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Outcomes of Thrombolytic Treatment for Acute Ischemic Stroke

in Dialysis-Dependent Patients in the United States

Nauman Tariq, MD,* Malik M. Adil, MD,* Fahad Saeed, MD,*

Saqib A. Chaudhry, MD,* and Adnan I. Qureshi, MD*

Objective: To determine the outcomes of dialysis-dependent renal failure patients

who had ischemic stroke and were treated with intravenous (IV) thrombolytics in
the United States. Methods: We analyzed the data from Nationwide Inpatient Sample
(2002-2009) for all thrombolytic-treated patients presenting with acute ischemic
stroke with or without dialysis dependence. Patients were identified using the Inter-
national Classification of Disease, Ninth Revision, Clinical Modification codes. Baseline
characteristics, in-hospital complications including secondary intracerebral hemor-
rhage (ICH), sepsis, pneumonia, pulmonary embolism, deep venous thrombosis, uri-
nary tract infections, and discharge outcomes (mortality, minimal disability, and
moderate-to-severe disability) were compared between the groups. Results: Of the
82,142 patients with ischemic stroke who receive thrombolytic treatment,
1072 (1.3%) was dialysis dependent. The ICH rates did not differ significantly
between patients with ischemic stroke with or without dialysis who received throm-
bolytics (5.2% versus 6.1%). The in-hospital mortality rate was higher in dialysis-
dependent patients treated with thrombolytics (22% versus 11%, P # .0001). After
adjusting for age, sex, and comorbidities, dialysis dependence was associated with
higher rates of in-hospital mortality in patients treated with thrombolytics (odds
ratio, 1.92; 95% confidence interval, 1.33-2.78, P 5 .0005). Conclusions: The 2-fold
higher odds of in-hospital mortality associated with administration of IV thrombo-
lytics in dialysis-dependent patients who present with acute ischemic stroke warrant
a careful assessment of riskbenefit ratio in this population. Key Words: Ischemic
strokethrombolysisdialysisrenal failure.
2013 by National Stroke Association

Introduction higher mortality rate attributed to stroke (both hemor-

rhagic and ischemic) compared with general population.2
Cardiovascular disease is the leading cause of death
Because of a high prevalence of ischemic stroke and
among dialysis-dependent renal failure patients.1
regular medical contact, dialysis-dependent patients are
Dialysis-dependent renal failure patients have a 9-fold
likely to present within the time window of thrombolytic
administration. Ischemic strokes are not infrequent
From the *Zeenat Qureshi Stroke Research Center, University during and immediately after dialysis with rapid access
of Minnesota, Minneapolis, Minnesota; and Department of Neph-
to medical care. Up to 34% of the ischemic stroke in
rology, Dartmouth Hitchcock Medical Center, Lebanon, New
patients on maintenance dialysis occur during or less
Received January 13, 2013; revision received March 2, 2013; than 30 minutes after the dialysis procedure.3 However,
accepted March 14, 2013. despite the potential of administering thrombolytic treat-
Address correspondence to Nauman Tariq, MD, Zeenat Qureshi ment to reduce the high rate of death and disability,
Stroke Center, University of Minnesota, Minneapolis, Minnesota.
the NINDS rt-PA trial4 and subsequent thrombolytic
E-mail: nomitq@gmail.com.
1052-3057/$ - see front matter
therapy trials5,6 did not include patients with renal
2013 by National Stroke Association failure requiring dialysis. There are small reports that
http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2013.03.016 document a high rate of intracerebral hemorrhage (ICH)

e354 Journal of Stroke and Cerebrovascular Diseases, Vol. 22, No. 8 (November), 2013: pp e354-e359

