Validation of SPECT-CT to assess improvement in airway clearance following expiratory muscle strength training (EMST) to reduce chronic aspiration in patients with head and neck cancer treatment related dysphagia

Introduction

Head and neck cancer treatment involves a combination of surgery, radiotherapy, and chemotherapy all of which can impact on acute and long-term swallowing function. Radiation associated dysphagia is estimated to be present in 31% of survivors (1). Aspiration following non-surgical head and neck cancer treatment occurs in up to 60% of patients (2) and is especially perilous because it is often silent (2). We have previously demonstrated that aspiration related pulmonary disease accounts for at least 32% of all non-cancer-related deaths in patients treated for head and neck cancer (3). Despite advances in treatment, using chemoradiation to better target the tumour tissue, collateral damage to functionally important adjacent healthy tissue remains high. Damage to nerve and muscle account for late treatment effects, especially dysphagia-related aspiration which carries a significant risk of mortality and morbidity (4,5).

The current gold standard for detecting deglutitive aspiration is a videofluoroscopic swallowing study (VFSS). A VFSS is useful to assess swallowing physiology, establish both the safety (penetration/aspiration) and efficiency (bolus residue) of swallowing. In a recent retrospective cross-sectional study, the VFSS factors most associated with the highest risk of aspiration were advanced age, reduced pharyngeal constriction and bolus clearance ratio (6). There are, however, significant limitations with VFSS; it is not possible to quantify the amount of material that is aspirated before, during or after the swallow (from residue or reflux). It also may not truly reflect what happens outside the testing environment as VFSS is a single timepoint and patients may modulate their usual swallowing by concentrating on the single task without distractions. Also, during a VFSS, swallowing is tested under optimal conditions using smaller volume boluses in an upright posture and examinations rarely test patients to the point of fatigue when aspiration may be more likely to occur. Additionally, the volume and properties of the aspirated material and competence of clearance mechanisms are all likely to play an important role in whether aspiration detected on VFSS leads to a pneumonia. Consequently, existing studies lack an objective measure to directly quantify deglutitive aspiration and lung clearance.

Scintigraphy during and after a swallow of a radioisotope-labelled bolus has been used in the past to evaluate swallowing function (7) as well aspiration and clearance of aspirate from airways (8). However, this mode of imaging is limited to two dimensions and lacks anatomical landmarks, which can be problematic. For example, residual tracer in the lung left lower lobe may be incorrectly classified or obscured due to residual tracer in the stomach and pharyngeal residue can obscure tracer in the proximal airways.

Single-photon emission computed tomography (SPECT), while similar to conventional scintigraphy, circumvents problems with localisation by providing 3D images, and when coupled with CT, permits both quantification and precise anatomical localisation of the tracer. SPECT-CT has been successfully used to assess aspiration in a diagnostic radionuclide salivagram, predominantly used in the paediatric population (9), but has not been validated to assess the clearance rate of aspirated material.

Therapeutic options to limit or stop deglutitive aspiration are currently limited. Over the last few decades, attempts have been made to improve swallow function by exercise therapy of the muscles involved in swallowing. However, the results from recent randomised controlled trials of both intensive swallowing exercises (10) and neuromuscular electrical stimulation (11) are disappointing. Surgical options to rectify significant aspiration are radical, including a narrow field laryngectomy to surgically separate the airway and alimentary tract. This treatment is only done in severe cases as this carries significant sacrifices such as loss of voice and the risks inherent with surgery. More often, patients with significant dysphagia and evidence of substantial prandial aspiration are recommended to modify diet and fluid consistencies, use swallowing manoeuvres, and postures to reduce aspiration or more frequently limiting or ceasing oral intake necessitating the insertion of feeding tube. These therapeutic options also carry a significant reduction in quality of life and neither eliminate the risk of aspiration of secretions or pneumonia.

