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Evaluation of left ventricular function with strain/strain rate imaging in patients with rheumatic mitral stenosis/Romatizmal mitral darligi olan hastalarda sol ventrikul fonksiyonlarmm strain/strain rate goruntuleme ile degerlendirilmesi.

ABSTRACT

Objective: The most important sequel of acute rheumatic fever is mitral stenosis in long-term. The aim of the study is to determine left ventricular (LV) functions by tissue Doppler imaging (TDI) and strain/strain rate echocardiography (SE/SRE) in mitral stenosis patients who had no clinical signs of heart failure.

Methods: Our study was designed as cross-sectional study The study population consisted of 32 patients with isolated mitral stenosis and mitral valve area < 2.0 [cm.sup.2] (Group 1) and 25 healthy control subjects (Group 2). In addition to standard echocardiographic methods, TDI and SE/SRE were performed to assess LV functions in all participants. Student's t-test was used to compare continuous variables. Fisher- exact test was used to compare categorical variables.

Results: Systolic myocardial velocity (Sm) were significantly lower in Group 1 than in Group 2 (6.0 [+ or -] 1.4 cm/sec vs 7.9 [+ or -] 1.8 cm/sec, p<0.001) also, early diastolic myocardial velocity (Em) were significantly lower in Group 1 than in Group 2 (4.4 [+ or -] 1.5 cm/sec vs 10.8 [+ or -] 2.1 cm/sec, p<0.001). But there was no significant difference in late diastolic myocardial velocity (Am) between two groups. Peak systolic strain and strain rate of septal wall in Group 1 were significantly lower than Group 2 (p<0.001 for both). Besides, peak systolic strain and strain rate of lateral wall in Group 1 were significantly lower than in Group 2 (p<0.001 for both).

Conclusion: Although, global ejection fraction was normal and there were no symptoms of heart failure clinically in the patients with mitral stenosis, LV dysfunction demonstrated that using by echocardiography. TDI and strain/strain rate imaging to be new echocardiographic methods may be used reliably for detection LV function in early stage of mitral stenosis. (Anadolu Kardiyol Derg 2010; 10:328-33)

Key words: Mitral stenosis, echocardiography, strain/strain rate imaging, left ventricular function

OZET

Amac: Akut romatizmal atesin uzun ddnem en onemli sekeli mitral darligidir. Bu calismanin amaci, klinik olarak kalp yetersizligi bulgulari olmayan mitral darligi olan hastalarda, sol ventrikul (LV) fonksiyonlarinin doku Doppler goruntuleme (TDI) ve strain/strain rate ekokardiyografi (SE/SRE) teknikleri ile degerlendirilmesidir.

Yontemler: Calismamiz enine-kesitli olarak dizayn edildi. Calismamiza 32 izole mitral darligi olan, mitral kapak alani <2.0 [cm.sup.2] (Grup 1) ve 25 saglikli gonullu birey (Grup 2) alindi. Tum bireylerin konvansiyonel ekokardiyografilerine ek olarak, TDI ve SE/SRE teknikleri uygulanarak LV fonksiyonlari degerlendirildi. Surekli degiskenlerin karsilastinlmasinda Studentt-testi, kategorik degiskenlerin karsilastirilmasinda Fisher-exact testi kullanildi.

Bulgular: Sistolik miyokardiyal hiz (Sm) Grup 1'de, Grup 2'den onemli oranda daha dusuk bulundu (6.0 [+ or -] 1.4 cm/sn karsin 7.9 [+ or -] 1.8 cm/sn, p<0.001), ayni zamanda erken diyastolik miyokardiyal hiz (Em) Grup 1'de, Grup 2'den onemli oranda daha dusuk bulundu (4.4 [+ or -] 1.5 cm/sn karsin 10.8 [+ or -] 2.1 cm/sn, p<0.001). Fakat iki grup arasinda gec diyastolik miyokardiyal hiz (Am)'lar acisindan anlamli bir farklilik gorulmedi. Grup 1'de septal duvar pik sistolik strain/strain rate degerleri, Grup 2'den anlamli olarak dusuk bulundu (p<0.001, p<0.001). Beraberinde Grup 1 lateral duvar pik sistolik strain/strain rate degerleri de Grup 2' den onemli oranda dusuk bulundu (p<0.001, p<0.001).

