Growth of targeted neonatal echocardiography in Chinese neonatal intensive care units: gaps in practice and training

To evaluate clinical practice, neonatologists’ attitudes, and the extent of training and accreditation regarding targeted neonatal echocardiography (TnEcho) among Chinese neonatologists. A web-based questionnaire was emailed to 331 neonatologists across China who completed training in subspecialty neonatology. The survey covered various aspects of TnEcho, including the characteristics of clinical practice, attitudes towards its usefulness, and perceived barriers to implementation and training methods. Survey response rate was 68.0% (225/331). Seventy-nine (35.1%) respondents stated that TnEcho was utilized in their NICUs. Most respondents reported the use of echocardiography to evaluate hemodynamic significance of the patent ductus arteriosus (PDA, 94.9%). The eyeballing technique was most used to evaluate left (82.3%) and right (77.2%) ventricular function. Most respondents (87.3–96.2%) positively valued the role of TnEcho in providing timely and longitudinal hemodynamic information to guide cardiovascular care. Access to TnEcho was more likely in centers with on-site pediatric cardiology service (p = .003), larger bed capacity (p = .004), or level IV status (p = .003). Lack of experienced practitioners with echocardiography expertise (88.9%) and accredited training programs (85.8%) was perceived to be the major barrier to implementation. Of concern, most practitioners with TnEcho skills received training in an informal manner through workshops (60.8%) or self-directed learning (54.4%). Conclusions: The use of TnEcho for longitudinal evaluation of infants with hemodynamic instability is growing within Chinese NICUs. There is an urgent need to develop standardized training programs and accreditation for TnEcho which are adapted to the Chinese context. What is Known: • Targeted neonatal echocardiography (TnEcho) is an emerging technique to aid characterization of the hemodynamics of sick neonates in the neonatal intensive care units (NICUs) around the world. • Evidence is accumulating which supports the positive impact of TnEcho service on clinical management and patient outcomes. What is New: • This is the first report to show that the use of TnEcho for longitudinal evaluation of infants with hemodynamic instability is growing within Chinese NICUs. • There is an urgent need to develop standardized training programs and accreditation for TnEcho which are adapted to the Chinese context.


Introduction
Targeted neonatal echocardiography (TnEcho) is an emerging technique to aid characterization of the hemodynamics of sick neonates in the neonatal intensive care units (NICU) around the world [1][2][3][4]. TnEcho represents a comprehensive standardized assessment of heart function and pulmonary or systemic hemodynamics, usually directed by a specific clinical question, to enhance clinical decision making [5][6][7]. There is growing recognition that TnEcho provides timely and longitudinal hemodynamic information which helps to understand the physiological nature of circulatory instability and monitor the response to therapeutic intervention [8][9][10][11]. Evidence is accumulating which supports the positive impact of TnEcho service on clinical management and patient outcomes [12][13][14][15]. The introduction of an TnEcho-based approach to screening for hemodynamically significant patent ductus arteriosus (PDA) was associated with lower rate of severe intraventricular hemorrhage (IVH) and pulmonary hemorrhage in premature infants [16]. Jain et al. demonstrated that TnEcho-guided management prevented cardiorespiratory instability and improved patient outcomes following PDA ligation [17]. Finally, the merits of enhanced characterization of heart function in congenital diaphragmatic hernia to guide care is another noteworthy example of imaging-guided care [18]. To date, several international societies, including the American Society of Echocardiography (ASE), European Society for Pediatric Research, and European Society for Neonatology, have published guidelines to standardize the clinical practice and training in TnEcho [19][20][21]. Recent publications have demonstrated that practice of TnEcho is expanding across Canadian NICUs over the last decade, with an increasing number of centers now having access to hemodynamic specialists and training programs [2,15,22]. In Europe, neonatologists with skills in TnEcho were employed in 74% of the surveyed units, although lack of dedicated training programs and a formal accreditation process were raised as concerns [23,24]. Despite the global evolution of TnEcho, to our knowledge, no data are available from the Asian continent. The aims of this study were to gather perspectives regarding TnEcho use within the context of Chinese NICUs and describe the extent of training and accreditation offered.

