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Changes in the Risk of Stroke in Dialysis Patients: a Retrospective Analysis Over the Last 40 Years

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Changes in the Risk of Stroke in Dialysis Patients: a Retrospective Analysis Over the Last 40 Years toxins Article Changes in the Risk of Stroke in Dialysis Patients: A Retrospective Analysis over the Last 40 Years Toshiya Aono 1,†, Yuki Shinya 1,2,*,† , Satoru Miyawaki 2 , Takehiro Sugiyama 3,4, Isao Kumagai 5, Atsumi Takenobu 1, Masahiro Shin 2 , Nobuhito Saito 2 and Akira Teraoka 1 1 Department of Neurosurgery, Teraoka Memorial Hospital, Hiroshima 729-3103, Japan; [email protected] (T.A.); [email protected] (A.T.); [email protected] (A.T.) 2 Department of Neurosurgery, The University of Tokyo Hospital, Tokyo 113-8655, Japan; [email protected] (S.M.); [email protected] (M.S.); [email protected] (N.S.) 3 Diabetes and Metabolism Information Center, Research Institute, National Center for Global Health and Medicine, Tokyo 162-8655, Japan; [email protected] 4 Department of Health Services Research, Faculty of Medicine, University of Tsukuba, Ibaraki 305-8575, Japan 5 Department of Nephrology, Teraoka Memorial Hospital, Hiroshima 729-3103, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-3-5800-8853 † These two authors have contributed equally to this study and are thus co-first authors. Abstract: The stroke incidence in hemodialysis (HD) patients is high, but the associated factors remain largely unknown. This study aimed to analyze stroke incidence in HD patients and changes in risk factors. Data of 291 patients were retrospectively analyzed. The cumulative stroke incidences were 21.6% at 10 years and 31.5% at 20. Diabetic nephropathy (DN) significantly increased overall stroke (hazard ratio (HR), 2.24; 95% confidence interval (CI), 1.21–4.12; p = 0.001) and ischemic p stroke (HR, 2.16; 95% CI, 1.00–4.64; = 0.049). Patients treated with online HDF were less likely to have overall stroke (HR, 0.13; 95% CI, 0.03–0.56; p = 0.006) and ischemic stroke (HR, 0.08; 95% CI, 0.01–0.60; p = 0.014). DN (HR, 1.56; 95% CI, 1.08–2.27; p = 0.019) and age >80 years at HD initiation Citation: Aono, T.; Shinya, Y.; Miyawaki, S.; Sugiyama, T.; Kumagai, (20–49 years old; HR 0.13, 95% CI, 0.05-0.35, p < 0.001 and age 50–79 years; HR 0.42, 95% CI, 0.26–0.66, I.; Takenobu, A.; Shin, M.; Saito, N.; p < 0.001 (reference: age >80 years)) were significantly associated with stroke and/or death events. Teraoka, A. Changes in the Risk of Over time, stroke risk increased in HD patients, due to the increasing number of DN. Although Stroke in Dialysis Patients: A dialysis technology has advanced over time, these advances could not overcome other risk factors Retrospective Analysis over the Last for stroke. Further increase in stroke and mortality due to aging remains a concern. 40 Years. Toxins 2021, 13, 350. https://doi.org/10.3390/toxins Keywords: dialysis; stroke; diabetes mellitus; diabetic nephropathy; uremic toxin 13050350 Key Contribution: The incidence of stroke in hemodialysis patients is exceedingly high. Although Received: 21 April 2021 dialysis technology has definitely advanced over time, these technological advances could not Accepted: 11 May 2021 overcome other risk factors for stroke, including DM, DN, and the aging population. Published: 13 May 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- iations. The increasing number of patients with end-stage renal disease (ESRD) on dialysis and the high incidence of stroke remains a major concern. Compared to the general population, patients with ESRD on dialysis have a 4 to 20 times increased risk of stroke [1–7]. Reducing stroke incidence is important for prognosis in patients with ESRD on dialysis, considering the high mortality and recurrence rates [8,9]. