Safety and Efficacy of Lung Recruitment Maneuvers in Pediatric Post-Operative Cardiac Patients

Renee L. Devor MD^1,2

Harjot K. Bassi MD³

Paul Kang MPH⁴

Tiffany Morandi MD²

Kristi Richardson RT⁵

John J. Nigro MD^2,6

Christine Tenaglia RT⁵

Chasity Wellnitz RN, BSN, MPH⁶

Brigham C. Willis MD^1,2,7

¹Division of Cardiac Critical Care, Phoenix Children’s Hospital, Phoenix, Arizona

²Department of Child Health, University of Arizona College of Medicine, Phoenix, Arizona

³Division of Critical Care, Phoenix Children’s Hospital, Phoenix, Arizona

⁴Department of Epidemiology and Biostatistics, University of Arizona College of Medicine, Phoenix, Arizona

⁵Department of Respiratory Therapy, Phoenix Children’s Hospital, Phoenix, Arizona

⁶Division of Cardiology, Phoenix Children’s Hospital, Phoenix, Arizona

⁷Department of Pediatrics, Creighton University School of Medicine, Phoenix, Arizona

Abstract

Background: Recruitment maneuvers are a dynamic process of transient increases in transpulmonary pressure intended to open unstable airless alveoli. Due to concerns regarding the hemodynamic consequences of recruitment maneuvers in children with heart disease, these maneuvers have not been widely utilized in this population. The objective of this study was to demonstrate the safety and efficacy of lung recruitment maneuvers in post-operative pediatric cardiac patients. We hypothesized that multiple recruitment maneuvers are physiologically beneficial and hemodynamically tolerated in children with congenital cardiac disease. 

Methods: Retrospective chart review was conducted of post-operative cardiac surgical subjects who received recruitment maneuvers, as well as a matched control group who did not, at a Cardiac ICU in a quaternary care free-standing children’s hospital. Repetitive lung recruitment maneuvers using incremental positive end-expiratory pressure were performed. Hemodynamic and respiratory physiologic variables were recorded.

Results: Sixty-one post-operative cardiac subjects had a total of 435 lung recruitment maneuvers. Assessment of hemodynamic tolerability demonstrated no change in MAP, HR, or CVP during or after the maneuvers. There was a 28% increase in dynamic compliance following recruitment maneuvers (p <0.01, 95% CI). Specific outcomes in the 59 matched control subjects demonstrated no significant difference in length of mechanical ventilation (p = 0.26), length of hospital stay (p = 0.28), mortality (p = 0.58) or difference in occurrence of pneumothorax (p = 0.26). 

Conclusions: Post-operative pediatric cardiac surgical subjects tolerated repeated lung recruitment maneuvers without significant hemodynamic changes. The maneuvers successfully improved dynamic compliance without any adverse effects.

Introduction

Mechanical ventilation is a common therapy used for pediatric patients in the intensive care unit and is frequently used for children with congenital cardiac disease following surgical repair. However, it is well known that mechanical ventilation can induce lung injury or worsen preexisting lung disease (1-3). In patients with congenital cardiac disease, it is crucial to protect the lung from injury and optimize ventilation and oxygenation due to their underlying hemodynamic and physiologic fragility (4, 5). Post-operatively, several factors including general anesthesia, cardiopulmonary bypass, atelectasis, and hypoxemia can contribute to lung dysfunction, which may lead to prolonged mechanical ventilation (6). Children with such prolonged ventilation are at a higher risk for poor overall outcome due to a variety of ventilator-associated morbidities (7, 8). Therefore, it is of practical value to protect the lungs and reduce the length of time mechanical ventilation is required.

Alveolar injury can be caused by the repetitive opening and closing of alveoli when inadequate positive end-expiratory pressure (PEEP) is provided and this can generate shear stress within the alveoli and promote injury (9-10). Lung recruitment maneuvers have been defined as transient increases in the transpulmonary pressure used to open recruitable collapsed alveoli and increase end expiratory lung volume (11-13). Recruitment maneuvers are often considered useful in patients, especially those with acute respiratory distress syndrome (ARDS), to potentially decrease ventilator-induced lung injury by improving oxygenation and lung compliance while reducing the risk of atelectrauma by re-opening and stabilizing collapsed alveoli (11,13-18).

Increased intrathoracic pressure can affect right and left ventricular preload due to decreased venous return, changed right ventricular afterload, and altered biventricular compliance (4,10,14,19-21). This may lead to decreased stroke volume leading to short periods of hypotension, bradycardia, and impaired cardiac output, which is of significant concern in patients with congenital cardiac disease (14). Many patients with congenital cardiac disease must undergo surgical procedures which lead to lung collapse after induction of general anesthesia and during mechanical ventilation (15,22). In those patients undergoing cardiac surgery with cardiopulmonary bypass, significant atelectasis occurs which impairs right ventricular (RV) function. However, lung recruitments using positive pressure have been shown to re-expand collapsed alveoli and improve RV function (23-26). There is a theoretical risk of developing barotrauma leading to pneumomediastinum or pneumothorax during a recruitment; however this is likely less a risk in cardiac surgical patients with relatively healthy lungs (10,27,28).

These cardiopulmonary interactions and hemodynamic concerns limit the willingness of many clinicians to perform positive-pressure recruitment maneuvers in patients with underlying cardiac pathology, making studies involving this population uncommon. One study (29) evaluated the use of a recruitment maneuver performed in twenty pediatric patients with congenital cardiac disease who underwent surgical repair. A single recruitment maneuver was performed shortly after coming off of cardiopulmonary bypass and repeated once in the intensive care unit. Although this study was able to demonstrate an improvement in oxygenation, dynamic lung compliance, arterial to end-tidal CO₂ gradient, and end expiratory lung volume, it excluded patients with residual intracardiac lesions following surgery, patients with valvular regurgitation, or respiratory failure defined as FiO2 >0.8. Due to the relatively small number of patients included in this study, as well as their protocol prescribing only two recruitment maneuvers performed per patient, it is difficult to ascertain the overall long-term safety and potential benefits that repeated lung recruitments may provide.

