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INTRODUCTION

Parkinson’s disease (PD) is a complex, chronic, progressive, and debilitating neurodegenerative disease that develops slowly and irreversibly.1,2 It is characterized as a movement disorder with 3 main signs: tremor, rigidity, and bradykinesia. Some patients may develop postural instability as the disease progresses.3 Its etiology is not fully known. Even so, loss of dopamine in the brain is recognized as the cause of motor impairment in people with PD.4 Unhealthy eating, lack of physical activity, and alcohol consumption, which may lead to overweight or obesity and increase blood pressure and cholesterol levels, have been recognized as risk factors common to PD and other chronic noncommunicable diseases.5

PD is the second most prevalent neurodegenerative disease, affecting 1 to 2% of the world population at any age,6 and has the fastest growing rates of prevalence, disability, and death.7 Its incidence and prevalence increase with age, affecting up to 3% of the population over 55 years of age.8 In 2016, PD caused more than 211,000 deaths in addition to 3.2 million cases of functional disability (1.4 million females and 1.8 million males).7 Also, people with PD commonly require assistance due to functional impairment, movement difficulties, gait disturbances, and lack of balance. This comprehensive care involves both caregivers and family members and may generate high levels of stress.9

Physical exercise, due to its safety and efficacy, has been proposed as an effective non-pharmacological intervention to minimize harm in patients with PD.10 The positive effects of properly prescribed physical exercise include lowering of blood pressure,11 prevention and management of diabetes,12 control of body weight by improving the lipoprotein profile and increasing insulin sensitivity,13 prevention and improvement of mild symptoms of depression, anxiety, and dyspnea with a positive impact on quality of life,14 improvement of cognitive function and mind-body connection,15 and increase in the concentration of biomarkers related to neurogenesis and neuroprotection.16 For people with PD, physical exercise is believed to improve motor symptoms, namely bradykinesia, gait, and turning performance, and also to affect positively non-motor aspects, such as mood disturbance, cognitive deficits, and sleep disorder.17,18

Although physical exercise is considered a safe and effective intervention in PD, the appropriate dose to potentiate its effects, considering exercise type, frequency, volume, and intensity, has not yet been established. Health care must be provided considering the patient’s context and preferences, professional experience, and the best available evidence.19 In this respect, a considerable number of systematic reviews addressing different types of physical exercise protocols and evaluating different outcomes in patients with PD have been published. Therefore, an umbrella review, which is a scoping review of systematic reviews,20 was first proposed to characterize the level of evidence available to support the prescription of physical exercise for people with PD, considering the gaps related to exercise dose and type of outcome analyzed. This study is a subanalysis of the umbrella review and focuses on the bibliometric characterization of the scientific production on the issue.

METHODS

Search strategy

For this bibliometric review, systematic reviews reporting the effects of physical exercise on people with PD were searched in Web of Science (Clarivate Analytics), Scopus (Elsevier), Cochrane Library, and MEDLINE (via PubMed) databases. The search strategy was developed by a librarian experienced in health information recovery and run on May 22, 2022, to allow the bibliometric analysis of the retrieved studies. No date or language filter was used.

The terms ‘Systematic reviews,’ ‘Exercise,’ and ‘Parkinson’s Disease’ were used as indexed terms (MeSH terms) and synonymous (free terms) to build the query using Boolean operators. The search strategy applied to each database is depicted in Table S1.

Study selection

The information retrieved from each database was uploaded to the open-source science mapping package Bibliometrix 4.0 for R,21 which removed duplicate references and generated an Excel spreadsheet (Microsoft Office version 365, Microsoft Corp.) containing 544 references. These references were cross-checked with those previously included in the umbrella review by 2 authors and updated to produce the final dataset for bibliometric analysis.

