Validity of Clinical Indications of Pediatric Bedside Echocardiography in Critically Ill Children: A Single Center Study

Document Type : Original Research

Authors

Pediatric Department, Faculty of Medicine, Cairo University, Egypt

Abstract

Background: Management of critically ill pediatric patients is a demanding task that relies on a combination of clinical skills and measurement of hemodynamic variables. Echocardiography is currently considered a key tool for the hemodynamic assessment in intensive care units, able to identify causes of hemodynamic instability and to correctly guide therapy.
Aim of the work: To determine the type of indications for requesting bedside echocardiography in neonatal and pediatricintensive care units in our center, and to find which of these indications have the highest sensitivity to confirm the presence of echocardiographic abnormalities.
Methods: We conducted a prospective study at Cairo University Children’s Hospital on 271 critically ill patients admitted to neonatal and pediatric intensive care units and who underwent bedside echocardiography examination. Detailed clinical examination, chest X-ray and echocardiography were done for all patients and comparative results were evaluated.
Results: The commonest encountered condition detected with bedside echocardiography in the neonatal intensive care units was pulmonary hypertension representing 35.8% of the examined neonates, while in the pediatric intensive care units it was impaired cardiac contractility representing 33.1% of the totally examined children. The commonest indication for requesting bedside echocardiography was screening for hemodynamically significant patent ductus arteriosus in preterm infants (n= 73, 42%) in neonatal intensive care units’ group, while the most common indication for requesting bedside echocardiography was in pediatric intensive care units’ group assessment of the cardiac function (n= 60, 61.9%). Of the total requested bedside echocardiography examinations, we found that 51.7% of those performed in neonatal intensive care units’ and 19.6% in the pediatric intensive care units’ had no significant cardiac abnormality.
Conclusion: The use of bed side echocardiography by intensivists and pediatric cardiologists is necessary. Adequate training to attain skills for bedside echocardiography examination by neonatal and pediatric intensivists is an essential requisite for sound primary echocardiographic assessment.

Keywords


Introduction

Prompt management of critically ill pediatric patients necessitates proper diagnosis and timely intervention (2). Hemodynamic assessment is vital to the management of critically ill patients (3). Echocardiography has become a bedside tool in the pediatric intensive care unit (PICU) and neonatal intensive care unit (NICU) (4). It has become indispensable in diagnosis because of its real time ability to visualize the heart, lack of invasiveness and because it does not need specific installation precautions (5). Echocardiography provides confirmation of disease suggested by clinical findings, or rules it out (6). Echocardiography has limitations and the most important limitation is that it is operator dependent, and needs training to achieve the required  skill. Yet, echocardiography is not a replacement for  physical examination and clinical assessment for hemodynamic stability while making clinical decisions (7).

Clinical indications for request of echocardiography in the pediatric and neonatal intensive care units are summarized as TINEC (training in intensive care and neonatal echocardiography). The indications include, evaluation of cardiac function, structural anomalies of cardiac muscle and valves, pulmonary hypertension, pericardial effusion and tamponade, transitional circulation of the newborn, evaluation of line placement and as a guide for interventions within the intensive care unit(8). 

Subjects and Methods 

This prospective study was conducted at Cairo University Children’s Hospital. Bedside echocardiography was performed in critically ill children and neonates who were admitted to the neonatal and pediatric intensive care units between November 2020 and April 2021. The study was approved by Higher Studies Research Committee of Faculty of Medicine, Cairo University, in compliance with Helsinki declaration guidelines (9). 

Participants

The study included 271 patients with critically ill conditions; 174 neonates admitted in neonatal intensive care units and 97 children admitted in pediatric intensive care units.

Methods

All enrolled children underwent:

Careful history taking, clinical examination and relevant investigations. Examination inluded anthropometric measures (length/height, body weight), oxygen saturation, blood pressure and heart ratecardiac examination and hemodynamic stability (inotropes and degree of respiratory support). Indications for bedside echocardiography in the echocardiography request and the included clinical signs that caused the physicians to ask for echocardiography such as presence of a cardiac murmur, or abnormal heart sound, congenital anomalies, unexplained cyanosis, or otherwise.

Imaging and Conventional Echocardiography:

Chest X-ray was done to assess cardiac size and pulmonary vasculature.

