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Efficacy survey of swallowing function and quality of life in response to therapeutic intervention following rehabilitation treatment in dysphagic tongue cancer patients
European Journal of Oncology Nursing 16 (2012) 54e58
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
Efficacy survey of swallowing function and quality of life in response to therapeutic intervention following rehabilitation treatment in dysphagic tongue cancer patients Yan Zhen a, Jian-guang Wang a, Duo Tao b, Hua-Jun Wang c, Wei-Liang Chen a, * a b c
Department of Oral and Maxillofacial Surgery, Sun Yet-sen Memorial Hospital (Second Affiliated Hospital) of Sun Yat-sen University, 107 Yan-jiang Road, Guangzhou 510120, China Department of Otolaryngology Surgery, Sun Yet-sen Memorial Hospital (Second Affiliated Hospital) of Sun Yat-sen University, Guangzhou, China Department of nurses management of Guangdong Provincial People’s Hospital, Guangzhou, China
a b s t r a c t Keywords: Dysphagia Tongue resection and rehabilitation Swallowing training Quality of life Oral cancer Screening tool Swallowing function
Purpose: This quasi-experimental parallel cluster study was carried out to investigate the utility of interdisciplinary swallowing therapy exercises in improving swallowing function and quality of life (QOL) in dysphagic cancer patients following tongue resection and subsequent rehabilitation treatment. Methods: All subjects in the experimental group underwent a structured swallowing training program. The subjects in the experimental group (n ¼ 23) received 30 min of swallowing training each day, 6 days per week for 2 weeks. The control group (n ¼ 23) received no training. Analysis of variance was used, and the M.D. Anderson Dysphagia Inventory (MDADI) discriminated between groups of subjects. Results: Patients who underwent structured swallowing training (n ¼ 23) showed improvement in the overall MDADI score (P < 0.01) compared with the control population. Furthermore, a separate analysis of individual domains of the MDADI (global, emotional, functional, and physical) demonstrated improved QOL. Although the mean score for tongue rehabilitation indicated that 50% subjects in the functional subscale were improved compared with the control population, the difference was not statistically significant (P > 0.05). Conclusions: This study used objectively timed swallowing tests, an interdisciplinary swallowing therapy protocol, and a swallowing questionnaire to evaluate the effects of swallowing training. We found that implementation of swallowing education and exercises improved dysphagia and QOL in cancer patients following tongue resection and rehabilitation. Furthermore, this study indicated that swallowing safety and dysphagia training for nursing professionals is effective. Ó 2011 Elsevier Ltd. All rights reserved.
Introduction Postsurgical dysphagia in tongue cancer patients is a common and serious problem that can lead to pneumonia, dehydration, malnutrition, and a reduced quality of life (QOL) (Gaziano, 2002). Financial costs include a longer length of stay, expenses for antibiotics, X-rays, increased nursing time, and physician consultations (Cichero et al., 2009). In terms of speech and swallowing, patients undergoing 3/4 or total anterior glossectomy had poorer outcome than those receiving either 1/4 or 1/2 glossectomy (Brown et al., 2006). The tongue and soft palate are the most important organs in the oral cavity and oropharynx for the provision of speech and swallowing. The mandible and maxilla are static structures that can
* Corresponding author. Tel.: þ86 020 81332429; fax: þ86 020 81332853. E-mail address: [email protected] (W.-L. Chen). 1462-3889/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ejon.2011.03.002
be replaced with vascularized bone, restoring both the form and function of the ablated tissues (Brown, 2008). Appropriate replacement of ablated tissue with free tissue transfer greatly improves functional and QOL outcomes. As long as the tissue is replaced and contraction avoided, the detrimental effect on function is limited. Free flaps can provide vascularized and sensitized skin cover to increase the rate of healing and avoid contraction of the remaining tissues, but they cannot replace the complex muscular movements of the tongue and soft palate (Brown et al., 2006). Therefore, organ preservation appears to translate into functional preservation, at least in tongue cancer. These findings lend objective support to the recommendation for concurrent swallowing therapy as the treatment of choice in cases of stage III and IV tongue cancer. Dysphagia occurs in up to 50% of head and neck cancer survivors, and is estimated to affect 10,000e20,000 new cases per year in the USA (Kazi et al., 2008), especially those with oral cavity and
Y. Zhen et al. / European Journal of Oncology Nursing 16 (2012) 54e58
oropharyngeal cancers (Pauloski et al., 2006). The recovery of swallowing function is integral to rehabilitation of surgically treated cancer patients; however, recovery is very slow and often incomplete following treatment (Nicoletti et al., 2004). Videofluoroscopy is often used to determine the extent of dysphagia. However, patient-reported scales or questionnaires are helpful for assessing how patients view their swallowing ability following treatment and how changes in swallowing affect their QOL (Kazi et al., 2008). The M.D. Anderson Dysphagia Inventory (MDADI) is a validated and reliable self-administered survey designed specifically for evaluating the impact of dysphagia on QOL in patients who have undergone treatment for head and neck cancer (Chen et al., 2001; Kazi et al., 2008). There is accumulating evidence that learning new motor skills leads to significant changes in corticomotor control. Appropriate swallowing treatment could reduce complications related to impairment of swallowing function. Several reviews have highlighted the neuroanatomical pathways involved in the control of the tongue musculature (Miller, 2002; Sawczuk and Mosier, 2001), and a series of studies with intracortical microstimulation in conscious monkeys have been systematically outlined. The functional properties of neurons in the primary motor cortex, primary somatosensory cortex, cortical masticatory area, and swallowing cortex are related to tongue movements (Yamamura et al., 2002; Yao et al., 2002). Recently, several studies involving swallowing function have been reported. There is increasing evidence for the effectiveness of different treatments, such as direct dysphagia treatment, compensatory training (Lin et al., 2003), electrical stimulation treatment, and the Mendelsohn maneuver (Peck et al., 2010). Diagnosis and management of dysphagia are most commonly performed by speech pathologists because of their training in the anatomy, neuroanatomy, and physiology of deglutition (Cichero et al., 2009). However, speech pathologists are usually available only during standard working hours on weekdays. Nurses, however, provide 24-h care. Early signs and symptoms of swallowing problems are more likely to go unnoticed by the healthcare team. A dysphagia clinical nurse specialist can focus attention on this critical problem, and nurses play a key role in identifying, assessing, managing, and preventing complications related to dysphagia (Werner, 2005). This study was performed to evaluate the efficacy of an interdisciplinary swallowing therapy protocol by well-trained nursing professionals in improving swallowing function and QOL in patients following tongue surgery for squamous cell cancer. Materials and methods Study design A quasi-experimental parallel cluster design of swallowing function and QOL was performed to determine the efficacy of swallowing exercises. Subjects who fulfilled the following criteria were eligible for participation: (1) those who had undergone tongue resection and rehabilitation; (2) complete wound healing after surgery, allowing for functional training; (3) receiving nutrition and hydration via oral intake; (4) MDADI score of 60 or lower; and (5) able to understand Mandarin or Chinese dialect. Between September 2007 and December 2009, 62 of 146 tongue cancer patients who had undergone tongue resection and rehabilitation were diagnosed with dysphagia. Of these, 46 were selected for the study (23 in the control group and 23 in the experimental group). All subjects and their families gave informed consent and received compensation for their participation. All subjects were patients at the Department of Oral and Maxillofacial Surgery of the Second Affiliated Hospital of Sun Yat-sen University,
