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Current Neurovascular Research, 2019, 16, 166-172

RESEARCH ARTICLE
ISSN: 1567-2026
eISSN: 1875-5739

Association between Blood Urea Nitrogen-to-creatinine Ratio and Three-

Impact
Factor:
1.811

Month Outcome in Patients with Acute Ischemic Stroke

BENTHAM
SCIENCE

Linghui Deng1,#, Changyi Wang1,#, Shi Qiu2,3,#, Haiyang Bian4, Lu Wang1, Yuxiao Li1, Bo Wu1,*
and Ming Liu1,*

1
Department of Neurology, Center of Cerebrovascular Diseases, West China Hospital, Sichuan University, Chengdu,
Sichuan, P.R. China; 2Department of Urology, Institute of Urology, West China Hospital, Sichuan University, Chengdu,
Sichuan, P.R. China; 3Center of Biomedical Big Data, West China Hospital, Sichuan University, Chengdu, Sichuan,
P.R. China; 4Department of Epidemiology and Biostatistics, School of Public Health, Peking University, Beijing, P.R.
Current Neurovascular Research

China

  Abstract:
  Background: Hydration status significantly affects the clinical outcome of acute
A R T I C L E H I S T O R Y
Received: October 20, 2018
Revised: March 05, 2019
Accepted: April 26, 2019
DOI:
10.2174/1567202616666190412123705
  with the three-month outcome (OR 1.02, 95% CI 1.00-1.03, p=0.04). However, after adjusting for
ischemic stroke (AIS) patients. Blood urea nitrogen-to-creatinine ratio (BUN/Cr) is a biomarker of
hydration status. However, it is not known whether there is a relationship between BUN/Cr and
three-month outcome as assessed by the modified Rankin Scale (mRS) score in AIS patients.
Methods: AIS patients admitted to West China Hospital from 2012 to 2016 were prospectively and
consecutively enrolled and baseline data were collected. Poor clinical outcome was defined as
three-month mRS > 2. Univariate and multivariate logistic regression analyses were performed to
determine the relationship between BUN/Cr and three-month outcome. Confounding factors were
identified by univariate analysis. Stratified logistic regression analysis was performed to identify
effect modifiers.
Results: A total of 1738 patients were included in the study. BUN/Cr showed a positive correlation
potential confounders, the correlation was no longer significant (p=0.95). An interaction between
BUN/Cr and high-density lipoprotein (HDL) was discovered (p=0.03), with a significant correla-
tion between BUN/Cr and three-month outcome in patients with higher HDL (OR 1.03, 95% CI
1.00-1.07, p=0.04).
Conclusion: Elevated BUN/Cr is associated with poor three-month outcome in AIS patients with
high HDL levels.

Keywords: Acute Ischemic Stroke, blood urea nitrogen, creatinine, high-density lipoprotein, modified ranking scale (mRS),
therapeutics, score.

1. INTRODUCTION Recent studies indicate that hydration status significantly

affects AIS patient outcomes [3, 4]. As a biomarker of hy-
Acute ischemic stroke (AIS) is a major cause of death dration status, the prognostic value of blood urea nitrogen-
and disability worldwide and poses a significant socioeco-
to-creatinine ratio (BUN/Cr) in AIS has been discussed in
nomic burden [1]. In the United States, the cost of hospitali-
several studies [5-7]. One study found that elevated BUN/Cr
zation for ischemic stroke is approximately $20,000 per per-
in AIS patients was associated with poor 30-day outcomes
son, without considering the expenses for stroke care [2].
(death or placement in a nursing home) [7]. A second study
Identifying AIS patients at high risk of poor outcome and
suggested that BUN/Cr-based hydration therapy was linked
adjusting therapeutic strategies accordingly are therefore of to favorable three-month outcome after AIS onset [6]. Few
great priority.
studies have investigated the association between BUN/Cr
and functional outcomes as assessed by the modified ranking
*Address correspondence to these authors at the  Department of Neurology,
scale (mRS) score.
West China Hospital, No. 37 Guoxue Alley, Chengdu, 610041 Sichuan,
P.R. Chinal; E-mails: wyplmh@hotmail.com; dragonwb@126.com In the current study, we explored the association between
#
These authors contributed equally to this work. BUN/Cr and three-month mRS outcomes in AIS patients.
 