In this study, we aimed to investigate the safety and efficacy of increment-decrement recruitment maneuvers in a larger pediatric patient population following surgery for congenital cardiac disease, hypothesizing that multiple recruitment maneuvers are physiologically beneficial and hemodynamically tolerated in these patients. The safety of these maneuvers was evaluated by examining changes in mean arterial pressure (MAP), heart rate (HR), and central venous pressure (CVP) before, during, and after the recruitment maneuvers. The efficacy of the recruitment maneuvers was determined by changes in oxygenation index (OI) and dynamic lung compliance (Cdyn) following recruitment. To further evaluate the safety of repetitive recruitment we reviewed specific clinical outcomes that included length of mechanical ventilation, length of hospital stay (LOS), mortality and occurrence of pneumothorax and compared to a control group.

Materials and Methods

This study was reviewed and approved by the Institutional Review Board at Phoenix Children’s Hospital. Subjects who received lung recruitment maneuvers post-operatively, as identified in the electronic medical record, in the Phoenix Children’s Hospital cardiac intensive care unit, a quaternary referral center, from July 2011 through June 2012 following implementation of a lung recruitment protocol, were included in the study. Further inclusion criteria included subjects from 0-18 years of age who were admitted immediately after having open heart surgery with both single- and two-ventricle physiology and who remained on invasive mechanical ventilation. All subjects were mechanically ventilated with Servo-I ventilators (Maquet Critical Care, Solna, Sweden). Subjects with a tracheostomy or who were receiving extracorporeal membrane oxygenation (ECMO) support were excluded from the analysis. A comparison group of consecutive control subjects who did not receive recruitment maneuvers was selected in the following year from July 2012 to June 2013 following an institutional hiatus of the maneuvers during which time quality data was reviewed and the safety of the protocol was assessed. Recruitment maneuvers have subsequently been reinstated and are now standard care in our post-operative cardiac patients on invasive mechanical ventilation.

During the study period, lung recruitment maneuvers were a new standard of care implemented at our institution in the cardiac intensive care unit. They were performed by either the respiratory therapist or attending physician. Most patients had twice daily recruitment maneuvers unless more were clinically indicated based on chest x-ray findings or lung mechanics. The patients may also have fewer recruitment maneuvers if they were hemodynamically unstable, having other procedures, if there was ongoing resuscitation or at the discretion of the attending physician.

The recruitment maneuver was performed in pressure control mode regardless of the subject’s baseline mode of ventilation. Initial settings were adjusted to achieve a tidal volume of 6mL/kg. PEEP was increased from baseline by 1-2 cmH₂O increments while maintaining a fixed inspiratory driving pressure (PIP-PEEP) with each increase sustained for one-minute intervals until either the tidal volume (V_T) or dynamic compliance (Cdyn) declined (Figure 1).

Figure 1. Lung recruitment maneuver: recruitment maneuver protocol courtesy of Boriosi et al. (11). Each horizontal bar represents an incremental increase of PEEP by 2 cm H₂O in one-minute increments from baseline PEEP.

The recruitment maneuver was terminated if the mean airway pressure surpassed 28 cm H₂O. V_T and Cdyn were documented with each increase in PEEP. Once the critical opening pressure was identified, PEEP was decreased in a step-wise manner in one-minute 1-2 cmH₂O decrements to the critical closing pressure identified by a decrease in V_T or Cdyn. Following this point, the PEEP was again increased to the identified critical opening pressure for one minute. It was then brought back down to 2 cmH₂O above the critical closing pressure (i.e. “optimal PEEP” level demonstrated by improved compliance and increased tidal volume with less ventilating pressure). The subject was then placed back on their original mode of ventilatory support with the PEEP adjusted to the optimal level, as determined during the recruitment maneuver in order to maintain the newly recruited areas of the lungs open.

Data Collected: A database was generated with 61 subjects who had lung recruitment maneuvers, and a convenience sample of 59 matched control subjects were selected from our Society for Thoracic Surgeons (STS) database. Demographic data was collected including age, body surface area, associated anomalies or chromosomal abnormalities, cardiac diagnosis, and type of surgical procedure. Clinical outcomes data collected included length of mechanical ventilation, length of hospital stay, mortality, and occurrence of pneumothorax.

Hemodynamic variables including MAP, HR, and CVP were monitored and recorded by the bedside nurse and/or respiratory therapist. For each variable, the two hourly vital sign measurements prior to the start of the maneuver, two measurements during, and the first two hourly measurements following the maneuver were included for analysis. In an attempt to minimize error and to provide a more accurate representation of the subject’s status at the time of interest, the two vital sign measurements in each category were averaged as physiologic variables are dynamic. The respiratory physiologic variables monitored were dynamic compliance and oxygenation index. In order to further investigate the clinical effects of potentially decreased cardiac output, we reviewed the changes in inotropic and vasopressor support before, during, and after the performance of each recruitment maneuver.

Statistical Analysis: Subject demographic and clinical characteristics between the control and recruitment maneuver groups were reported as medians, interquartile ranges (IQR) for continuous variables and frequencies, percentages for categorical variables. The Wilcoxon Rank Sum was used to compare the continuous variables; while Chi-squared/Fisher’s Exact Tests were used to compare the categorical variables.  The Linear Mixed Model was used to ascertain trends in hemodynamic outcomes (mean arterial pressure, heart rate, and central venous pressure) across three timepoints (before, during and after the recruitment maneuver).  If the overall trend showed statistical significance, the Wilcoxon Signed Rank Test was used to ascertain differences via multiple comparisons followed by the Bonferroni adjustment for multiple comparisons.  Before and after differences in physiological outcomes (oxygenation index and dynamic compliance) were assessed using the Wilcoxon Signed Rank.  All p-values were 2-sided and p<0.05 was considered statistically significant. All data analyses were conducted using STATA version 14 (STATACorp; College Station, TX).  

