REVIEW URRENT C OPINION
Contemporary management of voice and swallowing disorders in patients with advanced lung cancer Grainne C. Brady a, Paul N. Carding b, Jaishree Bhosle a, and Justin W.G. Roe a
Purpose of review Advanced lung cancer can cause changes to swallowing and communication function. Direct tumour invasion, dyspnoea and deconditioning can all impact on swallowing function and communication. Cancer treatment, if administered, may cause or compound symptoms. In this study, the nature of swallowing and communication difficulties in patients with advanced lung cancer will be discussed, and management options including medical management, speech and language therapy (SLT) intervention, and surgical interventions will be considered. Recent findings Advanced lung cancer can result in voice and swallowing difficulties, which can increase symptom burden and significantly impact on quality of life (QOL). There is a growing evidence base to support the use of injection laryngoplasty under local anaesthetic to offer immediate improvement in voice, swallowing and overall QOL. Summary There is limited literature on the nature and extent of voice and swallowing impairment in patients with lung cancer. Well designed studies with robust and sensitive multidimensional dysphagia and dysphonia assessments are required. Outcome studies examining interventions with clearly defined treatment goals are required. These studies should include both functional and patient-reported outcome measures to develop the evidence base and to ensure that interventions are both timely and appropriate. Keywords advanced lung cancer, dysphagia, dysphonia, palliative care, rehabilitation
INTRODUCTION Lung cancer is the most common cancer in the world with at least 1.83 million cases diagnosed worldwide, including more than 410 000 new lung cancer cases diagnosed in Europe alone in 2012 [1]. Lung cancer has one of the poorest survival outcomes for any cancer, as more than two-thirds of cases are diagnosed at an advanced stage when curative treatment options are not possible [1]. The median survival rate for lung cancer in the UK is 203 days postdiagnosis [2], and 60–120 days in the United States [3]. For the purposes of this article, advanced lung cancer is defined as lung disease in which no further curative treatment options are available. Surgery, radiotherapy and chemotherapy are all used to treat lung cancer [2]. Treatment selection depends on a number of factors, including the type of cancer, the position of the cancer within the lung, disease staging and the patient’s overall general
health [2]. Surgery remains the mainstay of treatment for curative intent for nonsmall cell lung cancer (NSCLCA) [2,3]. Chemotherapy is most often used in the treatment of small cell lung cancer (SCLCA) frequently with addition of concurrent radiotherapy [2,4]. SCLCA accounts for approximately 18% of all lung cancers [1]. It is considered to be the more aggressive form of cancer and has often metastasized beyond the lung at the time of diagnosis [2]. a The Royal Marsden NHS Foundation Trust, London, UK and bSchool of Allied Health, Faculty of Health Sciences, Australian National Catholic University, Brisbane, Queensland, Australia
Correspondence to Grainne C. Brady, BSc, MRCSLT, The Royal Marsden NHS Foundation Trust, Fulham Road, London SW3 6JJ, UK. Tel: +44 207 808 2815; fax: +44 207 808 2336; e-mail: grainne.bra [email protected] Curr Opin Otolaryngol Head Neck Surg 2015, 23:191–196 DOI:10.1097/MOO.0000000000000155
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Speech therapy and rehabilitation
KEY POINTS Advanced lung cancer can result in voice and swallowing difficulties, which can increase symptom burden and significantly impact on QOL. It is imperative that health professionals involved in the care of patients with lung cancer are aware of the potential for swallowing and voice difficulties and the role of the professionals including oncologists, SLTs and surgeons, in amelioration of these symptoms. Injection laryngoplasty under local anaesthetic has been identified as well tolerated and effective in vocal cord medialization with the potential to improve voice and swallowing in patients with advanced lung cancer with a known unilateral vocal cord palsy (UVCP). With developments in personalized medicine, patients may have improved survival times but with the potential for ongoing voice and swallowing problems. To minimize complications and symptom burden resulting from dysphagia and dysphonia, a prompt multidisciplinary approach to care is essential.
There is extensive literature available regarding voice and swallowing difficulties relating to head and neck cancer and to a lesser extent oesophageal malignancy. However, there has been little consideration of voice and swallowing difficulties in relation to patients with lung cancer. Previous articles have focused on dysphagia in patients with a diagnosis of advanced malignant disease, rather than focusing specifically on patients with lung cancer. Roe et al. [5] investigated the patient experience of dysphagia in patients with malignancies other than head and neck cancer. The study revealed that patients with cancers not affecting the head and neck area are at risk of developing dysphagia and suffering from a consequential deterioration in quality of life (QOL). Raber-Durlacher et al. [6] also examined dysphagia in patients with multiple types and sites of cancer looking specifically at assessment tools, prevalence, complications and impact on QOL. Mediastinal disease was reported as the main cause of dysphagia in patients with lung cancer resulting from oesophageal compression. However, detailed presentation and management options for dysphagia were not discussed. Previous articles that have specifically focused on lung cancer have mainly considered voice or swallowing difficulties in isolation. Again, the authors focus on the nature of the voice or swallowing difficulties rather than management techniques. Camidge [7] reported the causation of swallowing difficulties in a series of patients with lung cancer. Six condition-related causes were identified, 192
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including mediastinal disease, cervical lymphadenopathy, brain stem lesion, gastrointestinal tract metastases, associated systemic disorders and second primary disease. Two treatment-related causes were also identified: oropharyngeal and oesophageal infections and radiation-induced oesophageal toxicity. These aetiological categories were described using a series of case studies. However, as critiqued by Sasaki and Leder [8], figures regarding the total number and the proportion of patients presenting with dysphagia were not recorded. Similarly, it was also critiqued that hypercalcaemia, a common metabolic disorder in advanced cancer, was not considered as a potential cause for dysphagia in these patients [9]. Lee et al. [10] investigated the nature and severity of voice disorders in a group of lung cancer patients. Outcome measures included clinician perceptual rating of voice and the patients’ opinion regarding the impact/severity of the voice disorder. Results showed that 90% (n ¼ 40) of patients had perceptible dysphonia. However, only 27.5% (n ¼ 11) of these patients were concerned about their voice. Again, no management strategies were discussed. Therefore, the aim of this article is to review the most up-to-date literature relating to swallowing difficulties (dysphagia) and voice problems (dysphonia) in patients with advanced lung cancer. For the purposes of this review, advanced lung cancer refers to lung disease wherein no curative treatment options are available. The review will report on causes and management options and will conclude with some recommendations for areas of further research.