Echocardiography 2 D and M mode, (GE Vivid 5 Echo machine, USA) was used to assess pulmonary artery pressure (PAP), hemodynamically significant patent ductus arteriosus, global left ventricular systolic function major congenital heart defects including duct dependent circulation and diagnose of infective endocarditis especially in patients with long-standing central venous lines. 

Statistical Analysis 

The collected data were revised, coded, tabulated and introduced to a PC using statistical package for social sciences (SPSS 16.0 for windows; SPSS Inc., Chicago, IL, 2001). Data were presented and the suitable analysis was done according to the type of data obtained for each parameter. Descriptive data were presented as mean, standard deviation (±SD), range for numerical data and frequency and percentage for non-numerical data. For independent samples t test was used to assess the statistical significance of the difference between means. Chi-square test was used to examine the relations between qualitative variables. One way ANOVA test was used to assess the statistical significance of the difference between means. P

Results

Neonatal ICU Group:

The mean age of the enrolled 174 neonates was 5 days (range 1 to 51 days); while the mean weight was 2.1 kg. Seventy nine (45.4%) were full term, and 95 (54.6%) were preterm (mean ±SD= 37± 2 weeks; range 34-39 weeks). (Tables 1 and 2).  Thirteen (7.5%) of the examined infants did not require respiratory support, 10.3% were on nasal oxygen, 31.6% were on continuous positive airway pressure and non-invasive synchronized intermittent mandatory ventilation, and 50.6% were on invasive mechanical ventilation. Upon cardiac auscultation, 36 infants had cardiac murmurs while 138 had no audible murmurs. Screening for a hemodynamically significant PDA in the preterm infants was the most encountered indication representing 42%, while exclusion of cardiac abnormalities in infants of diabetic mothers was the least common indication representing 6.9%. (Figure 1). The bedside echocardiographic examination confirmed that 37 of 66 infants with clinical signs suggestive of pulmonary hypertension did have pulmonary hypertension, and that 22 of the 36 infants who were clinically suspected to have congenital heart defects, did have congenital heart defects. Table 3 outlines correlation between the clinical assessment and findings encountered after echocardiographic examination in neonates admitted to the NICU.

Table 1. Characteristics of studied neonates in the NICU (n= 174)

  

                       Mean

SD

Minimum

Maximum

Age (days)

5

7

1

51

Length (percentile)

5

7

3

10

Weight (percentile)

10

2

3

15

SpO2 (%)

94

5

65

99

Heart rate (beat/min)

143

15

118

270

SBP (mmHg)

55

12

30

100

DBP (mmHg)

31

8

16

70

Respiratory rate (/min)

52

6

37

70

 

 

 

Number

%

Gender

Male

 

108

62.1

Female

 

66

37.9

Maturity

Preterm

 

95

54.6

Full term

 

79

45.4

Respiratory support

Nil

 

13

7.5

Nasal oxygen

 

18

10.3

CPAP/NI-SIMV

 

55

31.6

Invasive ventilation

 

88

50.6

Cardiac murmur

No 

 

138

79.3

Yes 

 

36

20.7

Need for inotropes

No 

 

85

48.9

Yes 

 

89

51.1

Chest X-ray

Normal

 

27

15.5

RDS

 

121

69.5

Cardiomegaly

 

9

5.2

Pneumonia

 

12

6.9

Diaphragmatic hernia

 

1

0.6

Pleural effusion

 

4

2.3

           

CPAP= continuous positive airway pressure; DBP= diastolic blood pressure NI-SIMV: non-invasive synchronized intermittent mandatory ventilation; RDS: respiratory distress syndrome; SD: standard deviation; SBP: systolic blood pressure; SpO2: oxygen saturation.

 

 

 

The most common clinical signs associated with echocardiographic abnormalities were those indicating the presence of pulmonary hypertension in neonates 37 (55.2%), such as a preductal-post ductal saturation gradient and a loud single second heart sound. Figure 2 and 4 represent the receiver operating characteristic curve, which shows that clinical cues suggestive of the presence of pulmonary hypertension are the most sensitive to detection after echocardiographic examination in NICU and PICU respectively.

