The content and effects of trunk rehabilitation on trunk and upper limb performance in people with multiple sclerosis: a systematic review

Abstract

INTRODUCTION

Persons with multiple sclerosis (pwMS) could have an impaired trunk and reduced postural control, which negatively impacts activities of daily living. Evidence is growing to consider the positive effects of trunk training on fall incidence and balance problems. Effects on trunk and upper limb performance is unknown. This systematic review provides an overview of trunk training programs and their effects in MS, specifically focusing on the content of training modalities and the effects on trunk and upper limb performance.

EVIDENCE ACQUISITION

Two electronic databases were used: PubMed and Web Of Science (WOS). Intervention studies (with- and without control group) published in English, investigating the effects of active trunk training on trunk and upper limb performance in pwMS, were included.

EVIDENCE SYNTHESIS

Sixteen studies met the criteria, investigating different rehabilitation modalities. The included interventions in the review varied between more generic postural interventions such as Pilates (N.=8) and Ai Chi (N.=1), with a focus on abdominal muscle activation, breathing, neutral position and lower extremity movements. Further, specifically developed trunk training programs like GroupCoreDIST/ SIT / CoDuSe (N.=6) and Bobath based trunk training (N.=1) are detected, with the main focus on trunk strengthening and dynamic movements. An overall improvement in trunk performance was reported in several tests on trunk strength, stability and coordination. While the majority of the programs integrated the upper limb, only half of them used upper limb outcome measures to evaluate the effect. Here, overall significant improvements were found for the upper limb.

CONCLUSIONS

This systematic review showed that different types of trunk training programs can improve trunk and upper limb function in PwMS. The findings of this review suggest that a focus on trunk training to achieve effects on upper limb is reasonable. Future research is needed to further explore relations and the effect sizes.

Introduction

In daily life, functional tasks are executed unconscious. Nevertheless, behind these tasks complex interaction among many bodily systems are going on. Postural control is playing a crucial factor in the orientation and stability of the body and the functional task will contribute to shape the postural system.¹ For example during reaching the movement starts and ends with (anticipatory/ compensatory) postural adjustments in which the trunk plays a central role² and complex skills based on the interaction of dynamic sensorimotor processes are needed.³ Coordinated trunk muscle activation will provide proximal stability that is needed for distal mobility.⁴

In persons with multiple sclerosis (pwMS), a neurodegenerative disease of the central nervous system, postural control can be affected at any stage of the disease,⁵ even in an early phase, from a range of Expanded disability status scale (EDSS) 0 until 5.5.⁶ A delayed activation and smaller magnitude of muscles activation prior to manual tasks are seen by Krishnan et al..⁷ Comber et al. suggests that pwMS exhibit substantial deficits in postural control regardless of task complexity or sensory condition in standing position.⁸ Korkmaz et al. in turn shows a clear relation between trunk and upper limb performance and found a moderate-to-high relationship between the Nine hole peg test vs. Trunk Impairment Scale.⁶ These findings suggest that it is reasonable to focus therapy specifically on the trunk and upper limb in order to make clinical differences for pwMS.

In recent years, there has been a growing interest in developing new interventions addressing the trunk, however primarily aiming to improve balance and walking.^9-12 These interventions triggered us to investigate if these studies involve upper limb function or elements to regain functional use of the upper limbs. Since a normal upper limb function is important for autonomy in everyday live, and the trunk performance is imperative to accomplish this, potential effects from interventions addressing trunk and upper limb function are needed. To our knowledge, systematic reviews on interventions emphasizing trunk exercises are not available in pwMS. For comparison, in stroke the effects of these interventions are shown, on trunk performance, balance and gait.¹³ A systematic review conducted by Van Crieking suggested improvements of trunk control, sitting and standing balance and mobility induced by trunk training.¹⁴ However no conclusive evidence for the effect of trunk exercise on upper limb function was found.¹⁵

Besides dedicated trunk training programs, also more generic and alternative therapies based on trunk training, like Pilates, Tai Chi and Yoga are reported in literature. These intervention strategies improve dynamic balance and lower extremity strength in the elderly¹⁶ and in stroke patients,¹⁷ enhance aerobic capacity, muscular strength and balance,¹⁸ and have an effect on balance, hip and neck range of motion.¹⁹ For the upper limb, these alternative therapies suggest positive outcomes on upper limb strength¹⁹ and fine motor coordination in stroke patients.²⁰

In summary, we can conclude that there is a consensus on the current evidence of trunk training exercises and the effect on mobility outcomes in neurological patients. On the other hand, the effects on trunk performance itself and upper limb function and performance are unclear. The aim of the current review was to describe the specific content of the different trunk training modalities that are used in pwMS. The secondary objective was to describe the effects of trunk training exercises on trunk and upper limb function and performance in pwMS.

