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Musculoskeletal Imaging |
1 Department of Radiology, Stanford University Medical Center, 300 Pasteur Dr.,
Stanford, CA 94305-5105.
2 Present address: Franklin & Seidelmann Virtual Radiologists, El Dorado
Hills, CA.
3 Department of Orthopaedic Surgery, Division of Physical Medicine and
Rehabilitation, Stanford University Medical Center, Stanford, CA
94305-5336.
4 Sand Hill Imaging, Menlo Park, CA 94025.
5 Department of Orthopaedic Surgery, Division of Sports Medicine, Burnham
Pavilion, Stanford University, Stanford, CA 94305-6175.
Received March 6, 2000; accepted after revision March 30, 2004.
Address correspondence to G. O. Matheson.
OBJECTIVE. The purpose of this study was twofold: to determine if asymptomatic elite distance runners exhibit stress reactions of the tibia on MR images and to determine if the presence of bone stress lesions predicts later development of symptomatic tibial stress injuries.
CONCLUSION. Signs of a tibial stress reaction were found on MRI in 43% of the 21 asymptomatic college distance runners in this study. The presence of these changes was not found to be a predictor of future tibial stress reactions or stress fractures. Our findings underscore the importance of correlating MRI findings with clinical findings before making therapeutic decisions.
Symptomatic stress reactions of bone and soft tissues are common in athletes. Runners have been shown to be particularly prone to these injuries, and in distance runners, the most frequent location for osseous stress reactions is the tibial diaphysis [1]. Osseous stress reactions are believed to occur along a continuum from accelerated remodeling with bone marrow inflammatory changes to the presence of a frank fracture line in cortical bone. In the majority of these patients, conventional radiograph findings are negative both at presentation of symptoms and on followup examinations. A cortical fracture line is infrequently seen, although subtle periosteal new bone formation may sometimes be detected. Radionuclide bone scans have been widely used for the diagnosis of stress lesions of the tibia because they show increased uptake in regions of bone stress and remodeling. More recently, MRI has emerged as a highly sensitive method for detecting stress reactions of bone [2, 3]. MR images can reveal features of stress reactions of bone such as subtle periosteal edema, marrow edema, and fracture lines that are often not seen on radiographs. We previously devised an MRI-based grading system to determine the time line for return to full impact activity [4].
In two earlier reports using radionuclide bone scanning to examine a painful site, incidental findings away from the site of symptoms were present in athletes [5] and ballet dancers [6], most consistent with asymptomatic tibial stress reactions. This phenomenon has not been well studied using MRI. MRI is a sensitive tool for detecting bone marrow edema, an early finding in bone stress injury, but its low specificity [2] requires care in clinical interpretation [7]. For example, MRI of fatigue stress injuries is affected by the acquisition protocol (T1-weighted vs STIR) and intra- and interobserver agreement [8]. A previous study followed cases of abnormal MRI findings in subjects who remained symptomatic [9]. We undertook the present study to investigate whether MRI findings of tibial stress reactions similar to those found in symptomatic individuals also occur in asymptomatic distance runners. Another purpose of this study was to find out whether the presence of stress reaction predicts development of future clinically symptomatic tibial stress injuries.
Subjects and Methods
Twenty-one college runners (11 men, 10 women; age range, 18–19 years) agreed to participate in the study, which was approved by the panel on human subjects in medical research at Stanford University. These subjects were a convenience sample of all the scholarship freshmen and top-ranked sophomore members of the university's distance running team. All participated in an intensive preseason training program for 8 weeks during which the men ran 50–70 miles per week (4- to 6-min pace) and women ran 40–60 miles per week (5- to 7-min pace). This mileage had been constant for 3 months, although the intensity (pace) was increased during the 8-week training period. The MRI examinations were performed within 1 week of completing this training. All subjects were asymptomatic for lower extremity pain. All subjects had been followed clinically by a physician for 8 weeks preceding the MRI and were asymptomatic during that period. Exclusion criteria were recent tibial pain or tenderness or any history of a tibial stress fracture or stress injury.
