Association between Parkinson’s disease stages and locomotor performance classification: a pilot study

Associação dos estágios da doença de Parkinson com a classificação do desempenho locomotor: um estudo piloto

Asociación entre los estadios de la enfermedad de Parkinson y la clasificación del rendimiento locomotor: un estudio piloto

ABSTRACT

The study aimed to evaluate the impairment of locomotion capacity in people with Parkinson's disease (PwP) using the 6-Minute Walk Test (6MWT), classify performance against predicted distance, and investigate the association between the Locomotion Performance Classification (LPC) (A1, A2, and A3) with the stages between 1 to 4 of the disease, according to the Hoehn & Yahr (H&Y) scale. 32 individuals in stages 1 to 4 of the disease participated. We used Pearson's test in Jamovi software to correlate clinical and performance variables. The performance in the 6MWT was higher than predicted (465m covered; 439m predicted). The stages of the disease and the proposed LPC showed a moderate inverse correlation, r= -0.521; p= 0.002.

Keywords:
Motor Disorder; 6-Minute Walk Test; Locomotion; Gait; Functional Ability

RESUMO

O objetivo do estudo foi avaliar o comprometimento da capacidade de locomoção de pessoas com Parkinson (PcP) a partir do Teste de Caminhada de 6 minutos (TC6), classificar o desempenho em relação a distância predita, e verificar a associação entre a Classificação de Desempenho Locomotor (CDL) (A1, A2 e A3) com os estágios entre 1 a 4 da doença, conforme a escala de Hoehn & Yahr (H&Y). Participaram 32 pessoas, em estadiamento 1 a 4 da doença, utilizamos o teste de Pearson no software Jamovi para correlacionar as variáveis clínicas e de desempenho. O desempenho no TC6 foi maior que o previsto (465m percorrido; 439m predito). Os estágios da doença e a proposta de CDL apresentou correlação inversa e moderada r= -0.521; p= 0.002.

Palavras-chave:
Distúrbio Motor; Teste de Caminhada de 6 minutos; Locomoção; Marcha; Capacidade Funcional

RESUMEN

El objetivo del estudio fue evaluar el compromiso de la capacidad de locomoción en personas con Parkinson (PcP) a partir de la Prueba de Caminata de 6 minutos (PC6), clasificar el rendimiento frente a la distancia prevista, y verificar la asociación entre la Clasificación del Desempeño Locomotor (CDL) (A1, A2 y A3) con estadios 1 a 4 de la enfermedad, según la escala de Hoehn & Yahr (H&Y). Participaron 32 personas, en estadios 1 a 4 de la enfermedad. Utilizamos la prueba de Pearson en el software Jamovi para correlacionar las variables clínicas y de desempeño. El desempeño en el PC6 fue mayor que el previsto (465m recorridos; 439m predichos). Los estadios de la enfermedad y la propuesta de CDL mostraron una correlación inversa y moderada r= -0.521; p= 0.002.

Palabras-clave:
Trastorno Motor; Prueba de Marcha de 6 minutos; Locomoción; Marcha; Capacidad Funcional

INTRODUCTION

Parkinson’s disease (PD) affects dopaminergic neurons, leading to motor symptoms such as postural control and gait disturbances (Bohnen and Cham, 2006; Jankovic and Tan, 2020). Gait abnormalities in PD include shorter steps, decreased gait speed, reduced stride length, and decreased distance traveled. Additionally, PD causes changes in gait cadence, known as festination, characterized by increased stride frequency and a shorter duration of double support (Cho et al., 2010; Mirelman et al., 2019). The progression of motor symptoms worsens the functional capabilities of individuals with PD (Elren Passos Monteiro et al., 2017b). Besides changes in gait and posture, other motor symptoms affect locomotion, including bradykinesia, akinesia, freezing, muscle rigidity, and dyskinesia, among others (Carpinella et al., 2007; Balestrino and Schapira, 2020).

