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DOI:10.2214/AJR.05.0656
AJR 2007; 188:509-514
© American Roentgen Ray Society

Clinical Observations

MRI Features of Bone Marrow Necrosis

Yu Ming Tang1,2, Susanne Jeavons1, Stephen Stuckey1, Helen Middleton3 and Devinder Gill3

1 Department of Radiology, Princess Alexandra Hospital, Ipswich Rd., Woolloongabba, Brisbane, Queensland 4102, Australia.
2 South Coast Radiology, Gold Coast, Queensland, Australia.
3 Department of Haematology, Princess Alexandra Hospital, Brisbane, Queensland, Australia.

Received April 16, 2005; accepted after revision August 17, 2005.

 
Address correspondence to Y. M. Tang.


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to illustrate and review the MRI appearance of histologically proven cases of bone marrow necrosis (BMN) and to review the literature on this clinicopathologic entity with emphasis on its distinction from avascular necrosis (AVN) of bone.

CONCLUSION. BMN is a rare clinicopathologic entity separate from AVN and has a distinctive MRI appearance. As MRI comes to play an increasingly important role in the evaluation of bone marrow disease, BMN is likely to be more frequently encountered. Awareness of BMN and its MRI appearance and appreciation of the frequent association between BMN and underlying malignancy may assist in the early diagnosis of BMN and initiate an intensive search for occult malignancy.

Keywords: bone • lymphoma • MRI • musculoskeletal imaging • spine


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Bone marrow necrosis (BMN) is a unique clinicopathologic entity distinct from avascular necrosis (AVN) of bone and marrow aplasia. The histologic features of BMN are disruption of the normal marrow architecture and necrosis of myeloid tissue and medullary stroma with loss of fat spaces. Unlike in AVN, in BMN the spicular architecture is preserved, and unlike in aplastic anemia, in BMN the reticular structure is destroyed [1]. In the early stages of BMN, however, differentiation of these entities may not be possible. BMN has been associated with malignancy (usually hematologic), sickle cell disease, infection, and medication. BMN can occur before the diagnosis of malignancy, after chemotherapy, or at recurrence. Because BMN can occur before the diagnosis of malignancy, an extensive search for malignant disease is justified whenever BMN is diagnosed in isolation.

Patients with BMN usually present with bone pain (80% of cases), fever (70%), and fatigue [1-3]. Pancytopenia, anemia, or thrombocytopenia may be present. Elevation of lactate dehydrogenase, alkaline phosphatase, uric acid, and alanine transferase levels is common [1]. The diagnosis is usually made on the basis of findings at bone marrow aspiration and biopsy. Bone marrow aspirate may yield a dry tap, but trephine biopsy characteristically shows necrosis of the myeloid tissue on a background of amorphous eosinophilic material [3]. The histologic diagno sis is said to correlate best with the clinical features when necrosis is extensive [1]. The prognosis of patients with BMN depends greatly on the underlying disorder [1] but is generally considered poor, death usually occurring within weeks or months [2].

The pathophysiologic mechanism of BMN has not been clearly elicited, but failure of the microcirculation is thought to be the critical event [1]. This microcirculatory occlusion may be the result of tumor emboli, tumor compression, fibrin thrombi, or cytotoxic injury [4]. In the three cases in this series, the changes were widespread and occurred either immediately before or during chemotherapy for lymphoma or at the time of relapse of lymphoma. Although MRI is being used increasingly in the evaluation of bone marrow disease, there have been few reports in the English-language literature on the MRI features of BMN. We present the MRI features of three histologically proven cases of BMN in patients with lymphoma and describe the MRI features of this entity.


Materials and Methods
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 Abstract
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 Materials and Methods
Results
 Discussion
 References
 
We retrospectively reviewed the MR images of three patients with BMN. The diagnosis was made on the basis of clinical course and results of bone marrow trephine biopsy. The clinical course, biochemical values, and histologic findings in each case were reviewed by a consultant hematologist and a trainee hematologist. The MR images were reviewed in conjunction with the clinical data by two consultant radiologists and a senior trainee radiologist. All MRI was performed on a 1.5-T unit (Signa, GE Healthcare). Sagittal T1- and T2-weighted sequences of the entire spine were performed in all cases. A third sagittal sequence, differing among the three cases but including gadolinium enhancement in two cases, also was performed.


