E ORIGINAL ARTICLE

Shoulder & Elbow

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sensory receptors in the human DOI: 10.1177/1758573218760245
journals.sagepub.com/home/sel
elbow joint capsule

Erica Kholinne1,3, Hyun-Joo Lee2, Maria F Deslivia1,

Kim Ga Yeong3, Suk-Joong Lee4, Sungjoon Lim3
and In-Ho Jeon3

Abstract
Background: The topographic arrangement of sensory receptors in the human elbow joint capsule is pertinent to their
role in the transmission of neural signals. The signals from stimuli in the joint are concisely delivered via afferent pathways
to allow recognition of pain and proprioception. Sensory receptors in the elbow joint include mechanoreceptors and
free nerve endings acting as nociceptors, although the distribution of each of the structures has not been determined,
despite their importance for the integrity of the joint. We therefore aimed to investigate the neuroanatomical distri-
bution and densities of mechanoreceptors and free nerve endings in the capsule of the elbow, at the same time as
considering surgical approaches that would result in the minimum insult to them.
Methods: Four elbow joint capsules were harvested from fresh cadavers. The specimens were carefully separated from
adjacent osteoligamentous attachments and the capsular complex was stained with a modified gold chloride method.
Evaluations of free nerve endings, and Golgi, Ruffini and Pacinian corpuscles were performed under an inverted light
microscope. The number and density of each structure were recorded.
Results: Ruffini corpuscles observed to be the dominant mechanoreceptor type. No Golgi corpuscle was observed.
Free nerve endings were found at the highest density at posterodistal sites, whereas mechanoreceptors were most
frequent at bony attachment sites.
Conclusions: A consistent distribution pattern of articular sensory receptors was observed, which allows further
understanding of elbow pathology. An awareness of the neuroanatomical distribution of sensory receptors in the
elbow joint capsule may allow their preservation during surgical procedures for elbow joint pathology.

Keywords
capsule, elbow, distribution, neuroanatomical, sensory receptors
Date received: 4th October 2017; revised: 6th December 2017; accepted: 19th January 2018

