Brazilian version of the Multidimensional Fatigue Inventory for Parkinson’s disease

Versão brasileira do Inventário Multidimensional de Fadiga na doença de Parkinson

Josiane Lopes Hayslenne Andressa Gonçalves de Oliveira Araújo Suhaila Mahmoud Smaili About the authors

Abstract

Introduction:

The multidimensional fatigue inventory (MFI) has not been applied in Brazilian Parkinson`s disease (PD) population due to the lack of validation.

Objective:

The aim of this study was to cross-culturally adapt, to validate, and investigate the psychometric properties of Brazilian version of the MFI in PD.

Method:

Idiopathic PD individuals (N = 90) were recruited. The MFI was translated into Brazilian Portuguese using established forward-backward translation procedures, and the psychometric properties were evaluated. All individuals were assessed by socio-clinical questionnaire, Mini-Mental State Examination (MMSE), Unified Parkinson’s Disease Rating Scale (MDS-UPDRS Part I-IV), Hoehn-Yahr disability scale (HY), hospital anxiety and depression scale (HADS), fatigue severity scale (FSS), Parkinson Fatigue Scale (PFS-16) and MFI-PD/ BR with retest of the MFI-PD/BR after seven days.

Results:

The adaptation phase kept the same items of original MFI-PD. No data missing, floor nor ceiling effects were found. The overall Cronbach's alpha coefficient for the 20 items was 0.81, ranging from 0.73 to 0.81 for each of the five subscales. Bland and Altman analysis showed no systematic differences between assessments. The intraclass correlation coefficient test-retest was higher or equal 0.70 (p < 0.01) for the MFI-PD/BR score, which was moderately correlated with the HADS, MDS-UPDRS score (motor examination, motor and non-motor experiences of daily living and motor complications), FSS and PFS-16. It was revealed the MFI-PD/ BR > 55 points as cut-off point to indicate fatigued subjects with accuracy of 0.84 (p < 0.001).

Conclusion:

The MFI-PD/BR can be considered a valid and reproducible instrument for assessing PD-related fatigue.

Keywords:
Parkinson Disease; Fatigue; Psychometrics

Resumo

Introdução:

O inventário multidimensional da fadiga (MFI) não tem sido administrado em indivíduos brasileiros com doença de Parkinson (DP) devido à falta de validação.

Objetivo:

Adaptar transculturalmente, validar e investigar as propriedades psicométricas da versão brasileira do MFI na DP.

Método:

Foram recrutados indivíduos com DP (N=90). O MFI foi traduzido para o português falado no Brasil usando procedimentos de tradução e retrotradução e as propriedades psicométricas foram avaliadas. Todos os indivíduos foram avaliados por meio de um questionário sócio-clínico, mini-exame do estado mental (MEEM), escala modificada de avaliação na DP (MDS-UPDRS Parte I-IV), escala de incapacidade de Hoehn-Yahr (HY), escala de ansiedade e depressão (HADS), escala de gravidade de fadiga (FSS), escala de fadiga da DP (PFS-16) e MFI-DP/ BR com reteste do MFI-PD/BR em sete dias.

Resultados:

A adaptação manteve os mesmos itens do instrumento original do MFI-PD. Nenhum dado perdido, efeito chão ou teto foram encontrados. O coeficiente alpha de Cronbach de todos os 20 itens foram 0.81, variando entre 0.73 a 0.81 entre as cinco subescalas. A análise de Bland-Altman não demonstrou nenhuma diferença sistemática entre as avaliações. O coeficiente de correlação intraclasse teste-reteste foi maior ou igual a 0.70 (p < 0.01) para os escores do MFI-DP/BR com correlações moderadas com HADS, MDS-UPDRS escore (exame físico, experiências motoras e não motoras de atividades de vida diária e complicações motoras), FSS e PFS-16. Foi revelado MFI-DP/ BR > 55 pontos como ponto de corte para indicar indivíduos com fadiga com acurácia de 0.84 (p < 0.001).

Conclusão:

O MFI-DP/BR pode ser considerado um instrumento válido e reprodutível para avaliar fadiga na DP.

