Journal of Neurology (2022) 269:1335–1352 https://doi.org/10.1007/s00415-021-10739-8 REVIEW A multinational consensus on dysphagia in Parkinson's disease: screening, diagnosis and prognostic value Giuseppe Cosentino1,2 · Micol Avenali1,3 · Antonio Schindler4 · Nicole Pizzorni4 · Cristina Montomoli5 · Giovanni Abbruzzese6 · Angelo Antonini7 · Filippo Barbiera8 · Marco Benazzo9 · Eduardo Elias Benarroch10 · Giulia Bertino9 · Emanuele Cereda11 · Pere Clavè12,13 · Pietro Cortelli14,15 · Roberto Eleopra16 · Chiara Ferrari4 · Shaheen Hamdy17 · Maggie‑Lee Huckabee18 · Leonardo Lopiano19 · Rosario Marchese Ragona20 · Stefano Masiero21 · Emilia Michou22 · Antonio Occhini9 · Claudio Pacchetti23 · Ronald F. Pfeiffer24 · Domenico A. Restivo25 · Mariangela Rondanelli26 · Giovanni Ruoppolo27 · Giorgio Sandrini1 · Anthony H. V. Schapira28 · Fabrizio Stocchi29 · Eduardo Tolosa30 · Francesca Valentino23 · Mauro Zamboni31 · Roberta Zangaglia23 · Mario Zappia32 · Cristina Tassorelli1,3 · Enrico Alfonsi2 Received: 20 May 2021 / Revised: 1 August 2021 / Accepted: 2 August 2021 / Published online: 21 August 2021 © The Author(s) 2021 Abstract Background Parkinson’s disease (PD) is a neurodegenerative disorder characterized by a combination of motor and non- motor dysfunction. Dysphagia is a common symptom in PD, though it is still too frequently underdiagnosed. Consensus is lacking on screening, diagnosis, and prognosis of dysphagia in PD. Objective To systematically review the literature and to define consensus statements on the screening and the diagnosis of dysphagia in PD, as well as on the impact of dysphagia on the prognosis and quality of life (QoL) of PD patients. Methods A multinational group of experts in the field of neurogenic dysphagia and/or PD conducted a systematic revision of the literature published since January 1990 to February 2021 and reported the results according to PRISMA guidelines. The output of the research was then analyzed and discussed in a consensus conference convened in Pavia, Italy, where the consensus statements were drafted. The final version of statements was subsequently achieved by e-mail consensus. Results Eighty-five papers were used to inform the Panel’s statements even though most of them were of Class IV quality. The statements tackled four main areas: (1) screening of dysphagia: timing and tools; (2) diagnosis of dysphagia: clinical and instrumental detection, severity assessment; (3) dysphagia and QoL: impact and assessment; (4) prognostic value of dysphagia; impact on the outcome and role of associated conditions. Conclusions The statements elaborated by the Consensus Panel provide a framework to guide the neurologist in the timely detection and accurate diagnosis of dysphagia in PD. Keywords Parkinson's disease · Dysphagia · Swallowing disorders · Deglutition disorders Introduction likely increase worldwide with increased life expectancy [2]. PD is characterized by motor features such as tremor, Parkinson’s disease (PD) is the second most common neu- rigidity and bradykinesia, and several non-motor features rodegenerative disorder worldwide [1]. The prevalence of such as dysphagia, autonomic dysfunction, sleep disorders, PD is estimated at 6.1 million individuals globally and will cognitive impairment, depression, and psychosis that may occur at any time during the disease course, but become more frequent with advanced disease [3, 4]. Giuseppe Cosentino and Micol Avenali have contributed equally Dysphagia in PD is a manifestation of swallowing dysfunc- to this paper. tion that may involve oral, pharyngeal or esophageal phases of swallowing and may be present in every stage of the disease * Micol Avenali micol.avenali@mondino.it [5]. Indeed, even though swallowing disorders become appar- ent mostly in the advanced stage of PD, they may already be Extended author information available on the last page of the article 13 Vol.:(0123456789) 1336 Journal of Neurology (2022) 269:1335–1352 present in the early stages, when they often go undetected [5]. dysphagia that has been held biannually since 2008 under Dysphagia frequently worsens with disease progression and the patronage of the Italian Society of Neurology, the may vary with motor fluctuations [6–8]. Globally, the preva- Italian Society of Neurorehabilitation, and the European lence of dysphagia in PD is estimated between 40 and 80% Society for Swallowing Disorders. The MCC method was depending on type of assessment performed [7]. designed according to the US National Institutes of Health Dysphagia can negatively affect the quality of life (QoL) Consensus Development Program (http://​conse​nsus.​nih.​ of individuals because of the progressive difficulty of oral gov) [16] and the Methodological Handbook of the Italian intake (food, drinks or oral medication), weight loss, dehy- National Guideline System [17]. dration, malnutrition and limitation of social activities [9]. The project was developed over a period of 36 months Moreover, aspiration pneumonia due to swallowing dysfunc- following five steps: (1) assignment phase, (2) scoping tion is an important and common cause of hospitalization in phase, (3) assessment phase, (4) face-to-face MCC, held patients with PD [10, 11], resulting in severe complications on 27–28th September 2019, at the IRCCS Mondino Foun- and even death [12–14]. dation, and finally (5) update of the evidence (up to Febru- To date, there is no generally accepted approach to the ary 2021) and refinement of statements by e-mail. screening and the diagnosis of dysphagia in PD. Therefore, The core of the consensus panel was formed by Ital- there is an urgent need to identify standardized protocols for ian neurologists who met regularly at the ‘Dysphagia the clinical assessment and investigation of dysphagia in this Update’ meetings. Additional specialists, also from dif- population. Moreover, it is important to emphasize the need for ferent medical disciplines and from other Countries were the early identification of swallowing abnormalities in patients invited to achieve a broad geographic and multidiscipli- with PD, especially as initially they may be asymptomatic [6]. nary representation. Participants were selected based on An established and formal methodology to provide reli- their recognized involvement in the care of large cohorts of able guidance in complex health issues in the absence of PD patients and/or their involvement in research projects high-quality evidence is represented by a consensus-based on PD and/or neurogenic dysphagia, and/or because of process. In this process, expert professionals reach a con- their publication record on neurogenic dysphagia in peer- sensus on statements aimed at providing a guide for clinical reviewed journals. Participants were invited by e-mail. A practice on the basis of the best available evidence and the single reminder was sent to those who did not reply to the group’s expertise. Typically, a panel of experts, after exam- first invitation. The final group was formed by 21 neurolo- ining the relevant scientific information and discussing the gists, 4 ENT specialists, three phoniatricians, two gastro- clinical issues, produce statements that reflect their shared enterologists, 4 speech-language pathologists, 2 clinical views, in agreement with available evidence [15]. nutritionists, one radiologist and a statistician. To increase the awareness of dysphagia in PD in the neu- In the assignment phase, four working teams with spe- rological health care practice and to optimize its screening cific roles were identified: and diagnosis, a group of experts in the field of dysphagia and/or PD set forth a Multinational Consensus Conference 1. The Scientific Committee, comprising seven members, (MCC) with the following objectives: planned and organized the whole project and developed the questions following the Classification of Evidence (1) To define the appropriate timing for screening dyspha- Schemes of the Clinical Practice Guideline Process gia in patients with PD and to identify reliable modali- Manual of the American Academy of Neurology [18]. ties; Several clinically relevant questions were proposed by (2) To define appropriate investigations for detecting swal- the Scientific Committee and discussed during several lowing alterations in PD and to assess their severity; iterations according to the PICO format as stated in (3) To assess the impact of dysphagia on the QoL of Appendix 1. The selection of the final questions to be patients; answered in this review was also guided by the results (4) To assess the prognostic values of dysphagia in PD out- of a preliminary literature search conducted to evalu- come; ate whether there was available evidence to support the (5) To identify unmet needs and highlight areas for future answers. The selection of the clinical questions was ulti- research. mately driven by the following criteria: i) to identify clinically relevant, focused topics (not taking too narrow Methods a focus nor too broad), ii) to select questions that could be answered, at least partly, on the basis of published, The project was initiated by the Organizing Committee peer-reviewed evidence. during the 2018 edition of the ‘Dysphagia Update’ Meet- 2. The Technical Committee, formed by six members, sys- ing, an international scientific event focused on neurogenic tematically reviewed the evidence, organized the results 13 Journal of Neurology (2022) 269:1335–1352 1337 into tables, and assisted the other teams in all steps of electronically: a first set of statements were generated and the project; sent by e-mail to the experts of the WG. Answers were 3. A working group (WG) formed by nine members whose collected and analyzed to inform necessary changes. The tasks were: 1) to prepare the first draft of answers to the second and the third rounds were carried out face-to-face, proposed questions prior to the consensus conference during the first and the second day of the MCC, respectively, and 2) to point out the research gaps in current knowl- with the participation of the entire panel. The fourth round edge and to propose areas for future research; was performed electronically: the final version of the state- 4. The consensus development panel, comprising six mem- ments, adapted, when required, according to the additional bers, was responsible for defining the presentation pro- analysis of paper published since the consensus conference, cedures at the MCC and for the assessment of the final was circulated by e-mail to the experts. On every round, a statements. minimum of 80% agreement for each statement was required for inclusion in the final consensus statement (25/31). In the scoping phase, the details of the literature review Ultimately, the systematic literature analysis covered the necessary to answer the questions developed by the Scien- period from January 1990 to February 2021. tific Committee (Appendix 1) were defined, together with protocol for the conference. In the assessment phase, the Technical Committee carried out a systematic review of the Results literature, which was reported according to PRISMA guide- lines [19]. Studies eligible for inclusion were those reporting Questions of the consensus conference