview to have at At 3 months, 42 PD patients (81%) had reached their pre- least one persistent symptom, of which 31% had fatigue [14]. COVID-19 functional status and 46 (88%) had reached their In a study from China, patients who survived COVID-19 pre-COVID-19 mental health status. The small numbers of were interviewed after hospital admission with a series of patients who did not reach their previous functional (n = 10) questionnaires [15]. Fatigue or muscle weakness was reported and mental health (n = 6) status precluded a meaningful by as many as 63% of patients 6 months after COVID- analysis of the time needed to recover and factors that limited 19 onset. A report from Italy demonstrated that 54% of recovery in this group. COVID-19 survivors had some form of functional impairment after hospital admission as measured by a short physical performance battery and 2-minute walking test [16]. The DI S C U S SION frequency of nonrecovery of functional health after surviving This study shows that functional and mental health had recov- COVID-19 seems less distinct in our dialysis cohort. The ered to the pre-existent level according to their nephrologists difference in findings may be explained, at least in part, by the in the majority of dialysis patients who were alive at 3 months fact that dialysis patients are already adapted to having limited Recovery of dialysis patients with COVID-19 1145 Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 FIGURE 3: Functional and mental health status in HD patients at 3 months after a COVID-19 diagnosis, as judged by the treating nephrologist. pre-existent functional capacity. [17]. In addition, mortality 21% of patients reported cognitive disturbances 4 months after is high in these patients, which may also lead to the most fit a COVID-19 diagnosis [14]. In a Chinese cohort of COVID- patients surviving. Lastly, differences between these previous 19 survivors from the general population, sleep difficulties studies and our study in the way of assessing functional status and anxiety or depression were reported by 26% and 23% may have played a role. of patients, respectively [15]. No other data have previously Notably, the COVID-19 pandemic has raised levels of been published on the recovery of mental health status after anxiety and depression in the general population and in surviving COVID-19 in dialysis patients. In the present study, patients with various chronic conditions [18–21]. In contrast, mental health had not yet recovered to the pre-COVID-19 level Bonenkamp et al. [22] showed that the mental health of a at 3 months after a COVID-19 diagnosis in only 6% of HD small group of chronic dialysis patients without a diagnosis of patients. In contrast with functional recovery, mental health COVID-19 was not affected during the pandemic as measured recovery to pre-COVID-19 status was not significantly worse by the mental component summary score of Short Form in HD patients who had been admitted to the ICU compared 12 and items of the Dialysis Symptom Index. This suggests with the other two subgroups in our analysis. The most that the dialysis population may be different from other frequently reported limiting factors for mental health recovery populations with respect to the impact of the COVID-19 were memory loss (35%), depression (31%) and anxiety (18%). pandemic on mental health, maybe because patients already Survival at 3 months was almost identical to the survival at suffer greatly from their kidney disease and treatment [23]. 