Dysphagia in Parkinson´s disease. A 5-year follow-up study

Vol.:(0123456789)
Neu ological Sciences
h ps://doi.o g/10.1007/s10072-025-08027-8
ORIGINAL ARTICLE
Dysphagia inPa kinson´s disease. A5‑yea ollow‑up s udy
DiegoSan os‑Ga cía1,2,3,4 · Te esadeDeusFon icoba5· Sil iaJesús6,7· Ma inaCosgaya8· JuanGa cíaCalden ey9·
Nu iaCaballol10· InesLega da11· Jo geHe nándezVa a7,12· I iaCabo13· LydiaLópezManzana es14·
IsabelGonzálezA ambu u7,15· Ma iaA. Á ilaRi e a16· Víc o GómezMayo domo17· Víc o Noguei a18·
JulioDo o Ga cía‑So o19· Ca menBo ué20· Be aSolanoVila21· Ma íaÁl a ezSauco22· LydiaVela23·
SoniaEscalan e24· Es he Cubo25· ZebenzuiMendoza26· IsabelPa eés27· Pila SánchezAlonso28·
Ma iaG.AlonsoLosada29· Nu iaLópezA iz egui30· I zia Gas ón31· JaimeKulise sky7,32· ManuelSeijo13·
Ca idadVale o33· RubenAlonsoRedondo18· Ca losO dás34· ManuelMenéndez‑González35· Da ianMcA ee36·
PabloMa inez‑Ma in7· PabloMi 6,7,37· COPPADIS S udy G oup
Recei ed: 17 Augus 2024 / Accep ed: 25 Janua y 2025
© The Au ho (s) 2025
Abs ac
Backg ound and objec i e Dysphagia a ime o diagnosis sugges s a ypical pa kinsonism ins ead Pa kinson´s disease (PD).
Ou aim was o analyze he equency o dysphagia in pa ien s wi h ea ly PD compa ing wi h a con ol g oup and o iden i y
ela ed ac o s.
Pa ien s and me hods Pa ien s wi h ea ly PD (≤ 2yea s om symp oms onse ) who we e ec ui ed om Janua y/2016 o
No embe /2017 (baseline isi ; V0) and e alua ed annually o 5yea s om he Spanish coho COPPADIS we e included
in his p ospec i e s udy. Con ols we e assessed a baseline and a 2-, 4-, and 5-yea ollow-up. Dysphagia was de ined as
a sco e ≥ 1 in he i em 20 o he Non-Mo o Symp oms Scale (NMSS).
Resul s Dysphagia was mo e equen a baseline in PD pa ien s (19.6% [36/184]; 62.3 ± 8.3yea s old; 56.8% males) han in
con ols (5.3% [11/206]; 60.9 ± 8.3yea s old; 50% males) (p < 0.0001) and in all isi s as well (p < 0.0001). A wo se quali y
o sleep (Pa kinson´s Disease Sleep Scale; OR = 0.974; p = 0.005), a g ea e impulse-con ol beha io (ICB) (Ques ionnai e
o Impulsi e-Compulsi e Diso de s in Pa kinson's Disease-Ra ing Scale; OR = 1.066; p = 0.014), and non-mo o symp oms
bu den (Non-Mo o Symp oms Scale; OR = 1.016; p = 0.021) we e independen ac o s associa ed wi h dysphagia a baseline.
In hose subjec s wi h dysphagia, no di e ences we e obse ed be ween pa ien s and con ols in he mean NMSS-i em 20
o e ime, and i didn´ change h oughou he ollow-up.
Conclusion Dysphagia was equen in ea ly PD pa ien s compa ed o con ols. Howe e , i was mino and did no p og ess
o e ime. Sleep, ICB, and non-mo o symp oms bu den we e ela ed o dysphagia.
Keywo ds Coho · Ea ly· Dysphagia· Impulse con ol diso de · Non-mo o symp oms· Pa kinson's disease
In oduc ion
Dysphagia is highly p e alen in Pa kinson disease (PD) bu
is no ypically iden i ied no ea ed un il la e in he disease
p ocess. In ac , se e e dysphagia wi hin he i s 5yea s is
a known ed lag o diagnosis o PD [1]. Dysphagia in PD
a ies signi ican ly when i is based on subjec i e han on
objec i e measu emen s [2]. A ecen me a-analysis ound
a pooled p e alence a e o dysphagia in PD o 36.9% (95%
CI: 30.7–43.6%), whe eas ins umen al examina ion showed
a highe p e alence (57.3%, 95% CI: 44.3–69.1%) [3]. Dys-
phagia is associa ed wi h olde age, male sex, lowe body
mass index, longe disease du a ion, highe Hoehn and Yah
(H&Y) s age and le odopa equi alen daily dose (LEDD),
PIGD (Pos u al Ins abili y Gai Di icul ies) sub ype, se e e
mo o symp oms, cogni i e impai men , d ooling, highe
le els o dep ession, and lowe quali y o li e (QoL) [3–5].
Fu he mo e, dysphagia educes quali y o li e (QoL), com-
plica es medica ion in ake, p edic s a wo se ou come in la e-
s age PD [6] and plays a ole in weigh loss and ecu en
o ai way in ec ions [7]. Howe e , dysphagia can be p esen
a ea ly phases o PD as well and o en is unde es ima ed.
Ex ended au ho in o ma ion a ailable on he las page o he a icle
Neu ological Sciences
In ac , dysphagia has no been well s udied in ea ly PD [8].
In a ecen me a-analysis abou dysphagia p e alence and
associa ed ac o s in PD in ol ing 58 s udies [3], he mean
disease du a ion was 7.4 ( ange om 0.5 o 17.8), and only 2
s udies had a mean disease du a ion o 2yea s o less [9, 10].
The p e alence o dysphagia in a coho o ea ly d ug-naï e
PD pa ien s om he PPMI da abase was 12.3% (49/398)
wi h a mean disease du a ion o 0.5 ± 0.5yea s [9]. Dys-
phagia occu ed in 20.1% (349/1738) o he pa ien s om
he Uni ed Kingdom T acking Pa kinson's S udy wi h ecen
onse symp oms (mean disease du a ion 1.3 ± 0.9yea s)
[10]. Howe e , bo h s udies we e c oss-sec ional and wi h-
ou a con ol g oup. Thus, mo e in o ma ion abou he ole
o dysphagia in ea ly PD is needed.
The aim o he p esen s udy was o analyze he equency
o dysphagia in pa ien s wi h ea ly PD, and i o compa e
wi h a con ol g oup. Speci ically, we iden i ied he p e -
alence o dysphagia, he bu den o he symp om, and i s
change o e a 5-yea span in pa ien s and con ols. Mo eo-
e , we iden i ied ac o s ela ed o dysphagia and analyzed
he co ela ion o dysphagia wi h d ooling, hypomimia, and
speech p oblems.
Ma e ial andme hods
Pa ien s wi h ea ly PD (≤ 2yea s om symp oms onse )
who we e ec ui ed om Janua y/2016 o No embe /2017
(baseline isi ; V0) and e alua ed annually o 5yea s
om he Spanish coho COPPADIS [11] we e included in
his longi udinal p ospec i e s udy. This is a mul i-cen e ,
obse a ional, p ospec i e, 5-yea ollow-up s udy designed
o analyze disease p og ession in a Spanish popula ion o
PD pa ien s. Me hodology abou COPPADIS-2015 s udy
can be consul ed in h ps:// bmcne u ol. biome dcen al. com/
a ic les/h ps:// doi. o g/ 10. 1186/ s12883- 016- 0548-9 [12].