Introduction 1
Department of Orthopedic Surgery, St Carolus Hospital, Jakarta,
The elbow joint is stable as a result of its native gyn- Indonesia
2
Department of Orthopedic Surgery, Kyungpook National University
glymoid shape.1 However, the elbow capsule and its
Hospital, Daegu, Republic of Korea
ligamentous structure have been described as contribut- 3
Department of Orthopedic Surgery, Asan Medical Center, University of
ing to elbow joint stability.2 Mechanoreceptors in tissue Ulsan, Seoul, Republic of Korea
4
sense proprioception and transmit afferent signals as a Department of Orthopedic Surgery, Keimyung University, Dongsan
protective reflex against instability.3–6 The role of col- Medical Center, Daegu, Korea
lateral ligaments in the stability of the elbow has been
Corresponding author:
well studied;7 however, there nevertheless remains a In-Ho Jeon, Department of Orthopedic Surgery, University of Ulsan,
paucity of research on the elbow capsule. A previous Asan Medical Center, 86 Asanbyeongwon-gil, Songpa-gu, Seoul, Korea.
anatomical study has demonstrated that oblique and Email: jeonchoi@gmail.com
2 E
transverse fibrous bands exist in the anterior side of the
elbow capsule.8 In the clinical perspective, the capsule
of the elbow joint plays a major part in arthrofibrosis
cases.9 The intrinsic contractures present in such cases
have led to the identification of the elbow capsule as the
main site of pathology. Recently, the elbow capsule was
observed to contribute to painful elbow conditions such
as tendinopathy of the common extensor tendon and,
in addition, innervation of the undersurface of the
elbow capsule may generate pain in common extensor
tendon malady.10 In the present pilot study, which
aimed to provide an increased understanding of the
elbow capsule, we observed the microanatomy of four
fresh-frozen cadaveric elbows for the existence and dis-
tribution of mechanoreceptors and free nerve endings.
Our hypotheses were: (i) sensory receptors exist in the
human elbow capsule and (ii) the density of sensory
receptors varies according to location within the
elbow capsule.
Materials and methods
Cadaver dissection and specimen preparation
The capsules of four elbow joints were harvested from
fresh-frozen cadavers. All were males and had a mean
age of 69 years. No history of previous elbow injury
was found on the medical records. The elbow capsules
were harvested within 12 hours of the cadavers being
thawed at room temperature. Dissection was carefully
performed, taking care to obtain the entire capsule por-
tions, without causing damage to them. The attachment
to the bone was peeled off. After dissection, the speci-
mens were immersed in 4% paraformaldehyde solution
with a neutral pH. After fixation in the solution for at
least 24 hours, the specimens were divided into regions
of interest according to their location (anterior and pos-
terior) and bony attachment site (proximal, distal bony
attachment and mid-substance).
Modified gold chloride staining
The O’Connor and Gonzales modified gold chloride
staining method was applied to the specimens.11 Vials
consisting of fresh lemon juice and 98% formic acid
solution in a 3 : 1 ratio were prepared and shaken
with a penetron shaker (Penetron Swirling Shaker
Model Mark IV; SPI Supplies, Sunkay Laboratories,
Tokyo, Japan) inside a fume hood for 30 minutes.
Gold chloride solution (Gold chloride solution
200 mg/dL in deionized water, HT1004; Sigma-
Aldrich, St Louis, MO, USA) was then added to the
vials and they were shaken for a further 90 minutes.
This process was repeated for later batches after recy-
cling the gold chloride solution from the previous batch
Shoulder & Elbow 0(0)
through a filtration process. The gold chloride solution
was subsequently removed, and the specimens were
soaked with 2.5% formic acid solution and shaken
for at least another 12 hours. Following this shaking,
the specimens were washed three times with running
distilled water for 5 minutes to remove the solution.
Each specimen was then transported to a conical tube
prefilled with 30% sucrose solution and stored in a
refrigerator at 4 C for 1 day to 2 days. After a specimen
had sunk to the bottom of the conical tube, it was
transferred to a new vial containing 30% sucrose and
optimum cutting temperature compound (OCT). These
vials were then shaken with the penetron shaker for 2
hours. Once this process was completed, the stained
specimens were embedded in 30% sucrose and OCT
compound in a 3 : 2 ratio and then frozen, in accord-
ance with a previously reported technique.12 A cryo-
sectioning machine (Leica CM3050-S Research
Cryostat; Leica Biosystems, Nussloch, Germany) was
then used to section the frozen specimens parallel to
their longitudinal (horizontal) axis and perpendicular
to their vertical axis, with 30 -mm thick slices being
attached to glass microscope slides.
Microscopic examination
An inverted light microscope was used for observation
of mechanoreceptors. The Freeman and Wyke classifi-
cation with the modification of Hagert et al. was used
as a reference for evaluating the types and numbers of
Golgi, Ruffini, and Pacinian corpuscles.6,13,14 The slides
were first visualized under low power magnification
( 100) and then at higher magnification ( 200) to
identify each receptor. During inspection of the mech-
anoreceptor structures, checks were made on previous
and lateral serial slides to determine whether the struc-
ture was continuously visible. If a structure was con-
firmed, it was counted as one unit. Discontinued objects
with uncertain or doubtful morphology were not
counted. We reconfirmed each structure using  400
magnification to minimize any misreading or poten-
tial bias that might alter the quantification.
Mechanoreceptors were evaluated and recorded in
accordance with their location (anterior and posterior)
and bony attachment site (proximal, distal bony attach-
ment and mid-substance).
Density calculation
To measure the volume of region of interest, custo-
mized software was used to automatically measure the
area on the slide. This customized software was design
based on object detection and recognition. Software
was written in OpenCV-Python, version 2.7 (Python
Software Foundation, Reston, VA, USA).15 The area
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was then multiplied by 30 mm (the slice thickness) to
estimate the total volume. In this manner, the total
volume of each compartment was calculated. The dens-
ity of mechanoreceptors was defined as the number of
mechanoreceptors divided by the unit volume (number/
cm3) of tissue. Density comparisons were made between
the anterior and posterior sites, as well as between the
proximal, distal bony attachment and mid-substance
sites.
Results
We observed Ruffini and Pacinian corpuscles (Figures 1
and 2) and free nerve endings (Figure 3) within the
capsules. These sensory receptors were located mostly
in the subsynovial layer. They were mostly surrounded
Figure 1. A coil-shaped Ruffini corpuscle (yellow arrow) with
partial encapsulation. This low threshold and slow adapting
mechanoreceptor has arborizing nerve branches with bulbous
