MRI Appearance of Chronic Stress Injury of the Iliac Crest Apophysis in Adolescent Athletes

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1 Pediatric Imaging Clinical Observations Hébert et al. MRI of Iliac Crest pophysis Pediatric Imaging Clinical Observations Downloaded from by on 01/24/18 from IP address Copyright RRS. For personal use only; all rights reserved Kenneth J. Hébert 1 Tal Laor 1 Jon G. Divine 2 Kathleen H. Emery 1 Eric J. Wall 3 Hébert KJ, Laor T, Divine JG, Emery KH, Wall EJ Keywords: adolescent athletes, growth plate, iliac apophysis, pelvic avulsion, sports medicine, stress fracture DOI: /JR Received November 9, 2007; accepted after revision December 31, Department of Radiology, Cincinnati Children s Hospital Medical Center and University of Cincinnati College of Medicine, 3333 urnet ve., Cincinnati, OH ddress correspondence to T. Laor (laor@cchmc.org). 2 Division of Sports Medicine, Cincinnati Children s Hospital Medical Center and University of Cincinnati College of Medicine, Cincinnati, OH. 3 Department of Orthopedic Surgery, Cincinnati Children s Hospital Medical Center and University of Cincinnati College of Medicine, Cincinnati, OH. JR 2008; 190: X/08/ merican Roentgen Ray Society MRI ppearance of Chronic Stress Injury of the Iliac Crest pophysis in dolescent thletes OJECTIVE. The objective of our study was to describe the MRI appearance of chronic repetitive stress injury of the iliac crest apophysis in adolescent athletes. CONCLUSION. Increased signal intensity on water-sensitive sequences and mild widening of the physis, often with adjacent bone marrow and muscle edema, are characteristic of chronic stress injury of the iliac apophysis in adolescent athletes who may present with hip, pelvic, or back pain. n apophysis in a child is a secondary center of ossification that contributes to the size or shape of a bone, but not to its length [1], and is connected to a parent bone by an associated physis. n apophysis also has been termed traction epiphysis. It is the site of attachment or origin of muscles and tendons and thus is a common site for acute and chronic injury [1]. lthough acute apophyseal injury is the end point of excessive forces transmitted through the adjacent muscles and tendons, often resulting in an avulsion during athletic activities [1], a chronic injury may have minimal, if any, displacement or widening of the apophyseal physis and is associated with ongoing reparative inflammation [2]. pophyseal injury to the pelvis has increased in prevalence over the past several decades because more adolescents are participating in highly competitive athletic activities [3]. thletic activities that have been associated with pelvic apophyseal injury include gymnastics, track and cross-country running, soccer, and baseball [3, 4]. Sites of apophyseal injury around the pelvis include the ischial tuberosity, anterior inferior iliac spine, anterior superior iliac spine, pubic symphysis, and iliac crest [3]. The radiographic appearance of acute apophyseal injury has been described extensively [1], and most often radiography is the initial and only imaging evaluation performed. Sonography, MRI [4], and CT [5] have been used to evaluate acute apophyseal injuries of the pelvis. Chronic stress injury specifically, of the iliac crest has been evaluated with nuclear scintigraphy [6]. We encountered several adolescent athletes who presented with chronic pelvic, hip, or lumbar region pain associated with sports activities and were referred for MRI either to confirm a suspected injury or to evaluate the extent of an abnormality, with the ultimate diagnosis of chronic injury to the iliac crest apophysis. To our knowledge, the MRI characteristics of this injury have not been reported in children. Therefore, the purpose of this study was to describe the MRI appearance of chronic repetitive stress injury to the iliac crest apophysis in adolescent athletes. Materials and Methods Institutional review board approval for this retrospective study was obtained and informed consent was waived. Over a 16-month period (pril 2006 ugust 2007), seven teenage athletes (five girls and two boys) ranging in age from 14 years 4 months to 16 years 10 months (mean, 15 years 7 months) were referred for MRI evaluation of chronic hip, pelvis, or lower back pain and were shown to have an injury to the iliac crest apophysis. The clinical history and presenting symptoms were obtained from the clinic notes of the referring orthopedic surgeon or sports medicine physician and the patient radiology information system. The offending sporting activity and the duration of participation, if available, and the location of the symptoms were recorded. Each MRI study included at least one watersensitive sequence in either the coronal or the axial plane: a fat-suppressed fast spin-echo T2-weighted sequence (TR range/te range, 2,500 5,000/64 85; echo-train length, 6 8; matrix, ; slice JR:190, June

