The effect of a multi-modal boxing exercise program on cognitive locomotor tasks and gait in persons with Parkinson disease

Abstract

BACKGROUND:

Parkinson disease (PD) is a progressive neurological disease resulting in motor impairments, postural instability, and gait alterations which may result in self-care limitations and loss of mobility reducing quality of life.

OBJECTIVE:

This study’s purpose was to determine the impact of a community-based boxing program on gait parameters, dual task and backwards walking in individuals with PD.

METHODS:

This study included 26 community dwelling individuals with PD who participated in 12-week boxing classes (1 hour, 2 times a week). The focus was on upper/lower extremity exercises using punching bags, agility drills, and strengthening activities. Pre/post testing was performed for dual task and gait parameters and was analyzed using t-tests.

RESULTS:

Analysis of the scores indicated participants performed significantly better at post-test compared to pre-test on self-selected walking velocity (P = 0.041), cadence (P = 0.021); backwards walking velocity (P = 0.003), step length (P = 0.022); dual task walking velocity (P = 0.044), step length (P = 0.023), and gait variability index (P = 0.008). No significant differences for fast walking.

CONCLUSIONS:

Multi-modal boxing produced improvements in gait velocity, dual task velocity, step length, and gait variability, as well as backwards walking velocity and step length. These improvements may impact independence with functional mobility and may improve safety but require further studies.

Keywords

Parkinson’s disease gait boxing community program physical therapy rehabilitation

1 Introduction

Parkinson disease (PD) is a progressive neurological disease that results in motor impairments, postural instability, and gait alterations (Nallegowda et al., 2004). As a result, individuals with PD often have self-care limitations and loss of mobility reducing quality of life (QoL) (Soh et al., 2013). In particular, changes to gait are a red flag for disability (Shulman et al., 2008). For individuals living with PD, gait impairments lead to reduced mobility often with subsequent reductions in quality of life (Curtze, et al., 2016). Typical gait changes related to PD include decreased stride length, slowness of gait, increased double support time, and reduced arm swing (Amano et al., 2013). Additionally, impairments in backwards walking and gait with a dual task are common impairments for persons with PD and also serve as effective predictors of falls (Hackney & Earhart, 2009) and detrimental mobility changes (Fritz, et al., 2013; Heinzel et al., 2016). Dual tasks and backward walking are critically important to performing daily activities such as backing away from the sink, carrying groceries, or simply walking while in a conversation. As a result, treatment for individuals with PD is frequently focused on maintaining gait mechanics often in multiple directions such a backwards or with dual task requirements (Bryant, et al., 2016; Strouwen et al., 2017). To compliment typical gait training treatment of these impairments often includes visual cues, treadmill training, exercise (Morris et al., 2010). King et al. suggest that PD, resulting from damage to the basal ganglia, impacts mobility (King & Horak, 2009). They report that mobility requires dynamic neural control to quickly and effectively adapt locomotion, balance, and postural transitions to changing environmental and task conditions. Such dynamic control requires sensorimotor agility, which involves coordination of complex sequences of movements, ongoing evaluation of environmental cues and contexts, the ability to quickly switch motor programs when environmental conditions change, and the ability to maintain safe mobility during multiple motor and cognitive tasks (King et al., 2009). Boxing has potential therapeutic value secondary to a high degree of variability in cognitive and motor planning, total body movement in multiple planes of motion, and upper extremity punching motions in combination with lower extremity footwork in multiple directions (King et al., 2009). While non-contact boxing is increasingly growing in popularity for persons with PD, there is limited evidence available on its impact on gait (Combs et al., 2013). One small case series examining improvements for mobility outcome (the Times Up and Go) and gait endurance (6 Minute Walk Test) (Combs et al., 2011). In addition, a randomized control trial did not find a difference between groups (general exercise vs boxing) in gait speed and gait endurance while there was a within group difference in the boxing group over 12-weeks (Combs et al., 2013). These studies have examined the impact of boxing on mobility and gait endurance but to our knowledge, no one has studied standard gait speed, dual task or backwards walking. Understanding the impact of boxing on gait speed, dual task and backwards walking may affect safety and mobility in individuals with PD while providing guidance on interventions.

