Diaphragm Contractility in Individuals with

Chronic Ankle Instability

MASAFUMI TERADA1, KYLE B. KOSIK2, RYAN S. MCCANN2, and PHILLIP A. GRIBBLE2
1
College of Sport and Health Science, Ritsumeikan University, Kusatus, Shiga, JAPAN; and 2Department of Rehabilitation
Science, University of Kentucky, Lexington, KY

ABSTRACT
TERADA, M., K. B. KOSIK, R. S. MCCANN, and P. A. GRIBBLE. Diaphragm Contractility in Individuals with Chronic Ankle
Instability. Med. Sci. Sports Exerc., Vol. 48, No. 10, pp. 2040–2045, 2016. Introduction/Purpose: Previous investigations have iden-
tified impaired trunk and postural stability in individuals with chronic ankle instability (CAI). The diaphragm muscle contributes to trunk
and postural stability by modulating the intra-abdominal pressure. A potential mechanism that could help to explain trunk and postural
stability deficits may be related to altered diaphragm function due to supraspinal sensorimotor changes with CAI. The purpose of this
study was to examine the diaphragm contractility in individuals with CAI and healthy controls. Methods: Twenty-seven participants
with self-reported CAI and 28 healthy control participants volunteered. A portable ultrasound unit was used to visualize and measure the
right and left hemidiaphragm thickness at the end of resting inspiration and expiration in supine while breathing quietly. The diaphragm
movement was imaged and recorded on B-mode ultrasonography. The degree of diaphragm contractility was calculated from the mean of
three images from the end of resting inspiration and expiration. Independent t-tests were used to compare the degree of diaphragm
thickness of right and left sides between the CAI and the control groups. Results: The CAI group had a smaller degree of left
hemidiaphragm contractility compared with the control group (P = 0.03). There was no between-group difference in other diaphragm
variables. Conclusion: Individuals with CAI appear to have altered diaphragm contractility, which may be an illustration of diaphragm
dysfunction and central nervous system changes in CAI population. The association between CAI and altered diaphragm contractility
provides clinicians a more comprehensive awareness of proximal impairments associated with CAI. Future investigation is needed to
determine whether altered contractility of the diaphragm contributes to functional impairments, activity limitations, and participant
restrictions commonly observed in patients with CAI. Key Words: ANKLE SPRAIN, SENSORIMOTOR CONTROL, NEURO-
MUSCULAR FUNCTION, POSTURAL STABILITY

C
hronic ankle instability (CAI) is a highly prevalent
musculoskeletal disorder characterized by life-long
residual symptoms and recurrent ankle sprains
(10,18) that develop in up to 70% of initial ankle injuries
(31,42). CAI can lead to persistent disability and significant
negative squealae (25,26,28,31). More importantly, more
than 70% of patients with CAI can develop early onset of
degenerative disease of the articular cartilage at the ankle
joint (15,45), forcing them to limit their level of physical
activity (28,47), potentially decreasing health-related quality
of life (1,25,26). Despite an increase in the attention and
focus CAI receives, effective intervention strategies may be
still limited. To stop a cascade of patients with CAI from
entering paths of long-term disability, it is important to
APPLIED SCIENCES
further understand the underlying mechanism that may
contribute to CAI. This may provide clinicians valuable in-
formation for identifying relevant impairments on which to
focus during interventions for CAI.
Altered sensorimotor control that leads to global dysfunction
is considered to be an important contributing factor to CAI
(21,49). It has been suggested that after an initial lateral ankle
sprain, altered sensory inputs from the somatosensory system
around the ankle and supraspinal changes in the central ner-
vous system (CNS) may lead to proximal joint maladaptations
to compensate for residual symptoms and decreased function
(4,12,21,33,46). In particular, Marshall et al. (33) identified
impaired trunk stability in individuals with CAI that was as-
sociated with postural control deficits. Deficits in postural

control have been well documented in patients with CAI

(17,36). de la Motte et al. (9) reported altered movement pat-
terns at the trunk and pelvis during a dynamic postural stability
Address for correspondence: Masafumi Terada, Ph.D., A.T.C., Integration
Core Building 602, 1-1-1 Noji-higashi, Kusatsu, Shiga 525-8577, Japan; task in a CAI population. In addition, insufficient ability to
E-mail: mterada@fc.ritsumei.ac.jp. coordinate muscles surrounding the hip joint has been ob-
Submitted for publication January 2016. served in individuals with CAI (4,12,46), which also influence
Accepted for publication May 2016. trunk and postural stability.
0195-9131/16/4810-2040/0 The diaphragm muscle, synergistically working with the
MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ muscles of the deep abdominal wall, pelvic floor, and deep
Copyright Ó 2016 by the American College of Sports Medicine posterior trunk, creates the basis of the body_s core (5). The
DOI: 10.1249/MSS.0000000000000994 diaphragm significantly contributes to trunk and postural

