J Med Ultrasonics (2016) 43:263270

DOI 10.1007/s10396-015-0680-y

ORIGINAL ARTICLE

Associations between increased renal resistive index

and cardiovascular events
Kaoru Komuro1 Noriko Yokoyama2 Misaki Shibuya2 Kazuyuki Soutome2
Masanori Hirose1 Kazuya Yonezawa3 Teisuke Anzai1

Received: 2 July 2015 / Accepted: 1 October 2015 / Published online: 22 October 2015
The Japan Society of Ultrasonics in Medicine 2015

Abstract
Background and purpose Chronic kidney disease is a risk
factor for cardiovascular disease (CVD). Renal resistive
index (RI) measured by Doppler ultrasonography is associated with renal impairment. We investigated the relationship between RI and cardiac function, and evaluated
the utility of RI for predicting cardiac events in patients
with CVD.
Methods and results Renal Doppler ultrasonography and
echocardiography were performed in a total of 452 patients
with CVD. Correlations of RI with serum creatinine and
& Kaoru Komuro
kkaoru@hnh.hosp.go.jp
Noriko Yokoyama
nfujikaw@hnh.hosp.go.jp
Misaki Shibuya
mshibuya@hnh.hosp.go.jp
Kazuyuki Soutome
ksoutome@hnh.hosp.go.jp
Masanori Hirose
mhirose@hnh.hosp.go.jp
Kazuya Yonezawa
kyonezaw@hnh.hosp.go.jp
Teisuke Anzai
tanzai@hnh.hosp.go.jp
1

Department of Cardiology, National Hospital Organization

Hakodate Hospital, 18-16 Kawahara, Hakodate,
Hokkaido 041-8512, Japan

Clinical Laboratory, National Hospital Organization

Hakodate Hospital, 18-16 Kawahara, Hakodate,
Hokkaido 041-8512, Japan

Department of Clinical Research, National Hospital

Organization Hakodate Hospital, 18-16 Kawahara, Hakodate,
Hokkaido 041-8512, Japan

estimated glomerular filtration rate (eGFR) were significant

but not strong (r = 0.37, p \ 0.001; r = -0.42,
p \ 0.001, respectively). RI correlated positively with age,
left atrial volume index, left ventricular mass index, and
early transmitral velocity to mitral annular early diastolic
velocity (e0 ) ratio (E/e0 ), and showed significant negative
correlations with e0 and diastolic blood pressure. Between
two subgroups112 patients hospitalized with cardiovascular events (Group A) and 200 age- and eGFR-matched
controls (Group B)RI was significantly higher in Group
A than in Group B, although age and eGFR were similar.
Conclusions RI reflects the impairment of intrarenal
hemodynamics that cannot be adequately elucidated by
eGFR alone. Assessment of renal RI may be useful in
conjunction with prognostic estimates for patients with
CVD.
Keywords Cardiovascular disease  Cardiac events 
Renal Doppler ultrasonography  Resistive index

Introduction
Recent studies have suggested that chronic kidney disease
(CKD) is a risk factor for cardiovascular disease (CVD) [1
4]. To improve the treatment and prognosis of CVD,
detection of subclinical renal damage relevant to CVD is
necessary. Renal Doppler sonography has been widely
applied to evaluate renal anatomical abnormalities and to
yield intrarenal hemodynamic information. Renal resistive
index (RI), measured from intrarenal arterial waveforms
recorded by renal Doppler sonography, reflects vascular
resistance in the kidney and is useful for evaluating renal
dysfunction caused by various renal diseases [59]. RI has
also been applied as a predictor of the progression of renal

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dysfunction [10] and poor allograft survival after renal

transplantation [11].
In the clinical setting, however, even when the renal
dysfunction denoted by serum creatinine (Cr) or estimated
glomerular filtration rate (eGFR) is only slight, we frequently encounter patients with higher RI who require
treatment for CVD. Previous studies have revealed that RI
correlates with markers of systematic atherosclerosis, such
as intima-media thickness (IMT) and pulse wave velocity
(PWV) [1214]. RI is also associated with left ventricular
(LV) diastolic dysfunction and can predict outcomes in
patients with heart failure with preserved ejection fraction
(EF) [15, 16]. These results suggest that renal vascular
resistance, as indicated by RI, can reflect the degree of
systemic atherosclerosis and target organ damage. However, the status of RI as a cardiovascular risk marker
remains unclear. The purpose of this study was, therefore,
to investigate the relationship between RI and cardiac
function and to evaluate the utility of renal RI as a predictor of outcomes in patients with CVD.

