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Keywords: Background: Altered breathing pattern is a consequence of dysfunctional breathing. The respiratory pattern might
Breathing pattern be impaired in patients with cervical radiculopathy due to the involvement of common nerve roots with the
Cervical radiculopathy phrenic nerve (C3– C5).
Manual assessment of respiratory motion
Objective: The aim of this study was to investigate the inter-rater and intra-rater reliability of a technique for
Reliability
evaluating the breathing pattern known as manual assessment of respiratory motion (MARM) in patients with
unilateral cervical radiculopathy.
Design: Cross-sectional study.
Setting: Rehabilitation Sciences Research Center
Participants: Twenty-five patients with unilateral cervical radiculopathy aged 30–55 years participated in this
study.
Methods: Two experienced physical therapists investigated the respiratory pattern of the patients during normal
and deep breathing using MARM, separately. Assessments were repeated again a week apart by each examiner.
The inter- and intra-rater reliability of the MARM were calculated.
Results: “Very good” inter-rater and intra-rater reliability were found with the MARM values during both normal
and deep breathing patterns. (Inter-rater: ICC range = 0.71 to 0.82; intra-rater: ICC range = 0.72 to 0.80).
Conclusions: MARM is a reliable clinical and research tool for assessing breathing patterns with very good inter-
and intra-rater reliability in patients with unilateral cervical radiculopathy.
• Highlighting the importance of respiratory assessment in patients Cervical radiculopathy is a clinical condition resulting from
with unilateral cervical radiculopathy. compression of cervical nerve roots due to spondylosis or disc hernia
• Introducing the manual assessment of respiratory motion as a clin tion, known as a common cause of neck and arm pain [1]. The average
ical, time-efficient, and inexpensive method with an acceptable level annual incidence rate of cervical radiculopathy was 83.2 per 100 000
of inter-rater reliability to assess and quantify the breathing pattern population in Rochester [2]. The clinical manifestations of cervical
in these patients. radiculopathy are diverse and may include pain, sensory and motor
• Manual assessment of respiratory motion has an acceptable level of deficits, diminished reflexes, or any combination of these signs and
intra-rater reliability for investigating breathing pattern in patients symptoms. The pain may radiate into the ipsilateral arm in a derma
with unilateral cervical radiculopathy. tomal pattern [3,4]. Previous studies have shown that dysfunctional
breathing patterns have been associated with musculoskeletal pain in
* Corresponding author. Physical Therapy Department, School of Rehabilitation Sciences, Shiraz University of Medical Sciences, School of Rehabilitation Sciences,
1 Abivardi Avenue, Chamran Blvd., Shiraz, 71345, Iran.
E-mail address: irezaei@sums.ac.ir (I. Rezaei).
1
Amin Kordi Yoosefinejad and Raziyeh Yousefiyan contributed equally to this work.
https://doi.org/10.1016/j.ijosm.2024.100708
Received 31 May 2023; Received in revised form 20 December 2023; Accepted 2 January 2024
Available online 7 January 2024
1746-0689/© 2024 Elsevier Ltd. All rights reserved.
A. Kordi Yoosefinejad et al. International Journal of Osteopathic Medicine 51 (2024) 100708
various parts of body such as chest wall [5], neck, shoulder [6,7] and cervical radiculopathy. The study was approved by the local Ethics
lower back [8]. Furthermore, the association between chronic neck pain committee of the vice chancellery of research, Shiraz University of
and respiratory dysfunction has been previously demonstrated [9]. Medical Sciences, in accordance with the standards of the Helsinki
Respiratory pattern can refer to the relative contribution of thoracic declaration (Ethics Number: IR. SUMS.REHAB.REC.1401.017). The
and abdominal regions during breathing, regardless of respiratory fre study was performed between December 2022 and February 2023 at the
quency and volume, and other parameters [10]. Optimal breathing oc Rehabilitation Sciences Research Center. The evaluation was performed
curs when the respiratory effort is evenly distributed between the two by two experienced physical therapists that were trained to use MARM.
main functional parts of breathing including the upper chest and lower Breathing pattern assessment was performed twice, a week apart, by
ribs cage/abdomen. Therefore all diaphragmatic abdominal and rib cage each examiner. The examiners performed the MARM separately and
muscles contribute equally to their relevant length-tension relationships were blind to the results of each other.
and co-ordination patterns [11,12].
