Ultrasonography of the Deep Abdominal 2013-Becirovic

Isokinetics and Exercise Science 21 (2013) 187–193 187DOI 10.3233/IES-130512IOS Press

Ultrasonography of the deep abdominalmuscles at rest and during the drawing-inmaneuver: A comparative study of Japaneseadolescent vs. adult soccer players1

Hiroyuki Watanabea,∗, Hiroshi Abeb, Michio Tojimac, Masumi Yoshimotod, Naonobu Takahiraa andSuguru ToriieaDepartment of Rehabilitation, School of Allied Health Sciences, Kitasato University, Kanagawa, JapanbDepartment of Rehabilitation, University Kitasato Institute Hospital, Kitasato, Tokyo, JapancDepartment of Rehabilitation Medicine, Graduate School of Medicine, The University of Tokyo, Tokyo, JapandDepartment of Rehabilitation, Nippon Koukan Hospital, Kanagawa, JapaneFaculty of Sports Sciences, Waseda University, Saitama, Japan

Received 1 August 2012

Accepted 14 May 2013

Abstract.OBJECTIVE: The purpose of this study was to clarify the characteristics of abdominal deep muscles in adolescent soccerplayers.METHODS: Participants were 53 soccer players from junior high school and 14 adult soccer players. The deep abdominalmuscles of both sides were imaged by ultrasonography. Abdominal muscles on the dominant leg side were selected as the targetsof measurements, and measurements of the transversus abdominis (TrA) and internal oblique (IO) muscle were conducted. Themuscle thickness of these muscles was measured at rest and during contraction (while drawing-in of the abdominal wall) andserved as the basis for comparing the adolescent and adult players.RESULTS: While no significant inter-group differences were noted in the thickness of the TrA or IO muscle at rest, a significantdifference was observed during the drawing-in maneuver.CONCLUSION: The deep abdominal muscles of adolescent soccer players have not likely reached full maturity.

Keywords: Ultrasound image, transverses abdominis muscle, internal oblique muscle, adolescent soccer player

1. Introduction

Soccer is the most commonly played sport in Japanand enjoys widespread popularity among young peo-

∗Corresponding author: Hiroyuki Watanabe, 1-15-1 Kitasato,Minami-ku, Sagamihara, Japan. Tel.: +81 42 778 9968; Fax: +81 42778 9968; E-mail: [email protected].

1The ethics committee of Kitasato University approved the studyprotocol of this study.

ple [16]. In particular, soccer appears to be the pre-ferred sports activity, among many kinds of sports,for the younger generation, from childhood to adoles-cence. Injuries among young soccer players are com-mon [9,14]. A previous study demonstrated that mostof these injuries involve the joints of the lower extrem-ities, such as the knee (26%) and ankle (23%). Lowback pain (LBP) is the third most common type of in-jury according to this report, occurring in about 14%of young soccer athletes [29]. It is highly probable that

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188 H. Watanabe et al. / Ultrasonography of the deep abdominal muscles in adolescent soccer players

Table 1Participant characteristics in adolescent soccer players and adult soc-cer players

Adolescent players Adult players(n = 53) (n = 14)

Age (yrs) 13.6 ± 0.5 22.4 ± 2.4Height (cm) 162.9 ± 6.9 170.0 ± 5.3Body weight (kg) 50.7 ± 7.7 64.6 ± 8.3Body mass index (kg/m2) 19.0 ± 2.0 22.3 ± 2.0

Values are expressed as mean ± SD.

the onset of LBP in adolescents engaging in sports iscaused by spondylolysis [4,20,26]. Numerous studieshave demonstrated a higher prevalence of spondylol-ysis in adolescent soccer players [8,28]. The spondy-lolysis in the young athletes often subsequently devel-ops into spondylolisthesis [4]. However, few studieshave been conducted on the treatment and preventionof spondylolysis in persons engaging in sports activi-ties [21,33].

