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Aging With a Progressive Neurologic Disease

Presbyphagia Versus Dysphagia

Normal Versus Abnormal Swallowing Symptoms in Older Adults With Parkinson Disease and Multiple Sclerosis

Barrera, Marissa A. PhD, MSCS, CCC-SLP; O'Connor Wells, Barbara PhD, CCC-SLP

Author Information
Topics in Geriatric Rehabilitation: July/September 2019 - Volume 35 - Issue 3 - p 217-233
doi: 10.1097/TGR.0000000000000237
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Abstract

Dysphagia” is the clinical term for impaired, or abnormal swallowing. The root, “dys” refers to disorder or abnormality, and the suffix “phagia” arises from the Greek word “phagos,” which means “to swallow”.1,2 This clinical term refers to any abnormality in the transport of food and/or liquids from the mouth to the stomach. It is not a disease or primary medical diagnosis itself; it is a symptom of an underlying disease or disorder, such as stroke or Parkinson disease (PD). Some noticeable signs and symptoms of dysphagia include difficulty chewing, drooling of food and/or liquids, residue in the mouth after the swallow, choking or coughing, and complaints of food getting stuck.3

There are 3 phases of the swallow. These include the oral preparatory and oral transit (often spoken of as one phase), pharyngeal and esophageal phases. The oral phase of the swallow begins when food or liquid is received into the mouth. Once the consumed material is in the mouth, the teeth, tongue, lips, and cheeks work together with salivary enzymes to form a bolus. The timing of the oral preparation of a bolus is highly variable, and dependent on the type of food or liquids being consumed. The oral phase ends when the bolus moves from the front of the mouth posteriorly, and passes the anterior faucial arches. This anterior to posterior movement of the bolus typically takes 1 second. The pharyngeal phase of the swallow begins with the activation of the swallow reflex. This phase involves a complex sequence of anatomical and muscular movements intended to protect the airway from the misdirection the bolus into the trachea, and guide it appropriately toward to opening of the esophagus. The pharyngeal phase of the swallow is of overt concern because a poorly managed bolus places an individual at risk for penetration (bolus sitting at the level of, or on the vocal folds), and/or aspiration (bolus passing below the level of the vocal folds into the upper airway). In the final phase, the esophageal phase, the bolus enters the esophagus, and via top-to-bottom muscular contractions, the bolus is pushed down the length of the esophagus to the opening of the stomach. The transit time for the esophageal phase is highly variable, with a normal range from 8 to 20 seconds. Speech-language pathologists are allied health professionals trained to evaluate and treat dysphagia in all phases of the swallow.3

INCIDENCE AND PREVALENCE OF DYSPHAGIA IN THE ELDERLY

Approximately 9.4 million adults have dysphagia in the United States. Challenges or changes in swallowing are common among the elderly, due to the normal aging process or medical complications.4 Up to 60% of residents in nursing home settings are identified as having some form of dysphagia that requires therapeutic or medical intervention. In these same settings, speech-language pathologists often have a caseload of approximately 70% or more of dysphagic individuals. Statistics suggest that, by the year 2030, the number of individuals 65 years and older will double; those 85 years and older is likely to increase 5-fold. With advancing age comes the increased possibility of the need for long-term care.2

Groher and Crary3 provided some additional statistics regarding the prevalence of dysphagia in a variety of medical settings. They suggest that 16% to 22% of adults living in our communities have some level of dysphagia. In medical environments, approximately one-third of adult patients in acute rehabilitation settings have some presentation of swallowing impairment.

Dysphagia can lead to serious health risks, which are particularly concerning for the elderly. These risks can include malnutrition, dehydration, weight loss, impaired skin integrity, and/or aspiration pneumonia. Such health risks can have grave consequences on the health and quality of life of the elderly.2

There are a variety of conditions and disease processes that may result in dysphagia. These include acute-onset conditions, such as stroke or traumatic brain injury, or progressive neurological disorders, such as PD and multiple sclerosis (MS).

The purpose of this article is to describe normal, age-related changes in the swallowing mechanism, clinically referred to as “presbyphagia.” The authors compare presbyphagia to dysphagia in the oral, pharyngeal, and esophageal phases of the swallow in older individuals with PD and MS. As a reference point to readers, the authors used 65 years and older as an inclusion criterion when reviewing and considering articles for this publication.