All pa ien s included a baseline we e diagnosed acco d-
ing o UK PD B ain Bank c i e ia [13]. Exclusion c i e ia
we e: a ypical pa kinsonism; Mini Men al S a e Examina-
ion [MMSE] < 26; age < 18 o > 75yea s; inabili y o ead
o unde s and he ques ionnai es; o ecei e any ad anced
he apy (con inuous in usion o le odopa o apomo phine;
and/o wi h deep b ain s imula ion a baseline); and he p es-
ence o como bidi ies, sequelae, o any o he diso de ha
could in e e e wi h he assessmen . Con ol subjec s om
he COPPADIS coho assessed a baseline and a 2-, 4-, and
5-yea ollow-up we e also included.
A each isi , o ha e dysphagia was de ined as a non-
ze o sco e ( om 1 o 12) in he i em 20 (“Does he pa ien
ha ing di icul y swallowing?”) o he Non-Mo o Symp-
oms Scale (NMSS) [14]. A sco e ≥ 6 was conside ed as
ele an dysphagia bu den ( om o en x se e e o equen
x mode a e [6 poin s] o always x se e e [12 poin s]). The
same me hod was used o de ine d ooling, acco ding o he
NMSS-i em 19 (Does he pa ien d ibble sali a du ing he
day?). Rega ding speech p oblems, PD pa ien s we e clas-
si ied in 5 g oups acco ding o he i em-18 o he Uni ied
Pa kinson´s Disease Ra ing Scale – pa III (UPDRS-III):
0 = No mal; 1 = Sligh loss o exp ession, dic ion and/o
olume; 2 = Mono one, slu ed bu unde s andable; mod-
e a ely impai ed; 3 = Ma ked impai men , di icul o
unde s and; 4 = Unin elligible [15]. The UPDRS-III was
also used o de ine acial exp ession (i em-19): 0 = No -
mal; 1 = Minimal hypomimia, could be no mal "Poke
Face"; 2 = Sligh bu de ini ely abno mal diminu ion o
acial exp ession; 3 = Mode a e hypomimia; lips pa ed
some o he ime; 4 = Masked o ixed acies wi h se e e
o comple e loss o acial exp ession; lips pa ed 1/4 inch
o mo e.
In o ma ion on sociodemog aphic aspec s, ac o s ela ed
o PD, and ea men was collec ed. The H&Y, UPDRS-III
and pa IV (UPDRS-IV), NMSS and ADLS (Schwab &
England Ac i i ies o Daily Li ing Scale) we e applied
annually in PD pa ien s. O he da a abou mo o s a us,
non-mo o symp oms (NMS) and QoL we e assessed a V0,
V2, V4, and V5 using di e en alida ed scales: F eezing
o Gai Ques ionnai e (FOGQ); Beck Dep ession In en o y-
II (BDI-II); Pa kinson's Disease Sleep Scale (PDSS); Neu-
opsychia ic In en o y (NPI); Ques ionnai e o Impulsi e-
Compulsi e Diso de s in Pa kinson's Disease-Ra ing Scale
(QUIP-RS); Visual Analog Scale-Pain (VAS-Pain); Visual
Analog Fa igue Scale (VAFS]); he 39-i em Pa kinson's dis-
ease Ques ionnai e (PDQ-39); he EUROHIS-QOL 8-i em
index (EUROHIS-QOL8) [12]. In pa ien s wi h mo o luc-
ua ions, he mo o assessmen was made du ing he OFF
s a e (wi hou medica ion in he las 12h) and du ing he ON
s a e. The assessmen was only pe o med wi hou medica-
ion in pa ien s wi hou mo o luc ua ions. Mo o pheno-
ype, mo o luc ua ions, FOG, alls, and majo dep ession
we e de ined in he COPPADIS p o ocol acco ding o he
li e a u e and scales used [12]. Mo eo e , impulse con ol
beha io s (ICBs) we e conside ed, bo h impulse con ol
diso de s (ICDs) (pa hological gambling, compulsi e shop-
ping, hype sexuali y, and compulsi e ea ing beha io ) and
compulsi e beha io s (CBs) (punding, hobbyism, and dys-
egula ion dopamine gic synd ome). We applied p e iously
published cu o poin s o he QUIP-RS: gambling ≥ 6, buy-
ing ≥ 8, sex ≥ 8, ea ing ≥ 7, hobbyism-punding ≥ 7 [16]. Fo
dopamine gic dys egula ion synd ome (DDS), we accoun ed
o he esea che ´s c i e ia, since an es ablished cu o does
no exis [17]. Pa ien s su e ing om a leas one ICD and/
o CB we e conside ed as pa ien s p esen ing ICB. The same
e alua ion as o he pa ien s, excep o he mo o assess-
men , was pe o med in con ol subjec s a he same isi s
(V0; V2; V4; V5). LEED was calcula ed based on he li -
e a u e [18].
Neu ological Sciences
S a is ical analysis
Da a we e p ocessed using SPSS 20.0 o Windows. Di e -
en a iables we e exp essed as quan i a i e and/o quali a i e
a iables. Dis ibu ion o a iables was e i ied by one-sample
Kolmogo o –Smi no es . All subjec s om he COPPADIS
coho who me de ined c i e ia we e selec ed o compa i-
sons a he baseline isi . Howe e , i was manda o y ha all
selec ed pa icipan s mus ha e been e alua ed a all isi s o
compa e he changes in he ollow-up: V0; V1 (a 1-yea );
V2 (a 2-yea ); V3 (a 2-yea ); V4 (a 4-yea ); V5 (a 5-yea ).
Fo compa isons be ween subjec s (pa ien s s con ols) and
om a di e en g oup (wi h s wi hou dysphagia) a each
isi (V0; V2; V4; V5), he S uden 's - es , Mann–Whi ney
U, Chi squa e, o Fishe es we e applied. Bina y eg ession
models we e used o de e mine independen ac o s associ-
a ed wi h dysphagia (dysphagia as dependen a iable). Va i-
ables wi h uni a ia e associa ions wi h p- alues < 0.20 we e
included in a mul i a iable model, and a backwa ds selec ion
p ocess was used o emo e a iables indi idually un il all
emaining a iables we e signi ican a he 0.10 le el excep
age, gende , disease du a ion and LEDD, added as co a ia es.
Spea man’s o Pea son’s co ela ion coe icien , as app op ia e,
we e used o analyzing he ela ionship be ween dysphagia
and d ooling, speech p oblems, and hypomimia. Co ela ions
we e conside ed weak o coe icien alues ≤ 0.29, mode a e
o alues be ween 0.30 and 0.59, and s ong o alues ≥ 0.60.
Gene al linea model (GLM) epea ed measu es we e used
o es o changes in he mean NMSS-i em 20 sco e in PD
pa ien s and in con ols. In he models, age, gende , disease
du a ion, and LEED a each isi we e included as co a ia es
o PD pa ien s and age and gende o con ols. The Bon-
e oni me hod was used as a pos -hoc es a e ANOVA.
Cohen´s d o mula was applied o measu ing he e ec size.
I was conside ed: < 0.2 – Negligible; 0.2 – 0.49 – Small; 0.50
– 0.79 – Mode a e; ≥ 0.80 – La ge. The alue o p was consid-
e ed signi ican when i was < 0.05.
S anda d p o ocol app o als, egis a ions,
andpa ien consen s
Fo his s udy, we ecei ed app o al om he Comi é de
É ica de la In es igación Clínica de Galicia om Spain
(2014/534; 02/DEC/2014). W i en in o med consen s om
all pa icipan s (pa ien s and con ols) in his s udy we e
ob ained.
Resul s
A o al o 184 ea ly PD pa ien s (62.3 ± 8.3yea s old; 56.8%
males) and 206 con ols (60.9 ± 8.3yea s old; 50% males)
we e included. Mean disease du a ion was 1.3 ± 0.7yea s.
A baseline, dysphagia was signi ican ly mo e equen in
PD pa ien s han con ols (19.6% s 5.3%; p < 0.0001) and
mean sco e o he NMSS-i em 20 was signi ican ly highe
in PD pa ien s (0.4 ± 1 s 0.1 ± 0.8; p < 0.0001). Howe e ,
only one pa ien had ele an dysphagia (NMSS-i em 20 ≥ 6)
and no di e ences we e de ec ed in he NMSS-i em 20 sco e
in pa ien s compa ed o con ols when only subjec s wi h
dysphagia we e included (2.1 ± 1.3 s 2.4 ± 2.4; p = 0.685).
