Abstract
BACKGROUND:
Neurodevelopmental treatment (NDT) and dynamic core-postural chain stabilization (DCS)- based exercise is effective for improving core stability and postural control in stroke patients. However, no study has reported respiratory function, increased fatigue and ADL function in subacute stroke patients by training using NDT and DCS exercises.
OBJECTIVE:
To compare the effects of DCS and NDT exercises on respiratory function, fatigue and activities of daily living in individuals with hemiparetic stroke.
METHODS:
Thirty-one participants with hemiparetic stroke (17 male, 14 female; mean age 60.4±14.58 years; post-stroke duration, 7.2±2.2 weeks) participated in this study. The participants were randomly allocated into DCS (n = 16) and NDT (n = 15). Respiratory function was determined using forced vital capacity (FVC), forced expiratory volume in 1 second (FEV1), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP). The fatigue severity scale (FSS) and functional independent measure (FIM) were used to evaluate fatigue severity and activities of daily living (ADL). Analysis of covariance (ANCOVA) was used to evaluate post-test differences in the DCS and NDT exercise groups.
RESULTS:
ANCOVA revealed the superior effects of DCS in respiratory function, as well as clinical FSS and FIM tests, compared with those of NDT (p < 0.05).
CONCLUSIONS:
The results suggest that DCS training was more effective than NDT training at improving respiratory function, fatigue severity and ADL via balanced co-activation of the diaphragm and increased diaphragm movement in individuals with hemiparetic stroke.
Keywords
Introduction
Stroke is the leading cause of a myriad of per-manent neuromuscular and associated respiratory system impairments and associated disabilities worldwide (Rochester, and Mohsenin 2002). In particular, insufficient diaphragm and deep abdominal muscle function have been identified as important biomarkers for respiratory function or breathing and postural control during activities of daily living (ADL) in individuals with subacute hemiparetic stroke. After cerebral diaschisis and the progression of functional depression of the spinal cord or the ipsilesional and contralesional sensorimotor cortex, the corticospinal and bulbospinal pathway, which modulates respiratory and postural muscles including the diaphragm, intercostals, and abdominal muscles, are disrupted (Hachmann et al., 2017; Redecker et al., 2000). Recent dynamic magnetic resonance imaging (MRI) and ultrasound imaging studies are shedding light on the respiratory and postural mechanisms that underlie coordinated feedforward activation of the diaphragm-transversus abdominis (TrA)/internal oblique (IO)-pelvic floor-multifidus chain (Kolar et al., 2009). For example, Kolar and his colleagues (2009) observed that the descending movement of the diaphragm during the inspiratory phase of voluntary breathing was activated prior to any dynamic upper or lower extremity movements. Cohen et al. (1994) reported that deteriorated diaphragmatic excursion and abdominal muscle thickness were associated with decreased coordinated diaphragm movement and abdominal muscle activation during spontaneous breathing in stroke patients. The diaphragm also assists with balance control against internal and external perturbations via increased intra-abdominal pressure (IAP), in conjunction with balanced co-activation of the abdominal and pelvic floor muscles (Jandt et al., 2011). IAP is thought to contribute to modulating extensor torque in the erector spinae muscles, thereby decreasing compressive loads. Decreased compression force on the spine and increased torque of the extensors improve postural stability and balance control using a feed forward mechanism (Hagins et al., 2004). Therefore, inefficient diaphragm-TrA/IO-pelvic floor-multifidus chains result in fatigue and bring about reductions in respiratory function, postural control, gait, and ADL. Clinical stroke respiration studies showed close relationships between diaphragmatic motion and decreased forced vital capacity (FVC), decreased force expiratory volume in 1 second (FEV1), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP) (Khedr et al., 2000; Teixeira et al., 2005). TrA/IO and external oblique (EO) muscle strengths are strongly related to FVC, FEV1, peak expiratory flow (PEF), MIP and MEP in respiratory function, postural control, and ADL (Functional Independence Measure (FIM) (Karatas et al., 2004; Misuri et al., 1997). Increased core stability is also related to gait performance and ADL (Haruyama, Kawakami, and Otsuka 2017). These findings further support an important role of coordination between the diaphragm and the deep core chain muscles during respiration in the design of effective management respiratory and ADL in stroke (Frank, Kobesova, and Kolar 2013).
