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Arterial Compression during Overhead Throwing: A Risk for Arterial Injury?
Ultrasound in Med. & Biol., Vol. 36, No. 8, pp. 1259–1266, 2010 Copyright Ó 2010 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
doi:10.1016/j.ultrasmedbio.2010.05.002
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Original Contribution ARTERIAL COMPRESSION DURING OVERHEAD THROWING: A RISK FOR ARTERIAL INJURY? CLAIRE H. STAPLETON,* JADE ELIAS,y DANNY J. GREEN,*z N. TIM CABLE,* and KEITH P. GEORGE* * Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, United Kingdom; y English Institute of Sport, Sportcity, Rowsley Street, Manchester, United Kingdom; and z School of Sport Science, Exercise and Health, The University of Western Australia, Perth, Australia (Received 22 January 2010; revised 17 March 2010; in final form 3 May 2010)
Abstract—Case studies reporting aneurysm formation in the axillary artery have been described in overhead throwing athletes, possibly due to repetitive arterial compression by the humeral head that has been transiently observed during sonographic diagnostic arm manoeuvres. Whether compression negatively alters arterial health has not been investigated and was the focus of this study. The throwing arm of elite overhead athletes was screened for inducible axillary artery compression. Compressors (COMP, n 5 11, mean age: 20 (SD: 2) year, 7 male, 4 female) were age and sex matched with noncompressing (NONCOMP) athlete controls. Four indices of arterial health (flow mediated dilation [FMD], conduit artery vasodilatory capacity [CADC], glyceryl-trinitrate [GTN]induced vasodilation and intima-media thickness [IMT]) were assessed with high-resolution ultrasound at the brachial and the axillary, artery. No significant between-group differences were observed at the brachial, or axillary, artery for FMD (brachial: COMP: mean (SD) 6.2 (3.1)%, NONCOMP: 6.1 (3.5)%, p 5 0.967, axillary: COMP: 8.0 (5.5)%, NONCOMP: 9.0 (3.6)%, p 5 0.602), CADC (brachial: COMP: 10.4 (3.4)%, NONCOMP: 10.4 (5.4)%, p 5 0.999, axillary: COMP: 9.6 (4.2)%, NONCOMP: 8.5 (3.2)%, p 5 0.492), GTN-induced vasodilation (brachial: COMP: 17.9 (5.1)%, NONCOMP:14.1 (7.2)%, p 5 0.173, axillary: COMP: 9.5 (4.3)%, NONCOMP: 7.7 (3.1)%, p 5 0.302) or IMT (brachial: p 5 0.084, axillary: p 5 0.581). These results suggest that transient arterial compression, observed during diagnostic arm manoeuvres in overhead throwing athletes, is not associated with abnormal indices of artery function or structure and that other mechanisms must be responsible for the published cases of aneurysm formation in elite athletes performing overhead throwing actions. (E-mail: [email protected]) Ó 2010 World Federation for Ultrasound in Medicine & Biology. Key Words: Vascular compression, Endothelial function, Elite athletes, Overhead throwing, Flow mediated dilation, Intima media thickness.
unclear but excessive translation of the humeral head at the glenohumeral joint and/or a hypertrophied or tight pectoralis minor muscle, combined with repetitive overhead arm motion, have been implicated as the cause of transient compression at the third and second portions of the axillary artery, respectively (Dijkstra and Westra 1978; Stapleton et al. 2008). Repetitive compression is thought to result in damage to the arterial wall, including the endothelial layer with subsequent thrombus and/or aneurysm formation (Schneider et al. 1999; Stapleton et al. 2009). However, the proposed link between repetitive arterial compression with overhead arm motion and arterial health in elite overhead throwing athletes remains speculative. Our group recently studied the arterial health of eight nonathletic individuals who did not participate in activities requiring repetitive overhead activity but who did demonstrated such compression and compared them
INTRODUCTION AND LITERATURE Case reports in overhead throwing athletes have documented a continuum of findings from intermittent compression of the axillary artery and its branches, with the arm in an overhead position, to thrombosis, aneurysm formation and peripheral embolisation (Dijkstra and Westra 1978; Kee et al. 1995; Schneider et al. 1999). No epidemiologic data exists for the occurrence of thrombus or aneurysms in overhead throwing athletes, however, Rohrer et al. (1990) reported clinically significant inducible compression (.50% reduction in diameter) in 8% of baseball players. The cause of compression is
Address correspondence to: Claire Stapleton, Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Tom Reilly Building, Byrom Street Campus, Liverpool, Merseyside, L3 3AF. E-mail: [email protected] 1259
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with age and sex matched noncompressor controls. Mean flow-mediated dilation (FMD), an index of conduit artery endothelial function (Kooijman et al. 2008; Mullen et al. 2001), assessed downstream to the site of compression revealed a significantly (p 5 0.006) lower response in the ‘compressor’ group (mean (SD): 6.38 (3.28) vs. 10.38 (2.74)%) (Stapleton et al. 2009). These results suggest that the finding of clinically significant inducible axillary artery compression maybe of pathologic significance, potentially inducing endothelial dysfunction, an early sign of compromised vascular health and a potential precursor for the more serious arterial injuries described in published case reports (Dijkstra and Westra 1978; Kee et al. 1995; Schneider et al. 1999). Therefore, the aim of this investigation is to investigate if performance of repeated, transient arterial compression in an athletic population results in similar changes in arterial function and structure? MATERIALS AND METHODS Subjects The Great Britain (GB) men’s and women’s waterpolo squads were recruited. Inclusion criteria included participation in the squad’s full training programme for at least 2 months prior to testing. However, all subjects had been competing in waterpolo for at least 5 years. All male and female squad members undertook the same training routine with two pool sessions a day, 5 days a week and an additional strength and conditioning session, 2 days of the week. Subjects provided written informed consent prior to completing a health screening questionnaire to exclude those with factors known to influence the indices of vascular health, flow mediated dilation (FMD) and conduit artery vasodilatory capacity (CADC) response, e.g. diabetes, asthma, amenorrhea, recent allergic reactions, infections or injuries. Subjects underwent subjective and objective musculoskeletal screening to exclude any past or present musculoskeletal injury that may predispose them to neurovascular compression. The presence or absence of the Arch of Langer (an anomalous musculotendinous slip) was assessed by visual inspection and palpation. Ethical approval was granted from Liverpool John Moores University ethics committee. All subjects (n 5 37, mean age (SD): 20 (3) years, sex: 24 males, 13 females) were screened for clinically significant inducible axillary artery compression. A priori sample size estimation (n 5 8 per group) was based on detecting a clinically significant difference in FMD at the brachial artery of 2.5%, with an alpha level of 0.05 and a power of 80% (Woodman et al. 2001). Measurement of FMD at the brachial artery was used for sample size estimation as it has been used extensively in cardiovas-
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cular research and has been validated as an indicator of arterial health (Celermajer et al. 1992; Hashimoto et al. 2003; Tsuchiya et al. 2007). Data collection – Phase 1: Screening for clinically significant inducible axillary artery compression Following 10 min rest in the supine position to stabilise heart rate and blood flow, the subjects’ dominant (throwing) arm was passively supported in the baseline position (60 abduction) or the stress position (120 abduction, 30 horizontal extension and 90 external rotation) (Fig. 1). The axillary artery was located and imaged at the axilla and, therefore, it was necessary to incorporate some abduction into the baseline position to (1) accommodate the ultrasound transducer and (2) to optimise image clarity. To aid standardisation of the stress position, the posterior corner of the acromion was positioned over a marker on the treatment table and the arm supported in a custom made arm rest. A high-resolution ultrasound machine (Terason t3000; Teratech, MA, USA) with an 8-10 MHz linear array transducer was used to record arterial diameter and peak systolic flow velocity (PSV) for 1 min in each position. Post-test analysis was performed with wall tracking and edge detection computer software (LabVIEW 7.0; Version 3, National Instruments, Austin, TX). The software (Woodman et al. 2001) produces a mean diameter and a mean PSV from the pre-recorded 60 s of data. A doubling of PSV with the arm in the stress position compared with the baseline position is indicative of a 75% reduction in the cross-sectional area, which is classified as clinically significant arterial compression (Fig. 2a and b; Strandness 2002). Subjects demonstrating this degree of compression formed the compressor (COMP) group whereas the noncompressor (NONCOMP) group comprised of subjects demonstrating less than a 20% rise in PSV with the arm in the stress position
Fig. 1. The subject is pictured in the supine position with the dominant arm passively supported, with a purpose built arm rest, in the stress position (120 abduction, 30 horizontal extension and 90 external rotation).
