Effect of acute volume overload on echocardiographic indices of right ventricular function and dyssynchrony assessed by use of speckle tracking echocardiography in healthy dogs

Tomoya Morita Laboratory of Veterinary Internal Medicine, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido 060-0818, Japan.

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Kensuke Nakamura Organization for Promotion of Tenure Track, University of Miyazaki, Miyazaki 889-2192, Japan.

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Tatsuyuki Osuga Veterinary Teaching Hospital, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido 060-0818, Japan.

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Nozomu Yokoyama Department of Veterinary Internal Medicine, Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo 113-8657, Japan.

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Keitaro Morishita Veterinary Teaching Hospital, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido 060-0818, Japan.

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Noboru Sasaki Laboratory of Veterinary Internal Medicine, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido 060-0818, Japan.

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Hiroshi Ohta Laboratory of Veterinary Internal Medicine, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido 060-0818, Japan.

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Mitsuyoshi Takiguchi Laboratory of Veterinary Internal Medicine, Department of Veterinary Clinical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Hokkaido 060-0818, Japan.

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Abstract

OBJECTIVE To determine the relationship between acute volume overload and echocardiographic indices of right ventricular (RV) function and dyssynchrony in healthy dogs.

ANIMALS 7 healthy Beagles.

PROCEDURES Right heart catheterization and echocardiography were performed in 7 healthy anesthetized Beagles at baseline and after induction of volume overload. Volume overload was induced by IV infusion of lactated Ringer solution (150 mL/kg/h for 90 minutes). Echocardiographic indices of RV function, including peak velocity of systolic tricuspid annular motion, tricuspid annulus plane systolic excursion, fractional area change, RV Tei index, RV longitudinal strain (RVLS), and systolic RV longitudinal strain rate (RVLSR), were obtained by use of speckle tracking echocardiography (STE). In addition, SD of the systolic shortening time of the right ventricle for the 6 segments (RV-SD6) was determined with STE.

RESULTS Volume overload significantly increased the RV end-diastolic pressure, compared with the baseline value. Echocardiographic indices of RV function, except for septal RVLSR, were significantly enhanced by volume overload. In contrast, RV-SD6 did not change with volume overload. Although echocardiographic indices of RV function, except for septal RVLSR, were correlated with RV end-diastolic pressure, RV-SD6 was not correlated.

CONCLUSIONS AND CLINICAL RELEVANCE Echocardiographic indices of RV function, including RVLS and RVLSR, were affected by acute short-term volume overload. Therefore, results for assessment of RV function by use of STE in dogs with clinical conditions associated with right-sided chronic volume overload, such as tricuspid and pulmonic regurgitation, should be interpreted with caution.

Abstract

OBJECTIVE To determine the relationship between acute volume overload and echocardiographic indices of right ventricular (RV) function and dyssynchrony in healthy dogs.

ANIMALS 7 healthy Beagles.

PROCEDURES Right heart catheterization and echocardiography were performed in 7 healthy anesthetized Beagles at baseline and after induction of volume overload. Volume overload was induced by IV infusion of lactated Ringer solution (150 mL/kg/h for 90 minutes). Echocardiographic indices of RV function, including peak velocity of systolic tricuspid annular motion, tricuspid annulus plane systolic excursion, fractional area change, RV Tei index, RV longitudinal strain (RVLS), and systolic RV longitudinal strain rate (RVLSR), were obtained by use of speckle tracking echocardiography (STE). In addition, SD of the systolic shortening time of the right ventricle for the 6 segments (RV-SD6) was determined with STE.

RESULTS Volume overload significantly increased the RV end-diastolic pressure, compared with the baseline value. Echocardiographic indices of RV function, except for septal RVLSR, were significantly enhanced by volume overload. In contrast, RV-SD6 did not change with volume overload. Although echocardiographic indices of RV function, except for septal RVLSR, were correlated with RV end-diastolic pressure, RV-SD6 was not correlated.

CONCLUSIONS AND CLINICAL RELEVANCE Echocardiographic indices of RV function, including RVLS and RVLSR, were affected by acute short-term volume overload. Therefore, results for assessment of RV function by use of STE in dogs with clinical conditions associated with right-sided chronic volume overload, such as tricuspid and pulmonic regurgitation, should be interpreted with caution.

Assessment of RV function has attracted increasing interest. Assessment of RV function by use of various modalities (eg, MRI, cardiac catheterization, and echocardiography) is closely associated with the clinical outcome in human patients with right-sided heart disease (eg, pulmonary hypertension)1,2 as well as left-sided heart disease (eg, mitral valvular disease and dilated cardiomyopathy).3,4

Accurate assessment of RV function by use of echocardiography is challenging because of the complex geometry and contractile properties of the right ventricle. Current guidelines for echocardiographic assessment of RV size and function recommend that multiple echocardiographic indices should be used to assess RV function in human patients.5,6

Echocardiographic indices of RV function have been used for healthy dogs in clinical settings, and several indices, such as the peak velocity of systolic tricuspid annular motion, TAPSE, fractional area change, and RV Tei index, can be impaired in dogs with pulmonary hypertension, compared with results for healthy dogs.7–20 There is good repeatability of RVLS and RVLSR derived by use of STE in healthy dogs.13–15 In addition, in another study10 conducted by our research group, we determined that the RV Tei index is an independent predictor of cardiac death for dogs with MMVD.