The MRI examinations were performed using a 1.5-T scanner (GE Healthcare). Both lower legs were positioned together and imaged using the body coil from the level of the knee joint to approximately 10 cm proximal to the tibiotalar joint. In the axial plane, T1-weighted spin-echo (TR/TE, 300/16) and T2-weighted fast spin-echo (5,000/102) images were obtained. In the sagittal plane, T2-weighted fast spin-echo images (5,000/102) were obtained. Fat saturation was used on the T2-weighted fast spin-echo images. The field of view was 24–28 cm in the axial plane and 32 cm in the sagittal plane. Slice thickness was 4 mm with a 4-mm interslice gap in the axial plane and 3 mm with a 1-mm interslice gap in the sagittal plane. The matrix was 256 x 192 for the T1-weighted images and 256 x 256 for the T2-weighted fast spin-echo images.
All MR images were evaluated and scored by two experienced musculoskeletal radiologists in consensus. The image evaluation included normal versus abnormal signal of the periosteum, cortex, and bone marrow; presence of a fracture line; and tibial location for proximal, middle, or distal third of the tibia in patients exhibiting a stress injury. All MR images were also graded according to a five-level grading scheme for stress reactions [4]. Grade 0 indicated normal MRI findings. The other grades were cumulative, with each grade adding further characteristics. Grade 1 indicated increased signal involving the periosteal region as seen on T2-weighted images only, with normal marrow signal intensity on all images. Grade 2 added bone marrow signal increase on T2-weighted images. Grade 3 added the presence of bone marrow signal changes on T1-weighted images, and grade 4 added the presence of a clearly visible fracture line [4].
Other MRI abnormalities involving the lower leg were noted and recorded, including edema involving muscle and subcutaneous fat and edema along fascial structures.
After MRI, the subjects were followed by their team physician for clinical symptoms or signs of lower leg pain. Stanford University uses a system in which athletic trainers and physical therapists file weekly injury reports for athletes on every team. Athletes who had transferred to other universities or elected to give up running were contacted by telephone to obtain follow-up information. Other clinically significant overuse injuries were also recorded. The observation period included the full 4-year college athlete career or shorter periods for the four individuals who discontinued their college running careers.
Results
For the 21 asymptomatic runners, both tibiae appeared normal on MRI in 12 subjects. The nine remaining runners (43%) had MRI abnormalities indicating the presence of a tibial stress injury. Unilateral stress injuries were found in four of the nine subjects. The other five subjects showed bilateral stress reactions Twenty-eight tibiae (67%) were normal (grade 0) and 14 tibiae (33%) were abnormal (grades 1–3) on MRI. Two subjects (four tibiae) had grade 1 injuries (Fig. 1), six subjects (two bilateral, four unilateral) had grade 2 injuries (Fig. 2), and two subjects had unilateral grade 3 injuries (Figs. 3A and 3B). No grade 4 injuries were identified. Other abnormalities detected in these asymptomatic individuals included muscle edema (Fig. 4) and edema along fascial planes.
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Tibial stress changes of grades 1–3 were present in five men and four women. Of the total of 11 men and 10 women in the study, six men and six women had normal bilateral MRI findings.
None of the 21 subjects reported lower leg symptoms during the observation period of 8 weeks before MRI. During the follow-up period, 17 subjects continued with the university cross-country training program for the full 4 academic years. During this time, 10 of those 17 achieved all-American college athlete ranking in distance (cross-country) running.
One subject in the group with normal MRI findings discontinued running after 1 year. In the group with abnormal MRI findings, six of the nine subjects were followed for 48 months, during which time none developed symptoms or signs of a tibial stress injury. One of the nine subjects transferred to another college, continued running, and did not develop a tibial stress injury during the 48-month follow-up period. Two of the nine discontinued running after 1 year and had not developed symptoms or signs of a tibial stress injury during that 12-month period.
Discussion
MRI has been shown to be a sensitive method for the detection of stress reactions in the tibia in symptomatic runners [4, 10]. The severity of tibial changes can be graded on the basis of MRI features and correlated with the severity of involvement. This grading schema can be of clinical value to guide the duration of rehabilitation required before return to full activity [4].
