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ORIGINAL ARTICLE
Nephrol Dial Transplant (2016) 31: 128132
doi: 10.1093/ndt/gfv246
Advance Access publication 9 July 2015
Outcomes of transient ischemic attack in maintenance
dialysis patients and those with chronic kidney disease
Fahad Saeed1, Malik M. Adil2, Gabriel A. Vidal2, Bilal Hussain Piracha3, Fadi Nahab4, Abdus Salam Khan5 and
Sankar D. Navaneethan1
1
Department of Nephrology and Hypertension, Cleveland Clinic, Cleveland, OH, USA, 2Department of Neurology, Ochsner Clinic Foundation
and Ochsner Neuroscience Institute, New Orleans, LA, USA, 3Integris South west hospital, Oklahoma City, OK, USA, 4Department of Neurology,
Emory Healthcare, Atlanta, GA, USA and 5Department of Emergency Medicine, Shifa International Hospital, Islamabad, Pakistan
Correspondence and offprint requests to: Fahad Saeed; E-mail: fahadsaeed20@gmail.com
A B S T R AC T
Background. In-hospital outcomes of transient ischemic attack
(TIA) in patients with chronic kidney disease (CKD) and end-
stage renal disease (ESRD) requiring maintenance dialysis are
largely unknown. We evaluated TIA-related in-hospital out-
comes in these patients using a national database.
Methods. Our study is observational in nature. Data from all
adult (18 years) patients admitted to US hospitals between
2005 and 2011 with a primary discharge diagnosis of TIA
The Author 2015. Published by Oxford University Press
on behalf of ERA-EDTA. All rights reserved.
therapy pre-kidney transplantation? Adv Perit Dial 2012; 28: 8993
35. Snyder JJ, Kasiske BL, Gilbertson DT et al. A comparison of transplant out-
comes in peritoneal and hemodialysis patients. Kidney Int 2002; 62: 14231430
36. van de Luijtgaarden MW, Noordzij M, Stel VS et al. Effects of comorbid and
demographic factors on dialysis modality choice and related patient
survival in Europe. Nephrol Dial Transplant 2011; 26: 29402947
37. Karopadi AN, Mason G, Rettore E et al. Cost of peritoneal dialysis and haemo-
dialysis across the world. Nephrol Dial Transplant 2013; 28: 25532569
38. Castledine CI, Gilg JA, Rogers C et al. Renal centre characteristics and phys-
ician practice patterns * associated with home dialysis use. Nephrol Dial
Transplant 2013; 28: 21692180
39. Hingwala J, Diamond J, Tangri N et al. Underutilization of peritoneal dia-
lysis: the role of the nephrologists referral pattern. Nephrol Dial Transplant
2013; 28: 732740
40. Jager KJ, Korevaar JC, Dekker FW et al. The effect of contraindications and
patient preference on dialysis modality selection in ESRD patients in The
Netherlands. Am J Kidney Dis 2004; 43: 891899
41. Brookhart MA, Schneeweiss S. Preference-based instrumental variable
methods for the estimation of treatment effects: assessing validity and in-
terpreting results. Int J Biostat 2007; 3: 14
42. Garabedian LF, Chu P, Toh S et al. Potential bias of instrumental variable
analyses for observational comparative effectiveness research. Ann Intern
Med 2014; 161: 131138
Received for publication: 23.3.2015; Accepted in revised form: 9.7.2015
and secondary diagnosis of CKD and ESRD were included
using the Nationwide In-Patient Sample. We aimed to compare
the following TIA-related outcomes between CKD and ESRD
patients: (i) degree of disability (mainly functional status) de-
rived from discharge destination, (ii) length of stay, (iii) charges
of hospitalization, and (iv) mortality. The comparisons of TIA-
related mortality and discharge outcomes between CKD and
ESRD were analyzed after adjusting for potential confounders
using logistic regression analysis. We adjusted for age, sex, co-
morbidities, hospital size and hospital teaching status.
128
Results. A total of 18 316 dialysis and 67 256 CKD patients were
admitted with TIA in the study period (200511). On univariate
analysis, there was no difference in the rates of moderate-to-
severe disability (20.5% versus 20.2%, P = 0.7) and in-hospital
mortality (0.4% versus 0.2%, P = 0.07) in ESRD patients com-
pared with those with CKD. After adjusting for age, sex and po-
tential confounders, ESRD patients with TIA had higher odds of
moderate-to-severe disability at discharge [odds ratio (OR): 1.53,
95% condence interval (CI): 1.371.71, P 0.0001] and in-
hospital death (OR: 2.87, 95% CI: 1.296.37, P = 0.009).
Conclusion. ESRD patients with TIA have signicantly higher
rates of moderate-to-severe disability at discharge and in-
hospital mortality when compared with the patients of other
stages of CKD who are not dialysis-dependent.
Keywords: chronic kidney disease, dialysis, transient ischemic
attack
INTRODUCTION
Patients with chronic kidney disease (CKD) and end-stage renal
disease (ESRD) requiring maintenance dialysis are at a higher
risk of cerebrovascular diseases than the general population
[1]. Transient ischemic attack (TIA) is a clinical diagnosis de-
ned by an acute transient episode of neurologic dysfunction
caused by the focal brain spinal cord or retinal ischemia, with-
out acute infarction [2]. TIA is an important predictor of stroke
and subsequent death within the next 3 months and thereafter
[35]. According to one population level study, the risk of
stroke within 2 days is 5% after an episode of TIA [6]. Another
study from the same data set has shown that the in-hospital
mortality after TIA in the general population during the years
200608 was 0.4% [7]. In another population level study [8],
renal failure was associated with a higher length of stay (OR: 1.5,
95% CI: 1.41.5, P < 0.0001) in TIA patients. However, this
study did not elaborate on the duration of renal failure or
dialysis status. Overall, there is a paucity of data regarding the
in-hospital outcomes of TIA in patients with CKD and ESRD.
We aimed to study (i) degree of disability mainly functional
status derived from discharge destination, (ii) length of stay,
(iii) charges of hospitalization, and (iv) mortality, by using
the Nationwide Inpatient Sample (NIS) for TIA patients with
CKD and ESRD.
M AT E R I A L S A N D M E T H O D S
We used the data les from NIS from 2005 to 2011 for our
analysis. A comprehensive synopsis on NIS data is available
at http://www.hcup-us.ahrq.gov.
The Medicare severity diagnosis-related group (DRG) code
524 was used to identify the patients admitted with TIA between