Results

A total of 61 subjects underwent lung recruitment from June 2011 to June 2012 (Table 1) accounting for a total of 439 recruitment maneuvers during this time.

Table 1. Comparison of subjects receiving recruitment maneuvers versus controls.

Recruitment was initiated in the post-operative period once deemed safe by the primary intensivist. The maneuvers were performed as frequently as every two hours but, on average, subjects in the cohort received 2 recruitment maneuvers per ventilator day. Both groups had similar congenital heart disease diagnoses with an average Society of Thoracic Surgeons-European Association for Cardiothoracic Surgery Congenital Heart Surgery Mortality Score of 3 in each group covering a variety of anatomical defects and surgical procedures performed. Subjects with residual intracardiac lesions on intraoperative transesophageal echocardiogram were included in the study.

Hemodynamics: All 61 subjects tolerated the maneuvers with no hemodynamic instability defined as hypotension, need for fluid bolus during the recruitment, bradycardia, or dysrhythmias. No subject had any of the maneuvers discontinued prematurely. We found no significant difference in the MAP (p = 0.13, 95% CI) (Figure 2a) or HR (p = 0.74, 95% CI) (Figure 2b) during the time intervals measured.

Figure 2. Hemodynamics: comparison of hemodynamic measurements before, during, and after the recruitment maneuvers. There was no significant change in MAP (Fig 2a), HR (2b), or CVP (2c) during or after the maneuvers. Boxplot with whiskers with minimum/maximum 1.5 IQR.

Due to the transient increase in intrathoracic pressure that theoretically results in a decrease in venous return and therefore cardiac output, CVP was monitored throughout the recruitments. The CVP measurement did not show a significant change with the recruitment maneuver (p = 0.79, 95% CI) (Figure 2c).

In order to further investigate the clinical effects of potentially decreased cardiac output, we reviewed the changes in inotropic and vasopressor support surrounding the performance of the recruitment maneuvers. All infusion rates of epinephrine, norepinephrine, vasopressin, dopamine, milrinone, and calcium were documented prior to, during, and after lung recruitments. Of the 439 recruitment maneuvers performed, 84% were performed without any change in inotropic support during or within 1 hour after completion of the maneuver. Inotropic support was decreased after the recruitment in 12% of maneuvers. Only 3% of maneuvers required an increase in support. No subjects had any significant hypotension requiring fluid bolus administration during or immediately after the maneuvers.

Efficacy: The efficacy of recruitment maneuvers on lung function was determined by measuring changes in the OI and Cdyn before and after recruitment. There was no statistically or clinically significant change in the OI with a median OI before recruitment of 7.3 (IQR 4.1-12.6) and after 7.7 (IQR 4.6-12.6) (p = 0.96, 95% CI) (Figure 3a).

Figure 3. Efficacy: comparison of physiologic measures used to assess efficacy of the recruitment maneuvers. No significant change was demonstrated in the OI before and after recruitment (3a). There was a significant increase in Cdyn by an average of 28% immediately after the maneuvers (3b). Boxplot with whiskers with minimum/maximum 1.5 IQR.

Of the 439 maneuvers, 83% resulted in a measurable improvement of the Cdyn with all 61 of the subjects demonstrating an increase at least once over the course of the interventions. The Cdyn increased from 0.45 ml/cmH₂O/kg (IQR 0.37-0.57) to 0.58 ml/cmH₂O/kg (IQR 0.47-0.75) afterwards (p < 0.001, 95% CI). (Figure 3b). The duration of improved Cdyn was an average of 8 hours +/- 11.4 hours. Subjects continued to show improvement with repeated efforts.

Clinical Outcomes. All subjects included in this study were on invasive mechanical ventilation support on return from cardiac surgery for a minimum of 24 hours. As shown in Table 2, there was no significant difference in the number of ventilator days between the recruitment maneuver and control groups (p = 0.26, 95% CI).

Table 2. Clinical outcomes.

There was also no difference in the occurrence of extubation failure requiring reintubation between both groups (p = 0.52). There was no difference in hospital LOS with the RM group staying 17.5 days (10.5 – 27) and control group 15 days (9.5 – 23) (p = 0.28, 95% CI) or in the rate of in-hospital mortality (p = 0.58, 95% CI). Despite the theoretical concern for development of pneumothorax with recruitment maneuvers, there was no significant difference in the occurrence between the two groups (p = 0.26, 95% CI).

Discussion

Our results suggest that lung recruitment maneuvers are well tolerated in the pediatric post-operative cardiac patient population both with and without residual intracardiac shunts, and may be repeated for the duration of their time requiring invasive mechanical ventilation. Despite being at high risk of hemodynamic instability shortly after surgery, especially following complex repair and prolonged cardiopulmonary bypass time, our subjects did not require significant preload optimization or escalation of inotropic support during the maneuvers. We were also able to demonstrate that there was an improvement in dynamic lung compliance following the maneuver. Not only were these maneuvers tolerated from a hemodynamic standpoint, but there were no adverse outcomes when compared to control subjects with no difference in the length of mechanical ventilation, LOS, mortality, or the occurrence of pneumothorax.