The purpose of this study is to determine the impact of a community-based comprehensive boxing program (non-task specific to gait) on specific spatial-temporal gait parameters during normal walking, cognitive locomotor dual task, and backwards walking in individuals with mild to moderate PD. This study hypothesizes that engagement in non-contact boxing training interventions will positively impact gait impairment as measured by clinical outcome measurements.

2 Methods

2.1 Participants

This study is a pre-post intervention study and included a sample of convenience of community dwelling individuals with PD living in Dallas, TX, USA. The study was designed to be conducted through a 12-week boxing program. There were 4, 12-week sessions included in this manuscript. For each session, a new cohort consisting of 8–10 participants started and completed the session together. It was determined a priori that participants who attended less than 19 of 24 sessions were excluded from data analysis. Inclusion criteria included: confirmed diagnosis of Parkinson disease in mild to moderate stages of PD (Hoehn & Yahr 1–3, a widely used descriptive scale which defines broad categories of motor function in PD with 1-2 being mild and 4-5 advanced disease) (Goetz et al., 2004) by a licensed physician, no greater than 85 years of age, had the ability to follow two and three-step verbal commands, possessed access to adequate transportation to attend classes, obtained medical clearance from a physician for moderate to high intensity exercise, and had a Body Mass Index measurement (BMI) below 40. Exclusion criteria included those who did not speak English as not all outcome measures were translated into languages other than English and the need to dynamically instruct and communicate during fast paced exercise for safety and effectiveness of the community program. The study was approved by the Institutional Review Board at UT Southwestern Medical Center. Prior to participation informed consent was obtained from each individual.

2.2 Outcome measures

Outcome measures were taken before and after completion of the 12-week session utilizing the Zeno walkway. This mat consists of a 20-foot walkway embedded with multiple levels of sensors to record temporal spatial data. Data is processed using the PKMAS Software (ProtoKinetics, Havertown, PA, USA). The validity and reliability of the Zeno Mat system has previously been established for temporal spatial characteristics (Egerton, Thingstad, & Helbostad, 2014; Vallabhajosula, Humphrey, Cook, & Freund, 2019). The gait variables included velocity, cadence, step length, single limb support, double limb support, and the enhanced gait variability index. The enhanced gait variability index (EGVI) incorporated in the PKMAS software is a unit less conglomerate measure that provides a composite score relating the variability measured in spatiotemporal variables during gait to a reference standard with a mean of 100 and standard deviation of 10 (Gouelle, Rennie, Clark, Megrot, & Balasubramanian, 2018). There are five gait measures utilized to calculate EGVI: step length (cm), step time (swing), stance time, single limb support, and velocity as a measure of gait stability and variability. The EGVI is most appropriate to be utilized for self-selected and not fast (for norms) for comparison to the reference standard. An EGVI value < 100 corresponds to less variability than the reference standard,>100 indicates a greater step-to-step variability composite score than the reference standard. There were four testing conditions: self-selected walking (SSW), fast walking (FW), backwards walking (BW), and a counting dual task while walking (DT).

Participants ambulated 4 passes on the 20-foot mat for both self-selected and fast walking. Instructions for the self-selected walking were to walk at a comfortable pace as if they were walking down the hall. For fast walking, they were told to walk as fast as they safely could without running. Backwards and dual task walking trials included 2 passes on the 20 foot mat. This was limited secondary to activity difficulty and to prevent fatigue. Instructions for backwards and dual task walking was to walk at a comfortable pace. For the dual task trial, individuals were asked to count backwards by 3’s from 100. This test was chosen as it has previously resulted in significant gait interference in people with PD when combined with walking (Fok, Farrell, & McMeeken, 2010).