A V0 and compa ing pa ien s wi h s wi hou dyspha-
gia, a highe sco e on he UPDRS-IV (1.4 ± 1.6 s 0.9 ± 1.4;
p = 0.014), FOGQ (3.3 ± 3.8 s 1.9 ± 2.9; p = 0.010), NMSS
(62.2 ± 35.3 s 35.7 ± 30.8; p < 0.0001), BDI-II (10.9 ± 7.8
s 7.8 ± 7.1; p = 0.019), QUIP-RS (7.8 ± 14 s 2.3 ± 4.9;
p = 0.007), VASF – physical (3.6 ± 2.7 s 2.4 ± 2.7;
p = 0.007), VASF – men al (3.4 ± 2.8 s 1.8 ± 2.3; p = 0.001),
and PDQ-39SI (23.2 ± 14.4 s 12.6 ± 11.3; p < 0.0001) and
a lowe sco e on he PDSS (98.8 ± 30.2 s 120.8 ± 25.7;
p < 0.0001) and ADLS (87.5 ± 11.6 s 92.8 ± 8.2; p = 0.028)
we e de ec ed in hose pa ien s wi h dysphagia (Table1).
Speci ically, FOG (36.1% s 18.2%; p = 0.021), alls (22.2%
s 6.2%; p = 0.007), d ooling (55.6% s 29.7%; p = 0.015),
and o ha e any ICB (21.4% s 6.6%; p = 0.024) we e mo e
equen in pa ien s wi h dysphagia. Bo h ICDs and CBs
we e associa ed wi h dysphagia wi h compulsi e ea ing he
mos signi ican ICB associa ed wi h dysphagia (14.3% in
pa ien s wi h dysphagia s 1.5% in hose wi hou dyspha-
gia; p = 0.008) (Fig.1). Dysphagia co ela ed mode a ely
wi h d ooling ( = 0.348; p < 0.0001) bu no wi h speech
p oblems ( = −0.115; p = 0.445) o hypomimia ( = −0.098;
p = 0.515). In a eg ession bina y model (dysphagia a base-
line as dependen a iable), he ac o s iden i ied as inde-
penden ly associa ed wi h dysphagia we e a wo se qual-
i y o sleep (PDSS; OR = 0.974; p = 0.005) and a g ea e
ICB (QUIP-RS; OR = 1.066; p = 0.014) and NMS bu den
(NMSS; OR = 1.016; p = 0.021) (Table2). The associa ion
be ween he QUIP-RS and dysphagia was main ained a e
adjus ing o be ecei ing a dopamine agonis (QUIP-RS;
OR = 1.073; p = 0.008). Speci ically, o ha e any ICD as
a whole (OR = 3.848; 95% CI 1.246 – 11.887; p = 0.019),
any ICD (OR = 5.696; 95% CI 1.527 – 21.245; p = 0.010),
any CB (OR = 4.746; 95% CI 1.337 – 16.848; p = 0.016),
compulsi e ea ing (OR = 11.25; 95% CI 1.951 – 64.871;
p = 0.007), hobbyism-punding (OR = 4.4; 95% CI 1.002
– 11.575; p = 0.007), and DDS (OR = 13.364; 95% CI 1.347
– 132.553; p = 0.027) we e associa ed wi h dysphagia, bu
none we e a e adjus ing o co a ia es o he model. A V5
(N = 116), he QUIP-RS was associa ed again o dysphagia
(OR = 1.042; 95% CI 1.001 – 1.086; p = 0.046), bu i was
no signi ican a e adjus men o co a ia es (p = 0.274).
In he ollow-up analysis (all da a in all isi s o all pa -
icipan s, om V0 o V5), 89 pa ien s (61 ± 8.6yea s old;
53.9% males) and 72 con ols (63.1 ± 6.7yea s old; 50%
males) we e included. Dysphagia was clea ly mo e equen
Neu ological Sciences
Table 1 Disease ela ed cha ac e is ics, mo o and non-mo o symp oms, au onomy o ac i i ies o daily li ing and quali y o li e in PD pa ien s
wi h s wi hou dysphagia a baseline (N = 184)
The esul s ep esen pe cen ages, mean ± SD o median [p25, p75]. Chi-squa ed, Fishe and ANOVA es we e applied. Da a abou H&Y and
UPDRS-III a e du ing he OFF s a e ( i s hing in he mo ning wi hou aking medica ion in he p e ious 12h)
ADLS Schwab and England Ac i i ies o daily li ing Scale), BDI-II Beck Dep ession In en o y-II, CB compulsi e beha io , FOGQ F eezing
o Gai Ques ionnai e, FOG eezing o gai , ICB impulse con ol beha io , ICD impulse con ol diso de , NMSS Non-Mo o Symp oms Scale,
NPI Neu opsychia ic In en o y, PD Pa kinson´s disease, PD-CRS Pa kinson’s Disease Cogni i e Ra ing Scale, PDSS Pa kinson’s Disease Sleep
Scale, PIGD Pos u al Ines abili y Gai Di icul y, QUIP-RS Ques ionnai e o Impulsi e-Compulsi e Diso de s in Pa kinson’s Disease-Ra ing
Scale, UPDRS Uni ied Pa kinson’s Disease Ra ing Scale, VAFS Visual Analog Fa igue Scale, VAS-Pain Visual Analog Scale-Pain
All coho (N = 184) Wi hou dysphagia
(N = 148)
Wi h dysphagia (N = 36) p
Age 62.3 ± 8.3 62.2 ± 8.4 62.8 ± 8.1 0.702
Males (%) 56.8 58.1 52.8 0.346
Disease du a ion (yea s) 1.3 ± 0.7 1.3 ± 0.7 1.1 ± 0.8 0.207
L-dopa daily dose (mg) 317 ± 247.4 317.1 ± 252.5 316.6 ± 228.1 0.753
Weigh (kgs) 75.8 ± 13.5 75.7 ± 14.2 76 ± 10.9 0.660
Mo o pheno ype (%): 0.777
- T emo ic dominan 58.7 57.5 63.9
- PIGD 28.3 29.7 22.2
- Inde e mina e 13 12.8 13.9
Hoehn & Yah – OFF 2 [1.5,2] 2 [1.5,2] 2 [1.5,2] 0.440
- S age 3 – 5 (%) 2.5 3.1 0 0.299
UPDRS-III—OFF 19.1 ± 9.1 19.2 ± 9.4 18.8 ± 7.6 0.814
UPDRS-IV 1 ± 1.4 0.9 ± 1.4 1.4 ± 1.6 0.014
- Mo o luc ua ions (%) 8.7 6.8 16.7 0.060
FOGQ 2.2 ± 3.1 1.9 ± 2.9 3.3 ± 3.8 0.010
- FOG (%) 21.7 18.2 36.1 0.021
- Falls (%) 9.4 6.2 22.2 0.007
MMSE 29.3 ± 1 29.4 ± 1 29.1 ± 1.1 0.242
PD-CRS o al sco e 90.7 ± 14.9 90.8 ± 15.1 90.6 ± 14.3 0.858
PD-CSR FS sub-sco e 62.8 ± 13.5 62.7 ± 13.6 63.4 ± 13.3 0.806
PD-CRS PC sub-sco e 27.9 ± 3.5 28.1 ± 3.3 27.2 ± 4.3 0.761
NMSS 40.9 ± 33.4 35.7 ± 30.8 62.2 ± 35.3 < 0.0001
- D ooling (%) 34.8 29.7 55.6 0.004
- Speech p oblems (%) 39 38 42.9 0.368
- Hypomimia (%) 76.1 81.2 64.3 0.192
BDI-II 8.4 ± 7.4 7.8 ± 7.1 10.9 ± 7.8 0.019
- Majo dep ession (%) 16.3 14.2 25 0.096
NPI 5.3 ± 6.8 4.7 ± 6.1 7.7 ± 8.5 0.063
QUIP-RS 3.3 ± 7.6 2.3 ± 4.9 7.8 ± 14 0.007
- Any ICB (ICD o CB) (%) 9.1 6.6 21.4 0.024
- Any ICD (%) 6.1 3.7 17.9 0.014
- Any CB (%) 6.7 4.4 17.9 0.022
PDSS 116.6 ± 27.9 120.9 ± 25.7 98.8 ± 30.2 < 0.0001
VAS-PAIN 2.7 ± 2.9 2.6 ± 2.8 3 ± 3.1 0.467
VASF − physical 2.6 ± 2.7 2.4 ± 2.7 3.6 ± 2.7 0.007
VASF – men al 2.1 ± 2.5 1.8 ± 2.3 3.4 ± 2.8 0.001
ADLS 91.1 ± 9.1 92 ± 8.2 87.5 ± 11.6 0.028
PDQ-39SI 14.7 ± 12.6 12.6 ± 11.3 23.2 ± 14.4 < 0.0001
EUROHIS-QOL8 3.8 ± 0.6 3.9 ± 0.5 3.7 ± 0.6 0.050
PQ-10 7.4 ± 1.6 7.4 ± 1.6 7.3 ± 1.6 0.424
Neu ological Sciences
in PD pa ien s han con ols (p < 0.0001 a V0, V2, V4 and
V5): 23.6% a V0, 28.1% a V1, 28.1% a V2, 29.2% a V3,
25.8% a V4, and 32.6% a V5 in pa ien s; 5.6% a V0, 4.2%
a V2, 2.8% a V4, and 6.9% a V5 in con ols (Fig.2A).