To mitigate deep abdominal muscle weakness and inefficient respiration and postural control with increased superficial muscle activation (rectus abdominis muscle, EO), neurodevelopmental treatment (NDT) exercise has been conventionally used and showed positive results (Crisp, and Stanley 2013; Yoon, and You 2017). NDT approach involves more “conscious” proprioceptive feedback to facilitate upright postural stabilization while maintaining the neutral “pelvic tilting exercise” to selectively activate the deep core muscles. NDT utilizes rib cage horizontal and vertical expansion mobility (i.e., rib-to-spine, rib-to-sternum, and rib-to-rib), stiff chest wall musculature elongation (diaphragm, intercostals, and abdominals) in the sagittal and frontal planes, and proprioceptive facilitation of the abdominal musculature (e.g., rectus abdominus, internal abdominal oblique, external abdominal oblique) for respiration and postural stabilization. A clinical stroke trial attempted to examine whether NDT-based respiration and postural stabilization exercises improved pulmonary function and postural control (Hafsteinsdottir et al., 2005) in hemiparetic stroke patients. The potential neuromechanical mechanisms that underpin respiratory and postural control in adults with hemiparetic stroke following the intervention remain unknown.
In contrast, the dynamic core-postural chain stabilization (DCS) treatment approach was designed to activate the integrated spinal stabilizing system (ISSS) based on neurodevelopmental kinesiology and emphasizes core stabilization via co-activation of the TrA/IO, diaphragm, pelvic floor, and multifidus muscles in coordination with the superficial core muscles, which generates sufficient IAP to dynamically stabilize the spine. This IAP provides overall postural stability in response to internal or external perturbations during dynamic limb movements. The DCS also emphasized movement of the diaphragm to activate the IAP and ISSS. Optimal descending movement of diaphragm reduces spinal compression, postural perturbation, and inefficient postural control when regulating the dynamic standing balance (Frank, Kobesova, and Kolar 2013). A recent stroke study compared the effects of ultrasound-guided DCS and NDT on anticipatory postural adjustment (APA) time and postural trunk muscles (TrA/IO, EO, erector spinae) and compared the effect of diaphragm concentrically contracts in the caudal direction to increase activity of and responses in stroke patients (Lee et al., 2018). A similar comparative study investigated the therapeutic efficacy of DCS- and NDT-based core stabilization exercises on TrA/IO and EO muscle activity and found that DCS treatment improved deep abdominal muscle thickness and activity in healthy and stroke-affected participants (Yoon et al., 2017). These new findings suggest that DCS is more effective than NDT for reflex-mediated core stabilization. Nevertheless, to date there is a dearth of clinical evidence to account for the neurorespiratory function, fatigue, ADL and mechanisms that underlie NDT- and DCS-based core exercises in stroke patients. Therefore, the purpose of the present study was to compare the effects of DCS and NDT on respiratory function, fatigue severity and ADL in hemiparetic stroke patients.
Methods
Participants
Thirty-one adults with sub-acute hemiparetic stroke (males 17, females 14; mean age 60.4±14.58 years; Post-stroke duration 7.22±2.21 weeks) were recruited from a university medical center. (Table 1). The participants were randomly allocated either into the DCS (n = 16) or NDT (n = 15) group using a computerized randomization method. All participants provided informed consents and underwent both conventional NDT and DCS core exercises. The inclusion criteria were as follows: (1) More than three months after hemiparetic stroke; (2) a Mini-Mental State Examination score ≥ 24; and (4) ≥ 2 on the Trunk Impairment Scale (TIS). The exclusion criteria were as follows: stroke patients with visual hemianopsia, sensory neuropathy, and a history of orthopedic or associated surgery.
Demographic and clinical characteristics of the subjects
Demographic and clinical characteristics of the subjects
aNDT: Neurodevelopmental treatment; bDCS: Dynamic core-postural chain stabilization; cMMSE-K: Korean mini-mental state examination; dMean±Standard deviation.
