Permanent cardiac pacing in patients with end-stage renal disease undergoing dialysis

Nephrology Dialysis Transplantation, Dec 2016

Studies investigating the risk of cardiac dysrhythmia warranting permanent pacemaker therapy for end-stage renal disease (ESRD) patients are limited. This study investigated the incidence rate of permanent cardiac pacing in dialysis patients.

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Permanent cardiac pacing in patients with end-stage renal disease undergoing dialysis

Nephrol Dial Transplant Permanent cardiac pacing in patients with end-stage renal disease undergoing dialysis I-Kuan Wang 0 1 2 3 4 5 12 Kuo-Hung Lin 0 2 4 9 12 Shih-Yi Lin 0 1 2 3 4 5 12 Cheng-Li Lin 0 2 4 7 8 12 Chiz-Tzung Chang 0 1 2 4 12 Tzung-Hai Yen 0 2 4 6 11 12 Fung-Chang Sung 0 2 4 5 8 10 12 0 Hospital , Taipei , Taiwan 1 Division of Nephrology, China Medical University Hospital , Taichung , Taiwan 2 Hospital , Taichung , Taiwan 3 Department of Internal Medicine, College of 4 Medicine, China Medical University , Taichung , Taiwan 5 Graduate Institute of Clinical Medical Science, China Medical University , Taichung , Taiwan 6 Division of Nephrology , Chang Gung Memorial 7 College of Medicine, China Medical University , Taichung , Taiwan 8 Management Office for Health Data, China Medical University 9 Division of Cardiology, China Medical University Hospital , Taichung , Taiwan 10 Department of Health Services Administration 11 Chang Gung University College of Medicine , Taoyuan , Taiwan 12 China Medical University , Taichung , Taiwan Correspondence and offprint requests to: Fung-Chang Sung; E-mail: dysrhythmia; end-stage renal disease; hemodialysis; pacemaker; peritoneal dialysis - A B S T R A C T Background. Studies investigating the risk of cardiac dysrhythmia warranting permanent pacemaker therapy for end-stage renal disease (ESRD) patients are limited. This study investigated the incidence rate of permanent cardiac pacing in dialysis patients. Methods. Using the Taiwan National Health Insurance Database, we identified 28 471 newly diagnosed ESRD patients in 2000–2010 [9700 on peritoneal dialysis (PD) and 18 771 on hemodialysis (HD)] and 113 769 randomly selected controls without kidney disease, frequency-matched by sex, age and diagnosis date. We also established propensity score-matched HD and PD cohorts with 9700 patients each. Incidence rates and hazard ratios (HRs) of implantation were evaluated by the end of 2011. Complications were also evaluated among patients with implantation. Results. The incidence rates of permanent pacemaker implantation were 5.93- and 3.50-fold greater in HD and PD patients than in controls (1.44 and 0.85 versus 0.24 per 1000 personyears, respectively). The adjusted HRs (aHRs) of implantation were 3.26 [95% confidence interval (CI) = 2.41–4.42] and 2.36 (95% CI = 1.56–3.58) for HD and PD patients, respectively, compared with controls. The pacemaker implantation rate was 0.33 per 1000 person-years greater in the propensity score-matched HD cohort than in the PD cohort, with an aHR of 1.30 (95% CI = 0.82– 2.05) for the HD cohort compared with the PD cohort. Conclusions. Dialysis patients are at an increased risk of dysrhythmia requiring pacemaker implantation compared with the general population. The risks are not significantly different between HD and PD patients. I N T R O D U C T I O N Cardiovascular disease (CVD) is the leading cause of morbidity and mortality in patients with end-stage renal disease (ESRD), accounting for over 40% of all deaths [ 1, 2 ]. Approximately 60% of cardiac deaths or 26% of all deaths in ESRD patients are presumed to be arrhythmic in etiology [3]. The high arrhythmia burden in ESRD patients deserves a comprehensive investigation. Pathological bradyarrhythmias resulting from sinus node dysfunction or atrioventricular conduction dysfunction may account for 15–20% of sudden cardiac deaths [4]. Sinus node dysfunction, known as sick sinus syndrome, is often secondary to senescence of the node with reduced node cells and increased connective tissue and fat in the nodal area [4]. Sick sinus syndrome can be accompanied by supraventricular tachycardia or tachycardia–bradycardia syndrome and is the major cause for permanent pacemaker implantation [4, 5]. Fibrosis and sclerosis of the conduction systems are the major