Download PDF Export Search ScienceDirect Advanced search

Recommended articles

Journal of Biomechanics
Citing articles ((00)
Available online 6 December 2017

In Press, Corrected Proof — Note to users

Related book content

Biomechanical consequences of running with deep core

muscle weakness
Margaret E. Raabea, ,
, Ajit M.W. Chaudharib
Show more

https://doi.org/10.1016/j.jbiomech.2017.11.037
https://doi.org/10.1016/j.jbiomech.2017.11.037
Get rights and content

Abstract
The deep core muscles are often neglected or improperly trained in athletes. Improper
function of this musculature may lead to abnormal spinal loading, muscle strain, or injury
to spinal structures, all of which have been associated with increased low back pain
(LBP) risk. The purpose of this study was to identify potential strategies used to
compensate for weakness of the deep core musculature during running and to identify
accompanying changes in compressive and shear spinal loads. Kinematically-driven
simulations of overground running were created for eight healthy young adults in
OpenSim at increasing levels of deep core muscle weakness. The deep core muscles
(multifidus, quadratus lumborum, psoas, and deep fascicles of the erector spinae) were
weakened individually and together. The superficial longissimus thoracis was a
significant compensator for 4 out of 5 weakness conditions (p​<​0.05). The deep erector
spinae required the largest compensations when weakened individually (up to a 45​±​10%
increase in compensating muscle force production, p​=​0.004), revealing it may contribute
most to controlling running kinematics. With complete deep core muscle weakness, peak
anterior shear loading increased on all lumbar vertebrae (up to 19%, p​=​0.001).
Additionally, compressive spinal loading increased on the upper lumbar vertebrae (up to
15%, p​=​0.007) and decreased on the lower lumbar vertebrae (up to 8%, p​=​0.008).
Muscular compensations may increase risk of muscular fatigue or injury and increased
spinal loading over numerous gait cycles may result in damage to spinal structures.
Therefore, insufficient strength of the deep core musculature may increase a runner’s
risk of developing LBP.

Keywords
Low back pain; Stability; Spine; Spinal loading; Injury; Musculoskeletal modeling

1. Introduction
In 2014, almost 19 million people completed a running road race in the USA, a 300%
increase from 1990 (Running, 2015). Unfortunately healthy running habits are often
interrupted by running injuries, with the annual running injury rate ranging from 24% to
65% (Macera et al., 1989; Marti et al., 1988 ; van Mechelen, 1992), and novice runners
may be the most susceptible to developing these injuries (Tonoli et al., 2010). The
prevalence of low back pain (LBP) in runners has been reported to be as high as 14%
(Taunton et al., 2002; Taunton et al., 2003 ; Woolf et al., 2002). LBP is most often a
chronic and recurrent condition that limits numerous activities of daily living (Hoy et al.,
2010). Despite its high prevalence, the root cause of LBP remains unclear (Hoy et al.,
2010). Improving core muscle strength and stability has shown potential to alleviate
symptoms of LBP (Chang et al., 2015), however it remains unknown how one’s level of
core strength may affect LBP risk.

The core musculature can be functionally separated into two groups, the superficial
muscles and deep muscles (Willson et al., 2005). The superficial muscles (rectus
abdominis (RA), external obliques (EO), internal obliques (IO), latissimus dorsi (LD),
superficial fascicles of the erector spinae (ES)) primarily function to produce movement
and transmit forces from the thoracic cage and pelvis to the extremities (Bergmark,
1989). The deep muscles (quadratus lumborum (QL), psoas major (PS), multifidus (MF),
and the deep fascicles of the ES) attach directly to the lumbar vertebrae and are believed
to function primarily to stabilize the lumbar spine (Fredericson and Moore, 2005). The
deep core muscles have been shown to activate prior to voluntary movement of the lower
extremities (Hodges and Richardson, 1997), suggesting they may act to stabilize the
spine in preparation for the loads experienced during dynamic tasks like running
(Fredericson and Moore, 2005). While a sufficient level of deep core muscle activation is
needed to stabilize the spine, excessive or improper activation of these muscles could
lead to abnormal spinal loading and consequently, LBP (Freeman et al., 2010 ; Hides et
al., 2008). The transversus abdominis (TrA) is another deep core muscle which may
contribute to spinal stability (Hodges, 1999), however it does not attach directly to the
lumbar vertebrae and its mechanism for providing stability by increasing intra-abdominal
pressure is different than the other deep core muscles (Hodges, 1999). The deep core
muscles are often targeted by clinicians for treating musculoskeletal injuries primarily
associated with the spine. The MF, QL, and TrA are the deep core muscles currently most
often targeted (Martuscello et al., 2013), as research has associated dysfunction of these
muscles with LBP (Freeman et al., 2010; Hides et al., 2008 ; Hodges, 1999). Dysfunction
of the PS, especially during running, may affect back pain as it not only attaches to the
spine but is also a primary hip flexor (Barker et al., 2004).