2005 and 2007 and DRG code 069 for 200811 period. The diag-
nosis of TIA was further conrmed by International Classication
of Diseases, Ninth Revision, Clinical Modication (ICD-9-CM)
435 either as primary or secondary discharge diagnosis. We
used ICD-9-CM secondary diagnosis codes of CKD III (585.3),
IV (585.4), V (585.5) and unspecied (585.9) in the CKD
Transient ischemic attack in chronic kidney disease and maintenance dialysis patients
group. Maintenance dialysis status was dened as patients with
an ICD-9-CM code for ESRD (585.6) or procedure code for
hemodialysis (39.95) or peritoneal dialysis (54.98), but absence
of ICD-9-CM code for acute kidney injury (584.X). ICD-9-CM
codes 584.X have >90% sensitivity and negative predictive value
for acute kidney injury [9]. We excluded patients with renal trans-
plant (V42.0 and 996.81). We divided TIA patients into two
groups: CKD and ESRD requiring dialysis. We further compared
the outcomes in each group with the general population, that is,
population with no documented kidney disease. Study variables
included were patients age, gender, race/ethnicity and co-
morbidities obtained from AHRQ co-morbidity data les includ-
ing congestive heart failure, diabetes mellitus, hypertension, alco-
hol abuse and chronic lung disease. We used ICD-9-CM
secondary diagnosis codes to identify co-morbidity atrial brilla-
tion (427.30 and 427.31), dyslipidemia (272.0272.9), stroke
(430434 and 436437) and nicotine dependence (305.1).
ICD-9-CM secondary diagnosis codes were used to identify
those with TIA-associated complications such as pneumonia
(486, 481, 482.8 and 482.3), sepsis (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), pulmonary embolism
(415.1), gastrointestinal hemorrhage (578) and myocardial infarc-
tion (410.0410.9). We also used ICD-9-CM procedure codes to
estimate the percentage of TIA patients who underwent related
ORIGINAL ARTICLE
procedures such as cerebral angiography (88.41), mechanical ven-
tilation (9672), transfusion (99.04), intubation (96.04), gastros-
tomy (431.1431.9) and thrombolytic administration (99.10).
The admitting hospitals were classied as teaching or non-
teaching and were further characterized into small, medium and
large on the basis of available hospital beds. Outcome measures in-
cluded discharge disposition and hospital charges. Discharge dis-
position is categorized into routine, home healthcare, short-term
hospital and other facility including intermediate care and skilled
nursing home or death in the NIS data les. We categorized rou-
tine discharge as none or minimal disability, any other discharge
status as moderate-to-severe disability as previously described [10].
Statistical analysis
The SAS 9.3 software (SAS Institute, Cary, NC, USA) was
used to convert the NIS database data into weighted counts to
generate national estimates, following Healthcare Cost and
Utilization Project recommendations. We performed univari-
ate analysis, chi-square for categorical variables and t-test for
continuous variables to identify differences in study variables
and end points between two groups ( patients with ESRD and
CKD) and to do comparison with the general population. We
also performed multivariate logistic regression analysis to assess
the outcome of patients with ESRD and CKD. Two logistic re-
gression models were created. Model 1 included all patients,
and stepwise logistic regression analysis was used to identify
the association between ESRD and odds of in-hospital mortal-
ity. Model 2 included patients who were discharged alive and
logistic regression analysis was used to identify the association
between ESRD and odds of moderate-to-severe disability. Lo-
gistic regression model was adjusted for age (as a continuous
variable), sex (as a categorical variable), and confounding fac-
tors. Confounding factors were dened as all the factors
129
 signicant in univariate analysis based on a type-I error of 0.05. Table 1. Patients demographic and clinical characteristics, in-hospital
Similar methodology was used to compare the outcomes of TIA procedures, hospital characteristics and discharge outcomes of TIA
patients with ESRD and CKD.
in CKD and ESRD patients with the general population.
TIA P-value
ESRD CKD
R E S U LT S Overall number (%) 18 316 67 256
Age mean (SD) 68 28 77 26 <0.0001
A total of 18 316 ESRD and 67 256 CKD patients were admitted Women 9931 (54.2) 33 461 (49.8) <0.0001
with TIA in the study period ( 20052011). Patients with CKD Race/ethnicity
were older (mean age 77 26 versus 68 28, P 0.0001). Dia- White 7273 (47.8) 40 736 (72.1) <0.0001
lysis patients had a higher percentage of women than non- African Americans 4981 (32.7) 9912 (17.5)
Hispanic 2105 (13.8) 3505 (6.2)
dialysis patients (54.2 versus 49.8%, P 0.0001). Co-morbid Other 872 (5.7) 2403 (4.2)
conditions such as hypertension and diabetes mellitus were sig- Co-morbid conditions
nicantly higher in ESRD patients (Table 1). Prevalence of at- Hypertension 17 126 (93.5) 59 943 (89.1) <0.0001
rial brillation, dyslipidemia, congestive heart failure, chronic Diabetes mellitus 6017 (33.0) 20 732 (30.8) 0.03
lung disease, history of stroke and alcohol abuse were higher Atrial brillation 2643 (14.4) 14 463 (21.5) <0.0001
Dyslipidemia 1332 (7.2) 6515 (9.7) <0.0001
in the CKD patients. Moreover, in-hospital complications Congestive heart failure 3443 (18.8) 13 506 (20.1) 0.09
such as deep venous thrombosis and sepsis were seen in a high- Chronic lung disease 2739 (15.0) 12 461 (18.5) <0.0001
er percentage age for patients with ESRD (Table 1), and they Stroke 1712 (9.3) 7979 (11.9) <0.0001
were also more likely to receive procedures such as intubation. Nicotine dependence 862 (4.7) 3884 (5.8) 0.007
Average length of stay (4 6 versus 3 5, P 0.0001) and Alcohol abuse 147 (0.8) 790 (1.2) 0.03
In-hospital complications
mean hospital charges ($24 386 49 136 versus $19 075 32 Pneumonia 257 (1.4) 1019 (1.5) 0.6
076, P 0.0001) were higher in patients with ESRD when com- Deep venous thrombosis 110 (0.6) 72 (0.1) 0.0001
pared with those with CKD. Pulmonary embolism 5 (0.03) 60 (0.1) 0.1
On multivariate analysis, patients with ESRD had higher Sepsis 137 (0.7) 122 (0.2) 0.0002
Myocardial infarction 179 (1.0) 463 (0.70) 0.10
ORIGINAL ARTICLE

