Assessment of left ventricle myocardial deformation in a hemorrhagic shock swine model by two-dimensional speckle tracking echocardiography : Journal of Trauma and Acute Care Surgery

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Assessment of left ventricle myocardial deformation in a hemorrhagic shock swine model by two-dimensional speckle tracking echocardiography

Doria de Vasconcellos, Henrique MD, MSc, PhD; Saad, Karen Ruggeri PhD; Saad, Paulo Fernandes MD, PhD; Otsuki, Denise Aya PhD; Ciuffo, Luisa A. MD; Lester, Laeben MD; Koike, Marcia Kiyomi PhD; Armstrong, Anderson da Costa MD, PhD; Lima, Joao A. C. MD, MBA; Montero, Edna Frasson de Souza MD, PhD

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Journal of Trauma and Acute Care Surgery: December 2022 - Volume 93 - Issue 6 - p 838-845
doi: 10.1097/TA.0000000000003644
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Despite significant advances in emergency and urgent care in the last years, trauma is still one of the most important causes of mortality worldwide, disproportionally affecting younger individuals, and stands as the single most significant cause of years lost and productivity lost in the United States.1,2 Moreover, hemorrhagic shock (HS) is the most potentially preventable cause related to deaths after trauma, occurring early before arriving at the hospital, and associated with coagulopathy, microcirculation dysfunction, and prominent inflammatory response.3,4

Several studies demonstrated the development of trauma-induced secondary cardiac injury (TISCI) and dysfunction, independent of direct heart trauma, due to myocardial ischemia and ischemia-reperfusion injury, prompted by cardiomyocyte death and microvascular injury, and leading to increased morbidity and risk of death.5,6

The analysis of myocardial deformation or strain by speckle tracking echocardiography (STE) is a novel noninvasive imaging tool to measure cardiac performance, and it has been shown to have superior sensitivity, reproducibility, accuracy, and predicted power to cardiovascular (CV) events when compared with established methods such as left ventricle (LV) ejection fraction.7,8 The STE is based on imaging processing algorithms that identify and track myocardial footprints (speckles) originated from the interaction between the ultrasound and myocardial tissue within the region of interest (usually a square measuring 10 × 10 mm). The distance between the speckles is tracked during the cardiac cycle frame by frame. By convention, positive values are assigned to thickening, whereas negative values are assigned to shortening. Longitudinal and circumferential strain parameters reflect shortening, and more negative values represent enhanced deformation.9

Previous investigations demonstrated an independent prognostic value of lower LV and right ventricle global longitudinal strain (GLS) in the mortality of patients with sepsis and septic shock.10,11 However, there is a lack of data investigating the role of the strain assessment by STE on HS. Adopting a swine model of controlled HS, this study sought (1) to examine the usefulness of LV strain as a diagnostic tool of subclinical cardiac dysfunction associated ischemia-reperfusion myocardial injury, (2) to assess the temporal relationship between the LV strain and traditional hemodynamic and tissue oxygenation parameters, and (3) to investigate the efficacy of the experimental study protocol of HS to determine myocardial ischemic-reperfusion injury. We hypnotized that the myocardial strain would reduce during severe HS, rapidly improving after a complete blood reposition. Differences in the strain parameters between the baseline and postreposition research times would be attributed to TISCI.

MATERIALS AND METHODS

The research experiments were performed in the Anesthesia Research Medical Laboratory — LIM 08, School of Medicine, University of São Paulo (Faculty of Medicine of the University of São Paulo, São Paulo, Brazil). Seven healthy male Landrace pigs were obtained from an accredited farm specialized in supply animals for scientific studies and were brought to the laboratory on the day of the experiment. All animals were handled following the Statement of Ethical Principles for the Care and Use of Animals in Biotechnology Research guidelines. The University of São Paulo School of Medicine's Research Ethics Committee previously approved the research project. Supplementary data online describes in detail the methods (Supplementary Figs. S1 and S2, https://links.lww.com/TA/C493) and provide additional tables and figures results (Supplementary Figs. S3–S6, https://links.lww.com/TA/C493; Supplementary Tables S1–S5, https://links.lww.com/TA/C493). All experimental details are reported per Animal Research: Reporting of In Vivo Experiments guidelines (Supplemental Digital Content, Supplementary Data 1, https://links.lww.com/TA/C494).