28 days after presentation with COVID-19. Only in patients Many dialysis patients have developed coping mechanisms who at any time had been admitted to the ICU, a moderate in order to maintain satisfactory mental health. In a French decrease in survival probability from 47% to 40% observed cohort of COVID-19 survivors from the general population, between 28 days and 3 months after a COVID-19 diagnosis. 1146 M.H. Hemmelder et al. Table 2. Functional status at 3 months after a COVID-19 diagnosis in HD patients Total Not hospitalized Hospitalized, no ICU Hospitalized, ICU Characteristics (N = 854) (n = 363) (n = 448) (n = 43) P-value Functional status Reached pre-COVID-19 status, n(%) 0.005 Yes 743 (87) 328 (90) 383 (85) 32 (74) No 111 (13) 35 (9.6) 65 (15) 11 (26) Limiting factora , n(%) Thromboembolic eventsb 1 (0.9) 0 1 (1.5) 0 0.7 Impaired lung function 10 (9.0) 4 (11) 4 (6.2) 2 (18) 0.36 Reduced mobility 45 (41) 14 (40) 26 (40) 5 (45) 0.94 Reduced muscle strength 53 (48) 16 (46) 29 (45) 8 (73) 0.22 Tiredness 41 (37) 10 (29) 28 (43) 3 (27) 0.28 Disturbed mental status 8 (7.2) 2 (5.7) 5 (7.7) 1 (9.1) 0.91 Declined cognitive function 12 (11) 4 (11) 8 (12) 0 0.31 Otherc 82 (74) 25 (71) 47 (72) 10 (91) 0.40 Estimated time needed to reach pre-COVID-19 status, n(%)a Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 0.52 0–3 months 18 (16) 6 (17) 12 (18) 0 3–6 months 27 (24) 8 (23) 15 (23) 4 (36) 6–12 months 20 (18) 6 (17) 10 (15) 4 (36) >1 year 11 (10) 4 (11) 7 (11) 0 Never 31 (28) 9 (26) 20 (31) 2 (18) Missing 4 3.6) 2 (5.7) 1 (1.5) 1 (9.1) a Figures do not add up to 100% since more than one answer was possible. b Including stroke and pulmonary embolism. c Including anxiety, depression and post-traumatic stress disorder. Table 3. Mental health status in HD patients at 3 months after COVID-19 diagnosis Total Not hospitalized Hospitalized, no Hospitalized, ICU Characteristics (N = 854) (n = 363) ICU (n = 448) (n = 43) P-value Mental health status Reached pre-COVID-19 status, n(%) 0.08 Yes 803 (94) 343 (94) 423 (94) 37 (86) No 51 (6.0) 20 (5.5) 25 (5.6) 6 (14) Limiting factora , n(%) Depression 16 (31) 9 (45) 6 (24) 1 (17) 0.23 Anxiety 9 (18) 5 (25) 3 (12) 1 (17) 0.52 Bereavement/grief 2 (3.9) 0 1 (4) 1 (17) 0.18 Memory loss 18 (35) 7 (35) 10 (40) 1 (17) 0.56 Delirium 2 (3.9) 0 2 (8) 0 0.34 Sleep disturbances 5 (9.8) 2 (10) 1 (4) 2 (33) 0.10 Otherb 9 (18) 2 (10) 5 (20) 2 (33) 0.38 Estimated time needed to reach pre-COVID-19 status, n(%)a 0.35 0–3 months 6 (12) 2 (10) 4 (16) 0 3–6 months 12 (24) 7 (35) 3 (12) 2 (33) 6–12 months 10 (20) 5 (25) 4 (16) 1 (17) >1 year 5 (9.8) 0 4 (16) 1 (17) Never 14 (27) 4 (20) 9 (36) 1 (17) Missing 4 (7.8) 2 (10) 1 (4) 1 (17) a Figures do not add up to 100% since more than one answer was possible. b Including, for example, itchy skin, diabetes mellitus type 1 complications and pain. Survival in patients admitted to the ICU (40%) was much of patients who were admitted to the ICU, this suggests that lower than in those who were not admitted (90%) and in those strict triage has been performed. After ICU admission, 26% of who were admitted to the hospital but not to the ICU (73%). the surviving HD patients had impaired functional outcome at The lower survival in dialysis patients who were admitted to 3 months follow-up, whereas there was no association between the ICU is remarkable, especially considering the fact that ICU admission and mental health recovery at 3 months. This these patients were younger and had a lower frailty score. In observation suggests that it is important to consider physical our opinion, this indicates that physicians in times of limited revalidation after discharge, especially after ICU discharge. resources