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Year : 2023  |  Volume : 26  |  Issue : 1  |  Page : 39-43

Non-Motor symptoms burden in early stages of parkinson's disease

1 Department of Neurology, District Hospital Nankana Sahib, Lahore, Pakistan
2 Department of Neurology, Hussain Lakhani Hospital, Karachi, Pakistan
3 Department of Neurology, Central Park Teaching Hospital, Lahore, Pakistan
4 Department of Neurology, King Edward Medical University, Lahore, Pakistan

Date of Submission31-May-2022
Date of Decision06-Oct-2022
Date of Acceptance13-Oct-2022
Date of Web Publication22-Dec-2022

Correspondence Address:
Zomer Sardar
District Hospital Nankana Sahib Lahore
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/aian.aian_483_22

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Background: Non-motor symptoms (NMSs) in Parkinson's disease (PD) are often overlooked and thus can impede clinical management and significantly reduce the patient's quality of life. Aims: The study aimed to determine the burden of NMS in the early stages of PD. Material and Methods: A 1-year observational cross-sectional study was conducted at Mayo Hospital, Lahore, in 2019. The MDS-PD criteria were used to diagnose PD patients. The study included patients with Hoehn and Yahr (HY) stages 1–3. The frequency of NMSs was assessed using a non-motor symptom questionnaire (NMSQ), and the non-motor symptom scale (NMSS) score was derived using the NMSS. Results: A total of 100 PD patients were enrolled in the study. Sixty-three (63%) were males and 37 (37%) were females. Their age ranged between 45 and 75 years with a mean ± SD of 57.46 ± 8.46. At least one NMS was reported by 84% of patients, with neuropsychiatric symptoms (68%) preponderant, followed by a change in taste and smell (64%). The mean NMSS score is 46.22 ± 22.098 (median 44) with a range from 0 to 88, with the trend being increasing score with the advancing stage. Conclusion: The use of the NMSQ and NMSS tools should be standard in clinical practice to identify the severity of the disease and commence appropriate care.

Keywords: Hoehn and Yahr stage, non-motor symptoms, non-motor symptom questionnaire, non-motor symptom scale, Parkinson's disease

How to cite this article:
Sardar Z, Liaquat S, Yousaf Q, Bano S, Numan A. Non-Motor symptoms burden in early stages of parkinson's disease. Ann Indian Acad Neurol 2023;26:39-43

How to cite this URL:
Sardar Z, Liaquat S, Yousaf Q, Bano S, Numan A. Non-Motor symptoms burden in early stages of parkinson's disease. Ann Indian Acad Neurol [serial online] 2023 [cited 2023 Feb 1];26:39-43. Available from:

   Introduction Top

Non-motor symptoms (NMSs) in Parkinson's disease (PD) include neuropsychiatric disturbances and cardiovascular, urinary, and gastrointestinal symptoms among others.[1] The majority of PD patients experience gastrointestinal dysfunction (60–80%), followed by neuropsychiatric disturbances (84%), and sleep disorders in varying percentages (38–98%).[2] NMS can be assessed by a non-motor symptom questionnaire (NMSQ), and the frequency and severity of NMSs are determined by a non-motor symptom scale (NMSS) score.[3] Both are validated tools for the assessment of the NMS in PD.[3] The unified PD rating scale (UPDRS) is a tool that not only assesses non-motor and motor symptoms but also evaluates complications with therapy and the disease's impact on the activities of daily life. However, the UPDRS is a lengthy tool and usually is used by a neurologist.

We aim to appraise the NMS burden in Hoehn and Yahr (HY) stages 1–3 of PD. Our secondary objective is to raise awareness among neurologists about the impact of NMSs on management.

   Materials and Methods Top

An observational cross-sectional study was conducted in the Department of Neurology, Mayo Hospital Lahore, Pakistan. The duration of this study was of 1 year, spanning from January 2019 to December 2019. A total of 100 patients who fulfilled the inclusion criteria were recruited after approval from the chairman of the Department of Neurology, Mayo Hospital, Lahore. Approval from the Ethics committee is obtained. Reference number 812/RC/KEMU.