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Fig. 2. Duplex ultrasound images of the axillary artery in (a) the baseline position and (b) the stress position. Note the change in peak systolic velocity indicative of clinically significant arterial compression.
compared with baseline. The stress position is similar, but less extreme, to the arm position achieved during the cocking phase of the throwing motion, it was therefore assumed that athletes classified as compressors would repeatedly compress the axillary artery when performing throwing motions in waterpolo training and competition. The subjects’ opposite limb also underwent screening, however, it was not used as the control arm as, concordant with our previous research, some subjects demonstrated bilateral compression or bilateral noncompression. Furthermore, due to the imbalance in frequency of performing overhead motions between the dominant and nondominant limb it was preferable to compare a dominant ‘‘compressor’’ limb with a dominant ‘‘noncompressor’’
limb. Consequently, control subjects were training, age and sex matched. Data collection – Phase 2 Subjects allocated to a group underwent phase two of data collection. Four indices of arterial health, flow mediated dilation (FMD; an index of endothelial function), conduit artery dilator capacity (CADC; an index of arterial structure), glyceryl tri-nitrate (GTN) induced vasodilation (an index of vascular smooth muscle function) and intima media thickness (IMT; an index of arterial wall structure) were assessed at the third portion of the axillary artery and at the brachial artery. Theoretically, arterial compression at the axillary artery is likely to alter blood flow patterns
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and shear stress locally but also immediately downstream to the compression potentially causing a disturbance to the equilibrium of the endothelium at both brachial and axillary artery sites. All ultrasound scans were performed by one trained sonographer who was blinded to group allocation. FMD, CADC and GTN-induced vasodilation Prior to testing, subjects were required to fast and abstain from caffeine, alcohol and exercise for 4 h (Corretti et al. 2002). Female subjects were tested within the early follicular phase of the menstrual cycle (Williams et al. 2001). Following 10 min rest in the supine position, arterial diameter and blood flow velocity were recorded via the previously described high-resolution ultrasound machine with parameters set to optimize B-mode longitudinal images of the target artery. FMD, CADC and GTN-induced vasodilation were assessed at both arterial sites with the dominant arm supported at 60 abduction. The brachial artery was imaged at the middle third of the humerus and the third portion of the axillary artery in the axilla just distal to the subscapular artery. The order of testing was randomized (computer generated) and a 10-min rest period in the supine position was enforced between tests to allow the arterial diameter to return to baseline (Corretti et al. 2002). To ensure GTN administration did not influence the basal diameter measures for subsequent assessments, GTN-induced vasodilation was the final test. The second assessment for GTN-induced vasodilation at the second arterial site was performed on a separate occasion (within 24–48 h). This avoided any potential side effects of administering a double-dose of GTN. Assessment of FMD/CADC and GTN-induced vasodilation A sphygmomanometer pressure cuff (Clinicus I; Aneroid, Boso, Germany) was placed 3 cm distal to the olecranon process and provided the stimulus for forearm ischemia. Following recording of baseline measurements for 1 min, the cuff was inflated to a supra-systolic pressure (220 mm Hg) for 5 min. Recording of the arterial diameter and blood flow velocity resumed 30 s prior to cuff release and continued for 3 min post cuff release (Black et al. 2008). For the assessment of CADC, handgrip exercises were performed by the subject, during the third and fourth minute of cuff inflation of the above protocol. The speed of gripping was guided by a metronome set at 1 Hz and the power output was monitored with a dynamometer (Grip D; Takei, Tokyo, Japan) and standardised to a predetermined 20% of the subjects’ maximal voluntary contraction. The use of handgrip exercises during a 5-min
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ischaemic period has been reported as sufficient stimulus to induce a peak dilator response (Naylor et al. 2005). GTN-induced vasodilation assesses the responsiveness of the smooth muscle cells to nitric oxide indicated by the magnitude of dilation. The nitrates within GTN bypass the endothelium and act directly on the smooth muscle cells within the tunica media layer of the arterial wall. The target artery was imaged for 1 min prior to sublingual administration of 400 mg of GTN and continued for 6 min postadministration (Celermajer et al. 1992).
Analysis of FMD, CADC and GTN data Post-test analysis was performed with an automated edge detection and wall tracking computer-software program (LabVIEW 7.0; Version 3, National Instruments; Woodman et al. 2001). The operator highlighted a portion of the B-mode image with optimum clarity and enclosed it in a region-of-interest (ROI) window. The software identifies and tracks the walls of the artery within the ROI window and detects changes in arterial diameter over time. The program produced an averaged diameter measure from approximately 300 measurements per frame, with an estimated 20 to 30 frames per s and automatically detected the peak response. FMD, CADC and GTN-induced vasodilation were expressed as the percentage increase in diameter from baseline to peak. The intraobserver coefficient of variation, for FMD with this software, is 6.7% (Woodman et al. 2001). For FMD and CADC responses, the Doppler waveform analysis function allowed simultaneous recording and analysis of the flow and shear rate stimulus, from cuff deflation to peak vasodilation. A ROI window encapsulated the spectral waveform and the blood flow velocity profile was tracked from baseline (pre-cuff inflation) to 3 min post-cuff release. Pyke and Tschakovsky (2005) highlighted the importance of controlling for the flow stimulus. They reported that endothelium dependent vasodilator responses were not only dependent on the health of the vascular endothelium but also on the magnitude of shear stimulus imposed on the endothelium and that individual differences in arterial diameter size can result in different magnitudes of shear rate despite the same volumetric flow. Therefore, for comparison between individuals and groups it is necessary to normalise the FMD and CADC response to the magnitude of the shear stress stimulus. The magnitude of the shear stimulus was quantified by calculation of the area under the curve (AUC) imposed during the period from cuff release to peak dilation (Pyke and Tschakovsky 2007). The FMD and CADC (percentage) response was divided by the AUC for the relevant portion of the shear rate profile to give a normalised FMD and CADC response.