2040

Copyright © 2016 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
stability by modulating the intra-abdominal pressure (22,
23,29,30,35). A potential mechanism that could help to ex-
plain trunk and postural stability deficits may be related to the
altered function of the diaphragm due to supraspinal senso-
rimotor changes with CAI. Researchers have reported that
patients with lower back pain exhibited postural control def-
icits and poor diaphragm function (29,48). Furthermore,
Bradley and Eshormes (3) found a potential association be-
tween the poor coordination of the diaphragm and the dys-
functional movement patterns. However, we are unaware of
any previous study designed specifically to examine the dia-
phragm structural integrity and contractility in individuals
with CAI. By establishing an association of diaphragm con-
tractility with CAI, it will provide a foundation for continued
work to identify specific factors that contribute to persistent
self-reported and physical disability in patients with CAI.
A more comprehensive awareness of proximal impairments
associated with CAI will allow clinicians to target specific
impairments during rehabilitation and prevention programs.
Therefore, the purpose of this study was to examine the
diaphragm contractility between individuals with CAI and
healthy controls.
METHODS
Study design. This study was conducted with a single-
blinded, case–control design. A single investigator screened
participants for inclusion criteria, and the investigator re-
sponsible for measuring diaphragm contractility was blinded
to group membership. Participants reported to the research
laboratory for a single testing session.
Participants. Fifty-five physically active participants
from the university community volunteered for the current
study (Table 1). Participants_ physical activity levels were
determined using the Godin Leisure-Time Exercise Ques-
tionnaire (14), and physically active was defined as a Godin
leisure-time score of 24 or higher (13). All participants read
and signed an informed consent approved by the university
institutional review board before the study. All participants
TABLE 1. Demographic and ankle injury characteristics for CAI and control groups (mean T SD).
CAI
n 27 (4 males, 23 females)
Age (yr) 22.58 T 3.33
Height (cm) 168.86 T 7.67
Body mass (kg) 70.01 T 13.53
Godin leisure-time exercise 94.25 T 73.50
AII 6.37 T 1.69
IdFAI 19.85 T 4.87
CAIT 14.96 T 5.34
No. lateral ankle sprains 3.63 T 2.37 (range = 1–10)
Time since last ankle sprain (month) 44.33 T 42.37
No. giving-way episodes in past 6 months 8.33 T 13.53 (range = 2–72)
Modified physical activity because of CAI Yes: 14
No: 13
Feel a risk for injury when playing sports Yes: 17
No: 10
Concerned with surrounding environment Yes: 16
No: 11
*Significant differences in AII, IdFAI, and CAIT between groups (P G 0.05).
DIAPHRAGM CONTRACTILITY AND ANKLE INSTABILITY
Copyright © 2016 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
had no history of 1) diagnosed balance or vestibular disorders;
2) self-reported low back pain; 3) surgery in the lower ex-
tremity; 4) a concussion in the past 6 months; 5) diagnosed
cardiopulmonary disorder, scoliosis, ankylosing spondylitis, or
any other disorders that can affect/alter the function of respi-
ratory system; and 6) any self-reported musculoskeletal and
neurovascular injuries and disorders in the lower extremity in
the past 2 yr (other than lateral ankle sprains).
After enrolling and screening participants with self-
reported questionnaires, they were allocated to the CAI or
control group. Twenty-seven participants were included in
the CAI group based on the guidelines endorsed by the In-
ternational Ankle Consortium (18). The specific inclusion
criteria for participants with CAI included the following: 1)
a previous history of at least one significant lateral ankle
sprain resulting in swelling, pain, and temporary loss of
function; 2) a history of feelings of giving way at least twice
in the past 6 months; 3) ongoing perceived ankle instability
and dysfunction during daily activities; and 4) a score of Q5
on the Ankle Instability Instrument (AII), Q11 on the Iden-
tification of Functional Ankle Instability (IdFAI), and G24
on the Cumberland Ankle Instability Tool (CAIT) (18). No
participant with CAI had acutely sprained his/her ankle in
the previous 3 months of testing. If a CAI participant had
bilateral lateral ankle sprain history, the limb that was self-
reported to have more instability was screened with the
procedures described previously and included if the criteria
were met. The control group included 28 participants. The
control group participants were required to have no history
of lateral ankle sprain, score 0 on both the AII and the
IdFAI, and score 30 on CAIT.
Structural integrity assessment of the diaph-
ragm. Participants laid supine comfortably on an examina-
tion table for the experiment. A portable ultrasound unit
(LOGIO e2008; GE Healthcare, Wauwatosa, WI) was used to
visualize and measure the left hemidiaphragm thickness at the
end of resting inspiration and expiration and the degree of
contractility in supine while breathing quietly. It has been
suggested that the left hemidiaphragm in a condition associated
Control P
28 (9 males, 19 females) —
21.04 T 1.88 0.08 APPLIED SCIENCES
168.50 T 9.80 0.88
66.12 T 12.39 0.27
82.52 T 82.00 0.82
0.00 G0.001*
0.00 G0.001*
30.00 T 0.00 G0.001*
— —
— —
— —
Yes: 0 —
No: 28
Yes: 0 —
No: 28
Yes: 0 —
No: 28
Medicine & Science in Sports & Exercised 2041
 FIGURE 1—B-mode ultrasonography image during inspiration during inspiration (A) and expiration (B).

