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Intra-epiphyseal stress injury of the proximal tibial epiphysis: Preliminary experience of magnetic resonance imaging findings
European Journal of Radiology 83 (2014) 2051–2057
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Intra-epiphyseal stress injury of the proximal tibial epiphysis: Preliminary experience of magnetic resonance imaging findings G. Tony a,1 , A. Charran b,2 , B. Tins e,3 , R. Lalam e,3 , P.N.M. Tyrrell e,3 , J. Singh e,3 , P. Cool d,4 , N. Kiely c,4 , V.N. Cassar-Pullicino e,∗ a
Stafford General Hospital, Weston Road, Stafford, Staffordshire ST16 3SA, UK Hillingdon Hospital, Pield Heath Rd, Uxbridge, Middlesex UB8 3NN, UK c Paediatric Orthopaedics, Robert Jones and Agnes Hunt, Orthopaedic Hospital, Oswestry, Shropshire SY10 7 AG, UK d Orthopaedic Oncology, Robert Jones and Agnes Hunt, Orthopaedic Hospital, Oswestry, Shropshire SY10 7 AG, UK e Department of Diagnostic Imaging, Robert Jones and Agnes Hunt, Orthopaedic Hospital, Oswestry, Shropshire SY10 7 AG, UK b
a r t i c l e
i n f o
Article history: Received 23 May 2014 Received in revised form 31 July 2014 Accepted 8 August 2014 Keywords: Stress injury Proximal tibial epiphysis MRI
a b s t r a c t Stress induced injuries affecting the physeal plate or cortical bone in children and adolescents, especially young athletes, have been well described. However, there are no reports in the current English language literature of stress injury affecting the incompletely ossified epiphyseal cartilage. We present four cases of stress related change to the proximal tibial epiphysis (PTE) along with their respective magnetic resonance imaging (MRI) appearances ranging from subtle oedema signal to a pseudo-tumour like appearance within the epiphyseal cartilage. The site and pattern of intra-epiphyseal injury is determined by the type of tissue that is affected, the maturity of the skeleton and the type of forces that are transmitted through the tissue. We demonstrate how an awareness of the morphological spectrum of MRI appearances in intra-epiphyseal stress injury and the ability to identify concomitant signs of stress in other nearby structures can help reduce misdiagnosis, avoid invasive diagnostic procedures like bone biopsy and reassure patients and their families. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Stress-induced injury to the immature skeleton has been well documented [1–4] and in some cases a pseudo-tumour like appearance has been described in children and adolescents as a result of a high levels of sporting activity [5–7]. Stress or overuse related injuries are particularly common within the proximal tibia and can mimic infection [8] or tumour [8–10]. To our knowledge, there are no reports in the English language literature of stress-induced injury to the incompletely ossified epiphysis. We present our
∗ Corresponding author. Tel.: +44 1691404189; fax: +44 1691404170. E-mail addresses: [email protected] (G. Tony), [email protected] (A. Charran), [email protected] (B. Tins), [email protected] (R. Lalam), [email protected] (P.N.M. Tyrrell), [email protected] (J. Singh), [email protected] (P. Cool), [email protected] (N. Kiely), [email protected] (V.N. Cassar-Pullicino). 1 Tel.: +44 07960146176. 2 Tel.: +44 07894282366. 3 Tel.: +44 01691404189. 4 Tel.: +44 01691404000. http://dx.doi.org/10.1016/j.ejrad.2014.08.008 0720-048X/© 2014 Elsevier Ireland Ltd. All rights reserved.
experience of the MRI findings in chronic/repetitive stress injury to the proximal tibial epiphysis (PTE) in four different adolescents each demonstrating this injury in varying degrees of severity and at varying stages of maturation in an attempt to help understand the underlying pathomechanics. 2. Patients 2.1. Case 1 A 12-year-old boy, a keen footballer with many other sporting pursuits, presented with a 3 month history of activity-related pain on the anteromedial aspect of his right proximal tibia. There was no relevant history of direct trauma. On examination, this otherwise healthy boy held his right knee in slight flexion. He had a normal gait and had no tenderness, effusion, muscle wasting or evidence of ligamentous laxity, tendon damage or a loose body. The right knee had a full range of movement and the right hip was unremarkable. Radiographs of the knee revealed a subtle area of ill-defined sclerosis in the anteromedial aspect of the proximal tibial epiphysis. There was a horizontal sclerotic area in the anterior cortex and subchondral bone of the middle third of the patella
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Fig. 1. (a) Lateral plain film of the knee in the 15 year old male with a high level of sporting activity showing subtle sclerosis in the anteromedial proximal tibial epiphysis (solid arrow) and linear horizontal dense sclerosis in the anterior patella (broken arrow). (b) Computed tomography in the same patient only demonstrates subtle sclerosis corresponding to the area seen on plain film (arrow) with preservation of trabecular pattern. (c, d) Magnetic resonance imaging shows a well-defined rounded pseudotumourlike appearance within the anteromedial epiphysis corresponding to the area seen on plain film low on T1w and high signal on PD fat sat sequences (solid arrows). Note the signs of stress reaction at the tibial tuberosity attachment of the patellar tendon and at the distal femoral and proximal tibial metaphyses (broken arrows).
