Correction: Clinical indications and triaging for adult transthoracic echocardiography: a statement by the British Society of Echocardiography

Transthoracic echocardiography (TTE) is widely utilised within many aspects of clinical practice, as such the demand placed on echocardiography services is ever increasing. In an attempt to provide incremental value for patients and standardise patient care, the British Society of Echocardiography have devised updated guidance for the indications and triaging of adult TTE requests for TTE services to implement into clinical practice.


Introduction
Transthoracic echocardiography (TTE) is widely accepted as the first choice non-invasive imaging modality for the assessment of cardiac structure and function. TTE is versatile, widely available and low-cost as such it forms a crucial part for a patient's pathway throughout clinical practice including initial diagnosis, management and follow-up of many cardiac [1,2] but also non-cardiac conditions.
The demand on TTE services continues to rise year upon year with data from National Health Service England indicating a ~ 3% increase in TTE activity for 2019 alone [3]. This continued increase in activity will invariably result in delays to patients accessing TTE's services. As such, the British Society of Echocardiography (BSE) have written an update to the previous 'Clinical Indications for Echocardiography' [4] in an attempt to assist healthcare professionals in recognising when TTE is indicated and will provide incremental value to the management of a patient. This guide also provides guidance on the implementation of a standardised triaging system for TTE requests. It is thought that together this can achieve a more sustainable service for the benefit of our patients.
This guideline is based on evidence from relevant clinical studies and/or general agreement from clinical practice. It is intended to be used by all BSE members throughout the United Kingdom. It will be regularly reviewed (5 yearly) and updated in accordance with changes as directed by publications and/or changes in clinical practice as and when required. This guideline is not intended to include recommendations specifically relating to the practice of transoesophageal or stress echocardiography. Occasionally, attention may be drawn to circumstances where utilisation of an alternative cardiac imaging modality such as cardiac computed tomography (cCT) or cardiac magnetic resonance imaging (cMRI) may be preferable, this will be highlighted where appropriate.
It is important to recognise that although there is a need to expand and diversify TTE services, it remains imperative that a well performed TTE, undertaken by an appropriately trained healthcare professional, is essential to ensure a cost effective, high quality and sustainable TTE service [2]. The BSE strive to ensure that patients receive the correct test at the correct time by the most appropriately skilled and qualified staff. This is paramount to ensuring patient safety and the safety and wellbeing of those staff performing these procedures. As such, the use of level I studies [5] should be performed only for the exclusion of immediate life-threatening pathology (to trigger a more advanced level II study or other appropriate test) in an acutely unwell patient, following request from an appropriate attending clinician. Level I echocardiography is not recommended in order to reduce waiting list burden. The use of 'abbreviated' or 'abridged' echocardiography protocols is also not currently recommended as a tool to reduce waiting list burden. The BSE does support the use of focussedrepeat studies in certain clinical scenarios and only where a recent comprehensive level II dataset has already been acquired as a baseline. These include Herceptin monitoring, acute pathologies where therapy has been given (e.g. thrombolysis), re-assessment of pericardial effusion or re-assessment of endocarditis lesions. The BSE has published practical guidance on the comprehensive level II dataset recommended for a standard adult TTE [6] and these should be implemented in practice.

Incorporating clinical assessment by telephone into triage
For long-standing TTE referrals, individual services may wish to utilise appropriately trained clinical colleagues (Cardiology Consultant/Specialist Registrar, Cardiac Scientist or Specialist Cardiac Nurse) to re-contact patients to ascertain the clinical appropriateness and/or urgency of TTE request. The content of these discussions will be bespoke to each individual patient and should only be undertaken with sight of a patient's medical records. This process may also be guided by locally available resources as outlined in Figs. 1 and 2. In light of these complex dependencies, triage using clinical assessment by telephone can be undertaken for follow-up requests if needed whilst acknowledging that it may be difficult to grade symptoms or undertake a clinical examination remotely. Furthermore, where follow-up periods of tests are lengthened, patients should be provided with the necessary information required to reconnect with the appropriate teams should there be a change in symptoms. It is vital that this is communicated sensitively to the patient explaining the rationale behind these decision. Any change in the patient's clinical status should prompt a thorough reassessment.