J Med Ultrasonics (2016) 43:263270

age- and eGFR-matched patients from the remaining 340

patients as controls.
The study protocol was approved by the ethics committee of our institution, and all subjects provided informed
consent prior to participating in this study.
Baseline clinical characteristics

Materials and methods

Blood samples were obtained within 2 days of ultrasonographic examination. Levels of total cholesterol, triglycerides, high- and low-density lipoprotein cholesterol
(HDL- and LDL-cholesterol, respectively), glucose,
hemoglobin (Hb)A1c, and Cr were determined. We calculated eGFR using the Japanese coefficient-modified
Chronic Kidney Disease Epidemiology Collaboration
equation. For females, the product of this equation was
multiplied by a correction factor of 0.742 [17]. Diabetes
mellitus (DM) was defined according to the criteria recommended by the American Diabetes Association by
fasting blood glucose or HbA1c, in addition to a medical
history of diabetes [18]. Hypercholesterolemia (HL) was
defined as LDL-cholesterol C140 mg/dl and a medical
history of HL.

Study subjects

Renal Doppler ultrasonography

Subjects were selected from among patients who underwent regular follow-up at the outpatient department of
National Hakodate Hospital as of September 2012 and who
had visited the Department of Cardiology and undergone
renal Doppler ultrasonography and echocardiography
between April 2009 and September 2010 for assessment of
CVD, chronic kidney disease, or secondary hypertension
(HT). In our laboratory, renal Doppler ultrasonography was
routinely conducted in patients with CVD to assess for
renal arterial stenosis and to evaluate for renal insufficiency
or atherosclerosis of the abdominal aorta. Renal Doppler
ultrasonography and echocardiography were performed on
the same day in each patient. Exclusion criteria included
absence of sinus rhythm, significant aortic valve regurgitation, and renal arterial stenosis. A total of 452 patients
were ultimately enrolled in the study. The patients were
divided into two subgroups. Group A was composed of 112
patients who experienced cardiovascular events, including
cardiac death, hospital admission for congestive heart
failure (CHF), acute coronary syndrome, worsening of
exertional angina, coronary revascularization [percutaneous coronary intervention (PCI) or coronary artery
bypass grafting (CABG)] due to coronary artery disease
(CAD), endovascular intervention therapy (EVT) due to
peripheral vascular disease, and stroke after the day of
ultrasonic examination. Group B was composed of 200

Renal Doppler ultrasonographic examinations were performed using commercially available ultrasound systems
(Vivid 7 ultrasonographic machine; GE Healthcare UK,
Little Chalfont, England) with a 2.5- to 3.75-MHz convex
or sector array transducer. With patients in the prone and
supine positions, the transducer was placed on the posterior and anterior approaches, respectively. Intrarenal segmental arteries were localized by color Doppler
sonography, and pulse Doppler signals were obtained
from these arteries (Fig. 1). Because clear signals need to
be obtained, segmental arteries were chosen. Peak systolic
flow velocity (PSV) and end-diastolic flow velocity
(EDV) of the segmental arteries were determined using
the angle correction menu of the apparatus (Fig. 2). RI
was defined as follows: (PSVEDV)/PSV. All velocities
were determined for each segmental artery and averaged
to obtain the mean value for each patient. In general, 0.70
is the upper threshold of normal RI in adults without renal
sufficiency [8]. All measurements were performed by
three experienced physicians who were blinded to the
clinical data of patients. The reproducibility of RI measurements from two investigators was assessed in a subgroup of 20 patients. Intra- and interobserver coefficients
of variation for measurements were 3.5 and 4.3 %,
respectively. Blood pressure was measured by renal
ultrasonography.

