Magnetic resonance imaging in osteomalacic ... - Clinical Radiology

Clinical Radiology (2005) 60, 105–111

Magnetic resonance imaging in osteomalacic insufficiency fractures of the pelvis K. Kanberoglua,*, F. Kantarcia, D. Cebia, M.H. Yilmaza, S. Kurugoglua, A. Bilicib, H. Koyuncuc Departments of aRadiology, bInternal Medicine, cPhysical Medicine and Rehabilitation, Cerrahpasa Medical Faculty, Istanbul University, Istanbul, Turkey Received 3 March 2004; received in revised form 13 April 2004; accepted 30 April 2004

KEYWORDS Osteomalacia; Magnetic resonance (MR); Fractures; Insufficiency; Pelvis

AIMS: To report the magnetic resonance imaging (MRI) findings of osteomalacic insufficiency fractures of the pelvis. MATERIALS AND METHODS: In all, 12 persons presenting with chronic pelvic pain and with a definitive diagnosis of osteomalacia (OM) were enrolled in this study. Radiological work-up included direct radiographs (nZ12), computed tomography (nZ5), scintigraphy (nZ12) and MRI (nZ12). The location of the insufficiency fractures and corresponding MRI appearances were evaluated. Depending on the presence or absence of signal intensity around the fractures, the lesions were grouped into active and chronic forms. RESULTS: A total of 34 insufficiency fractures were depicted on imaging studies. MRI demonstrated 33 of the lesions. All the insufficiency fractures were seen as a hypointense lines or fissures on T1- and T2-weighted and STIR MR images. There was a high frequency of insufficiency fractures at the sacrum and iliac bone (16/34, 47%). Overall, 11 chronic-type (no abnormal signal intensity around the fissure) and 22 active-type (abnormal signal intensity around the fissure) insufficiency fractures were detected by MRI. Follow-up MR examinations of 2 subjects showed that abnormal signal intensity had disappeared after appropriate treatment. CONCLUSION: The results of this study showed that the iliac and sacral bones are frequently involved in patients with OM. MRI can determine the clinical activity of the disease, and can monitor the response to treatment of the active type of insufficiency fractures. q 2005 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction Insufficiency-type stress fractures occur in structurally weakened bone that cannot withstand the stresses of normal activity. The predisposing condition for an insufficiency fracture is usually osteoporosis; other metabolic diseases, metastatic neoplasms, long-term exposure to corticosteroids, * Guarantor and correspondent: K. Kanberoglu, Department of Radiology, Cerrahpasa Medical Faculty, Istanbul University, 34300-Istanbul, Turkey. Tel.: C90-212-4143176; fax: C90-2124143167. E-mail address: [email protected] or fatihkan@ hotmail.com (K. Kanberoglu).

and bone atrophy after irradiation may also be contributing factors.1,2 Chronic pelvic pain is the most common presenting symptom and the clinical history often suggests the leading pathological event. The sacrum, sacroiliac joints and iliac bones are the major weight-bearing structures of the body and are therefore prone to such fractures.3,4 Insufficiency fractures in the pelvic region mostly involve the sacrum, and there are numerous reports on sacral insufficiency fractures.1–4 The other bones are also affected and so recent studies have used the general term ‘pelvic insufficiency fractures’.5–8 The initial radiological work-up in patients with chronic pelvic pain and clinical suspicion of pelvic

0009-9260/$ - see front matter q 2005 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2004.04.021

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insufficiency fractures includes direct radiographs. However, the findings on such films are frequently indefinite or misleading.4,9 There are numerous reports regarding the magnetic resonance imaging (MRI) appearances of pelvic insufficiency fractures, mostly of osteoporotic, radiation-induced or metastatic insufficiency fractures.10–12 As MRI becomes more available to persons with chronic pelvic pain, it is important to be aware of the differential MR appearances of such fractures; the differentiation of metastatic from benign causes is clinically important and affects the approach to treatment.10,11,13 Osteomalacia (OM) is also a cause of pelvic insufficiency fractures. The classic radiographical findings of OM in the pelvic region are pseudofractures or Looser’s zones that occur typically in the pubic rami.14 In our series of cases of OM, we addressed the high rate of insufficiency fractures in the pelvic region. To the best of our knowledge, the MR appearances of pseudofractures and insufficiency fractures in the pelvic region due to OM have not previously been described. The purpose of this study was to report our experience with the MRI appearances of insufficiency fractures at the pelvic region secondary to OM.