PRESBYPHAGIA

Presbyphagia” is the clinical term for normal, age-related changes in the swallowing mechanism in individuals who are otherwise medically healthy.5 It has a pervasive occurrence in adults 65 years and older, similar to changes in hearing acuity (presbycusis), vision (presbyopia), or muscle tone5 Advances in medicine have led to longer life expectancy; however, with aging comes the increased likelihood of the onset of an acute (eg, stroke) or chronic (eg, PD) condition, which may have dysphagia as a comorbidity.2

Medications also play a multifactorial role in swallowing. As a person ages, there is an exponential increase in the likelihood that he or she will need to take one or more daily medications. Medications can affect all phases of swallowing by interfering with the central nervous system (eg, causing fatigue), lubrication (eg, causing dry mouth—xerostomia), and/or the gastrointestinal system (eg, causing constipation). Reduction in appetite, paired with normal age-related changes in olfaction and gustation, can disrupt daily caloric consumption and lead to dehydration and malnutrition in the elderly.3

In order to distinguish between presbyphagia (normal, age-related changes in swallowing) versus dysphagia (impaired and atypical swallowing), clinicians must be versed in the normal and expected functional changes in the swallowing mechanism associated with typical aging, versus the clinical signs and symptoms of dysphagia that are unrelated to normal aging.

Next, we discuss normal, age-related changes in each of the 3 phases of the swallow.

PRESBYPHAGIA: WHAT TO EXPECT WITH NORMAL AGING

Presbyphagia affects the oral phase of the swallow in a variety of ways. Changes in dentition, oral hygiene, saliva flow, and texture perception can individually, or collectively, alter the rate and efficiency of bolus movement in the oral cavity. Reduced tongue pressure and a decrease in overall tongue strength can further impact bolus clearance in the oral phase of the swallow.5

Looking specifically at the important anatomical landmarks in the oral phase, presbyphagia can impact the strength and function of the tongue, lips, and/or velum due to reduced muscle mass and muscle contraction.5 These changes can lead to slower and longer oral preparation and oral bolus transit times. Due to the aforementioned changes, older adults may avoid certain foods because they find the textures “too difficult” to manage. Oral transit time may also be slightly longer than the expected average of 1 second; however, the swallow remains within functional limits.3

Presbyphagia also impacts the pharyngeal phase of swallowing. The pharyngeal and laryngeal events, such the initiation of the swallowing reflex and airway protection, may also take slightly longer in older adults, and laryngeal excursion can also be significantly reduced. In older adults, it is more common to have the bolus bifurcate, or split, around the open airway, leading to the bolus pooling in the valleculae. These age-related changes can lead to a mismanagement of the bolus, resulting in increased risk for penetration and/or aspiration. These penetration/aspiration events may be more frequent and of greater severity compared with younger adults. Furthermore, when the body is taxed due to non-life-threating medical occurrences (eg, bronchitis and sinus infection), older adults, when compared with younger adults, may be less able to make the required physical accommodations due to their diminished functional reserve.

The final phase of the swallow, the esophageal phase, is most vulnerable to the aging process. The normal timing of 8 to 20 seconds for bolus clearance through the esophagus may take longer in older adults. In addition, there is reduced flexibility in the upper esophageal sphincter muscle, which can lead to shorter durations and a smaller diameter of cricopharyngeal opening at the top of the esophagus. These esophageal changes can leave older adults vulnerable to upper gastrointestinal dysfunction, such as heartburn, reflux, and other serious conditions, such as achalasia.2

DYSPHAGIA IN OLDER ADULTS WITH PARKINSON DISEASE AND MULTIPLE SCLEROSIS

We have previously discussed normal, age-related changes to swallowing. What happens when a neurological disorder is superimposed over these expected changes? In this section of the article, we discuss the “older swallow” in persons diagnosed with PD and MS.

Parkinson disease is a progressive, neurodegenerative disorder of the cortical and subcortical neurons, midbrain, and brainstem that affects more than 1 million Americans.