Palavras-chave:
Doença de Parkinson; Fadiga; Psicometria

Introduction

Fatigue is a problem for up to 75% of Parkinson`s disease (PD) patients [11 Siciliano M, Trojano K, Santangelo G, De Micco R, Tedeschi G, Tessitore A. Fatigue in Parkinson's disease: a systematic review and meta-analysis. Mov Disord. 2018;33:1712-23., 22 Kluger BM, Garimella S, Garvan C. Minimal clinically important difference of the Modified Fatigue Impact Scale in Parkinson's disease. Parkinsonism Relat Disord. 2017;43:101-4.], and over half consider fatigue to be one of their 3 most disabling symptoms [33 Chou KL, Kotagal V, Bohnen N. Neuroimaging and clinical predictors of fatigue in Parkinson disease. Parkinsonism Relat Disord. 2016;23:45-9.]. It may manifest even present during premotor stages of PD [44 Stocchi F, Abbruzzese G, Ceravolo R, Cortelli P, D'Amelio M, De Pandis MF, et al. Prevalence of fatigue in Parkinson disease and its clinical correlates. Neurology. 2014;83(3):215-20.], and while most studies have found no significant association between fatigue and PD motor severity [55 Friedman JH, Brown RG, Comella C, Garber CE, Krupp LB, Lou JS, et al. Fatigue in Parkinson's disease: a review. Mov Disord. 2007;22(3):297-308.], other studies have reported significant correlations between increasing fatigue and increasing disease severity [11 Siciliano M, Trojano K, Santangelo G, De Micco R, Tedeschi G, Tessitore A. Fatigue in Parkinson's disease: a systematic review and meta-analysis. Mov Disord. 2018;33:1712-23., 33 Chou KL, Kotagal V, Bohnen N. Neuroimaging and clinical predictors of fatigue in Parkinson disease. Parkinsonism Relat Disord. 2016;23:45-9., 66 Kluger BM, Herlofson K, Chou KL, Lou JS, Goetz CG, Land AE, et al. Parkinson's disease-related fatigue: a case definition and recommendations for clinical research. Mov Disord. 2016;31(5):625-31.]. Fatigue negatively impacts on activities of daily living and quality of life in PD [44 Stocchi F, Abbruzzese G, Ceravolo R, Cortelli P, D'Amelio M, De Pandis MF, et al. Prevalence of fatigue in Parkinson disease and its clinical correlates. Neurology. 2014;83(3):215-20., 66 Kluger BM, Herlofson K, Chou KL, Lou JS, Goetz CG, Land AE, et al. Parkinson's disease-related fatigue: a case definition and recommendations for clinical research. Mov Disord. 2016;31(5):625-31.] and is commonly associated with other non-motor symptoms such as sleepiness, anxiety, and depression [33 Chou KL, Kotagal V, Bohnen N. Neuroimaging and clinical predictors of fatigue in Parkinson disease. Parkinsonism Relat Disord. 2016;23:45-9.].

The assessment of PD fatigue is not a easy task. It is a complex and highly subjective symptom with many uncertainties regarding its pathophysiology. One of the challenges is the lack of a widely accepted definition [77 Lou J, Kearns G, Oken B, Sexton G, Nutt J. Exacerbated physical fatigue and mental fatigue in Parkinson's disease. Mov Disord. 2001;16(2):190-6.] and with that, differentiating its many dimensions such as motor, mental and social [33 Chou KL, Kotagal V, Bohnen N. Neuroimaging and clinical predictors of fatigue in Parkinson disease. Parkinsonism Relat Disord. 2016;23:45-9., 88 Kluger BM, Krupp LB, Enoka RM. Fatigue and fatigability in neurologic illnesses: proposal for a unified taxonomy. Neurology. 2013; 80(4):409-16., 99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25.]. Fatigue usually refers to the difficulty initiating or sustaining voluntary activities [1010 Chaudhuri A, Behan P. Fatigue in neurological disorders. Lancet. 2004;363(9413): 978-88.]. Its multidimensionality is believed to result from a complex interplay between the underlying disease process, peripheral control systems, central control systems and environmental factors [33 Chou KL, Kotagal V, Bohnen N. Neuroimaging and clinical predictors of fatigue in Parkinson disease. Parkinsonism Relat Disord. 2016;23:45-9.]. This complexity may be reflected in the large number of instruments that are currently available to measure fatigue in patients with PD [1111 Elbers RY, Rietberg MB, van Wegen EE, Verhoef J, Kramer SF, Terwee CB, et al. Self-report fatigue questionnaires in multiple sclerosis, Parkinson's disease and stroke: a systematic review of measurement properties. Qual Life Res. 2012;21(6):925-44.].