Considering this, it is crucial to evaluate and monitor the progression of the disease. We emphasize utilizing the primary clinical monitoring scales for Parkinson's disease: the MDS-UPDRS (part III), which tracks motor symptoms, and the Hoehn & Yahr scale (H&Y), which assesses disease stages (Hoehn and Yahr, 1967; Schenkman et al., 2001; Goetz et al., 2004, 2008). Furthermore, evaluating functional aspects, particularly gait, is essential as it directly impacts the quality of life and independence of People with Parkinson's (PwP) (Mirelman et al., 2019; Santos Delabary et al., 2020). In this context, we draw attention to the 6-minute walk test (6MWT), recognized as a straightforward tool for assessing locomotion capacity. It is cost-effective, safe, submaximal, reliable, well-tolerated, and widely employed in PwP evaluations (Steffen and Seney, 2008; Kobayashi et al., 2017; Peyré-Tartaruga et al., 2022).

At PD, the 6MWT is an essential instrument for assessing mobility and locomotion; current findings point to significant improvements in several interventions, especially locomotor ones (Peyré-Tartaruga et al., 2022; Haas et al., 2024). Furthermore, the test is used in the periodization of Nordic Walking (NW) and Free Walking (FW) interventions, together with the 10-meter walk test, demonstrating its versatility and effectiveness. The parameters considered for the prescription of individualized training sessions for PwP are the self-selected speed and the distance covered, thus constituting the intensity and volume of the sessions (Zanardi et al., 2019; Peyré-Tartaruga et al., 2022).

However, the correlate the performance of the 6MWT with the Hoehn & Yahr disease stage scale, they consider its results weak and insensitive to the stages of the disease (Combs et al., 2014; Kobayashi et al., 2017). Considering the clinical progression of the disease and the reduction of functional parameters, one objective of this study is the Locomotor Performance Classification (LPC) of PwP in the 6MWT. This classification reasoned on the performance percentage relative to the expected distance to be achieved in the test (Enright et al., 2003). Healthcare professionals can use LPC in clinical practice by considering the intensity and volume of locomotor intervention sessions in PwP. The percentages obtained from evaluations can help to prescribe, periodize, and monitor these interventions more effectively (Peyré-Tartaruga et al., 2022). Therefore, this study aims to assess the impairment of locomotion capacity in trained PwP, classify them based on the coefficient achieved, and correlate the LPC with the stages of the disease H&Y.

METHODS

Study design

The Hospital de Clínicas de Porto Alegre (HCPA) from Federal University of Rio Grande do Sul (UFRGS) ethics committee (approval number 24595713.4.0000.5327) approved this study, which is characterized as an observational, cross-sectional, analytical pilot study following the “Strengthening the Reporting of Observational Studies in Epidemiology-STROBE” guidelines (Cuschieri, 2019). Additionally, the study adhered to the recommendations of the Declaration of Helsinki and the Resolution of the National Health Council (CNS), resolution no. 510/2016, for studies involving human subjects.

Setting

We conducted the study at the Exercise Research Laboratory (LAPEX) of the School of Physical Education, Physiotherapy and Dance (ESEFID) at UFRGS. In 2017, we recruited participants from the Parkinson's Research and Treatment Program (PPT-PARKINSON-UFRGS).

Participants

Sample recruitment

Participants recruited from the Nordic Walking locomotor training program for people with Parkinson's (PwP) at UFRGS, Porto Alegre, Brazil, received an explanation about the research procedures after initial contact and were instructed to attend on two consecutive pre-scheduled days. The sample was drawn by convenience from participants in the Parkinson's Research and Treatment Program (PPT-PARKINSON - UFRGS).

Eligibility criteria

Participants regularly enrolled in the Nordic Walking Extension Program for individuals with PD have received a clinical diagnosis of idiopathic PD for at least one year, according to the diagnostic criteria of the UK Parkinson's Disease Society Brain Bank Diagnostic Criteria, and are staged between 1 and 4 on the H&Y scale (Hoehn and Yahr, 1967; Schenkman et al., 2001; Goetz et al., 2004), must be under medical supervision and using antiparkinsonian medication. Exclusion criteria include participants who have been clinically diagnosed with other neurological disorders, are using brain stimulation devices, have clinical conditions influencing gait abnormalities, cannot walk unassisted or require an auxiliary device, and disagree with the research definition terms.