Parkinson disease is associated with motor and nonmotor symptoms, including tremor, rigidity, dementia, and dysphagia. During the early stages of the disease, up to 80% of all patients with PD may present with oropharyngeal dysphagia; in the advanced stages, the incidence of dysphagia may reach as high as 95%. Individuals with PD are 3.8 times more susceptible to developing aspiration pneumonia in comparison to the general population.6

Multiple sclerosis is one of the most common neurological diseases worldwide, with an estimated 400 000 people living with MS in the United States.7 MS is a progressive disorder of the central nervous system that results in demyelination of nerve fibers and causes axonal injury.8 The development of scattered lesions, plaques, or both within the brain produces varying combinations of motor, sensory, and cognitive-communication impairments.9 A study investigating persons with MS found a link between dysphagia, brainstem impairment, and severity of illness in 34% of participants. Although dysphagia is not typically a first sign of MS, it has been observed in mildly impaired patients with low levels of disability and increases as the disease progresses, reaching as high as 65% in severely disabled individuals with MS.10 Guan et al11 conducted a meta-analysis and determined an estimated dysphagia prevalence of 36% in persons with MS—concluding that approximately one-third of persons living with MS have swallowing difficulties.

In short, persons with medical conditions, such as PD and MS, are vulnerable to dysphagia beyond those swallowing changes observed and anticipated with normal aging. In both diseases, neural and physical fatigue are predominant symptoms that can interfere with swallowing safety and increase the likelihood for life-threatening consequences due to dysphagia.

There is a vast array of symptoms associated with dysphagia in persons with PD. In the oral phase, these symptoms may include delayed oral transit time, tongue pumping, oral repetitive movements, and premature loss of the bolus.3 In older adults with PD, Argolo et al12 suggested there is an association between the characteristic tongue pumping observed in PD and food consistencies: they noted a positive correlation between tongue pumping and managing more viscous, or thick and sticky consistencies. The co-occurrence of an unstable positioning of the bolus on the tongue, food leakage, and uncoordinated bolus propulsion into the pharynx contributed to penetration and/or aspiration for patients with PD when consuming thicker consistencies.12 Sialorrhea (drooling) is also highly prevalent in persons with PD, and is anecdotally reported in advanced MS. As measured by fiberoptic endoscopic evaluation of swallowing, which is the use of a flexible scope passed through the nose and into the throat to examine the swallow, patients with PD with daily sialorrhea present with more saliva penetration and/or aspiration events compared with healthy older adults.13 The ability to manage one's oral secretions is a prognostic indicator for a patient's inability to safely manage an oral diet.14 In other words, patients' difficulty swallowing their own saliva impacts their ability to safely swallow food and liquids.

In MS, there is evidence that tongue function is more compromised compared with lip function. Approximately 10% of persons with MS present with facial paresis.15 Oral phase dysphagia findings in MS can include bolus loss, poor bolus cohesion, pocketing of the bolus in the lateral sulci (the space between the lower gums and the inside of the cheek), and delayed oral transit time. The coexistence of multiple oral phase dysphagia symptoms can lead to fatigue, prolonged mealtimes, and reduced oral intake associated with disease progression.

There are a multitude of pharyngeal phase symptoms evident in persons with PD and MS. These include delayed swallow trigger, reduced and delayed laryngeal excursion, reduced epiglottic inversion, residue in the vallecula and/or pyriform sinuses, and increased pharyngeal transit time.3 Common physiological features in the pharyngeal phase for persons with severe PD include delayed timing of airway closure and reduced pharyngeal muscle constriction.16 Postmortem evidence illustrates that pharyngeal wall weakness may be significantly influenced by a denervation of the cricopharyngeus and inferior pharyngeal constrictor muscles, along with muscle atrophy.17

Persons with PD and MS are both vulnerable to death due to respiratory complications associated with toxic aspirates from saliva, food, and/or liquid entering the lungs. Due to rigidity associated with PD, and spasticity associated with MS, the respiratory system has increased difficulty managing foreign materials in the upper respiratory track. When a bolus is misdirected toward the airway, this can lead to penetration and/or aspiration. These conditions are of overt concern, due to the high risk of aspiration pneumonia among persons with PD and MS. Statistics indicate there has been a “10-fold increase”18 in the incidence of aspiration pneumonia in PD; however, due to medical interventions, mortality rate has decreased. Persons with both PD and MS are living longer, but they are at increased risk for one or more medical comorbidities that challenge their disease course.