Evidence acquisition

This systematic review was conducted according the Preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) statement. The literature search started in November 2018 and ended in January 2020. During the review and writing process, the literature search was updated. The electronic databases (PubMed and WOS) were screened using the following string of Medical Subject Headings (MeSH) and keywords respectively. The search string in Pubmed was: (((((multiple sclerosis[MeSH Terms]) AND (core stability[Title/Abstract]) OR pilates[Title/Abstract]) OR postural balance[Title/Abstract]) OR tai chi[Title/Abstract]) OR trunk exercises[Title/Abstract]) OR yoga[Title/Abstract]) OR postural[Title/Abstract]) AND core[Title/Abstract]))). The search string in WOS was (TS= (multiple sclerosis) AND (TS= (core stability) OR TS= (pilates) OR TS= (postural balance) OR TS= (tai chi) OR TS= (trunk exercises) OR TS= (yoga) OR TS= (postural) OR TS= (core))))

In both databases, filters were used for publication date (2005) and language (English). All selected articles were screened based on title and abstract by 3 independent reviewers (JR, IM and JB). The full text was read when more information was needed to decide to exclude the study. Articles were included when they investigated the effects of active trunk training (more than one therapy session) in MS and outcome measures targeted at trunk or upper limb function and performance. Studies were excluded when outcome measures were exclusively targeted at mobility or balance parameters. Additionally, the reference lists of the included articles were screened for other relevant articles (Figure 1).

Figure 1.

—Literature search strategy and results.

Quality assessment

The overall quality of randomized controlled trials was assessed with the Consolidated Standards of Reporting Trials (CONSORT) checklist by four reviewers independently (JR, IM, JB and BS). Disagreement was discussed to attain a consensus. If the study design differed from randomized controlled trial (RCT), some items did not apply, and were filled out with “NA.”

Data-extraction

Relevant outcome of patient characteristics according to age, number of participants, type and severity of MS and number of drop-outs was reported. Therapy parameters were summarized according to different exercise modalities, frequency, duration and total amount of practice. Furthermore, relevant outcome measures regarding trunk performance and upper limb functions were described including clinical tests, pre-post measures, p-value and representing level of significance. Lastly, effect size (Hedges’ g) was calculated by dividing the standardized mean difference between post and pre measurements by pooled standard deviation. All data were extracted by three independent reviewers (JR, IM and JB). For the meta analysis, Cochrane Review Manager 5.3. was used.

Evidence synthesis

Results literature search

The search strategy resulted in 263 articles on PubMed and 930 articles on WOS. After removal of duplicates, 1155 remaining articles were screened on title and abstract. Of these, 1091 articles were excluded based on the predetermined criteria. Based on full text, 48 articles were excluded. One article was excluded because it was not possible to obtain the full text after consulting several university resources and contacting the author. The reference list screening resulted in 11 extra articles relevant for further reading. Based on the inclusion criteria, none of these articles were included. The included studies contained different types of articles like randomized controlled trial (N.=10), non-equivalent control group design (N.=3), time-series design (N.= 3).

Quality assessment

The Consolidated Standards of Reporting Trials (CONSORT) checklist for randomized controlled trials was used to assess the overall quality. The results of quality assessment are presented in Supplementary Digital Material 1, Supplementary Table I.^{5, 10, 11, 21-33} When studies had a non-equivalent control group design, not all items were possible to evaluate, these items were mentioned in Supplementary Table I as “not apply.” Overall, studies had difficulties with blinding the subjects and therapist and presenting the protocol. Positive reported items were baseline data and numbers that were analyzed in the included articles.

Patient characteristics

An overview of the study objectives and patient characteristics are presented in Supplementary Digital Material 2, Supplementary Table II.^{5, 10, 11, 22-33} Samples sizes ranged from 8 to 80. Three studies had a sample size equal or smaller than 10 pwMS in the intervention group. The mean EDSS score of the included participants was reported in all studies, and ranged from one to eight. Overall all types of MS were included, but only two out of three reported the MS type. The majority of the studies included a the different types of MS (relapse remitting, secondary progressive, and primary progressive). The mean age ranged between 30 to 65 years

Therapy content

The different types of intervention and the dosage are described in Supplementary Digital Material 3, Supplementary Table III.^{5, 10, 11, 21-33} Here, three “different” types of therapy are noted: Pilates (N.=8), Ai chi (N.=1) and specific targeted trunk exercises (N.= 7). Pilates was seen as the most common therapy, where the focus is on abdominal muscle activation and breathing. Furthermore, the Pilates exercises give attention to a neutral position of the spine while performing upper and lower extremity movements. Other exercises targeted pelvic motion, abdominal strengthening, and core stability. The duration for Pilates ranged from 8 to 12 weeks and the total amount of training ranged from 12 to 72 hours.^21-27 Ai Chi exercises were performed in a pool and targeted extremity and trunk movements to work on balance and strength while focusing on breathing pattern. The duration was 8 weeks and the total amount of training was 16 hours.²⁸ Besides these emerging training modalities, as described above, specially designed training programs were employed in seven articles. Among these were: home-based exercise training (N.=1),²⁹ Group-based CoreDIST (N.=1)³⁰ CoDuSe intervention program (N.=1),¹¹ Bobath-based trunk training (N.=1),⁵ and core stability training (N.=3).^{10, 31, 32}

