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NDT Advance Access published online on November 28, 2007
Nephrology Dialysis Transplantation, doi:10.1093/ndt/gfm766
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© The Author [2007]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org


Pre-Transplant Predictors of Cerebrovascular Events After Kidney Transplantation

Susanne Aull-Watschinger1, Hermina Konstantin2, Demetrakis Demetriou2, Martin Schillinger3, Antje Habicht2, Walter H. Hörl2 and Bruno Watschinger2

1 Department of Neurology, Medical University of Vienna, Austria 2 Department of Internal Medicine III, Medical University of Vienna, Austria 3 Department of Internal Medicine II, Medical University of Vienna, Austria

Correspondence and offprint requests to: Bruno Watschinger, Universitätsklinik für Innere Medizin III, Medizinische Universität Wien, Währinger Gürtel 18-20, A-1090 Wien, Austria. Tel: +43-1-40-400-2195; Fax: +43-1-40-400-2194; E-mail: bruno.watschinger{at}meduniwien.ac.at



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. We evaluated cerebrovascular events (CVE) after kidney transplantation (KTx) and sought to identify pre-transplant predictors of transient ischaemic attacks (TIA) and strokes post-transplantation.

Methods. A total of 1617 consecutive kidney and 16 kidney–pancreas recipients transplanted between 1995 and 2005 were analysed in this retrospective single-centre study. Risk factors for CVE, e.g. recipient and donor age and gender, diagnosis of chronic kidney disease, end-stage renal disease (ESRD) duration, histories of hypertension, hyperlipidaemia, smoking, atrial fibrillation (AF), diabetes mellitus (DM), ischaemic heart, peripheral- and cerebro-vascular disease, as well as pre-transplant myocardial infarction or CVE (i.e. TIA/strokes) were analysed. Furthermore, the predictive value of pre-transplant screening tests, i.e. echocardiography (n = 1184) and carotid ultrasound (n = 922), was investigated.

Results. During a median follow-up of 4 years, 64 CVE (54 strokes and 10 TIA) were observed. Nineteen (5.1%) of 373 deceased patients died from fatal stroke. Recipient age, history of AF and hyperlipidaemia (P = 0.00, respectively), reduced left ventricular function (LVF) (P = 0.01) and the degree of stenosis by carotid ultrasound (P = 0.002), duration of ESRD (P = 0.03) and interstitial nephritis as renal disease cause (P = 0.04) evolved as predictors of TIA/stroke post-transplant in univariate analysis. In multivariable analysis, AF (P = 0.001) and DM (P = 0.037) were significant predictors for post-transplant CVE.

Conclusions. AF and DM are independent predictors of CVE after KTx. Beyond their general ability to detect sev- erely comorbid patients, pre-transplant screening tests (e.g. carotid ultrasound or echocardiography) were not able to identify renal transplant candidates at risk for CVE after transplantation.

Keywords: atrial fibrillation; left ventricular function; outcome; renal transplantation; stroke



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 References
 
Kidney transplantation (KTx) has become the preferred treatment for patients with end-stage renal disease (ESRD). Graft survival has increased considerably over the last decades, due to improvements in patient care including patient selection, new immunosuppressive strategies and post-transplant surveillance. These interventions have allowed patients with a higher cardiovascular risk, to be accepted for transplantation and led to significant survival benefits for transplant patients when compared to dialysis patients remaining on the waiting list [1]. Nevertheless, cardiovascular problems remain important factors for morbidity and mortality after KTx and contribute most prominently to the yet unsolved problem of death with a functioning allograft. [2–4] Cardiovascular complications and risk factors have been investigated in a large series of patients with ESRD [3,5–11]. Several studies investigated strokes in chronic dialysis patients and reported a high frequency of cerebrovascular events (CVE) in this patient population [12–16]. In contrast, reports on cerebrovascular outcomes in kidney transplant recipients are scarce [17–21].