are in general more inclined to admit younger The strength of our study is that we collected data on patients to an ICU, while they tend to be more hesitant to admit functional and mental health outcomes at 3 months after older and more frail patients, as it is assumed they have a lower diagnosis in a large cohort of dialysis patients. The ERA- chance of survival. Together with the relatively low proportion CODA database of patients with kidney replacement treatment Recovery of dialysis patients with COVID-19 1147 Table 4. Crude and adjusted ORs with 95% CIs for the likelihood that functional and mental health status recover 3 months after a COVID-19 diagnosis (yes versus no), among HD patients who survived 3 months after a COVID-19 diagnosis Recovery of pre-COVID-19 functional status (n = 854) Recovery of pre-COVID-19 mental health status (n = 854) Crude OR (95% Adjusted* OR Crude OR (95% Adjusted* OR Variables CI) (95% CI) Variables CI) (95% CI) Age (per year) 0.97 (0.96–0.99) 0.98 (0.97–1.0) Age (per year) 0.97 (0.95–0.99) 0.99 (0.96–1.01) Sex (male versus female) 0.99 (0.66–1.49) 0.94 (0.63–1.40) Sex (male versus 1.17 (0.66–2.06) 1.02 (0.57–1.80) female) Frailty score (per unit) 0.77 (0.68–0.86) 0.79 (0.70–0.90) Frailty score (per 0.71 (0.61–0.83) 0.75 (0.63–0.90) unit) Heart failure (yes versus no) 0.60 (0.39–0.95) 0.76 (0.49–1.19) Heart failure (yes 0.46 (0.25–0.83) 0.75 (0.40–1.41) versus no) Coronary artery 0.49 (0.28–0.87) 0.77 (0.43–1.37) disease (yes versus no) Respiration rate (per minute) 0.93 (0.89–0.97) 0.97 (0.92–1.02) Respiration rate 0.93 (0.88–0.98) 0.96 (0.90–1.02) Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 (per minute) Shortness of breath (yes 0.50 (0.33–0.74) 0.75 (0.48–1.18) Shortness of 0.49 (0.27–0.87) 0.71 (0.38–1.35) versus no) breath (yes versus no) Hospitalization No hospitalization 1.0 (ref) 1.0 (ref) No hospitalization 1.0 (ref) 1.0 (ref) Hospitalization, no ICU 0.63 (0.41–0.97) 0.81 (0.51–1.28) Hospitalization, 0.99 (0.54–1.81) 1.31 (0.68–2.51) no ICU Hospitalization, ICU 0.31 (0.14–0.67) 0.43 (0.18–0.99) Hospitalization, 0.36 (0.14–0.95) 0.52 (0.17–1.57) admitted ICU admitted Statistically significant results are in bold. *All variables analyzed crude were included in the multivariable models. admitted for COVID-19 contains specifically collected granu- In summary, survival in dialysis patients who survive lar data at the individual patient level, which enables detailed after the initial COVID-19 episode is relatively preserved. analysis of long-term effects of COVID-19. Data on outcome The surviving patients recovered to the pre-existent level of were complete for 84% of the patients with a known vital status functional and mental health within 3 months and most of at 3 months. Our analysis was not adversely influenced by them were living at home. Only patients who were admitted selection bias on long-term outcome, because no significant to the ICU have a substantial risk of mortality between 28 days or clinically relevant differences could be observed between and 3 months after diagnosis and of functional impairment. patients with missing data on outcome and patients with These are important clinical observations in which dialysis complete data on outcome. We therefore consider our results patients can find consolation in a rather uncertain time. representative for measuring functional and mental health outcomes in relation to the course of COVID-19 in HD patients. SU P P L E M E N TA RY DATA This study also has limitations. First, not all dialysis Supplementary data are available at ndt online. patients with COVID-19 