terminals (magnification  200).
Figure 2. A Pacinian corpuscle (yellow arrow) observed as an
ovular corpuscle with a thick lamellar capsule; it was embedded
in ligament fibres. Pacinian corpuscles have a low threshold and
rapidly adapting mechanoreceptor characteristics
(magnification  200).
3
by loose connective synovial tissue and medium to large
sized vessels.
Density of mechanoreceptors and free nerve endings
The mean densities of mechanoreceptors and free nerve
endings grouped according to their location and attach-
ment site are provided in Table 1.
Discussion
As a gynglymoid hinged joint, the elbow is stable
according to its native structure. Bony and soft tissue
constraints form the primary elbow joint stabilizers,
with the capsule and muscle complex acting as second-
ary stabilizers. Elbow instability may deteriorate fol-
lowing insult to secondary stabilizers.16 A previous
study showed that elbow capsule lesions were almost
always associated with complex elbow instability.17 The
functions of mechanoreceptors in relation to capsular
structures are unclear. The proprioceptive organs in a
normal intact elbow joint provide active elbow joint
stability. The maximal stimulation of afferent signals
from an articular site occurs when the joint is max-
imally loaded.18 This supports not only the idea of
the capsule as a mechanical stabilizer, but also as it
having a protective reflexogenic function. Hence,
there is an urgent need to understand the mechano-
receptors as a protective reflexogenic organ for the
joint. The role of mechanoreceptors has been studied
widely in the knee joint. The existence of
Figure 3. Large nerve fibres observed under synovial tissue
(magnification  200).
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Table 1. Mean (SD) densities of mechanoreceptors and free nerve endings according to location (per cm3 of tissue).
Mechanoreceptors
Location Golgi corpuscle Ruffini corpuscle
Anterior Proximal 0 1.60 (0.33)
Mid-substance 0 1.84 (0.87)
Distal 0 1.94 (0.52)
Posterior Proximal 0 1.40 (0.45)
Mid-substance 0 0.82 (0.11)
Distal 0 1.23 (0.28)
mechanoreceptors in the elbow joint has also been
reported; however, there has been a lack of information
on their spatial arrangement within the capsule.19 The
present study now provides a description of their dis-
tributions and densities.
We did not observe the presence of Golgi corpuscles
within the elbow capsule. This suggests that not all
types of mechanoreceptors are present in the elbow
capsule, a finding that is supported by a study that
only found Golgi corpuscles in joint ligaments.20 The
density of mechanoreceptors was higher in the anterior
part of the capsule than in the posterior part, with
Ruffini corpuscles being found to be the major receptor
type. As a slow adapting receptor, Ruffini corpuscles
are always active, even when a joint is static. They sense
changes in intra-articular pressure, as well as the direc-
tion and amplitude of joint movements. These cor-
puscles also regulate muscle reflex and tone under
continuous tonic conditions. Any extreme torque
within the joint caused by extension, flexion or rotation
will be signalled by Ruffini corpuscles.21 Pacinian cor-
puscles were also shown to co-exist with Ruffini cor-
puscles. As a fast adapting receptor, Pacinian
corpuscles control acceleration, quick joint movement
and vibration. Pacinian corpuscles will signal mechan-
ical stimuli at the onset or cessation of a movement.20
The concurrent equilibrium action between these two
sensory receptors is important for joint stabilization.
We were not able to identify the existence of Pacinian
corpuscles in the posterior capsule (mid-substance and
distal site) and the paucity of this region might indicate
that this area of the capsule does not have a major
contribution to fast acceleration in joint movements.
This is also supported by the scarcity of other mech-
anoreceptors in the mid-substance site. Therefore, we
suggest that surgical approaches might be best con-
ducted through this site, rather than bony attachment
sites. Approaches through bony attachment sites would
likely insult the articular mechanoreceptors, which
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Pacinian corpuscle Total Free nerve endings
0.80 (0.16) 2.4 (0.49) 1.94 (0.15)
0.27 (0.55) 2.12 (1.16) 2.40 (0.33)
0.13 (0.29) 2.07 (0.40) 1.49 (0.75)
0.54 (0.77) 1.95 (0.31) 2.27 (1.67)
0 0.82 (0.11) 2.11 (0.88)
0 1.23 (0.28) 2.77 (1.89)
could result in a proprioceptive deficit leading to recur-
rent instability.22 Awareness of the mechanoreceptor
distribution in the elbow capsule may allow the surgeon
to preserve proprioceptive integrity during surgery and
improve postoperative joint stability.
Free nerve endings will detect pain stimuli and trans-
mit them to the central nervous system; they have been
studied widely in respect to their association with pain
generation in lateral epicondylitis pathology.10,23 The
present study showed that free nerve endings were at
a higher density in the posterior distal sites. An anat-
omy study on cadavers showed that the attachment of
the joint capsule at the posterior site, under the poster-
odistal of the extensor carpi radialis brevis origin,
merges with the supinator muscle complex.23 At this
site, the joint capsule forms an enthesis structure. By
taking both this and our findings into consideration,
this attachment site of the joint capsule could be a
pain generator in lateral epicondylitis pathology.
Limitations
The present study was solely an anatomical study and
involved a low number of samples; therefore, no statis-
tical analysis was performed in this pilot study. The
staining method used has not been tested on multiple
specimens in different age groups; hence, we were
unable to draw any conclusions regarding the morpho-
logical differences of sensory receptors in respect to the
age of tissue donors.
Conclusions
A consistent distribution pattern for articular sensory
receptors was observed; this allows further understand-
ing of elbow pathology. Awareness of the neuroana-
tomical distribution of the receptors in the elbow
joint capsule may allow their preservation during sur-
gical procedures for elbow joint pathology.
 E Kholinne et al.
Author Contributions
EK contributed to study design, data analysis and
drafting of the manuscript. HJL, MFD, KGY, SJL
and SJL contributed to study design and drafting of
the manuscript. IHJ contributed to study design and
critical revision of the manuscript.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest
with respect to the research, authorship, and/or publi-
cation of this article.
Funding
The author(s) disclosed receipt of the following financial
support for the research, authorship, and/or publication of
this article: This research was supported by the convergence
technology development program for bionic arm through the
National Research Foundation of Korea(NRF) funded by
the Ministry of Science, ICT & Future Planning (No.
2014M3C1B2048422).
Ethical review and patient consent
The present study was approved by our Institutional Review
Board.
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