Coordination between respiration and swallowing is a known challenge for persons with PD.19 Compared with healthy aging adults, persons with PD have been found to swallow at atypical moments in the respiratory cycle, such as upon inhalation and during low tidal volume, leading to increased aspiration due to reduced airway protection.19 In a 2016 study by Simons et al,20 the authors found that 37% of study participants with PD (N = 77) penetrated and/or aspirated during instrumental evaluation via fiberoptic endoscopic evaluation of swallowing.

In healthy individuals with an intact neurological system, a normal physiological response to penetration and/or aspiration is a strong throat clear and/or cough reflex. Persons with PD have decreased awareness of bolus residue, due to somatosensory deficits, which further contributes to their reduced airway protection.21 When patients are made aware of residue in their upper airway, verbal cueing for a strong cough and a reswallow is a common compensatory intervention taught by speech-language pathologists. Pitts et al22,23 found a direct correlation between airway protection and voluntary coughing. Their study found significant evidence suggesting that the reduced ability to voluntarily cough is linked to a higher probability of penetration/aspiration events.

In the final phase of the swallow, the esophageal phase, there is additional evidence of dysphagia beyond the characteristics associated with presbyphagia. For example, persons with MS may present with upper esophageal sphincter dysfunction, leading to a frequent complaint of gastroesophageal reflux disease.24 Moreover, in the early disease course of PD, patients may illustrate changes in pharyngoesophageal motility prior to the onset of oropharyngeal dysphagia symptoms.25 Via instrumental evaluation, Suttrup et al26 found the most common pathological finding for persons with PD was impairment of the esophagus (87.5%). A significant number of persons with PD also display dysfunction of the upper and lower esophageal sphincter muscles.15,27 Additional esophageal dysphagia symptoms may include delayed esophageal transport, esophageal residue, abnormal muscular contractions within the esophagus, evidence of gastroparesis, and difficulty with elimination.15

PSYCHOSOCIAL AND EMOTIONAL IMPACTS OF DYSPHAGIA FOR PERSONS WITH PD AND MS

There are a variety of psychosocial and emotional impacts from dysphagia for older adults with PD and MS. These may include loss of mealtime enjoyment, extended mealtimes, fear of choking, embarrassment of drooling during meals, loss of independence, and the need for caregiver assistance with meals. Caregivers report that these symptoms of dysphagia can lead to a disruption in family life.28 Healthy aging should not have an impact on overall quality of life, despite the increased likelihood of dysphagia in older adults compared with younger adults. However, Leow et al29 showed that dysphagia related to PD may significantly affect a person's quality of life.

Several studies have stressed the importance of early detection of dysphagia in patients with neurological diseases, to minimize these aforementioned swallowing deficits. For many persons with PD and MS, dysphagia and self-imposed dietary changes are often some of the early symptoms that are noticed by individuals and their family members. In many cases, these changes precede the onset of the typical neurological features of PD and MS.30 As described in Silbergleit et al, “self-perception of the emotional and functional handicapping effects of dysphagia in individuals with PD becomes significantly worse with longer duration of disease.”31(p502) Therefore, the time from disease diagnosis is indicative of the impairments or difficulties occurring in swallowing for persons with PD. “

Simons et al32 developed the Munich Dysphagia Test-Parkinsons Disease, a valid and reliable assessment tool to aid in the early detection of dysphagia in persons with PD. The authors concluded that early detection is key; early diagnosis and determination of the severity of swallowing dysfunction can minimize the risk of aspiration and improve overall quality of life.

Alfonsi et al33 suggested that swallowing abnormalities during the oral and pharyngeal phase of swallowing were frequently present in person with MS, even more than was previously known.33 For persons with MS, swallowing impairments are often underreferred and/or underidentified: only a small number of patients with MS (2%) are appropriately referred for speech, language, voice, and/or swallowing treatment.34 A contributing factor for this underreferral and underdiagnosis of dysphagia is that the Kurtzke Expanded Disability Status Scale (EDSS),35 the most commonly utilized neurological examination tool for MS, does not account for, or detect, mild to moderate swallowing impairment.36,37 In contrast, the Dysphagia in Multiple Sclerosis Questionnaire (DYMUS) is a reliable, valid, and easy-to-use tool for the early detection of dysphagia for both liquids and solids in persons with MS.38 Utilization of the DYMUS, in addition to the standard battery of neurological assessments given to individuals at medical appointments, would help improve the early detection of swallowing impairment in persons with MS.