55
Guangzhou, China. This study was approved and reviewed by the Institutional Review Board of Sun Yat-sen Memorial Hospital of Sun Yat-sen University. The subjects ranged in age from 28 to 71 years (median, 55.8 years); 29 were men and 17 were women. Clinically, 6, 10, 21, and 9 patients had stage IeIV cancer, respectively. Of the 46 subjects, 12 had tumors located at the floor of the tongue, 14 at the side of the tongue, 7 near the throat, and 13 at the top of the tongue. Nine of the 46 patients underwent in-continuity segmental mandibular resection, and the remainder underwent mandibular rim resection only. The extent of tongue resection in each patient varied between 10% and 75%. All histological evaluations showed squamous cell carcinoma without psilate regional lymph node metastasis, and the margins were tumor-free. Hypoglossal and lingual nerves were resected on the affected side but preserved on the contralateral side in patients who underwent subtotal glossectomy. Bilateral hypoglossal and lingual nerves were resected in patients who underwent total glossectomy. Laryngeal suspension and cricopharyngeal myotomy procedures were based on the following 2 criteria: (1) excision of the bilateral suprahyoid muscles, and (2) excision of 50% or more of the tongue base. To avoid confounding the effects of subjects in the experimental and control groups in the same ward, 2 floors of 8 wards each were assigned to the control and experimental groups based on a subject ratio of 1:1 (control:experimental). Thus, 25 subjects on the first floor (8 wards) were assigned to the control group, and 25 subjects on the second floor (8 wards) were assigned to the experimental group. Four subjects were lost because they left China, died, or withdrew from the study. Finally, a total of 46 (92%) subjects participated in the present study (23 subjects in each group). Research procedure The experimental group received 30 min general swallowing therapy sessions 6 days per week for 2 weeks. The control group received no therapy. For ethical reasons, the control group received identical swallowing therapy after collection of the post-test data. All experts agreed with the training protocol. The expert team consisted of a rehabilitation physician, a rehabilitation nurse, and a speech therapist from the Department of Rehabilitation in the Department of Oral and Maxillofacial Surgery, Second Affiliated Hospital of Sun Yat-sen University, Guangzhou, China. The rehabilitation nurse had more than 5 years of clinical experience in surgery units and underwent 1 month of clinical training on swallowing therapy for dysphagic patients to ensure competency in the screening and management of swallowing problems. The rehabilitation nurse completed a questionnaire before beginning the training, which was used to assess baseline knowledge, skills, and confidence in the area of dysphagia. The rehabilitation nurse’s training and questionnaire were administered by a speech therapist and the therapist performing the training protocol. The subjects’ data were collected by a rehabilitation physician, and swallowing therapy was performed by the rehabilitation nurse. All data were collected at the beginning of the study and at the end of 2 weeks. However, to prevent any changes in behavior of the rehabilitation nurse at the time of the study, ward managers were not contacted. Swallowing symptoms questionnaire The MDADI performance status scale, which measures a patient’s global, physical, emotional, and functional perceptions of swallowing dysfunction, was administered to each patient (Barringer et al., 2009). The global assessment consists of a single question assessing how swallowing affects the overall daily routine and represents a general overall assessment of swallowing-related
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Y. Zhen et al. / European Journal of Oncology Nursing 16 (2012) 54e58
QOL. The emotional subscale of the MDADI consists of statements representing the individual’s affective or emotional responses to dysphagia. The functional subscale assesses the impact of the individual’s swallowing problems on his/her daily activities/life. The physical subscale represents self-perception of swallowing difficulties. For each item on the MDADI scale, 5 possible responses (strongly agree, agree, no opinion, disagree, and strongly disagree) were available, and these were scored. The first question (global subscale) was scored individually. All other questions regarding each aspect (emotional, functional, and physical) of dysphagia were summed, and the mean score was calculated. This score was within the range of 0 (extremely low function) to 100 (high function). Thus, a higher MDADI score represented better day-to-day functioning and better QOL. Swallowing training protocol The design of the swallowing training protocol was based on a literature review and the experience of the research team. The protocol included direct and indirect therapies. Direct therapy usually focused on the particular tasks or skills to be learned, and included compensatory strategies such as diet modification; environmental arrangement; positioning (including chin-down and head rotation); and feeding and compensatory swallowing strategies, including the Mendelsohn maneuver and supraglottic and effortful swallowing. Compensatory training may teach the patient to implement strategies for further reduction of aspiration risk. These strategies may be the only option for the patient to continue feeding by mouth. For example, a chin-tuck strategy is commonly recommended. This strategy places the epiglottis, a cartilage flap located immediately above the larynx, in a more forward position, allowing for improved airway protection during swallowing. A head turn may be beneficial for patients with unilateral vocal fold paralysis to improve vocal fold closure when swallowing, or for patients with hemiparesis affecting movement of the bolus on one side of the throat. The Mendelsohn maneuver raises the larynx and opens the esophagus when swallowing; supraglottic swallowing offers laryngeal protection; and effortful swallowing increases pharyngeal constriction and reduces pharyngeal residue. Indirect therapy focuses on rehabilitating the underlying dysfunction of the central nervous system, in the hope that improvement of the dysfunction will transfer to skill attainment. Indirect therapies used in this study included physical maneuvers and thermal stimulation. Thermal stimulation was used in patients with a delayed trigger of the swallowing reflex. Physical maneuvers included lip and lingual exercises. Oral motor exercises (lip, cheek, lingual, and laryngeal exercises) were used for subjects showing oral motor weakness or incoordination. Results Of the questionnaires initially distributed, 92 were completed and returned. Inclusion criteria were met by 73 patients (79.3%). Swallowing problems were reported by 51 patients (69.8%). A total of 46 patients with swallowing problems completed the study, including 23 in the experimental group and 23 in the control group. Objective assessments of swallowing were performed pre- and post-training. Postoperative studies were performed 2e3 weeks and 4e1 months following surgery. These timings allowed for the performance of postoperative assessments and training. The minimum time to obtain the questionnaire was 2 weeks after treatment, and the maximum time was 4 weeks (experimental group 20.87 4.65 days; control group, 21.13 3.89 days). Comparisons between the 2 groups revealed no significant
Table 1 Characteristics of patients with tongue rehabilitation.
