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Stress-related bone injuries with emphasis on MRI
Clinical Radiology (2007) 62, 828e836
PICTORIAL REVIEW
Stress-related bone injuries with emphasis on MRI A.P. Datir*, A. Saini, A. Connell, A. Saifuddin Department of Radiology, Royal National Orthopaedic Hospital, Brockley Hill, Stanmore Middlesex, London HA7 4LP, UK Received 14 May 2006; received in revised form 14 February 2007; accepted 19 February 2007
Stress-related bone injuries are common in professional athletes and in military personnel. However, in an increasingly health conscious society undertaking more, and often unsupervised, exercise regimes, these injuries may increase. Early diagnosis is of paramount importance to detect the signs of stress reaction, allow healing, and prevent progression to frank fracture. This review illustrates the classical magnetic resonance imaging (MRI) features of stress injury and fracture with emphasis on its role in the diagnosis and follow-up, as well as its limitations. ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Stress-related bone injuries (SRBI) occur in normal or abnormal bone that is subjected to repeated trauma with a load less than that which causes acute fracture. Stress fractures can be sub-grouped into two types: insufficiency fracture and fatigue fracture. A fatigue fracture is caused by the application of abnormal muscular stress or torque to a bone that has normal elastic resistance. The following triad is associated with most fatigue fractures: the activity is (1) new or different for the person, (2) strenuous, and (3) repeated with a frequency that ultimately produces signs and symptoms.1e4 An insufficiency fracture results when normal or physiological muscular activity is applied to a bone that is deficient in mineral or elastic resistance.5
Aetiology and distribution Fatigue fracture The first recording of stress related injury was in 1855 by Briethaupt, a Prussian military physician, * Guarantor and correspondent: A.P. Datir, Department of Radiology, Royal National Orthopaedic Hospital, Stanmore, Middlesex HA7 4LP, UK. Tel.: þ44 208 864 3232; fax: þ44 208 869 3907. E-mail address: [email protected] (A.P. Datir).
who recorded the painful swollen feet of marching soldiers. It was not until 1897 that this condition was shown to be due to fracture of the metatarsal shaft and hence termed a ‘‘march fracture’’.6 Previously reported in military recruits, sports and recreational injuries now account for up to 10% of patients in a typical sports medicine practice.7 Prospective studies indicate an incidence of stress fractures that reaches 31% in soldiers8 and 21% in athletes.9 Risk factors implicated in such injuries can be extrinsic or intrinsic (Table 1).10
Insufficiency fracture Bone strength depends on factors such as elasticity and stiffness, which are in turn related to bone mineral density, bone composition, and bone structure. Any process that can affect these parameters could also alter bone resistance and favour development of fracture. Conditions predisposing to insufficiency fractures are listed in Table 2.11,12 Stress fractures are most common in the lower extremity, especially the tibia, metatarsals and fibula. They may also occur in the pelvis and nonweight bearing bones including the ribs and upper limb.5 The distribution of bone stress injuries depends upon the type and level of activity as well as the patient population (Table 3). In athletes the distribution differs from that in military
0009-9260/$ - see front matter ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2007.02.018
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Table 1 Commonly implicated extrinsic and intrinsic factors in fatigue fracture
Table 3 Site of stress fracture and association with physical activity
Extrinsic factors
Intrinsic factors
Activity
Common sites of stress fracture
1. Excessive load on the body 2. Training errors 3. Unsuitable environmental conditions 4. Poor training equipment 5. Ineffective training rules
1. Malalignments (e.g., pes planus, tibia vara) 2. Leg length discrepancy 3. Tarsal coalition
Long-distance running
Femur: neck and shaft Tibiaa: plateau and shaft Fibula Pubic ramus Metatarsal Calcaneus Navicular Pubic ramus Femur: neck Tibia: shaft Fibula Metatarsala Sesamoid bones of the foot Talus Pars interarticularisa Ulna Pars interarticularisa Humerus Olecranon Ulna Metatarsala Ribs
Military marching 4. Previous surgery 5. Muscle weakness or imbalance 6. Overweight
recruits. The tibia and shaft of femur are the commonest sites of stress injury in athletes who run. The metatarsal shaft and the femoral neck are the sites typically stressed by marching.13
Sprinting Ballet
Pole vaulting Gymnastics Racquet sports/throwing
Pathomechanics of stress injury Bone is a dynamic tissue that requires stress for normal development and continually remodels itself in response to changes in the distribution and quantity of stresses through it. In this manner, bone is able to optimally adapt to its new mechanical environment (Wolf’s law of transformation).5 The persistent overuse of bone unaccustomed to such forces causes the development of microscopic trabecular fractures. These micro-fractures stimulate local osteoclast-mediated periosteal resorption, peaking at approximately 3 weeks, and characterized by local hyperaemia and oedema. Simultaneously, but proceeding at a lower rate, the resorbed bone is replaced by new stronger lamellar bone being laid down along the lines of stress, taking at least 12 weeks. The resultant imbalance leads to a transient weakening of the cortex, which if left to rest will heal, but if stressed further will worsen and eventually fail. The term ‘‘stress response’’ refers to the pre-failure events occurring at a cellular level that result in structural Table 2
Conditions predisposing to insufficiency fractures
Osteoporosis of any cause Rheumatoid arthritis Osteomalacia or rickets Diabetes mellitus Fibrous dysplasia Paget’s disease Pyrophosphate arthropathy Osteogenesis imperfecta Osteopetrosis Hyperparathyroidism Scurvy Irradiation
Dancing Rowing/golf
Modified from14. a The commonest site of stress fracture.