Respiratory pattern might be impaired in patients with unilateral 3.2. Participants
cervical radiculopathy. It may occur secondary to the involvement of the
primary respiratory muscles (i.e. diaphragm, scalenes, trapezius, etc.) The minimum sample size was calculated as 21, based on a pilot
receiving innervation from cervical nerve roots. The diaphragm is the study on 10 participants, regarding the expected calculated ICC as 0.83,
main inspiratory muscle innervated by the phrenic nerve. Impaired an alpha level of 0.05, and power of 0.80. The sampling method was
diaphragmatic function in patients with cervical radiculopathy occurs convenient and the participants were recruited through the purposive
following the phrenic nerve involvement. Previous studies highlighted sampling method via flyers from the physiotherapy and neurology
the association between diaphragmatic paralysis and cervical radicul clinics. Twenty-five volunteers with unilateral C3–C7 cervical radicul
opathy [13–18]. Moreover, the diaphragm is firmly connected to neck opathy, involvement of C3–C4 or C4–C5 nerve roots, aged between 30
muscles via fascia transversalis originating from the endothoracic fascia; and 55 years, and a body mass index of less than 30 Kg/m2 participated
hence, diaphragm and neck muscles have mutual effects on each other in the study. Onset of cervical radiculopathy was at least 3 months with
[19]. Fahad et al. found that respiratory parameters including vital ca pain score of 3–10 based on a numerical rating scale and moderate to
pacity in expiration, forced expiratory volume, forced vital capacity, severe disability (15–50) based on the neck disability index. All patients
peak expiratory flow and mean voluntary ventilation were less in pa were clinically assessed and diagnosed by a specialist supported by MRI
tients with cervical spinal stenosis in comparison to healthy control findings.
group. The observed changes were attributed to the partial damage of Exclusion criteria were chest or lung disorders, acute respiratory
the phrenic nerve and subsequent decreased strength of the respiratory infections, long-term use of steroids or steroid injection during the last
muscles [20]. two weeks, nonsteroidal anti-inflammatory drugs consumption during
There are several methods for evaluating respiratory pattern. Manual the previous day, previous neck or thoracic surgeries, musculoskeletal
assessment of respiratory motion (MARM) is a clinical, time-efficient malalignments like scoliosis and kyphoscoliosis, pregnancy, recent
and inexpensive evaluation method used to assess and quantify the physiotherapy for the neck, currently smoking, respiratory complica
breathing pattern. Respiratory pattern usually is measured with respi tions of COVID-19, positive test for COVID-19 in the last three months,
ratory induction plethysmography (RIP) and magnetometry [21], and professional athletes.
whilst, a cheaper, quick, yet valid and reliable method seems helpful in
clinical environments. MARM was first developed by Dixhoorn in the 3.3. Description of MARM
1980s [22] to determine the contribution of the upper and lower parts of
the rib cage and abdomen into breathing pattern and also, to illustrate The examiner sat behind the patient who was sitting on a backless
the asymmetry between the sides of rib cage [10]. It is based on the chair with hands on the lower lateral rib cage. The examiner’s hands
estimation of motion perceived by the examiners’ hands at the posterior rested with full contact while neither assisting nor restricting the pa
and lateral lower rib cage. The examiner constructs a mental picture of tient’s breathing. The hands were open such that the little and ring
global breathing motion, drawing an upper line and a lower line from fingers were below the lower ribs in a horizontal orientation to feel
the center of a pie chart [10]. abdominal expansion and thumbs were vertical and parallel to the spine.
