Influence of phase of respiratory cycle on ultrasound imaging of deep abdominal muscle thickness





Abstract


Background


It is difficult to evaluate the transversus abdominis (TrA) and internal oblique (IO) due to their dual role in both trunk control and breathing.


Objectives


To investigate whether TrA and IO thickness as measured by ultrasound differs across the respiratory cycle in upright standing.


Design


Observational study.


Methods


Thickness of TrA and IO was measured with ultrasound in 67 subjects in upright standing. Measures were performed 3 times and by 2 assessors, at the end of relaxed expiration, at the end of a full inspiration, and at the end of full expiration. Differences were assessed by ANOVA. Intra- and inter-rater reliability (of a single measure and the average of 3 measures) were assessed by intra-class correlation (ICC).


Results


Thickness of the TrA and IO was higher at full expiration than at the end of relaxed expiration (p < 0.001), and in turn compared to at full inspiration (p < 0.001). Intra-rater reliability was excellent at all respiratory phases (ICC 0.76–0.87). Whereas inter-rater reliability for a single measure was only fair to good for TrA (ICC 0.52–0.71) and good to excellent for IO (ICC 0.61–0.78), the inter-rater reliability of the average was excellent at all respiratory phases (ICC 0.75–0.90).


Conclusions


Thickness of TrA and IO increases when lung volume decreases. The intra- and inter-rater reliability of an average measure were excellent at the end of relaxed expiration, full inspiration and full expiration. This provides new opportunities to evaluate the deep abdominal muscles, and their role in respiration, in a physiotherapeutic setting.


Highlights





  • Transversus abdominis and internal oblique act in both trunk control and breathing.



  • Thickness was measured by ultrasound during 3 phases of the respiratory cycle.



  • Thickness of these muscles increases when lung volume decreases.



  • Reliability of an average of 3 measures is excellent during the respiratory cycle.



  • These results provide valuable opportunities in a physiotherapeutic setting.




Introduction


Electromyography (EMG) studies demonstrated that transversus abdominis (TrA) onsets are delayed in patients with low back pain (LBP) ( ). Similarly, studies using musculoskeletal ultrasound (MSKUS) have shown a reduced thickness of the TrA during functional activities in patients with LBP ( ; ; ; ). Another MSKUS study has shown that morphological changes of the internal oblique (IO) may be related to the incidence of LBP, because IO asymmetry increased the odds of LBP by at least 2.4 times in the examined population ( ). However, it remains unclear how TrA and IO muscle thickness is influenced by breathing, and whether this is detectable by MSKUS. This might be relevant regarding the dual role of TrA and IO in breathing (i.e., expiration) and trunk control, as well as regarding the effect of breathing on these muscles’ shape and length ( ).


MSKUS is increasingly being used by physiotherapists who treat musculoskeletal disorders, such as LBP, patellofemoral pain or rotator cuff pathology ( ; ; ). Because MSKS can quantify changes in muscle thickness and echogeneity, it has become a popular clinimetric tool to assess muscle function ( ; ). recently summarized studies investigating the reproducibility of MSKUS for the deep abdominal muscles, and generally found good levels of intra- and inter-rater reliability. However, most of the studies included in this review acquired MSKUS images at the end of expiration to control for the influence of respiration. Hence, intra- and interrater reliability of abdominal muscle thickness measures at different phases across the respiratory cycle remains unknown. Moreover, only a few studies examined the reliability of MSKUS for trunk muscles during upright standing (versus supine lying) ( ). However, upright standing increases the efficiency of lung function ( ), and represents a more functionally relevant posture considering the role of the deep abdominal muscles in trunk control ( ).


Therefore, the main objective of this study was to investigate whether thickness of TrA and IO as measured with MSKUS in upright standing depends on the respiratory phase, more specifically at the end of relaxed expiration, at full inspiration or at full expiration. The second objective was to investigate the intra- and inter-rater reliability of MSKUS to measure TrA and OI muscle thickness in upright standing at the different respiratory phases. The results would provide more insight into the dual role of the abdominal muscles in breathing and trunk control, which is particularly relevant for patients with dysfunctional breathing, such as individuals with LBP ( ).



