|Year : 2014 | Volume
| Issue : 4 | Page : 740-747
Cerebrovascular stroke in chronic kidney disease
Mohammad Ezzat Elwan1, Wafik Mahmoud El Sheikh1, Ahmad Mohammad El Shereef1, Rasha Ali El Kapany1, Enas Attef Al Naggar2
1 Department of Neurology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Neuropsychiatry, Kafr El Sheikh General Hospital, Kafr El Sheikh, Egypt
|Date of Submission||14-Jul-2013|
|Date of Acceptance||17-Nov-2013|
|Date of Web Publication||22-Jan-2015|
Enas Attef Al Naggar
Department of Neuropsychiatry, Kafr El Sheikh General Hospital, 4th Othman Ben Affan Street, Kafr El Sheikh
Source of Support: None, Conflict of Interest: None
The aim of the present study was to investigate the traditional and nontraditional risk factors in chronic kidney disease (CKD) patients with stroke and the role of renal function in the short-term outcome of stroke.
Over the past decade, considerable evidence has accumulated on the increased incidence of stroke and mortality associated with CKD.
Patients and methods
A total of 67 patients with first ever stroke, either ischemic or hemorrhagic, with CKD were compared with 30 first ever stroke patients who were free from the signs and symptoms of CKD.
All patients were assessed on admission (day 0) and then followed up at day 7 and day 30. Motor and functional disability was assessed using the National Institutes of Health Stroke Scale, and stroke outcome was assessed using the Barthel index scale.
CKD patients had a significantly higher rate of hemorrhagic stroke than the control group (37.3 vs. 16.6%; P < 0.05). In the hemodialysis population in group II CKD ischemic stroke showed a predominance of vertebrobasilar arterial territory infarcts (P < 0.05). Patients with estimated glomerular filtration rate less than 15 ml/min/1.73 m 2 had the highest motor and functional disability, with a mean National Institutes of Health Stroke Scale score of 16.3 ± 5.9. Patients with CKD had a significantly higher risk of case fatality rate, reaching 41.7%, compared with the control group (30%).
CKD patients with stroke had a significantly higher risk of case fatality rate; reduced estimated glomerular filtration rate on admission is related to poor stroke outcome. In CKD patients, as serum albumin and hemoglobin level decrease, the severity of stroke increases.
Keywords: Chronic kidney disease, stroke, glomerular filtration rate, mortality rate, cerebelovascular stroke
|How to cite this article:|
Elwan ME, El Sheikh WM, El Shereef AM, El Kapany RA, Al Naggar EA. Cerebrovascular stroke in chronic kidney disease. Menoufia Med J 2014;27:740-7
|How to cite this URL:|
Elwan ME, El Sheikh WM, El Shereef AM, El Kapany RA, Al Naggar EA. Cerebrovascular stroke in chronic kidney disease. Menoufia Med J [serial online] 2014 [cited 2020 Feb 16];27:740-7. Available from: http://www.mmj.eg.net/text.asp?2014/27/4/740/149727
| Introduction|| |
Chronic kidney disease (CKD) is defined as dysfunction of the kidney lasting longer than 3 months, with or without reduced glomerular filtration rate (GFR) . Chronic renal failure requiring dialysis or transplantation is known as end-stage renal disease (ESRD) . The prevalence of stroke in patients with CKD may reach 10% and up to 17% in the hemodialysis population compared with 4% in the general population. The incidence of a new stroke is 9.5% for patients with CKD and 15% for hemodialysis patients compared with 2.4% in patients without CKD . Stroke is also 6-9 times more common in hospitalized hemodialysis patients than in non dialysis patients .
