February 2007, VOLUME 188
NUMBER 2

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February 2007, Volume 188, Number 2

Musculoskeletal Imaging

Clinical Observations

Hip Pain in Renal Transplant Recipients: Symptomatic Gluteus Minimus and Gluteus Medius Tendon Abnormality as an Alternative MRI Diagnosis to Avascular Necrosis

+ Affiliations:
1Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, University of Bern, Freiburg Strasse, 24 Thunstrasses, Bern CH-3010, Switzerland.

2Department of Nephrology and Hypertension, Inselspital, University of Bern, Bern, Switzerland.

3Department of Orthopedic Surgery, Inselspital, University of Bern, Bern, Switzerland.

4Department of Nephrology, Fremantle Hospital, University of Western Australia, Perth, WA, Australia.

5Department of Radiology, University of California San Francisco, San Francisco, CA.

Citation: American Journal of Roentgenology. 2007;188: 515-519. 10.2214/AJR.05.1097

ABSTRACT
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OBJECTIVE. The purpose of this study was to review the diagnosis on MRI and radiography of 24 renal transplant recipients with hip pain suspicious for avascular necrosis and to investigate whether there is an association between kidney transplant patients with end-stage renal disease and symptomatic gluteus minimus and medius tendon abnormality.

CONCLUSION. Symptomatic gluteus minimus and medius tendon lesions and abnormalities can occur in renal allograft recipients. The MRI findings of this entity allow an alternative diagnosis in this patient population.

Keywords: avascular necrosis, glucocorticoid treatment, hip, kidney disease, MRI, musculoskeletal imaging, renal transplantation, tendons

Introduction
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Bone and musculoskeletal pain is a common problem after kidney transplantation and occurs in one third of all transplant recipients [1]. The causes of this condition include preexisting uremic osteodystrophy, persisting hyperparathyroidism, kidney transplant malfunction, obesity, and treatment with cyclosporine and glucocorticoids [2]. A frequent disease manifestation is hip pain syndrome with an increased incidence of avascular necrosis of the femoral heads [1, 2].

Hip pain is a frequent complication after renal transplantation with an increased incidence of avascular necrosis of bone in this population. The failure to detect a bone lesion suggests the presence of a soft-tissue abnormality, but to date this aspect has not been appropriately reported. In some renal transplant patients diagnostic imaging fails to provide an osteal explanation for the pain, thus raising the possibility of a soft-tissue abnormality. Symptomatic gluteal tendon lesions of the hip have been described previously in elderly women [3] and in patients with buttock, lateral hip, or groin pain [4].

We reviewed the MRI appearances of symptomatic hip pain in a cohort of renal transplant recipients, who were evaluated for presumptive avascular necrosis of the hip. To our knowledge, this is the first description of an association between symptomatic gluteus minimus and medius tendon abnormality and kidney transplant recipients with end-stage renal disease.

Subjects and Methods
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Twenty-four consecutive patients with a functioning kidney after renal allograft underwent MRI for new-onset hip pain clinically suspicious for avascular necrosis. The onset of hip pain relative to the time from allograft transplantation was nonspecific but was more than 6 months in all patients. The patients ranged in age from 26 to 71 years, with a mean age of 57.1 years. There were eight men and 16 women. Written informed consent was obtained from patients before imaging, and ethics board review was obtained.

All patients underwent transplantation during the previous 15 years and regularly attended the outpatient clinic of a subspecialized university unit between the years 1998 and 2002. The immunosuppressive regimen was based on cyclosporine and glucocorticoids. For each patient, a complete renal disease history, laboratory results, and detailed clinical review regarding the hip pain were available. Surgical results were available in three patients with avascular necrosis who had undergone prosthetic hip replacement. MR images (n = 24, all with contrast medium [gadopentetate dimeglumine, Magnevist, Schering]) and radiographs (n = 19) were prospectively reviewed by two radiologists in consensus, one senior musculoskeletal radiologist and one in training.

MRI was performed using a 1.5-T scanner (Signa, GE Healthcare) in all patients and included the whole pelvis. The MRI protocol consisted of coronal STIR (TR range/TE range, 4,652-5,680/15-30) and T1-weighted (480-680/14-20) images, axial T1-weighted (430-600/12-15) and T2-weighted fat-saturated (3,200-2,400/80-96) images, and T1-weighted fat-saturated images after the administration of IV contrast material in the coronal and axial planes (510-554/12-14).

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Fig. 1A —66-year-old woman with bilateral hip pain suspicious for avascular necrosis complicating renal transplantation with MRI of dual findings. Coronal T1-weighted image (TR/TE, 360/17) shows bilateral avascular necrosis of femoral head, marked bilateral fatty atrophy of gluteus minimus muscles, and right-sided greater trochanter bursitis (arrow).