Materials and methods


Sixty-seven healthy individuals (31 males/36 females; 22 ± 2 years old, body mass index (BMI) 23 ± 3 kg/m 2 ) participated after providing informed consent. Exclusion criteria were voice impairments in the last three weeks, an episode of LBP in the past six months, respiratory or neuromuscular disorders, pregnancy, abdominal surgery, and BMI>30 kg/m 2 . The study conformed to the principles of the Declaration of Helsinki, was approved by the Ethical Committee of Fontys University and was registered at The Netherlands Trial Register (7596).


Participants stood barefoot (hip-width) with their scapulae and buttocks lightly touching the wall. They were asked to place their left hand on their right shoulder to ensure an unrestrained positioning of the transducer ( Fig. 1 ) and to slightly lift their chin to avoid airway obstruction ( ). Before the start of the experiment, the participants were instructed verbally and by demonstration how to breathe (as described below), followed by a practice trial. Subsequently, MSKUS measurements were performed at the three different respiratory phases (conditions), while participants were asked to hold each phase for 3 s ( Table 1 ). At each phase, MSKUS of TrA and IO thickness was captured. Two assessors (R1-R2) acquired three images at each respiratory phase for each muscle. Between assessors, participants rested for 15 min to prevent hyperventilation symptoms ( ).




Fig. 1


Experimental set-up.


Table 1

Experimental conditions.
















Condition number Respiratory phase
1 at the end of a natural breathing cycle
2 at the end of a maximal inspiration
3 at the end of maximal expiration


Based on its common use in clinical practice, the MSKUS images were recorded with an Esaote MyLabTM One device (Italy), which allows low-end quality b-mode ultrasound. A linear-array transducer (model SL3323) with a frequency of 6–13 MHz and a size of 33 mm was used, which is the most optimal for superficial structures ( ). The left body side was chosen to allow the most convenient positioning by the dominant hand (right) of the assessors. The transducer was placed transversally, 2.5 cm medially of the mid-axillary line and half way between the lowest rib and ilium ( ). Data analysis is described in detail in Appendix 1 .


Statistical analysis was performed with SPSS v25 (IBM Corporation, USA) with the significance level set at α < 0.05. To assess differences between respiratory phases, a one-way repeated measures ANOVA of the averaged measurements for each respiratory phase was used. Comparisons between the respiratory phases were made with Bonferroni corrections for multiple comparisons. To assess intra- and inter-rater reliability, intra-class correlation coefficients (ICCs) (absolute agreement) were calculated. Cases were excluded based on the formula for extreme outliers: Q1-(3*IQR) and Q3+(3*IQR). The interpretation of the ICCs was as follows: ICCs<0.40 represents poor, ICCs 0.40–0.59 fair, ICCs 0.60–0.74 good and ICCs>0.75 excellent reliability ( ). We calculated a 95% confidence interval, standard error of measurement (SEM) and minimal detectable change (MDC): SEM=SD*√(1-ICC) and MDC = 1.96*SEM*√2. Finally, Bland & Altman plots were created.



Results


The intra-rater reliability of measuring TrA and IO thickness with MSKUS was excellent at all respiratory phases ( Table 2 ). Table 3 shows the inter-rater reliability of a single MSKUS measurement of TrA and IO thickness. For TrA, this was fair (at full expiration) to good (at the end of relaxed expiration and at full inspiration). For IO, this was good (at full inspiration and full expiration) to excellent (at the end of relaxed expiration). Table 4 shows the inter-rater reliability of the average of 3 single measurement of TrA and IO thickness. For both TrA and IO, the interrater reliability was excellent at all respiratory phases. Bland & Altman plots showed that the average difference between raters was <1 mm, and that the 95% limits of agreement included zero, regardless of the muscle that was assessed or the use of single or average measurements (See Appendices 2 and 3 ). No systematic bias could be seen along the x-axis, and except for rare cases, all measurements fell within the 95% limits of agreement.



