Abdominal pain in Parkinson’s disease

Pilipovich A.A.; Vorobeva O.V.; Makarov S.A.

doi:https://doi.org/10.17116/pain20232102112

Close metadata

OBJECTIVE

To evaluate abdominal pain in patients with Parkinson’s disease (PD) and its relationship with motor and non-motor symptoms of disease.

MATERIAL AND METHODS

We analyzed 118 patients with PD Hoehn-Yahr grade 1—3 using the following scales: the Unified Parkinson’s Disease Rating Scale (UPDRS), the Schwab and England Activities of Daily Living Scale (Sch&En), the Parkinson’s Disease Quality of Life Questionnaire-39 (PDQ-39), the Gastrointestinal Symptom Rating Scale (GSRS) including abdominal pain domain, the Glasgow Dyspepsia Severity Score (GDSS), the Mini-Mental State Examination (MMSE), the Beck Depression Inventory (BDI), the Spielberg’s State-Trait Anxiety Inventory (STAI-S and STAI-T), the Parkinson’s Disease Fatigue Scale (PFS-16), the Non-Motor Symptoms Questionnaire (NMSQ), the American Urological Association Symptom Score (AUA) and Body Mass Index (BMI).

RESULTS

Predominate mild-to-moderate abdominal pain (mean GSRS score 2.48, σ=1.696) was found in 62 (52.5%) patients. Pain syndrome did not depend on gender, age or BMI, intake and dose of dopaminergic drugs, duration of PD. Abdominal pain was associated with H&Y stage, total UPDRS and its subscales I, II, III and some other factors (swallowing, gait, falls, postural instability, posture and orthostasis), depression, anxiety, fatigue, NMSQ score, urological symptoms and all domains of the GSRS scale. Abdominal pain was more severe in patients with reflux, dyspepsia and constipation. Abdominal pain had negative impact on daily activities and quality of life (Sch&En and PDQ-39). According to stepwise linear multiple regression (R²=0.631), the following predictors of abdominal pain were revealed: dyspepsia (GSRS score), swallowing (UPDRS score), reflux (GSRS score) and AUA score.

CONCLUSION

Mild-to-moderate abdominal pain syndrome is widespread in patients with PD stage 1-3 and significantly reduces quality of life. Abdominal pain has a complex mechanism and depends on the following factors: stage of PD, severity of postural disorders, presence and intensity of affective and autonomic disorders. According to our data, predictors of pain in PD are dyspepsia, dysphagia, reflux and urinary disorders.

Keywords:

Parkinson’s disease

abdominal pain

dyspepsia

autonomic disorders

gastrointestinal dysfunction

Authors:

Pilipovich A.A.

Sechenov First Moscow State Medical University (Sechenov University)

ORCID: 0000-0001-7416-9050

Vorobeva O.V.

Chuvash state university named after I.N. Ulyanov

SPIN RSCI: 5084-1379
ORCID: 0000-0003-3259-3691

Makarov S.A.

Center for Surgical Treatment of Obesity and Metabolic Disorders — St. George Hospital

ORCID: 0000-0002-8423-8002

Received:

26.02.2023

Accepted:

27.03.2023

Close metadata

References:

Parkman HP, Wilson LA, Hasler WL, McCallum RW, Sarosiek I, Koch KL, Abell TL, Schey R, Kuo B, Snape WJ, Nguyen L, Farrugia G, Grover M, Clarke J, Miriel L, Tonascia J, Hamilton F, Pasricha PJ. Abdominal Pain in Patients with Gastroparesis: Associations with Gastroparesis Symptoms, Etiology of Gastroparesis, Gastric Emptying, Somatization, and Quality of Life. Dig Dis Sci. 2019;64(8):2242-2255. https://doi.org/10.1007/s10620-019-05522-9
Heetun ZS, Quigley EM. Gastroparesis and Parkinson’s disease: A systematic review. Parkinsonism Relat Disord. 2012;18:433-440. https://doi.org/10.1016/j.parkreldis.2011.12.004
Goetze O, Nikodem AB, Wiezcorek J, Banasch M, Przuntek H, Mueller T, Schmidt WE, Woitalla D. Predictors of gastric emptying in Parkinson’s disease. Neurogastroenterol Motil. 2006;18(5):369-375. https://doi.org/10.1111/j.1365-2982.2006.00780.x
Pfeiffer RF, Isaacson SH, Pahwa R. Clinical implications of gastric complications on levodopa treatment in Parkinson’s disease. Parkinsonism Relat Disord. 2020;76:63-71. https://doi.org/10.1016/j.parkreldis.2020.05.001
Siddiqui MF, Rast S, Lynn MJ, Auchus AP, Pfeiffer RF. Autonomic dysfunction in Parkinson’s disease: A comprehensive symptom survey. Parkinsonism Relat Disord. 2002;8:277-284. https://doi.org/10.1016/S1353-8020(01)00052-9
Soliman H, Coffin B, Gourcerol G. Gastroparesis in Parkinson Disease: Pathophysiology, and Clinical Management. Brain Sci. 2021;11:831. https://doi.org/10.3390/brainsci11070831
Doi H, Sakakibara R, Sato M, Masaka T, Kishi M, Tateno A, Tateno F, Tsuyusaki Y, Takahashi O. Plasma levodopa peak delay and impaired gastric emptying in Parkinson’s disease. J Neurol Sci. 2012;319:86-88. https://doi.org/10.1016/j.jns.2012.05.010
Rana AQ, Depradine J. Abdominal pain: A symptom of levodopa end of dose wearing off in Parkinson’s disease. West Indian Med J. 2011;60(2):223-224.
Kataoka H, Tonomura Y, Eura N, Terashima M, Kawahara M, Ueno S. Painful abdominal contractions in patients with Parkinson disease. J Clin Neurosci. 2012;19(4):624-627. https://doi.org/10.1016/j.jocn.2011.06.026
Nashatizadeh MM, Lyons KE, Pahwa R. A review of ropinirole prolonged release in Parkinson’s disease. Clin Interv Aging. 2009;4:179-186. https://doi.org/10.2147/cia.s3358
Gordin A, Kaakkola S, Teräväinen H. Clinical advantages of COMT inhibition with entacapone — a review. J Neural Transm (Vienna). 2004;111(10-11):1343-1363. https://doi.org/10.1007/s00702-004-0190-3
Pogarell O, Gasser T, van Hilten JJ, Spieker S, Pollentier S, Meier D, Oertel WH. Pramipexole in patients with Parkinson’s disease and marked drug resistant tremor: a randomised, double blind, placebo controlled multicentre study. J Neurol Neurosurg Psychiatry. 2002;72(6):713-720. https://doi.org/10.1136/jnnp.72.6.713
Woitalla D, Kassubek J, Timmermann L, Lauterbach T, Berkels R, Grieger F, Müller T. Reduction of gastrointestinal symptoms in Parkinson’s disease after a switch from oral therapy to rotigotine transdermal patch: A non-interventional prospective multicenter trial. Parkinsonism Relat Disord. 2015;21(3):199-204. https://doi.org/10.1016/j.parkreldis.2014.11.024
Block G, Liss C, Reines S, Irr J, Nibbelink D. Comparison of immediate-release and controlled release carbidopa/levodopa in Parkinson’s disease. A multicenter 5-year study. The CR First Study Group. Eur Neurol. 1997;37(1):23-27. https://doi.org/10.1159/000117399
Kamel WA, Al-Hashel JY. LCIG in treatment of non-motor symptoms in advanced Parkinson’s disease: Review of literature. Brain Behav. 2020;10(9):e01757. https://doi.org/10.1002/brb3.1757
Fernandez HH, Vanagunas A, Odin P, Espay AJ, Hauser RA, Standaert DG, Chatamra K, Benesh J, Pritchett Y, Hass SL, Lenz RA. Levodopa-carbidopa intestinal gel in advanced Parkinson’s disease open-label study: interim results. Parkinsonism Relat Disord. 2013;19(3):339-345. https://doi.org/10.1016/j.parkreldis.2012.11.020
Epstein M, Johnson DA, Hawes R, Schmulewitz N, Vanagunas AD, Gossen ER, Robieson WZ, Eaton S, Dubow J, Chatamra K, Benesh J. Long-Term PEG-J Tube Safety in Patients With Advanced Parkinson’s Disease. Clin Transl Gastroenterol. 2016;7(3):e159. https://doi.org/10.1038/ctg.2016.19