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Fig. 1B —66-year-old woman with bilateral hip pain suspicious for avascular necrosis complicating renal transplantation with MRI of dual findings. Axial T2-weighted fat-saturated image (3,740/96) shows bilateral avascular necrosis. Crescent sign is noted on left (short arrow), and right-sided tendon abnormalities (long arrow) are seen.

The MR images were analyzed for the presence of hip abnormality—in particular, for avascular necrosis and gluteal tendon and greater trochanteric region findings. Avascular necrosis was defined as the presence of focal altered bone marrow signal intensity with the presence of geographic double lines. Partial tear or tendinosis of the gluteus minimus and medius tendons was diagnosed when the tendons appeared thickened or had irregular signal intensity on T2-weighted and STIR images, and a complete tear was diagnosed when there was an absence of continuity of the tendon from the greater trochanter. Osseous spurring, small or large bone erosions, irregularities, and altered bone marrow signal intensity of the greater trochanter were noted as well as trochanteric bursitis. The muscle quality of the gluteus medius and minimus muscles was reviewed and determined to be normal or to show evidence of marked fatty atrophy. Features suggesting possible insufficiency fractures of the pelvis, sacroiliitis, and osteitis pubis were also reviewed. Both radiologists were blinded to the site of hip pain.

Results
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Nineteen of the 24 kidney transplant recipients undergoing MRI for bone pain of the femoral head had evidence of either avascular necrosis or gluteal tendon abnormalities. MRI revealed avascular necrosis in eight (33%) patients (unilateral, n = 4; bilateral, n = 4 [Fig. 1A, 1B]). Thirteen patients (54%) of the study group had gluteus minimus and medius tendon abnormalities, with MRI findings consistent with tendinosis or a partial tear in 12 patients (92%) and a complete tear avulsion in one patient (8%) (Table 1 and Figs. 2A, 2B, 2C, 2D, 2E, 2F and 3A, 3B, 3C). Two of these patients had dual abnormality with bilateral gluteus minimus and medius tendon entities (Fig. 1A, 1B), one of whom had a unilateral partial tear of the gluteus minimus tendon.

TABLE 1: Baseline Characteristics and Findings in 24 Renal Transplant Patients with Hip Pain

In addition, in patients with enthesopathy there was marked fatty atrophy of the gluteus minimus muscle (n = 5) and gluteus medius muscle (n = 1), enthesopathy of the greater trochanter with small bone erosions and bone spurring (n = 6), and greater trochanteric bursitis (n = 4) (Table 1). The greater trochanter bone marrow signal was normal in all cases in this series. Marked gluteus minimus muscle atrophy was also noted in two patients without gluteal tendon entities. Other abnormalities (n = 5) included presumed amyloid of the hip (n = 1) (being associated with large focal sclerotic rimmed capsule-oriented erosions and decreased in signal intensity on T2 weighting), nonspecific crystal arthropathy of the hip (n = 1), degenerative joint disease (n = 2), and one patient without morphologic pain correlation. There was no evidence of gout or rheumatologic disorders, which were ruled out on the basis of laboratory test results, in the patient group.

Radiographs (n = 19) revealed bilateral calcification adjacent to the greater trochanter in three patients with and in one patient without gluteal tendon abnormalities. There were no cases of insufficiency fractures within the pelvis or evidence of sacroiliitis or osteitis pubis.

There was positive clinical correlation to the side of hip pain in nine patients with gluteal tendon entities (n = 13 [70%]). There was a positive correlation in the avascular necrosis patient group (n = 8) to the side of pain in 50% (n = 4). Imaging findings and correlation with clinical data are summarized in Table 1.

Regarding the patients with gluteal tendon abnormalities, clinical pain evaluation revealed a variety of pain quality. All patients (n = 13) had pain on weight-bearing, seven patients reported pain during the night, and six patients had focal tenderness and pain directly over the greater trochanter. Seventy percent of these patients were female (n =9) compared with a lower incidence in the male group (n = 4 [30%]). A higher incidence of gluteal tendon entities was found in patients without avascular necrosis (n = 11) and an elevated body mass index (BMI) (> 25 kg/m2; n = 8 [72%]). The incidence of persisting hyperparathyroidism after transplantation (parathyroid hormone [PTH] > 100 pg/mL; n =6) in the same patient group (n = 11) was 55%. MRI findings of avascular necrosis were confirmed surgically in three cases that required hip replacement.

In the five patients without evidence of avascular necrosis or enthesopathy, the possible cause of pain was amyloid of the hip (n =1; classic MRI features), nonspecific crystal arthropathy of the hip (n = 1; histologic result), degenerative joint disease (n = 2; both with classic MRI findings and one with a surgical correlation), and one patient without any morphologic pain correlation (Table 1).