Materials and methods This was a retrospective study and included 12 individuals, 10 women and 2 men, with a definitive clinical, radiological, biochemical and histopathological diagnosis of OM with MR examinations in addition to direct radiographs. The mean age of the participants was 59.7 years (range 30–82 years) and informed consent was obtained. Institutional ethics committee approval was not deemed to be necessary by the committee chairperson. The presenting symptom was chronic pelvic pain in all cases. Additionally, there was pain in the left thigh and hip joint in 2 cases; 1 subject had pelvic deformity and presented with pain during sexual intercourse. For 8 persons the precipitating factor for the development of OM was decreased sun exposure. This group comprised mostly women who were wearing traditional long garments and veils (nZ7). Intestinal malabsorption (nZ3), and gastrectomy due to peptic ulcer disease (nZ1) were predisposing factors in the remainder. None of the participants had a history of a primary neoplasm, exposure to excessive doses of radiation (radiotherapy) or trauma. Laboratory investigation consisted of measuring the calcium, phosphorus and alkaline phosphatase serum levels. Anterior iliac crest bone biopsy was performed in all cases and OM

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was diagnosed if the osteoid volume was greater than 10% and there was an abnormal tetracycline uptake. Direct radiographs of the pelvis, spine, rib cage and upper and lower extremities were obtained in all cases, and for some computed tomography (CT) (nZ5), bone scintigraphy (nZ12), and MRI (nZ12) were performed. The MR examinations were carried out before (nZ5) and/or during (nZ5) the treatment for OM, and 2 patients had follow-up MRI after treatment. The MRI was carried out using a 1 T (Magnetom Impact, Siemens, Erlangen, Germany) or 1.5 T (Magnetom Symphony, Siemens, Erlangen, Germany) MR unit and a body coil. All sections were 5 mm or 7 mm thick with an intersection gap of 1.0– 2.5 mm. A matrix 256!198 and two signals averaged were used. The examination protocol included T1- (TR: 400–650 msn, TEZ15–20 msn) and T2- (TR: 3500–4500 msn, TEZ90–110 msn) weighted spin echo sequences on axial and coronal planes. STIR (TR: 6600 msn, TE: 80 msn, inversion recovery: 150 msn) images on axial and coronal planes were obtained as well. In 2 subjects the left hip joint and the left femur were included in the examination protocol. The appearances of the insufficiency fractures on T1- and T2-weighted and STIR MR examinations were evaluated and abnormal signal intensities present in the bone adjacent to the insufficiency fractures were noted. The insufficiency fractures on MR examination were considered chronic (sequel or healed) if there was no abnormal signal intensity adjacent to the fissure line on T2-weighted and STIR images. They were considered active if there was abnormal signal intensity adjacent to the fracture on T2-weighted and STIR images.

Results Laboratory examination The laboratory results showed decreased levels of serum calcium in 50% and serum phosphorus in 58.3% of participants and an increased level of alkaline phosphatase in 50%. The classical biochemical changes, comprising low serum calcium and phosphorus together with elevated alkaline phosphatase levels, was seen in only 4 patients (4/12, 33.3%).

Location of the lesions In all, 34 insufficiency fractures were observed on imaging studies (direct radiography, CT,

MRI of osteomalacic insufficiency fractures

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scintigraphy and MR): 16 in the pubic rami, 9 in the sacrum, 7 in the iliac bones, 1 in the head of the femur and 1 in the diaphysis of the femur. The age and gender of the participants, results of biochemical assays and location of lesions are summarized in Table 1.

Radiological appearances other than MRI Direct radiographs of 8 subjects revealed 16/34 (47%) lesions, including all of the insufficiency fractures involving the pubic rami but none of those involving the femur, sacrum or iliac bones. These were detected by MRI, except for 1 insufficiency fracture of the right iliac bone which was seen on CT. Generalized osteopenia was recognized on plain radiographs by the reduced secondary trabeculation in 5 subjects. The initial scintigraphic examinations depicted an increased activity in all cases in the affected areas. CT examination showed 13 insufficiency fractures in 5 subjects.

MRI appearances All the insufficiency fractures were seen as a hypointense line or fissures on T1- and T2-weighted and STIR MR images. They were considered chronic (nZ11) if there was no pathological signal intensity change around the hypointense fissure on any image (Fig. 1) or active (nZ22) if there was an increased signal intensity around the hypointense fissure on T2-weighted and STIR MR images (Fig. 2). In 2 cases with active insufficiency fractures there was accompanying soft tissue oedema on T1- and T2weighted and STIR MR images. When compared with

Table 1 Case

1 2 3 4 5 6 7 8 9 10 11 12

Figure 1 30-year-old woman with gross pelvic deformity and history of chronic pelvic pain and dyspareunia. (a) CT examination on axial plane reveals bilateral insufficiency fractures (pseudofractures) of the ramus pubis. (b) Axial T2- weighted MRI shows hypointense fissures and deformity of the ramus pubis bilaterally. Note absence of abnormal signal intensity around the fissures (chronic type of insufficiency fracture).