CAUSES OF DYSPHAGIA AND DYSPHONIA IN PATIENTS WITH ADVANCED LUNG CANCER Swallowing and voice difficulties may arise in patients with lung cancer as a result of nerve compression, direct tumour invasion, comorbidities and/or treatment effects.
Nerve compression An estimated 43% of patients with lung cancer are diagnosed as having a unilateral vocal cord palsy (UVCP) caused by bronchogenic carcinoma [11]. The damage to the recurrent laryngeal nerve (RLN) is commonly caused by compression from a left apical lung tumour, enlarged bronchial glands or from mediastinal nodes [12]. Patients with lung cancer with known UVCP are at an increased risk of swallowing difficulties [5]. Volume 23 Number 3 June 2015
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Management of voice and swallowing disorders Brady et al.
UVCP can result in compromised airway protection and reduced laryngeal sensation, leading to increased penetration and/or aspiration [12]. Altered subglottic air pressure may result in increased pharyngeal residue [13]. In patients with compromised pulmonary function, an inability to clear aspirated material secondary to ineffective cough reflex can be a lifethreatening event [14]. UVCP is associated with severe dysphonia and compromised voice-related QOL [15 ,16]. Patients usually present with a weak and breathy voice quality and associated hoarseness. This is because the left vocal fold is commonly immobile and fixed in the paramedian position [12]. The specific vocal characteristics depend on a number of factors, including the position of the immobile vocal cord, the degree of vocal fold atrophy and the degree of compensation from the contralateral cord (and/or false vocal cords) [15 ]. &&
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Direct tumour invasion Extrinsic compression of the oesophagus, most often caused by mediastinal disease, can result in dysphagia [7]. The subcarinal lymph nodes extend posteriorly and are the group of nodes most likely to cause compression. Compression at the level of the thoracic inlet can be caused by enlarged lymph nodes of the neck [5]. In addition to affecting the passage of bolus flow, compression can produce secondary achalasia, causing oesophageal dysmotility [17 ]. Direct tumour invasion may also result in tracheo-oesophageal fistula leading to aspiration of saliva and food/fluids [18]. &&
Individual patient considerations and comorbidities Lung cancer is associated with age and smoking. Changes in the swallowing mechanism with age (presbyphagia) may increase the risk for aspiration. The ageing process may result in changes in the structure, motility, coordination and sensitivity of the swallowing process [19]. Oral stage swallowing may be longer and triggering of the pharyngeal swallow can be more delayed. Some increased pharyngeal residue may be present postswallow, necessitating additional clearing swallows [20]. Presbyphonia refers to voice changes related to ageing of the larynx. This results from ossification of the cartilages and descent of the larynx within the neck. Changes in the connective tissue of the vocal folds, in addition to atrophy, may lead to glottal insufficiency [21]. Voice can become weak, breathy with undesirable and unintentional pitch and loudness variation changes.
About 80–90% of lung cancer patients in the UK and USA are smokers [1,22]. Smoking is associated with COPD and respiratory compromise [3] and the impact of this on swallowing has been described [23,24]. Respiratory disruption can also result in an increased risk of aspiration [23]. Respiration is the power source of vibration of the vocal folds during phonation [21] and consequently reduced breath support can result in voice changes [10]. Smoking may also result in a laryngeal disease, including Reinke’s oedema, laryngeal hyperplasia and leukoplakia, all of which can result in marked dysphonia [25]. A host of other potential comorbidities including metastatic cancer, thyroid/glandular disease, neurological disease, congestive heart failure and pulmonary fibrosis may also be present with patients with lung cancer [26]. When coupled with the disease trajectory – including gradual deterioration in respiratory function, increased fatigue and overall reduced reserve – swallowing and voice difficulties are likely to result.
Treatment effects on swallowing Toxicity from both radiotherapy and chemotherapy treatment can lead to significant difficulties with swallowing. For patients with advanced NSCLCA, radiotherapy is often given for palliation if a patient is presenting with symptoms, including haemoptysis, cough, pain and dysphagia [27]. Dosage generally depends on the patient’s overall performance status but can range from 10–12.4 Gy in a single fraction for any metastatic disease [27,28], to 30–39 Gy in 10–13 fractions [27,28]. Radiotherapy to the mediastinum causes changes to the oesophageal mucosa, which can result in oesophagitis. This causes difficult and painful swallowing characterized by a burning sensation when swallowing. It is often a dose-limiting complication for the treatment of lung cancer [29]. Radiation-induced oesophagitis can result in prolonged treatment duration and subsequent poorer treatment and survival outcomes. Rare occurrences of oesophageal stenosis as a result of antecedent radiotherapy have also been reported [30]. A number of different chemotherapy drugs and targeted agents are used to treat patients with lung cancer. Traditional chemotherapy drugs include platinum drugs (carboplatin and cisplatin), vinca alkaloids (vinorelbine) and taxanes (paclitaxel and docetaxel). A number of these drugs can cause an alteration in a patient’s taste or a dry mouth, both of which can affect swallowing [31]. Patients receiving chemotherapy can also develop oral thrush, which can result in dysphagia and occasionally mucosal ulceration causing pain [31].
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Mucositis/stomatitis can cause erythema, swelling, bleeding and painful ulceration of the mucosal lining of the mouth, which can result in difficulties maintaining nutrition orally [32,33]. Generally, with standard chemotherapies used in lung cancer, the incidence is low. However, in patients with advanced NSCLCA, in whom an activating mutation in the epidermal growth factor receptor (EGFR) has been identified, treatment includes tyrosine kinase inhibitors, which target EGFR. There are currently three drugs in use, gefitinib, erlotinib and afatinib [2,28]. With gefitinib, the incidence of grade 3 mucositis was reported as 0.2% compared with a rate of 8.7% with afatinib [34].
INTERVENTIONS TO OPTIMIZE SWALLOWING AND VOICE The previous literature that has reported on lung cancer and dysphagia and dysphonia has failed to consider treatment options. The second half of this review details the evidence for medical interventions, speech and language therapy (SLT) interventions and surgical interventions.