suggestive of a healing injury. New bone formation was also visible at the lower pole of patella. The secondary centre of the tibial tuberosity had not begun to ossify (Fig. 1a). Computed tomography (CT) performed at the time demonstrated only a faint sclerosis within the corresponding area in the proximal tibial epiphysis with preservation of the trabecular pattern and no evidence of bone loss (Fig. 1b). Magnetic resonance imaging (MRI) demonstrated a well-defined rounded area of abnormal signal within the anterolateral aspect of the incompletely ossified proximal
tibial epiphysis abutting the subchondral bone superiorly and the physeal plate inferiorly which corresponded to the area of sclerosis on the radiograph. This area returned a heterogeneously low to intermediate signal on T1-weighted (T1w) images, high signal on the proton density (PD) fat-saturated (fat-sat) (Fig. 1c and d) and Short Tau Inversion Recovery (STIR) images with moderate post-gadolinium enhancement but was poorly visible on the T2-weighted (T2w) gradient echo images. No discernible transitional zone, surrounding sclerosis or convincing
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evidence of space occupation were evident. Blood tests including an infection, inflammation and metabolic screen were negative. The MRI also revealed a number of horizontal and oblique linear areas of low signal on the T1w and T2w images and subtle high signal on PD fat-sat and STIR. These lines extended from the anterolateral cortex posteriorly into the abnormal area within the anterior third of the proximal tibial epiphyseal cartilage. The abnormality at the anterior aspect of the patella was low signal on all sequences confirming sclerosis in keeping with a chronic stress injury. Oedema signal at the tibial tuberosity attachment of the patellar tendon, minimal widening and irregularity of the proximal tibial and distal femoral physes and subtle abnormal signal within the adjacent metaphyses were also evident in keeping with a generalised multifocal stress phenomenon. In view of these striking additional findings and the absence of any aggressive features, stress related injury was felt to be the cause for the proximal tibial intra-epiphyseal abnormality. The consensus was to monitor this lesion with serial MRIs whilst advising a restriction in activity for the patient as long as there was no deterioration in symptoms. On a repeat MRI 6 months later the stress related changes were more obvious with the stress lines in the anterior proximal tibial epiphysis best demonstrated on the T1w images (Fig. 2a). In addition, on the PD fat-sat images there was a potential subchondral breach immediately superior to the abnormal area (Fig. 2b). In view of this and to confirm the non-aggressive nature of the lesion, further follow up imaging was planned 2 years after the index MRI. On this most recent scan the proximal tibial epiphyseal pseudotumour-like appearance had become less distinct. However, the signs of overuse and stress injury around the knee had become slightly more established with marked traction apophysitis at the completely ossified and fused tibial tuberosity, an increase in the number, thickness and obliquity of the stress lines at the anterior third of the proximal tibial epiphysis and more pronounced oedema within the distal femoral, proximal tibial and proximal fibular metaphyses (Fig. 2c and d). During this period the patient had returned to his sporting pursuits as the symptoms had steadily subsided. 2.2. Case 2 A 14 year old female gymnast experienced acute onset anteroinferior knee pain whilst trampolining. Although the symptoms settled with rest after 2–3 weeks, she experienced multiple recurrences with similar activity over the next 8 months. An MRI performed after the most recent exacerbation showed striking high PS fat-sat signal in a similar pattern as the other case but this time in an almost completely ossified proximal tibial epiphysis (Fig. 3a and b). After conservative management, the symptoms settled and on clinical follow-up 1 month later the patient was discharged. 2.3. Case 3 A 15-year-old boy keen on sporting pursuits presented with ongoing anterior right knee pain for 8 months with associated soft tissue swelling over the tibial tuberosity. Conventional radiography showed fragmentation of the anterior aspect of the tibial tuberosity with soft tissue swelling in keeping with Osgood–Schlatter disease. MRI did not demonstrate any discrete rounded area of signal abnormality but there was a pattern of stress injury strikingly similar to the first case which included prominent, thick oblique and horizontal stress lines in the anterior third of the proximal tibial epiphysis, florid traction apophysitis at the tibial tuberosity and an acute fatigue fracture involving the anterior cortex of the patella (Fig. 4a and b). Note was also made of a small old osteochondral injury to the weight bearing aspect of one of the femoral condyles.
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The patient became asymptomatic within 8 weeks following cessation of athletic activities. 2.4. Case 4 An 13-year-old girl presented with a 6 month history of aching of her knee after sporting activity. MRI showed similar abnormal signal within the anterior aspect of the proximal tibial epiphysis (Fig. 5a and b). There was no other convincing evidence of stress reaction elsewhere in the knee. On clinical follow up, the patient became asymptomatic in 4 weeks after rest from activity and was discharged. 3. Results All four cases show evidence of stress induced changes within the anterior portion of the proximal tibial epiphysis, the pattern and site of which are dependent on both the severity or chronicity of repetitive stress injury and the stage of epiphyseal maturation. Evidence of stress injury in the proximal tibial epiphysis can be seen either in isolation or along with other ancillary signs of stress in the nearby structures. MRI appears to be the most valuable modality for evaluation of these injuries and can demonstrate a spectrum of abnormalities ranging from subtle stress response lines to a pseudotumour-like appearance. All patients were followed up, the first for over 2 years and the others for an average of 2 months each. In all the cases, symptoms subsided with diminished activity. 4. Discussion Stress injuries can be broadly classified as insufficiency injuries resulting from normal stresses on abnormal tissue and fatigue injuries resulting from abnormal repetitive stresses on normal tissue [11]. In fatigue injuries, frequent repetitive minor stresses will eventually result in biological remodelling (referred to as plastic deformation in mechanics) that manifests as stiffening, brittleness and permanent alterations in the form of the tissue. Most stress injuries represent tissues at the stage of plastic deformation prior to complete failure and are therefore reversible, especially in the immature skeleton which has good regenerative potential [11–14]. Fatigue of the muscles which normally confer some degree of protection from loading [12,14], impaired bone perfusion from repetitive trauma and the weaker bone produced as a result of accelerated, unbalanced reparative osteoclastic activity [13,14] all contribute towards the stress phenomenon. The manifestation of stress around a joint is dependent on the intrinsic characteristics of the tissue involved (for e.g., mature/ossified vs immature/unossified) and the nature of the forces that are exerted across it. These forces include gravity and the complex tensile stresses exerted by the various ligaments and tendons that act upon the joint during weight-bearing and different types of movement. Stress analysis using photo-elastic methods can diagrammatically depict these forces at a joint as lines [15]. Stress or overuse related injuries are common in children and adolescents [1–4], especially young male athletes during a growth spurt, because of their immature weaker skeletons, decreased strength in the incompletely fused physeal plates, lag of bone mineralisation behind bone growth, increased activity and consequently higher ligamentous strain [3,16–18]. Unlike in the adult, the incompletely ossified cartilage of the epiphysis is weaker than the ligaments, muscles and tendons that attach to it and therefore apophyseal avulsion injuries and injuries to the physeal plates are more common than ligamentous disruption in children and adolescents [18,19]. Stress related physeal injuries have been
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Fig. 2. (a, b) Follow up MRI of the same patient as in Fig. 1 6 months later demonstrates a much more striking pseudotumour-like appearance (solid arrows) but also accentuation of the stress lines in the anterior proximal tibial epiphysis on T1w images and a subchondral breach along the superior border of this area on PD fat-sat images (broken arrow). (c, d) An MRI 2 years after the initial MRI shows that the pseudotumour-like appearance in the epiphysis is no longer obvious but the signs of stress injury have become more prominent (solid arrows).