The real burden of stroke is chronic disability rather than death. Stroke is the leading cause of serious, long-term disability in the USA . However, stroke remains the third leading cause of death in the general population . Also, it was found that stroke itself has an adverse effect on the kidney functions of stroke patients without CKD. Stroke may produce this effect through elevated sympathetic activity, renal ischemia/reperfusion injury, or increased oxidative stress .
| Patients and methods|| |
This study was carried out on 67 patients with first ever stroke who had CKD recruited from among those attending Kafr El Sheikh General Hospital and Menoufia University Hospital as inpatients in medical wards, the Hemodialysis Unit, and the ICU within 24 h of the onset of stroke symptoms. Thirty first ever stroke patients who were free from the signs and symptoms of CKD were included as a control group.
Patients with a previous history of cerebrovascular disease, any other neurological disease (epilepsy, dementia, migraine, cerebral abscess, primary central nervous system tumors), blood diseases and dyscrasias (vitamin K deficiency, leukemia), known cardiac disease (unstable cardiac dysrhythmia, rheumatic heart disease or any other definite embolic source), chronic liver disease, or any debilitating general medical condition other than CKD were excluded.
Ethical approval to carry out the study was granted by the University Ethical Committee of Scientific Research. Written consent forms were obtained from all participants or their relatives.
Patients were subjected to the following: complete assessment of medical history including, with a focus on the history of recognized risk factors for cerebrovascular stroke and CKD. A full general systemic and neurological examination was performed.
Laboratory investigations including complete blood picture, erythrocyte sedimentation rate, coagulation profile, fasting and postprandial blood sugar, total protein and serum albumin, renal function tests (blood urea, creatinine), serum uric acid, and lipid profile (total cholesterol, triglycerides, liver function tests (liver enzyme assays: ALT, AST) were carried out.
Computed tomography scan of the brain was performed for all patients with suspected stroke at onset to be repeated after 72 h if the initial computed tomography was free.
Staging of CKD was determined according to the Kidney Disease Outcomes Quality Initiative (KDOQI) guidelines using the Modification of Diet in Renal Disease Study Group formula to calculate the estimated glomerular filtration rate (eGFR) :
eGFR = 186 serum creatinine -1.154 age -0.203 (1.212 if Black) (0.742 if female)
The severity of CKD was described by the following stages according to the position statement of the KDOQI :
- Normal kidney function: eGFR above 90 ml/min/1.73 m 2 of the body surface area (BSA) and no proteinuria.
- CKD1: eGFR above 90 ml/min/1.73 m 2 of BSA with evidence of kidney damage by imaging studies or through renal biopsy.
- CKD2 (mild): eGFR of 60-89 ml/min/1.73 m 2 of BSA with evidence of kidney damage (small sized kidney, renal masses, and cysts).
- CKD3 (moderate): eGFR of 30-59 ml/min/1.73 m 2 of BSA.
- CKD4 (severe): eGFR of 15-29 ml/min/1.73 m 2 of BSA.
- CKD5 kidney failure: eGFR less than 15 ml/min/1.73 m 2 of BSA referred to ESRD.
All patients in our study group had eGFR less than 90 ml/min/1.73 m 2 . Patients were divided into two groups on the basis of eGFR:
- Group I CKD: included 37 patients with eGFR 15 ml/min/1.73 m 2 or more of BSA with its three subgroups (mild, moderate, and severe).
- Group II CKD: included 30 patients with eGFR less than 15 ml/min/1.73 m 2 of BSA; these were ESRD patients who were on hemodialysis.
Patients were hemodialyzed on three times per week dialysis regimens of about 3-h sessions using machines with controlled ultrafiltration and synthetic membranes. Bicarbonate buffer and high-flux dialyzers were used in all patients.
All patients were subjected to a complete assessment on admission (day 0) and then followed up prospectively at day 7 and day 30 for stroke outcome using the following:
- National Institutes of Health Stroke Scale (NIHSS) to assess motor disability and functional ability . Patients with scores below 7 had good neurological status, those with scores between 8 and 12 had poor neurological status, and those with scores more than 12 had poor neurological status.
- Barthel index scale for activity of daily living to assess stroke functional outcome , with good outcome at 60 or more points and poor outcome at less than 60 points.