Expiratory muscle strength training (EMST) is a simple, inexpensive, home exercise therapy that targets pulmonary aspirate clearance mechanisms. During EMST the patient expires forcefully into a device that provides adjustable resistance to airflow. The load can be elevated incrementally as expiratory muscles strengthen over time. The rationale for using EMST is to improve the subglottic expiratory forces to enhance clearance of any aspirate. Improved airway clearance is achieved by generating a more powerful cough to clear aspirate from the airway (12) and/or improving airway closure through activation and strengthening of the submental suprahyoid muscles during swallowing (13).

Evidence provided by randomised controlled trials confirms that EMST is effective in improving dysphagia resulting from various neurological disorders. A trial in 48 patients with amyotrophic lateral sclerosis (ALS) (14) found significant improvements in maximum expiratory pressure, as well as total DIGEST (Dynamic Imaging Grade of Swallowing Toxicity) scores (15). Clinically meaningful trends, in peak cough flow and oral intake, were also noted. Another randomised controlled trial in 60 Parkinson’s patients (16) demonstrated improved swallow safety and improved hyolaryngeal function during swallowing compared to sham treatment. A recent systematic review of good quality randomised controlled trials of EMST in stroke (pooled n=179) found a significantly lower likelihood of respiratory complications after respiratory muscle training [risk ratio (RR) 0.38, 95% CI: 0.15, 0.96], compared with no or sham respiratory intervention (17).

Although encouraging, these results cannot be extrapolated to radiotherapy-related dysphagia because of a different pathophysiological mechanism. Currently, evidence for any therapeutic effect of EMST in head and neck cancer survivors with radiation associated aspiration is limited to one retrospective case series (18), however, several randomised controlled trials are registered using EMST in the head and neck cancer population (19). Notwithstanding, the evidence is encouraging, with 23 head and neck cancer patients who completed the EMST training improving their maximum expiratory pressures by an average of 57% as well as their swallowing safety which was assessed using a videofluoroscopic swallow study using validated DIGEST criteria (15).

Evidence from the above trials (14,16-18) of EMST is promising, however, these previous studies have relied on indirect pulmonary measures or videofluoroscopy to assess airway pollution during swallowing. Pulmonary measures such as maximum expiratory pressure and peak cough flow, although relevant, do not directly address the issue of aspirate clearance. VFSS can semi-quantitatively detect aspiration but cannot be used to assess the rate of clearance of aspirate from the airways and further delayed pollution, over time, from residue. Hence, performing a pilot using SPECT-CT to assess effect of EMST on aspiration will provide invaluable preliminary data to undertake a definitive randomised controlled trial in head and neck cancer patients.

We hypothesised that SPECT-CT can quantify bolus aspiration and its temporal changes enabling assessment of clearance which is improved by EMST training. We present this article in accordance with the TREND reporting checklist (available at https://www.theajo.com/article/view/10.21037/ajo-24-28/rc).

Methods

Study design

This was a single-institution, prospective cohort proof of principle study. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013), and approved by the Human Research Ethics Committee of South Eastern Sydney Local Health District of New South Wales Health (Ethics approval 2019/ETH12586) and informed consent was taken from all individual participants. Participants underwent pre-intervention (EMST) assessments comprising of VFSS (as part of screening and eligibility), pulmonary function tests and an index SPECT-CT. Following these assessments patients completed an 8-week EMST training programme. SPECT was then repeated as per the pre-intervention protocol to assess and changes in rates of lung clearance.