Respiratory function tests (Spirometer, MasterScreen Pneumo Jaeger, Wurzburg, Germany) were used to measure the FVC and FEV1 in individuals with hemiparetic stroke. FVC is the amount of air that can be forcibly exhaled from the lungs after taking the deepest breath possible, while FEV1 is the amount of air that can be forcibly exhaled from the lungs in the first 1 second of a forced exhalation. The therapist performed a sufficient demonstration and explanation to ensure participant understanding of the FVC and FEV1 test. The test was performed with 90° of flexion of the hip and knee joint and a nose clip in a seated position on a chair. FVC and FEV1 were analyzed using a maximal-effort expiratory spirogram (Ranu, Wilde and Madden 2011). The mean value was recorded three times to reduce the error of the result. A Micro Spirometer (Micro RPM, Micro Medical Ltd, UK) was used to measure respiratory muscle strength. MIP and MEP are known to sensitively reflect the weakening of respiratory muscles in stroke patients (Schoser et al., 2017). It is also widely used to measure the strength of respiratory muscles. To prevent muscle fatigue, MIP and MEP was measured after 2 hours of respiratory function test.
Clinical tests
Fatigue is a symptom commonly reported by stroke patients, and FSS has a high correlation with one’s ability to perform ADL (r = 0.77) (Valderramas et al., 2013). The FSS is a 9-item instrument that was designed to assess fatigue as a symptom of a variety of different chronic conditions and disorders. Respondents use a scale of 1 (completely disagree) –7 (completely agree) to indicate their agreement with 9 statements about fatigue. The sum of all items is 9–63. The total score is obtained by the sum of all items added divided by the number of assertions of the instrument. A final score≥4 indicates fatigue; the higher the score, the greater the fatigue severity (Krupp et al., 1989).
FIM is widely used as an evaluation tool for activities of daily living; it was provided an index to evaluate functional level and neurological recovery level in stroke patients. FIM is a highly reliable assessment tool with an inter-rater reliability of 0.83–0.96. The 18 items on the FIM evaluate the degree of disability and burden of care. Thirteen items define disability in motor functions and five items define disability in cognitive functions. Each item is rated on a 7 point scale, with 1 point = total assist and 7 point = complete independence (Chumney et al., 2010).
Intervention
Two different core stabilization exercises (NDT and DCS) were used. The core stabilization techniques were as follows. The DCS involves a synkinesis descending movement of the diaphragm during inspiration that co-activates the pelvic floor and abdominal muscles and adjusts IAP to provide core stabilization. In the NDT group, the participants performed the pelvic tilting exercise (Appendix). Since all designated therapists were certified for NDT, we could minimize the risk of individual bias. Each session was performed in 5 positions (supine, prone, quadruped, sitting, and standing). Shoulder flexion-extension and hip flexion-extension were maintained for 10 seconds per session and the implementation was repeated 10 times. A 2-minute rest period was given for each session. The entire group received treatment interventions for 30 minutes each session for 3 times per week for a total of 4 weeks.
Statistical analyses
PASW Statistics ver. 22.0 software (SPSS, Chi-cago, IL, USA) was used for all statistical analyses. The Kolmogorov-Smirnov test was used to test for normal distribution. Levene’s test was performed to examine the homogeneity of variances. Descriptive statistical data were expressed in means and standard deviations. Statistical significance level was set at 0.05. The parametric tests included paired t-tests to examine intervention-related changes before and after the treatment in each group. An analysis of covariance (ANCOVA) test were used to verify the group differences in respiratory function, fatigue severity and ADL between the DCS and NDT exercise groups while controlling for the covariate.
Results
Respiratory function data
A comparison of respiratory muscle functions between DCS and NDT are shown in Table 2. Paired t-tests were used to compare the pre- and post-test outcome measures in the DCS and NDT groups. The respiratory muscle functions (FVC and FEV1) and respiratory muscle strength (MIP and MEP) were significantly increased within each group (p < 0.01). Analysis of covariance was used to evaluate the differences between the post-test for the DCS and NDT exercise groups while controlling for covariates. The FVC was significantly increased by 12% in DCS than NDT after 4 weeks of intervention (p < 0.01). Also, FEV1, MIP and MEP were significantly increased by 14% in DCS than NDT after 4 weeks of intervention (p < 0.05).
