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Detection of Myocardial Dysfunction in Septic Shock: A Speckle-Tracking Echocardiography Study

Shahul, Sajid MD, MPH*; Gulati, Gaurav MD; Hacker, Michele R. ScD, MSPH; Mahmood, Feroze MD*; Canelli, Robert MD*; Nizamuddin, Junaid MD*; Mahmood, Bilal BA§; Mueller, Ariel MA*; Simon, Brett A. MD, PhD*; Novack, Victor MD, PhD‖¶; Talmor, Daniel MD, MPH*

doi: 10.1213/ANE.0000000000000943
Critical Care, Trauma, and Resuscitation: Research Report

BACKGROUND: Patients with septic shock are at increased risk of myocardial dysfunction. However, the left ventricular ejection fraction (EF) typically remains preserved in septic shock. Strain measurement using speckle-tracking echocardiography may quantify abnormalities in myocardial function not detected by conventional echocardiography. To investigate whether septic shock results in greater strain changes than sepsis alone, we evaluated strain in patients with sepsis and septic shock.

METHODS: We prospectively identified 35 patients with septic shock and 15 with sepsis. These patients underwent serial transthoracic echocardiograms at enrollment and 24 hours later. Measurements included longitudinal, radial, and circumferential strain in addition to standard echocardiographic assessments of left ventricular function.

RESULTS: Longitudinal strain worsened significantly over 24 hours in patients with septic shock (P < 0.0001) but did not change in patients with sepsis alone (P = 0.43). No significant changes in radial or circumferential strain or EF were observed in either group over the 24-hour measurement period. In patients with septic shock, the significant worsening in longitudinal strain persisted after adjustment for left ventricular end-diastolic volume and vasopressor use (P < 0.0001). In patients with sepsis, adjustment for left ventricular end-diastolic volume and vasopressor use did not alter the finding of no significant differences in longitudinal strain (P = 0.48) or EF (P = 0.96).

CONCLUSIONS: In patients with septic shock, but not sepsis, myocardial strain imaging using speckle-tracking echocardiography identified myocardial dysfunction in the absence of changes in EF. These data suggest that strain imaging may play a role in cardiovascular assessment during septic shock.

Published ahead of print September 22, 2015

From the *Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; University of Pennsylvania, Philadelphia, Pennsylvania; Beth Israel Deaconess Medical Center Harvard Medical School, Boston, Massachusetts; §University of Albany Medical School, Albany, New York; Clinical Research Center, Soroka University Medical Center, Beer-Sheva, Israel; and Faculty of Health Sciences, Ben–Gurion University of Negev, Israel.

Accepted for publication June 15, 2015.

Published ahead of print September 22, 2015

Funding: This work was conducted with support from FAER (Foundation for Anesthesia Research) and Harvard Catalyst|The Harvard Clinical and Translational Science Center (National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health Award 8UL1TR000170-05 and financial contributions from Harvard University and its affiliated academic health care).

The authors declare no conflicts of interests.

Reprints will not be available from the authors.

Address correspondence to Sajid Shahul, MD, MPH, Anesthesia and Critical Care, Beth Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA 02215. Address e-mail to sshahul@bidmc.harvard.edu.

Key recommendations of the current Surviving Sepsis Campaign guidelines include early recognition and treatment of sepsis-induced myocardial dysfunction.1 Although the exact mechanism of sepsis-induced myocardial dysfunction is unclear, current evidence suggests that intrinsic cellular depression (e.g., mitochondrial or β-receptor downregulation), circulating tumor necrosis factor-α, interleukin-6β, and volume resuscitation may be involved.2 Evidence from cardiac magnetic resonance imaging also suggests that this dysfunction may be because of a combination of myocardial inflammation and acidosis.3 However, despite these processes, the ejection fraction typically remains preserved in septic shock,4,5 preventing ready diagnosis and treatment. The importance of early recognition is supported by autopsy studies in patients dying from septic shock that demonstrate potentially reversible mitochondrial injury.6,7 Potential benefits of early recognition may include optimized coronary perfusion, tailored volume resuscitation, appropriately targeted use of inotropes and vasopressors, and possibly, the use of cardioprotective agents such as β-blockers.8