Mean sco e o he NMSS-i em 20 was signi ican ly highe
in PD pa ien s han con ols (p < 0.0001 in all isi s): V0,
0.6 ± 1.2 s 0.2 ± 1.2; V2, 0.7 ± 1.6 s 0.2 ± 1.1; V4, 0.7 ± 1.5
s 0.1 ± 0.5; V5, 0.7 ± 1.5 s ± 0.2 ± 0.7. Howe e , no s a is-
ically signi ican di e ences (p ≥ 0.05) be ween PD pa ien s
and con ols in he NMSS-i em 20 sco e we e de ec ed in
any o he isi s when only subjec s wi h dysphagia we e
included (Fig.2B). No di e ences (Cohen´s d o mula < 0.2
and p > 0.05 o all analysis) in he mean NMSS-i em 20
sco e we e de ec ed be ween he di e en isi s ( om V0 o
V5; om V0 o V1; om V1 o V2; om V2 o V3; om
V3 o V4; om V4 o V5) h oughou he ollow-up nei he
in pa ien s no con ols. Rele an dysphagia bu den was
de ec ed only in 1.1%, 6.6%, 3.3%, 6.7%, 4.5%, and 3.3%
o he pa ien s a V0, V1, V2, V3, V4, and V5, espec i ely.
Discussion
The p esen s udy obse ed ha dysphagia is equen in
ea ly PD pa ien s (≤ 2yea s o disease du a ion), a ec -
ing abou 1 ou o 4 pa ien s. Howe e , dysphagia bu den
was low and did no p og ess o e ime, like in con ols.
Al hough many ac o s we e associa ed wi h dysphagia
in ea ly s ages o PD, only a wo se quali y o sleep and a
g ea e ICB and NMS bu den we e independen ac o asso-
cia ed wi h dysphagia. To ou knowledge, his is he i s
ime ha an associa ion be ween dysphagia and ICBs ha e
been desc ibed.
Fig. 1 Pe cen age o PD pa ien s wi h dysphagia (in g een) s wi hou dysphagia (in black) su e ing om impulse and/o compulsi e symp-
oms. Fishe es was applied. CBs, compulsi e beha io s; ICBs, impulsi e-compulsi e beha io s; ICDs, impulse con ol diso de s
Table 2 Independen ac o s
associa ed wi h dysphagia in PD
pa ien s a baseline (N = 184)
Dependen a iable: Dysphagia a baseline. OR and 95% IC a e shown. a, uni a ia e analysis; b, mul i a i-
a e analysis. The model was adjus ed o age, gende , disease du a ion and LEDD. LEDD le odopa equi -
alen daily dose, NMSS Non-Mo o Symp oms Scale, PDSS Pa kinson´s Disease Sleep Scale, QUIP-RS
Ques ionnai e o Impulsi e-Compulsi e Diso de s in Pa kinson's Disease-Ra ing Scale
Va iables a baseline ORaORbHosme –
Lemeshow
es
R295% ICa95% ICbpapb
PDSS 0.976 0.974 0.59 0.35 0.96 – 0.99 0.96 – 0.99 < 0.0001 0.005
QUIP-RS 1.074 1.066 1.03 – 1.13 1.02 – 1.12 0.003 0.014
NMSS 1.021 1.016 1.01 – 1.03 1.01 – 1.03 < 0.0001 0.021

Neu ological Sciences
Th oughou he 5yea s o ollow-up o ou coho , he
p e alence o dysphagia was clea ly highe in PD pa ien s
( om 23.6% a baseline o 32.6% a e 5yea s o ollow-up)
han in con ols ( om 2.8% o 6.9%) and conside ably high
o e all conside ing he ac ha hey had less han 2yea s
om symp oms onse a baseline. PD is one o he impo -
an e iologies o dysphagia, showing a pooled p e alence o
35% and up o 82% using subjec i e measu es and objec i e
measu es, espec i ely [2]. Di e ences in he me hodology
including dysphagia de ini ion and he cha ac e is ics o PD
popula ions explain he g ea p e alence ange. Since dys-
phagia is conside ed a ed lag ha would sugges a ypical
pa kinsonism [1], i is impo an o pa se ou how equen
dysphagia is in PD a diagnosis. Ve y li le in o ma ion has
been published abou his. Only 2 ou o 58 s udies abou
dysphagia in PD we e conduc ed in PD pa ien s wi h a dis-
ease du a ion ≤ 2yea s [3, 9, 10]. Ou inding o a dyspha-
gia p e alence o 19.6% (36 ou o 184 pa ien s) a base-
line ag ees wi h he 20.1% epo ed by Malek e al. [10] in
1746 pa ien s ha had been diagnosed wi hin he p eceding
3.5yea s (mean disease du a ion o 1.3yea s) and 20.1% ( s
3% in con ols) de ec ed by Khoo e al. [19] in 159 pa ien s
wi h a median disease du a ion o 4.4mon hs. Howe e , his
was highe han he 12.3% epo ed by Polych onis e al. [9]
in 398 PD pa ien s wi h a mean disease du a ion o 0.5yea s.
As in ou s udy, dysphagia was eco ded in all hese s ud-
ies [9, 10, 19] acco ding o a ques ion o a gene al scale,
he SCOPA-AUT [9, 10] and he NMSQues [19], and no
wi h objec i e me hods. We used a ques ion (i em 20) o he
NMSS and esul s mus be in e p e ed wi h cau ion because
he p e alence could be highe i a mo e speci ic scale ali-
da ed o he de ec ion o dysphagia o especially objec i e
me hods we e used [20]. In ac , and su p isingly, 0 ou o
41 newly diagnosed PD pa ien s had “di icul y swallow-
ing ood o d inking o p oblems wi h choking” in a s udy
in which he NMSQues was used [21]. Compa ing o all
s udies conduc ed in ea ly PD pa ien s, we demons a ed
ha al hough dysphagia could be equen e en in he i s
2yea s om symp oms onse and is clea ly mo e common
han in con ols, ele an dysphagia is a e, and dysphagia
bu den doesn’ p og ess o e ime a e a 5-yea ollow-up.