Study design and participants
The survey was conducted between September and December 2022 among the attending neonatologists from tertiary hospitals in China. From September 2017 to August 2022, 508 attending neonatologists from 331 tertiary hospitals throughout China completed training and certification process in subspecialty neonatology at Children's Hospital of Fudan University. The database of the trained professionals was acquired from the educational department of Children's Hospital of Fudan University. To elicit site-specific practice preference, we randomly selected one representative from each center.

Survey instrument and data collection
A comprehensive questionnaire was designed by the authors Y.D. and P.M. for the purpose of this survey. The content was modified after receiving feedback from two other neonatologists with interest in TnEcho at Children's Hospital of Fudan University. The survey was pilot tested by six neonatologists from other centers to assess content validity, clarity of questions, and ease of use. Based on the feedback, a modified version of the questionnaire was developed and uploaded to the Chinese professional survey website Wenjuanxing (www. wjx. cn) for dissemination. Data from pilot testing were not included in the results. The final questionnaire included 48 questions related to (i) epidemiological and organizational characteristics of the NICUs; (ii) access to neonatology staff with experience in TnEcho; (iii) indications and details of specific measurements in the hemodynamic assessment; (iv) access to and details of training, and standards for accreditation; AND (iv) attitudes towards the use of TnEcho (Electronic Supplement 1). The survey questions were either (a) yes/no answers or (b) multiple-choice or a five-point scales of "Strongly Agree", "Agree", "Neither Agree nor Disagree", "Disagree", and "Strongly Disagree" for questions related to attitudes or perspectives. Skip logic was incorporated to reduce respondent burden. The survey was designed to only capture complete responses for the entire questionnaire. A letter of invitation with a hyperlink to the survey was disseminated to a total of 331 recipients in September 2022, and responses were collected between September and December 2022. The participants implied consent by completing and submitting the questionnaire. Data from respondents who started the survey but failed to finish it were not collected or saved. Non-responders were subsequently contacted by phone call or message bimonthly. An incentive of e-book, Gomella's Neonatology, was offered for participation in the survey.

Statistical analysis
Data were automatically transferred from the Wenjuanxing web tool into one integrated Excel file. Descriptive statistics were performed using IBM SPSS Statistics. Data were analyzed in a de-identified manner and presented as absolute numbers or percentages. Non-parametric chi-square tests (alpha = 0.05) were performed to examine differences in characteristics of NICUs or the presence of the most common barriers to TnEcho implementation between respondent centers with and without access to TnEcho. A p value < 0.05 was defined as statistically significant.  reported that the primary use of TnEcho in NICU was to obtain real-time information on cardiovascular physiology and hemodynamics, as an adjunct to clinical evaluation, to guide management and refine decision making. Other factors, valued by respondents, included evidence of improved clinical outcomes with TnEcho guided care [n = 44, (55.7%)] and concern related to the limited hemodynamic (physiologic) information provided by conventional echocardiography [n = 46, (58. More participants from large NICUs (greater than 80 beds, p = 0.004) or level IV NICUs (p = 0.003) used TnEcho in their practice. There was no association between volume of very low birth weight infants and the use of TnEcho (p > 0.05) ( Table 3). TnEcho service was not provided earlier (more than 4 years ago) in large units (p > 0.05) or level IV units (p > 0.05).

Attitude towards the use of TnEcho and barriers to implementation
Most respondents were confident ("strongly agreed" or "agreed") that TnEcho aids disease characterization and the selection of cardiovascular agents (Fig. 1). Lack of practitioners with echocardiography expertise [n = 200, (88.9%)], organized training programs [n = 193, (85.8%)], and echocardiography equipment [n = 107, (47.6%)] was reported as the major barrier to TnEcho implementation ( Fig. 1). More respondents from level IV units (p = 0.002) reported inability to bill for the service as potential barriers to the implementation of TnEcho in stating that findings were documented in a written note ( Table 5). The adoption of TnEcho was significantly associated with the presence of on-site pediatric cardiology (p = 0.003) and availability of a dedicated cardiac ultrasound machine on the ward (p = 0.000) ( Table 3).

