Scandinavian Cardiovascular Journal, 2014; 48: 79–84
ORIGINAL ARTICLE
Effects of respiration on the velocity of tricuspid regurgitation and estimation of systolic pulmonary artery pressure in patients with right ventricle systolic dysfunction
XIAO-YONG ZHANG & YU-ZENG DING Department of Ultrasound Diagnostics, Shanxi Provincial People’s Hospital, Xi’an, P. R. China
Abstract Objective. We investigated the effects of quiet respiration on the peak velocity of tricuspid regurgitation (TR) and estimation of systolic pulmonary artery pressure (SPAP) in patients with right ventricle (RV) systolic dysfunction using Doppler echocardiography. Methods. Continuous-wave Doppler spectra of TR were recorded in 32 patients with and 28 controls without RV systolic dysfunction. Electrocardiography and respiratory tracing were recorded simultaneously. Expiratory and inspiratory peak velocities of TR were acquired and averaged for five consecutive respiratory cycles. The SPAP during expiration and inspiration was calculated. Results. The velocity of TR and SPAP was not significantly different between expiration and inspiration in controls (2.77 ⫾ 0.23 and 2.82 ⫾ 0.26 m/s, P ⫽ 0.776; 35.94 ⫾ 4.96 and 36.18 ⫾ 5.12 mmHg, P ⫽ 0.747), whereas the velocity of TR and SPAP decreased significantly from expiration to inspiration in patients with RV systolic dysfunction (3.27 ⫾ 0.35 and 2.59 ⫾ 0.22 m/s, P ⬍ 0.001; 53.72 ⫾ 7.39, 38.45 ⫾ 5.63 mmHg, P ⬍ 0.001). Conclusions. Quiet respiration has significant effects on the velocity of TR in patients with RV systolic dysfunction. This factor should be taken into account when using Doppler echocardiography to estimate these patients’ SPAP, and the measurements should be performed in patients at the end of expiration. Key words: Doppler echocardiography, quiet respiration, systolic pulmonary artery pressure, velocity of tricuspid regurgitation
Introduction Noninvasive determination of systolic pulmonary artery pressure (SPAP) using echocardiography is a widely utilized method. It relies mainly on measurements of the velocity of tricuspid regurgitation (TR) using a simplified Bernoulli equation to calculate gains in tricuspid pressure gradients. However, this noninvasive method is affected by many factors, including the effects of respiration on the velocity of TR and estimation of SPAP. These effects have seldom been studied and, if they have been studied, have provided inconsistent results (1–3). Presently, mechanisms of the effects of respiration on hemodynamics still remain unknown (3–6). In the present study, we investigated the effects of quiet respiration on the velocity of TR and SPAP in patients with right ventricle (RV) systolic dysfunction. We then compared the data with those of
patients without RV systolic dysfunction. We sought to investigate whether quiet respiration affects the velocity of TR and SPAP in patients with RV systolic dysfunction as well as to explore the potential mechanisms of action. Methods This research protocol was approved by the Review Board of the Shanxi Provincial People’s Hospital (Xi’an, China). Written informed consent was received from all subjects whose data were used. Subjects From January to May 2012, 32 consecutive patients (17 males; age range, 38–79 years; mean age, 54.2 years) with RV systolic dysfunction accompanied by
Correspondence: Xiao-Yong Zhang, MD, Department of Ultrasound Diagnostics, Shanxi Provincial People’s Hospital, No. 256, Youyi West Road, Bei Lin District, Xi’an 710068, P. R. China. Tel: ⫹ 86-29-84777898. Fax: ⫹ 86-29-83510181. E-mail: [email protected] (Received 25 July 2013 ; revised 7 December 2013 ; accepted 10 December 2013) ISSN 1401-7431 print/ISSN 1651-2006 online © 2014 Informa Healthcare DOI: 10.3109/14017431.2013.875624
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variable degrees (mild to severe) of TR from our inpatient department were enrolled. At first, there were 59 RV systolic dysfunction patients eligible before consent was asked, of which 27 patients were not included since they were not interested in taking part in the study, and at last 32 patients were recruited in this study. Of these 32 subjects, nine cases had coronary heart disease (CHD), seven had hypertension, six had pulmonary heart disease, five had dilated cardiomyopathy, four had mitral stenosis of rheumatic heart disease, and one had peripartum cardiomyopathy. No patient had acute RV systolic dysfunction. Twenty-eight patients (15 males; age range, 33–75 years; mean age, 52.3 years) with normal right ventricular function accompanied with variable degrees (mild to severe) of TR from our inpatient department were selected based on ageand sex-matched RV systolic dysfunction patients as control subjects. Of these 28 subjects, seven cases had CHD, six had hypertension, three had pulmonary heart disease, three had mitral stenosis of rheumatic heart disease, three had a chest infection, and six cases had undiagnosed disease. Common characteristics of the patients are described in Table I. We ensured that subjects with RV systolic dysfunction and control subjects did not have organic tricuspid-valve disease. Inclusion criteria for the present study were (i) TR of a mild degree and holosystolic type as assessed using color Doppler flow imaging, (ii) stable TR and clear Doppler spectra envelopes as displayed by continuous-wave Doppler flow imaging, and (iii) regular cardiac rhythms. Exclusion criteria included absent or trivial TR, apparent arrhythmia, moderate-to-large pericardial effusion, restrictive cardiomyopathy, and congenital heart diseases.