However, ventricular loading conditions can vary over time in patients with heart disease, and echocardiographic indices are a measure of intrinsic myocardial contractility but can also be influenced by changes in loading conditions. The ability to clarify the relationship between volume overload and echocardiographic indices will be important for the use of echocardiographic indices in clinical settings. Some echocardiographic indices of RV function are affected by volume change in healthy humans,21,22 human patients,23–25 and research animals.26,27 In dogs, left-sided heart disease, especially MMVD, is the most common cause of pulmonary hypertension, and a large proportion of dogs with MMVD also have tricuspid valve regurgitation.10,20 As a consequence, volume overload occurs in clinical settings. Recently, the possibility that echocardiographic indices of RV function can be influenced by volume overload in dogs with MMVD has been reported.18–20

Additionally, RV intraventricular mechanical dyssynchrony has been described in human patients with pulmonary hypertension, and the condition has been associated with more pronounced RV dysfunction, worsening of clinical signs, and a poor prognosis.28–32 In human medicine, RV intraventricular mechanical dyssynchrony reportedly can be caused by several factors.28–31,33 The repeatability and reference values of the RV dyssynchrony index for healthy Beagles have been reported.15 To our knowledge, it has not been clarified whether chamber dilation attributable to volume overload without pressure overload and electrical activation delay can cause RV dyssynchrony.

Therefore, the objective of the study reported here was to examine the relationship between volume overload and echocardiographic indices of RV function and dyssynchrony in healthy dogs. We hypothesized the echocardiographic indices of RV function would be enhanced by acute short-term volume overload.

Materials and Methods

Animals

Seven laboratory Beagles (1 female and 6 males) were used in the study. Dogs were 1 to 3 years old with a body weight of 8.8 to 11.4 kg. All dogs were deemed healthy and had an anatomically normal heart and physiologically normal myocardial function, as determined on the basis that no abnormalities were detected during a complete physical examination, ECG, and standard echocardiographic examinations (including B-mode, M-mode, pulsed-wave Doppler, and color flow Doppler imaging). All procedures were performed at the Graduate School of Veterinary Medicine, Hokkaido University, and approved by the Laboratory Animal Experimentation Committee, Graduate School of Veterinary Medicine, Hokkaido University (approval No. 15-0087).

Study protocol

Each dog received atropine sulfatea (0.05 mg/kg, SC) and was sedated by IV administration of butorphanol tartrateb (0.2 mg/kg) and midazolam hydrochloridec (0.1 mg/kg). Then, cefazolin sodium hydrated (20 mg/kg, IV) and heparin sodiume (100 U/kg, IV) were administered. Anesthesia was induced with propofolf (6 mg/kg, IV), and dogs were endotracheally intubated. Anesthesia was maintained by administration of isofluraneg (1.5% to 2.0%) in oxygen. The end-tidal partial pressure of carbon dioxide was monitored and maintained between 35 and 45 mm Hg by use of mechanical ventilation. Tidal volume was 10 to 15 mL/kg, and the respiratory rate was maintained at 10 to 14 breaths/min. Heart rate and arterial blood pressure (via an arterial catheter) were monitored and recorded with a polygraph instrument.h

Anesthetized dogs were allowed a stabilization period of approximately 10 minutes, and baseline values for hemodynamic variables and echocardiographic indices were then recorded. After baseline measurements were obtained, an IV infusion of lactated Ringer solutioni (150 mL/kg/h for 90 minutes) was administered to increase the preload. Volume of the infusion was determined on the basis of previous studies26,34 and results of a preliminary experiment conducted by our laboratory group. Hemodynamic variables were measured after the start of the infusion, and echocardiography was performed every 15 minutes. After all data were collected, the IV infusion was stopped, furosemidej (4 to 6 mg/kg, IV) was administered, and dogs were allowed to recover from anesthesia.

Hemodynamic measurements

Hemodynamic variables were recorded with a polygraph instrument. Anesthetized dogs were positioned in left lateral recumbency. A 6F introducer sheathk was percutaneously inserted into the right jugular vein, and then a 5F Swan-Ganz catheterl was inserted and advanced into the pulmonary artery under fluoroscopic guidance. Mean pulmonary arterial pressure, mean RV pressure, RVEDP, mean right atrial pressure, and mean pulmonary artery wedge pressure were measured; values were calculated as the mean for 5 consecutive cardiac cycles. Cardiac output was measured by use of the thermodilution technique with an injection of 5 mL of cold saline (0.9% NaCl) solution; values were calculated as the mean for 4 measurements. Cardiac index was calculated by dividing cardiac output by body surface area. The first derivatives of the maximum and minimum change in RV pressure (maximum positive rate of RV pressure change and maximum negative rate of RV pressure change, respectively) were calculated from the RV pressure data.

Echocardiographic measurements

Echocardiographic examinations were performed by an echocardiographer (KN) using 2 ultrasound machinesm,n equipped with a 3- to 7-MHz sector probeo and a 3- to 6-MHz sector probe.p A color Doppler ultrasound machinen was used to measure the RV Tei index via DPWD. All dogs were positioned in left lateral recumbency for echocardiographic examinations. An ECG tracing (lead II) was recorded simultaneously with echocardiographic imaging and used to automatically measure heart rate.

The early diastolic tricuspid inflow velocity, late diastolic tricuspid inflow velocity, and ratio of the early diastolic tricuspid inflow velocity to the late diastolic tricuspid inflow velocity were determined by use of pulsed-wave Doppler echocardiography. Peak velocity of early diastolic septal mitral annular motion, peak velocity of late diastolic septal mitral annular motion, and peak velocity of systolic septal mitral annular motion were measured by use of TDI. Peak velocity of systolic tricuspid annular motion was determined by use of TDI at the lateral tricuspid annulus with an apical 4-chamber view. The TAPSE was obtained by placing an M-mode cursor over the tricuspid valve annulus in an apical 4-chamber view and measuring the amplitude of motion during systole. The RV end-diastolic area and end-systolic area were obtained by tracing the RV endocardium in systole and diastole from the annulus to the apex in a modified apical 4-chamber view, which included the RV apex. Fractional area change was calculated as ([RV end-diastolic area – RV end-systolic area]/ RV end-diastolic area) × 100.