Medical interventions Extrinsic compression of the oesophagus may be treated with chemotherapy and radiotherapy with the aim of tumour size reduction. Pharmacological management options for dysphagia resulting from oral mucositis and oesophagitis may include analgesics [35], anti-inflammatory and/or antifungal medication. Oral thrush should be considered in all patients undergoing chemotherapy treatment and signs should be treated promptly to prevent exacerbation of problems. Patients should be assessed prior to each new cycle of treatment. If patients are having problems with mucositis, a dry mouth or alteration in taste, to an extent that it is affecting their nutritional status, then careful consideration for continuing with further chemotherapy should be made. The options would include delaying treatment to allow the resolution of symptoms, the addition of supportive measures, dietetic input and pharmacological management whilst continuing with treatment or continuing with treatment at a reduced dose.
Speech and language therapy interventions The underlying cause for the swallowing difficulty must be identified before any treatment can be initiated. The SLT conducts a clinical evaluation 194
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of swallowing, including a detailed case history, oro-motor examination and oral trials if appropriate [36]. The SLT may recommend instrumental assessments [such as a modified barium swallow (MBS) or fibreoptic endoscopic evaluation of swallowing (FEES)], to evaluate the nature and extent of swallowing disorder and to plan rehabilitation/intervention [37]. Behavioural and dietary treatments are often the most effective intervention techniques for immediate relief of symptoms [36] and close working with the dietician is essential. Given that healthcare staff may not be aware of the potential swallowing issues for these patients, education of staff should form a major part of any intervention. In severe cases wherein the patient is unable to maintain nutrition and hydration orally, nonoral feeding may be required. However, the relative benefits should be considered in the context of deteriorating disease and in partnership with the multidisciplinary team [38]. If the swallowing difficulty is suspected to result from laryngeal dysfunction, the SLT should initiate a referral to the otoloaryngologist for assessment and consideration of vocal cord augmentation [39]. In addition, the SLT should assess the patient for suitability for behavioural interventions to optimize swallowing safety and comfort [36,37]. For patients with dysphonia, an assessment of voice should be undertaken by the SLT following consultation with an otolaryngologist. The extent of vocal dysfunction must be quantified and a range of compensatory techniques can be trialled. Interventions should aim to maximize both vocal function and voice-related QOL [14]. Voice therapy should focus on vocal hygiene, maximal phonatory coordination, optimal breath support for speech and avoidance of hyper-functional behaviours [40]. In the case of UVCP, the patient should be considered for vocal cord augmentation [38,39]. The SLT should contribute to decision-making regarding the potential for vocal cord augmentation [10,40]. Voice therapy may be indicated pre or post or for some patients in preference to vocal cord medialization [40].
Surgical interventions Surgical techniques for the management of oesophageal compression causing obstruction and tumour invasion resulting in fistulization are available [18]. The surgical procedure often includes the insertion of a stent [18,30]. There are several surgical techniques available for the management of UVCP, many of which have shown positive outcomes for swallowing [41,42] and voice [14,15 ,38,39,43]. &&
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Historically, Isshiki type I thyroplasty was considered the ‘gold standard’ surgical technique for UVCP providing a permanent augmentation of the paralysed vocal cord [15 ]. Previously, vocal cord augmentation using injection thyroplasty under general anaesthetic with materials such as Teflon has been used [43]. Teflon is no longer used due to complications such as granulation formation [12,42]. More recently, injection thyroplasty under general anaesthetic has been completed using biomaterials such as Bioplastique [14]. However, there has been an increasing interest in the use of injection thyroplasty, which is administered under local anaesthetic, for example, using calcium hydroxylapatite [38]. The procedure can be completed in an outpatient clinic [15 ,38,39]. Office-based procedures offer several advantages for patients with lung cancer. As well as allowing for prompt intervention, it avoids anaesthetic and other risk factors for this patient group [15 ,38,40]. The ability to perform the procedure without interruption to treatment schedules or anticoagulation regimes is an important consideration [39]. Given the advantages and success in improving voice, swallowing and QOL outcomes, this technique has now become the standard approach in many settings [39]. &&
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CONCLUSION The number of worldwide cancer cases is set to increase by 75% in the next two decades [44]. Lung cancer will remain a major cause of morbidity and mortality [45]. Given limited life expectancy for patients with lung cancer, the aim of care is to maximize QOL and minimize symptom burden. Central to that aim is the identification and treatment of swallowing and voice dysfunction associated with lung cancer. To date, there is a lack of literature on the nature and extent of voice and swallowing impairment. There is an urgent need for well constructed prevalence studies that employ robust and sensitive multidimensional dysphagia and dysphonia assessments. Similarly, outcome studies examining SLT, medical and surgical interventions with clearly defined treatment goals are clearly required. These studies should include functional and patient-reported outcome measures to develop the evidence base and to ensure that interventions are both timely and appropriate. Acknowledgements Grainne Brady, Dr Jaishree Bhosle and Dr Justin Roe acknowledge support from the National Institute for Health Research NIHR RM/ICR Biomedical Research Centre.