original data on patients with PD suffering from dysphagia on screening, diagnosis, prognosis and QoL, regardless of The Scientific Committee formulated and submitted three the design type, published since January 1990. The follow- questions each on the screening and the diagnosis of dys- ing types of studies were excluded: studies published in phagia in PD and two questions each on the QoL and the abstract form only, case reports, reviews, editorials, letters, prognosis of patients with PD and dysphagia. studies on animals, and studies including patients with dys- Questions on screening: phagia of mixed etiology where data regarding PD could not be clearly enucleated. Published studies were identified from a) When is it indicated to screen for dysphagia in patients the National Library of Medicine's MEDLINE database, by with PD? means of specific search strategies, using a combination b) When should dysphagia be suspected in patients with of exploded MeSH terms and free text (search strategy is PD? reported in Appendix 2). Reference lists of identified articles c) What clinical tools should be used to screen for dyspha- were reviewed to find additional references. All abstracts or gia in patients with PD? full papers without electronic abstracts were reviewed inde- pendently by two reviewers to identify potentially relevant Questions on diagnosis: studies. Disagreement was resolved by discussion. Each study was classified according to various descriptors, includ- a) What clinical tools should be used to detect the presence ing topic domain, sample size, design, and level of evidence of dysphagia? according to the Classification of Evidence Schemes of the b) What instrumental investigations should be used to Clinical Practice Guideline Process Manual of the American detect the presence of dysphagia? Academy of Neurology [18]. c) How should severity of dysphagia be assessed? Each study was graded according to its risk of bias from Class I (highest quality) to Class IV (lowest quality). Risk of Questions on QoL: bias was judged by assessing specific quality elements (i.e., study design, patient spectrum, data collection, masking) for a) What is the effect of dysphagia on the QoL of patients each clinical topic (screening, diagnosis, prognosis, treat- with PD? ment). This classification was performed by two reviewers, b) How should dysphagia-related QoL in patients with PD with disagreement resolved by discussion. be clinically assessed? In consideration of the multidisciplinary of the expert groups and the generally weak strength of evidence emerged Questions on prognosis: from the systematic analysis of the literature, we adopted the modified Delphi method [18] to achieve consensus a) Does dysphagia influence the prognosis of PD? and develop the final statements. The method consisted b) What factors or associated conditions can influence the in four subsequent rounds. The first one was performed prognosis of dysphagia in PD? 13 1338 Journal of Neurology (2022) 269:1335–1352 For each question, specific eliciting questions were for- characteristics of the studies retrieved (see Supplementary mulated by the Technical Committee to stimulate and guide material 2 for complete list of references), whereas Table 2 the discussion among the members of the WG (Supplemen- depicts the main information on the single studies used as tary material 1). the basis for the statements. Systematic review Screening of dysphagia in PD The literature search retrieved 747 citations from electronic Although dysphagia is a common symptom in PD, most search and 8 records from manual search in the reference patients with PD do not complain of swallowing difficulties lists (Fig. 1). The abstract of the 747 citations were reviewed even when specifically asked, because they are generally not to assess potential relevance, and 249 were included for aware of their swallowing problems [20, 21]. full text evaluation. A total of 174 papers finally met the Therefore, there is a gap in the literature on dyspha- prespecified inclusion criteria. Of these, 117 papers dealt gia prevalence between subjectively reported impairment with the questions posed, but only 85 contained useful (35%) and objectively confirmed swallowing impairments findings to elaborate the statements. The majority of stud- by screening questionnaires or clinical evaluations (85%) [7, ies were of Class IV quality. Table 1 summarizes the main 22]. Indeed, signs of penetration and/or aspiration may be Records idenfied through database Addional records idenfied through searching other sources (n = 747) (n = 8) Records screened Records excluded (n = 755) (n = 506) Full-text arcles assessed for eligibility Full-text arcles excluded (n = 249) (n = 75) Studies included in the quantave descripon (n = 174) Studies on treatment and nutrion (n = 64) Studies included in the evaluaon of screening, diagnosis, QoL and prognosis (n = 117) Studies included in the statements (n = 85) Studies at the basis of statements for Quesons Studies at the basis of statements for Quesons on on screening and diagnosis quality of life and prognosis (n = 61) (n = 24) Fig. 1  PRISMA flow diagram 13 Journal of Neurology (2022) 269:1335–1352 1339 Table 1  Descriptive features of the 117 eligible studies included in the evaluation of screening, diagnosis, QoL and prognosis Topic domain All studies Number of patients = number Cross-sectional/pro- Case–control/retro- Class of evidence of studies spective studies spective study N N N N N Screening and diag- 82 < 10 pts = 1 58 24 4 Class I nosis of dysphagia 10–19 pts = 16 studies 4 Class II in PD 20–50 pts = 28 studies 18 Class III > 50 pts = 37 studies 56 Class IV QoL and prognosis of 35 < 50 pts = 13 20 15 4 Class I dysphagic patients 50–199 pts = 13 8 Class II with PD 200–500 pts = 5 8 Class III > 500 pts = 4 15 Class IV Studies were classified according to various descriptors, including topic domain, sample size, design, presence of diagnostic criteria of the syn- drome and level of evidence according to the Classification of Evidence Schemes of the Clinical Practice Guideline Process Manual of the American Academy of Neurology 17. Each study was graded according to its risk of bias from Class I to Class IV (with I corresponding to the highest quality and IV to the lowest quality) detected in 20% of the PD population without any complaint In these cases, a screening evaluation should be com- of swallowing difficulties [23, 24]. pleted regardless of PD disease stage [5, 34]. The early diagnosis of dysphagia in PD may be challeng- The presence of different symptoms and/or signs in com- ing. However, many symptoms and signs may indicate the bination can increase the sensitivity and specificity of the need for a screening. These are: increased duration of meals, screening procedures [35, 36]. difficulty in tablet swallowing and sensation of food sticking Different clinical scales and questionnaires have been or persisting in the throat after swallowing, coughing and proposed for screening dysphagia in neurodegenerative choking during ingestion of food and liquids, post-swallow- diseases [35–45], though there is no agreement on the best ing changes in voice (e.g. gurgling voice), weight loss or low algorithm for evaluating patients with PD. body mass index while recurrent chest infections [25–29]. The following clinical scale and questionnaires (evidence Also, drooling is considered by some authors as a possi- of class III and IV) may be used for screening of dysphagia ble indirect marker of dysphagia, since it can be the conse- in PD: quence of oropharyngeal swallowing alterations [30]. Using a modified barium swallowing videofluoroscopy, Nóbrega • Swallowing disturbance questionnaire (SDQ) [38]: a et al. [30] showed that all patients with PD and drooling also self-reported questionnaire containing 15 items on swal- presented changes in the oral phase of swallowing, whereas lowing disturbances. It is considered a validated tool to alterations in the pharyngeal phase were detected in 94% of detect early dysphagia in patients with PD. It has a good subjects. Drooling also correlates with dysphagia severity sensitivity and specificity (80.5 and 81.3%, respectively). and may have a negative prognostic value, as it is associated • Munich Dysphagia test-Parkinson’s disease (MDT-PD) with an increased risk of salivary aspiration without any [39]: a self-reported questionnaire useful to screen for outward sign of coughing, choking, or respiratory change initial oropharyngeal symptoms and the risk of laryn- (silent aspiration) [30–32]. geal penetration and/or aspiration in PD. It consists of A recent study [33] conducted in patients with PD 26 items divided into 4 categories. The MDT-PD is con- aged > 63.5 years identified the following characteristics as sidered a sensitive and specific questionnaire; however, predictors of an increased risk to develop dysphagia: a daily it was reported that compared with FEES it has a low levodopa equivalent dose higher than 475 mg and a PD clini- sensitivity in detecting aspiration, though maintaining cal subtype characterized by early postural instability and good specificity [46]. gait difficulty. • Swallowing Clinical Assessment Score in Parkinson’s Altogether, the data from the literature suggest that dys- disease (SCAS-PD): a quantitative clinical scale con- phagia in PD should be suspected in the presence of direct sisting of 12 items designed to detect alterations in the symptoms (coughing or choking when eating or drinking, oral and pharyngeal phases of swallowing in PD [36]. wet-sounding voice when eating or drinking, sensation of Branco et al. [40] validated this scale using the vide- food stuck in the throat and difficulty of chewing food prop- ofluoroscopic swallow study (VFSS) as the reference erly), or indirect signs (congestion of the lower respiratory diagnostic test. They showed that SCAS-PD has a high tract, bronchitis or pneumonia and unintentional weight sensitivity (100%) and specificity (87.5%) and it enables loss). to detect clinical signs of aspiration with a good con- 13 1340 Journal of Neurology (2022) 269:1335–1352 Table 2  Studies used as basis for the development of statements regarding questions on A) screening and diagnosis of dysphagia and B) dyspha- gia-related QoL and prognostic value of dysphagia in PD A) Question First author, y Study design Screening /Diagnostic test assessed N. patients Level of evidence 2.1 a Ali, 1996 Case–control VFSS and manometry 12 III 2.2. b 2.1 a Bird, 1994 Cross-sectional Clinical examination 16 IV 2.1 a Hartelius, 1994 Cross-sectional Questionnaire 258 II 2.1 a Monteiro, 2014 Case–control Spirometry and VFSS 30 IV 2.1 b Buhmann, 2019 Case–control FEES 118 IV 2.1 b Claus, 2020 Case–control FEES 200 III 2.1 b Lam, 2007 Cross-sectional Questionnaire, WST, and VFSS 45 I 2.1 b Loureio, 2013 Case–control Questionnaire 174 IV 2.1 b Pflug, 2018 Case–control FEES 122 I 2.1 b Potulska, 2003 Case–control Electromyography and esophageal scintigraphy 18 IV 2.1 b Rodrigues, 2011 Cross-sectional FEES 28 IV 2.2 b 2.1 b Sampaio, 2014 Cross-sectional FEES and voice recording 19 III 2.1 b Troche, 2016 Cross-sectional Voluntary and reflex cough and cough airflow (PEFR) 64 IV 2.1 c Belo, 2014 Case–control WST 10 IV 2.1 c Buhmann, 2019 Case–control Questionnaire 119 IV 2.1 c Kalf, 2011 Cross-sectional Questionnaire 178 IV 2.1 c Manor, 2007 Cross-sectional Questionnaire 57 III 2.1 c Minagi, 2018 Case–control WST, tongue pressure measurement 30 IV 2.1 c Simons, 2014 Cross-sectional Questionnaire 82 IV 2.1 c Singer, 1992 Case–control Questionnaire 48 IV 2.1 c Vogel, 2017 Cross-sectional Questionnaire 60 III 2.1 c Volontè, 2002 Cross-sectional Questionnaire 65 IV 2.2 a Hegland, 2014 Case–control Reflex cough testing 22 IV 2.2 a Kanna, 2014 Case–control WTS 100 IV 2.2 a Mari, 1997 Cross-sectional Questionnaire 27 II 2.2 a Miller, 2009 Cross-sectional WST 137 III 2.2 a Miyazaki, 2002 Cross-sectional WST 24 II 2.2 a Monte, 2005 Cross-sectional VFSS 27 IV 2.2 a Pitts, 2010 Cross-sectional PEFR and VFSS 58 III 2.2 a Pitts, 2018 Cross-sectional Tongue pressure measurement 28 IV 2.2 a Silverman, 2016 Cross-sectional PEFR 68 IV 2.2 a Troche, 2014 Cross-sectional Reflex cough testing and VFSS 20 IV 2.2 b Alfonsi, 2007 Case–control EKSS 28 IV 2.2 b Argolo, 2015a Cross-sectional VFSS 69 IV 2.2 b Argolo, 2015b Cross-sectional VFSS 71 IV 2.2 b Bassotti, 1998 Case–control Manometry 18 IV 2.2 b Castell, 2001 Cross-sectional Manometry 16 IV 2.2 b Cosentino, 2020 Cross-sectional Electrophysiological assessment of swallowing 19 IV 2.2 b Ding, 2018 Cross-sectional VFSS 116 III 2.2 b Ellerston, 2016 Case–control VFSS 34 IV 2.2 b Ertekin, 2002 Case–control Surface electromyography 58 III 2.2 b Fuh, 1997 Cross-sectional VFSS 19 IV 2.2 b Gaeckle, 2019 Cross-sectional VFSS 89 IV 2.2 b Hammer, 2013 Cross-sectional FEES 18 IV 2.2 b Johnston, 1997 Case–control VFSS and manometry 7 IV 2.2 b Jones, 2016 Cross-sectional VFSS 26 IV 2.2 b Jones, 2018 Case–control HRM 31 III 2.2 b Kim, 2020 Cross-sectional surface electromyography 14 IV 2.2 b Lee, 2015 Case–control VFSS 29 IV 2.2 b Lee, 2019 Case–control VFSS 23 IV 2.2 b Moreau, 2015 Cross-sectional VFSS 70 I 2.2 b Nagaya, 1998 Case–control VFSS 16 IV 13 Journal of Neurology (2022) 269:1335–1352 1341 Table 2  (continued) A) Question First author, y Study design Screening /Diagnostic test assessed N. patients Level of evidence 2.2 b Schiffer, 2019 Case–control VFSS 68 IV 2.2 b Stroudley, 1991 Cross-sectional VFSS 24 III 2.2 b Su, 2017 Cross-sectional HRM 33 IV 2.2 b Suttrup, 2017 Cross-sectional HRM and FEES 65 IV 2.2 b Taira, 2020 Cross-sectional HRM 51 IV 2.2 b Tomita, 2018 Case–control VFSS 184 II 2.2 b Wakasugi, 2017 Cross-sectional VFSS 201 IV 2.2 b Wang, 2017 Cross-sectional EKSS 42 IV 2.2 b Ws Coriolano, 2012 Cross-sectional Surface electromyography 15 IV B) Question First author, y Study design Outcome measure N. patients Level of evidence 2.3 a Akbar, 2015 Retrospective Incidence of aspiration pneumonia; survival 5,665,710 I 2.4 a 2.3 a Carneiro, 2014 Prospective Impact of dysphagia on QoL 62 IV 2.3 a Cilia, 2015 Retrospective Survival, confinement to wheelchair or bed, fracture, 401 II 2.4 a PEG placement 2.3 a Han, 2011 Prospective Depression related to dysphagia 127 IV 2.3 a Leow, 2010 Prospective Impact of dysphagia on QoL 32 III 2.3 b 2.3 a Lorefält, 2006 Prospective Impact of dysphagia on QoL/Severity of dysphagia 26 IV 2.4 a 2.3 a Manor, 2009 Prospective Mood changes related to dysphagia 69 II 2.3 b 2.3 a Miller, 2006 Retrospective Impact of dysphagia on QoL 137 III 2.3 a Plowman-Prine, 2009 Prospective Impact of dysphagia on QoL 36 III 2.3 a Silbergleit, 2012 Prospective Impact of dysphagia on emotional changes 14 IV 2.3 a Storch, 2013 Prospective Impact of dysphagia on QoL 100 IV 2.3 b 2.3 a Van Hooren, 2016 Prospective Impact of dysphagia on emotional changes 100 IV 2.3 b 2.4 a Auyeung, 2012 Retrospective Survival 171 II 2.4 a Fabbri, 2019 Retrospective and Survival, institutionalization 50 I Prospective Cross- sectional 2.4 a Hussain, 2018 Retrospective Survival 51 III 2.4 a Lo, 2009 Retrospective Survival 573 II 2.4 a Malmgren, 2011 Retrospective Survival 191 III 2.4 a Müller, 2001 Retrospective Survival 17 II 2.4 a Robbins, 2008 Prospective Pneumonia 255 I 2.4 a Barichella, 2013 Prospective Nutritional status 208 I 2.4 a Cereda, 2014 Retrospective Non-motor symptoms 6462 IV 2.4 a Goh, 2016 Retrospective Pneumonia and choking 194 II 2.4 a Lee, 2016 Prospective Pneumonia 66 IV 2.4 a Miller, 2009 Prospective Impact of dysphagia on PD 137 III Studies were classified according to various descriptors (e.g., study design, presence or not of a reference standard diagnostic test, sampling method, sample size, blinding, presence of clearly stated inclusion and exclusion criteria) according to the Classification of Evidence Schemes of the Clinical Practice Guideline Process Manual of the American Academy of Neurology 17. Each study was graded according to its risk of bias from Class I to Class IV (with I corresponding to the highest quality and IV to the lowest quality) EKSS Electro-Kinesiologic Swallowing Study; FEES Fiberoptic endoscopic evaluation of swallowing; HRM High-resolution manometry; PEG Percutaneous Endoscopic Gastrostomy; PEFR Peak expiratory airflow rate; VFSS Videofluoroscopic study of swallowing; WST Water swallow test 13 1342 Journal of Neurology (2022) 269:1335–1352 cordance with the gold standard VFSS (weighted kappa c. What clinical tools should be used to screen for dysphagia in concordance rate of 0.71). patients with PD? • Radboud Oral Motor Inventory for Parkinson’s disease Statements are based on core literature consisting of Class III [38, 43] and IV [36, 37, 39, 41, 42, 44–46] level studies and expert (ROMP) [41]: a questionnaire developed to assess three opinion. main domains: speech, swallowing, and saliva control. - The swallowing disturbance questionnaire (SDQ) represents the This scale represents a valid tool to identify swallowing most appropriate self-reported patient test for screening swallow- difficulties in PD, though it contains a limited number of ing disorders in PD. -The MDT-PD test, SCAS-PD and ROMP may be also considered items. valid questionnaire-based tools for dysphagia screening in PD. • Handheld Cough Testing (HCT), a novel tool for cough - Positive results at a screening test impose further investigation assessment and dysphagia screening in PD. The HCT with diagnostic tests to confirm the presence of dysphagia and to is able to identify differences in cough airflow during assess its severity. Comment: A thorough medical history evaluation is also needed to reflex and voluntary cough tasks, and screen for people complete the screening assessment of dysphagia in PD. with dysphagia in PD with high sensitivity and specific- ity (90.9% sensitivity; 80.0% specificity)[47]. Although these screening tools look promising for an Diagnosis of dysphagia in PD early diagnosis of dysphagia in patients with PD, they are not cross-culturally validated. Therefore, there is an unmet The clinical swallowing examination has a higher sensitivity need to translate, adapt, and cross-culturally validate screen- to identify swallowing abnormalities compared to screening ing measures. questionnaires [6, 24]. Thus, it is indicated in all patients with a positive screening test result. The clinical swallowing Box 1. Recommendations on the screening of dysphagia examination is performed preferably by a speech-language in PD pathologist and includes a patient/caregiver interview, evalu- ation of cognition and communication abilities, oral motor assessment, and swallowing trials. For those centres who do not have a speech-language therapist with an expertise in a. When is it indicated to screen for dysphagia in patients with the evaluation of neurogenic dysphagia, a referral pathway PD? should be put in place. The statement is based on core literature consisting of Class II [21], The Water Swallow Test (WST) is among the most com- III [23] and IV [20, 24] level studies and expert opinion. -The search for symptoms or signs that are suspicious for the pres- mon tools used during clinical swallowing examination ence of dysphagia is recommended at the first neurologic visit. If because of its rapidity and ease of use. The WST may detect symptoms or signs are detected, a screening test is always recom- dysphagia early in PD [48] and identify subjects at risk of mended. Re-evaluations are recommended at every follow-up aspiration [49]. However, it may underestimate the incidence visit, preferably at least once a year. b. When should dysphagia be suspected in patients with PD? of oropharyngeal dysphagia, since its diagnostic accuracy Statements are based on core literature consisting of Class I [5, 35], depends on the preservation of the cough reflex and phar- III [28, 33] and IV [27, 29–31, 34, 36] level studies and expert yngo-laryngeal sensitivity. Therefore, the combination of the opinion. WST with clinical tests assessing voluntary and/or reflex - In the presence of at least one of the conditions listed below: Increased eating time (meal duration), post-swallowing cough- cough function increases the positive and negative predictive ing, post-swallowing gurgling voice, drooling, choking, breathing value of the clinical swallowing assessment [50, 51]. disturbance, unintentional weight loss, difficulty to swallow pills, In addition to the above, cough testing can be useful for sensation of retention of food, pneumonia episode(s). assessing severity of dysphagia and aspiration risk [27, 52]. - In patients who answer ‘yes’ to either of the following questions: "have you experienced any difficulty in swallowing food or In particular, compared to voluntary cough testing, reflex- drink?" ive cough testing can be more sensitive in distinguishing "have you ever felt choked with food?" between patients with PD with mild (PAS 3–5) or severe Comment: The risk of dysphagia increases with the number of dysphagia (PAS 6–8), as well as between patients with pen- symptoms or signs observed, age, and disease progression. etration above (PAS 2–3) or below (PAS 4–8) the level of the vocal folds [27]. Two studies have shown that reduced tongue pressure and motility are among other possible indicators of early dysphagia in PD [42, 53]. Several instrumental investigations detect swallowing abnormalities with higher sensitivity than the clinical swal- lowing examination. Swallowing abnormalities of swallow 13 Journal of Neurology (2022) 269:1335–1352 1343 have been observed in almost all patients using different [78, 79]. In the former case, botulinum toxin injection into diagnostic techniques, even in the early stages of disease in the cricopharyngeal muscle may be beneficial [78, 79]. studies performed by different groups [23, 24, 54–59]. There However, very few centers use UES electromyography is no consensus on whether these investigations should be routinely, thus this examination cannot currently be con- carried out in all patients with PD regardless of the presence sidered as a standard test for dysphagia. of signs and symptoms associated with dysphagia. This rep- Gastroenterological investigations including esophageal resented one of the main subjects of debate during the MCC. manometry, upper gastrointestinal endoscopy, acid- and On one hand, when considering that silent aspiration may reflux-related