 

 

 

Table 2: Indications for requesting bedside echocardiographic in the NICU group:

 

Number

%

Concerning fetal echocardiogram suspicious for cardiovascular abnormality

7

4

Murmur with pathological acoustic characteristics

36

20.7

Abnormal chest X-ray findings including cardiomegaly (transverse diameter of the cardiac silhouette ≥ 50% of the transverse diameter of the chest), boot-shaped heart in tetralogy of Fallot, and gooseneck in endocardial cushion defect

9

5.2

Desaturation demonstrated on pulse oximetry (a pulse oxygen level <90% in either right hand or foot, or a level <95% that continued to be low after repeated measurements) that was not explained by pulmonary diseases

33

18.9

Suspected cases of congenital heart diseases by history and examination including central cyanosis, respiratory distress, murmurs and certain syndromes that are known to be associated with cardiac abnormalities as Down syndrome

36

20.7

Assessment of the pulmonary artery pressure in cases with history of obstructed labor or meconium aspiration that were followed by respiratory distress and desaturation

53

30.5

 

 

 

Pediatric  ICU Group:

The mean age of the studied 97 children admitted to pediatric ICU was 58.6 ± 53.7 months (range 1 to 168 months). Table 4 summarizes  their findings. Table 5 and Figure 3 summarizes the indications for bedside echocardiography among this group. The bedside echocardiographic examination confirmed that 25 of 29 children with clinical signs suggestive of pulmonary hypertension were found to have pulmonary hypertension, 32 of 44 children suspected clinically of having impaired cardiac contractility showed impaired cardiac contractility after echocardiographic examination, 5 of the 8 children who were clinically suspected of having cardiac vegetation revealed cardiac vegetation after echocardiographic examination and 5 of the 7 children who were clinically suspected of having pericardial effusion did indeed have pericardial effusion. Table 6 outlines the correlation between the clinical assessment and findings encountered after echocardiographic examination in children admitted to the PICU.

 

Table 4. Characteristics of children admitted to the PICU (n= 97).

  

 

Number

%

Gender

Male

46

47.4

Female

51

52.6

Respiratory support

Nil

5

5.2

Nasal oxygen

66

68.0

Invasive ventilation

26

26.8

Cardiac murmur

No

78

80.4

Yes

19

19.6

Need for Inotropes

No

41

42.3

Yes

56

57.7

Chest X-ray

Normal

27

27.8

Cardiomegaly

22

22.7

Pneumonia

45

46.4

Pleural effusion

3

3.1

 

            

 

Table 5: Indications for requesting bedside echocardiographic in the pediatric ICU group.

 

Number

%

Follow up of cases that were known to have cardiac abnormality e.g. cardiomyopathy, congenital structural heart diseases

11

11.4

Murmur with pathological acoustic characteristics

19

19.5

Abnormal chest X-ray findings including cardiomegaly (transverse diameter of the cardiac silhouette ≥ 50% of the transverse diameter of the chest), boot-shaped heart in tetralogy of Fallot, and gooseneck in endocardial cushion defect

11

11.4

Desaturation demonstrated on pulse oximetry (a pulse oxygen level <90% in either right hand or foot, or a level <95% that continued to be low after repeated measurements) that was not explained by pulmonary diseases

12

12.4

Suspected cases of infective endocarditis especially in patients with central venous catheters who had fever, positive blood culture and elevated sepsis markers

8

8.2

Systemic disorders with suspected cardiac abnormalities as dilated coronaries in Kawasaki disease and signs of congestive heart failure as tachycardia, tachypnea and tender hepatomegaly in patients admitted with septic shock to assess fractional shortening

29

29.9

Suspected pericardial effusion e.g. hypoalbuminemia patients with nephrotic syndrome who had muffled heart sounds

7

7.2

 

 

 

 

Discussion

Echocardiography is a valuable tool that has become a standard service in neonatal and pediatric intensive care units to provide prompt timely assessment of cardiac structure and function, follow up of medications and guide intervention (10). Bedside echocardiography is increasingly being relied upon as an extension of physical examination, and in conjunction with the existing clinical parameters in making clinical decisions (1112).