described in various parts of the body including the ribs and ulnae [2]. The imaging features of cortical stress fractures and stress injuries to the physis have been well described [5,11,14,19,20]. Purely medullary stress lesions affecting only the unossified cartilage or incompletely ossified epiphysis and do not demonstrate the classic imaging features associated with cortical or physeal stress injuries. All that is visible on plain film or CT is a faint focal sclerosis and coarsening of the trabeculae representative of peritrabecular callus formation at the site of micro-fracturing [5,11,14].
MRI in these patients is probably the only definitive investigation which usually demonstrates quite marked abnormal high signal within the intra-epiphyseal cancellous bone on PD fat-sat and STIR sequences [5,22,23,25] representing the haemorrhage and oedema from the repeated trabecular micro-fractures. The other potential findings are thin linear horizontal intramedullary bands of lowsignal on all MRI sequences that are continuous with the cortex [23] and most often concentrated at the area most affected by stress. In the acute setting, these linear clefts can be filled with fluid appearing high signal on fluid sensitive sequences [21–24].
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Fig. 3. (a, b) T1w and PD fat-sat images of 2nd case showing similar pattern of oedema but within an almost completely ossified proximal tibial epiphysis (arrows).
These sclerotic lines need to be differentiated from the normal stress lines seen in the anterior proximal tibial epiphysis near the ACL attachment [24] and the normal growth lines that are seen on the metaphyseal side of the physis [21]. It is not unusual on MR imaging of children’s knees to see thin linear areas of low signal on T1 and high signal on fluid-sensitive sequences in the anterior part of the proximal tibial epiphysis. These can often be difficult to differentiate from normal blood vessels and physiological stress lines. At the other end of the spectrum, sometimes the abnormal bone marrow signal and extensive soft tissue oedema associated with these stress injuries can demonstrate quite a circumscribed morphology giving them a pseudotumour-like appearance [9]. Sports or overuse related pseudotumours have been described at tendon insertion sites like the adductor insertion on the femur [6], the ischial tuberosity [7] and other sites based on the type of activity or sport [5,11].
The tibia is the most common site of stress fractures in the skeletally immature patient [1,2,16] with Salter–Harris type injuries involving the proximal tibial physeal plate and avulsion injuries involving the tibial tuberosity being the most common type of injuries seen [10]. However, stress reaction within the proximal tibial epiphyseal unossified cartilage or immature cancellous bone has not been described before. The proximal tibial epiphysis and the tibial tuberosity share a common cartilage anlage with the primary centre of the proximal tibial tuberosity ossifying first followed by the secondary centre of the tibial tuberosity. As maturation progresses they are seen to grow towards each other before finally fusing near the anterior third of the proximal tibia. Simultaneously, the proximal tibial physeal plate progressively fuses from posterior to anterior [10,25,26]. Stress analysis of the knee shows that the main stress affecting the proximal tibial epiphysis, apart from the compression related to
Fig. 4. (a, b) T1w and PD fat-sat MRI images of the 3rd case, another active 15 year old boy presenting with anterior knee pain show a stress pattern involving the anterior proximal tibial epiphysis and tibial tuberosity (arrows) strikingly similar to the previous cases.
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Fig. 5. (a, b) MRI in the 4th case, an 13 year old with a history of sporting activity and anterior knee pain demonstrates a similar pattern of stress reaction at the anterior aspect of the proximal tibial epiphysis and tibial tuberosity (arrows).
weight-bearing, is the anterosuperior pull at the tibial tuberosity via the extensor mechanism which is exaggerated during activities like running and jumping. The crowding of the stress lines at the anterior third of the proximal tibial epiphysis on stress analysis of the knee shows that this area is subjected to the maximum strain during such activities [15] (Fig. 6). The focus of stress and resultant injury across the proximal tibia therefore varies with the
Fig. 6. Illustrative diagram demonstrating the change in the stress modulus through the knee during activity resulting in an area of concentrated stress in the anterior third of the proximal tibial epiphysis corresponding to the site of pseudotumour development in our index case. Adapted from Smith JW [15].
