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Incorporating oral health into interprofessional care teams for patients with Parkinson's disease
Parkinsonism and Related Disorders xxx (2017) 1e6
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Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Review article
Incorporating oral health into interprofessional care teams for patients with Parkinson's disease Natalia S. Rozas a, June M. Sadowsky b, Deborah J. Jones c, Cameron B. Jeter a, * a
The University of Texas Health Science Center at Houston (UTHealth) School of Dentistry, Department of Diagnostic and Biomedical Sciences, 7500 Cambridge Street, Houston, TX 77054, USA b UTHealth School of Dentistry, Department of General Practice and Dental Public Health, 7500 Cambridge Street, Houston, TX 77054, USA c UTHealth School of Nursing, Department of Nursing Systems, 6901 Bertner Ave., Houston, TX 77054, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 April 2017 Received in revised form 4 July 2017 Accepted 15 July 2017
Parkinson's disease (PD) is a progressive neurodegenerative disorder that primarily affects the motor system. However, non-motor symptoms such as cognitive, autonomic, sleep-related and sensory dysfunctions are often reported. A subgroup of non-motor symptoms, oropharyngeal problems, also affects these patients in ways that greatly deteriorate quality of life. Each patient may develop a different set of non-motor symptoms, making interprofessional collaboration among health care providers a must to treat patients with PD. In this review, we argue that dental health professionals must be included in this interprofessional health care team. Patients with PD are at a higher risk for developing oral health problems that can exacerbate or be exacerbated by other non-motor symptoms, such as mental health and dysphagia This accelerates decline in quality of life and even increases the risk of death by aspiration pneumonia. Dentists can create preventive oral health plans as soon as a diagnosis is made and promptly treat a patient's dental problems, preventing them from affecting other health areas. We describe major oral health concerns and how health professionals and dentists can participate and collaborate to improve the health of patients with PD. © 2017 Elsevier Ltd. All rights reserved.
Keywords: Parkinson's disease Oral health Dental care Interprofessional Interdisciplinary
1. Interprofessional care for patients with Parkinson’s disease Parkinson's disease (PD) is a complex and heterogeneous disorder with motor and non-motor symptoms, environmental and genetic risk factors, and several affected brain structures and cellular functions [1]. PD has a 1% prevalence in people 60 years or older, equating to between 7 and 9 million elderly in the world that suffer from this disorder [2]. The complexity of the disease makes each patient a unique case with a different set of symptoms. Current epidemiological studies are attempting to identify non-motor subtypes of PD with the hope that categorization will help health professionals better diagnose and treat each patient [3]. In the meantime, interprofessional collaborations among health care professionals remain a highly recommended model to manage PD
* Corresponding author. Department of Diagnostic and Biomedical Sciences, The University of Texas Health Science Center at Houston School of Dentistry, 7500 Cambridge St., Suite 5371, Houston, TX 77054, USA. E-mail addresses: [email protected] (N.S. Rozas), june.sadowsky@uth. tmc.edu (J.M. Sadowsky), [email protected] (D.J. Jones), cameron.b. [email protected] (C.B. Jeter).
[4]. In this review, we argue that the dentist should be a part of a patient's multispecialty team. In support, we enumerate oral health problems in PD and describe how dental health professionals are vital to prevent, manage or improve these potentially life-altering symptoms (Fig. 1). Non-motor symptoms in PD may appear years before or after diagnosis and include behavioral and cognitive dysfunctions (e.g., depression, anxiety, dementia and psychosis), autonomic dysfunction (e.g., dysphagia, gastric and intestinal problems, urinary incontinence, constipation, sexual dysfunction and cardiac autonomic dysfunction), sleep related dysfunctions (e.g., insomnia, REM sleep behavior disorder and excessive daytime sleepiness) and sensory and sensorimotor dysfunctions (e.g., hyposmia, visual and oculomotor dysfunction, pain syndromes and fatigue) [5]. In addition, PD medication side effects include dyskinesia (involuntary movements), dry mouth, impulse control disorders and psychosis [5]. Diverse symptoms affecting varied body systems make interprofessional care a must for patients with PD. Several recent studies have shown the positive effects that a multispecialty team can provide for the overall quality of life [6,7]. Trend et al. performed
http://dx.doi.org/10.1016/j.parkreldis.2017.07.012 1353-8020/© 2017 Elsevier Ltd. All rights reserved.
Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012
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Fig. 1. Oral health-PD link and the interprofessional care team. PD's cognitive, motor and non-motor symptoms increase the risk for oral health problems. These in turn exacerbate cognitive and non-motor symptoms and decrease quality of life of the patient. The interprofessional care team for patients with PD should include a dentist among other specialists. PD ¼ Parkinson's disease.
pre-and post-tests in 118 patients treated by a health care team. Visits included patient education and consultation for both a patient's general and specific needs. Over the six-week intervention, patients significantly improved in mobility and gait, speech, depression and health-related quality of life [8]. Guo et al. designed a single-blind, randomized trial with a pre- and post-test, quasi experimental design for 44 non-demented patients with PD treated by a multispecialty team (neurologist, physical therapist, occupational therapist, dietician, psychologist and nurse). They also provided three group lectures regarding meal routines, movement strategies and mood problems. After 8 weeks of treatment, the treatment group scored significantly better [9]. Miyasaki et al. used the Symptom Assessment System Scale for PD (ESAS-PD) before and after patients were referred to each patient's needed specialists (social worker, speech therapist, dietician, occupational therapist, physical therapist, psychiatrist, orthopedic surgeon, neurosurgeon and urologist). The mean ESAS-PD score improved significantly after multidisciplinary treatment and the symptoms that showed better improvement after interventions were dysphagia, constipation, anxiety, pain and drowsiness [10]. Most interprofessional care teams in these studies included a neurologist, physical therapist, speech therapist, occupational therapist, dietician, psychologist or psychiatrist and nurse practitioner [7e9] and even a sexologist [11]. The goal of this review is to increase awareness and educate about the oral health problems encountered in patients with PD. We argue that dentists should be part of the core interprofessional health care team for patients with PD.
