Support Care Cancer DOI 10.1007/s00520-017-3858-6

ORIGINAL ARTICLE

An investigation of the prevalence of swallowing difficulties and impact on quality of life in patients with advanced lung cancer Grainne C. Brady 1 & Justin W. G. Roe 1,2,3 & Mary O’ Brien 4 & Annette Boaz 5 & Clare Shaw 6

Received: 21 April 2017 / Accepted: 16 August 2017 # Springer-Verlag GmbH Germany 2017

Abstract Background Dysphagia can occur in advanced lung cancer due to direct tumour invasion or nerve compression. Anticancer treatments and co-morbid conditions may also cause or compound dysphagic symptoms. Speech and language therapy (SLT), medical and surgical interventions are available to address dysphagic symptoms in patients with lung cancer, however, management options are not described in national guidelines. Given the potentially short prognoses for patients with lung cancer, the aim of care should be to reduce symptom burden and maximise quality of life (QOL). Central to that aim is the identification and treatment of swallowing difficulties. Purpose This study sought to identify the prevalence and impact of dysphagia on QOL in patients with advanced lung cancer. Methods A single-site, prospective, exploratory study was undertaken. Previously validated patient-reported outcome

* Grainne C. Brady [email protected]

1

Speech and Language Therapy, The Royal Marsden NHS Foundation Trust, London, UK

2

Speech and Language Therapy Department, Imperial College Healthcare NHS Trust, London, UK

3

Department of Surgery and Cancer, Imperial College London, London, UK

4

Lung Unit, The Royal Marsden NHS Foundation Trust, London, UK

5

Centre for Health and Social Care Research, St George’s University of London, London, UK

6

Therapies Department, The Royal Marsden NHS Foundation Trust, London, UK

measures of swallowing were used to identify the presence and impact of dysphagia on QOL: EAT-10 assessment and the SWAL-QOL assessment. Results Seventy-two participants were recruited with 18.1% identified as having dysphagia on completion of the EAT-10 assessment. On further evaluation using the SWAL-QOL, compromised quality of life was noted with increased fatigue and meal time duration, difficulties with food selection and reduced eating desire. Frequent throat clearing, coughing and perceived pharyngeal stasis were reported. Conclusions Dysphagia is a potential symptom in advanced lung cancer which may impact QOL. Patients, carers and healthcare professionals should be aware of this so that early referral to SLT can be expedited. More robust prevalence and interventional studies are required to inform optimal management of this distressing condition. Keywords Lung cancer . Dysphagia . End of life care . Quality of life . Rehabilitation

Introduction Lung cancer is the second most common cancer in the UK [1] and is the most common cause of cancer death in the UK [2]. In comparison to other cancer types, lung cancer has one of the poorest survival rates with a median survival rate from point of diagnosis of 203 days in the UK and 60–120 days in the USA [3, 4]. In the UK, more than two thirds of cases are diagnosed at an advanced stage where no further curative treatment options are available [2]. Surgery, radiotherapy and chemotherapy are all used to treat lung cancer. Treatment selection depends on the type of lung cancer, the disease staging, position of the tumour within the lung and the patient’s overall condition [3]. Palliative