Perceptions of fatigue are typically measured using self-reported scales of fatigue severity or impact [1212 Friedman JH, Alves G, Hagell P, Marinus J, Marsh L, Martinez-Martin P, et al. Fatigue rating scales critique and recommendations by the Movement Disorders Society task force on rating scales for Parkinson's disease. Mov Disord. 2010;25(7):805-22., 1313 Herlofson K, Kluger BM. Fatigue in Parkinson's disease. J Neurol Sci. 2017;374:38-41.]. The International Movement Disorders Society (IMDS) task force on fatigue rating scales reviewed all nine fatigue-specific rating instruments that had been used in previous PD studies [1313 Herlofson K, Kluger BM. Fatigue in Parkinson's disease. J Neurol Sci. 2017;374:38-41.]. Only three scales, the Fatigue Severity Scale (FSS) [1414 Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD. The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol. 1989;46(10):1121-3.], Parkinson Fatigue Scale (PFS-16) [1515 Brown RG, Dittner A, Findley L, Wessely SC. The Parkinson fatigue scale. Parkinsonism Relat Disord. 2005;11(1):49-55.], and Multidimensional Fatigue Inventory (MFI) [99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25.] were recommended for rating fatigue severity in PD.

MFI is a commonly used instrument to assess the multidimensional aspects of fatigue in PD patients [99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25.]. It is a self-report questionnaire that assesses general fatigue, physical fatigue, reduced activity, mental fatigue and reduced motivation. IMDS suggested the MFI as a screening instrument for fatigue and recommended the MFI for the assessment of fatigue severity in patients with PD [1212 Friedman JH, Alves G, Hagell P, Marinus J, Marsh L, Martinez-Martin P, et al. Fatigue rating scales critique and recommendations by the Movement Disorders Society task force on rating scales for Parkinson's disease. Mov Disord. 2010;25(7):805-22.]. In Brazil, FSS [1616 Valderramas S, Feres AC, Melo A. Reliability and validity study of a Brazilian-Portuguese version of the fatigue severity scale in Parkinson's disease patients. Arq Neuropsiquiatr. 2012;70(7):497-500.] and PFS-16 [1717 Kummer A, Scalzo P, Cardoso F, Teixeira AL. Evaluation of fatigue in Parkinson's disease using the Brazilian version of Parkinson's Fatigue Scale. Acta Neurol Scand. 2011;123(2):130-6.] have been widely used to assess PD fatigue. MFI provides a potential guide for PD fatigue assessment that can be used in research and clinical practice. Thus, this instrument is the possibility to complement the assessment of this symptom in other dimensions that are not assessment. However, it has limited Brazilian applicability due to the lack of a validated version.

Considering psychometric properties of design and administration that can satisfy the current standards for outcome measurements. From the possibility of applicability of MFI in Brazilian PD individuals, the aim of the present study was to cross-culturally adapt and investigate the psychometric properties of Brazilian version of the MFI in PD.

Method

Population and design

An observational cross-sectional study following the criteria proposed by Beaton et al. (2000) [1818 Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine. 2000;25(24):3186-91.] was carried out. Participants were recruited from the physical therapy outpatient clinic at the State University of Londrina. The study was approved by the Ethics Committee of the State University of Londrina, University Hospital (Opinion report No. 2.481.213). All participants voluntarily gave written informed consent.

The study comprised a convenience sample including 90 individuals diagnosed with idiopathic PD by a board certified neurologist specializing in movement disorders. The sample size was estimated in accordance with the criteria recommended for adaptation (20 subjects) and for validation study design (70 subjects) [1818 Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine. 2000;25(24):3186-91.].

Subjects

Individuals were recruited according to the following criteria: aged 50 years or older; diagnosis of idiopathic PD using the UK Brain Bank criteria (Hughes et al., 1993) [1919 Hughes AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathologic study of 100 cases of Parkinson's disease. Arch Neurol. 1993;50(2):140-8.]; Brazilian nationality; Hoehn and Yahr disability scale (HY) stage I - IV [2020 Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;,17(5):427-42.]; stable use of antiparkinsonian medication; able to walk independently without gait aids; score ≥ 24 on the Mini-Mental Status Examination (MMSE) [2121 Folstein MF, Folstein SE, McHugh PR. "Mini-Mental State". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189-98.].

Individuals were excluded if they: a) presenting other types of Parkinsonism or other associated neurological diseases, vestibular, cardiovascular, musculoskeletal, cognitive or comprehension disorders, visual or auditory impairment that could affect motor performance; b) under treatment other than drug therapy or had surgery for PD such as deep brain stimulation; or c) had participated in a physiotherapy program two months before starting the trial. Individuals who missed the second interview or whose medication changed over the course of the study were considered losses.