2.3 Interventions

Classes occurred for 12 weeks, twice weekly for 60-minute sessions and were held at a community church. During the class, the participants were referred to as fighters and the students were referred to as coaches to instill a sense of ability and importance for both groups. The classes were designed to provide general strengthening, balance, and PD specific interventions (large amplitude, high repetitions) and were not specifically focused on gait. The classes consisted of the following: a dynamic group warm up (5 minutes), education review on techniques and proper biomechanics (5 minutes), ten rounds of repetition of an activity (2.5 minutes each – 25 minutes). Early on, the focus of each round alternated between upper and lower extremity activities. As the program progressed over 12 weeks, activities were combined to include leg strength with punching combinations. A 1-minute rest break for fighters was provided after each 2.5-minute round in addition to a midpoint water break (3–5 minutes). A seated trunk and lower extremity stretching session with patient education and group discussion ( 10 minutes) completed each class. Intensity was monitored through The Modified Borg Rating of Perceived Exertion Scale (RPE). Fighters were encouraged to self-monitor exercise intensity, targeting an intensity level between 4/10 to 7/10. This was suggested but was not recorded. This suggested intensity was commonly seen to induce mild shortness of breath, sweating, and mild recoverable fatigue. The rest of 1 minute between rounds was sufficient to allow for continued participation. For details on each component of class, its purpose/goals, areas of emphasis, see Table 1.

Table 1
Boxing intervention

Activity Goal(s) Key points of emphasis

Dynamic group warm up •Emphasizing big, dynamic movements which encourage activating muscles of the posterior chain. 1. Prepare the body and mind for exercise 2. Reinforce rationale behind exercise selection for the class 3. Remind fighters of common compensatory movements to avoid •Education on goals or themes for the class •Large amplitude movements •Dynamic weight shifting •Dynamic flexibility •Starting and stopping large-amplitude movements

Punching Combinations: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •Simple repetitions of basic punches with varying punch selection, varying punch location, and varying “footwork” •Procedural memory challenges created through multi-step approaches to combinations •Difficulty increased gradually through addition of stance changes, side stepping, varying timing, etc. 1. Build/strengthen movement patterns with proper body mechanics 2. Build cognitive load by encouraging fighters to focus on improving one aspect of technique at a time – adding other areas of focus after mastery of previous aspect 3. Gradually push VO2 Max through increasing aerobic intensity gradually, as tolerated, over a period of many weeks 4. Encourage intensive focus on controlled movements during aerobic exercise 5. Encourage coordination of multiplanar, symmetrical, BUE movements •Intensity – reaching and staying within a 4/10 to 7/10 intensity on modified BORG RPE Scale •Biomechanics education for minimizing injury •Repetition of correct mechanics more than power or speed •Dynamic reaching •Varying punch cadence •Varying punch location •Upright posture •Proper stance alignment •Proper footwork (e.g. not crossing feet over during side steps, maintaining wide BOS, keeping a staggered stance) •Pulling punches all the way back to “fight stance” starting position •to encourage continued focus on controlled movements

Leg/Hip Strength Exercises: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •SLE or BLE exercises in weightbearing as tolerated with use of support from punching bag or volunteer coach as needed 1. Build/strengthen movement patterns with proper body mechanics 2. Improving functional leg strength 3. Addressing chronically weakened BLE muscle groups 4. Minimizing compensatory movement strategies 5. Building hip stability 6. Minimizing incidence of knee pain 7. Maintaining COM over BOS 8. Building activity tolerance in weight-bearing activity •Intensity – reaching and staying within a 4/10 to 7/10 intensity on modified BORG RPE Scale •Eccentric control •Postural alignment during strength activities •Repetition of correct mechanics more than power or speed

Footwork: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •Cone drills •Tape walking Punches or dual task challenges added as tolerated 1. Dynamic balance 2. Time on task challenging balance in multiple directions 3. Encouraging starting and stopping with good control 4. Encouraging awareness of COM over BOS •Posture •Step length •Sequence and location of foot placement •Pausing with control before advancing into the next step