Arterial compression during overhead throwing d C. H. STAPLETON et al.
Assessment and analysis of intima-media thickness (IMT) An 8-10 MHz linear array transducer recorded highresolution B mode images at the two arterial sites for approximately 30 s. Ultrasound parameters were set to optimise image clarity at the far arterial wall only (Poredos 2004). Custom designed computer software for the detection of the distance between the lumen-intima interface and the media-adventitia interface was used to extract the intima-media thickness (IMT version 3.0, National Instruments). This edge detection software and its analysis has been described in detail elsewhere (Potter et al. 2007). In brief, following the selection of frames for analysis and calibration, the operator selected a portion of the artery with optimum clarity within a ROI window. An edge detection algorithm detected the near and far arterial lumen edges and the far wall IMT within the specified ROI. When the lumen edge was detected, the pixels of the intima and media were removed and the automated edge detection process is repeated to find the far wall media-adventitia interface. Near and far wall lumen edges and the far wall mediaadventitia interface were detected on every frame within the selected image recording.
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Table 1. Background characteristics for compressor (COMP) and noncompressor (NONCOMP) groups
Indicator of compression* Age Sex BMI Systolic BP Hand dominance Resting brachial artery diameter (cm) Resting axillary artery diameter (cm)
COMP
NONCOMP
125 (49) % 20 (2) 7_4\ 24.8 (2.0) 124 (12) 11 right, 0 left 0.43 (0.06)
–15 (21) % 20 (2) 7_4\ 24.5 (2.0) 124 (12) 11 right, 0 left 0.42 (0.07)
0.55 (0.08)
0.51 (0.07)
BP 5 blood pressure; BMI 5 body mass index. *Percent change in peak systolic flow velocity from baseline position to stress position.
Statistical analysis All analyses were performed using SPSS (version 15.0, Chicago, IL) computer software program with the alpha level set to p , 0.05. The method of comparison between the COMP and NONCOMP groups for absolute and normalised FMD, CADC and GTN-induced vasodilation at the brachial and axillary artery depended upon the data meeting parametric assumptions. Zar (1999) proposes that where two groups show moderate correlation the paired t-test is more powerful than an independent t-test. Therefore, where paired group data demonstrated adequate correlation (r . 0.4) paired t tests were performed; otherwise independent t tests were adopted. RESULTS Eleven subjects met Strandness’s (2002) criteria for arterial compression and formed the compressor group (COMP: mean age (SD): 20 (2), sex: 7 male, 4 female). These were age, sex and training matched with noncompressor athlete controls (NONCOMP). Table 1 presents the background characteristics. The anatomical anomaly, ‘‘the arch of Langer’’, was not detected in any subjects. Flow mediated dilation No significant differences were revealed at the brachial artery for FMD (COMP: 6.2 (3.1)%, NONCOMP: 6.1 (3.5)%, t10 5 –0.042, p 5 0.967) (Fig. 3a) or normalised FMD (COMP: 0.00026 (0.00016) s21,
Fig. 3. Compressor (COMP) and noncompressor (NONCOMP) groups means and standard deviations for flow-mediated dilation (FMD) (%) for the three vasodilatory test conditions, conduit artery vasodilatory capacity (CADC), FMD and glyceryl trinitrate (GTN) at (a) the brachial artery and (b) the axillary artery.
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NONCOMP: 0.00022 (0.00013) s21, t20 5 –0.590, p 5 0.562). The same was true for FMD (COMP: 8.0 (5.5)%, NONCOMP: 9.0 (3.6)%, t2050.530, p 5 0.602) and normalised FMD (COMP: 0.00046 (0.00030) s21, NONCOMP: 0.00050 (0.00036) s21, t10 5 0.413, p 5 0.688) at the axillary artery (Fig. 3b). Conduit artery dilatory capacity Neither CADC (COMP: 10.4 (3.4)%, NONCOMP: 10.4 (5.4)%, t10 5 0.001, p 5 0.999) (Fig. 3a) or CADC normalised for shear rate (COMP: 0.00020 (0.00013) s21, NONCOMP:0.00014 (0.000087) s21, t20 5 –1.209, p 5 0.241) demonstrated significant between group differences. Similar results were found at the axillary artery for CADC (COMP: 9.6 (4.2)%, NONCOMP: 8.5 (3.2)%, t20 5 –0.701, p 5 0.492) (Fig. 3b) and CADC normalised for shear rate (COMP: 0.008 (0.001) s21, NONCOMP: 0.001 (0.002) s21, t20 5 0.230, p 5 0.821). GTN-induced vasodilation No significant differences were observed for GTNinduced vasodilation at the brachial (COMP: 17.9 (5.1)%, NONCOMP:14.1 (7.2)%, t20 5 –1.413, p 5 0.173) (Fig. 3a) or axillary artery (COMP: 9.5 (4.3)%, NONCOMP: 7.7 (3.1)%, t19 5 –1.061, p 5 0.302) (Fig. 3b). Intima media thickness IMT observed at the brachial artery (COMP: 1.03 (0.18) mm, NONCOMP: 0.86 (0.24) mm, t20 5 1.820, p 5 0.084) and axillary artery (COMP: 0.89 (0.28) mm, NONCOMP: 0.84 (0.14) mm, t19 5 –0.561, p 5 0.581) were no different between groups (Fig. 4).
Fig. 4. Mean intima-media thickness (mm) for compressor (COMP) and noncompressor (NONCOMP) groups s at the brachial and axillary artery. Error bars represent standard deviations.
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DISCUSSION AND SUMMARY The aim of the present study was to determine whether transient compression at the third portion of the axillary artery in elite overhead athletes resulted in diminished indices of arterial function or structure. Elite overhead athletes demonstrating transient compression did not present with any deterioration in FMD, CADC, GTN-induced vasodilation or IMT when compared with age, sex and training matched noncompressor athletes. Overall these athletes have healthy arterial structure and function with FMD responses lying within the normal range (Celermajer et al. 1992) and, indicative of their exercise training, mean resting arterial diameter sizes (brachial: 0.43 cm, axillary: 0.53 cm) greater than their less active counterparts observed in our previous study (brachial: 0.37 cm, axillary: 0.48 cm) (Stapleton et al. 2009). The lack of a significant difference in brachial artery FMD between COMP (6.2 [3.1]%) and NONCOMP (6.1 [3.5]%) groups differ to findings from our previous study (Stapleton et al. 2009) where FMD was significantly reduced (p 5 0.006) in nonathletic healthy subjects demonstrating inducible axillary artery compression with an overhead arm manoeuvre compared with a matched noncompressor group (6.38 [3.28] vs. 10.38 [2.74] %). We concluded from this data that the finding of clinically significant inducible axillary artery compression maybe of pathologic significance and a potential precursor for the more serious arterial injuries described in published case reports (Fields et al. 1986; Ishitobi et al. 2001; Rohrer et al. 1990; Vlychou et al. 2001). One explanation for the absence of deterioration in arterial health in the present study is that any potential deleterious effects of intermittent compression may have been counter-balanced by the beneficial impact of regular physical activity. Unlike the individuals described in the case reports, subjects from our previous study were not highly trained. It is well established that repeated exercise training can be associated with enhanced endothelial function (Green et al. 2004). Acute bouts of exercise are associated with increases in endothelial shear stress, which, through a series of complex interactions, mediates an increase in the release of nitric oxide [NO] and consequent vasodilation (Deanfield et al. 2007; Green et al. 2004; Maiorana et al. 2003). Recurrent bouts of exercise result in up-regulation of NO bioactivity and increased capacity for vasodilation (Deanfield et al. 2007; Maiorana et al. 2003; Walther et al. 2004). Improved FMD responses following exercise training have been observed in healthy individuals as well as those demonstrating endothelial dysfunction a priori (Maiorana et al. 2001, 2003; Tinken et al. 2008). Whilst untrained individuals demonstrate impaired endothelial function as a result of
Arterial compression during overhead throwing d C. H. STAPLETON et al.