Variables and outcome measures

Researchers subjected the participants to clinical evaluations for monitoring and staging Parkinson's disease (MDS-UPDRS and H&Y– Part III, and H&Y, we specified the clinical data of MDS-UPDRS and H&Y in absolute values), anthropometric assessments for sample characterization and prediction outcomes of locomotor performance (age in years, height in centimeters, and body mass in kilograms), and physical tests for locomotion capacity (6MWT), we expressed the predicted and actual walking distance in the 6MWT in meters. We described LPC as a coefficient and categorized it into groups A1, A2, and A3 based on performance in the 6MWT.)

Data collection

Data collection occurred over consecutive days. We conducted clinical assessments (H&Y and MDS-UPDRS) on the first day, followed by anthropometric data collection. On the second day, we administered the 6MWT in a 30-meter flat corridor, marked every three meters by the recommendations of the American Thoracic Society (ATS Committee on Proficiency Standards for Clinical Pulmonary Function Laboratories, 2002). We instructed participants to walk as far as possible within 6 minutes, to pause or discontinue if they experienced any discomfort, and we encouraged them with pre-established phrases during the test, such as “very well!” and “keep it up.” We collected data during the “ON” period, up to two hours after medication intake.

Data processing

After collecting data, we used anthropometric information, including height, body mass, and age, to calculate predicted distance values for the 6-minute walk test (6MWT) for Men Equation 1 and Women Equation 2 (Enright et al., 2003). We also derived a new equation based on the ratio of the distance covered to the predicted distance in the 6MWT (actual 6MWT/predicted 6MWT), where LPC represents the coefficient of predicted distance achieved (Equation 3).

Furthermore, LPC categorizes participants into three groups (A1, A2, and A3) based on the achieved coefficient. LPC classification relies on clinical assessment for Chronic Obstructive Pulmonary Disease (COPD) in the 6MWT, with a cutoff point of ≤80% of the predicted distance indicating exacerbation risks (Moreira et al., 2015; Morakami et al., 2017). However, for participant classification, we used the following coefficient thresholds from the test: low-performance A1 (<0.85 of predicted distance), moderate performance A2 (0.86 to 1.20 of predicted distance), and high-performance A3 (>1.20 of predicted distance).

Men:

$$\begin{array}{l}Predicteddistance=493+\left(2.2xheightcm\right)–\\ \left(0.93xbodymasskg\right)–\left(5.3xage\right)+17m\end{array}$$ (1)

Women:

$$\begin{array}{l}Predicteddistance=493+\left(2.2xheightcm\right)–\\ \left(0.93xbodymasskg\right)–\left(5.3xage\right)\end{array}$$ (2)

Locomotor Performance Classification:

$$Covereddistance/Predicteddistance=LPC$$ (3)

Bias

In the present study, we considered potential bias such as age, time since diagnosis, anthropometric characteristics, and duration of physical exercise practice.

Sample size

Since this was a pilot study, we recruited participants from the PPT-PARKINSON program for convenience; therefore, we did not calculate the sample size.

Statistical analysis

We conducted descriptive analysis tests on the data, presenting them as mean values accompanied by their corresponding standard deviations. Additionally, we examined the correlation between performance and clinical variables using the Pearson correlation test. Furthermore, we investigated the correlation between the LPC and their classifications (A1, A2, and A3) with the Hoehn and Yahr disease scale stages. We performed all data analyses using Jamovi 2.4.14 software, with a significance level of α = 0.05.

RESULTS

We included 32 individuals diagnosed with Parkinson's disease (PD) in the study, consisting of 23 men and 9 women, all capable of completing the 6-Minute Walk Test (6MWT) without requiring rest or interruption. Table 1 presents the descriptive characteristics of the participants, including clinical and anthropometric data.

Table 1
Demographic, anthropometric and clinical data.

