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Abstract. – OBJECTIVE: Hemodialysis treat-
ment has been revealed to increased the sys-
tolic pulmonary artery pressure (sPAP). Right
ventricular dysfunction (RVD) had been demon-
strated to predict mortality in chronic renal fail-
ure patients. We investigate the prevalence of
pulmonary hypertension and RVD among pa-
tients and possible contributing factors for pul-
monary hypertension.
PATIENTS AND METHODS: A cross-section-
al survey consisted of 70 hemodialysis patients
was performed in our hemodialysis center. By
using echocardiography, an estimated systolic
pulmonary ar tery pressu re of > 35 mmHg at
rest met the criterion of pulmonary hyperten-
sion. Tissue Doppler imaging (TDI) of the right
ventricle was performed in all patients.
RESULTS: 27 out of 70 (38.57%) patients met
the definition of pulmonary hypertension, while
32 out of 70 (45.71%) patients met the definition
of RVD. Co m pare d t o p atie n ts with o ut pul-
monary hypertension, patients with pulmonary
hypertension demonstrated higher systolic
blood pressure and lower left ventricular ejec-
tion fraction (LVEF). RVD, indicated by TDI my-
ocardial performance index (MPI), was worse
impaired in patients with pulmonary hyperten-
sion. Echocardiographic findings suggested el-
evated MPI values of right ventricular and right
ventricular wall thickness were significantly as-
sociated with sPAP. While a high level of LVEF
and Kt/V values was inversely correlated with
sPAP. The mul tivari ate d etermin ant s of pul-
monary hypertension were systolic blood pres-
sure and Kt/V values.
CO N CLU S I ON S : Among hemodialysis pa-
tients, pulmonary hypertension is extraordinary
common and is significantly associated with
RVD. The poor control of systolic blood pres-
sure and volume overload have played an im-
portant role in the mechanism of pulmonary hy-
pertension in chronic uremia patients.
Key Words:
Pulmonary hypertension, Right ventricular dys-
function, Hem o d i a l y s i s , A r t e r i oven o u s f i s t u l a ,
Echocardiography.
European Review for Medical and Pharmacological Sciences
Pulmonary hypertension and right ventricular
dysfunction in hemodialysis patients
L.-J. ZHAO, S.-M. HUANG, T. LIANG1, H. TANG1
Department of Nephrology, and 1Department of Cardiology; West China Hospital, Sichuan
University, Chengdu, Sichuan Province, China
Corresponding Author: Song-Min Huang, MD, Ph.D; e-mail: hsongm@medmail.com.cn 3267
Introduction
Cardiovascular disease is one of the leading
cause of mortality in chronic renal failure patients,
accounting for 34.1% of deaths1. While mainte-
nance hemodialysis treatment has been suggested
in chronic uremia patients, it has become a finan-
cial burden in chronic kidney disease patients in
Southeast China2. Hemodialysis treatment has
been revealed to increased the systolic pulmonary
artery pressure (sPAP). According to the recent
studies3-8, the prevalence of pulmonary hyperten-
sion in hemodialysis patients ranges from 20%-
41.1%. Pulmonary hypertension was an indepen-
dent predictor of all-cause and cardiovascular
mortality in maintenance hemodialysis patients9.
However, right ventricular dysfunction (RVD) on
patients under dialysis has been rarely revealed.
Once the vascular access fistulation was suc-
cessfully founded, the shunt determines a chronic
increase in afterload which leads to right ventricu-
lar hypertrophy (RVH). Right ventricular (RV)
compensatory hypertrophy reduces ventricular
compliance and might display an underlying role
in impairing left ventricular filling via interventric-
ular interaction10. Echocardiography can detect suf-
ficiently right ventricular abnormality, which can
suggest prognosis in patients with pulmonary hy-
pertension11. Our study investigates the prevalence
of pulmonary hypertension and RVD in chronical-
ly uremia patients under hemodialysis and possible
contributing factors for pulmonary hypertension.