with neuromuscular dysfunction in the lumbar–pelvic–femoral
region trends to be more of a postural stabilizer than a respira-
tory muscle because of altered force–length relationship of a
diaphragm muscle fiber (5,27). Therefore, in this current study,
we assessed the structural integrity and contractility only of left
half of the diaphragm.
Ultrasound evaluation for diaphragm thickness and the
degree of contractility was performed as previously de-
scribed (19,40). An 8- to 13-MHz linear-array transducer
(12 L-RS; GE Healthcare) was placed perpendicularly over
the chest wall in the intercostal space between the eighth and
the ninth ribs at the midaxillary line on the right and left
sides to visualize the zone of apposition of the diaphragm
(19,40). The diaphragm was identified as a structure with a
three-layered appearance (hypoechogenic central layer bor-
dered by two echogenic layers, including the peritoneum
and the diaphragmatic pleurae) (44).
Three images were captured at the end of quiet expiration
(Fig. 1A) and inspiration (Fig. 1B) and recorded on B-mode
ultrasonography. The diaphragm thickness (cm) was mea-
sured as the distance from the middle of the pleural line to
the peritoneum lines using electronic calipers (19,40). Eval-
uation of diaphragm thickness and contractility using B-mode
ultrasound has been demonstrated to be valid (7) and reliable
(ICC = 0.94–0.98) (19). The diaphragm muscle contracts con-
centrically during inspiration, shortening the muscle fibers and
increasing diaphragmatic thickness (16,19). During expiration,
the diaphragm muscle fibers become lengthened with eccentric
contraction (23), decreasing the thickness. The degree of dia-
phragm contractility was calculated from the mean of three im-
ages from the end of resting inspiration (Tinsp) and expiration
(Texp) using the following formula: (Tinsp j Texp)/Texp  100
APPLIED SCIENCES
Statistical analysis. An a priori alpha level was set at
P G 0.05 using SPSS 23.0 (SPSS Inc. Chicago, IL) for all
statistical tests. Physical activity levels (Godin Leisure-Time
Exercise Questionnaire), height, body mass, and body mass
index were compared between the CAI and the control
groups using independent t-tests. On the basis of data anal-
ysis using a Kolmogorov–Smirnov Z test for normality, we
found that age and scores from self-reported ankle instability
questionnaires (AII, IdFAI, and CAIT) were not normally
distributed (P G 0.05). Therefore, a separate Mann–Whitney
U test was performed to compare these variables between
the CAI and the control groups.
Independent t-tests were used to assess group difference in
diaphragm outcome measures. Cohen_s d effect sizes using
the mean and the pooled SD values were calculated (6), along
with 95% confidence interval (CI), to determine the magni-
tude of differences in outcome variables between groups. The
strength of effect sizes was interpreted as weak (d G 0.40),
moderate (0.40 e d G 0.80), or strong (d Q 0.80) (6).
RESULTS
Anthropometric characteristics and levels of physical ac-
tivity on the Godin Leisure-Time Exercise Questionnaire
were not different between the CAI and the control groups
(P 9 0.05, Table 1). Participants with CAI scored signifi-
cantly higher on the AII and IdFAI as well as lower on the
CAIT compared with healthy controls (P G 0.001, Table 1).
Additional ankle injury characteristic information is provided
in Table 1. The mean and SD values of each diaphragm
variable can be found in Table 2.