Financial support and sponsorship Miss Brady is funded by the National Institute for Health Research (NIHR) for a Master’s of Research programme at Kingston and St George’s University of London. Dr Roe’s work is funded by the Royal Marsden Cancer Charity, The Royal Marsden Hospital, Fulham Road, London, SW3 6JJ, UK. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Cancer Research UK. Cancer statistics key facts lung cancer. 2014. http:// publications.cancerresearchuk.org/downloads/Product/CS_KF_LUNG.pdf. [Accessed 9 December 2014] 2. NICE. The diagnosis and treatment of lung cancer (update). 2011. http:// www.nice.org.uk/guidance. [Accessed 30 November 2014] 3. National Cancer Institute. Small cell lung cancer treatment. 2014. http:// www.cancer.gov/cancertopics/pdq/treatment/small-cell-lung/healthprofessional/page1#Section_25. [Accessed 3 December 2014] 4. NICE. 2004. http://www.nice.org.uk/guidance/csgsp/evidence/supportiveand-palliative-care-the-manual-2. [Accessed 2 November 2004] 5. Roe JW, Leslie P, Drinnan MJ. Oropharyngeal dysphagia: the experience of patients with nonhead and neck cancers receiving specialist palliative care. Palliat Med 2007; 10:567–574. 6. Raber-Durlacher J, Brennan M, Verdonck-de Leeuw I, et al. Swallowing dysfunction in cancer patients. Support Care Cancer 2012; 20:433–443. 7. Camidge DR. The causes of dysphagia in carcinoma of the lung. J R Soc Med 2001; 94:567–572. 8. Sasaki CT, Leder SB. Comments on selected recent dysphagia literature. Dysphagia 2003; 18:64–68. 9. Amin R. Dysphagia in lung cancer. J R Soc Med 2002; 95:55–56. 10. Lee CF, Carding PN, Fletcher M. The nature and severity of voice disorders in lung cancer patients. Logoped Phoniatr Vocol 2008; 33:93–103. 11. Loughran S, Alves C, MacGregor FB. Current aetiology of unilateral vocal fold paralysis in a teaching hospital in the West of Scotland. J Laryngol Otol 2002; 116:907–910. 12. Huins C, Lobeck E, Roe J. Unilateral vocal cord paralysis in patients with lung cancer. Eur J Palliat Care 2009; 16:214–217. 13. Bhattacharyya N, Kotz T, Shapiro J. Dysphagia and aspiration with unilateral vocal cord immobility: incidence, characterization, and response to surgical treatment. Ann Otol Rhinol Laryngol 2002; 111:672–679. 14. Alves CB, Loughran S, MacGregor FB, et al. Bioplastique medialization therapy improves the quality of life in terminally ill patients with vocal cord palsy. Clin Otolaryngol 2002; 27:387–391. 15. Powell J, Carding P, Birdi R, Wilson JA. Injection laryngoplasty in the out&& patient clinic under local anaesthetic: a case series of sixty- eight patients. Clin Otolaryngol 2014; 39:224–227. An investigation of self-reported and perceptually rated voice outcomes in patients undergoing local anaesthetic injection laryngoplasty in the outpatient clinic setting. 16. Spector BC, Netterville JL, Billante C, et al. Quality-of-life assessment in patients with unilateral vocal cord paralysis. Otolaryngol Head Neck Surg 2001; 125:176–182. 17. Hassan WA, Darwish K, Shalan IM, et al. Aetiologic mechanisms of dysphagia && in lung cancer: a case series. Egypt J Chest Dis Tuber 2014; 63:435–442. To date this is the only prospective study we are aware of investigating the prevalence of dysphagia in patients with lung cancer. This paper also highlights the different aetiologic mechanisms for dysphagia among lung cancer patients based on clinican diagnosis. 18. Ahmet Dobrucali EC. Palliation of malignant esophageal obstruction and fistulas with self expandable metallic stents. World J Gastroenterol 2010; 16:5739–5745. 19. Leslie P, Drinnan MJ, Ford GA, Wilson JA. Swallow respiratory patterns and aging: presbyphagia or dysphagia? J Gerontol A Biol Sci Med Sci 2005; 60:391–395. 20. Logemann J. Evaluation and treatment of swallowing disorders. 2nd ed. Texas: PRO-ED; 1998. 21. Cohen SM, Elackattu A, Noordzij JP, et al. Palliative treatment of dysphonia and dysarthria. Otolaryngol Clin North Am 2009; 42:107–121.
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Speech therapy and rehabilitation 22. National Cancer Institute. Tobacco statistics snapshot. 2012. http:// www.cancer.gov/cancertopics/tobacco/statisticssnapshot. [Accessed 10 December 2014] 23. Diez-Gross R, Atwood CWJJr, Charles W Jr, et al. The coordination of breathing and swallowing in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2009; 179:559–565. 24. Martin-Harris B. Optimal patterns of care in patients with chronic obstructive pulmonary disease. Semin Speech Lang 2000; 21:311–321. 25. Awan SN. The effect of smoking on the dysphonia severity index in females. Folia Phoniatr Logop 2011; 63:65–71. 26. Tammemagi CM, Neslund-dudas C, Simoff M, Kvale P. Impact of comorbidity on lung cancer survival. Int J Cancer 2003; 103:792–802. 27. London Cancer Alliance. LCA Lung Cancer Clinical Guidelines. 2013. http:// www.londoncanceralliance.nhs.uk/media/62369/Lung%20Cancer%20Clini cal%20Guidelines%20041213%20FINAL%20REV.pdf. [Accessed 27 October 2013] 28. National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology: non-small cell lung cancer version 2. NCCN; 2014. 29. De-Ruysscher D, Meerbeeck J, Vandecasteele K, et al. Radiation-induced oesophagitis in lung cancer patients. Strahlenther Onkol 2012; 188:564–567. 30. Altemur Karamustafaoglu Y, Yoruk Y. Self-expandable esophageal stents placement for the palliation of dysphagia as a result of lung cancer. Dis Esophagus 2010; 23:561–564. 31. Wilberg P, Hjermstad MJ, Ottesen S, Herlofson BB. Chemotherapy-associated oral sequelae in patients with cancers outside the head and neck region. J Pain Symptom Manage 2014; 48:1060–1069. 32. Quinn B, Potting CMJ, Stone R, et al. Guidelines for the assessment of oral mucositis in adult chemotherapy, radiotherapy and haematopoietic stem cell transplant patients. Eur J Cancer 2008; 44:61–72. 33. Sonis ST, Elting LS, Keefe D, et al. Perspectives on cancer therapy-induced mucosal injury. Cancer 2004; 100:1995–2025. 34. Mok TS, Wu Y, Thongprasert S, et al. Gefitinib or carboplatin–paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009; 361:947–957.