Data extraction and analysis

The following bibliometric indicators were extracted: number of articles and sources, time span, average publication time (years), annual scientific production, annual growth rate, number of citations, average citations per document, average citations per year per document, top 20 most productive and most cited journals, institutions, and countries, study publications and citations per country per year, total number of authors, authors of single-authored documents, authors of multi-authored documents, articles per author, authors per article, co-authors per article, collaboration index, collaboration between authors and between countries, indexed keywords (keywords plus), topic trends, and thematic evolution based on authors’ keywords.

Data were analyzed in R package Bibliometrix 4.0 and Excel™. Scientific collaboration based on co-authorship was analyzed based on a collaboration network where the nodes represent the authors, and the links represent the co-authorships.20 Louvain clustering algorithm with normalization by association was used. Other network parameters were the number of nodes (n=50) and a minimum number of one link. Thematic maps and evolution analysis were based on 250 authors’ keywords, with a minimum cluster frequency per thousand documents of 5, inclusion index weighted by word occurrences with a minimum weight index of 0.1, and 3 cutting points (2010, 2015, and 2020). A keyword co-occurrence matrix was expressed graphically as undirected weighted networks, based on the simple center algorithm, allowing the identification of subgroups of strongly linked terms. Thematic diagrams were plotted based on 2 parameters, the Callon centrality and Callon density. The former expresses the importance of the topic within the study collection, and the latter expresses a measure of the topic development. The diagram is divided into 4 quadrants: the upper-right quadrant characterizes the motor themes, with high centrality (important) and high density (well developed) in the field; the lower-right quadrant represents basic and transversal themes, with high centrality and low density; the lower-left quadrant represents emerging or declining themes, which translate into weakly developed or marginal themes (low centrality and low density); and the upper-left quadrant characterizes highly developed and isolated themes, with limited importance to the field.22

RESULTS

Figure S1 shows the study flow diagram. A total of905 records were identified by searching the 4 electronic databases, from which 361 records were identified as duplicates and removed with Bibliometrix. The remaining 544 records were screened, and other 398 records were removed mainly for not being related to the topic. Therefore, 146 records were analyzed as to bibliometric indicators and properties. Twenty-one other studies from the umbrella review were not identified for the bibliometric analysis.

The first systematic review assessing the effects of physical exercise on PD was published in 2005. After that, more than 100 reviews were published addressing the issue with a 14.72% annual growth rate (Table S2 and Figure S2). The average publication time was 3.72 years, showing that reviews have been published recently. Most published studies had more than 1 author, with an average of 5 authors per article (Table S2).

Table 1 presents the most relevant journals. The highest number of articles published in one journal was 8, in Clinical Rehabilitation and PLoS One. The most cited journal was Movement Disorders.

Table 2 shows the most productive and cited institutions. Queensland University of Technology was the most productive institution, being involved in the production of 12 studies. The most cited institution was the University of Exeter, accounting for 14.36% of the citations.

Table 3 shows the most productive and cited countries based on corresponding author affiliation. Figure S3 depicts the production of the 10 most productive countries and the citations of the 10 most cited countries per year.

Collaboration networks (Figure S4) depicted individual collaborations and collaborations between institutions and countries, while Figure S5 maps scientific collaborations between countries. Small clusters of authors mainly from the same country represent the individual collaborations (Figure S4.A). Institutional collaboration was observed mostly between universities from the same country, such as the Spanish universities of León and Vigo and the Australian universities James Cook University and Queensland University of Technology. Also, Australian universities such as La Trobe University and Deakin University were linked to Limerck University from Ireland. Other links between universities from different countries are depicted in Figure S4.B. Figure S4.C shows 5 clusters representing collaboration between countries. The most central clusters reveal USA and Australia as the most collaborative countries. The main between-country collaborations, depicted by the thickness of the links between nodes, involved mainly USA/China, USA/South Korea, and Australia/Spain (Figures S4.C and S5).

Themes explored in the systematic reviews were analyzed based on indexed keywords. The analysis revealed that, other than Parkinson’s disease, exercise,people, and humans, gait, balance, and quality of life were also indexed as keywords in the studies. These words express some of the outcomes assessed in the systematic reviews (Figure S6). Most of these words represent the themes of systematic reviews conducted mostly from 2016 to 2020, while physical therapy, for instance, has been proposed and assessed as an intervention for people with PD since 2012 (Figure S7).

