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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 7  |  Issue : 1  |  Page : 75-83

Evaluation of different patterns of sepsis-induced myocardial dysfunction by echocardiographic tissue Doppler imaging as early predictors of mortality


Critical Care Medicine Department, Faculty of Medicine, Alexandria University, Alexandria, Egypt

Date of Submission04-Aug-2018
Date of Acceptance09-Jun-2019
Date of Web Publication16-Apr-2020

Correspondence Address:
PhD Hany E Elsayed
Mostafa Kamel Street At Intersection With Street 313, El-Marwa Building, Smouha, Alexandria, 21431
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/roaic.roaic_65_18

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  Abstract 

Background Cardiovascular dysfunction in sepsis is associated with a significantly increased mortality rate. Tissue Doppler imaging is useful in detecting sepsis-induced myocardial dysfunction (SIMD) by quantification of systolic and diastolic functions.
Aim To evaluate the different patterns of SIMD, by pulsed-wave tissue Doppler imaging (pwTDI), as early predictors of mortality.
Settings and design A prospective observational cross-sectional study was conducted.
Patients and methods Our study included 120 patients with severe sepsis/septic shock. All patients were assessed during the first 24 h of diagnosis using transthoracic echocardiography. Tissue velocities were obtained by pwTDI, and patterns of SIMD were determined and correlated with the patients’ outcome.
Results In the systolic dysfunction group, a cutoff value for peak systolic annular velocity (S′) of more than 5.8 cm/s was associated with significant mortality, whereas in diastolic dysfunction group, a cutoff value for early diastolic transmitral flow velocity to early diastolic mitral annular tissue velocity (E/e′) of more than 12.5 was associated with significant mortality. In the combined dysfunction group, a cutoff value for S′ of less than 5.2 cm/s and a cutoff value for E/e′ of more than 12 were associated with significant mortality. Regarding the hyperkinetic group, a cutoff value for S′ of more than 11 cm/s was associated with significant mortality.
Conclusion Tissue velocities measured by pwTDI were able to predict mortality in patients with severe sepsis/septic shock, with the highest mortality in the hyperkinetic pattern, whereas left ventricular systolic dysfunction was common in survivors, with the lowest mortality rate.

Keywords: diastolic dysfunction, sepsis-induced myocardial dysfunction, septic shock, systolic dysfunction, tissue Doppler imaging


How to cite this article:
Zaytoun TM, Helmy TA, Elsayed HE, El Bourini MM. Evaluation of different patterns of sepsis-induced myocardial dysfunction by echocardiographic tissue Doppler imaging as early predictors of mortality. Res Opin Anesth Intensive Care 2020;7:75-83

How to cite this URL:
Zaytoun TM, Helmy TA, Elsayed HE, El Bourini MM. Evaluation of different patterns of sepsis-induced myocardial dysfunction by echocardiographic tissue Doppler imaging as early predictors of mortality. Res Opin Anesth Intensive Care [serial online] 2020 [cited 2020 Jun 2];7:75-83. Available from: http://www.roaic.eg.net/text.asp?2020/7/1/75/282591


  Introduction Top


Sepsis is a major public health problem, accounting for more than $20 billion (5.2%) of total hospital costs in the USA, and is a leading cause of mortality and critical illness worldwide [1],[2].

In 2016, the Third International Consensus defined sepsis as a life-threatening organ dysfunction caused by a dysregulated host response to infection. Septic shock is defined as a subset of sepsis in which underlying circulatory and cellular metabolism abnormalities are profound enough to substantially increase mortality [3].

Myocardial dysfunction in sepsis is associated with a significantly increased mortality rate of 70–90%. Defining septic myocardial dysfunction as a disorder of reduced left ventricular ejection fraction (LVEF) during sepsis is too simplistic [4],[5]. Septic cardiomyopathy has two main criteria: the first is that it is acute and reversible left ventricular (LV) systolic impairment, which allows the patient to recover [6],[7], and the second is that depressed LV systolic function is accompanied with normal or low LV filling pressure, unlike the ‘classic’ picture of cardiogenic shock [4]. The absence of elevated LV pressures can be explained by two reasons. The first one may be owing to the frequent incidence with right ventricular (RV) dysfunction in sepsis [8],[9],[10],[11], and the second reason relates to LV compliance change, which often occurs [12].