Courtney and Dixhoorn compared the MARM with RIP, an estab The patient was asked to breathe normally in an upright and
lished standard for measuring breathing pattern, in twelve experienced comfortable sitting position. The examiner got a global sense based on
breathers [10]. It was concluded that the MARM was a valid and reliable palpatory impression of the magnitude and freedom of rib cage motion.
clinical tool with acceptable levels of agreement between the examiners Based on palpation, the examiner determined if the relative motion of
(r = 0.85, p < .001) [10]. It does require practice, but once the skill of the chest was predominantly vertical (upper rib cage motion) or hori
using this technique and recording the findings are acquired, it is a zontal (lower rib cage motion) or evenly distributed.
practical and valuable technique [10]. MARM could be regarded as a The examiner drew an upper line (A) in the pie chart diagram of the
diagnostic method in patients with respiratory disorders [23]. MARM which represents the upper thoracic motion and a lower line (B)
MARM can be used as a clinical diagnostic tool instead of laboratory to represent the lower ribs motion (Fig. 1). The two lines of the MARM
equipment to evaluate and quantify the respiratory pattern. To the best are a simplified way for describing the area of expansion and predom
of our knowledge, the reliability of the MARM was investigated in inant direction of breathing motion in either the upper rib cage/sternum
healthy people, or it was suggested for patients with pulmonary dis or the lower rib cage/abdomen. The upper line of diagram can represent
eases. This is the first study assessing the reliability of the MARM in the upward motion of the sternum/upper thorax (pump-handle motion)
patients with cervical radiculopathy. The aim of this study was to as a vertical direction of breathing and the lower line can represent the
determine the inter-rater and intra-rater reliability of the MARM in lateral expansion and sideways elevation of the lower ribs (bucket-
patients with unilateral cervical radiculopathy. handle movement) as a horizontal direction. The upper line will be
further from the horizontal and closer to the top if there is more upper
3. Materials and methods rib cage motion and the lower line will be further from the horizontal
and closer to the bottom if there is lower rib cage motion [10]. Three
3.1. Study design variables are calculated from the MARM graphic notation (Table 1). The
MARM variables are derived from one sitting posture and two breathing
This cross-sectional study was conducted to determine the intra- and instructions. The participants are asked to breathe in an upright or easy
inter-rater reliability of the MARM method in patients with unilateral sitting posture, once normally and then more deeply [10].
2
A. Kordi Yoosefinejad et al. International Journal of Osteopathic Medicine 51 (2024) 100708
using SPSS (SPSS Inc. SPSS Statistics for Windows, Version 25.0. Chi
cago: SPSS Inc.).
4. Results
Fig. 1. Graphic notation of the manual assessment of respiratory motion. Note: 5. Discussion
A: the vertical motion of the upper rib cage; B: the horizontal motion of the
lower rib cage; C: horizontal line, AC angle: the upper chest motion and CB
The objective of this study was to determine the intra- and inter-rater
angle: the lower chest motion.
reliability of the MARM in patients with unilateral cervical radiculop
athy. The results suggested that the MARM is a reliable tool for the
Table 1 assessment of breathing pattern in patients with unilateral cervical
Calculation of the MARM variables. radiculopathy with "very good" inter-rater and intra-rater reliability.
Variable Description Calculation
In the study by Courtney et al., MARM and RIP were performed on
healthy people who were instructed to voluntarily alter their breathing
Volume/area of angle between AandB Angle AB
pattern and posture [10]. Two examiners assessed breathing patterns
breathing
Balance difference of AC angle and CB angle based AC – CB using the MARM and RIP. "Good" levels of agreement between the ex
on the MARM diagram aminers and between MARM and RIP were reported. It was concluded
Percent rib cage angle aboveC/total angle (AB) × 100 AC/AB × that MARM is a reliable method for assessing breathing pattern in
motion 100
healthy individuals. Hence, the results of their study could not be
Note: Note: A: the vertical motion of the upper rib cage; B: the horizontal motion generalized to any group of patients. However, the altered breathing
of the lower rib cage; C: horizontal line based on the MARM diagram (Fig. 1), pattern observed in our participants was due to the involvement of the
Abbreviations: MARM: manual assessment of respiratory motion. cervical nerve roots innervating the diaphragm.