Sonuc: Bu ekokardiyografi metodlari ile global ejeksiyon fraksiyonlari normal ve klinik olarak kalp yetersizligi olmayan mitral darligi olan hastalarda LV disfonksiyonu oldugu goruldu. TDI ve strain/strain rate goruntuleme teknikleri, yeni ekokardiyografik yontemler olup mitral darlikli hastalarda erken evrede LV fonksiyonlarini degerlendirmede kullanilabilirler. (Anadolu Kardiyol Derg 2010; 10:328-33)

Anahtar kelimeler: Mitral darligi, ekokardiyografi, strain/strain rate goruntuleme, sol ventrikul fonksiyonlari

Introduction

Measuring myocardial performance has a critical importance in diagnosis and treatment of patients with cardiac diseases. The researches for the most appropriate method to measure contractile characteristics of myocardium are still carrying on.

Rheumatic mitral valve stenosis affects the left ventricle (LV) functions at various levels due to inflammatory and hemodynamic factors. Generally, LV systolic function in isolated mitral valve stenosis is well preserved (1). In a few patients with mitral valve stenosis, ultrastructural, pathological alterations might occur in the muscle cells of the LV. In proportion with these alterations, contractile functions of the LV also decrease (2). Subclinical systolic dysfunction has been shown via tissue Doppler imaging (TDI) in patients with mitral valve stenosis (3-5). In TDI velocity analysis, used for the evaluation of regional myocardial functions, some problems, such as continuing elongation of myocardium-like structures and transmission of active and passive deformation in adjacent segments have been encountered. Additionally, the heart becomes relatively distant from the transducer due to respiration, which affects velocities results (6). In order to overcome these problems, strain echocardiography (SE) and strain rate echocardiography (SRE) techniques have been developed. SE and SRE techniques are found to be superior to tissue Doppler velocities since they are independent from the push-pull effect of adjacent segments. While SE is affected by preload and heart rate, SRE shows parallelism to inotropic conditions and contractility, independently from the loading conditions (7,8). Recently, it was reported in several studies that, subclinical LV dysfunction was demonstrated via that imaging methods in patients having pure mitral stenosis and normal LV function with traditional echocardiography (9-11). In these studies, commonly, particular segments of LV were evaluated. However, in this study, we evaluated all of the LV segments globally.

The aim of the present study was to investigate whether the SE/SRE technique is advantageous in evaluation of LV systolic function in patients with pure mitral valve stenosis.

Methods

In the present cross-sectional study, 32 patients (25 females, 7 males; mean age 39 [+ or -] 8 years) with isolated mitral valve stenosis that were asymptomatic or had minimal symptoms (class I or class II according to NYHA) and 25 control cases (19 females, 6 males; mean age 38 [+ or -] 6 years) were included. According to the mitral valve area (MVA), 14 patients had mild stenosis (MVA: 1.52.0 [cm.sup.2]), 15 had moderate (MVA: 1-1.5 [cm.sup.2]), and 3 had severe stenosis (MVA: <1.0 [cm.sup.2]). None of the patients presented clinical symptoms of heart failure. Those with atrial fibrillation, diabetes mellitus, hypertension, coronary artery disease, moderatesevere aortic and mitral regurgitation, aortic stenosis, hyperthyroidism, chronic obstructive pulmonary disease, atrioventricular conduction abnormality, segmental wall motion abnormalities, severely calcified mitral valve structure, and decreased global LV systolic function were not included in this study.

All of the participants were informed about the procedure and their written consents obtained. The University's Ethics Committee granted approval for the present study.

Echocardiography

The echocardiographic examination was performed in the left lateral position with a Vingmed ultrasound system (Vingmed System 7, General Electric, Horten, Norway) and a 2.5 MHz transducer. The patients were monitored through a single-lead electrocardiogram. Diameters of the LV end-systolic (LVSD), LV end-diastolic (LVDD) and left atrium (LA), thickness of interventricular septum (IVS) and LV posterior wall (PW) were measured in M-mode from the parasternal long-axis (12). Right atrial (RA) and right ventricular (RV) diameters were measured from the apical four chambers. Peak and mean transmitral pressures were measured via Doppler. MVA was measured planimetrically in 2-dimensional (2D) images from the parasternal short axis and using the pressure half-time method by applying continuous wave (CW) Doppler during apical four-chamber view of the mitral valve. The area was calculated by the mean value of two measurements. The valvular insufficiency was evaluated by color flow Doppler imaging. LV ejection fraction (LVEF) was calculated via both Teichholz and modified Simpson's methods. Systolic myocardial velocity (Sm), early (Em) and late diastolic velocities (Am) were measured in the basal lateral segment and basal interventricular septum from the apical four chambers views using TDI. The velocities were calculated by the mean value of two measurements. Pulmonary artery systolic pressure (PASP) was measured by adding 10 mmHg, considering the diameter of vena cava inferior and the level of its collapse resultant from respiration, to the value measured by evaluating Bernoulli equation, which is simplified from tricuspid insufficiency velocities.