Three main definitions for determining RV systolic dysfunction were (7,8) (i) changes in fractional area of the RV less than 35% as measured by a two-dimensional echocardiography; (ii) tricuspid annular plane systolic excursion (TAPSE) less than 16 mm as displayed by a M-mode echocardiography; and (iii) tricuspid annular plane systolic velocity (S′) less than 10 cm/s as determined by a tissue Doppler velocity imaging. Enrolled RV systolic dysfunction patients satisfied all of the above definitions. Study protocol A Siemens Sequoia 512 echocardiographic system (Siemens, Munich, Germany) was used with a 4–V1c probe and frequencies of 2.5–4.0 MHz. All cases were examined by an experienced sonographer blinded to the diagnosis. The left lateral decubitus position was adopted in all subjects with quiet breathing. Respiratory curves and electrocardiography (ECG) were recorded simultaneously. Initially, the parameters of left ventricle ejection fraction (LVEF), RV middle diameter (RVMD), RV outflow tract diameter (RVOTD), RV fractional area change (FAC), TAPSE, and S′ were measured. We then studied the effects of respiration on TR velocity. We obtained clear images in the modified parasternal long axis view including the tricuspid valve, apical four-chamber view, and short axis of aortic valve view. We then focused on the area under the tricuspid valve. TR velocity was detected using a continuous Doppler function. The probe position was adjusted to ensure that the plane of maximum TR was always included in the ultrasound beam during the respiratory
Table I. Demographic characteristics of the control and RV systolic dysfunction patients.
Age, years Male/female Height, cm Weight, kg BMI, kg/m2 Heart rate, beats/minute SBP, mmHg DBP, mmHg LVEF, % RVMD, mm RVOTD, mm FAC, % TAPSE, mm S′, cm/s
Controls (n ⫽ 28)
RV systolic dysfunction (n ⫽ 32)
P
52.3 ⫾ 19 15/13 166.2 ⫾ 6.3 58.9 ⫾ 6.1 21.31 ⫾ 1.95 71.3 ⫾ 8.9 129.4 ⫾ 12.7 76.8 ⫾ 7.1 68.7 ⫾ 7.5 27.5 ⫾ 2.1 25.6 ⫾ 2.3 45.2 ⫾ 5.1 20.7 ⫾ 1.8 12.6 ⫾ 1.0
54.2 ⫾ 18 18/14 165.3 ⫾ 6.2 57.2 ⫾ 5.8 20.91 ⫾ 1.97 72.6 ⫾ 11.5 128.1 ⫾ 13.6 75.1 ⫾ 7.2 67.9 ⫾ 6.4 39.4 ⫾ 3.2 33.8 ⫾ 2.2 31.4 ⫾ 3.3 14.1 ⫾ 1.6 9.0 ⫾ 0.7
NS NS NS NS NS NS NS NS NS ⬍ 0.001 ⬍ 0.001 ⬍ 0.001 ⬍ 0.001 ⬍ 0.001
BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; LVEF, left ventricular ejection fraction; RVMD, right ventricular middle diameter; RVOTD, right ventricular outflow tract diameter; FAC, fractional area change; TAPSE, tricuspid annular plane systolic excursion; S′, tricuspid annular plane systolic velocity.