bone weakening, and therefore, represents a physiological continuum from normal to maladaptive remodelling.14 A stress fracture can be considered as the final consequence of the preceding events. Stress responses of bone are best distinguished from stress fracture by the absence of a fracture line.15
Clinical presentation The classic clinical presentation of SRBI is localized pain initiated and exacerbated by a certain activity and relieved by rest. Examination findings include localized tenderness, warmth, and swelling.16 Treatment is mainly medical, by optimizing nutrition, excluding endocrine abnormalities, and most importantly, modifying activities to allow the stressed bone time to rest. By allowing the repair process to dominate over resorption most fractures heal in 6e8 weeks, although certain sites, such as pubic ramus injuries, may need 2e5 months.17
Imaging of stress fractures Imaging plays an important role in confirming the diagnosis of stress injury. The development of stress fractures is a continuous process, and
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therefore, has a variable appearance, depending on the timing of the investigation.11 It is important to avoid biopsy of a potential stress fracture, as the biopsy specimen may contain immature cells and osteoid tissue related to the healing process, which could lead to a mistaken diagnosis of malignancy.5 The usual imaging options in stress fracture are plain radiography, bone scintigraphy, computed tomography, and magnetic resonance imaging (MRI). Recently the use of ultrasound has also been described.18
stress injury. Computed tomography (Fig. 1c) is less sensitive than bone scintigraphy or MRI in the early detection of stress injury. However, it is useful in areas where plain radiography is limited, and is more sensitive than either radiographs or MRI for the detection of cortical fracture lines. CT is thus well suited to demonstrate stress fractures of the sacrum, pars interarticularis, tarsal navicular, and longitudinal stress fractures of the tibia.14
Imaging options
MRI is extremely sensitive in the detection of pathophysiological soft-tissue, bone, and marrow changes associated with stress injuries. It allows depiction of abnormalities weeks before the development of a radiographic lesion and has comparable sensitivity and superior specificity to scintigraphy. In addition to bony changes, it also details information about the surrounding muscular or ligamentous insults associated with or responsible for symptoms.14 In the evaluation of stress injury, MRI should include an oedema-sensitive sequence to detect early changes of stress reaction, such as STIR (short tau inversion recovery) or fat-suppressed T2-weighted images (WIs). A T1WI better depicts
Plain radiography (Fig. 1a) is often the first technique used in the investigation of stress fractures, but the sensitivity is poor, generally revealing a range of relatively late skeletal responses from endosteal or periosteal reactions to frank fractures. Early radiographs are often normal with detection rates as low as 15%, and serial examinations are diagnostic in only 50% of cases.19 Triple-phase bone scintigraphy (Fig. 1b) detects the osteoblastic activity associated with remodelling and is highly sensitive in detecting stress injury. Despite its high sensitivity, bone scintigraphy lacks specificity; infection, osteonecrosis, and tumours can all mimic
MRI
Figure 1 Plain radiograph (a), scintigraphy (b), and computed tomography (c) in a patient with stress fracture of fifth metatarsal.
Stress-related bone injuries with emphasis on MRI
anatomy and more advanced fractures. Contrast studies are not considered essential as STIR and contrast-enhanced, fat-suppressed T1WIs demonstrate identical imaging patterns (Fig. 2).20,21 This sensitivity of MRI relies on the ability to detect early bone marrow oedema, the hallmark of the stress response.17,22 A grading system developed by Kiuru et al.23 (Table 4) demonstrates how the sequential detection of oedema using STIR, T2WIs and T1WIs increases as the severity of the stress response increases. Early (grade 1) injuries are visible on STIR sequences alone (Fig. 3); whereas more advanced grade 2 and 3 injuries (Figs. 2 and 4) are conspicuous on all sequences. True (grade 4) stress fractures are seen as focal linear areas of low signal on T1 and T2WIs (Fig. 5). The fracture line is typically orientated perpendicular to the cortex and extends into the medullary space. The classification system by Arendt et al.15 (Table 5) takes into consideration the plain radiographic, scintigraphic, and MRI findings. It is based on particular MRI sequences and grades 1 and 2 both represent the same degree of stress reaction. The grading system by Kiuru et al. is clearly based on the extent of bone involvement on MRI in stress-related injury, is easier to use in routine practice, and is preferable to the older
Figure 2 Coronal STIR (a) and gadolinium-enhanced, T1-weighted (b) MRI images of the fibula with a grade 3 stress injury. Both sequences show identical information, including endosteal (arrow), periosteal, and surrounding muscle oedema (arrowheads).
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Table 4 injuries23
Magnetic resonance imaging grading of stress
Grade
Magnetic resonance imaging findings
I II III IV V
Endosteal oedema Periosteal and endosteal oedema Muscle, periosteal and endosteal oedema Fracture line Callus at the endosteal and/or periosteal surface of cortical bone
classification system by Arendt et al. In these grading systems, the effectiveness of MRI to differentiate between the early stress response and late stress fracture enables an estimation of the degree of disability and the period required for healing. MRI is also useful in the follow-up of healing stress fractures (Fig. 6). Stress fractures show resolution of abnormally bright STIR signal intensity within 6 months of the first imaging study in about 90% of cases.24 At this time patients are asymptomatic. It may be hypothesized that if the patient were to be imaged after this time, a diffuse bright signal would be abnormal, and in a patient with new or increased symptoms, this would represent a new injury.24 The low signal intensity on T1WIs may persist even after the disappearance of oedema on STIR and is consistent with sclerosis. The occasional late finding of
Figure 3 Sagittal, STIR MRI image of the tibia revealing endosteal oedema (arrows) without any associated periosteal response consistent with a grade 1 stress injury.