All data were tabulated and analyzed using the GraphPad statistical package (GraphPad Prism and GraphPad InStat, version 5; GraphPad). Quantitative data were expressed as mean and SD, and analyzed using the Student t-test for comparison of two independent groups of normally distributed variables; the Mann-Whitney Wilcoxon U-test was used for non-normally distributed variables. The c2 -test was used to compare qualitative variables. Univariate analyses of variance test were carried out for continuous data. The Tukey-Kramer multiple-comparisons post-hoc test was used for further analysis of significant analyses of variance. Correlation coefficients were calculated by simple regression analysis. Multiple regression analysis was carried out to explore the relationship of two variables.
A P-value of less than 0.05 was considered statistically significant difference and P-value less than 0.005 was considered highly statistically significant.
| Results|| |
In the present study, stroke patients with CKD were significantly older (62.8 ± 11 years) than the individuals in the control group (58.3 ± 9.9 years). [Table 1] shows that stroke patients with CKD had a history of hypertension significantly more frequently (80.6%), than the control group. Anemia was significantly higher in CKD (P < 0.005).
|Table 1: Distribution of different risk factors among the groups studied|
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CKD patients had a significantly higher rate of hemorrhagic stroke than the control group (37.3 vs. 16.6%; P < 0.05).
As shown in [Table 2], ischemic stroke patients in group II CKD (hemodialysis population) showed a significant predominance of vertebrobasilar arterial territory infarcts (P < 0.05).
|Table 2: Vascular territory of brain infarction classified by the severity of chronic kidney disease in comparison with the control group|
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Patients with CKD had a significantly higher risk of case fatality rate, reaching 41.7%, compared with the control group (30%). Outcomes after stroke in ESRD patients were poor, with a high case fatality rate, reaching 53.3% of all events; 25% of ischemic strokes were fatal, whereas 71.4% of hemorrhagic strokes were fatal [Table 3].
|Table 3 Case fatality rate in the groups studied in relation to the time of stroke onset|
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In the present study, patients with eGFR less than 15 ml/min/1.73 m 2 had a higher mean NIHSS (16.3 ± 5.9) compared with patients with eGFR 15-90 ml/min/1.73 m 2 and the control group at day 0, day 7, and day 30, indicating a worse neurological state on admission and through follow-up [Table 4]. Patients with eGFR less than 15 ml/min/1.73 m 2 showed significantly poorer outcome compared with other groups on admission as assessed by the Barthel index [Table 5].
|Table 4: National Institutes of Health Stroke Scale in the groups studied|
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Analysis of the correlation between eGFR and stroke outcome showed a significant negative correlation between eGFR and NIHSS at all time points, whereas the Barthel index of the daily activity score was correlated positively with eGFR only on admission [Figure 1].
|Figure 1: Correlation of estimated glomerular filtration rate (eGFR) values with the National Institutes of Health Stroke Scale (NIHSS) scores and the Barthel index score. Each circle represents a patient. A significant negative correlation between eGFR and NIHSS (a) on admission (n = 67, r = −0.3015, P = 0.0132), (b) at day 7 (n = 47, r = −0.5334, P = 0.0001), (c) at day 30 (n = 39, r = −0.5095, P = 0.0009) was found. (d) A significant positive correlation was found between eGFR and the Barthel index on admission (n = 67, r = 0.3432, P = 0.0045).|
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At the end of the study, the control group had a better short-term outcome compared with group II CKD as a significantly higher number of patients had good outcome (P < 0.05).
The results show that there is a significant correlation between severity of stroke in CKD patients and both serum albumin and hemoglobin level, implying that the lower the serum albumin level or hemoglobin level, the worse the outcome.