More specifically, the programs differed from each other with adding movements of extremities. Five out of seven studies included the lower limb^{5, 10, 11, 29, 30} and only three included explicit the upper limb in the training program.^{10, 29, 30} Furthermore, a difference is found in the postural modality in which the exercises of these seven programs are executed: supine, sitting or standing position. Two studies adding or motor dual tasks and different sensory strategies, such as uneven surface or withdrawing visual input.^{11, 30} Furthermore, it can be established that these specific programs give more attention in general, compared with Pilates, to dynamic movements in (un)stable environment where the focus is on balance. Lastly, it is observed that the therapy content of the trunk focused interventions^{10, 11, 30, 32} is often based on existing programs like Jeffrey core stabilization program³⁴ or a previous study of Freeman et al.⁹

Therapy effects

Supplementary Digital Material 4, Supplementary Table IV, V, VI.^{5, 10, 11, 21-33} provide a general overview of the effects of each intervention. Although the articles reported several different outcome measures, only the relevant measures are shown, being those that are targeted towards the trunk and upper limb function and performance.

It was found that interventions targeted at the trunk have a positive impact on the trunk performance. Positive effects on trunk performance are seen for the interventions that are specifically targeted at the trunk, as well as Pilates and Tai-Chi. Positive effects targeted at the upper limb are six times reported: three times for the NHPT, once on the interscapular distance, and twice on upper limb strength and functional reach performance. A schematic representation of targeted outcome measures and rehabilitation can be found in Figure 2.^{5, 10, 11, 21-33} For the Trunk Impairment scale the meta-analysis show a positive effect over the four different studies, with a major weight of Artnzen et al. Still, without this powered study, an overall positive effect is seen in favor of the intervention (Figure 3).^{5, 11, 26, 30}

Figure 2.

—An overview of the targeted included outcome measures and treatment, with a division between upper limb and/ or trunk.^{5, 10, 11, 21-33}

Figure 3.

—Treatment effect on the Trunk Impairment scale.^{5, 11, 26, 30}

Discussion

This systematic review provided an overview of interventions on active trunk training, with specific attention to the content and the effectiveness of these therapy programs. As mentioned before the trunk plays a central role during reaching and a coordinated trunk muscle activation is needed for distal mobility. It is important to understand the concept of postural control to provide well targeted rehabilitation programs. Posture control is attained by central commands to lower motor neurons, nevertheless the output is adjusted by sensory input. The sensory input (somatosensation, vestibular and vision) are essential for the feedback and feedforward mechanisms,³⁵ also called the anticipatory and compensatory postural adjustment. Persons with MS have smaller magnitudes of anticipatory muscle activation³⁶ and a delayed latency of anticipatory postural adjustment.^{7, 8, 37} The focus of the review is on the motor outcome, however if sensory input was mentioned in the different training modalities, it was stated in the Supplementary Digital Material 3, Supplementary Table III.

We looked on one hand to the different contents of the programs and on the other hand to the effectiveness on trunk or upper limb performance. All included studies, except one, showed an improvement after intervention on the trunk and/or upper limb performance.

Patient characteristics

A variety in the patient inclusion criteria and characteristics between the different studies is seen, including type of MS and age. Overall EDSS scores ranged from zero to eight, representing a high heterogeneity of the study population. This implies that trunk and upper limb dysfunction of the included participants also varies between studies and generalization is challenging. For the mild and moderate impaired persons, an overall consensus was found regarding the effectiveness of the trunk training.^{5, 10, 21-24, 26, 28-33} For the severe impaired persons (EDSS>6) no clear consensus was found. However, we note that only two studies included severe impaired persons.^{11, 27} Van Der Linden reported improvements in an adapted functional reach test, where the Centre of pressure was measured, the interscapular distance and pain.²⁷ In contrast, Carling et al. did not found significant improvements in any outcome measure specifically in the scope of this review. Nevertheless, it is considered to concentrate therapy also on the more severely disabled population because of the improvements they found on the secondary outcomes (balance, walking and fatigue).¹¹

