|Year : 2023 | Volume
| Issue : 1 | Page : 9-14
The relationship between transversus abdominis and internal oblique thickness and disease-related characteristics in Parkinson's disease: An ultrasound-based study
Burcin Aktar1, Seher Ozyurek2, Evrim Goz3, Berril Donmez Colakoglu4, Birgul Balci2
1 Department of Physical Therapy and Rehabilitation, Institute of Health Sciences; Department of Physiotherapy and Rehabilitation, Faculty of Physical Therapy and Rehabilitation, Dokuz Eylul University, Izmir, Turkey
2 Department of Physiotherapy and Rehabilitation, Faculty of Physical Therapy and Rehabilitation, Dokuz Eylul University, Izmir, Turkey
3 Department of Physiotherapy and Rehabilitation, Faculty of Health Sciences, Tarsus University, Mersin, Turkey
4 Department of Neurology, Faculty of Medicine, Dokuz Eylul University, Izmir, Turkey
|Date of Submission||24-May-2022|
|Date of Decision||08-Feb-2023|
|Date of Acceptance||02-Mar-2023|
|Date of Web Publication||29-Mar-2023|
Department of Physical Therapy and Rehabilitation, Institute of Health Sciences, Dokuz Eylul University, TR-35340, Balcova, Izmir
Source of Support: None, Conflict of Interest: None
Background and Aim: The core muscles are essential for spinal stability during functional activities. Trunk muscle function is affected by specific neurodegenerative processes of Parkinson's disease (PD). This study aimed to investigate whether changes in transversus abdominis (TrA) and internal oblique (IO) thickness during the abdominal drawing-in maneuver (ADIM) were associated with clinical manifestations, core endurance, and functional mobility in patients with PD. Materials and Methods: We included patients with a modified Hoehn and Yahr staging of 3 or lower. TrA and IO muscle thickness were measured using ultrasound both at rest and during ADIM, and the percent change (%) was calculated to assess TrA and IO activation. Patients performed core endurance (prone bridge and sit-ups) and functional mobility tests (timed “up and go” [TUG] and five times sit-to-stand [FTSTS]). All assessments were conducted during the “on” phase. Results: Five female and 17 male patients were included in this study. We found a statistically significant correlation between ultrasound parameters of IO and the clinical manifestations of PD (P < 0.05). Correlations were observed between TrA percent change and prone bridge, sit-ups, TUG, and FTSTS (P < 0.05). Conclusion: To the best of our knowledge, this is the first ultrasound imaging-based study to demonstrate the relationship between TrA and IO muscle thickness and clinical outcomes, and functional performance in patients with PD. Percentage changes in IO were associated with the clinical manifestations of PD. Increased activation of TrA during ADIM was associated with improved core endurance and mobility. The results suggest that a trunk-specific exercise program may be the cornerstone in the treatment of PD-related changes.
Keywords: Internal oblique, Parkinson's disease, transversus abdominis, ultrasound imaging
|How to cite this article:|
Aktar B, Ozyurek S, Goz E, Colakoglu BD, Balci B. The relationship between transversus abdominis and internal oblique thickness and disease-related characteristics in Parkinson's disease: An ultrasound-based study. Neurol Sci Neurophysiol 2023;40:9-14
|How to cite this URL:|
Aktar B, Ozyurek S, Goz E, Colakoglu BD, Balci B. The relationship between transversus abdominis and internal oblique thickness and disease-related characteristics in Parkinson's disease: An ultrasound-based study. Neurol Sci Neurophysiol [serial online] 2023 [cited 2023 Jun 10];40:9-14. Available from: http://www.nsnjournal.org/text.asp?2023/40/1/9/372787
| Introduction|| |
Parkinson's disease (PD) is one of the most common age-related neurodegenerative diseases, manifesting as bradykinesia, rigidity, tremor, and postural instability. Rigidity, dystonia, impaired sensory input, and musculoskeletal muscle weakness contribute to axial deformities that are disabling motor complications in patients with PD.
Trunk control has been identified as an important prerequisite for normal head, trunk, and pelvis movements and functional tasks such as sitting, standing, and walking., In particular, the transversus abdominis (TrA) and internal oblique (IO) muscles are essential for maintaining the stability of posture and controlling the body during occupational and daily living skills, as well as prevention of falls in older people.,, When thinking about patients with camptocormia or severe postural instability, it is highly unlikely that the trunk muscle function of patients with PD is effective and functional., In addition, the increased axial rigidity of patients with PD impairs their trunk function and locomotion., Therefore, these factors may lead to decreased independence in daily life and an increased risk of falls.