Deep abdominal muscles are divided into the super-ficial layer and deep layer. The external oblique muscleand internal oblique muscle (OI) belong to the super-ficial layer, and the transversus abdominis (TrA) andlumbar multifidus belong to the deep layer. Generally,the superficial layer muscles are called global mus-cles and the deep layer muscles are called local mus-cles. Improvement in the functions of the local mus-cles, such as the TrA, has been shown to be one ofthe effective methods for the prevention and control ofLBP [21]. The lumbar spine corset, which is relatedto the stability of the lumbar-pelvic region, is aided byTrA contraction [10,12,25]. Methods to train the TrAto contract for the control of LBP or stabilization of thetrunk have been reported [1,37,38,40]. However, it isdifficult to evaluate the contractility of the TrA and IOas these muscles attach to the thoracolumbar fascia attheir origin. Therefore, the isolated force of contractionof the TrA and IO muscles cannot be measured usinga dynamometer. Recently, assessment of the deep ab-dominal musculature by ultrasound imaging has beenapplied clinically and for research [41]. Ultrasoundimaging is also one of the noninvasive methods that hasbeen used to evaluate the characteristics of contractionof the TrA and IO muscles. The reproducibility and va-lidity of measurement of TrA thickness by ultrasonog-raphy has been established [3,17,18]. Furthermore, acomparison of ultrasound imaging and fine-wire elec-tromyography has shown clear changes with increas-ing muscle activation and muscle thickness even at ef-fort levels of less than 20% of the maximal voluntarycontraction for the TrA and IO [2,13,19]. Therefore,

Fig. 1. The ultrasonographic probe was arranged at right angles to thecenter between the bottom edge of a 11th rib on the anterior axillaryline and the iliac crest. A: anterior axillary line; B, ultrasonographicprobe arrangement.

the level of contractility used in this study is presentedin terms of muscular dimension (thickness in mm).

The development and increased contractility of thelocal muscles have been found to be related to im-provement of spinal instability and control of LBP [21,22]. In general, it is thought that the ability of the TrAto contract is important for decreasing the likelihoodof onset of LBP during sports activities. Clinically, theefficiency of TrA contraction is evaluated by conduct-ing measurements during the drawing-in maneuver ofthe abdominal wall [40], a preferential contraction ofmode of the TrA among the abdominal deep muscles.It is presumed that immaturity of the TrA functioningis one of the factors leading to spondylolysis and insta-bility of the trunk in adolescent soccer players.

The purpose of this study was to clarify the dimen-sional characteristics of the deep abdominal musclesin adolescent soccer players in comparison with adultplayers.

2. Materials and methods

2.1. Participants

Participants were 53 soccer players from the 2nd and3rd grades of junior high school and 14 adult soccerplayers. The mean (± SD) age, height and weight ofthe junior soccer players were 13.6 ± 0.5 years, 162.9± 7.1 cm and 51.4 ± 10.1 Kg, while those of the adultsoccer players were 22.4 ± 2.4 years, 170.0 ± 5.3 cm

H. Watanabe et al. / Ultrasonography of the deep abdominal muscles in adolescent soccer players 189

Fig. 2. Ultrasound images of transversus abdominis (TrA), internal oblique (IO) and external oblique (EO) muscles at rest (left image). Musclethickness was measured as the maximum distance between the lower and upper fascia, except for the thickness of upper and lower fascia (rightimage); dashed double arrow, muscle thickness of IO; double arrow, muscle thickness of TrA.

Fig. 3. Ultrasound images of transversus abdominis (TrA), internal oblique (IO) and external oblique muscles (EO) during draw-in maneuver(left image). Muscle thickness was measured as the maximum distance between the lower and upper fascia, except for the thickness of upper andlower fascia (right image); dashed double arrow, muscle thickness of IO; double arrow, muscle thickness of TrA.

and 54.2 ± 11.1 Kg, respectively (Table 1). Exclusioncriteria included a current complaint of LBP, previouslumbar surgery and any injury affecting posture. Theexperimental protocol was approved by the ethics com-mittee of Kitasato University.

2.2. Procedure

The deep abdominal muscles on both sides wereimaged by brightness-mode (b-mode) ultrasonogra-phy (SSD-4000, ALOCA Co Ltd, Tokyo). Participantswere positioned in the supine posture with the kneesand hip joints bent at 45 degree on the bed [31]. Theultrasonographic probe was arranged at right angles tothe center between the bottom edge of a 11th rib on theanterior axillary line and the iliac crest [11] (Fig. 1).