Age in years and gender of participants, biochemical analysis and location of the lesions Age Sex Aetiology

81 82 70 30 38 80 65 35 78 55 50 53

F F F F F M F F F M F F

Laboratory findings a

Y sun exposure Y sun exposurea Y sun exposurea Y sun exposurea Intestinal malabsorption Y sun exposure Y sun exposurea Intestinal malabsorption Y sun exposurea Intestinal malabsorption History of gastrectomy Y sun exposurea

Location of insufficiency fractures

Ca

P

ALP Ramus pubis

Sacrum

Ilium

Other

N N N Y Y N Y N Y Y Y N

N N N Y Y Y Y N Y Y Y N

N [ N [ [ [ N N [ N [ N

– R Bilateral – – Bilateral – Bilateral R R – –

R – – – Bilateral – – – – – Bilateral Bilateral

– – – – – – L caput femori – L femur diaphysis – – –

R inf L sup R sup R, L sup and inf L sup – R,L sup – – – R,L sup R, L sup and inf

M, male; F, female; Y, decreased; Ca, serum calcium; P, serum phosphorus; ALP, serum alkaline phosphatase; N, normal; [, increased; R, right; L, left; sup, superior; inf, inferior. a These patients were wearing long garments and veils.

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Figure 2 53-year-old female woman who presented with chronic pelvic pain and history of decreased sun exposure (she was wearing long garments and veils). (a) Pelvic radiograph reveals insufficiency fractures at the superior and inferior pubic rami (white arrowheads). No pathological lesion was seen in the iliac and sacral bones. (b) Coronal T2weighted MRI shows insufficiency fractures as hypointense fissures (arrows) without pathological signal intensity (sequel or healed fractures) at the pubic rami. (c) Coronal T1 and (d) T2-weighted MRI demonstrate a hypointense fissure line (white arrow) with pathological signal intensity (white arrowhead) at the right iliac bone (active type of insufficiency fracture). (e) Second-year follow-up coronal STIR MRI depicts the hypointense fissure and disappearance of the pathological signal intensity (white arrowhead). (f) Follow-up MR coronal STIR image also depicts a new hyperintense lesion at the left ramus pubis (arrowhead). Note the sequel or healed fracture lines at the pubic rami on this image (white arrows).


scintigraphic examinations, all the active insufficiency fractures demonstrated increased radionuclide uptake on MRI. The chronic insufficiency fractures did not show radionuclide uptake on follow-up scintigraphic examinations.

Location and MRI appearance Of the 12 insufficiency fractures of the pubic rami, 5 were chronic and 7 were active. Of the 15 insufficiency fractures of the sacrum and iliac bones, 2 were chronic and 13 were active. All the insufficiency fractures that involved the head and diaphysis of the femur were of active type. In 4 cases, the preliminary diagnosis of OM was suggested by the MR examinations. These participants were wearing long garments and veils and therefore had a decreased exposure to sunlight.

Follow-up In 2 cases follow-up MR examinations were available (cases 7 and 12) after treatment. These revealed that the T2-weighted hyperintense signal intensity changes around the hypointense fissures previously found on MRI (Fig. 2e) had disappeared. In case 12, however, there was a new hyperintense lesion at the ramus pubis (Fig. 2f).

Discussion OM is a generalized bone disorder characterized by impairment of mineralization, leading to accumulation of unmineralized matrix or osteoid in the skeleton.18 The disease affects mainly the elderly and less often middle-aged women. There are more than 50 diseases that may induce OM.19–21 Intestinal malabsorption, and hypovitaminosis D due to lack of sun exposure and inadequate intake of dairy products, are the most common causes of OM. Persons with OM usually present with non-characteristic generalized or localized bone pain involving the spine, rib cage, pelvis and shoulder girdle; this may be associated with polyarthralgias and/or proximal muscle weakness.22 A high index of suspicion is usually necessary for an early diagnosis, as often OM may present with protean radiographical manifestations. The variable presentation may range from normal direct radiographs to florid osteopenia and fractures; the biochemical changes also may be non-specific. The definitive diagnosis may be made by anterior iliac crest biopsy.23 The radiological diagnosis of OM is difficult and many changes seen on the radiographs are non-