Hypertension and suspected left ventricular hypertrophy Not indicated:
• Routine assessment of any patient with essential hypertension • Routine assessment of asymptomatic patients with an established genetic or infiltrative cause of LVH where there is no change in clinical status and where an echo has been performed within the last 12 months • Repeat assessment of LV function in asymptomatic patients • Repeat assessment for left ventricular mass regression (if clinical concern is present regarding hypertrophic cardiomyopathy then repeat assessment with cMRI is preferable)

Indicated:
• Suspected LV dysfunction • Evaluation of clinically suspected aortic co-arctation (e.g., hypertension in the young) • Elevated blood pressure with concerns for end organ damage • Patients with a suspected or established genetic or infiltrative cause of LVH (with support from appropriate specialist teams where relevant)

Urgent:
• Accelerated hypertension with breathlessness or other clinical concerns of acute LV dysfunction • Patients with terminal illness whose management would not be affected by identification of any TTE abnormalities • Patients in whom TTE will not affect the decision to commence anticoagulation (e.g., patients in AF with cerebrovascular event and no suspicion of structural heart disease)

Indicated:
• Embolic peripheral or neurological events suggesting intracardiac mass: • Acute interruption of blood flow to major peripheral or visceral artery • Unexplained stroke or TIA without evidence of prior cerebrovascular disease or without significant risk factors for other cause (consider saline-contrast echocardiography by TTE or TOE, this may only be appropriate in < 55 year old patients) • Cross-sectional imaging or clinical findings suggesting intracardiac mass (if possible left atrial appendage thrombus then TOE preferable) • Periodic repeat assessment following removal of cardiac mass/tumour (usually annual review will suffice after an initial post-op scan) • Known primary malignancies where echocardiographic surveillance for cardiac involvement forms part of the normal staging process (e.g., renal cell carcinoma)

Urgent:
• Embolic event in the presence of clinical or ECG suspicion of significant left ventricular impairment (e.g., anterior Q waves on 12 lead ECG or clinical examination findings suggestive of LV dysfunction)

Pulmonary disease Not indicated:
• Repeat assessment to evaluate the probability of PHT in the absence of a meaningful tricuspid regurgitation jet or other echo markers of PHT on echo within the last 12 months. If there is clinical concern regarding PHT then advice from a pulmonary hypertension specialist service is recommended • Lung disease with no clinical suspicion of cardiac involvement or PHT

Indicated:
• Lung disease combined with a clinical suspicion of RV failure (e.g., peripheral oedema, raised jugular venous pressure) • Following pulmonary embolism when clinical concern for right ventricular impairment and/or presence of developing • Patients with AF of less than 48 h duration together with a clinical suspicion of structural heart disease and not adequately anticoagulated (TOE required)

Urgent:
• Not applicable

Palpitations and pre-syncope/syncope Not indicated:
• Palpitations without ECG proof of arrhythmia or clinical suspicion of structural heart disease on examination • Low-burden (< 5%) or isolated ventricular ectopy in absence of a clinical suspicion of structural heart disease • Classic neuro-cardiogenic syncope Indicated: • Clinical suspicion of structural heart disease in proven arrhythmia (e.g., AF or ventricular ectopy at greater than 10% frequency or ventricular ectopy occurring on exertion) • Routine assessment of ventricular function to assist with the calculation of risk of sudden cardiac death post-myocardial infarction or following documented ventricular tachycardia • Evaluation of cardiac structure and function to assist with future management (e.g., commencement of anti-arrhythmic medications) • Syncope in a patient with high-risk occupation (e.g., pilot, bus driver) • Assessment of patients without clinical suspicion of structural heart disease who have an arrhythmia commonly associated with structural heart disease (e.g., ventricular tachycardia)

Urgent:
• Syncope in a patient with clinically suspected structural of functional heart disease • Exertional syncope

Suspected pericardial disease Not indicated:
• Repeat assessment of small pericardial effusion (< 1 cm) with no hemodynamic compromise and without a change in clinical status • Follow-up studies in patients with terminal illness whose management would not be affected by echocardiographic abnormalities

Indicated:
• Clinically suspected pericarditis, pericardial effusion, or pericardial constriction • Periodic repeat assessment of moderate or large pericardial effusion • Repeat assessment of small pericardial effusion with change in clinical status

Urgent:
• Clinical suspicion of cardiac tamponade (especially if predisposing factors are present, e.g., known malignancy, suspected myopericarditis and recent cardiac surgery)

Established cardiomyopathy Not indicated:
• Patients with terminal illness whose management would not be affected by identification of any change in TTE appearance • Routine repeat assessment in clinically stable patients in whom no change in management is contemplated

Indicated:
• Repeat assessment in documented cardiomyopathy where the result may change management or following procedures that may improve ventricular function (e.g., cardioversion or coronary revascularisation) • Repeat assessment in documented cardiomyopathy where there has been a change in clinical status

Urgent:
• New onset class 3 or 4 heart failure symptoms

Aortopathy Not indicated:
• Patients with terminal illness whose management would not be affected by identification of any change in TTE appearance

Indicated:
• Assessment of suspected or proven genetic disorders in which aortic pathology may be a feature, (e.g., Marfan Syndrome) • Diagnosis and periodic assessment of aortic aneurysm, dilatation of the aorta and previous surgical repair of the aorta (an annual default interval between scans, but this timeline may be superseded following multi-disciplinary team review). Due to the limited ability of TTE to visualise the thoracic aorta the appropriate concomitant use of cross-sectional imaging is recommended Urgent: • Clinical suspicion of an acute aortic event (should not replace or delay cross-sectional imaging if more clinically appropriate)