level of skeletal maturity at the knee joint and the kind of activity or movement that it is subjected to. The angular morphology of the proximal tibial epiphysis and lever-arch biomechanics associated with the extensor mechanism also probably play a role in the pattern of injury. In a more mature skeleton where the tibial tuberosity has completely ossified and fused to the PTE with only the posterior aspect of the physeal plate fused, an acute traction stress at the tibial tuberosity could result in complete avulsion of the tibial tuberosity, separation of the anterior proximal tibial physis and extension of the fracture line superiorly into the epiphysis from the most anterior point of physeal fusion. This would be in keeping with a Type 4 injury of the modified Watson–Jones Classification as described by Ryu et al. [27–29]. It is therefore entirely reasonable to assume that in a less mature skeleton where the secondary centre of the tibial tuberosity is yet to ossify, a similar mechanism of injury in a less intense but repetitive manner would result in maximal stress similarly being transmitted through the anterior third of the proximal tibial epiphysis. This would explain the concentration of the imaging abnormalities in the anterior third of the PTE in all our patients with immature skeletons and increased levels of activity and the differences in the type and focus of stress injury at the proximal tibia depending on the stage of maturation. As the tibial tuberosity ossifies and fuses with the PTE and the common physeal plate closes, maximal stress is shifted from the anterior third of the PTE down towards the tibial tuberosity (Fig. 7). This phenomenon is dramatically depicted in our first patient on serial MRIs. We therefore postulate that a stress phenomenon acting on the cartilage and immature cancellous bone of the anterior proximal tibial epiphysis has resulted in the imaging features seen in all our patients. Stress-induced intra-epiphyseal injury does not necessarily have a single set of specific diagnostic imaging criteria because this can vary widely dependent on the factors alluded to above. Therefore, it is important to emphasise that such a diagnosis can only be arrived at if there is other supportive evidence indicative of a generalised stress phenomenon in the vicinity. In the knee, as demonstrated in our four cases, MRI evidence of stress injury can be seen in the form of old patellar stress fractures, tibial tuberosity apophysitis), widening and abnormally high signal of the physeal plates and abnormal oedema signal in the metaphyses. The differential of stress injury in this location would include Osgood–Schlatter disease and other causes for non-specific bone
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Fig. 7. Illustrative diagram demonstrating the shift of stress modulus across the anterior knee along with normal maturation and ossification.
marrow oedema including infection, osteonecrosis and reflex sympathetic dystrophy [30]. The symptoms associated with stress injuries in immature skeletons usually resolve rapidly with avoidance of the causative stress and rest [1,5,13,17]. In a series of 34 stress fractures at various sites in children and adolescents that were followed up, all had complete resolution of symptoms and return to normal activity after adequate rest [1]. The imaging findings follow suit and disappear after a variable lag phase. In our first patient, restriction of activity and serial MRIs proved the stress-induced nature of the proximal tibial epiphyseal changes. The other three patients, have also been advised a limitation of activity with promising early clinical signs. 5. Conclusion With increasing levels of sporting and recreational activity amongst children and adolescents stress related injuries are becoming increasingly common. Purely intra-epiphyseal stress related lesions are a hitherto undescribed phenomenon. The site and pattern of intra-epiphyseal stress injury is dependent on the stage of maturation of bone, the ossification of the secondary centres, the extent of physeal fusion and the type and frequency of repetitive loading that the tissue is subjected to. MRI is very often the only modality on which this type of abnormality can be detected. In the proximal tibial epiphysis, maximal stress is exerted through the anterior third of the epiphysis which is exaggerated during jumping activities. This can manifest as a wide continuum of abnormality within the proximal tibial epiphysis ranging from subtle oedema and a few thin stress lines to a pseudotumourlike appearance. The key to diagnosing such lesions is to look for the ancillary signs of stress injury elsewhere within the knee and ensure resolution by means of serial MRIs along with activity restriction and rest. This will help avoid unnecessary invasive investigations and significantly reduce anxiety. Conflict of interest The author hereby confirm that none of the authors or the institution where the work was carried out have any conflicts of interest to declare. References [1] Walker RN, Green NE, Spindler KP. Stress fractures in skeletally immature patients. J Pediatr Orthop 1996;16(5):578–84. [2] Papadimitriou NG, Christophorides J, Papadimitriou A, Beslikas TA, Ventouris TN, Goulios BA. Stress fractures in children: a review of 37 cases. Eur J Orthop Surg Traumatol 2007;17:131–7.