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. To date, several risk factors for stroke in patients with ESRD on dialysis have been This article is an open access article reported, and include diabetes mellitus (DM), hypertension, atrial fibrillation (Af), old distributed under the terms and age, anemia, malnutrition, asymmetric dimethylarginine, and elevated C-reactive protein conditions of the Creative Commons (CRP) [4,6,10–14]. Additionally, we have previously reported that diabetic nephropathy Attribution (CC BY) license (https:// (DN) is a significant risk factor for stroke [9]. creativecommons.org/licenses/by/ Recent improvements in treatment of DM and dialysis technology have resulted in 4.0/). better long-term prognosis in patients with DM or DN. However, the impact of these Toxins 2021, 13, 350. https://doi.org/10.3390/toxins13050350 https://www.mdpi.com/journal/toxins Toxins 2021, 13, 350 2 of 14 advances on patients with ESRD on dialysis has not been fully elucidated; the effect on the reduction of stroke incidence should be evaluated. We performed a single-institution-based retrospective study to analyze changes in the incidence and risk factors of stroke in patients with ESRD on dialysis over time. 2. Results 2.1. Baseline Characteristics The baseline characteristics of patients on hemodialysis (HD) in each period are shown in Table1. The timing of HD introduction was divided into three periods, considering the advances in dialysis techniques in each era: 1979–2009 (early period), 2010–2014 (middle period), and 2015–2020 (late period), and analysis was conducted for each period. A total of 119 HD patients in the early period, 71 in the middle period, and 101 in the late period were included. Patients who had HD initiated in the early period were significantly younger, had a longer observation period, and were more likely to receive anticoagulant therapy, while those in the middle period had a significantly higher incidence of DM and DN. Those in the middle period also had a significantly lower level of CRP and urea reduction ratio (URR). Patients in the late period were more likely to have dyslipidemia (DL) and smoking history, but less likely to have ischemic heart disease and arteriosclerosis obliterans. The differences in the baseline characteristics of patients on HD between with and without online hemodialysis filtration (HDF) are shown in Table S1. Table 1. Clinical characteristics of patients in each period of dialysis initiation. All 1979–2009 2010–2014 2015–2020 p Value Number of patients, n 291 119 71 101 / Age at initiation of dialysis Mean ± SD 65.6 ± 14.4 59.1 ± 13.9 70.4 ± 11.4 69.8 ± 14.2 <0.001 * Range (years) 21–95 21–90 43–93 33–95 Follow-up period (years) Mean ± SD 8.1 ± 7.8 14.3 ± 8.5 6.3 ± 2.5 2.1 ± 1.5 <0.001 * Range (years) 0.1–38.3 0.3–38.3 0.2–10.3 0.1–5.1 Male, n (%) 187 (64.3%) 68 (57.1%) 46 (64.8%) 73 (72.3%) 0.065 Underlying diseases, n (%) Hypertension 283 (97.3%) 118 (99.2%) 69 (97.2%) 96 (95.0%) 0.178 Diabetes 177 (60.8%) 65 (54.6%) 52 (73.2%) 60 (59.4%) 0.037 * Dyslipidemia 114 (39.2%) 34 (28.6%) 28 (39.4%) 52 (51.5%) 0.002 * Ischemic heart diseases 132 (45.4%) 63 (52.9%) 38 (53.5%) 31 (30.7%) 0.001 * Arteriosclerosis obliterans 92 (31.6%) 42 (35.3%) 28 (39.4%) 22 (21.8%) 0.026 * Atrial fibrillation 31 (10.7%) 47 (14.3%) 6 (8.5%) 8 (7.9%) 0.252 Smoking, n (%) 110 (37.8%) 32 (26.9%) 26 (36.6%) 52 (51.5%) 0.001 * Alcohol, n (%) 51 (17.5%) 16 (13.5%) 12 (16.9%) 23 (22.8%) 0.191 Online HDF, n (%) 69 (23.1%) 29 (24.4%) 18 (25.4%) 22 (21.8%) 0.842 Antiplatelet therapy, n (%) 148 (50.9%) 62 (52.1%) 40 (56.3%) 46 (45.5%) 0.356 Anticoagulant therapy, n (%) 35 (12.0%) 21 (17.7%) 7 (9.9%) 7 (6.9%) 0.042 * Primary renal diagnosis of the patients, n (%) Diabetic nephropathy 116 (39.9%) 40 (33.6%) 33 (46.5%) 43 (42.6%) Nephrosclerosis 75 (25.8%) 22 (18.5%) 26 (36.6%) 27 (26.7%) Glomerulonephritis 44 (15.1%) 29 (24.4%) 6 (8.5%) 9 (8.9%) 0.001 * Polycystic kidney disease 11 (3.8%) 5 (4.2%) 2 (2.8%) 4 (4.0%) Others 45 (15.5%) 23 (19.3%) 4 (5.6%) 18 (17.8%) Laboratory parameters CRP (mg/dL) Mean ± SD 0.97 ± 3.27 0.92 ± 2.93 0.59 ± 1.42 1.29 ± 4.38 0.001 * Range (mg/dL) 0.00–30.98 0.00–26.1 0.00–10.1 0.00–30.98 PTH (pg/mL) Mean ± SD 183 ± 177 191 ± 179 187 ± 227 172 ± 126 0.965 Toxins 2021, 13, 350 3 of 14 Table 1. Cont. All 1979–2009 2010–2014 2015–2020 p Value Range (pg/mL) 5–1842 6–1260 5–1842 7–724 Kt/V Mean ± SD 1.27 ± 0.33 1.30 ± 0.33 1.20 ± 0.31 1.29 ± 0.33 0.061 Range 0.48–2.21 0.48–2.21 0.59–1.82 0.51–2.16 URR (%) Mean ± SD 62.9 ± 10.6 63.5 ± 11.3 59.6 ± 11.1 64.4 ± 8.8 0.011 * Range (%) 26.7–93.9 26.7–93.9 32.6–77.8 36.1–82.5 n, number; SD, standard deviation; HDF, hemodialysis filtration; CRP, C-reactive protein; PTH, parathyroid hormone; Kt/V, K dialyzer clearance of urea, t dialysis time, V volume of distribution of urea; URR, urea reduction ratio. * Values of p < 0.05 are considered statistically significant.
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