Parkinson's Disease Sleep Scale-2: The Brazilian Version's Cross-cultural Adaptation and Validation

Abstract

Objective To translate, cross-culturally adapt, and validate the Brazilian version of the Parkinson's Disease Sleep Scale-2 (PDSS-2/BR).

Methods This cross-sectional study addressed 80 patients with PD, and it was organized into two phases: 1) Translation and cross-cultural adaptation, which included 30 individuals in the scale's pretest stage and 2) Validation, when 50 individuals were assessed by the PDSS-2/BR, Pittsburgh Sleep Quality Index (PSQI), Parkinson's Disease Questionnaire-39 (PDQ-39), MDS-Unified Parkinson's Disease Rating Scale (MDS-UPDRS), and Hoehn and Yahr rating scale (HY); the PDSS-2/BR was retested 7 days later. The significance level was set at 5%.

Results The participants rated the PDSS-2/BR as having more than 90% comprehension. It also showed good reliability (Cronbach's alpha = 0.782) and excellent test–retest reliability (ICC_interrater = 0.901; p = 0.570; ICC_intrarater = 0.905; p = 0.116). Additionally, the scale showed good precision, with low standard error of measurement (SEM_inter = 1.040; SEM_intra = 0.908), and moderate to strong correlation with the PSQI, MDS-UPDRS, and PDQ-39 scales (rho = 0.46–0.74); only the HY scale showed no correlation.

Discussion The PDSS-2/BR is a reliable, precise, and valid instrument for evaluating sleep among Brazilian individuals with PD. Hence, it is expected to help researchers and clinicians improve the investigation of these symptoms, promoting early and assertive diagnoses and guiding the treatment and clinical management of this population.

Keywords

Parkinson disease - sleep - sleep quality

Introduction

Sleep disorders are highly prevalent in Parkinson's disease (PD), affecting 60 to 98% of individuals.[1] [2] Such disorders can emerge in the disease's prodromal phase and increase in frequency and severity as PD progresses.[2] They manifest mainly as nocturnal akinesia, rapid eye movement (REM) sleep behavior disorder, insomnia, sleep fragmentation, restless legs syndrome, excessive daytime sleepiness, obstructive sleep apnea, vivid dreams, hallucinations, and nocturia.[2] [3] They present a multifactorial etiology due to the involvement of non-dopaminergic pathways related to sleep (noradrenergic, cholinergic, and serotonergic), associated with other factors such as the typical aging process, motor dysfunction, dopaminergic therapy, depression, and antidepressant medications.[1] [4]

Even though non-motor symptoms, like sleep disorders, severely impact the progression and severity of the disease, compared to motor symptoms, they are much less frequently studied. Furthermore, the clinical management of these symptoms is challenging, worsening patients' cognitive status and motor symptoms, compromising their independence in performing activities of daily living and, consequently, their quality of life.[2] [5] [6]

Despite their clinical importance, one potential reason why sleep disorders are often neglected and underreported[2] is that the gold standard method (polysomnography) used to assess it is an exam not widely accessible to the population due to its logistics and high costs.[7] [8] In this context, actigraphy is another instrument used to objectively evaluate sleep patterns. This equipment consists of a portable accelerometer with sensors capable of detecting movement and light, resulting in information about an individual's sleep–wake cycle.[8] [9] However, even though it is a method validated for the PD population and is economically much more accessible than polysomnography, its use in clinical practice may be limited due to unavailability, need for specific training, and software installation.[8] [9] Therefore, subjective assessments using scales are vital to screen such disorders, considering that low-cost and easy-to-apply instruments can support researchers and clinicians in their professional practice.[7] [8] [10]

For this reason, Hogl and collaborators[9] conducted a task force to identify the best scales to assess the sleep of individuals with PD. Only six scales met the recommendation criteria: the PD Sleep Scale (PDSS), Pittsburgh Sleep Quality Index (PSQI), SCOPA-sleep (SCOPA), Epworth Sleepiness Scale (ESS), Inappropriate Sleep Composite Score (ISCS), and the Stanford Sleepiness Scale (SSS); though, only the PDSS and SCOPA-sleep are specific scales to assess sleep in PD.