Previous investigations have characterized many aspects of myocardial function in sepsis5,9,10; however, few data have detailed the evolution of myocardial dysfunction in septic shock and whether these changes depend on initial sepsis severity. Such information may be valuable in sepsis management, because recent studies have shown that ejection fraction at the onset of septic shock does not differ between survivors and nonsurvivors.4,5 This contrast between ongoing myocardial dysfunction during sepsis and the lack of detectable changes in ejection fraction may potentially be resolved with more sophisticated measures of myocardial dysfunction such as myocardial strain. In other disease states, echocardiographic assessment of myocardial strain can detect changes in myocardial function not measured by conventional echocardiographic indices of systolic function.11

Strain measurement using speckle-tracking echocardiography is a recently developed technique based on the generation of ultrasound B-mode echoes called “speckles” that represent discrete myocardial areas and are tracked throughout the cardiac cycle.12 Changes in the distance between individual speckles can then be used to assess changes in the length of segments in longitudinal (long axis from base to apex), radial (inward short axis), and circumferential (rotational short axis) planes (Fig. 1).13 Strain is defined as the difference between the final length of the cardiac segment relative to its resting length. Because the myocardial length shortens in ventricular systole, longitudinal and circumferential strain values are negative with normal heart function, whereas radial strain is positive (Fig. 2).13 This method is more sensitive than ejection fraction, which is based on fractional change in volume between systole and diastole. Because inward movement in systole tethers diseased and normal segments together, ejection fraction can be relatively insensitive to subtle changes in myocardial function.14 In contrast to left ventricular ejection fraction, which measures global function, strain with speckle-tracking measures both regional and global functions. Measurement of global longitudinal strain also assesses the function of subendocardial longitudinal fibers that are particularly disposed to ischemia and changes in wall stress.15 Furthermore, this calculation may detect myocardial dysfunction under conditions of reduced afterload, such as in sepsis.16 Longitudinal, radial, and circumferential strain measurements are also less prone to measurement error because they avoid the geometric assumptions used in the calculation of left ventricular ejection fraction.17–19 Speckle tracking has been used to detect subclinical myocardial dysfunction in other disease states19–21 and can prognosticate mortality and heart failure in patients with preserved ejection fractions.22,23

Figure 1

Figure 1

Figure 2

Figure 2

To better describe changes in strain in septic patients, we examined changes in myocardial strain over 24 hours in patients with a diagnosis of sepsis or septic shock. We hypothesized that we would detect changes in left ventricular myocardial strain in patients with septic shock despite normal ejection fractions, whereas patients with sepsis without associated shock would not show such changes.

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METHODS

Assembly of the Cohort

The IRB of Beth Israel Deaconess Medical Center in Boston, Massachusetts, approved this prospective study via a verbal consent process. We offered participation to all patients who met eligibility criteria. The study was conducted between March 2010 and July 2014. From March 2010 to April 2012, we enrolled 35 subjects. An interim analysis of the data was performed, and the sample size was recalculated. We then resumed enrollment from July 2013 to 2014 and enrolled an additional 15 subjects.

Patients were eligible if they were at least 18 years of age, not pregnant, without significant valvular stenosis or regurgitation, without ST-segment elevation or arrhythmia, which included bundle branch blocks on the monitor and met the Surviving Sepsis Campaign definition of sepsis or septic shock.24 Sepsis was defined as probable or documented infection combined with systemic manifestations of infection. Septic shock was defined as sepsis-induced hypotension, despite appropriate fluid management. Participants were recruited consecutively from the intensive care units (ICUs) or emergency department/wards.

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Echocardiography

Transthoracic echocardiography was performed in the ICUs and wards on the day of admission with a Philips CX50 machine by 1 of 3 expert sonographers at enrollment (hour 0) and 24 hours later. At the conclusion of the study, strain measurements were read in a blinded manner as related to both timing (0 vs 24 hours) and diagnosis (sepsis versus septic shock). Images were obtained with the patient lying in the supine or left lateral position and reported according to the American Society of Echocardiography guidelines.25 Images were stored in a cine-loop format of 3 cardiac cycles of uncompressed data with associated electrocardiogram information. A comprehensive examination for each patient was performed, including a complete 2-dimensional (2D) and color flow Doppler valvular assessment.

