Research Open Access: Singh Et Al. Critical Care (2020) 24:65
Research Open Access: Singh Et Al. Critical Care (2020) 24:65
Research Open Access: Singh Et Al. Critical Care (2020) 24:65
Abstract
Background: Point-of-care ultrasound (POCUS) is nowadays an essential tool in critical care. Its role seems more
important in neonates and children where other monitoring techniques may be unavailable. POCUS Working
Group of the European Society of Paediatric and Neonatal Intensive Care (ESPNIC) aimed to provide evidence-based
clinical guidelines for the use of POCUS in critically ill neonates and children.
Methods: Creation of an international Euro-American panel of paediatric and neonatal intensivists expert in POCUS
and systematic review of relevant literature. A literature search was performed, and the level of evidence was
assessed according to a GRADE method. Recommendations were developed through discussions managed
following a Quaker-based consensus technique and evaluating appropriateness using a modified blind RAND/UCLA
voting method. AGREE statement was followed to prepare this document.
Results: Panellists agreed on 39 out of 41 recommendations for the use of cardiac, lung, vascular, cerebral and
abdominal POCUS in critically ill neonates and children. Recommendations were mostly (28 out of 39) based on
moderate quality of evidence (B and C).
Conclusions: Evidence-based guidelines for the use of POCUS in critically ill neonates and children are now
available. They will be useful to optimise the use of POCUS, training programs and further research, which are
urgently needed given the weak quality of evidence available.
Keywords: Neonate, Children, Ultrasound, Point of care ultrasound (POCUS), Paediatric intensive care unit (PICU),
Neonatal intensive care unit (NICU)
* Correspondence: [email protected]
Yogen Singh and Cecile Tissot equally contributed and shall be considered
as first authors
1
Department of Paediatrics - Neonatology and Paediatric Cardiology,
Cambridge University Hospitals and University of Cambridge School of
Clinical Medicine, Biomedical Campus, Hills Road, Cambridge CB2 0QQ, UK
2
Addenbrooke’s Hospital, Box 402, Cambridge, UK
Full list of author information is available at the end of the article
© The Author(s). 2020 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Singh et al. Critical Care (2020) 24:65 Page 2 of 16
Table 1 Summary of recommendations on the use of POCUS in the neonatal and paediatric critical care
No. Recommendation Level of Quality of
agreement evidence
1. POCUS should not be used as a screening tool for diagnosing congenital heart defects in neonates and children, Strong A
unless neonatologists/paediatric intensivists have received an advanced echocardiography training specifically for agreement
this purpose
2. POCUS may be helpful to assess cardiac filling (preload assessment) and intravascular volume status in neonates Strong D
and children agreement
3. POCUS may be helpful to assess fluid responsiveness in neonates and children Strong D
agreement
4. POCUS may be helpful for qualitative assessment of cardiac function on visual inspection in neonates and Strong D
children agreement
5. POCUS is helpful for semi-quantitative assessment of cardiac function in neonates and children [however, a de- Agreement C
tailed functional assessment should be performed by a person with advanced echocardiography training]
6. POCUS is helpful for assessment of pulmonary artery systolic pressure in pulmonary hypertension in neonates and Strong B
children agreement
7. POCUS is helpful for semi-quantitative assessment of pulmonary hypertension in neonates and children Strong B
agreement
8. POCUS is helpful to diagnose pericardial effusion in neonates and children Strong B
agreement
9. POCUS is helpful to guide pericardiocentesis in neonates and children Strong B
agreement
10. POCUS should be used to assess the patency of ductus arteriosus in neonates and children Strong A
agreement
11. POCUS may be used to detect vegetation to make or exclude the diagnosis of endocarditis [however, a definitive Disagreement D
diagnosis requires a detailed assessment by a paediatric cardiologist].
12. POCUS is helpful to distinguish between respiratory distress syndrome (RDS) and transient tachypnoea of the Agreement B
neonate (TTN)
13. POCUS is helpful to detect pneumonia in neonates and children Agreement B
14. POCUS is helpful to semi-quantitatively evaluate lung aeration and help the management of respiratory interven- Agreement B
tion in acute respiratory distress syndrome (ARDS) in neonates and children
15. POCUS is helpful to recognise meconium aspiration syndrome (MAS) Agreement C
16. POCUS is helpful for descriptive purposes in viral bronchiolitis but cannot provide a differential aetiological Strong C
diagnosis agreement
17. POCUS is helpful to accurately detect pneumothorax in neonates and children Strong B
agreement
18. POCUS is helpful to insert chest tube or perform needle aspiration in neonatal tension pneumothorax Strong B
agreement
19. POCUS is helpful to detect pleural effusions in neonates and children Strong B
agreement
20. POCUS is helpful to guide thoracentesis in neonates and children Strong B
agreement
21. POCUS is helpful to evaluate lung oedema in neonates and children Agreement C
22. POCUS is helpful in detecting anaesthesia-induced atelectasis in neonates and children Agreement C
23. POCUS-guided technique should be used for internal jugular vein (IJV) line placement in neonates and children Strong A
agreement
24. POCUS-guided technique is helpful for subclavian vein line placement in neonates and children Strong B
agreement
25. POCUS-guided technique is helpful for femoral line placement in neonates and children Strong B
agreement
26. POCUS-guided technique is helpful for arterial catheters placement in children Agreement B
27. POCUS-guided technique is helpful for peripherally inserted central catheters in children Agreement B
28. POCUS is helpful to locate catheter tip position in neonates and children Strong C
agreement
29. POCUS is helpful to detect cerebral blood flow changes in neonates and children Agreement B
Singh et al. Critical Care (2020) 24:65 Page 5 of 16
Table 1 Summary of recommendations on the use of POCUS in the neonatal and paediatric critical care (Continued)
No. Recommendation Level of Quality of
agreement evidence
30. POCUS should be used to detect germinal matrix and intraventricular haemorrhage (IVH) in neonates Strong A
agreement
31. POCUS is helpful to detect cerebral blood flow patterns suggesting the presence of cerebral circulatory arrest in Agreement C
children with fused skull bones
32. POCUS is helpful to detect cerebral blood flow changes secondary to vasospasm in patients with traumatic brain Agreement C
injury and non-traumatic intracranial bleeding.
33. POCUS is helpful to detect changes in optic nerve sheath diameter (ONSD) indicative of raised ICP in children Agreement B
with fused skull bones
34. POCUS is helpful to detect cerebral midline shift in neonates and children Agreement C
35. POCUS is helpful for detection of free intra-abdominal fluid in neonates and children Strong C
agreement
36. POCUS may detect parenchymal changes of abdominal organs in neonates and children [although for a definitive Agreement D
diagnosis a detailed assessment should be performed by a paediatric radiologist]
37. POCUS may detect obstructive uropathy in neonates and children [although for a definitive diagnosis a detailed Agreement D
assessment should be performed by a paediatric radiologist]
38. POCUS may assess bowel peristalsis in neonates and children Agreement D
39. POCUS may recognise hypertrophic pyloric stenosis [although for a definitive diagnosis a detailed assessment Disagreement D
should be performed by a paediatric radiologist]
40. POCUS my guide peritoneal drainage or aspiration of peritoneal fluid in neonates and children Strong D
agreement
41. POCUS is helpful to detect signs of necrotising enterocolitis [although for a definitive diagnosis a detailed Agreement C
assessment should be performed by a paediatric radiologist or a person with specific advanced ultrasound
training]
of evidence C). POCUS can be used to assess assessment of pulmonary hypertension by evalu-
cardiac function semi-quantitatively by assessing ating the interventricular septal position and
ejection fraction (EF) and fraction shortening movement at the end of systole and by assessing
(FS) [14, 15]. In experienced hands, POCUS can flow direction and velocities across a patent
be used for further assessment of left and right ductus arteriosus and/or foramen ovale [14, 15].
ventricular function as summarised in Table 2 8. POCUS is helpful to diagnose pericardial
[14, 15, 32–45]. However, a detailed assessment effusion in neonates and children—strong
of cardiac function should be performed by a agreement (quality of evidence B). Pericardial
neonatologist/paediatric intensivist with ad- effusion can reliably be seen on POCUS by
vanced echocardiography training or a paediat- using multiple echocardiographic views [15, 46].
ric cardiologist. Cardiac tamponade should be detected within
6. POCUS is helpful for the assessment of the SAFE (Sonographic Assessment of liFe
pulmonary artery systolic pressure in pulmonary threatening Events) algorithm dedicated to
hypertension in neonates and children—strong recognise the main causes of life-threatening
agreement (quality of evidence B). In the events in children [47].
presence of tricuspid regurgitation, pulmonary 9. POCUS is helpful to guide pericardiocentesis in
artery systolic pressure (PASP) can be reliably neonates and children—strong agreement
estimated using bedside POCUS. In the absence (quality of evidence B). Ultrasound-guided peri-
of right outflow tract obstruction, the cardiocentesis has lower complication rates
regurgitation velocity represents the difference compared to the traditional landmark technique
in pressure between the right atrium and the [48–50].
right ventricle. PASP is derived using a modified 10. POCUS should be used to assess the patency of
Bernoulli equation [14, 15, 32]. ductus arteriosus—strong agreement (quality of
7. POCUS is helpful for semi-quantitative assess- evidence A). Cardiac POCUS can reliably be
ment of pulmonary hypertension in neonates used to assess patency of ductus arteriosus in
and children—strong agreement (quality of evi- preterm infants [8–10]. In experienced hands, it
dence B). In the absence of tricuspid regurgita- may be used for hemodynamic evaluation of the
tion, POCUS can be used for semi-quantitative ductus arteriosus [8, 10].