causes of atrioventricular block [ 6 ]. Patients with sick sinus syndrome are also prone to develop atrioventricular block [ 7 ]. The indications for pacemaker implantation in ESRD patients are the same as for the general population [ 8 ]. A recent study used implantable cardiac monitors to demonstrate that a high prevalence of sudden cardiac death in hemodialysis (HD) patients is associated with bradyarrhythmia [ 9 ]. Permanent pacemaker implantation might be important for preventing sudden cardiac death in ESRD patients. Studies investigating the risk of cardiac dysrhythmia warranting permanent pacemaker therapy for ESRD patients are limited [10, 11]. The present study attempted to investigate the incidence rate of permanent cardiac pacing for ESRD patients undergoing dialysis, using claims data of the National Health Insurance Research Database (NHIRD) of Taiwan. We compared the permanent pacemaker implantation rates between ESRD patients and the general population, and between propensity score-matched cohorts of HD patients and of peritoneal dialysis (PD) patients. M AT E R I A L S A N D M E T H O D S Data source The NHIRD is an electronic database consisting of longitudinal medical records for over 99% of the population in Taiwan [12]. Diseases were coded using the International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM). Medical records were linked using ‘unique encrypted identification numbers’ and could be analyzed anonymously ‘to protect individuals’ privacy’. We performed this study in compliance with guidelines of the Declaration of Helsinki. The Research Ethics Committee at China Medical University and Hospital approved this study (CMU-REC-101-012). The need for informed consent from study subjects was waived. Study subjects We identified patients with ESRD aged 20 years and older newly diagnosed from 2000 to 2010 and who had received dialysis treatment for 90 days or longer. The first day to initiate dialysis was defined as the index date. Patients with a history of permanent pacemaker implantation (ICD-9 procedure codes 377 and 378) (N = 606) or renal transplantation (ICD-9 codes V42.0, 996.81) (N = 298) were excluded. Because ∼10% of ESRD patients received PD in Taiwan, we randomly selected the HD cohort with a sample size 2-fold larger than the PD cohort, frequencymatched by age, sex and the index year. These two cohorts were also considered as the ESRD cohort. For each dialysis patient identified, four controls free of kidney disease (ICD-9 codes 580– 589), permanent pacemaker implantation and renal transplantation were randomly selected from the same data, frequencymatched by age (every 5 years), sex and the index year. Based on the PD cohort, we further identified a propensity score-matched HD cohort with a similar sample size. Baseline variables used to calculate the propensity score included age, sex, the year to initiate dialysis, medication use (aspirin and clopidogrel) and comorbidities including coronary artery disease (CAD) (ICD-9-CM codes 410–413, 414.01–414.05, 414.8 and 414.9), diabetes (ICD-9-CM code 250), stroke (ICD-9-CM codes 430–438), Downloaded from21h1tt6ps://academic.oup.com/ndt/article-abstract/31/12/2115/2661706 by guest on 21 April 2018 hyperlipidemia (ICD-9-CM code 272), atrial fibrillation (AF) (ICD-9-CM code 427.31), hypertension (ICD-9-CM codes 401– 405) and congestive heart failure (CHF) (ICD-9-CM codes 428, 398.91 and 402.x1). Outcome measurement The primary outcome assessed was the incident permanent pacemaker implantation (ICD-9 procedure codes 3771, 3773, 3781, 3782, 3772, 3783, 3770 and 3780) for patients with arrhythmia diagnosed, including conduction disorders (ICD-9-CM code 426) and cardiac dysrhythmia (ICD-9-CM code 427). All individuals were followed up to the date of receiving permanent pacemaker implantation, or to the date of being censored due to death, renal transplantation or withdrawal from the insurance program, or 31 December 2011. We also evaluated the risk of major complications that required the revision or removal of permanent pacemaker (ICD-9 procedure codes 377.5, 377.6, 377.9 and 378.9) among patients with the implantation. Statistical analysis The baseline distributions of demographic characteristics, comorbidities and medications, among ESRD, HD, PD and control cohorts, and between propensity