Additionally, to date, only the PSQI, ESS, and PDSS-1 scales have been translated for the Brazilian population. Sleep disorders in PD are very specific, and there are few valid and reliable instruments to assess such disorders in this population. In Brazil, the PDSS-1 is the only instrument specifically designed to assess sleep quality in individuals with PD.[11] However, as its first version did not address daytime sleepiness, obstructive sleep apnea, restless legs syndrome, or REM sleep disorders, it was updated in 2011.[10] Hence, its current version (PDSS-2) includes six modified questions, and the response format changed from a visual analog scale to a Likert scale to facilitate understanding. The PDSS-2 consists of 15 questions rated according to five categories ranging from 0 (never) to 4 (very frequent). Its total score ranges from 0 (no disturbance) to 60 (maximum nighttime disturbance).[10]

Thus, considering these important adjustments and improvements in the screening of sleep disorders in this population, translating and validating the PDSS-2 for Brazil is needed to obtain more accurate assessments and contribute to research and the improvement of the therapeutic management of specific sleep disorders. This study aimed to translate, culturally adapt, and validate the Brazilian Portuguese version of this scale PDSS-2.

Methods

Design, Location, and Setting

This observational, cross-sectional study was performed from April 2022 to May 2023 in a single outpatient clinic specializing in PD in Londrina, PR, Brazil. The patients cared for by the Neurofunctional Physiotherapy Research Group (GPFIN) were invited and consecutively recruited through telephone calls. The Institutional Review Board at the State University of Londrina (Approval No. 5.271.985) approved this study. All participants received clarification regarding objectives and procedures, and those who voluntarily agreed to participate signed informed consent forms.

A convenience sample comprised 80 individuals diagnosed with idiopathic PD. As recommended by Beaton et al.,[12] 30 participants were assessed in phase 1 (cross-cultural adaptation), and, according to Terwee et al.,[13] 50 participants were included in phase 2 (reliability and validity).

Subjects

The participants were recruited according to the following criteria: 1) having a diagnosis of idiopathic PD, according to the United Kingdom's Parkinson's Disease Society Brain Bank Criteria.[14] 2) being Brazilian and able to communicate in Portuguese; 3) older than 45 years; 4) classified at I to IV stages, according to the modified Hoehn and Yahr disability scale (HY);[15] 5) having experienced no recent changes in antiparkinsonian medication (6 weeks); 6) having no cognitive impairments, and scoring equal to the cut-off point for the Brazilian population ( ≥ 21 for the illiterate; ≥ 23 for those who attended up to middle school; and ≥ 24 for those who completed high school) or higher on the Mini-Mental State Examination (MMSE).[16]

Exclusion criteria include other types of Parkinsonism, associated neurological, vestibular, cardiovascular, or musculoskeletal diseases, as well as visual or auditory impairments that could affect motor performance and comprehension during interviews. Individuals who missed the retest interview or whose medication changed over the data collection were considered losses.

Assessment Tools

The instruments include the PDSS-2, designed to assess sleep in PD during the previous week. It contains three domains and 15 items, distributed as follows: 1) motor symptoms at night (items 4, 5, 6, 12, and 13); 2) PD symptoms at night (items 7, 9, 10, 11, and 15); and 3) disturbed sleep (items 1, 2, 3, 8, and 14). The total score ranges from 0 to 60; the higher the score, the worse one's sleep perception.

The PSQI,[17] MMSE,[16] Parkinson's disease questionnaire-39 (PDQ-39)[18]; MDS-Unified Parkinson's Disease Rating Scale (MDS-UPDRS),[19] and HY[15] were also adopted in this study.

Assessment Procedures

Interviews were held with patients, and the following data were collected: age, gender, years of schooling, occupation, disease duration, body mass index (BMI), and levodopa equivalent daily dose (LEDD). The participants were included either in phase 1 or 2, according to the sequence in which they were recruited. They were instructed not to change their sleeping habits, medications, or eating habits during the study. They were all assessed at the same time of the day, in the “on” phase of antiparkinsonian medication (approximately 1 hour after medication intake).