In addition, PD and MS are frequently associated with the feelings of depression. Depression, which can take on many forms, is a common symptom. Clinical depression, a severe subtype, is more frequent among persons with MS than those with other chronic illnesses.39 The inflammation associated with MS, paired with medication side effects and changes in quality of life, contributes to feelings of depression. Changes in mealtime, food enjoyment, and physical symptoms with dysphagia can also lead to alterations in quality of life and feelings of depression.

Manor et al40 linked higher depression scores with more severe dysphagia symptoms in persons with PD. Comparison between patients who scored in the high depression range to participants in the lower ranges determined that swallowing disturbances occur more frequently in patients with high levels of depression. Higher anxiety and depression levels are associated with a severely progressed state of PD, which, in turn, leads to a greater number of swallowing disturbances.40

In the final section of this article, the authors highlight several treatment and management strategies frequently employed to alleviate the symptoms of dysphagia and improve swallowing safety and nutritional state in persons with PD and MS.

TREATMENT FOR DYSPHAGIA IN PARKINSON DISEASE AND MULTIPLE SCLEROSIS

While a detailed discussion on the rehabilitation of dysphagia is beyond the scope of this article, it is important to highlight some key points regarding the treatment of dysphagia in persons with PD and MS. Studies have shown that treatment has carryover benefits to the overall quality of life of individuals with such neurological diseases. In a study conducted by Ayres et al,41 individuals with PD were administered the Swallow Related Quality of Life42 before and after therapy; this is a clinician-facilitated questionnaire used to evaluate the impact of dysphagia on quality of life. A significant difference in total scores following therapy was observed, and participants with PD reported an overall improvement in swallowing-related quality of life following dysphagia intervention.

Simons et al20 found a difference between the clinical evaluation of dysphagia and a patient's self-assessment. Their participants with PD reported that dysphagia had a strong negative impact on their overall quality of life; for this reason, the authors suggest that it is essential to take into account each patient's psycho-emotional state when developing a comprehensive and personalized rehabilitation plan.

Some treatment approaches for dysphagia in neurological populations include surface electromyography (sEMG), neuromuscular electrical stimulation (NMES), intensive exercise programs (eg, effortful swallow, Masako maneuver, and Mendelsohn maneuver), dietary modifications, and postural changes (eg, chin tuck and head tilt). Oftentimes, one or more approaches are combined for maximum effectiveness.

Athukorala et al43 investigated the use, effectiveness, and retention of skilled therapy benefits for dysphagia in older adults with PD (X = 67.4 years). Utilizing sEMG and biofeedback, participants were able to make improvements in swallowing rate for liquids and lessened their overall symptoms of dysphagia. Effortful swallow, combined with biofeedback, was also found to be a successful treatment for patients with dysphagia secondary to PD.44

Bogaardt et al45 found that the application of NMES to the suprahyoid muscles in adults with advanced MS aided in the reduction of saliva pooling in the pyriform sinuses and reduced incidences of aspiration on thin liquids. In addition, their participants reported noticing improvements in their swallowing capability and overall quality of life after the treatment. Mu et al46 provided additional support for the use of surface electrical stimulation when applied to the internal superior laryngeal nerve during dysphagia therapy. They concluded that the swallow reflex could be significantly improved, as well as overall swallowing safety via improved airway closure, using NMES for older adults with PD. Expiratory muscle strength training (EMST), or the process of increasing the strength of respiratory muscles to improve cough, voice, and swallowing via a hand-held device, is an increasingly popular approach used with persons with PD, MS, and other neurological conditions. Troche et al47 concluded that EMST was effective in improving laryngeal elevation during swallowing for persons with PD. In Chiara et al,48 the use of EMST was determined to be beneficial for improving the strength of the respiratory muscles in participants with MS, especially those with a longer disease course and more severe EDSS ratings.

There is high importance in following the diet modifications recommended by speech-language pathologists, to reduce and manage the risk factors for choking, and minimize the development of aspiration pneumonia.49 Often, diet modifications are a necessary compensation for dysphagia in persons with PD and MS. Van Lieshout et al50 inferred that thicker liquids stimulate greater tongue movement amplitudes and durations, which affords patients additional time to control their bolus flow. This was also supported by Troche et al,51 who noted longer oral transit times and increased tongue pumping when swallowing a thicker bolus in persons with PD. A positive outcome from the use of thicker consistencies is reduced risk of penetration and/or aspiration.