Singh et al. Critical Care (2020) 24:65 Page 6 of 16
Table 2 Semi-quantitative systolic ventricular function measures that might be used by the clinician with more evolved training in
cardiac POCUS. Normative values are taken from the available literature on the topic [32–45] and represent the best reference data
available so far, although, in some cases, specific level for a different class of patients’ age are lacking
Parameter View Measurement Reference values
LV fraction shortening PSAX, PLAX, LV intraluminal diameter change 28–46% for all ages
(FS%) (2D or M
mode)
LV ejection fraction A4C, A2C Percentage change of LV volume between end-diastole and end-systole 55–80% for all ages
(Simpson’s method)
E-point septal PLAX (2D or Distance between anterior leaflet of the mitral valve and intraventricular > 7 mm in adults predictive of
separation (EPSS) M mode) septum during the diastolic phase. This measurement is associated with severe LV dysfunction *
LV systolic volume.
LV output (stroke A5C, PLAX Product of VTI measured by pulse wave Doppler at LVOT in A5C and Z-scores available for different
volume) LVOT cross-sectional area measured in PLAX ages and should be used;
neonates: 150–400 ml/kg/min
Mitral annular plane A4C Systolic excursion of lateral (or medial) mitral annulus toward apex to Z-scores available for different
systolic excursion assess LV systolic function. ages and should be used;
(MAPSE) term neonates: > 8 mm (8–11
mm)
Adults 12–14 mm (< 8 mm
predictive of severe LV
dysfunction)
RV output (stroke PSAX or Product of VTI measured by pulsed-wave Doppler at RVOT and RVOT Z-scores available for different
volume) sweep PLAX cross-sectional area ages and should be used;
neonates: 150–400 ml/kg/min
Tricuspid annular plane A4C Systolic excursion of lateral (or medial) tricuspid annulus toward apex to Term neonates: > 8 mm (8–11
systolic excursion assess RV systolic function. mm)
(TAPSE) Children–Z-score available;
generally > 12 mm (12–17 mm)
Adults or grown-up children >
17 mm (17–25 mm)
A4C Apical 4 chamber view, A5C Apical 5 chamber view, A2C Apical 2 chamber view, PSAX parasternal short-axis view, PLAX parasternal long-axis view, M mode
motion mode, LV left ventricle, LVOT left ventricular outflow tract, VTI velocity time integral
*No data are available in neonates or children
11. POCUS may be used to detect vegetations to B. Recommendations for use of lung POCUS
make a diagnosis of endocarditis [however, a 1. POCUS is helpful to distinguish between
definitive diagnosis requires a detailed respiratory distress syndrome (RDS) and
assessment by a paediatric cardiologist or a transient tachypnoea of the neonate
person with advanced echocardiography (TTN)—agreement (quality of evidence B). RDS
training]—disagreement (quality of evidence D). is characterised by a poorly aerated lung with
There was no agreement on using POCUS for the absence of A-lines, presence of small “sub-
the diagnosis of endocarditis. Detecting pleural” consolidations and diffuse white lung
vegetations to make a diagnosis of endocarditis (confluent B-lines). Conversely, in TTN, the
should be done by more expert (paediatric interstitial pattern alternates with areas of near-
cardiologist or by an intensivist with advanced normal lung (with A-lines). Pleural line thicken-
POCUS skills, and not expected to rule out by ing might be seen in late preterm and term ba-
neonatal and paediatric intensivists with bies [53–61]. The double lung point has been
competencies in basic POCUS). However, proposed as a pathognomonic finding [62, 63]
intracardiac masses may be detected on POCUS but it is debated, as it does not seem necessary
examination and should be referred to a for TTN diagnosis if normal lung areas are evi-
paediatric cardiologist or a neonatologist/ dent [64]. High inter-observer agreement be-
paediatric intensivist with advanced tween physicians with different lung ultrasound
echocardiography training [51, 52]. (LUS) expertise has been reported, which makes
the differential diagnosis between RDS and TTN
Semi-quantitative systolic ventricular function mea- reliable, irrespective of the operator [65]. In pre-
sures that may be used in POCUS have been sum- term neonates with RDS, various studies showed
marised in Table 2 [32–45]. that a semiquantitative ultrasound evaluation of
Singh et al. Critical Care (2020) 24:65 Page 7 of 16
lung aeration is very predictive of the need for bronchiolitis are similar to those seen during
surfactant [66, 67] and, therefore, this POCUS influenza outbreaks [87] but it is not currently
tool is helpful to decide about surfactant re- possible to differentiate between different forms
placement and improve its timeliness [68]. of viral respiratory infections.
2. POCUS is helpful to detect pneumonia in 6. POCUS is helpful to accurately detect
neonates and children—agreement (quality of pneumothorax in neonates and children—strong
evidence B). LUS signs of pneumonia are the agreement (quality of evidence B). In adults, LUS
presence of consolidations and dynamic air has a high diagnostic accuracy for the diagnosis
bronchograms, B-lines and pleural effusion. Ab- of pneumothorax [88, 89] and has been reported
normal pleural line and decreased lung sliding to be more sensitive than conventional
may be observed [58, 65]. LUS has been re- radiology [90]. Neonatal data confirm this high
ported to have higher diagnostic accuracy com- diagnostic performance for tension
pared with chest X-rays for the diagnosis of pneumothorax [91].
pneumonia [69]. However, there is no defined 7. POCUS is helpful to insert chest tube or
threshold for consolidation size or a consensual perform needle aspiration in neonatal tension
method of measurement. pneumothorax—strong agreement (quality of
3. POCUS is helpful to semi-quantitatively evalu- evidence B). LUS should not only be used to
ate lung aeration and help the management of diagnose pneumothorax but also to provide
respiratory intervention in acute respiratory dis- static guidance for pleurocentesis [91]. Thus,
tress syndrome (ARDS) in neonates and chil- POCUS should be used to identify lung margin,
dren—agreement (quality of evidence B). LUS in hemidiaphragm and sub-diaphragmatic organs
neonatal and paediatric ARDS shows bilateral throughout the respiratory cycle before needle
diffuse areas of reduced lung aeration with areas or tube insertion to safely avoid them.
of the interstitial syndrome and consolidations, 8. POCUS is helpful to detect pleural effusions in
pleural line abnormalities and pleural effusion neonates and children—strong agreement (quality
[70–73]. Although current diagnostic criteria for of evidence B). Policy statements in adults
ARDS do not yet include LUS, it represents a recommend the use of LUS for the detection of
useful tool for its detection [73, 74]. Several LUS effusions and evaluation of pleural fluid volume to
aeration scores are used to semi-quantitatively guide management [55, 92, 93]. In children, LUS
measure the effect of fluid restriction, alveolar shows high accuracy in the diagnosis of
recruitment and surfactant administration [75– pneumonia-related pleural effusion [47].
79]. Scores based on the main lung ultrasound 9. POCUS is helpful to guide thoracentesis in
semiology (including A lines, alveolar-interstitial neonates and children—strong agreement
pattern and presence of consolidations) should (quality of evidence B). Ultrasound-guided thora-
be preferred over the simple B lines count, as centesis reduces the risk of complications and
they describe better the lung aeration and have increases success rates [55, 92, 93]. It should be
been validated with various techniques [80]. used to identify lung margin, hemidiaphragm
4. POCUS is helpful to recognise meconium and sub-diaphragmatic organs throughout the
aspiration syndrome (MAS)—agreement (quality respiratory cycle before needle or tube insertion
of evidence C). MAS is now recognised as a to safely avoid them.
cause of neonatal ARDS [73] and shares the 10. POCUS is helpful to evaluate lung oedema in
same LUS findings. However, this LUS pattern neonates and children—agreement (quality of
is dynamic and changes with the spread of evidence C). Although LUS is accurate in
meconium plugs during mechanical ventilation detecting extra-vascular lung fluid [94], it can-
[81, 82]. not distinguish between cardiogenic and non-
5. POCUS is helpful for descriptive purposes in cardiogenic oedema [55, 94]. LUS has been used
viral bronchiolitis but cannot provide a in children to evaluate cardiogenic lung oedema,
differential aetiological diagnosis—strong by assessing extravascular lung fluid counting
agreement (quality of evidence C). LUS signs in numbers of B-lines after cardiac surgery [79].
viral bronchiolitis consist of pleural line However, extravascular lung water may obvi-
irregularities, “sub-pleural” consolidations and ously be affected by the pressure delivered dur-
areas with interstitial pattern [83–85]. Good ing mechanical ventilation. Thus, in these
concordance between operators has been shown conditions, LUS globally evaluates the lung aer-
in wheezing infants [86]. LUS findings in viral ation rather than extravascular lung fluid.
Singh et al. Critical Care (2020) 24:65 Page 8 of 16
136] by evaluation of the middle cerebral Abdominal POCUS is widely used as a clinical
(MCA) and basilar artery. The following tool for the management and diagnosis of pa-
patterns are compatible with cerebral tients with abdominal pathology [144–148].
circulatory arrest [126, 136]: (a) oscillating Evaluation of free fluid is particularly useful
waveform or sustained reversal of diastolic flow, when sudden clinical deterioration and
(b) small systolic spikes and disappearance of all hypotension occur and may provide insight into
intra-cranial flow, (c) no flow in MCA, (d) re- the ongoing pathophysiologic process [149,
versal of diastolic flow in extracranial Internal 150].