In group II CKD, most patients with ESRD (56.7%) had dialysis duration of more than 1 year. They had a significantly higher mortality rate (P < 0.05). Dialysis duration also had a significant effect on the functional outcome of our patients; the mean NIHSS for patients with dialysis duration 12 or more months was significantly higher (P < 0.05) than that in patients with dialysis duration less than 12 months.
| Discussion|| |
In the present study, stroke patients with CKD were significantly older than the participants in the control group; this was in agreement with the studies of Yahalom et al. , and Chinda et al. , and may be because of the presence of more risk factors in the older group.
Age is the single most important risk factor for stroke. Age is also considered an independent risk factor for CKD . Because age is one of the factors in the determination of eGFR, it is reasonable that the renal function of the elderly patients was lower.
In this study, CKD patients had a significantly higher rate of hemorrhagic stroke than the control group; this was in agreement with Bos et al. , who found a strong and graded inverse association between GFR and a risk of hemorrhagic stroke. Again, Shimizu et al.  found that CKD was associated with an increased risk of hemorrhagic stroke for men, whereas Holzmann et al.  concluded that mildly decreased GFR increases the risk of ischemic fatal or nonfatal stroke and severely decreased GFR increases the risk of hemorrhagic stroke in the general population.
The increased incidence of cerebral hemorrhage in CKD and dialysis patients was ascribed to the high prevalence of hypertension, protein malnutrition, and hypoalbuminemia, which directly affected erythrocyte deformability and endothelial dysfunction. Decreased GFR indicates small-vessel disease not only in the kidney but also in the brain, which is the main pathophysiological mechanism in hemorrhage .
Also, platelet dysfunction is an important sequel of CKD. This becomes apparent by prolonged bleeding time, mucocutaneous ecchymoses, and mucosal oozing in patients with severe CKD, explaining the increased risk of hemorrhagic stroke in patients with decreased GFR .
However, other studies have reported that brain infarcts are more common than brain hemorrhage in CKD patients in the USA  and India . The increased prevalence of large-artery disease, decrease in intravascular blood volume secondary to hemodialysis, use of erythropoietin, which increases blood viscosity, autonomic neuropathy, and hyperhomocysteinemia were reported to be important factors for the higher incidence of brain infarcts in CKD. The inclusion of older patients with multiple risk factors and advanced diagnostic facilities in the form of MRI are some of the reasons reported for the increased recognition of brain infarcts in these studies [17,18].
In this study, stroke patients in group II CKD (hemodialysis population) showed a significant predominance of vertebrobasilar arterial territory infarcts. The same observation was made by Toyoda et al. . Dizziness and light-headedness are symptoms of vertebrobasilar insufficiency; these symptoms are also common in patients during and after hemodialysis. Thus, these symptoms must be monitored to exclude stroke .
In contrast, Krishnan et al.  found no significant vascular territory distribution in CKD patients with stroke, whereas Jung et al.  reported more common stroke events in the territories supplied by the anterior circulation in ESRD patients.
In terms of traditional risk factors, irrespective of age, CKD patients had a history of hypertension significantly more frequently (80.6%). CKD patients in group II (ESRD) showed a significantly higher systolic blood pressure at the time of admission.
This was in agreement with Hoshino et al. , who reported a 75.6% prevalence of hypertension in CKD patients with stroke. Kokubo et al.  found a stronger association between blood pressure and stroke in the presence of CKD.
Hypertension, notably elevated systolic blood pressure, is a risk factor for stroke in the general population. In addition, hypertension is a major component of CKD, both as a cause and as a result of impaired kidney function . Hypertension promotes the formation of atherosclerotic plaques in cerebral arteries and arterioles, which may lead to arterial occlusions and ischemic injury. Hypertension alters endothelium-dependent relaxation of cerebral blood vessels. In addition, hypertension induces fibrinoid necrosis of penetrating arteries and arterioles supplying the white matter, resulting in small white matter infarcts (lacunes) or brain hemorrhage .