Effects of respiration on SPAP cycle,and ultrasound beam angle was adjusted to be as parallel as possible to the direction of maximum TR. To avoid overestimating the TR signal, appropriate Doppler gains were acquired for all tests. Five consecutive measurements of the velocity of TR were averaged during the inspiration phase or expiration phase. The scan sweep was set to 50 mm/s (or 25 mm/s) simultaneously. Tricuspid pressure gradients were acquired based on the velocity of TR measured using Doppler echocardiography according to the simplified Bernoulli equation (ΔP ⫽ 4V2). Right atrial pressure (RAP) was estimated by the diameter of the inferior vena cava and its response to inspiration, as previously described (9–10). SPAP was calculated during different respiratory phases based on the formula SPAP ⫽ RAP ⫹ ΔP. Statistical analyses SPSS ver13.0 statistical software (SPSS, Chicago, IL, USA) was used. Data are presented as mean ⫾ standard deviation. Continuous data were compared using a paired Student’s t-test. P ⬍ 0.05 was considered statistically significant. Results Clinical characteristics and the results of routine echocardiographic examination in RV systolic dysfunction and control groups There were no significant differences between the two groups with respect to age, sex, body mass index
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(BMI), heart rate, systolic blood pressure (SBP), and diastolic blood pressure (DBP). Statistical analysis showed no significant differences between the two groups with regard to LVEF. RVMD and RVOTD were significantly higher and FAC, TAPSE, and S′ were significantly lower in patients with RV systolic dysfunction than in controls (Table I). Velocity of TR, pressure gradients and SPAP in RV systolic dysfunction patients and controls during the inspiratory and expiratory phases In controls, no significant difference between inspiratory and expiratory phases was found in TR velocity (Figure 1), pressure gradients, or SPAP (P ⬎ 0.05). In RV systolic dysfunction patients, significant difference between the inspiratory and expiratory phases was found in TR velocity (Figure 2), pressure gradients, and SPAP (P ⬍ 0.001) (Table II). Discussion In 1980, Skjaerpe and Hatle (11) proposed that the pressure gradient across a regurgitant tricuspid valve could be estimated from the peak velocity of the systolic trans-tricuspid jet recorded using Doppler ultrasound. The authors concluded that prediction of RV systolic pressure (RVSP) should be possible in patients with TR by adding the Doppler-determined trans-tricuspid pressure gradient to the RAP estimated clinically. In 1984, Yock and Popp (12) studied 62 patients with clinical signs
Figure 1. Continuous-wave Doppler spectra displaying respiratory variance of TR velocity in a 59-year-old control man. In turn, the spectra of TR velocity, respiratory curve (ascending branch represents the inspiratory phase and the descending branch represents the expiratory phase) and ECG. There is no significant change in the TR velocity between the inspiratory and expiratory phases.
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Figure 2. Continuous-wave Doppler spectra displaying respiratory variance of TR velocity in a 64-year-old woman with RV systolic dysfunction. TR velocity in the inspiratory phase decreases significantly compared with that in the expiratory phase.
of elevated right-sided pressures. They used continuous-wave Doppler ultrasonography to record the maximum velocity of TR, and used the simplified Bernoulli equation (ΔP ⫽ 4V2) to calculate the systolic pressure gradient, with the sum of tricuspid gradient and RAP being RVSP. Their results demonstrated that the tricuspid gradient method correlated with catheterization values. In the absence of a RV outflow tract or pulmonary valve stenosis, RVSP is almost equal to SPAP. When using the tricuspid gradient method to estimate SPAP, the error comes mainly from the velocity of TR measured using Doppler ultrasonography. Many factors affect the measurement of TR. For instance, during quiet respiration, the thorax and heart may undergo a little displacement, which may result in a displacement of the focal area of continuous Doppler near the orifice of the tricuspid valve. However, because valve regurgitation is usually a jet beam, this displacement affects only the quality of the spectrum recorded. If the reflux spectrum has a complete envelope line, it may not
affect the measurement of TR velocity (2). Another factor is the angle between the ultrasound beam and reflux beam (13). Two-dimensional echocardiography cannot comprehensively and accurately display the direction of the TR beam, but by adjusting the probe position and rotating the scanning plane, in most cases, the reflux beam can be included in the scanning plane. With respect to the relationship between respiration and TR velocity, previous studies concluded that respiration affects the velocity of TR, but did not undertake the noninvasive measurement of SPAP (2). Our results showed that there were significant effects of quiet breathing on TR velocity in subjects with RV systolic dysfunction, and that TR velocity decreased during the inspiratory phase and increased during the expiratory phase. Changes in TR velocity were converted to tricuspid pressure gradients; the maximum difference was less than or equal to 15 mmHg. The mechanisms of respiratory effects on hemodynamics are controversial. We believe that the
Table II. Velocity of TR, pressure gradient, and SPAP during the inspiratory or expiratory phase in control and RV systolic dysfunction patients. Controls (n ⫽ 28)
Expiration Inspiration Change with inspiration P
RV systolic dysfunction (n ⫽ 32)