The RV Tei index was calculated as (ICT + IRT)/ ejection time, where ICT is the isovolumic contraction time and IRT is the isovolumic relaxation time. The Tei index was calculated after images were acquired with DPWD and TDI. Tricuspid inflow and pulmonary artery flow were measured simultaneously by use of DPWD in a left parasternal short-axis view, and ICT + IRT was derived by subtracting ejection time from the time of the cessation of the tricuspid valve A-wave to the onset of the tricuspid valve E-wave in 1 image.16 For measurement of the RV Tei index by use of TDI, ejection time was defined as the duration of the peak velocity of systolic tricuspid annular motion, and ICT + IRT was calculated by subtracting the duration of the peak velocity of systolic tricuspid annular motion from the interval from the end of the late diastolic tricuspid annulus velocity to the onset of the early diastolic tricuspid annulus velocity.5 The LV Tei index was calculated by use of TDI. Ejection time was defined as the duration of the peak velocity of systolic septal mitral annular motion, and ICT + IRT was calculated by subtracting the duration of the peak velocity of systolic septal mitral annular motion from the interval from the end of the late diastolic septal mitral annulus velocity to the onset of the early diastolic septal mitral annulus velocity.34

RVLS, RVLSR, and RV-SD6 determined by use of STE

The RVLS, RVLSR, and RV-SD6 were determined by use of conventional gray-scale echocardiography with a modified apical 4-chamber view. Frame rate was optimized to > 200 frames/s by narrowing the imaging sector and reducing the depth to focus on the RV. Three consecutive cardiac cycles were stored on a hard drive, and images were analyzed offline with software.q Values for STE indices were determined from the mean of 3 cardiac cycles. The investigators carefully obtained the best visual image of the RV endocardial border from the base to apex. The endocardial border was manually traced in an end-diastolic frame, and a region of interest was generated, which was then adjusted to incorporate the entire RV wall myocardial thickness. The RV wall was divided into inner and outer layers, and the RV free and septal walls were divided into 3 segments (basal, middle, and apical). The RVLS is defined as the shortening of a region of interest relative to its original length and is expressed as a negative percentage.35 The RVLSR is defined as the speed of deformation of a region of interest and is the temporal derivative of strain.35 Both RVLS and RVLSR were obtained for each segment at the highest peak of the software-generated strain curves. Global RVLS and RVLSR were calculated as the mean of values determined for all 6 segments of the RV. Free wall RVLS and RVLSR and septal RVLS and RVLSR were calculated as the mean of 3 segments along the entire RV (Figure 1). Systolic shortening time was calculated from the onset of the QRS complex to peak longitudinal strain of each of the 6 RV segments. To quantify RV intraventricular mechanical dyssynchrony, RV-SD6 was calculated by use of offline software,q and the RV-SD6 was corrected for the R-R interval by use of the Bazett equation as follows36: corrected RV-SD6 = RV-SD6/√R-R interval.

Figure 1—
Figure 1—

Echocardiographic images (left) and software-generated strain curves (right) illustrating the technique used to measure RVLS (A) and RVLSR (B) obtained by use of STE in dogs. The RV free wall and septum were each automatically divided into 3 segments (apical, middle, and basal). In panel A, the global RVLS is determined by calculating the mean peak longitudinal strain values of all 6 segments of the right ventricle in a modified apical 4-chamber view. The RV-SD6 is calculated and corrected for the R-R interval by use of the Bazett formula. Colored arrows indicate each segmental systolic shortening time. In panel B, the global RVLSR is determined by calculating the mean systolic peak longitudinal strain rate values of all 6 segments of the right ventricle in a modified apical 4-chamber view. The areas in the echocardiographic images enclosed by the colored lines correspond to adjusted regions of interest to incorporate the RV wall myocardium. Notice that the units are indicated in brackets at the top of the y-axis of the RVLS or RVLSR and that the ECG tracing (thin green line) is in the bottom right corner of each panel. AL = Apical lateral free wall. AS = Apical septum. BL = Basal lateral free wall. BS = Basal septum. ML = Middle lateral free wall. MS = Middle lateral septum.

Citation: American Journal of Veterinary Research 80, 1; 10.2460/ajvr.80.1.51

Statistical analysis

Analysis was performed with statistical programs.r,s Normal distribution of the data was confirmed with the Shapiro-Wilk test. A linear mixed model was developed with time (baseline and at 15, 30, 45, 60, 75, and 90 minutes) as a categorical fixed effect and dog as a random effect. The F test was used to assess the effect of time on values of measured variables. Pairwise comparisons between baseline and each time point were performed by obtaining least squares means; a Bonferroni correction was used to account for multiple comparisons. Partial correlation analysis controlling for the effect of dog was used to determine the relationship between hemodynamic variables and echocardiographic indices. Partial correlation analysis was performed with echocardiographic indices as outcome variables and hemodynamic variables as explanatory variables. Dogs were treated as a categorical factor by use of a dummy variable with 6 degrees of freedom. Values of P < 0.05 were considered significant.

Results

Changes in hemodynamic variables

Changes in hemodynamic variables before (baseline) and after IV infusion of lactated Ringer solution were summarized (Table 1). Mean pulmonary arterial pressure, mean pulmonary artery wedge pressure, mean RV pressure, mean right atrial pressure, RVEDP, and cardiac index were significantly increased at 15 to 90 minutes, compared with baseline values. Pulmonary vascular resistance was significantly decreased at 15 to 90 minutes, compared with the baseline value. There were no changes in mean arterial blood pressure, heart rate, maximum positive rate of RV pressure change, and maximum negative rate of RV pressure change after acute short-term volume overload.

Table 1—

Least squares mean (95% confidence interval) values for hemodynamic variables determined before (baseline) and during IV infusion of lactated Ringer solution to create volume overload in 7 healthy Beagles.