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specific. The classical radiographical appearances of OM are relatively rare and may not be found in the early stages of the disease.14–17,23,24 There may be radiological evidence of deformity of the rib cage, pelvis and long bones, but osteopenia and pseudofractures are the two radiographical hallmarks of OM. In osteopenia, lucent sites in the cortex reflect the accumulation of osteoid and the widened irregular haversian canals of OM. Osteoid may be deposited in excessive amounts at various sites, particularly in the spine and pelvis. These lucent areas are oriented at right angles to the cortex and incompletely span the diameter of the bone. They are known as pseudofractures or Looser’s zones or Milkman’s fractures24 and tend to occur in characteristic sites, such as the axillary margin of the scapula, ribs, superior and inferior pubic rami, inner margin of the proximal femur and posterior margin of the ulna. Pseudofractures are typically bilateral and symmetrical. Sclerosis often demarcates the intraosseous margins; new bone on the periosteal aspect suggests callus. In this study, direct radiographs demonstrated all the insufficiency fractures in the pubic rami but those in the femur, sacrum and iliac bones were missed. True fractures may occur in these weakened areas MRI has been widely used for the evaluation of various disease processes, such as pelvic insufficiency fractures and metastasis of the pelvic skeleton.10–13 However, to the best of our knowledge, there are no reports that deal directly with the MRI findings of OM in the pelvic region. On the other hand, MRI has been extensively used for the purpose of skeletal survey in oncogenic OM to detect the causative neoplasm. 25 Our study addressed the MRI findings of pelvic insufficiency fractures in patients with OM. The insufficiency fractures in OM typically appeared as hypointense lines or fissures in both the T1- and T2-weighted sequences. Besides the hypointense fissures, there were areas of hyperintensity on T2-weighted images adjacent to these hypointense fissures in some cases and absent in others. We considered these the active and chronic phases of the disease, respectively. In chronic insufficiency fractures the hypointense lines may be due to persisting sclerosis at the fracture site. The hyperintense signal intensity change found adjacent to Looser’s zones may be caused by bone marrow oedema or inflammation adjacent to active insufficiency fractures. The clinical importance of this may be the institution of appropriate treatment before bone deformities occur. Direct radiographs do not provide such essential information. In our study, the disappearance of the original hyperintense signal intensity around the hypointense

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fissures on follow-up MR examinations after appropriate treatment in 2 patients supported this suggestion. The active type of insufficiency fracture may also be monitored by radionuclide scintigraphy, exhibiting increased radionuclide uptake. The sensitivities of MRI, CT and scintigraphy are high, but the specificity of scintigraphy is low.9–12,26,27 In our experience the advantage of MRI over scintigraphy is the visualization of both the active and chronic types of insufficiency fractures in the same case. Another interesting finding in this study was the high rate of insufficiency fractures in the sacrum and iliac bones. Osteopenia in the pelvic region has several causes, particularly radiotherapy and osteoporosis. OM also results in osteopenia in this region and there are reports of pelvic insufficiency fractures secondary to OM.2,26,27 Direct radiographs are not sensitive in demonstrating insufficiency fractures of the femur, sacrum or iliac bones,4,9 and did not reveal any of these in our study. However, MRI clearly demonstrated 15 of 16 insufficiency fractures involving the femur, sacrum and iliac bones. Around the hypointense fissures, 13 of these lesions showed hypointense signal intensity change on T1-weighted images and hyperintense signal intensity change on T2-weighted and STIR images. The signal intensity change was absent in 2 cases. Interestingly, in 4 subjects MRI was suggestive of OM. In all of these the MR examinations were performed because of chronic pelvic pain. The clinical history revealed decreased sun exposure. The radiographs of these cases lacked the typical features of OM at the pubic rami; all the insufficiency fractures were in the iliac and sacral bones, for which the radiographs were inconclusive. In view of the clinical history, the MR signal changes were interpreted as insufficiency fractures secondary to OM. However, such appearances may also be due to osteoporotic insufficiency fractures. Laboratory and histopathological examination of these participants finally revealed OM. In 3 subjects the skeletal manifestations of OM in the pelvic region showed the very variable location of the active and chronic types of insufficiency fracture in the same subject. In 2 cases there were only insufficiency fractures of the pubic rami. In another 3 participants there were only insufficiency fractures of the sacrum and iliac bones without accompanying insufficiency fractures of the pubic rami. In the remaining cases a combination of these were seen. Since direct radiographs were not suggestive of insufficiency fractures of femur, sacrum or iliac bones, MRI was instituted to explain the reason for pelvic pain in all of the cases. MRI provides essential information regarding the


pelvic manifestations of OM. Insufficiency fractures of the sacrum and iliac bone in patients with OM are frequent and they can be depicted by MRI, whereas direct radiography is inconclusive. The results of this study showed that MRI may also determine the clinical activity of the lesion. The presence of abnormal signal intensity around the fissures indicates an active disease process, whereas absence of abnormal signal intensity represents a chronic disease process. The response of the active-type of insufficiency fracture to the treatment can also be monitored by MRI.

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