Despite the benefits of thicker consistencies for patients with neurological conditions, patients are not always compliant with the suggested dietary changes. In a large-scale study by Logemann et al,52 participants with PD showed a preference for head posture compensations (ie, chin tuck) over using thickened liquids (ie, nectar and honey) to prevent penetration and aspiration. Although the thickened liquids lessened the penetration and aspiration events compared with use of the chin tuck, patients reported a dislike of thickened liquids and a preference for use of the chin tuck.

Beyond the traditional therapeutic approaches discussed earlier, South et al53 suggested that the simple act of chewing gum increases sensorimotor input to the oral cavity, which improves swallowing frequency and decreased the latency of swallowing. This is a cost-effective and simple, self-administered strategy that can improve secretion management in persons with PD and other neurological diseases where drooling is of concern.

In summary, compliance with therapeutic recommendations, whether compensatory (eg, diet modifications) or facilitatory (eg, NMES; traditional dysphagia therapy), supports the overall health, nutrition, and disease management of persons with dysphagia due to PD or MS.

CONCLUSIONS

The purpose of this article was to inform the reader about the differences between presbyphagia and dysphagia in older adults with PD and MS. All members of the rehabilitation team, whether speech-language pathologist, occupational therapist, or physician, need to be well informed about the expected changes in swallowing with age, as well as the likely symptoms of dysphagia in older persons with neurological diseases like PD and MS. Most importantly, the rehabilitation team needs to develop individualized and patient-specific treatments that will alleviate the impact of dysphagia on health, nutrition, disease course, psychosocial and emotional state, and overall quality of life for persons with neurological diseases like PD and MS.