Instrument

The Multidimensional Fatigue Inventory (MFI) was originally developed and validated in the Dutch language in patients with cancer and patients with chronic fatigue syndrome [99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25.] and was translated and validated in English in patients with cancer [2222 Smets E, Garsen B, Cull A, De Haes J. Application of the multidimensional fatigue inventory (MFI-20) in cancer patients receiving radiotherapy. Br J Cancer 1996;73(2):241-45.]. The MFI is a self-report questionnaire that assesses the impact of fatigue and comprises five dimensions: general fatigue (GF), physical fatigue (PF), reduced activity (RA), mental fatigue (MF) and reduced motivation (RM). Each subscale contains four items, with two items formulated in a positive and two formulated in a negative direction. The addressed recall period is ‘lately’. All items are scored on a five-point Likert scale ranging from 1 (yes, that is true) to 5 (no, that is not true). The negative formulated items must be recoded before adding up scores. The obtainable score within each subscale ranges from 4 (absence of fatigue) to 20 (maximum fatigue) [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.].

Procedures

The subjects were assessed using a socio-clinical questionnaire, MMSE [2121 Folstein MF, Folstein SE, McHugh PR. "Mini-Mental State". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189-98.], Movement Disorder Society - Unified Parkinson’s Disease Rating Scale (MDS-UPDRS, Part I - IV) [2424 Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-Sponsored Revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): Scale Presentation and Clinimetric Testing Results. Mov Disord. 2008;23(15):2129-70.], HY [1919 Hughes AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathologic study of 100 cases of Parkinson's disease. Arch Neurol. 1993;50(2):140-8.] by same examiner. Following this, they were included either in phase 1 or phase 2 of the study, according to the sequence of recruitment. All assessments were performed in the subjects 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 the MFI-PD

The MFI was culturally adapted from English to Brazilian Portuguese language in accordance with the guidelines proposed by Beaton et al. [1818 Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine. 2000;25(24):3186-91.]. The translations were performed by two native Portuguese translators independently. The translations were synthesized into a single Portuguese version by the translators and a third person (a healthcare professional). After, this Portuguese version was back-translated into English independently by two American native translators. The backward translations were synthesized by the translators and compared with the MFI [99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25.]. The forward and backward translations were submitted to a bilingual expert committee (biostatistician, linguist, neurologists, psychologist and physiotherapist) to analyze the equivalences. Subsequently, a trained interviewer administered the Brazilian version of the MFI (MFI-PD/ BR) to 20 PD subjects to verify their comprehension of the instrument. At the end of this process, the MFI-PD/BR was ready for psychometric testing and keep the same items and structure as proposed in study performed by Baptista et al. [2525 Baptista RLR, Biasoli I, Sheliga A, Soares A, Brabo E, Morais JC, et al. Psychometric Properties of the multidimensional fatigue inventory in Brazilian Hodgkin's lymphoma survivors. J Pain Symptom Manage. 2012;44(6):908-15.].

The content validity was assessed by the expert committee, by verifying the conceptual, cultural, idiomatic and semantic equivalences between the MFI-PD/BR and MFI [99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25.]. It was checked in this PD group if they understood all items of the instrument. This is only a small part of content validity that also includes face validity and extends to the degree to which the content of a questionnaire is adequate to be measured [1818 Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine. 2000;25(24):3186-91., 2626 Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, et al. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol. 2010;63(7):737-45.].

Phase 2: Assessment of psychometric properties

Seventy PD subjects were assessed. Testing-retesting was applied by two examiners, physiotherapists (A and B) administered the MFI-PD/BR separately with a one-hour interval and then, seven days later, examiner A performed the retest. Additionally, subjects also answered the Hospital Anxiety and Depression Scale (HADS) [2727 Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand, 1983;67(6):361-70.], FSS [1616 Valderramas S, Feres AC, Melo A. Reliability and validity study of a Brazilian-Portuguese version of the fatigue severity scale in Parkinson's disease patients. Arq Neuropsiquiatr. 2012;70(7):497-500.] and PFS-16 [1717 Kummer A, Scalzo P, Cardoso F, Teixeira AL. Evaluation of fatigue in Parkinson's disease using the Brazilian version of Parkinson's Fatigue Scale. Acta Neurol Scand. 2011;123(2):130-6.] to examiner B in a separate room. The time taken was recorded by a digital chronometer.

Statistical analyses

Data were analyzed with the Statistical Package for the Social Sciences (SPSS®, Release 20.0), and MedCalc® (Release 19.1.3). A two-tailed significance level of 0.05 was used for all tests. The normality of data distribution was checked by means of the Shapiro-Wilk test. Data quality and acceptability satisfactory were considered if missing data comprise < 5 % of the data set [2828 Smith SC, Lamping DL, Banarjee S, Harwood R, Foley B, Smith P, et al. Measurement of health-related quality of life for people with dementia: development of a new instrument (DEMQOL) and an evaluation of current methodology. Health Technol Assess. 2005;9(10):1-93.]. The time taken to apply the MFI-PD/BR and the score distributions of floor and ceiling effects were also taken into consideration in assessing the acceptability. A floor or ceiling effect was present if more than 15% of patients achieved the lowest or highest score in a questionnaire [2929 Terwee CB, Bot SD, De Boer MR, Van der Windt DA, Knol DL, Dekker J, et al. Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol. 2007;60(1):34-42.].