The bibliometric analysis revealed 269 authors’ keywords. Thematic evolution analysis (Figure 1) highlighted the co-occurrence of authors’ keywords that expressed various types of exercise interventions and outcomes assessed, since the population and the type of study were the same.

In the first subperiod, 1 main theme emerged (Figure 1A, 1B), being expressed by the Parkinson’s disease cluster (centrality: 1.4; density: 247.9) and composed of the words Parkinson’s disease, exercise, and systematic review. In the second subperiod, the 5 main themes were Parkinson’s disease, exercise therapy, rehabilitation, humans, and parkinsonism (Figure 1C). PD was the most central, transversal theme (centrality: 5.1; density: 325.2), consisting mainly of the words Parkinson’s disease, exercise, balance, gait, and systematic review, while exercise therapy was the motor theme (centrality: 4.6; density: 379.5), highlighting Parkinson’s disease and exercise therapy. During this subperiod, the term quality of life showed up in the rehabilitation cluster, appearing in the lower-left quadrant.

The third subperiod was the most productive of systematic reviews addressing physical exercise interventions for people with PD (Figure 1D). The most central theme in this subperiod was Parkinson’s disease (centrality: 8.2; density: 259.5), highlighting exercise, rehabilitation, physical therapy, and physical activity as interventions, andfreezing of gait, mobility, and quality of life as outcomes. The motor theme was systematic review (centrality: 4.8; density: 447.3), which was linked to the central theme and addressed dance as an intervention and mood, cognition, and sleep as outcomes. Another Parkinson’s disease cluster resulting from the exercise therapy cluster of the second subperiod presented Tai Chi, Yoga, Qigong, and virtual reality as interventions.

The most central theme in the fourth subperiod was rehabilitation (centrality: 7.0; density: 251.9) (Figure 1E), which consisted mainly of the words rehabilitation, systematic review, meta-analysis, exercise, Parkinson’s disease, and pain that came from the Parkinson’s disease and systematic review clusters of the third subperiod. It was closely linked to the Parkinson’s disease clusters, one of which was also rather central and more densely developed (centrality: 5.2; density: 294.0). This cluster involved the co-occurrence of Parkinson’s disease, gait, aerobic exercise,physical activity, quality of life, multiple sclerosis, postural balance, and resistance training. The higher density may be interpreted as a potential theme for further exploration. Two other themes were in the upper-left quadrant, with a Callon density of 350 and low centrality, meaning that they had been sufficiently explored and have unimportant external links. The stroke theme consisted of virtual reality exposure therapy and telerehabilitation, which were linked to other clusters by the term stroke. The physical cluster involved insomnia, fall prevention, and therapy and was linked to the main themes by the term physical.

DISCUSSION

The increasing number of older people around the world has raised the global burden of PD by 20%, with a more than doubling of the number of cases in 2016 compared to 1990.7 Also, disability-adjusted life years (DALYs), which are a sum of the years lived with disability and years of life lost, were 2.5 times higher in 2016 than in 1990.7 Additionally, high direct and indirect costs and resource use have been associated with assistance to people with PD, mainly in advanced and late stages.23 This review identified and characterized the effort to synthesize evidence by means of systematic reviews of the effects of physical exercise on people with PD. Its results reflect the impact imposed by PD on the society globally, since more than 100 studies have attempted to synthesize evidence related to the effects of physical exercise on people with PD since 2005 (Table S2). Also, the average publication time and annual growth rate reveal that these attempts are recent and growing in number (Table S2).

The first systematic review identified here analyzing the effects of physical exercise on PD was published in 2005. The movement towards evidence-based practice in health care began in the medical field in the 1980s, a period that also marked the beginning of the synthesis of evidence from systematic reviews.19 Yet, other health fields joined this movement later, in the early 2000s. Therefore, the time of the first publication in the field agrees with the moment that evidence-based health care became more widespread.