intermittent arterial compression (Stapleton et al. 2009), the athletes in the present study may be protected against any detrimental effects by virtue of their training status. Frequent combined upper limb and lower limb exercise, as performed by elite waterpolo players, may act both locally and systemically to affect upper limb measures of endothelial function and to ameliorate any possible damaging effects related to intermittent compression. In the present study, IMT at the brachial and axillary artery showed no significant between-group differences. Whilst the difference in brachial artery IMT between COMP and NONCOMP approached statistical significance (p 5 0.084) it should be interpreted with caution as (1) the a priori power calculations were based on FMD, the more sensitive primary outcome measure and (2) this level of between-group difference is unlikely to classify as clinically significant (mean difference: 0.17 mm). Without observing any demonstrable differences in FMD measures it is unlikely, in this sample population, that evidence of intimal thickening would be exhibited. The data presented suggest that elite overhead athletes demonstrating inducible axillary artery compression with the performance of a diagnostic arm manoeuvre are not at any greater risk of developing an arterial injury i.e., thrombus and aneurysm formation, compared with noncompressing overhead athletes. However, as the athletes reported in case studies with aneurysm and/or thrombus formations were also highly trained, another mechanism, or an additional mechanism to inducible compression, must precipitate arterial injury. It should be noted that this study focused specifically on the third portion of the axillary artery and that some overhead throwing athletes have demonstrated arterial damage at other portions or branches of the axillary artery (Dijkstra and Westra 1978; Redler et al. 1986; Todd et al. 1998). Therefore, the results of this study should not be used to explain or describe the potential causes or impact of transient compression at these other sites. Several limitations are worthy to note. Whilst this study assessed common and valid surrogate indicators of arterial structure, function and health (e.g., FMD) no outcome measures directly assessed the presence of arterial injury and aneurysmal formation. These are outcomes that have been indentified in case reports of overhead athletes and linked, speculatively to axillary artery compression by the humeral head. Diminished FMD, CADC, GTN-induced-vasodilation responses and increased IMT have all been associated with individuals with known cardiovascular risk factors (Celermajer et al. 1992; Potter et al. 2007; Rickenlund et al. 2005) but not other types of arterial pathology or injury. However, although atherogenesis and aneurysm formation are different pathologic states, it is thought that the inflammatory mediators responsible for vessel wall
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changes are similar (Deanfield et al. 2005; Wills et al. 1996). Thus, it is likely that FMD measures would reflect an impaired arterial function resulting from past or present inflammatory reactions caused by biomechanical compression. It has been assumed that those athletes demonstrating clinically significant axillary artery compression in the supine position incur repeated compression through overhead motion during waterpolo training and competition. Although it is likely that similar compression would occur in the upright position haemodynamics may differ due to reduced hydrostatic pressure, which may impact on the changes seen in blood flow velocity and shear stress. However, it was thought that the performance of upper and lower limb exercise throughout overhead arm motion would counteract the gravitational changes on blood flow. One further issue to consider is the clinical criteria used. The criteria were based on the vascular capabilities of sedentary individuals. It may be that athletes are afforded enhanced endothelial health through high physical activity levels and require greater magnitudes of compression before detrimental changes to the endothelium are observed. Future research should explore other potential mechanisms, or combination of factors that predispose elite throwing athletes to arterial damage i.e., aneurysm and/ or thrombus formation. Similar to proposed causes of other conditions at the shoulder, such as subacromial impingement syndrome, factors such as changes in upper body posture (i.e. forward head posture) and an altered position of the scapula should be considered (Lewis et al. 2005) as well as the anatomical size of the humeral head (Nuber et al. 1990). In conclusion, transient axillary artery compression induced with overhead arm motion does not pose an obvious or immediate concern for the vascular health of elite overhead athletes. This study cannot confirm a role for transient axillary artery compression as an initial step in the mechanism(s) underpinning arterial damage and injury. The data suggest that other processes or mechanisms must contribute to the case reports of aneurysm and thrombus formation in elite level baseball pitchers and handball, tennis and volleyball players. REFERENCES Black MA, Cable NT, Thijssen DHJ, Green DJ. Importance of measuring the time course of flow-mediated dilatation in humans. Hypertension 2008;51:203–210. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE. Noninvasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992;340:1111–1115. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated
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Volume 36, Number 8, 2010 measured on multiple ultrasound frames: Evaluation of a DICOMbased software system. Cardiovasc Ultra 2007;5:1–10. Pyke KE, Tschakovsky ME. The relationship between shear stress and flow-mediated dilatation: Implications for the assessment of endothelial function. J Physiol 2005;568:357–369. Pyke KE, Tschakovsky ME. Peak vs. total reactive hyperemia: Which determines the magnitude of flow-mediated dilation? J Appl Physiol 2007;102:1510–1519. Redler MR, Ruland LJ III, McCue FC III. Quadrilateral space syndrome in a throwing athlete. Am J Sports Med 1986;14:511–513. Rickenlund A, Eriksson MJ, Schenck-Gustafsson K, Hirschberg AL. Oral contraceptives improve endothelial function in amenorrheic athletes. J Clin Endocrinol Metab 2005;90:3162–3167. Rohrer MJ, Cardullo PA, Pappas AM, Phillips DA, Wheeler HB. Axillary artery compression and thrombosis in throwing athletes. J Vasc Surg 1990;11:761–768. Schneider K, Kasparyan NG, Altchek DW, Fantini GA, Weiland AJ. An aneurysm involving the axillary artery and its branch vessels in a major league baseball pitcher: A case report and review of the literature. Am J Sports Med 1999;27:370–375. Stapleton C, Green D, Cable N, George K. Flow mediated dilation and intima media thickness of the brachial and axillary arteries in individuals with and without inducible axillary artery compression. Ultrasound Med Biol 2009;35:1443–1451. Stapleton C, Herrington LC, George KP. Anterior translation at the glenohumeral joint: A cause of axillary artery compression? Am J Sport Med 2008;36:539–544. Strandness D. Chapter 4: Hemodynamics of arterial stenosis and occlusion. In: Strandness D, (ed). Duplex scanning in vascular disorders. Philadelphia: Lippincott Williams and Wilkins; 2002. 68. Tinken TM, Thijssen DHJ, Black MA, Cable NT, Green DJ. Time course of change in vasodilator function and capacity in response to exercise training in humans. J Physiol 2008;586:5003–5012. Todd GJ, Benvenisty AI, Hershon S, Bigliani LU. Aneurysms of the mid axillary artery in major league baseball pitchers-A report of two cases. J Vasc Surg 1998;28:702–707. Tsuchiya K, Nakayama C, Washima F, Sakai H, Izumiyama H, Doi M, Hirata Y. Advanced endothelial dysfunction in diabetic patients with multiple risk factors: Importance of insulin resistance. J Atheroscler Thromb 2007;14:303–309. Vlychou M, Spanomichos G, Chatziioannou A, Georganas M, Zavras GM. Embolisation of a traumatic aneurysm of the posterior circumflex humeral artery in a volleyball player. Br J Sports Med 2001;35:136–137. Walther C, Gielen S, Hambrecht R. The effect of exercise training on endothelial function in cardiovascular disease in humans. Exerc Sport Sci Rev 2004;32:129–134. Williams MRI, Westerman RA, Kingwell BA, Paige J, Blombery PA, Sudhir K, Komesaroff PA. Variations in endothelial function and arterial compliance during the menstrual cycle. J Clin Endocrinol Metab 2001;86:5389–5395. Wills A, Thompson MM, Crowther M, Sayers RD, Bell PRF. Pathogenesis of abdominal aortic aneurysms - Cellular and biochemical mechanisms. Eur J Vasc Endovasc Surg 1996;12:391–400. Woodman RJ, Playford DA, Watts GF, Cheetham C, Reed C, Taylor RR, Puddey IB, Beilin LJ, Burke V, Mori TA, Green D. Improved analysis of brachial artery ultrasound using a novel edge-detection software system. J Appl Physiol 2001;91:929–937. Zar JH. Chapter 9: Paired-sample hypotheses. In: Ryu T, Snavely SL, (eds). Biostatistical analysis. New Jersey: Prentice Hall; 1999. p. 164.