Advocacy for the optimization of oxygenation and ventilation through the use of an “open lung” strategy, especially in the treatment of ARDS, has been present in the critical care literature for decades. Multiple reports have described the importance of lung recruitment with high inspiratory pressures in addition to the appropriate PEEP above closing pressures to maintain optimal gas exchange and minimize hypercapnia (30). Recruitment maneuvers are recommended in the protective ventilation strategy in adult post-operative patients who have undergone cardiac surgery with significant benefits as compared to traditional ventilation (31,32). To our knowledge, there is very limited data on the use of lung recruitment maneuvers in the pediatric cardiac patient population with the majority of the pediatric literature focusing on the use of these maneuvers in patients with ARDS. Scohy et al. (29) previously evaluated the use of recruitment maneuvers in subjects undergoing surgery for congenital cardiac disease but excluded several key subgroups of these subjects and did not evaluate the continued use of recruitment maneuvers over the entire course of mechanical ventilation. Amorim et al. (6) assessed the tolerance of recruitment maneuvers in a small population of infants who were prone to pulmonary arterial hypertension and excessive pulmonary circulation just after skin closure for open heart surgery. In general, data on the safety of these maneuvers in pediatric patients is very limited.

The efficacy of lung recruitment maneuvers in patients with ARDS remains controversial with some studies suggesting an improvement in oxygenation and dynamic or static compliance (1,11,20,21,33-35), some demonstrating brief or no improvement (36,37), and others that show improvement but suggest that the deleterious hemodynamic effects may outweigh the benefits (14). In children with ARDS, a staircase recruitment strategy has been described to improve oxygenation with increasing PaO_2. In order to sustain improved oxygenation, the PEEP must be set above the critical closing pressure of the lung following recruitment (11,21,38,39). Boriosi et al. (11) further described that a “re-recruitment” maneuver that was performed at critical opening pressures for a short period of time improved the PaO₂/FiO₂ ratio for up to 12 hours and OI for up to four hours following the recruitment maneuver. In our study, we were not able to demonstrate an improvement in the OI. However, we did demonstrate a significant improvement in Cdyn of 29% following completion of each recruitment which was sustained for eight hours. The lack of improvement in oxygenation may be secondary to less primary lung injury in our patient population, or due to the common presence of residual intracardiac shunts. The increase in Cdyn may be a clinically significant change for some patients and could help reduce the time on invasive mechanical ventilation.

The overall goal of recruitment maneuvers is to open atelectatic alveoli, increase end expiratory lung volume, and improve gas exchange. However, as discussed, generation of high intrathoracic pressures during the maneuvers can theoretically result in hemodynamic instability (4,10,14,20,21). Currently, there is no specific non-invasive monitoring that is the best indicator for hemodynamic assessment during recruitment maneuvers, with vital sign changes serving as a surrogate marker for the safety of the recruitment maneuver (40). In our study, there was no change in MAP, HR, or CVP from baseline, during, or after the maneuvers indicating that they were well tolerated from a hemodynamic standpoint with 97% of the recruitment maneuvers using the same or less inotropic support and no subject required fluid bolus administration for hypotension during any of the maneuvers.

The occurrence of barotrauma, including pneumomediastinum and pneumothorax, has been reported with the intermittent increase in peak airway inspiratory pressures (10,27,28). In our study, there was no significant difference in the occurrence of pneumothorax between the two groups. With the preponderance of studies on recruitment maneuvers being performed in the adult ARDS patient population, there is limited data on pediatric outcomes in mortality and duration of mechanical ventilation. A Cochrane review performed by Hodgson et al. (41) demonstrated no reduction in mortality or length of mechanical ventilation following recruitment maneuvers in adult ARDS patients. In our study, we demonstrated similar findings in that there was no difference in mortality, length of mechanical ventilation, or LOS in pediatric post-operative congenital cardiac patients with or without the maneuvers.

There were several limitations to our study. This was a single-center, retrospective study that involved a small pediatric cardiac population. Our assessment of cardiac output was dependent on measurements of MAP and CVP. We also did not investigate the occurrence of hypercapnia during the recruitment maneuvers. Overdistension of open alveoli can occur resulting in an increase in pulmonary vascular resistance and a decrease in blood flow to the alveoli, thereby increasing dead space ventilation (21). There are a number of studies demonstrating that throughout recruitment maneuvers there is an increase in PaCO₂, with a potential need to titrate the respiratory rate on the ventilator in order to maintain constant minute ventilation throughout the maneuver, as this development of hypercapnia during the maneuvers may result in adverse effects (11,34,36,41). A multifaceted approach to monitoring the effectiveness as well as any negative consequences of these maneuvers including end-expiratory lung volumes, dead space ventilation, pulmonary compliance, volumetric capnography as well as bedside ultrasound would be beneficial (40). This study was conducted prior to our institution utilizing volumetric CO₂ analysis to monitor physiologic gas exchange as well as dead-space ventilation during mechanical ventilation.

Conclusion

Overall, our study demonstrated that pediatric post-operative cardiac subjects, having a wide variety of cardiopulmonary physiology, tolerated repeated recruitment maneuvers without significant hemodynamic changes or adverse outcomes. As has been the case in many previous studies, we did not find any significant improvement in oxygenation, length of mechanical ventilation, or length of stay. However, as recruitment maneuvers have been shown to be an integral part of lung protection strategies and to benefit adults following open heart surgery, it is possible that our pediatric post-operative cardiac patients could benefit from the integration of recruitment maneuvers into ventilator management strategies while on invasive mechanical ventilation. Future prospective studies need to be conducted to further evaluate the potential benefit and utility of lung recruitment maneuvers in pediatric patients without significant lung disease.

Acknowledgements

We would like to thank the staff of the Pediatric Cardiovascular Intensive Care Unit at Phoenix Children’s Hospital for their assistance and support in this study. We would also like to acknowledge the work of Juan P Boriosi, MD and his colleagues for use of their recruitment protocol and RM diagram (Figure 1) in our study.