More than 650 authors were associated with the published studies. The average number of authors was 4.5, and only 1 study was single authored. This study may be considered an anomaly, since a minimum of 2 authors are expected in the development of a systematic review.24 The main guidelines for conducting systematic reviews indicate that these are team-performed studies,24,25 requiring at least 2 authors for the phases of study selection and data extraction. In addition, a systematic review team requires experts in epidemiology and statistics, in the subject being investigated, and in literature search. Consequently, the average number of authors found may be explained by team demands to produce the type of study under analysis.

Clinical Rehabilitation and PLoS One were the most relevant journals, with 8 systematic reviews of the effects of physical exercise interventions on people with PD. Clinical Rehabilitation is a peer-reviewed, multiprofessional journal that publishes highly ranked articles on research and scientific discussions about disability and rehabilitation. It combines the theoretical aspects and practical application of results mainly from studies on the effectiveness of therapeutic interventions and evaluation of new methodologies.26 PLoS One publishes multidisciplinary research, including systematic reviews in the biomedical sciences. It provides open access to its articles, which may contribute to the dissemination and reading of the information.

The most cited journal was Movement Disorders, which is managed by the International Parkinson and Movement Disorder Society (MDS), the largest society of physicians, researchers, and human movement professionals. The journal’s scope involves movement in PD, movement disorders, neurodegeneration, genetic alterations, hyperkinetic movement, and motor control abnormalities.27 Both journal scope and prestige have been shown to be positively correlated with citations.28

The most productive institution was the Queensland University of Technology with 12 published studies, followed by the Henan University of Chinese Medicine, IRCCS San Raffaele Science Institute, and La Trobe University with the production of 9 studies each. The most cited institutions were the University of Exeter, with 3 studies, and Vrije University, with 2 studies. These institutions happened to produce some of the first studies on the issue and to be cited by the following studies.

When analyzing the most productive countries, those with long-established older populations stand out. Also, the countries responsible for the main methodological recommendations in systematic reviews (United Kingdom, Canada, and Australia) are among the 10 most productive countries (Table 3). The exception is Brazil, which was the most productive country despite the comparatively smaller older population. Brazil was the seventh most cited country, which may be explained by the recent publication of a large number of studies (Figure S3). The United Kingdom, Australia, and Netherlands, with older studies, had the highest number of citations (Figure S3).

Scientific collaboration may be analyzed at individual, cross-national, and multinational levels.29 The individual level refers to collaboration between individual scientists, while the cross-national level characterizes the collaboration between affiliated scientists in different countries and the multinational level characterizes the collaboration between more than 2 countries.29 Most of the research collaboration at the individual level was observed between authors from the same research group or country (Figure S4A). Most of the between-country collaboration involved a single article. Greater collaboration involved mainly USA/China, USA/South Korea, and Australia/Spain (Figure S5). Noteworthy, training and a learning curve are required to develop a qualified review team, which would benefit from the collaboration between groups. Besides, given that PD is a global reality that poses health-care, emotional, and economic challenges,7 the effort to synthesize evidence and to develop and apply guidelines could be potentiated by the collaboration between countries. This collaboration behavior has been previously identified in other fields of study and is characterized as an obstacle to the progress of the understanding of the issue under study.30

Systematic reviews of the effects of physical exercise on people with PD were mostly published in European countries, with increased life expectancy.9 USA and China also have a considerable older adult population, and in both, life expectancy and aging have been positively correlated with PD.7 Even Brazil, which produced 19 reviews and whose population’s life expectancy is not as high as that of the abovementioned countries, has estimated that approximately 200,000 people will develop PD,31 reinforcing the impact of this increasingly occurring and highly demanding disease.