odds of moderate-to-severe disability (OR: 1.53, 95% CI:

Gastrointestinal bleeding 77 (0.4) 408 (0.6) 0.1
1.371.71, P 0.0001), and in-hospital mortality (OR: 2.87, In-hospital procedure
95% CI: 1.296.37, P 0.009) after adjusting with potential Cerebral angiography 825 (4.5) 2559 (3.8) 0.10
confounders (Table 2). Thrombolytic therapy 19 (0.1) 48 (0.07) 0.6
We performed a sub-analysis of the TIA outcomes compar- Gastrostomy 35 (0.2) 70 (0.1) 0.2
ing CKD stages 3, 4, and 5 with each other. We did not nd any Mechanical ventilation 14 (0.1) 19 (0.02) 0.30
Intubation 75 (0.4) 89 (0.1) 0.01
difference in mortality or disability based on the stages of CKD. Transfusion 431 (2.4) 1413 (2.1) 0.40
Odds of death (OR: 3.95, 95% CI: 2.017.78, P 0.0001) and Hospital bed size
moderate-to-severe disability (OR: 1.82, 95% CI: 1.652.01, Small 1429 (7.9) 8643 (13.0) <0.0001
P 0.0001) were signicantly higher in ESRD patients than Medium 4599 (25.2) 16 443 (24.7)
the general population. We did not observe any difference in Large 12 159 (66.9) 41 619 (62.3)
Hospital teaching status
the TIA-related mortality between CKD patients and the gen- Non-teaching 9945 (54.7) 40 539 (60.8) <0.0001
eral population. However, rates of moderate-to-severe disability Teaching 8243 (45.3) 26 165 (39.2)
were higher in the CKD patients than the general population Length of stay mean (SD) 46 35 <0.0001
[OR: 1.82, 95% CI: 1.652.01, P 0.0001) (Table 3). Hospital charges $ mean 24 386 49 136 19 075 32 076 <0.0001
(SD)
Discharge disposition
None-to-minimal 14 489 (79.1) 53 421 (79.5) 0.7
DISCUSSION disability
Moderate-to-severe 3752 (20.5) 13 613 (20.2) 0.7
Our study identied that ESRD patients with TIA had more in- disability
hospital complications, higher odds of moderate-to-severe dis- In-hospital mortality 75 (0.4) 152 (0.2) 0.07
ability and in-hospital mortality when compared with those NIS 200511.
SD, standard deviation.
with CKD and the general population. ESRD patients also had
higher cost and length of hospitalization than the CKD patients.
CKD and ESRD patients are at an increased risk of cerebro- cannot be ascertained with condence from the data if this stroke
vascular events [1]. Neurologic symptoms can also occur due to represented a new complication or represented a previous stroke
metabolic complications resulting in missing or over diagnosing episode. These ndings warrant further investigation.
TIA. TIA is a future predictor of stroke in the general population Only 63% of the patients with TIA are hospitalized in the
[5]. However, data regarding TIA as a predictor of stroke in pa- USA [7], and some of these patients are managed in the emer-
tients with kidney dysfunction are lacking. In our study, 9.3% of gency room or TIA clinics. The decision about admission of
ESRD patients and 11.9% of CKD patients had a mention of these patients is based on multiple factors including the
stroke as a secondary diagnosis. It is plausible that TIA pro- ABCD2 score [11]. However, this score is not validated for
gressed to stroke within the same hospitalization. However, it patients with CKD and ESRD. Our data show that ESRD