Velocity of TR (m/s)
Pressure gradient (mmHg)
SPAP (mmHg)
Velocity of TR (m/s)
Pressure gradient (mmHg)
SPAP (mmHg)
2.77 ⫾ 0.23 2.82 ⫾ 0.26 0.05 ⫾ 0.01 0.766
31.09 ⫾ 4.83 31.4 ⫾ 4.96 0.30 ⫾ 0.03 0.478
35.94 ⫾ 4.96 36.18 ⫾ 5.12 0.29 ⫾ 0.04 0.747
3.27 ⫾ 0.35 2.59 ⫾ 0.22 ⫺0.67 ⫾ 0.08 ⬍ 0.001
42.51 ⫾ 6.84 27.01 ⫾ 4.32 ⫺15.49 ⫾ 3.26 ⬍ 0.001
53.72 ⫾ 7.39 38.45 ⫾ 5.63 ⫺15.46 ⫾ 3.15 ⬍ 0.001
Effects of respiration on SPAP mechanisms of these phenomena involve a reduction in intrathoracic pressures during inspiration that cause a decline in the pressure in the right side of the heart. However, the decline in the RAP is almost entirely offset by increased venous return. Hence, only the pressure in the RV declines. The reduction in intrathoracic pressure during inspiration causes a decline in trans-tricuspid pressure gradients in systole, and the velocity of TR decreases. Conversely, reduced RV pressure during inspiration causes an increase in RV volume in diastole, and RV contractile forces, which increase the velocity of TR. Therefore, the effects of inspiration on the velocity of TR are the combined results of these two factors. For patients with normal RV function, these two factors offset each other, so there will be a smaller (or nonsignificant) influence of quiet breathing on TR velocity. For patients with RV systolic dysfunction, increased diastolic filling does not increase RV contractile forces, so the velocity of TR will decrease during inspiration. Clinical perspective: The present study showed that quiet inspiration can cause a decrease in TR velocity and underestimation of SPAP. Taking into account that the changes in intrathoracic pressure during quiet inspiration total ~4 mmHg, if subjects have an airway obstruction, deep breathing caused by acidosis (Kussmaul breathing) or forced inspiration in dyspnea, the changes in intrathoracic pressure will be much greater, so the errors in estimating SPAP using echocardiography will also be much greater. Accurately assessing SPAP in these patients is very important. According to the results of the present study, we believe that the use of echocardiography for measuring TR velocity should be performed when patients are at the end of expiration.This practice will avoid the reduced intrathoracic pressure during inspiration that leads to a decreased velocity of TR and an underestimation of SPAP. This measure can improve the accuracy and comparability in the noninvasive estimation of SPAP using Doppler echocardiography. There were several limitations in the present study. First, we did not divide the subjects into groups in terms of the causes of RV systolic dysfunction, thereby ignoring the possible impact of various diseases and their clinical parameters on the results. Second, we did not study the three-dimensional shape and area of the orifice of the tricuspid valve as well as other parameters related to TR (e.g., velocity time integral in the respiratory cycle). However, according to the simplified Bernoulli equation ( P ⫽ 4V2), TR velocity is related only to the crosstricuspid pressure gradient, and has no relationship with the area of the tricuspid valve orifice or other factors mentioned above, so bias was not introduced
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into the results. Third, the numbers in this study were small, and further studies should be performed. In summary, quiet inspiration can cause a decrease in the velocity of TR in patients with RV systolic dysfunction. This factor should be taken into account when using Doppler echocardiography to estimate these patients’ SPAP, and the measurements should be performed when patients are at the end of expiration.
Acknowledgment We acknowledge the enthusiastic participation of all subjects in this study and are particularly grateful to Ling Jiang Wei from the Chindex International Trade Co., Ltd (Xi’an, China), for technology assistance. We thank Medjaden Bioscience Limited for assisting in the preparation of this manuscript. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Klodas E, Nishimura RA, Appleton CP, Redfield MM, Oh JK. Doppler evaluation of patients with constrictive pericarditis: use of tricuspid regurgitation velocity curves to determine enhanced ventricular interaction. J Am Coll Cardiol. 1996;28:652–7. 2. Xiong HQ, Cao TS, Luo XH, Yuan LJ, Duan YY. Effects of the thoracic pressure on the velocity of tricuspid regurgitation and estimation of pulmonary artery systolic pressure. Chinese J Ultrasonography 2009;18:284–7. 3. Topilsky Y, Tribouilloy C, Michelena HI, Pislaru S, Mahoney DW, Enriquez-Sarano M. Pathophysiology of tricuspid regurgitation: quantitative Doppler echocardiographic assessment of respiratory dependence. Circulation. 2010;122:1505–13. 4. Braunwald E. Heart disease: a textbook of cardiovascular medicine. Philadelphia, PA: Saunders WB Publishing Press; 2001. pp. 1825–45. 5. Yuan L, Cao T, Duan Y, Yang G, Wang Z, Ruan L. Noninvasive assessment of influence of resistant respiration on blood flow velocities across the cardiac valves in human: a quantification study by echocardiography. Echocardiography. 2004;21: 391–8. 6. Li Y, Yuan LJ, Cao TS, Jian HP, Liu J. Effects of respiration on pulmonary venous flow and its clinical applications by Doppler echocardiography. Echocardiography. 2009;26: 150–4. 7. Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, et al. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American society of echocardiography. J Am Soc Echocardiogr. 2010;23:685–713. 8. Carvalho VT, Barbosa MM, Nunes MC, Cardoso YS, de Sá Filho IM, Oliveira FR, et al. Early right cardiac dysfunction in patients with schistosomiasis mansoni. Echocardiography. 2011;28:261–7.