Research Experimental Protocol

The experimental control HS was obtained through three sequentially blood withdraws, an interval of 30 minutes, of 20% of estimated blood volume through the femoral artery catheter. All blood drawn was stored in sterile plastic blood collection bags. Severe shock status was maintained for 60 minutes. Subsequently, aggressive volume replacement was performed by rapid intravenous administration of all collected blood using the left femoral venous access. Calcium gluconate (30 mg/kg) intravenous was administered slowly at the end of the blood infusion, intending to avoid hypocalcemia occasionated to the citric acid contained in the stored blood bags. The animals were observed for 120 minutes after complete blood volume replacement and were submitted to euthanasia after this period.

The study data collection protocol occurred in five predetermined times: T0, after anesthetic induction and hemodynamic stabilization; T1, 1 hour after a severe shock status was established; T2, immediately after complete blood volume replacement; T3, 1 hour after complete blood volume replacement; and T4, 2 hours after complete blood volume replacement (Figs. 1 and 2).

F1
Figure 1:
The study data collection protocol. T0, after anesthetic induction and hemodynamic stabilization; T1, 1 hour after a severe HS status was established; T2, immediately after complete blood volume replacement; T3, 1 hour after complete blood volume replacement; and T4, 2 hours after complete blood volume replacement.
F2
Figure 2:
Study design's infographic. T0, after anesthetic induction and hemodynamic stabilization; T1, 1 hour after a severe HS status was established; T2, immediately after complete blood volume replacement; T3, 1 hour after complete blood volume replacement; and T4, 2 hours after complete blood volume replacement.

Echocardiography

The echocardiographic evaluation was performed using Artida ultrasound system (Toshiba Medical Systems, Otawara, Japan) by a single experienced echocardiographic examiner, certified by the Brazilian Society of Cardiology, following a standard protocol based on the American Society of Echocardiography guidelines.12 The animals were scanned in a dorsal decubitus, an open chest, and the ultrasound transducer was in direct contact with the heart. Standard parasternal short axis, apical four cameras, and apical two cameras views were acquired. Electrocardiogram tracing was recorded during the entire examination. All the recorded images and measurements were done at the end of the expiration, with a total capture of three cardiac cycles.

A 1.8- to 4.2-MHz PST-30BT phased-array transducer was used to acquire the two-dimensional (2D) tissue harmonic imaging, color Doppler, pulse-wave Doppler, continuous-wave Doppler, and 2D images dedicated to speckle tracking analysis. Two-dimensional LV end-diastolic volume, LV end-systolic volume, and LV ejection fraction (LVEF) were measured by the biplane disc method (modified Simpson's rule) in the four-chamber view. Pulse wave Doppler echocardiography was used to measure the transmitral flow peak velocities from the early (E) and late (A) diastolic phases. Tissue Doppler imaging was applied to calculate the early septal and lateral mitral annulus diastolic peak (E prime). M-mode was used in the lateral tricuspid annulus in the four-chamber view and used to calculate the tricuspid annulus posterior systolic excursion.

Detailed quality control procedures were performed during the study period to ensure adequate reproducibility and accuracy of the data. The echocardiograms were stored digitally and transferred electronically to the Johns Hopkins reading center using a protected web-based technology, where an expert reader analyzed the images using standard software (Digiview; Digisonics Systems, Houston, TX) following the American Society of Echocardiography guidelines.13

Speckle Tracking Echocardiography

Speckle tracking echocardiography evaluation was performed using Advanced Cardiology Package Wall Motion Tracking version 3.0 (Toshiba Medical Systems) following the American Society of Echocardiography consensus and guidelines.14,15 Longitudinal myocardial deformation (strain) was measured in the apical four cameras, setting landmarks in the endocardial border level of the mitral septal annulus, mitral lateral annulus, and LV apex. The circumferential strain was assessed in the parasternal short axis at the midventricular LV level, setting landmarks in the endocardial border level counter-clockwise at nine, six, and three position, not including trabeculation. After those anatomical references were indicated, a region of interest was automatically defined, and myocardium tracking was obtained. If necessary, further manual adjustments were made. End-diastole was considered as the beginning of the QRS complex, while end-systole was defined as the lowest LV volume. The strain was calculated as a ratio of the peak systolic segment length relative to the end-diastolic segmental length and represented as a percentage. Each echocardiographic view was divided into a six-segment model, and global values were defined as the average of segmental peaks (Supplemental Digital Content, Supplementary Video S1, https://links.lww.com/TA/C495, and Supplementary Video S2, https://links.lww.com/TA/C496).