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and death in patients with renal dysfunction treated with discharge status is categorized into routine, home health
intravenous (IV) thrombolytics,7,8 but no large-scale stud- care, short-term hospital, and other facilities including in-
ies have addressed this issue. termediate care and skilled nursing home or death. We
We sought to determine the outcomes of dialysis- categorized routine discharge as none or minimal disabil-
dependent renal failure patients who had ischemic ity (discharge to home with or without home health care
stroke and were treated with IV thrombolytics in the and short-term hospital stay) and any other discharge sta-
United States and also compared the outcomes with tus as moderate-to-severe disability (intermediate care
thrombolytic-treated patients without dialysis depen- and skilled nursing home) as previously described.9 Pre-
dence using a nationally representative inpatient database. dictive values of discharge destination as a surrogate for
defining unfavorable outcome at 3- and 12-month post-
stroke as defined by modified Rankin scale (mRS) scores
have been validated previously in 1 study.10 The positive
We used the data files from National Inpatient Sample predictive value of discharge to nursing home and reha-
(NIS) from 2002 to 2009 for our analysis. NIS is the largest bilitation facility was 95% for unfavorable outcome at
all-payer database in the United States. Using appropriate 3 months defined by mRS score 2-6.
sampling weights, national estimates are derived based
on the data from 20% of nonfederal hospitals. The data- Statistical Analysis
base contains information on patients demographic and
The SAS 9.1 software (SAS Institute, Cary, NC) was used
clinical characteristics, in-hospital procedures, hospital
to convert NIS database data into weighted counts to gen-
characteristics, and discharge outcomes. A comprehen-
erate national estimates, following Healthcare Cost and
sive synopsis on NIS data is available at http://www.
Utilization Project recommendations.11 We performed
hcup-us.ahrq.gov. All thrombolytic-treated patients pre-
univariate analysis, chi-square for categorical, and t test
senting with acute ischemic stroke with or without under-
for continuous variables to identify differences in study
lying dialysis-dependent renal failure were included. We
variables and outcome end points between patients with
used the International Classification of Disease, Ninth Revi-
and those without dialysis-dependent renal failure.
sion, Clinical Modification (ICD-9-CM) primary diagnosis
To assess the effect of dialysis-dependent renal failure
codes 433-437.1 to identify the patients admitted with
on outcome of thrombolytic-treated patients, 2 models
ischemic stroke and ICD-9-CM code 99.10 to identify the
were created. Model 1 included all patients, and logistic
patients who received thrombolytics.
regression analysis was used to identify the association
Dialysis-dependent renal failure patients were identi-
between dialysis-dependent renal failure and odds of
fied by using ICD-9-CM codes 54.98 (peritoneal dialysis)
in-hospital mortality. Model 2 included patients who
and 39.95 (hemodialysis).
were discharged alive, and logistic regression analysis
Study variables included were patients age, gender,
was used to identify the association between dialysis-
race/ethnicity, and comorbidities obtained from Agency
dependent renal failure and odds of moderate-to-severe
for Healthcare Research and Quality comorbidity data
disability. All variables that were significant in the univar-
files, including diabetes mellitus, hypertension, renal fail-
iate analysis were included in the logistic regression model
ure, congestive heart failure, chronic lung disease, and coa-
as potential confounders. All analyses were performed
gulopathy. ICD-9-CM secondary diagnosis codes were
using the SAS 9.1 software (SAS Institute, Cary, NC).
used to identify those patients with stroke-associated com-
plications such as ICH (431 and 432), pneumonia (486, 481,
482.8, and 482.3), urinary tract infection (599.0, 590.9), sep-
sis (995.91, 996.64, 038, 995.92, and 999.3), deep venous Of 82,142 patients with ischemic stroke who were
thrombosis (451.1, 451.2, 451.81, 451.9, 453.1, 453.2, 453.8, treated with IV thrombolytics, 1072 (1.3%) had dialysis-
and 453.9), and pulmonary embolism (415.1) that occurred dependent renal failure. Of the 1072 patients, 1007 (94%)
as a consequence of ischemic stroke during hospitaliza- were on hemodialysis and 65 (6%) were on peritoneal
tion. However, we were unable to differentiate with abso- dialysis. There was a difference in the race/ethnicity of pa-
lute certainty whether the occurrence was before or during tients in the 2 groups: the proportion of white patients was
hospitalization. We also used ICD-9-CM procedure codes lower than those of African-American and Hispanic
to estimate the percentage of stroke patients who under- patients among dialysis-dependent patients treated with
went in-hospital procedures such as cerebral angiography thrombolytics (Table 1). The proportion of patients with
(88.41), mechanical ventilation (96.72), carotid angio- pre-existing hypertension, diabetes mellitus, congestive
plasty/stent placement (.63/.64), carotid endarterectomy heart failure, myocardial infarction, or coagulopathy was
(38.10-38.19), intubation (96.04), tracheostomy (31.20- higher in dialysis-dependent renal failure patients. The
31.29), and gastrostomy (431.1-431.9). rate of in-hospital complicationspneumonia, deep vein
We determined the length of stay and hospital charges thrombosis, and sepsis, was higher in dialysis-dependent
associated with hospitalization. In the NIS data set, renal failure patients. The rates of cerebral angiography

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e356 N. TARIQ ET AL.