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35. Yang JC, Hirsh V, Schuler M, et al. Symptom control and quality of life in LUXLung 3: a phase III study of afatinib or cisplatin/pemetrexed in patients with advanced lung adenocarcinoma with EGFR mutations. J Clin Oncol 2013; 31:3342–3350. 36. Langmore SE, Grillone G, Elackattu A, Walsh M. Disorders of swallowing: palliative care. Otolaryngol Clin North Am 2009; 42:87–105. 37. Bu¨low M, Martin-Harris B. The therapeutic swallow study. In: Ekberg E, editor. Dysphagia: diagnosis and treatment. Berlin: Springer; 2012. pp. 411–424. 38. Karagama Y, Hurren A, Carding P, Lindsey L. Short-term voice quality results following percutaneous medialisation of the paralysed vocal cord under local anaesthesia using calcium hydroxyapatite gel: how we do it. Clin Otolaryngol 2008; 33:362–366. 39. Kupferman ME, Acevedo J, Hutcheson KA, Lewin JS. Addressing an unmet need in oncology patients: rehabilitation of upper aerodigestive tract function. Ann Oncol 2011; 22:2299–2303. 40. Heuer RJ, Thayer Sataloff R, Emerich K, et al. Unilateral recurrent laryngeal nerve paralysis: the importance of ‘preoperative’ voice therapy. J Voice 1997; 11:88–94. 41. Kraus DH, Ali MK, Ginsberg RJ, et al. Vocal cord medialization for unilateral paralysis associated with intrathoracic malignancies. J Thorac Cardiovasc Surg 1996; 111:334–339. 42. Nayak VK, Bhattacharyya N, Kotz T, Shapiro J. Patterns of swallowing failure following medialization in unilateral vocal fold immobility. Laryngoscope 2002; 112:1840–1844. 43. Hughes RGM, Morrison M. Vocal cord medialization by transcutaneous injection of calcium hydroxylapatite. J Voice 2005; 19:674–678. 44. Bray F, Jemal A, Grey N, et al. Global cancer transitions according to the Human Development Index (2008-2030): a population- based study. Lancet Oncol 2012; 13:790–801. 45. America Lung Association. Key facts about tobacco use among children and teenagers. 2010. http://www.lung.org/stop-smoking/about-smoking/ facts-figures/children-teens-and-tobacco.html. [Accessed 3 December 2014]
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Contemporary management of voice and swallowing disorders in patients with advanced lung cancer Grainne C. Brady a, Paul N. Carding b, Jaishree Bhosle a, and Justin W.G. Roe a
Purpose of review Advanced lung cancer can cause changes to swallowing and communication function. Direct tumour invasion, dyspnoea and deconditioning can all impact on swallowing function and communication. Cancer treatment, if administered, may cause or compound symptoms. In this study, the nature of swallowing and communication difficulties in patients with advanced lung cancer will be discussed, and management options including medical management, speech and language therapy (SLT) intervention, and surgical interventions will be considered. Recent findings Advanced lung cancer can result in voice and swallowing difficulties, which can increase symptom burden and significantly impact on quality of life (QOL). There is a growing evidence base to support the use of injection laryngoplasty under local anaesthetic to offer immediate improvement in voice, swallowing and overall QOL. Summary There is limited literature on the nature and extent of voice and swallowing impairment in patients with lung cancer. Well designed studies with robust and sensitive multidimensional dysphagia and dysphonia assessments are required. Outcome studies examining interventions with clearly defined treatment goals are required. These studies should include both functional and patient-reported outcome measures to develop the evidence base and to ensure that interventions are both timely and appropriate. Keywords advanced lung cancer, dysphagia, dysphonia, palliative care, rehabilitation
INTRODUCTION Lung cancer is the most common cancer in the world with at least 1.83 million cases diagnosed worldwide, including more than 410 000 new lung cancer cases diagnosed in Europe alone in 2012 [1]. Lung cancer has one of the poorest survival outcomes for any cancer, as more than two-thirds of cases are diagnosed at an advanced stage when curative treatment options are not possible [1]. The median survival rate for lung cancer in the UK is 203 days postdiagnosis [2], and 60–120 days in the United States [3]. For the purposes of this article, advanced lung cancer is defined as lung disease in which no further curative treatment options are available. Surgery, radiotherapy and chemotherapy are all used to treat lung cancer [2]. Treatment selection depends on a number of factors, including the type of cancer, the position of the cancer within the lung, disease staging and the patient’s overall general
health [2]. Surgery remains the mainstay of treatment for curative intent for nonsmall cell lung cancer (NSCLCA) [2,3]. Chemotherapy is most often used in the treatment of small cell lung cancer (SCLCA) frequently with addition of concurrent radiotherapy [2,4]. SCLCA accounts for approximately 18% of all lung cancers [1]. It is considered to be the more aggressive form of cancer and has often metastasized beyond the lung at the time of diagnosis [2]. a The Royal Marsden NHS Foundation Trust, London, UK and bSchool of Allied Health, Faculty of Health Sciences, Australian National Catholic University, Brisbane, Queensland, Australia
Correspondence to Grainne C. Brady, BSc, MRCSLT, The Royal Marsden NHS Foundation Trust, Fulham Road, London SW3 6JJ, UK. Tel: +44 207 808 2815; fax: +44 207 808 2336; e-mail: grainne.bra [email protected] Curr Opin Otolaryngol Head Neck Surg 2015, 23:191–196 DOI:10.1097/MOO.0000000000000155
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Speech therapy and rehabilitation
KEY POINTS Advanced lung cancer can result in voice and swallowing difficulties, which can increase symptom burden and significantly impact on QOL. It is imperative that health professionals involved in the care of patients with lung cancer are aware of the potential for swallowing and voice difficulties and the role of the professionals including oncologists, SLTs and surgeons, in amelioration of these symptoms. Injection laryngoplasty under local anaesthetic has been identified as well tolerated and effective in vocal cord medialization with the potential to improve voice and swallowing in patients with advanced lung cancer with a known unilateral vocal cord palsy (UVCP). With developments in personalized medicine, patients may have improved survival times but with the potential for ongoing voice and swallowing problems. To minimize complications and symptom burden resulting from dysphagia and dysphonia, a prompt multidisciplinary approach to care is essential.
There is extensive literature available regarding voice and swallowing difficulties relating to head and neck cancer and to a lesser extent oesophageal malignancy. However, there has been little consideration of voice and swallowing difficulties in relation to patients with lung cancer. Previous articles have focused on dysphagia in patients with a diagnosis of advanced malignant disease, rather than focusing specifically on patients with lung cancer. Roe et al. [5] investigated the patient experience of dysphagia in patients with malignancies other than head and neck cancer. The study revealed that patients with cancers not affecting the head and neck area are at risk of developing dysphagia and suffering from a consequential deterioration in quality of life (QOL). Raber-Durlacher et al. [6] also examined dysphagia in patients with multiple types and sites of cancer looking specifically at assessment tools, prevalence, complications and impact on QOL. Mediastinal disease was reported as the main cause of dysphagia in patients with lung cancer resulting from oesophageal compression. However, detailed presentation and management options for dysphagia were not discussed. Previous articles that have specifically focused on lung cancer have mainly considered voice or swallowing difficulties in isolation. Again, the authors focus on the nature of the voice or swallowing difficulties rather than management techniques. Camidge [7] reported the causation of swallowing difficulties in a series of patients with lung cancer. Six condition-related causes were identified, 192
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including mediastinal disease, cervical lymphadenopathy, brain stem lesion, gastrointestinal tract metastases, associated systemic disorders and second primary disease. Two treatment-related causes were also identified: oropharyngeal and oesophageal infections and radiation-induced oesophageal toxicity. These aetiological categories were described using a series of case studies. However, as critiqued by Sasaki and Leder [8], figures regarding the total number and the proportion of patients presenting with dysphagia were not recorded. Similarly, it was also critiqued that hypercalcaemia, a common metabolic disorder in advanced cancer, was not considered as a potential cause for dysphagia in these patients [9]. Lee et al. [10] investigated the nature and severity of voice disorders in a group of lung cancer patients. Outcome measures included clinician perceptual rating of voice and the patients’ opinion regarding the impact/severity of the voice disorder. Results showed that 90% (n ¼ 40) of patients had perceptible dysphonia. However, only 27.5% (n ¼ 11) of these patients were concerned about their voice. Again, no management strategies were discussed. Therefore, the aim of this article is to review the most up-to-date literature relating to swallowing difficulties (dysphagia) and voice problems (dysphonia) in patients with advanced lung cancer. For the purposes of this review, advanced lung cancer refers to lung disease wherein no curative treatment options are available. The review will report on causes and management options and will conclude with some recommendations for areas of further research.