We therefore investigated 1633 adult patients transplanted at our institution between 1995 and 2005 with regard to neurological complications after KTx. We intended to identify risk factors and predictors of strokes after renal transplantation. As the value of pre-transplant screening evaluations at the time of wait-listing is often a matter of debate [22–25], it was an additional aim of our study to evaluate their relevance in predicting CVE in kidney transplant recipients.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 References
 
Patients
We analysed data from 1633 consecutive ESRD patients (age > 18 years), who received a kidney allograft (n = 1617) or a combined kidney–pancreas transplant (n = 16) at the Medical University of Vienna between January 1995 and December 2005. Demographics and clinical characteristics of the study cohort are given in Tables 1 and 2. The past medical history of the patients was recorded retrospectively by an extensive review of all patient charts. Relevant clinical data and events were recorded (i.e. recipient age and gender, diagnosis of chronic kidney disease, duration of ESRD, donor age and gender). At the time of KTx histories of hypertension, hyperlipidaemia, smoking, AF, DM, ischaemic heart and peripheral vascular disease or myocardial infarction and CVE, i.e. stroke or transient ischaemic attacks (TIA), as well as current medications (lipid-lowering, antihypertensive and antiplatelet and/or anticoagulant therapy) and laboratory values (haemoglobin, serum albumin, C-reactive protein) were noted. The presence of hypertension or hyperlipidaemia was defined by the need for the respective medication. We relied on the necessity for drug treatment rather than on a single blood pressure or laboratory measurement at the time of KTx, for identifying patients with hypertension or hyperlipidaemia. Diabetes mellitus was defined by a diagnosis of diabetes prior to or the need of diabetic medication at the time of KTx. In addition, we reviewed all available pre-transplant evaluation examinations (usually performed by experienced investigators at the referring centres). Those considered relevant for neurological outcomes (electrocardiogram, carotid duplex ultrasound and echocardiography) were included for further analysis. Other than in transplant centres elsewhere, it has become a prerequisite to perform an echocardiography and a carotid ultrasound in order to be accepted for KTx at our centre. These investigations are covered by social insurance in Austria. The majority of patients were followed after KTx at the Department of Nephrology of the Medical University of Vienna; all others are followed exclusively by other hospital-based nephrology departments. This is typical for Austria, where nephrologists in private practice are scarce. Data from patients, followed in these other centres (n = 15), were obtained by actual review of patient charts by one of us visiting these centres or by personal communication from the respective treating physicians, who reported the occurrence of neurological complications and of major endpoints by filling in a standardized questionnaire. All these physicians responded as they are well trained and motivated in reporting data on renal patients by regularly reporting to the Austrian Dialysis and Transplantation Registry. For this reason and due to the fact that more events were observed in patients treated elsewhere, completeness and validity of the data can be assumed and underreporting of events is unlikely. The observation period started at the time of KTx and ended, with the date of transplant failure, death, loss to follow-up or in June 2007, whichever came first. Thus the observation period is restricted to the time span with a functional transplant and does not include time on dialysis. CVE were defined as transient ischaemic attack (TIA), when focal neurological symptoms resolved within 24 h of onset or stroke, defined as a focal neurological deficit persisting longer than 24 h, with CT or MRI documentation. The study was approved by the Institutional Review Board.


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  		Table 1. Demographic data and clinical characteristics of 1633 patients undergoing kidney transplantation or combined kidney– pancreas transplantation with or without a cerebrovascular event (TIA/stroke) during follow-up—transplant related data

 

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  		Table 2. Demographic data and clinical characteristics of 1633 patients undergoing kidney transplantation or combined kidney pancreas transplantation with or without a cerebrovascular event (TIA/stroke) during follow-up—comorbidity-related data

 
Description and interpretation of pre-transplant evaluation test results
Heart rhythm: Patients were assigned to the AF group, if AF was recorded from the electrocardiogram performed at the time of wait-listing or at transplantation or in the case of a positive history of intermittent or permanent AF at the time of KTx.

Carotid duplex ultrasound: All available results of carotid ultrasounds performed for the purpose of wait-listing were included for analysis and were quantified as plaques, mild stenosis between 25 and 50%, moderate stenosis between 51 and 70% and high-grade stenosis >70%.