Newly and previously diagnosed PD patients (treatment naïve or under treatment) between HY stages of 1–3 were included in the study. Patients were diagnosed with idiopathic PD using Movement Disorder Society – Parkinson's Disease criteria 2015 (MDS-PD) by a neurologist.[4] Patients were further classified in stages by modified HY scale criteria.[5] Informed consent was obtained from all patients. Patients with Parkinson's plus (cortico-basilar degeneration, progressive supranuclear palsy, and multisystem atrophy) and who had cognitive impairment on mini-mental state examination (score <24), and those with HY stage >3 were excluded from the study.[6]

Demographic data (age and gender) of patients were recorded on pre-designed proforma. All patients were screened for NMS with a self-reported NMSQ (assisted by a resident, if necessary).[3] If any symptom was present, it was marked “yes” and marked “no” if the symptom was not experienced. Symptoms displayed on the NMSQ, their frequency, and severity were further evaluated by NMSS and the total NMSS score was noted. The NMSS score was obtained by interview. The score of each item in nine domains is determined by multiples of frequency (1–4) and severity (0–3).[7]

Data were analyzed using IBM SPSS version 22. The qualitative variables like gender, PD stage, and NMS were presented in frequency and percentages. The mean and standard deviation were calculated for quantitative variables like age and NMSS score. Post-stratification of data was carried out using Chi-square tests according to the NMSS score with age groups and gender. A P value ≤0.05 was taken as significant.

   Results Top

The total number of patients enrolled was 100. Their age ranged between 45 to 75 years with a mean ± SD of 57.46 ± 8.46. Fifty patients (50%) were in the age group of 50 to 65 years, whereas 21 (21%) were aged more than 65 years, and 29 (29%) were younger than 50 years. A preponderance of males was observed in our study. There were 63 (63%) males, and only 37 (37%) were females [Table 1].
Table 1: Sample characteristics [n=100]

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PD severity as evaluated by the modified HY scale, showing most of the patients in stage 2 and stage 2.5 (27% each), followed by stage 1, stage 1.5, and stage 3 with 19 (19%), 18 (18%), and 9 (9%) patients, respectively [Figure 1].
Figure 1: PD modified HY stage of sample [n = 100]

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Although the type of NMSs experienced by our sample was quite variable, 84% (n = 84) of patients, out of 100 PD patients screened, were reported to have at least one of the 23 symptoms.

Neuropsychiatric symptoms (mood/cognition domain) were preponderant in our study with 68% (n = 68) of patients reporting feeling worried for no apparent reason (anxiety). Depressive symptoms were present in 60 (60%), whereas 52 (52%) patients complained of flat mood without normal highs and lows (apathy).

The second most frequent symptom experienced was a change in taste/smell (64%) followed by lightheadedness or fainting on standing from sitting or lying position in 63 (63%) patients. In the sleep/fatigue domain, fatigue or lack of energy (not slowness) was present in 59 (59%) patients, followed by insomnia, excessive daytime sleepiness, and restless leg syndrome in 50%, 49%, and 48%, respectively.

Problems with memory and sustaining concentration were described by 42% and 46% of patients respectively. Sixty-one percent of patients suffered from constipation. Urinary symptoms were reported by 63% of patients. The frequency of NMSs according to NMSQ is listed in [Table 2].
Table 2: Frequency of NMSs in early stages of PD [n=100]

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The mean NMSS score is 46.22 ± 22.098 (median 44) with a range from 0 to 88 [Figure 2].
Figure 2: Histogram NMSS score

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The mean NMSS scores were 29.79 ± 16.69 in stage 1, 43.06 ± 23.52 in stage 1.5, 48.26 ± 15.54 in stage 2, 44.89 ± 18.09 in stage 2.5, and 85.11 ± 2.47 in stage 3 [Table 3]. Stratified analysis of the NMSS score with gender (P: 0.53) and age groups (P: 0.97) demonstrated no significant association.
Table 3: Mean NMSS score in HY stages 1-3