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Figure 4 Same patient as in Fig. 1. Sagittal STIR (a) and T1-weighted (b) MRI images of the second metatarsal showing grade 2 stress responses comprising of endosteal (arrows) and periosteal (arrowhead) oedema but no surrounding soft-tissue inflammation.
increased signal intensity on T1WIs around the injury site is likely to represent fatty marrow replacement, especially in the femoral neck, which is normally composed of haematopoietic marrow.25,26
Specific sites Tibia The tibia is the most commonly involved bone, primarily due to the increased prevalence of running. Tibial stress fractures typically occur in the proximal or mid shaft and usually display a horizontal or oblique orientation (Fig. 7).13 The activityrelated lower leg pain is typically associated with diffuse tenderness along the posteromedial tibia Table 5
Figure 5 Coronal, fat-suppressed, T2-weighted image of the navicular demonstrating a well-defined incomplete fracture line in the central third (arrow) without any cortical response (grade 4).
in its middle to distal aspect and various terms such as shin splints syndrome, soleus syndrome, and medial tibial stress syndrome have been applied to describe this.27,28 Four MRI patterns have been described in two different studies by Anderson et al.29 and Fredericson et al.,17 who demonstrated a continuum of changes on MRI images in patients with activity-related leg pain, including (1) normal appearance, (2) periosteal fluid, (3) bone marrow oedema, and (4) stress fracture, all of which concurred with findings on bone scintigraphy. These studies concluded that MRI (Fig. 7a) should be preferred over triple-phase bone scintigraphy for acute symptoms in shin splint syndrome, whereas in chronic cases scintigraphy (Fig. 7b) takes precedence. This suggestion was largely based on a large number of normal MRI studies in patients with
Radiological grading of stress fractures15 Plain radiography
Bone scintigraphy
Magnetic resonance imaging
Treatment
Grade 1
Normal
Positive STIR
3 weeks rest
Grade 2 Grade 3
Normal Discrete line or periosteal reaction Fracture or periosteal reaction
Poorly defined area of increased activity More intense but still poorly defined Sharply marginated area of increased activity (focal or fusiform) More intense transcortical localized uptake
Positive STIR and T2WI Positive T1WI and T2WI but without definite cortical break Positive T1WI and T2WI with fracture line
3e6 weeks rest 12e16 weeks rest
Grade 4
STIR, short Tau inversion recovery; T2WI, T2-weighted image, T1WI, T1-weighted image.
>16 weeks rest
Stress-related bone injuries with emphasis on MRI
Figure 6 Coronal STIR MRI image of the tibia demonstrating grade 5 stress response with callus formation involving the periosteal (arrow) and endosteal (arrowhead) surface of the cortex.
chronic symptoms. Longitudinal stress fractures have been described and may account for up to 10% of tibial stress fractures. MRI demonstrates extensive diaphyseal oedema and periostitis, and a fracture line may be evident on axial images (Fig. 8), otherwise thin-section CT should be performed.30
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Figure 7 Classical longitudinal stress fracture of tibia. Coronal, T1-weighted MRI image (a) demonstrates the extent of endosteal (black arrows) and periosteal response (white arrowhead). Bone scintigraphy (b) showing increased uptake in the same distribution.
Foot Metatarsals Among the metatarsal bones, stress fractures involving the middle and distal portions of the second and third metatarsal shafts are most common (Fig. 4). Stress fractures at the base of first or second metatarsals (or, rarely, other metatarsal bones) are less frequent.31
Talus In the talus, the classic pattern of stress fracture is linear bone oedema perpendicular to the trabecular flow, paralleling the talonavicular articulation at the talar neck. Rarely, vertically or horizontally oriented insufficiency fractures of the medial
Figure 8 Same patient as in Fig. 7. A clear fracture line (white arrowhead) is seen on the T2-weighted, fat-suppressed axial image with a moderate degree of periosteal response (black arrows).
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aspect of the postero-inferior talus or transverse (horizontal) fracture of the talar body have been described.32
Calcaneum Stress fracture of calcaneum is often seen in jumpers and is due to the associated axial compression forces. It most commonly involves the dorsal posterior aspect and is frequently bilateral (Fig. 9).21 Insufficiency fracture of the posterior calcaneum is also described in diabetics.
Navicular Tarsal navicular stress fractures are commonly seen in physically active individuals, especially
Figure 9 T1-weighted (a) and sagittal STIR (b) MRI images of the calcaneum showing a fracture line (arrows) with surrounding marrow oedema (arrowheads).
A.P. Datir et al.
basketball players and runners. The fractures are linearly oriented, in the sagittal plane in the central third of the navicular, and can be complete or partial (Fig. 5). These fractures are often complicated by slow healing, delayed union or nonunion, osteonecrosis of the lateral fragment, and refracture.21
Pelvis and proximal femur In this region, about 60% of stress injuries are located in the proximal femur, of which 67% are located in the femoral neck (Fig. 10), 32% in the proximal femoral shaft, and 1% in the femoral head. About 40% of stress injuries in this region are located the pelvis with the following distribution: sacrum 41%, inferior pubic ramus 49%, superior pubic ramus 4%, iliac bone 4%, and acetabulum 1%.33 Sacral stress fractures are caused by stress concentration of vertical body forces that are dissipated from the spine to the sacrum and then onto the sacral ala. The clinical presentation of runners with sacral stress fractures can mimic disk disease. MRI shows unilateral low signal intensity in a vertical and linear orientation in the lateral aspect of the sacrum, parallel to the sacroiliac joint on T1WIs and corresponding high signal on T2WIs or
Figure 10 Coronal STIR MRI image showing a stress fracture in the proximal femoral neck region.