2. Major oral health concerns in PD Patients with PD may have higher rates of caries and periodontal disease, difficulty retaining their dentures, a susceptibility to crack their teeth due to bruxism and masticatory problems, and suffer from sialorrhea, orofacial pain, burning mouth syndrome, xerostomia and taste impairment [12]. Whereas the prevalence for some of these symptoms are unknown, oropharyngeal problems are a growing concern of patients with PD. Dentists should be aware of them in order to plan preventive programs and provide early diagnosis and treatment. We will focus on the four most common and bothersome problems: tooth and gingival loss, xerostomia, drooling and sialorrhea, and dysphagia. 2.1. Tooth and gingival loss An individual's quality of life is closely related to oral health. Eating, speaking and appearance are all linked to the mouth. Dental caries and periodontitis are the main cause of tooth loss, which may affect chewing, nutrition, self-esteem, speech communication and social interactions. Periodontal disease may also be associated with systemic diseases and increase the risk of cardiovascular problems and arthritis [13]. Finally, it has been shown that poor oral health increases bacterial infections in the mouth, leading to an increased risk for aspiration pneumonia in a great number of patients with PD that also suffer dysphagia [14,15]. Due to chewing and swallowing problems, patients with advanced PD must change their diets from hard foods to soft foods [16]. It has also been reported that patients
Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012
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with PD crave sweets more often [17]. These dietary changes, along with poor oral hygiene habits due to hand tremors, depression and dementia may increase cavities, periodontal disease and tooth loss. Globally, about 10e35% of elderly people are affected by severe caries, periodontitis and consequent tooth loss [18]. A handful of scientific studies, from different countries, have surveyed the PD patient population regarding their oral health. Persson et al. found that patients with PD in Sweden had equal or even better oral health than controls [19]. Fukayo et al. had similar results and found that patients with PD in Japan practiced better oral hygiene habits than controls [20]. However, other studies from Iceland, Japan, India, Italy and Germany counter these results. They showed that PD patients had a higher number of decayed teeth, poorer periodontal health, fewer number of remaining teeth and poorer oral hygiene habits than controls [14,21e27]. The results from the majority of these studies are a warning that patients with PD may be at risk of rapid oral health decay, and are indeed in great need of oral health prevention and treatment. Even though it is still unclear exactly when oral health starts to decline in patients with PD, it seems that this decline accelerates as PD becomes more severe. A 2009 study by Hanaoka et al. suggests that the number of caries increases with disease severity, age and cognitive decline. In this study, patients at Hoehn & Yahr stage 2 (of 5 in this PD severity scale) already showed a significantly higher number of caries than controls [21]. A 2013 study by Pradeep et al. showed similar results regarding periodontal disease; probing depth, clinical attachment levels, gingival index, plaque index and percentage of bleeding at probing sites were initially worse in patients with PD than in controls, and worsened with PD severity [26]. Diagnosis of tooth decay, gingivitis and periodontal disease is fairly routine at the dental office; the main barrier is getting the patient to the dental appointment and keeping the patient comfortable. The role of the dentist as a member of the interprofessional care team is to diagnose and treat dental and gingival problems as well as prevent them through patient education. Patients should be reminded that oral health problems are preventable by maintaining good oral hygiene habits, a low-sugar diet and regular visits to the dentist. Dentists and dental hygienists should regularly survey patients for PD symptoms that may affect oral health: severity of tremors and how they affect teeth brushing, sugar consumption, type of food consumption (soft vs hard foods), salivary problems (drooling or dry mouth), dysphagia status, depression and cognitive problems. Finally, dentists and primary care physicians (or neurologists) should be in contact for consultation and to suggest appropriate treatments for each patient depending on the disease stage. 2.2. Xerostomia Xerostomia, the subjective complaint of dry mouth, can cause demineralization of tooth enamel, rapid tooth decay, severe oral infections, dehydration of the gingiva and loss of salivary antimicrobial protection. Xerostomia may also impair swallowing, produce taste changes, halitosis, burning mouth and affect speech articulation [28]. Dentists are critical for diagnosis, treatment and prevention of xerostomia as it is under-reported in patients with PD [29]. A speech and language pathologist may also diagnose this problem and should immediately refer patients to a dentist to prevent dental deterioration. Xerostomia is an autonomic dysfunction that affects as many as 60% of patients with PD (twice the prevalence in the general elderly population). Furthermore, 30% of these patients may concomitantly suffer sialorrhea (drooling problems) [29,30]. These contradicting symptoms may arise due to reduced salivary production (caused by
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PD and anti-cholinergic medication), the inability to properly clear saliva from the mouth (dysphagia), and/or stooped posture with weak lip muscles that exacerbate drooling [19,31,32]. A small percentage of patients report that xerostomia appears before the onset of motor symptoms, suggesting this problem is due to autonomic dysfunction resultant of PD [31]. The majority of patients reports it after the onset of motor symptoms, though, and generally experience worsening with increased PD medication dosage [32]. Proactive clinicians must carefully listen for patient complaints of dryness of the mouth like difficulty chewing, swallowing or speaking. Patients may report drinking fluids to aid swallowing dry foods and avoiding spicy or crunchy foods. Clinicians can use available surveys (e.g., Thomson Xerostomia Inventory [33], Pai Xerostomia Visual Analogue Scale [34]) to ask about the duration and frequency of symptoms and medications used. Upon oral examination, the provider may note frothy saliva that does not pool, a loss of tongue papillae and altered gingiva. The tongue and lips may be cracked or fissured. In addition, salivary flow rate can be objectively measured by a variety of methods that include total unstimulated or stimulated salivary flow rates [35]. To battle symptoms, patients can be encouraged to take frequent sips of water, eat moist foods, and use lip balms and artificial saliva. Patients can select alcohol-free mouthwash, chew sugar-free gum or take medications to stimulate salivation [12,28,36]. Including dental health professionals in the interprofessional care team can increase early recognition and symptom management for patients suffering from xerostomia. 2.3. Sialorrhea and excessive drooling We know that patients with advanced PD have decreased salivary flow rate, and yet many experience excessive drooling [37]. Excessive drooling can cause perioral dermatitis, impede effective oral hygiene, produce bad breath, increase amounts of oral bacteria, impair eating and speaking, and put patients at a higher risk for silent aspiration of saliva leading to respiratory tract infections [38]. In addition, drooling forces patients to adopt the undignified practice of relentlessly spitting into a cup. Patients who suffer from prolonged social embarrassment or isolation may also develop depression. The pathophysiology of drooling in PD patients is not fully understood, but dysphagia, poor facial muscle control, and complex stooped posture may contribute to the problem. For example, patients with PD that suffer from dysphagia or cannot control facial muscles have more severe drooling symptoms [39]. Although many studies have shown that patients with PD have a decreased salivary flow rate, a study by Nicaretta et al. suggested that drooling patients with PD may secrete saliva at higher speeds than normal controls [40]. The risk for developing drooling problems is 5 times higher in patients with PD than the control population, the pooled prevalence is estimated to be 56% for patients with PD [37]. The time of onset is unknown and may depend on each case and history of symptoms. For example, drooling is seen in about 86% of patients with PD that also suffer from dysphagia, but only 44% of PD patients without dysphagia [41]. These percentages, however, may have an even broader gap if objective diagnostic measures of dysphagia are used. A health care team to diagnose and treat sialorrhea and drooling should include a speech and language pathologist, dentist, gastroenterologist and otolaryngologist. Salivary flow rate can be measured objectively or subjectively. Objective measures employ techniques including saliva collection in a cup, suctioning, the Lashley disk, patient self-swallow counts, and cotton pads weighed before and after absorbing saliva [41]. Subjective measures of drooling and sialorrhea employ any number of patient and clinical
Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012
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surveys (i.e., Sialorrhea clinical scale for PD [42], RADBOUD Oral Motor Inventory for PD [43]). Objective methods can be time consuming and uncomfortable for the patient. Moreover, they neither quantify how drooling and sialorrhea affect quality of life, nor identify the root cause as dysphagia or overproduction of saliva. Subjective measures can be administered quickly by a trained health professional. Importantly, they rate the impact of drooling and sialorrhea on quality of life of the patient. There are currently no preventive methods for drooling. However, early dysphagia diagnosis followed by rehabilitation programs may also delay the onset of drooling. Treatments for sialorrhea and drooling range from non-invasive (physiotherapy and neuromuscular rehabilitation techniques) to pharmacological therapy with anticholinergics, adrenergic receptor agonists and botulinum toxin injections to invasive methods such as surgery and radiotherapy [28,38]. Dental health professionals can help detect drooling problems and prevent further oral health decline. 2.4. Dysphagia Dysphagia is defined as difficulty in swallowing that may include delayed oral transit time, tongue fasciculations, impaired laryngeal, pharyngeal and esophageal motility that alter bolus control, and reflux [44]. This symptom greatly decreases the quality of life of these patients since it is associated with weight loss, malnutrition, dehydration, social impairment, poor psychological well-being and even risk of death through aspiration pneumonia [45]. Patients that develop dysphagia may progressively switch from regular diets to soft foods and even liquid diets, diminishing the nutrient value of their meals and increasing the risk of oral health problems [16]. As mentioned above, dysphagia is also associated with an impairment in saliva swallowing, which leads to excessive drooling and further deterioration of quality of life. Dysphagia has a direct link to aspiration pneumonia, and patients diagnosed with dysphagia may have an increased risk of death in the following two years [14]. The increased retention time of food material along the swallowing tract promotes bacterial growth, and teeth and gingival deterioration, increasing the chances for aspiration pneumonia and mortality [15,46]. The dental problems brought about by dysphagia create the need to have a dental health professional as part of the multispecialty care team of patients with PD. Several case-control studies from different countries suggest that between 15 and 87% of patients with PD suffer from dysphagia and the pooled prevalence is estimated to be 82%; more than three times higher than the normal population [47]. The big gap between studies is most likely due to age differences in the population studied, as well as method of dysphagia diagnosis. Patient-report studies of dysphagia symptoms suggest that this problem arises late in the disease (10e12 years after PD diagnosis) [14]. However, studies that use objective measures of dysphagia suggest that this symptom may start earlier (less than 6 years after PD diagnosis) [48]. Although early diagnosis of swallowing problems may be useful for prevention and early intervention, it should not be confused with presbyphagia. Presbyphagia is the mild deterioration of swallowing mechanisms in healthy older adults. Although presbypaghia does not necessarily end in severe dysphagia, additional illnesses, such as PD, may cause presbyphagia to turn into dysphagia [49]. The interprofessional health team to treat patients with PD and dysphagia should be comprised of a speech and language pathologist (swallowing specialist), dietitian, nurse, radiologist, geriatrician, dentist, gastroenterologist, otolaryngologist and neurologist [49]. Screening for dysphagia typically proceeds in two steps: bedside screening based on questions and interactions with the
patient from care staff, and secondary screening done by specialized health care professionals [45]. Daily questions, interactions and observation of habits of the patient by caregivers may be the first clue that dysphagia is a problem. Health care providers should pay attention to the eating habits of the patient (Have they changed? Is the patient having trouble with hard foods? Is the patient coughing or choking more often while eating? Does the patient avoid eating in front of others?). Several sensitive and reliable surveys are available, of which the Swallowing Disturbance Questionnaire [50], the Dysphagia-Specific Quality of Life [51] and the Munich Dysphagia Test [52] are good options for patients with PD. Secondary screening can make a more accurate diagnosis, and include assessment by observation, videography or endoscopy. As a symptom with no cure, dysphagia is best managed under the direction of a neurologist who can refer the patient to the appropriate specialist. Available treatment options can be categorized into compensatory strategies, that reduce or avoid the effects of dysphagia, and rehabilitative strategies that improve dysphagia. Swallow specialists can recommend compensatory strategies such as postural adjustments (i.e., upright posture while eating, chin tuck to reduce speed of bolus passage) and rehabilitation programs (i.e., head lifting and tongue resistance exercises) [49]. Dieticians can supervise dietary modifications as compensatory strategies (i.e., substitute thin liquids for thickened ones, recommend specific food textures and viscosities depending on dysphagia severity) [53]. Other interprofessional health care team members should be vigilant and recognize the problem first, give general management advice and refer to the neurologist and appropriate specialist. A patient with PD and dysphagia can be advised to make time for each meal, eat small bites consciously biting and swallowing, and avoid eating and drinking simultaneously to decrease the risk for aspiration. Because dysphagia is greatly linked to oral health, it is important for the dentist to be aware of this problem and take preventive and proactive measures. 2.5. Other oral cavity problems Orofacial pain, burning mouth syndrome, taste impairment, denture problems, masticatory problems and bruxism have also been reported by patients with PD [12,22,30,54]. However, more studies are needed to determine if these symptoms are indeed more prevalent in patients with PD than the general population. Dental health professionals should be aware that these symptoms can occur concomitantly, and early diagnosis and interventions may help improve a patient's quality of life. 3. Conclusion Parkinson's disease is characterized by motor and non-motor symptoms that may compound with each other, further decreasing the health status and quality of life of the patient. Motor symptoms such as tremors and rigidity may prevent patients from following an optimal oral hygiene routine. Likewise, non-motor symptoms such as depression, dementia, pain and fatigue may further decrease oral hygiene habits. Hence, both classes of symptoms can lead to poor oral health, such as caries and periodontal disease. As PD progresses, a majority of patients will battle additional oral symptoms like dry mouth and dysphagia. Dysphagia can lead to drooling, which in turn can aggravate oral symptoms, as well as put dysphagic patients at higher risk for aspiration pneumonia. Unsightly drooling and prolonged eating duration resulting from tremors and dysphagia may lead a patient to refrain from social interaction. A resulting sense of helplessness can compound the physical and mental toll of existing non-motor symptoms, closing this negative feedback loop (Fig. 1).
Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012
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The complete interprofessional health care team for patients with PD should comprise a host of members with complementary expertise to prevent symptoms from intensifying each other (Fig. 1). We recommend dentists join this team to create preventive oral health plans, educate patients and proactively manage oral symptoms. Participation in such a multidisciplinary team could be difficult for dentists working in private practices who do not actively collaborate with other health care providers. Thus, we recommend the neurologist lead each patient's unique team with the responsibility to educate any team member less familiar with PD. We encourage patients diagnosed with PD to be immediately referred to a dentist and start an education and prevention program. This referral must come from the physician or neurologist that initially diagnoses a patient. However, dentists can have an active role by initiating a consult and collaboration with other health care providers specific to each patient with PD. Dentists competent to care for the oral health of patients with PD should add their names to the list of providers on PD advocacy websites. The successful interprofessional healthcare team must keep open communication channels with patients and one another to prevent progression of insidious oral symptoms. Ethics Conflict of interests: None. Author contributions: Rozas, Sadowsky, Jones and Jeter participated in the manuscript concept and design; Rozas, Sadowsky, Jones and Jeter participated in literature search and selection. Rozas and Jeter drafted the article and Jones and Sadowsky revised it critically for important intellectual content. Rozas, Sadowsky, Jones and Jeter gave final approval of this version to be published. Funding Sources: This work was supported by the National Interprofessional Initiative on Oral Health (NIIOH) Interprofessional Oral-Systemic Health Curricular Innovation Award (OHNEP), 2015. References [1] L.V. Kalia, A.E. Lang, Parkinson's disease, Lancet 386 (2015) 896e912. [2] A. Lee, R.M. Gilbert, Epidemiology of Parkinson disease, Neurol. Clin. 34 (2016) 955e965. [3] A. Sauerbier, P. Jenner, A. Todorova, K.R. Chaudhuri, Non motor subtypes and Parkinson's disease, Park. Relat. Disord. 22 (2016) S41eS46. [4] M.A. van der Marck, B.R. Bloem, How to organize multispecialty care for patients with Parkinson's disease, Park. Relat. Disord. 20 (Suppl 1) (2014) S167eS173. [5] R.F. Pfeiffer, I. Bodis-Wollner, Parkinson's Disease and Nonmotor Dysfunction, second ed., Humana Press Inc, 2013. [6] L.P. Prizer, N. Browner, The integrative care of Parkinson's disease: a systematic review, J. Park. Dis. 2 (2012) 79e86. [7] M.A. van der Marck, M. Munneke, W. Mulleners, E.M. Hoogerwaard, G.F. Borm, S. Overeem, B.R. Bloem, H.W. Nijmeijer, T.J. Tacke, O.L.G.F. Sinnige, J.N. Wessel, Integrated multidisciplinary care in Parkinson's disease: a non-randomised, controlled trial (IMPACT), Lancet Neurol. 12 (2013) 947e956. [8] P. Trend, J. Kaye, H. Gage, C. Owen, D. Wade, Short-term effectiveness of intensive multidisciplinary rehabilitation for people with Parkinson's disease and their carers, Clin. Rehabil. 16 (2002) 717e725. [9] L. Guo, Y. Jiang, H. Yatsuya, Y. Yoshida, J. Sakamoto, Group education with personal rehabilitation for idiopathic Parkinson's disease, Can. J. Neurol. Sci. 36 (2009) 51e59. [10] J.M. Miyasaki, J. Long, D. Mancini, E. Moro, S.H. Fox, A.E. Lang, C. Marras, R. Chen, A. Strafella, R. Arshinoff, R. Ghoche, J. Hui, Palliative care for advanced Parkinson disease: an interdisciplinary clinic and new scale, the ESAS-PD, Park. Relat. Disord. 18 (2012) S6eS9. [11] N. Giladi, Y. Manor, A. Hilel, T. Gurevich, Interdisciplinary teamwork for the treatment of people with Parkinson's disease and their families, Curr. Neurol. Neurosci. Rep. 14 (2014) 1e7. [12] Y. Zlotnik, Y. Balash, A.D. Korczyn, N. Giladi, T. Gurevich, Disorders of the oral cavity in Parkinson ’ s disease and parkinsonian syndromes, Park. Dis. 2015 (2015) 379482. [13] W.S. Borgnakke, Does treatment of periodontal disease influence systemic disease? Dent. Clin. North Am. 59 (2015) 885e917. [14] J. Müller, G.K. Wenning, M. Verny, a McKee, K.R. Chaudhuri, K. Jellinger, W. Poewe, I. Litvan, Progression of dysarthria and dysphagia in postmortem-
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Fox, Xerostomia: recognition and management, Dent. Assist. (2008) 18e47. [37] J.G. Kalf, B.J.M. de Swart, G.F. Borm, B.R. Bloem, M. Munneke, Prevalence and definition of drooling in Parkinson's disease: a systematic review, J. Neurol. 256 (2009) 1391e1396. [38] P. Srivanitchapoom, S. Pandey, M. Hallett, Drooling in Parkinson's disease: a review, Park. Relat. Disord. 20 (2014) 1109e1118. [39] A.C. Nobrega, B. Rodrigues, A.C. Torres, R.D. Scarpel, C.A. Neves, A. Melo, Is drooling secondary to a swallowing disorder in patients with Parkinson's disease? Park. Relat. Disord. 14 (2008) 243e245. [40] D.H. Nicaretta, A.L.Z. de Rosso, C. Maliska, M.M.B. Costa, Scintigraphic analysis of the parotid glands in patients with sialorrhea and Parkinson's disease, Park. Relat. Disord. 14 (2008) 338e341. [41] K.L. Chou, M. Evatt, V. Hinson, K. Kompoliti, Sialorrhea in Parkinson's disease: a review, Mov. Disord. 22 (2007) 2306e2313. [42] S. Perez Lloret, G.P. Arce, M. Rossi, M.L.C. Nemet, P. 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Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Review article
Incorporating oral health into interprofessional care teams for patients with Parkinson's disease Natalia S. Rozas a, June M. Sadowsky b, Deborah J. Jones c, Cameron B. Jeter a, * a
The University of Texas Health Science Center at Houston (UTHealth) School of Dentistry, Department of Diagnostic and Biomedical Sciences, 7500 Cambridge Street, Houston, TX 77054, USA b UTHealth School of Dentistry, Department of General Practice and Dental Public Health, 7500 Cambridge Street, Houston, TX 77054, USA c UTHealth School of Nursing, Department of Nursing Systems, 6901 Bertner Ave., Houston, TX 77054, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 April 2017 Received in revised form 4 July 2017 Accepted 15 July 2017