None heless, his could be a cue o di e en ia e pa kinson-
ism wi h dysphagia is due o PD s. an a ypical pa kinson-
ism [22].
Some ac o s ha e been iden i ied o be associa ed wi h
dysphagia in PD such as olde age, male sex, lowe body
mass index, longe disease du a ion, highe H&Y s age and
le odopa equi alen daily dose (LEDD), PIGD sub ype,
se e e mo o symp oms, cogni i e impai men , d ooling,
highe le els o dep ession and anxie y, and lowe QoL
[3–5]. Many o hem a e ela ed o he p og ession o he
disease and in ac , he p e alence o dysphagia is highe in
ad anced PD, eaching up o mo e han 80% [23]. Howe e ,
despi e ou analysis being conduc ed in ea ly PD pa ien s
Fig. 2 A. Numbe o PD pa ien s and/o con ols wi h and wi h-
ou dysphagia a V0, V1, V2, V3, V4 and V5. A V0, V2, V4 and
V5, he pe cen age o dysphagia was signi ican ly highe in pa ien s
han in con ols (p < 0.0001 o all analysis). The Chi-squa e es was
applied. B. NMSS-i em 20 sco e in PD pa ien s wi h dysphagia a
V0, V1, V2, V3, V4 and V5 and in con ols a V0, V2, V4 and V5.
Mean and s anda d de ia ion a e shown. No signi ican di e ences
(p > 0.05) we e de ec ed be ween pa ien s and con ols in any isi o
be ween he di e en isi s h oughou he ollow-up in ei he pa ien s
and con ols. T-S uden and/o Gene al linea model (GLM) epea ed
measu e was adjus ing o age, gende , disease du a ion and le odopa
equi alen daily dose a each isi
Neu ological Sciences
(mean disease du a ion 1.3 ± 0.7) wi h 97.5% in he s age 2
o H&Y, signi ican di e ences be ween pa ien s wi h and
wi hou dysphagia we e obse ed in mo o aspec s (UPDRS-
IV, FOG and alls), NMS including d ooling, mood (BDI-II),
ICBs (QUIP-RS), sleep (PDSS), and a igue (VAFS), dis-
abili y (ADLS), and PD ela ed QoL (PDQ-39SI). O hem,
only a wo se quali y o sleep and a g ea e ICB and NMS
bu den we e independen ac o s associa ed wi h dyspha-
gia. In e es ingly, Ma ano e al. [23] obse ed ha excessi e
day ime sleepiness was s ongly ela ed o he de elopmen
o swallowing impai men a e a 3-yea ollow-up in a e -
ospec i e s udy conduc ed in ea ly-s age PD pa ien s who
we e no on dopamine gic ea men a baseline. D ooling
and dysphagia a e ela ed [3, 24], as we ound, and can a ec
he sleep. Mean o al sleep ime (minu es) was 350.8 ± 79.3
in 5 PD pa ien s wi h dysphagia compa ed o 406.4 ± 119.9
in 16 PD pa ien s wi hou dysphagia in a s udy conduc ed in
21 PD pa ien s s 18 con ols wi h all-nigh sleep ideo-EEG
and elec omyog aphy in o ma ion collec ed [25]. Mo eo e ,
sleep is one o he i ems commonly a ec ed in s udies ana-
lyzing he QOL ela ed o swallowing [26].
NMS bu den was also ela ed o dysphagia in ou coho .
A g ea e bu den o NMS in pa ien s wi h dysphagia could
sugges he p esence o a pheno ype wi h mo e non-mo o
in ol emen . Addi ionally, he p esence o dysphagia could
be a use ul indica ion o in es iga e he p esence o o he
NMS. The pa hophysiology o dysphagia is complex and
many a eas o he b ain and e en in he pe iphe al ne -
ous sys em could be in ol ed [27], which could explain he
g ea e NMS bu den ha we ound associa ed wi h dys-
phagia. On he o he hand, ou limi ed knowledge on he
ela ionship be ween dysphagia and ICB is mo e di icul
o explain. Impo an ly, his is he i s ime desc ibed, bu
p obably, he i s ime explo ed as well [28]. As we did
no collec ed in o ma ion o classi y he pa ien ’s swallow
di icul y (i.e., o al phase s pha yngeal phase s esopha-
geal phase), all possible sugges ions a e pu ely specula i e.
Dysphagia is also associa ed wi h dep ession and anxie y
due o (i) he se e i y and impac o he symp om i sel , (ii)
he unde lying cause, and/o (iii) inapp op ia e esponses o
swallowing p oblems leading o subsequen impulsi e ea ing
beha io s o o he maladap i e beha io s, among o he ea-
sons [29]. To hink o a on al lobe dys unc ion as a cause
[30], we did no obse e di e ences in cogni i e unc ion
be ween PD pa ien s wi h s wi hou dysphagia, like in some
s udies [3]. In e es ingly, in he ICARUS s udy [31], pa ien s
who we e ICD-posi i e a s udy baseline had mo e se e e
NMS (including mood and sexual unc ion) and dep ession,
as well as had poo e sleep quali y and educed PD- ela ed
QoL compa ed wi h hose who we e ICD-nega i e, like in
ou coho wi h hose pa ien s wi h dysphagia. This possible
ela ionship be ween ICBs and dysphagia should be p op-
e ly explo ed. In a o o i , a signi ican associa ion wi h
he QUIP-RS was ob ained again a e he 5-yea ollow-
up in his coho o ea ly PD pa ien . When conside ing all
he coho , he QUIP-RS was associa ed o dysphagia as
well (da a no shown; N = 691; OR = 1.027; 95% CI 1.003
– 1.051; p = 0.027) a e adjus men o age, gende , disease
du a ion, H&Y s age, dopamine agonis ea men , UPDRS-
IV, NMSS, and PDSS. Finally, and ega ding QoL, pa ien s
wi h dysphagia had a wo se QoL acco ding o he PDQ-39,
some hing p e iously epo ed in a me a-analysis [3]. This
ein o ces he impo ance o dysphagia as a disabling symp-
om o he pa ien [26].
The p esen s udy has limi a ions. The mos impo an ,
as i has been men ioned, dysphagia was de ined acco d-
ing o subjec i e me hods using one ques ion o a gene al
ques ionnai e (NMSS). Seconda ily, mechanisms in ol ed
in dysphagia in hese pa ien s we e no analyzed. Howe e ,
his is equen in he li e a u e applying pos -hoc analysis,
like ou s, in big coho s [9, 10]. Second, o some analysis
compa ing g oups (e.g., ICB), he sample was small. Thi d,
ou indings may no be applicable o all PD pa ien s in he
communi y clinical se ing be-cause PD pa ien s en olled in
he COPPADIS s udy ep esen a selec ed popula ion wi h
less disabili y a baseline han he gene al popula ion (e.g.,
no olde han 75yea s old, no being unde a second line
he apy, e c.). Finally, o he ma ke s (neu oimaging, gene ic,
sleep s udy, e c.) we e no used o explain he associa ion
be ween dysphagia and o he a iables (e.g., ICD). On he
o he hand, and as s eng hs, his is a 5-yea ollow-up s udy
wi h a compa ing con ol g oup in which ex ensi e in o -
ma ion abou sociodemog aphic aspec s, mo o and NMS,
disabili y and QoL has been compa ed ega ding dysphagia.
Fo he i s ime, a ela ionship be ween he QUIP-RS sco e
and dysphagia has been epo ed.
In conclusion, dysphagia was equen in ea ly PD
pa ien s and clea ly highe compa ed o con ols. Howe e ,
i was mino and did no p og ess o e ime. Sleep, ICB,
and non-mo o symp oms bu den we e ela ed o dysphagia.
Mo e s udies speci ically designed o analyze he ela ion-
ship be ween dysphagia wi h o he symp oms using subjec-
i e combined wi h objec i e me hods a he same ime a e
equi ed. Replica ion o his associa ion be ween dysphagia
and ICD is equi ed.