Statistical Analysis

Continuous variables are presented as medians and interquartile ranges. The comparison between experimental study times for each variable was made using Wilcoxon rank-sum test (Mann-Whitney). Univariable linear regression analyses were used to assess the relationship between hemodynamic, metabolic, and echo variables with LV myocardial deformation. All analyses were conducted using STATA 14.2 (StataCorp LP, College Station, TX). A p value of <0.05 was considered statistically significant.

RESULTS

Seven healthy male Landrace pigs were used in the experiments with a median weight of 32 (26.1–33) kg and a median body surface area of 0.91 (0.79–0.94) m2. The median total blood withdrawn was 1,100 (1,080–1,190) mL, and the median diuresis during the entire procedure was 950 (530–1,450) mL.

Hemodynamic Variables

At 1 hour after a severe HS status was established (T1—evaluation time), there was a statistically significant reduction from the baseline values in the mean arterial pressure (70 [67–80] vs. 39 [36–46] mm Hg, p < 0.001), end-diastolic volume (153 [140–174] vs. 79.5 [67–89] mL, p < 0.001), cardiac index (3.5 [2.6–4.1] vs. 1.7 [1.6–2.0] L/min/m2, p < 0.001), and central venous pressure (10 [10–11] vs. 8 [8–9] mm Hg, p = 0.002) parameters. Also, there was a statistically significant increase on the heart rate (107 [92–116] vs. 209 [199–228] bpm, p = 0.018) and pulmonary vascular resistance (169 [121–205] vs. 494 [374–634] dyn/s/cm−5, p = 0.018) (Supplemental Digital Content, Supplementary Table S1 and Fig. S3, https://links.lww.com/TA/C493).

The majority of the hemodynamics parameters return to the initial values at the end of the experiment (T4—evaluation time) except for the heart rate (107 [92–116] vs. 135 [119–153] bpm, p = 0.018) and the systolic pulmonary artery pressure (25 [23–28] vs. 32 [28–37] mm Hg, p = 0.001), which persisted higher, and for the end-diastolic volume (153 [140–174] vs. 135 [118–159] mL, p = 0.024), which was lower compared with the baseline values (Supplemental Digital Content, Supplementary Table S1 and Fig. S3, https://links.lww.com/TA/C493).

Blood Gases Analysis

At 1 hour after a severe HS status was established, there was a statistically significant reduction in the arterial PH (7.46 [7.44–7.55] vs. 7.15 [7.10–7.33], p = 0.018), base excess (3.3 [2.4–3.4] vs. −15.3 [−16.3 to −3.1], p = 0.018), partial venous pressure of oxygen (PVO2) (40.9 [36.1–44.7] vs. 26.7 [23.2–29.1] mm Hg, p = 0.018), and mix-venous oxygen saturation (SVO2) (58.5% [52.4–61.0%] vs. 15.4% [10.5–27.5%], p = 0.018) and a statistically significant increase in the lactate (19 [16–26] vs. 74 [49–85] mg/dL) (Supplemental Digital Content, Supplementary Table S2 and Fig. S4, https://links.lww.com/TA/C493).

Two hours after complete blood volume reposition (T4—reposition time), the majority of the blood gases parameters tended to return to the normal range values; however, there was a statistically significant decrease on the PH (7.46 [7.44–7.55] vs. 7.40 [7.34–7.42], p = 0.022), PaO2 (149 [135–164] vs. 128 [122–142] mm Hg, p = 0.018), and arterial oxygen saturation (SaO2) (99.5 [98.8–99.9] vs. 98.7 [97.9–99.1] %, p = 0.028) and a statistically significant increase in the partial arterial pressure of carbon dioxide (PaCO2) (36.9 [32.7–39.3] vs. 41.5 [38.5–44.1] mm Hg, p = 0.018), PVO2 (40.9 [36.1–44.7] vs. 43.3 [41.2–46.9] mm Hg, p = 0.018), and SVO2 (58.5% [52.4–61%] vs. 63.4% [59.9–67%], p = 0.043), when comparing with the initial values (Supplemental Digital Content, Supplementary Table S2 and Fig. S4, https://links.lww.com/TA/C493).

Microdynamic Tissue Oxygenation Variables

At 1 hour after a severe HS status was established, there was a statistically significant reduction on the mix-venous oxygen content (6.2 [5.8–7.2] vs. 1.8 [1.3–3.4] mL/dL), p = 0.018) and oxygen deliver (48.1 [42.4–51.3] vs. 20.8 [17.8–26.5] mL/min, p = 0.018), with a compensatory increase in the oxygen extraction (42.6% [39.8–48.4%] vs. 84.2% [72.7–89%], p = 0.018) (Supplemental Digital Content, Supplementary Table S3 and Fig. S5, https://links.lww.com/TA/C493).

