Introduction
The incidence of hypertension is increasing year by
year and may cause severe organ damage and increase the risk of
patient mortality (1,2). Hypertensive heart disease (HHD) may be
associated with diastolic and systolic heart dysfunction, and
eventually lead to heart failure (3,4).
The primary pathological characteristic of HHD is
left ventricular hypertrophy (LVH), which is independently
associated with a number of cardiovascular endpoints, including
coronary heart disease and stroke (5). Therefore, hypertensive patients with
LVH have an increased risk of experiencing cardiovascular events
compared to hypertensive patients without LVH (6,7).
There is a strong correlation between high blood
pressure and LVH (8,9). However, it has been indicated that
nonhemodynamic factors, including transforming growth factor β1,
the renin-angiotensin system and tumor necrosis factor α may induce
profibrotic effects and proinflammation, thus contributing to LVH
(10,11). Furthermore, studies using animal
models have demonstrated that macrophage, T cell and monocytic
fibroblast precursors serve important roles in angiotensin II
infusion-induced or pathological cardiac remodeling (12–15).
Although studies using animal models have
demonstrated that nonhemodynamic factors, including inflammatory
cells and cytokines, contribute to left ventricular hypertrophy
(LVH) (12,14), there is little clinical data to
confirm this association. Based on the aforementioned results, the
present study aimed to determine whether circulating leukocyte
subtypes are associated with LVH in hypertensive patients treated
with anti-hypertensive drugs.
Patients and methods
Patients
A total of 144 consecutive hypertensive patients
currently taking anti-hypertensive drug therapy were enrolled in
the current study between January 2012 and December 2014 in the
Department of Cardiology, Beijing Friendship Hospital, Capital
Medical University (Beijing, China). All enrolled patients had a
5–20 year history of hypertension and had all previously taken
anti-hypertensive drugs. Exclusion criteria included secondary
hypertension, heart failure symptoms, idiopathic cardiomyopathy,
ischemic heart disease and the presence of other heart diseases.
Blood pressure (BP) was measured at an office at the Beijing
Friendship Hospital on two separate occasions. A calibrated mercury
sphygmomanometer was used while patients were seated following a 10
min rest. Normal BP was defined as systolic BP (SBP) of 90–140 mmHg
or diastolic BP (DBP) of 60–90 mmHg (16,17).
Patients were excluded from the current study if they had secondary
hypertension, heart failure symptoms, idiopathic cardiomyopathy,
ischemic heart disease or other heart diseases. Patient
characteristics are summarized in Table
I. The protocol of the current study was approved by the
Institutional Committee of the Capital Medical University (Beijing,
China) and was performed in accordance with the ethical standards
laid down in the 1964 Declaration of Helsinki and its later
amendments. Written informed consent was given by all patients.
 | Table I.Clinical characteristics of patients
in each group. |
Table I.
Clinical characteristics of patients
in each group.
| Characteristic | Lower LVMI | Higher LVMI | P-value |
|---|
| Age, years | 59.4±12.8 | 61.9±12.6 | 0.301 |
| Proportion of
males, % | 55.7 | 61.5 | 0.526 |
| Systolic blood
pressure, mmHg | 138.2±23.6 | 145.8±23.7 | 0.086 |
| Diastolic blood
pressure, mmHg | 87.0±12.6 | 84.1±14.6 | 0.384 |
| Hyperlipidemia,
% | 12.3 | 15.8 | 0.582 |
| Diabetes mellitus,
% | 23.6 | 13.2 | 0.174 |
| Laboratory
parameters |
|
|
|
| Blood
platelet, 109/l | 218.0±57.4 | 228.3±60.8 | 0.354 |
|
Hemoglobin, g/l | 136.7±14.9 | 131.7±12.4 | 0.065 |
| Serum
creatinine, µmol/l | 83.7±37.6 | 88.6±37.3 | 0.493 |
| Blood
urea nitrogen, mmol/l | 6.29±7.65 | 6.95±4.97 | 0.622 |
| Blood
uric acid, µmol/l | 324.7±105.6 | 355.1±89.1 | 0.116 |
| Medicine |
|
|
|
| ACEI
and/or ARB | 67.0% | 66.7% | 0.945 |
|
Calcium-channel blockers | 51.0% | 51.3% | 0.971 |
|
β-Blocker | 47.2% | 41.0% | 0.510 |
|
Aspirin | 52.8% | 56.4% | 0.701 |
Laboratory analyses
Baseline clinical data was collected for all
patients. Counts for total white blood cells (WBC) and
differentiated subtypes (neutrophils, lymphocytes, monocytes,
eosinophils and basophils) were measured immediately following
presentation using peripheral venous blood in an automated blood
cell counter (ADVIA 2120: Siemens Healthcare Diagnostics,
Camberley, UK). The WBC count was treated as a continuous and
categorical variable and was classified as low
(<6.65×109/l, <33th percentile), intermediate
(6.65–10.11×109/l, 33th-66th percentiles) or high
(>10.11×109/l, >66th percentile) (18,19).