Gender (M/F) Age (years) Tongue resection and rehabilitation 50% <50% Flap Free flap Pedicled flap Neck dissection Unilateral Bilateral Tumor stage I II III IV Mandibulectomy resection Segmental Marginal/preserved
Experimental group (n ¼ 23)
Control group (n ¼ 23)
Univariate
P-value
17/6 60.52 5.55
14/9 57.47 5.72
c2 ¼ 0.890 t ¼ 1.829 c2 ¼ 0.090
0.345 0.074 0.765
10 13
9 14
c2 ¼ 0.093
0.760
9 14
8 15
c2 ¼ 1.786
0.181
7 5
8 4
c2 ¼ 0.031
0.861
3 5 11 4
3 5 10 5
c2 ¼ 0.119
0.730
5 18
6 17
differences in age, gender, extent of rehabilitation, tumor stage, or tongue defect reconstruction type. The demographic features of the 2 groups are shown in Table 1. The mean MDADI score in the experimental group after swallowing training was 60.84 4.61. The mean MDADI global score was 60.00 5.29, mean emotional score was 57.04 6.08, mean functional score was 64.74 5.34, and mean physical score was 61.57 5.41; all scores were significantly higher in the controls than in the experimental group (P ¼ 0.018). The individual mean global, emotional, and physical subscale scores were also significantly higher in the experimental group after swallowing training than at baseline (P ¼ 0.017). With regard to reconstruction modalities, there were significant differences between patients with <50% tongue rehabilitation, who had a higher swallowing QOL score, and those with 50% tongue rehabilitation. Patients with 50% tongue rehabilitation had significantly reduced MDADI scores (median, 55.69 2.86) (Table 2). Although the mean functional subscale score of patients with 50% tongue rehabilitation improved, the difference was not statistically significant (P ¼ 0.734). Tumor staging and MDADI scores were also compared. Stage I patients’ MDADI scores were significantly higher than those of stage IV patients, and this difference was statistically significant (P ¼ 0.000). Tumors located in the posterior of the tongue resulted in poorer scores than those in other locations (P ¼ 0.022), and smaller, earlystage tumors resulted in better swallowing scores (P ¼ 0.000). With regard to treatment modalities, patients who received rehabilitation with either a free or pedicled flap after tongue cancer surgery did not show any difference in the quality of scoring in any domain, including the overall score, in comparison with the overall score of patients who did not receive swallowing training (P ¼ 0.432) (Table 3). Discussion The traditional focus of oncologists of all disciplines has been the cure of patients. Unfortunately, this focus on cure has sometimes resulted in neglect of the functional outcomes and patients’ QOL. Although cure must clearly remain the major goal, the latter outcomes are equally important. This is especially true for tumors such as cancer of the tongue base, which, when treated, can produce profound changes in the patient’s life.
Y. Zhen et al. / European Journal of Oncology Nursing 16 (2012) 54e58
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Table 2 Extent of tongue rehabilitation and MDADI subscale scores. MDADI
Extent of tongue rehabilitation <50% 1 (n ¼ 9)
Global Emotional Functional Physical
64.56 61.22 69.78 67.00
P-value
2 (n ¼ 10)
3.28 2.95 3.77 2.87
60.60 57.50 68.60 62.00
Extent of tongue rehabilitation 50% 1 (n ¼ 14)
2.84 2.27 4.33 3.56
0.012 0.006 0.537 0.004
57.07 54.36 61.50 58.07
4.14 6.11 3.25 3.29
P-value
2 (n ¼ 13) 52.92 48.85 60.77 52.92
5.12 4.56 4.51 4.01
0.029 0.014 0.632 0.001
MDADI ¼ M.D. Anderson Dysphagia Inventory; 1 ¼ experimental group; 2 ¼ control group.