Lang AE, Rodriguez RL, Boyd JT, Chouinard S, Zadikoff C, Espay AJ, Slevin JT, Fernandez HH, Lew MF, Stein DA, Odin P, Fung VS, Klostermann F, Fasano A, Draganov PV, Schmulewitz N, Robieson WZ, Eaton S, Chatamra K, Benesh JA, Dubow J. Integrated safety of levodopa-carbidopa intestinal gel from prospective clinical trials. Mov Disord. 2016;31(4):538-546. https://doi.org/10.1002/mds.26485
Pilipovich AA, Vorob’eva OV, Makarov SA, Shindryaeva NN, Vorob’eva YD. Gastrointestinal Dysfunction Impact on Life Quality in a Cohort of Russian Patients with Parkinson’s Disease I—III H&Y Stage. Parkinsons Dis. 2022:1571801. https://doi.org/10.1155/2022/1571801
Lubomski M, Davis RL, Sue CM. Health-Related Quality of Life for Parkinson’s Disease Patients and Their Caregivers. J Mov Disord. 2021;14(1):42-52. https://doi.org/10.14802/jmd.20079
Salat-Foix D, Suchowersky O. The management of gastrointestinal symptoms in Parkinson’s disease. Expert Rev Neurother. 2012;12(2):239-248. https://doi.org/10.1586/ern.11.192
Gibb WR, Lees AJ. Relevance Lewy body pathogenesis of idiopathic disease. J Neurol Neurosurg Psychiatry. 1988;51:745-752. https://doi.org/10.1136/jnnp.51.6.745
Jenkinson C, Fitzpatrick R, Peto V, Greenhall R, Hyman N. The Parkinson’s Disease Questionnaire (PDQ-39): development and validation of a Parkinson’s disease summary index score. Age and Ageing. 1997;26(5):353-357. https://doi.org/10.1093/ageing/26.5.353
Hagell P, Nygren C. The 39 item Parkinson’s disease questionnaire (PDQ-39) revisited: implications for evidence based medicine. Journal of Neurology, Neurosurgery & Psychiatry. 2007;78(11):1191-1198. https://doi.org/10.1136/jnnp.2006.111161
Chaudhuri KR, Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, Brown RG, Koller W, Barone P, MacPhee G, Kelly L, Rabey M, MacMahon D, Thomas S, Ondo W, Rye D, Forbes A, Tluk S, Dhawan V, Bowron A, Williams AJ, Olanow CW. International multicenter pilot study of the first comprehensive self-completed nonmotor symptoms questionnaire for Parkinson’s disease: The NMSQuest study. Mov Disord. 2006;21(7):916-923. https://doi.org/10.1002/mds.20844
Testy i shkaly v nevrologii. Kadykov AS, Manvelov LS, eds. M.: MEDpress-inform; 2015;224. (In Russ.).
Brown RG, Dittner A, Findley L, Wessely SC. The Parkinson fatigue scale. Parkinsonism Relat Disord. 2005;11(1):49-55. https://doi.org/10.1016/j.parkreldis.2004.07.007
Dimenäs E, Carlsson G, Glise H, Israelsson B, Wiklund I. Relevance of norm values as part of the documentation of quality of life instruments for use in upper gastrointestinal disease. Scand J Gastroenterol Suppl. 1996;221:8-13. https://doi.org/10.3109/00365529609095544
Kulich KR, Madisch A, Pacini F, Piqué JM, Regula J, Van Rensburg CJ, Ujszászy L, Carlsson J, Halling K, Wiklund IK. Reliability and validity of the Gastrointestinal Symptom Rating Scale (GSRS) and Quality of Life in Reflux and Dyspepsia (QOLRAD) questionnaire in dyspepsia: A six-country study. Health Qual Life Outcomes. 2008;6:12. https://doi.org/10.1186/1477-7525-6-12
Novik AA, Ionova TI. Rukovodstvo po issledovaniyu kachestva zhizni v meditsine. M.: OLMA Media Grupp; 2007;320. (In Russ.).
El-omar E, Banerjee S, Wirz A, McColl KEL: The Glasgow Dyspepsia Severity Score — a tool for the global measurement of dyspepsia. Euro J Gastroenterol Hepatol. 1996;8:967-971. https://doi.org/10.1097/00042737-199610000-00006
Veldhuyzen van Zanten SJO. Assessment of outcome in dyspepsia: has progress been made? Gut. 2002;50:iv23-iv25. https://doi.org/10.1136/gut.50.suppl_4.iv23
O’Leary MP, Barry MJ, Fowler FJ Jr. Hard measures of subjective outcomes: validating symptom indexes in urology. J Urol. 1992;148(5):1546-1548; discussion 1564. https://doi.org/10.1016/s0022-5347(17)36965-3
Bolezni predstatel’noj zhelezy. Alyaeva YuG, ed. M.: GEOTAR-Media; 2009;240. (In Russ.). https://medknigaservis.ru/wp-content/uploads/2019/01/Q0008940.pdf
Lemack GE, Dewey RB Jr, Roehrborn CG, O’Suilleabhain PE, Zimmern PE. Questionnaire-based assessment of bladder dysfunction in patients with mild to moderate Parkinson’s disease. Urology. 2000;56(2):250-254. https://doi.org/10.1016/s0090-4295(00)00641-5
