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1 Department of Medical Imaging, Flinders Medical Centre, Flinders Dr., Bedford
Park, Adelaide, South Australia 5042, Australia.
2 Sportsmed SA (Sports Medicine Clinic), 32 Payneham Rd., Stepney, South
Australia 5069, Australia.
3 Perrett Medical Imaging, 199 Ward St., North Adelaide, South Australia 5006,
Australia.
Received February 1, 2002;
accepted after revision June 6, 2002.
Presented at the annual meeting of the Radiological Society of North
America, Chicago, November 2000.
Abstract
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SUBJECTS AND METHODS. Thirty-seven athletes with suspected hamstring injury underwent T1 and inversion recovery T2 turbo spin-echo MR imaging in axial and sagittal planes. The presence and dimensions of abnormal focal intra- and extramuscular T2 hyperintensity were independently recorded by two radiologists, and the muscles involved and intramuscular location of injury were noted. The percentage of abnormal cross-sectional muscle area, abnormal muscle volume, and length of extramuscular T2 hyperintensity were measured from T2-weighted images depicting the maximal extent of the injury. Time (days) lost from competition was noted during follow-up.
RESULTS. MR imaging detected hamstring muscle and linear extramuscular T2 hyperintensity in 30 (81%) and 25 (68%) of 37 athletes, respectively. The long head of the biceps was the dominant site of injury in 21 cases. The musculotendinous junction was involved in 28 (76%) of 37 cases. A relationship was seen between days lost from competition and percentage of abnormal muscle area (r = 0.63, p = 0.001) and volume of muscle affected (r = 0.46, p = 0.01), but only a trend for linear extramuscular T2 hyperintensity (r = 0.33, p = 0.12) was shown.
CONCLUSION. Rehabilitation time was related to MR measurements such as the percentage of abnormal muscle area and approximate volume of muscle injury. Hamstring injury most frequently involved the long head of the biceps femoris muscle, and involvement of the intramuscular tendon was common.
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Appearances of hamstring injury have been documented using MR imaging [3,4,5,6,7], but little attention has been directed to the prognostic value of MR imaging in assessing the injury. One article [5] has indicated that objective information regarding the extent and nature of muscle injury may allow prediction of the convalescence interval in high-performance athletes. In that retrospective study of 14 athletes, poor prognostic factors indicated by MR imaging included complete muscle rupture and retraction, hemorrhage, ganglionlike fluid collections, involvement of large cross-sectional areas, and distal myotendinous junction involvement. That relatively small study implies that MR imaging may provide prognostic information relevant to the management of these common injuries.
We therefore undertook a larger prospective study to further investigate the association between the extent and nature of hamstring injury shown on MR imaging and the amount of time a group of high-performance athletes lost from competition.
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All 37 athletes were male, the median age was 24 years (range, 17-32 years), and the body mass index ranged from 20.9 to 28.2 kg/m2. During clinical assessment, athletes were asked to rate their pain on a scale of 0-10 (0 = no pain, 10 = maximal pain intensity). All athletes were treated according to a predefined protocol involving an initial period of immobilization (rest, ice compression, and elevation) immediately after injury followed by gradually increasing mobilization (walking, stretching, and physiotherapy) and activity according to athlete pain levels. Sonography and electric stimulation were not part of the protocol. MR imaging data other than the presence or absence of hamstring abnormality were not made available to managing physicians. The number of days between injury and recommencement of competition was noted during follow-up.
MR Imaging
Athletes underwent MR imaging with a 1.5-T imaging unit (Vision; Siemens
Medical Systems, Erlangen, Germany) 2-6 days (median, 3 days) after injury.