A variety of validated questionnaires for dysphagia, such as the Functional Assessment of Cancer Therapy-General (FACT-G) Scale and The European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC, QLQ-C30), have been adopted by other researchers (Kazi et al., 2008). However, these tools were considered to be too long to be efficient for triage. The acceptability of a screening tool is determined by the cost of the test and time taken to administer it (Cichero et al., 2009). In addition, these questionnaires have limited numbers of items specifically related to swallowing function, and cannot be used readily by diagnostic head and neck cancer groups (Lin et al., 2003). Although the MDADI was specifically designed for head and neck cancer patients, we used it as a dysphagia-related QOL questionnaire because it is sensitive, validated, and easily applicable. The MDADI provides useful information and can contribute to decision-making based on patient feedback. In addition, the MDADI is a patientfriendly, easy-to-follow questionnaire that usually takes less than 5 min to complete. We compared patients who had received swallowing therapy with those who performed the swallowing exercises after tongue rehabilitation. The results of the present study support the previously observed trend of better swallowing outcomes with swallowing therapy compared with no swallowing therapy for oropharyngeal cancer. The significant differences observed in the experimental group on the MDADI functional and emotional subscales indicated that survivors with swallowing therapy had more confidence in their swallowing ability and had less problems with food preparation and eating in public places. These findings were similar to those reported in a recent study of oropharyngeal carcinoma patients (Svensson et al., 2006). The global, emotional, and physical subscale scores on the MDADI showed significant improvement after swallowing therapy in patients who had undergone resection of 3/4 or all of the anterior, and especially the posterior, tongue (P < 0.005); however, the improvement in functional subscale score was not significant (P > 0.05). This lack of difference may have been because the scores of each item were dichotomous. It is also difficult to see significant changes over a short period of time. An alternative explanation is that the surgery treatment period resulted in deconditioning. If this
Table 3 Type of rehabilitation and MDADI subscale scores.
Experimental group
Control group
Free flap
Pedicled flap
t
P-value
Global Emotional Functional Physical
9 59.56 57.89 64.33 60.56
5.55 5.18 5.43 5.34
14 60.29 56.50 65.00 62.21
5.31 6.72 5.46 5.55
0.316 0.526 0.286 0.710
0.755 0.604 0.777 0.486
Global Emotional Functional Physical
8 57.13 51.88 63.50 57.00
4.73 5.30 5.59 5.35
15 55.80 53.00 64.53 56.80
6.29 6.07 6.01 6.39
0.520 0.441 0.394 0.075
0.608 0.664 0.698 0.941
is correct, strategies aimed at maintaining the physiological components of swallowing function, such as hyolaryngeal excursion, pharyngeal contraction, or pharyngeal dilation during treatment, may result in better long-term swallowing outcomes. However, the neurological examination score in the experimental group showed a significant improvement compared with that in the control group. Further investigation of the differences between groups showed that patients in the experimental group had greater improvement in clearing their throats, coughing, and moving their tongues, suggesting that muscles controlled by the glossopharyngeal, vagus, and hypoglossal nerves had improved. China currently experiences a much greater shortage of speech therapists than most Western countries. Even acute care hospitals have difficulty recruiting speech therapists, and no long-term care facility has “on-call” speech therapists available. Nurses should refer patients only when essential; the nursing role could be expanded to include swallowing therapies. The protocol for swallowing training is noninvasive and includes oral exercises, positioning of the head and neck, and food modification. This study confirms the effectiveness of swallowing training by trained nurses for postsurgical tongue cancer patients. By facilitating appropriate management of patients with swallowing impairments, nurses may also decrease inappropriate referrals, increase their confidence in managing patients, and maximize the contribution of speech therapists in clinical practice. Study limitations Although this study confirmed the effectiveness of swallowing training in improving swallowing functions and QOL, there were several limitations. First, the sample size was small, and patients were not randomized into the two groups. Second, we did not use video fluoroscopy to diagnose swallowing disorders, but instead used MDADI. Third, we did not measure actual strength using a force transducer during the lip and tongue exercises for disorders in the oral stage. Therefore, we could not conclude that tongue muscle strength had actually increased. Furthermore, we did not measure laryngeal movement during laryngeal exercises for disorders in the pharyngeal stage. We reported the elevation of the tongue rather than the hyolaryngeal complex. In conclusion, effortful swallowing stimulation increases the degree of hyoid elevation after tongue cancer treatment. However, its short- and long-term effectiveness in increasing tongue and laryngeal elevation and improving swallowing safety in patients with dysphagia must be evaluated in future studies. Disclosure The authors declare that there is no source of financial or other support or any financial or professional relationships that may pose a competing interest. Conflict of interest statement The authors declare no conflict of interests.
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References Barringer, D.A., Hutcheson, K.A., Sturgis, E.M., Kies, M.S., Lewin, J.S., 2009. Effect of induction chemotherapy on speech and swallowing function in patients with oral tongue cancer. Head and Neck 31, 611e617. Brown, J.S., Rogers, S.N., Lowe, D., 2006. A comparison of tongue and soft palate squamous cell carcinoma treated by primary surgery in terms of survival and quality of life outcomes. International Journal of Oral and Maxillofacial Surgery 35, 208e214. Brown, J.S., 2008. Reconstruction of the maxilla with loss of the orbital floor and orbital preservation: a case for the iliac crest with internal oblique. Seminars in Plastic Surgery 22, 161e174. Chen, A.Y., Frankowski, R., Bishop-Leone, J., Hebert, T., Leyk, S., Lewin, J., Goepfert, H., 2001. The development and validation of a dysphagia-specific quality-of-life questionnaire for patients with head and neck cancer: the M.D. Anderson dysphagia inventory. Archives of Otolaryngology-Head and Neck Surgery 127, 870e876. Cichero, J.A., Heaton, S., Bassett, L., 2009. Triaging dysphagia: nurse screening for dysphagia in an acute hospital. Journal of Clinical Nursing 18, 1649e1659. Gaziano, J.E., 2002. Evaluation and management of oropharyngeal dysphagia in head and neck cancer. Cancer Control 9, 400e409. Kazi, R., Prasad, V., Venkitaraman, R., Nutting, C.M., Clarke, P., Rhys-Evans, P., Harrington, K.J., 2008. Questionnaire analysis of swallowing-related outcomes following glossectomy. Journal for Oto-Rhino-Laryngology, Head and Neck Surgery 70, 151e155. Lin, L.C., Wang, S.C., Chen, S.H., Wang, T.G., Chen, M.Y., Wu, S.C., 2003. Efficacy of swallowing training for residents following stroke. Journal of Advanced Nursing 44, 469e478.