Core Strength and Spinal Mobility: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •Emphasizing floor transfers •Challenging core strength and mobility in multiple planes •Modifications could include leaning against a wall, sitting on a chair, or enabling participants to transfer with use of a railing, chair, etc. 1. Thoracic spine mobility 2. Core stability 3. Endurance of type 1 core musculature 4. UE weightbearing activity 5. Reduced fear of being on the floor 6. Strategies to rise from the floor •Biomechanics •Strategies for managing cramps (commonly with bridging)•Neutral head posture during activity/Preventing excessive cervical flexion•Encouraging breathing/avoiding Valsalva•Assisting as needed with floor transfers•Reducing risks of shoulder impingement during UE weightbearing•Education on pain vs. discomfort

Cool Down and Connect •Seated BLE stretching and T-spine mobility: HS, Piriformis, Lumbar spine rotation, Upper trap stretching, Cat/Cow, etc. •Group discussion: symptoms, previous treatment, recommendations from their neurologists/Movement Disorder Specialists, any improvements or changing symptoms, appropriate jokes, etc. •Patient education: PD community resources, role of exercise in managing symptom severity, value of staying active, strategies for self-management, differentiating pain from muscular fatigue or poor biomechanics 1. Improve mobility and flexibility of chronically tight joints and muscles 2. Encourage continued participation of fighters in the program 3. Emphasize aspects of treating symptoms that are within their locus of control 4. Increase awareness of community resources to improve quality of life 5. Encourage hard work or triumph over previous challenges 6. Recognize effort publicly to peers 7. Foster a sense of community 8. Drive consistency •Recognize people who challenged their “comfort zone” •Encourage fighters to focus on what is improving •Discuss strategies for working around pain without quitting or making existing aches/pains worse •Continue education of the role of physical activity in managing symptoms •Continue education on rationale behind exercises selected •Continue education on common resources or strategies for managing other PD-related symptoms