Discussion
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We have analyzed the MRI findings in patients after renal transplantation with hip pain suspicious for avascular necrosis of the femoral heads. The incidence of avascular necrosis in renal allograft recipients treated with glucocorticoids is increased and is a wellknown complication after allograft transplantation [1, 2, 5, 6]. Causes are thought to be related to glucocorticoid treatment, hyperparathyroidism, fibrinolytic activity imbalance by genetic PAI-1 (plasminogen activator inhibitor-1) determination, and metabolic or hormonal disorders [6, 7]. Stress fractures of the femoral head may mimic avascular necrosis appearances and are described in this patient group [8, 9]. We had no cases of stress or insufficiency fractures within the proximal femur in our series, although after this study we did see some cases.

Apart from avascular necrosis, MRI-defined gluteal tendon abnormality was a common cause of hip pain in our patient group.

Usually one third of all patients after organ transplantation develop bone and musculoskeletal pain [1]. Gluteal tendon abnormalities in this patient group have not been previously described, to our knowledge. Tears and tendinopathy of the gluteus medius and minimus tendons are potentially an underrecognized source of hip pain. The exact cause of gluteal tendon abnormality in this patient group is unknown and is probably due to a combination of several features. Three patients had evidence of soft-tissue calcification adjacent to the greater trochanter, raising the possibility of calcium hydroxyapatite deposition disease [10]. All patients with tendon entities had pain on weight-bearing, suggesting a mechanical cause, and seven of 13 patients had notable night pain at rest, suggesting an inflammatory component. Six patients had focal tenderness and pain directly over the greater trochanter.

Gluteal tendon abnormalities seem to be the cause of hip pain in our series. The MRI findings had a high correlation with the side of pain and with the specific clinical examination with focal greater trochanter tenderness. Other intraosseous, intraarticular, and softtissue paraarticular entities were excluded on the basis of MRI findings.

Proposed causes of the gluteal tendon abnormality in this group also include preexisting uremia with renal failure and associated calcium phosphate imbalance, steroid-related tendon abnormalities, calcium pyrophosphate or other calcium deposition disease, dialysisrelated arthropathy owing to amyloid deposition, or an inflammatory enthesopathy or enthesitis [11-13]. The latter was thought to be present in one patient in our series given the large, focal sclerotic-rimmed bone erosions associated with decreased signal intensity on T2 weighting, as has been described in terms of shoulder rotator cuff abnormality in longterm dialysis recipients [11].

There is a wide overlap of the causes of avascular necrosis after kidney transplantation and of possible greater trochanter tendon abnormalities, thus complicating reliable differentiation. Because hyperparathyroidism and an increased BMI are established predisposing factors for avascular necrosis, we found an increased incidence of tendon entities, with 55% being associated with hyperparathyroidism and an increased BMI in 72% of our patients.

Biomechanical instability and overuse syndrome may also contribute because the hip joint, like the glenohumeral joint, has a wide range of motion. Analogous to the abnormality of the rotator cuff tear of the shoulder, the term “rotator cuff tear of the hip” has been described by Bunker et al. [14]. The proposed mechanism is an overuse and age-related degeneration mechanism, with tears occurring initially within the gluteus minimus and medius tendons probably starting within gluteus minimus near the digital fossa at the anterior aspect of the greater tuberosity [14]. Chung et al. [3] and Kingzett-Taylor et al. [4] also proposed a multifactorial cause for “greater trochanteric pain syndrome” in their series of largely elderly and middle-age women. At surgery, these tendon tears have rolled, mature edges, often associated with free fluid in the trochanteric bursa with bone deep in relation to the tear having reactive sclerosis with osteophyte-like formation on the anterior edge [14]. With only a very small operative series, resection of sclerotic and osteophytic bone with débridement and possible direct tendon reattachment is suggested as being potentially helpful in patients with hip weakness and a Trendelenburg gait [14].

Beck et al. [15] developed a gluteus minimus and greater trochanter bone model and determined that the gluteus minimus acts as an abductor and internal or external rotator of the femur, stabilizing the head of the femur in the acetabulum by tightening the capsule. Kumagai et al. [16] described altered MR signal intensities when they evaluated the hip abductor muscles during weight-bearing and exercise with a dynamometer and integrated electromyography; their results indicated that gluteus minimus and medius muscles play an important biomechanical role in hip abduction, gait, and pelvic stabilization. Gluteus medius and minimus tendon abnormalities have also been described in elderly women without allograft transplantation and are described in isolated case reports in the literature as a spontaneous entity [17].

We hypothesize that gluteus medius and minimus tendon abnormality is frequently a result of predisposing conditions and that the incidence of this entity seems to be increased after kidney transplantation. In former MRI series, the prevalence of gluteal tendon abnormalities in nonallograft kidney patients is described in 14% in the series of Kingzett-Taylor et al. [4] and 33% in the study of Cvitanic et al. [18]. The data in patients who have not undergone kidney transplantation are heterogeneous, and to the best of our knowledge, no specific data have been reported in the literature regarding these findings for patients after renal allograft transplantation.