Table 1. Characteristics and outcomes of patients with ischemic stroke treated with thrombolytics with or without
dialysis-dependent renal failure*

Dialysis-dependent renal Dialysis-dependent renal

failure present failure not present P value

Overall number 1072 81,070

Age, mean (CI) 67.3 (65.5-69.1) 69.0 (68.5-69.2) .01
Women 585 (54.5) 39,179 (48.3) .07
Race/ethnicity ,.0001
White 478 (54.6) 47,610 (75.7)
African-American 254 (29.0) 7720 (12.2)
Hispanic 79 (9.0) 4013 (6.3)
Other 65 (7.4) 3522 (5.6)
Comorbid conditions
Hypertension 937 (88.0) 58,421 (72.6) ,.0001
Diabetes mellitus 491 (45.8) 19,037 (23.4) ,.0001
Congestive heart failure 411 (38.6) 12,317 (15.2) ,.0001
Chronic lung disease 147 (13.8) 11,176 (13.8) .9918
Myocardial infarction 82 (7.6) 2364 (2.9) .0115
Coagulopathy 86 (8.0) 1836 (2.2) .002
Renal failure 984 (92.3) 4967 (6.1) ,.0001
Alcohol use 34 (3.2) 2925 (3.6) .74
In-hospital complications
Pneumonia 126 (11.7) 3067 (3.7) .0003
Deep venous thrombosis 84 (7.8) 665 (.8) .0002
Urinary tract infection 160 (14.9) 11,395 (14) .7245
Sepsis 133 (12.4) 1145 (1.4) ,.0001
Pulmonary embolism 16 (1.4) 446 (.5) .282
Respiratory insufficiency 9 (.8) 608 (.7) .809
In-hospital procedures
Cerebral angiography 165 (15.3) 19,093 (23.5) .0021
Gastrostomy 144 (13.4) 7826 (9.6) .1148
Mechanical ventilation 120 (11.1) 3754 (4.6) .0038
Carotid artery stent placement 9 (.8) 2090 (2.5) .0073
Carotid endarterectomy 26 (2.5) 1434 (1.7) .5138
Tracheostomy 14 (1.3) 148 (.1) .1244
Intubation 231 (21.6) 9026 (11.1) .0002
Hospital teaching status .79
Nonteaching 426 (40) 32,930 (40.7)
Teaching 640 (60.0) 47,832 (59.2)
Length of stay 14.24 (12.1-16.3) 7.12 (7.0-7.3) ,.0001
Hospital charges 112,610 (93534.4-131685.1) 62,083 (58678.4-65488.0) ,.0001
Discharge disposition
None-to-minimal disability 365 (34.0) 29,697 (36.6) .4397
Moderate-to-severe disability 466 (43.4) 42,143 (51.9) .0129
Intracerebral hemorrhage 56 (5.2) 4995 (6.1) .5599
In-hospital mortality 240 (22.4) 8938 (11.0) ,.0001

Abbreviation: CI, confidence interval.

*Data from the Nationwide Inpatient Sample 2005 through 2008. P , .05 for 2 3 2 tables. For 2 3 n tables, individual P values were tested if
c2 P , .05, and the P value was considered significant if P , .05/(n 2 1) (Bonferroni correction).

and carotid angioplasty/stent placement were lower in The ICH rates did not differ significantly between
dialysis-dependent patients treated with thrombolytics. patients with ischemic stroke with or without dialysis-
The in-hospital mortality rate were higher in dialysis- dependent renal failure who received thrombolytics
dependent renal failure patients treated with thrombo- (5.2% versus 6.1%, P 5 0.5, see Table 1). We also analyzed
lytics (22% versus 11%, P , .0001). The mean hospital the data for 42,15,004 patients with ischemic stroke
charges were $112,610 in dialysis-dependent patients ver- who did not receive thrombolytic treatment and found
sus $62,083 in non-dialysis-dependent patients. The mean that dialysis-dependent patients (61,400, ie, 1.4% of total)
length of stay was longer in dialysis-dependent patients. compared with those without dialysis dependence had

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The outcomes were divided into 2 models. Model 1 includes outcomes of all patients with discharged alive taken as reference and model 2 includes only patients that were alive at the time of discharge.
higher rates of inpatient mortality (9.8% versus 4.1%,
P , .0001).