References

1. Mann G. MASA: The Mann Assessment of Swallowing Ability. Clifton, NY: Singular; 2002.
2. Aslam M, Vaezi MF. Dysphagia in the elderly. Gastroenterol Hepatol. 2012;9(12):784–795.
3. Groher M, Crary M. Dysphagia: Clinical Management in Adults and Children. 2nd ed. St Louis, MO: Elsevier; 2015.
4. Bhattacharyya N. The prevalence of dysphagia among adults in the United States. Otolaryngol Head Neck Surg. 2014;151(5):765–769.
5. McCoy YM, Desai RV. Presbyphagia versus dysphagia: identifying age-related changes in swallow function. Perspect ASHA Spec Interest Groups. 2018;3(15):15–21.
6. Heijnen JB, Speyer R, Baijens WJL, Bogaardt CAH. Neuromuscular electrical stimulation verses traditional therapy in patients with Parkinson's disease and oropharyngeal dysphagia: effects on quality of life. Dysphagia. 2012;27(3):336–345.
7. National Multiple Sclerosis Society. MS Prevalence. https://www.nationalmssociety.org/Symptoms-Diagnosis/MS-Symptoms/Depression. Accessed June 10, 2018.
8. Bjartmar C, Trapp BD. Axonal and neuronal degeneration in multiple sclerosis: mechanisms and functional consequences. Curr Opin Neurol. 2001;14(3):271–8.
9. Yorkston KM, Klasner ER, Swanson KM. Communication in context: a qualitative study of the experiences of individuals with multiple sclerosis. Am J Speech Lang Pathol. 2001;10(2):126–37.
10. Calcagno P, Ruoppolo G, Grasso MG, De Vincentiis M, Paolucci S. Dysphagia in multiple sclerosis—prevalence and prognostic factors. Acta Neurol Scand. 2002;105:40–43.
11. Guan XL, Wang H, Huang HS, Meng L. Prevalence of dysphagia in multiple sclerosis: a systematic review and meta-analysis. Neurol Sci. 2015;36(5):671–681.
12. Argolo N, Sampaio M, Pinho P, Melo A, Nóbrega AC. Swallowing disorders in Parkinson's disease: impact of lingual pumping. Int J Lang Commun Disord. 2015;50(5):659–664.
13. Rodrigues B, Nóbrega AC, Sampaio M, Argolo N, Melo A. Silent saliva aspiration in Parkinson's disease. Mov Disord. 2011;26(1):138–41.
14. Nóbrega AC, Rodrigues B, Torres AC, Scarpel RDA, Neves CA, Melo A. Is drooling secondary to a swallowing disorder in patients with Parkinson's disease? Parkinsonism Relat Disord. 2008:14(3):243–245.
15. Duffy RJ. Motor Speech Disorders: Substrates, Differential Diagnosis, and Management. 3rd ed. St Louis, MO: Elsevier Mosby; 2013.
16. Ellerston JK, Heller AC, Houtz DR, Kendall KA. Quantitative measures of swallowing deficits in patients with Parkinson's disease. Ann Otol Rhinol Laryngol. 2016;125(5):385–392.
17. Mu L, Sobotka S, Chen J, et al. Altered pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol. 2012:71(6):520–530.
18. Akbar U, Dham B, He Y, et al. Incidence and mortality trends of aspiration pneumonia in Parkinson's disease in the United States, 1979-2010. Parkinsonism Relat Disord. 2015;21(9):1082–1086.
19. Gross RD, Atwood CW, Ross SB, Eichhorn KA, Olszewski JW, Doyle PJ. The coordination of breathing and swallowing in Parkinson's disease. Dysphagia. 2008;23:136–145.
20. Simons JA, von Clarmann S, Warnecke T. Reliability of a newly developed protocol for fiberoptic endoscopic evaluation of swallowing in Parkinson's patients (PARK-FEES). Mov Disord. 2016;31(2):S517–S518.
21. Hammer MJ, Murphy CA, Abrams TM. Airway somatosensory deficits and dysphagia in Parkinson's disease. J Parkinson Dis. 2013;3(1):39–44.
22. Pitts T, Bolser D, Rosenbek J, Troche M, Sapienza C. Voluntary cough production and swallow dysfunction in Parkinson's disease. Dysphagia. 2008;23(3):297–301.
23. Pitts T, Troche M, Mann G, Rosenbek J, Okun MS, Sapienza C. Using voluntary cough to detect penetration and aspiration during oropharyngeal swallowing in patients with Parkinson disease. Chest. 2010;138(6):1426–1431.
24. De Pauw A, Dejaeger E, D'hooghe B, Carton H. Dysphagia in multiple sclerosis. Clin Neurol Neurosurg. 2002;104(4):345–351.
25. Sung HY, Kim JS, Lee KS, et al. The prevalence and patterns of pharyngoesophageal dysmotility in patients with early stage Parkinson's disease. Mov Disord. 2010;25(14):2361–2368.
26. Suttrup I, Suntrup S, Hamacher C, et al. Prevalence and patterns of esophageal dysphagia in patients with Parkinson's disease or atypical Parkinsonism. Dysphagia. 2015;30:660.
27. Kim YH, Oh BM, Jung IY, Lee JC, Lee GJ, Han TR. Spatiotemporal characteristics of swallowing in Parkinson's disease. Laryngoscope. 2015;125(2):389–395.
28. Miller N, Noble E, Jones D, Burn D. Hard to swallow: dysphagia in Parkinson's disease. Age ageing. 2006;35(6):614–618.
29. Leow LP, Huckabee ML, Anderson T, Beckert L. The impact of dysphagia on quality of life in ageing and Parkinson's disease as measured by the swallowing quality of life (SWAL-QOL) questionnaire. Dysphagia. 2010;25(3):216–220.