Real-time ultrasound imaging is commonly used to assess the size and activation of the core muscles in rehabilitation. It is a quick and easy-to-administer, noninvasive method of assessing muscle performance. Many researchers have focused on evaluating the thickness of the TrA under both static and dynamic conditions because it plays a unique role in spinal stability. The abdominal drawing-in maneuver (ADIM) is a fundamental component of activation or training of isolated TrA contraction. This maneuver is designed for preferential activation of the TrA with minimal recruitment of the internal and external oblique muscles., Due to the above mechanism, ADIM is a popular volitional test among physicians to assess TrA function using ultrasound imaging. The reliability of ultrasound imaging for abdominal muscles is ≥0.86 for intra-rater and inter-rater determination of resting position, and ≥0.76 for percentage change in muscle thickness in older adults.
Recently, increasing evidence has been presented in observational studies of the architectural features of these muscle groups in patients with neurologic diseases., However, the relationship between activations of TrA and IO using ultrasound imaging and clinical manifestations, core muscle performance, and functional mobility in PD has not been investigated previously. Therefore, the current study aimed to investigate whether changes in TrA and IO thickness during ADIM were associated with clinical signs, core endurance, and functional mobility in patients with idiopathic PD.
| Materials and Methods|| |
The study had a cross-sectional design and data were collected from May 2018 to November 2019. The study was approved by the Ethics Committee of Dokuz Eylul University (protocol number: 3958-GOA, decision number: 2018/11-06) and conducted in accordance with the principles of the Declaration of Helsinki. All subjects who agreed to participate gave written informed consent.
Twenty-two patients with idiopathic PD were recruited according to the United Kingdom Parkinson's Disease Society Brain Bank diagnostic criteria. The inclusion criteria were Modified Hoehn and Yahr staging <4, body mass index (BMI), which is a confounding factor in measuring muscle thickness, <30 kg/m2, and a mini-mental state examination score ≥ 24. The exclusion criteria were dystonia and camptocormia, the presence of neurologic conditions other than PD, and orthopedic/musculoskeletal and cognitive impairments that would affect assessment procedures. All assessments were conducted during the “on” phase.
A two-dimensional ultrasonography device (LOGIQ-e, GE Healthcare, Milwaukee, WI, USA) with a multi-frequency linear array transducer (GE 12 L-RS, bandwidth 5–13 MHz, footprint 12.7 mm × 47.1 mm) at a central frequency of 10 MHz was used for capturing B-mode images of the TrA and IO both at rest and during ADIM.
The ultrasound images were taken while the participants were in the supine hook-lying position with pillows under their knees and hips at 45° of flexion. The transducer was placed perpendicular to the right anterolateral abdominal muscle along a line midway between the inferior angle of the rib cage and the iliac crest. To obtain the standardized transducer position, the anterior fascial insertion of the TrA muscle was located approximately 2.0 cm from the medial edge of the ultrasound image [Figure 1].,
|Figure 1: Transducer location (pink, top line: the inferior angle of the rib cage; pink, bottom line: the iliac crest; green, middle line: a line midway between the inferior angle of the rib cage and the iliac crest)|
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Ultrasound images for the right side were obtained after calm expiration at rest and immediately upon performing the ADIM. Participants were provided with standard instructions on how to perform ADIM. Then, the following instructions were given: “Take a relaxed breath in and out, hold the breath out, and then draw in your lower abdomen without moving your spine.”