Phase 1: Cross-Cultural Adaptation of Parkinson's Disease Sleep Scale-2

The procedures used in the PDSS-2 cross-cultural adaptation followed the methodology recommended by Beaton et al.[12] The process (stages I–VI) is described in [Figure 1]. The MAPI research trust (https://eprovide.mapi-trust.org), managing the copyright, kindly authorized the scale's cross-cultural adaptation to obtain the Brazilian version.

Fig. 1 Cross-cultural process of PDSS-2/BR. Adapted from Beaton et al.[12]

Additionally, an expert committee performed the content validity, verifying the conceptual, cultural, idiomatic, and semantic equivalences between the original and translated versions.[12] [20]

Finally, 30 PD patients were interviewed in the final step of the adaptation process to verify their understanding of the items in the pretest version of the PDSS-2/BR. All subjects completed the questionnaire and were again interviewed to probe what they thought each item and the corresponding answer meant. This stage is critical to ensure the scale is adequately translated and adapted for the specific population to obtain its final version ([Fig. 2]).

Fig. 2 Brazilian version of PDSS-2. For permission to use PDSS-2, please contact: [e-mail].

Phase 2: Assessment of Psychometric Properties

In this phase, 50 patients with PD were assessed in three steps. First, the following questionnaires were applied: a form addressing demographic and clinical data, the MDS-Unified Parkinson's Disease Rating Scale (MDS-UPDRS),[19] the HY),[15] and MMSE.[16] Next, the Pittsburgh Sleep Quality Index (PSQI)[17] and Parkinson's Disease Questionnaire-39 (PDQ-39)[18] were applied, followed by the PDSS-2/BR being administered twice by two independent researchers; there was a 60-minute interval between assessments to check for interrater reliability. Finally, the same researcher who performed the first assessment (intrarater reliability analysis) applied the PDSS-2/BR 7 days later.

Statistical Analyses

The patients' demographic data and clinical characteristics are presented with descriptive statistics. Data are described in means and standard deviation or medians and quartiles according to data distribution, verified by the Shapiro-Wilk test. The analysis was performed using the IBM SPSS Statistics for Windows (IBM Corp., Armonk, NY, USA), version 27.0. The significance level was set at 5%. Floor and ceiling effects were considered in the score distribution when assessing acceptability. Floor or ceiling effects occur when more than 15% of respondents score the minimum or maximum possible score in the PDSS-2/BR, respectively.[13]

Reliability

The reliability of the PDSS-2/BR was assessed by internal consistency and test-retest-reliability.[10] The Cronbach's alpha coefficient was used to examine the internal consistency of items and was analyzed by the measure of the average correlations among all items.[21] A Cronbach's alpha > 0.7039 is considered satisfactory.[22] [23]

The intraclass correlation coefficient (ICC) in a two-way random effects model was used to assess the test-retest reliability. The PDSS-2/BR was applied 1 hour (interrater reliability) and 7 days (intrarater reliability) after the first application.[23] Results below 0.40 indicate poor clinical significance; between 0.40 and 0.59 fair; between 0.60 and 0.74 good; and 0.75 to 1.00 excellent clinical significance.[24] The standard error of measurement (SEM), calculated as SEM = SDp*√(1-ICC), was used to verify the precision of PDSS-2/BR. The lower the SEM, the more reliable the test, as it should be less than half of the standard deviation (SDp).[23]

Validity

An expert committee verified the PDSS-2/BR's content and face validity. Convergent validity was determined considering the PSQI and the sleep-related items of the MDS-UPDRS scores (UPDRS_Sleep, items 1.7 concern sleep problems and 1.8 daytime sleepiness). Additionally, divergent validity was assessed considering the correlation with indirect constructs related to nocturnal sleep disturbances, such as PDQ-39 total score (measuring the PD-specific health status and quality of life), and symptoms and disability using MDS-UPDRS and HY.[10] Validity between the PDSS-2/BR total score and the other measures was determined using the Pearson's (rs) or Spearman's (rho) correlation coefficients. Correlations below 0.30 were considered weak evidence of validity, between 0.30 and 0.59 were moderate, and above 0.59 were strong.[10]