Before imaging, we affixed a vitamin E capsule to the athlete's leg overlying
the point of maximal tenderness indicated by the athlete. A flexible
circularly polarized body array coil was used with the patient in the supine
position. After coronal localization, we acquired axial T1-weighted turbo
spin-echo MR images (TR/TE, 802/12; section thickness, 10 mm; field of view,
30-32 x 40.0-42.7 cm; echo-train length, 3; matrix, 213 x 512;
intersection gap, 20%; acquisitions, 2) and axial inversion recovery
T2-weighted turbo spin-echo images (5032/30; section thickness, 10 mm; field
of view, 30.0-31.9 x 40.0-42.5 cm; echo-train length, 7; matrix, 182
x 256; inversion time, 150 msec; intersection gap, 20%; acquisitions,
1). Additionally, we obtained sagittal T1-weighted turbo spin-echo images
(676/12; section thickness, 7 mm; field of view, 24 x 32 cm; echo-train
length, 3; matrix, 213 x 512; intersection gap, 20%; acquisitions, 2),
sagittal inversion recovery T2-weighted turbo spin-echo images (5000/30;
section thickness, 7 mm; field of view, 24 x 32 cm; matrix, 189 x
256; echo-train length, 7; inversion time, 150 msec; intersection gap, 20%;
acquisitions, 1), and axial gradient-echo images (610/18; flip angle, 20°;
section thickness, 10 mm; field of view, 30.0-31.4 x 40.0-41.9 cm;
matrix, 192 x 512; intersection gap, 20%; acquisitions, 1). The latter
images were acquired with the intent of detecting hemorrhage with greater
sensitivity than on turbo spin-echo sequences.
Images were independently interpreted by two radiologists who were unaware of clinical details other than the suspected hamstring injury. Each radiologist recorded the presence or absence of abnormal focal intra- and extramuscular T2 hyperintensity, the muscles involved, and the location of the abnormality in each muscle. The muscle exhibiting the most extensive T2 hyperintensity was noted, and abnormal signal in this muscle was categorized as involving the musculotendinous junction (proximal or distal) or the muscle belly (adjacent to the intramuscular tendon or not). Injuries in the muscle belly were denoted as proximal (above the femoral origin of the short head of the biceps) or distal. Hamstring muscle injury was considered to be present when abnormal T2 signal was seen in one or more hamstring muscles. Discordant cases (regarding either the presence or absence of hamstring muscle injury or the muscle most involved) were reviewed and consensus reached. At that time, transverse images showing the maximal intra- and extramuscular extent of T2 hyperintensity were selected for further analysis.
Measurements were performed at the console of the MR imaging unit and were
directed to the selected transverse T2-weighted image of the muscle showing
the most extensive hyperintensity. The maximal anteroposterior and transverse
dimensions of the region of intramuscular hyperintensity were measured from
the designated image (Fig. 1A).
Slice position notation on images was used to estimate the craniocaudal extent
of intramuscular T2 hyperintensity in that muscle belly. Sagittal T2-weighted
images were not used for the latter measurement because in some cases T2
hyperintensity was obliquely oriented with respect to the sagittal plane. The
volume of abnormal muscle was approximated using the formula for a prolate
ellipsoid ([
/6] x anteroposterior x transverse x
craniocaudal extent) [8].
Irregular regions of interest were drawn around the muscle to obtain the
cross-sectional area of the whole muscle belly and of intramuscular T2
hyperintensity (Fig. 1B). The
ratio of abnormal to total muscle cross-sectional area was thus obtained. The
length of extramuscular T2 hyperintensity was also measured (multiple line
segments) from the selected transverse T2-weighted image that best displayed
this finding (Fig. 2).
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Statistical Analysis
Statistical analysis was performed using Statistical Package for the Social
Sciences software (version 10.0; SPSS, Chicago, IL). The numbers of patients
in this study were relatively small, so statistical analysis was used to
indicate patterns of association.