tests, and/or radiological investigations such go undetected by clinical evaluation and it may be present as barium swallow should always be carried out in the even in the early stages of the disease, it seems reasonable presence of esophageal symptoms (e.g. dysphagia for solid to apply instrumental investigations also in subjects with foods, regurgitation, food sticking after swallowing) and/ clinically safe and functional swallowing, [5, 20, 58]. On or when oropharyngeal evaluations detect findings sug- the other hand, it seems important to consider that some gestive of structural or functional deficits in the esopha- instrumental diagnostic investigations for dysphagia are not gus, including a Zenker’s diverticulum, a neoplasm or an widely available. Thus, the prevailing view was to consider esophageal motility dysfunction [58, 80]. In recent years, mandatory such evaluation only in patients with clinical pharyngo-esophageal HRM has provided useful insights signs of dysphagia (see statement below). into the process of swallowing by enabling the detec- Several studies have evaluated the role of different inves- tion of esophageal dysmotility, with particular interest in tigation methods in the diagnosis of dysphagia in PD. VFSS upper and lower esophageal sphincters [81, 82]. Manom- and FEES should be used as a first approach, as they enable etry studies, often in combination with VFSS or FEES, detection of aspiration, penetration, and residue with similar have shown that dysphagia in PD is associated with a high high sensitivity and specificity [60]. VFSS directly reveals prevalence of esophageal motility disturbances [57, 80, 83, penetration/aspiration [61–63], also providing useful infor- 84]. However, the impact of these alterations on swallow- mation when the oral and/or esophageal phase is impaired ing and their role in influencing the clinical management [64–68]. FEES ensures an appropriate assessment of the of dysphagia remain to be clarified [58]. pharyngeal phase of swallowing and the detection of pen- Clinicians should keep in mind that findings from clini- etration/aspiration phenomena, both directly (before or after cal and instrumental investigations of swallowing may not the swallow, i.e. in case of premature spillage and residue, be entirely representative of the patient’s eating and drink- respectively) and indirectly [5, 31, 69–71]. FEES has the ing performance in real life. Variables such as distractions, advantage over VFSS of being easier to perform, even at the specific consistencies and bolus size, medications, motor patient’s bedside, and allows to test swallowing of real food fluctuations and dyskinesias may impact the testing results and to assess secretion management. Moreover, as FEES [85, 86]. Thus, it is important to observe patients in their does not require the use of radiation, it can be repeated even usual eating and drinking habits, or alternatively gather at short time intervals, thus allowing accurate follow-ups. this information in the case history or with questionnaires Oro-Pharyngo-Esophageal Scintigraphy (OPES) is a use- [87]. The therapeutic effect of the anti-parkinsonian drugs ful tool for the early detection of dysphagia [72], but its diag- on swallowing function is highly variable and can affect nostic role in PD remains to be ascertained as only a single results from swallowing investigations. Though the dopa- study has been carried out in this patient population [73]. minergic medications might improve dysphagia in some Although only preliminary evidence is available, swallowing patients, in others, they either showed no effect or nega- evaluation with high-resolution manometry (HRM) repre- tively affected the swallowing function, also depending on sents another interesting diagnostic tool, capable to show the stage of the disease [88–90]. Similarly, studies testing subtle swallowing changes in the early stages of PD even in the effect of deep brain stimulation (DBS) on swallowing the absence of swallowing changes on VFSS [57, 74]. function have yielded conflicting findings, showing ben- The Electro-Kinesiologic Swallowing Study (EKSS) eficial, absent or detrimental effects [91]. represents an additional useful diagnostic tool to explore Once the diagnosis of dysphagia is provided, stand- the pathophysiological mechanisms of oropharyngeal ardized methods to assess swallowing severity should be dysphagia and provide clues for treatment selection carried out to guide the best treatment strategy and for [56, 75–77]. For example, electromyography of the cri- prognostic assessment. Most of the studies conducted in copharyngeal muscle (i.e., the main component of the patients with PD have adopted the Penetration-Aspiration upper esophageal sphincter, UES) helps to clarify whether Scale (PAS) [92]. A few studies have used other validated failure in UES opening during the pharyngeal phase of scales such as the Dysphagia Outcome and Severity Scale swallowing is due to persistent sphincter hyperactivity or (DOSS) [93], and the Functional Oral Intake Scale (FOIS) to reduced elevation of the pharyngeal-laryngeal structures [94]. 13 1344 Journal of Neurology (2022) 269:1335–1352 Box 2. Recommendations on the diagnosis of dysphagia - The electrophysiological evaluation of oropharyngeal swallowing might provide further insights into the pathophysiological basis of dysphagia in PD and give useful clues for treatment. a. What clinical tools should be used to detect the presence of c. How should severity of dysphagia be assessed? dysphagia? In the literature, there are no validated scales specific for PD to rate Statements are based on core literature consisting of Class II [49, dysphagia severity. The following statement is, therefore, entirely 50], III [6, 95] and IV [24, 27, 42, 48, 50–53, 85, 96, 97] level based on expert opinion. studies and expert opinion. - Several scales exist to rate the severity of neurogenic dysphagia. -PD patients with a positive screening for dysphagia should The most widely used and available in multiple languages are PAS, undergo an in-depth clinical swallowing examination by a FOIS and DOSS. PAS is based on imaging data, FOIS on clinical speech-language pathologist with special training in swallow- assessment, DOSS on both clinical and instrumental parameters. ing disorders. If a speech-language therapist with an expertise in the evaluation of neurogenic dysphagia is not available on site, a referral pathway should be put in place. -The clinical swallowing examination should include: 1) a thorough Relevance of dysphagia for the quality of life examination of cranial nerves; 2) the evaluation of dry swallows; 3) of patients with PD on-command and/or reflexive cough testing; 4) the evaluation of swal- lowing of various food and liquid consistencies; and 5) the detection Dysphagia negatively affects QoL in PD. The progression of possible signs or symptoms of reduced swallowing efficiency and safety. Assessment of cognition and speech should always be carried of swallowing difficulties may cause choking, coughing or out in conjunction with the clinical swallowing examination. breathing problems during the meal, and often leads to die- -In PD patients with motor fluctuations, the swallowing examina- tary restrictions and prolonged meal duration. Altogether, tion should be performed during an ON phase. In the presence of these changes have an important psychosocial burden for cervical-cranial dyskinesias, clinical evaluation should preferably be conducted during both phases (ON or OFF) to identify the patients with PD because they may discourage or impair safest moment for the patient to eat or drink. The clinical exami- social activities and relationships [106–109]. Swallowing nation should not be performed during exacerbation periods of problems negatively influence wellbeing, self-confidence cervical-cranial dyskinesias interfering with the ability of feeding. and social integrations [108], which in turn result in frus- -Meal observation, assessing a higher number of swallowing acts and including information on feeding dependency and meal duration, can tration and isolation. Depression is indeed frequently associ- provide valuable information on swallowing function. However, this ated with reduced QoL in patients with PD with swallowing is often not feasible in the outpatient setting. In these cases, we recom- disorders [107, 110–112]. mend gathering information about typical eating/drinking patterns and Moreover, difficulty in taking oral anti-parkinsonian experiences by clinical history or questionnaires. - Patients with DBS implants should be tested in an ON medication therapy with consequent worsening of motor and non-motor phase with the stimulator turned ON. In case of a strong suspicious symptoms is another problem that frequently affects patient’s of detrimental effects of DBS on swallowing, the patient should be QoL [113]. assessed in both conditions: with the stimulator turned ON and with In the late stages of the disease, due to severe dyspha- the stimulator OFF. Assessment in both conditions should be per- formed after an adequate interval of time (generally several hours) gia, PEG placement becomes mandatory when medium/ to allow for the full array of motor and non-motor features to mani- long-term enteral feeding is needed to prevent malnutrition, fest. Different combinations of the DBS/medication states should weight loss and aspiration. This interventional procedure is be also tested in selected patients in which detrimental interactions often not well accepted by the patients and their caregivers between different DBS and medication states are suspected. b. What instrumental investigations should be used to detect the and may thus have a further negative impact on QoL [108, presence of dysphagia? 114]. Statements are based on core literature consisting of Class I [5, 98], Though not specific for PD, the Swallowing Quality of II [62], III [23, 55, 61, 74, 75] and IV [20, 31, 56–59, 63–69, 73, Life (SWAL-QOL) is the most widely used questionnaire to 76, 77, 80, 82–84, 99–105] level studies and expert opinion. - When the clinical evaluation suggests the presence of dysphagia, assess the impact of dysphagia on the QoL of patients with patients should undergo an instrumental investigation for the PD both in the literature and in the clinical practice [107, assessment of swallowing. 109, 115]. SWAL-QOL [116] assesses different aspects of Depending on local availability and on specific advantages of each the swallowing function that are experienced by the patient method, either FEES or VFSS are recommended as first-line diagnostic tools. (i.e., food selection, social functioning, fear, eating dura- - On suspicion of esophageal disorders, patients should be referred for tion, eating desire, communication) with a recall period of further investigations such as upper gastrointestinal endoscopy, barium 1 month. The questionnaire is available and validated in swallow, esophageal manometry, and/or acid- and reflux-related tests. several languages. - If impaired motility of the upper esophageal sphincter is suspected based on FEES or VFSS, pharyngo-esophageal manometry (pos- The 39-item Parkinson’s disease Questionnaire (PDQ-39) sibly with the high-resolution modality) and/or electromyographic and the short-form 8-item Parkinson’s disease Questionnaire examination of the cricopharyngeal muscle should be considered. (PDQ-8) are also used in PD to assess the psychosocial impact of dysphagia on QoL, but they are not specific for swallowing disturbances [117]. 