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-

Cardiovascular disease is the leading cause of death
among dialysis-dependent renal failure patients.1
Dialysis-dependent renal failure patients have a 9-fold
From the *Zeenat Qureshi Stroke Research Center, University
of Minnesota, Minneapolis, Minnesota; and Department of Neph-
rology, Dartmouth Hitchcock Medical Center, Lebanon, New
Hampshire.
Received January 13, 2013; revision received March 2, 2013;
accepted March 14, 2013.
Address correspondence to Nauman Tariq, MD, Zeenat Qureshi
Stroke Center, University of Minnesota, Minneapolis, Minnesota.
E-mail: nomitq@gmail.com.
1052-3057/$ - see front matter
2013 by National Stroke Association
http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2013.03.016
rhagic and ischemic) compared with general population.2
Because of a high prevalence of ischemic stroke and
regular medical contact, dialysis-dependent patients are
likely to present within the time window of thrombolytic
administration. Ischemic strokes are not infrequent
during and immediately after dialysis with rapid access
to medical care. Up to 34% of the ischemic stroke in
patients on maintenance dialysis occur during or less
than 30 minutes after the dialysis procedure.3 However,
despite the potential of administering thrombolytic treat-
ment to reduce the high rate of death and disability,
the NINDS rt-PA trial4 and subsequent thrombolytic
therapy trials5,6 did not include patients with renal
failure requiring dialysis. There are small reports that
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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OUTCOMES OF DIALYSIS-DEPENDENT PATIENTS
and death in patients with renal dysfunction treated with
intravenous (IV) thrombolytics,7,8 but no large-scale stud-
ies have addressed this issue.
We sought to determine the outcomes of dialysis-
dependent renal failure patients who had ischemic
stroke and were treated with IV thrombolytics in the
United States and also compared the outcomes with
thrombolytic-treated patients without dialysis depen-
dence using a nationally representative inpatient database.
Methods
We used the data files from National Inpatient Sample
(NIS) from 2002 to 2009 for our analysis. NIS is the largest
all-payer database in the United States. Using appropriate
sampling weights, national estimates are derived based
on the data from 20% of nonfederal hospitals. The data-
base contains information on patients demographic and
clinical characteristics, in-hospital procedures, hospital
characteristics, and discharge outcomes. A comprehen-
sive synopsis on NIS data is available at http://www.
hcup-us.ahrq.gov. All thrombolytic-treated patients pre-
senting with acute ischemic stroke with or without under-
lying dialysis-dependent renal failure were included. We
used the International Classification of Disease, Ninth Revi-
sion, Clinical Modification (ICD-9-CM) primary diagnosis
codes 433-437.1 to identify the patients admitted with
ischemic stroke and ICD-9-CM code 99.10 to identify the
patients who received thrombolytics.
Dialysis-dependent renal failure patients were identi-
fied by using ICD-9-CM codes 54.98 (peritoneal dialysis)
and 39.95 (hemodialysis).
Study variables included were patients age, gender,
race/ethnicity, and comorbidities obtained from Agency
for Healthcare Research and Quality comorbidity data
files, including diabetes mellitus, hypertension, renal fail-
ure, congestive heart failure, chronic lung disease, and coa-
gulopathy. ICD-9-CM secondary diagnosis codes were
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
thrombosis (451.1, 451.2, 451.81, 451.9, 453.1, 453.2, 453.8,
and 453.9), and pulmonary embolism (415.1) that occurred
as a consequence of ischemic stroke during hospitaliza-
tion. However, we were unable to differentiate with abso-
lute certainty whether the occurrence was before or during
hospitalization. We also used ICD-9-CM procedure codes
to estimate the percentage of stroke patients who under-
went in-hospital procedures such as cerebral angiography
(88.41), mechanical ventilation (96.72), carotid angio-
plasty/stent placement (.63/.64), carotid endarterectomy
(38.10-38.19), intubation (96.04), tracheostomy (31.20-
31.29), and gastrostomy (431.1-431.9).
We determined the length of stay and hospital charges
associated with hospitalization. In the NIS data set,
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e355
discharge status is categorized into routine, home health
care, short-term hospital, and other facilities including in-
termediate care and skilled nursing home or death. We
categorized routine discharge as none or minimal disabil-
ity (discharge to home with or without home health care
and short-term hospital stay) and any other discharge sta-
tus as moderate-to-severe disability (intermediate care
and skilled nursing home) as previously described.9 Pre-
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
predictive value of discharge to nursing home and reha-
bilitation facility was 95% for unfavorable outcome at
3 months defined by mRS score 2-6.
Statistical Analysis
The SAS 9.1 software (SAS Institute, Cary, NC) was used
to convert NIS database data into weighted counts to gen-
erate national estimates, following Healthcare Cost and
Utilization Project recommendations.11 We performed
univariate analysis, chi-square for categorical, and t test
for continuous variables to identify differences in study
variables and outcome end points between patients with
and those without dialysis-dependent renal failure.
To assess the effect of dialysis-dependent renal failure
on outcome of thrombolytic-treated patients, 2 models
were created. Model 1 included all patients, and logistic
regression analysis was used to identify the association
between dialysis-dependent renal failure and odds of
in-hospital mortality. Model 2 included patients who
were discharged alive, and logistic regression analysis
was used to identify the association between dialysis-
dependent renal failure and odds of moderate-to-severe
disability. All variables that were significant in the univar-
iate analysis were included in the logistic regression model
as potential confounders. All analyses were performed
using the SAS 9.1 software (SAS Institute, Cary, NC).
Results
Of 82,142 patients with ischemic stroke who were
treated with IV thrombolytics, 1072 (1.3%) had dialysis-
dependent renal failure. Of the 1072 patients, 1007 (94%)
were on hemodialysis and 65 (6%) were on peritoneal
dialysis. There was a difference in the race/ethnicity of pa-
tients in the 2 groups: the proportion of white patients was
lower than those of African-American and Hispanic
patients among dialysis-dependent patients treated with
thrombolytics (Table 1). The proportion of patients with
pre-existing hypertension, diabetes mellitus, congestive
heart failure, myocardial infarction, or coagulopathy was
higher in dialysis-dependent renal failure patients. The
rate of in-hospital complicationspneumonia, deep vein
thrombosis, and sepsis, was higher in dialysis-dependent
renal failure patients. The rates of cerebral angiography
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
dialysis-dependent patients treated with thrombolytics.
The in-hospital mortality rate were higher in dialysis-
dependent renal failure patients treated with thrombo-
lytics (22% versus 11%, P , .0001). The mean hospital
charges were $112,610 in dialysis-dependent patients ver-
sus $62,083 in non-dialysis-dependent patients. The mean
length of stay was longer in dialysis-dependent patients.
The ICH rates did not differ significantly between
patients with ischemic stroke with or without dialysis-
dependent renal failure who received thrombolytics
(5.2% versus 6.1%, P 5 0.5, see Table 1). We also analyzed
the data for 42,15,004 patients with ischemic stroke
who did not receive thrombolytic treatment and found
that dialysis-dependent patients (61,400, ie, 1.4% of total)
compared with those without dialysis dependence had

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OUTCOMES OF DIALYSIS-DEPENDENT PATIENTS e357

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

.0005

.0008
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

,.0001

.0208
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).

,.0001

.0136
Discussion

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