Furthermore, internal validity was performed using the Pearson's correlation between the PDSS-2/BR domains (motor symptoms at night, PD symptoms at night, and disturbed sleep). The internal validity of an instrument is considered adequate when the correlation between its domains is neither too low (rs < 0.30) nor too high (rs > 0.70).[23] [25]

Results

In total, 80 patients were included in this study, of which 51 (63.75%) were men. The mean age of the participants was 68.15 ± 10.08. The average schooling was 12.78 ± 5.63 years, and the disease duration was 6.86 ± 5.81 years.

Phase 1: Cross-Cultural Adaptation of Parkinson's Disease Sleep Scale-2

The translation and back-translation versions were equivalent to the original PDSS-2; equivalence was achieved in all aspects. The scale was applied to 30 patients with PD in the pre-testing, and all items were rated as having more than 90% comprehension. Therefore, the scale can be applied to the Brazilian population of individuals with PD,[12] as its adapted version kept the same number of items allocated in the same domains, with the format and response alternatives as the original version.

Phase 2: Assessment of Psychometric Properties

Fifty individuals who did not participate in Phase 1 were included in Phase 2, and their sociodemographic and clinical characteristics are presented in [Table 1]. The PDSS-2/BR's mean score was 15.78 ± 10.30 (ranging from 0–60). There were no ceiling (0% in the first interview and retest) or floor effects (2% - first interview, 4% - retest).

Table 1 Characterization of the sample in phase 2.

Variables	Sample (n = 50)
Sex (M/F)	32 (64%)/18 (36%)
Age (years)	66.30 ± 9.52
Time since diagnosis (months)	66.00 (24.00–120.00)
LEDD (mg)	489.37 (340.50–901.25)
MMSE	28.00 (26.00–30.00)
Hoehn & Yahr	2.00 (2.00–2.50)
Schooling (years)	11.36 ± 4.21
PDSS-2/BR	15.78 ± 10.30
PSQI	7.72 ± 3.63
MDS-UPDRS I	10.50 (6.00–20.00)
MDS-UPDRS II	14.40 ± 7.71
MDS-UPDRS III	32.50 (21.00–42.00)
MDS-UPDRS IV	1.00 (0.00–6.00)
MDS- UPDRS (total)	63.86 ± 27.46

Abbreviations: F, female; LEDD, Levodopa equivalent daily dose; M, male; MMSE, Mini-Mental State Examination; PDQ-39, Parkinson's Disease Questionnaire-39; PDSS-2/BR, Parkinson's disease sleep scale-2 Brazilian version; PSQI, Pittsburgh sleep quality index. MDS-UPDRS: MDS-unified Parkinson's disease rating scale. Notes: In which MDS-UPDRS I: non-motor experiences of daily living, II: motor experiences of daily living, III: motor examination, and IV: motor complications. Data presented as n (%) or mean (SD).

Reliability

This study presents evidence of good reliability. The PDSS-2/BR obtained a Cronbach's alpha of 0.782 when all response items were scored. The ICC indicated excellent interrater (0.901, 95%CI: 0.832–0.942; F = 19.160; p < 0.001) and intrarater reliability (0.905, 95%CI: 0.838–0.945; F = 20.011; p < 0.001).

Good precision was found, as the SEM (interrater: 1.040; intrarater: 0.908) was lower than the criterion < 0.5 pooled SD_p (interrater: 1.653; intrarater: 1.474) which is considered satisfactory.[23] The analysis of Bland and Altman plots showed that the difference between the two assessments did not differ significantly from zero (interrater: p = 0.57; intrarater: p = 0.116) ([Fig. 3]). A high level of agreement was found in addition to a small mean intra- and interobserver differences ([Table 2]).

Fig. 3 Bland-Altmann plot shows the difference between the (A) inter- and (B) intrarater total scores of PDSS plotted against the average of the two measurements (mean). Three solid lines mark the differences' mean and 95% confidence interval.