13 Journal of Neurology (2022) 269:1335–1352 1345 A limited number of studies have investigated the rela- Survival after onset of dysphagia is poor in PD [120]. tionship between dysphagia severity and the impact on QoL Moreover, the severity of dysphagia represents the most [106, 112, 115, 118, 119]. The severity of dysphagia signifi- important prognostic factor for the occurrence of death in cantly affects QoL and the progression of the disease [12, 13, the later stages of the disease. [13, 14] Pneumonia repre- 120], though this relationship is not linear. In the study by sents the most common cause of death in PD [123, 124]. Leow et al. [106], QoL deterioration was proportional to the Aspiration of solid food, liquids, saliva or gastric contents progression of dysphagia, and the subjects who required diet represents the leading cause of pneumonia in this patient modifications presented with significantly reduced SWAL- population, [11] and it is significantly associated with sur- QOL scores. vival from diagnosis [125]. As regards the factors that may be associated to dyspha- gia severity, disease progression is associated with more Box 3. Recommendations on the relevance of dysphagia severe swallowing difficulties. [6, 41, 126] Furthermore, an for QoL in PD impaired cough response has a negative impact on dysphagia severity [52]. This agrees with the notion that integrity of pharyngeal–laryngeal sensitivity and cough efficiency influ- ence the risk of aspiration pneumonia, as reflex and vol- a. What is the impact of dysphagia on QoL of patients with PD? Statements are based on core literature consisting of Class I [12], untary cough are important mechanisms of airway protec- II [13, 107], III [106, 108, 112] and IV [109, 111, 113, 115, 117, tion during swallowing [27, 127]. The association between 118] level studies and expert opinion. pneumonia and reduced oral hygiene is well documented -Dysphagia affects the QoL of patients with PD. [128, 129]. However, we did not find any specific evidence -Dysphagia severity seems to correlate with poorer QoL. -The three main domains of QoL affected by dysphagia in PD regarding the prognostic value of reduced oral hygiene on patients are: dysphagia and/or PD outcome. Yet, it is conceivable that - loss of the social aspect of eating; poor oral hygiene may have a negative impact on dysphagic - loss of personal autonomy; patients with PD. Finally, a relationship between cognitive - difficulties in taking oral therapy. impairment, dysphagia severity and risk of aspiration pneu- b. How should dysphagia-related QoL in patients with PD be clinically assessed? monia has been shown in PD [6, 130]. Statements are based on core literature consisting of Class II [107], III [106] and IV [109, 115–117] level studies and expert opinion. Box 4.Recommendations on prognostic value of dyspha- - In the absence of validated dysphagia-related QoL scales for PD, the SWAL-QOL scale can be used for the purpose gia in PD PDQ39 is a validated scale for QoL in PD and can be used for indirectly evaluating the impact of dysphagia in PD. a. Does dysphagia influence the prognosis of the PD? - Patients’ cognitive abilities should be considered when using ques- Statements are based on core literature consisting of Class I [12, 14, tionnaires for assessing QoL. 126], II [13, 120–122, 124], and III[125, 131] and IV [113, 130, 132] level studies and expert opinion. The presence of dysphagia negatively influences the prognosis of patients with PD. Prognostic value of dysphagia and prognostics factors The presence of dysphagia, and more specifically, anterograde aspiration in the lungs is strongly correlated to a higher risk of for dysphagia in PD choking and aspiration pneumonia. Poor oral care, load of comorbidities and cognitive impairment are In this paragraph, we focus on the impact of dysphagia on possibly associated to a worse prognosis in dysphagic PD patients. comorbidities and life expectancy of subjects with PD, and b. What factors or associated conditions can influence the prog- on the factors that are associated to dysphagia severity. nosis of dysphagia in PD? Long duration and greater severity of PD has a negative impact on The incidence of aspiration pneumonia is more than the swallowing function. three-fold higher in PD subjects than age-matched controls An impaired cough response has a negative impact on dysphagia [12], and patients with dysphagia are more likely to die of severity. pneumonia than those with normal swallowing [121]. Pres- ence of comorbidities (e.g., chronic respiratory and cardio- vascular diseases, cerebrovascular disease, chronic renal Limitations of the study or liver disease) and lower level of compliance to enteral feeding in PD patients with severe dysphagia increases the Some limitations of the present work are worth mention- risk of pneumonia and choking [122]. Weight loss is more ing. The first regards the recruitment of participants, which, frequent in patients with PD with eating problems [113], and in the absence of a strictly codified methodology for selec- the risk of malnutrition appears to be dependent on dysauto- tion, was based on practical considerations and on their nomic symptoms including dysphagia [9]. voluntary acceptance of our invitation. This approach led 13 1346 Journal of Neurology (2022) 269:1335–1352 to the formation of an expert group with a prevalent repre- tion of patients in specific situations (severe dyskinesias, sentation of neurologists compared to other specialists, and DBS, etc.)? a prevalence of Italian specialists compared to specialists 7) Are the biomechanical or pathophysiological elements from other countries. Thus, it is possible that the statements of dysphagia in PD affected by different anti-parkinso- elaborated by this panel group do not reflect entirely the nian treatment strategies or different complications? point of view of the wider international medical and scien- tific communities. It is worth noting, however, that we put in place several measures to involve as many experts in the Appendix 1. Research questions based field as possible and that, once the panel was created based on PICO on voluntary adhesion, the ruling process was supported by a thorough revision of the data available from the literature. Participants/population This approach seemed the best compromise between spend- ing more time in trying to include a larger group of experts Patients with Parkinson’s disease. and the need to deliver this consensus in an acceptable time frame to provide timely guidance to clinician on a critical Intervention(s), exposure(s) issue in the management of PD patients. Another shortcom- ing of our consensus statements is that PD patients, their Questions on screening and diagnosis: presence and absence carers or representatives were not involved in the process. of oropharyngeal dysphagia, and any diagnostic test or Indeed, their contribution would have certainly been rel- screening test. evant, especially as regards the quality of life topic. Questions on prognosis: oropharyngeal dysphagia as exposures. Question on treatment: any treatment of oropharyngeal Unmet needs, areas for future research dysphagia. This consensus process identified several critical areas for the timely and correct diagnosis of dysphagia in PD that Comparator(s)/control could not be properly addressed by the panel of experts due to the lack of reliable evidence. Future studies need to focus Not applicable. on the reliability of clinical methods to screen and assess dysphagia in PD and should better define the conditions Main outcome(s) when instrumental investigations are required. Other areas worth attention are the development of validated all-inclu- The primary outcome of the systematic review is to gather sive (clinical and instrumental) scales for rating dysphagia evidence on: (1) screening approach to oropharyngeal dys- severity in PD, and of PD-specific tools to assess the impact phagia in PD; (2) definition of the diagnostic criteria of oro- of dysphagia on QoL. pharyngeal dysphagia in PD; (3) definition of the prognostic In particular, there was agreement among the consensus value of oropharyngeal dysphagia on QoL and PD outcome. participants that future research should aim to address the Such evidence will inform the statements of a Multina- following additional questions: tional Consensus Conference to provide guidance to clini- cians on the above listed topics. 1) What are the pathophysiological elements of dysphagia in PD and their neurophysiological correlates in terms of oropharyngeal sensory and motor impairment? Appendix 2. Search strategy on MEDLINE 2) What is the role played by esophageal dysmotility in PD? ("deglutition disorders"[MeSH] OR ("deglutition 3) In which way malnutrition and dehydration in PD affect disorder"[All Fields] OR "deglutition disorders"[All Fields] dysphagia severity and the risk of complications? OR "swallowing disorders"[All Fields] OR "swallowing 4) Does PEG insertion change the prognosis and QoL of disorder"[All Fields] OR ("deglutition disorders"[MeSH patients with severe dysphagia? Terms] OR ("deglutition"[All Fields] AND "disorders"[All 5) Are there useful biomarkers for the early detection Fields]) OR "deglutition disorders"[All Fields] OR of PD-related dysphagia, e.g. levels of substance P in "dysphagia"[All Fields]))). saliva?[133] AND 6) How should we choose the best timing of clinical and instrumental evaluation in relation to the motor fluctua- 13 Journal of Neurology (2022) 269:1335–1352 1347 ("Parkinson Disease"[Mesh] OR ("Parkinson's meta-analysis. Parkinsonism Relat Disord 18:311–315. https://​ disease"[All Fields] OR "Parkinson disease"[All Fields] OR doi.​org/​10.​1016/j.​parkr​eldis.​2011.​11.​006 8. Sapir S, Ramig L, Fox C (2008) Speech and swallowing disorders Parkinson[All Fields])). in Parkinson disease. Curr Opin Otolaryngol Head Neck Surg 16:205–210. https://​doi.​org/​10.​1097/​MOO.​0b013​e3282​febd3a 9. Barichella M, Cereda E, Madio C et al (2013) Nutritional risk Supplementary Information The online version contains supplemen- and gastrointestinal dysautonomia symptoms in Parkinson’s tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 00415-0​ 21-1​ 0739-8. disease outpatients hospitalised on a scheduled basis. Br J Nutr 110:347–353. https://​doi.​org/​10.​1017/​S0007​11451​20049​41 Author contribution All authors made an intellectual contribution 10. Martinez-Ramirez D, Almeida L, Giugni JC et al (2015) Rate through discussion at a consensus meeting and approved the manu- of aspiration pneumonia in hospitalized Parkinson’s disease script. Paper writing: GC, MA (these authors contributed equally to patients: a cross-sectional study. BMC Neurol 15:104. https://​ this paper). Study supervision: EA, CM, AS, CT. Intellectual content: doi.​org/​10.​1186/​s12883-​015-​0362-9 all authors. 