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Zeitschrift für

Gerontologie+Geriatrie
Themenschwerpunkt

Z Gerontol Geriat 2019 · 52:330–335 Tobias Warnecke1 · Rainer Dziewas1 · Rainer Wirth2 · Jürgen M. Bauer3 · Tino Prell4,5
https://doi.org/10.1007/s00391-019-01563-x 1
Department of Neurology, University Hospital Münster, Muenster, Germany
Received: 12 February 2019 2
Department for Geriatric Medicine, Marien Hospital Herne, University Hospital Bochum, Herne, Germany
Accepted: 8 May 2019
3
Published online: 28 May 2019 Center for Geriatric Medicine, Heidelberg University, Heidelberg, Germany
4
© Springer Medizin Verlag GmbH, ein Teil von Department of Neurology, Jena University Hospital, Jena, Germany
Springer Nature 2019 5
Center for Healthy Ageing, Jena University Hospital, Jena, Germany

Dysphagia from a neurogeriatric


point of view
Pathogenesis, diagnosis and management

Introduction diagnosis algorithm and (iv) the man- and are summarized under the term
agement of dysphagia in neurogeriatric primary presbyphagia. Older people
Dysphagia is a common syndrome in patients. can have a prolonged oropharyngeal
older people and its prevalence increases phase, decreased posterior and superior
with age [27]. Although the reported Age-related changes of lingual movement, delayed pharyngeal
prevalence estimates across studies were swallowing: primary and triggering and initiation of the swal-
highly variable, it can be assumed that the secondary presbyphagia low reflex, smaller swallowing volume,
mean prevalence of dysphagia in commu- reduced hyolaryngeal movement, de-
nity dwelling older people is 15% and up The deglutition process can be divided layed opening of the upper esophageal
to 30% in those admitted to hospital [13]. into three sequential phases. 1. Oral sphincter, increased residual matter in
The highest prevalence of dysphagia has phase: during the voluntary preparatory the pharynx and a higher proportion of
been observed in neurological patients in phase the food enters the mouth and silent aspiration or penetration [10, 24,
up to 64% of those with a stroke and over the bolus is actively masticated. The bo- 31]. The reasons for these changes are
80% of those with dementia [1]. Despite lus is then placed on the anterior tongue multifactorial and include aspects such
its high prevalence, dysphagia is still un- and directed toward the posterior part of as decrement in taste and smell acuity,
derdiagnosed and frequently not actively the oral cavity by a posterior and supe- tooth problems, loss of muscle mass,
reported by older patients because they rior lingual movement (transport phase) sarcopenia, decrease of tissue elasticity,
may regard swallowing difficulties as a 2. Pharyngeal phase: at the beginning cervical spine changes and hyposaliva-
normal process during ageing. Further- of the involuntary pharyngeal phase the tion [17, 29]. These age-related changes
more, dysphagia contributes to a worse soft palate rises to close the nasopharynx are usually compensated and clinically
outcome, most notably increased risk of and to prevent nasopharyngeal regurgi- inapparent; however, they can impair
malnutrition, pneumonia and a higher tation. Then the hyoid bone rises, elevat- the ability to compensate disease-related
mortality as well as increased readmis- ing the larynx while the closed epiglottis swallowing dysfunction and lead to clini-
sions and institutionalization [21]. Age- protects the larynx. At the same time cally significant dysphagia ([17]; . Fig. 1;
related changes in the mouth, pharynx, the tongue contacts the pharyngeal wall, . Table 1). This secondary presbyphagia
larynx, and esophagus together with age- the inferior pharyngeal muscles contract, is the key mechanism in older patients
related neurological diseases predispose the cricopharyngeal muscle relaxes and with neurological disorders, such as
for dysphagia in older people. Therefore, the upper esophageal sphincter opens. stroke, Parkinson’s disease and dementia
according to a white paper published by 3. Esophageal phase: finally, the bolus [7].
the Dysphagia Working Group, a com- passes into the esophagus and moves to
mittee of members from the European the stomach with peristaltic movements. Complications of dysphagia:
Society for Swallowing Disorders and the These complex mechanisms greatly de- pneumonia and malnutrition
European Union Geriatric Medicine So- pend on the correct integration of sensory
ciety, dysphagia should be classified as inputs via the V, VII, IX, and X cranial Dysphagia in older age is an independent
a geriatric syndrome [1]. This review nerves, cortical central nervous system predictor of serious complications and is
provides an overview on (i) age-related input and medullary structures. associated with an increased mortality
changes of swallowing, (ii) the clinical Age-related changes of swallowing [4, 30]. Dysphagia can double the risk of
implications and complications, (iii) the can occur in every deglutition phase developing pneumonia [25]. The major-