The reliability was examined by the internal consistency, reproducibility, and measurement error. Cronbach’s alpha was used to examine the internal consistency of items. The reproducibility was tested by means of testing-retesting using the intraclass correlation coefficient (ICC) and the Bland-Altman method with mean differences. The ICC was calculated in two-way random effects model for agreement with optimal values were taken ICC ≥ 0.70. Measurement error was assessed by calculating the standard error of the measurement (SEM). SEM agreement was derived from the error variance in the ICC formula [2929 Terwee CB, Bot SD, De Boer MR, Van der Windt DA, Knol DL, Dekker J, et al. Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol. 2007;60(1):34-42.].

The construct validity was tested through correlations between the MFI-PD/ BR and subscale scores of other instruments considering convergent validity and divergent validity. To evaluate convergent validity, the MFI-PD/ BR total score was compared to the FSS and PFS-16. To evaluate divergent validity, the MFI-PD/ BR total score was compared to several measures of disease related symptoms and disability (MDS-UPDRS, HY), psychological functioning (HADS) and cognitive performance (MMSE). Correlations were estimated using Pearson’s (rs) or Spearman’s correlation coefficients (rho). Coefficient values of 0.25 to 0.49 were deemed low correlations, values of 0.50 to 0.75 were moderate and values >0.75 were deemed high correlations [3030 Fisk JD, Brown MG, Sketris IS, Metz LM, Murray TJ, Stadnyk KJ. A comparison of health utility measures for the evaluation of multiple sclerosis treatments. J Neurol Neurosurg Psychiatry. 2005;76(1):58-63.].

A receiver operating characteristic (ROC) curve was drawn to provide a sensitivity, specificity ratio and accuracy of MFI-PD/ BR. For the clinical diagnosis of fatigue, it was considered the PFS-16 ≥ 3.3 points as cut-off point to indicate on diagnostic criteria for fatigue related PD [66 Kluger BM, Herlofson K, Chou KL, Lou JS, Goetz CG, Land AE, et al. Parkinson's disease-related fatigue: a case definition and recommendations for clinical research. Mov Disord. 2016;31(5):625-31.].

The total amount of dopaminergic medication was expressed as the levodopa equivalent daily dosage (LEDD), determined by previously reported methods [44 Stocchi F, Abbruzzese G, Ceravolo R, Cortelli P, D'Amelio M, De Pandis MF, et al. Prevalence of fatigue in Parkinson disease and its clinical correlates. Neurology. 2014;83(3):215-20.].

Results

Ninety PD individuals were enrolled in the study. The baseline characteristics of the adaptation and validation sample are described in Table 1. The median disease duration is more than 50 months. The MDS-UPDRS mean score indicated a moderate to severe impairment. More than 45% of sample who participated of validation phase showed clinically relevant fatigue (Table 2). The translation and back-translation versions were similar to the MFI-PD original [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.]. All equivalences of the MFI-PD/BR were achieved. In pretesting, there was no problem in understanding the MFI-PD/BR confirming the content and face validity. The instrument kept the same number and allocation of items, domains, format and response patterns as original version [99 Smets E, Garsen B, Bonke B, Haes J. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315-25., 2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.]. It was completed in a median time of 5 minutes and 47 seconds (4.1 - 6.8). No missing data, ceiling (2.78% - first interview, 3.17% - retest), and nor floor effects (2.86% - first interview, 3.94% - retest) were found for the MFI-total and subscales.

The presence of clinical significant fatigue associated with increased scores in HADS total and in its subscales: anxiety and depression. Individuals with major disability (HY) and impairment (MDS-UPDRS total, part I, II and IV) scored higher in PFS-16. There was no association between the fatigue and medication usage for DP (levodopa, dopaminergic drugs or antidepressants) (Table 2).

The Cronbach`s alpha for the MFI-PD/ BR was 0.81 when all responses items were scored. All item-total correlations were acceptable (Table 3). The mean inter-item correlation was 0.70 (Table 3). Good reliability was demonstrated. No systematic differences were found between the observers administration and interviews. There was high agreement and small mean intra and interobserver differences (Table 4).