2 Hébert et al. Downloaded from by on 01/24/18 from IP address Copyright RRS. For personal use only; all rights reserved thickness, 3 4 mm; 1-mm slice gap) or fast spinecho inversion recovery weighted sequence (TR/ TE, 3,000/34; inversion time, 155 milliseconds; echo-train length, 8; matrix, ; slice thickness, 3 5 mm; 1- to 2-mm slice gap). These sequences included both iliac crests. Several children also underwent additional sagittal or oblique coronal water-sensitive sequences of the sympto matic side at the discretion of the interpreting radiologist. The MRI examinations were reviewed by two staff radiologists (with 15 and 18 years experience) by consensus to document the side of injury; appearance of the iliac crest apophysis, including the width of the adjacent physis on coronal images; and the signal characteristics of the physis, bone marrow, and surrounding musculature. dditional imaging studies performed for evaluation of the patient s symptoms and their prospective interpretations were also reviewed. The Risser index for each patient was recorded using available radiographs [7]. Follow-up radiographs, if obtained, were also reviewed. Results Table 1 summarizes the patients clinical information and MRI findings. Pain was present from 3 weeks to 1 year before presentation in five patients. In the remaining two children, the duration was not specified and was described only as chronic. Four athletes had pain over the affected iliac crest; however, three had only referred pain to the hip (n = 2) or lower back (n = 1). One patient TLE 1: Patient Characteristics and MRI Findings Patient Side (R/L) and Symptoms pophyseal No. ge Sex Sport(s) (Duration of Symptoms) Displacement Side 1 14 y 4 mo F Soccer R hip and iliac crest pain (chronic) 2 16 y 3 mo M aseball, cross-country R and L hip pain, R iliac crest pain (6 mo) Physeal Widening Width (mm) (patient 2 in Table 1) had bilateral symptoms but only unilateral imaging findings. One patient (patient 7 in Table 1) had unilateral symptoms, but bilateral asymmetric imaging findings. variety of offending sports were documented, the most common being shortdistance (track) or long-distance running (n = 4). The MRI findings showed mild physeal widening and increased signal intensity on water-sensitive sequences in all children (right, n = 5; left, n = 1; bilateral, n = 1), none of whom had substantial apophyseal displacement (Figs. 1 and 2). ll MRI examinations also showed varying degrees of bone marrow edema within the iliac crest. Five athletes showed edema within the adjacent musculature, including the gluteus medius, gluteus minimus, and iliacus muscles (Figs. 3 and 4). Six children underwent radiography of the pelvis 0 22 days before MRI examination that showed complete or near-complete ossification of the iliac apophysis (Risser type 4, n = 4; Risser type 3, n = 2). Three prospective radiographic interpretations suggested physeal widening of the iliac crest apophysis prospectively, and three were interpreted as normal. Retrospective review of all radiographs showed at least minimal widening of the iliac apophyseal physis. One child had widening of both iliac apophyseal physes (Fig. 2), although she was symptomatic initially on the right side only. One patient underwent radiography of the lumbar spine and nuclear scintigraphy for back pain 5 weeks before MRI examination, both of which were interpreted as normal. The iliac crest on the scintigram at that time was considered normal. Treatment consisted of 4 12 weeks of physical therapy that included activity modification to avoid running; strength training of the core postural muscles of the back, hips, and pelvis; and flexibility training for the iliopsoas, hamstring, and hip adductor and abductor muscles. efore being allowed to participate in sports activities, all