This study also showed that, as a nontraditional risk factor, anemia was most prevalent in the CKD group (83.5%) and the control group, but was significantly higher in CKD patients. Del Fabbro et al.  reported 45-55% anemia in CKD patients with stroke. Krishnan et al.  reported anemia in 81.48% of CKD patients with stroke. Anemia was second only to hypertension as a prevalent risk factor .
Abramson et al.  concluded that when anemia was present, the risk and severity of stroke increased. The reasons are not entirely clear; reduced renal function and impaired erythropoietin could limit erythropoietin-induced neuronal protection. Anemia also facilitates cerebral ischemia; it may be that CKD and anemia each have independent pathways through which they lead to stroke or anemia may simply be a marker of the duration and/or the severity of CKD .
This study showed that patients with CKD had a significantly higher case fatality rate, reaching 41.7%, compared with the control group (30%). The findings are consistent with those of Tsagalis et al. , who found that even a moderate reduction in renal function appeared to be an independent and clinically relevant risk factor for the overall mortality. The role of renal dysfunction was apparent early (1 month) after the acute event . Brzosko et al.  showed that a low GFR was associated with a higher in-hospital mortality rate.
In this study, the highest case fatality rate was recorded in group II CKD patients (hemodialysis population). Hemodialysis treatment is an independent indicator for poor functional outcome and mortality after stroke [4,19]. This may likely reflect the comorbid conditions that our patients on dialysis developed before they experienced a stroke. Discontinuation of dialysis may be another factor, a point that needs to be further investigated.
In the present study, patients in group II CKD had a higher mean NIHSS compared with group I and the control group at day 0, day 7 and day 30, indicating worse neurological state on admission and through follow-up.
Further analysis on the correlation between eGFR and the neurological state and stroke outcome showed a significant negative correlation between eGFR and NIHSS at all the time points. Patients with renal dysfunction have many risk factors that accelerate atherothrombotic and comorbid underlying diseases. These concomitant diseases may explain the higher neurologic severity of stroke observed in patients with renal dysfunction.
The Barthel index of daily activity score was correlated positively with eGFR on admission and the good functional outcome group had a higher eGFR. This indicates that a worse neurological impairment is related to the degree of decrease in eGFR. This was in agreement with Tsagalis et al. , who observed that patients with eGFR less than 30 ml/min/1.73 m 2 presented with the most severe stroke. Hao et al.  reported a higher proportion of poor outcomes (27.2%) in patients with lower eGFR.
Thus, measurement of eGFR could potentially serve as an easy, quick, and feasible prognostic parameter for clinicians if considered as a recommendation for the management of stroke patients; thus, recently, it was added to the recommendations for the management of hypertension .
Unlike most organs, both the kidney and the brain are low-resistance end-organs. In the systemic circulation, the brain and kidney are unique in that their cells are passively perfused throughout systole and diastole by pulsatile flow. The two organs, the brain and the kidney, throb with each beat of the heart. High-pressure fluctuations that exist in the carotid, vertebral, and renal arteries expose the small vessels of these two organs to pressure and flow fluctuations, which explains the microvascular damage and the resulting renal failure and neurological and cognitive alterations .
Thus, information on microvascular damage in one organ may provide information on damage in the other organ. For the kidney, the damage markers proposed by KDOQI are albuminuria/proteinuria and, for decrease in function, eGFR. For the brain, damage markers could be MRI-described small-vessel alterations in the form of the presence of lacunar cerebral infarction, white matter lesions, or hyperintensities .
Serum albumin is the principal nutritional marker used to identify malnutrition and chronic inflammation in patients with CKD. In the present study, the severity of stroke in CKD patients was highly affected in a negative correlation with serum albumin level. This is in agreement with Kisialiou . Albumin has several biochemical properties including regulation of colloid osmotic pressure of plasma and regulation of microvascular permeability, antioxidant activity, antithrombotic activity, and anti-inflammatory activity, in addition to its ability to regulate hemodynamic properties of the brain circulation as well as the direct neuroprotective actions on neuronal and glial cells .