After the complete blood volume resuscitation, all the tissue oxygenation parameters reached supranormal levels, which at the end of the experiment persisted statically significant elevated in relation to the initial values for mix-venous oxygen content (6.2 [5.8–7.2] vs. 7.6 [7.1–9.0] vs. 7.6 [7.1–9] mL/dL, p = 0.018) and oxygen deliver (48.1 [42.4–51.3] vs. 57.3 (43.2–66.9) mL/min, p = 0.018) (Supplemental Digital Content, Supplementary Table S3 and Fig. S5, https://links.lww.com/TA/C493).

2D Echocardiography Variables

At 1 hour after a severe HS status was established, there was a statistically significant reduction on LV end-diastolic volume (45.7 [43.1–53.5] vs. 20.4 [16.6–22.1] mL, p = 0.018), LV end-systolic volume (23.8 [21.9–28.4] vs. 10.4 [8.1–11.3] mL, p = 0.018), left atrium maximum area (5.2 [4.7–7.6] vs. 2.6 [2.4–3.2] cm2, p = 0.018), left atrium maximum volume (12.4 [10.7–21.0] vs. 4.2 [3.8–5.9] mL, p = 0.018), and mitral annular diastolic peak velocity (9.8 [8–13] vs. 5.8 [4.8–7.5] cm/s, p = 0.018), and there was a statistically significant increase on the ratio between peak transmitral flow velocities from the early (E) diastolic phase and early mitral annular diastolic peak velocities (5.1 [4.4–7.9] vs. 9.2 [6.2–11.5], p = 0.018), comparing with the baseline values. All the 2D echocardiogram parameters return to the initial measurements at the end of the experiment (Supplemental Digital Content, Supplementary Table S4 and Fig. S6, https://links.lww.com/TA/C493).

LV Speckle Tracking Variables

At 1 hour after a severe HS status was established, there was a statistically significant absolute reduction on the LV GLS (−10.7% [−14.4 to −9%] vs. −5.3% [−6.6 to −4.6%], p = 0.018) and LV global circumferential strain (−9.6% [−10.7 to −8.0%] vs. −3.8% [−5.2 to −2.5%], p = 0.018) (Supplemental Digital Content, Supplementary Table S4, https://links.lww.com/TA/C493, and Figs. 3 and 4).

F3
Figure 3:
Box plots (A) and diamond plots (B) showing the global longitudinal strain data distribution during the experimental HS swine model. Data are presented as median (interquartile range). *p Value = 0.028, calculated by Wilcoxon rank-sum test comparing T0 and T4 protocol times. T0, after anesthetic induction and hemodynamic stabilization; T1, 1 hour after a severe HS status was established; T2, immediately after complete blood volume replacement; T3, 1 hour after complete blood volume replacement; and T4, 2 hours after complete blood volume replacement.
F4
Figure 4:
Box plots (A) and diamond plots (B) showing the GCS data distribution during the experimental HS swine model. Data are presented as median (interquartile range). ns p Value = 0.06, calculated Wilcoxon rank-sum test comparing T0 and T4 evaluation times. GCS, global circumferential strain; T0, after anesthetic induction and hemodynamic stabilization; T1, 1 hour after a severe HS status was established; T2, immediately after complete blood volume replacement; T3, 1 hour after complete blood volume replacement; and T4, 2 hours after complete blood volume replacement.

At 2 hours after complete blood volume replacement, there was a statistically significant reduction in the LV GLS (−10.7% [−14.4 to −9%] vs. −8.5% [−8.6 to −5.2%], p = 0.028) (Supplemental Digital Content, Supplementary Table S4, https://links.lww.com/TA/C493, and Fig. 3).

Qualitative changes in the segmental strain curves characteristics during the implementation of the HS were observed. We found dyssynchrony of the segmental strain curves with a late systolic peak during this experimental time. Those abnormal findings tend to recover after complete blood volume replacement but could be seen at the end of the study (Fig. 5).

F5
Figure 5:
Qualitative and quantitative assessment of the LV global longitudinal (I) and circumferential (II) strain through the analyses of the segmental strain curves at the basal time (A) and the end of experiment (B).