Discussion
This is the first survey investigating the clinical utility, extent of training, and attitudes towards TnEcho in China. The results revealed that currently only 35.1% of the respondent neonatologists had access to TnEcho for evaluation of the cardiovascular function in sick neonates. The most common indications for TnEcho included evaluation of hsPDA, myocardial performance, and systemic and pulmonary hemodynamics. Most respondents valued use of TnEcho to obtain real-time information on cardiovascular physiology and enhance diagnostic/therapeutic precision.
Bedside functional echocardiography has been used by the intensivists since the 1990s to guide cardiovascular assessment of critically ill patients [25][26][27]. This non-invasive technique provides objective and reliable information on cardiovascular function and enhanced diagnostic precision, compared with physical examination. Additional benefits include safety, low cost, ease of use, absence of radiation exposure, and need of displacement of critical patient to the imaging department [28][29][30]. The newly born is at a much higher risk for hemodynamic instability due to the changes in cardiac loading conditions during the fetal to postnatal circulation. In addition, the immature cardiovascular system predisposes neonates, especially the preterm infants, to hemodynamic compromise in various clinical situations including hsPDA, sepsis, acute or chronic pulmonary hypertension, systemic inflammatory diseases such as necrotizing enterocolitis, hypovolemia, or inappropriate ventilation [31]. With increased understanding of the importance of developmental hemodynamics and cardiovascular physiology in these settings, there is substantial need for comprehensive and longitudinal hemodynamic assessment in a timely manner to guide the circulatory management in NICUs [31][32][33][34][35].
The use of bedside echocardiography has been adopted by neonatologists in routine clinical practice globally. In Australia and New Zealand, a survey in 2014 showed that 85% of the neonatologists reported that echocardiography was performed by neonatologists in their units [36]. Several publications have reported increased prevalence of TnEcho programs  [2]. Specific indications for TnEcho were comparable to our experience in addition to previously reported studies [2,3,15,22]. Another retrospective cohort study from a tertiary Canadian center reported that TnEcho recommendations led to a change in clinical management following 492 (66%) echos [15]. Our results suggest that, although the prevalence of TnEcho in China does not yet match the practice in western countries, there is growing interest in TnEcho for hemodynamic evaluation, monitoring, and diagnosis in critical neonates. Most respondents "strongly agreed"/"agreed" that TnEcho is useful for hemodynamic evaluation of patients with hypotension/shock, hsPDA, and pulmonary hypertension.
Of concern, many of the echocardiography studies are limited and include subjective measurement techniques. For example, our data showed that eyeballing was the most used parameter to assess cardiac function. Although it is widely practiced and offers a rapid judgment of the cardiac function, the eyeball technique has been recognized as inaccurate and has wide intra-and inter-observer variability [37,38]. Regarding the assessment of PDA, the transductal pulse Doppler and ductal diameter were most frequent measurements to determine the hemodynamic significance of PDA. Current guidelines by the ASE recommend a comprehensive protocol which includes evaluation of the magnitude of the transductal shunt by characterizing its effect on myocardial performance, systemic and/or end-organ perfusion (e.g., abdominal aortic flow), and cardiac volume overload (e.g., left ventricular output and left atrial-to-aortic root ratio). The guidelines were drafted based on the principle that an overly simplistic approach to TnEcho evaluation may lead to incorrect diagnostic assignment and suboptimal therapeutic choices. To date, several international guidelines for TnEcho have set standards for image acquisition and measurement techniques, which are the fundamental principles to enable formulation of an accurate interpretation and medical recommendations [39,40]. TnEcho use was more common in large centers or level IV NICUs in China. This may relate to a higher volume of critical infants with complex medical conditions required day-to-day assessment and management of hemodynamic complications in these centers. Accessibility to on-site pediatric cardiology was also associated with increased use of TnEcho, which highlights the importance of close collaboration between neonatologists and pediatric cardiologists. Of note, respondents from level III or small units cited lack of equipment as potential barrier to program implementation. The presence of a dedicated ultrasound machine on the unit ensures immediate availability for image acquisition and allows serial follow-up. In addition, digital image archiving and standardized reporting systems are essential components of TnEcho service [41]. Many respondents reported lack of access to centralized storage and reporting systems, which further increases the likelihood of issues related to quality assurance and medicolegal concerns.