The MFI-PD/BR correlated moderately with HADS (total score) and its subscale depression, impairment (UPDRS score total and non-motor experiences of daily living) and fatigue (FSS, PFS-16) (Table 5). Disability (HY), impairment (motor experiences of daily living, motor examination and motor complications) showed a low positive correlation with MFI-PD/BR. In other words, higher depression, disability, and advanced stages of PD, more fatigue is perceived by subject. Analysis on ROC curve revealed the MFI-PD/ BR > 55 points as cut-off point to indicate fatigued subjects with value of accuracy of 0.84 [0.72; 0.91](p < 0.001), sensitivity=100% and 1-Specificity=60%.

Table 1
Demographic and clinical characteristics for sample
Table 2
Comparison of Parkinson's disease fatigued and nonfatigued individuals
Table 3
Corrected item-total correlations and Cronbach's alpha (α) if item or subscale are deleted from the Multidimensional Fatigue Inventory (MFI/PD-BR)
Table 4
Reproducibility of the MFI-PD/BR
Table 5
Correlation between MFI-PD/BR and other variables

Discussion

The MFI has already been validated in Brazil for Hodgkin's Lymphoma Survivors [2525 Baptista RLR, Biasoli I, Sheliga A, Soares A, Brabo E, Morais JC, et al. Psychometric Properties of the multidimensional fatigue inventory in Brazilian Hodgkin's lymphoma survivors. J Pain Symptom Manage. 2012;44(6):908-15.], however, the current study presents the first attempt to validate the instrument in idiopathic PD subjects. Considering the high prevalence of fatigue in PD, many instruments were developed and submit to psychometric studies but the available existing instruments only provided a limited understanding of the level of fatigue. There is a continuous necessity to have other instruments to complement all aspects of fatigue. The MFI appears to be a promising measure for evaluating fatigue in PD [11 Siciliano M, Trojano K, Santangelo G, De Micco R, Tedeschi G, Tessitore A. Fatigue in Parkinson's disease: a systematic review and meta-analysis. Mov Disord. 2018;33:1712-23.].

The frequency of fatigue in this study confirmed the high prevalence demonstrated in various studies, with worldwide rates of up to 75% [11 Siciliano M, Trojano K, Santangelo G, De Micco R, Tedeschi G, Tessitore A. Fatigue in Parkinson's disease: a systematic review and meta-analysis. Mov Disord. 2018;33:1712-23., 22 Kluger BM, Garimella S, Garvan C. Minimal clinically important difference of the Modified Fatigue Impact Scale in Parkinson's disease. Parkinsonism Relat Disord. 2017;43:101-4.], and Brazilian rates of around 41.3 to 67.4% [1616 Valderramas S, Feres AC, Melo A. Reliability and validity study of a Brazilian-Portuguese version of the fatigue severity scale in Parkinson's disease patients. Arq Neuropsiquiatr. 2012;70(7):497-500., 1717 Kummer A, Scalzo P, Cardoso F, Teixeira AL. Evaluation of fatigue in Parkinson's disease using the Brazilian version of Parkinson's Fatigue Scale. Acta Neurol Scand. 2011;123(2):130-6.]. This is a subjective finding with great perception sense involved and a considerable variability in the description of fatigue. Common definitions include a sense of exhaustion or a subjective lack of physical and/ or mental energy that is perceived by the individual or caregiver to interfere with usual or desired activity [3131 Spirgi S, Meyer A, Calabrese P, Gschwandtner U, Fuhr P. Effects of Cognitive Performance and Affective Status on Fatigue in Parkinson's Disease. Dement Geriatr Cogn Disord Extra. 2019;9(3):344-51.]. However, these terms may be differently interpreted depending on subject’s cultural background [3232 Weeks A, Swerissen H, Belfrage J. Issues, challenges, and solutions in translating study instruments. Eval Rev. 2007;31(2):153-65.].

Since most scales and questionnaires have been developed in English-speaking countries, a validation process is required before these instruments can be used in other countries. Therefore, for these instruments to be considered appropriate for clinical or research use, it is necessary to evaluate all psychometric properties [1616 Valderramas S, Feres AC, Melo A. Reliability and validity study of a Brazilian-Portuguese version of the fatigue severity scale in Parkinson's disease patients. Arq Neuropsiquiatr. 2012;70(7):497-500., 3333 Guillemim F, Bombardier C, Beaton D. Cross-cultural adaptation of health-related quality of life measures: literature review and proposed guidelines. J Clin Epidemiol. 1993;46(12):1417-32.]. Different societies have its own beliefs and behavior and, in the cross-cultural adaptation process these particularities must be considered [3232 Weeks A, Swerissen H, Belfrage J. Issues, challenges, and solutions in translating study instruments. Eval Rev. 2007;31(2):153-65.]. According to the cross-cultural adaptation process proposed [1818 Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine. 2000;25(24):3186-91.] all equivalences, content and face validity between the original MFI and MFI-PD/BR were achieved assuming the maintenance of the psychometric properties of the MFI-PD/BR as properly documented in prior study [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.].