SE/SRE Imaging

Echocardiographic measurements were obtained by two different cardiologists separately and then mean value of the both measures was calculated. Firstly, the wall on which the measurements from 2D imaging would be performed was positioned parallel to the transducer and the tissue velocity imaging (TVI) function was selected. Color Doppler myocardial imaging of LV lateral, septal, anterior and inferior walls were obtained in apical two and four chambers views with a frame rate >120/s. The images were acquired including one wall by obtaining the probable narrowest angle and the maximum frame rate values. These images, consisting of a minimum of three sequential sinus beats atthe end of the expirium, were recorded on digital media. These color Doppler myocardial images were analyzed offline via Workstation, GE. Both longitudinal peak systolic strain rate (PSSR) and peak systolic strain (PSS) were measured from the basal, middle and apical segments of all walls (Fig. 1, 2). Measurements were performed just below the endocardium, by leaving a 10 mm distance between the two points. For each participant, either in patient or control groups, 12 segments were analyzed. Segments presenting either a weak image or an angle gradient greater than 25[degrees] were not evaluated.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Statistical analysis

The Statistical Package for the Social Sciences (SPSS Inc, Chicago, Illinois, USA) version 10.0 was used for statistical analysis. Continuous variables were expressed as mean ([+ or -]) standard deviation (SD). Student's t-test was used to compare the normally distributed continuous variable between the patients with mitral valve stenosis and the healthy control group. Fisher-exact test and Chi-square test were used to compare categorical variables.

Results

The echocardiographic and demographic parameters of the participants are shown in Table 1. The groups were similar in terms of age, gender and body mass index (BMI). There was no difference between the groups regarding echocardiographic parameters, namely the LVSD, LVDD, IVS, PW and LVEF. In the patient group, the mean MVA was 1.42 [+ or -] 0.3 [cm.sup.2], whereas the peak and the mean mitral pressure gradients were 16 [+ or -] 4.3 mmHg and 8.8 [+ or -] 2.8 mmHg, respectively. The diameters of LA, RA and RV were significantly greater in the patient group compared to the control group. The mean PASP was found to be 40+17.5 mmHg in the patient group.

Sm was significantly lower in Group 1 than in Group 2 (6.0 [+ or -] 1.4 cm/sec vs 7.9 [+ or -] 1.8 cm/sec, p<0.001). Also, Em was significantly lower in Group 1 than in Group 2 (4.4 [+ or -] 1.5 cm/sec vs 10.8 [+ or -] 2.1 cm/sec, p<0.001). However, there was no significant difference in Am between two groups.

Of the total 684 segments evaluated in patient and control groups, 56 segments (8%) for PSSR and 29 segments (4%) for PSS were excluded from the study due to increased angle gradient (>25[degrees]) and poor signal-image. The PSS and PSSR values of the basal, mid and apical segments of the LV's lateral, septal, anterior and inferior walls were found significantly lower in the patient group than the control group (p<0.001) (Table 2).

Discussion

In this study, a subclinical LV dysfunction was documented in patients having normal LV function and pure mitral stenosis that showed via traditional echocardiography methods.

Myocardial performance measurement has critical importance on diagnosis and treatment of patients with cardiac disease. Though how long time passed, studies for discovering the most useable method that can evaluate myocardial contractile capacity are still carrying on (13). Relatively a small number of studies for the patients with mitral stenosis according to evaluation of clinical and echocardiographic monitoring and progression of the disease are present in the literature. In a prospective clinical study that related to mitral stenosis patients with mean age of 28, it was reported that one half of the patients were asymptomatic at the time of diagnosis. Ten and twenty-year mortality rates were reported as 38% and 78%, respectively. Most of the death cases were resulted from heart failure or arterial emboli (14). In another study that related to mitral stenosis patients with mean age of 42, it was reported that at the time of diagnosis, 86% of the patients were asymptomatic and 10-year mortality rate was reported as higher (70%) (15). In the present study, mean age was 39.1 [+ or -] 8 years. It was closer to the reported in the second study. None of the patients had any signs of congestive heart failure. If high mortality rates were taken in account, the importance of earlier diagnosis was apparent whether patients were asymptomatic at the time of diagnosis.