CAUSES OF DYSPHAGIA AND DYSPHONIA IN PATIENTS WITH ADVANCED LUNG CANCER Swallowing and voice difficulties may arise in patients with lung cancer as a result of nerve compression, direct tumour invasion, comorbidities and/or treatment effects.
Nerve compression An estimated 43% of patients with lung cancer are diagnosed as having a unilateral vocal cord palsy (UVCP) caused by bronchogenic carcinoma [11]. The damage to the recurrent laryngeal nerve (RLN) is commonly caused by compression from a left apical lung tumour, enlarged bronchial glands or from mediastinal nodes [12]. Patients with lung cancer with known UVCP are at an increased risk of swallowing difficulties [5]. Volume 23 Number 3 June 2015
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Management of voice and swallowing disorders Brady et al.
UVCP can result in compromised airway protection and reduced laryngeal sensation, leading to increased penetration and/or aspiration [12]. Altered subglottic air pressure may result in increased pharyngeal residue [13]. In patients with compromised pulmonary function, an inability to clear aspirated material secondary to ineffective cough reflex can be a lifethreatening event [14]. UVCP is associated with severe dysphonia and compromised voice-related QOL [15 ,16]. Patients usually present with a weak and breathy voice quality and associated hoarseness. This is because the left vocal fold is commonly immobile and fixed in the paramedian position [12]. The specific vocal characteristics depend on a number of factors, including the position of the immobile vocal cord, the degree of vocal fold atrophy and the degree of compensation from the contralateral cord (and/or false vocal cords) [15 ]. &&
&&
Direct tumour invasion Extrinsic compression of the oesophagus, most often caused by mediastinal disease, can result in dysphagia [7]. The subcarinal lymph nodes extend posteriorly and are the group of nodes most likely to cause compression. Compression at the level of the thoracic inlet can be caused by enlarged lymph nodes of the neck [5]. In addition to affecting the passage of bolus flow, compression can produce secondary achalasia, causing oesophageal dysmotility [17 ]. Direct tumour invasion may also result in tracheo-oesophageal fistula leading to aspiration of saliva and food/fluids [18]. &&
Individual patient considerations and comorbidities Lung cancer is associated with age and smoking. Changes in the swallowing mechanism with age (presbyphagia) may increase the risk for aspiration. The ageing process may result in changes in the structure, motility, coordination and sensitivity of the swallowing process [19]. Oral stage swallowing may be longer and triggering of the pharyngeal swallow can be more delayed. Some increased pharyngeal residue may be present postswallow, necessitating additional clearing swallows [20]. Presbyphonia refers to voice changes related to ageing of the larynx. This results from ossification of the cartilages and descent of the larynx within the neck. Changes in the connective tissue of the vocal folds, in addition to atrophy, may lead to glottal insufficiency [21]. Voice can become weak, breathy with undesirable and unintentional pitch and loudness variation changes.
About 80–90% of lung cancer patients in the UK and USA are smokers [1,22]. Smoking is associated with COPD and respiratory compromise [3] and the impact of this on swallowing has been described [23,24]. Respiratory disruption can also result in an increased risk of aspiration [23]. Respiration is the power source of vibration of the vocal folds during phonation [21] and consequently reduced breath support can result in voice changes [10]. Smoking may also result in a laryngeal disease, including Reinke’s oedema, laryngeal hyperplasia and leukoplakia, all of which can result in marked dysphonia [25]. A host of other potential comorbidities including metastatic cancer, thyroid/glandular disease, neurological disease, congestive heart failure and pulmonary fibrosis may also be present with patients with lung cancer [26]. When coupled with the disease trajectory – including gradual deterioration in respiratory function, increased fatigue and overall reduced reserve – swallowing and voice difficulties are likely to result.
Treatment effects on swallowing Toxicity from both radiotherapy and chemotherapy treatment can lead to significant difficulties with swallowing. For patients with advanced NSCLCA, radiotherapy is often given for palliation if a patient is presenting with symptoms, including haemoptysis, cough, pain and dysphagia [27]. Dosage generally depends on the patient’s overall performance status but can range from 10–12.4 Gy in a single fraction for any metastatic disease [27,28], to 30–39 Gy in 10–13 fractions [27,28]. Radiotherapy to the mediastinum causes changes to the oesophageal mucosa, which can result in oesophagitis. This causes difficult and painful swallowing characterized by a burning sensation when swallowing. It is often a dose-limiting complication for the treatment of lung cancer [29]. Radiation-induced oesophagitis can result in prolonged treatment duration and subsequent poorer treatment and survival outcomes. Rare occurrences of oesophageal stenosis as a result of antecedent radiotherapy have also been reported [30]. A number of different chemotherapy drugs and targeted agents are used to treat patients with lung cancer. Traditional chemotherapy drugs include platinum drugs (carboplatin and cisplatin), vinca alkaloids (vinorelbine) and taxanes (paclitaxel and docetaxel). A number of these drugs can cause an alteration in a patient’s taste or a dry mouth, both of which can affect swallowing [31]. Patients receiving chemotherapy can also develop oral thrush, which can result in dysphagia and occasionally mucosal ulceration causing pain [31].