The gamma statistic [9] was used to investigate the association between the number of days lost from competition and the presence or absence of intramuscular T2 hyperintensity. Spearman's rank correlation coefficient was used to assess relationships between the number of days lost from competition and the following MR indexes of muscle injury: percentage of cross-sectional area of abnormal muscle, approximate volume of abnormal muscle, and length of linear extramuscular T2 hyperintensity. Spearman's rank correlation coefficient was also used to examine relationships between an athlete's subjective pain scores and the percentage of cross-sectional area of abnormal muscle, the approximate volume of abnormal muscle, and the length of extramuscular T2 hyperintensity. The Mann-Whitney U test (exact) for nonpaired comparisons was used to assess relationships between the number of days lost from competition and the following factors: primary involvement of the long head of the biceps femoris muscle, primary involvement of the semitendinosus muscle, proximal muscle injury, muscle injury extending to the upper or lower musculotendinous junction, and the presence of greater than 50% cross-sectional area of abnormal muscle. The same statistical test was used to examine relations between MR imaging measurements of the extent of muscle injury and primary involvement of the biceps femoris and semitendinosus muscles.
A p value of 0.05 was considered an indicator of statistical significance; however, because of the number of statistical tests undertaken, the levels of statistical significance should be viewed with caution.
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Altered muscle signal intensity was least evident on T1-weighted images, most obvious on inversion recovery T2-weighted images, and of intermediate conspicuity on gradient-echo images (Fig. 3A,3B,3C,3D). Gradient-echo images revealed focal hypointensity suggestive of blood products in evolution in only one case (primary adductor magnus injury, Fig. 4A,4B,4C). Linear extramuscular T2 hyperintensity (range, 1.8-24.9 cm; median, 8.6 cm) was present in 25 (68%) of 37 cases.
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Distribution of Muscle Abnormality
The distribution of hamstring muscle injury is shown in
Table 1. No avulsion injuries
and no complete tendon ruptures were present. The long head of the biceps
muscle was the most commonly affected muscle (26 [87%] of 30 cases), and this
occurred in association with semitendinosus muscle strain in 11 (37%) of 30
athletes (long head of biceps muscle the dominant injury in six cases and
semitendinosus muscle injury dominant in five cases). The long head of the
biceps was the only muscle injured or the major site of abnormality in 21
(70%) of 30 cases, and the semitendinosus muscle was the sole or dominant
abnormality in nine cases (30%). The short head of the biceps was affected in
five (17%) of 30 cases of hamstring muscle injury, but in each case
involvement was minor and adjacent to the long head of the biceps muscle
belly. When the long head of the biceps was the sole or primary site of
injury, no greater intramuscular extent of injury occurred on the basis of
approximate volume (Mann-Whitney U test, p = 0.26) or
percentage of abnormal surface area (Mann-Whitney U test, p
= 0.48). Similarly, sole or primary involvement of the semitendinosus muscle
was not associated with greater intramuscular extent of injury.
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The musculotendinous junction was involved in 28 (93%) of the 30 cases with hamstring muscle injury at MR imaging, the two exceptions being small isolated injuries to the long head of the biceps that extended to the epimysium. Of these 28 cases, the intramuscular tendon was involved in 24 (86%) and the musculotendinous junction at the muscle end was solely involved in the other four cases (14%; three distal, one proximal). Five (21%; five proximal, none distal) of 24 injuries affecting the intramuscular tendon extended to the musculotendinous junction. Muscle or tendon injury was situated above the origin of the short head of the biceps in 11 instances (37%).
Influence of Injury Location on Rehabilitation Time
Although the long head of the biceps was the sole or dominant site of
injury in 21 cases, involvement of this muscle did not influence the duration
of absence from professional sport (Mann-Whitney U test, p =
0.86). Similarly, sole or dominant semitendinosus muscle injury did not appear
to result in greater rehabilitation time (Mann-Whitney U test,
p = 0.86). Using the short head of the biceps as a criterion for
classifying injury as proximal (above femoral origin) or distal, we noted 11
proximal and 19 distal injuries. No association was shown (Mann-Whitney
U test, p = 0.17) between proximal muscle injury and time
lost from competition. Hamstring muscle injury involving both muscle belly and
the adjacent musculotendinous junction did not influence the convalescence
interval (Mann-Whitney U test, p = 0.93).