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9. Kircher BJ, Himelman RB, Schiller NB. Noninvasive estimation of right atrial pressure from the inspiratory collapse of the inferior vena cava. Am J Cardiol. 1990;66: 493–6. 10. Nagueh SF, Kopelen HA, Zoghbi WA. Relation of mean right atrial pressure to echocardiographic and Doppler parameters of right atrial and right ventricular function. Circulation. 1996;93:1160–9. 11. Skjaerpe T, Hatle L. Diagnosis and assessment of tricuspid regurgitation with Doppler ultrasound. In:
Rijsterborgh H, ed. Echocardiology. The Hague: Martinus Nijhoff Publishing Press; 1981. pp 299–304. 12. Yock PG, Popp RL. Noninvasive estimation of right ventricular systolic pressure by Doppler ultrasound in patients with tricuspid regurgitation. Circulation. 1984;70: 657–62. 13. Abramson SV, Burke JB, Pauletto FJ, Kelly JJ Jr. Use of multiple views in the echocardiographic assessment of pulmonary artery systolic pressure. J Am Soc Echocardiogr. 1995;8:55–60.
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ORIGINAL ARTICLE
Effects of respiration on the velocity of tricuspid regurgitation and estimation of systolic pulmonary artery pressure in patients with right ventricle systolic dysfunction
XIAO-YONG ZHANG & YU-ZENG DING Department of Ultrasound Diagnostics, Shanxi Provincial People’s Hospital, Xi’an, P. R. China
Abstract Objective. We investigated the effects of quiet respiration on the peak velocity of tricuspid regurgitation (TR) and estimation of systolic pulmonary artery pressure (SPAP) in patients with right ventricle (RV) systolic dysfunction using Doppler echocardiography. Methods. Continuous-wave Doppler spectra of TR were recorded in 32 patients with and 28 controls without RV systolic dysfunction. Electrocardiography and respiratory tracing were recorded simultaneously. Expiratory and inspiratory peak velocities of TR were acquired and averaged for five consecutive respiratory cycles. The SPAP during expiration and inspiration was calculated. Results. The velocity of TR and SPAP was not significantly different between expiration and inspiration in controls (2.77 ⫾ 0.23 and 2.82 ⫾ 0.26 m/s, P ⫽ 0.776; 35.94 ⫾ 4.96 and 36.18 ⫾ 5.12 mmHg, P ⫽ 0.747), whereas the velocity of TR and SPAP decreased significantly from expiration to inspiration in patients with RV systolic dysfunction (3.27 ⫾ 0.35 and 2.59 ⫾ 0.22 m/s, P ⬍ 0.001; 53.72 ⫾ 7.39, 38.45 ⫾ 5.63 mmHg, P ⬍ 0.001). Conclusions. Quiet respiration has significant effects on the velocity of TR in patients with RV systolic dysfunction. This factor should be taken into account when using Doppler echocardiography to estimate these patients’ SPAP, and the measurements should be performed in patients at the end of expiration. Key words: Doppler echocardiography, quiet respiration, systolic pulmonary artery pressure, velocity of tricuspid regurgitation
Introduction Noninvasive determination of systolic pulmonary artery pressure (SPAP) using echocardiography is a widely utilized method. It relies mainly on measurements of the velocity of tricuspid regurgitation (TR) using a simplified Bernoulli equation to calculate gains in tricuspid pressure gradients. However, this noninvasive method is affected by many factors, including the effects of respiration on the velocity of TR and estimation of SPAP. These effects have seldom been studied and, if they have been studied, have provided inconsistent results (1–3). Presently, mechanisms of the effects of respiration on hemodynamics still remain unknown (3–6). In the present study, we investigated the effects of quiet respiration on the velocity of TR and SPAP in patients with right ventricle (RV) systolic dysfunction. We then compared the data with those of
patients without RV systolic dysfunction. We sought to investigate whether quiet respiration affects the velocity of TR and SPAP in patients with RV systolic dysfunction as well as to explore the potential mechanisms of action. Methods This research protocol was approved by the Review Board of the Shanxi Provincial People’s Hospital (Xi’an, China). Written informed consent was received from all subjects whose data were used. Subjects From January to May 2012, 32 consecutive patients (17 males; age range, 38–79 years; mean age, 54.2 years) with RV systolic dysfunction accompanied by
Correspondence: Xiao-Yong Zhang, MD, Department of Ultrasound Diagnostics, Shanxi Provincial People’s Hospital, No. 256, Youyi West Road, Bei Lin District, Xi’an 710068, P. R. China. Tel: ⫹ 86-29-84777898. Fax: ⫹ 86-29-83510181. E-mail: [email protected] (Received 25 July 2013 ; revised 7 December 2013 ; accepted 10 December 2013) ISSN 1401-7431 print/ISSN 1651-2006 online © 2014 Informa Healthcare DOI: 10.3109/14017431.2013.875624