Stress-related bone injuries with emphasis on MRI
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STIR images (Fig. 11). Although MRI is highly sensitive in the detection of early sacral insufficiency fractures, diagnosis may be difficult, and CT or even bone scintigraphy are often required. This is particularly true in patients with pelvic cavity tumours who have undergone radiotherapy. Recently, the important finding of fluid within the fracture itself has been described and is considered to be highly suggestive of the diagnosis of sacral insufficiency fractures, especially if they co-exist with concomitant fractures of the pubis and ilium.34 Para-acetabular insufficiency fractures are particularly difficult to diagnose, if not suspected, as they are often radiographically subtle and easily Figure 12 Coronal T1-weighted MRI image showing a stress fracture of the acetabulum (arrow) in a patient with previous radiotherapy for carcinoma.
overlooked. On MRI, para-acetabular insufficiency fractures have a typical appearance and location with the fracture line being curvilinear and parallel to the acetabular roof in most cases (Fig. 12). Sometimes, a less common pattern of linear fracture line running obliquely in the acetabular region can be seen.34
Differential diagnosis of stress fracture The diagnosis of stress fractures should be readily apparent when a specific activity leads to signs and symptoms in an area typical for stress fracture. Sometimes, the patient cannot recall such specific activity in association with the onset of signs and symptoms. The differential diagnoses of stress fractures include osteoid osteoma, acute and chronic sclerosing osteomyelitis, osteomalacia, metastasis, osteosarcoma, and Ewing’s tumour. Most tumours are discernable on MRI by their mass effect, although those involving the marrow (myeloma, lymphoma, leukaemia) may be more difficult. Advanced osteomyelitis may be distinguished by the presence of a sequestrum or abscess, but the clinical presentation is most important in the early stages.10
Conclusion Figure 11 Coronal oblique T1-weighted (a) and STIR (b) MRI images demonstrating typical findings of stress fractures of sacrum at different stages. A well-defined fracture line (black arrow) with surrounding oedema (black arrowheads) is seen in the right sacral ala, while healing of a left sacral stress fracture has resulted in replacement by fatty marrow (white arrows).
In most of the cases with suspicion of SRBI, an accurate clinical history with examination and serial plain radiographs establishes the diagnosis. However, it is the earlier detection of stress injury that allows rest and avoids progression to true fracture. MRI is more sensitive than two-phase
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bone scintigraphy, and should be used as the gold standard in the assessment of stress injuries of bone. The detection of oedema on MRI also helps to define the age of the injury. The MRI grading system devised by Kiuru et al.23 is not only easily understood by the radiologist and the clinician, but also allows a more accurate determination of the period of rest required for healing.15
References 1. Devas MB. Stress fractures. London: Churchill Livingstone; 1975. 2. Daffner RH. Stress fractures: current concepts. Skeletal Radiol 1978;2:221e9. 3. Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15:46e58. 4. Wilson ES, Katz FN. Stress fractures: an analysis of 250 consecutive cases. Radiology 1969;92:481e6. 5. Bennell KL, Malcolm SA, Thomas SA, et al. The incidence and distribution of stress fractures in competitive track and field athletes. Am J Sports Med 1974;2:189e98. 6. Knapp TP, Garrett WE. Stress fractures: general concepts. Clin Sports Med 1997;16:339e56. 7. Hulkko A, Orava S. Stress fractures in the athletes. Int J Sports Med 1987;8:221e6. 8. Milgrom C, Giladi M, Stein M, et al. Stress fractures in military recruits. A prospective study showing an unusually high incidence. J Bone Joint Surg Br 1985;67:732e5. 9. Lassus J, Tulikoura I, Konttinen Y, et al. Bone stress injuries of the lower extremity: a review. Acta Orthop Scand 2002; 73:359e68. 10. Daffner RH, Pavlov H. Stress fractures: current concepts. AJR Am J Roentgenol 1992;159:245e52. 11. Pentecost RL, Murray RA, Brindley HH. Fatigue, insufficiency, and pathologic fractures. J Am Med Assoc 1964; 187:1001e4. 12. Peris P. Stress fractures. Best Pract Res Clin Rheumatol 2003;17:1043e61. 13. Bennell KL, Brukner PD. Epidemiology and site specificity of stress fractures. Clin Sports Med 1997;16:179e96. 14. Spitz DJ, Newberg AH. Imaging of stress fractures in the athlete. Radiol Clin North Am 2002;40:313e31. 15. Arendt EA, Griffiths HJ. The use of MR imaging in the assessment and clinical management of stress reactions of bone in high performance athletes. Clin Sports Med 1997;16:291e306. 16. Matin P. The appearance of bone scans following fractures including intermediate and long-term studies. J Nucl Med 1979;20:1227e31.