Patients and Methods
Selection of Patients
This cross-sectional investigation was undertak-
en in West China Hospital of Sichuan University
Blood Purification Center, Chengdu, China, from
September 2011 until June 2013. The study popula-
2014; 18: 3267-3273
3268
tion consisted of 70 ESRD patients (males/females:
42/28, age 54.9 ± 12.9 years) who were maintained
on long-term hemodialysis therapy via surgically
created native arteriovenous access. Patients ≥18
years who had been on maintenance therapy for at
least 3 months and were receiving hemodialysis
sessions 3 times per week, were enrolled. Each ses-
sions lasted for 4h and used bicarbonate-buffered
dialysate. All of these patients were used radial arte-
riovenous fistula. 48 patients were exclude due to
comorbid conditions with a high probability of sec-
ondary pulmonary hypertension (sever valvular
heart disease [n = 11], congenital left-right shunts
[n = 3], a history of coronary artery stent installa-
tion [n=5 ], connective tissue disorders [n = 4], pul-
monary thromboembolic disease [n = 5], chronic
cor pulmonale [n = 7], chronic obstructive pul-
monary disease [n = 13]). 5 patients had renal trans-
plantation and 3 patients had atrial fibrillation were
also not enrolled. All patients signed an informed
consent before entering the study. Our study has
been approved by West China Hospital Ethics
Committee.
Clinical and Laboratory Investigations
Each patient’s general data (age, sex, systolic
blood pressure, diastolic blood pressure, medica-
tion used, etiology of renal disease) and data re-
garding the hemodialysis (dialytic age, interdialyt-
ic weight gain, Kt/V values) were recorded. Kt/V
values were calculated by Daugirdas second gen-
eration equation: Kt/Vsp = -In(R-0.08×t) + [(4-
3.5×R) × UF/W], where twas the session length
in hours and R was the ratio of postdialysis to the
predialysis plasma urea nitrogen concentrations.
UF is short for ultrafiltrate volume in liters. W is
the postdiamysis weight in kilograms12. Laborato-
ry investigations (hemoglobin, hematocrit, albu-
min, serum calcium, phosphorus, parathyroid hor-
mone) were also determined. All the laboratory
data were done in the same week when the patient
underwent Doppler echocardiography.
Echocardiography
All enrolled patients underwent Doppler
echocardiography within 1-2 hours after comple-
tion of the hemodialysis to avoid volume overload
which may lead to overestimated of sPAP. Each pa-
tient were examined by an experienced echocardio-
graphist. All echocardiography parameters were
measured by a Philips (Eindhoven, The Nether-
lands) iE-33 ultrasound machine. The following
measurements were taken on two-Dimensional and
M-mode echocardiography: diameter of left atria
(LA), diameter of left ventricular (LV), diameter of
right atria (RA), diameter of RV, thickness of inter-
ventricular septum (IVS) and thickness of left ven-
tricular posterior wall (LVPW)13. Ejection fraction
of the left ventricular was calculated using the
modified Simpson method in the 4-chamber view.
The tricuspid systolic jet (TR) was measured by
from the 4-chamber view with the continues-wave
Doppler probe. In the presence of tricuspid valve
regurgitation, systolic pulmonary artery pressure
was calculated using the simplified Bernoulli equa-
tion: sPAP = 4*(TR)2+ right artrial pressure. Right
atrium pressure was estimated from inferior vena
cava (IVC) and its collapsibility. Pulmonary hyper-
tension is defined as an increased of mean pul-
monary artery pressure above 25 mmHg at rest in
the setting of normal or reduced cardiac output and
normal pulmonary capillary pressure.However, ac-
cording to the echocardiographic criteria, pul-
monary hypertension is defined as sPAP > 35
mmHg at rest14.
Early (E) and late (A) right ventricular inflow
ve locities we r e m easured with p u l se-wave
Doppler by placing the sample volume in between
the tips of the tricuspid valve in the apical 4-cham-
ber window. S’ (systolic myocardial velocity), E’
(protodiastolic myocardial velocity) and A’ (late
peak diastolic myocardial velocity) of the right
ventricular were recorded by tissue Doppler imag-
ing (TDI). The deceleration time (DT-E), ejection
time (ET), isovolumic relaxation time (IVRT) and
isovolumic contraction (IVCT) were also mea-
sured. Calculation of right ventricular myocardial
performance index (MPI) by tissue Doppler imag-
ing is defined as the ratio of isovolumic time di-
vided by (IVRT + IVCT)/ET. TDI of MPI value is
reproducible and relatively independent of pre-
load. The upper reference limit for the right-sided
TDI of MPI value is 0.5515. Tricuspid annular
plane systolic excursion (TAPSE), indices of right
ventricular systolic function, was acquired by
placing an M-mode cursor through tricuspid annu-
lus. TAPSE is a method to measure the amount of
longitudinal motion of the RV annular segment at
peak systole. It is inferred that the greater the de-
scent of the base in systole is associated with bet-
ter RV systolic function14. The four chambers were
measured through apical 4-chamber view at the
same time. RV wall thickness was measured at
end-diastole by M-mode from the subcostal win-
dow, at the level of the tip of the anterior tricuspid
leaflet or left parasternal windows. Right ventricu-
lar hypertrophy was defined as RV wall thickness
≥5 mm16.