Left ventricular functions can be evaluated by M-mode, 2-dimensional and Doppler echocardiography. Measurements by these methods differ from physician to physician. Therefore, global ejection fraction could be determined in normal limits and deteriorations at the subclinical level could not be revealed, until the end stage of mitral stenosis. In this study, we aimed to evaluate systolic functions via SE/SRE methods among asymptomatic mitral stenosis patients who had normal conventional echocardiography findings.

Ejection performance of the LV is decreased in certain patients with mitral stenosis. This physiopathology is multifactorial; chronically decreased preload and increased afterload, regional hypokinesia caused by expansion of the scarred mitral valve over the posterobasal myocardium, and decrease in LV compliance due to IVS movement to the left side resultant from the rapid filling of the RV are the probable factors (16). In our study, the global LV functions of the patients, measured via EE were within normal ranges. No segmental wall motion abnormalities were detected. The PASP was moderately increased and there was no difference between two groups regarding right heart dilatation. On the contrary, a considerable decrease was verified in LV systolic function on both SE and SRE.

Sengupta et al. (17) reported a significant improvement in tissue Doppler velocities after percutaneous mitral valvuloplasty in most of the patients with mitral stenosis that developed LV dysfunction. This improvement was found to be correlated with MVA and hemodynamic parameters. No improvement was observed in LVEF The LV myocardium is affected at different levels due to the rheumatic inflammatory process. Through electron microscopy, Lee et al. (2) showed that there were ultra structural pathological alterations within the myocardial cells of patients with mitral stenosis. These alterations were also seen within myofibrils and other cellular components. This finding was consistent in all the specimens examined regardless of the level of left ventricular contractile function. However, more extensive loss of myofibrils was detected in patients with impaired left ventricular ejection performance. This rheumatic process probably is partly responsible for the persistence of reduced ejection performance despite the improvement in preload and afterload after mitral valvuloplasty (18). All these changes indicate that a decrease in LV myocardial performance in patients with mitral stenosis is possibly caused by the inflammatory rheumatic process ratherthan hemodynamic parameters.

Measurement of myocardial functions via SE/SRE might be important to understand the physiological effects of valvular cardiac disease on the LV. Dray et al. (10) showed dramatic improvement after mitral balloon valvuloplasty with SE/SRE imaging method in fourteen- years- old patient with severe mitral stenosis and normal fractional shortening.

It has been shown that SRE is beneficial to determine the subclinical global dysfunction of LV long-axis and contractile reserve in asymptomatic patients with advanced mitral regurgitation (19). Through SE/SRE, Bauer et al. (20) demonstrated a dramatic improvement in global and regional systolic functions of the LV after percutaneous aortic valve replacement in patients with advanced aortic stenosis. Therefore, SE/SRE can be used to evaluate treatment response of the patients with cardiac valve disease.

The mitral valve is integrated with the other heart structures. The fibers at the subendocardial site array longitudinally and converge with the mitral annulus (21). Anterior mitral leaflet is bound both to the septum and the fibrous annulus of the heart and at the same time, it is a direct prolongation of the non-coronary cusp of the aortic valve. The posterior mitral valve runs along the free wall of the LV (22). Pathological events that affect the mitral valve can involve the LV functions as well. Currently, LV functions of patients with mitral stenosis are evaluated through M-mode, 2D, and Doppler echocardiography. However, it cannot detect an impairment of myocardial functions, particularly at an early phase. Despite its certain limitations, SE/SRE might be beneficial in detecting early phase myocardial function impairment. Early phase myocardial function impairment has been determined via these echocardiographic techniques in patients with amyloidosis, asymptomatic severe mitral insufficiency, end-stage chronic renal failure and morbid obesity (19,23-25). Nevertheless, there are not enough studies regarding these methods in patients with mitral stenosis.

Dogan et al. (9) found that the PSSR and end-systolic strain values at the IVS and basal segment of the lateral LV wall were significantly lower in patients with pure mitral stenosis, who had normal ejection fraction compared to healthy subjects. In our study as well, the SE/SRE value was found to be significantly lower in the patient group compared to the control group. However, if it is considered that fibrosis primarily affects the valve, and the adjacent structures in the case of mitral stenosis, measurements only at a basal level might not be appropriate and any comment about global LV functions based on these measurements will be wrong. Therefore, in this study, the measurements were performed not only at a basal level, but also at mid and apical segments as well. Furthermore, in addition to the LV lateral-septal wall, the inferior and anterior walls were also evaluated.