Study participants

Eligible patients were recruited from the St George Hospital Swallow Clinic (Department of Gastroenterology and Hepatology), by the Speech Pathologist, between August 2022 and April 2023. Patients who presented to the St George Swallow Clinic with significant dysphagia and having completed their head and neck cancer treatments (surgery and radiation/chemoradiation) >12 months previously were assessed for eligibility. Participants underwent a videofluoroscopy to determine severity of dysphagia and were deemed eligible for the trial if safety scores were >2 on the DIGEST (15) scale indicating that all patients in this cohort had penetration aspiration scores (PAS) of 7–8. Specifically, a ‘DIGEST 2 score’ indicates intermittent aspiration, a ‘DIGEST 3 score’ indicates either chronic but not gross or gross but not chronic aspiration and a ‘DIGEST 4 score’ indicates chronic and gross aspiration. The DIGEST score is a well-validated and utilised tool in head and neck, based on the National Cancer Institute’s Common Terminology Criteria for Adverse Events (CTCAE), to grade pharyngeal safety and efficiency of swallowing from VFSS. The safety score is based on the well-established PAS (20), however, has incorporated both the frequency and quantity of aspiration observed across the VFSS. Oral intake and nutritional status were assessed using the Functional Oral Intake Scale (FOIS). FOIS scores range from one to seven, with higher scores indicating better swallowing function. Scores of 1–3 show a reliance on tube feeding with 1 (nothing by mouth), 2 (tube dependent with minimal attempts of food or liquid) and 3 (tube dependent with consistent oral intake of food or liquid). A score of 4–7 indicates total oral intake but with varying swallow function from 4 (total oral intake of a single consistency), 5 (total oral consistency with multiple consistencies, but requiring special preparation or compensation), 6 (total oral diet with multiple consistencies, without special preparation, but with specific food limitations) and 7 (total oral diet with no restrictions) (21).

Exclusion criteria included any local cancer recurrence, any neurological disorders known to cause oropharyngeal dysfunction [e.g., Parkinson’s, cerebrovascular accident (CVA), inflammatory myopathy, ALS] and any underlying lung disease which pre-dates radiotherapy for head and neck cancer.

Ten consecutive patients who met inclusion study were recruited. All patients who were invited to participate in the trial agreed and provided written consent.

Pulmonary function tests

Patients underwent baseline pulmonary function tests using spirometry to measure peak expiratory flow, forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1). Body plethysmography was used to derive total lung capacity (TLC) and residual volume. Diffusing capacity was measured using the single breath carbon monoxide diffusion capacity method (DLCO). All results were performed to ATS/ERS (American Thoracic Society/European Respiratory Society) quality criteria. Some patients, following their head and neck cancer treatment, had difficulty in being able to seal the testing system adequately leading to some measures being unable to be recorded.

SPECT and SPECT-CT

Participants attended the Nuclear Medicine Department and were given 100 mL of sterile water labelled with Technetium Tc-99m Sulphur colloid and were instructed to swallow it at a comfortable pace. A 50 mL plain water rinse was then given to clear the oral cavity of residue and then expectorate to avoid delayed seepage of the tracer into the airway. Participants were set up supine on the SPECT scanner with careful measurements taken to allow exact replication of their position at each assessment time point. SPECT-CT images of the neck, chest and abdomen were acquired to assess the amount of aspirate (T₀) and to allow correlation of anatomical structures. This low dose CT was conducted following the T₀ SPECT scan, at the index appointment, with careful marking of the patient position, to minimise radiation exposure and to replicated patient sent up on all subsequent SPECT scans. Further SPECT (alone) imaging was conducted at one (T₁) and three (T₃) following ingestion of the initial tracer at the baseline assessment, to assess the amount of residual aspirate in the airways allowing quantification of lung clearance. This imaging sequence of SPECT scans was repeated, without CT scan, at the completion of EMST training, to facilitate comparison of pre and post EMST intervention aspiration and clearance of aspirate.

Image analysis

Tomographic images were reconstructed using Siemens’ Flash 3D algorithm (4 iterations, 8 subsets, 5 mm Gaussian filter) incorporating inline corrections for photon attenuation and scatter based on co-registered CT images. Volumetric region of interest analysis was performed with in-house image analysis software (22), using the CT images to define the lung regions. The total counts confined to the lung regions and the total in all fields of view (representing the total body) were measured and the ratio reported as a percentage.