Adjusted for age, gender, and

P value


After adjusting for age and gender, dialysis-dependent

Table 2. Multivariate analyses analyzing effect of dialysis-dependent renal failure on various outcomes among patients with ischemic stroke treated with IV thrombolytics

medical comorbidities*
renal failure was associated with higher rates of in-
hospital mortality in patients treated with thrombolytics
(odds ratio [OR], 2.5; 95% confidence interval [CI],

1.9 (1.33-2.78)
1.0 (reference)

1.0 (reference)
OR (95% CI)
1.80-3.38, P # .0001). After adjusting for age, gender, and

.6 (.43-.80)
comorbidities (hypertension, diabetes mellitus, congestive
heart failure, renal failure), and hospital teaching status,
dialysis-dependent renal failure was associated with
higher rates of in-hospital mortality in patients treated
with thrombolytics (OR, 1.9; 95% CI, 1.33-2.78, P 5 .0005)

Adjusted for age and gender


P value
(Table 2, model 1). After adjusting for age and gender,
dialysis-dependent renal failure was associated with
lower rates of moderate-to-severe disability in patients
treated with thrombolytics (OR, .7; 95% CI, .54-.95, P 5

2.5 (1.80-3.38)
1.0 (reference)

1.0 (reference)
OR (95% CI)
.01). After adjusting for age, gender, and comorbidities,

.7 (.54-.95)
dialysis was associated with lower rates of moderate-to-
severe disability in patients treated with thrombolytics
(OR, .6; 95% CI, .43-.80, P 5 .0008) (see Table 2, model 2).



P value
Unadjusted analysis

*Adjusted for hypertension, diabetes mellitus, congestive heart failure, renal failure, and hospital teaching status.
The important finding in our study is the 2-fold higher
odds of in-hospital mortality associated with administra-

2.3 (1.70-3.20)
1.0 (reference)

1.0 (reference)
OR (95% CI)
tion of IV thrombolytics in dialysis-dependent renal fail-

.7 (.54-.93)
ure patients who presented with acute ischemic stroke.
We also found that dialysis-dependent renal failure pa-
tients who underwent thrombolytic treatment had longer
inpatient stay and higher rate of in-hospital complica-

Analysis comprising of patients alive at discharge

tions. The hospital charges were more than 2-fold higher
Clinical outcomes subdivided in 2 models

in thrombolytic-treated patients undergoing dialysis.

Ischemic stroke is the more common type of stroke in di-
alysis patients.12 However, there is lack of data on efficacy
of thrombolytics in dialysis patients. Previous studies
Analysis comprising of all patients

have reported variable findings regarding comparative

Moderate-to-severe disability

rates of favorable outcomes and ICH. In a recent case

None-to-minimal disability

series of 4 patients13 who developed ischemic stroke on

the day of dialysis, IV rt-PA use resulted in 1 patient devel-
In-hospital mortality

oping intraventricular hemorrhage. The mRS score at

Abbreviations: CI, confidence interval; OR, odds ratio.
Discharged alive

3 months was 2 or less in 3 of the 4 patients. In a study

by Lyrer et al,8 renal dysfunction was associated with
poor outcomes (26% mortality at 3 months). Risk of bleed-
ing was slightly higher in patients with renal dysfunction
but was not statistically significant in the latter study. In
another observational study by Toyoda et al,3 glomerular
Model 1 (includes all patients)

filteration rate less than 60 mL/min/1.73 m2 was associ-

Model 2 (includes patients

ated with poor outcomes, high mortality (33% versus

18% at 4 weeks), and high rates of symptomatic ICH
alive at discharge)

(28% at 4 weeks). However, in another study by Agrawal

et al,14 in-hospital outcomes were statistically insignificant
in IV rt-PAtreated patients with normal renal function
compared with patients with renal dysfunction (estimated
GFR , 60 mL/min/1.73 m2), that is, in-hospital death 10%
versus 7.4% and rate of ICH 20% versus 11%. Of note,
these outcomes are very likely different from the dialysis