in the participating hospitals were recorded in ERACODA. Second, due to the design of the study, the assessment of functional and mental health status was performed by physicians, because we could not contact AC K NOW L E D G E M E N T S patients. This may have led to misclassification. However, the The ERACODA collaboration is an initiative to study progno- assessment by physicians was performed using a structured sis and risk factors for mortality due to COVID-19 in patients questionnaire, and nephrologists meet their HD patients with a kidney transplant or on dialysis that is endorsed by on a regular basis in the dialysis facilities as part of a the European Renal Association. The organizational structure multidisciplinary team including social workers. Because they contains a Working Group assisted by a Management Team and know their patients well, in general they are able to detect Advisory Board. important differences in performance. Indeed, we found ERACODA Working Group: C.F.M. Franssen, R.T. Gan- that nonrecovery of both functional and mental status at sevoort (coordinator), M.H. Hemmelder, L.B. Hilbrands and 3 months after a COVID-19 diagnosis was associated with K.J. Jager. clinical characteristics and disease severity parameters at ERACODA Management Team: R. Duivenvoorden, M. admission, as well as with a greater likelihood of still being Noordzij and P. Vart. hospitalized and living in a nursing home. This reflects that the ERACODA Advisory Board: D. Abramowicz, C. Basile, clinical judgement of treating nephrologists on these outcomes A. Covic, M. Crespo, Z.A. Massy, S. Mitra, E. Petridou, JE. is valid. Sanchez and C. White. 1148 M.H. Hemmelder et al. We thank all people who entered information in the Vila Nova de Gaia/Espinho, Vila Nova de Gaia, Portugal); ERACODA database for their participation, and especially Daniela Radulescu (‘Carol Davila’ University of Medicine and all healthcare workers who have taken care of the included Pharmacy, Bucharest, Romania/Emergency Clinical Hospital COVID-19 patients. ‘Sf. Ioan’); Elena V. Zakharova (City Hospital n.a. S.P. Botkin, Moscow, Russia); Patrice Max Ambuehl, Rebecca Guidotti and Andrea Walker (City Hospital Zuürich, Zürich, Switzerland); DATA AVA I L A B I L I T Y STAT E M E N T Fanny Lepeytre, Clémentine Rabaté and Guy Rostoker Collaborators who entered data in ERACODA remain the (Claude Galien Hospital Ramsay santé, Quincy-sous-Sénart, owners of these data. The database can therefore not be France); Sofia Marques (Clínica de Hemodiálise de Felgueiras, disclosed to any third party without prior written consent from Felgueiras, Portugal); Tijana Azasevac and Gordana all data providers, but the database will be made available Strazmester Majstorovic (Clinical Centre of Vojvodina, Novi to the editorial offices of medical journals when requested. Sad, Serbia); Dajana Katicic (Croatian Society of Nephrology, Research proposals can be submitted to the Working Group Dialysis and Transplantation, Zagreb, Croatia); Marc ten Dam via COVID.19.KRT@umcg.nl. If deemed of interest and (CWZ Nijmegen, Nijmegen, The Netherlands); Thilo Krüger methodologically sound by the Working Group and Advisory (DaVita Geilenkirchen, Geilenkirchen, Germany); Szymon Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 Board, the analyses needed for the proposal will be carried out Brzosko (DaVita, Wrocław, Poland); Vassilios Liakopoulos by the Management Team. (1st Department of Internal Medicine, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece); Adriaan L. Zanen (Deventer Ziekenhuis, Deventer, The F U N DI NG Netherlands); Susan