11. Fujioka S, Fukae J, Ogura H et al (2016) Hospital-based study on emergency admission of patients with Parkinson’s disease. eNeurologicalSci 4:19–21. https://​doi.​org/​10.​1016/j.​ensci.​2016.​ Funding Open access funding provided by Università degli Studi di 04.​007 Pavia within the CRUI-CARE Agreement. The consensus conference 12. Akbar U, Dham B, He Y et al (2015) Incidence and mortal- was funded by the IRCCS Mondino Foundation, Pavia, Italy. ity trends of aspiration pneumonia in Parkinson’s disease in the United States, 1979–2010. Park Relat Disord 21:1082–1086. Declarations https://​doi.​org/​10.​1016/j.​parkr​eldis.​2015.​06.​020 13. Cilia R, Cereda E, Klersy C et al (2015) Parkinson’s disease Conflicts of interest The authors report no disclosures relevant to the beyond 20 years. J Neurol Neurosurg Psychiatry 86:849–855. manuscript. https://​doi.​org/​10.​1136/​jnnp-​2014-​308786 14. Fabbri M, Coelho M, Abreu D et al (2019) Dysphagia predicts poor outcome in late-stage Parkinson’s disease. Park Relat Dis- Open Access This article is licensed under a Creative Commons Attri- ord 64:73–81. https://​doi.​org/​10.​1016/j.​parkr​eldis.​2019.​02.​043 bution 4.0 International License, which permits use, sharing, adapta- 15. Institute of Medicine (US) (1992) Committee on Clinical Prac- tion, distribution and reproduction in any medium or format, as long tice Guidelines. Guidelines for Clinical Practice: From Devel- as you give appropriate credit to the original author(s) and the source, opment to Use. Field MJ, Lohr KN, editors. Washington (DC): provide a link to the Creative Commons licence, and indicate if changes National Academies Press (US). PMID: 25121254 were made. The images or other third party material in this article are 16. Nair R, Aggarwal R, Khanna D (2011) Methods of formal included in the article's Creative Commons licence, unless indicated consensus in classification/diagnostic criteria and guideline otherwise in a credit line to the material. If material is not included in development. Semin Arthritis Rheum 41:95–105. https://​doi.​ the article's Creative Commons licence and your intended use is not org/​10.​1016/j.​semar​thrit.​2010.​12.​001 permitted by statutory regulation or exceeds the permitted use, you will 17. Candiani G., Colombo C. et al (2009) Come organizzare need to obtain permission directly from the copyright holder. To view a una conferenza di consenso. Manuale metodologico, Roma, copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. ISS-SNLG. 18. AAN (American Academy of Neurology) (2011) Clinical Prac- tice Guideline Process Manual. MN: The American Academy of Neurology. Ed. St. Paul References 19. Moher D, Shamseer L, Clarke M et al (2016) Preferred report- ing items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Rev Esp Nutr Humana y Diet. 1. Elbaz A, Carcaillon L, Kab S, Moisan F (2016) Epidemiology of https://​doi.​org/​10.​1186/​2046-​4053-4-1 Parkinson’s disease. Rev Neurol (Paris) 172:14–26. https://​doi.​ 20. Monteiro L, Souza-Machado A, Pinho P et al (2014) Swal- org/​10.​1016/j.​neurol.​2015.​09.​012 lowing impairment and pulmonary dysfunction in Parkinson’s 2. Armstrong MJ, Okun MS (2020) Diagnosis and treatment of disease: the silent threats. J Neurol Sci 339:149–152. https://​ Parkinson disease. JAMA 323:548. https://d​ oi.o​ rg/1​ 0.1​ 001/j​ ama.​ doi.​org/​10.​1016/j.​jns.​2014.​02.​004 2019.​22360 21. Hartelius L, Svensson P (1994) Speech and swallowing symp- 3. Jankovic J (2008) Parkinson’s disease: clinical features and diag- toms associated with Parkinson’s disease and multiple sclero- nosis. J Neurol Neurosurg Psychiatry 79:368–376. https://​doi.​ sis: a survey. Folia Phoniatr Logop 46:9–17. https://​doi.​org/​10.​ org/​10.​1136/​jnnp.​2007.​131045 1159/​00026​6286 4. Postuma RB, Berg D, Stern M et al (2015) MDS clinical diagnos- 22. Takizawa C, Gemmell E, Kenworthy J, Speyer R (2016) A tic criteria for Parkinson’s disease. Mov Disord 30:1591–1601. systematic review of the prevalence of oropharyngeal dyspha- https://​doi.​org/​10.​1002/​mds.​26424 gia in stroke, Parkinson’s disease, Alzheimer’s disease, head 5. Pflug C, Bihler M, Emich K et al (2018) Critical dysphagia is injury, and pneumonia. Dysphagia 31:434–441. https://​doi.​org/​ common in Parkinson disease and occurs even in early stages: a 10.​1007/​s00455-​016-​9695-9 prospective cohort study. Dysphagia 33:41–50. https://​doi.​org/​ 23. Ali G, Wallace K, Schwartz R et al (1996) Mechanisms of 10.​1007/​s00455-​017-​9831-1 oral-pharyngeal dysphagia in patients with Parkinson’s disease. 6. Miller N, Allcock L, Hildreth AJ et al (2009) Swallowing prob- Gastroenterology 110:383–392. https://​doi.​org/​10.​1053/​gast.​ lems in Parkinson disease: frequency and clinical correlates. J 1996.​v110.​pm856​6584 Neurol Neurosurg Psychiatry 80:1047–1049. https://​doi.​org/​10.​ 24. Bird MR, Woodward MC, Gibson EM et al (1994) Asympto- 1136/​jnnp.​2008.​157701 matic swallowing disorders in elderly patients with parkinson’s 7. Kalf JG, de Swart BJM, Bloem BR, Munneke M (2012) Preva- disease: a description of findings on clinical examination and lence of oropharyngeal dysphagia in Parkinson’s disease: a 13 1348 Journal of Neurology (2022) 269:1335–1352 videofluoroscopy in sixteen patients. Age Ageing 23:251–254. saliva control in parkinson’s disease. Arch Phys Med Rehabil https://​doi.​org/​10.​1093/​ageing/​23.3.​251 92:1152–1158. https://​doi.​org/​10.​1016/j.​apmr.​2011.​02.​011 25. Wallace KL, Middleton S, Cook IJ (2000) Development and 42. Minagi Y, Ono T, Hori K et al (2018) Relationships between validation of a self-report symptom inventory to assess the dysphagia and tongue pressure during swallowing in Parkinson’s severity of oral-pharyngeal dysphagia. Gastroenterology disease patients. J Oral Rehabil 45:459–466. https://​doi.​org/​10.​ 118:678–687. https://​doi.​org/​10.​1016/​S0016-​5085(00)​70137-5 1111/​joor.​12626 26. Roy N, Stemple J, Merrill RM, Thomas L (2007) Dysphagia 43. Vogel AP, Rommel N, Sauer C et al (2017) Clinical assessment of in the elderly: preliminary evidence of prevalence, risk fac- dysphagia in neurodegeneration (CADN): development, validity tors, and socioemotional effects. Ann Otol Rhinol Laryngol and reliability of a bedside tool for dysphagia assessment. J Neu- 116:858–865. https://​doi.​org/​10.​1177/​00034​89407​11601​112 rol 264:1107–1117. https://d​ oi.​org/​10.​1007/​s00415-​017-​8499-7 27. Troche MS, Schumann B, Brandimore AE et al (2016) Reflex 44. Volonte’ MA, Porta M, Comi G (2002) Clinical assessment of cough and disease duration as predictors of swallowing dys- dysphagia in early phases of Parkinson’s disease. Neurol Sci function in Parkinson’s disease. Dysphagia 31:757–764. 23:s121–s122. https://​doi.​org/​10.​1007/​s1007​20200​099 https://​doi.​org/​10.​1007/​s00455-​016-​9734-6 45. Belo LR, Gomes NAC, Coriolano MDGWDS et al (2014) The 28. Sampaio M, Argolo N, Melo A, Nóbrega AC (2014) Wet voice relationship between limit of dysphagia and average volume per as a sign of penetration/aspiration in Parkinson’s disease: does swallow in patients with Parkinson’s disease. Dysphagia 29:419– testing material matter? Dysphagia 29:610–615. https://​doi.​ 424. https://​doi.​org/​10.​1007/​s00455-​013-​9512-7 org/​10.​1007/​s00455-​014-​9552-7 46. Buhmann C, Flügel T, Bihler M et al (2019) Is the Munich dys- 29. Buhmann C, Bihler M, Emich K et al (2019) Pill swallow- phagia Test-Parkinson’s disease (MDT-PD) a valid screening tool ing in Parkinson’s disease: a prospective study based on flex- for patients at risk for aspiration? Parkinsonism Relat Disord ible endoscopic evaluation of swallowing. Park Relat Disord 61:138–143. https://​doi.​org/​10.​1016/j.​parkr​eldis.​2018.​10.​031 62:51–56. https://​doi.​org/​10.​1016/j.​parkr​eldis.​2019.​02.​002 47. Curtis JA, Troche MS (2020) Handheld cough testing: a novel 30. Nóbrega AC, Rodrigues B, Torres AC et al (2008) Is drooling tool for cough assessment and dysphagia screening. Dysphagia secondary to a swallowing disorder in patients with Parkin- 35:993–1000. https://​doi.​org/​10.​1007/​s00455-​020-​10097-z son’s disease? Parkinsonism Relat Disord 14:243–245. https://​ 48. Kanna SV, Bhanu K (2014) A simple bedside test to assess the doi.​org/​10.​1016/j.​parkr​eldis.​2007.​08.​003 swallowing dysfunction in Parkinson’s disease. Ann Indian Acad 31. Rodrigues B, Nóbrega AC, Sampaio M et al (2011) Silent Neurol 17:62–65. https://​doi.​org/​10.​4103/​0972-​2327.​128556 saliva aspiration in Parkinson’s disease. Mov Disord 26:138– 49. Miyazaki Y, Arakawa M, Kizu J (2002) Introduction of simple 141. https://​doi.​org/​10.​1002/​mds.​23301 swallowing ability test for prevention of aspiration pneumonia in 32. van Wamelen DJ, Leta V, Johnson J et al (2020) Drooling in the elderly and investigation of factors of swallowing disorders. Parkinson’s disease: prevalence and progression from the non- Yakugaku Zasshi 122:97–105. https://​doi.​org/​10.​1248/​yakus​hi.​ motor international longitudinal study. Dysphagia 35:955–961. 122.​97 https://​doi.​org/​10.​1007/​s00455-​020-​10102-5 50. Mari F, Matei M, Ceravolo MG et al (1997) Predictive value of 33. Claus I, Muhle P, Suttrup J et al (2020) Predictors of pharyn- clinical indices in detecting aspiration in patients with neurologi- geal dysphagia in patients with Parkinson’s disease. J Parkin- cal disorders. J Neurol Neurosurg Psychiatry 63:456–460. https://​ sons Dis 10:1727–1735. https://​doi.​org/​10.​3233/​JPD-​202081 doi.​org/​10.​1136/​jnnp.​63.4.​456 34. Potulska A, Friedman A, Królicki L, Spychala A (2003) Swal- 51. Clarke CE, Gullaksen E, Macdonald S, Lowe F (2009) Referral lowing disorders in Parkinson’s disease. Parkinsonism Relat criteria for speech and language therapy assessment of dyspha- Disord 9:349–353. https://​d oi.​o rg/​1 0.​1 016/​S 1353-​8 020(03)​ gia caused by idiopathic Parkinson’s disease. Acta Neurol Scand 00045-2 97:27–35. https://​doi.​org/​10.​1111/j.​1600-​0404.​1998.​tb006​05.x 35. Lam K, Kwai Yi Lam F, Kwong Lau K et al (2007) Simple 52. Troche MS, Brandimore AE, Okun MS et al (2014) Decreased clinical tests may predict severe oropharyngeal dysphagia in cough sensitivity and aspiration in Parkinson disease. Chest Parkinson’s disease. Mov Disord 22:640–644. https://​doi.​org/​ 146:1294–1299. https://​doi.​org/​10.​1378/​chest.​14-​0066 10.​1002/​mds.​21362 53. Pitts LL, Morales S, Stierwalt JAG (2018) Lingual pressure as a 36. Loureiro F, Caline A, Sampaio M et al (2013) A Swallowing clinical indicator of swallowing function in Parkinson’s disease. Clinical Assessment Score (SCAS) to evaluate outpatients with J Speech Lang Hear Res 61:257–265. https://​doi.​org/​10.​1044/​ Parkinson’s disease. Pan Am J Aging Res 1:16–19 2017_​JSLHR-S-​17-​0259 37. Singer C, Weiner WJ, Sanchez-Ramos JR (1992) Autonomic 54. Coates C, Bakheit AMO (1997) Dysphagia in Parkinson’s dis- dysfunction in men with Parkinson’s disease. Eur Neurol ease. Eur Neurol 38:49–52. https://​doi.​org/​10.​1159/​00011​2902 32:134–140. https://​doi.​org/​10.​1159/​00011​6810 55. Ertekin C, Tarlaci S, Aydogdu I et al (2002) Electrophysiological 38. Manor Y, Giladi N, Cohen A et al (2007) Validation of a swal- evaluation of pharyngeal phase of swallowing in patients with lowing disturbance questionnaire for detecting dysphagia in Parkinson’s disease. Mov Disord 17:942–949. https://​doi.