Echocardiography: Left ventricular function (LVF) was defined as normal if ejection fraction (EF) exceeded 50% or fractional shortening (FS) was >28%. Impaired LVF was defined as EF <50% or FS <28%.

Statistical analysis
Continuous data are presented as the median and the interquartile range (range from the 25th to the 75th percentile), or the total range. Discrete data are given as counts and percentages. We used Mann–Whitney U tests (for continuous variables) and Fisher exact tests or chi-square tests (for categorical variables), as appropriate for univariate analyses. Multivariable Cox proportional hazards models were applied to assess the association between potential risk factors and the occurrence of a first CVE and to adjust for confounding effects of other baseline variables. Results of the Cox models are presented as the hazards ratio (HR) and the 95% confidence interval (95% CI). Baseline variables were considered for inclusion in the multivariate model (a) if they were imbalanced between patients with and without neurological events as indicated by a univariate P-value <0.2 (Table 1) or (b) if they were clinically established risk factors for TIA/stroke. We tested for interactions between baseline variables by multiplicative interaction terms and log likelihood ratio chi-square tests. We assessed the overall model fit using Cox–Snell residuals. Furthermore, we tested the proportional hazard assumption for all covariates using Schoenfeld residuals (overall test) and the scaled Schoenfeld residuals (variable-by-variable testing). According to the tests the proportional hazards assumption was not violated. A two-sided P-value <0.05 was defined as statistically significant. Calculations were performed with Stata (release 8.0; Stata) and SPSS for Windows (version 10.0; SPSS Inc.).



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 References
 
We analysed data from 1633 adult patients (age >18 years), who received a kidney allograft (n = 1617) or a combined kidney–pancreas transplant (n = 16). Most of the patients (n = 1459; 89.3%) received a deceased donor transplant. Only 174 (10.7%) patients received a living donor kidney. The vast majority of patients (n = 1379) received a first transplant, 194 (11.9%) were transplanted for the 2nd time and 60 (3.7%) were transplanted for the 3rd, 4th, 5th or 6th time. During a median follow-up of 4 years (IQR 1.5; 6.7; total range 0 to 12.4 years) a total of 64 CVE (54 strokes and 10 TIA) were observed in the study cohort. Only the first event (in the case of recurrent TIA/stokes) was accounted for in a single patient. Forty-seven of 64 events (37 strokes and 10 TIA) were ischaemic, 14 were haemorrhagic and 3 remained unclear. Nineteen (29.7%) of the 64 CVE were fatal (9 ischaemic and 7 haemorrhagic strokes). In three fatal cases the underlying pathology for the CVE remained uncertain. Strokes accounted for 5.1% (n = 19) of the 373 patient deaths in the cohort during the observation period.

Patient characteristics for the groups, with or without stroke, are given in Tables 1 and 2. Univariate analysis revealed that patients who experienced a CVE were older (57.9 versus 51.0 years; P = 0.00), had a longer duration of renal replacement therapy (3.4 versus 2.6 years; P = 0.03) and were more likely to have interstitial nephritis (7.8 versus 2.9%; P = 0.04) or hyperlipidaemia (46.9 versus 27.8%; P = 0.00). A history of AF (P = 0.00) and a reduced LVF (P = 0.01) evolved as significant predictors of TIA/stroke after KTx in univariate analysis. Donor age (48.0 versus 48.0 years; P = 0.7) and the rate of previous TIA/strokes were comparable (7.8 versus 6.2%; P = 0.59) between the groups. Other signs of atherosclerotic disease (ischaemic heart and peripheral vascular disease or a history of myocardial infarction) did not differ significantly.

In the subsequent multivariable Cox analysis a history of AF (P = 0.001) and DM (P = 0.037) was detected as predictors of a TIA/stroke after renal transplantation (Table 3 and Figures 1 and 2). The other parameters did not evolve as independent predictors of CVE in the multivariable analysis.


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  		Table 3. Cox proportional hazards model assessing the risk for transient ischaemic attacks, minor and major strokes in 1633 patients after renal transplantation

 

Figure 1
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  		Fig. 1. Adjusted risk for transient ischaemic attacks, minor and major strokes in 1633 patients after renal transplantation by multivariable Cox proportional hazards analysis. Model was adjusted for variables as listed in Table 3. AF = atrial fibrillation.