In this study, low serum albumin was associated significantly with a high fatality rate. Low serum albumin at admission correlated with higher rates of death and disability in ischemic stroke patients in general as well as in stroke patients with CKD .
Experimental studies showed that high-dose or moderate-dose human albumin therapy, after stroke onset, is highly effective in improving neurological status and in reducing infarction volume and extent of brain swelling. The Albumin in Acute Stroke Study (ALIAS), in its phase III, suggested a trend toward favorable outcomes in patients in the albumin arm and further results from the study are awaited . CKD with stroke may be a good target for albumin therapy as hypoalbuminemia is more prevalent in this group.
In group II CKD, most patients with ESRD (56.7%) had a dialysis duration of more than one year. Several studies have observed an early risk of stroke associated with the start of dialysis, with 24.4% of strokes occurring within 1 year and 57.7% occurring within 5 years after the initiation of dialysis, whereas others found that the majority of incident cerebrovascular events occurred after being on dialysis for over 2 years . Whether this is directly related to the dialysis procedure or simply reflects pre-existing comorbid conditions such as longstanding hypertension, atherosclerosis, and malnutrition is not clear. The increased incidence of cerebral hemorrhage in CKD and dialysis patients was ascribed to the high prevalence of hypertension, protein malnutrition, and hypoalbuminemia, which directly affected erythrocyte deformability and endothelial dysfunction.
Furthermore, patients with longer dialysis duration had more hemorrhagic insults (52.9%); even the relation was not statistically significant. This was in agreement with Sozio et al. , who reported that ischemic stroke is more frequent in the early months of dialysis treatment. On the one hand, the reduction in blood pressure values during dialysis could reduce cerebral perfusion, leading to ischemic stroke. On the other, bleeding diathesis and routine heparin administration during hemodialysis could increase the risk of hemorrhagic stroke whereas long-term dialysis treatment could be related to risk factors acquired for hemorrhagic stroke .
This study showed a significant influence of the duration of hemodialysis on stroke. Patients with dialysis duration 12 or more months had a significantly higher mortality rate and significantly poor outcome. Our results are in agreement with those of Chertow , who showed that the risk of mortality increased by 6% with each year on dialysis therapy, and with those of Iseki et al. , who concluded that prolonged dialysis is a significant predictor of death and poor outcome in chronic hemodialysis patients.
We reported 60% vascular access complications; patients with vascular access infection had a further more mean NIHSS score for patients with history of vascular access infection was higher than other patients, indicating a worse neurological state. Even the mortality rate was higher in patients with a history of vascular access infection (50%) than others (35%).
Ishani et al.  suggested that septicemia plays a role in the excessive burden of cardiovascular disease in dialysis patients. They found that bacteremic episodes were also associated with poor outcomes. They also reported that acute infection was associated with an increased short-term risk of myocardial infarctions and stroke. It has been suggested that the full-blown sepsis syndrome has significant effects on endothelial function as well as the coagulation system and overall cardiac function .
In conclusion, in CKD patients with stroke, hypertension and anemia were the most prevalent traditional and nontraditional risk factor, respectively. These patients had a significantly higher rate of hemorrhagic stroke and higher case fatality rates.
Reduced eGFR on admission is related to poor stroke outcome. Also, reduced serum albumin and hemoglobin levels are related to poor outcome and prolonged dialysis duration is an indicator for poor functional outcome and mortality after stroke.