L.-J. Zhao, S.-M. Huang, T. Liang, H. Tang
Variable sPAP ≤35 mmHg sPAP > 35 mmHg
(n: 43) (n: 27) pvalue
Age (years) 55.49 ± 11.74 55.46 ± 14.95 0.765
Gender, male/female ratio 1.39 1.70 0.488
BMI (kg/m2) 23.20 ± 3.37 21.70 ± 2.63 0.059
Heart rate (beats/min) 77.47 ± 9.35 72.19 ± 15.69 0.084
Systolic blood pressure (mmHg) 138.72 ± 15.01 152.08 ± 16.11 0.001
Diastolic blood pressure (mmHg) 80.44 ± 10.27 83.16 ± 11.53 0.313
Etiology of renal failure 0.549
• Hypertension (%) 78ns
• Diabetes mellitus (%) 11.6 15.4 ns
• Glomerulonephritis (%) 48.8 57.7 ns
• Others (%) 25.6 8 ns
• Unknown (%) 7 10.9 ns
Antihypertension therapy ns
• ACE-inhibitors (%) 7 12 0.833
• ARBs (%) 32 46 0.259
•β-Blockers (%) 42 69 0.057
• CCB (%) 90 81 0.413
•α-Blockers (%) 28 38 0.869
Dialytic age (months) 40.16 ± 38.89 31.25 ± 16.67 0.193
Interdialytic weight gain (kg) 2.18 ± 0.71 2.10 ± 0.72 0.681
Kt/V value 1.85 ± 0.90 1.31 ± 0.30 0.001
Table I. Demographic and Clinical data of patients (n=number of patients).
Footnote: ARBs, angiotensin receptor blockers; CCB, calcium channel blockers. 1 mmHg = 0.1333 kPa.
Pulmonary hypertension and right ventricular dysfunction in hemodialysis patients
3269
< 0.05 to remain in the final model. All analyses
were conducted using standard statistical software
(IBM, SPSS 20.0 New York, NY, USA). All pval-
ues < 0.05 were considered to be statistically sig-
nificant.
Results
Baseline Characteristics
Data from the 27 patients with pulmonary hyper-
tension were compared with those of the 43 patients
without pulmonary hypertension (Table I). Groups
did not show significant differences regarding the
age, gender, body mass index (BMI), heart rates
and diastolic blood pressure. However, the systolic
blood pressure was significant higher in pulmonary
hypertension patients as compared with those with-
out pulmonary hypertension (Table I). The common
etiologies of renal failure were hypertension, dia-
betes mellitus, glomerulonephritis. The incidence of
antihypertensive medications were distributed in
similar proportions (Table I). The mean duration of
dialysis as well as the interdialytic weight gain in
patients demonstrated no significant differences be-
tween the two subgroups.Interestingly, the Kt/V
values was lower in patients with pulmonary hyper-
tension (Table I).
The vascular access was acquired soon after in
the longitudinal and transverse planes from the ar-
terial anastomosis through the entire access by
means of ultrasonic Doppler (Philips iE-33 ultra-
sound machine). Vascular blood flow was calculat-
ed by multiplying the time-averaged velocity
(TAV) by the cross-sectional area of the access17.
The calculations of vascular blood flow is Qa =
TAV×πr2×60. Here, r is the radius of the arterial
anastomosis.
Statistical Analysis
Values are expressed as means ± standard devi-
ation and as a percentage for categorical parame-
ters. Clinical variables were compared between
patients with and without pulmonary hyperten-
sion. Differences between continuous variables of
the two subgroups were compared with Student’s
t-test and Mann-Witney-U test, as applicable. Chi-
square test was used to evaluate the categorical pa-
rameters between the groups. Two-tailed bivariate
correlations were estimated by the Pearson’s coef-
ficient. Multivariate regression analysis was per-
formed to determine the relationship between pul-
monary hypertension and other covariates (demo-
graphic, clinical or hemodynamic). Those convari-
ates were required to have a p-value of < 0.2 to en-
ter the stepwise forward selection and a p-value of
Variable sPAP ≤35 mmHg sPAP > 35 mmHg
(n:43) (n:27) pvalue
Hemoglobin (g/L) 102.24 ± 16.55 93.19 ± 14.27 0.024
Hematocrit (%) 0.32 ± 0.05 0.29 ± 0.05 0.020
Albumin (g/L) 42.60 ± 3.33 41.98 ± 3.99 0.491
Calcium (mmol/l) 2.33 ± 0.31 2.29 ± 0.24 0.651
Phosphate (mmo/l) 1.85 ± 0.55 1.65 ± 0.46 0.139
PTH (pg/ml) 20.99 ± 17.89 21.44 ± 18.35 0.854
Table II. Laboratory characteristics of patients (n=number of patients).