Most of the core strength and stability training exercises commonly performed by
athletes emphasize the superficial rather than the deep musculature (Faries and
Greenwood, 2007). Neglect or improper training of the deep core muscles will likely
result in under-utilized and weak deep core muscles. Runners competing at elite levels,
who have extensive training resources available, have been observed to have
underdeveloped core musculature (Fredericson and Moore, 2005). Dysfunction of the
deep core musculature during a repetitive, dynamic activity like running may lead to
improper loading placed on the spine, poor muscular coordination, compensatory
movement patterns, muscle strain, or injury to spinal structures (Fredericson and Moore,
2005 ; Hibbs et al., 2008). While there are many current opinion and review articles
addressing the importance of core strength and stability in athletic function (Fredericson
and Moore, 2005; Hibbs et al., 2008; Kibler et al., 2006; McGill, 2010; Willardson, 2007 ;
Willson et al., 2005), very few high quality research studies exist that directly investigate
this relationship in regards to running performance and injuries.

The deep core muscles directly influence spinal loading during dynamic tasks. Both
elevated compressive and shear forces exerted on the spine have been associated with
low back injuries like LBP (Marras et al., 2001). Compressive forces have higher
magnitudes when compared to shear magnitudes, however spinal structures are much
stronger in the axial direction than when loaded in shear (Gallagher and Marras, 2012).
Therefore both increased compressive and shear loads may be detrimental to spinal
structures, especially when this loading is repeated over thousands of gait cycles.

The purposes of this study were to identify potential strategies that could be used to
compensate for weakness of the deep core musculature during running and to identify
accompanying changes in spinal loading using simulations. We hypothesized that the
superficial core musculature and other unaffected deep core muscles could compensate
for muscle weakness by increasing their force production during running. Additionally, we
hypothesized that the muscular compensations associated with deep core muscle
weakness would result in increased loading on the lumbar spine.
2. Methods
2.1. Participants
Eight healthy participants (6F/2M, 1.71​±​0.07​m, 66.00​±​14.68​kg, 22.37​±​3.93​y) provided
IRB-approved informed consent. Participants were recruited from surrounding
communities and were included if they had no history of musculoskeletal injury for at
least 3​months and were between the ages of 18 and 55. Exclusion criteria included a
history of recurrent back pain, previous abdominal or lower extremity surgery, and a BMI
greater than 30. Participants had minimal to no athletic experience, participating in
athletic activities 2.4​±​2.1 times per week.

2.2. Jogging
Participants jogged overground at a self-selected comfortable pace (2.80​±​0.21​m/s)
continuously around a 27​m loop in the laboratory through a motion capture volume with
force plates embedded into the floor. One good trial, where all reflective markers were
present and each force plate was contacted by at most one foot at a time, was used as
input into OpenSim to create a subject-specific simulation.

2.3. Kinematic and kinetic data collection

Marker data were collected at 300​Hz using 10 Vicon MX-F40 cameras (Vicon Motion
Systems; Oxford, UK) and ground reaction force data were sampled at 1500​Hz from six
Bertec 4060-10 force plates (Bertec Corp; Columbus, OH). Marker data were filtered with
a fourth order low-pass Butterworth filter at a cutoff frequency of 15​Hz. Retro-reflective
markers were placed on the upper and lower body using a modified point cluster
technique (Jamison et al., 2013). The kinematic and kinetic data from the motion capture
system were used as input to the musculoskeletal modeling software OpenSim (Delp et
al., 2007).

2.4. Simulation procedures

Multiple subject-specific simulations were generated for each participant. The full-body
lumbar spine (FBLS) model (Fig. 1) we previously developed consisting of 21 segments,
30 degrees-of-freedom, and 324 musculotendon actuators was used to create each
simulation (Raabe and Chaudhari, 2016). This model is the first OpenSim full-body
model to include the major muscle groups of the lower extremities in addition to the eight
major muscle groups of the lumbar spine (RA, EO, IO, LD, QL, MF, PS and the ES which
is comprised of the superficial and deep longissimus thoracis (LT) and iliocostalis
lumborum (IL)). The lumbar spine muscle groups are modeled as multiple fascicles to
account for their large surface area and multiple lines of action. The spine consists of the
sacrum, five individual lumbar vertebrae, and lumped thoracic and cervical vertebrae.
The lumbar vertebrae are connected by a 6 degree-of-freedom joints and coupling
constraints are imposed to describe the net lumbar movement as three rotational
degrees-of-freedom: flexion-extension, lateral bending, and axial rotation (Christophy et
al., 2012). The FBLS model is freely available on the SimTK website (https://simtk.org/ho
me/fullbodylumbar). This model does not include the TrA due to modeling limitations.
 Fig. 1.
Full-body lumbar spine model with modified point cluster technique marker set (Jamison et al., 2013).