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265

volumes were also measured, and LAVI was calculated in

the same manner. LV inflow was recorded using the pulsed
Doppler method, and early diastolic peak velocity (E) was
measured. Mitral annular velocity was recorded using tissue Doppler imaging with the sample volume placed at the
septal and lateral sites of the mitral annulus in the apical
four-chamber view, and early diastolic peak annular
velocity (e0 ) was calculated and averaged to obtain the
mean value for each patient. The E/e0 ratio was calculated.
Statistical analysis

Fig. 1 Color Doppler imaging of the segmental artery in a healthy

subject (arrow)

Statistical analysis was performed with Statistical Package

for the Social Sciences (SPSS) software (SPSS, Chicago,
IL, USA). Continuous variables are expressed as
mean standard deviation. The relationship between
variables was assessed using linear regression analysis and
Pearsons correlation coefficient. Significant differences
between two groups were estimated using the unpaired
Students t test. For comparison of the frequency of risk
factors, the Chi square method was used. A statistical
significance threshold of 0.05 was applied throughout.

Echocardiography
Echocardiography was performed using the same machine
as that for renal ultrasonographic examination with an M4S
transducer. LV end-diastolic dimension (LVDd) was
measured from a parasternal long-axis B-mode image.
Thicknesses of the interventricular septum (IVS) and LV
posterior wall (LVPW) were measured on parasternal
short-axis images at the level of the chordae tendinae in
end-diastole. LV mass index (LVMI) was calculated from
LVDd, IVS, and LVPW using a standard formula, in
accordance with the methods of the American Society of
Echocardiography [19]. LV end-diastolic and end-systolic
volumes were measured from apical four- and two-chamber images using the biplane method of disks, and EF was
calculated. Left arterial (LA) end-systolic and end-diastolic

Results
Baseline clinical characteristics of all study patients are
summarized in Table 1. Mean age was 69 13 years
(range 1596 years), and 42 % were female. Clinical
indications for consultation with the Department of Cardiology were CAD (41.8 %), peripheral vascular disease
(9.5 %), CHF (12.8 %), arrhythmia (7.1 %), myopathy
(4.9 %), CKD (15.7 %), valvular heart disease (4.4 %),
and stroke (2.9 %). HT was present in 65.2 % of patients,
HL in 36.9 %, and DM in 25.2 %. Some patients had
multiple conditions. Furthermore, 38.7 % of patients were
receiving an angiotensin-converting enzyme inhibitor
(ACE) or reninangiotensin system inhibitor (ARB),

Fig. 2 Normal intrarenal

Doppler spectrum of the
segmental artery from the
kidney in a healthy subject.
Resistive index is defined as
(PSVEDV)/PSV. PSV peak
systolic velocity (cm/s), EDV
end-diastolic velocity (cm/s)

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Table 1 Baseline clinical characteristics of all study subjects

Variables

Total

Table 2 Correlation between RI and biochemical variables,

echocardiographic parameters and clinical characteristics of all
subjects
Variables

452

Age (years)

69 13

Gender (male/female)

260/192

Systolic blood pressure (mmHg)

136 21

Diastolic blood pressure (mmHg)

78 14

Serum creatinine (mg/dl)

0.9 0.3

eGFR (ml/min/1.73 m2)

68.7 21.2

Total cholesterol (mg/dl)

142.2 95.2

HDL-cholesterol (mg/dl)

54.6 15.5

LDL-cholesterol (mg/dl)

105.0 29.3

Triglycerides (mg/dl)
Hemoglobin A1c (%)

142.2 95.2
5.5 0.8

Hypertension (%)

65.2

Hyperlipidemia (%)

36.9

Diabetes (%)