sPAP ≤35 mmHg sPAP > 35 mmHg
Variable (n:43) (n:27) pvalue
sPAP (mmHg) 25.95 ± 5.81 44.15 ± 7.80 < 0.001
LA diameter (mm) 37.09 ± 5.22 42.12 ± 3.94 < 0.001
LV diameter (mm) 46.47 ± 4.57 52.80 ± 6.16 < 0.001
RA diameter (mm) 41.44 ± 7.11 46.88 ± 7.14 0.003
RV diameter (mm) 21.19 ± 2.14 23.85 ± 4.67 0.010
IVS (mm) 11.99 ± 1.88 12.81 ± 1.90 0.085
LVPW (mm) 10.51 ± 1.65 11.31 ± 1.80 0.066
RV wall thickness (mm) 4.17 ± 0.51 4.56 ± 0.72 0.012
Presence of RV hypertrophy (%) 9.30 % 33.33% < 0.001
Pulse Doppler imaging
Tricuspid E (cm/s) 59.52 ± 12.39 56.75 ± 11.74 0.296
Tricuspid A (cm/s) 52.40 ± 12.39 48.32 ± 9.54 0.154
E/A ratio 1.19 ± 0.30 1.22 ± 0.36 0.653
DT-E (ms) 114.21 ± 27.89 114.85 ± 29.31 0.928
Tissue Doppler imaging
Tricuspid E’ (cm/s) 9.80 ± 2.53 11.47 ± 2.03 0.006
Tricuspid A’ (cm/s) 13.97 ± 3.39 15.56 ± 4.75 0.145
Tricuspid annulus systolic peak velocity S’(cm/s) 13.16 ± 2.13 14.08 ± 1.71 0.068
E'/A’ ratio 0.74 ± 0.29 0.82 ± 0.34 0.348
TAPSE (mm) 23.61 ± 2.95 22.11 ± 2.66 0.033
ET (ms) 254.70 ± 27.29 264.85 ± 27.42 0.140
IVRT (ms) 60.2 ± 15.11 76.12 ± 12.41 < 0.001
IVCT (ms) 70.51 ± 10.99 73.88 ± 10.52 0.214
MPI value 0.52 ± 0.09 0.57 ± 0.06 0.010
LVEF (%) 67.84 ± 7.52 60.19 ± 10.81 0.039
Table III. Echocardiographic parameters of patients (n=number of patients).
L.-J. Zhao, S.-M. Huang, T. Liang, H. Tang
Indices of Right Ventricular Function
Patients on hemodialysis with pulmonary hy-
pertension presented higher left and right ventricu-
lar diameters (Table III). In particularly, sPAP and
RV wall thickness were significantly higher in pa-
tients with pulmonary hypertension compared
with those without pulmonary hypertension (44.15
± 7.80 vs 25.95 ± 5.81 mmHg, p< 0.001; 4.56 ±
0.72 vs 4.17 ± 0.51 mm, p= 0.012,respectively)
(Table III). Moreover, 33.33% of patients were re-
Indices of Laboratory Investigations
The levels of hemoglobin and hematocrit were
significantly lower in patients with pulmonary
hypertension. Although the albumin seemed to be
lower in patients with pulmonary hypertension,
the two subgroups did not differ significantly dif-
ferent. Other variables, such as serum calcium,
phosphorus and parathyroid hormone (PTH) did
not differ significantly between the examined
subgroups (Table II).
3270
vealed to developed to RVH in patients with pul-
monary hypertension. While only 9.30% patients
without pulmonary hypertension resulted in RVH.
Compared with the patients without pulmonary
hypertension, patients with pulmonary hyperten-
sion showed a prolonged IVRT but lower TAPSE
(Table III). MPI values, echocardiography para-
meters of right ventricular systolic and diastolic
function,was significantly higher in patients with
pulmonary hypertension (p= 0.033 and p= 0.010
respectively) (Table III). It indicated that right
ventricular function was impaired in patients with
pulmonary hypertension than those without pul-
monary hypertension.
Indices of Vascular Access
Vascular access parameters including the di-
ameter of the arteriovenous fistula and the vascu-
lar access flow (Qb) were measured by ultrasonic
Doppler at the same time. Patients with pul-
monary hypertension had higher Qb compared
with patients with normal sPAP (1004.25 ±
179.83 ml/min vs. 996.80 ± 220.03 ml/min).