	Mean (± SD)			95% Confidence Interval
Total participants	32
Gender (male/female)	23/9
Age (years)	68.3 ± 8.1			63.8-70.4
Height (cm)	164 ± 9.6			161-167
Body mass (kg)	70.3 ± 14.0			64.4-74.0
MDS-UPDRS	20.9 ± 8.2			18.3-25.0
H&Y	2.5 (1-4)
H&Y stage	1	1.5	2	2.5	3	4
PwP	(3)	(4)	(8)	(5)	(10)	(2)

• Note: SD – standard deviation; CI – confidence interval; H&Y – Hoehn & Yahr; MDS-UPDRS - Unified Parkinson’s Disease Rating Scale; PwP – People with Parkinson’s.

Table 2 presents the data on predicted and achieved distances in the 6MWT and performance stratified by H&Y stages, the calculated coefficient of the achieved distance relative to the expected distance, and the corresponding classifications of participants according to the LPC proposal.

Table 2
Predicted and covered 6MWT distance. LPC calculated the percentage and distance in stages of H&Y disease.

	Mean (± SD)			95% Confidence Interval
6MWT predicted (m)	439 ± 50.1			426-467
6MWT covered (m)	465 ± 68.0			438-486
LPC percentage (%)	1.07 ± 0.17			0.98-1.11
A1 classification (n)	4
A2 classification (n)	23
A3 classification (n)	5
6MWT performance by H&Y stages (m)	1	1.5	2	2.5	3	4
	505 ± 67.1	478 ± 70.5	469 ± 58.0	481 ± 51.5	447 ± 76.6	394 ± 31.8

• Note: SD – standard deviation; 6MWT – 6-minute walk test; LPC – Locomotor Performance Classification; A1 (<0.85 of predicted distance); A2 (0.86 to 1.20 of predicted distance); A3 (>1.20 of predicted distance); LPC classification was represented for absolute values; H&Y – Hoehn & Yahr scale; 6MWT performance by H&Y stages (m) were represented in meters.

Figure 1 and Table 3 depicts the correlation between stages of disease and the proposed coefficient of LPC classification for performance in the 6MWT against predicted performance. Additionally, one can observe performance classifications A1, A2, and A3 from zones <85 and >120, indicated by dashed lines.

Figure 1
Correlation between disease stages and LPC. Note: Lines: Represent the classification zones of groups A1 (< 0.85 of the distance traveled), A2 (0.86 to 1.20 of the distance traveled), and A3 (> 1.20 of the distance traveled); Blue color: Classification of participants in the A1 group; Green color: Classification of participants in the A2 group; Color red: Classification of participants in the A3 group.

Table 3
Correlation values of age, performance, and clinical variables

Variables	Correlation	Age	6MWT	6MWT	LPC	MDS-UPDRS	H&Y
	Coefficient		predicted	covered
Age	Pearson r	-
	p-value	-
6MWT predicted	Pearson r	- 0.927*	-
	p-value	< 0.001	-
6MWT covered	Pearson r	- 0.315	0.343	-
	p-value	0.079	0.055	-
LPC	Pearson r	0.419*	- 0.453 *	0.675*	-
	p-value	0.017	0.009	< 0.001	-
MDS-UPDRS	Pearson r	0.084	0.032	- 0.459*	- 0.456*	-
	p-value	0.665	0.870	0.012	0.013	-
H&Y	Pearson r	0.009	0.009	- 0.451*	- 0.521*	0.659*	-
	p-value	0.961	0.560	0.010	0.002	< 0.001	-

• Note: 6MWT - 6-minute walk test; LPC - Locomotor Performance Classification; MDS-UPDRS - Movement Disorder Society (MDS) - Unified Parkinson's Disease Rating Scale; H&Y - Hoehn & Yahr scale.
• ^*
  Significant correlations.