Carotid Artery (ICA) and (e) mean velocity in 2. POCUS may detect parenchymal changes of
MCA less than 10 cm/s for more than 30 min. abdominal organs in neonates and children
However, interpretation of this assessment must [although for a definite diagnosis a detailed
be done with caution. assessment should be performed by a paediatric
4. POCUS is helpful to detect cerebral blood flow radiologist]—agreement (quality of evidence D).
changes secondary to vasospasm in patients Basic ultrasound knowledge of abdominal organ
with traumatic brain injury and non-traumatic anatomy is essential during POCUS
intracranial bleeding—agreement (quality of evi- examination. Furthermore, a detailed assessment
dence C). Vasospasm of cerebral arteries results should be performed by a paediatric radiologist
in increased flow velocities. The Lindegaard ra- if abnormal abdominal organ structures are
tio (LR) is calculated by dividing mean velocity detected by POCUS [151, 152].
in MCA by mean velocity in ipsilateral extracra- 3. POCUS may detect obstructive uropathy in
nial ICA. As hyperaemia may also increase mean neonates and children [although for a definite
velocities, LR is useful to distinguish between diagnosis a detailed assessment should be
hyperaemia and vasospasm (3:6 ratio is consid- performed by a paediatric
ered a sign of mild vasospasm, and > 6 a sign of radiologist]—agreement (quality of evidence D).
severe vasospasm) [136]. A renal ultrasound is useful to easily detect the
5. POCUS is helpful to detect changes in optic presence of hydronephrosis even by novices
nerve sheath diameter (ONSD) indicative of [152–154]. Urinary retention can be evaluated
raised ICP in children with fused skull by POCUS assessing postvoid residual volumes.
bones—agreement (quality of evidence B). In the case of anuria, a simple obstruction
Measurement of the ONSD is suggestive of requiring a urinary catheter placement can be
papilledema and increased ICP [137, 138]; ruled out.
however, data conflict on threshold 4. POCUS may assess bowel peristalsis in neonates
measurements [137–140] and papilledema may and children—agreement (quality of evidence D).
persist despite normalisation of intracranial Bowel POCUS may be used to assess peristalsis
pressure. Therefore, it must be reminded that [155] but insufficient data yet exist correlating
this technique may have relevant measurement peristalsis with feeding tolerance. However, the
errors because of the narrow margins that presence of peristalsis has strong negative
distinguish pathological from normal. predictive value in adults for ileus and gut
6. POCUS is helpful to detect cerebral midline ischemia in adults [156].
shift (MLS) in neonates and 5. POCUS may recognise hypertrophic pyloric
children—agreement (quality of evidence C). stenosis [although for a definitive diagnosis a
Measurement of the distance from both detailed assessment should be performed by a
temporal bones to the centre of the third paediatric radiologist]—disagreement (quality of
ventricle through the temporal acoustic window evidence D )[157]
determines the presence of MLS [141, 142]. 6. POCUS may guide peritoneal drainage or
Minimal shifts (less than 5 mm) in adults have aspiration of peritoneal fluid in neonates and
proven to identify abnormal conditions [143]. children—strong agreement (quality of evidence
Yet, normative values for MLS identification in D). A paracentesis may be required for either
children have not been reported, and this may diagnostic or therapeutic purposes. POCUS
reduce the helpfulness of this application. should be used for pre-procedural planning,
E. Recommendations for abdominal POCUS identification of epigastric vessels and real-time
1. POCUS is helpful for the detection of free intra- ultrasonographic guidance. In adult studies, the
abdominal fluid in neonates and children—- use of ultrasound has been shown to decrease
strong agreement (quality of evidence C). both bleeding complications and the overall cost
Singh et al. Critical Care (2020) 24:65 Page 10 of 16
of care for patients undergoing in-hospital para- patient population and specialty. Even within a unit,
centesis [158]. practice varies among clinicians and their expertise. We
7. POCUS is helpful to detect signs of necrotizing subdivided POCUS recommendations according to the
enterocolitis (NEC) [although for a definitive estimated level of training required for their use (Fig. 2),
diagnosis a detailed assessment should be and this may be helpful for their implementation.
performed by a paediatric radiologist or a person Defining a scope of practice is fundamental for
with specific advanced ultrasound POCUS, and these ESPNIC guidelines have been devel-
training]—agreement (quality of evidence C). oped for the targeted use of ultrasound in NICU and
Ultrasound may be a useful adjunct detecting PICU by any neonatologist or paediatric intensivist. For
changes consistent with NEC even when most diagnostic (heart, lungs, brain and abdomen) and
radiographs are inconclusive [159, 160]. procedural (line placement and fluid drainage) POCUS
Furthermore, radiographs have poor sensitivity in applications, these guidelines can be used at all ages in
the diagnosis of NEC [161, 162]. POCUS can children or neonates. However, while using cardiac
provide prognostic value identifying free fluid, POCUS in neonates, clinicians should be aware that un-
bowel wall thickness, pneumatosis intestinalis, diagnosed critical congenital heart defects can present
portal venous gas and vascular perfusion [159, just during this period. They should acknowledge the
163–166]. The International Neonatal limitations of skills, and it should not be used as a
Consortium’s NEC subgroup recently revisited screening tool for diagnosing or excluding congenital
the necrotizing enterocolitis (NEC) pathogenesis heart defects. A patient with a suspected critical con-
and new diagnostic criteria were proposed [167]. genital heart defect should be quickly referred to a
These were based on the so-called ‘two out of paediatric cardiologist, even if this implies out-of-
three’ model which includes pneumatosis intesti- hospital patient’s transportation. However, in cases of
nalis or portal venous gas by abdominal X-rays suspicion of a non-critical defect or for patients with low
and/or POCUS. POCUS was included since vari- pre-test probability a more expectative management can
ous studies demonstrated that it outperformed be provided. Moreover, the use of pulse-oximetry
conventional radiology to this end [159]. screening for congenital heart defects is useful and
should be integrated into the clinical decision-making
Discussion process, as internationally recommended [168, 169].
POCUS is increasingly being utilised in neonatal and These guidelines may help in standardising clinical
paediatric critical care as a valuable adjunct to clinical practice across acute care settings and physicians. It is
examination. The use of POCUS by the clinician is dif- not meant to be prescriptive, but rather to outline the
ferent than a complete diagnostic study by the specialist
and its role is dynamic—the same provider can perform
and interpret the study, rapidly integrate this informa-
tion within the current clinical setting, and then repeat
the study to identify changes associated with the inter-
vention. POCUS involves a focused assessment to an-
swer a specific question, and it provides anatomical and/
or physiological information to be integrated with clin-
ical and laboratory data and make timely and accurate
decisions possible. The statements on which panellists
disagreed concerned two particular indications (endocar-
ditis and hypertrophic pyloric stenosis), whose diagnosis
should be done by a detailed ultrasonography in the
hands of an expert paediatric cardiologist or radiologist.
The role of POCUS (i.e., point-of-care ultrasound per-
formed directly by neonatal/paediatric intensivists at the
bedside) for these indications is not clear, while the role
of ultrasound, in general, is indeed important.
There remains a significant variation in clinical prac-
tice—in indications, training program and clinical gov-
ernance. The application of POCUS in clinical practice Fig. 2 Estimated level of training required for the implementation of
POCUS recommendations. Recommendations are listed according to
is dependent on many factors including availability of
their progressive number for each section
ultrasound machines, providers, hospital setting, local
Singh et al. Critical Care (2020) 24:65 Page 11 of 16
important features of structured POCUS applications in and methods of POCUS training should be a sensible
clinical practice. The use of these guidelines often will follow-up article to this one.
not have any cost implication for the equipment, as
ultrasound machine is almost always available in most Conclusions
neonatal and paediatric intensive care units. ESPNIC will Despite the lack of published evidence-based guidelines
promote the diffusion of these guidelines by appropriate specifically for its use in the neonatal and paediatric inten-
advertisement, links and presentation in the society con- sive care units, POCUS is increasingly being used. ESPNIC
gresses and training events. POCUS guidelines provide the substrate to optimise
These guidelines have strengths and limitations as any POCUS use in neonatal and paediatric critical care and
other. Strengths are represented by (1) the fairly subdi- guide future research steps according to currently unmet
vided multidisciplinary panellists’ group (including both needs. Guidelines may help in making the clinical practice
neonatologists and paediatric intensivists, expert in dif- standardised and clinical governance robust.
ferent POCUS areas and coming from different geo-
graphical regions), and (2) the use of a standardised Supplementary information
methodology. In several fields, these recommendations Supplementary information accompanies this paper at https://doi.org/10.