  Volume overload (min)
VariableBaseline153045607590
Heart rate (beats/min)109103112113116116112
 (103 to 115)(97 to 109)(106 to 118)(107 to 119)(110 to 122)(110 to 122)(106 to 118)
Mean BP (mm Hg)54535456575857
 (48 to 60)(47 to 59)(48 to 60)(50 to 62)(51 to 63)(52 to 64)(51 to 63)
Mean PAP (mm Hg)1013*16*17*13*19*19*
 (8 to 12)(11 to 15)(14 to 18)(15 to 19)(11 to 15)(17 to 21)(17 to 21)
Mean RVP (mm Hg)611*13*14*15*16*16*
 (4 to 8)(9 to 13)(11 to 15)(12 to 16)(13 to 17)(14 to 18)(14 to 18)
Mean RAP (mm Hg)05*8*9*9*10*10*
 (−4 to 4)(1 to 9)(4 to 12)(5 to 13)(5 to 13)(6 to 14)(6 to 14)
RVEDP (mm Hg)28*10*11*11*11*12*
 (0 to 4)(6 to 10)(8 to 12)(9 to 13)(9 to 13)(9 to 13)(10 to 14)
Mean PAWP (mm Hg)48*11*13*14*15*15*
 (2 to 6)(6 to 10)(9 to 13)(11 to 15)(12 to 16)(13 to 17)(13 to 17)
Cardiac index4.35.4*6.1*6.5*6.6*6.6*6.8*
(L/min/m2)(3.5 to 5.1)(4.6 to 6.2)(5.3 to 6.9)(5.7 to 7.3)(5.8 to 7.4)(5.8 to 7.4)(6.0 to 7.6)
PVR (Wood U)3.01.8*1.7*1.3*1.4*1.4*1.1*
 (2.5 to 3.5)(1.3 to 2.3)(1.2 to 2.2)(0.8 to 1.8)(0.9 to 1.9)(0.9 to 1.9)(0.6 to 1.6)
RV max dP/dt144161136151160158170
(mm Hg/s)(110 to 178)(127 to 195)(102 to 170)(117 to 185)(126 to 194)(124 to 192)(136 to 204)
RV min dP/dt−134−132−110−114−121−114−122
(mm Hg/s)(−156 to −112)(−154 to −110)(−132 to −88)(−136 to −92)(−143 to −99)(−136 to −92)(−144 to −100)

Value differs significantly (P < 0.05) from the baseline value.

BP = Arterial blood pressure. PAP = Pulmonary arterial pressure. PAWP = Pulmonary artery wedge pressure. PVR = Pulmonary vascular resistance. RAP = Right atrial pressure. RV max dP/dt = Maximum positive rate of RV pressure change. RV min dP/dt = Maximum negative rate of RV pressure change. RVP = RV pressure.

Changes in echocardiographic indices

The RVLS, RVLSR, and RV-SD6 were determined by use of STE at baseline and various times after infusion (Figure 2). Changes in the RV Tei index and STE variables before (baseline) and after IV infusion of lactated Ringer solution were summarized (Table 2; Figure 3). Peak velocity of systolic tricuspid annular motion, TAPSE, and fractional area change were significantly higher during acute short-term volume overload than at baseline. The RV Tei indices determined with DPWD and TDI were significantly decreased, compared with the baseline value. Peak velocity of late diastolic septal mitral annular motion and peak velocity of early diastolic septal mitral annular motion were significantly increased, and LV Tei index was significantly decreased. Speckle tracking echocardiography could not be performed on 1 dog because of inadequate quality of the image. Acute volume overload led to a significant increase in global and free wall RVLS determined with STE at 15 to 90 minutes, and septal RVLS was significantly increased at 60 to 90 minutes, compared with the baseline value. Global and free wall RVLSR were significantly increased at 45 to 90 minutes, compared with the baseline values. This was in contrast to septal RVLSR, which remained unchanged. Although free wall and septal systolic shortening time were significantly longer than at baseline, the septal-to-free wall delay did not change. In addition, RV-SD6 did not change during acute volume overload.

Figure 2—
Figure 2—

Representative echocardiographic images (left) and software-generated strain curves (right) of RVLS (A and B) and RVLSR (C and D) obtained from a dog at baseline (A and C) and 90 minutes after onset of an IV infusion of lactated Ringer solution to create volume overload (B and D). Panels A and C are the same as panels A and B in Figure 1. When comparing panels A and B, notice that the global RVLS increases from the baseline value by 90 minutes after the start of the infusion. Both the free wall and septal segmental systolic shortening time are delayed, but RV-SD6 is not changed at 90 minutes. When comparing panels C and D, notice that the global RVLSR increases from the baseline value by 90 minutes after the start of the infusion. See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 80, 1; 10.2460/ajvr.80.1.51

Figure 3—
Figure 3—

Least squares mean and 95% confidence interval for the RV Tei (A), RVLS (B), RVLSR (C), and segmental systolic shortening time (SST) and RV-SD6 (D) determined with STE before (baseline [Base]) and during IV infusion of lactated Ringer solution to create volume overload in 7 dogs. Notice in panel A that the RV Tei index determined by use of DPWP (black circles) or TDI (white circles) is significantly decreased from the baseline value. In panel B, the global RVLS (white triangles), free wall RVLS (black circles), and septal RVLS (white circles) are significantly increased from the baseline values. In panel C, the global RVLSR (white triangles) and free wall RVLSR (black circles) are significantly increased from the baseline values, whereas the septal RVLSR (white circles) is not significantly changed from the baseline value. In panel D, the free wall SST (black circles) and septal SST (white circles) differ significantly from the baseline values, but the RV-SD6 (white triangles) is not significantly changed. *Value differs significantly (P < 0.05) from the baseline value.

Citation: American Journal of Veterinary Research 80, 1; 10.2460/ajvr.80.1.51

Table 2—

Least squares mean (95% confidence interval) values for echocardiographic indices determined before (baseline) and during IV infusion of lactated Ringer solution to create volume overload in 7 healthy Beagles.