Activity	Goal(s)	Key points of emphasis
Dynamic group warm up •Emphasizing big, dynamic movements which encourage activating muscles of the posterior chain.	1. Prepare the body and mind for exercise 2. Reinforce rationale behind exercise selection for the class 3. Remind fighters of common compensatory movements to avoid	•Education on goals or themes for the class •Large amplitude movements •Dynamic weight shifting •Dynamic flexibility •Starting and stopping large-amplitude movements
Punching Combinations: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •Simple repetitions of basic punches with varying punch selection, varying punch location, and varying “footwork” •Procedural memory challenges created through multi-step approaches to combinations •Difficulty increased gradually through addition of stance changes, side stepping, varying timing, etc.	1. Build/strengthen movement patterns with proper body mechanics 2. Build cognitive load by encouraging fighters to focus on improving one aspect of technique at a time – adding other areas of focus after mastery of previous aspect 3. Gradually push VO2 Max through increasing aerobic intensity gradually, as tolerated, over a period of many weeks 4. Encourage intensive focus on controlled movements during aerobic exercise 5. Encourage coordination of multiplanar, symmetrical, BUE movements	•Intensity – reaching and staying within a 4/10 to 7/10 intensity on modified BORG RPE Scale •Biomechanics education for minimizing injury •Repetition of correct mechanics more than power or speed •Dynamic reaching •Varying punch cadence •Varying punch location •Upright posture •Proper stance alignment •Proper footwork (e.g. not crossing feet over during side steps, maintaining wide BOS, keeping a staggered stance) •Pulling punches all the way back to “fight stance” starting position •to encourage continued focus on controlled movements
Leg/Hip Strength Exercises: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •SLE or BLE exercises in weightbearing as tolerated with use of support from punching bag or volunteer coach as needed	1. Build/strengthen movement patterns with proper body mechanics 2. Improving functional leg strength 3. Addressing chronically weakened BLE muscle groups 4. Minimizing compensatory movement strategies 5. Building hip stability 6. Minimizing incidence of knee pain 7. Maintaining COM over BOS 8. Building activity tolerance in weight-bearing activity	•Intensity – reaching and staying within a 4/10 to 7/10 intensity on modified BORG RPE Scale •Eccentric control •Postural alignment during strength activities •Repetition of correct mechanics more than power or speed
Footwork: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •Cone drills •Tape walking Punches or dual task challenges added as tolerated	1. Dynamic balance 2. Time on task challenging balance in multiple directions 3. Encouraging starting and stopping with good control 4. Encouraging awareness of COM over BOS	•Posture •Step length •Sequence and location of foot placement •Pausing with control before advancing into the next step
Core Strength and Spinal Mobility: (varying by round) – modifications made as needed – starting simply and gradually increasing difficulty •Emphasizing floor transfers •Challenging core strength and mobility in multiple planes •Modifications could include leaning against a wall, sitting on a chair, or enabling participants to transfer with use of a railing, chair, etc.	1. Thoracic spine mobility 2. Core stability 3. Endurance of type 1 core musculature 4. UE weightbearing activity 5. Reduced fear of being on the floor 6. Strategies to rise from the floor	•Biomechanics •Strategies for managing cramps (commonly with bridging)•Neutral head posture during activity/Preventing excessive cervical flexion•Encouraging breathing/avoiding Valsalva•Assisting as needed with floor transfers•Reducing risks of shoulder impingement during UE weightbearing•Education on pain vs. discomfort
Cool Down and Connect •Seated BLE stretching and T-spine mobility: HS, Piriformis, Lumbar spine rotation, Upper trap stretching, Cat/Cow, etc. •Group discussion: symptoms, previous treatment, recommendations from their neurologists/Movement Disorder Specialists, any improvements or changing symptoms, appropriate jokes, etc. •Patient education: PD community resources, role of exercise in managing symptom severity, value of staying active, strategies for self-management, differentiating pain from muscular fatigue or poor biomechanics	1. Improve mobility and flexibility of chronically tight joints and muscles 2. Encourage continued participation of fighters in the program 3. Emphasize aspects of treating symptoms that are within their locus of control 4. Increase awareness of community resources to improve quality of life 5. Encourage hard work or triumph over previous challenges 6. Recognize effort publicly to peers 7. Foster a sense of community 8. Drive consistency	•Recognize people who challenged their “comfort zone” •Encourage fighters to focus on what is improving •Discuss strategies for working around pain without quitting or making existing aches/pains worse •Continue education of the role of physical activity in managing symptoms •Continue education on rationale behind exercises selected •Continue education on common resources or strategies for managing other PD-related symptoms

A licensed physical therapist who was also an experienced martial arts fight trainer designed the program to bring unique aspects of boxing and his understanding of PD from clinical perspective to develop a program uniquely designed to improve mobility. The fighters were provided primary instruction from a licensed physical therapist as well as doctoral trained physical therapy students in the UT Southwestern DPT program. Often in the community, programs limited in the participant to coaching ratio and do not have the advantage of coaching by individuals with doctoral training. Personal coaching and safety monitoring were provided based on level of independence from doctoral physical therapy students. Coaches provided gait belt support, verbal cues, tactile cues, and visual cues as needed. Coaches were trained on guarding, boxing techniques, and how to provide verbal cues for safety and exercise intensity. Fighters are also encouraged to use the punching bags (free-standing Wavemaster XL punching bags with adjustable height and water-filled bases) for additional support for balance during activities if needed. Class format intentionally changed over the course of the 12-week period, initially starting with emphasis on techniques and biomechanics and motor learning of boxing techniques. As techniques were mastered (measured by ability to maintain proper biomechanics at higher intensity levels), exercise intensity was gradually increased by increasing the speed and power of punching and footwork techniques. Similarly, as tolerated by fighters, complexity of exercises were increased (more UE/LE combination exercise, variable movements, longer combinations) while verbal cues, tactile cues, and visual cues were gradually reduced (as participants moved from the cognitive stage of motor learning to automatic). Even though the 12-week course was designed to encourage progression, coaches had the ability to work with individuals fighters to individually progress considering their abilities and safety.