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   Discussion Top

NMSs are frequent in early PD and reflect multisystem involvement and heterogeneity of the disease.[8] It is increasingly recognized that a NMS is as debilitating as motor symptoms and is frequently under-appreciated in clinical practice.[9] Missed or delayed diagnosis of NMS in the early stages of PD may have implications on patient care and management and has been shown to negatively impact the quality of life.[9],[10],[11],[12]

The NMSQ is a self-reported screening questionnaire to flag patients in busy clinics.[4] The NMSS was developed and validated in 2007 to simply and comprehensively assess the frequency and severity to determine the burden of the NMS.[5] NMSS is translated into many languages, but its translation to Urdu does not exist yet.

The observed prevalence of NMS in our study was slightly higher in males than females with a mean age and standard deviation of 57.6 + 8.45 years. The mean age of the patients in other studies is reported to be higher than what we observed in our study. A cross-sectional study by Ojo OO et al. evaluated the NMS burden in PD in a Nigerian population. In their study, the mean age in a population of 825 was 63.7 ± 10.1 years.[6] Another study by Gökçal E et al.[7] also had a mean age of 65.22 ± 10.7 (range: 34–85) with male predominance.

Neuropsychiatric symptoms were dominating our study. Anxiety and depression were reported in 68% and 60% of patients, respectively. A change in taste/smell was the second most common symptom experienced by 64% of subjects. Lightheadedness/fainting and constipation were experienced by 64% and 61% of subjects in the NMSQ, respectively. Lightheadedness was observed in 69% in a study by Karri et al.[13] We observed that 84% of our patients reported at least one NMS in the screening questionnaire, which is consistent with a study carried out in Russia. They also concluded that more than 80% of subjects experienced at least one NMS. In the above study, sleep disturbances followed by psychiatric complaints predominated in HY stages 1–2. Psychiatric symptoms were experienced by a majority in stages 3–5.[12] Similarly, in the PRIAMO study, cognitive and psychiatric symptoms predominated in HY stages 1.5–3.[14] Our study showed the same trend of frequent neuropsychiatric disturbances in the early stages of the disease.[12],[14]

The mounting evidence on NMSs suggests that the NMS burden increases with the advancement of the disease.[15],[16] The majority of our cases were in HY stages 2 and 2.5, and NMS predominated in HY stages 2.5 and 3. Our results also demonstrated that the NMSS rose 4–5 times with the progression of the disease stage (the NMSS in stage 1 was 29.79 ± 16.69, and in stage 3, it was 85.11 ± 2.47), similar to the study by Chaudhuri K et al.[15]

In earlier studies, the burden of NMSS was graded into levels: 0 (none, score 0), 1 (mild, score 1–20), 2 (moderate, score 21–40), 3 (severe, score 41–70), and 4 (very severe, score ≥71).[17] According to this grading system of NMSS burden, our subjects with HY stage 1 disease fall into level 2 (moderate burden) and patients with stage 3 into level 4 (very severe). The burden of NMS in our population in the early stages of the disease is conspicuously shown to be high, which is somewhat similar to previous studies.[15],[17] A validation study, the Italian version of NMSS, 2017, by Cova et al.,[18] reported that the median of the HY stage was 2 and the mean NMSS score was 39.8 (0-154). In contrast, the overall mean NMSS score in our sample was slightly higher than what was observed in the Italian study (46.22 ± 22.09). The NMSS score in the Taiwanese population is rather contrasting. The mean NMS severity score (NMSSI) in one Taiwanese study was 39.1 ± 34.9 in males and 32.8 ± 33.9 in females.[19] Another study by Martinez-Martin et al.[20] reported a NMSSI of 47.6 ± 40.1 in males and 55.1 ± 43.4 in female cases.