Figure options

First, the generic musculoskeletal model was scaled to anthropometrically match the
individual participant for whom data had been collected (Delp et al., 2007). Next, motion
and mass properties of the model were optimized using inverse kinematics and residual
reduction algorithms to achieve a dynamically consistent set of kinematics and kinetics
that best matched the experimentally collected data (Delp et al., 2007). Next, static
optimization (SO) was performed to resolve the net joint moments into individual muscle
forces at each instant in time (Steele et al., 2012). Non-physical forces and moments
added to the model to resolve dynamic inconsistencies (residuals) or assist muscles that
are too weak to produce the necessary joint moment (reserves) were compared to the
established thresholds (Supplemental Fig. 1) to ensure all simulations were successful
(Hicks, 2011 ; Lund and Dembia, 2013). Lastly, the JointReaction analysis tool was used
to calculate the internal vertebral joint loads (Steele et al., 2012).

For each participant, a baseline simulation of the stance phase of one running gait cycle
was created. Additional simulations were then created for each participant at
progressively higher levels of deep core muscle weakness. The QL, MF, PS, and deep
ES (deep IL and LT) were progressively weakened individually and together from 20% to
100% weakness in 20% increments. Compensating muscle forces for individual muscle
weakness were reported at the point of peak baseline force production of the weakened
muscle, where the largest compensations were likely required. For simultaneous deep
core muscle weakness, peak muscle force was reported for compensating muscles. It is
important to note that all simulations were kinematically-driven. Additionally, since all
participants were healthy with no history of LBP, the assumption was made that baseline
spinal loads and muscle forces were at a healthy, desirable level, and therefore changes
away from this level would be undesirable. Simulated lumbar spine kinematics were
comparable to those measured experimentally (MacWilliams et al., 2014 ; Schache et
al., 2002). For all participants, all deep core muscles, both individually and together,
could successfully be weakened 100% while maintaining baseline running kinematics.

2.5. Statistics
Two-sided paired t-tests were used to determine significant differences in muscle forces
and spinal loading between a given condition of muscle weakness and the baseline
condition. A significance level of α​=​0.05 was used and corrections for multiple
comparisons were not made due to the exploratory nature of the study.

3. Results
3.1. Muscle compensations
 Only the superficial and deep trunk muscles were investigated as potential
compensators for deep core muscle weakness. As muscles were progressively
weakened, the level of required compensations increased. Table 1 shows all significant
muscle compensations required to maintain original running kinematics for individual and
all deep core muscle weakness. The MF and deep ES required the largest number of
muscles to compensate when each of these muscles was weakened individually, while
the PS required the least. In general, the superficial trunk muscles provided the majority
of the compensations for muscle weakness with some contribution from other deep core
muscles that were not weakened in the given condition. The superficial LT was the most
frequent compensator, significantly compensating for every condition of muscle
weakness except for the PS. Fig. 2 shows the significant muscle compensations when
the specified muscle was weakened 100%, normalized to the given muscle’s average
baseline force production. The largest compensations in terms of increased normalized
muscle force magnitude were required when the deep ES and all deep core muscles
were weakened, followed by the MF, PS, and QL, respectively.

Table 1.
Significant compensations for all conditions of muscle weakness. The number reported is the mean
difference in muscle force (N) between the baseline and 100% weakened conditions for all subjects.

Compensating Muscles (Mean difference in muscle force (N) ± SD (pval))

Weakened Superficial Superficial Deep LT Deep MF QL LD PS

Muscle(s) LT IL IL
QL 0.5​±​0.4 3.8​±​4.3 0.6​±​0.5
(0.009) (0.041) (0.01)
MF 14.1​±​8.5 10.0​±​11.5 5.3​±​4.4 0.5​±​0.4 0.9​±​1.0
(0.002) (0.043) (0.011) (0.022) (0.046)
PS 5.0​±​5.9
(0.047)
Deep ES 84.2​±​30.7 54.1​±​25.1 13.2​±​8.8 2.7​±​1.5 7.9​±​4.2
(deep IL, (0.0001) (0.0005) (0.004) (0.002) (0.001)
LT)
All deep 127.0​±​63.3 43.9​±​19.4 16.0​±​16.2
core (0.0008) (0.0004) (0.027)

Abbreviations: quadratus lumborum (QL), multifidus (MF), psoas (PS), erector spinae (ES), superficial and
deep longissimus thoracis (LT), superficial and deep iliocostalis lumborum (IL), latissimus dorsi (LD).

Full-size table

Table options

Note to users:
Corrected proofs are Articles in Press that contain the authors' corrections. Final citation
details, e.g., volume and/or issue number, publication year and page numbers, still need
to be added and the text might change before final publication.

Although corrected proofs do not have all bibliographic details available yet, they can
already be cited using the year of online publication and the DOI , as follows: author(s),
article title, Publication (year), DOI. Please consult the journal's reference style for the
exact appearance of these elements, abbreviation of journal names and use of
punctuation.

When the final article is assigned to volumes/issues of the Publication, the Article in
Press version will be removed and the final version will appear in the associated
published volumes/issues of the Publication. The date the article was first made available
online will be carried over.

About ScienceDirect Remote access Shopping cart Contact and support Terms and conditions Privacy policy

Cookies are used by this site. For more information, visit the cookies page.
Copyright © 2017 Elsevier B.V. or its licensors or contributors. ScienceDirect ® is a registered trademark of Elsevier B.V.