Results
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Discussion
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The clinical course and MRI appearances are summarized in Tables 1 and 2.


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  		TABLE 1: Summary of Clinical Features

 

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  		TABLE 2: Summary of MRI Findings

 

Case 1
An 80-year-old man presented with lower back pain, pancytopenia, low-grade fever, and a markedly elevated lactate dehydrogenase level of 2,470 U/L (normal, 110-250 U/L). He had a history of stage IIIE diffuse large B-cell lymphoma, which had been diagnosed and treated 7 years earlier. The initial therapy had been six cycles of CHOP (cyclophosphamide, doxorubicin hydrochloride, vincristine, and prednisolone) chemotherapy, and the disease had been in complete remission since that time.

The presentation raised suspicion about relapsed disease, and the patient underwent a number of diagnostic studies. CT of the neck, chest, abdomen, and pelvis revealed a 2.8-cm hypoechoic liver lesion and paraaortic and mesenteric lymphadenopathy as large as 2.5 cm. Bone marrow aspiration and trephine biopsy of the right posterior iliac crest revealed BMN and an infiltrate of large abnormal cells (Fig. 1A) that stained with B-cell markers (CD20 and CD79a), consistent with malignant lymphocytes. Because of focal sensory loss, MRI of the spine was performed (Figs. 1B, 1C, 1D). The images showed extensive abnormalities of all vertebral bodies, the sternum, and the sacrum. There were irregular patchy geographic areas of low T1-weighted and low T2-weighted signal intensity. Several of these lesions had an irregular serpiginous enhancing rim, and some of these had a T2-weighted hyperintense margin. Early anterior epidural extraosseous extension of disease was present at L5 (not shown).


Figure 1
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  		Fig. 1A —80-year-old man with bone marrow necrosis and relapse of lymphoma. History included diagnosis of diffuse large B-cell lymphoma diagnosed and managed with chemotherapy 7 years earlier. Early anterior epidural extraosseous extension of disease (not shown) was present at L5. MR images show extensive geographic pattern of signal abnormality of vertebral bodies. At follow-up MRI (not shown) 2 weeks after imaging, geographic abnormalities were stable, and epidural abnormalities had progressed, suggesting dual pathologic conditions. Photomicrograph of bone marrow trephine biopsy specimen shows extensive necrosis of hemopoietic and stromal elements (arrowhead) with loss of normal fat spaces and preservation of bone trabeculae (arrow). (H and E, x100)

 

Figure 2
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  		Fig. 1B —80-year-old man with bone marrow necrosis and relapse of lymphoma. History included diagnosis of diffuse large B-cell lymphoma diagnosed and managed with chemotherapy 7 years earlier. Early anterior epidural extraosseous extension of disease (not shown) was present at L5. MR images show extensive geographic pattern of signal abnormality of vertebral bodies. At follow-up MRI (not shown) 2 weeks after imaging, geographic abnormalities were stable, and epidural abnormalities had progressed, suggesting dual pathologic conditions. Sagittal T2-weighted MR image shows central areas of irregular patchy areas of low signal intensity (arrows). Margins of several lesions show irregular serpiginous rim of high signal intensity (arrowheads).

 

Figure 3
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  		Fig. 1C —80-year-old man with bone marrow necrosis and relapse of lymphoma. History included diagnosis of diffuse large B-cell lymphoma diagnosed and managed with chemotherapy 7 years earlier. Early anterior epidural extraosseous extension of disease (not shown) was present at L5. MR images show extensive geographic pattern of signal abnormality of vertebral bodies. At follow-up MRI (not shown) 2 weeks after imaging, geographic abnormalities were stable, and epidural abnormalities had progressed, suggesting dual pathologic conditions. Sagittal T1-weighted MR image shows central areas of irregular patchy areas of low signal intensity (arrows).