30. Noyce AJ, Silveira‐Moriyama L, Gilpin P, Ling H, Howard R, Lees AJ. Severe dysphagia as a presentation of Parkinson's disease. Mov Disord. 2012;27(3):457–458.
31. Silbergleit A, Sidiropoulos C, Konnai R, Schultz L, Kitowski A, LeWitt P. Self-perception of dysphagia in Parkinson's disease. Mov Disord. 2017;32(2):S502.
32. Simons JA, Fietzek UM, Waldmann A, Warnecke T, Schuster T, Ceballos-Baumann AO. Development and validation of a new screening questionnaire for dysphagia in early stages of Parkinson's disease. Parkinsonism Relat Disord. 2014;20(9):992–998.
33. Alfonsi E, Bergamaschi R, Cosentino G, et al. Electrophysiological patterns of oropharyngeal swallowing in multiple sclerosis. Clin Neurophysiol. 2013;124(8):1638–1645.
34. Hartelius L, Svensson P. Speech and swallowing symptoms associated with Parkinson's disease and multiple sclerosis: a survey. Folia Phoniatr Logop. 1994;46(1):9–17.
35. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology. 1983;33(11):1444–1452.
36. Poorjavad M, Derakhshandeh F, Etemadifar M, Soleymani B, Minagar A, Maghzi MA. Oropharyngeal dysphagia in multiple sclerosis. Mult Scler. 2010;16(3):362–365.
37. Barrera MA. The Effect of a Single Bout of Physical Exertion on Expressive Language and Word Finding in Individuals With Multiple Sclerosis [dissertation]. New York: City University of New York; 2017.
38. Bergamaschi R, Crivelli P, Rezanni C, et al. The DYSMUS questionnaire for the assessment of dysphagia in multiple sclerosis. J Neurol Sci. 2008;269(1):49–53.
39. Bergamaschi R, Minguzzi S, Amato MP, et al. Validation of the DYMUS questionnaire for the assessment of dysphagia in multiple sclerosis. Funct Neurol. 2009;24(3):159.
40. Manor Y, Balas M, Giladi N, Mootanah R, Cohen JT. Anxiety, depression and swallowing disorders in patients with Parkinson's disease. Parkinsonism Relat Disord. 2009;15(6):453–456.
41. Ayres A, Jotz GP, Rieder CR, Schuh AF, Olchik MR. The impact of dysphagia therapy on quality of life in patients with Parkinson's disease as measured by the swallowing quality of life questionnaire (SWALQOL). Int Arch Otorhinolaryngol. 2016;20(3):202–206.
42. McHorney CA, Bricker DE, Robbins J, Kramer AE, et al. The SWAL-QOL Outcomes tool for oropharyngeal dysphagia in adults: I. Conceptual foundation and item development. Dysphagia. 2000;15:115–121.
43. Athukorala RP, Jones RD, Sella OS, Huckabee ML. Skill training for swallowing rehabilitation in patients with Parkinson's disease. Arch Phys Med Rehabil. 2014;95(7):1374–1382.
44. Felix VN, Correa SMA, Soares RJ. A therapeutic maneuver for oropharyngeal dysphagia in patients with Parkinson's disease. Clinics. 2008;63(5):661–666.
45. Bogaardt H, van Dam D, Wever NM, Bruggeman CE, Koops J, Fokkens WJ. Use of neuromuscular electrostimulation in the treatment of dysphagia in patients with multiple sclerosis. Ann Otol Rhinol Laryngol. 2009;118(4):241–246.
46. Mu L, Sobotka S, Chen J, et al. Parkinson disease affects peripheral sensory nerves in the pharynx. J of Neuropathol Exp Neurol. 2013;72(7):614–623.
47. Troche MS, Okun MS, Rosenbek JC, et al. Aspiration and swallowing on Parkinson disease and rehabilitation with EMST: a randomized trial. Neurology. 2010;75(21):1912–1919.
48. Chiara T, Martin AD, Davenport PW, Bolser DC. Expiratory muscle strength training in persons with multiple sclerosis having mild to moderate disability: effect on maximal expiratory pressure, pulmonary function, and maximal voluntary cough. Arch Phys Med Rehabil. 2006;87(4):468–473.
49. Goh KH, Acharyya S, Ng SYE, et al. Risk and prognostic factors for pneumonia and choking amongst Parkinson's disease patients with dysphagia. Parkinsonism Relat Disord. 2016;29:30–34.
50. Van Lieshout PH, Steele CM, Lang AE. Tongue control for swallowing in Parkinson's disease: effects of age, rate, and stimulus consistency. Mov Disord. 2011;26(9):1725–1729.
51. Troche MS, Sapienza CM, Rosenbek JC. Effects of bolus consistency on timing and safety of swallow in patients with Parkinson's disease. Dysphagia. 2008;23(1):26–32.
52. Logemann JA, Gensler G, Robbins J, et al. A randomized study of three interventions for aspiration of thin liquids in patients with dementia or Parkinson's disease. J Speech Lang Hear Res. 2008;51(1):173–183.
53. South A, Jog M, Somers S. Gum chewing improves swallow frequency and latency in Parkinson patients. Parkinsonism Relat Disord. 2010;15:1198–1202.
Keywords:

aging swallow; aspiration; dysphagia; multiple sclerosis; older adults; Parkinson disease; penetration; presbyphagia

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