Bahan 3
Bahan 3
Bahan 3
Reviewed by: As changes in nerves’ shape and size are common ultrasonographic findings of
Regina Wing Shan Sit,
The Chinese University of Hong Kong, entrapment neuropathy, measurement of the nerve cross-sectional area (CSA) becomes
China the mostly used indicator to differentiate normality from pathology. Recently, more US
Hariharan Shankar,
Medical College of Wisconsin,
research has been conducted to measure the shape of the suprascapular notch and the
United States diameter of the suprascapular nerve. Because the suprascapular nerve is paramount
Montana Buntragulpoontawee, for various shoulder disorders, the present study aims to establish normal values of
Chiang Mai University, Thailand
suprascapular nerve sizes at different levels as well as to investigate potential influence
*Correspondence:
Ke-Vin Chang of participants’ characteristics on the CSA measurements. The present study used a
[email protected]; cross-sectional design investigating the CSA values of the suprascapular nerve from
[email protected]
the supraclavicular region to spinoglenoid notch. We employed the inside-epineurium
Specialty section: and outside-epineurium methods to quantify CSA of cervical roots (C5 and C6) and
This article was submitted to the suprascapular nerve on US imaging. Univariate comparisons of nerve sizes among
Applied Neuroimaging,
different age and gender groups were carried out. Multivariate analysis was performed to
a section of the journal
Frontiers in Neurology analyze the impact of participants’ characteristics on nerve CSA. Repeated measurement
Received: 27 July 2018 analysis of variance was conducted to examine segmental variations of CSA of the
Accepted: 05 October 2018 suprascapular nerve from its origin to infraspinatus fossa. Our study included 60 healthy
Published: 23 October 2018
adults with 120 shoulders and had three major findings: (1) the inside-epineurium
Citation:
Wu W-T, Chang K-V, Mezian K,
method was more reliable than the outside-epineurium approach for CSA measurements
Naňka O, Lin C-P and Özçakar L due to higher intra- and inter-rater reliability, (2) women had smaller sizes for cervical
(2018) Basis of Shoulder Nerve
nerve roots and for the most proximal segment of the suprascapular nerves, and (3)
Entrapment Syndrome: An
Ultrasonographic Study Exploring using the outside-epineurium method, the suprascapular nerve CSA was larger in its
Factors Influencing Cross-Sectional distal division than the portion proximal to the mid-clavicular line. In conclusion, the
Area of the Suprascapular Nerve.
Front. Neurol. 9:902.
inside-epineurium method has better reliability for nerve CSA assessment but
doi: 10.3389/fneur.2018.00902 the outside-epineurium method is needed for quantifying the size of distal
Keywords: suprascapular nerve, cervical root, sonography, shoulder pain, entrapment neuropathy
FIGURE 1 | Ultrasound imaging of (A) C5 nerve root, (B) C6 nerve root and the suprascapular nerve (solid yellow arrowhead) (C) departing from the superior trunk
(ST) of the brachial plexus, (D) at the mid-clavicular level, (E) inside the supraspinatus fossa, and (F) at the spinoglenoid notch of the infraspinatus fossa. Red
arrowhead: suprascapular artery.
up toward the acromion and the suprascapular nerve was (Figure 2D). How the transducer was placed on the participants
localized as departing from the superior trunk (18) (Figure 1C). was shown in Figure 3. The anatomy of the suprascapular nerve
Relocating the transducer laterally, the suprascapular nerve was was also elaborated using the cadaver shoulder model with the
seen at the mid-clavicular level underneath the omohyoid muscle approval of the Anatomical Donation Department of Charles
(Figure 1D, and Supplementary Video). The transducer was University in Prague (Figure 4).