score-matched HD and PD cohorts, were examined using a χ2 test for categorical variables and t-test for continuous variables. Incidence densities of permanent pacemaker implantation were calculated for each cohort ( per 1000 person-years) during the follow-up period, including overall incidence, and incidence identified within 1 year, in 1–3 years and after 3 years. The univariate and multivariate Cox proportion hazards regression models were used to calculate crude hazard ratios (cHRs) and adjusted hazard ratios (aHRs), and 95% confidence intervals (CIs) of permanent pacemaker implantation associated with ESRD and dialysis modality. Variables with a P-value <0.05 in the univariate Cox proportional hazards model were included for further analysis in the multivariate Cox model. Variable-specific stratified analyses were also performed by sex-, age- and index year-matched cohorts. The Kaplan–Meier method was used to plot cumulative proportions of the subjects with permanent pacemaker implantation for ESRD and control cohorts, and the log-rank test was used to assess the difference between the cumulative curves. We also measured the major incident complications leading to the removal or revision of a permanent pacemaker for both sex- and age-matched cohorts and propensity score-matched cohorts. aHRs were also calculated by considering the competing risk of death in the multivariate analysis. All statistical analyses were performed using the SAS statistical software (version 9.3 for Windows; SAS Institute, Inc., Cary, NC, USA), with a P-value of <0.05 considered to be statistically significant. R E S U LT S .0 .1 0 0 < 0 0 .1 .9 0 0 e v i t 1 1 1 1 1 1 1 se 0 0 0 0 2 0 0 0 0 g .0 .0 .0 .0 .9 .6 .0 .0 .0 n 0 0 0 0 0 0 0 0 0 co < < < < < < < , F H C ; n o i t a lli r 1 1 1 1 1 1 1 1 1 b 0 0 0 0 0 0 0 0 0 fi .0 .0 .0 .0 .0 .0 .0 .0 .0 la 0 0 0 0 0 0 0 0 0 ir < < < < < < < < < t a , F n a h t i w s t r o h o c y d u t s e h t n i s u t a t s d i b r o b a T m o c l a c i n d i e l c h c t d a .7 .5 .5 .4 .7 .2 .8 .39 .70 .32 .29 .67 .60 .30 6 0 7 1 6 6 2 / 5 1 1 2 / 2 1 / 1 3 / t c a r t s b a e l c i t r a / t d n / m o c . p u o . c i m e d a c a / / : s p t t h 8 m 1 o 0 r 2 f l d i e r d t p a s A o e l u 1 n g 2 w o y n D b o control persons. The study population was predominantly made up of subjects < 60 years old (66%) and women (53.2%). Comorbidities and medication use of aspirin and clopidogrel were more prevalent in the ESRD cohort than in the control cohort (all P-values <0.001). In the ESRD cohort, comorbidities and medication use were more common in the HD cohort than in the PD cohort, but not significant for hypertension and AF. The propensity score cohorts consisted of 9700 PD patients and 9700 HD, with similar distributions in age, gender, comorbidities and medication use. The mean follow-up periods for the age- and sex-matched PD, HD and control cohorts were 3.75 ± 2.70, 3.89 ± 2.86 and 5.08 ± 3.03 years, respectively (data not shown). During the follow-up periods, 756 (4.03%) HD patients and 803 (8.28%) PD patients received renal transplantation. In addition, there were 3650 (3.21%), 2609 (26.9%) and 5546 (29.6%) deaths in the control, PD and HD cohorts and there were 4107 (3.61%), 193 (1.99%) and 340 (1.81%) persons lost to follow-up due to withdrawal from the insurance in these three cohorts, respectively. Figure 1 shows that the cumulative proportions of persons with permanent pacemaker implantation were 1.09 and 0.78% higher in HD and PD cohorts than in the control cohort (P < 0.001 for both) during the follow-up years, respectively. The overall incidence rates of permanent pacemaker implantation were 0.24, 1.24, 1.44 and 0.85 per 1000 person-years in the control, and the ESRD, HD and PD cohorts, respectively (Table 2). The corresponding aHRs of the implantation were 2.98 (95% CI = 2.24–3.96), 3.26 (95% CI = 2.41–4.42) and 2.36 (95% CI = 1.56–3.58) compared with controls, respectively, after adjusting for age, sex, comorbidities, medication use and the year of dialysis initiation. During the follow-up period, the implantation rate was much higher in HD patients than PD patients in the earlier follow-up years. Table 2 also illustrates that the implantation rate was 1.39-fold greater in the propensity score-matched HD cohort than in the PD cohort, with an insignificant aHR of 