Supplemen a y In o ma ion The online e sion con ains supplemen-
a y ma e ial a ailable a h ps:// doi. o g/ 10. 1007/ s10072- 025- 08027-8.
Acknowledgemen s We would like o hank all pa ien s and hei ca -
egi e s who collabo a ed in his s udy. Many hanks also o Fundación
Española de Ayuda a la In es igación en En e medades Neu odegen-
e a i as y/o de O igen Gené ico (h ps:// unda ciond egen. o g/), Alpha
Bio esea ch (h p:// www. alpha bio e sea ch. com), Ins i u o de Salud
Ca los III and o he ins i u ions helping us.Finally, he paymen o he
ees o his publica ion has been ca ied ou by he Galician Public
Founda ion o Biomedical Resea ch INIBIC (h ps:// www. inibic. es/)
om he aid o open access publica ions.
Neu ological Sciences
COPPADIS STUDY GROUP
Ada mes AD, Alme ia M, Alonso Losada MG, Alonso Cáno as
A, Alonso F ech F, Alonso Redondo R, Ál a ez I, Ál a ez Sauco M,
Anei os Díaz A, A náiz S, A ibas S, Ascunce Vidondo A, Agui-
la M, Á ila MA, Be na do Lamb ich N, Bej -Kasem H, Blázquez
Es ada M, Bo í M, Bo ue C, Buongio no MT, Cabello González C,
Cabo López I, Caballol N, Cáma a Lo enzo A, Can ield Medina H,
Ca abajal Pendón E, Ca illo F, Ca illo Padilla FJ, Casas E, Ca alán
MJ, Cla e o P, Co ina Fe nández A, Cosgaya M, Co s Fo as e A,
C espo Cue as A, Cubo E, de Deus Fon icoba T, de Fáb egues-Boixa
O, Díez-Fai en M, Do o Ga cía-So o J, E o E, Escalan e S, Es el-
ich Pey e E, Fe nández Guillán N, Gámez P, Gallego M, Ga cía
Calden ey J, Ga cía Campos C, Ga cía Díez C, Ga cía Mo eno JM,
Gas ón I, Gómez Ga e MP, Gómez Mayo domo V, González Aloy
J, González-A ambu u I, González A du a J, González Ga cía B,
González Palmás MJ, González Toledo GR, Golpe Díaz A, G au Solá
M, Gua dia G, He nández Va a J, Ho a-Ba ba A, Idoa e Calde ón
D, In an e J, Jesús S, Kulise sky J, Ku is M, Labandei a C, Lab-
ado MA, Lac uz F, Lage Cas o M, Las es Gómez S, Lega da I,
López A iz egui N, López Díaz LM, López Domínguez D, López
Manzana es L, López Seoane B, Lucas del Pozo S, Macías Y, Ma a M,
Ma í And es G, Ma í MJ, Ma ínez Cas illo JC, Ma inez-Ma in P,
McA ee D, Mei ín MT, Mendoza Plasencia Z, Menéndez González M,
Méndez del Ba io C, Mi P, Mi anda San iago J, Mo ales Casado MI,
Mo eno Diéguez A, Mu o Ga cía I, Noguei a V, No o Amado A, No o
Pon e S, O dás C, Pagonaba aga J, Pa eés I, Pascual-Sedano B, Pas-
o P, Pé ez Fue es A, Pé ez Nogue a R, Planas-Ball é A, Planellas
L, P a s MA, P ie o Ju czynska C, Puen e V, Pueyo Mo lans M, Puig
Da í A, Redondo Ra ales N, Rod íguez Méndez L, Rod íguez Pé ez
AB, Roldán F, Ruíz De A cos M, Ruíz Ma ínez J, Sánchez Alonso
P, Sánchez-Ca pin e o M, Sánchez Díez G, Sánchez Rod íguez A,
San ac uz P, San os Ga cía D, Segundo Rod íguez JC, Seijo M, Sie a
Peña M, Solano Vila B, Suá ez Cas o E, Ta a i JP, Vale o C, Va gas
L, Vela L, Villanue a C, Vi es B.
Name (Las Name, Fi s Name) Loca ion Role Con ibu ion
As id Ada mes, Daniela Hospi al Uni e si a io Vi gen del
Rocío, Se illa, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Alme ia, Ma a Hospi al Uni e si a i Mu ua de
Te assa, Te assa, Ba celona,
Spain
Si e in es iga o Neu opsychologis ; e alua ion o pa ici-
pan s
Alonso Losada, Ma ia Gema Hospi al Ál a o Cunquei o, Com-
plejo Hospi ala io Uni e si a io
de Vigo (CHUVI), Vigo, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Alonso Cáno as, A aceli Hospi al Uni e si a io Ramón y
Cajal, Mad id, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Alonso F ech, Fe nando Hospi al Uni e si a io Clínico San
Ca los, Mad id, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Alonso Redondo, Ruben Hospi al Uni e si a io Lucus
Augus i (HULA), Lugo, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Anei os Díaz, Ángel Complejo Hospi ala io Uni e si-
a io de Fe ol (CHUF), Fe ol, A
Co uña, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Ál a ez, Ignacio Hospi al Uni e si a i Mu ua de
Te assa, Te assa, Ba celona,
Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Ál a ez Sauco, Ma ía Hospi al Gene al Uni e si a io de
Elche, Elche, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
A náiz, Sand a Complejo Asis encial Uni e si a io
de Bu gos, Bu gos, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
A ibas, Sonia Hospi al Uni e si a i Mu ua de
Te assa, Te assa, Ba celona,
Spain
Si e in es iga o Neu opsychologis ; e alua ion o pa ici-
pan s
Ascunce Vidondo, A ancha Complejo Hospi ala io de Na a a,
Pamplona, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Aguila , Miquel Hospi al Uni e si a i Mu ua de
Te assa, Te assa, Ba celona,
Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Á ila Ri e a, Ma ia Asunción Conso ci Sani a i In eg al, Hos-
pi al Gene al de L´Hospi ale ,
L´Hospi ale de Llob ega , Ba ce-
lona, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Neu ological Sciences
Name (Las Name, Fi s Name) Loca ion Role Con ibu ion
Be na do Lamb ich, Noemí Hospi al de To osa Ve ge de la
Cin a (HTVC), To osa, Ta -
agona, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Bej -Kasem, Helena Hospi al de San Pau, Ba celona,
Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Blázquez Es ada, Ma a Hospi al Uni e si a io Cen al de
As u ias, O iedo, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Bo í González, Ma ia Ángeles Hospi al Uni e si a i Mu ua de
Te assa, Te assa, Ba celona,
Spain
Si e in es iga o Neu opsychologis ; e alua ion o pa ici-
pan s
Bo ué, Ca men Hospi al In an a So ía, Mad id,
Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Buongio no, Ma ia Te esa Hospi al Uni e si a i Mu ua de
Te assa, Te assa, Ba celona,
Spain
Si e in es iga o (un il