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variable degrees (mild to severe) of TR from our inpatient department were enrolled. At first, there were 59 RV systolic dysfunction patients eligible before consent was asked, of which 27 patients were not included since they were not interested in taking part in the study, and at last 32 patients were recruited in this study. Of these 32 subjects, nine cases had coronary heart disease (CHD), seven had hypertension, six had pulmonary heart disease, five had dilated cardiomyopathy, four had mitral stenosis of rheumatic heart disease, and one had peripartum cardiomyopathy. No patient had acute RV systolic dysfunction. Twenty-eight patients (15 males; age range, 33–75 years; mean age, 52.3 years) with normal right ventricular function accompanied with variable degrees (mild to severe) of TR from our inpatient department were selected based on ageand sex-matched RV systolic dysfunction patients as control subjects. Of these 28 subjects, seven cases had CHD, six had hypertension, three had pulmonary heart disease, three had mitral stenosis of rheumatic heart disease, three had a chest infection, and six cases had undiagnosed disease. Common characteristics of the patients are described in Table I. We ensured that subjects with RV systolic dysfunction and control subjects did not have organic tricuspid-valve disease. Inclusion criteria for the present study were (i) TR of a mild degree and holosystolic type as assessed using color Doppler flow imaging, (ii) stable TR and clear Doppler spectra envelopes as displayed by continuous-wave Doppler flow imaging, and (iii) regular cardiac rhythms. Exclusion criteria included absent or trivial TR, apparent arrhythmia, moderate-to-large pericardial effusion, restrictive cardiomyopathy, and congenital heart diseases.
Three main definitions for determining RV systolic dysfunction were (7,8) (i) changes in fractional area of the RV less than 35% as measured by a two-dimensional echocardiography; (ii) tricuspid annular plane systolic excursion (TAPSE) less than 16 mm as displayed by a M-mode echocardiography; and (iii) tricuspid annular plane systolic velocity (S′) less than 10 cm/s as determined by a tissue Doppler velocity imaging. Enrolled RV systolic dysfunction patients satisfied all of the above definitions. Study protocol A Siemens Sequoia 512 echocardiographic system (Siemens, Munich, Germany) was used with a 4–V1c probe and frequencies of 2.5–4.0 MHz. All cases were examined by an experienced sonographer blinded to the diagnosis. The left lateral decubitus position was adopted in all subjects with quiet breathing. Respiratory curves and electrocardiography (ECG) were recorded simultaneously. Initially, the parameters of left ventricle ejection fraction (LVEF), RV middle diameter (RVMD), RV outflow tract diameter (RVOTD), RV fractional area change (FAC), TAPSE, and S′ were measured. We then studied the effects of respiration on TR velocity. We obtained clear images in the modified parasternal long axis view including the tricuspid valve, apical four-chamber view, and short axis of aortic valve view. We then focused on the area under the tricuspid valve. TR velocity was detected using a continuous Doppler function. The probe position was adjusted to ensure that the plane of maximum TR was always included in the ultrasound beam during the respiratory
Table I. Demographic characteristics of the control and RV systolic dysfunction patients.
Age, years Male/female Height, cm Weight, kg BMI, kg/m2 Heart rate, beats/minute SBP, mmHg DBP, mmHg LVEF, % RVMD, mm RVOTD, mm FAC, % TAPSE, mm S′, cm/s
Controls (n ⫽ 28)
RV systolic dysfunction (n ⫽ 32)
P
52.3 ⫾ 19 15/13 166.2 ⫾ 6.3 58.9 ⫾ 6.1 21.31 ⫾ 1.95 71.3 ⫾ 8.9 129.4 ⫾ 12.7 76.8 ⫾ 7.1 68.7 ⫾ 7.5 27.5 ⫾ 2.1 25.6 ⫾ 2.3 45.2 ⫾ 5.1 20.7 ⫾ 1.8 12.6 ⫾ 1.0
54.2 ⫾ 18 18/14 165.3 ⫾ 6.2 57.2 ⫾ 5.8 20.91 ⫾ 1.97 72.6 ⫾ 11.5 128.1 ⫾ 13.6 75.1 ⫾ 7.2 67.9 ⫾ 6.4 39.4 ⫾ 3.2 33.8 ⫾ 2.2 31.4 ⫾ 3.3 14.1 ⫾ 1.6 9.0 ⫾ 0.7
NS NS NS NS NS NS NS NS NS ⬍ 0.001 ⬍ 0.001 ⬍ 0.001 ⬍ 0.001 ⬍ 0.001
BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; LVEF, left ventricular ejection fraction; RVMD, right ventricular middle diameter; RVOTD, right ventricular outflow tract diameter; FAC, fractional area change; TAPSE, tricuspid annular plane systolic excursion; S′, tricuspid annular plane systolic velocity.