 

Figure 4
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  		Fig. 1D —80-year-old man with bone marrow necrosis and relapse of lymphoma. History included diagnosis of diffuse large B-cell lymphoma diagnosed and managed with chemotherapy 7 years earlier. Early anterior epidural extraosseous extension of disease (not shown) was present at L5. MR images show extensive geographic pattern of signal abnormality of vertebral bodies. At follow-up MRI (not shown) 2 weeks after imaging, geographic abnormalities were stable, and epidural abnormalities had progressed, suggesting dual pathologic conditions. Sagittal T1-weighted gadolinium-enhanced MR image shows central areas of irregular patchy areas of low signal intensity (arrows). Margins of several lesions show irregular serpiginous rim (arrowheads).

 
The patient chose palliative management but returned 2 weeks later with urinary retention, constipation, and a sensory level at T10 with features of spinal cord compression. MRI showed that the epidural abnormalities had progressed, extending from T1 to T7 and L4 to S1, resulting in marked compression on the spinal cord and cauda equina. Marked retroperitoneal lymphadenopathy also was present. The geographic pattern of abnormalities was stable, supporting the presence of a dual pathologic condition: relapsed lymphoma and BMN. The patient received palliative radiation therapy and steroids and died 2 weeks later as a consequence of progressive disease.

Case 2
A 65-year-old woman presented with hypercalcemia, B symptoms (weight loss, fever, and night sweats), abdominal pain, and widespread rapidly enlarging lymphadenopathy. CT revealed extensive lymphadenopathy, a renal mass, and thickening of the small-bowel wall. Findings at biopsy of an inguinal lymph node were consistent with those of diffuse large B-cell lymphoma. Staging bone marrow aspiration and trephine biopsy showed extensive involvement with lymphoma. Combination chemotherapy with HyperCVAD (cyclophosphamide, doxorubicin hydrochloride, vincristine, and dexamethasone alternating with cytarabine and methotrexate) and rituximab was begun.

Severe back pain developed the day before the start of chemotherapy and persisted for 10 days. Bone marrow aspiration and trephine biopsy from the right posterior iliac crest after the first cycle of chemotherapy showed BMN. Soon after the start of the second cycle of chemotherapy, severe back pain again developed, coinciding with administration of granulocyte colony-stimulating factor (G-CSF). The pain did not resolve with cessation of G-CSF administration. Febrile neutropenia developed, and blood cultures grew coagulase-negative staphylococci. CT of the lumbar spine did not reveal collections or diskitis. Pain and fever persisted, and MRI was performed.

MRI showed extensive bone abnormality involving the entire spine (Figs. 2A, 2B, 2C). Geographic areas of low T1 and low T2 signal intensity were present in the posterior aspect of the vertebral bodies. These areas were surrounded by a peripheral rim of T2 and STIR hyperintensity and a further external rim of intermediate signal intensity. The appearances were considered atypical of lymphomatous involvement and similar to those of bone infarcts seen at other sites.


Figure 5
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  		Fig. 2A —65-year-old woman with bone marrow necrosis after chemotherapy for diffuse large B-cell lymphoma. Images show extensive signal abnormality involving entire spine. Imaging appearance is atypical of lymphomatous involvement and similar to that of bone infarcts seen at other sites. Sagittal T2-weighted MR image shows geographic areas of low intensity in posterior aspect of vertebral bodies (arrows) surrounded by peripheral rim of hyperintensity and external rim of low signal intensity (arrowheads).

 

Figure 6
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  		Fig. 2B —65-year-old woman with bone marrow necrosis after chemotherapy for diffuse large B-cell lymphoma. Images show extensive signal abnormality involving entire spine. Imaging appearance is atypical of lymphomatous involvement and similar to that of bone infarcts seen at other sites. Sagittal T1-weighted MR image shows geographic areas low signal intensity in posterior aspect of vertebral bodies (arrows).

 

Figure 7
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  		Fig. 2C —65-year-old woman with bone marrow necrosis after chemotherapy for diffuse large B-cell lymphoma. Images show extensive signal abnormality involving entire spine. Imaging appearance is atypical of lymphomatous involvement and similar to that of bone infarcts seen at other sites. Sagittal STIR MR image shows geographic areas of low signal intensity in posterior aspect of vertebral bodies (arrows) surrounded by peripheral rim of hyperintensity and further external rim of low signal intensity (arrowheads).