patients were symptom-free with sport-specific activity and had no tenderness over the iliac crest. Follow-up conventional radiographs obtained in two patients at 6 weeks and 7 months after MRI showed improvement in the iliac apophyseal physeal widening (Figs. 2 and 5). However, one patient resumed dancing and presented 7 months later with contralateral hip pain. Discussion n apophysis with its apophyseal physis has anatomy similar to a secondary center of ossification of an epiphysis of a long bone and its adjacent transverse physis [8]. In growing children until the time of skeletal maturity, the hyaline cartilage of a physis, whether adjacent to an epiphysis or an apophysis, is the site Physeal Signal Intensity on Water-Sensitive Sequence ( or ) one Marrow Edema No R 3 Yes No Muscle Edema (Location) No R 4 Yes Yes (gluteus medius and minimus) 3 16 y 1 mo M Golf, track Lower back pain (7 mo) No R 4 Yes Yes (gluteus medius and minimus) 4 15 y 5 mo F Track L iliac crest pain (3 wk) No L 3 Yes Yes (gluteus medius) 5 14 y 10 mo F Track R hip and iliac crest pain No R 4 Yes No (10 mo) 6 15 y 6 mo F Soccer R hip pain (1 y) No R 3 Yes Yes (gluteus medius, iliacus) 7 16 y 10 mo F Dancing R hip pain (chronic) No R and L 5 and 4 Yes (bilateral) Yes (gluteus medius, bilateral) 1488 JR:190, June 2008

3 MRI of Iliac Crest pophysis Downloaded from by on 01/24/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-3-month-old male baseball player and cross-country runner with bilateral hip and right iliac crest pain (patient 2 in Table 1)., Frontal view of pelvis shows minimal widening of physis adjacent to right iliac crest apophysis (arrow); original study did not include complete iliac crests., Coronal fat-suppressed fast spin-echo T2-weighted image (TR/TE, 3,000/89) of pelvis shows bone marrow edema in right iliac crest. Physis (arrow) is minimally widened and of increased signal intensity compared with left side. of least resistance and is the most prone to injury. s adolescent participation in vigorous activities increases along with the development of greater muscle strength, acute and chronic physeal injuries are more likely to occur rather than injury to the stronger adjacent muscle, tendon, or ligament [9], especially at times of growth acceleration [10]. The apophyseal physis usually fuses later than the physes of long bones [8]. The iliac crest apophysis remains cartilaginous until adolescence. Ossification centers typically appear first along the anterolateral aspect of the iliac crest, at approximately years old. Ossification, which can develop from fragments, continues in a posteromedial direction toward the posterior iliac spine [7]. Fusion of the ossified apophysis to the iliac bone begins around the age of 15 years but can still occur up to the age of 25 years [2, 7]. The open physis measures up to approximately 2 mm in height. The lateral aspect of the iliac apophysis is the last to fuse. The iliac crest is the site of origin or insertion for the external and internal abdominal oblique muscles, transverse abdominis muscle, gluteus medius muscle, and the tensor fascia latae [6, 9]. The iliac crest apophysis can be the site of an acute avulsion, with a separation through the physis from the underlying iliac crest, such as from a sudden contraction of the abdominal muscles; it can be the site of a contusion from direct trauma, such as with a hip pointer in football [9]; or it can be subject to overuse and chronic trauma due to prolonged and repetitive muscle contraction, frequently termed apophysitis [11]. Injury to the iliac apophysis often results in pain over the site of injury; however, in children with chronic pain, the symptoms can be vague or referred elsewhere, as was seen in three of the seven children in our study. Chronic injury due to overuse from fitness and training activities in athletes is now more commonly recognized. Recurrent stress results in microtrauma to the physis, where the ability to repair is outpaced by the repetition of the insult [10]. Chronic tension or distraction on the growing physis has been studied experimentally. Stress injuries in athletes parallel the chondrodiastasis that results in increased metabolic activity of the growth plate or repeated microfractures with rapid healing [12]. Distraction from chronic and repetitive musculotendinous pull likely stimulates proliferation [13] or hypertrophy [14] of the chondrocytes and inflammatory cells [10] that results in the apparent physeal widening and adjacent muscle edema seen on MRI, and thus the term apophysitis. This traction force may be a different mechanical mechanism for physeal widening than the vascular disruption implicated in widening of the transverse physis of long bones described in child athletes [15]. pophyseal physes differ from transverse physes of long bones by their relatively slower rate of growth, fewer proliferative-layer cells, and increased longitudinal collagen fibers [10]. We speculate that the mechanism responsible for the MRI appearance of apophyseal widening without displacement in our group of children with a history of chronic pain may be similar to experimental models showing that repetitive stress results in hypertrophy of chondrocytes and possibly in microfractures not identifiable on MRI. Ogden [2] suggested that repetitive stress can result in failure of small chondroosseous interfaces. ll of the children in our study had partial or complete ossification of the iliac apophysis, possibly putting them at risk for this type of injury. Chronic apophyseal injury from overuse has been described throughout the body, including the ischial tuberosity, C Fig year-10-month-old female dancer with right hip pain (patient 7 in Table 1)., Frontal radiograph of pelvis shows symmetric irregularity and lacy widening of iliac crest apophyseal physes. Due to symmetry, this finding was not recognized prospectively., xial fat-suppressed T2-weighted image (TR/TE, 3,390/79) of pelvis shows bone marrow edema within iliac crests bilaterally, greater on right side than left side. Physeal widening (arrows), greater on right side than left side, is minimal. Minimal muscle edema is seen in both gluteus medius muscles. C, Frontal radiograph obtained 7 months after shows that irregular widening of iliac crest apophyses has improved. ilateral apophyses show symmetric fragmentation, which is likely developmental. JR:190, June

4 Hébert et al. Downloaded from by on 01/24/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-6-month-old female soccer player with 1 year of right hip pain (patient 6 in Table 1)., Frogleg lateral view of pelvis shows mild widening of right iliac apophysis (arrow). Normal fragmentation is seen on right. Gonadal shield overlies pelvis., xial fat-suppressed fast spin-echo T2-weighted image (TR/TE, 3,970/79) of pelvis shows edema within right iliacus muscle (straight arrow) and gluteus medius muscle (curved arrow). Fig year-1-month-old male golfer and track runner with lower back pain for 7 months (patient 3 in Table 1)., Coronal fat-suppressed fast spin-echo T2-weighted image (TR/TE, 4,110/76) of pelvis shows edema within adjacent muscles (straight arrow) and right iliac crest. There also is a mild widening of right apophyseal physis (curved arrow)., Sagittal fat-suppressed fast spin-echo T2-weighted image (3,090/71) of right iliac crest (asterisk) shows bone marrow and muscle edema. the anterior superior iliac spine and anterior inferior iliac spine, the medial epicondyle of the distal humerus, and the proximal tibial apophysis [9, 10]. Nuclear scintigraphy shows increased radiotracer uptake in the anterior iliac crest on blood pool and delayed images in children with chronic iliac apophyseal injury. This technique has been used when the clinical findings are atypical and radiography is unrevealing [6]. s in our series, MRI can be used to identify or confirm a diagnosis, usually after radiography has been performed. In some athletes in our study, the radiographic abnormalities were not identified prospectively, particularly when the clinical history submitted suggested hip or back injury or the findings were symmetric bilaterally. In three children, mild widening of the apophyseal physis was identified prospectively on radiography and MRI was requested to confirm the diagnosis and evaluate the extent of edema before restricting athletic activity. MRI of chronic repetitive stress to the iliac apophysis in the adolescents in our study showed mild physeal widening of 3 5 mm, increased signal intensity of the physis on water-sensitive sequences, and bone marrow edema and, frequently, associated muscle edema. Displacement of the apophysis was not seen. The patients spanned only a 2.5-year age interval during adolescence when