It has not, however, been well established whether tibial stress reactions detected on MRI are always related to clinical symptoms. Bone marrow edema has been reported in bones of the feet and ankles of 16 of 20 runners and four of 12 nonrunners [11] and in cases of altered loading mechanics such as overpronation [12]. Asymptomatic uptake of radionuclide on bone scans has been reported at sites that did not correspond to symptoms [5]. The same phenomenon probably occurs with MRI. In addition, the sensitivity and specificity of MRI for detecting bone stress lesions vary depending on coronal T1-weighted versus STIR images and intra- and interobserver agreement [8]. Thus, the efficacy of MRI has not been fully assessed with respect to bone stress lesions; therefore, it is valuable to know whether all tibial stress lesions ultimately lead to clinical symptoms or merely are accelerated osseous remodeling [5].
In this study, we have shown that 43% of asymptomatic distance runners have subclinical MRI abnormalities characteristic of a bone stress lesion.
The MRI features of bone stress lesions and their spectrum from mild to more severe abnormalities have previously been well described [4]. The tibial stress reactions reported in this study are of the posteromedial or posterolateral diaphyseal type. Several other less frequent types of tibial stress fractures have been reported. These include the anterior diaphyseal tibial cortex stress fracture with the characteristic transverse "dreaded black line" detected on conventional radiography [13] and the longitudinal diaphyseal tibial stress fracture [14, 15] that is often difficult to diagnose. The term "shin splints" is less precise and is often used to indicate any type of tibial stress injury or the earlier manifestations of a tibial stress lesion before a fracture component can be identified [2].
Differential diagnosis for the MRI features of a tibial stress reaction includes a normal nutrient vessel mimicking disease, the presence of hematopoietic bone marrow hyperplasia, and neoplastic marrow infiltration such as lymphoma. The normal finding of a nutrient vessel obliquely traversing the posterior tibial cortex at mid diaphyseal level is important to recognize because it may mimic a fracture line (Fig. 5). This nutrient vessel is usually well defined at the cortical level and tends to branch soon after entering the intraosseous marrow space of the tibia. It is consistently located in a position extending obliquely through the cortex proximally from the external tibial surface to an intraosseous position in the distal tibia. Hematopoietic bone marrow hyperplasia, seen as patchy regions of decreased signal on T1-weighted images and moderately increased signal on T2-weighted images, may also mimic a bone stress lesion and has been reported in long-distance runners [16]. In our subjects, marrow conversion appearing as signal changes of bone marrow in the tibiae may well be present but is not likely to be the cause of the linear marrow signal abnormalities seen along the tibial cortex with corresponding evidence of periosteal edema. We exclude the possibility that neoplastic marrow infiltration was causing the changes we describe because none of the subjects developed any neoplastic marrow disorders during the 4-year clinical follow-up period. Excellent reviews on this topic have been published [3, 17].
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The high frequency of asymptomatic stress reactions of the tibia in this group of college distance runners underscores the importance of a careful clinical examination to correlate any history and clinical findings with radiographic findings. In runners, particularly in competitive distance runners, it is likely that areas of bone stress reaction that are not clinically symptomatic may be present at various times during their training [18].
None of the nine patients with asymptomatic MRI findings developed a bone stress injury on follow-up (seven followed for 48 months, two followed for 12 months). Eighty-one percent of the athletes in this study experienced an overuse injury else-where during their collegiate careers.
In conclusion, we have shown that the presence of tibial stress reactions detected on MR images without corresponding clinical symptoms did not predict future tibial stress reactions but more likely reflects the high training load to which these elite distance runners are subjected. Our findings underscore the importance of correlating MRI findings with clinical findings for both type and location before making therapeutic decisions. Agreement is growing that MRI is the gold standard for assessment of stress injuries to bone [19].
Acknowledgments
We thank K. Hoffman for assistance with performing the MRI examinations in this study.
References
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  M. Fredericson, W. Moore, and S. Biswal Sacral Stress Fractures: Magnetic Resonance Imaging Not Always Definitive for Early Stage Injuries: A Report of 2 Cases Am. J. Sports Med., May 1, 2007; 35(5): 835 - 839. [Full Text] [PDF]
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 M. Gaeta, F. Minutoli, S. Vinci, I. Salamone, L. D'Andrea, L. Bitto, L. Magaudda, and A. Blandino High-resolution CT grading of tibial stress reactions in distance runners. Am. J. Roentgenol., September 1, 2006; 187(3): 789 - 793. [Abstract] [Full Text] [PDF]
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