Elective non-cardiac surgery Not indicated:
• Routine pre-operative assessment • Repeat assessment of previous echocardiogram in last 12 months with no intervening change in clinical status

Indicated:
• Murmur in an asymptomatic individual in whom clinical features suggest severe structural heart disease • Documented ischemic heart disease with reduced functional capacity (< 4 METs) • Murmur in the presence of cardiac or respiratory symptoms Urgent: • Not applicable

Clinical indications and triage of echocardiography
Appropriateness criteria for TTE will be classified with respect to the sub-headings below.
• Out-patient requests • Ward based and high dependency inpatients • Follow-up requests Didactic timeframes for the delivery of echocardiography services are inherently difficult and this decision-making process will require careful balance with additional clinical pressures on staff. As a broad outline, if an appropriate outpatient TTE is received and is triaged as "indicated" this should be undertaken within a six week time frame. For TTE requests that are triaged as "urgent" this should be undertaken within a two week time frame (unless otherwise indicated in Table 1). The list provided is not exhaustive but is designed to provide a framework for departments to streamline service provision whilst giving clear guidance to referring healthcare professionals for when TTE is appropriate. It is advocated that sufficient time is devoted to accurate triage; national experience suggests that a clinical focus on triage is able to increase capacity for TTE delivery.

Out-patient requests
A complete and comprehensive overview of appropriate TTE indications can be seen in Table 1. Out-patient requests have been broadly divided into those most often referred for TTE. These include: These 'most common' referral indications have also undergone further sub-classification to determine appropriateness and urgency.
1. 'Not indicated' TTE is unlikely to offer significant value to patient management and the request should therefore be declined.

'Indicated'
TTE is appropriate and should be completed routinely.

'Urgent' TTE is appropriate and should be undertaken as a clinical priority.
It is acknowledged that patients with suspected heart failure may present with a variety of clinical signs and symptoms. Suspected heart failure referrals that are described as "urgent" are consistent with NICE guideline [10]. Suspected heart failure referrals that are described as "indicated" are an attempt to include a broader range of clinical signs and symptoms where there is likely to be a high diagnostic yield for abnormality. Suspected heart failure referrals that are described as "not-indicated" are an attempt to reduce the rate of inappropriate referrals that are likely to yield a low level of abnormality whilst ensuring departments receive appropriate requests with pertinent details.

Ward based in-patient requests
The process for the handling of routine, urgent and emergency inpatient TTE referrals has been published previously [5]. This comprises the following indications and should be subject to immediate triage.
Clinical suspicion of: • Circulatory failure due to hypovolaemia.
• Acute decompensation in cardiac function.
• Acute or severe valve pathology: critical aortic stenosis/regurgitation or mitral valve dysfunction. • Acute right heart impairment due to pulmonary embolus. • Cardiac tamponade.
In addition to the above TTE guidance, the following indications and triage categories are specific to an inpatient setting (see Table 2). Where appropriate, inpatient TTE referrals are sub-classified with respect to urgency and subsequent change in clinical management of a given patient.

Follow-up requests
For those patients requiring longer term TTE follow-up, effective triage of referrals is vitally important to ensure resources are allocated to those with the most appropriate clinical need. Local clinical pathways, staffing and specialist skill-sets will, in some part, dictate appropriateness and timing of follow-up in these patients. However, this guidance advocates triage of referrals by experienced Healthcare Professionals to ensure clinical needs are met and an effective service is delivered.
TTE follow-up has been sub-classified into native valve disease (see Tables 3, 4 and 5) and prosthetic valves, valve repair and aortic disease (see Table 6). Latest NICE guidance [7] advocates the use of BSE guidelines for the assessment of valve disease severity. The included follow-up timeframes for native valve disease, valve replacement, valve repair and aortic diseases allow for standardisation of care and are in keeping with previously published literature [13][14][15][16]. These should be used in conjunction with the latest BSE recommendations for the echocardiographic assessment of aortic stenosis [17], tricuspid and pulmonary valve disease [18] and mitral valve disease [19]. The incorporation of "echo alerts" and "other alerts" are designed to highlight TTE features that should prompt urgent specialist review. There are no clinically significant differences between the recommendations herein and those published by the European Society of Cardiology [20] and the American College of Cardiology [21]. Patients under the care of a valve clinic and who require "Cardiologist / urgent Cardiologist review" should be undertaken by a valve clinic Cardiologist with valve disease competencies and expertise as this promotes best practice [22].
It is also acknowledged that a considerable number of patients will have more complex disease (e.g., moderate to severe multi-valve disease or post-operative Table 3 Native valve follow-up: aortic stenosis and aortic regurgitation*

