Respiratory maneuvers in echocardiography: a review of clinical applications

Evaluation of the inferior vena cava (IVC) from the subcostal view is part of the routine TTE examination. The diameter of the IVC decreases in response to inspiration with minimal size observed at end inspiration when the negative intrathoracic pressure leads to an increase in RV filling from the systemic veins. IVC size is significantly influenced by patient position, being largest in the right lateral position, intermediate in the supine position, and smallest in the left lateral position [10]. The diameter of the IVC, measured with the patient in the left decubitus position at 1.0 to 2.0 cm from the junction with the RA, using the long axis view, and the percent decrease in its diameter during inspiration (collapsibility index) correlate with RA pressure. A brief sniff is often required [see Additional files 8, 9] as normal inspiration may not elicit the inspiratory response [3]:

A small IVC (usually < 1.2 cm) with spontaneous collapse is often seen in the presence of intravascular volume depletion [11].

In a recent paper, Brennan et al evaluated the IVC diameter in patients undergoing right heart catheterization [12]. The measurements were made from the subcostal view with the patient in supine position. The authors questioned the traditional classification of RAP into narrow 5-mm Hg ranges based on IVC size and collapsibility. They found that the IVC size cutoff with optimum predictive use for RAP above or below 10 mm Hg was 2.0 cm (sensitivity 73% and specificity 85%). They also found that the optimal IVC collapsibility cutoff was 40% (sensitivity 73% and specificity 84%). Defining collapsibility as high (>55%), low (<35%), or normal (35%–50%) and the inferior vena cava as small (<1.7 cm), normal (1.7–2.1 cm), or large (>2.1 cm) the authors suggest a new classification of RAP:

There are several additional conditions to be considered when evaluating the IVC:

In patients with chronic obstructive pulmonary disease (COPD) pulmonary hypertension (PH) is sometimes difficult to assess by direct evaluation using the tricuspid regurgitant Doppler velocity because of emphysema or mediastinal deviation. An alternative method of respiration-aided evaluation of PH was proposed by Kunichika et al [14]. Authors found that the expiratory SVC peak systolic forward flow velocity (an index of the RA flow reserve during expiration) is increased in COPD patients with PH, owing to enhancement of the RA flow reserve through the respiratory cycle that compensates for the impaired right ventricular (RV) filling caused by PH. Therefore, respiratory variation in SVC systolic forward flow may be a useful Doppler flow index for the assessment of severity of PH in patients with stable, chronic COPD that cannot been assessed by conventional TTE

Transmitral Doppler flow parameters are widely used in the assessment of LV diastolic function. It is well known that with spontaneous respiration small changes (<15%) in transmitral peak flow velocities occur in healthy subjects. While some authors found no alteration in the ratio of early-to-late peak flow velocity (E/A) [15] other studies reported a significant decrease in E/A ratio with inspiration in normal subjects [16].

The potential effects of spontaneous respiration on mitral inflow Doppler patterns in patients with abnormal LV diastolic function are poorly understood. Tsai et al. [17] observed that during inspiration, the early diastolic peak flow velocity and E/A ratio were reduced in patients with coronary artery disease and abnormal LV relaxation pattern. More recently, Yuan et al. [18] evaluated 51 hypertensive patients presenting with different LV diastolic patterns and observed in 10 of them a characteristic trasmitral Doppler flow phenomenon that displayed E/A ratio > 1 on expiration and < 1 on inspiration. As 8 of 10 patients revealed an early-to-late diastolic tissue velocity ratio <1 authors suggested that this phenomenon could characterize either a new type of diastolic impairment or just pseudo-normal filling unmasked by inspiration. They also suggested that reversed E/A ratio at end-inspiration rather than at end-expiration might be a more sensitive and accurate indicator for abnormal LV diastolic function. Further studies using simultaneous invasive measures are needed to confirm these findings. As the potential effects of respiration on mitral inflow Doppler pattern is still under debate it seems reasonable to take measurements either with simultaneous recording of respiration or during short periods of apnea/by averaging multiple consecutive beats to minimize the effects of respiration.

In diseased ventricles, progressive shortening of the transmitral DT and increasing E/A ratio can be seen with decreasing ventricular compliance and increasing left atrial pressure. Impaired relaxation is frequently masked by elevated filling pressures resulting in a pseudonormal flow pattern (E/A ratio >1). The Valsalva maneuver has been found to effectively unload the heart and unmask an impaired relaxation pattern and high filling pressures in patients with a baseline pseudonormal flow pattern. This maneuver is accomplished first by cessation of breathing at any point in the respiratory cycle when assessment of mitral inflow is optimized. Next, the participant exerts a firm contraction of the abdominal muscles to force air against the closed glottis for approximately 10 seconds thereby increasing the intrathoracic pressure. In order to be properly performed, the Valsalva maneuver should be standardized. This can be done by attaching a mouthpiece (e.g. the tube of a syringe from which the plunger has been detached) to a sphygmomanometer and asking the patient to blow into it in order to raise the column of Hg to 40 mm and keep it stable at this value for 10 seconds [19]. This results in a decrease in both right ventricular and LV filling as a result of an increased thoracic-to-extrathoracic pressure gradient. The mitral inflow pattern is observed for changes during live 2D monitoring of the placement of the Doppler sample. An absolute decrease in the mitral E/A ratio of 0.5 or more can predict an elevated LV filling pressure with a specificity of 100% [20].