 
Findings at repeated bone marrow aspiration and trephine biopsy from both posterior iliac crests confirmed the presence of persistent BMN (Fig. 2D). Restaging CT did not show evidence of recurrent or residual disease. MRI performed 2 months later because of persistent bone pain showed no marked interval deterioration. After the fifth cycle of chemotherapy (cycle 3A), the patient experienced rapid and aggressive relapse and died of fulminant disease soon afterward.


Figure 8
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  		Fig. 2D —65-year-old woman with bone marrow necrosis after chemotherapy for diffuse large B-cell lymphoma. Images show extensive signal abnormality involving entire spine. Imaging appearance is atypical of lymphomatous involvement and similar to that of bone infarcts seen at other sites. Photomicrograph of bone marrow trephine biopsy specimen shows extensive necrosis of bone marrow stromal and hemopoietic elements with loss of normal fat spaces (arrow) and preservation of bony trabeculae. Arrowhead indicates region of preserved fat spaces. (H and E, x20)

 
Case 3
A 19-year-old woman presented 2 years after cadaveric renal transplantation because of medullary cystic disease with a short history of headaches, vomiting, and deteriorating level of consciousness. CT and MRI showed multifocal enhancing lesions in the right cerebral hemisphere with surrounding edema and mass effect. Stereotactic biopsy was performed, and the histopathologic findings confirmed a diagnosis of polymorphic posttransplantation lymphoproliferative disorder. Further staging, including bone marrow aspiration and trephine biopsy from the right posterior iliac crest, CT of the neck, chest, abdomen, and pelvis, and whole-body gallium scanning, showed no disease outside the central nervous system.

The patient started therapy with high-dose cytarabine and methotrexate followed by the Memorial Sloan-Kettering protocol for central nervous system lymphoma. Two weeks after starting therapy, the patient presented with severe lower back pain after a single dose of G-CSF. Findings on CT of the abdomen, pelvis, and lumbosacral spine were normal. The pain largely resolved with the use of narcotics over the next week. Approximately 3 weeks later, pain returned in the absence of G-CSF. Findings on bone scan were normal. MRI showed extensive abnormalities with a geographic pattern of signal abnormalities throughout the spine, a central region of T1 and T2 hyperintensity surrounded by a hypointense rim, and marked peripheral enhancement (Figs. 3A, 3B, 3C). Bone marrow aspiration and trephine biopsy (Fig. 3D) from the right posterior iliac crest revealed BMN.


Figure 9
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  		Fig. 3A —19-year-old woman with bone marrow necrosis after chemotherapy for central nervous system lymphoproliferative disorder after renal transplantation. Extensive signal abnormality involved vertebral bodies. Sagittal T2-weighted MR image shows geographic central areas of high signal intensity (arrows) surrounded by well-defined rim of low signal intensity (arrowheads).

 

Figure 10
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  		Fig. 3B —19-year-old woman with bone marrow necrosis after chemotherapy for central nervous system lymphoproliferative disorder after renal transplantation. Extensive signal abnormality involved vertebral bodies. Sagittal T1-weighted MR image shows geographic central areas of high signal intensity (arrows) surrounded by well-defined rim of low signal intensity (arrowheads).

 

Figure 11
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  		Fig. 3C —19-year-old woman with bone marrow necrosis after chemotherapy for central nervous system lymphoproliferative disorder after renal transplantation. Extensive signal abnormality involved vertebral bodies. Sagittal T1-weighted fat-suppressed gadolinium-enhanced MR image shows geographic central areas of low signal intensity (arrows) surrounded by intensely enhanced rim (arrowheads).

 

Figure 12
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  		Fig. 3D —19-year-old woman with bone marrow necrosis after chemotherapy for central nervous system lymphoproliferative disorder after renal transplantation. Extensive signal abnormality involved vertebral bodies. Photomicrograph of bone marrow trephine biopsy specimen shows hypocellular bone marrow (treatment related) with preservation of fat spaces (black arrow) and area of necrosis of hematopoietic and stromal elements (arrowhead). Preservation of bone trabeculae (red arrow) is evident. (H and E, x100)

 
Pain developed in the right hip and buttocks, and MRI showed a small effusion in the right hip joint (not shown) and surrounding muscle edema. The extensive signal abnormalities within the spine on the previous scan were also present in the pelvis and proximal aspects of the femurs (Figs. 3E and 3F). The effusion was surgically drained, and cultures grew Clostridium cadaveris. The patient completed chemotherapy and radiation therapy and was in complete remission.