The incidence of LV systolic dysfunction depends on the timing of the evaluation. Vasoplegia and LV afterload are corrected during initial resuscitation, thus unmasking septic cardiomyopathy. Despite high LVEF (>55%), stroke volume at initial phases of sepsis is low owing to deficiency of cardiac preload secondary to the high vascular permeability and vasodilation. The compensatory tachycardia is usually not sufficient to maintain adequate cardiac output during this initial phase of sepsis, as demonstrated by the high lactate levels [13]. After fluid administration, LVEF declined markedly (<45%) in all patients during the first few days of hemodynamic support. However, LV systolic dysfunction is a common finding and potentially reversible in survivors. However, in late stages of sepsis, nonsurvivors received more fluid than survivors but had lower LV end-diastolic volume suggesting a persistent state of preload deficiency. Other studies reported more severe cardiac depression in sepsis survivors compared with nonsurvivors [6],[12]. In very severe cases of sepsis, the presence of profound myocardial dysfunction defined by a decreased LVEF may represent a sort of good adaptation and preload optimization, whereas a normal LVEF might be caused by the persistent preload deficiency and/or the sustained harmful sympathetic overstimulation [13].

There were a lot of controversies regarding troponin elevation and survival. Previous studies suggest that cardiac troponin elevation is known to predict mortality in patients with sepsis [14],[15], whereas more recent studies showed that troponin elevation was not associated with increased mortality, compared with patients with no troponin elevation [16],[17].

Tissue Doppler imaging (TDI) has improved the usefulness of echocardiography in detecting subclinical heart failure. Annular tissue velocities based on pulsed-wave tissue Doppler imaging (pwTDI) can be used to assess the LV and RV longitudinal functions, and the ratio between early mitral flow velocity (E) and early diastolic tissue velocity (e′) can be used as a surrogate of LV filling pressure [18],[19].

The relation between LV systolic impairment and survival is a very controversial issue. Contrary to common sense, a significantly impaired LV systolic function was found in survivors rather than nonsurvivors [6],[20]. However, other studies denied that systolic dysfunction was associated with survival [21]. However, previous studies using TDI showed that the increased mortality in patients with diminished peak systolic annular velocity (S′) waves may suggest that systolic impairment is, in fact, a risk factor for death, rather than a temporary compensatory mechanism of the inflammatory response [22]. The major finding that was agreed upon is that increased S′ is an independent predictor of 90-day mortality in patients with septic shock [23].

Patients with septic shock frequently have diastolic dysfunction. The incidence of diastolic dysfunction using TDI is 20–92% [24], and diastolic dysfunction is the strongest independent predictor of early mortality, even after adjusting for other independent predictors of mortality [25],[26],[27],[28].

Occurrence of RV dysfunction in septic shock could be an isolated finding or in conjunction with LV dysfunction [9]. Although most patients develop RV failure as a result of an abnormally high RV afterload, others can develop RV dysfunction as a result of myocardial depression [9].

LV systolic and diastolic dysfunction in addition to RV affection was proved to take place in isolation or in combination in patients with sepsis. So, our study aimed to evaluate the different patterns of sepsis-induced myocardial dysfunction (SIMD), by echocardiographic TDI, as early predictors of mortality.


  Patients and methods Top


Patients

This prospective observational study was conducted on 120 patients, who were admitted with or developed severe sepsis or septic shock. Approval of the Medical Ethics Committee was taken. An informed consent from patients’ next of kin was taken before enrolment to the study.

Inclusion criteria

The following were the inclusion criteria:
  1. Age more than 18 or less than 80 years.
  2. Patients with the diagnosis of severe sepsis or septic shock with operational definitions according to Surviving Sepsis Campaign 2012 [29];
    1. Severe sepsis was defined in the presence of all three of the following criteria:
      1. Evidence of infection or serious clinical suspicion for infection.
      2. At least two signs of systemic inflammatory response syndrome:
        1. Temperature more than 38.8 C° or less than 36.8 C°.
        2. Heart rate more than 90 beats/min.
        3. Respiratory rate more than 20 breaths/min or mechanical ventilation.
        4. White blood cells more than 12 000 or less than 4000 or more than 10% bands.
      3. At least one organ dysfunction.
    2. Septic shock was defined as severe sepsis plus hypotension (systolic blood pressure<90 mmHg) lasting more than 1 h, not responding to fluid therapy (increased central venous pressure to 12–15 mmHg in patients with oliguria) and requiring vasopressor therapy.


Exclusion criteria

The following were the exclusion criteria:
  1. Pregnant females.
  2. Cardiac diseases:
    1. Known heart failure by history or previous echo data.
    2. Coronary heart disease by history or patients with echocardiographic evidence of regional wall motion abnormality suggesting regional previous infarction or ischemia.
    3. More than mild mitral and/or aortic valvular disease.
    4. Arrhythmia.
    5. Known abnormality in a recent echocardiography.
  3. Patients with poor-quality echocardiographic images and measurements (e.g. obesity, post-thoracic operation, and acute respiratory distress syndrome).