According to Picillo M et al., male patients experienced more severe NMSs in contrast to females.[21] Chen et al.[16] also observed sex differences in some of the domains of NMSS (attention/memory, urinary, and miscellaneous domains). In contrast, no sex differences in NMSS were observed in a Chinese study.[22] Males exhibited a higher number of NMSs compared to females in our study. The determination of sex differences in the NMSS score in our population was not determined as this was not the scope of this study. However, further study can be carried out to elucidate the gender differences among our population.

Furthermore, NMS has also demonstrated an association with motor fluctuations/complications in studies. Chaudhuri K et al.[15] group observed a positive association between NMS burden, stages of the disease, and the quality of life. According to Santos-García et al.,[23] the NMS score was found to be higher in patients who presented with motor fluctuations.

To the best of our knowledge, this is the first study in Pakistan in which NMSS burden has been determined in our populace of PD patients in HY stages 1–3. From this study, we report two important findings: first, NMS burden is not uncommon in the early stages of the disease, and second, the NMSS score increases with the advancement of the disease.

   Conclusion Top

NMS detection and management can help patients and their caregivers feel better, and it can also contribute to a reduction in institutional load. Screening for NMSs should thus be emphasized in clinical practice. We also propose that Urdu translation of NMSS by experts according to international standards should be carried out to accurately and effectively estimate the burden of NMSS scores in our population.


This study has several limitations. Firstly, the UPDRS score was not included in the study. Secondly, other tools for the validation of NMSs were not used. Furthermore, the NMSS burden was not determined in treated and treatment naïve patients separately.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