Alanine transaminase, creatinine, blood urea nitrogen, cholesterol,
triglycerides, uric acid and glucose were measured using an
established immunoassay (Biosite Inc., San Diego, CA, USA).
Quantitative C-reactive protein determination was performed with
the BN II Nephelometer (Siemens Healthcare Diagnostics). Cardiac
troponin T was measured on the Elecsys 10/10 (Roche Diagnostics,
Indianapolis, IN, USA).
Evaluation of cardiac structure and
function
Echocardiographic examination of the patients was
performed by two experienced cardiologists using a VIVID 7
cardiovascular ultrasound system (GE Healthcare Life Sciences,
Uppsala, Sweden) with an M4S 1.5–4.0-MHZ matrix array probe (GE
Healthcare Life Sciences) according to the guidelines of the
American Society of Echocardiography (20). Echocardiographic examination was
performed with patients in the left lateral decubitus position
breathing slowly. The cardiologists were blinded to the patients'
other data. The echocardiograph measurements included left
ventricular end-diastolic diameter (LVEDD), left ventricular
posterior wall thickness in diastole (LVPWT) and inter-ventricular
septal wall thickness in diastole (IVST). Left ventricular systolic
function was assessed using the left ventricular ejection fraction
(LVEF) and left ventricular fractional shortening (LVFS). Left
ventricular mass was calculated using the ASE-recommended formula:
Left ventricular mass (g) = 0.8 × {1.04[(IVST + LVEDD +
LVPWT)3 - (LVEDD)3]} (21). Left ventricular mass was divided by
body surface area to obtain the left ventricular mass index (LVMI).
Body surface (m2) was calculated using (0.0061 × height
+ 0.0124 × weight - 0.0099). LVH was defined as previously
described (22,23). Patients were divided into two
different groups according to LVMI. One group consisted of patients
with lower LVMI (≤100 g/m2) and the other group
consisted of patients with higher LVMI (>100
g/m2).
Statistical analysis
Data analysis was performed using the SPSS
statistical package ver. 16.0 for Windows (SPSS Inc., Chicago, IL,
USA). Differences in the distribution of demographics, laboratory
parameters and medical characteristics among hypertensive patients
with lower LVMI, compared with those who had higher LVMI, were
examined using the χ2 test for categorized variables and
either one-way analysis of variance for continuous variables, or
non-parametric tests if distribution was skewed. Multivariate
logistic regression analyses were performed to examine the
associations of total white blood cell and other potentially
confounding prognostic factors with LVMI. Other factors included in
the multivariate analyses were age, gender, hypercholesterolemia,
diabetes mellitus and medication (aspirin, β-blockers,
calcium-channel blockers, angiotensin converting enzyme inhibitor
and aldosterone receptor blocker). All P-values were the results of
two-tailed tests. A value of P<0.05 was considered to indicate a
statistically significant difference.
Results
White blood cells are increased in
patients with LVMI
Clinical characteristics of all patients are
presented in Table I. At baseline,
the 41% of the study population were male and the mean age was 53.7
years [range 44–66 years, standard deviation (SD) 5.8 years]. Out
of all the patients, 10% had diabetes mellitus and 28% had
hyperlipidemia. The mean SBP and DBP (mmHg) were 121.2 (SD 18.8)
and 74.0 (SD 11.3). Blood platelet, hemoglobin, serum creatinine,
urea nitrogen and uric acid levels did not significantly differ
between the two groups. The drug treatments received by patients in
the two groups were not significantly different.
Cardiac remodeling caused by hypertension is
accepted as an inflammatory response (14,15) in
which inflammatory cells play a critical role. Therefore the
current study measured levels of WBC. The LVMI of the study
population by tertiles of total WBC level is presented in Fig. 1. In the middle tertile (Tertile 2,
n=44), 16% of patients had higher LVMI, indicative of myocardial
hypertrophy (MH), which was lower than that in the highest tertile
(Tertile 3, n=51; P=0.012). Notably, in the lowest tertile (Tertile
1, n=49) 22.4% of patients had MH, higher than in the middle
tertile (Tertile 2), however, this difference was not statistically
significant (22.4% vs. 39.2%, P=0.425).
Neutrophil counts correlate with
LVMI
To determine which specific leukocyte types have a
critical role in hypertension-induced MH, different WBC subtypes
were measured. The LVMI of the study population by tertile of
neutrophil counts is presented in Fig.
2. A high LVMI indicates the presence of MH. The proportion of
patients with MH in both the lowest (n=48) and middle tertile
(n=48) was 18.8%. However, a larger proportion (39.6%) of patients
in the highest tertile had MH (18.8% vs. 39.6%, P=0.012) compared
with the middle and lowest tertiles.
As presented in Fig.