  Methods Top


All patients were subjected to the following;
  1. Complete history taking.
  2. Complete physical examination including Glasgow Coma Score, vital signs, oxygen saturation, central venous pressure, and urine output.
  3. Acute Physiology And Chronic Health Evaluation II (APACHE II) [30] and Sequential Organ Failure Assessment (SOFA) [31] scores were calculated on day 1 of the diagnosis.
  4. Cardiac troponin I and creatinine kinase muscle band were obtained on day 1 of the diagnosis from all patients.
  5. Patients were treated according to the Surviving Sepsis Campaign Guidelines 2012 [29].
  6. All hemodynamic, respiratory/ventilatory, vasoactive therapies and daily fluid balance data were recorded.
  7. Echocardiographic assessment:
    1. All patients were examined during the first 24 h of diagnosis by transthoracic echocardiography using Vivid 3 machine (General Electric Healthcare, Norway, Horten, 2008) with phased array 3.5–5 MHz probe.
    2. The following parameters were measured:
      1. LV end-systolic volume, LV end-diastolic volume, and LVEF were assessed by using the modified biplane Simpson equation in the apical four-chamber and two-chamber views [32].
      2. Peak mitral inflow E and A velocity waves on pulsed-wave Doppler, E/A ratio, and E-wave deceleration time, were measured using the apical four-chamber view. The average value of measures of three consecutive beats were taken. In patients with tachycardia or long systolic time (e.g. right or left bundle branch block), the fused EA waves were considered an E wave [33].
      3. The systolic (S′), diastolic (e′), and (a′) peak annular velocities were obtained by pwTDI at both the medial and lateral mitral annulus on four-chamber apical view, and LV filling index E/e′ ratio was calculated [19],[34].
      4. From the apical four-chamber 2D-view, the RV size was calculated. Tricuspid Annular Plane Systolic Excursion measured by M-mode and tricuspid annular systolic motion (RV S′) by pwTDI at the tricuspid level of the RV free wall were used to assess RV function [35].
    3. Although the echocardiography findings were not hidden from the treating physicians, patient therapy was not titrated to reach a specific echocardiographic target.
  8. According to TDI findings, myocardial dysfunction was categorized into the following:
    1. Systolic LV dysfunction.
    2. Diastolic LV dysfunction.
    3. Combined dysfunction (systolic and diastolic) pattern.
    4. Supernormal (hyperkinetic/vasoplegic) pattern.
    5. RV dysfunction associated with any of the previous patterns.
  9. The normal reference limits and cutoff values for the diagnosis of the previously mentioned patterns were according to the American Society and the European Association of Echocardiography [19],[23],[32],[33],[34],[35].
  10. Outcome measures:
    1. Primary outcome was ICU mortality rates.
    2. Secondary outcome was ICU length of stay (LOS).



  Results Top


The baseline characteristics of the study population are presented in [Table 1]. The different sources of infection causing severe sepsis/septic shock among our patients poulation are presented in [Figure 1].
Table 1 Patients’ baseline characteristics

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Figure 1 Distribution of different sources of sepsis.

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The LV systolic velocity (S′) measured by pwTDI ranged from 4.5 to 13 cm/s. The hyperkinetic group had the greatest velocity with a mean of 11.49±1.08 cm/s, whereas the systolic dysfunction group had the smallest velocity with a mean of 5.49±0.64 cm/s. The diastolic dysfunction group is the only group with normal S′ velocity with a mean of 8.33±0.72 cm/s. There was a statistically significant difference between all groups regarding S′. Regarding the systolic dysfunction group, the receiver operator curve (ROC) showed that a cutoff for S′ of more than 5.8 cm/s was associated with significant mortality with area under the curve (AUC), senstivity, specificity, postive predictive valve (PPV), and negative predictive valve (NPV) of 0.91, 80, 90, 66.7, and 94.7%, respectively, which was statistically significant. An APACHE II score of more than 25 and intial SOFA score more than 9 had a comparable results with S′, as shown in [Figure 2]a.
Figure 2 Receiver operator curves of different patients groups S′: peak systolic mitral annular velocity measured by pulsed wave tissue doppler imaging - SOFA: sequential organ failure assessment - APACHE II: acute physiology and chronic health evaluation II - E/e′: ratio between peak velocity of early diastolic mitral inflow (measured by pulsed wave doppler) and peak mitral annular velocity of early diastolic wave(measured by pulsed wave tissue doppler imaging).