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17. Fredericson M, Bergman G, Hoffman KL, et al. Tibial stress reaction in runners: correlation of clinical symptoms and scintigraphy with a new magnetic resonance imaging grading system. Am J Sports Med 1995;23:472e81. 18. Bodner G, Stockl B, Fierlinger A, et al. Sonographic findings in the stress fractures of the lower limb: preliminary findings. Eur Radiol 2005;15:356e9. 19. Griffiths HJ, Priest DR, Rector BE, et al. Bone bruises: their aetiology and importance. Imaging 1995;7:286e90. 20. Schmid MR, Hodler J, Vienne P, et al. Bone marrow abnormalities of foot and ankle: STIR versus T1-weighted contrastenhanced fat-suppressed spin-echo MR imaging. Radiology 2002;224:463e9. 21. Muthukumar T, Butt S, Cassar-Pullicino V. Stress fractures and related disorders in foot and ankle: plain films, scintigraphy, CT and MR imaging. Semin Musculoskelet Radiol 2005;9:210e26. 22. Anderson MW, Greenspan A. Stress fractures. Radiology 1996;199:1e12. 23. Kiuru M, Pihlajamaki HK, Ahovuo J. Fatigue stress injuries of the pelvic bones and proximal femur: evaluation with MR imaging. Eur Radiol 2003;13:605e11. 24. Slocum KA, Gorman JD, Puckett ML, et al. Resolution of abnormal MR signal intensity in patients with stress fractures of the femoral neck. AJR Am J Roentgenol 1997; 168:1295e9. 25. Vogler JB, Murphy WA. Bone marrow imaging. Radiology 1988;168:679e93. 26. Wilson AJ, Murphy WA, Hardy DC, et al. Transient osteoporosis: transient bone marrow edema. Radiology 1988;167: 757e60. 27. Batt ME. Shin splints: a review of terminology. Clin J Sport Med 1995;5:53e7. 28. Michael RH, Holder LE. The soleus syndrome: a cause of medial tibial stress (shin splints). Am J Sports Med 1985; 13:87e94. 29. Anderson MW, Ugalde V, Batt M, et al. Shin splints: MR appearance in a preliminary study. Radiology 1997;204: 177e80. 30. Anderson MW, Ugalde V, Batt M, et al. Longitudinal stress fracture of tibia: MR demonstration. J Comput Assist Tomogr 1996;20:836e8. 31. Chowchuen P, Resnick D. Stress fractures of the metatarsal heads. Skeletal Radiol 1998;27:22e5. 32. Umans H, Pavlov H. Insufficiency fracture of the talus: diagnosis with MR imaging. Radiology 1995;197:439e42. 33. Peh WCG. Intrafracture fluid: a new diagnostic sign of insufficiency fractures of the sacrum and ilium. Br J Radiol 2000; 73:895e8. 34. Theodorou SJ, Theodorou DJ, Schweitzer ME, et al. Magnetic resonance imaging of para-acetabular insufficiency fractures in patient with malignancy. Clin Radiol 2006;61: 181e90.
PICTORIAL REVIEW
Stress-related bone injuries with emphasis on MRI A.P. Datir*, A. Saini, A. Connell, A. Saifuddin Department of Radiology, Royal National Orthopaedic Hospital, Brockley Hill, Stanmore Middlesex, London HA7 4LP, UK Received 14 May 2006; received in revised form 14 February 2007; accepted 19 February 2007
Stress-related bone injuries are common in professional athletes and in military personnel. However, in an increasingly health conscious society undertaking more, and often unsupervised, exercise regimes, these injuries may increase. Early diagnosis is of paramount importance to detect the signs of stress reaction, allow healing, and prevent progression to frank fracture. This review illustrates the classical magnetic resonance imaging (MRI) features of stress injury and fracture with emphasis on its role in the diagnosis and follow-up, as well as its limitations. ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Stress-related bone injuries (SRBI) occur in normal or abnormal bone that is subjected to repeated trauma with a load less than that which causes acute fracture. Stress fractures can be sub-grouped into two types: insufficiency fracture and fatigue fracture. A fatigue fracture is caused by the application of abnormal muscular stress or torque to a bone that has normal elastic resistance. The following triad is associated with most fatigue fractures: the activity is (1) new or different for the person, (2) strenuous, and (3) repeated with a frequency that ultimately produces signs and symptoms.1e4 An insufficiency fracture results when normal or physiological muscular activity is applied to a bone that is deficient in mineral or elastic resistance.5
Aetiology and distribution Fatigue fracture The first recording of stress related injury was in 1855 by Briethaupt, a Prussian military physician, * Guarantor and correspondent: A.P. Datir, Department of Radiology, Royal National Orthopaedic Hospital, Stanmore, Middlesex HA7 4LP, UK. Tel.: þ44 208 864 3232; fax: þ44 208 869 3907. E-mail address: [email protected] (A.P. Datir).