In the current study, clinical signs suggestive of pulmonary hypertension were found to be the most sensitive parameter, while signs suggestive of the presence of congenital heart defects (other than patent ductus arteriosus) were found to be the most specific parameter in detecting cardiac problems in neonatal intensive care units (NICU) settings. Bedside echocardiography has provided statistically significant more accurate diagnosis of pulmonary hypertension, structural cardiac anomalies and impaired cardiac contractility in both the NICU and the pediatric ICU. More diligent clinical examination and search for signs to improve the clinical examination accuracy and decision making is seen as a necessity. Again, there is a need for training of physicians caring for NICU and pediatric ICU patients to acquire bedside echocardiography skills (13). 

The need for bedside echocardiography is especially required in settings of ventilator care where child is not ambulant. Many cardiac abnormalities in neonates are associated with respiratory distress, which is one of the reasons for requesting a bedside echocardiographic evaluation in neonates who needed respiratory assistance but had no obvious cause for chest abnormalities. In our study, we found that a total of 31.6% neonates were on continuous positive airway pressure whereas 50.6% neonates were on synchronized intermittent mandatory ventilation plus pressure support ventilation. Out of 161 neonates with respiratory distress, 76 (47.2%) of cases showed abnormal echocardiographic findings. Fifty percent of the studied neonates and 26% of the children in our study were on ventilator care. The ambulation of the echo machine is another important factor that should be addressed in the NICU and pediatric ICU setting (8). Again the value of echocardiography extends to screening for peripheral lung pathology as well, for its proven high sensitivity and specificity (14). 

In the present study, it was observed that the most common indication for requesting bedside echocardiography in neonates was screening for hemodynamically significant patent ductus arteriosus (PDA) in preterm infants (n= 73, 42%). After the preterm screening, assessment of the pulmonary artery pressure in infants with severe respiratory distress (n= 53, 30.5%) and exclusion of congenital cardiac anomalies (20.6%) were the next most common indications. Physicians caring for preterm neonates were more commonly inclined to ask for confirmatory bedside echocardiography. Having immature organ systems, a preexisting intrauterine milieu that led to preterm delivery, and the resulting need for surfactant administration, ventilatory support, and vasoactive medications, make them more vulnerable to complications during the transition from fetal to postnatal life. The need for bedside diagnosis is highlighted by fact that the hemodynamically unstable cardiac anomalies are crucial predictors of the outcome (10). 

In the present study, it was observed that the most common indication for requesting bedside echocardiography in the pediatric intensive care unit (PICU) group was assessment of the cardiac function (n= 60, 61.9%). Diagnosis/follow up of congenital heart disease (n= 22, 22.7%) and exclusion of cardiac vegetation (7.2%) were the next most common indications. Among 56 examined cases who were on inotropic cardiac support, 16 (28.5%) cases demonstrated impaired FS (25, 30%) while 18 (32.1%) cases showed poor FS (<25%). This reflects that the decision for inotropic support is a purely clinical decision and does not correlate to the echocardiographic findings. 

Clinical signs suggestive of impaired cardiac contractility were found to be the most sensitive parameter in the current study, while signs suggestive of pericardial effusion were found to be the most specific parameter in detecting cardiac problems in pediatric intensive care units (PICU) settings.

By analyzing the total number of requested bedside echocardiography we found that 51.7% of the neonatal intensive care units (NICU) group and 19.6% of the pediatric intensive care units (PICU) group showed no significant cardiac abnormality. The excessive requests should not be viewed as abuse of resources but rather as an indication for the need for rendering the bedside echocardiography as a real time part of physical examination of the critically ill neonate or child.

Conclusion

Echocardiographic evaluation is a valuable tool and the requirement of echocardiographic assessment increases according to clinical severity. The most commonly encountered indication for requesting bedside echocardiography was screening for hemodynamically significant patent ductus arteriosus in the neonatal intensive care units and assessment of cardiac function in the pediatric intensive care units. Clinical signs of pulmonary hypertension were found to be the most sensitive parameter reflecting cardiac problems in neonatal intensive care unit, while clinical signs of impaired cardiac contractility were found to be the most sensitive parameter reflecting cardiac problems in pediatric intensive care units. In the neonatal intensive care units, the number of echocardiograms that revealed no cardiac abnormalities outnumbered those that revealed a cardiac problem. 