1186/s13054-020-2787-9.
are based upon a few studies with moderate/low evi-
dence or based upon experts’ opinions and this is a Additional file 1. Online supplementary material.
striking difference compared to similar guidelines in
adult critical care. In fact, authors answered to following Abbeviations
PICO questions: “Does point-of-care ultrasound for A4C: Apical 4-chamber; ARDS: Acute respiratory distress syndrome;
heart/lung/line placement/abdomen/brain provide any CPU: Clinician performed ultrasound; EF: Ejection fraction; ESPNIC: European
Society of Paediatric and Neonatal Intensive Care; FS: Fraction shortening;
clinical advantage in neonatal or paediatric intensive ICP: Intracranial pressure; IJV: Internal jugular vein; IVC: Inferior vena-cava;
care practice?” (supplementary methods). These ques- IVH: Intraventricular haemorrhage; LR: Lindegaard ratio; LUS: Lung ultrasound;
tions were purposely quite general, as POCUS is not a LVOT: Left ventricular outflow tract; MAS: Meconium aspiration syndrome;
MCA: Middle cerebral artery; MLS: Cerebral midline shift; NEC: Necrotizing
therapeutic intervention, but rather a diagnostic and enterocolitis; NICU: Neonatal intensive care unit; NPE: Neonatologist
monitoring technique and we expected few randomised performed echocardiography; ONSD: Optic nerve sheath diameter;
controlled trials or high-quality diagnostic accuracy PASP: Pulmonary artery systolic pressure; PI: Pulsatility index;
PICC: Peripherally inserted central catheters; PICU: Pediatric intensive care
studies about POCUS specifically aiming to improve any unit; PLAX: Parasternal long; POCUS: Point of care ultrasound; PSAX: Short
particular paediatric/neonatal outcome. Moreover, some axis; RDS: Respiratory distress syndrome; RI: Resistance index; TTN: Transient
of the POCUS applications may not be immediately used tachypnoea of the neonate; VTIs: Variation of velocity-time integrals
in all intensive care units as in ours, because of the spe- Acknowledgements
cific expertise required in some particular contexts (such Not applicable
as the extremely preterm neonates or non-sedated and
Authors’ contributions
non-collaborative patients). However, the existence of YS, CT and DDL conceptualised and designed the development of the
formal guidelines may help to improve the local expert- whole project. YS and CT wrote the first manuscript draft. DDL took care of
ise and foster new studies to expand knowledge in this the whole methodology and supervised the whole project. All authors
performed literature search and analysis, interpreted the literature data with
field and refine future recommendations. This is ex- their specific expertise, participate in meetings discussions and voted on
tremely important as further studies are warranted to recommendations and manuscript preparation. Moreover, all authors
demonstrate that POCUS actually improves patients’ critically reviewed the manuscript for important intellectual content,
approved it in its final version and agreed to be accountable for all aspects
management and outcome, similar to what has been of the work. The participation to the project did not entail any honorarium.
demonstrated in adult critical care [1–7, 55]. Another All authors read and approved the final manuscript.
concern is that the clinicians involved are all enthusiastic
Funding
users of POCUS and this may have theoretically contrib-
This project has no funding. ESPNIC provided technical and secretarial
uted to have ‘too positive’ recommendations. The ESP- assistance for free.
NIC POCUS Working Group recognises that there are
emerging indications for POCUS outside of those listed Availability of data and materials
Data sharing is not applicable to this article as no datasets were generated
here and needs for future research steps. Publication of or analysed during the current study.
new literature may require future revision and ESPNIC
POCUS Working Group is willing to update guidelines Ethics approval and consent to participate
Not applicable.
accordingly every 3 years.
These guidelines may provide a substrate to develop a Consent for publication
POCUS curriculum and structured training programs, Not applicable.
which are urgently needed for quality assurance. This Competing interests
guideline paper is not a training statement: requirements The authors declare that they have no competing interests.
Singh et al. Critical Care (2020) 24:65 Page 12 of 16
Author details 11. Australasian Society for Ultrasound Medicine. Proficiency & Appropriate Use
1
Department of Paediatrics - Neonatology and Paediatric Cardiology, Statement [Internet]. Available from: https://www.asum.com.au/files/public/
Cambridge University Hospitals and University of Cambridge School of SoP/Current/Paediatrics_and_Neo-Natal/Proficiency-and-Appropriate-Use-
Clinical Medicine, Biomedical Campus, Hills Road, Cambridge CB2 0QQ, UK. Statement-for-Neonatal-Ultrasound-G1.pdf.
2
Addenbrooke’s Hospital, Box 402, Cambridge, UK. 3Paediatric Cardiology, 12. Kneyber MCJ, de Luca D, Calderini E, Jarreau P-H, Javouhey E, Lopez-Herce
Centre de Pédiatrie, Clinique des Grangettes, Geneva, Switzerland. J, et al. Recommendations for mechanical ventilation of critically ill children
4
Department of Paediatrics, Children’s Hospital of Philadelphia and Perelman from the Paediatric Mechanical Ventilation Consensus Conference
School of Medicine, Philadelphia, USA. 5Division of Paediatrics and Neonatal (PEMVECC). Intensive Care Med. 2017;43:1764–80.
Critical Care, APHP - Paris Saclay University Hospitals, “A. Béclère” Medical 13. Brouwers MC, Kerkvliet K, Spithoff K, AGREE Next Steps Consortium. The
centre, Paris, France. 6Department of Paediatric Intensive Care, Gregorio AGREE Reporting Checklist: a tool to improve reporting of clinical practice
Marañón General University Hospital, Madrid, Spain. 7Department of guidelines. BMJ. 2016;352:i1152.
Paediatric Cardiology, Sant Joan de Déu Hospital, Barcelona, Spain. 14. Singh Y. Echocardiographic evaluation of hemodynamics in neonates and
8
Department of Paediatric Intensive Care, Great Ormond Street Hospital, children. Front Pediatr. 2017;5:201.
London, UK. 9Department of Paediatric Intensive Care, Hospital Universitario 15. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, et al.
Central de Asturias, Oviedo. CIBER-Enfermedades Respiratorias. Instituto de Recommendations for chamber quantification: a report from the American
Salud Carlos III, Madrid. Instituto de Investigación Sanitaria del Principado de Society of Echocardiography’s guidelines and standards committee and the
Asturias, Oviedo, Spain. 10Department of Paediatric Intensive Care, chamber quantification writing group, developed in conjunction with the
Nottingham University Hospitals, Nottingham, UK. 11Department of Paediatric European Association of Echocardiography, a branch of the European
and Cardiac Intensive Care, Children’s Hospital Colorado, Aurora, USA. Society of Cardiology. J Am Soc Echocardiogr. 2005;18:1440–63.
12
Division of Paediatric Critical Care, APHP - Paris Saclay University Hospitals, 16. Feissel M, Michard F, Faller J-P, Teboul J-L. The respiratory variation in
“Kremlin Bicetre” Medical Centre, Paris, France. 13Department of Paediatric inferior vena cava diameter as a guide to fluid therapy. Intensive Care Med.
Anaesthesia and Intensive Care, Children’s Hospital Banska Bystrica, Banska 2004;30:1834–7.
Bystrica, Slovakia. 14Department of Paediatrics, Medicins Sans Frontieres 17. Barbier C, Loubières Y, Schmit C, Hayon J, Ricôme J-L, Jardin F, et al.
(Suisse), Geneva, Switzerland. 15Department of Anaesthesiology and Critical Respiratory changes in inferior vena cava diameter are helpful in predicting
Care Medicine, Children’s Hospital of Philadelphia and Perelman School of fluid responsiveness in ventilated septic patients. Intensive Care Med. 2004;
Medicine, Philadelphia, USA. 16Department of Paediatrics, Division of 30:1740–6.
Paediatric Critical Care Medicine, Beatrix Children’s Hospital Groningen, 18. Levitov A, Marik PE. Echocardiographic assessment of preload
University Medical Center Groningen, Groningen, The Netherlands. responsiveness in critically ill patients. Cardiol Res Pract. 2012;2012:819696.
17
Physiopathology and Therapeutic Innovation Unit–INSERM Unit U999, 19. Lin EE, Chen AE, Panebianco N, Conlon T, Ju NR, Carlson D, et al. Effect of
South Paris Medical School, Paris Saclay University, Paris, France. inhalational anesthetics and positive-pressure ventilation on ultrasound
assessment of the great vessels: a prospective study at a children’s hospital.
Received: 9 December 2019 Accepted: 14 February 2020 Anesthesiology. 2016;124:870–7.
20. Via G, Tavazzi G, Price S. Ten situations where inferior vena cava ultrasound
may fail to accurately predict fluid responsiveness: a physiologically based
point of view. Intensive Care Med. 2016;42:1164–7.
References 21. Slama M, Masson H, Teboul J-L, Arnout M-L, Susic D, Frohlich E, et al.
1. On behalf of The Canadian Internal Medicine Ultrasound (CIMUS) Group*, Respiratory variations of aortic VTI: a new index of hypovolemia and fluid
Ma IWY, Arishenkoff S, Wiseman J, Desy J, Ailon J, et al. Internal Medicine responsiveness. Am J Physiol Heart Circ Physiol. 2002;283:H1729–33.
Point-of-Care Ultrasound Curriculum: Consensus Recommendations from 22. Feissel M, Michard F, Mangin I, Ruyer O, Faller JP, Teboul JL. Respiratory
the Canadian Internal Medicine Ultrasound (CIMUS) Group. J Gen Intern changes in aortic blood velocity as an indicator of fluid responsiveness in
Med. 2017;32:1052–7. ventilated patients with septic shock. Chest. 2001;119:867–73.
2. Expert Round Table on Ultrasound in ICU. International expert statement on 23. Bates S, Odd D, Luyt K, Mannix P, Wach R, Evans D, et al. Superior vena cava
training standards for critical care ultrasonography. Intensive Care Med. flow and intraventricular haemorrhage in extremely preterm infants. J
2011;37:1077–83. Matern Fetal Neonatal Med. 2016;29:1581–7.