Click here to view


Regarding the diastolic dysfunction group, the ROC showed that a cutoff for early diastolic transmitral flow velocity to early diastolic mitral annular tissue velocity (E/e′) of more than 12.5 was associated with significant mortality with AUC, senstivity, specificity, PPV, and NPV of 0.98, 80, 90, 80, and 90%, respectively, which was statistically significant. An APACHE II score of more than 15 and intial SOFA score more than 7 had comparable results with E/e′, as shown in [Figure 2]b.

Regarding the combined dysfunction group, the ROC showed that a cutoff for S′ of less than 5.2 cm/s was associated with significant mortality with AUC, senstivity, specificity, PPV, and NPV of 0.85, 100, 80, 66.7, and 100%, respectively, which was statistically significant. The ROC showed that a cutoff for E/e′ of more than 12 was associated with mortality with AUC, senstivity, specificity, PPV, and NPV of 0.99, 90, 96, 90, and 96%, respectively, which was statistically significant. An APACHE II score of more than 21 and intial SOFA score more than 9 had a comparable results with both S′ and E/e′, as shown in [Figure 2]c.

Regarding the hyperkinetic group, the ROC showed that a cutoff for S′ of more than 11 cm/s was associated with significant mortality with AUC, senstivity, specificity, PPV, and NPV of 0.93, 90, 93.3, 96.4, and 82.4%, respectively, which was statistically significant. An APACHE II score of more than 19 and intial SOFA score more than 9 had comparable results with S′, as shown in [Figure 2]d.

Ten patients of the study population had RV systolic dysfunction. The hyperkinetic group was not associated in any case with RV systolic dysfunction with statistically significant difference in relation to the systolic dysfunction and combined dysfunction groups. Mortality was 100% for the 10 patients who had RV systolic dysfunction.

Regarding outcome measures, the ICU LOS ranged from 3 to 16 days. The hyperkinetic group had the least ICU LOS with a mean of 5.16±1.97 days, whereas the systolic dysfunction group had the greatest ICU LOS with a mean of 10.88±2.01 days. There was a statistically significant difference between all groups (P<0.001; [Table 2]).
Table 2 Outcome measures

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Regarding ICU mortality, 50 (41.7%) patients died during the study. The highest mortality was in the hyperkinetic group, in which 30 (66.7%) patients died, which was statistically significant (P<0.001). On the contrary, the systolic dysfunction group had the least mortality, in which only five (20%) patients died, which was again statistically significant (P<0.001). There were five (33.3%) and 10 (28.6%) patients who died in the diastolic dysfunction and combined dysfunction groups, respectively ([Table 2]).


  Discussion Top


Assessment of SIMD is challenging. Most of the conventional echocardiographic parameters are affected by the cardiac loading conditions that are changing constantly in critically ill patients.

In this study, there were common statistically significant independent risk factors of mortality in SIMD. They included APACHE II score, SOFA score, age, positive cumulative balance, vasoactive agents, as well as pwTDI parameters, S′ and E/e′.

In agreement, several studies [16],[21],[23],[25],[36],[37] concluded that age, APACHE II score, SOFA score, and noradrenaline dose were considered independent risk factors of mortality in SIMD, whereas others included low urine output [27] and low PaO2/FiO2 [23],[25].

The cornerstone finding in this study was that the hyperkinetic pattern had significantly higher mortality rate (66.7%) and that LV systolic dysfunction was common in survivors with the lowest mortality rate (20%) among all patterns of myocardial dysfunction.

In concordance with our study, Parker et al. [12] concluded that survivors had reduced ejection fractions and significantly higher (LV) end-diastolic volumes, whereas nonsurvivors had normal ventricular volumes and significantly higher ejection fractions.

Furian et al. [38] found that LV function, as assessed by S′, was similar between survivors and nonsurvivors. However, survivors had higher LV end-diastolic diameter. Santos et al. [39] found that univariate analysis showed that reduced S′ waves had a protective effect on the risk of death (OR 0.517, P=0.0014).

In this study, the hyperkinetic pattern had the highest (66.7%) mortality rate, and ROC analysis for in-hospital mortality showed that a cutoff value of S′ more than 11 cm/s had AUC of 0.93, with P<0.001.