130 F. Saeed et al.

Table 2. Effect of ESRD on outcomes of TIA patients

Outcomes Unadjusted Adjusted for age and gender Adjusted for age, gender and
potential confoundersa

Odd ratio (95% CI) P-value Odd ratio (95% CI) P-value Odd ratio (95% CI) P-value
Model 1 Analysis comprising all patients
Discharged alive Reference Reference Reference
In-hospital mortality 1.83 (0.973.52) 0.07 2.74 (1.335.61) 0.007 2.84 (1.356.35) 0.009
Model 2 Analysis comprising alive patients
None-to- minimal disability Reference Reference Reference
Moderate-to-severe disability 1.04 (0.921.14) 0.7 1.42 (1.351.66) <0.0001 1.54 (1.321.73) <0.0001
Race/ethnicity, hypertension, diabetes, atrial brillation, dyslipidemia, chronic lung disease, nicotine dependence, alcohol abuse, stroke, hospital bed size and hospital teaching status.
a

OR, odds ratio; CI, condence interval.

Table 3. Disability and mortality in ESRD and CKD patients in comparison with the general population

ESRD/CKD versus general population ESRD/CKD (%) General P-value Adjusted for age, gender and potential
population (%) confoundersa

Odd ratio (95% CI) P-value

ESRD versus general population
Mortality 0.4 0.09 <0.0001 3.95 (2.017.78) <0.0001
Moderate-to-severe disability 20 13 <0.0001 1.82 (1.652.01) <0.0001
CKD versus general population
Mortality 0.2 0.09 <0.0001 1.30 (0.82.0) 0.2
Moderate-to-severe disability 20 13 <0.0001 1.82 (1.652.01) <0.0001
a
Variables signicant in univariate analysis.