330 Zeitschrift für Gerontologie und Geriatrie 4 · 2019


Fig. 1 8 Primary and secondary presbyphagia (modified from [17]). Even if the primary presbyphagia itself is clinical asymp-
tomatic, it permanently reduces the compensation reserve of the swallowing act, so that additional disease-related changes
can lead to more clinically relevant secondary dysphagia

ity of geriatric patients hospitalized for dysphagia and signs of impaired efficacy I. Anamnesis. A structured anamnesis
pneumonia have concomitant dysphagia, of swallowing were found to be relevant interview should systematically assess
which in turn determines the severity and risk factors of malnutrition [21]. More- causative underlying diseases, comor-
course of the infection [25]. Further- over, eating and drinking are integral bidities, drug history [28], onset and
more, dysphagia is associated with poor parts of social interaction and are par- progression of disease, current diet,
oral health, malnutrition and ultimately ticularly relevant for making and main- social situation, previous diagnosis and
with reduced physical and mental per- taining friendships and leisure activities. therapeutic trials. Subsequently, dyspha-
formance and frailty. In clinical practice, Dysphagia-associated anxiety and stigma gia-specific issues should be evaluated, in
the nutritional intake may be compro- is therefore associated with depression, particular changes in eating and drink-
mised in (1) pure chronic starvation with- social withdrawal, and reduced quality ing habits, avoidance of certain foods
out inflammation, (2) conditions with of life [18]. and consistencies, time required for eat-
sustained mild inflammation (e.g. can- ing, posture during eating, difficulty in
cer, rheumatoid arthritis) and (3) acute Diagnostic algorithm chewing, food residues after swallowing
diseases with significant inflammation in the mouth or throat, globus sensation,
which elevates resting energy expendi- Based on the available data and the rec- altered voice, throat clearing, coughing
ture (e.g. pneumonia) and decreases nu- ommendations of the white paper from or dyspnea during eating, leakage of food
tritional intake due to supressed appetite the European Society for Swallowing Dis- or liquids from the nose, etc. In addi-
[20]. Age-related changes that favor mal- orders and the European Union Geriatric tion, there is a specific need to ask about
nutrition are usually summarized under Medicine Society the following standard- possible complications of dysphagia,
the term anorexia of aging and include ized diagnostic algorithm for dysphagia such as the occurrence of pneumonia,
aspects such as loss of appetite and/or de- in geriatric patients is proposed: (1) dys- dehydration and weight loss. Special
creased food intake. As a result the com- phagia-specific anamnesis, (2) dysphagia questionnaires may be used to record
pensation of hypocaloric episodes during screening, (3) detailed clinical swallow- dysphagia symptoms and to assess the
acute illness is rendered more difficult ing examination, and (4) instrumental dysphagia risk. The swallowing distur-
in old people. Besides age, frailty, exces- examination methods. bance questionnaire (SDQ), originally
sive polypharmacy and cognitive decline, designed for use in Parkinson’s disease