2.4 Data analysis

Descriptive statistics (mean and SD) was generated for each dependent variable. Data was checked for normality utilizing Shapiro-Wilks test of normality. If the data was not normally distributed, a non-parametric Wilcoxon signed rank test was performed when appropriate. The results of the parametric and non-parametric tests are reported. The differences between the pre-test and post-test outcomes were analyzed with a paired-t test or Wilcoxon signed rank test using IBM SPSS Statistics ver. 26.0 (IBM Co., Armonk, NY, USA). All statistical tests used a significance level of p < 0.05.

3 Results

A total of 35 participants with PD were recruited for this study and 28 completed the determined number of training sessions for protocol completion however 2 were not able to undergo testing secondary to medical complications. Of the seven individuals who dropped out, reasons noted included transportation, other health conditions preventing them from exercising, and family emergencies. There were no adverse boxing events that impacted attendance. The demographic details of the 26 participants that completed the protocol are presented in Table 2. Analysis of the scores indicated that the participants performed significantly better at post-test compared to pre-test with respect to self-selected walking velocity (P = 0.041) and cadence (P = 0.021) (Table 3). For fast walking, there were no significant differences (Table 4). The participants performed significantly better at post-test for backwards walking velocity (P = 0.003) and step length (P = 0.022) (Table 5). Participants also demonstrated significant improvement in post-test for dual task walking velocity (P = 0.044), step length (P = 0.023), and enhanced gait variability index (P = .008) (Table 6).

Table 2
Participant demographics

Age Male/Female Years since diagnosis Hoehn and Yahr stage BMI Average sessions

68.38 20/6 4.75 2.12 26.2 21/24

Age	Male/Female	Years since diagnosis	Hoehn and Yahr stage	BMI	Average sessions
68.38	20/6	4.75	2.12	26.2	21/24

Table 3

Self-selected gait parameters

	Velocity	Step length	Cadence	Single support (%)	Double support (%)	Enhanced gait variability index
	(cm/sec)	(cm)
Initial	105.43 (21.60)	60.35 (10.58)	103.51 (9.99)	34.30 (1.73)	31.25 (3.38)	119.79 (12.07)
Post	110.45 (20.76)	61.64 (10.09)	106.48 (9.27)	34.60 (1.35)	30.75 (2.66)	116.88 (11.57)
P value	0.041	0.125	0.021	0.143	0.197	0.112

Table 4

Fast gait parameters

	Velocity	Step length	Cadence	Single support	Double support
Initial	144.05 (34.84)	70.28 (13.55)	121.47 (13.68)	36.11 (1.89)	27.66 (3.93)
Post	144.71 (34.35)	70.14 (12.69)	122.34 (14.16	36.17 (1.76)	27.34 (3.62)
P value	0.856	0.868	0.337	0.534	0.341

Table 5

Backwards walking

	Velocity	Step length	Cadence	Single support	Double support	Enhanced gait variability index
Initial	62.35 (26.31)	36.27 (13.33)	98.27 (21.85)	31.80 (5.04)	36.41 (10.19)	137.13 (9.37)
Post	68.52 (27.95)	39.93 (14.36)	101.65 (22.21)	32.25 (4.38)	35.62 (8.70)	136.15 (11.25)
P value	0.003	0.022	0.367	0.313	0.456	0.414