​org/​10.​ patients with Parkinson’s disease. Mov Disord 22:1917–1921. 1002/​mds.​10240 https://​doi.​org/​10.​1002/​mds.​21625 56. Alfonsi E, Versino M, Merlo IM et al (2007) Electrophysiologic 39. Simons JA, Fietzek UM, Waldmann A et al (2014) Develop- patterns of oral-pharyngeal swallowing in parkinsonian syn- ment and validation of a new screening questionnaire for dys- dromes. Neurology 68:583–589. https://​doi.​org/​10.​1212/​01.​wnl.​ phagia in early stages of Parkinson’s disease. Parkinsonism 00002​54478.​46278.​67 Relat Disord 20:992–998. https://​doi.​org/​10.​1016/j.​parkr​eldis.​ 57. Jones CA, Ciucci MR (2016) Multimodal swallowing evalua- 2014.​06.​008 tion with high-resolution manometry reveals subtle swallowing 40. Branco LL, Trentin S, Augustin Schwanke CH et al (2019) The changes in early and mid-stage Parkinson disease. J Parkinsons Swallowing Clinical Assessment Score in Parkinson’s Disease Dis 6:197–208. https://​doi.​org/​10.​3233/​JPD-​150687 (SCAS-PD) is a valid and low-cost tool for evaluation of dyspha- 58. Suttrup I, Suttrup J, Suntrup-Krueger S et al (2017) Esophageal gia: a gold-standard comparison study. J Aging Res 2019:1–7. dysfunction in different stages of Parkinson’s disease. Neurogas- https://​doi.​org/​10.​1155/​2019/​79846​35 troenterol Motil 29:1–7. https://​doi.​org/​10.​1111/​nmo.​12915 41. Kalf JG, Borm GF, De Swart BJ et al (2011) Reproducibility and 59. Ding X, Gao J, Xie C et al (2018) Prevalence and clinical cor- validity of patient-rated assessment of speech, swallowing, and relation of dysphagia in Parkinson disease: a study on Chinese 13 Journal of Neurology (2022) 269:1335–1352 1349 patients. Eur J Clin Nutr 72:82–86. https://​doi.​org/​10.​1038/​ejcn.​ 77. Kim J, Watts CR (2020) A comparison of swallow-related sub- 2017.​100 mandibular contraction amplitude and duration in people with 60. Giraldo-Cadavid LF, Leal-Leaño LR, Leon-Basantes GA et al Parkinson’s disease and healthy controls. Int J Speech Lang (2017) Accuracy of endoscopic and videofluoroscopic evalua- Pathol. https://​doi.​org/​10.​1080/​17549​507.​2020.​17665​66 tions of swallowing for oropharyngeal dysphagia. Laryngoscope 78. Alfonsi E, Merlo IM, Ponzio M et al (2010) An electrophysi- 127:2002–2010. https://​doi.​org/​10.​1002/​lary.​26419 ological approach to the diagnosis of neurogenic dysphagia: 61. Stroudley J, Walsh M (1991) Radiological assessment of dyspha- implications for botulinum toxin treatment. J Neurol Neurosurg gia in Parkinson’s disease. Br J Radiol 64:890–893. https://​doi.​ Psychiatry 81:54–60. https://​doi.​org/​10.​1136/​jnnp.​2009.​174698 org/​10.​1259/​0007-​1285-​64-​766-​890 79. Alfonsi E, Restivo DA, Cosentino G et al (2017) Botulinum 62. Tomita S, Oeda T, Umemura A et al (2018) Video-fluoroscopic toxin is effective in the management of neurogenic dysphagia. swallowing study scale for predicting aspiration pneumonia in Clinical-electrophysiological findings and tips on safety in dif- Parkinson’s disease. PLoS One 13:1–14. https://d​ oi.o​ rg/1​ 0.1​ 371/​ ferent neurological disorders. Front Pharmacol. https://​doi.​org/​ journ​al.​pone.​01976​08 10.​3389/​fphar.​2017.​00080 63. Gaeckle M, Domahs F, Kartmann A et al (2019) Predictors 80. Su A, Gandhy R, Barlow C, Triadafilopoulos G (2017) Clinical of penetration-aspiration in Parkinson’s disease patients with and manometric characteristics of patients with Parkinson’s dis- dysphagia: a retrospective analysis. Ann Otol Rhinol Laryngol ease and esophageal symptoms. Dis Esophagus 30:1–6. https://​ 128:728–735. https://​doi.​org/​10.​1177/​00034​89419​841398 doi.​org/​10.​1093/​dote/​dow038 64. Nagaya M, Kachi T, Yamada T, Igata A (1998) Videofluoro- 81. Blais P, Bennett MC, Gyawali CP (2019) Upper esophageal graphic study of swallowing in Parkinson’s disease. Dysphagia sphincter metrics on high-resolution manometry differentiate 13:95–100. https://​doi.​org/​10.​1007/​PL000​09562 etiologies of esophagogastric junction outflow obstruction. Neu- 65. Argolo N, Sampaio M, Pinho P et al (2015) Swallowing dis- rogastroenterol Motil 31:e13558. https://​doi.​org/​10.​1111/​nmo.​ orders in Parkinson’s disease: impact of lingual pumping. Int 13558 J Lang Commun Disord 50:659–664. https://​doi.​org/​10.​1111/​ 82. Taira K, Fujiwara K, Fukuhara T et al (2021) Evaluation of the 1460-​6984.​12158 pharynx and upper esophageal sphincter motility using high- 66. Argolo N, Sampaio M, Pinho P et al (2015) Videofluoro- resolution pharyngeal manometry for Parkinson’s disease. Clin scopic predictors of penetration-aspiration in Parkinson’s dis- Neurol Neurosurg 201:106447. https://​doi.​org/​10.​1016/j.​cline​ ease patients. Dysphagia 30:751–758. https://​doi.​org/​10.​1007/​ uro.​2020.​106447 s00455-​015-​9653-y 83. Bassotti G, Germani U, Pagliaricci S et al (1998) Esophageal 67. Wakasugi Y, Yamamoto T, Oda C et al (2017) Effect of an impaired manometric abnormalities in Parkinson’s disease. Dysphagia oral stage on swallowing in patients with Parkinson’s disease. J Oral 13:28–31. https://​doi.​org/​10.​1007/​PL000​09546 Rehabil 44:756–762. https://​doi.​org/​10.​1111/​joor.​12536 84. Castell JA, Johnston BT, Colcher A et al (2001) Manometric 68. Schiffer BL, Kendall K (2019) Changes in timing of swallow abnormalities of the oesophagus in patients with Parkinson’s events in Parkinson’s disease. Ann Otol Rhinol Laryngol 128:22– disease. Neurogastroenterol Motil 13:361–364. https://​doi.​org/​ 27. https://​doi.​org/​10.​1177/​00034​89418​806918 10.​1046/j.​1365-​2982.​2001.​00275.x 69. Hammer MJ, Murphy CA, Abrams TM (2013) Airway soma- 85. Monte FS, da Silva-Júnior FP, Braga-Neto P et al (2005) Swal- tosensory deficits and dysphagia in Parkinson’s disease. J Par- lowing abnormalities and dyskinesia in Parkinson’s disease. Mov kinsons Dis 3:39–44. https://​doi.​org/​10.​3233/​JPD-​120161 Disord 20:457–462. https://​doi.​org/​10.​1002/​mds.​20342 70. Suntrup S, Teismann I, Wollbrink A et al (2013) Magnetoenceph- 86. Broadfoot CK, Abur D, Hoffmeister JD et al (2019) Research- alographic evidence for the modulation of cortical swallowing based updates in swallowing and communication dysfunction in processing by transcranial direct current stimulation. Neuroimage parkinson disease: implications for evaluation and management. 83:346–354. https://​doi.​org/​10.​1016/j.​neuro​image.​2013.​06.​055 Perspect ASHA Spec Interes Groups 4:825–841. https://​doi.​org/​ 71. Warnecke T, Suttrup I, Schröder JB et al (2016) Levodopa 10.​1044/​2019_​pers-​sig3-​2019-​0001 responsiveness of dysphagia in advanced Parkinson’s disease and 87. Martin-Harris B, Jones B (2008) The videofluorographic swal- reliability testing of the FEES-Levodopa-test. Park Relat Disord lowing study. Phys Med Rehabil Clin N Am 19:769–785. https://​ 28:100–106. https://​doi.​org/​10.​1016/j.​parkr​eldis.​2016.​04.​034 doi.​org/​10.​1016/j.​pmr.​2008.​06.​004 72. Grosso M, Duce V, Fattori B et al (2015) The value of oro-phar- 88. Coelho M, Marti MJ, Tolosa E et al (2010) Late-stage Par- yngo-esophageal scintigraphy in the management of patients kinson’s disease: the Barcelona and Lisbon cohort. J Neurol with aspiration into the tracheo-bronchial tree and consequent 257:1524–1532. https://​doi.​org/​10.​1007/​s00415-​010-​5566-8 dysphagia. North Am J Med Sci 7:533–536. https://​doi.​org/​10.​ 89. Lim A, Leow LP, Huckabee ML et al (2008) A pilot study of 4103/​1947-​2714.​170628 respiration and swallowing integration in Parkinson’s disease: 73. Mamolar Andrés S, Santamarina Rabanal ML, Granda Membiela “On” and “Off” levodopa. Dysphagia 23:76–81. https://​doi.​org/​ CM et al (2017) Swallowing disorders in Parkinson’s disease. 10.​1007/​s00455-​007-​9100-9 Acta Otorrinolaringol (English Ed) 68:15–22. https://​doi.​org/​10.​ 90. Michou E, Hamdy S, Harris M et al (2014) Characterization of 1016/j.​otoeng.​2017.​01.​003 corticobulbar pharyngeal neurophysiology in dysphagic patients 74. Jones CA, Hoffman MR, Lin L et al (2018) Identification of with Parkinson’s disease. Clin Gastroenterol Hepatol 12:2037- swallowing disorders in early and mid-stage Parkinson’s disease 2045.e4. https://​doi.​org/​10.​1016/j.​cgh.​2014.​03.​020 using pattern recognition of pharyngeal high-resolution manom- 91. Suttrup I, Warnecke T (2016) Dysphagia in Parkinson’s disease. etry data. Neurogastroenterol Motil 30:e13236. https://​doi.​org/​ Dysphagia 31:24–32. https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 00455-0​ 15-9​ 671-9 10.​1111/​nmo.​13236 92. Rosenbek JC, Robbins JA, Roecker EB et al (1996) A penetra- 75. Ertekin C, Pehlivan M, Aydoǧdu I et al (1995) An electro- tion-aspiration scale. Dysphagia 11:93–98. https://​doi.​org/​10.​ physiological investigation of deglutition in man. Muscle Nerve 1007/​BF004​17897 18:1177–1186. https://​doi.​org/​10.​1002/​mus.​88018​1014 93. O’Neil KH, Purdy M, Falk J, Gallo L (1999) The dysphagia 76. Cosentino G, Tassorelli C, Prunetti P et al (2020) Reproduc- outcome and severity scale. Dysphagia 14:139–145. https://​doi.​ ibility and reaction time of swallowing as markers of dysphagia org/​10.​1007/​PL000​09595 in parkinsonian syndromes. Clin Neurophysiol 131:2200–2208. 94. Crary MA, Carnaby Mann GD, Groher ME (2005) Initial psycho- https://​doi.​org/​10.​1016/j.​clinph.​2020.​06.​018 metric assessment of a functional oral intake scale for dysphagia 13 1350 Journal of Neurology (2022) 269:1335–1352 in stroke patients. Arch Phys Med Rehabil 86:1516–1520. https://​ disease. Park Relat Disord 17:437–439. https://d​ oi.o​ rg/1​ 0.1​ 016/j.​ doi.​org/​10.​1016/j.​apmr.​2004.​11.​049 parkr​eldis.​2011.​03.​006 95. Pitts T, Troche M, Mann G et al (2010) Using voluntary cough 112. Miller N, Noble E, Jones D, Burn D (2006) Hard to swallow: dys- to detect penetration and aspiration during oropharyngeal swal- phagia in Parkinson’s disease. Age Ageing 35:614–618. https://​ lowing in patients with Parkinson disease. Chest 138:1426–1431. doi.​org/​10.​1093/​ageing/​afl105 https://​doi.​org/​10.​1378/​chest.​10-​0342 113. Lorefält B, Granérus AK, Unosson M (2006) Avoidance of solid 96. Silverman EP, Carnaby G, Singletary F et al (2016) Measure- food in weight losing older patients with Parkinson’s disease. J ment of voluntary cough production and airway protection in Clin Nurs. https://​doi.​org/​10.​1111/j.​1365-​2702.​2005.​01454.x parkinson disease. Arch Phys Med Rehabil 97:413–420. https://​ 114. White H, King L (2014) Enteral feeding pumps: efficacy, safety, doi.​org/​10.​1016/j.​apmr.​2015.​10.​098 and patient acceptability. Med Devices (Auckl)7:291-298. https://​ 97. Hegland KW, Okun MS, Troche MS (2014) Sequential voluntary doi.​org/​10.​2147/​MDER.​S50050. PMID: 25170284; PMCID: cough and aspiration or aspiration risk in Parkinson’s disease. PMC4146327 Lung 192:601–608. https://​doi.​org/​10.​1007/​s00408-​014-​9584-7 115. Carneiro D, Coriolano Md Ws, Belo LR et al (2014) Quality 98. Moreau C, Devos D, Baille G et al (2016) Are upper-body axial of life related to swallowing in Parkinson’s disease. Dysphagia symptoms a feature of early Parkinson’s disease? PLoS One 29:578–582. https://​doi.​org/​10.