then redirected to the scapular plane to target the suprascapular
nerve in the supraspinatus fossa (Figure 1E). Finally, the Outcome Measurement
transducer was placed along the inferior border of the scapular The image processing software, Image J (19), was employed
spine to scan the suprascapular nerve at the spinoglenoid notch for the CSA measurements of the C5 and C6 nerve roots
(Figure 1F). We also redirected the transducer to align with and the suprascapular nerve departing from the upper trunk,
the long axis of the suprascapular nerve to make sure that the at the mid-clavicular line under the omohyoid muscle, inside
target we visualized was a nerve instead of a random hypoechoic the supraspinatus fossa and at the spinoglenoid notch of
round structure (Figures 2A–C). Power Doppler imaging was the infraspinatus fossa. We employed two methods to define
also employed to distinguish the accompanying suprascapular the border of the target neural structures: inside-epineurium
vessels in order to exclude them from the CSA measurements (20) (Figure 5A) and outside-epineurium of the nerve (21)
FIGURE 2 | Ultrasound imaging of the suprascapular nerve (solid yellow arrowhead) in the long axis at (A) the supraclavicular region, (B) the supraspinatus fossa, and
(C) the infraspinatus fossa. Ultrasound Doppler imaging of the suprascapular nerve at the supraspinatus fossa (D). Dashed line: the border of the nerve sheath.
FIGURE 4 | Cadaver shoulder model for the suprascapular nerve (solid yellow arrowheads) (A) departing from the superior trunk (ST) of the brachial plexus, (B)
entering the supraspinatus fossa underneath the transverse scapular ligament (black arrow), (C) inside the supraspinatus fossa with perineural fat seen surrounding
the nerve, and (D) at the spinoglenoid notch of the infraspinatus fossa. Red arrowheads: suprascapular artery; dashed yellow arrowheads: branches of the
suprascapular nerve.
DISCUSSION
This investigation resulted in several important findings. First,
the inside-epineurium method was more reliable than the
outside-epineurium approach for measurement of suprascapular
nerve CSA due to its higher intra- and inter-rater reliability.
Secondly, the CSA values of the C5 and C6 nerve roots
and the suprascapular nerve near the brachial plexus were
associated with gender difference, but not age, laterality, and body
stature. Thirdly, employing the outside-epineurium method, the
suprascapular nerve CSA is larger in its distal division than the
portion at and proximal to the mid-clavicular line.
The suprascapular nerve, unlike the larger peripheral nerves
such as median and sciatic nerves, has less degree of somatic
organization. Therefore, its echotexture resembles the cervical
FIGURE 5 | Illustration of the inside-epineurium (A) and outside-epineurium nerve roots, which has a monofascicular pattern instead
(B) methods for measurement of the nerve cross-sectional area by using the
image processing software, Image J.
of a honeycomb appearance (23). Battaglia et al. measured
the proximal segment of the suprascapular nerve for 33
asymptomatic subjects aged between 21 and 42 years and
reported the mean nerve CSA to be 1.9 mm2 over the first rib
Univariate Analysis of Nerve CSA Across and 2.0 mm2 at the distal clavicle (23). The details regarding
CSA measurement (inside- or outside-epineurium) were lacking
Different Age and Gender Groups
in the aforementioned study. In addition, no available literature
Mean values and SD of nerve CSA in each subgroup are presented
reports the reference values of suprascapular nerve CSA from the
in Table 2. There was a trend of larger nerve CSAs in the male
brachial plexus level to infraspinatus fossa in different age and
groups than those in the female groups. The aforementioned
gender populations, as has been reported in this study.
trend was less significant for the suprascapular nerve measured
In this study, we reported that the inside-epineurium method
at the supraspinatus fossa and spinoglenoid notch using the
was more reliable than the outside-epineurium method in
outside-epineurium method. The nerve CSAs among the same
measuring the nerve CSA due to its higher intra- and inter-
sex but different age range were not significantly different across
rater reliability. In recent years, with advancements in US
subgroups.