  Volume overload (min)
VariableBaseline153045607590
E (m/s)0.430.510.560.560.59*0.560.58*
 (0.35 to 0.51)(0.43 to 0.59)(0.48 to 0.64)(0.48 to 0.64)(0.51 to 0.67)(0.48 to 0.64)(0.50 to 0.66)
A (m/s)0.360.390.47*0.47*0.55*0.51*0.54*
 (0.30 to 0.42)(0.33 to 0.45)(0.41 to 0.53)(0.41 to 0.53)(0.49 to 0.61)(0.45 to 0.57)(0.48 to 0.60)
E-to-A ratio1.221.331.221.241.111.101.11
 (1.20 to 1.24)(1.31 to 1.35)(1.20 to 1.24)(1.22 to 1.26)(1.09 to 1.13)(1.08 to 1.12)(1.09 to 1.13)
E'mv (cm/s)6.39.2*9.7*9.4*9.0*8.8*8.5*
 (5.2 to 7.5)(8.1 to 10.3)(8.5 to 10.8)(8.2 to 10.6)(7.8 to 10.3)(7.5 to 10.0)(7.3 to 9.7)
A'mv (cm/s)3.64.7*5.0*5.3*5.5*4.9*4.8*
 (2.8 to 4.3)(4.0 to 5.5)(4.3 to 5.8)(4.5 to 6.1)(4.6 to 6.4)(4.1 to 5.7)(4.0 to 5.7)
S'mv (cm/s)5.45.35.55.45.55.4*5.3
 (4.7 to 6.2)(4.5 to 6.0)(4.7 to 6.2)(4.6 to 6.1)(4.7 to 6.3)(4.6 to 6.2)(4.5 to 6.1)
LV Tei index0.710.55*0.51*0.46*0.45*0.42*0.40*
 (0.62 to 0.80)(0.46 to 0.64)(0.42 to 0.61)(0.37 to 0.56)(0.36 to 0.54)(0.33 to 0.51)(0.31 to 0.49)
S'TV (cm/s)6.48.69.1*10.1*10.0*9.5*10.3*
 (4.4 to 8.4)(6.6 to 10.6)(7.1 to 11.1)(8.1 to 12.1)(8.0 to 12.0)(7.5 to 11.5)(8.3 to 12.3)
TAPSE (mm)7.311.1*12.7*13.2*113.8*13.2*14.6*
 (4.7 to 9.9)(8.7 to 13.5)(10.3 to 15.1)(10.8 to 15.6)(11.4 to 16.2)(10.8 to 15.6)(12.2 to 17.0)
RVEDA (cm2)9.6610.77*10.72*10.62*11.06*10.55*10.85*
 (8.56 to 10.74)(9.69 to 11.85)(9.64 to 11.80)(9.54 to 11.70)(9.98 to 12.14)(9.47 to 11.63)(9.77 to 11.93)
RVESA (cm2)7.587.317.377.207.397.327.44
 (6.78 to 8.38)(6.51 to 8.11)(6.57 to 8.17)(6.40 to 8.00)(6.59 to 8.19)(6.52 to 8.12)(6.64 to 8.24)
FAC (%)21.531.7*31.1*32.1*33.3*30.6*31.3*
 (17.7 to 25.3)(27.9 to 35.5)(27.3 to 34.9)(28.3 to 35.9)(29.5 to 37.1)(26.8 to 34.4)(27.5 to 35.1)
RV Tei index
 DPWD0.370.18*0.20*0.18*0.16*0.17*0.17*
 (0.33 to 0.41)(0.14 to 0.22)(0.16 to 0.24)(0.14 to 0.22)(0.12 to 0.20)(0.13 to 0.21)(0.13 to 0.21)
 TDI0.550.37*0.36*0.34*0.32*0.29*0.29*
 (0.49 to 0.61)(0.31 to 0.43)(0.30 to 0.42)(0.28 to 0.40)(0.26 to 0.38)(0.23 to 0.35)(0.23 to 0.35)
RVLS (%)
 Global−11.3−14.2*−15.1*−16.7*−17.0*−17.7*−18.1*
 (−13.7 to −8.9)(−16.6 to −11.8)(−17.5 to −12.7)(−19.1 to −14.3)(−19.4 to −14.6)(−20.1 to −15.3)(−20.5 to −15.7)
 Free wall−12.6−17.4*−17.3*−19.5*−19.8*−20.1*−21.1*
 (−16.2 to −9.0)(−20.8 to −14.0)(−20.7 to −13.9)(−22.9 to −16.1)(−23.2 to −16.4)(−23.5 to −16.7)(−24.5 to −17.7)
 Septal−9.8−10.5*−12.5*−13.2−13.4*−14.6*−14.6*
 (−12.2 to −7.4)(−12.7 to −8.3)(−14.7 to −10.3)(−15.4 to −11.0)(−15.6 to −11.2)(−16.8 to −12.4)(−16.8 to −12.4)
RVLSR (/s)
 Global−0.75−0.87−0.91−1.02*−1.08*−1.05*−1.06*
 (−0.99 to −0.51)(−1.11 to −0.63)(−1.15 to −0.67)(−1.26 to −0.78)(−1.32 to −0.84)(−1.29 to −0.81)(−1.30 to −0.82)
 Free wall−0.82−1.11−1.09−1.28*−1.33*−1.25*−1.29*
 (−1.18 to −0.46)(−1.45 to −0.77)(−1.43 to −0.75)(−1.62 to −0.94)(−1.67 to −0.99)(−1.59 to −0.91)(−1.63 to −0.95)
 Septal−0.80−0.72−0.87−0.88−0.91−0.91−0.91
 (−1.00 to −0.60)(−0.92 to −0.52)(−1.07 to −0.67)(−1.08 to −0.68)(−1.11 to −0.71)(−1.11 to −0.71)(−1.11 to −0.71)
SST (ms)
 Free wall225288*299*306*294*307*310*
 (201 to 249)(264 to 312)(275 to 323)(292 to 330)(270 to 318)(283 to 331)(286 to 334)
 Septal238290*299*309*298*298*311*
 (210 to 266)(262 to 318)(271 to 327)(281 to 337)(270 to 326)(270 to 326)(283 to 339)
 Septal-to-free wall delay (ms)18−10−3−49−1
 (4 to 32)(−15 to 13)(−14 to 14)(−17 to 11)(−18 to 10)(−5 to 23)(−15 to 13)
RV-SD6 (ms)20.518.320.020.220.219.819.2
 (15.1 to 25.9)(13.3 to 23.3)(15.0 to 25.0)(15.2 to 25.2)(15.2 to 25.2)(14.8 to 24.8)(14.2 to 24.2)

Represents results for only 6 dogs; measurements could not be obtained for 1 dog because of inadequate image quality.