2024)
Nu se s udy coo dina o
Cabello González, Ca olina Complejo Hospi ala io de Na a a,
Pamplona, Spain
Si e in es iga o Scheduling o e alua ions
Cabo López, I ia Complejo Hospi ala io Uni e -
si a io de Pon e ed a (CHOP),
Pon e ed a, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Caballol, Nu ia Conso ci Sani a i In eg al, Hospi al
Moisés B oggi, San Joan Despí,
Ba celona, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Cáma a Lo enzo, Ana Hospi al Clínic de Ba celona,
Ba celona, Spain
Si e in es iga o Nu se s udy coo dina o
Can ield Medina, Héc o Complejo Hospi ala io Uni e si-
a io de Fe ol (CHUF), Fe ol, A
Co uña, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Ca abajal Pendón, Es e anía Hospi al La P incesa, Mad id,
Spain
Si e in es iga o ( om
MAR/23)
E alua ion o pa icipan s and/o da a
managemen
Ca illo, Fá ima Hospi al Uni e si a io Vi gen del
Rocío, Se illa, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Ca illo Padilla, F ancisco José Hospi al Uni e si a io de Cana ias,
San C is óbal de la Laguna, San a
C uz de Tene i e, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Casas, Elena Complejo Asis encial Uni e si a io
de Bu gos, Bu gos, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Ca alán, Ma ia José Hospi al Uni e si a io Clínico San
Ca los, Mad id, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Cla e o, Ped o Complejo Hospi ala io de Na a a,
Pamplona, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Co ina Fe nández, A Complejo Hospi ala io Uni e si-
a io de Fe ol (CHUF), Fe ol, A
Co uña, Spain
Si e in es iga o Coo dina ion o blood ex ac ions
Cosgaya, Ma ina Hospi al Clínic de Ba celona,
Ba celona, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Co s Fo as e , Anna Ins i u d'Assis ència Sani à ia
(IAS)—Ins i uí Cá ala de la
Salud. Gi ona, Spain
Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
C espo Cue as, Ane Hospi al del Ma , Ba celona, Spain Si e in es iga o E alua ion o pa icipan s and/o da a
managemen
Cubo, Es he Complejo Asis encial Uni e si a io
de Bu gos, Bu gos, Spain
Si e in es iga o / PI Coo dina ion a he cen e
E alua ion o pa icipan s and/o da a
managemen
Neu ological Sciences
Open Access This a icle is licensed unde a C ea i e Commons A i-
bu ion 4.0 In e na ional License, which pe mi s use, sha ing, adap a-
ion, dis ibu ion and ep oduc ion in any medium o o ma , as long
as you gi e app op ia e c edi o he o iginal au ho (s) and he sou ce,
p o ide a link o he C ea i e Commons licence, and indica e i changes
we e made. The images o o he hi d pa y ma e ial in his a icle a e
included in he a icle’s C ea i e Commons licence, unless indica ed
o he wise in a c edi line o he ma e ial. I ma e ial is no included in
he a icle’s C ea i e Commons licence and you in ended use is no
pe mi ed by s a u o y egula ion o exceeds he pe mi ed use, you will
need o ob ain pe mission di ec ly om he copy igh holde . To iew a
copy o his licence, isi h p://c ea i ecommons.o g/licenses/by/4.0/.
Re e ences
1. Pos uma RB, Be g D, S e n M e al (2015) MDS clinical diagnos-
ic c i e ia o Pa kinson’s disease. Mo Diso d 30:1591–1601
2. Kal JG, de Swa BJ, Bloem BR, Munneke M (2012) P e alence
o o opha yngeal dysphagia in Pa kinson’s disease: a me a-anal-
ysis. Pa kinsonism Rela Diso d 18:311–315
3. Gong S, Gao Y, Liu J e al (2022) The p e alence and associa ed
ac o s o dysphagia in Pa kinson’s disease: a sys ema ic e iew
and me a-analysis. F on Neu ol 13:1000527
4. Claus I, Muhle P, Su up J e al (2020) P edic o s o pha yngeal
dysphagia in pa ien s wi h Pa kinson’s disease. J Pa kinsons Dis
10:1727–1735
5. Wang P, Wang B, Chen X e al (2022) Six-yea ollow-up o
dysphagia in pa ien s wi h Pa kinson’s disease. Dysphagia
37:1271–1278
6. Fabb i M, Coelho M, Ab eu D e al (2019) Dysphagia p edic s
poo ou come in la e-s age Pa kinson’s disease. Pa kinsonism
Rela Diso d 64:73–81
7. Bachmann CG, T enkwalde C (2006) Body weigh in pa ien s
wi h Pa kinson’s disease. Mo Diso d 21:1824–1830
8. Volon é MA, Po a M, Comi G (2002) Clinical assessmen o dys-
phagia in ea ly phases o Pa kinson’s disease. Neu ol Sci 23(Suppl
2):S121–S122
9. Polych onis S, De enoulas G, Yousa T e al (2019) Dyspha-
gia is associa ed wi h p esynap ic dopamine gic dys unc ion and
g ea e non-mo o symp om bu den in ea ly d ug-naï e Pa kin-
son’s pa ien s. PLoS One 14:e0214352
10. Malek N, Law on MA, G osse KA e al; PRoBaND Clinical
Conso ium (2016) Au onomic dys unc ion in ea ly Pa kinson's
disease: esul s om he Uni ed Kingdom acking Pa kinson's
s udy. Mo Diso d Clin P ac 4:509–16
11. San os Ga cía D, Jesús S, Aguila M, e al; COPPADIS S udy
G oup (2019) COPPADIS-2015 (COho o Pa ien s wi h PA -
kinson's DIsease in Spain, 2015): an ongoing global Pa kinson's
disease p ojec abou disease p og ession wi h mo e han 1000
subjec s included. Resul s om he baseline e alua ion. Eu J
Neu ol 26:1399–407
12. San os-Ga cía D, Mi P, Cubo E, e al; COPPADIS S udy G oup
(2016) COPPADIS-2015 (COho o Pa ien s wi h PA kinson's
DIsease in Spain, 2015), a global--clinical e alua ions, se um bio-
ma ke s, gene ic s udies and neu oimaging--p ospec i e, mul i-
cen e , non-in e en ional, long- e m s udy on Pa kinson's disease
p og ession. BMC Neu ol 16:26
13. Hughes AJ, Daniel SE, Kil o d L, Lees AJ (1992) Accu acy o
clinical diagnosis o idiopa hic Pa kinson’s disease: a clinico-
pa hological s udy o 100 cases. J Neu ol Neu osu g Psychia y
55:181–184
14. Chaudhu i KR, Ma inez-Ma in P, B own RG e al (2007) The
me ic p ope ies o a no el non-mo o symp oms scale o
Pa kinson’s disease: Resul s om an in e na ional pilo s udy.