Parkinson's disease (PD) is a progressive neurodegenerative disorder that primarily affects the motor system. However, non-motor symptoms such as cognitive, autonomic, sleep-related and sensory dysfunctions are often reported. A subgroup of non-motor symptoms, oropharyngeal problems, also affects these patients in ways that greatly deteriorate quality of life. Each patient may develop a different set of non-motor symptoms, making interprofessional collaboration among health care providers a must to treat patients with PD. In this review, we argue that dental health professionals must be included in this interprofessional health care team. Patients with PD are at a higher risk for developing oral health problems that can exacerbate or be exacerbated by other non-motor symptoms, such as mental health and dysphagia This accelerates decline in quality of life and even increases the risk of death by aspiration pneumonia. Dentists can create preventive oral health plans as soon as a diagnosis is made and promptly treat a patient's dental problems, preventing them from affecting other health areas. We describe major oral health concerns and how health professionals and dentists can participate and collaborate to improve the health of patients with PD. © 2017 Elsevier Ltd. All rights reserved.
Keywords: Parkinson's disease Oral health Dental care Interprofessional Interdisciplinary
1. Interprofessional care for patients with Parkinson’s disease Parkinson's disease (PD) is a complex and heterogeneous disorder with motor and non-motor symptoms, environmental and genetic risk factors, and several affected brain structures and cellular functions [1]. PD has a 1% prevalence in people 60 years or older, equating to between 7 and 9 million elderly in the world that suffer from this disorder [2]. The complexity of the disease makes each patient a unique case with a different set of symptoms. Current epidemiological studies are attempting to identify non-motor subtypes of PD with the hope that categorization will help health professionals better diagnose and treat each patient [3]. In the meantime, interprofessional collaborations among health care professionals remain a highly recommended model to manage PD
* Corresponding author. Department of Diagnostic and Biomedical Sciences, The University of Texas Health Science Center at Houston School of Dentistry, 7500 Cambridge St., Suite 5371, Houston, TX 77054, USA. E-mail addresses: [email protected] (N.S. Rozas), june.sadowsky@uth. tmc.edu (J.M. Sadowsky), [email protected] (D.J. Jones), cameron.b. [email protected] (C.B. Jeter).
[4]. In this review, we argue that the dentist should be a part of a patient's multispecialty team. In support, we enumerate oral health problems in PD and describe how dental health professionals are vital to prevent, manage or improve these potentially life-altering symptoms (Fig. 1). Non-motor symptoms in PD may appear years before or after diagnosis and include behavioral and cognitive dysfunctions (e.g., depression, anxiety, dementia and psychosis), autonomic dysfunction (e.g., dysphagia, gastric and intestinal problems, urinary incontinence, constipation, sexual dysfunction and cardiac autonomic dysfunction), sleep related dysfunctions (e.g., insomnia, REM sleep behavior disorder and excessive daytime sleepiness) and sensory and sensorimotor dysfunctions (e.g., hyposmia, visual and oculomotor dysfunction, pain syndromes and fatigue) [5]. In addition, PD medication side effects include dyskinesia (involuntary movements), dry mouth, impulse control disorders and psychosis [5]. Diverse symptoms affecting varied body systems make interprofessional care a must for patients with PD. Several recent studies have shown the positive effects that a multispecialty team can provide for the overall quality of life [6,7]. Trend et al. performed
http://dx.doi.org/10.1016/j.parkreldis.2017.07.012 1353-8020/© 2017 Elsevier Ltd. All rights reserved.
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Fig. 1. Oral health-PD link and the interprofessional care team. PD's cognitive, motor and non-motor symptoms increase the risk for oral health problems. These in turn exacerbate cognitive and non-motor symptoms and decrease quality of life of the patient. The interprofessional care team for patients with PD should include a dentist among other specialists. PD ¼ Parkinson's disease.
pre-and post-tests in 118 patients treated by a health care team. Visits included patient education and consultation for both a patient's general and specific needs. Over the six-week intervention, patients significantly improved in mobility and gait, speech, depression and health-related quality of life [8]. Guo et al. designed a single-blind, randomized trial with a pre- and post-test, quasi experimental design for 44 non-demented patients with PD treated by a multispecialty team (neurologist, physical therapist, occupational therapist, dietician, psychologist and nurse). They also provided three group lectures regarding meal routines, movement strategies and mood problems. After 8 weeks of treatment, the treatment group scored significantly better [9]. Miyasaki et al. used the Symptom Assessment System Scale for PD (ESAS-PD) before and after patients were referred to each patient's needed specialists (social worker, speech therapist, dietician, occupational therapist, physical therapist, psychiatrist, orthopedic surgeon, neurosurgeon and urologist). The mean ESAS-PD score improved significantly after multidisciplinary treatment and the symptoms that showed better improvement after interventions were dysphagia, constipation, anxiety, pain and drowsiness [10]. Most interprofessional care teams in these studies included a neurologist, physical therapist, speech therapist, occupational therapist, dietician, psychologist or psychiatrist and nurse practitioner [7e9] and even a sexologist [11]. The goal of this review is to increase awareness and educate about the oral health problems encountered in patients with PD. We argue that dentists should be part of the core interprofessional health care team for patients with PD.