25.2

eGFR estimated glomerular filtration rate, HDL-cholesterol highdensity lipoprotein cholesterol, LDL-cholesterol low-density
lipoprotein cholesterol

40.5 % were receiving calcium channel blockers, 28.8 %

were receiving b-blockers, and 16.8 % were receiving
diuretics.
We examined correlations between RI and biochemical
variables of renal function associated with risk factors for
arteriosclerosis and LV systolic and diastolic function in all
subjects (Table 2). Although RI showed a significant positive correlation with Cr and a negative correlation with
eGFR, these correlations were not strong (r = 0.37,
p \ 0.001; r = -0.42, p \ 0.001, respectively). Many
subjects showed high RI despite low Cr (Fig. 3). RI correlated positively with age (r = 0.50, p \ 0.001), LAVI
(r = 0.45, p \ 0.001), and LVMI (r = 0.30, p \ 0.001). A
significant negative correlation was identified between RI
and e0 (parameter of LV diastolic function), and a positive
correlation was seen between RI and E/e0 (LV filling
pressure) [20]. On the other hand, RI did not correlate
significantly with parameters of LV systolic function, such
as LVEF or LVDd. RI did not correlate with systolic blood
pressure, but showed a relatively strong positive correlation
with diastolic blood pressure.
To clarify whether RI represents an index that is useful
for predicting events independent of renal function and age,
we compared our data against those from age- and eGFRmatched control subjects (Table 3). Patients were categorized into two groups: patients with cardiovascular events
(Group A) and age- and eGFR-matched controls (Group
B). Group A included four patients who experienced cardiac death, 40 patients requiring hospital admission for
CHF, seven patients with acute coronary syndrome, 22

123

Age

0.50

\0.001

Serum creatinine

0.37

\0.001

-0.42
0.41

\0.001
\0.001

eGFR
Left atrial volume index
Left ventricular diastolic dimension
Left ventricular ejection fraction
Left ventricular mass index
Early mitral annular velocity e0
E/e0
Systolic blood pressure

0.08
-0.07
0.30

0.10
0.16
\0.001

-0.27

\0.001

0.36

\0.001

0.10

0.06
\0.001

Diastolic blood pressure

-0.35

LDL-cholesterol

-0.04

0.43

0.08

0.16

Hemoglobin A1c

eGFR estimated glomerular filtration rate; E/e0 early transmitral

velocity to e0 ratio, LDL-cholesterol low-density lipoprotein
cholesterol

patients with worsening of exertional angina, 38 patients

requiring PCI, five patients with CABG, 14 patients
requiring EVT, and three patients with stroke. Nineteen
patients experienced more than one type of event. RI was
significantly higher in Group A (0.74 0.08) than in
Group B (0.70 0.07, p \ 0.001). Significant differences
were also seen between the two groups in terms of LVEF,
LVMI, E/e0 , and use of b-blockers and diuretics.

Discussion
The present study demonstrated that the correlation
between RI and renal function denoted by Cr or eGFR was
significant but not strong in patients with CVD. RI was
associated with age, LAVI, LVMI, parameters of LV
diastolic function, and diastolic blood pressure, in addition
to renal function. Moreover, high RI was recognized in
patients with cardiovascular events when compared with
age- and eGFR-matched controls.
Intrarenal RI measured by renal ultrasonography is
commonly used as an index reflecting vascular resistance
and compliance of intrarenal arteries. These intrarenal
vascular hemodynamic alternations are known to precede
functional renal impairment, as quantified by Cr or eGFR,
and are associated with the degree of intrarenal damage in
various renal diseases [59]. The utility of RI in the
assessment of early renal impairment, such as microalbuminuria, has also been described [21]. However, we often
encounter patients with high RI who require hospitalization

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267

Fig. 3 Correlations of RI with

Cr (left panel) and eGFR (right
panel). RI resistive index, Cr
creatinine, eGFR estimated
glomerular filtration rate

Table 3 Comparison of various

parameters between patients
with cardiovascular events
(Group A) and age- and eGFRmatched controls (Group B)