The MFI-PD/BR showed a good level of acceptability and required few minutes to fill out. For an instrument to be considered appropriate to investigate a sign/ symptom of a patient, it is necessary to evaluate, at least, its acceptability, reliability, and validity [3232 Weeks A, Swerissen H, Belfrage J. Issues, challenges, and solutions in translating study instruments. Eval Rev. 2007;31(2):153-65., 3333 Guillemim F, Bombardier C, Beaton D. Cross-cultural adaptation of health-related quality of life measures: literature review and proposed guidelines. J Clin Epidemiol. 1993;46(12):1417-32.]. Acceptability refers to the distribution of score as a symmetric way [3434 Scientific Advisory Committee of the Medical Outcomes Trust. Instrument review criteria. Washington, DC: Scientific Advisory Committee; 1995.]. The acceptability of MFI-PD/BR is in accordance with the original MFI [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.] only in GF and RM subscales that was not observed floor nor ceiling effects, too. Elbers et al. [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.] mentioned that the found floor effect for the MF subscale and the ceiling effects for the PF and RA subscales should be considered when evaluating one of these aspects of fatigue. Furthermore, these results suggest that mental fatigue and physical fatigue are two different aspects of fatigue and further confirm previous findings that mental fatigue and physical fatigue are different symptoms in PD [77 Lou J, Kearns G, Oken B, Sexton G, Nutt J. Exacerbated physical fatigue and mental fatigue in Parkinson's disease. Mov Disord. 2001;16(2):190-6., 3535 Elbers R, Van Wegen E, Rochester L, Hetherington V, Nieuwboer A, Willems A, et al. Is impact of fatigue an independent factor associated with physical activity in patients with idiopathic Parkinson's disease? Mov Disord. 2009;24(10):1512-8.].

In agreement of study that validated MFI for PD [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.], the current study evidenced the reliability of MFI-PD/ BR as good and showed small SEM on all subscales. The SEM allows one to make statements about the precision of test scores of individual examinees. The lower difference, the better is an instrument to obtain more realistic scores [2929 Terwee CB, Bot SD, De Boer MR, Van der Windt DA, Knol DL, Dekker J, et al. Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol. 2007;60(1):34-42.]. The Bland-Altman analysis demonstrated that there was low individual variability with satisfactory limits of agreement, such that the subjects answered the items similarly seven days later. These results suggest that the MFI-PD/BR is a stable instrument with low systematic difference indicating good concordance between the first and the last interview and the two observers. Elbers et al. [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.] also evidenced the same Bland-Altman analysis confirming the stability of MFI to assess fatigue in PD.

When an instrument is valid, it truly reflects the concept that it should measure [2626 Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, et al. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol. 2010;63(7):737-45.]. Investigating the validity of PD fatigue instruments is a complex task due the unclear definition and multidimensional factors. On this current study three aspects of validity was analyzed: content, criterion, and construct validity [1111 Elbers RY, Rietberg MB, van Wegen EE, Verhoef J, Kramer SF, Terwee CB, et al. Self-report fatigue questionnaires in multiple sclerosis, Parkinson's disease and stroke: a systematic review of measurement properties. Qual Life Res. 2012;21(6):925-44.]. Content validity has already been commented on, in describing the stage of cross-cultural adaptation. Since no gold standard exists for fatigue instruments, criterion validity was not evaluated. The degree to which scores of a questionnaire are consistent with other instruments which measures the similar (convergent validity) or associated (divergent validity) constructs was defined as construct validity [2626 Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, et al. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol. 2010;63(7):737-45.]. Convergent validity of the MFI-PD/BR was established with the FSS and PFS-16, suggesting a moderate level of association. The adequate divergent validity was established between MFI-PD/ BR and severity of PD, motor aspects (experiences of daily living, examination, and complications) and depression feeling.

In the study of validation of MFI for PD subjects [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.] was investigate only the structural validity where assume that MFI is validate for PD, however is not possible to establish any association with this current study. The results of the current study is in line with other studies that investigate the construct validity of the MFI in patients with cancer [3636 Fillion L, Gélinas C, Simard S, Savard J, Gagnon P. Validation evidence for the French Canadian adaptation of the multidimensional fatigue inventory as a measure of cancer-related fatigue. Cancer Nurs. 2003;26(2):143-54., 3737 Gentile S, Delarozière J, Favre F, Sambuc R, San Marco J. Validation of the French 'multidimensional fatigue inventory' (MFI 20). Eur J Cancer Care. 2003;12(1):58-64.]. It was not investigate the structural validity of MFI because it is not necessary to test again for the same disease if it is confirmed in the study of validation of MFI for PD subjects [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.].