Sung HY, Park JW, Kim JS. The frequency and severity of gastrointestinal symptoms in patients with early Parkinson’s disease. J Mov Disord. 2014;7(1):7-12. https://doi.org/10.14802/jmd.14002.
Silverdale MA, Kobylecki C, Kass-Iliyya L, Martinez-Martin P, Lawton M, Cotterill S, Chaudhuri KR, Morris H, Baig F, Williams N, Hubbard L, Hu MT, Grosset DG; UK Parkinson’s Pain Study Collaboration. A detailed clinical study of pain in 1957 participants with early/moderate Parkinson’s disease. Parkinsonism Relat Disord. 2018;56:27-32. https://doi.org/10.1016/j.parkreldis.2018.06.001
Register of Medicines of Russia. Levodopum + Carbidopum. https://www.rlsnet.ru/active-substance/levodopa-karbidopa-553
Register of Medicines of Russia. Levodopum + Benserazidum. https://www.rlsnet.ru/active-substance/levodopa-benserazid-1972
Register of Medicines of Russia. Pronoran. https://www.rlsnet.ru/drugs/pronoran-11831
Register of Medicines of Russia. Mirapex. https://www.rlsnet.ru/drugs/mirapeks-9675
Register of Medicines of Russia. Amantadine. https://www.rlsnet.ru/drugs/amantadin-81554
Kataoka H, Kazuma S. Persistent intolerable abdominal pain in patients with Parkinson’s disease. Clinical Neurology and Neurosurgery. 2022;224:107558. https://doi.org/10.1016/j.clineuro.2022.107558
Burke AL, Mathias JL, Denson LA. Psychological functioning of people living with chronic pain: A meta-analytic review. Br J Clin Psychol. 2015;3:345-360. https://doi.org/10.1111/bjc.12078
Levin OS, Illarioshkin SN, Golubev VL. Ekstrapiramidnye sindromy. Rukovodstvo dlya vrachej. M.: MEDpress-inform; 2022;772. (In Russ.).
Buhmann C, Wrobel N, Grashorn W, Fruendt O, Wesemann K, Diedrich S, Bingel U. Pain in Parkinson disease: A cross-sectional survey of its prevalence, specifics, and therapy. J Neurol. 2017;264(4):758-769. https://doi.org/10.1007/s00415-017-8426-y
Fil A, Cano-de-la-Cuerda R, Muñoz-Hellín E, Vela L, Ramiro-González M, Fernández-de-Las-Peñas C. Pain in Parkinson disease: A review of the literature. Parkinsonism Relat Disord. 2013;19(3):285-294; discussion 285. https://doi.org/10.1016/j.parkreldis.2012.11.009
Makhnev SO, Levin OS. Clinical variants of pain syndromes in patients with Parkinson’s disease. S.S. Korsakov Journal of Neurology and Psychiatry. Special Issues. 2013;113(7-2):39-44. (In Russ.). https://www.mediasphera.ru/issues/zhurnal-nevrologii-i-psikhiatrii-im-s-s-korsakova-2/2013/7/031997-72982013724
Kurushina OV, Barulin AE, Gordeeva IE, Ansarov KhSh, Chernovolenko EP. Diagnosis and treatment of pain syndromes in Parkinson’s disease. Russkij meditsinskij zhurnal. 2016;25:1715-1717. (In Russ.). https://www.rmj.ru/articles/bolevoy_sindrom/Diagnostika_i_lechenie_bolevyh_sindromov_pri_bolezni_Parkinsona/
Georgescu D, Ancusa OE, Georgescu LA, Ionita I, Reisz D. Nonmotor gastrointestinal disorders in older patients with Parkinson’s disease: is there hope? Clin Interv Aging. 2016;11:1601-1608. https://doi.org/10.2147/CIA.S106284
Lubomski M, Davis RL, Sue CM. Gastrointestinal dysfunction in Parkinson’s disease. J Neurol. 2020;267(5):1377-1388. https://doi.org/10.1007/s00415-020-09723-5
Su A, Gandhy R, Barlow C, Triadafilopoulos G. Utility of the wireless motility capsule and lactulose breath testing in the evaluation of patients with Parkinson’s disease who present with functional gastrointestinal symptoms. BMJ Open Gastroenterol. 2017;4(1):e000132. https://doi.org/10.1136/bmjgast-2017-000132
Bogdanov RR, Matyuk YuV, Bogdanov AR, Derbeneva SA, Zaletova TS. The spectrum of gastrointestinal motor dysfunction in patients with early stages of Pparkinson’s disease and efficiency of their dietary correction. Experimental and Clinical Gastroenterology. 2018;158(10):27-33. (In Russ.). https://doi.org/10.31146/1682-8658-ecg-158-10-27-33
Yu D, Ramsey FV, Norton WF, Norton N, Schneck S, Gaetano T, Parkman HP. The Burdens, Concerns, and Quality of Life of Patients with Gastroparesis. Dig Dis Sci. 2017;62(4):879-893. https://doi.org/10.1007/s10620-017-4456-7
DiBaise JK, Crowell MD, Driver-Dunckley E, Mehta SH, Hoffman-Snyder C, Lin T, Adler CH. Weight Loss in Parkinson’s Disease: No Evidence for Role of Small Intestinal Bacterial Overgrowth. J Parkinsons Dis. 2018;8(4):571-581. https://doi.org/10.3233/JPD-181386