 

Figure 2
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  		Fig. 2. Adjusted risk for transient ischaemic attacks, minor and major strokes in 1633 patients after renal transplantation by multivariable Cox proportional hazards analysis. Model was adjusted for variables as listed in Table 3. DM = diabetes mellitus.

 
The predictive value of pre-transplant screening tests was investigated.

Echocardiography: We performed echocardiography in 1184 patients. A reduction of LVF was found in 137 (11.6%) of the patients. Pre-transplant impairment of LVF (detected by echocardiography performed at the time of wait-listing) was significantly associated with TIA/stroke in our study cohort in univariate analysis (P = 0.01) but lost its significant value for predicting CVE post-KTx in the subsequent multivariate analysis (P = 0.055).

Carotid ultrasound: In 922 patients data from pre-transplant carotid ultrasound investigations were available. Degrees of stenosis were quantified as plaques (n = 819), mild stenosis between 25 and 50% (n = 44), moderate stenosis between 51 and 70% (n = 50) and high-grade stenosis > 70% (n = 9). The degree of stenosis by carotid ultrasound was significantly associated with the occurrence of TIA/stroke by univariate analysis (P = 0.002; Table 2) but not by multivariable Cox analysis (P = 0.61; Table 3). Adjusted odds ratios predicting CVE compared to patients without stenosis for mild-, moderate- and high-grade stenosis were 1.68 (0.59–4.78), 1.54 (0.47–2.76) and 1.71 (0.20–15.06), respectively (P = 0.61).



   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
References
 
Of 1633 kidney and simultaneous kidney–pancreas recipients included in our analysis, 64 (3.9%) patients experienced a TIA/stroke during a median post-operative observation period of 4 years. Nineteen patients suffered a fatal stroke. Multivariable analysis revealed that a history of AF is an independent risk factor for the occurrence of a CVE post-transplantation. In addition, the presence of DM at the time of KTx predicted TIA/stroke thereafter. An impaired LVF at the time of wait-listing showed a trend towards an adverse effect on cerebrovascular outcomes. Pre-transplant evidence of atherosclerotic disease, TIA/strokes before KTx, hypertension, hyperlipidaemia, the primary cause of renal disease, the duration of renal replacement therapy, a history of smoking or the gender of the patient are not predictive of a subsequent CVE.

The low incidence of neurological complications in our transplant patients is intriguing, as a high incidence of strokes is reported for dialysis patients [13–16]. Chronic dialysis patients were reported to be at particular risk for cerebral haemorrhage, which may have been significantly enhanced by the need of repetitive anticoagulation during the dialysis sessions [14]. In contrast, without the need of large-scale anticoagulation in our transplant population, the number of haemorragic events was significantly less and ischaemic events predominated. In addition, patients receiving a kidney transplant represent a positively selected group of chronic kidney disease patients and thus, can not be compared with the group of dialysis patients not undergoing KTx. Patients at high risk are usually excluded from the waiting list after a thorough pre-transplant evaluation process, or undergo correction of significant medical problems before KTx. Furthermore transplant candidates are generally younger than the average of all dialysis patients combined. The median age in our cohort was 51.4 years.

All available studies investigating neurological events after KTx were performed in patients transplanted before the year 2000 [18–21]. Oliveras et al. found a stroke prevalence of 8% at 10 years, and reported that events occurred at a mean of 49 months after transplantation [18]. This observation time is longer than the time frame in our study. It will be interesting to see if with longer observation time the incidence of strokes will rise in our patients. This would not be surprising as the stroke risk rises with increasing age. Wijdicks et al. studied intracranial haematomas and reported bleeding in 9 of 1573 transplant patients (0.6%) during an observation period of 57 months [20]. In contrast, we included TIA together with strokes as endpoints in our analysis and found a prevalence of 3.9%. Wijdicks et al. reported a stroke-related death rate (1%; 6 out of 530 patient deaths). Fatal strokes occurred in 19 patients of our cohort, representing 5.1% of all deaths. In American patients, strokes accounted for 8% of deaths in renal transplant patients [26]. This is higher than that seen in our cohort. However, variability in the patient populations (e.g. ethnic disparities, our Caucasian, middle European population did not include patients of African origin), in duration of follow-up, as well as differences in the standard of medical care at the time of the studies (e.g. more ambitious treatment goals and intensified blood pressure and lipid control in recent years) make a direct comparison of the results difficult.