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Mucositis/stomatitis can cause erythema, swelling, bleeding and painful ulceration of the mucosal lining of the mouth, which can result in difficulties maintaining nutrition orally [32,33]. Generally, with standard chemotherapies used in lung cancer, the incidence is low. However, in patients with advanced NSCLCA, in whom an activating mutation in the epidermal growth factor receptor (EGFR) has been identified, treatment includes tyrosine kinase inhibitors, which target EGFR. There are currently three drugs in use, gefitinib, erlotinib and afatinib [2,28]. With gefitinib, the incidence of grade 3 mucositis was reported as 0.2% compared with a rate of 8.7% with afatinib [34].
INTERVENTIONS TO OPTIMIZE SWALLOWING AND VOICE The previous literature that has reported on lung cancer and dysphagia and dysphonia has failed to consider treatment options. The second half of this review details the evidence for medical interventions, speech and language therapy (SLT) interventions and surgical interventions.
Medical interventions Extrinsic compression of the oesophagus may be treated with chemotherapy and radiotherapy with the aim of tumour size reduction. Pharmacological management options for dysphagia resulting from oral mucositis and oesophagitis may include analgesics [35], anti-inflammatory and/or antifungal medication. Oral thrush should be considered in all patients undergoing chemotherapy treatment and signs should be treated promptly to prevent exacerbation of problems. Patients should be assessed prior to each new cycle of treatment. If patients are having problems with mucositis, a dry mouth or alteration in taste, to an extent that it is affecting their nutritional status, then careful consideration for continuing with further chemotherapy should be made. The options would include delaying treatment to allow the resolution of symptoms, the addition of supportive measures, dietetic input and pharmacological management whilst continuing with treatment or continuing with treatment at a reduced dose.
Speech and language therapy interventions The underlying cause for the swallowing difficulty must be identified before any treatment can be initiated. The SLT conducts a clinical evaluation 194
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of swallowing, including a detailed case history, oro-motor examination and oral trials if appropriate [36]. The SLT may recommend instrumental assessments [such as a modified barium swallow (MBS) or fibreoptic endoscopic evaluation of swallowing (FEES)], to evaluate the nature and extent of swallowing disorder and to plan rehabilitation/intervention [37]. Behavioural and dietary treatments are often the most effective intervention techniques for immediate relief of symptoms [36] and close working with the dietician is essential. Given that healthcare staff may not be aware of the potential swallowing issues for these patients, education of staff should form a major part of any intervention. In severe cases wherein the patient is unable to maintain nutrition and hydration orally, nonoral feeding may be required. However, the relative benefits should be considered in the context of deteriorating disease and in partnership with the multidisciplinary team [38]. If the swallowing difficulty is suspected to result from laryngeal dysfunction, the SLT should initiate a referral to the otoloaryngologist for assessment and consideration of vocal cord augmentation [39]. In addition, the SLT should assess the patient for suitability for behavioural interventions to optimize swallowing safety and comfort [36,37]. For patients with dysphonia, an assessment of voice should be undertaken by the SLT following consultation with an otolaryngologist. The extent of vocal dysfunction must be quantified and a range of compensatory techniques can be trialled. Interventions should aim to maximize both vocal function and voice-related QOL [14]. Voice therapy should focus on vocal hygiene, maximal phonatory coordination, optimal breath support for speech and avoidance of hyper-functional behaviours [40]. In the case of UVCP, the patient should be considered for vocal cord augmentation [38,39]. The SLT should contribute to decision-making regarding the potential for vocal cord augmentation [10,40]. Voice therapy may be indicated pre or post or for some patients in preference to vocal cord medialization [40].
Surgical interventions Surgical techniques for the management of oesophageal compression causing obstruction and tumour invasion resulting in fistulization are available [18]. The surgical procedure often includes the insertion of a stent [18,30]. There are several surgical techniques available for the management of UVCP, many of which have shown positive outcomes for swallowing [41,42] and voice [14,15 ,38,39,43]. &&
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Historically, Isshiki type I thyroplasty was considered the ‘gold standard’ surgical technique for UVCP providing a permanent augmentation of the paralysed vocal cord [15 ]. Previously, vocal cord augmentation using injection thyroplasty under general anaesthetic with materials such as Teflon has been used [43]. Teflon is no longer used due to complications such as granulation formation [12,42]. More recently, injection thyroplasty under general anaesthetic has been completed using biomaterials such as Bioplastique [14]. However, there has been an increasing interest in the use of injection thyroplasty, which is administered under local anaesthetic, for example, using calcium hydroxylapatite [38]. The procedure can be completed in an outpatient clinic [15 ,38,39]. Office-based procedures offer several advantages for patients with lung cancer. As well as allowing for prompt intervention, it avoids anaesthetic and other risk factors for this patient group [15 ,38,40]. The ability to perform the procedure without interruption to treatment schedules or anticoagulation regimes is an important consideration [39]. Given the advantages and success in improving voice, swallowing and QOL outcomes, this technique has now become the standard approach in many settings [39]. &&
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CONCLUSION The number of worldwide cancer cases is set to increase by 75% in the next two decades [44]. Lung cancer will remain a major cause of morbidity and mortality [45]. Given limited life expectancy for patients with lung cancer, the aim of care is to maximize QOL and minimize symptom burden. Central to that aim is the identification and treatment of swallowing and voice dysfunction associated with lung cancer. To date, there is a lack of literature on the nature and extent of voice and swallowing impairment. There is an urgent need for well constructed prevalence studies that employ robust and sensitive multidimensional dysphagia and dysphonia assessments. Similarly, outcome studies examining SLT, medical and surgical interventions with clearly defined treatment goals are clearly required. These studies should include functional and patient-reported outcome measures to develop the evidence base and to ensure that interventions are both timely and appropriate. Acknowledgements Grainne Brady, Dr Jaishree Bhosle and Dr Justin Roe acknowledge support from the National Institute for Health Research NIHR RM/ICR Biomedical Research Centre.