1875-5739/19 $58.00+.00 © 2019 Bentham Science Publishers

Association Between Blood Urea Nitrogen-to-creatinine Ratio
Fig. (1). Flowchart for the selection of the study population.
Abbreviations: BUN, blood urea nitrogen; Cr, creatinine.
2. MATERIALS AND METHODS
2.1. Study Population
From January 2012 to December 2016, we prospectively
and consecutively enrolled first-ever ischemic stroke patients
admitted to the Department of Neurology of West China
Hospital, Sichuan University (Chengdu, China) within 7
days of onset. We included patients with a clinical diagnosis
of AIS confirmed by computed tomography or magnetic
resonance imaging. We extracted patient data from the
Chengdu Stroke Registry in conformity with local and inter-
national ethical criteria. Patients were excluded if they were
younger than 18 years, had primary subarachnoid hemor-
rhage, intracerebral hemorrhage, severe liver disease or end-
stage renal disease. Patients with missing BUN or Cr values
were excluded. The study was approved by the Ethics Com-
mittee of the Scientific Research Department of West China
Hospital.
2.2. Data Collection
Patient demographics, interval between stroke onset and
admission, and baseline National Institutes of Health Stroke
Scale (NIHSS) score were collected on admission. Risk fac-
tors for stroke were also collected, including diabetes, hyper-
tension, atrial fibrillation, dyslipidemia, smoking, and alco-
hol consumption. Patient blood samples were obtained
within 24 hours of admission. Laboratory data including
blood platelet count, serum albumin, BUN, Cr, triglycerides
(TG), cholesterol, high-density lipoprotein (HDL) and low-
density lipoprotein were determined with an AU-5400 auto-
matic analyzer (Olympus, Tokyo, Japan). Diabetes, hyper-
tension, and dyslipidemia were defined as an evident history
of disease based on a patient interview or diagnosis during
current treatment in hospital [8]. Atrial fibrillation was de-
fined as a history of persistent atrial fibrillation or paroxys-
mal atrial fibrillation, supported by past electrocardiograms
or electrocardiography during admission [9]. Three months
after stroke onset, well-trained neurologists used mRS to
Current Neurovascular Research, 2019, Vol. 16, No. 2 167
evaluate patient outcomes through follow-up on telephone.
Poor clinical outcome was defined as three-month mRS>2
[10].
2.3. Statistical Analysis
For continuous variables, results were analysed as means
± standard deviations, while categorical variables were
evaluated as frequencies or percentages. Statistical differ-
ences were determined by one-way ANOVA or Kruskal
Wallis H test for continuous variables, while the chi-squared
test was used for categorical variables. Where appropriate,
odds ratios (ORs) and 95% confidence intervals (CIs) were
reported. Subjects were grouped into tertiles according to
BUN/Cr levels. Multiple logistic regression analysis was
conducted to evaluate the association between BUN/Cr and
three-month outcome. Based on the guidelines in the
Strengthening the Reporting of Observational Studies
(STROBE) statement [11], we simultaneously performed
non-adjusted and multivariable-adjusted analysis. We de-
cided to adjust by one covariate if it altered the matched
odds ratio by at least 10% when added to the model [12], and
if variables were associated with p<0.1 in the univariate
analysis. Stratified logistic regression was used to perform
subgroup analyses. The likelihood ratio test was used to
evaluate modification and interaction of subgroups. Based on
previously published reference values [13, 14], we divided
subjects into three groups (low, normal, and high) along each
of the following variables: blood platelet count, serum albu-
min level, and HDL level.
A generalized additive model was used to explore a po-
tential non-linear relationship between BUN/Cr and out-
come. After a non-linear correlation was discovered, a two-
piecewise regression was conducted to identify whether the
relationship between BUN/Cr and three-month outcome
showed a threshold effect and to calculate the inflection
point [15]. The significance of interaction (p-interaction) was
tested using the likelihood ratio test. Trends across patient
tertiles (p for trend) were tested by entering the median value
of BUN/Cr in each tertile as a continuous variable in the
models [16]. Statistical analyses were carried out using the
software packages R (http://www.R-project.org, R Founda-
tion for Statistical Computing, Vienna, Austria) and Em-
powerStats (http://www.empowerstats.com, X&Y Solutions,
Boston, MA, USA). A 2-sided p<0.05 was identified as sta-
tistically significant.
3. RESULTS
3.1. Study Participants and Baseline Characteristics
Between January 2012 and December 2016, a total of
3458 AIS patients were evaluated for eligibility. Of those,
1720 patients were excluded and 1738 subjects were in-
cluded in the study. The flowchart for patient selection is
described in Fig. (1). Baseline characteristics of the study
population are shown in Table 1. Compared to patients in the
highest BUN/Cr tertile (T3), patients with intermediate (T2)
and low (T1) BUN/Cr levels were younger and were mostly
males, and they presented lower NIHSS scores, lower fre-
quency of atrial fibrillation history, and lower levels of
BUN, Cr, and HDL on admission. Conversely, they showed
higher rates of smoking and alcohol consumption.
168 Current Neurovascular Research, 2019, Vol. 16, No. 2 Deng et al.