Group A (n = 112)

Group B (n = 200)

Age (years)

71 12

72 9

eGFR (ml/min/1.732)

55.4 24.6

55.4 14.6

0.56
0.99

RI

0.74 0.08

0.70 0.07

\0.001

Systolic blood pressure (mmHg)

Diastolic blood pressure (mmHg)

137 27
74 13

136 22
76 13

0.78
0.25

Left ventricular ejection fraction (%)

56.7 11.3

61.3 10.2

\0.001

Left ventricular mass index (g/m2)

132.5 49.4

107.8 30.0

\0.001

Left atrial volume index (ml/m2)

40.8 13.7

37.6 14.3

E/e0

14.4 7.6

11.8 4.6

Hypertension (%)

78.6

68.3

0.06
\0.01
0.07

Hyperlipidemia (%)

42.9

39.7

0.63

Diabetes (%)

31.3

27.6

0.52

Calcium channel blocker

44.6

44.7

1.00

b-Blocker

48.2

25.1

\0.001

ACE or ARB

54.5

42.7

0.06

Diuretics

29.5

17.1

Medication (%)

0.01
0

eGFR estimated glomerular filtration rate, E/e early transmitral velocity to e ratio, ACE angiotensinconverting enzyme inhibitor, ARB reninangiotensin system inhibitor

for advanced medical treatment due to CVD or CHF,

despite having low Cr and high eGFR. The present data
show that the correlations of RI with Cr and eGFR are
significant but not strong, with many cases showing high
RI but low Cr. RI was thought to reflect the state of renal
function beyond that expressed by biochemical parameters
such as Cr or eGFR. Various histopathological characteristics are associated with RI, including glomerular sclerosis, edema, tubulointerstitial fibrosis, atrophy, infiltration,
and arteriosclerosis. Among these, arteriosclerosis affects
RI most strongly [22, 23]. RI probably strongly reflects
functional renal impairment resulting from the arteriosclerosis of intrarenal arteries. RI is reportedly associated with the severity of systemic atherosclerosis, as

expressed by carotid IMT or PWV [12, 24]. These results

suggest that renal vascular resistance as indicated by RI
reflects changes in intrarenal arterial sclerosis, as well as
the degree of systemic atherosclerosis. In the present study,
RI correlated with age, LAVI, LVMI, e0 (an echocardiographic index of LV diastolic function), and E/e0 (an index
reflecting LV filling pressure), in addition to renal functional indexes. Other studies have also found that RI is
associated with cardiovascular organ damage, such as LV
hypertrophy and diastolic dysfunction [25, 26]. These
findings suggest that RI may prove useful in screening for
early target organ damage caused by systematic
atherosclerosis and could serve as a useful marker to detect
and evaluate the degree of CVD.

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Doi et al. [27] recently reported that RI combined with