Comparison of change in respiratory muscle functions (L) and strength (cmH2O)
Comparison of change in respiratory muscle functions (L) and strength (cmH2O)
aNDT: Neurodevelopmental treatment; bDCS: Dynamic core-postural chain stabilization; cMean±standard deviation; dFVC: Forced vital capacity; eFEV1: Force expiratory volume at one second; fMIP: Maximal inspiratory pressure; gMEP: Maximal expiratory pressure; hPaired t-tests; iAnalysis of covariance tests; *p < 0.05; **p < 0.01.
A comparison of fatigue between DCS and NDT are shown in Table 3. Paired t-tests were used to compare the pre- and post-test outcome measures in the DCS and NDT groups. The FSS and FIM were significantly decreased within each group (p < 0.01). Analysis of covariance was used to evaluate the differences between the post-test for the DCS and NDT exercise groups while controlling for covariates. The FSS were significantly decreased by 8% in DCS than NDT after 4 weeks of intervention (p < 0.05). Also, The FIM were significantly increased by 12% in the DCS than NDT after 4 weeks of intervention (p < 0.05).
Comparison of changes in fatigue and activities of daily living
Comparison of changes in fatigue and activities of daily living
aNDT: Neurodevelopmental treatment; bDCS: Dynamic core-postural chain stabilization; cMean±standard deviation; dFSS: Fatigue severity scale; eFIM: Functional independent masurement; fPaired t-tests; gAnalysis of covariance tests; *p < 0.05; **p < 0.01.
The purpose of the present investigation was to compare the therapeutic effects of NDT and DCS exercises on respiratory function, fatigue and ADL in hemiparetic stroke patients. As hypothesized, the DCS-based core exercise was more beneficial for respiratory function, fatigue and ADL than the NDT-based core exercise. Most importantly, this is the first clinical trial to date that presents comparative findings that demonstrate the superior effects of DCS on the respiratory function, fatigue and ADL in subacute hemiparetic patients.
Respiratory function analyses showed greater improvements in FVC (12%), FEV1 (13%), MIP (9%), and MEP (19%) after DCS than after NDT. These novel findings suggest that DCS, which underscores diaphragmatic movement, may be more beneficial than NDT for restoring respiratory function. The present findings corroborated those of previous studies, which reported a significant correlation between diaphragmatic excursion during respiration and FVC (r = 0.86) and FEV1 (r = 0.70) in hemiparetic stroke patients as well as a close relationship between diaphragm excursion and MEP and MIP in chronic stroke patients with restrictive lung disease (Rocha et al., 2017; Teixeira-Salmela et al., 2005). A possible underlying mechanism is that the DCS exercise induces descending movements of the diaphragm and TrA/IO muscles by activating the deep core muscles and regulating the IAP (Liebenson 2007). However, no study to date has reported on the ability of respiratory interventions to facilitate the descending movements of the diaphragm in the NDT intervention (Sterba et al., 2002; Gjelsvik 2008). As a result, DCS was more effective than NDT at restoring respiratory function via synchronous activation of the TrA/IO and the diaphragm.
Clinical data analyses revealed superior effects of DCS versus NDT on FSS and FIM. Certainly, these clinical results indicate that DCS was better able than NDT to improve fatigue and ADL in subacute stroke patients. Further analyses showed greater improvements in FSS (–8%) and FIM (12%) after DCS than after NDT. Previous research on fatigue after neurorehabilitation exercise program showed desirable effects of neurorehabilitation on reducing fatigue on the FSS (37%) in patients with neurological damage (Oncu et al., 2009). FIM score was improved by 32% (49.8–65.7) after 4 weeks of NDT training in stroke patients (Bhalerao et al., 2013). The underlying rationale for such a superior effect may have resulted from the fact that NDT focuses on active postural core stabilization to selective movements and involves selectively activating the deep core muscles. However, no study has reported increased fatigue and ADL function in subacute stroke patients by training their diaphragm descending movements using DCS exercises. Nevertheless, our study showed that FSS and FIM scores were significantly increased in the DCS group versus the NDT group. Sutbeyaz et al. (2010) showed that the breathing exercises in the 6-weeks program in stroke patients improved cardiopulmonary function and ADL. Previous research on fatigue after respiratory training showed desirable effects of respiratory exercises on reducing fatigue intensity on the FSS in chronic obstructive pulmonary diseases patients (Zakerimoghadam et al., 2011). In the current study, the balanced co-activation mechanism of the increased diaphragm movements seems to have reduced fatigue and increased ADL ability compared to the NDT group in the DCS diaphragmatic breathing group.