J.J. Logtenberg (Dianet Dialysis Center, Unrestricted research grants were obtained from the European Utrecht, The Netherlands); Lutz Fricke (Dialysis Center Renal Association, the Dutch Kidney Foundation, Baxter and Bochum, Bochum, Germany); Olexandr Kuryata (Dnipro State Sandoz. No organization had any role in the design of the study, Medical University, Dnipro, Ukraine); Jeroen J.P. Slebe (Elyse interpretation of results or in writing of the manuscript. Klinieken voor Nierzorg, Kerkrade, The Netherlands); Samar Abd ElHafeez (Epidemiology Department, High Institute of Public Health, Alexandria University, Alexandria, Egypt); C ON F L IC T OF I N T E R E ST STAT E M E N T Delphine Kemlin (Erasme Hospital, Brussels, Belgium); The results presented in this article have not been published Jacqueline van de Wetering, Marlies E.J. Reinders, Dennis A. previously in whole or part, except in abstract format. Hesselink and J. Kal- van Gestel (Erasmus MC Transplant Institute, Department of Internal Medicine, University Medical Center Rotterdam, Rotterdam, The Netherlands); A P P E N DI X Jaromir Eiselt and Lukas Kielberger (Faculty of Medicine ERACODA Collaborators in Pilsen, Charles University, Pilsen, Czech Republic); Hala Jeroen B. van der Net (Albert Schweitzer Hospital, Dordrecht, S. El-Wakil (Faculty of Medicine, Alexandria University, The Netherlands); Marie Essig (Ambroise Pare Hospital, Alexandria, Egypt); Martine A.M. Verhoeven (Franciscus APHP Paris-Saclay University, Boulogne Billancourt, France); Gasthuis and Vlietland, Schiedam, The Netherlands); Ian Peggy W.G. du Buf-Vereijken, Betty van Ginneken and Logan (Freeman Hospital, Newcastle upon Tyne, UK); Nanda Maas (Amphia Hospital, Breda, The Netherlands); Cristina Canal and Carme Facundo (Fundació Puigvert, Brigit C. van Jaarsveld, Frederike J. Bemelman, Farah Barcelona, Spain); Ana M. Ramos (Fundación Jiménez Díaz, Klingenberg-Salahova, Frederiek Heenan-Vos, Marc G. Madrid, Spain); Alicja Debska-Slizien (Gdansk Medical Vervloet and Azam Nurmohamed (Amsterdam UMC, University, Gdansk, Poland); Nicoline M.H. Veldhuizen Amsterdam, The Netherlands); Daniel Abramowicz and (Gelre Hospital, Apeldoorn, The Netherlands); Eirini Tigka Sabine Verhofstede (Antwerp University Hospital, Antwerp, (General Hospital of Athens ‘G. Gennimatas’, Athens, Greece); Belgium); Omar Maoujoud (Avicennes Military Hospital, Maria Anna Polyzou Konsta (General Hospital of Serres, Faculty of Medicine, Cadi Ayyad University, Marrakech Serres, Greece); Stylianos Panagoutsos (General University Morocco); Thomas Malfait (AZ Delta, Roeselare, Belgium); Hospital of Alexandroupolis, Alexandroupolis, Greece); Adele Jana Fialova (B. Braun Avitum, Litomerice, Czech Republic); Postorino and Francesco Cambareri (Grande Ospedale Edoardo Melilli, Alexandre Favà, Josep M. Cruzado and Nuria Metropolitano and CNR, Reggio Calabria, Italy); Irina Montero Perez (Bellvitge University Hospital, Hospitalet de Matceac, Ionut Nistor and Adrian Covic (Grigore T Popa Llobregat, Barcelona, Spain); Joy Lips (Bernhoven Hospital, University of Medicine and Pharmacy, Iasi, Romania/Dr Uden, The Netherlands); Harmen Krepel (Bravis Hospital, Ci Parhon Hospital, Iasi, Romania); J.H.M Groeneveld and Roosendaal/Bergen op Zoom, The Netherlands); Harun Jolanda Jousma (Haaglanden Medisch Centrum, The Hague, Adilovic (Cantonal Hospital Zenica, Bosnia and Herzegovina); The Netherlands); Fritz Diekmann, Federico Oppenheimer Maaike Hengst and Constantijn J.A.M. Konings (Catharina and Miquel Blasco (Hospital Clínic de Barcelona, Barcelona, Hospital, Eindhoven, The Netherlands); Philippe