Miller, A.J., 2002. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Critical Reviews in Oral Biology and Medicine 13, 409e425. Nicoletti, G., Soutar, D.S., Jackson, M.S., Wrench, A.A., Robertson, G., 2004. Chewing and swallowing after surgical treatment for oral cancer: functional evaluation in 196 selected cases. Plastic and Reconstructive Surgery 114, 329e338. Pauloski, B.R., Rademaker, A.W., Logemann, J.A., Newman, L., MacCracken, E., Gaziano, J., Stachowiak, L., 2006. Relationship between swallow motility disorders on videofluorography and oral intake in patients treated for head and neck cancer with radiotherapy with or without chemotherapy. Head and Neck 28, 1069e1076. Peck, K.K., Branski, R.C., Lazarus, C., Cody, V., Kraus, D., Haupage, S., Ganz, C., Holodny, A.I., Kraus, D.H., 2010. Cortical activation during swallowing rehabilitation maneuvers: a functional MRI study of healthy controls. Laryngoscope 20, 2153e2159. Sawczuk, A., Mosier, K.M., 2001. Neural control of tongue movement with respect to respiration and swallowing. Critical Reviews in Oral Biology and Medicine 12,18e37. Svensson, P., Romaniello, A., Wang, K., Arendt-Nielsen, L., Sessle, B.J., 2006. One hour of tongue-task training is associated with plasticity in corticomotor control of the human tongue musculature. Experimental Brain Research 173, 165e173. Werner, H., 2005. The benefits of the dysphagia clinical nurse specialist role. Journal of Neuroscience Nursing 37, 212e215. Yamamura, K., Narita, N., Yao, D., Martin, R.E., Masuda, Y., Sessle, B.J., 2002. Effects of reversible bilateral inactivation of face primary motor cortex on mastication and swallowing. Brain Research 944, 40e55. Yao, D., Yamamura, K., Narita, N., Martin, R.E., Murray, G.M., Sessle, B.J., 2002. Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. Neurophysiology 87, 2531e2541.
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
Efficacy survey of swallowing function and quality of life in response to therapeutic intervention following rehabilitation treatment in dysphagic tongue cancer patients Yan Zhen a, Jian-guang Wang a, Duo Tao b, Hua-Jun Wang c, Wei-Liang Chen a, * a b c
Department of Oral and Maxillofacial Surgery, Sun Yet-sen Memorial Hospital (Second Affiliated Hospital) of Sun Yat-sen University, 107 Yan-jiang Road, Guangzhou 510120, China Department of Otolaryngology Surgery, Sun Yet-sen Memorial Hospital (Second Affiliated Hospital) of Sun Yat-sen University, Guangzhou, China Department of nurses management of Guangdong Provincial People’s Hospital, Guangzhou, China
a b s t r a c t Keywords: Dysphagia Tongue resection and rehabilitation Swallowing training Quality of life Oral cancer Screening tool Swallowing function
Purpose: This quasi-experimental parallel cluster study was carried out to investigate the utility of interdisciplinary swallowing therapy exercises in improving swallowing function and quality of life (QOL) in dysphagic cancer patients following tongue resection and subsequent rehabilitation treatment. Methods: All subjects in the experimental group underwent a structured swallowing training program. The subjects in the experimental group (n ¼ 23) received 30 min of swallowing training each day, 6 days per week for 2 weeks. The control group (n ¼ 23) received no training. Analysis of variance was used, and the M.D. Anderson Dysphagia Inventory (MDADI) discriminated between groups of subjects. Results: Patients who underwent structured swallowing training (n ¼ 23) showed improvement in the overall MDADI score (P < 0.01) compared with the control population. Furthermore, a separate analysis of individual domains of the MDADI (global, emotional, functional, and physical) demonstrated improved QOL. Although the mean score for tongue rehabilitation indicated that 50% subjects in the functional subscale were improved compared with the control population, the difference was not statistically significant (P > 0.05). Conclusions: This study used objectively timed swallowing tests, an interdisciplinary swallowing therapy protocol, and a swallowing questionnaire to evaluate the effects of swallowing training. We found that implementation of swallowing education and exercises improved dysphagia and QOL in cancer patients following tongue resection and rehabilitation. Furthermore, this study indicated that swallowing safety and dysphagia training for nursing professionals is effective. Ó 2011 Elsevier Ltd. All rights reserved.