2. Major oral health concerns in PD Patients with PD may have higher rates of caries and periodontal disease, difficulty retaining their dentures, a susceptibility to crack their teeth due to bruxism and masticatory problems, and suffer from sialorrhea, orofacial pain, burning mouth syndrome, xerostomia and taste impairment [12]. Whereas the prevalence for some of these symptoms are unknown, oropharyngeal problems are a growing concern of patients with PD. Dentists should be aware of them in order to plan preventive programs and provide early diagnosis and treatment. We will focus on the four most common and bothersome problems: tooth and gingival loss, xerostomia, drooling and sialorrhea, and dysphagia. 2.1. Tooth and gingival loss An individual's quality of life is closely related to oral health. Eating, speaking and appearance are all linked to the mouth. Dental caries and periodontitis are the main cause of tooth loss, which may affect chewing, nutrition, self-esteem, speech communication and social interactions. Periodontal disease may also be associated with systemic diseases and increase the risk of cardiovascular problems and arthritis [13]. Finally, it has been shown that poor oral health increases bacterial infections in the mouth, leading to an increased risk for aspiration pneumonia in a great number of patients with PD that also suffer dysphagia [14,15]. Due to chewing and swallowing problems, patients with advanced PD must change their diets from hard foods to soft foods [16]. It has also been reported that patients
Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012
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with PD crave sweets more often [17]. These dietary changes, along with poor oral hygiene habits due to hand tremors, depression and dementia may increase cavities, periodontal disease and tooth loss. Globally, about 10e35% of elderly people are affected by severe caries, periodontitis and consequent tooth loss [18]. A handful of scientific studies, from different countries, have surveyed the PD patient population regarding their oral health. Persson et al. found that patients with PD in Sweden had equal or even better oral health than controls [19]. Fukayo et al. had similar results and found that patients with PD in Japan practiced better oral hygiene habits than controls [20]. However, other studies from Iceland, Japan, India, Italy and Germany counter these results. They showed that PD patients had a higher number of decayed teeth, poorer periodontal health, fewer number of remaining teeth and poorer oral hygiene habits than controls [14,21e27]. The results from the majority of these studies are a warning that patients with PD may be at risk of rapid oral health decay, and are indeed in great need of oral health prevention and treatment. Even though it is still unclear exactly when oral health starts to decline in patients with PD, it seems that this decline accelerates as PD becomes more severe. A 2009 study by Hanaoka et al. suggests that the number of caries increases with disease severity, age and cognitive decline. In this study, patients at Hoehn & Yahr stage 2 (of 5 in this PD severity scale) already showed a significantly higher number of caries than controls [21]. A 2013 study by Pradeep et al. showed similar results regarding periodontal disease; probing depth, clinical attachment levels, gingival index, plaque index and percentage of bleeding at probing sites were initially worse in patients with PD than in controls, and worsened with PD severity [26]. Diagnosis of tooth decay, gingivitis and periodontal disease is fairly routine at the dental office; the main barrier is getting the patient to the dental appointment and keeping the patient comfortable. The role of the dentist as a member of the interprofessional care team is to diagnose and treat dental and gingival problems as well as prevent them through patient education. Patients should be reminded that oral health problems are preventable by maintaining good oral hygiene habits, a low-sugar diet and regular visits to the dentist. Dentists and dental hygienists should regularly survey patients for PD symptoms that may affect oral health: severity of tremors and how they affect teeth brushing, sugar consumption, type of food consumption (soft vs hard foods), salivary problems (drooling or dry mouth), dysphagia status, depression and cognitive problems. Finally, dentists and primary care physicians (or neurologists) should be in contact for consultation and to suggest appropriate treatments for each patient depending on the disease stage. 2.2. Xerostomia Xerostomia, the subjective complaint of dry mouth, can cause demineralization of tooth enamel, rapid tooth decay, severe oral infections, dehydration of the gingiva and loss of salivary antimicrobial protection. Xerostomia may also impair swallowing, produce taste changes, halitosis, burning mouth and affect speech articulation [28]. Dentists are critical for diagnosis, treatment and prevention of xerostomia as it is under-reported in patients with PD [29]. A speech and language pathologist may also diagnose this problem and should immediately refer patients to a dentist to prevent dental deterioration. Xerostomia is an autonomic dysfunction that affects as many as 60% of patients with PD (twice the prevalence in the general elderly population). Furthermore, 30% of these patients may concomitantly suffer sialorrhea (drooling problems) [29,30]. These contradicting symptoms may arise due to reduced salivary production (caused by
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PD and anti-cholinergic medication), the inability to properly clear saliva from the mouth (dysphagia), and/or stooped posture with weak lip muscles that exacerbate drooling [19,31,32]. A small percentage of patients report that xerostomia appears before the onset of motor symptoms, suggesting this problem is due to autonomic dysfunction resultant of PD [31]. The majority of patients reports it after the onset of motor symptoms, though, and generally experience worsening with increased PD medication dosage [32]. Proactive clinicians must carefully listen for patient complaints of dryness of the mouth like difficulty chewing, swallowing or speaking. Patients may report drinking fluids to aid swallowing dry foods and avoiding spicy or crunchy foods. Clinicians can use available surveys (e.g., Thomson Xerostomia Inventory [33], Pai Xerostomia Visual Analogue Scale [34]) to ask about the duration and frequency of symptoms and medications used. Upon oral examination, the provider may note frothy saliva that does not pool, a loss of tongue papillae and altered gingiva. The tongue and lips may be cracked or fissured. In addition, salivary flow rate can be objectively measured by a variety of methods that include total unstimulated or stimulated salivary flow rates [35]. To battle symptoms, patients can be encouraged to take frequent sips of water, eat moist foods, and use lip balms and artificial saliva. Patients can select alcohol-free mouthwash, chew sugar-free gum or take medications to stimulate salivation [12,28,36]. Including dental health professionals in the interprofessional care team can increase early recognition and symptom management for patients suffering from xerostomia. 2.3. Sialorrhea and excessive drooling We know that patients with advanced PD have decreased salivary flow rate, and yet many experience excessive drooling [37]. Excessive drooling can cause perioral dermatitis, impede effective oral hygiene, produce bad breath, increase amounts of oral bacteria, impair eating and speaking, and put patients at a higher risk for silent aspiration of saliva leading to respiratory tract infections [38]. In addition, drooling forces patients to adopt the undignified practice of relentlessly spitting into a cup. Patients who suffer from prolonged social embarrassment or isolation may also develop depression. The pathophysiology of drooling in PD patients is not fully understood, but dysphagia, poor facial muscle control, and complex stooped posture may contribute to the problem. For example, patients with PD that suffer from dysphagia or cannot control facial muscles have more severe drooling symptoms [39]. Although many studies have shown that patients with PD have a decreased salivary flow rate, a study by Nicaretta et al. suggested that drooling patients with PD may secrete saliva at higher speeds than normal controls [40]. The risk for developing drooling problems is 5 times higher in patients with PD than the control population, the pooled prevalence is estimated to be 56% for patients with PD [37]. The time of onset is unknown and may depend on each case and history of symptoms. For example, drooling is seen in about 86% of patients with PD that also suffer from dysphagia, but only 44% of PD patients without dysphagia [41]. These percentages, however, may have an even broader gap if objective diagnostic measures of dysphagia are used. A health care team to diagnose and treat sialorrhea and drooling should include a speech and language pathologist, dentist, gastroenterologist and otolaryngologist. Salivary flow rate can be measured objectively or subjectively. Objective measures employ techniques including saliva collection in a cup, suctioning, the Lashley disk, patient self-swallow counts, and cotton pads weighed before and after absorbing saliva [41]. Subjective measures of drooling and sialorrhea employ any number of patient and clinical