Changes in transmitral E/A ratio during the Valsalva maneuver across different stages of diastolic dysfunction were recently described by Reagan et al [21].

Because the E/A ratio increases as filling pressures rise it is generally assumed that an E/A ratio <1 (impaired relaxation pattern) indicates lower or even normal filling pressures when compared with patients who have a pseudonormal or restrictive filling pattern. However, Schwammenthal et al demonstrated that patients with an E/A ratio of <1 can nonetheless have severely elevated filling pressures. In these patients LV relaxation is so severely impaired that E/A ratio remains <1 despite increased filling pressures. The standardized Valsalva maneuver can unmask the presence of elevated filling pressures in patients with a baseline impaired relaxation pattern. The A wave will increase during the maneuver in patients with elevated filling pressures in proportion to the level of LV end-diastolic pressure, and independent of the baseline transmitral flow pattern [19].(Figure 5)

The increased pericardial pressure in cardiac tamponade produces reciprocal respiration-related changes in right and left ventricular volumes, diastolic filling, and systolic emptying that can be documented by echocardiography. The normal effects of respiration are accentuated such that venous return and right-sided filling occur during inspiration as intrathoracic pressures fall, providing a pressure gradient from the systemic veins to the RA. Because the total intrapericardial volume is fixed by the pressurized effusion, this increased inspiratory RV filling causes the interventricular septum to shift to the left, exaggerating the normal decrease in LV filling volume and, hence, stroke volume (ventricular interdependence). Thus, in tamponade, left heart filling occurs preferentially during expiration when there is less filling of the right heart. The small normal respiratory variation in left ventricular (LV) stroke volume and systolic arterial pressure (<10 mm Hg) is markedly accentuated in cardiac tamponade, resulting in the clinical finding of "paradoxical pulse" [1, 22‐24].

Echocardiography is particularly useful in demonstrating the exaggerated phasic variation in cardiac volumes and flows caused by tamponade [23]. The diastolic collapse of the free walls of the right atrium and/or right ventricle, due to compression of these relatively low-pressure chambers by the higher-pressure pericardial effusion, is exaggerated during expiration when right heart filling is reduced. The intermittent collapse of these structures is best documented with M-mode echo. [see Additional files 10, 11] Right ventricular collapse may not be seen in patients with PH and RV hypertrophy [25]

Respiratory variation in tricuspid and pulmonary flow is more dramatic than mitral and aortic flow, but there is progressive impairment in all intracardiac flows as the degree of tamponade worsens: with inspiration, the RV early diastolic filling is augmented (>25%), while LV diastolic filling diminishes (>15%). The flow velocity integral in the pulmonary artery increases with inspiration, while the aortic flow velocity integral decreases (>10%) [1].

The hepatic vein flow pattern may also reflect the exaggerated respiratory phase dependency of right ventricular filling. The loss of forward flow in the hepatic veins during the expiration phase of the respiratory cycle with flow out of the hepatic veins confined to the early inspiratory phase can be observed in patients with hemodynamically significant pericardial effusion [1]. Superior vena cava flow shows a reduction in diastolic flow velocities (<0.15 m/sec) initially in expiration, later in inspiration as well (systolic dominant and monophasic) [26]

In constrictive pericarditis, the rigid pericardium impedes the transmission of intrathoracic pressures to the cardiac chambers. During inspiration there is a lower driving force from the lungs into the left side of the heart and the LV becomes underfilled. The constricting pericardium also results in an increase interventricular interaction, so that with LV volume decrease, there is a corresponding increase in right ventricular volume [27] [see Additional file 12]

In Doppler echocardiographic studies the dissociation of intrathoracic and intracardiac pressures is manifested by an inspiratory increase in peak tricuspid flow velocity and a simultaneous decrease in mitral flow velocity, with opposite changes occurring in expiration [24].

A patent foramen ovale (PFO) can be reliably detected with contrast echocardiography, using agitated saline; the transthoracic and transesophageal echocardiography evaluation for detecting a patent foramen ovale is performed during normal respiration and during Valsalva maneuver During Valsalva, atrial shunting from right to left will begin during the release phase (phase III) [36]. The Valsalva maneuver may enhance atrial level shunting because of increase in right heart pressure, making the shunt detectable by either transthoracic echocardiography (TTE) or, with a better sensitivity, by transesophageal echocardiography (TEE). From a clinical point of view, it appears that a resting PFO may have a higher risk for clinical events than a PFO with shunt only during a provocative maneuver.

The right-to-left shunt of a large atrial septal defect may be nearly continuous, whereas for smaller atrial septal defects the appearance of contrast in the left atrium may be phasic, coordinated with the respiratory cycle; during inspiration, right heart filling increases, thus increasing the flow of contrast into the right atrium.

In patients with obstructive hypertrophic cardiomyopathy the obstruction of the LV outflow tract is dynamic and may be mild or nonexistent at rest. Echocardiography during Valsalva maneuver can unmask latent gradients in patients without resting obstruction and reveal the basis for drug treatment choices. During the strain phase of Valsalva maneuver, due to the decrease in preload, end-diastolic left ventricular volume and afterload, SAM occurs earlier in systole, mitral-septal contact lasts longer and left ventricular outflow tract gradient increases (Figure 8).