Ludwig et al. investigated the inter- and intra-rater reliability of the
3.4. Statistical analysis MARM in 16 participants with normal or minimal breathing dysfunc
tion. The findings demonstrated poor inter-rater reliability of the MARM
To evaluate the inter-rater and intra-rater reliability of MARM, Intra- and high intra-rater reliability [26]. Our results were similar to those by
class correlation coefficient using the two-way random model (ICC [1, Ludwig et al. regarding intra-rater reliability; however, we reported a
2]) was calculated. The ICC [1,2] values are interpreted as follows: "very good" inter-rater reliability in contrast to their findings. In Lud
excellent: 1.0–0.81, very good: 0.80–0.61, good: 0.60–0.41, fair: wig’s study, individuals with mild respiratory dysfunctions or healthy
0.40–0.21, and poor: 0.20–0.00 [24]. people without respiratory problems were recruited; while, our partic
Within-subjects variability and systematic changes were calculated ipants had moderate to severe respiratory dysfunctions. Thus, the
by standard errors of measurement (SEM) and change in mean respec observed difference could be attributed to different populations.
tively. The SEM was calculated using the following formula:
√̅̅̅ Table 2
SEM = SD × 1– ICC
Demographic information of radiculopathy group.
Where “SD” stands for standard deviation and “ICC” stands for intra- Variables Values
class correlation coefficient [25]. Moreover, the coefficient of varia Age (years) 44 (7.42)
tion (CV) was calculated to express the variation of measurement as a Sex (male %) 43.8
Body mass index (kilogram/meter2) 25.1 (3.25)
percentage rather than a raw value. CV values less than 10 % are
Onset of pain (months) 8.40 (9.23)
considered very good; CV values between 10 and 20% are interpreted as Visual analog scale (cm)) 6.68 (1.49)
good; values between 20 and 30% regarded as acceptable and values Neck disability index (0-50) 20.40 (6.64)
more than 30% are unacceptable. Statistical analyses were performed
Note: Values are mean (SD) or %.
3
A. Kordi Yoosefinejad et al. International Journal of Osteopathic Medicine 51 (2024) 100708
Table 5 The protocol of this study was approved by the local ethics com
Intra-rater reliability of the components of manual assessment of respiratory mittee of Shiraz University of Medical Sciences [Ethics code: IR. SUMS.
motion during normal and deep breathing patterns. REHAB.REC.1401.017].
Components ICC CI 95 % (Lower SEM CV
[1,2] limit, Upper limit) (%)
CRediT authorship contribution statement
Volume/area of normal 0.71 0.44, 0.86 3.23 16.72
breathing (degree)
Amin Kordi Yoosefinejad: Conceptualization, Data curation,
Balance of normal breathing 0.81 0.62, 0.91 3.45 NA
(degree) Formal analysis, Methodology, Project administration, Supervision,
Percent rib cage motion of 0.76 0.51, 0.88 5.69 24.59 Validation, Writing – original draft, Writing – review & editing. Raziyeh
normal breathing (%) Yousefiyan: Conceptualization, Formal analysis, Investigation, Meth
Volume/area ofdeep 0.71 0.45, 0.86 3.74 14.36 odology, Visualization, Writing – original draft, Writing – review &
breathing (degree)
Balance of deep breathing 0.81 0.62, 0.91 4.85 NA
editing. Raziyeh Nazari: Formal analysis, Investigation, Methodology,
(degree) Writing – original draft, Writing – review & editing. Iman Rezaei:
Percent rib cage motion of 0.82 0.63, 0.91 5.36 18.37 Conceptualization, Data curation, Formal analysis, Funding acquisition,
deep breathing (%) Methodology, Project administration, Supervision, Validation, Visuali
Abbreviations: ICC [1,2]: Intra-class Correlation Coefficient [two-way random zation, Writing – original draft, Writing – review & editing.
model], SEM: Standard Errors of Measurement, CV: Coefficient of Variation, NA:
Not applicable.
Declaration of competing interest
MARM is a time-efficient and inexpensive manual method to eval
uate the breathing patterns, not only in patients with asthma [23], but None.
also, based on our results, a method with "very good" intra-rater and
inter-rater reliability in patients with cervical radiculopathy. Acknowledgments
Instrumentation used to evaluate the breathing patterns in research
settings is invasive, expensive and time-consuming. Despite the impor This article is extracted as a part of a thesis for the master’s degree of
tance of breathing assessment, it is usually ignored or only examined in physical therapy by Raziyeh Yousefiyan. The authors would like to
patients with severe respiratory dysfunctions. The existence of a stan thank the Rehabilitation Sciences Research Center for facilitating the
dard, non-invasive, applicable and time-efficient method of breathing assessment process.
4
A. Kordi Yoosefinejad et al. International Journal of Osteopathic Medicine 51 (2024) 100708
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