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chemotherapy for all subtypes of advanced stage lung disease aims to improve symptoms, preserve or improve quality of life (QOL) and prolong survival [4]. In a retrospective study looking at symptoms experienced in the final year of life as reported by family members/carers, it has been reported that 63% (n = 238) of patients with cancer will experience swallowing difficulties in the last year of life [5]. This prevalence estimate was based on retrospective carer report only and so caution may be required when interpreting this figure. In any case, swallowing difficulties can lead to aspiration, chest infections and pneumonia and are often associated with increased morbidity and mortality [6]. Dysphagia can also have a significant impact on QOL [7]. In comparison to other cancer groups such as head and neck cancer (HNC) where there is extensive literature available on the cause, nature, severity and management of dysphagia, there has been minimal literature to date focusing on dysphagia in lung cancer. The limited number of papers available looking specifically at lung cancer are dominated by a description of the pathophysiology of the swallowing dysfunction detailing the multifactorial nature of dysphagia including anticancer treatment-related swallowing difficulties, direct tumour invasion and co-morbid conditions [8–10]. Treatment-related dysphagia may include radiationinduced oesophagitis [8, 9, 11] and oral mucositis [8, 9, 12]. With targeted treatment regimens, for example using tyrosine kinase inhibitors (TKIs) which target epidermal growth factor receptors (EGFR), increased oral toxicities have been noted [13]. Direct tumour invasion may result in recurrent laryngeal nerve (RLN) compression causing unilateral vocal cord palsy (UVCP) which can increase the risk of swallowing difficulties in patients with lung cancer due to reduced airway protection [14]. Oesophageal compression or tracheo-oesophageal fistulae can also occur [15]. Lung cancer is often associated with multiple co-morbidities such as COPD, secondary primary cancers, metastatic disease to head/neck or brain [16], all of which may cause or compound swallowing symptoms [10]. Only one other dysphagia prevalence study in lung cancer was sourced, where a prevalence estimate for clinician diagnosed oesophageal dysphagia was described at 12.1% (n = 165) [9]. In this study, oesophageal dysphagia was identified using endoscopic examination of the oesophagus and manometry. Assessment for oropharyngeal dysphagia was not undertaken. No studies regarding the benefits of interventions specifically in patients with lung cancer were identified. Interventions may include medical, SLT and surgical interventions [10]. Although positive swallowing outcomes for medical interventions addressing oral and pharyngeal mucositis and candidiasis have been reported [10], no primary research in lung cancer to support this opinion was identified. Only one

study reporting positive swallowing outcomes for SLT interventions for patients with UVCP in advanced malignancy was identified [17]. With regards to surgical interventions for dysphagia management, the literature again focuses on advanced malignancy rather than lung cancer specifically. Positive trends for dysphagia outcomes are noted for the surgical management of UVCP [18] and stenting procedures for oesophageal compression or tracheo-oesophageal fistula [15]. The number of worldwide cancer cases is set to increase by 75% in the next two decades [19]. Lung cancer is likely to remain a major cause of morbidity and mortality. Given limited life expectancy for patients with lung cancer, the aim of care is to maximise quality of life and minimise symptom burden. Central to that aim is the identification and treatment of swallowing dysfunction associated with lung cancer [10]. Further evidence on the prevalence and impact of swallowing difficulties in the lung cancer population is needed to inform future national guidance. The development and provision of future rehabilitation services to optimise QOL, patient outcomes and experience is in keeping with the current emphasis on survivorship in cancer care [20]. In this study, we sought to identify the prevalence and impact of dysphagia on QOL in patients with advanced lung cancer. For the purposes of this study, advanced lung cancer is defined as disease stages III/IV where no further curative treatment options are available. The study objectives were to: 1. Identify the prevalence of dysphagia in a sample of patients with advanced lung cancer 2. Identify the impact on QOL in a sample of patients with advanced lung cancer

Ethical approval An application to the National Research Ethics Committee (REC) was submitted in July 2015 and a favourable opinion was granted following proportionate review at meeting dated 15th July 2015. Subsequent approval was granted from the NHS trust host site Research and Development Department in September 2015.

Methods A single-site, prospective, exploratory questionnaire study was undertaken. Previously validated patient-reported outcome measures of swallow were employed. The Eating Assessment Tool (EAT-10) was used to identify the prevalence of dysphagia [21]. The SWAL-QOL was used to measure the impact of dysphagia on QOL [22].