Effects of respiration on SPAP cycle,and ultrasound beam angle was adjusted to be as parallel as possible to the direction of maximum TR. To avoid overestimating the TR signal, appropriate Doppler gains were acquired for all tests. Five consecutive measurements of the velocity of TR were averaged during the inspiration phase or expiration phase. The scan sweep was set to 50 mm/s (or 25 mm/s) simultaneously. Tricuspid pressure gradients were acquired based on the velocity of TR measured using Doppler echocardiography according to the simplified Bernoulli equation (ΔP ⫽ 4V2). Right atrial pressure (RAP) was estimated by the diameter of the inferior vena cava and its response to inspiration, as previously described (9–10). SPAP was calculated during different respiratory phases based on the formula SPAP ⫽ RAP ⫹ ΔP. Statistical analyses SPSS ver13.0 statistical software (SPSS, Chicago, IL, USA) was used. Data are presented as mean ⫾ standard deviation. Continuous data were compared using a paired Student’s t-test. P ⬍ 0.05 was considered statistically significant. Results Clinical characteristics and the results of routine echocardiographic examination in RV systolic dysfunction and control groups There were no significant differences between the two groups with respect to age, sex, body mass index
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(BMI), heart rate, systolic blood pressure (SBP), and diastolic blood pressure (DBP). Statistical analysis showed no significant differences between the two groups with regard to LVEF. RVMD and RVOTD were significantly higher and FAC, TAPSE, and S′ were significantly lower in patients with RV systolic dysfunction than in controls (Table I). Velocity of TR, pressure gradients and SPAP in RV systolic dysfunction patients and controls during the inspiratory and expiratory phases In controls, no significant difference between inspiratory and expiratory phases was found in TR velocity (Figure 1), pressure gradients, or SPAP (P ⬎ 0.05). In RV systolic dysfunction patients, significant difference between the inspiratory and expiratory phases was found in TR velocity (Figure 2), pressure gradients, and SPAP (P ⬍ 0.001) (Table II). Discussion In 1980, Skjaerpe and Hatle (11) proposed that the pressure gradient across a regurgitant tricuspid valve could be estimated from the peak velocity of the systolic trans-tricuspid jet recorded using Doppler ultrasound. The authors concluded that prediction of RV systolic pressure (RVSP) should be possible in patients with TR by adding the Doppler-determined trans-tricuspid pressure gradient to the RAP estimated clinically. In 1984, Yock and Popp (12) studied 62 patients with clinical signs
Figure 1. Continuous-wave Doppler spectra displaying respiratory variance of TR velocity in a 59-year-old control man. In turn, the spectra of TR velocity, respiratory curve (ascending branch represents the inspiratory phase and the descending branch represents the expiratory phase) and ECG. There is no significant change in the TR velocity between the inspiratory and expiratory phases.
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Figure 2. Continuous-wave Doppler spectra displaying respiratory variance of TR velocity in a 64-year-old woman with RV systolic dysfunction. TR velocity in the inspiratory phase decreases significantly compared with that in the expiratory phase.