Table 1. Patient characteristics, stratified by blood urea nitrogen-to-creatinine ratio (BUN/Cr).

Patient Characteristics BUN/Cr tertile

- T1 T2 T3

- (3.72-14.50) (14.51-19.13) (19.13-83.59)

Variable n=578 n=580 n=580 p-value

Age, years, mean (SD) 59.96 (14.56) 63.24 (13.96) 64.92 (13.06) <0.01*

Male, n (%) 438 (75.78) 369 (63.62) 240 (41.38) <0.01*

Interval between symptom onset and admission, h, mean

60.90 (47.73) 60.05 (48.94) 62.87 (51.11) 0.61
(SD)  

Baseline NIHSS score, median (Q1-Q3) 3 (2-8) 5 (2-9) 5 (2-10) <0.01*

Blood platelet count, x109/L, mean (SD) 173.33 (69.14) 165.83 (60.51) 168.80 (64.37) 0.14

Serum albumin, g/L, mean (SD) 40.84 (4.53) 41.00 (4.48) 40.45 (4.66) 0.11

BUN, mg/dL, mean (SD) 12.63 (6.46) 15.35 (4.52) 19.65 (6.55) <0.01*

Cr, mg/dL, mean (SD) 1.09 (0.70) 0.92 (0.27) 0.81 (0.27) <0.01*

Triglycerides, mmol/L, mean (SD) 1.64 (1.16) 1.60 (1.06) 1.55 (1.12) 0.38

Total cholesterol, mmol/L, mean (SD) 4.41 (1.11) 4.44 (1.13) 4.43 (1.10) 0.90

High-density lipoprotein, mmol/L, mean (SD) 1.27 (0.38) 1.29 (0.38) 1.32 (0.41) 0.04*

Low-density lipoprotein, mmol/L, mean (SD) 2.60 (0.95) 2.66 (0.97) 2.59 (0.93) 0.46

Hypertension, n (%) 278 (48.10) 296 (51.03) 290 (50.00) 0.60

Diabetes, n (%) 89 (15.40) 112 (19.31) 119 (20.52) 0.06

Hyperlipidemia, n (%) 30 (5.19) 27 (4.66) 27 (4.66) 0.89

Atrial fibrillation, n (%) 25 (4.33) 45 (7.76) 64 (11.03) <0.01*

Alcohol consumption, n (%) 185 (32.01) 156 (26.90) 104 (17.93) <0.01*

Smoking, n (%) 249 (43.08) 211 (36.38) 145 (25.00) <0.01*

Three-month mRS, median (Q1-Q3) 1 (1-2) 1 (1-3) 1 (1-3) 0.41

Abbreviations: BUN: blood urea nitrogen, Cr: creatinine, NIHSS: National Institutes of Health Stroke scale, mRS: modified rankin scale, SD: standard deviation.