Ozdemir et al. (11) determined subclinical insufficiency in all of the basal segments and some of the mid segments in 60 patients with mild- moderate mitral stenosis. However, in that study, measurements were taken differently via average global longitudinal strain and strain rate imaging techniques.

Currently, there is no treatment regimen for the patients who have subclinical LV dysfunction consequent to mitral stenosis. The medical treatment of patients with mitral stenosis that do not have any complication such as pulmonary congestion and atrial fibrillation includes oral or monthly intramuscular penicillin, which is used for acute rheumatic fever prophylaxis (26). SE/ SRE may provide a new opportunity for earlier treatment in those patients with systolic dysfunction even it is asymptomatic. However, a higher number of advanced studies should be performed on this subject.

Study limitations

The most significant limiting factor on SE and SRE based on Doppler imaging is the angle. During longitudinal evaluation of LV functions, the angle gradient increases from basal to apical. The amount of deformation markedly changes when the angle gradient is over 25[degrees] (27). In the present study, tissue side had to be lower than 25[degrees] and the ultrasound waves were kept as parallel as possible.

Second important limitation is presence of artifacts. Particularly, respiration and body motion of the patient decrease image quality. Therefore, measurements cannot be obtained at certain segments. In order to overcome this obstacle, measurements were performed from the images taken at the end of the expirium and including a minimum of three cycles. The total rate of segments that could not be examined in patient and control groups was 4% for SE and 8% for SRE. Moreover, intra-observer and inter-observer variables were computed 7% and 12%, respectively. These values were within acceptable ranges.

Conclusion

In conclusion, it is well known that mitral stenosis negatively affects LV functions. Our study revealed subclinical impairment of myocardial contractility via SE/SRE in patients with isolated mitral stenosis whom LVEF was within normal ranges via conventional echocardiography. SE and SRE can be used as strong indicators of LV systolic functions in either asymptomatic or minimally symptomatic patients, who do not have any sign of heart failure. In addition, SE/SRE can be used as a beneficial method to evaluate treatment initiation and patient response during this time period.

Conflict of interest: None declared.

References

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Ziya Simsek, Sule Karakelleogdu [1], Fuat Giindogdu [1], Enbiya Aksakal [1], Serdar Sevimli [1], Sakir Arslan [1], Yekta Gurlertop [1], Huseyin Senocak [1]

Department of Cardiology, Erzurum Regional Training and Research Hospital, Erzurum

[1] Department of Cardiology, Faculty of Medicine, Ataturk University, Erzurum, Turkey

Address for Correspondence/Yazisma Adresi: Dr. Ziya Sjmsek, Osman Gazi Mah. Gokdemir Sitesi A Blok Kat 2 No: 525100, Erzurum, Turkey

Phone: +90 442 342 64 79 Fax: +90 442 316 63 40 E-mail: ziyamposta@hotmail.com

This study was partly presented at the EuroEcho 2008meeting, 10-13 December2008, Lyon, France

Accepted/Kabul Tarihi: 28.01.2010

doi: 10.5152/akd.2010.091
Table 1. General characteristics of the patients with mitral
stenosis and healthy controls

Variables              Group 1 (n=32)       Group 2 (n=25)       p **

Age, years             39 [+ or -] 8         38 [+ or -] 6       0.42
Gender, F/M, n *            25/7                 19/6            0.87
BMI, kg/[m.sup.2]    27.1 [+ or -] 3.4     26.5 [+ or -] 3       0.5
MVA, [cm.sup.2]      1.42 [+ or -] 0.3     --
LVDD, mm             45.6 [+ or -] 5.1     44.2 [+ or -] 4.1     0.26
LVSD, mm             30.4 [+ or -] 3.5       30 [+ or -] 3.6     0.13
IVS, mm               8.3 [+ or -] 1.1      8.9 [+ or -] 1.4     0.09
PW, mm                8.8 [+ or -] 1.2      9.1 [+ or -] 1.4     0.42
LVEF Teichholz, %    63.4 [+ or -] 3.9     65.4 [+ or -] 4.4     0.07
LVEF Simpson, %      62.3 [+ or -] 4.6     64.5 [+ or -] 4.3     0.08
LA, mm                 46 [+ or -] 6.8     32.2 [+ or -] 3.5    <0.001
RA, mm               37.8 [+ or -] 5.1     35.3 [+ or -] 2.7    <0.05
RV, mm               37.9 [+ or -] 5.2     34.6 [+ or -] 2.9    <0.05
PASP mmHg              40 [+ or -] 17.5           --

Data are presented as mean ([+ or -]) standard deviation and
* proportions ** Student's t-test and Fisher-exact tests.