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Original Contribution ARTERIAL COMPRESSION DURING OVERHEAD THROWING: A RISK FOR ARTERIAL INJURY? CLAIRE H. STAPLETON,* JADE ELIAS,y DANNY J. GREEN,*z N. TIM CABLE,* and KEITH P. GEORGE* * Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, United Kingdom; y English Institute of Sport, Sportcity, Rowsley Street, Manchester, United Kingdom; and z School of Sport Science, Exercise and Health, The University of Western Australia, Perth, Australia (Received 22 January 2010; revised 17 March 2010; in final form 3 May 2010)
Abstract—Case studies reporting aneurysm formation in the axillary artery have been described in overhead throwing athletes, possibly due to repetitive arterial compression by the humeral head that has been transiently observed during sonographic diagnostic arm manoeuvres. Whether compression negatively alters arterial health has not been investigated and was the focus of this study. The throwing arm of elite overhead athletes was screened for inducible axillary artery compression. Compressors (COMP, n 5 11, mean age: 20 (SD: 2) year, 7 male, 4 female) were age and sex matched with noncompressing (NONCOMP) athlete controls. Four indices of arterial health (flow mediated dilation [FMD], conduit artery vasodilatory capacity [CADC], glyceryl-trinitrate [GTN]induced vasodilation and intima-media thickness [IMT]) were assessed with high-resolution ultrasound at the brachial and the axillary, artery. No significant between-group differences were observed at the brachial, or axillary, artery for FMD (brachial: COMP: mean (SD) 6.2 (3.1)%, NONCOMP: 6.1 (3.5)%, p 5 0.967, axillary: COMP: 8.0 (5.5)%, NONCOMP: 9.0 (3.6)%, p 5 0.602), CADC (brachial: COMP: 10.4 (3.4)%, NONCOMP: 10.4 (5.4)%, p 5 0.999, axillary: COMP: 9.6 (4.2)%, NONCOMP: 8.5 (3.2)%, p 5 0.492), GTN-induced vasodilation (brachial: COMP: 17.9 (5.1)%, NONCOMP:14.1 (7.2)%, p 5 0.173, axillary: COMP: 9.5 (4.3)%, NONCOMP: 7.7 (3.1)%, p 5 0.302) or IMT (brachial: p 5 0.084, axillary: p 5 0.581). These results suggest that transient arterial compression, observed during diagnostic arm manoeuvres in overhead throwing athletes, is not associated with abnormal indices of artery function or structure and that other mechanisms must be responsible for the published cases of aneurysm formation in elite athletes performing overhead throwing actions. (E-mail: [email protected]) Ó 2010 World Federation for Ultrasound in Medicine & Biology. Key Words: Vascular compression, Endothelial function, Elite athletes, Overhead throwing, Flow mediated dilation, Intima media thickness.
unclear but excessive translation of the humeral head at the glenohumeral joint and/or a hypertrophied or tight pectoralis minor muscle, combined with repetitive overhead arm motion, have been implicated as the cause of transient compression at the third and second portions of the axillary artery, respectively (Dijkstra and Westra 1978; Stapleton et al. 2008). Repetitive compression is thought to result in damage to the arterial wall, including the endothelial layer with subsequent thrombus and/or aneurysm formation (Schneider et al. 1999; Stapleton et al. 2009). However, the proposed link between repetitive arterial compression with overhead arm motion and arterial health in elite overhead throwing athletes remains speculative. Our group recently studied the arterial health of eight nonathletic individuals who did not participate in activities requiring repetitive overhead activity but who did demonstrated such compression and compared them
INTRODUCTION AND LITERATURE Case reports in overhead throwing athletes have documented a continuum of findings from intermittent compression of the axillary artery and its branches, with the arm in an overhead position, to thrombosis, aneurysm formation and peripheral embolisation (Dijkstra and Westra 1978; Kee et al. 1995; Schneider et al. 1999). No epidemiologic data exists for the occurrence of thrombus or aneurysms in overhead throwing athletes, however, Rohrer et al. (1990) reported clinically significant inducible compression (.50% reduction in diameter) in 8% of baseball players. The cause of compression is
Address correspondence to: Claire Stapleton, Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Tom Reilly Building, Byrom Street Campus, Liverpool, Merseyside, L3 3AF. E-mail: [email protected] 1259
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with age and sex matched noncompressor controls. Mean flow-mediated dilation (FMD), an index of conduit artery endothelial function (Kooijman et al. 2008; Mullen et al. 2001), assessed downstream to the site of compression revealed a significantly (p 5 0.006) lower response in the ‘compressor’ group (mean (SD): 6.38 (3.28) vs. 10.38 (2.74)%) (Stapleton et al. 2009). These results suggest that the finding of clinically significant inducible axillary artery compression maybe of pathologic significance, potentially inducing endothelial dysfunction, an early sign of compromised vascular health and a potential precursor for the more serious arterial injuries described in published case reports (Dijkstra and Westra 1978; Kee et al. 1995; Schneider et al. 1999). Therefore, the aim of this investigation is to investigate if performance of repeated, transient arterial compression in an athletic population results in similar changes in arterial function and structure? MATERIALS AND METHODS Subjects The Great Britain (GB) men’s and women’s waterpolo squads were recruited. Inclusion criteria included participation in the squad’s full training programme for at least 2 months prior to testing. However, all subjects had been competing in waterpolo for at least 5 years. All male and female squad members undertook the same training routine with two pool sessions a day, 5 days a week and an additional strength and conditioning session, 2 days of the week. Subjects provided written informed consent prior to completing a health screening questionnaire to exclude those with factors known to influence the indices of vascular health, flow mediated dilation (FMD) and conduit artery vasodilatory capacity (CADC) response, e.g. diabetes, asthma, amenorrhea, recent allergic reactions, infections or injuries. Subjects underwent subjective and objective musculoskeletal screening to exclude any past or present musculoskeletal injury that may predispose them to neurovascular compression. The presence or absence of the Arch of Langer (an anomalous musculotendinous slip) was assessed by visual inspection and palpation. Ethical approval was granted from Liverpool John Moores University ethics committee. All subjects (n 5 37, mean age (SD): 20 (3) years, sex: 24 males, 13 females) were screened for clinically significant inducible axillary artery compression. A priori sample size estimation (n 5 8 per group) was based on detecting a clinically significant difference in FMD at the brachial artery of 2.5%, with an alpha level of 0.05 and a power of 80% (Woodman et al. 2001). Measurement of FMD at the brachial artery was used for sample size estimation as it has been used extensively in cardiovas-