EMST intervention

Calibration and training using the EMST device were conducted during the SPECT-CT assessment. Individual patient’s maximum expiratory pressure (MEP) was determined as an average of 3 attempts within a 10% variance; the EMST device was set to 75% of this individualized maximum MEP and patients were instructed on how to use the device. The expiratory training was completed with a nose clip in place, they were instructed to support their cheeks to ensure a ‘closed system’ and to blow forcefully through the device ensuring that air is expelled through the open valve. Patients performed this exercise under supervision and were then instructed to complete the 8-week training on the established 5-5-5 schedule (5 sets of 5 breaths on 5 days of the week) (13). A participant diary was used to monitor compliance to treatment and the patients were monitored weekly to ensure that the EMST was set at 75% of their current MEP and that they were performing the exercise correctly.

Statistical analysis

A sample size (n=10) was chosen ensuring a homogenous group of patients, all of whom had demonstrated significant aspiration (DIGEST safety score >2) on the standard VFSS assessment. The primary outcome was assessing the ability for SPECT-CT to detect subtle changes in the amount of aspiration and most importantly lung clearance between index assessment and post treatment with EMST. Inference was performed on area under the curve (AUC) (aspiration % over time) with paired Student’s t-test.

To enable validation of SPECT comparison against next-best tool to assess aspiration, a VFSS was required, acknowledging that VFSS is almost certainly less accurate than SPECT. The relationship between the ordinal DIGEST score and continuous quantity of aspirate was measured using logistic regression modelling.

Changes to MEP were calculated pre and post EMST training and were compared using a paired Student’s t-test.

Adherence to the protocol was measured at each weekly visit using the protocol described by Hutcheson et al. (18). If patients completed the prescribed 5-5-5 schedule over the 8-week period, this would total 25 breaths per day and 125 breaths per week. Patients were deemed ‘fully adherent’ if they completed >900 EMST breaths over the 8-week trial.

Results

Baseline swallowing characteristics of patients (Table 1)

All participants were male and had completed curative treatment for head and neck cancers between 1 and 21 years previously with radical chemoradiation (CRT); 4 patients had also had surgery with adjuvant CRT. Patients had swallowing safety scores >2 on DIGEST demonstrating PAS scores of 7–8 where aspiration was not cleared and was either sensate (PAS 7) or silent (PAS 8). The aspiration occurred intermittently but was not gross in quantity in 5 patients, chronically but not gross in quantity in 1 patient and the aspiration was chronic and gross in 4 patients. The FOIS was graded to indicate the range of the baseline diet that the patient was able to tolerate. There were 60% of patients who were percutaneous endoscopic gastrostomy (PEG) tube dependent [n=6 with (FOIS 1–3) and 3 of these patients, were completely nil by mouth (FOIS 1)]. The remaining 40% (n=4) of patients tolerated all intake orally, however, had specific food limitations (FOIS 5–6).

Baseline respiratory function tests were performed in full by 9 of the 10 subjects and included spirometry, lung volumes by plethysmography and carbon monoxide diffusion capacity (Table 2). Spirometry testing alone was performed on the remaining patient. Nine of the ten patients had normal total lung capacity with the remaining one (Patient 7) having a mild restrictive pattern, in keeping with noted radiological changes consistent with pneumonitis. Eight of the ten participants had essentially normal airway function. One (Patient 4) demonstrated a significant bronchodilator response, indicating a potential diagnosis of asthma. Patient 5 had moderately severe airway obstruction, gas trapping, and severely impaired diffusion capacity, consistent with chronic obstructive pulmonary disease (COPD) and a significant smoking history.

SPECT and SPECT-CT

All participants tolerated the SPECT-CT at T₀ and SPECT at 1 hour (T₁) and 3 hours (T₃) following the index assessment and post-EMST SPECT scans at T₀, 1 hour (T₁) and 3 hours (T₃) post ingestion of the tracer. The tomographic images were then reconstructed to allow volumetric region of interest analysis using the CT images to define the lung regions (Figure 1).

Figure 1 Reconstructed tomographic images. (A) Simple MIP SPECT scans at baseline measurement timepoints and following EMST treatment. (B) MIP 3D projection fused with CT. SPECT-CT fused scans at baseline measurement timepoints and following EMST treatment. MIP, maximum intensity projection; SPECT, single-photon emission computed tomography; EMST, expiratory muscle strength training; CT, computed tomography.