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While it is preferable not to change validated questionnaires, minor modifications were required for this study. The demographics section of the SWAL-QOL questionnaire was excluded as factors such as education and marital status were of no relevance to this study. Although designed as selfadministered tools, both questionnaires were administered by the researcher to reduce increased burden on participants. A sample size calculation, in relation to the primary aim, based on expected prevalence and required level of precision (95% confidence interval) was completed [23]. Seventy-two participants were required to obtain a 95% confidence interval (CI) of +/− 20% around a prevalence estimate of 25%. The estimate was based on previous published studies where prevalence was calculated between 63 and 12.1% [5, 9]. Consecutive patients who presented to the lung cancer outpatient department who met all of the inclusion criteria and none of the exclusion criteria were recruited to the study. Inclusion/exclusion criteria were as follows: Inclusion criteria: 1. Diagnosis of advanced lung cancer (stages III-IV, with spread to lymph nodes and/or distant metastases, where no further curative treatment options are available) 2. Capacity to consent 3. Have received/be receiving treatment at the data collection site 4. Male or female > 18 years 5. Sufficient spoken English language skills to complete the assessment tasks 6. Medically fit enough to be able to attend for an appointment 7. Awareness of diagnosis Exclusion criteria: 1. Scheduled for radical surgical intervention/ curative treatment 2. Medically very frail/ unable to attend for appointment All participants completed the EAT-10 assessment tool to identify the presence of dysphagia. Participants were asked to report any swallowing difficulties that they may have experienced over the past month. Those identified as having dysphagia, present if a score of 3 or more is obtained [21] proceeded to completion of the SWAL-QOL [22] to measure the impact of dysphagia on QOL.

Results Seventy-two participants were recruited. Participant characteristics are detailed in Table 1. Fifty-four percent were female.

Table 1

Participant characteristics

Age Mean

67 years

SD

SD 11.6 years

Range

Range 37–85 years Number Percent

Gender Male

33

46%

Female

39

54%

Lung cancer type Non-small cell lung cancer

63

87.5%

Small cell lung cancer Pleural mesothelioma

6 3

8.3% 4.2%

Adenocarcinoma Squamous cell carcinoma

44 11

61.1% 15.3%

Unspecified non- small cell Mixed adenosquamous cell

6 2

8.3% 2.8%

2 4 63 3

2.8% 5.6% 87.5% 4.2%

Non-small cell lung cancer subtype

Disease stage Stage IIIa Stage IVa Stage IVb Stage IV (pleural mesothelioma)

The mean age was 67 years (range 37–85 years). Eighty-seven percent (n = 63) of the sample had non-small cell cancer, the majority of which had adenocarcinoma. Most participants, 87.5% (n = 63), had advanced stage IVb disease. All 72 participants were undergoing palliative chemotherapy. Previous radiotherapy to the chest, head and/or neck was reported in 21% (n = 15). Six percent (n = 4) had previous surgical intervention for lung cancer. Thirteen patients obtained a score of 3 or more confirming a dysphagia prevalence estimate for the sample of 18.1% (95% confidence interval 9.7–27.8%- bootstrapped based on 1000 samples). The mean EAT-10 score for the sample was 2.4 (SD 5.8, range 0–34). For the 13 patients identified as having dysphagia, all had stage IV disease and were undergoing palliative chemotherapy. The most common co-morbid condition was a neurological history (n = 2: cerebrovascular accident, n = 1: brain metastases) followed by COPD (n = 2). Of note, four of these participants had a history of previous radiotherapy treatment to the head/neck/thorax and one participant had a history of UVCP. None of the participants had undergone surgical intervention for their lung disease. The quality of life domains affected most in the sample include fatigue (mean score 51 +/− SD 23), meal time duration (mean score 63 +/− SD 38), eating desire (mean score 63 +/− SD 45) and food selection (mean score 68 +/− SD 35).