Data concerning factors associated with fatigue in PD are still scarce and contradictory. In contrast of results of the present study, some studies have found association between fatigue and education level, time from diagnosis, female gender, advanced age, severity of PD and advanced HY disease stages [1717 Kummer A, Scalzo P, Cardoso F, Teixeira AL. Evaluation of fatigue in Parkinson's disease using the Brazilian version of Parkinson's Fatigue Scale. Acta Neurol Scand. 2011;123(2):130-6., 3838 Martinez-Martin P, Wetmore JB, Arbelo JM, Catalán MJ, Valldeoriola F, Rodriguez-Blazquez C. Validation study of the Parkinson's Fatigue Scale in advanced Parkinson's disease. Patient Relat Outcome Meas. 2019;10:141-52., 3939 Bensing JM, Hulsman RL, Schreurs KM. Gender differences in fatigue: biopsychosocial factors relating to fatigue in men and women. Med Care. 1999;37(10):1078-83.]. Similar to the current study, low-to-high correlations were found between the fatigue (PFS-16) and depression measures [4040 Fu R, Cui S-S, Du JJ, Huang P, He YC, Gao C, et al. Validation of the Parkinson Fatigue Scale in Chinese Parkinson's disease patients. Brain Behav. 2017;7(6):e00712., 4141 Ozturk EA, Kocer BG, Umay E, Cakci A. Cross-cultural adaptation and psychometric evaluations of the Turkish version of Parkinson Fatigue Scale. Qual Life Res. 2018;27(10):2719-30.].

This is the first study to calculate the cut-off point for the MFI-PD. It was stated that it is impossible to calculate the sensitivity and specificity because of the absence of a gold standard instrument, which measure fatigue symptom [2323 Elbers RG, Van Wegen EEH, Verhoef J, Kwakkel G. Reliability and structural validity of the Multidimensional Fatigue Inventory (MFI) in patients with idiopathic Parkinson's disease. Parkinsonism Relat Dis. 2012;18(5):532-36.]. Therefore, it was used PFS-16 to screen who feels fatigue associated PD to drawn the ROC curve because PFS-16 captures the effects of fatigue considering the subjective experience of fatigue and the impact of this symptom on daily functioning, such as socialization and work [3838 Martinez-Martin P, Wetmore JB, Arbelo JM, Catalán MJ, Valldeoriola F, Rodriguez-Blazquez C. Validation study of the Parkinson's Fatigue Scale in advanced Parkinson's disease. Patient Relat Outcome Meas. 2019;10:141-52.] as the similar subscales of MFI-PD.

There are some limitations of this study need to be pointed out. It was accomplished a monocentric study with a convenience sample. A validation study requires many possibilities of changes to generalize the finds to the other parts of country whose speaks the idiom. It is important to observe that the sample of the present study was fairly early in disease course, which indicates a limitation to generalize the results to more advanced PD subjects. Moreover, the lack of a control group of healthy participants did not allow the comparison of the fatigue severity between PD patients and the general population. Another limitation is that FSS and PFS-16 were used as comparator instruments despite their problems regarding reliability and validity. These were administered in the present study because there were no other Brazilian specific instruments for assessing PD fatigue. With regard to use of the HADS instruments, it is important to consider that they are generic measurements, and may fail to address important areas of impact that are disease-specific.

Further research is necessary in order to be able to administer the MFI-PD/BR. Future studies could correlate it with imaging examinations, investigate samples composed by patients in hospital or more advanced stages of PD, analyze outcomes such as sleep and quality of life. A longitudinal study with a greater length of follow-up among those expected to change could determine the responsiveness of the MFI-PD/BR during the treatment protocol with the purpose to reduce fatigue.

Conslusion

MFI-PD/BR is a reliable and valid instrument to assess the multidimensional aspects of fatigue in Brazilian patients with PD. It holds the relevant psychometric properties and satisfies the modern standards for outcome measurements relating to the symptom of fatigue in PD. It can be used in clinical settings as well as in any design of research study thus promoting their use in cross-sectional and longitudinal clinical studies.

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Publication Dates

  • Publication in this collection
    26 Oct 2020
  • Date of issue
    2020

History

  • Received
    19 Dec 2019
  • Accepted
    10 July 2020
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