All measurements were performed by the same investigator (S.O), a physiotherapist with 5 years of experience who was trained in musculoskeletal and rehabilitative ultrasound imaging, involving a 2-day introductory course (accredited by the Royal College of Radiologists, the British Medical Ultrasound Society and the European Society of Musculoskeletal Radiology). The thickness of TrA at rest and during ADIM was obtained between the superficial and deep borders of the TrA muscle, as visualized by the hyperechoic fascial lines [Figure 2]. Measurements were performed perpendicular to the muscle fascia using caliper-based tools included in the software of the ultrasound scanner and were recorded in cm. Three measurements were recorded and the average of the three values was used for statistical analysis. In addition, the TrA and IO percent change (%) was calculated to determine the change in muscle thickness between at rest and during ADIM as per the following formula:
|Figure 2: Ultrasound image of right anterolateral abdominal wall muscles. (a) muscles at rest, (b) muscles during ADIM at end of calm expiration. The thickness of the TrA muscle is identified as the dashed line with arrows. EO: external oblique, IO: internal oblique, TrA: transversus abdominis, ADIM: Abdominal drawing-in maneuver|
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Clinical outcomes of Parkinson's disease
The Movement Disorder Society-Unified Parkinson's Disease Rating Scale (MDS-UPDRS) parts I, II, and III were used to define impairments and disabilities related to the disease. Part I and II, respectively, evaluate nonmotor and motor features of experiences in daily living. Part III assesses the motor signs of patients. We have summarized the following four subscores from MDS-UPDRS Part III: tremor (15–18 items), rigidity (item 3), bradykinesia (2, 4–9 items), and axial (1, 9–13 items) subscores.
Core muscle endurance
To evaluate core muscle endurance, the “prone bridge (plank)” and “sit-ups” were used. The prone bridge test was performed when the participant was in the prone position with their forearms and toes on the mat. Participants were asked to keep their shoulders, back, hips, and ankles in a straight position for as long as possible during the test. The test was terminated when the participants lost the straight posture. Two trials were performed and the best score was used for analysis. The test is valid and reliable for evaluating trunk muscle performance in the elderly. Sit-ups were performed by requesting the participant to lift the bottom corner of the scapula from the ground. The feet were held by the investigator while the knees were bent 90° in the supine position. We recorded how many times the participant was able to perform the test within 30 s.
To assess functional mobility, the timed “up and go” (TUG) and the “five times sit-to-stand (FTSTS)” tests were used. TUG consisted of standing up from a chair, walking a distance of 3 m, turning around, walking back to the chair, and sitting down again. Scores were recorded in seconds. A lower score indicates better balance and functional mobility. High test-retest and inter-rater reliability have been demonstrated in patients with PD. The FTSTS measured, in seconds, the time necessary for participants to fully stand up and sit down from a chair five times, as quickly as possible, and uninterruptedly. Participants were asked to keep their arms crossed over their chests during the task. High inter-rater and test-retest reliability has been established in PD.
Statistical analysis was conducted using the IBM SPSS software (version 24.0, IBM Corp., Armonk, New York, USA). The Shapiro–Wilk test was used to evaluate the normality of data distribution. Data are presented as median (25th–75th interquartile range) or frequencies and percentages. Spearman's correlation was performed to determine the correlation of the variables. The correlation coefficients (Rho) were classified as very weak (Rho = 0.00–0.19), weak (Rho = 0.20–0.39), moderate (Rho = 0.40–0.59), strong (Rho = 0.60–0.79), and very strong (Rho = 0.80–1.00). P < 0.05 was accepted for statistical significance.
A post hoc power analysis was performed using the G*Power (version 3.1, Dusseldorf University, Germany) software to detect the power of the study. The power of the present study was calculated based on the results of the correlation between “the percentage change in TrA” and “FTSTS” and found as 86.15%.
| Results|| |
A total of 22 patients with PD were included. The demographic data, disease-specific clinical characteristics, performance-based measures, muscle thickness, and percent change for TrA and IO are summarized in [Table 1].
The correlation coefficients between the ultrasound imaging parameters of the TrA and IO muscles and demographic and disease-specific clinical outcomes are shown in [Table 2]. We found no significant correlation between ultrasound parameters of TrA and age, BMI, and clinical manifestations of PD (P > 0.05), whereas ultrasound parameters of IO at rest and percentage change were significantly correlated with age, MDS-UPDRS I, MDS-UPDRS II, rigidity and bradykinesia subscores of MDS-UPDRS III (P < 0.05).
|Table 2: Correlation (rho) between muscle thicknesses and clinical manifestations of parkinson's disease|
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The correlations between the ultrasound imaging of the TrA and IO and performance-based measures are given in [Table 3]. The prone bridge (moderate; Rho = 0.513, P = 0.015), and sit-ups (strong; Rho = 0.663, P = 0.001) were positively correlated with TrA percent change, whereas a negative correlation was found between TrA percent change and TUG (moderate; Rho = −0.474, P = 0.026), and FTSTS (moderate; rho = −0.593, P = 0.004). No statistically significant correlation was found between the percentage change in IO and prone bridge, sit-ups, TUG, and FTSTS (P > 0.05). There were also no statistically significant correlations between TrA and IO muscle thickness (both at rest and during ADIM) and core muscle endurance and functional mobility (P > 0.05).