There was a statistically significant association between the arterial oxygen content at 1 hour after a severe HS status was established (T1—evaluation time) and LV GLS 2 hours after complete blood volume replacement (T4—evaluation time) (β = 0.64 (95% confidence interval [0.10–1.17]), p = 0.029, r2 = 0.65), with lower oxygen content during severe HS associated with lower strain at the end of the procedure (Supplemental Digital Content, Supplementary Table S5, https://links.lww.com/TA/C493).

Troponin

There was a statistically significant stepwise increase in the troponin levels during the observation time of experimental controlled HS (T0, 84 [14–218] vs. T1, 553 [1,760–3,330] vs. T2, 1,760 [969–3,150] vs. T4, 3,330 [1,480–10,520], p = 0.018) (Fig. 6 and Supplemental Digital Content, Supplementary Table S2, https://links.lww.com/TA/C493).

F6
Figure 6:
Box plots (A) and diamond plots (B) show the troponin data distribution during the experimental HS swine model. Data are presented as median (interquartile range). *p Value = 0.018, calculated by Wilcoxon rank-sum test comparing T0 and T4 protocol times. T0, after anesthetic induction and hemodynamic stabilization; T1, 1 hour after a severe HS status was established; T2, immediately after complete blood volume replacement; T3, 1 hour after complete blood volume replacement; and T4, 2 hours after complete blood volume replacement.

DISCUSSION

This study demonstrated that LV GLS was a sensible, reproducible, and accurate imaging tool to detect subclinical cardiac dysfunction associated with TISCI in a controlled HS swine model. Also, in agreement with other investigators, we showed an association between LV GLS and total blood volume, with a decrease of the absolute strain values during the severe hemorrhagic state.16 Our findings emphasize the superiority of myocardial deformation over the traditional hemodynamic and echocardiographic parameters in assessing cardiac performance during and after resuscitation of HS status.

We also demonstrated a linear correlation between the severity of the decrease in arterial oxygen content during severe HS and the decrease in LV GLS 2 hours after resuscitation, suggesting that an imbalance between the oxygenation supply and demand at the myocardial level during the severe HS would lead to greater severity of TISCI. These findings agree with other papers that demonstrated the correlation between measures of oxygenation (invasive and noninvasive) and subclinical cardiac dysfunction evaluated by myocardial deformation using featuring tracking cardiac magnetic resonance.17

Moreover, this study demonstrated the efficacy of our research protocol in determining a severe HS, systemic hypoxia, ischemia, and acidosis. The experimental HS model induced a significant decrease in the end-diastolic and end-systolic volumes, cardiac index, mean arterial pressure, oxygen delivery, and bicarbonate and an increase in lactate and oxygen extraction. Our findings of a stepwise increase in the troponin level agree with several investigators' results that demonstrated an association of higher admission levels of catecholamines, brain natriuretic peptide, troponin, and heart-type fatty acid binding protein with an increase morbid and mortality, and poor prognostic.18 Also, the troponin reached extremely high values, which may indicate a severe systemic hypoxic-ischemic reperfusion injury imposed by the experimental HS model.19 Trauma-induced secondary cardiac injury is an underrecognized entity and has been shown to happen in 10% of trauma patients, and it is associated with adverse cardiac events, prolonged hospitalization, and mortality.5 Its pathophysiology is poorly understood, with an ischemia-reperfusion injury being the primary mechanism leading to mitochondrial dysfunction, reactive oxygen species generation, endothelial dysfunction, systemic inflammatory response, and myocardial death.20 Contrary to what is described in some reports, this study did not find clinical CV manifestation of TISCI, such as supraventricular arrhythmias or myocardial infarction.21 Furthermore, the LV systolic dysfunction was only identified by LV longitudinal STE analysis, with normal LVEF and hemodynamics values.

Traditionally, the LVEF has been used as a cornerstone parameter of global cardiac performance, guiding therapeutic clinical decision making and risk stratification, because of its strong prognostic value to major adverse cardiovascular events.22,23 However, the LVEF measurement has several technical limitations related to adequately identifying LV endocardial borders, foreshortening, and mathematical calculation based on geometric assumptions.24

The STE assessment is obtained by tracking speckles or digital markers during the cardiac cycle and provides detailed qualitative and quantitative information regarding global and segmental myocardial deformation in three primordial spatial directions: longitudinal, circumferential, and radial.25,26 In clinical practice and the research field, the assessment of myocardial deformation has been increasing exponentially.27 The STE has been shown to be superior to the traditional cardiac imaging methods because of its low cost, high accuracy, feasibility and reproducibility, and no radiation or contrast use.28