Braconnier Spain); Tiago Assis Pereira (Hospital Curry Cabral—Central and Daniel Weis (Centre Hospitalier du Nord, Luxembourg); Lisbon University Hospital Center, Lisbon, Portugal); Augusto Ryszard Gellert (Centre of Postgraduate Medical Education, Cesar Soares dos Santos Junior (Hospital das Clinicas UFMG, Warsaw, Poland); Daniela G. Alferes (Centro Hospitalar Contagem, Brazil); Carlos Arias-Cabrales, Marta Crespo, Recovery of dialysis patients with COVID-19 1149 Laura Llinàs-Mallol, Anna Buxeda, Carla Burballa Tàrrega, Spain); Louis J.M. Reichert and Jacobien Verhave (Rijnstate Dolores Redondo-Pachon, Maria Dolores Arenas Jimenez and Hospital, Arnhem, The Netherlands); Denis Titov (RUDN Alberto Mendoza-Valderrey (Hospital del Mar, Barcelona, University, Moscow, Russia); Ekaterina V. Parshina (Saint Spain); Ana Cristina Martins, Catarina Mateus, Goncalo Petersburg State University Hospital, Saint-Petersburg, Alvila and Ivo Laranjinha (Hospital de Santa Cruz, Centro Russia); Luca Zanoli and Carmelita Marcantoni (San Marco Hospitalar de Lisboa Ocidental, Lisbon, Portugal); Julia M. Hospital, University of Catania, Catania, Italy); Gijs van Hofstra, and Machiel A. Siezenga (Hospital Gelderse Vallei, Kempen (Saxenburgh Medisch Centrum, Hardenberg, The Ede, The Netherlands); Antonio Franco (Hospital General of Netherlands); Liesbeth E.A. van Gils-Verrij (Sint Antonius Alicante, Alicante, Spain); Sandra Castellano and Maria Luisa Ziekenhuis, Nieuwegein, The Netherlands); John C. Harty Rodríguez-Ferrero (Hospital General Universitario Gregorio (Southern Health and Social Care Trust, Newry, Northern Marañón, Madrid, Spain); Sagrario Balda Manzanos (Hospital Ireland); Marleen Meurs (Spaarne Gasthuis, Haarlem, The Obispo Polanco, Salud Aragón, Spain); R. Haridian Sosa Netherlands); Marek Myslak (SPWSZ Hospital, Szczecinie, Barrios, (Hospital Universitario Ramón y Cajal, Madrid, Poland); Paolo Lentini (St. Bassiano Hospital, Bassano del Spain); Wim Lemahieu (Imelda Hospital, Bonheiden, Grappo, Italy); Edwin den Deurwaarder (Streekziekenhuis Belgium); Karlijn Bartelet (Isala, Zwolle, The Netherlands); Koningin Beatrix, Winterswijk, The Netherlands); Maria Downloaded from https://academic.oup.com/ndt/article/37/6/1140/6507563 by guest on 02 October 2023 Ahmet Burak Dirim, Erol Demir, Mehmet Sukru Sever, Aydin Stendahl (Swedish Renal Registry, Jönköping, Sweden); Turkmen and Seda Şafak (Istanbul Faculty of Medicine, Hormat Rahimzadeh (Tehran University of Medical Sciences, Istanbul University, Istanbul, Turkey); Daan A.M.J. Hollander Tehran, Iran); Marcel Schouten (Tergooi, Hilversum, The and Angele Kerckhoffs (Jeroen Bosch Ziekenhuis, Den Bosch, Netherlands); Ivan Rychlik (Third Faculty of Medicine, The Netherlands); Stefan Büttner (Klinikum Aschaffenburg- Charles University and Faculty Hospital Kralovske Vinohrady, Alzenau, Aschaffenburg, Germany); Aiko P.J. de Vries, Prague, Czech Republic); Carlos J. Cabezas-Reina and Ana Soufian Meziyerh, Danny van der Helm, Marko Mallat Maria Roca (Toledo University Hospital, Toledo, Spain); and Hanneke Bouwsma (Leiden University Medical Center, Ferdau Nauta (Treant/Scheper Ziekenhuis, Emmen, The Leiden, The Netherlands); Kristina Petruliene (Lithuanian Netherlands); İdris Sahin (Turgut Ozal Medical Center, University of Health Sciences, Kaunas, Lithuania); Iris Malayta, Turkey); Eric Goffin, Nada Kanaan, Laura Labriola Verberk (Maasstad Ziekenhuis, Rotterdam, The Netherlands); and Arnaud Devresse (Université Catholique de Louvain, Frank M. van der Sande and Maarten H.L. Christiaans Cliniques universitaires St Luc, Brussels, Belgium); Anabel (Maastricht University Medical Center, Maastricht, The Diaz-Mareque (University Clinical Hospital of Santiago de Netherlands); N. MohanKumar (Manipal Hospital, Manipal, Compostela, Santiago de Compostela, Spain); Armando Coca India); Marina Di Luca (Marche Nord Hospital, Pesaro, Italy); (University Clinical Hospital of Valladolid, Valladolid, Spain); Serhan Z. Tuğlular (Marmara University School of Medicine, Gabriel de Arriba (Universitary Hospital of Guadalajara, Istanbul, Turkey); Andrea Kramer (Martini Ziekenhuis, Guadalajara, Spain); Björn K.I. Meijers, Maarten Naesens, Dirk Groningen, The Netherlands); Charles Beerenhout (Maxima Kuypers and Bruno Desschans (University Hospital Leuven, Medisch Centrum, Veldhoven, The Netherlands); Peter Leuven, Belgium); Annelies Tonnerlier and Karl M. Wissing T. Luik (Meander Medisch Centrum, Amersfoort, The (University Hospital Brussels, Brussels, Belgium); Ivana Netherlands); Julia Kerschbaum (Austrian Dialysis and Dedinska (University Hospital Martin and Jessenius Faculty of Transplant Registry, Rohr, Austria); Martin Tiefenthaler Medicine Comenius University, Martin, Slovakia); Giuseppina (Medical University Innsbruck, Innsbruck, Austria); Bruno Pessolano (University Hospital Medical Center Verona, Watschinger (Medical University of Vienna, Vienna, Austria); Verona, Italy); Shafi Malik (University Hospitals of Coventry Aaltje Y. Adema (Medisch Centrum Leeuwarden, Leeuwarden, and Warwickshire NHS Trust, Coventry, UK); Evangelia The Netherlands); Vadim A. Stepanov and Alexey B. Dounousi (University Hospital of Ioannina, Ioannina, Zulkarnaev (Moscow Regional Research and Clinical Institute, Greece); Evangelos Papachristou (University Hospital of Moscow, Russia); Kultigin Turkmen (Necmettin Erbakan Patras, Patras, Greece); Stefan P. Berger, Esther Meijer and Jan University Meram School of Medicine, Konya, Turkey); Stephan F. Sanders (University Medical Center Groningen, Ilaria Gandolfini and Umberto Maggiore (Nephrology Unit, Groningen, The Netherlands); Akin Özyilmaz (Dialysis Department of Medicine and Surgery, University of Parma, Center Groningen, Groningen, The Netherlands); Jadranka Parma, Italy); Anselm Fliedner (Nierenzentrum Reutlingen- Buturović Ponikvar, Andreja Marn Pernat, Damjan Kovac and Tübingen, Reutlingen, Germany); Anders Åsberg and Geir Miha Arnol (University Medical Center Ljubljana, Ljubljana, Mjoen (Norwegian Renal Registry, Oslo University Hospital Slovenia); Femke M. Molenaar, Arjan D. van Zuilen, Sabine Rikshospitalet, Olso, Norway); Hitoshi Miyasato (Okinawa C.A. Meijvis and Helma Dolmans (University Medical Center Chubu Hospital, Nakagami, Japan); Carola W.H. de Fijter Utrecht, Utrecht, The Netherlands); Ekamol Tantisattamo (OLVG, Amsterdam, The Netherlands); Nicola Mongera (University of California Irvine School of Medicine, Orange, (Ospedale S. Maurizio Bolzano, Bolzano, Italy); Stefano CA, USA); Pasquale Esposito (University of Genoa, Genoa, Pini (Padua University Hospital, Padua, Italy); Consuelo de Italy); Jean-Marie Krzesinski and Jean Damacène Barahira Biase, Anne Els van de Logt and Rutger Maas (Radboud (University of Liége, Liége, Belgium); Maurizio Gallieni University Medical Center, Nijmegen, The Netherlands); (University of Milan, Milan, Italy); Paloma Leticia Martin- Olga Lebedeva (Regional Clinical Hospital, Yaroslavl, Russia); Moreno (University of Navarra Clinic, Pamplona, Spain); Veronica Lopez (Regional Hospital of Malaga, Malaga, Gabriele Guglielmetti (University of Piemonte Orientale, 1150 M.H. Hemmelder et al. 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