Table 6

Dual task gait

	Velocity	Step length	Cadence	Single support	Double support	Enhanced gait variability index
Initial	87.95 (30.42)	55.95 (13.03)	89.94 (22.45)	32.54 (4.66)	35.01 (9.56)	131.97 (17.10)
Post	99.41 (30.34)	58.77 (12.89)	97.52 (15.31)	33.52 (2.66)	32.92 (5.38)	124.50 (12.07)
P value	0.044	0.023	0.073	0.034	0.034	0.008

4 Discussion

The purpose of this study is to determine the impact of a community-based comprehensive boxing program (non-task specific to gait) to impact gait parameters, dual task and backwards walking associated with mild to moderate PD. The main findings included improvements in selected variables during self-selected walking, cognitive dual task during gait, and backwards walking with the completion of a community based multi-faceted exercise program. Previous studies have also seen increases in walking velocity for boxing participants compared to traditional exercise classes (Combs et al., 2013). In addition, improvements were found on other gait related outcome measures such as the 6 MWT after a community boxing program (Combs et al., 2013; Combs et al., 2011). For self-selected walking in this study’s cohort, step length did not change whereas cadence was significantly faster after completion of the 12-week program. Overall, this cohort had mildly higher mean self-selected velocity at baseline than established for individuals with a similar Hoehn and Yahr score (Hass et al., 2012) and made further significant increases in velocity and cadence with the boxing program. This cohort used a faster cadence rather than longer step lengths to increase velocity at post testing. Early work related to gait in PD showed that despite stage of PD, individuals maintain the ability to modulate or increase their cadence whereas they are unable to generate longer step length (Morris et al., 1994) as is seen in this cohort. However, gait velocity is most impacted by a reduction of stride length (Morris et al., 1994) which did not change for this group. Standard boxing training is not a task specific activity for gait, which may account for the lack of change to step length. Facilitating an increase in step length may require more focal use of external cues during training (Keus et al., 2007) than what was provided in this group class. It is possible that participants felt more confident and stable and thus showed faster cadence secondary to progress related to balance challenges or strength gains (Olson, Lockhart, & Lieberman, 2019). Additionally, the variables for fast walking were not substantially different from the pre-testing to post testing which may be due the difficulty of the participants because maximal ability did not change. This could be due to high maximal velocities from the beginning. The boxing classes were not designed to challenge maximal performance, if maximal velocity was a critical component, higher intensity and task focused activities could be integrated into programming.

In this cohort, the community involvement in an organized progressive boxing program did result in improvements in velocity, step length, single limb support, double limb support and gait variability during a cognitive challenge with the DT walking. These improvements have considerable importance considering the correlation of dual task gait in PD to increased risk of falling (Heinzel et al., 2016) and reduced functional mobility (Fuller et al., 2013). Previous studies also report improvements in DT gait velocity after consecutive and integrated specific training for DT performance (Strouwen et al., 2017; Yang 2019). The DT improvements in the current study were likely the result of the natural repetitive variability of the demands of boxing training. Boxing training requires diversity of motor planning (such as changing combinations), complexity of drills (coordinating UE and LE movements with a dual task such as counting), and dynamic variability of tracking targets (as is required with sparring) as well as cognitively processing further commands from coaches during a mobility task. The innate requirement of boxing drills challenges dynamic neural control and multiple neuromechanical tasks resulting in these positive outcomes. In addition to impacting gait velocity as previously discussed, cognitive challenges during gait increase gait variability (utilizing stride, double support and swing times) and results in an unstable gait pattern and thus increased falls for individuals with PD (Hausdorff, Balash, & Giladi, 2003). For dual task outcomes in this boxing program, the EGVI improvements indicated a decrease in variability. Improvements in single limb support, double limb support and EGVI for dual task gait, such as seen in this study, may relate to improved stability and safety with mobility (Heinzel et al., 2016). These improvements support that boxing is a potential intervention to improve DT abilities and warrants attention in future research.