Introduction Postsurgical dysphagia in tongue cancer patients is a common and serious problem that can lead to pneumonia, dehydration, malnutrition, and a reduced quality of life (QOL) (Gaziano, 2002). Financial costs include a longer length of stay, expenses for antibiotics, X-rays, increased nursing time, and physician consultations (Cichero et al., 2009). In terms of speech and swallowing, patients undergoing 3/4 or total anterior glossectomy had poorer outcome than those receiving either 1/4 or 1/2 glossectomy (Brown et al., 2006). The tongue and soft palate are the most important organs in the oral cavity and oropharynx for the provision of speech and swallowing. The mandible and maxilla are static structures that can
* Corresponding author. Tel.: þ86 020 81332429; fax: þ86 020 81332853. E-mail address: [email protected] (W.-L. Chen). 1462-3889/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ejon.2011.03.002
be replaced with vascularized bone, restoring both the form and function of the ablated tissues (Brown, 2008). Appropriate replacement of ablated tissue with free tissue transfer greatly improves functional and QOL outcomes. As long as the tissue is replaced and contraction avoided, the detrimental effect on function is limited. Free flaps can provide vascularized and sensitized skin cover to increase the rate of healing and avoid contraction of the remaining tissues, but they cannot replace the complex muscular movements of the tongue and soft palate (Brown et al., 2006). Therefore, organ preservation appears to translate into functional preservation, at least in tongue cancer. These findings lend objective support to the recommendation for concurrent swallowing therapy as the treatment of choice in cases of stage III and IV tongue cancer. Dysphagia occurs in up to 50% of head and neck cancer survivors, and is estimated to affect 10,000e20,000 new cases per year in the USA (Kazi et al., 2008), especially those with oral cavity and
Y. Zhen et al. / European Journal of Oncology Nursing 16 (2012) 54e58
oropharyngeal cancers (Pauloski et al., 2006). The recovery of swallowing function is integral to rehabilitation of surgically treated cancer patients; however, recovery is very slow and often incomplete following treatment (Nicoletti et al., 2004). Videofluoroscopy is often used to determine the extent of dysphagia. However, patient-reported scales or questionnaires are helpful for assessing how patients view their swallowing ability following treatment and how changes in swallowing affect their QOL (Kazi et al., 2008). The M.D. Anderson Dysphagia Inventory (MDADI) is a validated and reliable self-administered survey designed specifically for evaluating the impact of dysphagia on QOL in patients who have undergone treatment for head and neck cancer (Chen et al., 2001; Kazi et al., 2008). There is accumulating evidence that learning new motor skills leads to significant changes in corticomotor control. Appropriate swallowing treatment could reduce complications related to impairment of swallowing function. Several reviews have highlighted the neuroanatomical pathways involved in the control of the tongue musculature (Miller, 2002; Sawczuk and Mosier, 2001), and a series of studies with intracortical microstimulation in conscious monkeys have been systematically outlined. The functional properties of neurons in the primary motor cortex, primary somatosensory cortex, cortical masticatory area, and swallowing cortex are related to tongue movements (Yamamura et al., 2002; Yao et al., 2002). Recently, several studies involving swallowing function have been reported. There is increasing evidence for the effectiveness of different treatments, such as direct dysphagia treatment, compensatory training (Lin et al., 2003), electrical stimulation treatment, and the Mendelsohn maneuver (Peck et al., 2010). Diagnosis and management of dysphagia are most commonly performed by speech pathologists because of their training in the anatomy, neuroanatomy, and physiology of deglutition (Cichero et al., 2009). However, speech pathologists are usually available only during standard working hours on weekdays. Nurses, however, provide 24-h care. Early signs and symptoms of swallowing problems are more likely to go unnoticed by the healthcare team. A dysphagia clinical nurse specialist can focus attention on this critical problem, and nurses play a key role in identifying, assessing, managing, and preventing complications related to dysphagia (Werner, 2005). This study was performed to evaluate the efficacy of an interdisciplinary swallowing therapy protocol by well-trained nursing professionals in improving swallowing function and QOL in patients following tongue surgery for squamous cell cancer. Materials and methods Study design A quasi-experimental parallel cluster design of swallowing function and QOL was performed to determine the efficacy of swallowing exercises. Subjects who fulfilled the following criteria were eligible for participation: (1) those who had undergone tongue resection and rehabilitation; (2) complete wound healing after surgery, allowing for functional training; (3) receiving nutrition and hydration via oral intake; (4) MDADI score of 60 or lower; and (5) able to understand Mandarin or Chinese dialect. Between September 2007 and December 2009, 62 of 146 tongue cancer patients who had undergone tongue resection and rehabilitation were diagnosed with dysphagia. Of these, 46 were selected for the study (23 in the control group and 23 in the experimental group). All subjects and their families gave informed consent and received compensation for their participation. All subjects were patients at the Department of Oral and Maxillofacial Surgery of the Second Affiliated Hospital of Sun Yat-sen University,
55
Guangzhou, China. This study was approved and reviewed by the Institutional Review Board of Sun Yat-sen Memorial Hospital of Sun Yat-sen University. The subjects ranged in age from 28 to 71 years (median, 55.8 years); 29 were men and 17 were women. Clinically, 6, 10, 21, and 9 patients had stage IeIV cancer, respectively. Of the 46 subjects, 12 had tumors located at the floor of the tongue, 14 at the side of the tongue, 7 near the throat, and 13 at the top of the tongue. Nine of the 46 patients underwent in-continuity segmental mandibular resection, and the remainder underwent mandibular rim resection only. The extent of tongue resection in each patient varied between 10% and 75%. All histological evaluations showed squamous cell carcinoma without psilate regional lymph node metastasis, and the margins were tumor-free. Hypoglossal and lingual nerves were resected on the affected side but preserved on the contralateral side in patients who underwent subtotal glossectomy. Bilateral hypoglossal and lingual nerves were resected in patients who underwent total glossectomy. Laryngeal suspension and cricopharyngeal myotomy procedures were based on the following 2 criteria: (1) excision of the bilateral suprahyoid muscles, and (2) excision of 50% or more of the tongue base. To avoid confounding the effects of subjects in the experimental and control groups in the same ward, 2 floors of 8 wards each were assigned to the control and experimental groups based on a subject ratio of 1:1 (control:experimental). Thus, 25 subjects on the first floor (8 wards) were assigned to the control group, and 25 subjects on the second floor (8 wards) were assigned to the experimental group. Four subjects were lost because they left China, died, or withdrew from the study. Finally, a total of 46 (92%) subjects participated in the present study (23 subjects in each group). Research procedure The experimental group received 30 min general swallowing therapy sessions 6 days per week for 2 weeks. The control group received no therapy. For ethical reasons, the control group received identical swallowing therapy after collection of the post-test data. All experts agreed with the training protocol. The expert team consisted of a rehabilitation physician, a rehabilitation nurse, and a speech therapist from the