Contributions: Renee L. Devor MD^1,4,5,6, Harjot K. Bassi, MD^1-6, Paul Kang MPH⁴, Tiffany Morandi MD^1-3, Kristi Richardson RT^2,3, John J. Nigro MD², Christine Tenaglia RT^2,3, Chasity Wellnitz RN, BSN, MPH^2,4, and Brigham C. Willis MD^3,6

¹Literature search, ²Data collection, ³Study Design, ⁴Analysis of data, ⁵Manuscript preparation, ⁶Review of manuscript

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Cite as: Devor RL, Bassi HK, Kang P, Morandi T, Richardson K, Nigro JJ, Tenaglia C, Wellnitz C, Willis BC. Safety and efficacy of lung recruitment maneuvers in pediatric post-operative cardiac patients. Southwest J Pulm Crit Care. 2020;20(1):16-28. doi: https://doi.org/10.13175/swjpcc068-19 PDF 

Resuscitative EChocardiography for the Evaluation and management of Shock: The RECES protocol

Jarrod M. Mosier^1,2

Lori Stolz^1,

John Bloom²

Josh Malo²

Linda Snyder²

Albert Fiorello¹

Srikar Adhikari¹

¹ Department of Emergency Medicine, University of Arizona, Tucson, AZ

²Department of Medicine, Section of Pulmonary, Critical Care, Allergy and Sleep, University of Arizona, Tucson, AZ

Abstract  

Purpose: Ultrasound use by emergency medicine and critical care physicians in the evaluation of the critically ill patient has increased in recent years. Several protocols exist to aid in diagnosing the etiology of shock and identifying rapidly reversible conditions in the undifferentiated hypotension patient. Currently, no protocol provides hemodynamic data or is designed to guide ongoing resuscitation of the critically ill patient with hypotension.

Methods: An evidence-based protocol was developed based on the components of echocardiography that have been supported in the literature for bedside evaluation of the critically ill patient.

Results: The RECES protocol provides diagnostic and hemodynamic information regarding volume responsiveness , presence of pericardial effusion with tamponade physiology (right ventricular diastolic collapse), systolic failure (poor contractility, decreased stroke volume and cardiac output), diastolic dysfunction (mitral valve inflow velocities and tissue Doppler), Right ventricular systolic failure, acute valvular rupture, obvious wall motion abnormalities, and signs of pressure or volume overload (septal flattening on parasternal short axis).

Conclusion: The RECES protocol is a proposed instrument for rapidly and repeatedly assessing the etiology and initial hemodynamic parameters of the patient in shock. Additionally, repeated exams will allow monitoring interventions and guide ongoing resuscitation.

Introduction  

Ultrasound has become indispensible for emergency medicine physicians and intensivists in the evaluation and management of patients in shock. Bedside ultrasound is no longer used solely for central line placement and the diagnosis of intra-abdominal free fluid. The emergency bedside applications being used with frequency span nearly every body system. The body of literature substantiating the ability of clinicians to accurately perform and interpret point-of-care ultrasound studies is robust and growing.

For patients in shock, several goal-directed ultrasound protocols have been described in the literature. Each of these is aimed at finding rapidly reversible etiologies of shock in the undifferentiated hypotensive patient (i.e. tamponade, pneumothorax, intra-abdominal hemorrhage) (1-6). Though similar in their aim, they each differ in respect to the pathology sought, views obtained and the scope of the exam. Of these protocols, systematic study has been undertaken in only two. Jones et al. (2) have demonstrated that goal-directed ultrasound early in the presentation of patients with shock can improve the accuracy of the treating physician’s diagnosis within 15 minutes of patient arrival from 50% accuracy at baseline to 80% accuracy with the use of ultrasound. Manno et al. (6) found a bedside ultrasound protocol in all admitted ICU patients changed the admitting diagnosis in 25.6% of patients, prompted further testing in 18.4% of patients and altered medical therapy in 17.6% of patients.

Bedside cardiac ultrasound in particular has been adopted as a key component of the emergent evaluation of critically ill patients (7,8). Cardiac ultrasound in the hands of non-cardiologist and non-radiologist clinicians has been shown to be accurate and reliable in diagnosing a wide array of pathologies. One paper has described a limited echocardiography protocol for use in trauma intensive care patients with the aim of evaluating for pericardial effusion, ventricular function and volume status (9). All whole-body sonography protocols that have been described for the evaluation of shock incorporate a limited cardiac exam. Within both studies described above, the cardiac portion yielded positive findings most frequently (2,6). However, despite these advances in clinical practice, to our knowledge no standardized, goal-directed bedside echocardiography protocol currently exists to guide the ongoing resuscitation of patients in shock.

This novel goal-directed echocardiography protocol was developed to provide immediate diagnostic information as to the etiology of shock similar to other protocols as well as provide hemodynamic information useful to guiding and assessing therapy during ongoing resuscitation. The protocol is taught to critical care and emergency ultrasound fellows at our institution as well as emergency medicine residents rotating in the ICU. It is designed to go beyond diagnosing the etiology of shock and to guide on-going resuscitation of critically ill patients through their hemodynamic crisis. The initial exam serves as a benchmark to which future exams are compared, and subsequent exams monitor the hemodynamic response to interventions. The intention is that this protocol be used on a recurring and as-needed basis to supplement the standard hemodynamic monitoring in a patient with shock

This protocol [Table 1] is evidence-based.

Table 1. Evaluation parameters: Goal-directed Assessment.  (Editor's note: the size on your browser may need to be enlarged to adequately view the table).  

It incorporates the elements of the bedside cardiac exam that have been proven in the literature to be accurate and useful in the emergency setting. It is not designed to replace standard comprehensive echocardiography but rather to be used in locations or situations where obtaining a complete echocardiogram is not possible or feasible given time of day, availability of formal echo services and clinical condition of the patient. Additionally, the protocol can be repeated after an intervention to assess progress during resuscitation whereas repeated formal echocardiograms are not reasonable. The information obtained at the bedside from this protocol is potentially useful for diagnosing the etiology of shock, and guiding resuscitation of patients with hemodynamic instability. It is not intended to manage the subtleties of chronic cardiovascular disease or valvular disease.