who recorded the painful swollen feet of marching soldiers. It was not until 1897 that this condition was shown to be due to fracture of the metatarsal shaft and hence termed a ‘‘march fracture’’.6 Previously reported in military recruits, sports and recreational injuries now account for up to 10% of patients in a typical sports medicine practice.7 Prospective studies indicate an incidence of stress fractures that reaches 31% in soldiers8 and 21% in athletes.9 Risk factors implicated in such injuries can be extrinsic or intrinsic (Table 1).10
Insufficiency fracture Bone strength depends on factors such as elasticity and stiffness, which are in turn related to bone mineral density, bone composition, and bone structure. Any process that can affect these parameters could also alter bone resistance and favour development of fracture. Conditions predisposing to insufficiency fractures are listed in Table 2.11,12 Stress fractures are most common in the lower extremity, especially the tibia, metatarsals and fibula. They may also occur in the pelvis and nonweight bearing bones including the ribs and upper limb.5 The distribution of bone stress injuries depends upon the type and level of activity as well as the patient population (Table 3). In athletes the distribution differs from that in military
0009-9260/$ - see front matter ª 2007 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2007.02.018
Stress-related bone injuries with emphasis on MRI
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Table 1 Commonly implicated extrinsic and intrinsic factors in fatigue fracture
Table 3 Site of stress fracture and association with physical activity
Extrinsic factors
Intrinsic factors
Activity
Common sites of stress fracture
1. Excessive load on the body 2. Training errors 3. Unsuitable environmental conditions 4. Poor training equipment 5. Ineffective training rules
1. Malalignments (e.g., pes planus, tibia vara) 2. Leg length discrepancy 3. Tarsal coalition
Long-distance running
Femur: neck and shaft Tibiaa: plateau and shaft Fibula Pubic ramus Metatarsal Calcaneus Navicular Pubic ramus Femur: neck Tibia: shaft Fibula Metatarsala Sesamoid bones of the foot Talus Pars interarticularisa Ulna Pars interarticularisa Humerus Olecranon Ulna Metatarsala Ribs
Military marching 4. Previous surgery 5. Muscle weakness or imbalance 6. Overweight
recruits. The tibia and shaft of femur are the commonest sites of stress injury in athletes who run. The metatarsal shaft and the femoral neck are the sites typically stressed by marching.13
Sprinting Ballet
Pole vaulting Gymnastics Racquet sports/throwing
Pathomechanics of stress injury Bone is a dynamic tissue that requires stress for normal development and continually remodels itself in response to changes in the distribution and quantity of stresses through it. In this manner, bone is able to optimally adapt to its new mechanical environment (Wolf’s law of transformation).5 The persistent overuse of bone unaccustomed to such forces causes the development of microscopic trabecular fractures. These micro-fractures stimulate local osteoclast-mediated periosteal resorption, peaking at approximately 3 weeks, and characterized by local hyperaemia and oedema. Simultaneously, but proceeding at a lower rate, the resorbed bone is replaced by new stronger lamellar bone being laid down along the lines of stress, taking at least 12 weeks. The resultant imbalance leads to a transient weakening of the cortex, which if left to rest will heal, but if stressed further will worsen and eventually fail. The term ‘‘stress response’’ refers to the pre-failure events occurring at a cellular level that result in structural Table 2
Conditions predisposing to insufficiency fractures
Osteoporosis of any cause Rheumatoid arthritis Osteomalacia or rickets Diabetes mellitus Fibrous dysplasia Paget’s disease Pyrophosphate arthropathy Osteogenesis imperfecta Osteopetrosis Hyperparathyroidism Scurvy Irradiation
Dancing Rowing/golf
Modified from14. a The commonest site of stress fracture.
bone weakening, and therefore, represents a physiological continuum from normal to maladaptive remodelling.14 A stress fracture can be considered as the final consequence of the preceding events. Stress responses of bone are best distinguished from stress fracture by the absence of a fracture line.15
Clinical presentation The classic clinical presentation of SRBI is localized pain initiated and exacerbated by a certain activity and relieved by rest. Examination findings include localized tenderness, warmth, and swelling.16 Treatment is mainly medical, by optimizing nutrition, excluding endocrine abnormalities, and most importantly, modifying activities to allow the stressed bone time to rest. By allowing the repair process to dominate over resorption most fractures heal in 6e8 weeks, although certain sites, such as pubic ramus injuries, may need 2e5 months.17
Imaging of stress fractures Imaging plays an important role in confirming the diagnosis of stress injury. The development of stress fractures is a continuous process, and
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therefore, has a variable appearance, depending on the timing of the investigation.11 It is important to avoid biopsy of a potential stress fracture, as the biopsy specimen may contain immature cells and osteoid tissue related to the healing process, which could lead to a mistaken diagnosis of malignancy.5 The usual imaging options in stress fracture are plain radiography, bone scintigraphy, computed tomography, and magnetic resonance imaging (MRI). Recently the use of ultrasound has also been described.18
stress injury. Computed tomography (Fig. 1c) is less sensitive than bone scintigraphy or MRI in the early detection of stress injury. However, it is useful in areas where plain radiography is limited, and is more sensitive than either radiographs or MRI for the detection of cortical fracture lines. CT is thus well suited to demonstrate stress fractures of the sacrum, pars interarticularis, tarsal navicular, and longitudinal stress fractures of the tibia.14
Imaging options
MRI is extremely sensitive in the detection of pathophysiological soft-tissue, bone, and marrow changes associated with stress injuries. It allows depiction of abnormalities weeks before the development of a radiographic lesion and has comparable sensitivity and superior specificity to scintigraphy. In addition to bony changes, it also details information about the surrounding muscular or ligamentous insults associated with or responsible for symptoms.14 In the evaluation of stress injury, MRI should include an oedema-sensitive sequence to detect early changes of stress reaction, such as STIR (short tau inversion recovery) or fat-suppressed T2-weighted images (WIs). A T1WI better depicts
Plain radiography (Fig. 1a) is often the first technique used in the investigation of stress fractures, but the sensitivity is poor, generally revealing a range of relatively late skeletal responses from endosteal or periosteal reactions to frank fractures. Early radiographs are often normal with detection rates as low as 15%, and serial examinations are diagnostic in only 50% of cases.19 Triple-phase bone scintigraphy (Fig. 1b) detects the osteoblastic activity associated with remodelling and is highly sensitive in detecting stress injury. Despite its high sensitivity, bone scintigraphy lacks specificity; infection, osteonecrosis, and tumours can all mimic
MRI
Figure 1 Plain radiograph (a), scintigraphy (b), and computed tomography (c) in a patient with stress fracture of fifth metatarsal.