Abdominal muscles on the dominant leg side were se-lected as the targets for measurement, and measure-ment of the TrA and IO muscles was conducted. Mus-cles thickness was measured during rest and contrac-tion (drawing-in of the abdominal wall). Ultrasoundimaging during the drawing-in maneuver of the ab-dominal wall was performed after sufficient practicewith ultrasonography had been obtained. The cross-sectional area of the abdomen during the drawing-inmaneuver of the abdominal wall after expiration wasmeasured on the images. Measurements on the ultra-sound images of the deep abdominal muscles wereconducted in Scion Image software (Alpha 4.0.3.2,Maryland) on a personal computer. Muscle thicknesswas measured as the distance between the lower andupper fascia, excluding the thickness of the upper andlower fascia (Figs 2 and 3).


Table 2Comparison of deep abdominal muscles thickness at rest and during the draw-in maneuver between adolescent soccer players and adult soccerplayers

Adolescent players (n = 53)* Adult players (n = 14)* F -value p-valueRestTrA muscle thickness (mm) 3.4 ± 0.8 3.5 ± 0.9 3.9 0.98IO muscle thickness (mm) 8.5 ± 2.1 10.1 ± 2.5 6.0 0.18

Draw-in maneuverTrA muscle thickness (mm) 4.5 ± 1.3 6.1 ± 1.7 13.6 < 0.01IO muscle thickness (mm) 8.9 ± 2.2 12.7 ± 3.4 28.3 < 0.01

Abbreviation: TrA; transversus abdominis, IO; internal oblique; *Value are mean ± SD mm.

Table 3Comparison of the ratio and the percent change of the deep abdominal muscles thickness during the draw-in maneuver between adolescent soccerplayers and adult soccer players

Adolescent players (n = 53)* Adult players (n = 14)* F -value p-valueRestTrA/IO ratio† 0.29 ± 0.04 0.26 ± 0.04 3.4 0.29

Draw-in maneuverTrA/IO ratio† 0.34 ± 0.06 0.32 ± 0.05 1.5 0.48Percent change in TrA(%)†† 30.1 ± 38.7 77.3 ± 51.1 1.5 < 0.01Percent change in IO(%)†† 4.3 ± 26.0 26.3 ± 16.1 9.5 < 0.05

Abbreviation: TrA; transversus abdominis, IO; internal oblique; *Value are mean ± SD mm; †Ratio of TrA muscle thickness to IO musclethickness. ††Percent change in muscle thickness from rest to during draw-in maneuver.

Data on the changes in the muscle thickness of thedeep abdominal muscles on the dominant leg side werecollected. The percent change in the muscle thicknessand the ratio of the TrA thickness to IO muscle thick-ness (TrA/IO ratio) during the drawing-in maneuverwere calculated. In addition The TrA/IO ratio, at restand during the drawing-in maneuver was calculated.The percent change TrA (IO) was calculated as (TrAcontraction – TrA rest)/TrA rest × 100. The sonog-raphy parameters between the two groups were com-pared using analysis of covariance with adjustment forheight and weight (SPSS Ver 12, Tokyo).

2.3. Results

The mean ± SD values of the muscle thicknesses atrest and during the drawing-in maneuver of the abdom-inal wall are shown in Table 2. The ratio and percentchange of deep abdominal thickness are shown in Ta-ble 3. At rest, there were no significant differences inthe thickness of the IO or TrA between the adolescentand adult players. However, significant differences be-tween the two groups were noted during the drawing-in maneuver. No significant differences were noted inthe TrA/IO ratio at rest or during the drawing-in ma-neuver between the two groups. There were howeversignificant differences between the two groups in thepercent change of IO and TrA muscle thickness. Thepercent change in the TrA of adult soccer players was

approximately 6.1-fold that of adolescent soccer play-ers. Because muscle thickness was increased not onlyin TrA, but also in IO during the drawing-in maneu-ver, no change in the TrA/IO ratio was noted in eithergroup, despite the percent change of individual mus-cles differences between the groups.

2.4. Discussion

Adolescence, during which changes in body height,body weight and body constitution occur, is a periodof important consequence for the rest of one’s life. De-velopment starts from the distal upper and lower ex-tremities, ending in the proximal regions [23]. Whiledevelopment of the wrists and feet are completed ear-lier during the development period, that of the spineis completed towards the end of the development pe-riod [35]. Therefore, discordance of development be-tween the distal and proximal regions is noted dur-ing adolescence. The immature body structure is influ-enced by increased physical activity, such as when per-sons engage in sports activities, during adolescence. Inparticular, the functioning of the trunk is not commen-surate with the increased physical activity.