Although the present study has revealed meaningful findings, it has four main limitations. First, a larger sample size is required in further investigations because it was difficult to generalize findings obtained from the small sample sizes of the two groups. Second, core stabilization consists of the diaphragm –TrA/IO –pelvic floor kinetic chains, which regulate IAP to provide anterior lumbopelvic stability. The influence of the pelvic floor on core stabilization was not evaluated in the present study. And third, the carryover effect was not accounted for, so it is not known whether the increased respiratory and fatigue and ADL abilities were maintained after the intervention.
Conclusion
This study provided evidence of the comparative effects of 4-week DCS and NDT exercises on respiratory function, fatigue and ADL in subacute stroke patients. The study demonstrated that the DCS exercise was more effective than the NDT exercise to mitigate decreased respiratory function, fatigue and ADL because DCS uses a coordinated diaphragm and abdominal muscle movements to regulate IAP during spontaneous breathing. Our findings may provide conceptual and clinical insight into the examination and management of respiratory function, fatigue and ADL of individuals with subacute hemiparetic stroke.
Clinical trial registration
The study was registered (KCT0002801) at Clinical Research Information Service (CRiS), Republic of Korea.
Conflict of interest
The authors declare that there is no conflict of interest regarding the publication of this article.
Ethics approval
The study was approved by the Institutional Review Board (CNUH 2018-01-025).
Footnotes
Appendix
Dynamic core-postural chain stabilization procedure
The standardized DCS steps are as follows: (1) A DCS-certified therapist first centralized or normalized a participant’s sternum, ribcage, and thoracolumbar spine alignment in the supine position to allow for normalized or natural diaphragmatic breathing; (2) The participant was then required to maintain alignment of chest and spine during the automatic or subconscious descending diaphragm movement in normal inhalation to activate the TrA/IO. An accurate DCS movement emphasizes that the lower part of the sternum and the 10–12 ribs were anterolaterally expanded from the medioclavicular line and posteriorly along the angulus costae. As a result, descending movements of the diaphragm and expansion of the intercostal space activate the deep core muscles and regulation of the IAP; and (3) the therapist used ultrasound images to identify the descending movements of the diaphragm during performance of DCS. Once the basic DCS skills are learned in the supine position, the participants perform unilateral or bilateral shoulder and hip flexion-extension movement at the more difficult level (supine, prone, quadruped, sitting, and standing positions). In the NDT group, the participants performed the pelvic tilting exercise. Since all designated therapists were certified for NDT, we could minimize the risk of individual bias. (1) While pulling the belly button up and in toward the spine with pelvic posterior tilting movement and while breathing quietly, contract the deep abdominal muscles without overactivating the superficial muscles (sternocleidomastoid, upper trapezius, rectus abdominis). The therapist inspected each participant’s movements and made any necessary corrections. (2) Once the participant was able to correctly perform the selective pelvic tilting exercise, more advanced core stabilization exercises were performed, including (3) unilateral or bilateral shoulder and (4) hip flexion-extension movements in the sitting and standing positions.
Acknowledgments
This study was supported by the Brain Korea 21 PLUS Project Grant (2016-51-0009) from the Korean Research Foundation. This study was supported by Korea Health Industry Development Institute (grant no. 2019-51-0468) Institute of Information & communications Technology Planning & Evaluation (IITP) funded by the Korea government (MSIT) (grant no. 2020-0-01129); Brain Korea 21 PLUS Project (grant no. 2019-51-0018); Leaders in Industry-university Cooperation + Project supported by the Ministry of Education and National Research Foundation in Korea (Grant no. 2020-51-0260).