Figure 13
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  		Fig. 3E —19-year-old woman with bone marrow necrosis after chemotherapy for central nervous system lymphoproliferative disorder after renal transplantation. Extensive signal abnormality involved vertebral bodies. Coronal T1-weighted MR image obtained because of right hip and buttock pain shows extensive signal abnormalities in spine in A-C also present in pelvis (arrowheads) and proximal aspect of femur (arrow). Small effusion in right hip joint (not shown) with surrounding muscle edema was also present.

 

Figure 14
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  		Fig. 3F —19-year-old woman with bone marrow necrosis after chemotherapy for central nervous system lymphoproliferative disorder after renal transplantation. Extensive signal abnormality involved vertebral bodies. Coronal T2-weighted fat-suppressed MR image corresponding to E shows abnormalities in pelvis (arrowheads) and proximal aspects of femur (arrow).

 

Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
MRI is being used increasingly in evaluation of disease of the bone marrow because it is a noninvasive method of imaging large portions of the marrow in a short time. MRI can be used to complement bone marrow aspiration and biopsy in establishing the diagnosis of and in staging and follow-up of hematologic malignancies. The MRI appearances of marrow disorders often are nonspecific and reflect changes in the amount of trabecular bone, fat, and water within the marrow cavity [5].

There have been few reports in the English-language literature on the MRI features of BMN. Our literature search revealed six reports [3, 6-10] describing the MRI features of BMN in conjunction with the histologic features. In these articles, the unifying MRI feature in all cases was the characteristic diffuse, extensive, and geographic pattern of signal abnormalities. The pattern of signal abnormalities is similar to that of AVN and bone infarcts [3, 6], which have been well described in periarticular locations and long bones, especially the femoral head, but rarely in the vertebrae [11]. However, the imaging features differentiating these two entities are site and distribution. BMN is anatomically more extensive, diffusely involving the marrow of the spine and pelvis [3], whereas AVN is usually more focal and found in a periarticular distribution or in the appendicular skeleton. Furthermore, the lesions of BMN do not progress to vertebral body collapse, a feature often seen in vertebral AVN [11].

In all of our cases, the central region was surrounded by a peripheral band of low signal intensity. In both cases in which gadolinium was administered, this peripheral rim became enhanced. In two cases the peripheral rim consisted of an inner hyperintense line and an outer hypointense line on T2-weighted images, similar to the double line sign considered pathognomonic of AVN. This pattern has been well described in periarticular AVN, especially of the femoral head, but rarely in AVN of vertebrae [11]. The enhancing peripheral band is thought to represent reactive granulation tissue at the interface between necrotic and viable bone.

The central region of signal abnormality had varying signal characteristics. In two cases, central hypointensity was evident on T1- and T2-weighted images. In the third case, the central area was diffusely hyperintense on T1- and T2-weighted images and showed suppression of signal on T1 gadolinium-enhanced fat-suppressed images, a finding consistent with fat. In no case was enhancement found in the central area.

The varying appearances of the central area may reflect different stages of BMN, similar to those described by Mitchell and colleagues [12] for AVN. This classification was based on the qualitative assessment of alterations in MR signal intensity within the central region in AVN. In the earliest stage (class A), the signal is analogous to fat with hyperintensity on T1 and isointensity to mild hyperintensity on T2 images. This finding was seen in one of our cases, and the patient was well and in remission. The next stage (class B) shows signal characteristics of blood and hemorrhage with T1 and T2 hyperintensity. Chim et al. [3] described a similar pattern of T1 and T2 hyperintensity with enhancement in the central area. They attributed the pattern to the presence of blood and proteinaceous material within hyperemic marrow. The next stage (class C) exhibits signal characteristics of fluid with T1 hypointensity and T2 hyperintensity. This pattern was described by Weissman et al. [6] in two of three cases but was not seen in our patients. The fourth and presumably most advanced stage (class D) shows signal characteristics of fibrous tissue with hypointensity on all sequences. This appearance was found in two of our three patients and in one of the three patients described by Weissman et al. A similar appearance was found by Thuerl et al. [7] in a patient with antiphospholipid syndrome. Bone marrow fibrosis may develop in prolonged cases of BMN [2, 10]. In two of our cases and in the cases described by Weissman et al., the patients died soon after this appearance was found on MRI.