(40). A higher percentage of contractility indicates a greater The CAI group had a smaller degree of left hemidiaphragm
change in diaphragm thickness from the end of inspiration to contractility compared with the control group (t53 = j2.29,
expiration (i.e., more diaphragm contractile activity). P = 0.03), with a moderate effect size (d = j0.64, 95% CI =
TABLE 2. Mean and SD values for outcome measures of left hemidiaphragm structural integrity.
CAI Controls P Cohen_s d (95% CI)
Left Thickness: inspiration (cm) 0.16 T 0.05 0.19 T 0.05 0.07 j0.50 (j1.03 to 0.04)
Thickness: expiration (cm) 0.14 T 0.04 0.14 T 0.04 0.38 j0.24 (j0.76 to 0.30)
The degree of contractility (%) 21.62 T 11.76* 29.07 T 12.32 0.03 j0.62 (j1.15 to j0.07)
Right Thickness: inspiration (cm) 0.18 T 0.05 0.18 T 0.05 0.82 0.06 (j0.47 to 0.59)
Thickness: expiration (cm) 0.15 T 0.04 0.14 T 0.04 0.46 0.20 (j0.33 to 0.73)
The degree of contractility (%) 22.93 T 14.66 27.43 T 17.78 0.31 j0.28 (j0.80 to 0.26)
*The CAI group exhibited significantly less values than healthy control groups (P G 0.05).