3. Frankel HL, Kirkpatrick AW, Elbarbary M, Blaivas M, Desai H, Evans D, et al. 24. Kluckow M, Evans N. Superior vena cava flow in newborn infants: a novel
Guidelines for the appropriate use of bedside general and cardiac marker of systemic blood flow. Arch Dis Child Fetal Neonatal Ed. 2000;82:
ultrasonography in the evaluation of critically ill patients—part I: general F182–7.
ultrasonography. Crit Care Med. 2015;43:2479–502. 25. Lee A, Liestøl K, Nestaas E, Brunvand L, Lindemann R, Fugelseth D. Superior
4. Moore CL, Copel JA. Point-of-care ultrasonography. N Engl J Med. 2011;364: vena cava flow: feasibility and reliability of the off-line analyses. Arch Dis
749–57. Child Fetal Neonatal Ed. 2010;95:F121–5.
5. Evans N, Gournay V, Cabanas F, Kluckow M, Leone T, Groves A, et al. Point- 26. Groves AM, Kuschel CA, Knight DB, Skinner JR. Echocardiographic
of-care ultrasound in the neonatal intensive care unit: international assessment of blood flow volume in the superior vena cava and
perspectives. Semin Fetal Neonatal Med. 2011;16:61–8. descending aorta in the newborn infant. Arch Dis Child Fetal Neonatal Ed.
6. Longjohn M, Wan J, Joshi V, Pershad J. Point-of-care echocardiography by 2008;93:F24–8.
pediatric emergency physicians. Pediatr Emerg Care. 2011;27:693–6. 27. Ficial B, Bonafiglia E, Padovani EM, Prioli MA, Finnemore AE, Cox DJ, et al. A
7. Vignon P, Dugard A, Abraham J, Belcour D, Gondran G, Pepino F, et al. modified echocardiographic approach improves reliability of superior vena
Focused training for goal-oriented hand-held echocardiography performed caval flow quantification. Arch Dis Child Fetal Neonatal Ed. 2017;102:F7–11.
by noncardiologist residents in the intensive care unit. Intensive Care Med. 28. Pereira de Souza Neto E, Grousson S, Duflo F, Ducreux C, Joly H, Convert J,
2007;33:1795–9. et al. Predicting fluid responsiveness in mechanically ventilated children
8. Mertens L, Seri I, Marek J, Arlettaz R, Barker P, McNamara P, et al. Targeted under general anaesthesia using dynamic parameters and transthoracic
neonatal echocardiography in the neonatal intensive care unit: practice echocardiography. Br J Anaesth. 2011;106:856–64.
guidelines and recommendations for training. J Am Soc Echocardiogr. 2011; 29. Renner J, Broch O, Duetschke P, Scheewe J, Höcker J, Moseby M, et al.
24:1057–78. Prediction of fluid responsiveness in infants and neonates undergoing
9. Singh Y, Gupta S, Groves AM, Gandhi A, Thomson J, Qureshi S, et al. Expert congenital heart surgery. Br J Anaesth. 2012;108:108–15.
consensus statement ‘neonatologist-performed echocardiography 30. Choi DY, Kwak HJ, Park HY, Kim YB, Choi CH, Lee JY. Respiratory variation in
(NoPE)’—training and accreditation in UK. Eur J Pediatr. 2016;175:281–7. aortic blood flow velocity as a predictor of fluid responsiveness in children
10. de Boode WP, Singh Y, Gupta S, Austin T, Bohlin K, Dempsey E, et al. after repair of ventricular septal defect. Pediatr Cardiol. 2010;31:1166–70.
Recommendations for neonatologist performed echocardiography in 31. Ficial B, Finnemore AE, Cox DJ, Broadhouse KM, Price AN, Durighel G, et al.
Europe: consensus statement endorsed by European Society for Paediatric Validation study of the accuracy of echocardiographic measurements of
Research (ESPR) and European Society for Neonatology (ESN). Pediatr Res. systemic blood flow volume in newborn infants. J Am Soc Echocardiogr.
2016;80:465–71. 2013;26:1365–71.
Singh et al. Critical Care (2020) 24:65 Page 13 of 16
32. Jain A, Mohamed A, El-Khuffash A, Connelly KA, Dallaire F, Jankov RP, et al. 53. Escourrou G, De Luca D. Lung ultrasound decreased radiation exposure in
A comprehensive echocardiographic protocol for assessing neonatal right preterm infants in a neonatal intensive care unit. Acta Paediatr. 2016;105:
ventricular dimensions and function in the transitional period: normative e237–9.
data and z scores. J Am Soc Echocardiogr. 2014;27:1293–304. 54. Cattarossi L, Copetti R, Poskurica B. Radiation exposure early in life can be
33. McKaigney CJ, Krantz MJ, La Rocque CL, Hurst ND, Buchanan MS, Kendall JL. reduced by lung ultrasound. Chest. 2011;139:730–1.
E-point septal separation: a bedside tool for emergency physician 55. International Liaison Committee on Lung Ultrasound (ILC-LUS) for the
assessment of left ventricular ejection fraction. Am J Emerg Med. 2014;32: International Consensus Conference on Lung Ultrasound (ICC-LUS),
493–7. Volpicelli G, Elbarbary M, Blaivas M, Lichtenstein DA, Mathis G, et al.
34. Matzer L, Cortada X, Ferrer P, De Armendi F, Kinney EL. Widened E point International evidence-based recommendations for point-of-care lung
septal separation in a normal pediatric population. Chest. 1985;87:73–5. ultrasound. Intensive Care Med. 2012;38:577–91.
35. Engle SJ, DiSessa TG, Perloff JK, Isabel-Jones J, Leighton J, Gross K, et al. 56. Liu J, Wang Y, Fu W, Yang C-S, Huang J-J. Diagnosis of Neonatal Transient
Mitral valve E point to ventricular septal separation in infants and children. Tachypnea and Its Differentiation From Respiratory Distress Syndrome Using
Am J Cardiol. 1983;52:1084–7. Lung Ultrasound. Medicine. 2014;93:e197.
36. D’Cruz IA, Lalmalani GG, Sambasivan V, Cohen HC, Glick G. The superiority 57. Liu J, Chen X-X, Li X-W, Chen S-W, Wang Y, Fu W. Lung ultrasonography to
of mitral E point-ventricular septum separation to other echocardiographic diagnose transient tachypnea of the newborn. Chest. 2016;149:1269–75.
indicators of left ventricular performance. Clin Cardiol. 1979;2:140–5. 58. Chen S-W, Fu W, Liu J, Wang Y. Routine application of lung ultrasonography
37. Lew W, Henning H, Schelbert H, Karliner JS. Assessment of mitral valve E in the neonatal intensive care unit. Medicine. 2017;96:e5826.
point-septal separation as an index of left ventricular performance in 59. Sawires HK, Abdel Ghany EA, Hussein NF, Seif HM. Use of lung ultrasound in
patients with acute and previous myocardial infarction. Am J Cardiol. 1978; detection of complications of respiratory distress syndrome. Ultrasound
41:836–45. Med Biol. 2015;41:2319–25.
38. Favia I, Romagnoli S, Di Chiara L, Ricci Z. Predicting fluid responsiveness in 60. Copetti R, Cattarossi L, Macagno F, Violino M, Furlan R. Lung ultrasound in
children undergoing cardiac surgery after cardiopulmonary bypass. Pediatr respiratory distress syndrome: a useful tool for early diagnosis. Neonatology.
Cardiol. 2017;38:787–93. 2008;94:52–9.
39. Pees C, Glagau E, Hauser J, Michel-Behnke I. Reference values of aortic flow 61. Vergine M, Copetti R, Brusa G, Cattarossi L. Lung ultrasound accuracy in
velocity integral in 1193 healthy infants, children, and adolescents to quickly respiratory distress syndrome and transient tachypnea of the newborn.
estimate cardiac stroke volume. Pediatr Cardiol. 2013;34:1194–200. Neonatology. 2014;106:87–93.
40. Hashimoto I, Watanabe K. Z-score of mitral annular plane systolic excursion 62. Copetti R, Cattarossi L. The ‘double lung point’: an ultrasound sign
is a useful Indicator of evaluation of left ventricular function in patients with diagnostic of transient tachypnea of the newborn. Neonatology. 2007;91:
acute-phase Kawasaki disease. Pediatr Cardiol. 2017;38:1057–64. 203–9.
41. Terada T, Mori K, Inoue M, Yasunobu H. Mitral annular plane systolic 63. Raimondi F, Migliaro F, De Luca D, Yousef N, Rodriguez FJ. Clinical Data Are
excursion/left ventricular length (MAPSE/L) as a simple index for assessing Essential to Validate Lung Ultrasound. Chest. 2016;149:1575.
left ventricular longitudinal function in children. Echocardiography. 2016;33: 64. Raimondi F, Yousef N, Rodriguez Fanjul J, De Luca D, Corsini I, Shankar-
1703–9. Aguilera S, et al. A multicenter lung ultrasound study on transient
42. Koestenberger M, Ravekes W, Avian A, Grangl G, Burmas A, Raith W, et al. tachypnea of the neonate. Neonatology. 2019;115:263–8.
Right ventricular outflow tract (RVOT) changes in children with an atrial 65. Brusa G, Savoia M, Vergine M, Bon A, Copetti R, Cattarossi L. Neonatal
septal defect: focus on RVOT velocity time integral, RVOT diameter, and lung sonography: interobserver agreement between physician
RVOT systolic excursion. Echocardiography. 2016;33:1389–96. interpreters with varying levels of experience. J Ultrasound Med. 2015;
43. McLaughlin ES, Travers C, Border WL, Deshpande S, Sachdeva R. Tricuspid 34:1549–54.
annular plane systolic excursion as a marker of right ventricular dysfunction 66. Razak A, Faden M. Neonatal lung ultrasonography to evaluate need for
in pediatric patients with dilated cardiomyopathy. Echocardiography. 2017; surfactant or mechanical ventilation: a systematic review and meta-analysis.