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cular research and has been validated as an indicator of arterial health (Celermajer et al. 1992; Hashimoto et al. 2003; Tsuchiya et al. 2007). Data collection – Phase 1: Screening for clinically significant inducible axillary artery compression Following 10 min rest in the supine position to stabilise heart rate and blood flow, the subjects’ dominant (throwing) arm was passively supported in the baseline position (60 abduction) or the stress position (120 abduction, 30 horizontal extension and 90 external rotation) (Fig. 1). The axillary artery was located and imaged at the axilla and, therefore, it was necessary to incorporate some abduction into the baseline position to (1) accommodate the ultrasound transducer and (2) to optimise image clarity. To aid standardisation of the stress position, the posterior corner of the acromion was positioned over a marker on the treatment table and the arm supported in a custom made arm rest. A high-resolution ultrasound machine (Terason t3000; Teratech, MA, USA) with an 8-10 MHz linear array transducer was used to record arterial diameter and peak systolic flow velocity (PSV) for 1 min in each position. Post-test analysis was performed with wall tracking and edge detection computer software (LabVIEW 7.0; Version 3, National Instruments, Austin, TX). The software (Woodman et al. 2001) produces a mean diameter and a mean PSV from the pre-recorded 60 s of data. A doubling of PSV with the arm in the stress position compared with the baseline position is indicative of a 75% reduction in the cross-sectional area, which is classified as clinically significant arterial compression (Fig. 2a and b; Strandness 2002). Subjects demonstrating this degree of compression formed the compressor (COMP) group whereas the noncompressor (NONCOMP) group comprised of subjects demonstrating less than a 20% rise in PSV with the arm in the stress position
Fig. 1. The subject is pictured in the supine position with the dominant arm passively supported, with a purpose built arm rest, in the stress position (120 abduction, 30 horizontal extension and 90 external rotation).
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Fig. 2. Duplex ultrasound images of the axillary artery in (a) the baseline position and (b) the stress position. Note the change in peak systolic velocity indicative of clinically significant arterial compression.
compared with baseline. The stress position is similar, but less extreme, to the arm position achieved during the cocking phase of the throwing motion, it was therefore assumed that athletes classified as compressors would repeatedly compress the axillary artery when performing throwing motions in waterpolo training and competition. The subjects’ opposite limb also underwent screening, however, it was not used as the control arm as, concordant with our previous research, some subjects demonstrated bilateral compression or bilateral noncompression. Furthermore, due to the imbalance in frequency of performing overhead motions between the dominant and nondominant limb it was preferable to compare a dominant ‘‘compressor’’ limb with a dominant ‘‘noncompressor’’
limb. Consequently, control subjects were training, age and sex matched. Data collection – Phase 2 Subjects allocated to a group underwent phase two of data collection. Four indices of arterial health, flow mediated dilation (FMD; an index of endothelial function), conduit artery dilator capacity (CADC; an index of arterial structure), glyceryl tri-nitrate (GTN) induced vasodilation (an index of vascular smooth muscle function) and intima media thickness (IMT; an index of arterial wall structure) were assessed at the third portion of the axillary artery and at the brachial artery. Theoretically, arterial compression at the axillary artery is likely to alter blood flow patterns
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and shear stress locally but also immediately downstream to the compression potentially causing a disturbance to the equilibrium of the endothelium at both brachial and axillary artery sites. All ultrasound scans were performed by one trained sonographer who was blinded to group allocation. FMD, CADC and GTN-induced vasodilation Prior to testing, subjects were required to fast and abstain from caffeine, alcohol and exercise for 4 h (Corretti et al. 2002). Female subjects were tested within the early follicular phase of the menstrual cycle (Williams et al. 2001). Following 10 min rest in the supine position, arterial diameter and blood flow velocity were recorded via the previously described high-resolution ultrasound machine with parameters set to optimize B-mode longitudinal images of the target artery. FMD, CADC and GTN-induced vasodilation were assessed at both arterial sites with the dominant arm supported at 60 abduction. The brachial artery was imaged at the middle third of the humerus and the third portion of the axillary artery in the axilla just distal to the subscapular artery. The order of testing was randomized (computer generated) and a 10-min rest period in the supine position was enforced between tests to allow the arterial diameter to return to baseline (Corretti et al. 2002). To ensure GTN administration did not influence the basal diameter measures for subsequent assessments, GTN-induced vasodilation was the final test. The second assessment for GTN-induced vasodilation at the second arterial site was performed on a separate occasion (within 24–48 h). This avoided any potential side effects of administering a double-dose of GTN. Assessment of FMD/CADC and GTN-induced vasodilation A sphygmomanometer pressure cuff (Clinicus I; Aneroid, Boso, Germany) was placed 3 cm distal to the olecranon process and provided the stimulus for forearm ischemia. Following recording of baseline measurements for 1 min, the cuff was inflated to a supra-systolic pressure (220 mm Hg) for 5 min. Recording of the arterial diameter and blood flow velocity resumed 30 s prior to cuff release and continued for 3 min post cuff release (Black et al. 2008). For the assessment of CADC, handgrip exercises were performed by the subject, during the third and fourth minute of cuff inflation of the above protocol. The speed of gripping was guided by a metronome set at 1 Hz and the power output was monitored with a dynamometer (Grip D; Takei, Tokyo, Japan) and standardised to a predetermined 20% of the subjects’ maximal voluntary contraction. The use of handgrip exercises during a 5-min
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ischaemic period has been reported as sufficient stimulus to induce a peak dilator response (Naylor et al. 2005). GTN-induced vasodilation assesses the responsiveness of the smooth muscle cells to nitric oxide indicated by the magnitude of dilation. The nitrates within GTN bypass the endothelium and act directly on the smooth muscle cells within the tunica media layer of the arterial wall. The target artery was imaged for 1 min prior to sublingual administration of 400 mg of GTN and continued for 6 min postadministration (Celermajer et al. 1992).