In patients with CKD, strict control of blood pressure, hemoglobin, and albumin level is recommended to decrease the risk of stroke. eGFR may be used as a predictor of short-term stroke outcome.
| Acknowledgements|| |
Conflicts of interest
There are no conflicts of interest.
| References|| |
National Kidney Foundation Kidney Disease Outcome Quality Initiative - K/DOQI. Clinical practice guidelines evaluation, classification, and stratification. Am J Kidney Dis 2010; 37
Collins A, Xue JL, Ma JZ, Louis T. Estimating the number of patients and Medicare cost for end stage renal disease in the US to the year 2010. J Am Soc Nephrol 2000; 11
Kennedy R, Case C, Fathi R, Johnson D, Isbel N, Marwick TH. Does renal failure cause an atherosclerotic milieu in patients with end-stage renal disease? Am J Med 2001; 110
Seliger SL, Gillen DL, Longstreth WT Jr, Kestenbaum B, Stehman-Breen CO. Elevated risk of stroke among patients with end-stage renal disease. Kidney Int 2003; 64
Dean CM, Rissel C, Sharkey M, Sherrington C, Cumming RG, Barker RN, et al.
Exercise intervention to prevent falls and enhance mobility in community dwellers after stroke: a protocol for a randomised controlled trial. BMC Neurol 2009; 9
Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, et al.
American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics - 2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2006; 113
Ozbek E. Induction of oxidative stress in kidney. Int J Nephrol 2012; 2012:465897
Eckardt KU, Berns JS, Rocco MV, Kasiske BL Definition and classification of CKD: the debate should be about patient prognosis: a position statement from KDOQI and KDIGO. Am J Kidney Dis 2009; 53
Adams HP Jr, Davis PH, Leira EC, Chang KC, Bendixen BH, Clarke WR, et al.
Baseline NIH Stroke Scale score strongly predicts outcome after stroke: a report of the Trial of Org 10172 in Acute Stroke Treatment (TOAST). Neurology 1999; 53
O′Sullivan, Susan B, Schmitz, Thomas J. Physical rehabilitation. 5th ed. Philadelphia, PA: F.A. Davis Company 2007; 385.
Yahalom G, Schwartz R, Schwammenthal Y, Merzeliak O, Toashi M, Orion D, et al.
Chronic kidney disease and clinical outcome in patients with acute stroke. Stroke 2009; 40
Chinda J, Nakagawa N, Kabara M, Matsuki M, Endo H, Saito T, et al.
Impact of decreased estimated glomerular filtration rate on Japanese acute stroke and its subtype. Intern Med 2012; 51
Bos MJ, Koudstaal PJ, Hofman A, Breteler MM. Decreased glomerular filtration rate is a risk factor for hemorrhagic but not for ischemic stroke: the Rotterdam Study. Stroke 2007; 38
Shimizu Y, Maeda K, Imano H, Ohira T, Kitamura A, Kiyama M, et al.
Chronic kidney disease and drinking status in relation to risks of stroke and its subtypes: the Circulatory Risk in Communities Study (CIRCS). Stroke 2011; 42
Holzmann MJ, Aastveit A, Hammar N, Jungner I, Walldius G, Holme I Renal dysfunction increases the risk of ischemic and hemorrhagic stroke in the general population. Ann Med 2012; 44
O′Rourke MF, Safar ME. Relationship between aortic stiffening and microvascular disease in brain and kidney: cause and logic of therapy. Hypertension 2005; 46
U S Renal Data System. USRDS 2010 Annual Data Report: atlas of chronic kidney disease and end-stage renal disease in the United States, National Institutes of Health. Bethesda, MD, USA: National Institute of Diabetes and Digestive and Kidney Diseases; 2010.
Krishnan, AV, Pussell, BA, Kiernan, MC. Neuromuscular disease in the dialysis patient: an update for the nephrologist. Semin Dial 2009; 22
Toyoda K, Fujii K, Fujimi S, Kumai Y, Tsuchimochi H, Ibayashi S, Iida M. Stroke in patients on maintenance hemodialysis: a 22-year single-center study. Am J Kidney Dis 2005; 45
Jung S, Kwon SB, Hwang SH, Noh JW, Lee YK. Ischemic stroke among the patients with end-stage renal disease who were undergoing maintenance dialysis. Yonsei Med J 2012; 53
Hoshino H, Itoh Y, Yamada S, Miyaki K, Suzuki N. Clinical features and neurologic severity in stroke patients with mild to moderate renal dysfunction. J Stroke Cerebrovasc Dis 2012; 21
Kokubo Y, Iso H, Saito I, Yamagishi K, Yatsuya H, Ishihara J et al.