Ejection fraction was calculated using the Simpson biplane disc method. The tracking quality of all images was assessed before analysis. Strain measurement was performed using a validated, vendor-independent, 2D speckle-tracking echocardiographic tracking software (2D Cardiac Performance Analysis v1.1; TomTec Imaging Systems, Unterschleissheim, Germany).26 This software can use ultrasound data from any echocardiography machine and produces strain values that are in good agreement with other frequently used software packages.27 Strain was measured by tracing the endocardial border of the left ventricle at the initial frame with the best endocardial border definition across the maximal number of segments. Longitudinal strain was measured in the apical 4-chamber view; radial and circumferential strain were measured in the parasternal short-axis view. Peak systolic strain (longitudinal, radial, and circumferential) was measured using an average of 3 consecutive cardiac cycles. The average of 6 regional values in the apical 4-chamber and parasternal mid-papillary short-axis views was used to measure longitudinal, radial, and circumferential strain. Images with inadequate endocardial border tracking (>2 segments) were excluded from strain measurements. The frame rates used for strain acquisition and measurements were between 40 and 70 fps/sec.

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Resuscitation Algorithm for Septic Shock and Sepsis

During the first 6 hours, the goals of resuscitation were mean arterial pressure (MAP) ≥65 mm Hg, urine output ≥0.5 mL/kg/h, and superior vena cava oxygen saturation ≥70%. If hypotension persisted despite appropriate fluid resuscitation (30 mL/kg), vasopressors were initiated to target an MAP ≥65 mm Hg. The choice of vasopressors was based on the Surviving Sepsis Campaign guidelines in combination with an interdisciplinary protocol developed at Beth Israel Deaconess Medical Center to manage patients with septic shock. The initial vasopressor in the protocol was norepinephrine, unless contraindicated (e.g., tachyarrhythmia).28 Subsequent vasopressor choice was determined by patient physiology and Surviving Sepsis Campaign guidelines. During the first 3 hours, the goals of fluid resuscitation were 30 mL/kg in the sepsis group.

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Statistical Analysis

Descriptive statistics are presented as mean (±SD), median (interquartile range), or proportion, based on data type and distribution. Normality of continuous variables was assessed with the Shapiro–Wilk test. Comparisons between groups were made using the Student t, Wilcoxon rank sum, or χ2 test, as appropriate. Given the exploratory nature of this study, we did not perform an a priori sample size calculation.

To assess changes in echocardiographic measurements within each group, we created a separate regression model for each of the 3 strain measurements using a repeated measures model with robust standard error estimation and exchangeable correlation structure. For each model, the echocardiographic measurement was the outcome and time (0 or 24 hours) was the explanatory variable. Based on a priori knowledge that prior volume state and vasopressor use (phenylephrine, norepinephrine, and vasopressin) influence strain, the models were adjusted for the dose of each vasopressor and for left ventricular end-diastolic volume. A LOWESS function was used to assess the linearity of the relationship between the continuous predictor and the outcome. The model with the lowest QIC was deemed the best-fitting model. All tests were 2-sided, and P values <0.01 were considered statistically significant because of the exploratory nature of this study. Analyses were performed using Stata version 12.1 (Stata Corp., College Station,TX).

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RESULTS

All eligible participants whom we approached agreed to participate. We enrolled 59 patients. Six were excluded for inadequate image quality, and 3 were excluded because they died before we obtained echocardiographic measurements (3 patients who died were in the septic shock group; 1 sepsis and 2 septic shock patients were excluded for image quality). Of the included participants, 35 (70.0%) had septic shock and 15 (30.0%) were diagnosed with sepsis. Patients who had ever received vasopressors were included in the septic shock group. One patient who progressed to septic shock after initial enrollment in the sepsis group was analyzed in the septic shock group. The 2 groups were similar with respect to baseline characteristics, including baseline strain and ejection fraction measurements assessed on admission (all P ≥ 0.18; Table 1). Acute Physiology and Chronic Health Evaluation II, troponins, blood pressure, MAP, lactate, and creatinine were measured at the time of enrollment and 24 hours later (Table 2). At baseline, the septic shock group had a greater Acute Physiology and Chronic Health Evaluation II score (P = 0.04), a greater Sequential Organ Failure Assessment score (P = 0.0009), and lower MAP (P = 0.03). Among patients in the septic shock group, 24 (68.6%) were mechanically ventilated, as were 4 (26.7%) in the sepsis group.