TrA is attached to the thoracolumbar fascia and thelumbar vertebrae and is capable of directly control-ling the lumbar segments. Although the role of TrA ismaintaining dynamic stability of the spine, the TrA-generated joint moment cannot be measured. Hodges


demonstrated the relationship between muscle thick-ness and muscle activity in deep abdominal muscles byelectromyography [13]. Therefore, in this study assess-ment of muscle contractility in deep abdominal mus-cles was based on muscle thickness. The TrA musclethickness was approximately 4 mm less than that ofthe IO muscle in both groups, and the thickness of thismuscle during the abdominal drawing-in maneuver in-creases by 2- to 3-fold compared with that at rest. Al-though there was no significant difference between theadolescent and adult soccer players in TrA thickness atrest, adult soccer players showed significantly higherthickness values of this muscle during contraction. Fur-thermore, adult soccer players showed not only an in-crease of TrA thickness, but also an increase of the IOduring the drawing-in maneuver. This can therefore in-dicate that adult soccer players have higher contractil-ity of the TrA than their adolescent counterparts.

The drawing-in maneuver is associated with pref-erential contraction of the TrA and is used for evalu-ation of deep abdominal muscle contraction and as afacilitation exercise for maintaining trunk stability [6,24,39]. The abdominal drawing-in maneuver has re-cently been reported as allowing the clearest evaluationof the ability for contraction of the TrA [32]. However,participants in studies may initially have difficulty inunderstanding how to perform the maneuver for suchevaluations. It is thought that practicing the abdom-inal drawing-in maneuver is needed before the TrAmuscle contraction can be reliably evaluated. Sincethe drawing-in maneuver is also associated with slightcontraction of the IO, the ratio of the TrA thickness toIO thickness is usually calculated in such evaluations.Significantly higher TrA muscle thickness and IO mus-cle thickness were noted in adult soccer players thanin the adolescent soccer players. Consequently, no sig-nificant difference in the TrA/IO ratio was observed inthe adult players between rest and the drawing-in ma-neuver of the abdomen. Abdominal deep muscle con-traction in the adult players during the drawing-in ma-neuver was characterized by strong contractions of theTrA as well as IO. On the other hand, adolescent soc-cer players showed immature contraction of the trunkmuscles, not only of the TrA, but also of the IO. Thusadolescent soccer players may not be able to contractthe TrA significantly more than the IO during drawing-in maneuver.

Spondylolysis is known as one of the commonlyoccurring sports injuries during adolescence [5,7,15,28]. It is thought that spondylolysis is caused by ro-tation or extension of the trunk while being engaged

in sports activity [26,27,34]. Spondylolysis in soccerplayers has an incidence of approximately 20%, whileplayers without symptoms may belong to the sameteam [30]. We think that the likelihood of LBP onset isassociated with individual differences in developmentduring adolescence. Adolescents are known to showa growth velocity increase during the second growthspurt [36]. The process of body development in theadolescence starts at the distal extremities, and endsat the spine [23,35]. Therefore, instability of the trunkmay be caused by overloading of the spinal or vertebralmuscles that is associated with excessive rotation andextension of the spine. We think that the onset of LBPin the adolescent player might be related to immaturetrunk muscular stability in sports activities during ado-lescence. In general, both coaches and parents are un-aware of the immaturity of trunk stability in sports ac-tivities in adolescents or of methods for improving thetrunk stability. Adolescent soccer players cannot per-form appropriately due to immaturity. We believe thatthey should train specifically for trunk stability. Sinceultrasound imaging of the muscles is not widely avail-able, the magnitude of contraction of the TrA is dif-ficult to evaluate in athletes. For effective training ofthe TrA in these players, a more available evaluationmethod for the TrA needs to be established.

2.5. Conclusion

In the present study, the morphological features andthickness of the deep abdominal muscles were mea-sured. There was no difference in the thickness of theabdominal deep muscles between the adolescent andadult soccer players at rest; however, significant differ-ences were observed during the drawing-in maneuver.These findings suggest a developmental delay in thesemuscles in adolescent players, indicating the need totrain their deep abdominal muscles to prevent the onsetof LBP or other disorders related to trunk stability.

Acknowledgements

The authors thank the players in the junior highschool soccer team and the adult soccer players whovolunteered in this study.


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Ultrasonography of the Deep Abdominal 2013-Becirovic