Stress-related bone injuries with emphasis on MRI
anatomy and more advanced fractures. Contrast studies are not considered essential as STIR and contrast-enhanced, fat-suppressed T1WIs demonstrate identical imaging patterns (Fig. 2).20,21 This sensitivity of MRI relies on the ability to detect early bone marrow oedema, the hallmark of the stress response.17,22 A grading system developed by Kiuru et al.23 (Table 4) demonstrates how the sequential detection of oedema using STIR, T2WIs and T1WIs increases as the severity of the stress response increases. Early (grade 1) injuries are visible on STIR sequences alone (Fig. 3); whereas more advanced grade 2 and 3 injuries (Figs. 2 and 4) are conspicuous on all sequences. True (grade 4) stress fractures are seen as focal linear areas of low signal on T1 and T2WIs (Fig. 5). The fracture line is typically orientated perpendicular to the cortex and extends into the medullary space. The classification system by Arendt et al.15 (Table 5) takes into consideration the plain radiographic, scintigraphic, and MRI findings. It is based on particular MRI sequences and grades 1 and 2 both represent the same degree of stress reaction. The grading system by Kiuru et al. is clearly based on the extent of bone involvement on MRI in stress-related injury, is easier to use in routine practice, and is preferable to the older
Figure 2 Coronal STIR (a) and gadolinium-enhanced, T1-weighted (b) MRI images of the fibula with a grade 3 stress injury. Both sequences show identical information, including endosteal (arrow), periosteal, and surrounding muscle oedema (arrowheads).
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Table 4 injuries23
Magnetic resonance imaging grading of stress
Grade
Magnetic resonance imaging findings
I II III IV V
Endosteal oedema Periosteal and endosteal oedema Muscle, periosteal and endosteal oedema Fracture line Callus at the endosteal and/or periosteal surface of cortical bone
classification system by Arendt et al. In these grading systems, the effectiveness of MRI to differentiate between the early stress response and late stress fracture enables an estimation of the degree of disability and the period required for healing. MRI is also useful in the follow-up of healing stress fractures (Fig. 6). Stress fractures show resolution of abnormally bright STIR signal intensity within 6 months of the first imaging study in about 90% of cases.24 At this time patients are asymptomatic. It may be hypothesized that if the patient were to be imaged after this time, a diffuse bright signal would be abnormal, and in a patient with new or increased symptoms, this would represent a new injury.24 The low signal intensity on T1WIs may persist even after the disappearance of oedema on STIR and is consistent with sclerosis. The occasional late finding of
Figure 3 Sagittal, STIR MRI image of the tibia revealing endosteal oedema (arrows) without any associated periosteal response consistent with a grade 1 stress injury.
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Figure 4 Same patient as in Fig. 1. Sagittal STIR (a) and T1-weighted (b) MRI images of the second metatarsal showing grade 2 stress responses comprising of endosteal (arrows) and periosteal (arrowhead) oedema but no surrounding soft-tissue inflammation.
increased signal intensity on T1WIs around the injury site is likely to represent fatty marrow replacement, especially in the femoral neck, which is normally composed of haematopoietic marrow.25,26
Specific sites Tibia The tibia is the most commonly involved bone, primarily due to the increased prevalence of running. Tibial stress fractures typically occur in the proximal or mid shaft and usually display a horizontal or oblique orientation (Fig. 7).13 The activityrelated lower leg pain is typically associated with diffuse tenderness along the posteromedial tibia Table 5
Figure 5 Coronal, fat-suppressed, T2-weighted image of the navicular demonstrating a well-defined incomplete fracture line in the central third (arrow) without any cortical response (grade 4).
in its middle to distal aspect and various terms such as shin splints syndrome, soleus syndrome, and medial tibial stress syndrome have been applied to describe this.27,28 Four MRI patterns have been described in two different studies by Anderson et al.29 and Fredericson et al.,17 who demonstrated a continuum of changes on MRI images in patients with activity-related leg pain, including (1) normal appearance, (2) periosteal fluid, (3) bone marrow oedema, and (4) stress fracture, all of which concurred with findings on bone scintigraphy. These studies concluded that MRI (Fig. 7a) should be preferred over triple-phase bone scintigraphy for acute symptoms in shin splint syndrome, whereas in chronic cases scintigraphy (Fig. 7b) takes precedence. This suggestion was largely based on a large number of normal MRI studies in patients with
Radiological grading of stress fractures15 Plain radiography
Bone scintigraphy
Magnetic resonance imaging
Treatment
Grade 1
Normal
Positive STIR
3 weeks rest
Grade 2 Grade 3
Normal Discrete line or periosteal reaction Fracture or periosteal reaction
Poorly defined area of increased activity More intense but still poorly defined Sharply marginated area of increased activity (focal or fusiform) More intense transcortical localized uptake
Positive STIR and T2WI Positive T1WI and T2WI but without definite cortical break Positive T1WI and T2WI with fracture line
3e6 weeks rest 12e16 weeks rest
Grade 4
STIR, short Tau inversion recovery; T2WI, T2-weighted image, T1WI, T1-weighted image.