2042 Official Journal of the American College of Sports Medicine http://www.acsm-msse.org

Copyright © 2016 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
j1.18 to j0.08). There was no significant between-group
difference in other diaphragm variables (Table 2).
DISCUSSION
We used B-mode ultrasonography to examine structural
integrity and contractility of the diaphragm by measuring
thickness of the muscle and the thickening ratio during
normal respiration. The main finding from this current study
was that participants with CAI exhibited a smaller degree of
left hemidiaphragm contractility during a quiet breathing
compared with healthy controls. The moderate effect size
value for left hemidiaphragm contractility, with CI that did not
cross zero, suggests clinically meaningful differences may be
present. Although we did not observe significant differences
in left hemidiaphragm thickness at the end of inspiration be-
tween groups, the moderate effect size indicates that the left
hemidiaphragm thickness at the end of inspiration might be
decreased in the CAI group compared with the control groups.
Participants with CAI appear to have altered diaphragm
function, which may support the notion of potential CNS al-
terations related to CAI (20,21). This current study provides
valuable information to identify a potential factor for clinical
impairments and functional limitations associated with CAI
on which clinicians could target for interventions.
Although the exact neurophysiological mechanism of al-
tered diaphragm contractility associated with CAI remains
unknown, it is hypothesized that disrupted or insufficient
sensory inputs from damaged ankle joint receptors to the
CNS due to existing CAI may chronically create a centrally
mediated alteration in neuromuscular function (20,21,38).
Although the central mechanism for sensorimotor control
may be a consequence of CAI to compensate for impair-
ments at the injured ankle (9,17), it may be leading to a
chronic neuromuscular maladaptation in other body loca-
tions that manifests as decreased diaphragm contractile ac-
tivity. An abundance of existing literature provides evidence
of altered neuromuscular function in more body regions
proximal to the ankle (4,12,17,21,33,46), such as delayed
trunk muscle reflex reaction (33) and altered neural re-
cruitments of hip muscles (4,12,46), in patients with an acute
lateral ankle sprain and those with CAI. Recently, re-
searchers have demonstrated a decrease in the excitability of
the primary motor cortex and descending spinal tracts that
may negatively influence motor control (38). The motor
control of the diaphragm involves both the voluntary com-
mands from corticospinal pathway and the involuntary ac-
tivity of brainstem (8,32). Perhaps altered joint awareness
due to impaired somatosensory inputs from the lateral ankle
complex and altered motor outputs from higher brain center
may change the neural recruitment of the diaphragm,
resulting in altered diaphragm contractility in this patho-
logical population.
Another potential theory that explains our observations is
that increased psychological stress due to existing CAI may
influence the respiratory control and breathing patterns,
DIAPHRAGM CONTRACTILITY AND ANKLE INSTABILITY
Copyright © 2016 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
possibly altering diaphragm contractility. Houston et al. (26)
observed psychological deficits in individuals with CAI. It is
well documented that negative psychological and emotional
states increase sympathetic nervous system activity (43),
leading to improper breathing strategies (34,35). If improper
breathing strategies are maintained for an extended period,
the position and activity of the diaphragm may be chroni-
cally altered (32). Incorporating diaphragm breathing exer-
cises might have beneficial effects in patients with CAI. This
is on speculative and future examination of psychological
health outcomes and breathing patterns in addition to dia-
phragm structure, and activity in CAI population is needed
to support this theory.
Altered recruitment strategies used by the CNS to control
the diaphragm may result in subsequent reductions in intra-
abdominal pressure (32) conducive to trunk and postural
instability that has been observed in individuals with CAI
(33). Marshall et al. (33) reported that participants with CAI
demonstrated delayed reflex response of the trunk muscles
to a sudden perturbation. The researchers also observed that
diminished postural stability was significantly associated
with impaired trunk stability in those with CAI (33). Nadler
et al. (37) reported that athletes with CAI may have greater
rates of low back pain, which may be related to dysfunction of
trunk stabilizing musculature. We cannot assume whether al-
tered diaphragm contractility observed in this current study in-
fluences trunk stability and postural control in individuals with
CAI. However, diaphragm function is critical to maintaining
total postural control and trunk stability to provide a stable base
for human movement (5).
Although the diaphragm is the primary respiratory muscle,
its significant role in trunk and postural stability has previ-
ously been documented (22–24,29). Hodges et al. (22–24)
noted that the contraction of the diaphragm contributes to the
control of trunk and postural stability during sudden voluntary
movements of the extremities through modulating intra-
abdominal pressure. It has been also reported that poor coor-
dination of the diaphragm influenced functional movement
patterns (3). Recently, published literature has reported a re-
duction in diaphragm movement during postural actives in
patients with chronic low back pain (29), a musculoskeletal
condition associated with the trunk instability and the poor
coordination of postural muscles (11). Therefore, altered di-
aphragm contractility could be a potential source for clinical
deficiencies within patients with CAI. Clearly, additional
APPLIED SCIENCES
examination of the associations of diaphragm structural in-
tegrity and contractility with outcome measures for trunk
stability and postural control is needed to determine whether
diaphragm function contributes to functional impairments,
activity limitations, and participant restrictions commonly
observed in patients with CAI.
Furthermore, although we have observed altered left
hemidiaphragm contractility during a quiet breathing in
participants with CAI, there were no differences in right
hemidiaphragm contractility or thickness at the end of inspi-
ration and expiration between those with and without CAI.
Medicine & Science in Sports & Exercised 2043
 Because of neural and mechanical differences between right
and left hemidiaphragms (27,39), an alteration only in the left
hemidiaphragm may strengthen asymmetrical patterns by re-
lying more on the right side, possibly leading to the loss of the
ability to work the right and left hemidiaphragms together (2).
Limitation. An important limitation to consider is its
cross-sectional retrospective design, making it difficult to
determine whether reduced left hemidiaphragm contractility
observed in the CAI group is due to the pathology or if the
alteration existed before injury. Future studies should at-
tempt prospectively to identify short- and long-term changes
in the position and movement of the diaphragm immediately
after an ankle sprain and how these may influence the de-
velopment of CAI.
Although participants were instructed to relax and quietly
breathe normally, similar to activities of daily living, we did
not control breathing volume using a spirometer. The dia-
phragm controls pulmonary function, and the lung volume
influences the structural integrity and contractility of the
diaphragm (7). No participants reported pulmonary disease,
and no differences in physical activity levels between the
CAI and the control groups were observed. However, it is
possible that differences in respiratory volume during the
quiet breathing among participants in this current study in-
fluence our observations. Additional respiratory measures,
such as tidal volumes, with the quantification of the position
and the movement of the diaphragm are needed to confirm
the effect of CAI on diaphragm contractility.
Although there were no differences in demographic char-
acteristics and physical activity levels between the CAI and
the control groups, it is still possible that these factors had
some effects on our findings. A previous study reported that
the diaphragm structure was related to body weight, age, and
thoracic dimensions (41). However, any of previous studies
examining the diaphragm thickness using B-mode ultrasonog-
raphy did not normalize the diaphragm variables (19,40), and
we are unaware of what is the best predictive factor for nor-
malizing the diaphragm thickness variable. We did conduct
an exploratory correlation analysis between diaphragm mea-
sures and demographic characteristics and physical activity
levels, finding nonsignificant weak associations between these
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