Another aim of our study was to investigate pre-transplant factors that could be useful in predicting TIA/stroke after KTx and to elaborate a risk pattern for patients at the time of transplantation. We decided to focus exclusively on the pre-transplant period and not to include important post-transplant factors (such as changes in blood pressure, laboratory values (GFR, proteinuria, lipids, calcium, phosphate, etc.) that may also influence cerebrovascular outcomes in this patient population.

We now show, as yet unknown for renal transplant patients, that a history of AF is predictive of a later CVE. (Figure 1) AF is a well-accepted risk factor for CVE [27–29] and has been shown to be not uncommon in renal transplant patients [30]. Nevertheless, studies in non-transplant patients investigating the influence of heart rhythm on strokes yielded inconsistent results. In patients with heart failure for example, AF was found to be associated with an increased risk for stroke in some [31,32], but not all studies [32–35]. In our cohort AF remained a robust prognostic factor even when tested in a multivariable model.

In a small study using echocardiography in 141 patients immediately before transplantation, systolic function was an independent predictor of cardiovascular outcome after KTx, which was, however, not further specified [36]. An association between heart failure and stroke has been shown earlier but was never suggested in recipients of a renal allograft [35,37–40]. It would be interesting to test the role of LVF in a standardized and prospective study in transplant patients, as a reduction in LFV was significant in univariate but not in multivariate analysis in our patients. The relative wide confidence interval of ejection fraction as a marker for elevated risk indicates a high variability and a rather low specificity for predicting adverse outcome in this group of transplant patients. Furthermore, the number of patients with reduced ejection fraction (11.6%) was rather small and certainly also contributed to the loss of significance in the multivariable model. Carotid ultrasound performed at the time of wait-listing did not predict the occurrence of stroke after transplantation in multivariable analysis. While carotid changes are predictive of CVE in patients with ESRD and on dialysis in the long-term follow-up [41], asymptomatic lesions—in accordance with findings of others [42]—were not predictive of later events in our transplant recipients during the follow-up period.

The pattern of risk factors in our cohort differs in frequency from those identified earlier in Austrian stroke patients [43–45]. We could not identify a history of TIA/strokes or of other atherosclerotic comorbidities (ischaemic heart disease, myocardial infarction, peripheral artery disease) as predictors of subsequent TIA/strokes, even though they carry a poor prognostic value in other patient cohorts [46,47]. Similarly a history of cigarette smoking did not have any prognostic impact. DM however was identified as a risk factor for TIA/stroke after transplantation in our cohort (Figure 2). Eleven of the 284 patients with diabetes at KTx experienced a CVE during the follow-up (one of them after receiving a combined kidney/pancreas transplant). As polycystic kidney disease is associated with the occurrence of cerebral aneurysms and a higher risk of intracerebral bleeding was suggested for this patient group [16,20], we were interested in whether the primary cause of renal disease was associated with an increased risk for CVE. We did not find any association between the cause of renal disease and the occurrence of TIA/stroke in multivariate analysis. The significance of interstitial nephritis as positive predictor in univariate analysis may have been a type I error due to the small number of patients with this type of renal disease.

We defined hyperlipidaemia by statin therapy at the time of transplantation, as most of the patients did not undergo a period of fasting before their blood was analysed before receiving a transplant. Even though this investigation does not intend to study a treatment effect, it is interesting to note that statin treatment did not change the risk of the patients. This is in line with investigations that showed that statins, while reducing the risk of cerebral ischaemic events, did not decrease the risk of haemorrhagic stroke in the recently published Heart Protection Study [48] and did not reduce the risk of stroke in German diabetic dialysis patients [49].