|Table 3: Correlation (rho) between muscle thicknesses and performance-based outcomes|
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| Discussion|| |
To the best of our knowledge, there has been limited research into measuring the abdominal muscles of patients with PD using real-time ultrasound imaging. Therefore, this is the first study to indicate the association between TrA and IO muscle thickness and clinical outcomes, and functional performance in patients with PD. Our results showed that the percentage changes in IO were also associated with disease-specific manifestations of PD. Greater changes in the TrA muscle during ADIM were associated with better core endurance and mobility.
A previous report on normal subjects showed that the resting thickness of the TrA and IO muscles was 0.36 ± 0.09 cm and 0.85 ± 0.22 cm in women, respectively, whereas it was 0.45 ± 0.13 cm and 1.18 ± 0.27 cm, respectively, in men. Our results showed that the TrA and IO muscle thickness in women and men at rest was 0.35 ± 0.04 cm and 0.67 ± 0.12 cm, and 0.35 ± 0.08 cm and 0.69 ± 0.17 cm, respectively. It is well known that males have a significantly larger muscle mass than females, which explains the sex difference. In addition, TrA and IO muscle thicknesses were lower in our sample population compared with normal subjects.
We speculated that patients who had better PD-related motor clinical outcomes might be associated with greater TrA and IO muscle thickness change. Our results support the association between motor symptoms and the ability to activate IO, but not the ability to activate TrA. Our sample included 13 (59.1%) patients without clinically identifiable postural instability (modified Hoehn and Yahr scale ≤2). The current finding may illustrate that patients with early-to-mid-stage PD may have postural instability due to the inability to selectively activate TrA. Further high-quality clinical research with a larger sample size is needed to confirm the effects of abdominal muscle thickness on postural control in patients with PD who have different severities of postural deformities or who are at different stages of the disease. Furthermore, future studies should include longer follow-up periods.
Our results surprisingly revealed that the ability to activate the IO muscle was associated with the nonmotor experience of daily living (MDS-UPDRS Part I). This strong relationship may be dependent on the subjects' cognitive impairment, depressed mood, anxious mood, and apathy. It may be logical to speculate that a decline in apathy would contribute to a decrease in ADIM performance. We suggest disease-specific assessments for further investigation to explore the impact of nonmotor symptoms in patients with PD.
Mobility is defined as the physiologic ability of a person to move independently and safely in a variety of environments so that functional activities and tasks can be accomplished. The reason to use the FTSTS for mobility, which requires coordination, balance, mobility, and strength when rising from the chair, is that momentum control results from coordinated postural control. TUG includes the turning phase and turn-to-sit transition, in addition to sit-to-stand performance in the FTSTS. Turning while walking occurs frequently in activities of daily living, and is a challenging feature of locomotion. The successful maintenance of mobility in daily life depends on these skills. In patients with PD, the neuromuscular impairment of trunk muscles leads to a decline in physical function and mobility.
In our study, the ability to activate the TrA muscle of patients with PD was associated with mobility and physical performance (TUG and FTSTS). These results were expected because the TrA muscle plays a greater role in spinal stabilization compared with the other abdominal muscles in functional tasks.,
This study provided objective evidence for muscle thickness. However, it has several limitations. First, the current study included a relatively small sample, and 17 of the 22 patients were men. Second, only patients with mild-to-moderate PD were studied; neither patients with severe PD nor healthy controls were included. Finally, we performed ultrasound imaging to assess the activation by the change in muscle thickness, and this method could not provide information on the timing of muscle activation.
| Conclusion|| |
This study demonstrated that IO muscle activity could be an important biomarker for disease-related clinical outcomes of patients with PD. TrA activation in patients with PD may provide preliminary evidence of their core endurance and mobility. Therefore, we recommend an exercise program specifically aimed at improving the trunk muscle function of patients. Further studies are needed to determine the efficacy of TrA and IO muscle activation on abnormal posture and trunk muscle functions of trunk muscles in this population.
The authors would like to thank the invaluable help for English editing provided by David Chapman.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]