Rehabilitation Time and Injury Extent as Measured on MR Imaging
The number of days lost from competition by those with hamstring muscle
injury ranged from 13 to 48 (median, 27 days). An association between the
presence of focal intramuscular T2 hyperintensity and the number of days lost
from competition (
= 0.69, p = 0.04) was present. Measurements
of the percentage of abnormal cross-sectional area (range, 8-100%; median,
46%) and approximate volume of abnormal muscle (range, 0.04-175.6
cm3; median, 16.8 cm3) were widely and not normally
distributed and are provided in Table
2. Athletes with hamstring muscle injury recorded subjective pain
scores ranging from 2 to 8 (median, 5).
Table 3 provides statistics
indicating relationships between MR imaging measurements of injury extent and
the number of days missed because of injury as well as subjective pain scores.
Abnormal cross-sectional muscle area greater than 50% was associated with a
longer rehabilitation time (Mann-Whitney U test, p <
0.001).
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One of the major findings of our study was of an association between rehabilitation time and MR parameters of muscle injury, such as the approximate volume of muscle injury and the extent of cross-sectional muscle involvement. Furthermore, cases with abnormal muscle cross-sectional area greater than 50% were also associated with longer recovery times, which is in agreement with one of the previous findings of Pomeranz and Heidt [5]. The presence of a correlation between convalescence interval and the MR parameters of muscle damage supports the concept that rehabilitation time is related to the proportion of muscle units disrupted during injury. Furthermore, with the exception of the semimembranosus muscle (insufficient data), the specific muscle involved was not related to rehabilitation time, which suggests that no individual muscle has greater functional significance or different healing time.
Unlike Pomeranz and Heidt [5], we did not observe any effect of injury location (proximal or distal) on the duration of absence from sport. No complete muscle transection was observed in that series, and most athletes (28/30, 93%) had injury involving the musculotendinous junction. Thus, the influence of this type of injury on convalescence time could not be assessed.
In our study, linear T2 hyperintensity between muscles was present in slightly more than two thirds of cases and, to our knowledge, has not been reported previously. This appearance likely represents extension of intramuscular fluid through an epimysial tear and therefore is considered an indirect indicator of the degree of intramuscular injury. Accordingly, this parameter of injury exhibited a weaker correlation with convalescence interval than direct measurements of injury such as the percentage of cross-sectional area or the approximate volume of muscle injured.
Higher subjective pain scores provided by the athletes were also associated with more extensive muscle injury. MR imaging provided additional value because five (14%) of 37 patients in our series who had clinical suspicion of hamstring muscle injury did not have muscle abnormality. In these instances, the final diagnosis was of referred pain, possibly from the back region [10]. Clinical assessment alone would have led to inappropriate therapy for hamstring muscle injury rather than to a more rapid return to competition. Therapy for hamstring muscle injury typically involves a period of immobilization followed by mobilization, the timing and rate of mobilization being guided by clinical features that include the athlete's subjective perception of pain [11] and the perceived risk of recurrent hamstring muscle injury. Although comment regarding the future role of these measurements is speculative, in the future MR parameters of injury such as those described in this article may provide objective and quantitative assessment of the evolution of muscle injury and therefore assist management decisions regarding the adequacy of healing before return to competition.
CT and MR imaging have been used by a number of authors [1, 3,4,5,6,7] to examine the appearance of hamstring muscles after injury. Most reports have considered the distribution of abnormality within the hamstring muscle group, and early MR studies [3, 4, 6] recorded the signal intensity pattern on T1- and T2-weighted images. Previous studies [1,2,3, 5, 7] have indicated that the biceps femoris is the most common hamstring muscle injured, and this finding is supported by our study. The predominance of biceps tendon tears may be due to the limited extensibility of the muscle, which originates from both the femur and the ischial tuberosity [12]. Additional risk factors relevant to the biceps femoris muscle include its eccentric function and high proportion of type II fibers [13].
Our study lends support to the common observation that the semitendinosus muscle is the second most common site of hamstring muscle injury [1, 4, 7], but reports are not uniform in this regard [3, 5]. Our observation that semimembranosus muscle injuries are uncommon (two [7%] of 30 athletes with hamstring muscle injury) concurs with the findings of De Smet and Best (one [7%] of 15 athletes) [7] but differs from those of Pomeranz and Heidt (five [36%] of 14 athletes) [5]. Injuries of the short head of the biceps were relatively uncommon (five [17%] of 30 athletes) and minor in our series, which is in keeping with the established concept that muscles crossing two joints are more prone to injury [13].