Co-word analysis was performed to determine the thematic evolution of the studies during the 2005–2022 time span. In such analysis, clusters of co-words and their interconnections are considered themes and labelled after the most significant keyword, usually the most central one in the thematic network.32 Also, the importance of the theme in the field is put into perspective based on its evolutionary life cycle, which involves birth, growth, maturity, and decay.33 The themes expressed in the thematic evolution analysis were limited by the structured nature of the question and the PCC framework (Population, Concept, and Context) of the scoping review that refers to the study design, type of interventions being assessed, and the population involved. Noteworthy, the first subperiod depicted one main theme (Figure 1A and 1B), labelled Parkinson’s disease and consisting of the words Parkinson’s disease, exercise, and systematic review, which precisely represented the population under study, the type of intervention, and the study design.

In the second subperiod (Figure 1C), the number of themes increased and the most densely studied theme was the association between Parkinson’s disease and exercise therapy. However, the second most studied theme during the 2011–2015 period involved rehabilitation, which was closer to the main theme than the one involving exercise therapy. It may be interpreted as a growing theme that happens to comprise the main topic in the third subperiod and involves interventions such as dance, music, rhythm, and water-based exercise, along with quality of life as an outcome measure. Therefore, there has been a shift of attention from managing basic signs of PD to providing a more active life through physical activities that do not necessarily characterize dose-prescribed exercise.

Parkinson’s disease was the transversal theme of the third subperiod (Figure 1D), composed mainly of Parkinson’s disease, exercise, and rehabilitation. The 2016-2020 period revealed further attempts to synthesize evidence on the effect of exercise on PD, as expressed by the systematic review topic, consisting mainly of systematic review and meta-analysis. It also showed two closely related topics that involved Tai Chi, Yoga, virtual reality, Nintendo Wii, physical therapy, and treadmill. Aerobic exercise, aquatic therapy, Qigong, and walking endurance made up the topic balance, with lower centrality during this period. The analysis of the most recent period, from 2020 to 2022, revealed rehabilitation as the central theme. It also showed an increasing centrality of the words aerobic exercise, physical activity, and resistance training as interventions and gait, postural balance, and quality of life as outcome measures.

Study limitations

Limitations of the study were those inherent to a bibliometric analysis, which, in this case, involved a small number of databases searched for bibliometric purposes and was restricted to bibliometric outcomes. This means that the exhaustive search and study selection based on full-text reading used in the umbrella review was not reproduced in the bibliometric review. The databases searched are common in the biomedical field33 and allowed the identification of 87.4% of the systematic reviews on the theme. This study, though, avoided a common drawback of bibliometric studies, which is false-positive results generated by broad research queries.34 The focus of the review, which was limited to clinical trials involving physical exercise interventions for people with PD, and the individual selection of studies resulted in the inclusion of only studies that met the inclusion criteria.

This review does not address the potential impact of the included systematic reviews, since their content or methodological quality is better assessed in an umbrella review or overview. Although it suggests that Global North countries have dealt with PD longer than other countries, differences or similarities between countries in the effects of exercise on people with PD would be better represented by the primary studies included in the systematic reviews. Still, this review highlights the need for a global effort to identify gaps in the knowledge of exercise effects on people with PD and to propose a global guideline to enhance exercise prescription based on solid evidence.

CONCLUSION

A considerable number of systematic reviews addressing the effects of physical exercise interventions on people with PD have been published since the mid-2000s. Additionally, an increasing trend of evidence synthesis production is observed in recent years. Countries with long-established older populations were responsible for earlier publications, while countries with shorter life expectancy have increased the number of publications recently. Enhanced collaboration between countries could be established focusing on standardized guidelines and exercise prescription, since PD represents a major problem for the world’s aging population.

Acknowledgements

the authors thank the information specialist Cristiane Sinimbu Sanchez for her help developing and testing the search strategies.

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Notes

Author notes

Correspondence data Sinval Adalberto Rodrigues-Junior – Rua Servidão Anjo da Guarda, 295-D – Efapi – CEP 89809-000 – Chapecó (SC), Brazil. E-mail: rodriguesjunior.sa@unochapeco.edu.br

Conflict of interest declaration

IR