eGFR could provide a powerful predictor of cardiovascular
and renal outcomes in hypertensive patients. They reported
that the utility of RI for predicting cardiovascular and renal
outcomes was particularly high in hypertensive patients
with CKD. They also suggested that renal RI might serve
as a marker of systemic atherosclerotic vessel damage,
rather than a specific marker of renal damage. On the other
hand, the present study found higher RI in patients with
cardiovascular events when compared to controls matched
for eGFR. These data suggest that RI could predict outcomes for patients with CVD, independent of eGFR. We
also selected age-matched subjects as controls, because RI
increases with age [28]. Our data suggest that RI could
serves as a useful index for this purpose, independent of
age.
In the present study, patients requiring hospitalization
due to cardiovascular events (including worsening of CHF
and CVD) showed higher E/e0 and LVMI, and lower
LVEF, when compared with controls. E/e0 has been widely
applied as an index that reflects an increase in LV filling
pressure through LV diastolic dysfunction [20]. A rise in
LV filling pressure results in pulmonary congestion. In
other reports, RI predicted outcomes in patients with heart
failure with preserved EF [16]. In this investigation,
patients with heart failure and preserved EF also showed
high E/e0 , pulmonary artery hypertension, and high RI. The
importance of the relationship between venous congestion
and renal function in patients with cardiac dysfunction has
recently been described [29, 30]. Based on histopathological data, RI also appears to be influenced by renal
parenchymal edema [22]. We speculate that renal congestion could account for the increase in RI seen in patients
with congestive heart failure, in addition to the systematic
arteriosclerosis or LV diastolic dysfunction. Iwashima
et al. [31] demonstrated that RI improved after implantation of a left ventricular assist system in patients with
advanced heart failure. In that study, central venous pressure was an important determinant of RI, and the authors
speculated that elevated central venous pressure in CHF
patients resulted in changes in RI. Increased renal interstitial pressure caused by central venous pressure elevation
may diminish transmural pressure, the cross-sectional area
of segmental arteries, and diastolic blood flow, thereby
leading to increases in RI. Patients with CHF often show
concomitant CVD and CKD due to arteriosclerosis. In fact,
a close relationship exists between systematic arteriosclerosis and heart failure. Interstitial congestion of the kidney
secondary to elevation of central venous pressure might be
related to increased RI, as well as systemic and intrarenal
arteriosclerosis in patients with severe heart failure who
require hospitalization.

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Low LVEF and high LVMI were recognized in patients

with cardiovascular events. LVEF and LVMI have been
reported to predict outcomes in patients with CVD [3235].
The present data indicate that intrarenal vascular hemodynamic alterations are associated with the severity of
CVD and cardiac dysfunction and might predict outcomes
in a manner similar to that of LVEF or LVMI. However,
the mechanisms of increased RI and decreased LVEF in
patients with cardiovascular events may differ from those
of increased RI and increased LVMI. The associations
between RI and measures of cardiovascular organ damage,
such as LV hypertrophy or diastolic dysfunction, have been
described previously [25, 26]. According to univariate
analysis, although the correlation between RI and LVMI
was significant, the relationship between RI and LVEF was
not. Further investigation is required to elucidate the relationship between increased RI and low LVEF.
Furthermore, renal ultrasonography can be performed
along with echocardiography, because this method is very
simple, quick, and well tolerated. The combined use of
renal ultrasonography and echocardiography may help
assess the risk of cardiovascular events in patients with
CVD.
Several limitations must be considered when interpreting the present results. First, this study used a retrospective
design rather than a prospective cohort design. Unfortunately, this study did not enroll consecutive subjects. We
studied patients who had undergone renal ultrasonography
and echocardiography and who were able to undergo regular follow-up. This might have resulted in a population
bias relative to a prospective study. Second, our study
population included patients who were being treated using
medications such as ACE/ARB, calcium channel blockers,
b-blockers, and diuretics. This study was unable to elucidate whether these medications influenced the relationship
between cardiovascular events and RI. Third, because the
subjects of this research were primarily outpatients, the use
of medical treatments for cardiac risk factors (e.g., HT, HL,
and DM) was not uniform.

Conclusions
RI is associated with renal function, age, LAVI, LVMI,
parameters of LV diastolic function and LV filling pressure, and diastolic blood pressure. Moreover, high RI was
recognized in patients with cardiovascular events when
compared with age- and eGFR-matched controls. RI may
reflect the degree of systemic atherosclerosis and cardiovascular organ damage, as well as changes in intrarenal
arterial sclerosis, and may thus be useful in screening for
early target organ damage caused by systematic

J Med Ultrasonics (2016) 43:263270

atherosclerosis, predicting outcomes, and evaluating the

degree of CVD.

269

16.

Compliance with ethical standards

Conflict of interest There are no financial or other relations that
could lead to a conflict of interest.
Ethical considerations All procedures followed were in accordance with the ethical standards of the responsible committee on
human experimentation (institutional and national) and with the
Helsinki Declaration of 1975, as revised in 2008. Informed consent
was obtained from all patients prior to their inclusion in the study.

17.

18.

19.

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