 

Author Contributions: All authors shared in conceptualization, supervising, data curation, data analysis, writing original draft, data interpretation, writing original draft, supervising and revising. All authors reviewed the final manuscript. All authors have read and agreed to the published version of the manuscript.

 

FUNDING

Authors declare there was no extramural funding provided for this study. 

 

CONFLICT OF INTEREST

The authors declare no conflict of interest in connection with the study. 

1.         S. Tenny, M. Varacallo, Evidence Based Medicine. (StatPearls Publishing; Treasure Island (FL), 2020; https://www.ncbi.nlm.nih.gov/books/NBK470182/).
2.         World Health Organization, Guideline: Updates on Paediatric Emergency Triage, Assessment and Treatment: Care of Critically-Ill Children. (Geneva, 2016; https://www.ncbi.nlm.nih.gov/books/NBK350529/).
3.         Y. Singh, J. U. Villaescusa, E. M. da Cruz, S. M. Tibby, G. Bottari, R. Saxena, M. Guillén, J. L. Herce, M. Di Nardo, C. Cecchetti, J. Brierley, W. de Boode, J. Lemson, Recommendations for hemodynamic monitoring for critically ill children—expert consensus statement issued by the cardiovascular dynamics section of the European Society of Paediatric and Neonatal Intensive Care (ESPNIC). Crit. Care24, 620 (2020).
4.         On Behalf of Study Group of Neonatal Cardiology of the Italian Society of Neonatology, I. Corsini, B. Ficial, S. Fiocchi, F. Schena, I. Capolupo, R. M. Cerbo, M. Condò, D. Doni, S. La Placa, S. Porzio, K. Rossi, S. Salvadori, M. Savoia, Neonatologist performed echocardiography (NPE) in Italian neonatal intensive care units: a national survey. Ital. J. Pediatr. 45, 131 (2019).
5.         F. Rabah, K. Al-Senaidi, I. Beshlawi, A. Alnair, A.-A. A. Abdelmogheth, Echocardiography in PICU: when the heart sees what is invisible to the eye. J. Pediatr. (Rio J.)92, 96–100 (2016).
6.         R. T. Arntfield, S. J. Millington, Point of Care Cardiac Ultrasound Applications in the Emergency Department and Intensive Care Unit - A Review. Curr. Cardiol. Rev. 8, 98–108 (2012).
7.         Y. Singh, Echocardiographic Evaluation of Hemodynamics in Neonates and Children. Front. Pediatr. 5, 201 (2017).
8.         C. Tissot, V. Muehlethaler, N. Sekarski, Basics of Functional Echocardiography in Children and Neonates. Front. Pediatr.5, 235 (2017).
9.         World Medical Association, WMA Declaration of Helsinki- Ethical Principles for Medical Research Involving Human Subjects (2013), (available at https://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/2013/).
10.       B. Hanna, S. Nashed, M. Tadros, Z. Osman, Echocardiographic Parameters of Severity in Isolated Neonatal Patent Ductus Arteriosus. Pediatr. Sci. J. 1, 41–51 (2021).
11.       Y. Sedky, S. El-Saiedi, N. Habeeb, R. El Kaffas, M. Gabre, A. Badr, M. Eid, Function Heterogeneity of Different Segments of Left Ventricle in Pediatric Dilated Cardiomyopathy: A Tissue Doppler Study. Pediatr. Sci. J. 1, 52–61 (2021).
12.       K. T. Spencer, F. A. Flachskampf, Focused Cardiac Ultrasonography. JACC Cardiovasc. Imaging12, 1243–1253 (2019).
13.       S. Srivastava, B. F. Printz, T. Geva, G. S. Shirali, P. M. Weinberg, P. C. Wong, P. Lang, Task Force 2: Pediatric Cardiology Fellowship Training in Noninvasive Cardiac Imaging. J. Am. Coll. Cardiol. 66, 687–698 (2015).
14.       C. Basanti, M. A. Kotb, H. M. Seif, F. I. Farag, A. Abdelmegeid, Pediatric Chest Ultrasound for Bedside Diagnosis of Pneumonia: A Validation Study for Diagnostic Options in Developing Countries. Pediatr. Sci. J. 1, 15–24 (2020).