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e358 N. TARIQ ET AL.

population in our study because of a lack of residual kid- NIS data depend on the accuracy of diagnoses and proce-
ney function in these patients. Because of a lack of data dures listed on discharge summaries and on the data col-
and conflicting evidence in literature, there is no consen- lection system. We used primary ICD-9-CM codes for
sus on administration of IV rt-PA in dialysis patients identifying patients with ischemic stroke that has a true
presenting with ischemic stroke. A survey conducted on positive rate of up to 84% in previous population-based
stroke experts15 revealed that one third would treat hemo- studies.27 The discharge functional outcome cannot be
dialysis patients with this IV therapy and 78% of them measured with the available data, and the closest index
would consider intra-arterial/mechanical thrombectomy. is the destination of discharge. Previous studies among
The high mortality in ischemic stroke patients with patients with ischemic stroke receiving IV thrombolysis
dialysis-dependent renal failure receiving thrombolytics have suggested that discharge destination correlates
requires further elaboration. A previous study16 reported with severity of neurological deficits and thrombolytic-
35% mortality within 30 days of IV rt-PA treatment in related complications.28 The conclusions regarding dis-
dialysis-dependent renal failure patients. A high propor- ability incurred with ischemic stroke in this analysis
tion of these patients have medical comorbidities such as need to be interpreted with this understanding. Outcome
hypertension, diabetes mellitus, or dyslipidemia. There measures in our study are reported at the time of
are also other factors unique to this patient population discharge, which is suboptimal compared with 30- to
such as uremia, anemia,17-19 and the dialysis procedure20 it- 90-day outcomes usually provided by other studies;
self. All these factors and concomitant cardiovascular therefore, we may be underestimating the effect of late
disease may have contributed to increased mortality ob- recovery. Because of the limitation of the data, we cannot
served in rt-PAtreated dialysis-dependent renal failure pa- determine if the observed mortality and morbidity events
tients in our study. In addition, it has been suggested that were directly related to thrombolysis itself or a conse-
the uremic milieu in patients receiving dialysis potentiates quence of pre-existing comorbidities. We used multivari-
vascular and thrombus calcification.21 Calcified emboli are ate analysis to mitigate the effect of pre-existing
more resistant to lysis by thrombolytics and may result in comorbidities. Certain data sets, such as the United States
lower rates of recanalization.22,23 Almost one third of Renal Data System, that have a more standardized data
these stroke events occur in the peri-dialysis period.3 collection methodology and longitudinal follow-up may
Most of the hemodialysis patients receive heparin during be used in the future studies to provide more in-depth
the dialysis procedure. Elevated partial thromboplastin analysis.
time, which is frequent immediately after dialysis if not de-
tected, may lead to an increase in ICH rate after IVrt-PA ad- Conclusion
ministration. Moreover, renal dysfunction might impair
endothelial release of t-PA24 and increase plasminogen acti- We observed that there is substantially a high rate of
vator inhibitor-1 activity25 and plasma levels of lipopro- complications and mortality in dialysis-dependent renal
tein(a)26; these abnormalities may prevent reperfusion failure patients treated with IV thrombolytics for acute is-
within ischemic tissue because of microvascular compro- chemic stroke. Ischemic stroke frequently occurs during or
mise. In our study, the rate of ICH was comparable between immediately after the dialysis procedure3,20 within
patients with or without dialysis-dependent renal failure; a health care setting. Therefore, a substantial number of
therefore, the rate of higher mortality is not explained by these patients have access to time-dependent interventions
a differential rate of ICH. We also observed that the percent- such as thrombolytics. However, careful assessment of
age of patients with moderate-to-severe disability at the risks versus benefits must be undertaken in these patients
time of discharge was lower in the dialysis-dependent before administering IV thrombolytics. Future studies are
group. This latter phenomenon is because of the increased necessary in ischemic stroke patients with renal failure re-
inpatient mortality and shift from severe disability into quiring dialysis to identify patients who are most likely to
death in this group. The high mortality among dialysis- benefit from alternative acute therapies such as intra-
dependent patients is seen even in patients who do not re- arterial thrombolysis and mechanical thrombectomy.
ceive IV thrombolysis; therefore, the exact contribution of
treatment versus disease is not known. The higher mean References
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