This cohort had improvements in backwards walking velocity and step length after the boxing program. Backwards walking has been found to be an effective indicator of falls (Hackney & Earhart, 2009) and mobility changes (Fritz et al., 2013; Gilmore et al., 2019; Hackney & Earhart, 2009) thus the improvements attained in this study may translate to decreased falls and improved mobility changes. A previous study of forward and backward gait on the treadmill noted improvements in backwards gait velocity and stride length in individuals with PD (Bryant et al., 2016). Although the current study was not as task-specific as using a treadmill, boxing may allow for sufficient practice of backwards stepping during bag activities and cone drills as well as changing directions to improve backwards walking performance. Backwards walking over ground was previously found to be more effective at improving cadence and stride length than forward walking (Grobbelaar, Venter, & Welman, 2017) and thus these changes could also improve cadence of forward walking in this cohort. In addition, improved DT abilities may also improve backwards walking (Tseng, Jeng, & Yuan, 2012) indicating a potential relationship between improvements in DT testing and backwards walking for the current study. The new knowledge form this study adds to the limited literature on backwards gait at this time and further studies should explore the impact of exercise of backwards walking and as a result functional measures and reduction of falls.

This community based boxing program resulted in improvements in self-selected walking, DT gait and backwards walking. These improvements may be the result of the intense repetitious, multi-modal interventions provided during the program. Boxing is a higher intensity activity with increased speed of movement with reactionary movements and postures which may therefore give individuals a dynamic challenge in motor and cognitive components increasing both capabilities and confidence. In addition, qualitative feedback from the participants indicated that the impact of camaraderie and community aspect of this program, including the student coaches, was clearly a positive part of the experience. In the future, it would be beneficial to compare boxing to other currently used clinical and community interventions and possibly to investigate deeper the mental and psychological benefits of the boxing program.

5 Limitations and future research

Limitations of this research should be considered. First, this was a sample of convenience and the sample size was small impacting the generalizability of this information. This study was based upon a community exercise program and therefore did not have a control group or comparison to other forms of exercise. Although improvements were made by the participants it is unclear how these would compare to other interventions or the specificity that the unique elements of boxing may provide. This will be a focus of future, larger scale studies. Finally, availability and use of students as coaches may impact the results of the study as typical community programs do not have access to multiple staff members. However, community volunteers could be trained to provide this assistance as well. This allows for more focal input for participants potentially allowing them to work at a higher level without fear of falling.

6 Conclusions

This study illustrated that a 12-week, non-contact community boxing program for individuals with PD may an effective mode of exercise to positively impact gait, dual task and backwards walking for individuals with PD but further, larger scale studies are needed. This moderate to high intensity intervention of multi-modal boxing exercises produced improvements in gait velocity, dual task velocity, step length, and a composite score of gait variability, as well as backwards walking velocity and step length. These improvements may impact independence with functional mobility and may improve safety. Further studies are warranted to explore these results within a larger cohort while comparing boxing to standard interventions for outcomes such as falls.

Footnotes

Acknowledgments

This study was funded by the Parkinson’s Foundation Community Grants Program for two grant funding cycles in 2018-2019. The authors would also like to thank the Preston Hollow United Methodist Church for donating their space for the class and the student volunteers from the Doctor of Physical Therapy Program at UT Southwestern Medical Center.

Conflict of interest

There were no financial interests or benefits that arose from this project.

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The effect of a multi-modal boxing exercise program on cognitive locomotor tasks and gait in persons with Parkinson disease

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1 Introduction

2 Methods

2.1 Participants

2.2 Outcome measures

2.3 Interventions

3 Results

Table 2 Participant demographics Age Male/Female Years since diagnosis Hoehn and Yahr stage BMI Average sessions 68.38 20/6 4.75 2.12 26.2 21/24

5 Limitations and future research

6 Conclusions

Footnotes

Acknowledgments

Conflict of interest

References

Table 2
Participant demographics

Age Male/Female Years since diagnosis Hoehn and Yahr stage BMI Average sessions

68.38 20/6 4.75 2.12 26.2 21/24