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Discussion This study has shown that within the recruited sample of 72 participants with advanced lung cancer, 18.1% experienced dysphagia as defined by the EAT-10 assessment. All of the participants with dysphagia had stage IV disease and were undergoing palliative treatment. This is the first study to look specifically at the impact on dysphagia on QOL in patients with lung cancer. It has shown that as with other types of cancer, dysphagia can impact quality of life [7]. Troublesome dysphagic symptoms include having to throatclear, coughing and a feeling of food lodging in the throat and choking on food. Symptoms of throat clearing, coughing and pharyngeal stasis may be indicative of increased risk of aspiration [6] Fig. 1. The EAT-10 was used to obtain a self-reported prevalence estimate for dysphagia in the sample. This tool is specifically designed to identify the presence of both oropharyngeal and oesophageal dysphagia via patient report [21]. Screening tools are not without their limitations and direct assessment of swallowing using clinical bedside assessment +/− objective assessment of swallowing would have provided much more detail regarding the nature and severity of dysphagia in this patient group. Only outpatients undergoing palliative chemotherapy were recruited in this study and as such this patient group may represent those at least risk of dysphagia as they are not experiencing symptom exacerbation, or undergoing other treatments such as radiotherapy. Co-morbid conditions such as previous treatment for head and neck cancer or neurological conditions may have increased the dysphagia prevalence in this sample. In the study conducted by Hassan et al. [9], physician assessment and oesophageal endoscopy with manometry was used to identify oesophageal dysphagia only. These

Fig. 1 Dysphagic symptoms

methodological differences may account for the higher prevalence rate obtained in the current study. Limitations of this study include the fact that the study was limited to one research site only given time and funding constraints. The method by which the participants in this study were assessed and identified as having a dysphagia is also a potential limitation of this study. While the EAT-10 assessment is quick and easy to administer [21], it provides little detail on the nature of the patient’s dysphagia. Finally, it should be acknowledged that this study included only those patients who were undergoing palliative chemotherapy and who were being treated as outpatients. There is the potential for greater symptom burden including dysphagia amongst patients who are having other treatments such as radiotherapy, those patients who are admitted due to medical decline or symptom exacerbation and/or those patients who are not suitable for any further palliative treatment options.

Conclusion This study set out to investigate the prevalence and impact of dysphagia in patients with advanced lung cancer. This study provides new evidence that patients with advanced lung cancer undergoing palliative chemotherapy are at risk for swallowing difficulties and these difficulties can have an impact on QOL. Given the current emphasis on living with and beyond cancer, this research highlights a number of points for consideration regarding practice, future research and policy. Patients, carers and healthcare professionals need to be aware of the potential for dysphagia and its complications. Further research looking to identify ‘at risk’ groups and screening methods is required. More robust prevalence and interventional studies are required so that services can be commissioned

Symptom total score %

Dysphagic symptom severity for paents with lung cancer 100 90 80 70 60 50 40 30 20 10 0

Dysphagic symptoms almost always

oen

somemes

hardly ever

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and evidence-based interventions provided. Greater attention should be given to dysphagia in clinical guidelines to guide optimal symptom management.

8. 9.

Acknowledgements Miss Grainne Brady, Dr. Mary O′ Brien, Dr. Justin Roe and Dr. Clare Shaw acknowledge support from the National Institute for Health Research (NIHR) and the Royal Marsden/Institute of Cancer Research Biomedical Research Centre.

10.

Compliance with ethical standards 11. Conflict of interest Miss Brady received funding to complete a Masters of Research degree at Kingston and St. George’s University of London from the National Institute for Health Research (NIHR). The research was carried out as part of the academic programme of study. Miss Brady, Dr. Roe, Dr. Shaw and Dr. O′ Brien are employed by the Royal Marsden NHS Foundation Trust. Dr. Roe is also employed by Imperial College Healthcare NHS Trust. Professor Boaz is employed by Kingston and St George’s University of London. The authors have no other relevant financial or non-financial relationships to disclose. As sponsor for this research project, St George’s University of London have full control of all primary data and with their permission, primary data can be disclosed. Ethical approval An application to the National Research Ethics Committee (REC) was submitted in July 2015 and a favourable opinion was granted following proportionate review at meeting dated 15th July 2015. Subsequent approval was granted from the NHS trust host site Research and Development Department in September 2015.

12.

13.

14.

15.

16.

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