Index assessment quantification of aspiration and clearance

At the index T₀ SPECT-CT assessment, the group mean of aspiration was 3.2% (95% CI: 0.7%, 5.8%), this decreased to 2.6% (95% CI: 0.5%, 4.7%) at T₁ and decreased further to 1.9% (95% CI: 0.8%, 3.1%) at T₃. Examining individual scores, 60% of patients had improved clearance of aspirate between T₀ and T₃ with the decrement in percentage of aspiration ranging from 19–76%. Importantly however, aspiration increased in 40% of the cohort between T₀ and T₁ and in 30% between T₁ and T₃ indicating continued aspiration of residue and/or reflux. The increase between T₀–T₃ ranged between 115–336% (Table 3).

The amount of aspirate on SPECT-CT was associated with higher DIGEST Safety score, increasing 2.3% (95% CI: 0.6%, 4.0%; R²=0.54, P=0.015) per point increase in DIGEST.

Post EMST intervention quantification of aspiration and clearance

Following 8 weeks of EMST intervention the group mean percentage of aspiration of the cohort at T₀ was 5.1% (95% CI: 0.1%, 10.0%), at T₁ this decreased to 3.4% (95% CI: 0%, 6.8%) and the group mean at T₃ then decreased further to 2.6% (95% CI: 0.1%, 5.2%). Examining the individual scores, 70% of the cohort had improved clearance between T₀ and T₃. The percentage of bolus aspirated at T₀ did not improve, in fact, the amount of aspiration at the post EMST intervention scan was higher in 70% and markedly elevated in 1 (10%) participant (Figure 2A).

Figure 2 Percentage aspiration and the group mean change of aspiration pre and post EMST training. (A) Aspiration expressed as a % of the ingested 100 mL bolus at baseline (T₀), 1 hour (T₁) and 3 hours (T₃) post tracer ingestion pre and post-EMST intervention. (B) Group mean change of % aspiration from baseline (T₀), 1 hour (T₁) and 3 hours (T₃) post tracer ingestion. EMST, expiratory muscle strength training.

The mean clearance of aspirate of the group tended to improve post-EMST intervention at all the measured timepoints. At T₁ (T₁–T₀) clearance improved from ∆ of −0.7 (95% CI: −1.7, 0.33) at index assessment to ∆ of −1.7 (95% CI: −3.4, −0.06) post EMST intervention. At T₃ (T₃–T₀) following ingestion of contrast clearance improved from ∆ of −1.3 (95% CI: −2.9, 0.26) at index assessment to ∆ of −2.4 (95% CI: −4.9, 0.17) post EMST intervention. Overall, the area under the delta % aspiration over time curve improved by a mean difference of −1.6 (95% CI: −3.4, 0.3; t=1.94, P=0.08) (Figure 2B).

MEP changes

The average MEP across the cohort increased from 42.5 at baseline to 74.2 following the 8-week EMST training (P<0.001). All patients recorded improved MEP, with an average increase of 175% (range, 138–229%) over the 8-week training period.

Safety and adherence

All patients completed the index and post EMST intervention assessments in the scheduled timeframe. Evaluating compliance, all patients had recorded their practice schedules and all were compliant with scores of >900 breaths through the EMST per week over the 8-week training.

Participant 7 was feeling unwell prior to his post-EMST intervention assessment. Despite feeling unwell, he completed the follow-up SPECT, however, at the conclusion of the assessment he stated he was dizzy and was transferred to the emergency department (ED). He was admitted for hypotension which resolved with intravenous fluid therapy. He remained afebrile, his chest was clear to auscultation, and he was discharged the following day. His aspirate quantity measured on that day increased by 216% (10.3% at T₀ at index scans to 22.2% at to T₀ post-EMST intervention), his aspirate clearance remained the same or even improved slightly from 51% to 54% (aspirate quantity at T₃ was 5.3% at index assessment and 12.1% post-EMST intervention).