Mild
Moderate Severe Other alerts for Cardiologist review: • Development of symptoms • Trace-mild AR associated with normal aortic valve morphology, normal aortic root and normal ascending aorta does not usually require TTE surveillance regurgitation with ventricular dysfunction). For these patients, an individualised approach is essential and discussion amongst the clinical team to advise on the surveillance scan period is recommended. Cardio-oncology is a complex clinical field and established local pathways are encouraged. Discussion amongst key stakeholders is highly advised, and in certain situations it may be considered appropriate to extend out the interval between repeat TTE. However, where there is clinical deterioration with likely cardiac involvement, a shortened time interval between repeat TTE's may be more appropriate. It is advocated that baseline left ventricular systolic function assessment prior to the use of potentially cardiotoxic chemotherapy agents is triaged and prioritised as an urgent request to prevent delays to the commencement of treatment. A joint BSE and British Cardio-Oncology Society guideline on the TTE assessment of adult cancer patients receiving anthracycline therapy has previously been published [23].

Implementation of new indications and triage guidelines into real world practice
To assess the impact of the new indications and triage guidelines on service provision, two clinical service audits were undertaken within an inpatient setting (Craigavon Area Hospital, Southern Health and Social Care Trust) and outpatient valve surveillance clinic setting (University Hospitals of North Midlands). Both clinical service audits were registered with the respective Trust's research and development departments.

Clinical service audit 1: Craigavon Area Hospital
Craigavon Area Hospital is a District General Hospital in Northern Ireland serving an estimated local population of 241,000. It is commissioned to perform over 10,000 TTE's annually and has an inpatient bed capacity of 450.
In an attempt to reduce inpatient TTE waiting times a service audit was undertaken in March 2021. Inpatient TTE referrals were collated over a two week period and reviewed against the BSE indications as outlined in this   document. Over this two week time frame 200 referrals were received and audited against the new BSE guidance. The audit found that 95% of these referrals were undertaken within the recommended timeframes and 89% within 24 h. When inpatient TTE requests were vetted against the new BSE guidance, 44.5% of requests were triaged as "not indicated" for an inpatient basis. This reduction in workload enabled the remaining appropriate inpatient TTE referrals to be completed in a more timely fashion. The audit findings were effectively used as an educational tool to improve the knowledge of appropriate inpatient TTE requests with clinical referring teams. It is hoped that this will translate to fewer inappropriate inpatient TTE's being received in the future and enable patients with the greatest clinical need to have an inpatient TTE in a timely manner and allow for the freeing up of resources to be more effectively directed elsewhere.

Clinical service audit 2: University Hospital of North Midlands
The University Hospitals of North Midlands serves an estimated local population of 900,000. The centre has a Physiologist/Scientist led heart valve surveillance clinic which was established over 10 years ago. A clinical service audit was undertaken in November 2020 to better understand the patients' demographics, valve aetiology/ severity and follow-up requirements of the patient currently under its care. At the point of audit, the service incorporated the European Society of Cardiology guidelines for the management of valvular heart disease [12]. The results showed there were 1504 patients within the service, mean age 69 years (range 20-99 years). The most common native valve aetiology was aortic stenosis (30%) with mitral regurgitation and prosthetic valve replacements (aortic and mitral) accounting for 17% and 46% of patients respectively. This Physiologist/Scientist led service was shown to be safe with low between-appointment non-elective admission rates for patients with moderate/severe disease (5%) and a high proportion of patients referred for valvular intervention (80%) following referral back to medical follow-up when symptoms developed. The release of BSE indications for valvular heart disease follow-up, as outlined in this document, prompted an additional audit to be undertaken to assess the impact of this on the follow-up duration of patients within the service.
All patients who attended the clinic in March 2021 were reviewed. A total of 88 patients were included (mean age 70 years, 62% male). Of these, 19.6% of patients' no longer required routine follow-up due to either, mild aortic or mitral regurgitation with normal valvular structure and function or, mechanical valve replacements with no high risk features on baseline TTE. In 33.9% of patients, follow-up could be extended by an average of 41 months due to the presence of mild regurgitation or stenosis. This audit demonstrates that a portion of patients within heart valve surveillance clinics are potentially having follow-up at shorter time duration than is necessary. This may allow   for follow-up frequency to be safely extended therefore increasing additional capacity within the service.

Conclusion
This updated guideline for TTE indications and triage has been produced to aid healthcare professions who refer patients for TTE ensuring that referrals are appropriate and timely. It also allows TTE services across the United Kingdom to standardise their triaging practice allowing limited resources to be directed to those patients in whom the results will most effectively guide diagnosis, management and/or future follow-up. The clinical audit findings presented demonstrate how these guidelines can be implemented into real world practice and have a positive impact on TTE services.