Multiple researchers have demonstrated the crucial role of myocardial strain evaluation for patient management during cardiotoxic cancer therapy, with the LV GLS reduction of 10% to 15% from a preview baseline value, the most powerful prognosticator of cancer therapeutic-related cardiac dysfunction.29–31 Moreover, LV strain analysis has been broadly used as the main tool for differential diagnostic of LV hypertrophy associated with systemic arterial hypertension, hypertrophic cardiomyopathy, aortic valve stenosis, cardiac amyloidosis, and Fabry disease through the analysis of the GLS value and the pattern impairment distribution across the 17 segments.32–34 Furthermore, investigators have shown the importance of the left atrium structure and function analysis by STE on the CV assessment of healthy patients with diabetes mellitus, hypertension, heart failure, and stroke.35–37

In the clinical practice, with victims of trauma who present in shock, the initial diagnostic hypothesis is attributed to loss of blood volume. Eventually, not all patients will respond satisfactorily to fluid resuscitation and hemorrhage control. From this moment on, other etiologies need to be ruled out. In this context, our study protocol aimed to evaluate TISCI as possible etiology for subclinical cardiac dysfunction using imaging, hemodynamics, and tissue oxygenation tools already validated in clinical practice.

In this study, the LV longitudinal strain was the myocardial deformation parameter capable of detecting the subclinical cardiac dysfunction associated with TISCI, which is in agreement with several studies that demonstrated the critical prognostic value of longitudinal strain in patients with septic shock38–40 and with populational studies showing longitudinal strain as a predictor of incidence of heart failure, acute myocardial infarction, and CV disease.41 This selective higher sensitivity of longitudinal strain compared with circumferential strain could be related to the longitudinal myocardial fibers being located in the endocardial region where it is more vulnerable to ischemia42 and the inherent higher reproducibility of the longitudinal strain evaluated by STE.

This study suggests the potential for routine clinical use of LV LGS assessment in patients with trauma associated with severe HS, adding an early diagnostic tool to TISCI, guiding fluid resuscitation, and providing prognostic information. However, further research should be performed in both experimental animals and in clinical settings in humans to confirm the real role of this new imaging diagnostic technique in emergency and urgency scenarios associated with trauma, shock, and sepsis.

Strengths and Limitations

The main strength of the current study was the assessment of the subclinical cardiac dysfunction using a novel 2D-STE method, which seems to be a more sensitive, reproducible, and accurate technique compared with the traditional echocardiogram and macrodynamic and microdynamic parameters. Moreover, our experiment followed rigorous and stringent protocols, making its findings reliable and with high intrinsic validity. In terms of limitations, only a small number of animals were used, which could cause our study to be more susceptible to type 1 error bias. Also, the study follow-up time after complete blood resuscitation was restricted to 2 hours, which might not be long enough to identify completely the associated ischemic-reperfusion injuries. Lastly, echocardiography analysis is highly dependent on imaging quality, which was impaired by the pig's peculiar chest wall shape (more oval with a prominent sternum bone), small intercostal spaces, and relative mesocardia with the LV apex rotated posteriorly. However, we believe that limitation was inherent in the animal research model, which is not translated into the clinical human field. Several studies demonstrated the appropriateness of transthoracic echocardiography (point of care ultrasound and focused cardiac ultrasound) in patients with shock in the emergency department, critical care, and trauma arena, with excellent feasibility and reproducibility.43,44

CONCLUSION

In this experimental swine model of controlled HS, longitudinal LV strain analysis accurately characterizes the timing and magnitude of subclinical cardiac dysfunction associated with TISCI.

AUTHORSHIP

H.D.d.V., the first author, and E.F.d.S.M., the last author, were responsible for study design, data analysis, and drafting of the manuscript. K.R.S., D.A.O., M.K.K., and A.d.C.A. contributed in the raw data analysis for the study and revised the manuscript. L.A.C. and L.L. contributed to both data collection and revised the manuscript.

ACKNOWLEDGMENTS

We thank the staff of the laboratory (LIM-08 and LIM-62) of the School of Medicine, University of São Paulo (Faculty of Medicine of the University of São Paulo, São Paulo, Brazil) for their valuable work during the experimental research studies.

DISCLOSURE

The authors declare no conflicts of interest.

The manuscript represents original work that has not been published and is not being considered for publication elsewhere in whole except as an abstract. All authors gave final approval for publication.

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Keywords:

Hemorrhagic shock; reperfusion injury; cardiac imaging techniques; ventricular dysfunction; swine

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