Discussion

This is the first prospective study in a series of head and neck patients to validate the use of SPECT-CT as an assessment methodology to provide more accurate quantification of aspiration and lung clearance than a standard VFSS. Aspiration pneumonia is a leading complication after head and neck cancer treatment and the most significant cause of non-cancer related mortality (2). Clinicians utilise VFSS to identify the presence of aspiration and determine the underlying physiology of swallowing dysfunction. The limitations of videofluoroscopy are that it measures aspiration at a single time point, often with patients in an optimised position and it is not possible to accurately quantify aspiration or measure airway clearance.

Observations from this pilot study suggest that SPECT-CT offers new insights for clinicians in enabling accurate quantification of aspiration at different time points and more importantly calculate lung clearance. This research highlighted that 4 patients at T₁ index assessment, and 3 patients at T₁ following EMST intervention, displayed an increase in their percentage of aspiration after initial tracer ingestion. This is crucial, as it indicates that they had delayed aspiration from pharyngeal residue, or they aspirated refluxate. There may be occasions where following videofluoroscopy significant aspiration is not present, however delayed aspiration, from residue or regurgitation may be missed. Using a conventional VFSS a delayed aspiration is likely to be missed and this may have a significant impact on patients’ health outcomes and the decisions made regarding the risk of oral feeding. The next important step would be to trial this methodology, in an appropriately powered study, to ascertain the risk factors including whether delayed or reduced clearance of aspirate from SPECT-CT can accurately predict pneumonia risk. As radiographic demonstration of aspiration is a poor predictor of pneumonia risk, the clinical decision-making regarding feeding, the use of tube feeding and surgical interventions to alleviate aspiration are fraught with indecision, making management of these patients difficult. Better understanding of the risk factors for developing pneumonia would allow us to tailor our clinical decision making, in a truly evidence based, personalised medicine approach. Further, patients who are identified to be high-risk prior to definitive head and neck cancer surgery could receive prophylactic treatment and targeted respiratory physiotherapy interventions to decrease post operative morbidity and mortality.

Importantly, the ability to be able to reliably quantify aspiration and lung clearance will be able to be translated clinically into other populations with a high risk of aspiration such as stroke, neurodegenerative diseases, reflux, lung disease, lung transplant viability and paediatric feeding disorders.

Although not the primary outcome of this trial, EMST tended to have a positive effect on lung clearance in this small trial and MEP were seen to be able to be increased significantly over the 8-week intervention period. This warrants further assessment in a prospective cohort of patients. The amount that aspiration that occurred did not change significantly between the baseline and post intervention SPECT-CT however this is likely due to the severity of aspiration in this cohort as many were tube dependent and had been deemed not suitable to tolerate intake. Four of the 10 patients had moderate to severe impairment in their diffusion capacity and all those patients were noted to be PEG dependent for intake. A further subject (patient 6) was also PEG dependent but was noted to have normal lung function.

The potential for an inexpensive device (EMST) to improve airway clearance has been previously demonstrated and importantly this may have a significant positive impact on patient quality of life, and crucially, survival.

We chose patients with significant dysphagia and known aspiration for this pilot to ensure proof of principle could be demonstrated using SPECT-CT methodology to detect aspiration and lung clearance. It would now be useful to use this methodology to prospectively follow a large cohort of patients with varying amounts of aspiration to assess whether risk factors for the development of pneumonia can be attributed to a volume of aspiration and/or rate of clearance of aspirate from the lungs.

Limitations

We acknowledge the inherent limitations that exist in this proof of principle pilot study designed to validate SPECT-CT as a potential assessment methodology, to assess aspirate quantity and clearance more accurately. Although the population were all following head and neck cancer treatment and presented with significant dysphagia, as measured on DIGEST, there was heterogeneity regarding baseline swallowing and respiratory function. EMST was used as the intervention to effect a change in airway clearance rather than to measure change in swallowing and respiratory outcomes. For this reason, post EMST intervention VFSS were not conducted, therefore we are unable to report if patients had any improvement in DIGEST scores.