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surveys (i.e., Sialorrhea clinical scale for PD [42], RADBOUD Oral Motor Inventory for PD [43]). Objective methods can be time consuming and uncomfortable for the patient. Moreover, they neither quantify how drooling and sialorrhea affect quality of life, nor identify the root cause as dysphagia or overproduction of saliva. Subjective measures can be administered quickly by a trained health professional. Importantly, they rate the impact of drooling and sialorrhea on quality of life of the patient. There are currently no preventive methods for drooling. However, early dysphagia diagnosis followed by rehabilitation programs may also delay the onset of drooling. Treatments for sialorrhea and drooling range from non-invasive (physiotherapy and neuromuscular rehabilitation techniques) to pharmacological therapy with anticholinergics, adrenergic receptor agonists and botulinum toxin injections to invasive methods such as surgery and radiotherapy [28,38]. Dental health professionals can help detect drooling problems and prevent further oral health decline. 2.4. Dysphagia Dysphagia is defined as difficulty in swallowing that may include delayed oral transit time, tongue fasciculations, impaired laryngeal, pharyngeal and esophageal motility that alter bolus control, and reflux [44]. This symptom greatly decreases the quality of life of these patients since it is associated with weight loss, malnutrition, dehydration, social impairment, poor psychological well-being and even risk of death through aspiration pneumonia [45]. Patients that develop dysphagia may progressively switch from regular diets to soft foods and even liquid diets, diminishing the nutrient value of their meals and increasing the risk of oral health problems [16]. As mentioned above, dysphagia is also associated with an impairment in saliva swallowing, which leads to excessive drooling and further deterioration of quality of life. Dysphagia has a direct link to aspiration pneumonia, and patients diagnosed with dysphagia may have an increased risk of death in the following two years [14]. The increased retention time of food material along the swallowing tract promotes bacterial growth, and teeth and gingival deterioration, increasing the chances for aspiration pneumonia and mortality [15,46]. The dental problems brought about by dysphagia create the need to have a dental health professional as part of the multispecialty care team of patients with PD. Several case-control studies from different countries suggest that between 15 and 87% of patients with PD suffer from dysphagia and the pooled prevalence is estimated to be 82%; more than three times higher than the normal population [47]. The big gap between studies is most likely due to age differences in the population studied, as well as method of dysphagia diagnosis. Patient-report studies of dysphagia symptoms suggest that this problem arises late in the disease (10e12 years after PD diagnosis) [14]. However, studies that use objective measures of dysphagia suggest that this symptom may start earlier (less than 6 years after PD diagnosis) [48]. Although early diagnosis of swallowing problems may be useful for prevention and early intervention, it should not be confused with presbyphagia. Presbyphagia is the mild deterioration of swallowing mechanisms in healthy older adults. Although presbypaghia does not necessarily end in severe dysphagia, additional illnesses, such as PD, may cause presbyphagia to turn into dysphagia [49]. The interprofessional health team to treat patients with PD and dysphagia should be comprised of a speech and language pathologist (swallowing specialist), dietitian, nurse, radiologist, geriatrician, dentist, gastroenterologist, otolaryngologist and neurologist [49]. Screening for dysphagia typically proceeds in two steps: bedside screening based on questions and interactions with the
patient from care staff, and secondary screening done by specialized health care professionals [45]. Daily questions, interactions and observation of habits of the patient by caregivers may be the first clue that dysphagia is a problem. Health care providers should pay attention to the eating habits of the patient (Have they changed? Is the patient having trouble with hard foods? Is the patient coughing or choking more often while eating? Does the patient avoid eating in front of others?). Several sensitive and reliable surveys are available, of which the Swallowing Disturbance Questionnaire [50], the Dysphagia-Specific Quality of Life [51] and the Munich Dysphagia Test [52] are good options for patients with PD. Secondary screening can make a more accurate diagnosis, and include assessment by observation, videography or endoscopy. As a symptom with no cure, dysphagia is best managed under the direction of a neurologist who can refer the patient to the appropriate specialist. Available treatment options can be categorized into compensatory strategies, that reduce or avoid the effects of dysphagia, and rehabilitative strategies that improve dysphagia. Swallow specialists can recommend compensatory strategies such as postural adjustments (i.e., upright posture while eating, chin tuck to reduce speed of bolus passage) and rehabilitation programs (i.e., head lifting and tongue resistance exercises) [49]. Dieticians can supervise dietary modifications as compensatory strategies (i.e., substitute thin liquids for thickened ones, recommend specific food textures and viscosities depending on dysphagia severity) [53]. Other interprofessional health care team members should be vigilant and recognize the problem first, give general management advice and refer to the neurologist and appropriate specialist. A patient with PD and dysphagia can be advised to make time for each meal, eat small bites consciously biting and swallowing, and avoid eating and drinking simultaneously to decrease the risk for aspiration. Because dysphagia is greatly linked to oral health, it is important for the dentist to be aware of this problem and take preventive and proactive measures. 2.5. Other oral cavity problems Orofacial pain, burning mouth syndrome, taste impairment, denture problems, masticatory problems and bruxism have also been reported by patients with PD [12,22,30,54]. However, more studies are needed to determine if these symptoms are indeed more prevalent in patients with PD than the general population. Dental health professionals should be aware that these symptoms can occur concomitantly, and early diagnosis and interventions may help improve a patient's quality of life. 3. Conclusion Parkinson's disease is characterized by motor and non-motor symptoms that may compound with each other, further decreasing the health status and quality of life of the patient. Motor symptoms such as tremors and rigidity may prevent patients from following an optimal oral hygiene routine. Likewise, non-motor symptoms such as depression, dementia, pain and fatigue may further decrease oral hygiene habits. Hence, both classes of symptoms can lead to poor oral health, such as caries and periodontal disease. As PD progresses, a majority of patients will battle additional oral symptoms like dry mouth and dysphagia. Dysphagia can lead to drooling, which in turn can aggravate oral symptoms, as well as put dysphagic patients at higher risk for aspiration pneumonia. Unsightly drooling and prolonged eating duration resulting from tremors and dysphagia may lead a patient to refrain from social interaction. A resulting sense of helplessness can compound the physical and mental toll of existing non-motor symptoms, closing this negative feedback loop (Fig. 1).
Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012
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The complete interprofessional health care team for patients with PD should comprise a host of members with complementary expertise to prevent symptoms from intensifying each other (Fig. 1). We recommend dentists join this team to create preventive oral health plans, educate patients and proactively manage oral symptoms. Participation in such a multidisciplinary team could be difficult for dentists working in private practices who do not actively collaborate with other health care providers. Thus, we recommend the neurologist lead each patient's unique team with the responsibility to educate any team member less familiar with PD. We encourage patients diagnosed with PD to be immediately referred to a dentist and start an education and prevention program. This referral must come from the physician or neurologist that initially diagnoses a patient. However, dentists can have an active role by initiating a consult and collaboration with other health care providers specific to each patient with PD. Dentists competent to care for the oral health of patients with PD should add their names to the list of providers on PD advocacy websites. The successful interprofessional healthcare team must keep open communication channels with patients and one another to prevent progression of insidious oral symptoms. Ethics Conflict of interests: None. Author contributions: Rozas, Sadowsky, Jones and Jeter participated in the manuscript concept and design; Rozas, Sadowsky, Jones and Jeter participated in literature search and selection. Rozas and Jeter drafted the article and Jones and Sadowsky revised it critically for important intellectual content. Rozas, Sadowsky, Jones and Jeter gave final approval of this version to be published. Funding Sources: This work was supported by the National Interprofessional Initiative on Oral Health (NIIOH) Interprofessional Oral-Systemic Health Curricular Innovation Award (OHNEP), 2015. References [1] L.V. Kalia, A.E. Lang, Parkinson's disease, Lancet 386 (2015) 896e912. [2] A. Lee, R.M. Gilbert, Epidemiology of Parkinson disease, Neurol. Clin. 34 (2016) 955e965. [3] A. Sauerbier, P. Jenner, A. Todorova, K.R. Chaudhuri, Non motor subtypes and Parkinson's disease, Park. Relat. Disord. 22 (2016) S41eS46. [4] M.A. van der Marck, B.R. Bloem, How to organize multispecialty care for patients with Parkinson's disease, Park. Relat. Disord. 20 (Suppl 1) (2014) S167eS173. [5] R.F. Pfeiffer, I. Bodis-Wollner, Parkinson's Disease and Nonmotor Dysfunction, second ed., Humana Press Inc, 2013. [6] L.P. Prizer, N. Browner, The integrative care of Parkinson's disease: a systematic review, J. Park. Dis. 2 (2012) 79e86. [7] M.A. van der Marck, M. Munneke, W. Mulleners, E.M. Hoogerwaard, G.F. Borm, S. Overeem, B.R. Bloem, H.W. Nijmeijer, T.J. Tacke, O.L.G.F. Sinnige, J.N. Wessel, Integrated multidisciplinary care in Parkinson's disease: a non-randomised, controlled trial (IMPACT), Lancet Neurol. 12 (2013) 947e956. [8] P. Trend, J. Kaye, H. Gage, C. Owen, D. Wade, Short-term effectiveness of intensive multidisciplinary rehabilitation for people with Parkinson's disease and their carers, Clin. Rehabil. 16 (2002) 717e725. [9] L. Guo, Y. Jiang, H. Yatsuya, Y. Yoshida, J. Sakamoto, Group education with personal rehabilitation for idiopathic Parkinson's disease, Can. J. Neurol. Sci. 36 (2009) 51e59. [10] J.M. Miyasaki, J. Long, D. Mancini, E. Moro, S.H. Fox, A.E. Lang, C. Marras, R. Chen, A. Strafella, R. Arshinoff, R. Ghoche, J. Hui, Palliative care for advanced Parkinson disease: an interdisciplinary clinic and new scale, the ESAS-PD, Park. Relat. Disord. 18 (2012) S6eS9. [11] N. Giladi, Y. Manor, A. Hilel, T. Gurevich, Interdisciplinary teamwork for the treatment of people with Parkinson's disease and their families, Curr. Neurol. Neurosci. Rep. 14 (2014) 1e7. [12] Y. Zlotnik, Y. Balash, A.D. Korczyn, N. Giladi, T. Gurevich, Disorders of the oral cavity in Parkinson ’ s disease and parkinsonian syndromes, Park. Dis. 2015 (2015) 379482. [13] W.S. Borgnakke, Does treatment of periodontal disease influence systemic disease? Dent. Clin. North Am. 59 (2015) 885e917. [14] J. Müller, G.K. Wenning, M. Verny, a McKee, K.R. Chaudhuri, K. Jellinger, W. Poewe, I. Litvan, Progression of dysarthria and dysphagia in postmortem-
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Please cite this article in press as: N.S. Rozas, et al., Incorporating oral health into interprofessional care teams for patients with Parkinson's disease, Parkinsonism and Related Disorders (2017), http://dx.doi.org/10.1016/j.parkreldis.2017.07.012