Department of Rehabilitation in the Department of Oral and Maxillofacial Surgery, Second Affiliated Hospital of Sun Yat-sen University, Guangzhou, China. The rehabilitation nurse had more than 5 years of clinical experience in surgery units and underwent 1 month of clinical training on swallowing therapy for dysphagic patients to ensure competency in the screening and management of swallowing problems. The rehabilitation nurse completed a questionnaire before beginning the training, which was used to assess baseline knowledge, skills, and confidence in the area of dysphagia. The rehabilitation nurse’s training and questionnaire were administered by a speech therapist and the therapist performing the training protocol. The subjects’ data were collected by a rehabilitation physician, and swallowing therapy was performed by the rehabilitation nurse. All data were collected at the beginning of the study and at the end of 2 weeks. However, to prevent any changes in behavior of the rehabilitation nurse at the time of the study, ward managers were not contacted. Swallowing symptoms questionnaire The MDADI performance status scale, which measures a patient’s global, physical, emotional, and functional perceptions of swallowing dysfunction, was administered to each patient (Barringer et al., 2009). The global assessment consists of a single question assessing how swallowing affects the overall daily routine and represents a general overall assessment of swallowing-related
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QOL. The emotional subscale of the MDADI consists of statements representing the individual’s affective or emotional responses to dysphagia. The functional subscale assesses the impact of the individual’s swallowing problems on his/her daily activities/life. The physical subscale represents self-perception of swallowing difficulties. For each item on the MDADI scale, 5 possible responses (strongly agree, agree, no opinion, disagree, and strongly disagree) were available, and these were scored. The first question (global subscale) was scored individually. All other questions regarding each aspect (emotional, functional, and physical) of dysphagia were summed, and the mean score was calculated. This score was within the range of 0 (extremely low function) to 100 (high function). Thus, a higher MDADI score represented better day-to-day functioning and better QOL. Swallowing training protocol The design of the swallowing training protocol was based on a literature review and the experience of the research team. The protocol included direct and indirect therapies. Direct therapy usually focused on the particular tasks or skills to be learned, and included compensatory strategies such as diet modification; environmental arrangement; positioning (including chin-down and head rotation); and feeding and compensatory swallowing strategies, including the Mendelsohn maneuver and supraglottic and effortful swallowing. Compensatory training may teach the patient to implement strategies for further reduction of aspiration risk. These strategies may be the only option for the patient to continue feeding by mouth. For example, a chin-tuck strategy is commonly recommended. This strategy places the epiglottis, a cartilage flap located immediately above the larynx, in a more forward position, allowing for improved airway protection during swallowing. A head turn may be beneficial for patients with unilateral vocal fold paralysis to improve vocal fold closure when swallowing, or for patients with hemiparesis affecting movement of the bolus on one side of the throat. The Mendelsohn maneuver raises the larynx and opens the esophagus when swallowing; supraglottic swallowing offers laryngeal protection; and effortful swallowing increases pharyngeal constriction and reduces pharyngeal residue. Indirect therapy focuses on rehabilitating the underlying dysfunction of the central nervous system, in the hope that improvement of the dysfunction will transfer to skill attainment. Indirect therapies used in this study included physical maneuvers and thermal stimulation. Thermal stimulation was used in patients with a delayed trigger of the swallowing reflex. Physical maneuvers included lip and lingual exercises. Oral motor exercises (lip, cheek, lingual, and laryngeal exercises) were used for subjects showing oral motor weakness or incoordination. Results Of the questionnaires initially distributed, 92 were completed and returned. Inclusion criteria were met by 73 patients (79.3%). Swallowing problems were reported by 51 patients (69.8%). A total of 46 patients with swallowing problems completed the study, including 23 in the experimental group and 23 in the control group. Objective assessments of swallowing were performed pre- and post-training. Postoperative studies were performed 2e3 weeks and 4e1 months following surgery. These timings allowed for the performance of postoperative assessments and training. The minimum time to obtain the questionnaire was 2 weeks after treatment, and the maximum time was 4 weeks (experimental group 20.87 4.65 days; control group, 21.13 3.89 days). Comparisons between the 2 groups revealed no significant
Table 1 Characteristics of patients with tongue rehabilitation.
Gender (M/F) Age (years) Tongue resection and rehabilitation 50% <50% Flap Free flap Pedicled flap Neck dissection Unilateral Bilateral Tumor stage I II III IV Mandibulectomy resection Segmental Marginal/preserved
Experimental group (n ¼ 23)
Control group (n ¼ 23)
Univariate
P-value
17/6 60.52 5.55
14/9 57.47 5.72
c2 ¼ 0.890 t ¼ 1.829 c2 ¼ 0.090
0.345 0.074 0.765
10 13
9 14
c2 ¼ 0.093
0.760
9 14
8 15
c2 ¼ 1.786
0.181
7 5
8 4
c2 ¼ 0.031
0.861
3 5 11 4
3 5 10 5
c2 ¼ 0.119
0.730
5 18
6 17
differences in age, gender, extent of rehabilitation, tumor stage, or tongue defect reconstruction type. The demographic features of the 2 groups are shown in Table 1. The mean MDADI score in the experimental group after swallowing training was 60.84 4.61. The mean MDADI global score was 60.00 5.29, mean emotional score was 57.04 6.08, mean functional score was 64.74 5.34, and mean physical score was 61.57 5.41; all scores were significantly higher in the controls than in the experimental group (P ¼ 0.018). The individual mean global, emotional, and physical subscale scores were also significantly higher in the experimental group after swallowing training than at baseline (P ¼ 0.017). With regard to reconstruction modalities, there were significant differences between patients with <50% tongue rehabilitation, who had a higher swallowing QOL score, and those with 50% tongue rehabilitation. Patients with 50% tongue rehabilitation had significantly reduced MDADI scores (median, 55.69 2.86) (Table 2). Although the mean functional subscale score of patients with 50% tongue rehabilitation improved, the difference was not statistically significant (P ¼ 0.734). Tumor staging and MDADI scores were also compared. Stage I patients’ MDADI scores were significantly higher than those of stage IV patients, and this difference was statistically significant (P ¼ 0.000). Tumors located in the posterior of the tongue resulted in poorer scores than those in other locations (P ¼ 0.022), and smaller, earlystage tumors resulted in better swallowing scores (P ¼ 0.000). With regard to treatment modalities, patients who received rehabilitation with either a free or pedicled flap after tongue cancer surgery did not show any difference in the quality of scoring in any domain, including the overall score, in comparison with the overall score of patients who did not receive swallowing training (P ¼ 0.432) (Table 3). Discussion The traditional focus of oncologists of all disciplines has been the cure of patients. Unfortunately, this focus on cure has sometimes resulted in neglect of the functional outcomes and patients’ QOL. Although cure must clearly remain the major goal, the latter outcomes are equally important. This is especially true for tumors such as cancer of the tongue base, which, when treated, can produce profound changes in the patient’s life.