Table 2

Intra-rater reliability of three thickness measurements of transversus abdominis and internal oblique with musculoskeletal ultrasound at different respiratory phases – ICCs calculated based on a single-measurement, absolute-agreement, 2-way mixed-effects model.













































































End relaxed expiration Full inspiration Full expiration
Transversus abdominis
R1 ICC (95% CI) 0.81 (0.73–0.87) 0.82 (0.74–0.88) 0.81 (0.74–0.87)
SEM 0.66 mm 0.55 mm 0.95 mm
MDC 1.85 mm 1.51 mm 2.68 mm
R2 ICC (95% CI) 0.81 (0.73–0.87) 0.79 (0.70–0.85) 0.76 (0.66–0.83)
SEM 0.63 mm 0.57 mm 0.98 mm
MDC 1.76 mm 1.59 mm 2.73 mm
Internal obliqui
R1 ICC (95% CI) 0.84 (0.78–0.90) 0.83 (0.75–0.88) 0.83 (0.76–0.89)
SEM 1.04 mm 0.97 mm 1.32 mm
MDC 2.90 mm 2.70 mm 3.67 mm
R2 ICC (95% CI) 0.78 (0.69–0.85) 0.84 (0.78–0.89) 0.87 (0.81–0.91)
SEM 1.26 mm 0.86 mm 1.39 mm
MDC 3.50 mm 2.39 mm 3.86 mm

R = rater, ICC = intra-class correlation coefficient, CI = confidence interval, SEM = standard error of measurement, MDC = minimal detectable change.


Table 3

Inter-rater reliability of a single thickness measurement of transversus abdominis and internal oblique with musculoskeletal ultrasound at different respiratory phases – ICCs calculated based on a single-measurement, absolute-agreement, 2-way random-effects model.













































End relaxed expiration Full inspiration Full expiration
Transversus abdominis
R1 vs R2 ICC (95% CI) 0.71 (0.44–0.84) 0.60 (0.39–0.74) 0.52 (0.27–0.69)
SEM 0.82 mm 0.83 mm 1.50 mm
MDC 2.27 mm 2.31 mm 4.16 mm
Internal obliqui
R1 vs R2 ICC (95% CI) 0.78 (0.67–0.86) 0.61 (0.40–0.75) 0.72 (0.58–0.82)
SEM 1.32 mm 1.40 mm 1.83 mm
MDC 3.66 mm 3.86 mm 5.06 mm

R = rater, ICC = intra-class correlation coefficient, CI = confidence interval, SEM = standard error of measurement, MDC = minimal detectable change. For transversus abdominis, one case was excluded at ‘end of relaxed expiration’ after outlier analysis.


Table 4

Inter-rater reliability of the average measurement (i.e., of 3 single measures) of transversus abdominis and internal oblique with musculoskeletal ultrasound at different respiratory phases – ICCs calculated based on an average-measures, absolute-agreement, 2-way random-effects model.













































End relaxed expiration Full inspiration Full expiration
Transversus abdominis
R1 vs R2 ICC (95% CI) 0.88 (0.47–0.95) 0.84 (0.66–0.91) 0.73 (0.49–0.85)
SEM 0.49 mm 0.48 mm 1.01 mm
MDC 1.36 mm 1.32 mm 2.79 mm
Internal obliqui
R1 vs R2 ICC (95% CI) 0.90 (0.84–0.94) 0.82 (0.62–0.91) 0.86 (0.72–0.92)
SEM 0.79 mm 0.83 mm 1.29 mm
MDC 2.19 mm 2.28 mm 3.55 mm

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Aug 18, 2020 | Posted by in MUSCULOSKELETAL MEDICINE | Comments Off on Influence of phase of respiratory cycle on ultrasound imaging of deep abdominal muscle thickness
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