Although patients did report some minor changes in their ability to swallow certain consistencies or foods, the changes were not sufficient to see a change to the FOIS scores. The patients eligible for this proof of principle trial had severe dysphagia, with significant aspiration, to enable the efficacy of SPECT-CT to measure aspirate clearance. This is not a cohort of patients who would be expected to have improvements in swallowing function particularly in this short intervention trial and further work to test this methodology, with an appropriately powered sample size and range of swallowing dysfunction is required.

We also did not formally measure temporal stability of the SPECT-CT due to the time-consuming nature of this methodology, however, we did note that most patients only had a very small variance in the T₀ rates of aspiration. The patients in this cohort were those with significant swallowing dysfunction, so it is not surprising that the percentage of aspiration between index assessment and post EMST intervention did not alter. However, the trend to improved clearance of aspiration, post EMST intervention, is encouraging as this indicates that EMST may be able to assist in reliably clearing aspiration in this population with severe and chronic dysphagia. As most patients presented with significant aspiration a stable rate is aspiration between the baseline and post intervention is not surprising and pleasingly the aspirate clearance rates trended toward significance.

Conclusions

Aspiration following head and neck cancer treatment is well recognised as a common sequela with serious known health consequences. Clearance rates following aspiration and the correlation with potential to develop pneumonia are not well understood. SPECT-CT may offer clinicians an extra tool to enable temporal measurements of aspiration and clearance and a better understanding of the impact that both have on late dysphagia following head and neck cancer treatment. EMST has growing evidence that it assists with airway clearance and is still being investigated to ascertain whether there are also positive impacts on physiologic swallow function. The results from this pilot using SPECT-CT indicate this as a potential alternative to objectively quantify aspiration and clearance following head and neck cancer treatment. SPECT-CT certainly warrants validation in a large prospective trial to determine whether long-term pneumonia risk can be predicted to enable changing the potentially fatal course of this common sequela of head and neck cancer treatment.

Acknowledgments

The authors would like to thank the staff from the Nuclear Medicine Department, St Geroge Hospital for their generous support of this project; A/Prof Patrick Butler for assistance with the study design and approval to conduct the research; Ms Melissa Pack, Mr Arlen McDonald and Mr Seshan Seneviratne for their assistance with conducting the examinations and scheduling appointments.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the TREND reporting checklist. Available at https://www.theajo.com/article/view/10.21037/10.21037/ajo-24-28/rc

Data Sharing Statement: Available at https://www.theajo.com/article/view/10.21037/ajo-24-28/dss