3.2. The Relationship Between BUN/Cr and Three-month
mRS
The BUN/Cr ratio was significantly associated with age,
sex, atrial fibrillation, smoking, blood platelet count, and
serum albumin in the univariate analysis (p<0.05; Table 1
Supplementary Materials). The interval between stroke onset
and admission, baseline NIHSS score, hypertension, diabe-
tes, dyslipidemia, alcohol consumption, triglycerides, and
HDL were found to be significant confounders because they
altered the matched odds ratio by at least 10% when added to
the model (data not shown).
Multiple logistic regression showed that BUN/Cr posi-
tively correlated with three-month mRS when considered as
a continuous variable (OR 1.02, 95% CI 1.00-1.03, p=0.04).
After adjusting by potential confounders, the correlation was
no longer significant (OR 1.00, 95% CI 0.98-1.02, p=0.95).
When BUN/Cr was considered as a categorical variable, the
OR of poor outcome was 1.12 for T2 and 1.33 for T3 com-
pared to T1 without adjustment (Table 2). After adjustment,
however, neither of these OR values reached statistical sig-
nificance.
3.3. The Non-linear Relationship Between BUN/Cr and
Three-month mRS
A non-linear relationship between BUN/Cr and three-
month mRS was observed (Suppl. Fig. 1). Using a two-
piecewise regression model, the inflection point was 18.78.
Relationships between BUN/Cr and three-month mRS were
not significant on either the left of the inflection point (OR
0.98, 95%CI 0.94-1.02, p=0.30) or the right side (OR 1.01,
95%CI 0.99-1.03, p=0.45) (Table 3).
Association Between Blood Urea Nitrogen-to-creatinine Ratio Current Neurovascular Research, 2019, Vol. 16, No. 2 169

Table 2. Multiple logistic regression analysis to assess the potential relationship between blood urea nitrogen-to-creatinine ratio
(BUN/Cr) and three-month modified Rankin Scale (mRS) score.

Non-adjusted Model Adjusted Model I a Adjusted Model II b

Variable
Odds Ratio (95% Confidence Interval), Odds Ratio (95% Confidence Interval), Odds Ratio (95% Confidence Interval),
p-value p-value p-value

BUN/Cr (continuous) 1.02 (1.00,1.03), 0.046 1.01 (0.99, 1.02), 0.41 1.00 (0.98, 1.02), 0.95

BUN/Cr, tertile - - -

T1 (1.39-5.44) Reference Reference Reference

T2 (5.44-7.17) 1.12 (0.86, 1.46), 0.40 1.02 (0.78, 1.34), 0.86 0.94 (0.71, 1.24), 0.66

T3 (7.17-31.35) 1.33 (1.02, 1.72), 1.03 1.14 (0.86, 1.50), 0.36 1.02 (0.77, 1.36), 0.87

p for trend 0.01 0.26 0.71

a
Adjusted model I: adjusted for age and sex.
b
Adjusted model II: adjusted for age, sex, interval between stroke onset and admission, baseline score on the National Institutes of Health Stroke Scale, hypertension, diabetes,
dyslipidemia, atrial fibrillation, smoking, alcohol consumption, platelet count, serum albumin, triglyceride, and high-density lipoprotein.
 
Table 3. Two-piecewise regression to assess whether blood urea nitrogen-to-creatinine ratio (BUN/Cr) and three-month modified
Rankin Scale (mRS) score are related via a threshold effect.

BUN/Cr Odds ratio (95% Confidence Interval) * p-value*

< 18.78 0.98 (0.94, 1.02) 0.30

> 18.78 1.01 (0.99, 1.03) 0.45

* Adjusted for age, sex, interval between stroke onset and admission, baseline score on the National Institutes of Health Stroke Scale, hypertension, diabetes, dyslipidemia, atrial
fibrillation, smoking, alcohol consumption, platelet count, serum albumin, triglycerides, and high-density lipoprotein.