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Fig. 2A —59-year-old woman with right-sided hip pain and clinical suspicion of avascular necrosis after renal transplantation, with right-sided gluteal tendon abnormalities. Radiographs were negative for softtissue calcification. Coronal T1-weighted image (TR/TE, 480/13) shows focal thickening of gluteus minimus and medius tendons on right with gluteus minimus muscle fatty atrophy.

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Fig. 2B —59-year-old woman with right-sided hip pain and clinical suspicion of avascular necrosis after renal transplantation, with right-sided gluteal tendon abnormalities. Radiographs were negative for softtissue calcification. Coronal STIR image (3,400/14) shows inflammatory reaction around focally thickened gluteus minimus and medius muscle tendons (arrow).

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Fig. 2C —59-year-old woman with right-sided hip pain and clinical suspicion of avascular necrosis after renal transplantation, with right-sided gluteal tendon abnormalities. Radiographs were negative for softtissue calcification. Axial T1-weighted fat-saturated images after administration of IV contrast medium (580/14) shown on consecutive images reveal right-sided greater trochanter tendon abnormalities (arrows) and softtissue reaction.

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Fig. 2D —59-year-old woman with right-sided hip pain and clinical suspicion of avascular necrosis after renal transplantation, with right-sided gluteal tendon abnormalities. Radiographs were negative for softtissue calcification. Axial T1-weighted fat-saturated images after administration of IV contrast medium (580/14) shown on consecutive images reveal right-sided greater trochanter tendon abnormalities (arrows) and softtissue reaction.

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Fig. 2E —59-year-old woman with right-sided hip pain and clinical suspicion of avascular necrosis after renal transplantation, with right-sided gluteal tendon abnormalities. Radiographs were negative for softtissue calcification. Axial T1-weighted fat-saturated images after administration of IV contrast medium (580/14) shown on consecutive images reveal right-sided greater trochanter tendon abnormalities (arrows) and softtissue reaction.

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Fig. 2F —59-year-old woman with right-sided hip pain and clinical suspicion of avascular necrosis after renal transplantation, with right-sided gluteal tendon abnormalities. Radiographs were negative for softtissue calcification. Axial T1-weighted fat-saturated images after administration of IV contrast medium (580/14) shown on consecutive images reveal right-sided greater trochanter tendon abnormalities (arrows) and softtissue reaction.

In our small series, the prevalence of gluteal tendon abnormality was increased with 54% of patients, with a mean age of 57.1 years, which is less than the mean age reported in other series with study groups composed of patients with a mean age of 64 years [4] and 70 years [18]. This age difference may support our hypothesis of an association between symptomatic gluteal tendon entities and chronic renal failure patients after renal allograft transplantation because the prevalence of gluteal tendon abnormality is higher than in patients reported in the literature without a history of renal transplantation. The general incidence of this entity in patients with chronic renal disease remains unknown because only symptomatic patients after kidney transplantation were investigated in our patient group. The asymptomatic patients did not undergo MRI of the pelvis before kidney transplantation.

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Fig. 3A —65-year-old woman with bilateral hip pain clinically suspicious for avascular necrosis of hip after renal transplantation, with bilateral gluteal tendon abnormalities. Conventional radiograph shows bilateral calcifications adjacent to greater trochanter (arrows).

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Fig. 3B —65-year-old woman with bilateral hip pain clinically suspicious for avascular necrosis of hip after renal transplantation, with bilateral gluteal tendon abnormalities. Axial T1-weighted fat-saturated image after administration of contrast medium (TR/TE, 555/12) shows right-sided focal calcification within gluteus minimus (arrow) and medius muscles and subtle irregularity of greater trochanter.

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Fig. 3C —65-year-old woman with bilateral hip pain clinically suspicious for avascular necrosis of hip after renal transplantation, with bilateral gluteal tendon abnormalities. Coronal T1-weighted fat-saturated image after administration of contrast medium (562/20) shows bilateral greater trochanteric tendon abnormalities (arrows).

The pitfalls of this study include the small size of the series and lack of complete surgical correlation. However, MRI has been shown to be very useful in identifying gluteal tendon abnormality [18]. Identification of a T2 hyperintensity craniad to the greater trochanter region has the highest sensitivity and specificity for gluteal tendon tears with 73% and 95%, respectively [18]. The patients in the gluteal tendon abnormality group were conservatively treated with pain relief and physiotherapy; thus, surgical correlation was not available.

In conclusion, being aware of an association of kidney transplant patients with endstage renal disease and symptomatic gluteus minimus and medius tendon abnormality and the imaging findings—which may otherwise be overlooked—may allow an alternative diagnosis for hip pain in this patient population.

Address correspondence to S. E. Anderson ().

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