Attendance at workshops or self-directed learning was the most common reported methods of training. These findings highlight the need to develop a well-designed curriculum and standard training program in TnEcho suitable for Chinese neonatologists. In Australasia, since the late 2000s, neonatal functional echocardiography training has been included as a neonatal module of Certificate of Clinician Performed Ultrasound developed by the Australian Society of Ultrasound Medicine (Retrieved from https:// www. asum. com. au). The ASE guidelines for TnEcho training recommend 1 year of advanced  [19]. In addition, trainees are advised to maintain a logbook of scans performed and undergo formal evaluation of image acquisition competency on completion. It is important to recognize that these guidelines were developed based on expert consensus mostly applicable to the North American and European healthcare environment. Regional differences in learning environment, medical regulatory bodies, and healthcare organization must be considered when implementing clinical and training programs internationally. In addition, the selection of an arbitrary number of echocardiography studies or fixed duration of time may have limitations. First, the rate at which trainees achieve competence in image acquisition is unpredictable and likely to be influenced by trainee aptitude, prior experience of neonatal echocardiography, and the complexity of imaging for each individual patient [42]. Second, the curriculum should be designed such that trainees have an exposure to a critical volume of patients with the usual indications for TnEcho (e.g., heart function, pulmonary hypertension, PDA) rather than an arbitrary number of scans. This will ensure that sufficient attention is paid to the cognitive aspects of the hemodynamic consultation; specifically, it is imperative that trainees have sufficient exposure to advanced cardiovascular physiology, pharmacotherapeutics, and pathophysiology of common neonatal cardiovascular health problems. The cognitive skills of trainees can be further strengthened through daily hemodynamic clinical rounds. There were several important limitations. First, we only asked neonatologists who completed training in subspecialty neonatology at the national pediatric center to participate which limits the generalizability of the results. Nevertheless, respondents were from all the administrative divisions except Heilongjiang Province which provided meaningful regional data. Second, as with any survey, self-reporting bias may have influenced the results. Third, structured questions and answers may limit certain opinions of respondents. Furthermore, the survey was conducted at a unit level because we aimed to assess the characteristics of TnEcho practice in individual NICU. The number of survey respondents was suboptimal which may bias the survey results. Finally, we randomly selected one participant from the same center as surrogates for their unit perceptions which could lead to biased perspectives which are not broadly representative of every neonatologist in China.

Conclusion
This is the first report of the growth of TnEcho within Chinese NICUs. Although the clinical impact of TnEcho was positively regarded by the neonatologists surveyed, lack of sufficient numbers of practitioners with TnEcho expertise and structured training programs was considered the main barrier to dissemination. This survey highlights the need for national standards for TnEcho clinical practice and training in China.
Author contribution Yingping Deng, MD: writing-original draft, gaining ethical approval, data acquisition and analysis.
Xiang Cao, MD: data acquisition and analysis. Luc L. Mertens, MD: conceptualization. Patrick J. McNamara, MD: conceptualization, revising manuscript critically for important intellectual content.
Data Availability All data are within manuscript; data are available upon reasonable request to the corresponding author.

Ethics approval
The study described has been carried out in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study has been approved by the Research Ethics Board of Children's Hospital of Fudan University on February 25, 2022 [REB#. (2022)14].

Consent to participate
The participants implied consent by completing and submitting the questionnaire.

Competing interests
The authors declare no competing interests.