[3] Kerssemakers SP, Fotiadou AN, de Jonge MC, Karantanas AH, Maas M. Sport injuries in the paediatric and adolescent patient: a growing problem. Pediatr Radiol 2009;39:471–84. [4] Ohta-Fukushima M, Mutoh Y, Takasugi S, Iwata H, Ishii S. Characteristics of stress fractures in young athletes under 20 years. J Sports Med Phys Fitness 2002;42:198–206. [5] Vanhoenacker FM, Maas M, Gielen JL. Imaging of orthopedic sports injuries. New York: Springer; 2007. p. 86–8. [6] Anderson SE, Johnston JO, O’Donnell RO, Steinbach LS. MR imaging of sportsrelated pseudotumour in children: mid femoral diaphyseal periostitis at insertion site of adductor musculature. Am J Roentgenol 2001;176:1227–31. [7] Barnes ST, Hinds RB. Pseudotumour of the ischium. A late manifestation of avulsion of the ischial epiphysis. J Bone Joint Surg Am 1972;54:645–7. [8] Nanni B, Butt S, Mansour R, Muthukumar T, Cassar-Pullicino VN, Roberts A. Stress-induced Salter–Harris I growth plate injury of the proximal tibia: first report. Skeletal Radiol 2005;34:405–10. [9] Horev G, Korenreich L, Ziv N, Grunebaum M. The enigma of stress fractures in the pediatric age: clarification or confusion through the new imaging modalities. Pediatr Radiol 1990;20:469–71. [10] Slovis TL. Caffey’s pediatric diagnostic imaging. 11th ed. Philadelphia: Mosby Elsevier; 2010. [11] Pavlov H. Physical injury: sports related abnormalities. In: Resnick D, editor. Diagnosis of bone and joint disorders. 3rd ed. Philadelphia: Saunders; 1995. [12] Delee JC, Drez D, Miller MD. Orthopaedic sports medicine: principles and practice. 3rd ed. Philadelphia: Elsevier, Saunders; 2010. p. 93–6. [13] Romani WA, Gieck JH, Perrin DH, Saliba EN, Kahler DM. Mechanisms and management of stress fractures in physically active persons. J Athl Train 2002;37(3):306–14. [14] Anderson MW, Greenspan A. Stress fractures. Radiology 1996;199(1):1–12. [15] Smith JW. The relationship of epiphyseal plates to stress in some bones of the lower limb. J Anat 1962;96(1):58–78. [16] Peterson CA, Peterson HA. Analysis of the incidence of injuries to the epiphyseal growth plate. J Trauma 1972;12:275–81. [17] Caine D, DiFiori J, Mafulli N. Physeal injuries in children’s and youth sports: reasons for concern? Br J Sports Med 2006;40:749–60. [18] Ogden JA. Skeletal injury in the child. 3rd ed. New York: Springer; 2000. p. 399–418. [19] Sofka CM. Imaging of stress fractures. Clin Sports Med 2006;25:53–62. [20] Laor T, Jaramillo D. MR imaging insights into skeletal maturation: what is normal? Radiology 2009;250(1):28–38. [21] Laor T, Wall J, Vu LP. Physeal widening in the knee due to stress injury in child athletes. Am J Roentgenol 2006;186:1260–4. [22] Connolly SA, Connolly LP, Jaramillo D. Imaging of sports injuries in children and adolescents. Radiol Clin North Am 2001;39(4):773–90. [23] 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(2):291–306. [24] Hacking JC, Mackenzie R, Dixon AK. Proximal tibial stress lines – appearances on magnetic resonance imaging of the knee. Br J Radiol 1995;68:933–5. [25] Price CT, Herrera-Soto J. Extra-articular injuries of the knee. In: Beaty JH, Kasser Jr, editors. Rockwood and Wilkins’ fractures in children. 7th ed. Philadelphia: Lippincott Williams & Wilkins; 2010. p. 866. [26] Aitken AP, Ingersoll RE. Fractures of the proximal tibial epiphyseal cartilage. J Bon Joint Surg 1956;38-A(4):787–96. [27] Ogden JA, Tross RB, Murphy MJ. Fractures of the tibial tuberosity in adolescents. J Bone Joint Surg 1980;62-A(2):1980. [28] Ryu RKN, Debenham JO. An unusual avulsion fracture of the proximal tibial epiphysis. Clin Orthop 1985;194:181–4. [29] Poulsen TD, Skak SV, Toftgaard Jensen T. Epiphyseal fractures of the proximal tibia. Injury 1989;20:111–3. [30] Zanetti M, Steiner CL, Seifert B, Hodler J. Clinical outcome of edema-like bone marrow abnormalities of the foot. Radiology 2002;186:184–8.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Intra-epiphyseal stress injury of the proximal tibial epiphysis: Preliminary experience of magnetic resonance imaging findings G. Tony a,1 , A. Charran b,2 , B. Tins e,3 , R. Lalam e,3 , P.N.M. Tyrrell e,3 , J. Singh e,3 , P. Cool d,4 , N. Kiely c,4 , V.N. Cassar-Pullicino e,∗ a
Stafford General Hospital, Weston Road, Stafford, Staffordshire ST16 3SA, UK Hillingdon Hospital, Pield Heath Rd, Uxbridge, Middlesex UB8 3NN, UK c Paediatric Orthopaedics, Robert Jones and Agnes Hunt, Orthopaedic Hospital, Oswestry, Shropshire SY10 7 AG, UK d Orthopaedic Oncology, Robert Jones and Agnes Hunt, Orthopaedic Hospital, Oswestry, Shropshire SY10 7 AG, UK e Department of Diagnostic Imaging, Robert Jones and Agnes Hunt, Orthopaedic Hospital, Oswestry, Shropshire SY10 7 AG, UK b
a r t i c l e
i n f o
Article history: Received 23 May 2014 Received in revised form 31 July 2014 Accepted 8 August 2014 Keywords: Stress injury Proximal tibial epiphysis MRI
a b s t r a c t Stress induced injuries affecting the physeal plate or cortical bone in children and adolescents, especially young athletes, have been well described. However, there are no reports in the current English language literature of stress injury affecting the incompletely ossified epiphyseal cartilage. We present four cases of stress related change to the proximal tibial epiphysis (PTE) along with their respective magnetic resonance imaging (MRI) appearances ranging from subtle oedema signal to a pseudo-tumour like appearance within the epiphyseal cartilage. The site and pattern of intra-epiphyseal injury is determined by the type of tissue that is affected, the maturity of the skeleton and the type of forces that are transmitted through the tissue. We demonstrate how an awareness of the morphological spectrum of MRI appearances in intra-epiphyseal stress injury and the ability to identify concomitant signs of stress in other nearby structures can help reduce misdiagnosis, avoid invasive diagnostic procedures like bone biopsy and reassure patients and their families. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Stress-induced injury to the immature skeleton has been well documented [1–4] and in some cases a pseudo-tumour like appearance has been described in children and adolescents as a result of a high levels of sporting activity [5–7]. Stress or overuse related injuries are particularly common within the proximal tibia and can mimic infection [8] or tumour [8–10]. To our knowledge, there are no reports in the English language literature of stress-induced injury to the incompletely ossified epiphysis. We present our
∗ Corresponding author. Tel.: +44 1691404189; fax: +44 1691404170. E-mail addresses: [email protected] (G. Tony), [email protected] (A. Charran), [email protected] (B. Tins), [email protected] (R. Lalam), [email protected] (P.N.M. Tyrrell), [email protected] (J. Singh), [email protected] (P. Cool), [email protected] (N. Kiely), [email protected] (V.N. Cassar-Pullicino). 1 Tel.: +44 07960146176. 2 Tel.: +44 07894282366. 3 Tel.: +44 01691404189. 4 Tel.: +44 01691404000. http://dx.doi.org/10.1016/j.ejrad.2014.08.008 0720-048X/© 2014 Elsevier Ireland Ltd. All rights reserved.