Zeitschrift für Gerontologie und Geriatrie 4 · 2019 331


Abstract · Zusammenfassung

[14] has now been tested with satisfactory Z Gerontol Geriat 2019 · 52:330–335 https://doi.org/10.1007/s00391-019-01563-x
results in a mixed etiology dysphagia © Springer Medizin Verlag GmbH, ein Teil von Springer Nature 2019
collective [6]. For a less time-consum-
ing assessment of dysphagia symptoms T. Warnecke · R. Dziewas · R. Wirth · J. M. Bauer · T. Prell
the 10 questions eating assessment tool Dysphagia from a neurogeriatric point of view. Pathogenesis,
(EAT-10) was developed [3, 32]; how- diagnosis and management
ever, based on the currently available
data the authors recommend the SDQ Abstract
Dysphagia is becoming increasingly more Health (ICF) model, the diagnosis and
for neurogeriatric patients. To assess the
common in aging societies and, like the treatment of dysphagia in neurogeriatrics
health-related quality of life caused by classical geriatric syndromes, it is a relevant have already made progress, more research
dysphagia, the swallowing quality of life functional impairment. The prevalence is needed on the levels of activity/mobility,
(SWAL-QOL) questionnaire can be used of dysphagia is highest in the group of social environment, personal factors and the
[16] old patients with neurological disorders, environment. This article summarizes the
particularly in patients with stroke, dementia pathophysiological aspects as well as the
and Parkinson’s disease. In the various current evidence for diagnosis and treatment
II Dysphagia screening. Most of the pub- neurological diseases of older people disease- of neurogeriatric dysphagia. Due to its high
lished test protocols have been evaluated specific factors often have a decisive influence clinical relevance dysphagia should be added
in patients with stroke and are character- on the clinical management of dysphagia. to the geriatric syndromes as “impaired
ized by a relatively high sensitivity (>80%, In addition, the concept of primary and swallowing”.
sometimes >90%) and at best moder- secondary presbyphagia plays an important
role in understanding age-related dysphagia. Keywords
ate specificity (usually <60%) [9, 11]. Whereas at the organ level of the International Deglutition disorders · Malnutrition ·
Methodologically, the screening methods Classification of Functioning, Disability and Presbyphagia · Stroke · Dementia
can be differentiated into the following
two categories: (i) water swallowing tests
(e.g. 50, 70 or 90 ml water test, timed wa- Dysphagie aus neurogeriatrischer Sicht. Pathogenese, Diagnostik
ter swallow test, Toronto bedside swal- und Management
lowing screening test, TOR-BSST) and
(ii) tests with multiple food consisten- Zusammenfassung
Schluckstörungen (Dysphagien) werden des ICF-Modells die Diagnostik und Therapie
cies (Gugging swallowing screen, GUSS; von Schluckstörungen in der Neurogeriatrie
in alternden Gesellschaften zunehmend
volume viscosity test, VVST; semisolid häufiger und stellen wie die klassischen geria- bereits Fortschritte erzielt hat, gibt es auf
bolus swallow test); however, only multi- trischen Syndrome eine relevante funktionelle den Ebenen Aktivität/Mobilität, soziales
ple food consistency tests allow differen- Beeinträchtigung dar. Am höchsten ist die Umfeld, persönliche Faktoren und Umwelt
tiated recommendations regarding diet Prävalenz von Dysphagien in der Gruppe alter noch weitreichenden Forschungsbedarf.
Patienten mit neurologischen Erkrankungen, Dieser Artikel fasst die pathophysiologischen
and therapeutic procedures. According
insbesondere im Rahmen eines Schlaganfalls, Grundlagen sowie die derzeitige Evidenz für
to the available data so far, the VVST einer Demenz oder eines Morbus Parkinson. Diagnostik und Therapie neurogeriatrischer
seems to be particularly suitable for the Bei den verschiedenen neurologischen Dysphagien zusammen und kommt zu dem
use in neurogeriatric patients [1, 5]. The Erkrankungen des älteren Menschen haben Ergebnis, dass Schluckstörungen aufgrund
test has a sensitivity of 88.2% and a speci- krankheitsspezifische Faktoren oft einen ihrer klinischen Relevanz den geriatrischen
entscheidenden Einfluss auf das klinische „I’s“ als „impaired swallowing“ hinzugefügt
ficity of 64.7% for the detection of pen-
Management von Dysphagien. Darüber werden sollten.
etration or aspiration [5]. It has the ad- hinaus kommt dem Konzept der primären und
vantage in older, frail people, for whom sekundären Presbyphagie eine wichtige Rolle Schlüsselwörter
extended instrumental dysphagia diag- für das Verständnis altersassoziierter Schluck- Schluckstörung · Malnutrition · Presbyphagie ·
nostics are sometimes not available or störungen zu. Während auf der Organebene Schlaganfall · Demenz
are not desired to be performed, that
nevertheless an adequate compensatory
treatment strategy can be derived from dysphagia as a basis for further diag- IV: Instrumental procedures. The fiber-
the results [23]. The aim of the VVST is nostics, meal adjustment and treatment optic endoscopic examination of swal-
not only to detect an aspiration risk but planning. The survey begins with an ex- lowing (FEES) is currently the most
also to find a safe diet. amination of oropharyngeal structures widely used method and is recom-
and ends with swallowing experiments in mended in several guidelines of various
III: The detailed clinical swallowing ex- which different consistencies, usually in professional societies [8]. A flexible na-
amination. This falls within the scope the order semisolid, liquid, and solid, are sopharyngeal laryngoscope is inserted
of appropriately trained speech and lan- tested. For the documentation of dyspha- transnasally into the pharynx to directly
guage therapists. In addition to the as- gia severity several scores are available, visualize the swallow. The standard FEES
sessment of the aspiration risk, it also e.g. the Bogenhausen dysphagia score protocol consists of (i) an anatomical
includes the accurate determination of (BODS) [2], which has not yet been val- physiological examination, (ii) swallow-
the pattern and severity of neurogenic idated for neurogeriatric patients. ing examination, and (iii) assessment