technology, most high resolution US machines are able to
delineate the ultrastructure of the peripheral nerves (24). The
Multivariate Analysis of Factors Associated echotexture of nerve fascicles are hypoechoic, whereas the
With Nerve CSA Across Different Sites surrounding connective tissues like epineurium and perineurium
The analysis derived from the GEE model revealed that female appear hyperechoic (25). As the suprascapular nerve has a
gender was negatively associated with the CSA values of the C5 monofascicular pattern, the border between the nerve fascicle
and C6 nerve roots and the suprascapular nerve near the brachial and epineurium is usually clearly defined; thus, it contributes
plexus as measured by both methods (inside- and outside- to high reliability during CSA measurement. However, the
epineurium). The significant association between sex and nerve epineurium is laminated and continuous with the mesoneurium,
CSAs diminished when measuring the suprascapular nerve distal which is made up of loose areolar tissue (26, 27). The outer border
PARTICIPANTS’ CHARACTERISTICS
Age (year) 31.4 ± 5.8 33.8 ± 4.5 47.9 ± 5.7 49.6 ± 5.9 69.0 ± 6.2 69.7 ± 6.5 <0.001
Height (cm) 170.6 ± 6.4 160.2 ± 5.4 171.7 ± 5.7 159.6 ± 3.8 166.1 ± 6.0 166.1 ± 6.0 <0.001
Weight (kg) 66.9 ± 5.5 55.1 ± 8.2 70.2 ± 6.7 57.5 ± 9.1 64.9 ± 8.2 64.9 ± 8.2 <0.001
SHOULDER PATHOLOGY (n, PERCENT IN SUBGROUPS)
Biceps tendinopathy 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) N.A.
Subscapularis tendinopathy 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) N.A.
Subscapularis calcification 0 (0%) 0 (0%) 0 (0%) 1 (5%) 0 (0%) 0 (0%) 0.411
Supraspinatus tendinopathy 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) N.A.
Supraspinatus calcification 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (5%) 0 (0%) 0.411
Supraspinatus tendon tear 0 (0%) 0 (0%) 0 (0%) 1 (5%) 1 (5%) 0 (0%) 0.540
Infraspinatus tendinopathy 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) N.A.
Infraspinatus calcification 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) N.A.
Infraspinatus tendon tear 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) N.A.
Annotation: N.A, not applicable due to zero count in each selected cell.
TABLE 2 | Comparison of nerve cross-sectional area measurements (mm2 ) among different age and gender groups.
CSA (C5, IE) 8.37 ± 1.59a 6.38 ± 1.04adef 8.40 ± 1.30d 7.95 ± 0.72e 8.19 ± 1.59f 7.51 ± 0.91 <0.001
CSA (C6, IE) 9.14 ± 2.06 8.18 ± 1.54d 10.09 ± 1.44dgh 8.53 ± 0.89g 9.21 ± 1.27 8.33 ± 1.14h <0.001
CSA (SNBP, IE) 2.04 ± 0.54abc 1.58 ± 0.32adf 2.10 ± 0.43dgh 1.52 ± 0.23bgi 2.14 ± 0.38fij 1.37 ± 0.36chj <0.001
CSA (SNMC, IE) 2.07 ± 0.47bc 1.73 ± 0.61 2.03 ± 0.36h 1.63 ± 0.37bi 2.09 ± 0.43ij 1.42 ± 0.33chj <0.001
CSA (C5, OE) 15.63 ± 3.40ac 11.67 ± 1.76adef 16.17 ± 3.21dh 14.27 ± 2.38e 14.92 ± 2.77f 12.97 ± 1.76ch <0.001
CSA (C6, OE) 16.87 ± 3.10 14.90 ± 2.49d 18.11 ± 3.09d 15.68 ± 2.36 16.97 ± 2.13 16.45 ± 2.16 0.004
CSA (SNBP, OE) 4.98 ± 1.89c 4.20 ± 1.20 4.78 ± 1.07h 4.05 ± 0.99 4.99 ± 0.96j 3.55 ± 0.86chj <0.001
CSA (SNMC, OE) 4.38 ± 0.66c 4.12 ± 1.40k 4.59 ± 069h 4.07 ± 0.98l 4.97 ± 0.82j 2.58 ± 1.48ckhlj <0.001
CSA (SNSS, OE) 10.18 ± 2.29 9.34 ± 2.18 11.07 ± 2.80 9.31 ± 1.87 10.56 ± 1.31 9.73 ± 1.08 0.038
CSA (SNIS, OE) 10.99 ± 2.52 9.41 ± 9.62 9.62 ± 1.95 9.80 ± 1.67 9.35 ± 1.35 10.42 ± 1.40 0.048
CSA, cross-sectional area; IE, inside-epineurium method; OE, outside-epineurium method; SNBP, suprascapular nerve departing from the brachial plexus; SNMC, suprascapular nerve
at the mid-clavicular level; SNSS, suprascapular nerve at the floor of the supraspinatus fossa; SNIS, suprascapular nerve at the spinoglenoid notch of the infraspinatus fossa.