experience of the MRI findings in chronic/repetitive stress injury to the proximal tibial epiphysis (PTE) in four different adolescents each demonstrating this injury in varying degrees of severity and at varying stages of maturation in an attempt to help understand the underlying pathomechanics. 2. Patients 2.1. Case 1 A 12-year-old boy, a keen footballer with many other sporting pursuits, presented with a 3 month history of activity-related pain on the anteromedial aspect of his right proximal tibia. There was no relevant history of direct trauma. On examination, this otherwise healthy boy held his right knee in slight flexion. He had a normal gait and had no tenderness, effusion, muscle wasting or evidence of ligamentous laxity, tendon damage or a loose body. The right knee had a full range of movement and the right hip was unremarkable. Radiographs of the knee revealed a subtle area of ill-defined sclerosis in the anteromedial aspect of the proximal tibial epiphysis. There was a horizontal sclerotic area in the anterior cortex and subchondral bone of the middle third of the patella
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Fig. 1. (a) Lateral plain film of the knee in the 15 year old male with a high level of sporting activity showing subtle sclerosis in the anteromedial proximal tibial epiphysis (solid arrow) and linear horizontal dense sclerosis in the anterior patella (broken arrow). (b) Computed tomography in the same patient only demonstrates subtle sclerosis corresponding to the area seen on plain film (arrow) with preservation of trabecular pattern. (c, d) Magnetic resonance imaging shows a well-defined rounded pseudotumourlike appearance within the anteromedial epiphysis corresponding to the area seen on plain film low on T1w and high signal on PD fat sat sequences (solid arrows). Note the signs of stress reaction at the tibial tuberosity attachment of the patellar tendon and at the distal femoral and proximal tibial metaphyses (broken arrows).
suggestive of a healing injury. New bone formation was also visible at the lower pole of patella. The secondary centre of the tibial tuberosity had not begun to ossify (Fig. 1a). Computed tomography (CT) performed at the time demonstrated only a faint sclerosis within the corresponding area in the proximal tibial epiphysis with preservation of the trabecular pattern and no evidence of bone loss (Fig. 1b). Magnetic resonance imaging (MRI) demonstrated a well-defined rounded area of abnormal signal within the anterolateral aspect of the incompletely ossified proximal
tibial epiphysis abutting the subchondral bone superiorly and the physeal plate inferiorly which corresponded to the area of sclerosis on the radiograph. This area returned a heterogeneously low to intermediate signal on T1-weighted (T1w) images, high signal on the proton density (PD) fat-saturated (fat-sat) (Fig. 1c and d) and Short Tau Inversion Recovery (STIR) images with moderate post-gadolinium enhancement but was poorly visible on the T2-weighted (T2w) gradient echo images. No discernible transitional zone, surrounding sclerosis or convincing
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evidence of space occupation were evident. Blood tests including an infection, inflammation and metabolic screen were negative. The MRI also revealed a number of horizontal and oblique linear areas of low signal on the T1w and T2w images and subtle high signal on PD fat-sat and STIR. These lines extended from the anterolateral cortex posteriorly into the abnormal area within the anterior third of the proximal tibial epiphyseal cartilage. The abnormality at the anterior aspect of the patella was low signal on all sequences confirming sclerosis in keeping with a chronic stress injury. Oedema signal at the tibial tuberosity attachment of the patellar tendon, minimal widening and irregularity of the proximal tibial and distal femoral physes and subtle abnormal signal within the adjacent metaphyses were also evident in keeping with a generalised multifocal stress phenomenon. In view of these striking additional findings and the absence of any aggressive features, stress related injury was felt to be the cause for the proximal tibial intra-epiphyseal abnormality. The consensus was to monitor this lesion with serial MRIs whilst advising a restriction in activity for the patient as long as there was no deterioration in symptoms. On a repeat MRI 6 months later the stress related changes were more obvious with the stress lines in the anterior proximal tibial epiphysis best demonstrated on the T1w images (Fig. 2a). In addition, on the PD fat-sat images there was a potential subchondral breach immediately superior to the abnormal area (Fig. 2b). In view of this and to confirm the non-aggressive nature of the lesion, further follow up imaging was planned 2 years after the index MRI. On this most recent scan the proximal tibial epiphyseal pseudotumour-like appearance had become less distinct. However, the signs of overuse and stress injury around the knee had become slightly more established with marked traction apophysitis at the completely ossified and fused tibial tuberosity, an increase in the number, thickness and obliquity of the stress lines at the anterior third of the proximal tibial epiphysis and more pronounced oedema within the distal femoral, proximal tibial and proximal fibular metaphyses (Fig. 2c and d). During this period the patient had returned to his sporting pursuits as the symptoms had steadily subsided. 2.2. Case 2 A 14 year old female gymnast experienced acute onset anteroinferior knee pain whilst trampolining. Although the symptoms settled with rest after 2–3 weeks, she experienced multiple recurrences with similar activity over the next 8 months. An MRI performed after the most recent exacerbation showed striking high PS fat-sat signal in a similar pattern as the other case but this time in an almost completely ossified proximal tibial epiphysis (Fig. 3a and b). After conservative management, the symptoms settled and on clinical follow-up 1 month later the patient was discharged. 2.3. Case 3 A 15-year-old boy keen on sporting pursuits presented with ongoing anterior right knee pain for 8 months with associated soft tissue swelling over the tibial tuberosity. Conventional radiography showed fragmentation of the anterior aspect of the tibial tuberosity with soft tissue swelling in keeping with Osgood–Schlatter disease. MRI did not demonstrate any discrete rounded area of signal abnormality but there was a pattern of stress injury strikingly similar to the first case which included prominent, thick oblique and horizontal stress lines in the anterior third of the proximal tibial epiphysis, florid traction apophysitis at the tibial tuberosity and an acute fatigue fracture involving the anterior cortex of the patella (Fig. 4a and b). Note was also made of a small old osteochondral injury to the weight bearing aspect of one of the femoral condyles.