Analysis of FMD, CADC and GTN data Post-test analysis was performed with an automated edge detection and wall tracking computer-software program (LabVIEW 7.0; Version 3, National Instruments; Woodman et al. 2001). The operator highlighted a portion of the B-mode image with optimum clarity and enclosed it in a region-of-interest (ROI) window. The software identifies and tracks the walls of the artery within the ROI window and detects changes in arterial diameter over time. The program produced an averaged diameter measure from approximately 300 measurements per frame, with an estimated 20 to 30 frames per s and automatically detected the peak response. FMD, CADC and GTN-induced vasodilation were expressed as the percentage increase in diameter from baseline to peak. The intraobserver coefficient of variation, for FMD with this software, is 6.7% (Woodman et al. 2001). For FMD and CADC responses, the Doppler waveform analysis function allowed simultaneous recording and analysis of the flow and shear rate stimulus, from cuff deflation to peak vasodilation. A ROI window encapsulated the spectral waveform and the blood flow velocity profile was tracked from baseline (pre-cuff inflation) to 3 min post-cuff release. Pyke and Tschakovsky (2005) highlighted the importance of controlling for the flow stimulus. They reported that endothelium dependent vasodilator responses were not only dependent on the health of the vascular endothelium but also on the magnitude of shear stimulus imposed on the endothelium and that individual differences in arterial diameter size can result in different magnitudes of shear rate despite the same volumetric flow. Therefore, for comparison between individuals and groups it is necessary to normalise the FMD and CADC response to the magnitude of the shear stress stimulus. The magnitude of the shear stimulus was quantified by calculation of the area under the curve (AUC) imposed during the period from cuff release to peak dilation (Pyke and Tschakovsky 2007). The FMD and CADC (percentage) response was divided by the AUC for the relevant portion of the shear rate profile to give a normalised FMD and CADC response.
Arterial compression during overhead throwing d C. H. STAPLETON et al.
Assessment and analysis of intima-media thickness (IMT) An 8-10 MHz linear array transducer recorded highresolution B mode images at the two arterial sites for approximately 30 s. Ultrasound parameters were set to optimise image clarity at the far arterial wall only (Poredos 2004). Custom designed computer software for the detection of the distance between the lumen-intima interface and the media-adventitia interface was used to extract the intima-media thickness (IMT version 3.0, National Instruments). This edge detection software and its analysis has been described in detail elsewhere (Potter et al. 2007). In brief, following the selection of frames for analysis and calibration, the operator selected a portion of the artery with optimum clarity within a ROI window. An edge detection algorithm detected the near and far arterial lumen edges and the far wall IMT within the specified ROI. When the lumen edge was detected, the pixels of the intima and media were removed and the automated edge detection process is repeated to find the far wall media-adventitia interface. Near and far wall lumen edges and the far wall mediaadventitia interface were detected on every frame within the selected image recording.
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Table 1. Background characteristics for compressor (COMP) and noncompressor (NONCOMP) groups
Indicator of compression* Age Sex BMI Systolic BP Hand dominance Resting brachial artery diameter (cm) Resting axillary artery diameter (cm)
COMP
NONCOMP
125 (49) % 20 (2) 7_4\ 24.8 (2.0) 124 (12) 11 right, 0 left 0.43 (0.06)
–15 (21) % 20 (2) 7_4\ 24.5 (2.0) 124 (12) 11 right, 0 left 0.42 (0.07)
0.55 (0.08)
0.51 (0.07)
BP 5 blood pressure; BMI 5 body mass index. *Percent change in peak systolic flow velocity from baseline position to stress position.
Statistical analysis All analyses were performed using SPSS (version 15.0, Chicago, IL) computer software program with the alpha level set to p , 0.05. The method of comparison between the COMP and NONCOMP groups for absolute and normalised FMD, CADC and GTN-induced vasodilation at the brachial and axillary artery depended upon the data meeting parametric assumptions. Zar (1999) proposes that where two groups show moderate correlation the paired t-test is more powerful than an independent t-test. Therefore, where paired group data demonstrated adequate correlation (r . 0.4) paired t tests were performed; otherwise independent t tests were adopted. RESULTS Eleven subjects met Strandness’s (2002) criteria for arterial compression and formed the compressor group (COMP: mean age (SD): 20 (2), sex: 7 male, 4 female). These were age, sex and training matched with noncompressor athlete controls (NONCOMP). Table 1 presents the background characteristics. The anatomical anomaly, ‘‘the arch of Langer’’, was not detected in any subjects. Flow mediated dilation No significant differences were revealed at the brachial artery for FMD (COMP: 6.2 (3.1)%, NONCOMP: 6.1 (3.5)%, t10 5 –0.042, p 5 0.967) (Fig. 3a) or normalised FMD (COMP: 0.00026 (0.00016) s21,
Fig. 3. Compressor (COMP) and noncompressor (NONCOMP) groups means and standard deviations for flow-mediated dilation (FMD) (%) for the three vasodilatory test conditions, conduit artery vasodilatory capacity (CADC), FMD and glyceryl trinitrate (GTN) at (a) the brachial artery and (b) the axillary artery.
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NONCOMP: 0.00022 (0.00013) s21, t20 5 –0.590, p 5 0.562). The same was true for FMD (COMP: 8.0 (5.5)%, NONCOMP: 9.0 (3.6)%, t2050.530, p 5 0.602) and normalised FMD (COMP: 0.00046 (0.00030) s21, NONCOMP: 0.00050 (0.00036) s21, t10 5 0.413, p 5 0.688) at the axillary artery (Fig. 3b). Conduit artery dilatory capacity Neither CADC (COMP: 10.4 (3.4)%, NONCOMP: 10.4 (5.4)%, t10 5 0.001, p 5 0.999) (Fig. 3a) or CADC normalised for shear rate (COMP: 0.00020 (0.00013) s21, NONCOMP:0.00014 (0.000087) s21, t20 5 –1.209, p 5 0.241) demonstrated significant between group differences. Similar results were found at the axillary artery for CADC (COMP: 9.6 (4.2)%, NONCOMP: 8.5 (3.2)%, t20 5 –0.701, p 5 0.492) (Fig. 3b) and CADC normalised for shear rate (COMP: 0.008 (0.001) s21, NONCOMP: 0.001 (0.002) s21, t20 5 0.230, p 5 0.821). GTN-induced vasodilation No significant differences were observed for GTNinduced vasodilation at the brachial (COMP: 17.9 (5.1)%, NONCOMP:14.1 (7.2)%, t20 5 –1.413, p 5 0.173) (Fig. 3a) or axillary artery (COMP: 9.5 (4.3)%, NONCOMP: 7.7 (3.1)%, t19 5 –1.061, p 5 0.302) (Fig. 3b). Intima media thickness IMT observed at the brachial artery (COMP: 1.03 (0.18) mm, NONCOMP: 0.86 (0.24) mm, t20 5 1.820, p 5 0.084) and axillary artery (COMP: 0.89 (0.28) mm, NONCOMP: 0.84 (0.14) mm, t19 5 –0.561, p 5 0.581) were no different between groups (Fig. 4).