The imaging appearances of BMN may not necessarily follow the aforementioned stages or reach the final stage. Necrotic bone marrow can heal and become repopulated by normal hematopoietic tissue, leaving small fibrotic scars. BMN also is associated with development of bone marrow fibrosis and is a predisposing factor for idiopathic myelofibrosis [2, 10]. An alternative and perhaps more likely hypothesis is that different relative preexisting populations of marrow (hematopoietic and fatty) may cause the varying MRI appearances of BMN. We postulate that the extensive patterns of BMN in cases 2 and 3 were in some way related to cytotoxic injury from chemotherapy, whereas in case 1 there was evidence of recurrent hematologic malignancy. In case 2, the onset of BMN may have occurred on the day before chemotherapy (when severe back pain developed), although bone marrow aspiration and trephine biopsy and MRI were performed only after the start of chemotherapy. BMN may also have been associated with the underlying hematologic malignancy in this case.

BMN is a rare clinicopathologic entity that is distinct from AVN, having a different clinical course, risk factors, and histologic findings. BMN has a distinctive MRI appearance, unlike most marrow disorders, which often have nonspecific findings. BMN characteristically has an extensive, diffuse, geographic pattern of signal abnormality consisting of a central area of variable signal intensity surrounded by a distinct peripheral enhancing rim. These changes are similar to those of AVN in the periarticular areas and osteonecrosis of long bones but are differentiated on imaging on the basis of the site, extensive distribution, and natural history of the lesions. In the early stages, however, these entities can be indistinguishable on the basis of histologic and possibly of imaging findings.

In conclusion, as MRI comes to play an increasingly important role in the evaluation of bone marrow disease, BMN is likely to be more frequently encountered. Awareness of this entity and its MRI appearance and appreciation of its frequent association with underlying malignancy may assist in the early diagnosis of BMN and initiate an appropriate search for occult malignancy.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Jassens AM, Offner FC, Van Hove WZ. Bone marrow necrosis. Cancer 2000; 88:1769 -1780[CrossRef][Medline]
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  3. Chim CS, Ooi C, Ma SK, Lam C. Bone marrow necrosis in bone marrow transplantation: the role of MRI. Bone Marrow Transplant 1998; 22:1125 -1128[CrossRef][Medline]
  4. Maisel D, Lim JY, Pollock WJ, Liu PI. Bone marrow necrosis: an entity often overlooked. Ann Clin Lab Sci1998; 18:109 -115
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  7. Thuerl C, Altehoefer C, Spyridonidis A, Laubenberger J. Imaging findings in the rare catastrophic variant of the primary antiphospholipid syndrome. Eur Radiol 2002;12 : 545-548[Medline]
  8. Lee JL, Lee JH, Kim MK, et al. A case of bone marrow necrosis with thrombotic thrombocytopenic purpura as a manifestation of occult colon cancer. Jpn J Clin Oncol 2004;34 : 476-480[Abstract/Free Full Text]
  9. Venkateswaran L, Duerts R, Haut P, Kletzel M, Chou P. Bone marrow necrosis associated with relapse of acute myelogenous leukemia following unrelated hematopoietic stem cell transplantation using an immunoablative regimen. Med Pediatr Oncol 2002;38 : 148-149[CrossRef][Medline]
  10. Murphy PT, Sivakumaran M, Casey MC, Liddicoat A, Wood JK. Lymphoma associated bone marrow necrosis with raised anticardiolipin antibody. J Clin Pathol 1998;51 : 407-409[Abstract]
  11. Murakami H, Kawahara N, Gabata T, Nambu K, Tomita K. Vertebral body osteonecrosis without vertebral collapse. Spine2003; 28:323 -328
  12. Mitchell DG, Rao VM, Dalinka MK, et al. Femoral head avascular necrosis: correlation of MRI, radiographic staging, radionuclide imaging, and clinical findings. Radiology 1987;162 : 709-715[Abstract/Free Full Text]

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