The distribution of injuries in the biceps femoris and semitendinosus muscles was also recorded by De Smet and Best [7]. In that study, the injury was deemed to be proximal in nine (60%) of 15 athletes, the upper aspect of the short head of the biceps being used as the criterion for assignment of proximal or distal injury. Injury involved the musculotendinous junction (proximal, distal, or intramuscular tendon) in all 15 cases in that series. The same criteria were applied during our study, but our distribution was somewhat different with regard to proximal injury, and we also found injury involving the musculotendinous junction to be common.
The MR signal intensity pattern was not suggestive of hemorrhage in our patients with hamstring muscle injury, but hemorrhage was present in one patient with injury to the adductor magnus muscle. Specifically, in this patient hypointensity was present on gradient-echo images; but in this and all other cases, T1 hyperintensity was absent or subtle. Although the literature contains reports of high T1 signal intensity as a result of intramuscular hemorrhage [5, 6, 14], our observations are supported by two other studies [3, 4].
A number of factors may explain the absence of T1 hyperintensity in our study. First, the interval between injury and MR imaging was relatively short (median, 3 days). Therefore, at the time of imaging deoxyhemoglobin probably accounted for most of the blood products present. This molecular species has limited ability to shorten proton T1 relaxation [15] and, accordingly, little T1 hyperintensity may be observed on such images. Second, the quantity of hemorrhage may not be as great as anticipated, there being a predominance of inflammation and edema rather than hemorrhage in one experimental study of simulated muscle strain injury in dogs [16]. The absence of hamstring muscle hypointensity on T2-weighted images or "blooming" on gradient-echo images in our study also implies relatively small quantities of hemorrhage at the site of injury.
Several limitations of our study should be acknowledged. First, although an association between MR indexes of the severity of hamstring injury and the duration of convalescence was shown, the numbers in this study are only moderate, and confirmation with other larger studies is required. Second, it may not be possible to generalize findings derived from a population of Australian-rules football athletes to other athletic populations even though the mechanisms of injury (sprinting, jumping) are similar. The fact that MR measurements of hamstring muscle injury were related to convalescence interval in this study and that of Pomeranz and Heidt [5] does, however, suggest that this generalization may be sustained. Third, the possibility of bias because physicians treating athletes were told whether the MR examination had (30 cases) or had not (five cases) shown evidence of hamstring muscle injury, must be considered. No information regarding MR measurements or the location, extent, or severity of injury was provided, so information received by physicians regarding those athletes with hamstring muscle injury ("abnormal scan") was identical. Computation of correlation coefficients required only data from athletes with hamstring muscle injury; therefore, bias due to different information regarding hamstring status seems unlikely. Finally, the configuration of many muscle injuries did not conform well to that of a prolate ellipsoid. The measurement of the volume of muscle injury was therefore approximate but had the practical advantage of being derived from relatively simple measurements and straightforward calculation.
In summary, we examined the MR imaging appearance of the thigh in 37 athletes with clinical evidence of hamstring muscle strain injury. The biceps femoris and semitendinosus muscles were the most frequent sites of hamstring muscle strain, and an association was seen between rehabilitation time and MR imaging measurements of muscle injury, such as the percentage of cross-sectional area of abnormal muscle. In contradistinction to a previous study [5], we did not observe an association between longer convalescence interval and MR images that showed ganglionlike fluid collections, hemorrhagelike signal intensity, or distal injury. The amount of time lost from competition was not influenced by the specific muscle injured or by the intramuscular location of the injury.
Acknowledgments
We thank A. Esterman for advice and assistance with statistical analysis
and P. Barnes for his contribution to the clinical assessment of athletes. We
also thank the athletes who agreed to participate in this study and the
clerical and radiography staffs at Perrett Medical Imaging, who arranged and
performed MR imaging studies.
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