DISCUSSION

We aimed to evaluate the locomotion performance of trained PwP in the 6MWT and correlate their illness staging with the proposed LPC. Our main findings were that trained PWP reached a greater locomotion performance than the predicted distance (465 meters traveled versus 439 meters predicted). However, when the individuals were classified according to locomotion performance, LPC, we found that the distance covered during the 6MWT was lower than predicted by individuals from moderate to severe stages as observed in Table 1. As previously noted, moderate to severe PwP walk significantly slower than those with mild stages (Combs et al., 2014; Kobayashi et al., 2017).

Furthermore, the results indicate a weak inverse correlation between the distance covered and the H&Y stages. However, when correlating the H&Y stages with the classification of LPC proposal, the values are considered inverse, moderate, and significant, demonstrating that our proposal to express gender-dependent index, LPC, considering height, body mass, and age, seem more sensitive to PD stages than the 6MWT alone. Interestingly, the correlation suggests that the lower the clinical functional impairment, the better the LPC performance and classification. This index may be a future candidate to be used in clinical trials using the field tests as 6MWT, other than a strategy to periodize training loads in neurodegenerative disease patients (Peyré-Tartaruga et al., 2022).

The average LPC coefficient was 1.07, with classifications of four participants in A1, nineteen in A2, and five in A3. Indeed, classifying participants into different groups according to their abilities can help monitor and prescribe individualized locomotor interventions (Peyré-Tartaruga et al., 2022). Therefore, based on the distance traveled performance over predicted performance in the 6MWT, the Locomotor Performance Classification can be a valuable tool in the functional clinical evaluation of locomotor interventions for PwP (Zanardi et al., 2019; Peyré-Tartaruga et al., 2022; Haas et al., 2024). Interventions that prioritize the locomotion of PwP minimize asymmetric patterns and other functional deficits exacerbated by PD progression (Morris, 2006; Monteiro et al., 2017a; Zanardi et al., 2019; Mirelman et al., 2019). A previous study has used a similar approach applying multiple regression normalization strategy accounting for subject age, height, body mass, and gender, to identify differences in spatiotemporal gait features between PwP and controls. The model unveils a superior capacity to accurately classify the PwP than machine learning methods (Wahid et al., 2015). Future studies can verify the diagnostic and predictive potential of the LPC to evaluate cardiorespiratory fitness in PwP.

Our study has some limitations that need to be discussed. Although the findings on the use of the LPC are innovative, the sample used in our study precludes the possibility of validating this index definitively. In addition, this study analyzed a well-aerobically trained group of PwP, so the findings should be interpreted with caution and applied strictly to PwP with a history of long-term aerobic training. It is worth noting that locomotor training significantly improves cardiorespiratory fitness and 6MWT performance in individuals with PwP compared to pre-intervention parameters and control groups (Mak and Wong-Yu, 2021; Zhang et al., 2023). We suggest future systematic review studies to determine whether there is a well-established minimal clinically significant difference in the distance covered in the six-minute walk test between trained and untrained Parkinson's patients.

On the other hand, this study demonstrates the fundamental role of exercise as a non-pharmacological intervention impacting functional mobility and autonomy in PwP of varying degrees of disease progression. From a modern bio-psycho-social paradigm of disability (WHO, 2021), this study reinforces the need to pay attention to factors that inhibit or enhance PwP access to physical exercise. Further, the study also warns of the need for a review of predictive equations in PwP.

CONCLUSION

We conclude that physically trained people with Parkinson's disease perform better on the 6MWT than predicted, but clinical worsening may reduce locomotion. This proposal could serve as an alternative for clinical and functional evaluation, as well as a tool for individualization, prescription, and monitoring of locomotor training for individuals with Parkinson's disease.

ACKNOWLEDGEMENTS

We thank LABMOVHER-UFPA, PENDULUM, and Locomotion Groups at Universidade Federal do Pará (UFPA) and Universidade Federal do Rio Grande do Sul (UFRGS), Brazil, for discussions, comments, and individuals with Parkinson, especially PPT-Parkinson - UFRGS.

• FUNDING
  There was no funding for this research.

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Publication Dates

• Publication in this collection
  24 Mar 2025
• Date of issue
  2025

History

• Received
  10 July 2024
• Accepted
  03 Jan 2025