Table 1

Table 1

Table 2

Table 2

In the crude regression model, longitudinal strain in patients with septic shock significantly worsened over 24 hours (P < 0.0001), whereas in patients with sepsis alone no change in longitudinal strain was observed over 24 hours (P = 0.43). No significant changes during the 24-hour measurement period were observed in either group for radial strain, circumferential strain, or ejection fraction (Table 3).

Table 3

Table 3

After multivariate adjustment for vasopressor administration and end-diastolic volume, the change in longitudinal strain observed over 24 hours in patients with septic shock persisted (P < 0.0001). Multivariate adjustment did not alter our findings of no change in radial strain, circumferential strain, or ejection fraction. In the sepsis group, no significant differences in longitudinal strain, radial strain, circumferential strain, or ejection fraction were noted after adjustment for end-diastolic volume.

After we stratified the groups for ischemic heart disease, our findings with respect to longitudinal strain did not change in either group (P = 0.44 for sepsis and 0.10 for septic shock). In addition, no significant differences in troponin between sepsis and septic shock patients were found at enrollment (P = 0.84) or at 24 hours (0.17).

As noted previously, no patients in the sepsis group received vasoconstrictors. Among all septic shock patients, 54.29% received only norepinephrine, 14.29% received only phenylephrine, and no patients received vasopressin only. In our study, 2 patients (5.7%) received both norepinephrine and phenylephrine, whereas 3 patients (8.6%) received both norepinephrine and vasopressin. The proportion of patients receiving norepinephrine, phenylephrine, and vasopressin simultaneously was 11.2%.

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DISCUSSION

In this study of critically ill patients, speckle-tracking echocardiography identified worsening myocardial dysfunction over 24 hours in patients with septic shock but not sepsis alone. These changes were not detectable via echocardiographic measurement of ejection fraction but could be identified by assessment of myocardial strain. The time course of our findings also suggests that effects of septic shock on myocardial performance may occur early after the onset of shock. Targeting these patients early for intervention may improve outcomes.

Our study demonstrates the greater sensitivity of longitudinal strain as a measure of cardiac dysfunction in patients with septic shock and sepsis. After adjustment for vasopressor administration and end-diastolic volume, we found significant changes in longitudinal strain but saw no corresponding change in left ventricular ejection fraction over the same time period.

Our results are similar to previous animal and clinical studies in which authors compared strain echocardiography with ejection fraction measurement. Recently, Hestenes et al.16 demonstrated in a pig model a significant decrease in longitudinal strain without changes in ejection fraction (−17.2 ± 2.8 to −12.3% ± 3.2). Similar results in longitudinal strain were demonstrated by Basu et al.29 in a retrospective analysis of children admitted with septic shock.

Although left ventricular ejection fraction is used routinely for measuring left ventricular systolic function, newer techniques, such as speckle tracking, are increasingly used to monitor cardiac function in disease states, such as preeclampsia, cardiotoxic chemotherapy and Behcet disease.20,21,30 Although the mechanisms underlying changes in strain with septic shock are understood incompletely, one possibility is that microvascular vasoconstriction in the highly vulnerable subendocardial muscle layer might result in ischemic injury.31 Both coronary vasoconstriction and a decreased response to vasodilators, such as sodium nitroprusside in the coronary circulation, have been observed by Bogle et al.31 in a rabbit heart model of endotoxemia. This altered coronary microvascular tone may partly explain the changes in strain we observed.32 That we found changes in strain without corresponding changes in troponin levels suggests that strain identifies focal longitudinal muscle dysfunction rather than myocyte injury. Previous work suggests that the lack of change we observed in radial and circumferential strain represents compensation by the radial and circumferential fibers.33

Pulido et al.,5 Furian et al.,10 and Landesberg et al.34 have demonstrated previously the presence of myocardial dysfunction in severe sepsis using conventional echocardiography. The mean ejection fraction and standard deviation in these studies (Pulido et al.,5 56.8 ± 16; Furian et al.,10 57 ± 13) are in good agreement with our study. Our study further expands their work by demonstrating the presence of ongoing systolic myocardial dysfunction via strain measurement, despite preserved ejection fraction.5,10