We recognize the limitations of our single-centre study design, which was not performed as a prospective trial. Our findings require prospective confirmation. We were not able to measure the timing and duration of anticoagulant therapy. Practically all our patients were Caucasians. Thus the results are only representative for this ethnic group and should be confirmed in other patient populations. Pre-transplant examinations were not performed in a core facility by a single selected investigator (as is the case in controlled clinical trials) but by different physicians at the referring centres (inter-observer variations were not studied). We do not know whether all echocardiography studies were performed at the patients ‘dry weights’. Even though the lack of standardization limits the value of the test results, we believe that our collection of data reflects every day clinical practice, where many transplant centres need to rely on test results obtained outside the transplant facility. We cannot exclude underreporting of CVE, as patients were not seen by a neurologist on a regular basis. However, due to our national system, practically all patients are treated exclusively by a limited number of specialized nephrological clinics and are consistently seen by the same nephrologists. We think that this, the extensive review of the patients’ charts and the large number (n = 1633) of renal transplant recipients included in the analysis, contributes to the reliability of the data.

In summary we found that DM and AF are predictors of CVE after KTx in our transplant population, while other traditional risk factors are not. The value of pre-transplant screening tests such as echocardiography and carotid ultrasound with regard to CVE after KTx does not expand beyond their ability to identify patients with major comorbidities, which may lead to the exclusion of patients from being wait-listed for transplantation.



   Acknowledgments
 
The authors thank the physicians of all referring centres for their unanimous help.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