A = Late diastolic tricuspid inflow velocity. A'MV = Late diastolic septal mitral annular velocity. E = Early diastolic tricuspid inflow velocity. E'MV = Early diastolic septal mitral annular velocity. FAC = Fractional area change. RVEDA = RV end-diastolic area. RVESA = RV end-systolic area. S'MV = Systolic septal mitral annular velocity. S'TV = Peak velocity of systolic tricuspid annular motion. SST = Systolic shortening time.

See Table 1 for remainder of key.

Partial correlation analysis between echocardiographic indices and RVEDP

Partial correlations controlling for the effect of dog between echocardiographic indices and RVEDP were summarized (Table 3). Although there were significant correlations between RVEDP and peak velocity of systolic tricuspid annular motion, TAPSE, fractional area change, RV Tei index determined with DPWD and TDI, global RVLS, free wall RVLS, septal RVLS, global RVLSR, and free wall RVLSR, no significant correlation was found between RVEDP and septal RVLSR or between RVEDP and RV-SD6.

Table 3—

Results of partial correlation analysis of echocardiographic indices and RVEDP controlling for the effect of dog during acute volume overload in 7 healthy Beagles.

VariablerP value*
S'TV (cm/s)0.65< 0.001
TAPSE (mm)0.82< 0.001
FAC (%)0.66< 0.001
Tei index
 DPWD−0.81< 0.001
 TDI−0.79< 0.001
RVLS (%)
 Global−0.69< 0.001
 Free wall−0.56< 0.001
 Septal−0.520.001
RVLSR (/s)
 Global−0.67< 0.001
 Free wall−0.450.005
 Septal−0.210.22
RV-SD6−0.030.85

Values were considered significant at P < 0.05.

See Table 2 for remainder of key.

Discussion

The major findings of the study reported here revealed that echocardiographic indices of RV function, including RVLS and RVLSR derived by use of STE but excluding septal RVLSR, were enhanced in dogs with induced acute short-term volume overload. This result indicated that these indices were preload dependent. In addition, RV-SD6, an index of RV dyssynchrony, did not change during acute short-term volume overload. To our knowledge, this represented the first description of the effects of acute short-term volume overload on RV dyssynchrony.

Free wall RVLS and RVLSR derived by use of STE in the present study were significantly increased and were correlated with RVEDP in dogs with acute short-term volume overload. More negative values of free wall RVLS and RVLSR, which reflect increased RV function, have been found in MMVD stage B2 or C than in stage B1.20 Function of the right ventricle may be augmented via the Frank-Starling mechanism associated with left-sided volume overload and tricuspid regurgitation in dogs with MMVD.20 Results of the study reported here supported the fact that free wall RVLS and RVLSR were preload-dependent indices. Therefore, assessment of RV function on the basis of free wall RVLS and RVLSR underestimated the severity of disease and RV function by enhancing the effect in dogs with volume overload.

Septal RVLS did not change until 45 minutes, and it was significantly increased at 60 to 90 minutes in the present study. In addition, septal RVLSR did not change in response to acute short-term volume overload. Results of the study reported here suggested that septal RVLS was less affected by volume overload than was free wall RVLS and that septal RVLSR was a preload-independent index. In a previous study,20 global RVLS and RVLSR, including free wall and septal, did not change among MMVD stages B1, B2, and C, which was in contrast to results for free wall RVLS. This result may indicate that septal RVLS and RVLSR are less preload-dependent indices in dogs with MMVD. Results for the present study support the previous findings in dogs with MMVD. On the basis of these findings, it appears that septal RVLS and RVLSR would be useful for the assessment of RV function in dogs with volume overload. However, septal RVLS and RVLSR might reflect LV function as well as RV function, and results for STE could not be used to distinguish the RV and LV components of the septum. Indeed, several indices of LV function measured from the septum, including peak velocity of early diastolic septal mitral annular motion, peak velocity of late diastolic septal mitral annular motion, and the LV Tei index, were enhanced in the dogs of the present study. However, we did not measure LV chamber size and LV strain. Further studies are needed to validate the relationship between LV function and septal RVLS during volume overload.

The present study provided the first description of the effects of acute short-term volume overload on RV dyssynchrony in dogs. In human patients with pulmonary hypertension, RV dyssynchrony is associated with a poorer prognosis, more pronounced RV dysfunction, and worsening of clinical signs.29–32 In addition, RV dyssynchrony in human patients can be caused by RV pressure overload, chamber dilation, nonuniform distribution of regional myocardial wall stress, and electrical activation delay as well as prolonged systolic shortening time of the free wall, compared with that of the septum.28,30,31 However, to our knowledge, the relationship between RV dyssynchrony and volume overload has not been clarified. In the present study, volume overload caused RV dilation (increased RV end-diastolic area), and fractional shortening in both the free wall and septal systolic shortening times were prolonged. Therefore, RV-SD6 did not change in response to volume overload. These results may have reflected the fact that the distribution of regional myocardial wall stress of the RV myocardium might be uniform in dogs with induced acute short-term volume overload, compared with results for human patients with pulmonary hypertension. Findings for the study reported here indicated that RV dyssynchrony did not occur in response to volume overload or chamber dilation and that the interaction between chamber dilation and pressure overload or electrical activation delay would be important for RV dyssynchrony.