3, other subtypes of WBC were detected. A slightly higher
proportion of patients had MH (31.3%) in the middle tertile (n=48)
compared with the other tertiles; the percentages in the lowest
tertile (n=46) and highest tertile (n=50) were 25.0 and 22.0%
respectively (P=0.582; Fig. 3A). As
presented in Fig. 3B for the
monocyte count, a marked increase (37.8%) of MH in the highest
tertile (n=45) was observed, while the proportion of patients with
MH in the other two tertiles were 19.6% and 22.6% respectively.
However, none of these differences were statistically
significant.
Table II presents
the results from the logistic analysis. Total WBC counts differed
significantly between the two LVMI groups (the lowest and the
highest; P=0.013). Additionally, accompanied by an increase in
total WBCs particularly over the middle tertile, the percentage of
patients with higher LVMI (or MH) was significantly increased
(P=0.008). Furthermore, Table II
indicated that older patients (>65 years old) had higher LVMI
than those ≤65 years (P=0.042). However, there were no significant
differences in gender, DM, hypercholesterolemia and cardiovascular
drug treatment between the groups.
| Table II.Multivariate logistic regression
analyses for left ventricular mass index in hypertensive
patients. |
Table II.
Multivariate logistic regression
analyses for left ventricular mass index in hypertensive
patients.
|
|
|
| 95.0% C.I. for EXP
(B) |
|
|---|
|
|
|
|
|
|
|---|
| Variable | B | OR | Lower LVMI | Higher LVMI | P-value |
|---|
| Total WBC
count |
|
|
|
| 0.013a |
| WBC Tertile
(lowest) | 0.364 | 1.439 | 0.478 | 4.338 | 0.518 |
| WBC Tertile
(highest) | 1.415 | 4.117 | 1.452 | 11.693 | 0.008a |
| Old age (>65
years) | 0.865 | 2.374 | 1.037 | 5.473 | 0.042a |
| Male (%) | −0.314 | 0.731 | 0.312 | 1.716 | 0.469 |
|
Hypercholesterolemia | 0.414 | 1.512 | 0.493 | 4.636 | 0.469 |
| DM | −0.934 | 0.395 | 0.126 | 1.237 | 0.111 |
| ACEI or ARB | −0.047 | 0.955 | 0.507 | 1.796 | 0.885 |
| CCB | −0.011 | 0.989 | 0.444 | 2.203 | 0.979 |
| Aspirin | 0.165 | 1.179 | 0.517 | 2.693 | 0.695 |
| β-blocker | −0.277 | 0.758 | 0.339 | 1.695 | 0.511 |
Discussion
In the present study, a correlation was detected
between white blood cell count and LVMI in hypertensive patients
undergoing anti-hypertensive drug therapy. Hypertension is an
important risk factor for cardiovascular diseases including
atherosclerosis and myocardial hypertrophy, and is independent of
age, gender and ethnicity (24,25). The
incidence of hypertension is an important basis for the progress of
cardiovascular diseases, which itself is a result of many
interacting factors. There is evidence that nonhemodynamic factors,
which possibly lead to profibrotic effects and proinflammation, may
influence LVH (10,11).
Hypertension is a chronic disease (26,27).
Active drug therapy may reduce and delay the organ damage caused by
hypertension (27). Excluding the
impact of other factors, there are significant differences in LVH
among patients receiving the same drug therapy (28,29). LVH
is closely associated with the plasma levels of white blood cells
in patients, which gives an indication of hypertension (17,19).
Thus practitioners can focus on the level of white blood cell
intervention required, further reducing the patient's long-term
target organ damage.
The current study detected a strong correlation
between white blood cell counts (particularly neutrophil counts)
and LVMI in hypertensive patients undergoing anti-hypertensive drug
therapy. It demonstrates that modulating neutrophil number to a
moderate level for hypertensive patients alongside
anti-hypertensive drug therapy may benefit the long-term prognosis
of patients. Inflammation is an indicator for the progression of
myocardial remodeling underlying the pathogenesis of LVH (30–34).
Inflammatory factors are typically derived from white blood cells,
particularly neutrophils (35–39).
Myocardial expression of inflammatory mediators, including monocyte
chemoattractant protein-1 or fractalkine, is significantly
increased in experimental myocarditis or dilated cardiomyopathy
(40,41). The infiltrating inflammatory cells
and/or cardiomyocytes may account for enhanced LVH. Inflammatory
cells and cytokines participate in the pathological process of
cardiovascular remodeling and are a double-edged sword; they can
clear necrotic cells and foreign antigens and promote angiogenesis
and scar repair (42). However,
excessive inflammatory cell infiltration may seriously upset the
balance of the body microenvironment, causing organ damage
(42–44).
To the best of our knowledge, the present study is
the first to demonstrate that circulating specific types of
leukocyte may be associated with LVH in hypertensive patients
currently taking anti-hypertensive drugs and thus may provide a
novel preventative strategy for LVH by modulating myocardial
inflammation.
Acknowledgements
The present study was supported by the National
Natural Science Foundation of China (nos. 81300209, 81400263,
81230007 and 81200147) and Basic-Clinical Cooperation Project of
Chinese Capital Medical University (no. 13JL59).
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