However, the difference was no statistically sig-
nificant (p= 0.887).
Risk of Pulmonary Hypertension
in Hemodialysis Patients
A significantly positive correlation was noted be-
tween sPAP and those three parameters as RV wall
thickness (r = 0.460, p< 0.001), MPI values (r =
0283, p= 0.019) and systolic blood pressure (r =
0.279, p= 0.020). On the contrary, sPAP inversely
correlated with left ventricular ejection fraction
(LVEF) (r = -0.27, p= 0.025), hemoglobin (r = -
0.337, p= 0.005) and Kt/V values (r = -0.330, p=
0.006). A further comparison between the two ure-
mic subgroups revealed that LVEF was significant-
ly lower in patients with pulmonary hypertension
than those without pulmonary hypertension (Table
III). Logistic regression analysis adjusted for the
same confounding factors such as age, gender, BMI
and HR. The multivariate determinants of pul-
monary hypertension were systolic blood pressure
(regression coefficient b: 0. 050,odds ratio 1.051
per mmHg, p= 0. 011) and Kt/V values (regression
coefficient b: -1.394, odds ratio 0.248, p= 0. 044).
Discussion
The study confirmed that uremic patients on
chronic dialysis treatment showed a high preva-
lence of pulmonary hypertension which had been
reported in the previous studies18,19. The mecha-
nisms of pulmonary hypertension mainly derived
from elevated pulmonary blood flow and increased
pulmonary vascular resistance. Pulmoanry artery
pressure may be increased by high cardiac output
due to the arteriovenous access, further worsened
by fluid overload in hemodialysis patients. Pres-
sure-induced mediator regulation may represent an
early event in the development of secondary pul-
monary hypertension in chronic renal failure pa-
tients. Prolonged hypertension may effect pul-
monary circulation. A recent research confirmed
that endothelial dysfunction were associated with
increased vasoconstrictors like ehdothelin-1 and
decreased vasodilators such as NO2 0. Worsen,
chronic renal failure patients displayed metabolic
and hormonal derangements which may result in
pulmonary arterial vasoconstriction.
A positive relationship between the sPAP and
RV wall thickness was revealed. To adopting to
the high pressure of pulmonary circulation, end
sysytolic pressure of right ventricle increased.
Chronic right ventricular pressure overload leads
to functional tricuspid valve insufficiency, initiat-
ing pathological RV remodeling and results in
compensatory RVH to decrease wall stress, which
ultimately leading to right heart failure. It has at-
tributed direct ventricular interaction to the sep-
tum, via the trans-septal pressure gradient21. This
pathological physiology change was confirmed by
the negative correlation between LVEF and RV
wall thickness in our study.
Although researches have mainly focused their
attention on left ventricular function in hemodialy-
sis patients22,23, insight into the role of RV function
in pulmonary hypertension patients is scarce. TDI
has considered as a strong diagnostic method in
detecting subclinical abnormalities in cardiac
function, which had been demonstrated to predict
mortality24,25. Thus, the detection of RVD would
be helpful in early detection of higher risk of de-
veloping right heart failure. Our study revealed
that nearly half of hemodialysis were associated
with RVD. Interestingly, MPI values was positive-
ly correlated with sPAP. The potential mechanism
of this clinical feature is chronic volume overload
has affect right ventricular function independently
from post-load conditions10. Arteriovenous fistula
induced volume overload lead to increased sPAP
plays a crucial role in triggering RVD in mainte-
nance hemodialysis patients.
Although the present study showed no direct
relationship between access flow of AVF and
sPAP, which was similar to other clinical trails3-26.
3271
Pulmonary hypertension and right ventricular dysfunction in hemodialysis patients
3272
We avoided the patients with brachial AVFs. The
blood flow of AVF was confirmed to be higher in
upper arm AVFs than lower AVFs27 .Although
our study demonstrated a high prevalence of pul-
monary hypertension and RVD among hemodial-
ysis patients, it provoques some criticisms. All
the vascular access parameters were measured by
ultrasonic Doppler in the present study, which
will be less reliably than Transonic Hemodialysis
Monitor HD0228. As peritoneal dialysis patients
who were reported had pulmonary hypertension
in the recent research29, data of RVD in those pa-
tients are lacking up to now which will be a re-
search topic in the future.
–––––––––––––––––-––––
Conflict of Interest
The Authors declare that there are no conflicts of interest.
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