Peak velocity of systolic tricuspid annular motion, TAPSE, fractional area change, and RV Tei index reportedly are preload-dependent indices in human patients with atrial septal defect,22,23 healthy human subjects after blood donation,25 and dogs with experimentally induced volume overload.21 In dogs with MMVD, peak velocity of systolic tricuspid annular motion and fractional area change did not differ among dogs with MMVD B1, B2, and C.18–20 In one report,19 TAPSE did not differ among the MMVD stages, whereas in another report,20 TAPSE was increased in dogs with MMVD B2, compared with values for dogs with MMVD B1. In the present study, peak velocity of systolic tricuspid annular motion, TAPSE, and fractional area change were significantly increased by volume overload. On the basis of these findings, peak velocity of systolic tricuspid annular motion, TAPSE, and fractional area change were preload-dependent indices and may have underestimated RV dysfunction in dogs with volume overload.

The present study had several limitations. First, only a small number of healthy dogs were evaluated. Caution must be exercised when extrapolating these data to clinical settings. Dogs with pulmonary hypertension attributable to MMVD would be chronically affected, and adaptive mechanisms would develop. Therefore, there are several differences in the effects of volume overload on RV function between acute and chronic settings. Second, the sample size was so small that it may have resulted in a type 2 error. Although several echocardiographic indices did not change in response to acute volume overload in the present study, the small sample size may have rendered the study underpowered to detect actual differences. In addition, a control group was lacking, and there was a lack of data from examinations performed after the administration of furosemide; therefore, it is unknown whether the enhancing effects would be reversible and were attributable to volume overload or prolonged anesthesia in the present study. Isoflurane can cause impairment of myocardial contractility in the right ventricle, increases in afterload, and RV–pulmonary artery uncoupling.37,38 Therefore, prolonged anesthesia is unlikely to enhance echocardiographic indices. Third, the effects of anesthesia on RV function could not be excluded. Because isoflurane can cause impairment of myocardial contractility and increases in afterload, the enhancing effects in the present study may have been blunted by the administration of isoflurane. In addition, a complete autonomic blockade was not used in the present study. Finally, RV strain was measured with software designed for the measurement of LV strain.

Results of the study reported here indicated that echocardiographic indices of RV function were affected by acute short-term volume overload, but the RV dyssynchrony index did not change. Therefore, evaluation of RV function on the basis of echocardiographic indices should be interpreted with caution for dogs with clinical conditions associated with right-sided chronic volume overload, such as tricuspid valve and pulmonic valve regurgitation.

Acknowledgments

Supported in part by a Grant-in-Aid for Scientific Research from the Japanese Society for the Promotion of Science (No. 16K18800).

The authors declare that there were no conflicts of interest.

ABBREVIATIONS

DPWD

Dual pulsed-wave Doppler echocardiography

LV

Left ventricular

MMVD

Myxomatous mitral valve disease

RV

Right ventricular

RVEDP

Right ventricular end-diastolic pressure

RVLS

Right ventricular longitudinal strain

RVLSR

Right ventricular longitudinal strain rate

RV-SD6

SD of the systolic shortening time of the right ventricle for the 6 segments

STE

Speckle tracking echocardiography

TAPSE

Tricuspid annulus plane systolic excursion

TDI

Tissue Doppler imaging

Footnotes

a.

Atropine sulfate injection, Mitsubishi Tanabe Pharma Corp, Osaka, Japan.

b.

Vetorphale, Meiji Seika Pharma Co Ltd, Tokyo, Japan.

c.

Dormicum injection, Astellas Pharma Inc, Tokyo, Japan.

d.

Cefamezin α, Astellas Pharma Inc, Tokyo, Japan.

e.

Heparin sodium injection, Ajinomoto Pharmaceuticals Co Ltd, Tokyo, Japan.

f.

Propofol Mylan, Mylan Inc, Canonsburg, Pa.

g.

Isoflu, DS Pharma Animal Health Co Ltd, Osaka, Japan.

h.

RMC-4000, Nihon Kohden Co, Tokyo, Japan.

i.

Solulact, Terumo Corp, Tokyo, Japan.

j.

Lasix injection, Sanofi K, Tokyo, Japan.

k.

Fast-Cath hemostasis introducers, St Jude Medical Inc, Minnetonka, Minn.

l.

Swan-Ganz thermodilution catheter, Edwards Lifesciences Corp, Irvine, Calif.

m.

Artida, Toshiba Medical Systems Corp, Tochigi, Japan.

n.

Hi Vision Preirus, Hitachi Aloka Medical Ltd, Tokyo, Japan.

o.

PST-50BT, Toshiba Medical Systems Corp, Tochigi, Japan.

p.

EUP-S52, Hitachi Aloka Medical Ltd, Tokyo, Japan.

q.

2D wall motion tracking, Toshiba Medical Systems Corp, Tochigi, Japan.

r.

JMP, version 10.0, SAS Institute Inc, Cary, NC.

s.

SPSS, version 21, SPSS Inc, Chicago, Ill.

References

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Contributor Notes

Address correspondence to Dr. Nakamura (kenvet@cc.miyazaki-u.ac.jp).
  • Figure 1—

    Echocardiographic images (left) and software-generated strain curves (right) illustrating the technique used to measure RVLS (A) and RVLSR (B) obtained by use of STE in dogs. The RV free wall and septum were each automatically divided into 3 segments (apical, middle, and basal). In panel A, the global RVLS is determined by calculating the mean peak longitudinal strain values of all 6 segments of the right ventricle in a modified apical 4-chamber view. The RV-SD6 is calculated and corrected for the R-R interval by use of the Bazett formula. Colored arrows indicate each segmental systolic shortening time. In panel B, the global RVLSR is determined by calculating the mean systolic peak longitudinal strain rate values of all 6 segments of the right ventricle in a modified apical 4-chamber view. The areas in the echocardiographic images enclosed by the colored lines correspond to adjusted regions of interest to incorporate the RV wall myocardium. Notice that the units are indicated in brackets at the top of the y-axis of the RVLS or RVLSR and that the ECG tracing (thin green line) is in the bottom right corner of each panel. AL = Apical lateral free wall. AS = Apical septum. BL = Basal lateral free wall. BS = Basal septum. ML = Middle lateral free wall. MS = Middle lateral septum.