Table 2 Test-retest reliability.

PDSS-2/BR	ICC	95% CI	SDp	SEM	Bland-Altman
					d	95%CI	SD	p
Interrater	0.901	0.832–0.942	3.307	1.040	-1.24	-10.07–7.59	4.50	0.570
Intrarater	0.905	0.838–0.945	2.948	0.908	0.92	-7.04–8.88	4.06	0.116

Abbreviations: CI, confidence interval; d, average of difference; ICC, intraclass correlation coefficient; PDSS-2/BR, Parkinson's disease sleep scale-2 Brazilian version; SD_p, standard deviation of participant scores; SEM, standard error of measurement. Notes: SD = √SStot/(n-1).

A subanalysis including only individuals over 60 years (n = 36) was performed to minimize potential age-related biases. As a result, adequate PDSS-2/BR reliability values, very close to those obtained when the entire sample was analyzed, were found: Cronbach's alpha = 0.793, excellent interrater reliability (ICC = 0.920, 95%CI: 0.849–0.958; F = 23.604; p < 0.001) and intrarater reliability (ICC = 0.930, 95%CI: 0.822–0.968; F = 34.986; p < 0.001).

Validity

There was good evidence concerning the construct validity between the PDSS-2/BR and PSQI, MDS-UPDRS, and PDQ-39. Additionally, strong correlations were found between PDSS-2/BR and PSQI (rs = 0.70; p < 0.001), UPDRS-Sleep (rho = 0.62; p < 0,001), MDS-UPDRS I (rho = 0.66; p < 0.001), MDS-UPDRS total (rs = 0.63; p < 0.001) and PDQ-39 (rs = 0.74; p < 0.001). The correlations between PDSS-2/BR and MDS-UPDRS II (rs = 0.53; p < 0.001), MDS-UPDRS III (rho = 0.47; p = 0.001) and MDS-UPDRS IV (rho = 0.49; p < 0.001) were moderate; and no correlations were found between PDSS-2/BR and HY (rho = 0.19; p = 0.190) or MEMM (rho = -0.19; p = 0.203).

The internal validity of the PDSS-2/BR subdomains was acceptable: motor versus PD symptoms at night (r_s = 0.520 p < 0.001); motor symptoms at night versus disturbed sleep (r_s = 0.446, p = 0.001); and PD symptoms at night versus disturbed sleep (r_s  = 0.524, p < 0.001).

Discussion

The PDSS-2/BR presented satisfactory quality, reliability, construction, and validity evidence for evaluating sleep perception in individuals with PD. A specific instrument, cross-culturally adapted and validated, is necessary to properly assess sleep patterns in this population. For this reason, translating and adapting it to Brazilian Portuguese is extremely important. To the best of our knowledge, the PDSS-2 has been validated in English,[10] Spanish,[23] Italian,[26] Korean,[27] Persian,[28] and Japanese,[29] thus far.

Cross-cultural Adaptation and Reliability of PDSS-2/BR

Different beliefs and cultural and behavioral differences exist everywhere, and these particularities must be considered in a cross-cultural adaptation process. In this sense, the translation and cross-cultural adaptation process in this study followed the guidelines recommended by Beaton et al.[12] As a result, the individuals with PD understood all the PDSS-2/BR items (> 90%), and the scale could be subjected to reliability and validation processes.[12] [30]

The PDSS-2/BR's total score did not show ceiling or floor effects. The scale's reliability was verified through internal consistency and test-retest reliability. Its Cronbach's alpha coefficient was 0.7838, higher than the obtained in the scale's original study (0.73),[10] which aligns with the findings of studies validating it (0.73–0.86).[10] [23] [26] [31]

Lower SEM (SEM_intra = 0.908; SEM_inter = 1.040) were found in this study compared to previous PDSS-2 validation studies, in which SEM ranged from 2.140 to 5.840[11] [23] [26]; these results indicate that PDSS-2/BR has high sensitivity (precision). Furthermore, the PDSS-2/BR test–retest reliability was excellent (ICC_intra = 0.905; ICC_inter = 0.901). Finally, the Bland-Altman analysis showed low individual variability, meaning the subjects provided similar answers to the inter- (after 1 hour) and intrarater (after 7 days), confirming that the PDSS2/BR is a questionnaire to which participants respond as expected.