   References Top

Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P. Parkinson's disease: The non-motor issues. Parkinsonism Relat Disord 2011;17:717-23.  Back to cited text no. 1
Kumaresan M, Khan S. Spectrum of non-motor symptoms in Parkinson's disease. Cureus 2021;13:e13275.  Back to cited text no. 2
Carod-Artal FJ, Martinez-Martin P. Independent validation of the non-motor symptoms scale for Parkinson's disease in Brazilian patients. Parkinsonism Relat Disord 2013;19:115-9.  Back to cited text no. 3
Chaudhuri KR, Martinez-Martin P, Schapira AH, Stocchi F, Sethi K, Odin P, et al. International multicenter pilot study of the first comprehensive self-completed nonmotor symptoms questionnaire for Parkinson's disease: The NMSQuest study. Mov Disord 2006;21:916-23.  Back to cited text no. 4
Martinez-Martin P, Chaudhuri KR, Rojo-Abuin JM, Rodriguez-Blazquez C, Alvarez-Sanchez M, Arakaki T, et al. Assessing the non-motor symptoms of Parkinson's disease: MDS-UPDRS and NMS Scale. Eur J Neurol 2015;22:37-43.  Back to cited text no. 5
Ojo OO, Wahab KW, Bello AH, Abubakar SA, Ekeh BC, Otubogun FM, et al. A cross-sectional comprehensive assessment of the profile and burden of non-motor symptoms in relation to motor phenotype in the Nigeria Parkinson Disease Registry Cohort. Mov Disord Clin Pract 2021;8:1206-15.  Back to cited text no. 6
Gökçal E, Gür VE, Selvitop R, Babacan Yildiz G, Asil T. Motor and non-motor symptoms in Parkinson's disease: Effects on quality of life. Noro Psikiyatr Ars 2017;54:143-8.  Back to cited text no. 7
Bonnet AM, Jutras MF, Czernecki V, Corvol JC, Vidailhet M. Nonmotor symptoms in Parkinson's disease in 2012: Relevant clinical aspects. Parkinsons Dis 2012;2012:198316. doi: 10.1155/2012/198316.  Back to cited text no. 8
D'Iorio A, Vitale C, Piscopo F, Baiano C, Falanga AP, Longo K, et al. Impact of anxiety, apathy and reduced functional autonomy on perceived quality of life in Parkinson's disease. Parkinsonism Relat Disord 2017;43:114-7.  Back to cited text no. 9
Chaudhuri KR, Healy DG, Schapira AH, National Institute for Clinical Excellence. Non-motor symptoms of Parkinson's disease: Diagnosis and management. Lancet Neurol 2006;5:235-45.  Back to cited text no. 10
Marinus J, Zhu K, Marras C, Aarsland D, van Hilten JJ. Risk factors for non-motor symptoms in Parkinson's disease. Lancet Neurol 2018;17:559-68.  Back to cited text no. 11
Fernandes M, Pierantozzi M, Stefani A, Cattaneo C, Bonizzoni EA, Cerroni R, et al. Frequency of non-motor symptoms in Parkinson's patients with motor fluctuations. Front Neurol 2021;12:678373. doi: 10.3389/fneur.2021.678373.  Back to cited text no. 12
Karri M, Ramasamy B, Kalidoss R. Prevalence of non-motor symptoms in Parkinson's disease and its impact on quality of life in tertiary care center in India. Ann Indian Acad Neurol 2020;23:270-4.  Back to cited text no. 13
  [Full text]  
Barone P, Antonini A, Colosimo C, Marconi R, Morgante L, Avarello TP, et al. The PRIAMO study: A multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson's disease. Mov Disord 2009;24:1641-9.  Back to cited text no. 14
Ray Chaudhuri K, Antonini A, Robieson WZ, Sanchez-Soliño O, Bergmann L, Poewe W, et al. Burden of non-motor symptoms in Parkinson's disease patients predicts improvement in quality of life during treatment with levodopa-carbidopa intestinal gel. Eur J Neurol 2019;26:581-e43.  Back to cited text no. 15
Chen YC, Chen RS, Weng YH, Huang YZ, Chen CC, Hung J, et al. The severity progression of non-motor symptoms in Parkinson's disease: A 6-year longitudinal study in Taiwanese patients. Sci Rep 2021;11:1-9. doi: 10.1038/s41598-021-94255-9.  Back to cited text no. 16
Ray Chaudhuri K, Rojo JM, Schapira AH, Brooks DJ, Stocchi F, Odin P, et al. A proposal for a comprehensive grading of Parkinson's disease severity combining motor and non-motor assessments: Meeting an unmet need. PLoS One 2013;8:e57221. doi: 10.1371/journal.pone.0057221.  Back to cited text no. 17
Cova I, Di Battista ME, Vanacore N, Papi CP, Alampi G, Rubino A, et al. Validation of the Italian version of the non motor symptoms scale for Parkinson's disease. Parkinsonism Relat Disord 2017;34:38-42.  Back to cited text no. 18
Chen YC, Huang YZ, Weng YH, Chen CC, Hung J, Lin YY, et al. Nonmotor symptoms of 820 Taiwanese patients with Parkinson's disease: An exploratory-comparative study. J Neurol 2020;267:1499-507.  Back to cited text no. 19
Martinez-Martin P, Falup Pecurariu C, Odin P, van Hilten JJ, Antonini A, Rojo-Abuin JM, et al. Gender-related differences in the burden of non-motor symptoms in Parkinson's disease. J Neurol 2012;259:1639-47.  Back to cited text no. 20
Picillo M, Erro R, Amboni M, Longo K, Vitale C, Moccia M, et al. Gender differences in non-motor symptoms in early Parkinson's disease: A 2-years follow-up study on previously untreated patients. Parkinsonism Relat Disord 2014;20:850-4.  Back to cited text no. 21
Song Y, Gu Z, An J, Chan P, Chinese Parkinson Study Group. Gender differences on motor and non-motor symptoms of de novo patients with early Parkinson's disease. Neurol Sci 2014;35:1991-6.  Back to cited text no. 22
Santos-García D, de Deus Fonticoba T, Suárez Castro E, Aneiros Díaz A, McAfee D, Catalán MJ, et al. Non-motor symptom burden is strongly correlated to motor complications in patients with Parkinson's disease. Eur J Neurol 2020;27:1210-23.  Back to cited text no. 23


  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3]


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