Financial support and sponsorship Miss Brady is funded by the National Institute for Health Research (NIHR) for a Master’s of Research programme at Kingston and St George’s University of London. Dr Roe’s work is funded by the Royal Marsden Cancer Charity, The Royal Marsden Hospital, Fulham Road, London, SW3 6JJ, UK. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Cancer Research UK. Cancer statistics key facts lung cancer. 2014. http:// publications.cancerresearchuk.org/downloads/Product/CS_KF_LUNG.pdf. [Accessed 9 December 2014] 2. NICE. The diagnosis and treatment of lung cancer (update). 2011. http:// www.nice.org.uk/guidance. [Accessed 30 November 2014] 3. National Cancer Institute. Small cell lung cancer treatment. 2014. http:// www.cancer.gov/cancertopics/pdq/treatment/small-cell-lung/healthprofessional/page1#Section_25. [Accessed 3 December 2014] 4. NICE. 2004. http://www.nice.org.uk/guidance/csgsp/evidence/supportiveand-palliative-care-the-manual-2. [Accessed 2 November 2004] 5. Roe JW, Leslie P, Drinnan MJ. Oropharyngeal dysphagia: the experience of patients with nonhead and neck cancers receiving specialist palliative care. Palliat Med 2007; 10:567–574. 6. Raber-Durlacher J, Brennan M, Verdonck-de Leeuw I, et al. Swallowing dysfunction in cancer patients. Support Care Cancer 2012; 20:433–443. 7. Camidge DR. The causes of dysphagia in carcinoma of the lung. J R Soc Med 2001; 94:567–572. 8. Sasaki CT, Leder SB. Comments on selected recent dysphagia literature. Dysphagia 2003; 18:64–68. 9. Amin R. Dysphagia in lung cancer. J R Soc Med 2002; 95:55–56. 10. Lee CF, Carding PN, Fletcher M. The nature and severity of voice disorders in lung cancer patients. Logoped Phoniatr Vocol 2008; 33:93–103. 11. Loughran S, Alves C, MacGregor FB. Current aetiology of unilateral vocal fold paralysis in a teaching hospital in the West of Scotland. J Laryngol Otol 2002; 116:907–910. 12. Huins C, Lobeck E, Roe J. Unilateral vocal cord paralysis in patients with lung cancer. Eur J Palliat Care 2009; 16:214–217. 13. Bhattacharyya N, Kotz T, Shapiro J. Dysphagia and aspiration with unilateral vocal cord immobility: incidence, characterization, and response to surgical treatment. Ann Otol Rhinol Laryngol 2002; 111:672–679. 14. Alves CB, Loughran S, MacGregor FB, et al. Bioplastique medialization therapy improves the quality of life in terminally ill patients with vocal cord palsy. Clin Otolaryngol 2002; 27:387–391. 15. Powell J, Carding P, Birdi R, Wilson JA. Injection laryngoplasty in the out&& patient clinic under local anaesthetic: a case series of sixty- eight patients. Clin Otolaryngol 2014; 39:224–227. An investigation of self-reported and perceptually rated voice outcomes in patients undergoing local anaesthetic injection laryngoplasty in the outpatient clinic setting. 16. Spector BC, Netterville JL, Billante C, et al. Quality-of-life assessment in patients with unilateral vocal cord paralysis. Otolaryngol Head Neck Surg 2001; 125:176–182. 17. Hassan WA, Darwish K, Shalan IM, et al. Aetiologic mechanisms of dysphagia && in lung cancer: a case series. Egypt J Chest Dis Tuber 2014; 63:435–442. To date this is the only prospective study we are aware of investigating the prevalence of dysphagia in patients with lung cancer. This paper also highlights the different aetiologic mechanisms for dysphagia among lung cancer patients based on clinican diagnosis. 18. Ahmet Dobrucali EC. Palliation of malignant esophageal obstruction and fistulas with self expandable metallic stents. World J Gastroenterol 2010; 16:5739–5745. 19. Leslie P, Drinnan MJ, Ford GA, Wilson JA. Swallow respiratory patterns and aging: presbyphagia or dysphagia? J Gerontol A Biol Sci Med Sci 2005; 60:391–395. 20. Logemann J. Evaluation and treatment of swallowing disorders. 2nd ed. Texas: PRO-ED; 1998. 21. Cohen SM, Elackattu A, Noordzij JP, et al. Palliative treatment of dysphonia and dysarthria. Otolaryngol Clin North Am 2009; 42:107–121.
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35. Yang JC, Hirsh V, Schuler M, et al. Symptom control and quality of life in LUXLung 3: a phase III study of afatinib or cisplatin/pemetrexed in patients with advanced lung adenocarcinoma with EGFR mutations. J Clin Oncol 2013; 31:3342–3350. 36. Langmore SE, Grillone G, Elackattu A, Walsh M. Disorders of swallowing: palliative care. Otolaryngol Clin North Am 2009; 42:87–105. 37. Bu¨low M, Martin-Harris B. The therapeutic swallow study. In: Ekberg E, editor. Dysphagia: diagnosis and treatment. Berlin: Springer; 2012. pp. 411–424. 38. Karagama Y, Hurren A, Carding P, Lindsey L. Short-term voice quality results following percutaneous medialisation of the paralysed vocal cord under local anaesthesia using calcium hydroxyapatite gel: how we do it. Clin Otolaryngol 2008; 33:362–366. 39. Kupferman ME, Acevedo J, Hutcheson KA, Lewin JS. Addressing an unmet need in oncology patients: rehabilitation of upper aerodigestive tract function. Ann Oncol 2011; 22:2299–2303. 40. Heuer RJ, Thayer Sataloff R, Emerich K, et al. Unilateral recurrent laryngeal nerve paralysis: the importance of ‘preoperative’ voice therapy. J Voice 1997; 11:88–94. 41. Kraus DH, Ali MK, Ginsberg RJ, et al. Vocal cord medialization for unilateral paralysis associated with intrathoracic malignancies. J Thorac Cardiovasc Surg 1996; 111:334–339. 42. Nayak VK, Bhattacharyya N, Kotz T, Shapiro J. Patterns of swallowing failure following medialization in unilateral vocal fold immobility. Laryngoscope 2002; 112:1840–1844. 43. Hughes RGM, Morrison M. Vocal cord medialization by transcutaneous injection of calcium hydroxylapatite. J Voice 2005; 19:674–678. 44. Bray F, Jemal A, Grey N, et al. Global cancer transitions according to the Human Development Index (2008-2030): a population- based study. Lancet Oncol 2012; 13:790–801. 45. America Lung Association. Key facts about tobacco use among children and teenagers. 2010. http://www.lung.org/stop-smoking/about-smoking/ facts-figures/children-teens-and-tobacco.html. [Accessed 3 December 2014]
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