The impact of green tea and coffee consumption on the reduced risk of stroke incidence in Japanese population: the Japan public health center-based study cohort. Stroke 2013; 44
Weiner DE, Tighiouart H, Amin MG, Stark PC, MacLeod B, Griffith JL, et al.
Chronic kidney disease as a risk factor for cardiovascular disease and all-cause mortality: a pooled analysis of community-based studies. J Am Soc Nephrol 2004; 15
Iadecola C, Davisson RL. Hypertension and cerebrovascular dysfunction. Cell Metab 2008; 7
Del Fabbro P, Luthi JC, Carrera E, Michel P, Burnier M, Burnand B. Anemia and chronic kidney disease are potential risk factors for mortality in stroke patients: a historic cohort study. BMC Nephrol 2010; 11
Abramson JL, Jurkovitz CT, Vaccarino V, Weintraub WS, McClellan W. Chronic kidney disease, anemia, and incident stroke in a middle-aged, community-based population: the ARIC Study. Kidney Int 2003; 64
Tsagalis G, Akrivos T, Alevizaki M, Manios E, Stamatellopoulos K, Laggouranis A, Vemmos KN Renal dysfunction in acute stroke: an independent predictor of long-term all combined vascular events and overall mortality. Nephrol Dial Transplant 2009; 24
Brzosko S, Szkolka T, Mysliwiec M. Kidney disease is a negative predictor of 30-day survival after acute ischaemic stroke. Nephron Clin Pract 2009; 112
Hao Z, Wu B, Lin S, Kong FY, Tao WD, Wang DR, Liu M Association between renal function and clinical outcome in patients with acute stroke. Eur Neurol 2010; 63
Mancia G, De Backer G, Dominiczak A, Cifkova R, Fagard R, Germano G, et al.
ESH-ESC Task Force on the Management of Arterial Hypertension 2007 ESH-ESC Practice Guidelines for the Management of Arterial Hypertension: ESH-ESC Task Force on the Management of Arterial Hypertension. J Hypertens 2007; 25
Thompson CS, Hakim AM. Living beyond our physiological means: small vessel disease of the brain is an expression of a systemic failure in arteriolar function: a unifying hypothesis. Stroke 2009; 40
Kisialiou A, Pelone G, Carrizzo A, Grillea G, Trimarco V, Marino M, et al.
Blood biomarkers role in acute ischemic stroke patients: higher is worse or better?. Immun Ageing 2012; 9
Prajapati KD, Sharma SS, Roy N. Current perspectives on potential role of albumin in neuroprotection. Rev Neurosci 2011; 22
Dziedzic T, Slowik A, Szczudlik A. Serum albumin level as a predictor of ischemic stroke outcome. Stroke 2004; 35
Hill MD, Martin RH, Palesch YY, Tamariz D, Waldman BD, Ryckborst KJ, et al.
ALIAS Investigators; Neurological Emergencies Treatment Trials Network The Albumin in Acute Stroke Part 1 Trial: an exploratory efficacy analysis. Stroke 2011; 42
Sozio SM, Armstrong PA, Coresh J, Jaar BG, Fink NE, Plantinga LC, et al.
Cerebrovascular disease incidence, characteristics, and outcomes in patients initiating dialysis: the choices for healthy outcomes in caring for ESRD (CHOICE) study. Am J Kidney Dis 2009; 54
Iseki K, Yamazato M, Tozawa M, Takishita S. Hypocholesterolemia is a significant predictor of death in a cohort of chronic hemodialysis patients. Kidney Int 2002; 61
Ishani A, Collins AJ, Herzog CA, Foley RN. Septicemia, access and cardiovascular disease in dialysis patients: the USRDS Wave 2 study. Kidney Int 2005; 68
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]