A key element to the use of this protocol is the potential to determine response to therapy to help on-going resuscitation of patients with hemodynamic instability. In a volume-depleted patient, for example, a repeat exam could be performed following each fluid bolus. Traditionally, clinical exam findings of excessive fluid administration can be monitored but occur after the desired intravascular volume status has been surpassed and possible patient harm has been done. A patient in shock who, after several liters of fluid, no longer demonstrates intravascular volume depletion can be assuredly started on vasopressors. Additionally, a patient who continues to demonstrate volume responsiveness with a large stroke volume may be started on vasopressors in the setting of diastolic failure. This phenomenon is also seen as a result in increased arterial elastance which is unlikely to improve from further fluid administration.

This protocol [Table 1] proceeds with several qualitative questions along with obtaining several quantitative hemodynamic parameters in the process. Following is a description of each step in the protocol:

1. Pericardial effusion

Q: Is there a pericardial effusion present? Yes or No

Q: If there is a pericardial effusion present, is there evidence of tamponade physiology (i.e. right ventricular diastolic collapse and/or plethoric inferior vena cava)? Yes or No

This protocol begins with an evaluation for pericardial effusion. The use of bedside ultrasound to diagnose pericardial effusion was one of the first applications employed by emergency medicine and critical care specialists. Emergency physicians can detect pericardial effusion on bedside ultrasound with a sensitivity of 96% and a specificity of 98% (10). Hand-carried ultrasound units have been used in cardiac ICUs to identify pericardial effusion (11). Although the sensitivity and specificity of these handheld units was 75% and 88% respectively, for all effusions, all false negatives had less than 20 mls of pericardial fluid on contrast enhanced CT and all false positives were estimated to be trace as well (11). Bedside ultrasound in undifferentiated dyspneic patients found pericardial effusion in 13.6% of patients, 29% of which required pericardiocentesis (12). If identified, the clinician can then evaluate for echocardiographic signs of tamponade. The elements of comprehensive echocardiographic evaluation for tamponade that are likely to be obtainable with a bedside machine by a non-cardiologist clinician are right ventricular diastolic collapse and inferior vena cava plethora (Figure 1) (13,14). However, as described below, inferior vena cava plethora can be caused by any elevation of right-sided pressures and should be interpreted in the context of the other findings on the exam.

Figure 1. Panel A: Plethoric, non-collapsible IVC suggests elevated right sided pressures or tamponade physiology. Panel B: Presence of pericardial effusion on subxyphoid view is small, but shows diastolic right ventricular collapse. Panel C: M-mode on parasternal long axis suggests tamponade physiology.

2. Global systolic function

Q: Is the left ventricular global systolic function decreased, normal, or hyperdynamic?

Q: What is the stroke volume and cardiac output?

In this protocol, left ventricular systolic function is assessed globally and is graded as decreased, normal, or hyperdynamic, rather than quantitatively estimating left ventricular ejection fraction (LVEF). Although LVEF is a numerical representation of left ventricular function, it is difficult to obtain in the acute setting and influenced by critical illness, as well as anatomic and physiologic factors limiting adequate endocardial visualization (15). Additionally, as LVEF is not influenced by hemodynamic parameters (preload, afterload), it is less useful for the acute hemodynamic evaluation of the patient in shock (16). E-point septal separation (EPSS) has been compared to magnetic resonance imaging methods of calculating ejection fraction with good correlation; however that correlation declines in the presence of wall motion abnormalities and valvular disease (17,18). Ahmadpour et al. (19) demonstrated EPSS to be a reliable index of ventricular performance in coronary artery disease patients but only as a predictor of decreased ejection fraction rather than estimating the exact ejection fraction. Secko et al. (20) showed that novice emergency physician obtained EPSS measurements correlated well with visual estimates of EF; however EPSS as a continuous variable did not correlate well with fractional shortening measurements in a study by Weekes et al. (21). These data would suggest that estimating LVEF by either estimating quantitatively or by EPSS is inconsistent and not indicative of the underlying hemodynamic state. Instead of attempting to quantify ejection fraction, this protocol uses visual estimates of LV systolic function obtained in each view, which have been shown to be accurate and easily performed at the bedside (16,22-24).

3.   IVC

Q: Is the IVC small (<2cm) or large (>2cm)?

Q: Is the IVC dynamic (>20% change in diameter with respiration)?

Assessing volume responsiveness in hypotensive patients is of paramount importance for restoring intravascular volume without deleteriously volume overloading the patient, which has been shown to worsen outcomes (25-28).Traditionally, central venous pressure (CVP) has been used as an endpoint of volume resuscitation (29). CVP as a measure of ventricular preload has been shown to poorly correlate with intravascular volume status and volume responsiveness (30-32). Rather than static CVP measurements, dynamic volume assessments reflected by cardiopulmonary interactions are more accurate and reliable for predicting improved cardiac index with volume infusion (33-40). Bedside ultrasound assessment of dynamic changes in inferior vena cava diameter with either distensibility (IVCd) in the case of a mechanically ventilated patient or collapsibility in a spontaneous breathing is a pre-heart/lung observation of cardiopulmonary interactions and has been shown to be reliable for predicting volume responsiveness (34,35,39,41,42). This protocol uses IVCd as one of three assessments of volume responsiveness along with obliteration of the LV cavity on parasternal short axis (papillary level) and left ventricular outflow tract VTi. Since evidence of IVCd measurement in the presence of cirrhosis and alternative ventilator modes such as airway pressure release ventilation (APRV) is lacking, it is not ideal as the sole assessment for volume responsiveness. A plethoric IVC can be seen in both high right-sided pressure (pulmonary embolism, RV infarct) and in tamponade physiology. A plethoric IVC in the absence of pericardial effusion should alert the physician to the presence of high right-sided pressure or RV volume overload. Additionally, determination of adequate intravascular volume status can guide clinicians in initiation or titration of pressor support.