the apophysis is undergoing or has completed ossification and corresponding to the time when growth acceleration is thought to result in relative weakening and decreased elasticity of physeal cartilage [2, 4, 10]. The treatment for injury to the iliac crest, like that for other apophyses of the pelvis, is usually nonsteroidal antiinflammatory drugs, Fig year-10-month-old female track runner with right hip and iliac crest pain (patient 5 in Table 1)., Frogleg lateral radiograph shows mild widening of apophysis (arrow) of right iliac crest. This finding was not recognized at time of initial interpretation. Gonadal shield overlies pelvis., xial fat-suppressed T2-weighted image (TR/TE, 2,316/68) of pelvis shows minimal bone marrow edema and physeal widening (arrow) of right iliac apophysis. No muscle edema is seen. C, Frontal radiograph obtained 7 weeks after shows improvement in right iliac crest apophyseal widening. C 1490 JR:190, June 2008

5 MRI of Iliac Crest pophysis Downloaded from by on 01/24/18 from IP address Copyright RRS. For personal use only; all rights reserved activity modification, and rehabilitation [16]. Running is avoided and emphasis is placed on strengthening core or postural muscles and improving flexibility of the long muscles crossing the pelvis. The child may gradually return to athletic activity after resolution of clinical symptoms, usually after approximately 4 6 weeks [17]. Ultimately, symptoms will remit as the iliac crest apophysis fuses to the ilium. Conventional radiography occasionally is used to confirm resolution as symptoms improve. In summary, in adolescent athletes with a history of prolonged, sometimes vague symptoms involving the pelvis, hip, or lower back and who still have open pelvic apophyseal physes, chronic stress injury to the iliac crest apophyses should be included in the diagnostic possibilities. Consideration for a possible stress injury to the iliac crest apoph ysis should alert one to carefully evaluate this region on radiography. We suggest that MRI is useful to make the diagnosis if radiographs are indeterminate or if confirmation and evaluation of the extent of the injury are needed before altering sports activities, often in high-level athletes. The MRI appearance of chronic repetitive stress injury to the apophysis of the iliac crest includes widening of the affected apophyseal physis with adjacent bone marrow and muscle edema. References 1. El-Khoury GY, Daniel WW, Kathol MH. cute and chronic avulsive injuries. Radiol Clin North m 1997; 35: Ogden J. Skeletal injury in the child, 3rd ed. New York, NY: Springer-Verlag, 2000:407, Rossi F, Dragoni S. cute avulsion fractures of the pelvis in adolescent athletes: prevalence, location and sports distribution of 203 cases collected. Skeletal Radiol 2001; 30: Pisacano RM, Miller TT. Comparing sonography with MR imaging of apophyseal injuries of the pelvis in four boys. JR 2003; 181: ksoy, Ozturk K, Ensenyel CZ, Kara N. vulsion of the iliac crest apophysis. Int J Sports Med 1998; 19: Rockett JF. Three-phase radionuclide bone imaging in stress injury of the anterior iliac crest. J Nucl Med 1990; 31: Risser JC. The iliac apophysis: an invaluable sign in the management of scoliosis. Clin Orthop 1958; 11: Metzmaker JN, Pappas M. vulsion fractures of the pelvis. m J Sports Med 1985; 13: Combs J. Hip and pelvis avulsion fractures in adolescents. Phys Sports Med 1994; 22: Micheli LJ, Fehlandt F Jr. Overuse injuries to tendons and apophyses in children and adolescents. Clin Sports Med 1992; 11: Julsrud ME. Iliac apophysitis and a review of the osteochondroses. J m Podiatr Med ssoc 1985; 75: ldegheri R, Trivella G, Lavini F. Epiphyseal distraction: chondrodiastasis. Clin Orthop Relat Res 1989; 241: lberty, Peltonen J. Proliferation of the hypertrophic chondrocytes of the growth plate after physeal distraction: an experimental study in rabbits. Clin Orthop Relat Res 1993; 297: pte SS, Kenwright J. Physeal distraction and cell proliferation in the growth plate. J one Joint Surg r 1994; 76: Laor T, Wall EJ, Vu LP. Physeal widening in the knee due to stress injury in child athletes. JR 2006; 186: Diehl JJ, est TM, Kaeding CC. Classification and return-to-play considerations for stress fractures. Clin Sports Med 2006; 25: Clancy WG, Folitz S. Iliac apophysitis and stress fractures in adolescent runners. m J Sports Med 1976; 4: JR:190, June