Mo Diso d 22:1901–1911
15. Fanhn S, El on RL, Membe s o he UPDRS De elopmen Com-
mi ee (1987) Uni ied Pa kinson's Disease Ra ing Scale. In: Fahn
S, Ma sden CD, Calne DB, Golds ein M (eds) Recen de elop-
men s in Pa kinson's disease, Vol 2. Macmillan Heal h Ca e In o -
ma ion, Flo ham Pa k, NJ, p-153–64
16. Wein aub D, Mamikonyan E, Papay K, Shea JA, Xie SX, Side-
ow A (2012) Ques ionnai e o impulsi e-compulsi e diso de s
in Pa kinson’s disease- a ing scale. Mo Diso d 27:242–247
17. San os-Ga cía D, de Deus Fon icoba T, Co es Ba olomé C, e al;
COPPADIS S udy G oup (2021) Dep ession is Associa ed wi h
Impulse-compulsi e Beha io s in Pa kinson's disease. J A ec
Diso d 280(P B):77–89
18. Jos ST, Kaldenbach MA, An onini A, e al; In e na ional Pa -
kinson and Mo emen Diso de s Socie y Non-Mo o Pa kinson
Disease S udy G oup (2023) Le odopa dose equi alency in Pa -
kinson's disease: upda ed sys ema ic e iew and p oposals. Mo
Diso d 38:1236–52
19. Khoo TK, Ya nall AJ, Duncan GW, Coleman S, O’B ien JT,
B ooks DJ, Ba ke RA, Bu n DJ (2013) The spec um o nonmo-
o symp oms in ea ly Pa kinson disease. Neu ology 80:276–281
20. Cha S, Chang WK, Cho HM e al (2023) Dysphagia equi ing
medical a en ion in Pa kinson’s disease: a Ko ean popula ion-
based s udy. J Ko ean Med Sci 38:e114
21. Ragab OA, Elheneedy YA, Bahnasy WS (2019) Non-mo o symp-
oms in newly diagnosed Pa kinson’s disease pa ien s. Egyp J
Neu ol Psychia y Neu osu g 55:24
22. Glinze J, Flynn É, Tampouka i E, Ha pu I, Walshe M (2024)
Dysphagia p e alence in p og essi e sup anuclea palsy: a sys-
ema ic e iew and me a-analysis. Dysphagia 39:1052–1064
23. Ma ano M, Gup a D, Mo olese F e al (2020) Excessi e day ime
sleepiness is associa ed o he de elopmen o swallowing impai -
men in a coho o ea ly s age d ug naï e Pa kinson’s disease
pa ien s. J Neu ol Sci 410:116626
24. Su up I, Wa necke T (2016) Dysphagia in Pa kinson’s disease.
Dysphagia 31:24–32
25. Uludag IF, Ti ikcioglu BI, E ekin C (2016) Spon aneous swal-
lowing du ing all-nigh sleep in pa ien s wi h Pa kinson disease
in compa ison wi h heal hy con ol subjec s. Sleep 39:847–854
26. Ca nei o D, das G aças Wande ley de Sales Co iolano M, Belo
LR, de Ma cos Rabelo AR, Asano AG, Lins OG (2014) Quali y
o li e ela ed o swallowing in Pa kinson's disease. Dysphagia
29:578–82
27. Kwon M, Lee JH (2019) O o-pha yngeal dysphagia in Pa kin-
son’s disease and ela ed mo emen diso de s. J Mo Diso d
12:152–160
28. Liu B, Luo W, Mo Y, Wei C, Tao R, Han M (2019) Me a-analysis
o ela ed ac o s o impulse con ol diso de s in pa ien s wi h
Pa kinson’s disease. Neu osci Le 707:134313
29. Fe nández-A anda F, Jiménez-Mu cia S, Al a ez-Moya EM,
G ane o R, Vallejo J, Bulik CM (2006) Impulse con ol diso de s
in ea ing diso de s: clinical and he apeu ic implica ions. Comp
Psychia y 47:482–488
30. San angelo G, Raimo S, Ba one P (2017) The ela ionship
be ween Impulse con ol diso de s and cogni i e dys unc ions
in Pa kinson’s disease: a me a-analysis. Neu osci Biobeha Re
77:129–147
31. An onini A, Ba one P, Bonuccelli U, Annoni K, Asgha nejad M,
S anzione P (2017) ICARUS s udy: p e alence and clinical ea-
u es o impulse con ol diso de s in Pa kinson’s disease. J Neu ol
Neu osu g Psychia y 88:317–324
Publishe 's No e Sp inge Na u e emains neu al wi h ega d o
ju isdic ional claims in published maps and ins i u ional a ilia ions.

Neu ological Sciences
Au ho s and A ilia ions
DiegoSan os‑Ga cía1,2,3,4 · Te esadeDeusFon icoba5· Sil iaJesús6,7· Ma inaCosgaya8· JuanGa cíaCalden ey9·
Nu iaCaballol10· InesLega da11· Jo geHe nándezVa a7,12· I iaCabo13· LydiaLópezManzana es14·
IsabelGonzálezA ambu u7,15· Ma iaA. Á ilaRi e a16· Víc o GómezMayo domo17· Víc o Noguei a18·
JulioDo o Ga cía‑So o19· Ca menBo ué20· Be aSolanoVila21· Ma íaÁl a ezSauco22· LydiaVela23·
SoniaEscalan e24· Es he Cubo25· ZebenzuiMendoza26· IsabelPa eés27· Pila SánchezAlonso28·
Ma iaG.AlonsoLosada29· Nu iaLópezA iz egui30· I zia Gas ón31· JaimeKulise sky7,32· ManuelSeijo13·
Ca idadVale o33· RubenAlonsoRedondo18· Ca losO dás34· ManuelMenéndez‑González35· Da ianMcA ee36·
PabloMa inez‑Ma in7· PabloMi 6,7,37· COPPADIS S udy G oup
* Diego San os-Ga cía
diegosanga @yahoo.es
1 Depa men o Neu ology, Hospi al Uni e si a io de
ACo uña (HUAC), Complejo Hospi ala io Uni e si a io
de ACo uña (CHUAC), C/ As Xubias 84, 15006ACo uña,
Spain
2 G upo de In es igación en En e medad de Pa kinson y
O os T as o nos del Mo imien o, INIBIC (Ins i u o de
In es igación Biomédica de ACo uña), ACo uña, Spain
3 Hospi al San Ra ael, ACo uña, Spain
4 Fundación Degen, ACo uña, Spain
5 CHUF, Complejo Hospi ala io Uni e si a io de Fe ol,
ACo uña, Spain
6 Unidad de T as o nos del Mo imien o, Se icio de
Neu ología y Neu o isiología Clínica, Ins i u o de
Biomedicina de Se illa, Hospi al Uni e si a io Vi gen del
Rocío/CSIC/Uni e sidad de Se illa, Se ille, Spain
7 CIBERNED (Cen o de In es igación Biomédica en Red
En e medades Neu odegene a i as), Mad id, Spain
8 Hospi al Clínic de Ba celona, Ba celona, Spain
9 Cen o Neu ológico Oms 42, Palma, Spain
10 Conso ci Sani a i In eg al, Hospi al Moisés B oggi,
San JoanDespí,Ba celona, Spain
11 Hospi al Uni e si a io Son Espases, Palma, Spain
12 Hospi al Uni e si a io Vall d´Heb on, Ba celona, Spain
13 Complejo Hospi ala io Uni e si a io de Pon e ed a (CHOP),
Pon e ed a, Spain
14 Hospi al Uni e si a io La P incesa, Mad id, Spain
15 Hospi al Uni e si a io Ma qués de Valdecilla - IDIVAL,
San ande , Spain
16 Conso ci Sani a i In eg al, Hospi al Gene al de L´Hospi ale ,
L´Hospi ale de Llob ega , Ba celona, Spain
17 Neu ology Depa men , Ins i u e o Neu oscience, Vi has
Mad id La Milag osa Uni e si y Hospi al, Vi has Hospi al
G oup, Mad id, Spain
18 Hospi al Uni e si a io Lucus Augus i, Lugo, Spain
19 Hospi al Uni e si a io Vi gen Maca ena, Se ille, Spain
20 Hospi al In an a So ía, Mad id, Spain
21 Ins i u d‘Assis ència Sani à ia (IAS) - Ins i u Ca alà de La
Salu , Gi ona, Spain
22 Hospi al Gene al Uni e si a io de Elche, Elche, Spain
23 Fundación Hospi al de Alco cón, Mad id, Spain
24 Hospi al de To osa Ve ge de La Cin a (HTVC),
To osa,Ta agona, Spain
25 Complejo Asis encial Uni e si a io de Bu gos, Bu gos, Spain
26 Hospi al Uni e si a io de Cana ias, San C is óbal de La
Laguna, San aC uzdeTene i e, Spain
27 Hospi al Uni e si a io Ramón y Cajal, IRYCIS, Mad id,
Spain
28 Hospi al Uni e si a io Pue a de Hie o, Mad id, Spain
29 Hospi al Ál a o Cunquei o, Complejo Hospi ala io
Uni e si a io de Vigo (CHUVI), Vigo, Spain
30 Complejo Hospi ala io de Toledo, Toledo, Spain
31 Complejo Hospi ala io de Na a a, Pamplona, Spain
32 Hospi al de San Pau, Ba celona, Spain
33 Hospi al A nau de Vilano a, Valencia, Spain
34 Hospi al Rey Juan Ca los, Mad id, Spain
35 Hospi al Uni e si a io Cen al de As u ias, O iedo, Spain
36 Uni e si y o Ma yland School o Medicine, Bal imo e, MD,
USA
37 Depa amen o de Medicina, Facul ad de Medicina,
Uni e sidad de Se illa, Se ille, Spain