Annotation for post-hoc analysis of between-group difference: a indicates significant between men (age ≥ 20 and < 40) and women (age ≥ 20 and < 40); b indicates significant
between men (age ≥ 20 and < 40) and women (age ≥ 40 and < 60); c indicates significant between men (age ≥ 20 and < 40) and women (age ≥ 60); d indicates significant between
women (age ≥ 20 and < 40) and men (age ≥ 40 and < 60); e indicates significant between women (age ≥ 20 and < 40) and women (age ≥ 40 and < 60); f indicates significant
between women (age ≥ 20 and < 40) and men (age ≥ 60); g indicates significant between (age ≥ 40 and < 60)and women (age ≥ 40 and < 60); h indicates significant between men
(age ≥ 40 and < 60) and women (age ≥ 60); i indicates significant between women (age ≥ 40 and < 60) and men (age ≥ 60); j indicates significant between women (age ≥ 60) and
men (age ≥ 60); k indicates significant between women (age ≥ 20 and < 40) and women (age ≥ 60); l indicates significant between women (age ≥ 40 and < 60) and women (age ≥
60).
of the epineurium is sometimes not well defined, especially when factors (e.g., men are usually taller and heavier than women)
the nerve courses inside or passes through fasciae. Nevertheless, are inter-correlated and exhibit collinearity during multiple
we investigated the CSA by using the outside-epineurium regression analysis, the association of nerve sizes with subjects’
method for deeper nerves because the inner boundary of the features varies across different reports. Regarding the upper
epineurium was very hard to differentiate at the bottom of the extremity nerves, Sugimoto et al. studied 60 healthy Japanese
supraspinatus and infraspinatus fossae. adults and demonstrated that gender and wrist circumference
There are multiple studies that report a correlation between are associated with CSA of the median and ulnar nerves at the
the nerve CSA and participants’ characteristics, such as age, non-entrapment sites (excluding the carpal, cubital and Guyon’s
sex, hand dominance, and body stature. As the aforementioned canals) (14). In terms of the cervical regions, Huan et al. reported
FIGURE 6 | Intra-rater (A) and inter-rater (B) reliabilities for measurement of nerve cross-sectional area. CSA, cross-sectional area; IE, intra-epineurium method; OE,
outside-epineurium method; ICC, Intraclass correlation coefficient; CI, confidence interval; UCL, upper confidence limit; LCL, lower confidence limit, SNBP,
suprascapular nerve departing from the brachial plexus; SNMC, suprascapular nerve at the middle clavicular level; SNSS, suprascapular nerve at the floor of the
supraspinatus fossa; SNIS, suprascapular nerve at the spinoglenoid notch of the infraspinatus fossa.