of elevated right-sided pressures. They used continuous-wave Doppler ultrasonography to record the maximum velocity of TR, and used the simplified Bernoulli equation (ΔP ⫽ 4V2) to calculate the systolic pressure gradient, with the sum of tricuspid gradient and RAP being RVSP. Their results demonstrated that the tricuspid gradient method correlated with catheterization values. In the absence of a RV outflow tract or pulmonary valve stenosis, RVSP is almost equal to SPAP. When using the tricuspid gradient method to estimate SPAP, the error comes mainly from the velocity of TR measured using Doppler ultrasonography. Many factors affect the measurement of TR. For instance, during quiet respiration, the thorax and heart may undergo a little displacement, which may result in a displacement of the focal area of continuous Doppler near the orifice of the tricuspid valve. However, because valve regurgitation is usually a jet beam, this displacement affects only the quality of the spectrum recorded. If the reflux spectrum has a complete envelope line, it may not
affect the measurement of TR velocity (2). Another factor is the angle between the ultrasound beam and reflux beam (13). Two-dimensional echocardiography cannot comprehensively and accurately display the direction of the TR beam, but by adjusting the probe position and rotating the scanning plane, in most cases, the reflux beam can be included in the scanning plane. With respect to the relationship between respiration and TR velocity, previous studies concluded that respiration affects the velocity of TR, but did not undertake the noninvasive measurement of SPAP (2). Our results showed that there were significant effects of quiet breathing on TR velocity in subjects with RV systolic dysfunction, and that TR velocity decreased during the inspiratory phase and increased during the expiratory phase. Changes in TR velocity were converted to tricuspid pressure gradients; the maximum difference was less than or equal to 15 mmHg. The mechanisms of respiratory effects on hemodynamics are controversial. We believe that the
Table II. Velocity of TR, pressure gradient, and SPAP during the inspiratory or expiratory phase in control and RV systolic dysfunction patients. Controls (n ⫽ 28)
Expiration Inspiration Change with inspiration P
RV systolic dysfunction (n ⫽ 32)
Velocity of TR (m/s)
Pressure gradient (mmHg)
SPAP (mmHg)
Velocity of TR (m/s)
Pressure gradient (mmHg)
SPAP (mmHg)
2.77 ⫾ 0.23 2.82 ⫾ 0.26 0.05 ⫾ 0.01 0.766
31.09 ⫾ 4.83 31.4 ⫾ 4.96 0.30 ⫾ 0.03 0.478
35.94 ⫾ 4.96 36.18 ⫾ 5.12 0.29 ⫾ 0.04 0.747
3.27 ⫾ 0.35 2.59 ⫾ 0.22 ⫺0.67 ⫾ 0.08 ⬍ 0.001
42.51 ⫾ 6.84 27.01 ⫾ 4.32 ⫺15.49 ⫾ 3.26 ⬍ 0.001
53.72 ⫾ 7.39 38.45 ⫾ 5.63 ⫺15.46 ⫾ 3.15 ⬍ 0.001
Effects of respiration on SPAP mechanisms of these phenomena involve a reduction in intrathoracic pressures during inspiration that cause a decline in the pressure in the right side of the heart. However, the decline in the RAP is almost entirely offset by increased venous return. Hence, only the pressure in the RV declines. The reduction in intrathoracic pressure during inspiration causes a decline in trans-tricuspid pressure gradients in systole, and the velocity of TR decreases. Conversely, reduced RV pressure during inspiration causes an increase in RV volume in diastole, and RV contractile forces, which increase the velocity of TR. Therefore, the effects of inspiration on the velocity of TR are the combined results of these two factors. For patients with normal RV function, these two factors offset each other, so there will be a smaller (or nonsignificant) influence of quiet breathing on TR velocity. For patients with RV systolic dysfunction, increased diastolic filling does not increase RV contractile forces, so the velocity of TR will decrease during inspiration. Clinical perspective: The present study showed that quiet inspiration can cause a decrease in TR velocity and underestimation of SPAP. Taking into account that the changes in intrathoracic pressure during quiet inspiration total ~4 mmHg, if subjects have an airway obstruction, deep breathing caused by acidosis (Kussmaul breathing) or forced inspiration in dyspnea, the changes in intrathoracic pressure will be much greater, so the errors in estimating SPAP using echocardiography will also be much greater. Accurately assessing SPAP in these patients is very important. According to the results of the present study, we believe that the use of echocardiography for measuring TR velocity should be performed when patients are at the end of expiration.This practice will avoid the reduced intrathoracic pressure during inspiration that leads to a decreased velocity of TR and an underestimation of SPAP. This measure can improve the accuracy and comparability in the noninvasive estimation of SPAP using Doppler echocardiography. There were several limitations in the present study. First, we did not divide the subjects into groups in terms of the causes of RV systolic dysfunction, thereby ignoring the possible impact of various diseases and their clinical parameters on the results. Second, we did not study the three-dimensional shape and area of the orifice of the tricuspid valve as well as other parameters related to TR (e.g., velocity time integral in the respiratory cycle). However, according to the simplified Bernoulli equation ( P ⫽ 4V2), TR velocity is related only to the crosstricuspid pressure gradient, and has no relationship with the area of the tricuspid valve orifice or other factors mentioned above, so bias was not introduced
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into the results. Third, the numbers in this study were small, and further studies should be performed. In summary, quiet inspiration can cause a decrease in the velocity of TR in patients with RV systolic dysfunction. This factor should be taken into account when using Doppler echocardiography to estimate these patients’ SPAP, and the measurements should be performed when patients are at the end of expiration.
Acknowledgment We acknowledge the enthusiastic participation of all subjects in this study and are particularly grateful to Ling Jiang Wei from the Chindex International Trade Co., Ltd (Xi’an, China), for technology assistance. We thank Medjaden Bioscience Limited for assisting in the preparation of this manuscript. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
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