>16 weeks rest
Stress-related bone injuries with emphasis on MRI
Figure 6 Coronal STIR MRI image of the tibia demonstrating grade 5 stress response with callus formation involving the periosteal (arrow) and endosteal (arrowhead) surface of the cortex.
chronic symptoms. Longitudinal stress fractures have been described and may account for up to 10% of tibial stress fractures. MRI demonstrates extensive diaphyseal oedema and periostitis, and a fracture line may be evident on axial images (Fig. 8), otherwise thin-section CT should be performed.30
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Figure 7 Classical longitudinal stress fracture of tibia. Coronal, T1-weighted MRI image (a) demonstrates the extent of endosteal (black arrows) and periosteal response (white arrowhead). Bone scintigraphy (b) showing increased uptake in the same distribution.
Foot Metatarsals Among the metatarsal bones, stress fractures involving the middle and distal portions of the second and third metatarsal shafts are most common (Fig. 4). Stress fractures at the base of first or second metatarsals (or, rarely, other metatarsal bones) are less frequent.31
Talus In the talus, the classic pattern of stress fracture is linear bone oedema perpendicular to the trabecular flow, paralleling the talonavicular articulation at the talar neck. Rarely, vertically or horizontally oriented insufficiency fractures of the medial
Figure 8 Same patient as in Fig. 7. A clear fracture line (white arrowhead) is seen on the T2-weighted, fat-suppressed axial image with a moderate degree of periosteal response (black arrows).
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aspect of the postero-inferior talus or transverse (horizontal) fracture of the talar body have been described.32
Calcaneum Stress fracture of calcaneum is often seen in jumpers and is due to the associated axial compression forces. It most commonly involves the dorsal posterior aspect and is frequently bilateral (Fig. 9).21 Insufficiency fracture of the posterior calcaneum is also described in diabetics.
Navicular Tarsal navicular stress fractures are commonly seen in physically active individuals, especially
Figure 9 T1-weighted (a) and sagittal STIR (b) MRI images of the calcaneum showing a fracture line (arrows) with surrounding marrow oedema (arrowheads).
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basketball players and runners. The fractures are linearly oriented, in the sagittal plane in the central third of the navicular, and can be complete or partial (Fig. 5). These fractures are often complicated by slow healing, delayed union or nonunion, osteonecrosis of the lateral fragment, and refracture.21
Pelvis and proximal femur In this region, about 60% of stress injuries are located in the proximal femur, of which 67% are located in the femoral neck (Fig. 10), 32% in the proximal femoral shaft, and 1% in the femoral head. About 40% of stress injuries in this region are located the pelvis with the following distribution: sacrum 41%, inferior pubic ramus 49%, superior pubic ramus 4%, iliac bone 4%, and acetabulum 1%.33 Sacral stress fractures are caused by stress concentration of vertical body forces that are dissipated from the spine to the sacrum and then onto the sacral ala. The clinical presentation of runners with sacral stress fractures can mimic disk disease. MRI shows unilateral low signal intensity in a vertical and linear orientation in the lateral aspect of the sacrum, parallel to the sacroiliac joint on T1WIs and corresponding high signal on T2WIs or
Figure 10 Coronal STIR MRI image showing a stress fracture in the proximal femoral neck region.
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STIR images (Fig. 11). Although MRI is highly sensitive in the detection of early sacral insufficiency fractures, diagnosis may be difficult, and CT or even bone scintigraphy are often required. This is particularly true in patients with pelvic cavity tumours who have undergone radiotherapy. Recently, the important finding of fluid within the fracture itself has been described and is considered to be highly suggestive of the diagnosis of sacral insufficiency fractures, especially if they co-exist with concomitant fractures of the pubis and ilium.34 Para-acetabular insufficiency fractures are particularly difficult to diagnose, if not suspected, as they are often radiographically subtle and easily Figure 12 Coronal T1-weighted MRI image showing a stress fracture of the acetabulum (arrow) in a patient with previous radiotherapy for carcinoma.
overlooked. On MRI, para-acetabular insufficiency fractures have a typical appearance and location with the fracture line being curvilinear and parallel to the acetabular roof in most cases (Fig. 12). Sometimes, a less common pattern of linear fracture line running obliquely in the acetabular region can be seen.34
Differential diagnosis of stress fracture The diagnosis of stress fractures should be readily apparent when a specific activity leads to signs and symptoms in an area typical for stress fracture. Sometimes, the patient cannot recall such specific activity in association with the onset of signs and symptoms. The differential diagnoses of stress fractures include osteoid osteoma, acute and chronic sclerosing osteomyelitis, osteomalacia, metastasis, osteosarcoma, and Ewing’s tumour. Most tumours are discernable on MRI by their mass effect, although those involving the marrow (myeloma, lymphoma, leukaemia) may be more difficult. Advanced osteomyelitis may be distinguished by the presence of a sequestrum or abscess, but the clinical presentation is most important in the early stages.10
Conclusion Figure 11 Coronal oblique T1-weighted (a) and STIR (b) MRI images demonstrating typical findings of stress fractures of sacrum at different stages. A well-defined fracture line (black arrow) with surrounding oedema (black arrowheads) is seen in the right sacral ala, while healing of a left sacral stress fracture has resulted in replacement by fatty marrow (white arrows).
In most of the cases with suspicion of SRBI, an accurate clinical history with examination and serial plain radiographs establishes the diagnosis. However, it is the earlier detection of stress injury that allows rest and avoids progression to true fracture. MRI is more sensitive than two-phase
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bone scintigraphy, and should be used as the gold standard in the assessment of stress injuries of bone. The detection of oedema on MRI also helps to define the age of the injury. The MRI grading system devised by Kiuru et al.23 is not only easily understood by the radiologist and the clinician, but also allows a more accurate determination of the period of rest required for healing.15
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