a trend of larger root sizes at the C5 and C6 levels in men than in which is made up of the C5 and C6 nerve roots, it is rational
women (28). In our study, the multivariate analysis demonstrates to expect the size of the proximal suprascapular nerve to be in
a negative association between female gender and the CSA values accordance with its root origins. Nevertheless, tracking a nerve
at the C5 and C6 nerve roots and the suprascapular nerve near to its peripheral portion, the nerve may become thinner or gives
the brachial plexus but not at its more distal levels. As the off its muscular and articular branches (7). Both the above-
suprascapular nerve directly branches from the superior trunk, mentioned factors can impact the CSA measurements, thereby
FIGURE 7 | Comparison of the size of the suprascapular nerve measured by the inside-epineurium (A) and outside-epineurium (B) methods. CSA, cross-sectional
area; IE, intra-epineurium method; OE, outside-epineurium method; SNBP, suprascapular nerve departing from the brachial plexus; SNMC, suprascapular nerve at the
middle clavicular level; SNSS, suprascapular nerve at the floor of the supraspinatus fossa; SNIS, suprascapular nerve at the spinoglenoid notch of the infraspinatus
fossa.
rendering gender difference to be a less significant concern in the suprascapular nerve is accompanied by the suprascapular
reporting CSA values for the distal suprascapular nerve. vessels in the supraspinatus and infraspinatus fossae. Although
Another important observation was that the size of the distal we had employed power Doppler imaging to identify adjacent
suprascapular nerve as measured by the outside-epineurium vasculature, the small arterial and venous branches were still
method was significantly larger than at its proximal portion. difficult to detect and may have falsely contributed to the
We propose 3 possible reasons that may contribute to this enlarged nerve size. Third, the suprascapular nerve from
finding. First, the suprascapular nerve gives off the articular the transverse scapular notch to the spinoglenoid notch is
branch at the glenohumeral joint and muscular branch at surrounded with variable amounts of perineural fat (Figure 4C).
the supraspinatus muscle in the supraspinatus fossa and Some hyperechoic fatty tissues may have been included in the
muscular branch at the infraspinatus muscle in proximity to CSA measurements while employing the outside-epineurium
the spinoglenoid notch (7). As the high frequency transducer method.
has limited resolution for structures that are located deep, it This study has two potential clinical implications. First, the
is challenging to employ US imaging to differentiate the nerve CSA values of the most proximal suprascapular nerve are likely
main stem from its branches (Figures 4C,D), all of which to be smaller in women than in men, with a difference of 0.5
were therefore included in the CSA measurement. Second, mm2 by using the inside-epineurium method and a difference
Annotation: * indicates p < 0.05. CSA, cross-sectional area; IE, inside-epineurium method; OE, outside-epineurium method; SNBP, suprascapular nerve departing from the brachial plexus; SNMC, suprascapular nerve at the mid-clavicular
CSA (SNIS, OE)
Interpretation of pathological enlargement or atrophy of the
suprascapular nerve may be based on a gender-specific reference,
especially for observation in proximity to the brachial plexus.
Secondly, the distal suprascapular nerve is not the same size as
its proximal portion under US imaging. The clinicians should
−0.885* (p = 0.005) −1.074* (p = 0.011) −0.532* (p < 0.001) −0.294 (p = 0.105) −1.764* (p = 0.034) −2.221* (p = 0.001) −0.948* (p = 0.030) −0.518 (p = 0.263) −1.020 (p = 0.063)
0.001 (p = 0.968)
CSA (SNSS, OE)
0.029 (p = 0.398)
0.017 (p = 0216)
CSA (SNMC, OE)
0.700 (p = 0.090)
−0.029 (p = 0.640)
−0.019 (p = 0.637)
CSA (C6, OE)
CONCLUSIONS
0.013 (p = 0.539)
0.213 (p = 0.581)
0.072 (p = 0.265)
0.005 (p = 0.923)
CSA (C5, OE)
AUTHOR CONTRIBUTIONS
K-VC conceived and supervised this work. W-TW, KM,
0.004 (p = 0.677)
−0.125 (p = 0.609)
−0.011 (p = 0.767)
0.015 (p = 0.467)
validation, and analysis with input from K-VC. W-TW wrote the
manuscript with critical feedback from K-VC.
FUNDING
0.012 (p = 0.236)
0.203 (p = 0.303)
0.013 (p = 0.064)
0.002 (p = 0.930)
CSA (C5, IE)
SUPPLEMENTARY MATERIAL
explanatory
Age (year)
reference)
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