In agreement with our study, Weng et al. [23] concluded that compared with survivors, nonsurvivors exhibited significantly higher S′ (11.0 vs. 7.8 cm/s; P<0.0001). With a cutoff value of 9 cm/s for S′, the AUC was 0.83, and the sensitivity and specificity were 75 and 86%, respectively. Patients with a higher S′ value (>9 cm/s) showed a significantly higher mortality (75 vs. 17%, P<0.0001).

In addition, Weng et al. [23] concluded that survivors with septic shock exhibited significantly decreased S′. Concordantly, in our study, survivors had lower S′ than nonsurvivors (5.29±0.48 vs. 6.30±0.59 cm/s, P<0.001).

On the contrary, a meta-analysis by Huang et al. [36] failed to prove that the survivors from septic shock had lower ejection fractions. Meanwhile, the nonindexed dimensions were mildly but significantly increased in survivors indicating that survivors had larger LV dimensions.

Regarding the best parameters to assess diastolic dysfunction and its relation to mortality, both e′ and E/e′ best correlated with diastolic dysfunction-related mortality in septic shock. Garry et al. [24] showed that many studies proved that diastolic dysfunction was an independent predictor of mortality [21],[25],[26],[27]. Mortality related to diastolic dysfunction was 30%. Landesberg et al. [25] reported 36% mortality related to diastolic dysfunction.

In agreement with our work, Landesberg et al. [25] found that E/e′ more than 15 was the strongest predictor of mortality, even after adjusting for the other independent predictors of mortality. By using ROC curve analysis, E/e′ cutoff value of more than 11 (ρ=0.003) in the isolated diastolic dysfunction group in predicting mortality in septic shock had AUC, sensitivity, specificity, PPV, and NPV of 0.98, 100, 90.9, 83.3, and 100, respectively. In agreement with this study, Khalaf et al. [37] concluded that E/e′ ratio is a good tool for prediction the mortality at cutoff point of 10.02, with AUC of 0.884, a significant P value of 0.002, sensitivity of 85%, specificity of 75%, PPV of 89.5%, and NPP of 66.7%.

Regarding RV involvement in septic shock, all patients with RV dysfunction died in this study [10 (8.33%) patients]. Thomas et al. [40] found that RV dysfunction conferred a significant increased mortality rate (66%) and may aid in prognostication. In concordance with this, Umashankar et al. [41] concluded that persistent RV dysfunction in sepsis has been associated with increased mortality.

On the contrary, a meta-analysis by Huang et al. [36] found that there were no significant differences in RV ejection fractions and RV dimensions between the survivor and nonsurvivor groups. In agreement with these findings, Vallabhajosyula et al. [42] conducted a retrospective study and concluded that sepsis-induced acute RV dysfunction did not affect hospital outcomes including both LOS and mortality.

Kimchi et al. [9] concluded that not all cases of RV dysfunction should be related to sepsis as some may have an abnormally high RV afterload from high pulmonary vascular resistance which is common in septic shock. In agreement with this study, all patients with RV dysfunction were mechanically ventilated and four of the ten patients had pneumonia as a cause of septic shock and were hypoxic.

It is not clear whether the elevated troponin is of prognostic value in septic shock or whether patient heterogeneity or differences in timing and frequency of troponin measurement in the various studies accounts for these conflicting results.

Many studies showed that elevated cardiac troponin I was an independent prognostic indicator of mortality after adjusting for the other significant variables [17],[25],[43]. Others concluded that cardiac troponins could not be used as a tool for predicting mortality in patients with septic shock [16],[37],[44],[45].

Regarding the association between troponin level and patterns of SIMD, this study concluded that the highest troponin elevation was in the hyperkinetic group (1.29±0.8 ng/dl), and lowest in the isolated diastolic dysfunction group (0.17±0.14 ng/dl).

In concordance with this study, Landesberg et al. [25] concluded that a combined pattern of reduced LVEF and e′-wave showed significantly higher serum levels of high sensitivity troponin T (hs TnT) compared with patients having isolated patterns.

In 2014, Landesberg et al. [46] concluded that LV diastolic dysfunction and RV dilatation are the echocardiographic features that best correlate with concurrent hs TnT concentrations and mortality in patients with septic shock, independent of APACHE II score and estimated glomerular filtration rate, the strongest clinical variables correlating with hs TnT.


  Conclusion Top


Assessment of SIMD in critically ill patients is challenging. Annular tissue velocities (S′ and E/e′) measured by pwTDI were able to predict mortality in patients with septic shock. The cornerstone finding in this study was that the hyperkinetic pattern had significantly higher mortality rate and that LV systolic dysfunction was common in survivors with the lowest mortality rate among all patterns of myocardial dysfunction.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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