Validity

Validity is related to the ability of an instrument to measure the construct it is designed for, with accuracy. There are three types of validity: content, criterion, and construct. During this study's translation and cross-cultural adaptation, an expert committee considered the scale to present content and face validity.

Similar to other validation studies addressing the PDSS-2,[10] [23] we did not assess criterion validity in this study due to the difficulty in using the gold standard instrument for sleep assessment, the polysomnography. In addition to cost restrictions, the participants would be required to spend the night in a different environment than usual. Polysomnography assesses objective aspects of an individual's sleep for just one night, while PDSS-2 assesses the individuals' perception of the quality of their sleep over the last week. Hence, there would be divergences between subjective and objective assessments, as they focus on different aspects of sleep.[7] Therefore, polysomnography or actigraphy is not mandatory for cross-cultural validation of an existing scale.[31]

Construct validity was used to validate the PDSS-2 in previous and current studies. It concerns the degree to which the scores obtained in a questionnaire are consistent with others measuring similar (convergent validity) or associated constructs (divergent validity).[20] The PSQI and UPDRS_Sleep were used to verify convergent validity, with strong and moderate correlations being found, respectively. Trenkwalder et al.[10] found a moderate level of association (r = 0.54) between the PDSS-2 and the medical outcome study's (MOS) sleep disturbance scale. As this last one has not yet been validated for the Brazilian population, it could not be used in this study. Hence, we chose the PSQI to test the psychometric properties of the PDSS-2/BR.[32] Even though the PSQI is a generic instrument to assess sleep patterns, it is considered one of the best scales for evaluating sleep in PD;[12] it was translated into Portuguese and used to validate the first version of the PDSS in the Brazilian population.[32]

Divergent validity was verified between PDSS-2/BR, MDS-UPDRS I-IV (motor and non-motor symptoms), and PDQ-39 (quality of life). A strong association was found between PDSS-2/BR and PDQ-39 and a moderate association with MDS-UPDRS, from I to IV and total. Unlike previous studies, that found a moderate correlation between PDSS-2/BR and HY, no correlation was found in this study.[10] [23] [26] Internal validity was good as the correlation between the PDSS-2/BR domains was within the recommended range; the correlation should not be too low (rs < 0.30) nor too high (rs > 0.70).[25] [31]

Clinical Relevance

The PDSS-2 was revised to meet several unmet needs in the previous version, such as restless legs syndrome, nocturnal akinesia, pain, and sleep apnea. Furthermore, the PDSS-1 is difficult to apply because of its visual analog scale, used by the participants to classify their perception of sleep; it was challenging for them to understand it and respond appropriately.[10] Therefore, validating the updated version into Brazilian Portuguese is a significant advancement, considering the negative impact of sleep disorders on the quality of life of individuals with PD.[5] [33] [34]

This study's limitations include a lack of a gold standard instrument (polysomnography) to provide information for criterion validation; our sample had a low prevalence of patients in advanced stages of PD (one patient with HY-4 and none with HY-5); and, finally, the recruited patients belong to an outpatient clinic specializing in the treatment of people with PD. One of this study's advantages is the subanalysis according to age, in which the PDSS-2/BR was found to maintain good reliability in assessing the sleep of older individuals, minimizing age bias, considering how aging might strengthen sleep disorders in this population.

Therefore, considering the impact of sleep disorders on the quality of life and independence of patients with PD, and how such disorders are still underestimated in clinical practice, the conclusion is that the Brazilian version of the PDSS-2 is a reliable instrument with satisfactory construct validity and precision. Hence, it is expected to help researchers and clinicians improve the investigation of these symptoms, promoting early and assertive diagnoses as well as guiding the treatment and clinical management of patients with PD.

Conflict of Interests

The authors have no conflict of interests to declare.

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Publication History

Received: 15 January 2024

Accepted: 26 August 2024

Article published online:
11 March 2025