Although factors affecting myocardial wall stress, such as afterload and volume status, may affect longitudinal or circumferential strain values,35–37 we observed differences in longitudinal strain even after adjustment for vasopressors. We also note that, despite using different vasopressor resuscitation strategies than Landesberg et al.,34 we report similar longitudinal strain values at 24 hours (−12.7 ± 5.64 vs −12.3 ± 3.6). Recent data in animals support the utility of strain measurement in the presence of vasopressors. In a rabbit model, Ho et al.36 found that at comparable blood pressures, strain did not depend on whether norepinephrine or phenylephrine was used or on the dose of vasopressin. In addition, changes in longitudinal strain are not significantly affected by positive end-expiratory pressure titration, which supports the validity of our data.38,39

Our study may have clinical implications. Once detected, subclinical myocardial dysfunction may be amenable to cardioprotective strategies, including β-blocker use, even if the ejection fraction remains normal. In one study of patients given cardiotoxic chemotherapy, β-blockers reversed changes in longitudinal strain.14 Another preliminary study in septic patients receiving norepinephrine found an improved outcome with β-blocker administration.8

Myocardial strain measurement may also help with prognosis in septic shock patients. Recently, Orde et al.40 demonstrated that, despite a normal ejection fraction, severe right ventricular free wall longitudinal strain dysfunction was associated with a high rate of mortality in patients with severe sepsis and septic shock.

Our observational study has limitations. Despite statistically significant differences, our sample size was small, which underscores the need for large-scale prospective studies to replicate our findings. In addition, our initial strain measurement was performed on admission to the ICU, not upon meeting septic shock or sepsis criteria. As a result, we cannot describe changes in longitudinal strain that occurred before or after our 24-hour monitoring period. We also did not measure strain during recovery from septic shock, to determine whether strain values regress to baseline values. Patients in the septic shock group also had a greater proportion of ischemic heart disease, which may have contributed to the changes that we found. Finally, speckle-tracking technology is relatively new, and current implementations require adequate endocardial border definition, which may be challenging because of volume resuscitation, mechanical ventilation, or suboptimal positioning. In addition, no standard values or protocols exist for strain analysis.

In summary, we conclude that early (<24-hour) changes in myocardial function because of septic shock are detectable using echocardiographic speckle-tracking technology. Our data raise the possibility that monitoring strain may better identify patients with myocardial dysfunction because of septic shock than measurement of ejection fraction. Whether early detection of subclinical left ventricular dysfunction and subsequent treatment can improve long-term outcome needs to be evaluated in future studies.

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DISCLOSURES

Name: Sajid Shahul, MD, MPH.

Contribution: This author helped with conception and design, acquisition of data, analysis and interpretation of data; drafting the article; approving final version of article.

Attestation: Sajid Shahul approved the final manuscript.

Name: Gaurav Gulati, MD.

Contribution: This author helped with the acquisition of data, analysis and interpretation of data; drafting the article.

Attestation: Gaurav Gulati approved the final manuscript.

Name: Michele R. Hacker, ScD, MSPH.

Contribution: This author helped with analysis and interpretation of data and critically revising the article.

Attestation: Michele R. Hacker approved the final manuscript.

Name: Feroze Mahmood, MD.

Contribution: This author helped with the acquisition of data, analysis and interpretation of data, and critically revising the article.

Attestation: Feroze Mahmood approved the final manuscript.

Name: Robert Canelli, MD.

Contribution: This author helped with analysis and interpretation of data and critically revising the article.

Attestation: Robert Canelli approved the final manuscript.

Name: Junaid Nizamuddin, MD.

Contribution: This author helped with analysis and interpretation of data and critically revising the article.

Attestation: Junaid Nizamuddin approved the final manuscript.

Name: Bilal Mahmood, BA.

Contribution: This author helped with analysis and interpretation of data and critically revising the article.

Attestation: Bilal Mahmood approved the final manuscript.

Name: Ariel Mueller, MA.

Contribution: This author helped with analysis and interpretation of data and critically revising the article.

Attestation: Ariel Mueller approved the final manuscript.

Name: Brett A. Simon, MD, PhD.

Contribution: This author helped with the conception and design, analysis and interpretation of data, and critically revising the article.

Attestation: Brett A. Simon approved the final manuscript.

Name: Victor Novack, MD, PhD.

Contribution: This author helped with analysis and interpretation of data and drafting the article.

Attestation: Victor Novack approved the final manuscript.

Name: Daniel Talmor, MD, MPH.

Contribution: This author helped with the conception and design, acquisition of data, analysis, and approving the final version of article.

Attestation: Daniel Talmor approved the final manuscript.

This manuscript was handled by: Avery Tung, MD.

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