​1007/​s00455-​014-​9548-3 11:1–13. https://​doi.​org/​10.​1371/​journ​al.​pone.​01629​04 116. McHorney CA, Bricker DE, Kramer AE et al (2002) The SWAL- 99. Fuh JL, Lee RC, Wang SJ et al (1997) Swallowing difficulty in QOL outcomes tool for oropharyngeal dysphagia in adults: Parkinson’s disease. Clin Neurol Neurosurg 99:106–112. https://​ I conceptual foundation and item development. Dysphagia doi.​org/​10.​1016/​S0303-​8467(97)​00606-9 15:115–121 100. Johnston BT, Castell JA, Stumacher S et al (1997) Comparison 117. Storch A, Schneider CB, Wolz M et al (2013) Nonmotor fluctua- of swallowing function in Parkinson’s disease and progressive tions in Parkinson disease: severity and correlation with motor supranuclear palsy. Mov Disord 12:322–327. https://​doi.​org/​10.​ complications. Neurology 80:800–809. https://​doi.​org/​10.​1212/​ 1002/​mds.​87012​0310 WNL.​0b013​e3182​85c0ed 101. Ws Coriolano Md, R Belo L, Carneiro D, G Asano A, et al 118. Silbergleit AK, Lewitt P, Junn F et al (2012) Comparison of (2012) Swallowing in patients with Parkinson's disease: a surface dysphagia before and after deep brain stimulation in Parkinson’s electromyography study. Dysphagia 27(4):550-555. https://​doi.​ disease. Mov Disord 27:1763–1768. https://d​ oi.o​ rg/1​ 0.1​ 002/m ​ ds.​ org/​10.​1007/​s00455-​012-​9406-0 25259 102. Lee KD, Koo JH, Song SH et al (2015) Central cholinergic 119. Wang C-M, Tsai T-T, Wang S-H, Wu Y-R (2020) Does the M.D. dysfunction could be associated with oropharyngeal dysphagia Anderson Dysphagia Inventory correlate with dysphagia-limit in early Parkinson’s disease. J Neural Transm 122:1553–1561. and the Unified Parkinson Disease Rating Scale in early-stage https://​doi.​org/​10.​1007/​s00702-​015-​1427-z Parkinson’s disease? J Formos Med Assoc 119:247–253. https://​ 103. Ellerston JK, Heller AC, Houtz DR, Kendall KA (2016) Quan- doi.​org/​10.​1016/j.​jfma.​2019.​05.​005 titative measures of swallowing deficits in patients with Parkin- 120. Müller J, Wenning GK, Verny M et al (2001) Progression of son’s disease. Ann Otol Rhinol Laryngol 125:385–392. https://​ dysarthria and dysphagia in postmortem-confirmed parkinsonian doi.​org/​10.​1177/​00034​89415​617774 disorders. Arch Neurol 58:259–264. https://​doi.​org/​10.​1001/​ 104. Wang C-M, Shieh W-Y, Weng Y-H et al (2017) Non-invasive archn​eur.​58.2.​259 assessment determine the swallowing and respiration dysfunc- 121. Lo RY, Tanner CM, Albers KB et al (2009) Clinical features tion in early Parkinson’s disease. Parkinsonism Relat Disord in early Parkinson disease and survival. Arch Neurol 66:1353– 42:22–27. https://​doi.​org/​10.​1016/j.​parkr​eldis.​2017.​05.​024 1358. https://​doi.​org/​10.​1001/​archn​eurol.​2009.​221 105. Lee WH, Lim MH, Nam HS et al (2019) Differential kinematic 122. Goh KH, Acharyya S, Ng SYE et al (2016) Risk and prognostic features of the hyoid bone during swallowing in patients with factors for pneumonia and choking amongst Parkinson’s disease Parkinson’s disease. J Electromyogr Kinesiol 47:57–64. https://​ patients with dysphagia. Park Relat Disord 29:30–34. https://d​ oi.​ doi.​org/​10.​1016/j.​jelek​in.​2019.​05.​011 org/​10.​1016/j.​parkr​eldis.​2016.​05.​034 106. Leow LP, Huckabee M-L, Anderson T, Beckert L (2010) The 123. Morgante L, Salemi G, Meneghini F et al (2000) Parkinson dis- Impact of dysphagia on quality of life in ageing and Parkinson’s ease survival: a population-based study. Arch Neurol 57:507– disease as measured by the Swallowing Quality of Life (SWAL- 512. https://​doi.​org/​10.​1001/​archn​eur.​57.4.​507 QOL) questionnaire. Dysphagia 25:216–220. https://​doi.​org/​10.​ 124. Auyeung M, Tsoi TH, Mok V et al (2012) Ten year survival and 1007/​s00455-​009-​9245-9 outcomes in a prospective cohort of new onset Chinese Parkin- 107. Manor Y, Balas M, Giladi N et al (2009) Anxiety, depression and son’s disease patients. J Neurol Neurosurg Psychiatry 83:607– swallowing disorders in patients with Parkinson’s disease. Par- 611. https://​doi.​org/​10.​1136/​jnnp-​2011-​301590 kinsonism Relat Disord 15:453–456. https://​doi.​org/​10.​1016/j.​ 125. Hussain J, Allgar V, Oliver D (2018) Palliative care triggers in parkr​eldis.​2008.​11.​005 progressive neurodegenerative conditions: an evaluation using 108. Plowman-Prine EK, Sapienza CM, Okun MS et al (2009) The a multi-centre retrospective case record review and principal relationship between quality of life and swallowing in Parkin- component analysis. Palliat Med 32:716–725. https://​doi.​org/​ son’s disease. Mov Disord 24:1352–1358. https://​doi.​org/​10.​ 10.​1177/​02692​16318​755884 1002/​mds.​22617 126. Robbins J, Gensler G, Hind J et al (2008) Comparison of 2 inter- 109. Van Hooren MRA, Baijens LWJ, Vos R et al (2016) Voice- and ventions for liquid aspiration on pneumonia incidence: a rand- swallow-related quality of life in idiopathic Parkinson’s disease. omized trial. Ann Intern Med 148:509–518. https://​doi.​org/​10.​ Laryngoscope 126:408–414. https://​doi.​org/​10.​1002/​lary.​25481 7326/​0003-​4819-​148-7-​20080​4010-​00007 110. Barone P, Antonini A, Colosimo C et al (2009) The PRIAMO 127. Ebihara S, Saito H, Kanda A et al (2003) Impaired efficacy of study: a multicenter assessment of nonmotor symptoms and their cough in patients with Parkinson disease. Chest 124:1009–1015. impact on quality of life in Parkinson’s disease. Mov Disord https://​doi.​org/​10.​1378/​chest.​124.3.​1009 24:1641–1649. https://​doi.​org/​10.​1002/​mds.​22643 128. El-Solh AA (2011) Association between pneumonia and oral care 111. Han M, Ohnishi H, Nonaka M et al (2011) Relationship between in nursing home residents. Lung 2011189(3):173-180. https://​ dysphagia and depressive states in patients with Parkinson’s doi.​org/​10.​1007/​s00408-​011-​9297-0. Epub 2011 Apr 30. PMID: 21533635 13 Journal of Neurology (2022) 269:1335–1352 1351 129. El-Solh AA, Pietrantoni C, Bhat A et al (2004) Colonization of 132. Cereda E, Cilia R, Klersy C et al (2014) Swallowing disturbances dental plaques: a reservoir of respiratory pathogens for hospital- in Parkinson’s disease: a multivariate analysis of contributing acquired pneumonia in institutionalized elders. Chest. https://d​ oi.​ factors. Park Relat Disord 20:1382–1387. https://​doi.​org/​10.​ org/​10.​1378/​chest.​126.5.​1575 1016/j.​parkr​eldis.​2014.​09.​031 130. Lee JH, Lee KW, Kim SB et al (2016) The functional dyspha- 133. Schröder JB, Marian T, Claus I et al (2019) Substance P saliva gia scale is a useful tool for predicting aspiration pneumonia in reduction predicts pharyngeal dysphagia in Parkinson’s disease. patients with Parkinson disease. Ann Rehabil Med 40:440–446. Front Neurol 10:1–5. https://​doi.​org/​10.​3389/​fneur.​2019.​00386 https://​doi.​org/​10.​5535/​arm.​2016.​40.3.​440 131. Malmgren A, Hede GW, Karlström B et al (2011) Indications for percutaneous endoscopic gastrostomy and survival in old adults. Food Nutr Res 55:1–6. https://​doi.​org/​10.​3402/​fnr.​v55i0.​6037 Authors and Affiliations Giuseppe Cosentino1,2 · Micol Avenali1,3 · Antonio Schindler4 · Nicole Pizzorni4 · Cristina Montomoli5 · Giovanni Abbruzzese6 · Angelo Antonini7 · Filippo Barbiera8 · Marco Benazzo9 · Eduardo Elias Benarroch10 · Giulia Bertino9 · Emanuele Cereda11 · Pere Clavè12,13 · Pietro Cortelli14,15 · Roberto Eleopra16 · Chiara Ferrari4 · Shaheen Hamdy17 · Maggie‑Lee Huckabee18 · Leonardo Lopiano19 · Rosario Marchese Ragona20 · Stefano Masiero21 · Emilia Michou22 · Antonio Occhini9 · Claudio Pacchetti23 · Ronald F. Pfeiffer24 · Domenico A. Restivo25 · Mariangela Rondanelli26 · Giovanni Ruoppolo27 · Giorgio Sandrini1 · Anthony H. V. Schapira28 · Fabrizio Stocchi29 · Eduardo Tolosa30 · Francesca Valentino23 · Mauro Zamboni31 · Roberta Zangaglia23 · Mario Zappia32 · Cristina Tassorelli1,3 · Enrico Alfonsi2 1 14 Department of Brain and Behavioral Sciences, University IRCCS Istituto di Scienze Neurologiche, Bologna, Italy of Pavia, Via Mondino 2, 27100 Pavia, Italy 15 DIBINEM, University of Bologna, Bologna, Italy 2 Clinical Neurophysiology Unit, IRCCS Mondino Foundation, 16 Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Pavia, Italy Italy 3 Neurorehabilitation Unit, IRCCS Mondino Foundation, 17 Division of Diabetes, Endocrinology and Gastroenterology, Pavia, Italy University of Manchester, Salford Royal Hospital, Salford, 4 Department of Biomedical and Clinical Sciences “Luigi UK Sacco”, University of Milan, Milan, Italy 18 Department of Communication Disorders, Rose Centre 5 Department of Public Health, Experimental and Forensic for Stroke Recovery and Research, University of Canterbury, Medicine, Unit of Biostatistics and Clinical Epidemiology, Christchurch, New Zealand University of Pavia, Pavia, Italy 19 Department of Neuroscience “Rita Levi Montalcini”, 6 Department of Neuroscience, Rehabilitation, Ophthalmology, University of Torino, Turin, Italy Genetics and Maternal Child Health, University 20 ENT Department, University of Padova, Padua, Italy of Genoa-IRCCS Ospedale Policlinico San Martino, Genova, 21 Italy Rehabilitation Unit, Department of Neuroscience, University 7 of Padova, Padua, Italy Parkinson and Movement Disorders Unit, Department 22 of Neuroscience, University of Padua, Padua, Italy Department of Speech and Language Therapy, School 8 of Health Rehabilitation Sciences, University of Patras, Azienda Sanitaria Provinciale Agrigento—UO Complessa Patras, Greece Radiologia Distretto Ag 2 Sciacca-Ribera. Presidio 23 Ospedaliero di Sciacca (AG), Sciacca, Agrigento, Italy Parkinson’s Disease and Movement Disorders Unit, IRCCS 9 Mondino Foundation, Pavia, Italy Department of Otolaryngology Head Neck Surgery, 24 University of Pavia, IRCCS Policlinico San Matteo Department of Neurology, Oregon Health and Science Foundation, Pavia, Italy University, Portland, OR, USA 10 25 Department of Neurology, Mayo Clinic, Rochester, MN, Department of Neurology, Garibaldi Hospital, Catania, Italy USA 26 Department of Public Health, Experimental and Forensic 11 Clinical Nutrition and Dietetics Unit, Fondazione IRCCS Medicine, Unit of Human and Clinical Nutrition, University Policlinico San Matteo, Pavia, Italy of Pavia, IRCCS Mondino Foundation, Pavia, Italy 12 27 Gastrointestinal Physiology Laboratory, Hospital de Mataró, Department of Sense Organs, Sapienza University of Rome, Universitat Autónoma de Barcelona, Mataró, Spain Rome, Italy 13 28 Centro de Investigación Biomédica en Red de Enfermedades Department of Clinical and Movement Neurosciences, UCL, Hepáticas y Digestivas (Ciberehd), Instituto de Salud Carlos Queen Square Institute of Neurology, London, UK III, Barcelona, Spain 13 1352 Journal of Neurology (2022) 269:1335–1352 29 University and Institute for Research and Medical Care (CIBERNED:CB06/05/0018‑ISCIII), University IRCCS San Raffaele, Rome, Italy of Barcelona, Barcelona, Spain 30 31 Parkinson Disease and Movement Disorders Unit, Department of Medicine, Division of Geriatrics, Healthy Neurology Service, Hospital Clínic de Barcelona, Aging Center, University of Verona, Verona, Italy Institut d’Investigacions Biomèdiques August Pi i 32 Department GF Ingrassia, University of Catania, Catania, Sunyer (IDIBAPS), Centro de Investigación Biomédica Italy en Red Sobre Enfermedades Neurodegenerativas 13