34:102–7. Arch Dis Child Fetal Neonatal Ed. 2019. https://doi.org/10.1136/archdischild-
44. Goldberg DJ, French B, Szwast AL, McBride MG, Paridon SM, Rychik J, et al. 2019-316832. [Epub ahead of print]
Tricuspid annular plane systolic excursion correlates with exercise capacity 67. De Martino L, Yousef N, Ben-Ammar R, Raimondi F, Shankar-Aguilera S, De
in a cohort of patients with hypoplastic left heart syndrome after Fontan Luca D. Lung ultrasound score predicts surfactant need in extremely
operation. Echocardiography. 2016;33:1897–902. preterm neonates. Pediatrics. 2018;142(3). https://doi.org/10.1542/peds.2018-
45. Koestenberger M, Nagel B, Ravekes W, Avian A, Heinzl B, Cvirn G, et al. 0463. Epub 2018 Aug 14.
Reference values of tricuspid annular peak systolic velocity in healthy 68. Raschetti R, Yousef N, Vigo G, Marseglia G, Centorrino R, Ben-Ammar R,
pediatric patients, calculation of z score, and comparison to tricuspid et al. Echography-guided surfactant therapy to improve timeliness of
annular plane systolic excursion. Am J Cardiol. 2012;109:116–21. surfactant replacement: a quality improvement project. J Pediatr. 2019;
46. Nagdev A, Stone MB. Point-of-care ultrasound evaluation of pericardial 212:137–43 e1.
effusions: does this patient have cardiac tamponade? Resuscitation. 2011;82: 69. Pereda MA, Chavez MA, Hooper-Miele CC, Gilman RH, Steinhoff MC,
671–3. Ellington LE, et al. Lung ultrasound for the diagnosis of pneumonia in
47. Raimondi F, Yousef N, Migliaro F, Capasso L, De Luca D. Point-of-care lung children: a meta-analysis. Pediatrics. 2015;135:714–22.
ultrasound in neonatology: classification into descriptive and functional 70. Acute Respiratory Distress Syndrome. The Berlin Definition. JAMA. 2012;307
applications. Pediatr Res. 2018; [cited 2019 Jan 14]; Available from: http:// [cited 2019 Jan 15]. Available from: http://jama.jamanetwork.com/article.
www.nature.com/articles/s41390-018-0114-9. aspx?doi=10.1001/jama.2012.5669.
48. Tsang TS, Freeman WK, Sinak LJ, Seward JB. Echocardiographically guided 71. On behalf of Respiratory Section of the European Society for Pediatric
pericardiocentesis: evolution and state-of-the-art technique. Mayo Clin Proc. Neonatal Intensive Care (ESPNIC), De Luca D, Piastra M, Chidini G, Tissieres
1998;73:647–52. P, Calderini E, et al. The use of the Berlin definition for acute respiratory
49. Nagdev A, Mantuani D. A novel in-plane technique for ultrasound-guided distress syndrome during infancy and early childhood: multicenter
pericardiocentesis. Am J Emerg Med. 2013;31:1424 e5–9. evaluation and expert consensus. Intensive Care Med. 2013;39:2083–91.
50. Spurney CF, Sable CA, Berger JT, Martin GR. Use of a hand-carried 72. Khemani RG, Smith LS, Zimmerman JJ, Erickson S. Pediatric acute respiratory
ultrasound device by critical care physicians for the diagnosis of pericardial distress syndrome: definition, incidence, and epidemiology. Pediatr Crit Care
effusions, decreased cardiac function, and left ventricular enlargement in Med. 2015;16:S23–40.
pediatric patients. J Am Soc Echocardiogr. 2005;18:313–9. 73. De Luca D, van Kaam AH, Tingay DG, Courtney SE, Danhaive O, Carnielli VP,
51. Gaspar HA, Morhy SS, Lianza AC, de Carvalho WB, Andrade JL, do Prado RR, et al. The Montreux definition of neonatal ARDS: biological and clinical
et al. Focused cardiac ultrasound: a training course for pediatric intensivists background behind the description of a new entity. Lancet Respir Med.
and emergency physicians. BMC Med Educ. 2014;14:25. 2017;5:657–66.
52. Pershad J, Myers S, Plouman C, Rosson C, Elam K, Wan J, et al. Bedside 74. De Luca D, van Kaam AH, Tingay DG, Courtney SE, Danhaive O, Carnielli VP,
limited echocardiography by the emergency physician is accurate during et al. Lung ultrasound and neonatal ARDS: is Montreux closer to Berlin than
evaluation of the critically ill patient. Pediatrics. 2004;114:e667–71. to Kigali? – authors’ reply. Lancet Respir Med. 2017;5:e32.
Singh et al. Critical Care (2020) 24:65 Page 14 of 16
75. Brat R, Yousef N, Klifa R, Reynaud S, Shankar Aguilera S, De Luca D. Lung 96. de Souza TH, Brandão MB, Santos TM, Pereira RM, Nogueira RJN. Ultrasound
ultrasonography score to evaluate oxygenation and surfactant need in guidance for internal jugular vein cannulation in PICU: a randomised
neonates treated with continuous positive airway pressure. JAMA Pediatr. controlled trial. Arch Dis Child. 2018;103:952–6.
2015;169:e151797. 97. Zanolla GR, Baldisserotto M, Piva J. How useful is ultrasound guidance for
76. Bouhemad B, Brisson H, Le-Guen M, Arbelot C, Lu Q, Rouby J-J. Bedside internal jugular venous access in children? J Pediatr Surg. 2018;53:789–93.
ultrasound assessment of positive end-expiratory pressure–induced lung 98. Verghese ST, McGill WA, Patel RI, Sell JE, Midgley FM, Ruttimann UE.
recruitment. Am J Respir Crit Care Med. 2011;183:341–7. Comparison of three techniques for internal jugular vein cannulation in
77. CAR’Echo Collaborative Network, AzuRea Collaborative Network, Haddam M, infants. Paediatr Anaesth. 2000;10:505–11.
Zieleskiewicz L, Perbet S, Baldovini A, et al. Lung ultrasonography for 99. Verghese ST, McGill WA, Patel RI, Sell JE, Midgley FM, Ruttimann UE.
assessment of oxygenation response to prone position ventilation in ARDS. Ultrasound-guided internal jugular venous cannulation in infants: a
Intensive Care Med. 2016;42:1546–56. prospective comparison with the traditional palpation method.
78. Mongodi S, Bouhemad B, Orlando A, Stella A, Tavazzi G, Via G, et al. Anesthesiology. 1999;91:71–7.
Modified lung ultrasound score for assessing and monitoring pulmonary 100. de Souza TH, Brandão MB, Nadal JAH, Nogueira RJN. Ultrasound guidance
aeration. Ultraschall Med. 2017;38:530–7. for pediatric central venous catheterization: a meta-analysis. Pediatrics. 2018;
79. Kaskinen AK, Martelius L, Kirjavainen T, Rautiainen P, Andersson S, Pitkänen 142.
OM. Assessment of extravascular lung water by ultrasound after congenital 101. Brass P, Hellmich M, Kolodziej L, Schick G, Smith AF. Ultrasound guidance
cardiac surgery: lung ultrasound after congenital cardiac surgery. Pediatr versus anatomical landmarks for subclavian or femoral vein catheterization.
Pulmonol. 2017;52:345–52. Cochrane Database Syst Rev. 2015;1:CD011447.
80. De Luca D. Semi-quantititative lung ultrasound scores are accurate and 102. Oulego-Erroz I, González-Cortes R, García-Soler P, Balaguer-Gargallo M, Frías-
useful and in critical care, irrespective of patients’ age: the power of data Pérez M, Mayordomo-Colunga J, et al. Ultrasound-guided or landmark
over opinions. J Ultrasound Med. 2020. techniques for central venous catheter placement in critically ill children.
81. Liu J, Cao H-Y, Fu W. Lung ultrasonography to diagnose meconium Intensive Care Med. 2018;44:61–72.
aspiration syndrome of the newborn. J Int Med Res. 2016;44:1534–42. 103. Hosokawa K, Shime N, Oulego-Erroz I, González-Cortes R, Rodríguez-Núñez
82. Piastra M, Yousef N, Brat R, Manzoni P, Mokhtari M, De Luca D. Lung A. Ultrasound-guided central venous catheter placement in children: what
ultrasound findings in meconium aspiration syndrome. Early Hum Dev. is a really good practice? Intensive Care Med. 2018;44:546–7.
2014;90:S41–3. 104. Montes-Tapia F, Rodríguez-Taméz A, Cura-Esquivel I, Barreto-Arroyo I,
83. Caiulo VA, Gargani L, Caiulo S, Fisicaro A, Moramarco F, Latini G, et al. Lung Hernández-Garduño A, Rodríguez-Balderrama I, et al. Efficacy and safety of
ultrasound in bronchiolitis: comparison with chest X-ray. Eur J Pediatr. 2011; ultrasound-guided internal jugular vein catheterization in low birth weight
170:1427–33. newborn. J Pediatr Surg. 2016;51:1700–3.