1.30 (95% CI = 0.82–2.05). Compared with the PD cohort, the HD cohort had an aHR of 3.85 (95% CI = 1.43–10.4) in the first year of dialysis; it then declined to 0.78 (95% CI = 0.40–1.54) after 3 years of dialysis. Table 3 illustrates the variable-specific stratified incidence rates and aHRs of permanent pacemaker implantation for dialysis cohorts compared with the control cohort. The implantation F I G U R E 1 : The cumulative proportions of persons with permanent pacemaker implantation in HD, PD and control cohorts. Downloaded from21h1tt8ps://academic.oup.com/ndt/article-abstract/31/12/2115/2661706 by guest on 21 April 2018 ESRD, end-stage renal disease; HD, hemodialysis; PD, peritoneal dialysis; aHR, adjusted hazard ratio; CI, confidence interval; CAD, coronary artery disease; AF, atrial fibrillation; CHF, congestive heart failure. aAdjusting for age, coronary artery disease, diabetes, hyperlipidemia, atrial fibrillation, CHF, aspirin use, clopidogrel use and the year of dialysis initiation. *P < 0.05; **P < 0.01; ***P < 0.001. incidence increased with age in all cohorts. However, age-specific HR was higher for younger patients, particularly for the youngest PD patients. The aHRs for implantation in the ESRD cohort were 2.84 (95% CI = 1.94–4.15) and 3.29 (95% CI = 2.13–5.08) for women and men, respectively, compared with the control cohort. Comorbidity increased the incidence of the implantation, except for stroke in the PD cohort. Among ESRD patients, the implantation hazard increased with age (aHR 1.07, 95% CI = 1.05–1.09; Table 4). Comorbidities that increased the implantation hazard were CAD (aHR = 1.72, 95% CI = 1.01–2.96) and AF (aHR = 2.94, 95% CI = 1.30–6.61). Table 5 shows that the rate of major complications needing removal or revision of the pacemaker was higher in dialysis patients than in controls (29.5 versus 18.6 per 1000 person-years after implantation). The risk was also higher for HD patients than for PD patients. The Cox analyses showed no significant hazard difference. D I S C U S S I O N Our study demonstrated that dialysis patients were at a nearly 3-fold greater hazard of cardiac dysrhythmia requiring permanent pacemaker implantation compared with age- and sexmatched controls. In addition, although uncommon, the major complication rate was somewhat higher in dialysis patients. There was no significant difference in the overall implantation hazard between HD patients and PD patients. However, the implantation risk occurred earlier in the propensity score-matched HD cohort than in the PD cohort, with an aHR of 3.85 in the first year of dialysis. There are limited reports concerning bradyarrhythmia requiring permanent cardiac pacing in ESRD patients. Leman et al. reported that the permanent pacemaker implantation rate was 2.34-fold greater for HD patients than for the general population (0.68 versus 0.29%) during a 10-year span [11]. 3.03 (0.42, 21.9) 5.74 (2.54, 13.0)*** 4.16 (2.38, 7.27)*** 2.13 (1.35, 3.35)** 3.37 (2.26, 5.03)*** 3.28 (2.05, 5.24)*** 5.98 (3.44, 10.4)*** 2.47 (1.72, 3.55)*** 3.50 (2.39, 5.14)*** 2.85 (1.74, 4.64)*** 3.22 (2.32, 4.47)*** 3.02 (1.35, 6.77)** 3.27 (2.13, 5.02)*** 3.24 (2.11, 4.97)*** 3.38 (2.45, 4.67)*** 2.42 (0.96, 6.13) 8.12 (2.99, 22.1)*** 3.04 (2.22, 4.17)*** 3.71 (2.57, 5.37)*** 2.26 (1.33, 3.85)** 3.72 (1.98, 6.96)*** 3.07 (2.18, 4.33)*** 3.54 (2.55, 4.93)*** 1.84 (0.88, 3.83) Dasgupta et al. also found >3-fold greater complication rates after permanent pacemaker or cardioverter-defibrillators implantation in dialysis patients than in matched controls (39 versus 11%) [13]. They also found that the most common causes of complications leading to the removal or revision of permanent pacemaker are infections. The present study demonstrated that the risk factors for permanent cardiac pacing in dialysis patients are older age, and comorbidities of CAD and AF. Studies have reported that mechanisms responsible for cardiac dysrhythmias in ESRD patients are related to structural and electrophysiological abnormalities of heart, volume and electrolyte shifts, vascular calcification and autonomic dysfunction [14, 15]. Cardiac fibrosis and left ventricular hypertrophy are common disorders in dialysis patients [16, 17]. Myocardial fibrosis disrupts the Downloaded from21h2tt0ps://academic.oup.com/ndt/article-abstract/31/12/2115/2661706 by