Fig. 4. Mean intima-media thickness (mm) for compressor (COMP) and noncompressor (NONCOMP) groups s at the brachial and axillary artery. Error bars represent standard deviations.
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DISCUSSION AND SUMMARY The aim of the present study was to determine whether transient compression at the third portion of the axillary artery in elite overhead athletes resulted in diminished indices of arterial function or structure. Elite overhead athletes demonstrating transient compression did not present with any deterioration in FMD, CADC, GTN-induced vasodilation or IMT when compared with age, sex and training matched noncompressor athletes. Overall these athletes have healthy arterial structure and function with FMD responses lying within the normal range (Celermajer et al. 1992) and, indicative of their exercise training, mean resting arterial diameter sizes (brachial: 0.43 cm, axillary: 0.53 cm) greater than their less active counterparts observed in our previous study (brachial: 0.37 cm, axillary: 0.48 cm) (Stapleton et al. 2009). The lack of a significant difference in brachial artery FMD between COMP (6.2 [3.1]%) and NONCOMP (6.1 [3.5]%) groups differ to findings from our previous study (Stapleton et al. 2009) where FMD was significantly reduced (p 5 0.006) in nonathletic healthy subjects demonstrating inducible axillary artery compression with an overhead arm manoeuvre compared with a matched noncompressor group (6.38 [3.28] vs. 10.38 [2.74] %). We concluded from this data that the finding of clinically significant inducible axillary artery compression maybe of pathologic significance and a potential precursor for the more serious arterial injuries described in published case reports (Fields et al. 1986; Ishitobi et al. 2001; Rohrer et al. 1990; Vlychou et al. 2001). One explanation for the absence of deterioration in arterial health in the present study is that any potential deleterious effects of intermittent compression may have been counter-balanced by the beneficial impact of regular physical activity. Unlike the individuals described in the case reports, subjects from our previous study were not highly trained. It is well established that repeated exercise training can be associated with enhanced endothelial function (Green et al. 2004). Acute bouts of exercise are associated with increases in endothelial shear stress, which, through a series of complex interactions, mediates an increase in the release of nitric oxide [NO] and consequent vasodilation (Deanfield et al. 2007; Green et al. 2004; Maiorana et al. 2003). Recurrent bouts of exercise result in up-regulation of NO bioactivity and increased capacity for vasodilation (Deanfield et al. 2007; Maiorana et al. 2003; Walther et al. 2004). Improved FMD responses following exercise training have been observed in healthy individuals as well as those demonstrating endothelial dysfunction a priori (Maiorana et al. 2001, 2003; Tinken et al. 2008). Whilst untrained individuals demonstrate impaired endothelial function as a result of
Arterial compression during overhead throwing d C. H. STAPLETON et al.
intermittent arterial compression (Stapleton et al. 2009), the athletes in the present study may be protected against any detrimental effects by virtue of their training status. Frequent combined upper limb and lower limb exercise, as performed by elite waterpolo players, may act both locally and systemically to affect upper limb measures of endothelial function and to ameliorate any possible damaging effects related to intermittent compression. In the present study, IMT at the brachial and axillary artery showed no significant between-group differences. Whilst the difference in brachial artery IMT between COMP and NONCOMP approached statistical significance (p 5 0.084) it should be interpreted with caution as (1) the a priori power calculations were based on FMD, the more sensitive primary outcome measure and (2) this level of between-group difference is unlikely to classify as clinically significant (mean difference: 0.17 mm). Without observing any demonstrable differences in FMD measures it is unlikely, in this sample population, that evidence of intimal thickening would be exhibited. The data presented suggest that elite overhead athletes demonstrating inducible axillary artery compression with the performance of a diagnostic arm manoeuvre are not at any greater risk of developing an arterial injury i.e., thrombus and aneurysm formation, compared with noncompressing overhead athletes. However, as the athletes reported in case studies with aneurysm and/or thrombus formations were also highly trained, another mechanism, or an additional mechanism to inducible compression, must precipitate arterial injury. It should be noted that this study focused specifically on the third portion of the axillary artery and that some overhead throwing athletes have demonstrated arterial damage at other portions or branches of the axillary artery (Dijkstra and Westra 1978; Redler et al. 1986; Todd et al. 1998). Therefore, the results of this study should not be used to explain or describe the potential causes or impact of transient compression at these other sites. Several limitations are worthy to note. Whilst this study assessed common and valid surrogate indicators of arterial structure, function and health (e.g., FMD) no outcome measures directly assessed the presence of arterial injury and aneurysmal formation. These are outcomes that have been indentified in case reports of overhead athletes and linked, speculatively to axillary artery compression by the humeral head. Diminished FMD, CADC, GTN-induced-vasodilation responses and increased IMT have all been associated with individuals with known cardiovascular risk factors (Celermajer et al. 1992; Potter et al. 2007; Rickenlund et al. 2005) but not other types of arterial pathology or injury. However, although atherogenesis and aneurysm formation are different pathologic states, it is thought that the inflammatory mediators responsible for vessel wall
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changes are similar (Deanfield et al. 2005; Wills et al. 1996). Thus, it is likely that FMD measures would reflect an impaired arterial function resulting from past or present inflammatory reactions caused by biomechanical compression. It has been assumed that those athletes demonstrating clinically significant axillary artery compression in the supine position incur repeated compression through overhead motion during waterpolo training and competition. Although it is likely that similar compression would occur in the upright position haemodynamics may differ due to reduced hydrostatic pressure, which may impact on the changes seen in blood flow velocity and shear stress. However, it was thought that the performance of upper and lower limb exercise throughout overhead arm motion would counteract the gravitational changes on blood flow. One further issue to consider is the clinical criteria used. The criteria were based on the vascular capabilities of sedentary individuals. It may be that athletes are afforded enhanced endothelial health through high physical activity levels and require greater magnitudes of compression before detrimental changes to the endothelium are observed. Future research should explore other potential mechanisms, or combination of factors that predispose elite throwing athletes to arterial damage i.e., aneurysm and/ or thrombus formation. Similar to proposed causes of other conditions at the shoulder, such as subacromial impingement syndrome, factors such as changes in upper body posture (i.e. forward head posture) and an altered position of the scapula should be considered (Lewis et al. 2005) as well as the anatomical size of the humeral head (Nuber et al. 1990). In conclusion, transient axillary artery compression induced with overhead arm motion does not pose an obvious or immediate concern for the vascular health of elite overhead athletes. This study cannot confirm a role for transient axillary artery compression as an initial step in the mechanism(s) underpinning arterial damage and injury. The data suggest that other processes or mechanisms must contribute to the case reports of aneurysm and thrombus formation in elite level baseball pitchers and handball, tennis and volleyball players. REFERENCES Black MA, Cable NT, Thijssen DHJ, Green DJ. Importance of measuring the time course of flow-mediated dilatation in humans. Hypertension 2008;51:203–210. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE. Noninvasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992;340:1111–1115. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, Vallance P, Vita J, Vogel R. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated
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