3.4. HDL Level Affects the Relationship Between
BUN/Cr and Three-month mRS
Stratified logistic regression showed a significant interac-
tion between BUN/Cr and HDL (p for interaction=0.03)
(Table 4). The association between BUN/Cr and three-month
mRS was significant in patients with high HDL after adjust-
ment (OR 1.03, 95% CI 1.00-1.07, p=0.04). However, this
association was not significant in patients with low HDL
level (OR 0.99, 95% CI 0.95-1.02, p=0.41) or normal HDL
level (OR 0.98, 95% CI 0.95-1.01, p=0.15).
4. DISCUSSION
In our study, we investigated the relationship between
BUN/Cr and three-month outcome in AIS patients and found
that BUN/Cr positively correlated with three-month outcome
among AIS patients with high HDL level, after adjustment
for several confounders.
Dehydration is associated with reduced total plasma vol-
ume, decreased cardiac output, and increased blood viscosity
[5]. Early during stroke recovery, ischemia-related impair-
ment of the autoregulatory system makes the brain more
susceptible to changes in blood viscosity and pressure [17].
In this way, dehydration, which often results in decreased
brain perfusion and concomitantly decreased oxygen and
nutrients, can contribute to brain damage and influence clini-
cal outcomes [18]. In addition, several studies have shown
that brain perfusion after AIS is significantly associated with
patient outcomes [19]. These considerations mean that it is
reasonable to speculate that elevated BUN/Cr, which is
linked to poor hydration status, may be linked to poor out-
come in AIS patients.
Thirst is the main mechanism that prevents the body from
dehydration [20]. AIS patients are less likely to have ade-
quate fluid consumption due to dysphagia, physical limita-
tion, and loss of consciousness [21]. However, in our study
population, the median NIHSS score on admission was 4.
Our patients were highly likely being able to restore fluid
themselves. Sufficient fluid therapy after admission can im-
prove patient hydration status and clinical outcome [6], so
fluid therapy may help explain why we failed to observe a
significant relationship between BUN/Cr ratio and three-
month outcome in our patient population as a whole. Unfor-
tunately, we did not collect data on this parameter, so our
results should be verified in future work that explicitly con-
trols for this. Such work is important for addressing the
170 Current Neurovascular Research, 2019, Vol. 16, No. 2 Deng et al.

Table 4. Stratified logistic regression analysis to identify variables that modify the correlation between blood urea nitrogen-to-
creatinine ratio (BUN/Cr) and three-month modified Rankin Scale (mRS).