  1. Wolfe RA, Ashby VB, Milford EL, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med (1999) 341:1725–1730.[Abstract/Free Full Text]
  2. Aakhus S, Dahl K, Wideroe TE. Cardiovascular disease in stable renal transplant patients in Norway: morbidity and mortality during a 5-yr follow-up. Clin Transplant (2004) 18:596–604.[CrossRef][Web of Science][Medline]
  3. Holdaas H, Fellstrom B, Jardine AG, et al. Effect of fluvastatin on cardiac outcomes in renal transplant recipients: a multicentre, randomised, placebo-controlled trial. Lancet (2003) 361:2024–2031.[CrossRef][Web of Science][Medline]
  4. Ojo AO. Cardiovascular complications after renal transplantation and their prevention. Transplantation (2006) 82:603–611.[Web of Science][Medline]
  5. Dimeny EM. Cardiovascular disease after renal transplantation. Kidney Int Suppl (2002) (80):78–84.
  6. Kasiske BL. Ischemic heart disease after renal transplantation. Kidney Int (2002) 61:356–369.[CrossRef][Web of Science][Medline]
  7. Kasiske BL, Maclean JR, Snyder JJ. Acute myocardial infarction and kidney transplantation. J Am Soc Nephrol (2006) 17:900–907.[Abstract/Free Full Text]
  8. Kendrick E. Cardiovascular disease and the renal transplant recipient. Am J Kidney Dis (2001) 38(Suppl_6):S36–S43.[Web of Science][Medline]
  9. Marcen R, Morales JM, Arias M, et al. Ischemic heart disease after renal transplantation in patients on cyclosporine in Spain. J Am Soc Nephrol (2006) 17(Suppl 3):S286–S290.[Abstract/Free Full Text]
  10. Rigatto C, Parfrey P, Foley R, et al. Congestive heart failure in renal transplant recipients: risk factors, outcomes, and relationship with ischemic heart disease. J Am Soc Nephrol (2002) 13:1084–1090.[Abstract/Free Full Text]
  11. Marcen R. Cardiovascular risk factors in renal transplantation–current controversies. Nephrol Dial Transplant (2006) 21(Suppl 3):iii3–iii8.
  12. Toyoda K, Fujii K, Fujimi S, et al. Stroke in patients on maintenance hemodialysis: a 22-year single-center study. Am J Kidney Dis (2005) 45:1058.[CrossRef][Web of Science][Medline]
  13. Iseki K, Fukiyama K. Predictors of stroke in patients receiving chronic hemodialysis. Kidney Int (1996) 50:1672–1675.
  14. Iseki K, Kinjo K, Kimura Y, et al. Evidence for high risk of cerebral hemorrhage in chronic dialysis patients. Kidney Int (1993) 44:1086–1090.[Web of Science][Medline]
  15. Kawamura M, Fijimoto S, Hisanaga S, et al. Incidence, outcome, and risk factors of cerebrovascular events in patients undergoing maintenance hemodialysis. Am J Kidney Dis (1998) 31:991–996.[Web of Science][Medline]
  16. Pirson Y, Christophe JL, Goffin E. Outcome of renal replacement therapy in autosomal dominant polycystic kidney disease. Nephrol Dial Transplant (1996) 11(Suppl 6):24–28.[Free Full Text]
  17. Ponticelli C, Campise MR. Neurological complications in kidney transplant recipients. J Nephrol (2005) 18:521–528.[Web of Science][Medline]
  18. Oliveras A, Roquer J, Puig JM, et al. Stroke in renal transplant recipients: epidemiology, predictive risk factors and outcome. Clin Transplant (2003) 17:1–8.[CrossRef][Web of Science][Medline]
  19. Adams HP Jr, Dawson G, Coffman TJ, et al. Stroke in renal transplant recipients. Arch Neurol (1986) 43:113–115.[Abstract/Free Full Text]
  20. Wijdicks EF, Torres VE, Schievink WI, et al. Cerebral hemorrhage in recipients of renal transplantation. Mayo Clin Proc (1999) 74:1111–1112.[Abstract]
  21. Bruno A, Adams HP Jr. Neurologic problems in renal transplant recipients. Neurol Clin (1988) 6:305–325.[Web of Science][Medline]
  22. Scandling JD. Kidney transplant candidate evaluation. Semin Dial (2005) 18:487–494.[CrossRef][Web of Science][Medline]
  23. Knoll G, Cockfield S, Blydt-Hansen T, et al. Canadian Society of Transplantation: consensus guidelines on eligibility for kidney transplantation. CMAJ (2005) 173:S1–S25.[Free Full Text]
  24. Kasiske BL, Cangro CB, Hariharan S, et al. The evaluation of renal transplantation candidates: clinical practice guidelines. Am J Transplant (2001) 1(Suppl 2):3–95.[Medline]
  25. European best practice guidelines for renal transplantation (part 1). Nephrol Dial Transplant (2000) 15(Suppl 7):1–85.[Free Full Text]
  26. Howard RJ, Patton PR, Reed AI, et al. The changing causes of graft loss and death after kidney transplantation. Transplantation (2002) 73:1923–1928.[CrossRef][Web of Science][Medline]
  27. Hart RG, Palacio S, Pearce LA. Atrial fibrillation, stroke, and acute antithrombotic therapy: analysis of randomized clinical trials. Stroke (2002) 33:2722–2727.[Abstract/Free Full Text]
  28. Wolf PA, Abbott RD, Kannel WB. Atrial fibrillation: a major contributor to stroke in the elderly. The framingham study. Arch Intern Med (1987) 147:1561–1564.[Abstract/Free Full Text]