84. Basile V, Di Mauro A, Scalini E, Comes P, Lofù I, Mostert M, et al. Lung 105. Nardi N, Wodey E, Laviolle B, De La Brière F, Delahaye S, Engrand C, et al.
ultrasound: a useful tool in diagnosis and management of bronchiolitis. Effectiveness and complications of ultrasound-guided subclavian vein
BMC Pediatrics. 2015; [cited 2019 Jan 15];15. Available from: http:// cannulation in children and neonates. Anaesth Crit Care Pain Med. 2016;35:
bmcpediatr.biomedcentral.com/articles/10.1186/s12887-015-0380-1. 209–13.
85. Taveira M, Yousef N, Miatello J, Roy C, Claude C, Boutillier B, et al. Un score 106. Breschan C, Graf G, Jost R, Stettner H, Feigl G, Neuwersch S, et al. A
échographique pulmonaire simple peut-il prédire la durée de ventilation retrospective analysis of the clinical effectiveness of supraclavicular,
des nourrissons atteints de bronchiolite aiguë sévère ? Arch Pediatr. 2018; ultrasound-guided brachiocephalic vein cannulations in preterm infants.
25:112–7. Anesthesiology. 2018;128:38–43.
86. Varshney T, Mok E, Shapiro AJ, Li P, Dubrovsky AS. Point-of-care lung 107. Lausten-Thomsen U, Merchaoui Z, Dubois C, Eleni Dit Trolli S, Le Saché N,
ultrasound in young children with respiratory tract infections and wheeze. Mokhtari M, et al. Ultrasound-guided subclavian vein cannulation in low
Emerg Med J. 2016;33:603–10. birth weight neonates. Pediatr Crit Care Med. 2017;18:172–5.
87. Tsung JW, Kessler DO, Shah VP. Prospective application of clinician- 108. Lamperti M, Bodenham AR, Pittiruti M, Blaivas M, Augoustides JG, Elbarbary
performed lung ultrasonography during the 2009 H1N1 influenza a M, et al. International evidence-based recommendations on ultrasound-
pandemic: distinguishing viral from bacterial pneumonia. Crit Ultrasound J. guided vascular access. Intensive Care Med. 2012;38:1105–17.
2012;4:16. 109. Merchaoui Z, Lausten-Thomsen U, Pierre F, Ben Laiba M, Le Saché N,
88. Cattarossi L, Copetti R, Brusa G, Pintaldi S. Lung ultrasound diagnostic Tissieres P. Supraclavicular approach to ultrasound-guided brachiocephalic
accuracy in neonatal pneumothorax. Can Respir J. 2016;2016:1–5. vein cannulation in children and neonates. Front Pediatr. 2017;5:211.
89. Liu J, Chi J-H, Ren X-L, Li J, Chen Y-J, Lu Z-L, et al. Lung ultrasonography to 110. Hind D, Calvert N, McWilliams R, Davidson A, Paisley S, Beverley C, et al.
diagnose pneumothorax of the newborn. Am J Emerg Med. 2017;35:1298– Ultrasonic locating devices for central venous cannulation: meta-analysis.
302. BMJ. 2003;327:361.
90. Alrajab S, Youssef AM, Akkus NI, Caldito G. Pleural ultrasonography versus 111. Pirotte T, Veyckemans F. Ultrasound-guided subclavian vein cannulation in
chest radiography for the diagnosis of pneumothorax: review of the infants and children: a novel approach. Br J Anaesth. 2007;98:509–14.
literature and meta-analysis. Crit Care. 2013;17:R208. 112. Byon H-J, Lee G-W, Lee J-H, Park Y-H, Kim H-S, Kim C-S, et al. Comparison
91. Raimondi F, Rodriguez Fanjul J, Aversa S, Chirico G, Yousef N, De Luca D, between ultrasound-guided supraclavicular and infraclavicular approaches
et al. Lung Ultrasound for Diagnosing Pneumothorax in the Critically Ill for subclavian venous catheterization in children—a randomized trial. Br J
Neonate. J Pediatr. 2016;175:74–8 e1. Anaesth. 2013;111:788–92.
92. Dancel R, Schnobrich D, Puri N, Franco-Sadud R, Cho J, Grikis L, et al. 113. Eldabaa AA, Elgebaly A, Elhafz A, Bassun A. Comparison of ultrasound-
Recommendations on the use of ultrasound guidance for adult guided vs. anatomical landmark-guided cannulation of the femoral vein at
thoracentesis: a position statement of the Society of Hospital Medicine. J the optimum position in infant. South Afr J Anaesth Analg. 2012;18:162–6.
Hosp Med. 2018;13:126–35. 114. Smit JM, Raadsen R, Blans MJ, Petjak M, Van de Ven PM, Tuinman PR.
93. Havelock T, Teoh R, Laws D, Gleeson F, BTS Pleural Disease Guideline Bedside ultrasound to detect central venous catheter misplacement and
Group. Pleural procedures and thoracic ultrasound: British Thoracic associated iatrogenic complications: a systematic review and meta-analysis.
Society Pleural Disease Guideline 2010. Thorax. 2010;65(Suppl 2):ii61– Crit Care. 2018;22:65.
76. 115. Ablordeppey EA, Drewry AM, Beyer AB, Theodoro DL, Fowler SA, Fuller BM,
94. Volpicelli G, Skurzak S, Boero E, Carpinteri G, Tengattini M, Stefanone V, et al. et al. Diagnostic accuracy of central venous catheter confirmation by
Lung ultrasound predicts well extravascular lung water but is of limited bedside ultrasound versus chest radiography in critically ill patients: a
usefulness in the prediction of wedge pressure. Anesthesiology. 2014;121: systematic review and meta-analysis. Crit Care Med. 2017;45:715–24.
320–7. 116. Aouad MT, Kanazi GE, Abdallah FW, Moukaddem FH, Turbay MJ, Obeid MY,
95. Acosta CM, Maidana GA, Jacovitti D, Belaunzarán A, Cereceda S, Rae E, et al. et al. Femoral vein cannulation performed by residents: a comparison
Accuracy of Transthoracic Lung Ultrasound for Diagnosing Anesthesia- between ultrasound-guided and landmark technique in infants and children
induced Atelectasis in Children. Anesthesiology. 2014;120:1370–9. undergoing cardiac surgery. Anesth Analg. 2010;111:724–8.
Singh et al. Critical Care (2020) 24:65 Page 15 of 16
117. Siddik-Sayyid SM, Aouad MT, Ibrahim MH, Taha SK, Nawfal MF, Tfaili YJ, 138. Young AMH, Guilfoyle MR, Donnelly J, Scoffings D, Fernandes H, Garnett M,
et al. Femoral arterial cannulation performed by residents: a et al. Correlating optic nerve sheath diameter with opening intracranial
comparison between ultrasound-guided and palpation technique in pressure in pediatric traumatic brain injury. Pediatr Res. 2017;81:443–7.
infants and children undergoing cardiac surgery. Paediatr Anaesth. 139. Ballantyne J, Hollman AS, Hamilton R, Bradnam MS, Carachi R, Young DG,
2016;26:823–30. et al. Transorbital optic nerve sheath ultrasonography in normal children.
118. Gu W-J, Tie H-T, Liu J-C, Zeng X-T. Efficacy of ultrasound-guided radial artery Clin Radiol. 1999;54:740–2.
catheterization: a systematic review and meta-analysis of randomized 140. Malayeri AA, Bavarian S, Mehdizadeh M. Sonographic evaluation of optic
controlled trials. Crit Care. 2014;18:R93. nerve diameter in children with raised intracranial pressure. J Ultrasound
119. de Carvalho Onofre PS, da Luz Gonçalves Pedreira M, Peterlini MAS. Med. 2005;24:143–7.
Placement of peripherally inserted central catheters in children guided by 141. Motuel J, Biette I, Srairi M, Mrozek S, Kurrek MM, Chaynes P, et al.
ultrasound: a prospective randomized, and controlled trial. Pediatr Crit Care Assessment of brain midline shift using sonography in neurosurgical ICU
Med. 2012;13:e282–7. patients. Crit Care. 2014;18:676.
120. Li Z, Chen L. Comparison of ultrasound-guided modified Seldinger 142. Llompart Pou JA, Abadal Centellas JM, Palmer Sans M, Pérez Bárcena J,
technique versus blind puncture for peripherally inserted central Casares Vivas M, Homar Ramírez J, et al. Monitoring midline shift by
catheter: a meta-analysis of randomized controlled trials. Crit Care. 2015; transcranial color-coded sonography in traumatic brain injury. A
19:64. comparison with cranial computerized tomography. Intensive Care Med.
121. Alonso-Quintela P, Oulego-Erroz I, Rodriguez-Blanco S, Muñiz-Fontan M, 2004;30:1672–5.
Lapeña-López-de Armentia S, Rodriguez-Nuñez A. Location of the central 143. Fernando SM, Tran A, Cheng W, Rochwerg B, Taljaard M, Kyeremanteng K,
venous catheter tip with bedside ultrasound in young children: can we et al. Diagnosis of elevated intracranial pressure in critically ill adults:
eliminate the need for chest radiography? Pediatr Crit Care Med. 2015;16: systematic review and meta-analysis. BMJ. 2019;366:l4225.
e340–5. 144. Scalea TM, Rodriguez A, Chiu WC, Brenneman FD, Fallon WF, Kato K, et al.
122. Simanovsky N, Ofek-Shlomai N, Rozovsky K, Ergaz-Shaltiel Z, Hiller N, Bar-Oz Focused assessment with Sonography for trauma (FAST): results from an
B. Umbilical venous catheter position: evaluation by ultrasound. Eur Radiol. international consensus conference. J Trauma. 1999;46:466–72.