4. Volume Responsiveness

Q: Does this patient appear to be volume responsive (i.e. in addition to IVC collapsibility, is there a hyperdynamic LV with cavity obliteration on systole and is there variability in the LVOT VTi)? Yes or No

In addition to IVCd, this protocol uses a global assessment of the left ventricular dynamics and the left ventricular outflow tract velocity time integral (LVOT VTi) respiratory variation as assessments of volume responsiveness (Figure 2).

Figure 2. Collapsibility of the IVC (Panel A, top left), hyperdynamic left ventricle with obliteration of the LV cavity on parasternal short axis (Panel B, top right), and variability of the left ventricular outflow tract with inspiration (Panel C, bottom) are indicators of volume responsiveness.

Left ventricular end diastolic area (LVEDA), if seen as cavitary obliteration or “kissing papillary muscles” on parasternal short axis, has been shown to correlate with the presence of hypovolemia (43,44). LVOT VTi variability has recently been shown to correlate well with non-invasive cardiac output monitors to determine volume responsiveness in hypotensive patients (45,46). The LVOT VTi obtained on an apical 5 chamber can be used with the LVOT diameter obtained in the parasternal long axis view to calculate the stroke volume and cardiac output (Figure 3) (47,48).

Figure 3. Stroke volume (SV) and cardiac output. The stroke volume is calculated by measuring the diameter of the LVOT on parasternal long axis (Panel A, left) and the LVOT VTi (Panel B, right) [SV= Vti x π(LVOTd/2)²]. Cardiac output is calculated by multiplying SV by the heart rate.

The LVOT VTi represents a Doppler assessment of cardiopulmonary interactions that translates to stroke volume variation, pulse pressure variation, and systolic pressure variation as seen on an arterial line tracing which has been well correlated with volume responsiveness (33,36,37,41,42,49).

Case 1:  A 48-year-old male is admitted to the intensive care unit (ICU) with septic shock secondary to spontaneous bacterial peritonitis. He had received several liters of crystalloid in the ED and remains hypotensive with poor perfusion. RECES protocol was performed on admission to the ICU, which demonstrated the patient was volume responsive; however the stroke volume and cardiac output were elevated suggesting increased vascular elastance rather than intravascular volume depletion. The patient was placed on a vasopressor with improved tissue perfusion and indicators of shock.

5. Diastolic dysfunction

Q: Is there diastolic dysfunction? Yes or No

Q: Is there evidence of elevated left atrial pressure? Yes or No

Diastoloic dysfunction plays an increased role as patients age or have chronic hypertension (50). Hemodynamically, this leads to an increased likelihood of pulmonary edema with aggressive fluid resuscitation, which has been shown to increase mortality (25,27,28). In this protocol, mitral valve inflow velocities by pulsed wave Doppler (PWD) are used to assess diastolic dysfunction. Mitral E and A waves accurately reflect the pressure gradient between the left atrium and left ventricle and have been shown to be superior to LVEF for estimation of left ventricular function (50). Mitral annulus tissue Doppler (TDI) is used to differentiate between pseudonormal inflow velocity patterns and decreased LV compliance as well as estimate left atrial pressure (50). In grade I diastolic dysfunction, mitral inflow velocities demonstrate an E-A reversal. As left ventricular compliance worsens, the E-A pattern returns to normal; however, the velocities increase, representing the left atrium “pushing” the blood into the left ventricle rather than the ventricle “sucking” blood from the atrium as the cavitary pressure drops below atrial pressure in the normal heart (51). In mechanically ventilated patients diastolic velocities may be altered to some degree by changes in left ventricular compliance, mainly through changes in right ventricular compliance via ventricular interdependence. Additionally, estimated pulmonary artery systolic pressures >40mmHg in the absence of known pulmonary hypertension, lung disease, or systolic failure may indicate undiagnosed diastolic dysfunction and caution over-resuscitation with fluids. Emergency physicians can accurately perform this exam at the bedside as shown by Unluer and colleagues (52).

Case 2:  An 81-year-old male presents with 3 days of productive cough and fever. The patient is found to be hypotensive and tachycardic with high suspicion for severe sepsis. Electrocardiogram demonstrates LVH with strain, and labs are consistent with a severe sepsis syndrome. RECES protocol is performed on this patient which demonstrates grade III diastolic dysfunction and moderate mitral regurgitation which limited the amount of crystalloid given to avoid worsened pulmonary edema and ARDS.

6. Wall motion abnormalities

Q: Is there any obvious wall motion abnormality (global or regional)? Yes or No

In a critically ill patient, differentiating shock-induced cardiac dysfunction from cardiogenic shock is difficult. Serial troponins may be helpful but may also be misleading, as in the case of sepsis-induced cardiomyopathy. The consensus statement on the use of focused cardiac ultrasound in the emergent setting recommends comprehensive echocardiography for the diagnosis of wall motion abnormalities (8). To our knowledge, there exists only one paper evaluating the ability of non-cardiologist clinicians to diagnose wall-motion abnormalities. This study showed that a 30-minute training module significantly improved the ability of emergency physicians to identify wall motion abnormalities (53). Though this has not been studied directly, we postulate that a negative exam performed and interpreted by a non-cardiologist clinician, given the skill required in image acquisition and interpretation, does not rule out the presence of wall motion abnormalities. However, a clearly positive exam noted by a bedside clinician in a patient with undifferentiated or multi-factorial shock could dramatically improve the quality of their resuscitation. A positive exam will require interpretation in consideration with the clinical picture and ancillary data. For example, sepsis-induced cardiomyopathy may present as global hypokinesia or unmask underlying ischemic cardiac disease especially in the presence of vasopressors or inotropes. 

7. Right ventricle

Q: Is the right ventricle dilated? Yes or No

Q: Is there tricuspid regurgitation? Yes or No

Q: What is the systolic function of the right ventricle (TAPSE)?