Therapy characteristics

The included interventions in the review varied between more generic postural interventions such as Pilates^{21, 23-27, 31, 33} and Ai Chi,²⁸ to specifically designed trunk training programs like GroupCoreDIST/ SIT^{10, 30} or CoDuSe program¹¹ and finally also Bobath based trunk training.⁵ It must be stated that alternative therapies, like Pilates, are not strictly focussing on the trunk, but also focus on f.e. facilitating the control of shoulder and upper limb movements.^21-27 When investigating more closely to the content of the trunk training programs: four important aspects are frequently reported in the Pilates exercises: activation and strength of abdominal muscles, stretching, balance and postural stability. In the other group, specifically developed trunk training programs, like Bobath, CoDuSe and GroupCoreDIST program, the focus lies on core activation and optimal alignment, coordination and functional dual tasks. For the Ai-Chi program the therapy focus is directed towards balance, strength, relaxation, flexibility and breathing in a swimming pool.

Looking to the integration of the sensory input to shape the motor output of postural control. We see that vestibular input is given by unstable or uneven surface^{5, 11, 29, 32} and various positions,^{5, 10, 21-23, 25, 26, 29, 30} somatosensation is given by sensory input.^{10, 11, 30} It should be clear that the sensory input is not the main component in these therapies but an integrated aspect. In contrast to studies as Gandolfi et al. exclusively address specific sensory inputs to improve balance disorders in pwMS.³⁸

Outcome measures

Within the different outcome measures used in the included studies, two main groups can be distinguished: outcome measures targeted towards the trunk and the upper limb. Firstly, the trunk was measured by abdominal muscle endurance and strength or on a broader general performance by the trunk Impairment Scale. In the trunk outcome measure targeted toward evaluating function (endurance and power), a positive effect was consequently seen on these trunk outcomes. For the Trunk Impairment Scale (TIS) statistical significant improvement were found, like presented in the meta- analysis.^{5, 11, 26} Arntzen et al. showed a large significant improvement on the TIS-NV,¹⁰ these well powered study is particularly weighing on the general conclusion of the meta-analysis. In this Norwegian version of the TIS (TIS-NV), a redundant item of the TIS (specific static balance) is removed, just like in the TIS 2.0 compared with TIS 1.0.^{39, 40}

For the upper limb, only half of the included articles reported any primary or secondary upper limb outcome. Although most of these interventions reported significant improvements on upper limb function. The Pilates-based intervention had the highest improvements regarding the calculated effect sizes. Specific for hand grip strength, Pilates based intervention and aquatic training exceed the threshold of minimal important change from the patient’s perspective. Concerning the NHPT, the minimal important change is rather expressed in a 15-20% change.^{41, 42} Only the study of Kara et al. is showing this percentage change.²⁵

Clinical and methodological considerations

No clear consensus is found when linking the different components of therapy content with the effectiveness, neither on trunk nor on upper limb function. For training based on Pilates improvements are found on trunk and upper limb and for specific developed programs similar findings are seen. However, the specific developed trunk programs included almost exclusively trunk outcomes, but barely upper limb outcomes. An equal distribution for trunk and upper limb outcomes are seen for the Pilates interventions.

Another important point to mention is the discrepancy between the chosen targeted components of postural control in therapy versus the measured outcome (alignment, muscle and postural tone and movement strategies). Alignment is five times mentioned in the intervention, but never measured. Also muscle and postural tone is rarely measured although it is integrated in therapy. However, one item turn up in the comparison: movement strategies. A vast majority of interventions is including movement strategies and find also significant improvements on this component. Therefore it would be appear to integrate it in the intervention. To our opinion, these finding encourages the integration of the upper limb in an active trunk training program. The trunk should not be seen as a single segment, but the upper limb and trunk components must been trained as a coordinated complex where the stability limits can be explored.

Conclusions

An active trunk training program can improve significantly the trunk performance of pwMS. For pwMS with a low EDSS there is more consensus about the effectiveness than for the ones with a high EDSS.

Concerning the effect on the performance of the upper limb a positive trend is seen. Nevertheless, due to the high heterogeneity of the research population, the widespread variation of therapy methods and dosage and outcome measures it is difficult to compare treatment effects and finally to draw a detailed conclusion considering trunk training effects on trunk and upper limb performance.

Supplementary Digital Material 1

Supplementary Table I

Consort checklist.^{5, 10, 11, 21-33}

Supplementary Digital Material 2

Supplementary Table II

Patient characteristics.^{5, 10, 11, 21-33}

Supplementary Digital Material 3

Supplementary Table III

Data-extraction: therapy parameters.^{5, 10, 11, 21-33}

Supplementary Digital Material 4

Supplementary Table IV

Experimental group.^{10, 27, 31}

Supplementary Table V

Experimental vs control group Control group.^{5, 11, 23, 24, 26, 28-30, 32, 33}

Supplementary Table VI

Experimental 1 vs experimental 2 vs control group.^{21, 22, 25}