Peer Review File: Available at https://www.theajo.com/article/view/10.21037/ajo-24-28/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://www.theajo.com/article/view/10.21037/ajo-24-28/coif). M.M.S. received part-time salary from St George and Sutherland Medical Research Foundation (SSMRF) with no restraint on the conduct, analysis and interpretation of the data and in the writing of this report. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013), and approved by the Human Research Ethics Committee of South Eastern Sydney Local Health District of New South Wales Health (Ethics approval 2019/ETH12586) and informed consent was taken from all individual participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Feng FY, Kim HM, Lyden TH, et al. Intensity-modulated chemoradiotherapy aiming to reduce dysphagia in patients with oropharyngeal cancer: clinical and functional results. J Clin Oncol 2010;28:2732-8. [Crossref] [PubMed]
2. Eisbruch A, Lyden T, Bradford CR, et al. Objective assessment of swallowing dysfunction and aspiration after radiation concurrent with chemotherapy for head-and-neck cancer. Int J Radiat Oncol Biol Phys 2002;53:23-8. [Crossref] [PubMed]
3. O'Hare J, Maclean J, Szczesniak M, et al. Laryngeal tumours and radiotherapy dose to the cricopharyngeus are predictive of death from aspiration pneumonia. Oral Oncol 2017;64:9-14. [Crossref] [PubMed]
4. Hunter KU, Lee OE, Lyden TH, et al. Aspiration pneumonia after chemo-intensity-modulated radiation therapy of oropharyngeal carcinoma and its clinical and dysphagia-related predictors. Head Neck 2014;36:120-5. [Crossref] [PubMed]
5. Szczesniak MM, Maclean J, Zhang T, et al. Persistent dysphagia after head and neck radiotherapy: a common and under-reported complication with significant effect on non-cancer-related mortality. Clin Oncol (R Coll Radiol) 2014;26:697-703. [Crossref] [PubMed]
6. Liu HC, Williamson CW, Zou J, et al. Quantitative prediction of aspiration risk in head and neck cancer patients treated with radiation therapy. Oral Oncol 2023;136:106247. [Crossref] [PubMed]
7. Shaw DW, Williams RB, Cook IJ, et al. Oropharyngeal scintigraphy: a reliable technique for the quantitative evaluation of oral-pharyngeal swallowing. Dysphagia 2004;19:36-42. [Crossref] [PubMed]
8. Silver KH, Van Nostrand D. The use of scintigraphy in the management of patients with pulmonary aspiration. Dysphagia 1994;9:107-15. [Crossref] [PubMed]
9. Hou P, Deng H, Wu Z, et al. Detection of salivary aspiration using radionuclide salivagram SPECT/CT in patients with COPD exacerbation: a preliminary study. J Thorac Dis 2016;8:2730-7. [Crossref] [PubMed]
10. Perry A, Lee SH, Cotton S, et al. Therapeutic exercises for affecting post-treatment swallowing in people treated for advanced-stage head and neck cancers. Cochrane Database Syst Rev 2016;2016:CD011112. [Crossref] [PubMed]
11. Langmore SE, McCulloch TM, Krisciunas GP, et al. Efficacy of electrical stimulation and exercise for dysphagia in patients with head and neck cancer: A randomized clinical trial. Head Neck 2016;38:E1221-31. [Crossref] [PubMed]
12. Pitts T, Bolser D, Rosenbek J, et al. Impact of expiratory muscle strength training on voluntary cough and swallow function in Parkinson disease. Chest 2009;135:1301-8. [Crossref] [PubMed]
13. Wheeler-Hegland KM, Rosenbek JC, Sapienza CM. Submental sEMG and hyoid movement during Mendelsohn maneuver, effortful swallow, and expiratory muscle strength training. J Speech Lang Hear Res 2008;51:1072-87. [Crossref] [PubMed]
14. Plowman EK, Tabor-Gray L, Rosado KM, et al. Impact of expiratory strength training in amyotrophic lateral sclerosis: Results of a randomized, sham-controlled trial. Muscle Nerve 2019;59:40-6. [Crossref] [PubMed]
15. Hutcheson KA, Barrow MP, Barringer DA, et al. Dynamic Imaging Grade of Swallowing Toxicity (DIGEST): Scale development and validation. Cancer 2017;123:62-70. [Crossref] [PubMed]
16. Troche MS, Okun MS, Rosenbek JC, et al. Aspiration and swallowing in Parkinson disease and rehabilitation with EMST: a randomized trial. Neurology 2010;75:1912-9. [Crossref] [PubMed]
17. Menezes KK, Nascimento LR, Ada L, et al. Respiratory muscle training increases respiratory muscle strength and reduces respiratory complications after stroke: a systematic review. J Physiother 2016;62:138-44. [Crossref] [PubMed]
18. Hutcheson KA, Barrow MP, Plowman EK, et al. Expiratory muscle strength training for radiation-associated aspiration after head and neck cancer: A case series. Laryngoscope 2018;128:1044-51. [Crossref] [PubMed]
19. Patterson JM, Lawton M. Dysphagia Advances in Head and Neck Cancer. Curr Otorhinolaryngol Rep 2023; Epub ahead of print. [Crossref] [PubMed]
20. Rosenbek JC, Robbins JA, Roecker EB, et al. A penetration-aspiration scale. Dysphagia 1996;11:93-8. [Crossref] [PubMed]
21. Crary MA, Mann GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 2005;86:1516-20. [Crossref] [PubMed]
22. McKay E. A software tool for specifying voxel models for dosimetry estimation. Cancer Biother Radiopharm 2003;18:379-92. [Crossref] [PubMed]