Q: Is there evidence of right ventricular pressure or volume overload (i.e. septal flattening in systole or diastole)?

Q: What is the estimated pulmonary artery systolic pressure?

The right ventricular systolic movement differs greatly from the left ventricle. As opposed to the rotational component to left ventricular contraction, the right ventricular free wall moves towards the septum, followed by longitudinal contraction bringing the base towards the apex (54). As such, the tricuspid annular plane systolic excursion (TAPSE) using M-mode through lateral tricuspid annulus on an apical 4-chamber view is a reliable measurement of right ventricular systolic function (Figure 4) (54-57).

Figure 4. Tricuspid annular plane systolic excursion (TAPSE). M-mode through the lateral tricuspid annulus will demonstrate the amount of longitudinal excursion of the tricuspid annulus during systole. This has been shown to be a reliable indicator of right ventricular systolic function.

Elevations in RV afterload or decreases in contractility are reflected by a lower TAPSE (<16mm) (54,55). Septal movement is also used to demonstrate pressure or volume overload of the right ventricle. Obtained from a parasternal short axis view, septal flattening in systole represents pressure overload of the right ventricle whereas septal flattening in diastole represents volume overload (54). The presence of septal flattening along with a decreased TAPSE should alert the practioner to elevated pulmonary pressures and RV failure in the acutely hypotensive patient. Pulmonary artery systolic pressure can be calculated by continuous wave (CW) Doppler of the tricuspid regurgitation jet obtained on an apical 4 chamber view (p=4V²) (58). PA systolic pressure may be helpful to determine acute vs. chronic RV failure as the right ventricle is unable to overcome acute elevations in PA pressure >40mmHg (54,59,60).

Case 3:  A 56-year-old female presents by EMS with a seizure. She is found to be hypoxemic, unresponsive to supplemental oxygen, and hypotensive. She is given a fluid bolus immediately in the emergency department (ED), which worsens her hypotension and hypoxemia. The RECES protocol performed showed a dilated, hypodynamic right ventricle with a measured TAPSE of 12mm (severely decreased). tPA was administered and repeat RECES exam demonstrated an improved TAPSE of 16mm after 2 hours.  

8. Valves

Q: Is there obvious mitral, tricuspid, or aortic valve regurgitation? Yes or No

No systematic study has been performed evaluating the ability of emergency or critical care physicians to diagnose valvular pathology with bedside ultrasound. A study done comparing handheld bedside sonography performed by cardiologists to standard echocardiography found good agreement between studies in diagnosing morphologic aortic and mitral valvular pathology (61). Literature describing clinician-performed bedside echocardiography to diagnose valvular disease is limited to case reports (62-64). Despite this, a grossly abnormal valve could be recognizable by bedside clinician sonographers. In scenarios of papillary muscle rupture or valvular vegetations, recognition of these conditions would dramatically influence care. A strong regurgitant jet across the aortic or mitral valve in the setting of shock should alert the physician to acute valvular incompetence or, in the right clinical setting, endocarditis with valvular deterioration.

Limitations

The RECES protocol is not without its limitations. First, there requires a training period to not only learn the mechanics of acquiring the ultrasound images, but also gaining the knowledge base to interpret the findings and manipulate hemodynamics based on those findings. The protocol attempts to simplify complex echocardiographic principles into simple questions, however still requires somewhat intricate knowledge of hemodynamic principles to interpret. Although ultrasound training has become a required component of emergency medicine training and enthusiasm is increasing in critical care training, there still remains a large proportion of physicians in both specialties with limited to no ultrasound skills and would be required to attend a national course to gain the prerequisite skill. Secondly, although echocardiography is immensely helpful in the critically ill, it can also be very difficult in some patients. Many patients are intubated and cannot cooperate with positioning, obese, or have chronic lung disease limiting the ability to acquire appropriate views.

Conclusion

This protocol does not intend to replace comprehensive echocardiography. The machine quality and level of training of bedside clinicians cannot match the level of expertise available with comprehensive echocardiography. However, there are many scenarios in which comprehensive echocardiography cannot be feasibly obtained for a critically ill patient. This protocol is intended to be rapidly performed and allow a treating physician to make immediate clinical decisions when circumstances do not allow for comprehensive echocardiography. Additionally, a limitation of comprehensive echocardiography in the early period of resuscitation is that the information obtained can quickly become obsolete in the setting of a dynamic situation of disease progression and aggressive resuscitation. However, a key component of this protocol is re-evaluation throughout the resuscitation to account for these rapid changes.

Our experience with this protocol shows that others with similar or adequate training in echocardiography can use this protocol to determine the volume responsiveness (IVCd, LVOT VTi) of their patient as well as presence of pericardial effusion with tamponade physiology (RV diastolic collapse, MV inflow variability), systolic failure (poor contractility, decreased SV and CO), diastolic dysfunction (MV inflow velocities and TDI), RV systolic failure (TAPSE), acute valvular rupture, obvious wall motion abnormalities, and signs of pressure or volume overload (septal flattening on parasternal short axis). Future studies should evaluate the learning curve for mastering the ultrasound skills necessary for reliably performing the RECES protocol.

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Corresponding Author: 

Jarrod M. Mosier, MD

Assistant Professor

Department of Emergency Medicine

Department of Medicine, Section of Pulmonary, Critical Care, Allergy and Sleep

University of Arizona

1609 N Warren

FOB 122C

Tucson, Az 85719

Phone: 775-527-1292

Fax: 520-626-2480

jmosier@aemrc.arizona.edu

Disclosures: None for any authors

Reference as: Mosier JM, Stolz L, Bloom J, Malo J, Snyder L, Fiorello A, Adhikari S. Resuscitative EChocardiography for the Evaluation and management of Shock: The RECES protocol. Southwest J Pulm Crit Care. 2014;8(2):110-25. doi: http://dx.doi.org/10.13175/swjpcc177-13 PDF