guest on 21 April 2018 normal tissue architecture and slows conduction velocity across the injured tissue favoring the development of arrhythmia [18]. CAD is also highly prevalent among ESRD patients, even at the time of dialysis initiation [19]. An earlier study showed that the coronary artery calcification scores were 2- to 5-fold higher in dialysis patients with angiographically proven CAD than agematched controls [20]. The diffuse vascular calcification in nature is related to hyperphosphatemia in dialysis patients [21]. The resultant calcification can further compromise the myocardial perfusion reserve, increasing ischemic events and triggering bradyarrhythmia. Furthermore, studies have found that ESRD and diabetes are risk factors for cardiac autonomic neuropathy associated with abnormal heart rate variability, increasing the cardiovascular and all-cause mortality [22, 23]. A sudden loss of sympathetic tone may induce bradyarrhythmia. Dialysis itself may predispose patients to the risk of CVD [24]. The HD procedure is a major stressor, leading to a higher risk of cardiac arrest and arrhythmia than PD therapy (62.2 versus 42.8 events/10 000 patient-years) [25]. The HD treatment induces rapid changes in blood pressure, pH, electrolytes and volume of blood, leading to electrical myocardial instability [3, 26]. In addition, HD may induce repetitive hemodynamic instability, leading to microvascular dysfunction, subsequent myocardial ischemia and prolonged left ventricular dysfunction, known as myocardial stunning [27]. HD patients with intradialytic recurrent myocardial stunning may progress to develop irreversible myocardial fibrosis, leading to CHF, arrhythmia and sudden cardiac death [ 28 ]. Bleyer and colleague found in a case–control study that the sudden death risk in HD patients increased within 12 h after the start of a dialysis session and in the last 12 h of the longer weekend (3-day) interdialytic period [ 29 ]. A recent study also found that the greatest risk of significant arrhythmia is during the 72-h long break between HD sections [ 9 ]. The sudden cardiac deaths were attributable to severe bradycardia and asystole [ 9 ]. On the other hand, glucose-based solutions used in PD patients may result in insulin resistance, dyslipidemia and metabolic syndrome, leading to atherosclerosis [30]. The present study showed that the propensity score-matched HD patients had an overall insignificant aHR of 1.30 for permanent pacemaker implantation compared with PD patients. However, we found a significantly higher risk of implantation for HD patients than PD patients in the first year of dialysis. A recent European study also showed a higher rate of cardiovascular events during the first 4 months of HD than during subsequent periods [31]. It is likely that the preservation of residual renal function may account for the early advantage of less cardiovascular events in PD patients [32]. As the residual renal function gradually declines, the peritoneal permeability may shift to a higher transport status over time, and PD patients may develop hypertension, fluid overload and left ventricular hypertrophy [33–35]. This may explain the increased implantation risk during the later follow-up period in PD patients. The present study has several limitations. First, information on body mass index and smoking habits was limited and the results of laboratory tests were unavailable. We were, therefore, unable to control these variables in the data analysis. However, the insurance system audited the indication and the quality of dialysis. Thus, the residual renal function at the start of dialysis and adequacy might not be different between HD and PD patients. Second, the choice of dialysis modality was up to patients and medical staff. The majority of patients choose to receive HD at dialysis centers. Thus, selection bias might exist. However, we established the propensity score-matched HD and PD cohorts, which could minimize the selection bias. Third, this study used coding to identify diseases. There was a possibility of coding errors for comorbidities. In addition, the age- and sex-matched control group was otherwise poorly matched. Furthermore, the “low” event rates of pacemaker implantation, especially for propensity-matched HD versus PD analysis and stratified analysis, could have led to imprecise estimates. In conclusion, dialysis patients are at a nearly 3-fold increased risk of dysrhythmia requiring pacemaker implantation compared with the general population. No significant difference is observed in the overall risk of dysrhythmia requiring pacemaker implantation between HD and PD patients. Our findings suggest that physicians may need to monitor the risk of dysrhythmia requiring permanent cardiac pacing among dialysis patients, particularly for those of older ages, or with CAD or AF. A U T H O R S ’ C O N T R I B U T I O N S I-K.W. designed the study and drafted the manuscript; C.