Characteristic Odds Ratio (95% Confidence Interval), p-value* p for Interaction*

Age, year - 0.92

<65 1.00 (0.98, 1.03), 0.88 -

≥65 1.01 (0.98, 1.02), 0.99 -

Sex - 0.38

female 1.01 (0.98, 1.03), 0.59 -

male 0.99 (0.96, 1.02), 0.49 -

Hypertension - 0.61

no 1.00 (0.97, 1.02), 0.73 -

yes 1.00 (0.98, 1.03), 0.72 -

Diabetes - 0.89

no 1.00 (0.98, 1.02), 0.95 -

yes 1.00 (0.96, 1.03), 0.90 -

Hyperlipidemia - 0.26

no 1.00 (0.98, 1.02), 0.85 -

yes 0.94 (0.84, 1.05), 0.29 -

Atrial Fibrillation - 0.35

no 1.00 (0.98, 1.02), 0.05 -

yes 1.03 (0.97, 1.08), 0.40 -

Alcohol consumption - 0.59

no 1.00 (0.98, 1.02), 0.09 -

yes 1.01 (0.97, 1.05), 0.07 -

Smoking - 0.60

no 1.00 (0.98, 1.02), 0.78 -

yes 0.99 (0.96, 1.03), 0.67 -

9
Blood platelet count, x10 /L** - 0.33

low (<150) 1.00 (0.97, 1.03), 0.79 -

normal (150, 400) 1.01 (0.98, 1.03), 0.71 -

a
high (≥400) - -

Serum albumin, g/L** - 0.76

low (<35) 1.03 (0.96,1.10), 0.39 -

normal (35, 50) 1.00 (0.98, 1.02), 0.94 -

high (≥50) a - -

High-density lipoprotein, mmol/L** - 0.03

low (<1.09) 0.99 (0.95, 1.02), 0.41 -

normal (1.09, 1.42) 0.98 (0.95, 1.01), 0.15 -

high (≥1.42) 1.03 (1.00, 1.07), 0.04 -

* Adjusted for age, sex, interval between stroke onset and admission, baseline score on the National Institutes of Health Stroke Scale, hypertension, diabetes, dyslipidemia, atrial
fibrillation, smoking, alcohol consumption, blood platelet count, serum albumin, triglycerides, and high-density lipoprotein.
** Patients were divided into three groups according to the reference values indicated in references [13, 14].
a
Sample size for high blood platelet count and serum albumin was too small to calculate the odds ratio and 95% confidence interval.
Note: In each stratification, the model was not adjusted for the stratification variable.
Association Between Blood Urea Nitrogen-to-creatinine Ratio
possibility that adequate fluid therapy can help improve
three-month outcome in AIS patients.
We found a significant interaction between BUN/Cr and
HDL since BUN/Cr positively correlated with three-month
outcome only in patients with high HDL level (OR 1.03,
95% CI 1.00-1.07, p=0.04). This correlation was not signifi-
cant in the tertiles with low HDL (p=0.41) or medium HDL
(p=0.15). High HDL level has been reported to correlate
with increased risk of poor outcome in AIS patients, which
may strengthen the effect of BUN/Cr on three-month out-
come [22]. Therefore, it was possible that we observed the
relationship between these two variables specifically in pa-
tients with high HDL level. However, other studies have
suggested that high HDL helps protect against poor stroke
outcomes [23-25]. Further investigations are warranted to
elucidate the interaction between BUN/Cr and HDL.
The validity of our conclusions is strengthened by the use
of a generalized additive model to clarify nonlinear relation-
ships, in addition to the generalized linear model; use of both
models can allow more comprehensive analysis of relation-
ships between exposure and outcome. Moreover, our analy-
sis of potential effect modifiers revealed an interaction be-
tween BUN/Cr and high HDL level.
This study presents some limitations, in addition to the
fact that we did not collect data on fluid therapy after admis-
sion. The study was performed at a single center, which may
limit the generalizability of our results to other geographic
regions and patient populations. In addition, the study did
not evaluate the mechanism underlying the interaction be-
tween BUN/Cr and HDL, which requires further investiga-
tion.
CONCLUSION
Elevated BUN/Cr is associated with poor three-month
clinical outcome in AIS patients with high HDL level. Moni-
toring of BUN/Cr may therefore be helpful identifying pa-
tients at high risk of poor outcome. Further studies will be
required to confirm these results and to elucidate the mecha-
nism underlying the interaction between BUN/Cr and HDL.
ETHICS APPROVAL AND CONSENT TO PARTICI-
PATE
The ethical approval was given by the Ethics Committee
of the Scientific Research Department of West China Hospi-
tal, P.R. China.
HUMAN AND ANIMAL RIGHTS
No animals were used for studies that are the basis of this
research. All the human procedures were followed in accor-
dance with the ethical standards of the committee responsi-
ble for human experimentation (institutional and national),
and with the Helsinki Declaration of 1975, as revised in
2013 (http://ethics.iit.edu/ecodes/node/3931).
CONSENT FOR PUBLICATION
Written informed consent was obtained from all partici-
pants.
Current Neurovascular Research, 2019, Vol. 16, No. 2 171
FUNDING
M. Liu and B. Wu obtained public funding. This study
was supported by National Natural Science Foundation of
China (81620108009, 81671146, 81870937), the Major
International (Regional) Joint Research Project, the
National Key Research and Development Program of
China, and Ministry of Science and Technology of China
(2016YFC1300500-505, 2017YFC0910004).
CONFLICT OF INTEREST
The authors declare no conflict of interest, financial or oth-
erwise.
ACKNOWLEDGEMENTS
M. Liu and B. Wu conceived and designed the study.
C.Y. Wang, L.H. Deng, S. Qiu, L. Wang and Y.X Li ac-
quired the data, which S. Qiu, H.Y. Bian and C.Y. Wang
analyzed. C.Y. Wang and L.H. Deng aided in data interpreta-
tion and wrote the manuscript. All authors were involved in
revising the article and approved the final version.
SUPPLEMENTARY MATERIAL
Supplementary material is available on the publisher’s
web site along with the published article.
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