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The patient became asymptomatic within 8 weeks following cessation of athletic activities. 2.4. Case 4 An 13-year-old girl presented with a 6 month history of aching of her knee after sporting activity. MRI showed similar abnormal signal within the anterior aspect of the proximal tibial epiphysis (Fig. 5a and b). There was no other convincing evidence of stress reaction elsewhere in the knee. On clinical follow up, the patient became asymptomatic in 4 weeks after rest from activity and was discharged. 3. Results All four cases show evidence of stress induced changes within the anterior portion of the proximal tibial epiphysis, the pattern and site of which are dependent on both the severity or chronicity of repetitive stress injury and the stage of epiphyseal maturation. Evidence of stress injury in the proximal tibial epiphysis can be seen either in isolation or along with other ancillary signs of stress in the nearby structures. MRI appears to be the most valuable modality for evaluation of these injuries and can demonstrate a spectrum of abnormalities ranging from subtle stress response lines to a pseudotumour-like appearance. All patients were followed up, the first for over 2 years and the others for an average of 2 months each. In all the cases, symptoms subsided with diminished activity. 4. Discussion Stress injuries can be broadly classified as insufficiency injuries resulting from normal stresses on abnormal tissue and fatigue injuries resulting from abnormal repetitive stresses on normal tissue [11]. In fatigue injuries, frequent repetitive minor stresses will eventually result in biological remodelling (referred to as plastic deformation in mechanics) that manifests as stiffening, brittleness and permanent alterations in the form of the tissue. Most stress injuries represent tissues at the stage of plastic deformation prior to complete failure and are therefore reversible, especially in the immature skeleton which has good regenerative potential [11–14]. Fatigue of the muscles which normally confer some degree of protection from loading [12,14], impaired bone perfusion from repetitive trauma and the weaker bone produced as a result of accelerated, unbalanced reparative osteoclastic activity [13,14] all contribute towards the stress phenomenon. The manifestation of stress around a joint is dependent on the intrinsic characteristics of the tissue involved (for e.g., mature/ossified vs immature/unossified) and the nature of the forces that are exerted across it. These forces include gravity and the complex tensile stresses exerted by the various ligaments and tendons that act upon the joint during weight-bearing and different types of movement. Stress analysis using photo-elastic methods can diagrammatically depict these forces at a joint as lines [15]. Stress or overuse related injuries are common in children and adolescents [1–4], especially young male athletes during a growth spurt, because of their immature weaker skeletons, decreased strength in the incompletely fused physeal plates, lag of bone mineralisation behind bone growth, increased activity and consequently higher ligamentous strain [3,16–18]. Unlike in the adult, the incompletely ossified cartilage of the epiphysis is weaker than the ligaments, muscles and tendons that attach to it and therefore apophyseal avulsion injuries and injuries to the physeal plates are more common than ligamentous disruption in children and adolescents [18,19]. Stress related physeal injuries have been
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Fig. 2. (a, b) Follow up MRI of the same patient as in Fig. 1 6 months later demonstrates a much more striking pseudotumour-like appearance (solid arrows) but also accentuation of the stress lines in the anterior proximal tibial epiphysis on T1w images and a subchondral breach along the superior border of this area on PD fat-sat images (broken arrow). (c, d) An MRI 2 years after the initial MRI shows that the pseudotumour-like appearance in the epiphysis is no longer obvious but the signs of stress injury have become more prominent (solid arrows).
described in various parts of the body including the ribs and ulnae [2]. The imaging features of cortical stress fractures and stress injuries to the physis have been well described [5,11,14,19,20]. Purely medullary stress lesions affecting only the unossified cartilage or incompletely ossified epiphysis and do not demonstrate the classic imaging features associated with cortical or physeal stress injuries. All that is visible on plain film or CT is a faint focal sclerosis and coarsening of the trabeculae representative of peritrabecular callus formation at the site of micro-fracturing [5,11,14].
MRI in these patients is probably the only definitive investigation which usually demonstrates quite marked abnormal high signal within the intra-epiphyseal cancellous bone on PD fat-sat and STIR sequences [5,22,23,25] representing the haemorrhage and oedema from the repeated trabecular micro-fractures. The other potential findings are thin linear horizontal intramedullary bands of lowsignal on all MRI sequences that are continuous with the cortex [23] and most often concentrated at the area most affected by stress. In the acute setting, these linear clefts can be filled with fluid appearing high signal on fluid sensitive sequences [21–24].
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Fig. 3. (a, b) T1w and PD fat-sat images of 2nd case showing similar pattern of oedema but within an almost completely ossified proximal tibial epiphysis (arrows).
These sclerotic lines need to be differentiated from the normal stress lines seen in the anterior proximal tibial epiphysis near the ACL attachment [24] and the normal growth lines that are seen on the metaphyseal side of the physis [21]. It is not unusual on MR imaging of children’s knees to see thin linear areas of low signal on T1 and high signal on fluid-sensitive sequences in the anterior part of the proximal tibial epiphysis. These can often be difficult to differentiate from normal blood vessels and physiological stress lines. At the other end of the spectrum, sometimes the abnormal bone marrow signal and extensive soft tissue oedema associated with these stress injuries can demonstrate quite a circumscribed morphology giving them a pseudotumour-like appearance [9]. Sports or overuse related pseudotumours have been described at tendon insertion sites like the adductor insertion on the femur [6], the ischial tuberosity [7] and other sites based on the type of activity or sport [5,11].