  29. Wolf PA, Abbott RD, Kannel WB. Atrial fibrillation as an independent risk factor for stroke: the framingham Study. Stroke (1991) 22:983–988.[Abstract/Free Full Text]
  30. Abbott KC, Reynolds JC, Taylor AJ, et al. Hospitalized atrial fibrillation after renal transplantation in the United States. Am J Transplant (2003) 3:471–476.[CrossRef][Web of Science][Medline]
  31. Cioffi G, Pozzoli M, Forni G, et al. Systemic thromboembolism in chronic heart failure. A prospective study in 406 patients. Eur Heart J (1996) 17:1381–1389.[Abstract/Free Full Text]
  32. Walsh MN, Prystowsky EN. Anti-thrombotic strategies for patients with atrial fibrillation and heart failure. Heart Fail Rev (2002) 7:261–266.[CrossRef][Medline]
  33. Dunkman WB, Johnson GR, Carson PE, et al. Incidence of thromboembolic events in congestive heart failure. The V-HeFT VA Cooperative Studies Group. Circulation (1993) 87(6 Suppl):VI94– V101.
  34. Natterson PD, Stevenson WG, Saxon LA, et al. Risk of arterial embolization in 224 patients awaiting cardiac transplantation. Am Heart J (1995) 129:564–570.[CrossRef][Web of Science][Medline]
  35. Witt BJ, Brown RD Jr, Jacobsen SJ, et al. Ischemic stroke after heart failure: a community-based study. Am Heart J (2006) 152:102–109.[CrossRef][Web of Science][Medline]
  36. McGregor E, Jardine AG, Murray LS, et al. Pre-operative echocardiographic abnormalities and adverse outcome following renal transplantation. Nephrol Dial Transplant (1998) 13:1499–1505.[Abstract/Free Full Text]
  37. Dries DL, Rosenberg YD, Waclawiw MA, et al. Ejection fraction and risk of thromboembolic events in patients with systolic dysfunction and sinus rhythm: evidence for gender differences in the studies of left ventricular dysfunction trials. J Am Coll Cardiol (1997) 29:1074–1080.[Abstract]
  38. Gottdiener JS, McClelland RL, Marshall R, et al. Outcome of congestive heart failure in elderly persons: influence of left ventricular systolic function. The Cardiovascular Health Study. Ann Intern Med (2002) 137:631–639.[Abstract/Free Full Text]
  39. Loh E, Sutton MS, Wun CC, et al. Ventricular dysfunction and the risk of stroke after myocardial infarction. N Engl J Med (1997) 336:251–257.[Abstract/Free Full Text]
  40. Pullicino PM, Halperin JL, Thompson JL. Stroke in patients with heart failure and reduced left ventricular ejection fraction. Neurology (2000) 54:288–294.[Abstract/Free Full Text]
  41. Schwaiger JP, Lamina C, Neyer U, et al. Carotid plaques and their predictive value for cardiovascular disease and all-cause mortality in hemodialysis patients considering renal transplantation: a decade follow-up. Am J Kidney Dis (2006) 47:888–897.[CrossRef][Web of Science][Medline]
  42. Massy ZA, Mamzer-Bruneel MF, Chevalier A, et al. Carotid atherosclerosis in renal transplant recipients. Nephrol Dial Transplant (1998) 13:1792–1798.[Abstract/Free Full Text]
  43. Aull S, Lalouschek W, Schnider P, et al. Dynamic changes of plasma lipids and lipoproteins in patients after transient ischemic attack or minor stroke. Am J Med (1996) 101:291–298.[CrossRef][Web of Science][Medline]
  44. Lechner H, Schmidt R, Reinhart B, et al. Cerebrovascular risk factors in an elderly Austrian population: first year results of the austrian stroke prevention study (ASPS). Wien Klin Wochenschr (1993) 105:398–403.[Web of Science][Medline]
  45. Zeiler K, Siostrzonek P, Lang W, et al. Different risk factor profiles in young and elderly stroke patients with special reference to cardiac disorders. J Clin Epidemiol (1992) 45:1383–1389.[CrossRef][Web of Science][Medline]
  46. Wolf PA, D’Agostino RB, Belanger AJ, et al. Probability of stroke: a risk profile from the framingham Study. Stroke (1991) 22:312–318.[Abstract/Free Full Text]
  47. Di Carlo A, Lamassa M, Baldereschi M, et al. Risk factors and outcome of subtypes of ischemic stroke. Data from a multicenter multinational hospital-based registry. The european community stroke project. J Neurol Sci (2006) 244:143–150.[CrossRef][Web of Science][Medline]
  48. MRC/BHF Heart Protection Study of cholesterol lowering with simvastatin in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet (2002) 360:7–22.[CrossRef][Web of Science][Medline]
  49. Wanner C, Krane V, Marz W, et al. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N Engl J Med (2005) 353:238–248.[Abstract/Free Full Text]
Received for publication: 7. 8.07
Accepted in revised form: 1.10.07


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D. Habedank, T. Kung, T. Karhausen, S. von Haehling, W. Doehner, J. C. Schefold, D. Hasper, S. Reinke, S. D. Anker, and P. Reinke
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