2011;21:1882–6. 145. Rozycki GS, Ochsner MG, Schmidt JA, Frankel HL, Davis TP, Wang D, et al. A
123. Katheria AC, Fleming SE, Kim JH. A randomized controlled trial of prospective study of surgeon-performed ultrasound as the primary adjuvant
ultrasound-guided peripherally inserted central catheters compared with modality for injured patient assessment. J Trauma. 1995;39:492–8 discussion
standard radiograph in neonates. J Perinatol. 2013;33:791–4. 498-500.
124. Nguyen J. Ultrasonography for central catheter placement in the neonatal 146. Dammers D, El Moumni M, Hoogland II, Veeger N, Ter Avest E. Should we
intensive care unit-a review of utility and practicality. Am J Perinatol. 2016; perform a FAST exam in haemodynamically stable patients presenting after
33:525–30. blunt abdominal injury: a retrospective cohort study. Scand J Trauma Resusc
125. Kalanuria A, Nyquist PA, Armonda RA, Razumovsky A. Use of transcranial Emerg Med. 2017;25:1.
Doppler (TCD) ultrasound in the neurocritical care unit. Neurosurg Clin N 147. Tummers W, van Schuppen J, Langeveld H, Wilde J, Banderker E, van As A.
Am. 2013;24:441–56. Role of focused assessment with sonography for trauma as a screening tool
126. Lau VI, Arntfield RT. Point-of-care transcranial Doppler by intensivists. Crit for blunt abdominal trauma in young children after high energy trauma. S
Ultrasound J. 2017;9:21. Afr J Surg. 2016;54:28–34.
127. Purkayastha S, Sorond F. Transcranial Doppler ultrasound: technique and 148. Kameda T, Taniguchi N. Overview of point-of-care abdominal ultrasound in
application. Semin Neurol. 2012;32:411–20. emergency and critical care. J Intensive Care. 2016;4:53.
128. American College of Radiology (ACR), Society for Pediatric Radiology (SPR), 149. McGahan JP, Richards J, Gillen M. The focused abdominal sonography for
Society of Radiologists in Ultrasound (SRU). AIUM practice guideline for the trauma scan: pearls and pitfalls. J Ultrasound Med. 2002;21:789–800.
performance of a transcranial Doppler ultrasound examination for adults 150. Pereira BM, Pereira RG, Wise R, Sugrue G, Zakrison TL, Dorigatti AE, et al. The
and children. J Ultrasound Med. 2012;31:1489–500. role of point-of-care ultrasound in intra-abdominal hypertension
129. Bellner J, Romner B, Reinstrup P, Kristiansson K-A, Ryding E, Brandt L. management. Anestezjologia Intensywna Terapia. 2017;49:373–81.
Transcranial Doppler sonography pulsatility index (PI) reflects intracranial 151. Akgür FM, Aktuğ T, Olguner M, Kovanlikaya A, Hakgüder G. Prospective
pressure (ICP). Surg Neurol. 2004;62:45–51 discussion 51. study investigating routine usage of ultrasonography as the initial
130. Bode H, Wais U. Age dependence of flow velocities in basal cerebral diagnostic modality for the evaluation of children sustaining blunt
arteries. Arch Dis Child. 1988;63:606–11. abdominal trauma. J Trauma. 1997;42:626–8.
131. Rodriguez RA, Cornel G, Alghofaili F, Hutchison J, Nathan HJ. Transcranial 152. Marin JR, Abo AM, Arroyo AC, Doniger SJ, Fischer JW, Rempell R, et al.
Doppler during suspected brain death in children: potential limitation in Pediatric emergency medicine point-of-care ultrasound: summary of the
patients with cardiac “shunt.”. Pediatr Crit Care Med. 2002;3:153–7. evidence. Crit Ultrasound J. 2016;8:16.
132. Vicenzini E, Pulitano P, Cicchetti R, Randi F, Papov P, Spadetta G, et al. 153. Pon MS, Scudamore C, Harrison RC, Cooperberg PL. Ultrasound
Transcranial Doppler for brain death in infants: the role of the fontanelles. demonstration of radiographically obscure small bowel obstruction. AJR Am
Eur Neurol. 2010;63:164–9. J Roentgenol. 1979;133:145–6.
133. Kluckow M, Evans N. Low superior vena cava flow and intraventricular 154. Conlon TW, Himebauch AS, Fitzgerald JC, Chen AE, Dean AJ, Panebianco N,
haemorrhage in preterm infants. Arch Dis Child Fetal Neonatal Ed. 2000;82: et al. Implementation of a pediatric critical care focused bedside ultrasound
F188–94. training program in a large academic PICU. Pediatr Crit Care Med. 2015;16:
134. Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of 219–26.
subependymal and intraventricular hemorrhage: a study of infants with 155. Nylund K, Maconi G, Hollerweger A, Ripolles T, Pallotta N, Higginson A, et al.
birth weights less than 1,500 gm. J Pediatr. 1978;92:529–34. EFSUMB recommendations and guidelines for gastrointestinal ultrasound -
135. Ducrocq X, Hassler W, Moritake K, Newell DW, von Reutern GM, Shiogai T, part 1: examination techniques and normal findings (long version).
et al. Consensus opinion on diagnosis of cerebral circulatory arrest using Ultraschall Med. 2017;38:e1–15.
Doppler-sonography: task force group on cerebral death of the 156. Wale A, Pilcher J. Current role of ultrasound in small bowel imaging. Semin
Neurosonology Research Group of the World Federation of Neurology. J Ultrasound CT MR. 2016;37:301–12.
Neurol Sci. 1998;159:145–50. 157. Dorinzi N, Pagenhardt J, Sharon M, Robinson K, Setzer E, Denne N, et al.
136. O’Brien NF, Maa T, Yeates KO. The epidemiology of vasospasm in children Immediate emergency department diagnosis of pyloric stenosis with point-
with moderate-to-severe traumatic brain injury. Crit Care Med. 2015;43:674– of-care ultrasound. Clin Pract Cases Emerg Med. 2017;1:395–8.
85. 158. Mercaldi CJ, Lanes SF. Ultrasound guidance decreases complications and
137. Padayachy LC, Padayachy V, Galal U, Pollock T, Fieggen AG. The relationship improves the cost of care among patients undergoing thoracentesis and
between transorbital ultrasound measurement of the optic nerve sheath paracentesis. Chest. 2013;143:532–8.
diameter (ONSD) and invasively measured ICP in children. : Part II: age- 159. Cuna AC, Reddy N, Robinson AL, Chan SS. Bowel ultrasound for predicting
related ONSD cut-off values and patency of the anterior Fontanelle. Childs surgical management of necrotizing enterocolitis: a systematic review and
Nerv Syst. 2016;32:1779–85. meta-analysis. Pediatr Radiol. 2018;48:658–66.
Singh et al. Critical Care (2020) 24:65 Page 16 of 16
160. Silva CT, Daneman A, Navarro OM, Moore AM, Moineddin R, Gerstle JT, et al.
Correlation of sonographic findings and outcome in necrotizing
enterocolitis. Pediatr Radiol. 2007;37:274–82.
161. Sharma R, Hudak ML, Tepas JJ, Wludyka PS, Marvin WJ, Bradshaw JA, et al.
Impact of gestational age on the clinical presentation and surgical outcome
of necrotizing enterocolitis. J Perinatol. 2006;26:342–7.
162. Tam AL, Camberos A, Applebaum H. Surgical decision making in
necrotizing enterocolitis and focal intestinal perforation: predictive value of
radiologic findings. J Pediatr Surg. 2002;37:1688–91.
163. Epelman M, Daneman A, Navarro OM, Morag I, Moore AM, Kim JH, et al.
Necrotizing enterocolitis: review of state-of-the-art imaging findings with
pathologic correlation. RadioGraphics. 2007;27:285–305.
164. Aliev MM, Dekhqonboev AA, Yuldashev RZ. Advantages of abdominal
ultrasound in the management of infants with necrotizing enterocolitis.
Pediatr Surg Int. 2017;33:213–6.
165. Dördelmann M, Rau GA, Bartels D, Linke M, Derichs N, Behrens C, et al.
Evaluation of portal venous gas detected by ultrasound examination for
diagnosis of necrotising enterocolitis. Arch Dis Child Fetal Neonatal Ed.
2009;94:F183–7.
166. He Y, Zhong Y, Yu J, Cheng C, Wang Z, Li L. Ultrasonography and
radiography findings predicted the need for surgery in patients with
necrotising enterocolitis without pneumoperitoneum. Acta Paediatr. 2016;
105:e151–5.
167. van Druten J, Khashu M, Chan SS, Sharif S, Abdalla H. Abdominal ultrasound
should become part of standard care for early diagnosis and management
of necrotising enterocolitis: a narrative review. Arch Dis Child Fetal Neonatal
Ed. 2019;104:F551–9.
168. Manzoni P, Martin GR, Sanchez Luna M, Mestrovic J, Simeoni U,
Zimmermann L, et al. Pulse oximetry screening for critical congenital heart
defects: a European consensus statement. Lancet Child Adolesc Health.
2017;1:88–90.
169. Martin GR, Beekman RH, Mikula EB, Fasules J, Garg LF, Kemper AR, et al.
Implementing recommended screening for critical congenital heart disease.
Pediatrics. 2013;132:e185–92.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.