  • Figure 2—

    Representative echocardiographic images (left) and software-generated strain curves (right) of RVLS (A and B) and RVLSR (C and D) obtained from a dog at baseline (A and C) and 90 minutes after onset of an IV infusion of lactated Ringer solution to create volume overload (B and D). Panels A and C are the same as panels A and B in Figure 1. When comparing panels A and B, notice that the global RVLS increases from the baseline value by 90 minutes after the start of the infusion. Both the free wall and septal segmental systolic shortening time are delayed, but RV-SD6 is not changed at 90 minutes. When comparing panels C and D, notice that the global RVLSR increases from the baseline value by 90 minutes after the start of the infusion. See Figure 1 for remainder of key.

  • Figure 3—

    Least squares mean and 95% confidence interval for the RV Tei (A), RVLS (B), RVLSR (C), and segmental systolic shortening time (SST) and RV-SD6 (D) determined with STE before (baseline [Base]) and during IV infusion of lactated Ringer solution to create volume overload in 7 dogs. Notice in panel A that the RV Tei index determined by use of DPWP (black circles) or TDI (white circles) is significantly decreased from the baseline value. In panel B, the global RVLS (white triangles), free wall RVLS (black circles), and septal RVLS (white circles) are significantly increased from the baseline values. In panel C, the global RVLSR (white triangles) and free wall RVLSR (black circles) are significantly increased from the baseline values, whereas the septal RVLSR (white circles) is not significantly changed from the baseline value. In panel D, the free wall SST (black circles) and septal SST (white circles) differ significantly from the baseline values, but the RV-SD6 (white triangles) is not significantly changed. *Value differs significantly (P < 0.05) from the baseline value.

  • 1. van De Veerdonk MC, Kind T, Marcus JT, et al. Progressive right ventricular dysfunction in patients with pulmonary arterial hypertension responding to therapy. J Am Coll Cardiol 2011;58:25112519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Brittain EL, Pugh ME, Wheeler LA, et al. Shorter survival in familial versus idiopathic pulmonary arterial hypertension is associated with hemodynamic markers of impaired right ventricular function. Pulm Circ 2013;3:589598.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Le Tourneau T, Deswarte G, Lamblin N, et al. Right ventricular systolic function in organic mitral regurgitation: impact of biventricular impairment. Circulation 2013;127:15971608.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Doesch C, Dierks DM, Haghi D, et al. Right ventricular dysfunction, late gadolinium enhancement, and female gender predict poor outcome in patients with dilated cardiomyopathy. Int J Cardiol 2014;177:429435.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Rudski LG, Lai WW, Afilalo J, 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;23:685713.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Lang RM, Badano LP, Mor-Avi V, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 2015;28:139.e14.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Serres F, Chetboul V, Gouni V, et al. Diagnostic value of echo-Doppler and tissue Doppler imaging in dogs with pulmonary arterial hypertension. J Vet Intern Med 2007;21:12801289.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Pariaut R, Saelinger C, Strickland KN, et al. Tricuspid annular plane systolic excursion (TAPSE) in dogs: reference values and impact of pulmonary hypertension. J Vet Intern Med 2012;26:11481154.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Teshima K, Asano K, Iwanaga K, et al. Evaluation of right ventricular Tei index (index of myocardial performance) in healthy dogs and dogs with tricuspid regurgitation. J Vet Med Sci 2006;68:13071313.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Nakamura K, Morita T, Osuga T, et al. Prognostic value of right ventricular Tei index in dogs with myxomatous mitral valvular heart disease. J Vet Intern Med 2016;30:6975.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Paradies P, Spagnolo PP, Amato ME, et al. Doppler echocardiographic evidence of pulmonary hypertension in dogs: a retrospective clinical investigation. Vet Res Commun 2014;38:6371.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Tai TC, Huang HP. Echocardiographic assessment of right heart indices in dogs with elevated pulmonary artery pressure associated with chronic respiratory disorders, heart-worm disease, and chronic degenerative mitral valvular disease. Vet Med (Praha) 2013;58:613620.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Visser LC, Scansen BA, Schober KE, et al. Echocardiographic assessment of right ventricular systolic function in conscious healthy dogs: repeatability and reference intervals. J Vet Cardiol 2015;17:8396.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Locatelli C, Spalla I, Zanaboni AM, et al. Assessment of right ventricular function by feature-tracking echocardiography in conscious healthy dogs. Res Vet Sci 2016;105:103110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Morita T, Nakamura K, Osuga T, et al. The repeatability and characteristics of right ventricular longitudinal strain imaging by speckle tracking echocardiography in healthy dogs. J Vet Cardiol 2017;19:351362.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Morita T, Nakamura K, Osuga T, et al. Repeatability and reproducibility of right ventricular Tei index derived from 3 echocardiographic methods for evaluation of cardiac function in dogs. Am J Vet Res 2016;77:715720.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Gentile-Solomon JM, Abbott JA. Conventional echocardiographic assessment of the canine right heart: reference intervals and repeatability. J Vet Cardiol 2016;18:234247.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Baron Toaldo M, Poser H, Menciotti G, et al. Utility of tissue Doppler imaging in the echocardiographic evaluation of left and right ventricular function in dogs with myxomatous mitral valve disease with or without pulmonary hypertension. J Vet Intern Med 2016;30:697705.

    • Crossref
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