The tibia is the most common site of stress fractures in the skeletally immature patient [1,2,16] with Salter–Harris type injuries involving the proximal tibial physeal plate and avulsion injuries involving the tibial tuberosity being the most common type of injuries seen [10]. However, stress reaction within the proximal tibial epiphyseal unossified cartilage or immature cancellous bone has not been described before. The proximal tibial epiphysis and the tibial tuberosity share a common cartilage anlage with the primary centre of the proximal tibial tuberosity ossifying first followed by the secondary centre of the tibial tuberosity. As maturation progresses they are seen to grow towards each other before finally fusing near the anterior third of the proximal tibia. Simultaneously, the proximal tibial physeal plate progressively fuses from posterior to anterior [10,25,26]. Stress analysis of the knee shows that the main stress affecting the proximal tibial epiphysis, apart from the compression related to
Fig. 4. (a, b) T1w and PD fat-sat MRI images of the 3rd case, another active 15 year old boy presenting with anterior knee pain show a stress pattern involving the anterior proximal tibial epiphysis and tibial tuberosity (arrows) strikingly similar to the previous cases.
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Fig. 5. (a, b) MRI in the 4th case, an 13 year old with a history of sporting activity and anterior knee pain demonstrates a similar pattern of stress reaction at the anterior aspect of the proximal tibial epiphysis and tibial tuberosity (arrows).
weight-bearing, is the anterosuperior pull at the tibial tuberosity via the extensor mechanism which is exaggerated during activities like running and jumping. The crowding of the stress lines at the anterior third of the proximal tibial epiphysis on stress analysis of the knee shows that this area is subjected to the maximum strain during such activities [15] (Fig. 6). The focus of stress and resultant injury across the proximal tibia therefore varies with the
Fig. 6. Illustrative diagram demonstrating the change in the stress modulus through the knee during activity resulting in an area of concentrated stress in the anterior third of the proximal tibial epiphysis corresponding to the site of pseudotumour development in our index case. Adapted from Smith JW [15].
level of skeletal maturity at the knee joint and the kind of activity or movement that it is subjected to. The angular morphology of the proximal tibial epiphysis and lever-arch biomechanics associated with the extensor mechanism also probably play a role in the pattern of injury. In a more mature skeleton where the tibial tuberosity has completely ossified and fused to the PTE with only the posterior aspect of the physeal plate fused, an acute traction stress at the tibial tuberosity could result in complete avulsion of the tibial tuberosity, separation of the anterior proximal tibial physis and extension of the fracture line superiorly into the epiphysis from the most anterior point of physeal fusion. This would be in keeping with a Type 4 injury of the modified Watson–Jones Classification as described by Ryu et al. [27–29]. It is therefore entirely reasonable to assume that in a less mature skeleton where the secondary centre of the tibial tuberosity is yet to ossify, a similar mechanism of injury in a less intense but repetitive manner would result in maximal stress similarly being transmitted through the anterior third of the proximal tibial epiphysis. This would explain the concentration of the imaging abnormalities in the anterior third of the PTE in all our patients with immature skeletons and increased levels of activity and the differences in the type and focus of stress injury at the proximal tibia depending on the stage of maturation. As the tibial tuberosity ossifies and fuses with the PTE and the common physeal plate closes, maximal stress is shifted from the anterior third of the PTE down towards the tibial tuberosity (Fig. 7). This phenomenon is dramatically depicted in our first patient on serial MRIs. We therefore postulate that a stress phenomenon acting on the cartilage and immature cancellous bone of the anterior proximal tibial epiphysis has resulted in the imaging features seen in all our patients. Stress-induced intra-epiphyseal injury does not necessarily have a single set of specific diagnostic imaging criteria because this can vary widely dependent on the factors alluded to above. Therefore, it is important to emphasise that such a diagnosis can only be arrived at if there is other supportive evidence indicative of a generalised stress phenomenon in the vicinity. In the knee, as demonstrated in our four cases, MRI evidence of stress injury can be seen in the form of old patellar stress fractures, tibial tuberosity apophysitis), widening and abnormally high signal of the physeal plates and abnormal oedema signal in the metaphyses. The differential of stress injury in this location would include Osgood–Schlatter disease and other causes for non-specific bone
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Fig. 7. Illustrative diagram demonstrating the shift of stress modulus across the anterior knee along with normal maturation and ossification.
marrow oedema including infection, osteonecrosis and reflex sympathetic dystrophy [30]. The symptoms associated with stress injuries in immature skeletons usually resolve rapidly with avoidance of the causative stress and rest [1,5,13,17]. In a series of 34 stress fractures at various sites in children and adolescents that were followed up, all had complete resolution of symptoms and return to normal activity after adequate rest [1]. The imaging findings follow suit and disappear after a variable lag phase. In our first patient, restriction of activity and serial MRIs proved the stress-induced nature of the proximal tibial epiphyseal changes. The other three patients, have also been advised a limitation of activity with promising early clinical signs. 5. Conclusion With increasing levels of sporting and recreational activity amongst children and adolescents stress related injuries are becoming increasingly common. Purely intra-epiphyseal stress related lesions are a hitherto undescribed phenomenon. The site and pattern of intra-epiphyseal stress injury is dependent on the stage of maturation of bone, the ossification of the secondary centres, the extent of physeal fusion and the type and frequency of repetitive loading that the tissue is subjected to. MRI is very often the only modality on which this type of abnormality can be detected. In the proximal tibial epiphysis, maximal stress is exerted through the anterior third of the epiphysis which is exaggerated during jumping activities. This can manifest as a wide continuum of abnormality within the proximal tibial epiphysis ranging from subtle oedema and a few thin stress lines to a pseudotumourlike appearance. The key to diagnosing such lesions is to look for the ancillary signs of stress injury elsewhere within the knee and ensure resolution by means of serial MRIs along with activity restriction and rest. This will help avoid unnecessary invasive investigations and significantly reduce anxiety. Conflict of interest The author hereby confirm that none of the authors or the institution where the work was carried out have any conflicts of interest to declare. References [1] Walker RN, Green NE, Spindler KP. Stress fractures in skeletally immature patients. J Pediatr Orthop 1996;16(5):578–84. [2] Papadimitriou NG, Christophorides J, Papadimitriou A, Beslikas TA, Ventouris TN, Goulios BA. Stress fractures in children: a review of 37 cases. Eur J Orthop Surg Traumatol 2007;17:131–7.
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