332 Zeitschrift für Gerontologie und Geriatrie 4 · 2019


Table 1 Patterns of dysphagia in neurogeriatric patients should be determined. Second, patients
Dysphagia Frequent findings at risk for malnutrition or a state of
Chronic post-stroke Significant premature spillage, delayed oral transfer, delayed pha- malnutrition should be identified using
ryngeal swallowing, reduced hyolaryngeal elevation, impaired the mini-nutritional assessment (MNA)
upper esophageal sphincter opening (Wallenberg syndrome) and receive a high-calorie, high-pro-
Alzheimer’s disease Oral residue, delayed oral transfer, oral apraxia, delayed pharyn- tein diet. Third, patients and caregivers
geal swallow, pharyngeal residue, reduced hyolaryngeal elevation should receive hands-on guidance to op-
Parkinson’s disease Repetitive pumping movements of the tongue, oral residue, timize oral hygiene. Preliminary results
premature spillage, piecemeal deglutition, residue in vallecu- suggest that the MMI might become
lae and pyriform sinuses, somatosensory deficits, esophageal a simple and cost-effective strategy to
hypomotility, esophageal spasms
reduce dysphagia complications in the
Drug-induced: tardive dyski- Reduced base of tongue retraction, disorganized tongue move-
geriatric population with an acute dis-
nesia ments, pharyngeal residue, irregular and insufficient pharyngeal
contractions ease admitted to a general hospital. In
addition, special drug or surgical treat-
ment options are available for specific
of the effectiveness of therapeutic mea- neurological disorders that are highly forms of neurogenic dysphagia. Neu-
sures. In addition to this standard prevalent in older people (. Table 1). rostimulation methods (e.g. transcranial
protocol, specific investigational pro- Based on the merits and disadvantages magnetic stimulation, transcranial direct
tocols have been validated for several of each of the diagnostic modalities pre- current stimulation and pharyngeal elec-
neurological disorders (FEES-tensilon sented above, as well as their varying site trical stimulation) are promising new
test and fatigable swallowing test for to site availability, a proposed diagnostic options that are currently being inves-
myasthenic dysphagia; FEES-L-dopa algorithm for geriatrics dysphagia diag- tigated in several clinical studies [27].
test for the detection of L-dopa-sensi- nostics is shown in . Fig. 2. Specific treatment options for stroke-re-
tive dysphagia in Parkinson’s disease; lated dysphagia with preliminary proof
fiberoptic endoscopic dysphagia severity Treatment of benefits are thermal tactile stimu-
scale (FEDSS) for grading and man- lation, electromyographic biofeedback,
agement of stroke-related dysphagia) The primary goal of therapy is an ad- Mendelsohn maneuver, Shaker exer-
[27]. The video fluoroscopic evaluation equate diet without any risk of aspi- cise, expiratory muscle strength training
of swallowing (VFSS) is a contrast-en- ration. For this purpose, speech and (EMST), and the abovementioned neu-
hanced radiographic examination that language therapists specialized in swal- rostimulation methods; however, all
allows a cinematic recording of the en- lowing treatment can resort to a variety of these methods have to be validated in
tire swallowing process [2, 12]. The different methods depending on the clin- further randomized and multicenter
VFSS is usually carried out according to ical aspects of dysphagia. Furthermore, studies. For dysphagia in patients with
the so-called Logemann standard [12] multidisciplinary collaboration between Alzheimer’s disease there is some ev-
with increasing swallowing volumes. neurologists, geriatricians, speech and idence that thickening of liquids may
The image sequences are evaluated both language therapists, nutrition specialists, reduce the aspiration risk [27]. For
qualitatively and quantitatively [26]. Fi- nurses, physiotherapists, occupational patients with Parkinson’s disease-related
nally, with the modern high-resolution therapists and social services is essen- dysphagia it is recommended to test
manometry (HRM) endoluminal pres- tial for optimal treatment of neurogenic if dysphagia improves after adjustment
sures in the pharynx and esophagus can dysphagia [22]. In geriatric patients of dopaminergic treatment. In Parkin-
be measured during swallowing. This the factors (i) dysphagia/reduced cough son’s disease the thickening of liquids
method is particularly suitable for de- reflex, (ii) frailty/malnutrition/impaired may be more effective that the Chin-
tecting relaxation disorders of the upper immunity and (iii) poor oral health/ tuck maneuver in avoiding aspiration;
esophageal sphincter and motility disor- colonization with pathogenic germs sig- however, on an individual level one
ders of the esophagus (achalasia, diffuse nificantly contribute to the etiology of might consider performing the Chin-
esophageal spasm). Further electromyo- aspiration pneumonia [19]. A useful in- tuck maneuver when thickening of liq-
graphy (surface or needle electrodes) tervention has to cover all these factors. uids is refused by the patients, which
as well as sonography and dynamic For this purpose the minimally massive frequently occurs in the long term. In
magnetic resonance imaging are pre- intervention (MMI) was developed to any case, the effectiveness of the chosen
dominantly experimental procedures for reduce nutritional and respiratory com- method should be evaluated by FEES or
the evaluation of the swallowing act, plications in older hospitalized patients VFSS. Effortful swallowing can be used
which have not yet found their way into with dysphagia [15]. The MMI consist to reduce pharyngeal residues and FEES
clinical routine. By using instrumen- of the following steps: first, with the help can serve as a biofeedback method dur-
tal tools specific disturbance patterns of the VVST the appropriate diet for the ing the swallowing therapy. Expiratory
of dysphagia can be found in different individual patient and, if necessary, the muscle strength training (EMST) for 4
required degree of thickening of liquids weeks can result in decreased severity