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Table 2 Extent of tongue rehabilitation and MDADI subscale scores. MDADI
Extent of tongue rehabilitation <50% 1 (n ¼ 9)
Global Emotional Functional Physical
64.56 61.22 69.78 67.00
P-value
2 (n ¼ 10)
3.28 2.95 3.77 2.87
60.60 57.50 68.60 62.00
Extent of tongue rehabilitation 50% 1 (n ¼ 14)
2.84 2.27 4.33 3.56
0.012 0.006 0.537 0.004
57.07 54.36 61.50 58.07
4.14 6.11 3.25 3.29
P-value
2 (n ¼ 13) 52.92 48.85 60.77 52.92
5.12 4.56 4.51 4.01
0.029 0.014 0.632 0.001
MDADI ¼ M.D. Anderson Dysphagia Inventory; 1 ¼ experimental group; 2 ¼ control group.
A variety of validated questionnaires for dysphagia, such as the Functional Assessment of Cancer Therapy-General (FACT-G) Scale and The European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC, QLQ-C30), have been adopted by other researchers (Kazi et al., 2008). However, these tools were considered to be too long to be efficient for triage. The acceptability of a screening tool is determined by the cost of the test and time taken to administer it (Cichero et al., 2009). In addition, these questionnaires have limited numbers of items specifically related to swallowing function, and cannot be used readily by diagnostic head and neck cancer groups (Lin et al., 2003). Although the MDADI was specifically designed for head and neck cancer patients, we used it as a dysphagia-related QOL questionnaire because it is sensitive, validated, and easily applicable. The MDADI provides useful information and can contribute to decision-making based on patient feedback. In addition, the MDADI is a patientfriendly, easy-to-follow questionnaire that usually takes less than 5 min to complete. We compared patients who had received swallowing therapy with those who performed the swallowing exercises after tongue rehabilitation. The results of the present study support the previously observed trend of better swallowing outcomes with swallowing therapy compared with no swallowing therapy for oropharyngeal cancer. The significant differences observed in the experimental group on the MDADI functional and emotional subscales indicated that survivors with swallowing therapy had more confidence in their swallowing ability and had less problems with food preparation and eating in public places. These findings were similar to those reported in a recent study of oropharyngeal carcinoma patients (Svensson et al., 2006). The global, emotional, and physical subscale scores on the MDADI showed significant improvement after swallowing therapy in patients who had undergone resection of 3/4 or all of the anterior, and especially the posterior, tongue (P < 0.005); however, the improvement in functional subscale score was not significant (P > 0.05). This lack of difference may have been because the scores of each item were dichotomous. It is also difficult to see significant changes over a short period of time. An alternative explanation is that the surgery treatment period resulted in deconditioning. If this
Table 3 Type of rehabilitation and MDADI subscale scores.
Experimental group
Control group
Free flap
Pedicled flap
t
P-value
Global Emotional Functional Physical
9 59.56 57.89 64.33 60.56
5.55 5.18 5.43 5.34
14 60.29 56.50 65.00 62.21
5.31 6.72 5.46 5.55
0.316 0.526 0.286 0.710
0.755 0.604 0.777 0.486
Global Emotional Functional Physical
8 57.13 51.88 63.50 57.00
4.73 5.30 5.59 5.35
15 55.80 53.00 64.53 56.80
6.29 6.07 6.01 6.39
0.520 0.441 0.394 0.075
0.608 0.664 0.698 0.941
is correct, strategies aimed at maintaining the physiological components of swallowing function, such as hyolaryngeal excursion, pharyngeal contraction, or pharyngeal dilation during treatment, may result in better long-term swallowing outcomes. However, the neurological examination score in the experimental group showed a significant improvement compared with that in the control group. Further investigation of the differences between groups showed that patients in the experimental group had greater improvement in clearing their throats, coughing, and moving their tongues, suggesting that muscles controlled by the glossopharyngeal, vagus, and hypoglossal nerves had improved. China currently experiences a much greater shortage of speech therapists than most Western countries. Even acute care hospitals have difficulty recruiting speech therapists, and no long-term care facility has “on-call” speech therapists available. Nurses should refer patients only when essential; the nursing role could be expanded to include swallowing therapies. The protocol for swallowing training is noninvasive and includes oral exercises, positioning of the head and neck, and food modification. This study confirms the effectiveness of swallowing training by trained nurses for postsurgical tongue cancer patients. By facilitating appropriate management of patients with swallowing impairments, nurses may also decrease inappropriate referrals, increase their confidence in managing patients, and maximize the contribution of speech therapists in clinical practice. Study limitations Although this study confirmed the effectiveness of swallowing training in improving swallowing functions and QOL, there were several limitations. First, the sample size was small, and patients were not randomized into the two groups. Second, we did not use video fluoroscopy to diagnose swallowing disorders, but instead used MDADI. Third, we did not measure actual strength using a force transducer during the lip and tongue exercises for disorders in the oral stage. Therefore, we could not conclude that tongue muscle strength had actually increased. Furthermore, we did not measure laryngeal movement during laryngeal exercises for disorders in the pharyngeal stage. We reported the elevation of the tongue rather than the hyolaryngeal complex. In conclusion, effortful swallowing stimulation increases the degree of hyoid elevation after tongue cancer treatment. However, its short- and long-term effectiveness in increasing tongue and laryngeal elevation and improving swallowing safety in patients with dysphagia must be evaluated in future studies. Disclosure The authors declare that there is no source of financial or other support or any financial or professional relationships that may pose a competing interest. Conflict of interest statement The authors declare no conflict of interests.
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