BMI-body mass index, IVS--interventricular septum, LA-left atrium,
LVDD-left ventricle end-diastolic diameter, LVEF--left ventricle
ejection fraction, LVSD--left ventricle end-systolic diameter,
MVA--mitral valve area, PASP--pulmonary artery systolic pressure,
PW--posterior wall, RA--right atrium, RV--right ventricle

Table 2. Values of peak systolic strain and peak systolic strain
rate in studied groups

                                      Peak systolic strain

Variables            Group 1 (n=32)         Group 2 (n=25)        P *

Basal Lateral      -13.2 [+ or -] 1.7     -15.8 [+ or -] 1.8     <0.001
Mid Lateral        -13.4 [+ or -] 1.5     -17.4 [+ or -] 1.9     <0.001
Apical Lateral     -13.5 [+ or -] 1.9     -16.5 [+ or -] 1.9     <0.001
Basal anterior     -14.1 [+ or -] 1.7     -17.4 [+ or -] 2.0     <0.001
Mid Anterior       -14.2 [+ or -] 2.4     -17.7 [+ or -] 1.9     <0.001
Apical anterior    -14.5 [+ or -] 1.9     -17.3 [+ or -] 2.1     <0.001
Basal septum       -14.6 [+ or -] 1.9     -19.6 [+ or -] 1.7     <0.001
Mid septum         -14.8 [+ or -] 2.1     -20.7 [+ or -] 1.8     <0.001
Apical septum      -16.1 [+ or -] 1.7     -20.3 [+ or -] 2.1     <0.001
Basal inferior     -13.9 [+ or -] 1.7     -16.9 [+ or -] 1.2     <0.001
Mid inferior       -14.4 [+ or -] 2.4     -17.5 [+ or -] 1.4     <0.001
Apical inferior    -15.1 [+ or -] 1.3     -17.9 [+ or -] 2.1     <0.001

                                    Peak systolic strain rate

Variables            Group 1 (n=32)         Group 2 (n=25)        P *

Basal Lateral      -1.22 [+ or -] 0.14    -1.49 [+ or -] 0.20    <0.001
Mid Lateral        -1.21 [+ or -] 0.17    -1.48 [+ or -] 0.20    <0.001
Apical Lateral     -1.27 [+ or -] 0.2     -1.52 [+ or -] 0.20    <0.001
Basal anterior     -1.31 [+ or -] 0.14    -1.53 [+ or -] 0.15    <0.001
Mid Anterior       -1.32 [+ or -] 0.12    -1.57 [+ or -] 0.14    <0.001
Apical anterior    -1.36 [+ or -] 0.16    -1.57 [+ or -] 0.19    <0.001
Basal septum       -1.29 [+ or -] 0.16    -1.69 [+ or -] 0.20    <0.001
Mid septum         -1.30 [+ or -] 0.18    -1.66 [+ or -] 0.13    <0.001
Apical septum      -1.35 [+ or -] 0.16    -1.66 [+ or -] 0.17    <0.001
Basal inferior     -1.28 [+ or -] 0.15    -1.46 [+ or -] 0.15    <0.001
Mid inferior       -1.28 [+ or -] 0.15    -1.53 [+ or -] 0.18    <0.001
Apical inferior    -1.37 [+ or -] 0.11    -1.55 [+ or -] 0.21    <0.001

Data are presented as mean ([+ or -]) standard deviation

* Student's t-test
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Title Annotation:Original Investigation/Ozgun Arastirma
Author:Simsek, Ziya; Karakelleoglu, Sule; Gundogdu, Fuat; Aksakal, Enbiya; Sevimli, Serdar; Arslan, Sakir;
Publication:The Anatolian Journal of Cardiology (Anadolu Kardiyoloji Dergisi)
Article Type:Report
Geographic Code:7TURK
Date:Aug 1, 2010
Words:4942
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