Zeitschrift für Gerontologie und Geriatrie 4 · 2019 333


Themenschwerpunkt

Fig. 2 8 Diagnostic algorithm for dysphagia in older patients. At the first level, this algorithm provides a history-based med-
ical record structured by the use of validated questionnaires (SDQ swallowing disturbance questionnaire EAT-10 eating as-
sessment tool) and the application of the volume viscosity swallow test (VVST). If there are no indications of the presence of
dysphagia, the dysphagia-specific examination at this point can be terminated and no therapeutic interventions are required;
however, if there are indications of the presence of dysphagia, at least one clinical swallowing examination should be carried
out but ideally also an instrumental procedure (preferably fiberoptic endoscopic examination of swallowing, FEES). BODS Bo-
genhausen dysphagia score, PEG percutaneous endoscopic gastrostomy, VFSS video fluoroscopic evaluation of the swallow-
ing act

of penetration and aspiration in mild impairment of swallowing and can


Corresponding address
to moderate Parkinson’s disease-related lead to secondary presbyphagia.
dysphagia [27]. 4 A neurogeriatric diagnostic algo- Prof. Dr. med. Tobias Warnecke
rithm should cover (i) dysphagia- Department of Neurology, University Hospital
Münster
Conclusion specific anamnesis, (ii) dyspha-
Muenster, Germany
gia screening, (iii) detailed clinical Tobias.warnecke@ukmuenster.de
4 The prevalence of dysphagia increases swallowing examination, and (iv) in-
PD Dr. med. Tino Prell
with age. strumental examination methods.
Department of Neurology, Jena University
4 Dysphagia is still underdiagnosed 4 There is an urgent need to study Hospital
and frequently not spontaneously dysphagia in out-patient settings to Jena, Germany
reported by the patients. explore barriers and facilitators of Tino.prell@med.uni-jena.de
4 Age-related changes of swallowing different diagnostic and therapeutic
(primary presbyphagia) impair the strategies in detail.
compensation of disease-related

334 Zeitschrift für Gerontologie und Geriatrie 4 · 2019


Fachnachrichten

16. Mchorney CA, Robbins J, Lomax K et al (2002)


Compliance with ethical The SWAL-QOL and SWAL-CARE outcomes
guidelines tool for oropharyngeal dysphagia in adults:
III. Documentation of reliability and validity.
Dysphagia 17:97–114
Conflict of interest T. Warnecke, R. Dziewas, R. Wirth, 17. Muhle P, Wirth R, Glahn J et al (2015) Age-
J.M. Bauer and T. Prell declare that they have no com- related changes in swallowing. Physiology and
peting interests. pathophysiology. Nervenarzt 86:440–451
18. Ney DM, Weiss JM, Kind AJ et al (2009) Senescent
For this article no studies with human participants swallowing: impact, strategies, and interventions.
or animals were performed by any of the authors. All Nutr Clin Pract 24:395–413
studies performed were in accordance with the ethical
Herbert Czitober-
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Zeitschrift für Gerontologie und Geriatrie 4 · 2019 335

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