-L.L. conducted the statistical analysis and result interpretation; K.-H.L., S.-Y.L., C.-T.C. and T.-H.Y. assisted in literature research and designed the study; and F.-C.S. revised the manuscript. A C K N O W L E D G E M E N T S The present study was supported by National Sciences Council, Executive Yuan, Taiwan (grant numbers NSC 100-2621-M-039-001); the research laboratory of pediatrics, Children’s Hospital of China Medical University (DMR-99-055), China Medical University Hospital (grant number DMR-105-021, DMR-104-015); Taiwan Ministry of Health and Welfare Clinical Trial and Research Center of Excellence (MOHW105-TDU-B-212-133019); Academia Sinica Taiwan Biobank, Stroke Biosignature Project (BM104010092); NRPB Stroke Clinical Trial Consortium (MOST 103-2325-B-039 -006); Tseng-Lien Lin Foundation, Taichung, Taiwan; Taiwan Brain Disease Foundation, Taipei, Taiwan; and Katsuzo and Kiyo Aoshima Memorial Funds, Japan. C O N F L I C T O F I N T E R E S T S T A T E M E N T None declared. (See related article by Kambur et al. The natural history of symptomatic cardiac conduction-system disease in end-stage renal disease. Nephrol Dial Transplant 2016; 31: 1973–1975) R E F E R E N C E S E L C I T R A L A N I G I R O Atypical haemolytic uraemic syndrome and pregnancy: outcome with ongoing eculizumab Aude Servais1,2, Nadège Devillard3, Véronique Frémeaux-Bacchi4,5, Aurélie Hummel1,2, Laurent Salomon2,6, Cécile Contin-Bordes7, Hélène Gomer8, Christophe Legendre1,2 and Yahsou Delmas9 1Department of Nephrology and Transplantation, Hôpital Necker-Enfants Malades, AP-HP, 149 rue de Sèvres, 75015 Paris, France, 2Université Paris Descartes, Paris, France, 3Department of Nephrology, CHU Besançon, Besançon, France, 4Cordeliers Research Center, INSERM UMRS 872, 75006 Paris, France, 5Department of Immunology, Hôpital Européen Georges Pompidou, AP-HP, Paris, France, 6Department of Obstetrics, Hôpital Necker-Enfants Malades, AP-HP, Paris, France, 7Department of Immunology, CHU Bordeaux, CNRS-UMR 5164 Bordeaux University, Bordeaux, France, 8Department of Obstetrics, CHU Bordeaux, Bordeaux, France and 9Department of Nephrology Transplantation-Dialysis, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France Correspondence and offprint requests to: Aude Servais; E-mail: A B S T R A C T Background. A therapeutic strategy based on complement blockade by eculizumab is widely used to treat atypical haemolytic uraemic syndrome (aHUS). Recent data are available on the administration of eculizumab during pregnancy in patients treated for paroxysmal nocturnal haemoglobinuria but there are very few data for aHUS patients. Methods. We analysed the use of eculizumab for the treatment of aHUS during five pregnancies in three patients and studied an additional pregnancy without eculizumab. Obstetrical data and maternal and foetal complications during pregnancy, at delivery, and during the post-partum period were recorded. Results. The mean age at pregnancy was 28.5 (range 25–33) years. The mean serum creatinine before pregnancy was 189 (range 130–300) µmol/L and the mean eGFR was 32 (range 18–45) mL/min/1.73 m2. One patient who stopped eculizumab 3 weeks after conception had a termination due to a relapse of HUS at 12 weeks of gestation (WG) during a first pregnancy and an intrauterine death at 24 WG despite continuous eculizumab treatment during a second pregnancy. In the other four © The Author 2016. 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Wang, I-Kuan, Lin, Kuo-Hung, Lin, Shih-Yi, Lin, Cheng-Li, Chang, Chiz-Tzung, Yen, Tzung-Hai, Sung, Fung-Chang. Permanent cardiac pacing in patients with end-stage renal disease undergoing dialysis, Nephrology Dialysis Transplantation, 2016, 2115-2122, DOI: 10.1093/ndt/gfw302