patients have a higher incidence of in-hospital complications
and suggest that ESRD patients presenting with TIA may war-
rant inpatient admission due to their higher rates of complica-
tions rather than outpatient or emergency room management.
We observed more in-hospital complications such as DVT
and sepsis in ESRD patients. These ndings warrant clinicians
to pay particular attention to the DVT prophylaxis, and symp-
toms such as fever, chills, constitutional symptoms or signs
such as catheter site erythema to prevent infection-related com-
plications. In our observational cohort, ESRD patients also had
a higher mean length of stay when compared with those with
CKD. This could also be explained by higher in-hospital com-
plications observed in the ESRD group. We also acknowledge
that the social situation (such as socioeconomic status and
marital status) of an individual patient may also have affected
the length of hospital stay and discharge destination and cannot
be accounted for in our analysis.
ESRD patients also had higher mean hospital charges pre-
sumably due to a more complicated hospital course. However,
these ndings need to be interpreted with the understanding
that in this data set total hospitalization charges represent
the amount that hospitals billed for services, but not how
much hospital services actually cost or the specic amounts re-
ceived in reimbursement. These charges, therefore, include
hospital overhead costs, charity care and bad debt, among
other costs, but do not include physicians professional fees.
The mean hospital charges were derived without any adjust-
ment for ination.
In our analysis, higher odds of disability and mortality were
observed after the adjustment of confounders. We report the
degree of disability derived from the discharge destination
ORIGINAL ARTICLE
(e.g. patients who were discharged to nursing homes were
deemed to have moderate-to-severe disability and those going
home were categorized to have none-to-minimal disability).
This methodology is well supported by the previous literature
[12]. We cannot infer from this data set if the patients with
ESRD were more disabled at baseline.
Interestingly, TIA-related mortality was similar in CKD
patients and the general population. However, higher odds of
disability were seen in the CKD group. There was no difference
in mortality and disability among different stages of CKD.
While it is plausible that CKD patients may be prone to a stroke
transformation after a TIA episode, our ndings need further
studies to identify a precise mechanistic explanation. ICD-9
codes for CKD are very specic but less sensitive and may have
inuenced the results as well [17]. Odds of disability and mortality
were much higher in the ESRD group than the general popula-
tion. These are novel ndings, and to our knowledge, they have
not been reported previously. Higher chances of TIA-related mor-
tality and disability in ESRD patients warrant an in-patient admis-
sion rather than an emergency room/TIA clinic management. It
should be noted that we have intentionally excluded patients with
acute kidney injury from our analysis to increase the reliability of
CKD and ESRD codes. In our previously published study [13],
TIA patients with AKI had higher odds of moderate-to-severe
disability (OR: 1.3, 95% CI: 1.21.4, P < 0.0001) and death (OR:
4.2, 95% CI: 3.06.1, P < 0.0001) when compared with patients
without acute kidney injury.
Our study is observational and based on the NIS data set.
Limitations of the NIS data set have been described previously
[14]. This data set depends on the accuracy of diagnoses and
procedure codes. In a previous study, sensitivity and positive

Transient ischemic attack in chronic kidney disease and maintenance dialysis patients 131
 predictive values for primary diagnosis of ICD-9-CM code 435,
TIA, were 75 and 80%, respectively [15]. A small proportion of
patients with TIA mimics are coded as TIA. The DRG system
has been used in previous studies pertaining to costs and length
of stay of stroke patients [16]. We think that using a combin-
ation of DRG and ICD-9-CM codes would result in higher ac-
curacy for TIA patient identication. Our study has several
limitations that are inherent to administrative data sets [10].
The specicity of administrative codes for CKD [17] is 93%
with a median of 98%. Negative predictive values are also gen-
erally high, that is, a median of 84%. Sensitivity of CKD codes is
low; (median, 41%; range, 388%). ICD-9 codes of AKI have
high specicity , making our data more accurate, although it
may underestimate the prevalence of CKD. Our study was
able to assess only in-hospital outcomes. Long-term outcomes
could be extrapolated from discharge destination as it strongly
correlates with modied Rankin scale at 3 and 12 months [18].
In summary, we observed higher odds of moderate-to-severe
disability and in-hospital mortality among TIA patients with
ESRD. Our ndings suggest having a lower threshold to admit
ESRD and CKD patients presenting with TIA as they are more
likely to have a complicated disease course than the general
population.
C O N F L I C T O F I N T E R E S T S TAT E M E N T
ORIGINAL ARTICLE
Prior publication in any form: none.
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Received for publication: 19.1.2015; Accepted in revised form: 13.5.2015
F. Saeed et al.