The Open Orthopaedics Journal




ISSN: 1874-3250 ― Volume 12, 2018
RESEARCH ARTICLE

Diffuse Appearance of Red Bone Marrow on MRI Mimics Cancer Metastasis and Might be Associated with Heavy Smoking



Akio Sakamoto1, *, Bungo Otsuki1, Takeshi Okamoto1, Takayuki Goto2, Tetsuro Yoshimura3, Shuichi Matsuda1
1 Department of Orthopaedic Surgery, Graduate School of Medicine, Kyoto University, Shogoin, Kawahara-cho 54, Sakyo-ku, 606-8507, Kyoto, Japan
2 Department of Urology Surgery, Graduate School of Medicine, Kyoto University, Shogoin, Kawahara-cho 54, Sakyo-ku, 606-8507, Kyoto, Japan
3 Shinyukuhashi Hospital, Fukuoka, Japan

Abstract

Background:

Red bone marrow develops early in life and converts into yellow bone marrow with aging. Reconversion occurs when yellow bone marrow reconverts into red bone marrow due to increased oxygen demands.

Objective:

Diffuse appearance of red bone marrow on Magnetic Resonance Imaging (MRI) is rarely encountered.

Materials and Methods:

Seven patients, five male and two female, with the diffuse appearance of red bone marrow were evaluated. The average age was 71.4 (47-86) years old. All patients had been referred based on a working diagnosis of cancer metastasis. All patients were eventually rediagnosed with bone marrow reconversion.

Results:

Spinal MRI was evaluated in all patients, including the whole spine in four patients and lumbar spine in three patients. Six patients had slight anemia or close to the lower limit of normal hemoglobin (within 1mg/dl). Six patients were heavy smokers, having more than 20 cigarettes per day. Four patients had a history of stomach or bladder cancer (2 cases each). MRI revealed red bone marrow with a diffuse appearance and low signal intensity on T1- and T2-weighted images. Compared with the spinal cord/conus, the red bone marrow appeared isointense in about half of the cases, and in the other cases, the intensities were either slightly high or low. The signal of yellow bone marrow was isointense with the retroperitoneal fat.

Conclusion:

Diffuse red marrow can be difficult to differentiate from cancer metastasis. Compared to the MRI, signal intensity of the cord/conus is useful in the diagnosis of red marrow. Slight anemia may also be present. Heavy smoking might be related to the appearance of diffuse red marrow.

Keywords: Bone marrow, Red marrow, Yellow marrow, Hematopoietic, Smoking, Magnetic resonance imaging.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 451
Last Page: 461
Publisher Id: TOORTHJ-12-451
DOI: 10.2174/1874325001812010451

Article History:

Received Date: 27/4/2018
Revision Received Date: 26/10/2018
Acceptance Date: 28/10/2018
Electronic publication date: 27/11/2018
Collection year: 2018

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© 2018 Sakamoto et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Orthopaedic Surgery, Graduate School of Medicine, Kyoto University, Shogoin, Kawahara-cho 54, Sakyo-ku, Kyoto 606-8507, Japan; Tel: +81-75-751-3366; E-mail: akiosaka@kuhp.kyoto-u.ac.jp




1. INTRODUCTION

At birth, bone marrow is cellular and hematopoietic and is called red bone marrow. Bone marrow becomes less hematopoietic with aging, and converts into the fat bone marrow, or yellow bone marrow [1Nouh MR, Eid AF. Magnetic resonance imaging of the spinal marrow: Basic understanding of the normal marrow pattern and its variant. World J Radiol 2015; 7(12): 448-58.[http://dx.doi.org/10.4329/wjr.v7.i12.448] [PMID: 26753060] ]. The cellular components of red bone marrow include 60% hematopoietic cells and 40% fat cells. In contrast, yellow bone marrow is composed of 95% fat cells and 5% hematopoietic cells [1Nouh MR, Eid AF. Magnetic resonance imaging of the spinal marrow: Basic understanding of the normal marrow pattern and its variant. World J Radiol 2015; 7(12): 448-58.[http://dx.doi.org/10.4329/wjr.v7.i12.448] [PMID: 26753060] ]. The conversion of red bone marrow to yellow bone marrow begins in the peripheral appendicular skeleton and proceeds to the central axial skeleton [2Vande Berg BC, Malghem J, Lecouvet FE, Maldague B. Magnetic resonance imaging of normal bone marrow. Eur Radiol 1998; 8(8): 1327-34.[PMID: 9853209] , 3Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, et al. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 1990; 177(1): 83-.[PMID: 2399343] ]. The spine has the largest store of bone marrow in the body [1Nouh MR, Eid AF. Magnetic resonance imaging of the spinal marrow: Basic understanding of the normal marrow pattern and its variant. World J Radiol 2015; 7(12): 448-58.[http://dx.doi.org/10.4329/wjr.v7.i12.448] [PMID: 26753060] ]. The pattern of spinal bone marrow conversion is centripetal, starting in the subcortical and subendplate regions and proceeding to the center of the vertebrae [4Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Normal bone marrow: dynamic aspects in magnetic resonance imaging. J Radiol 2001; 82(2): 127-35.[PMID: 11428207] ].

Bone marrow is a dynamic organ that continually changes. Red marrow may reconvert from yellow bone marrow when there is an increased oxygen requirement [5Hanrahan CJ, Shah LM. MRI of spinal bone marrow: part 2, T1-weighted imaging-based differential diagnosis. AJR Am J Roentgenol 2011; 197(6): 1309-21.[http://dx.doi.org/10.2214/AJR.11.7420] [PMID: 22109284] , 6Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875] ]. Red marrow reconversion occurs in the opposite sequence of bone marrow conversion with aging [7Poulton TB, Murphy WD, Duerk JL, Chapek CC, Feiglin DH. Bone marrow reconversion in adults who are smokers: MR Imaging findings. AJR Am J Roentgenol 1993; 161(6): 1217-21.[http://dx.doi.org/10.2214/ajr.161.6.8249729] [PMID: 8249729] ]. Reconversion can occur in the setting of chronic illnesses [5Hanrahan CJ, Shah LM. MRI of spinal bone marrow: part 2, T1-weighted imaging-based differential diagnosis. AJR Am J Roentgenol 2011; 197(6): 1309-21.[http://dx.doi.org/10.2214/AJR.11.7420] [PMID: 22109284] , 8Vande Berg BC, Lecouvet FE, Galant C, Maldague BE, Malghem J. Normal variants and frequent marrow alterations that simulate bone marrow lesions at MR imaging. Radiol Clin North Am 2005; 43(4): 761-70.[http://dx.doi.org/10.1016/j.rcl.2005.01.007] ]. A history of heavy smoking has also been associated with marrow reconversion [9Tall MA, Thompson AK, Vertinsky T, Palka PS. MR imaging of the spinal bone marrow. Magn Reson Imaging Clin N Am 2007; 15(2): 175-98.[http://dx.doi.org/10.1016/j.mric.2007.01.001] [PMID: 17599639] ]. Magnetic Resonance Imaging (MRI) is a non-invasive technique to evaluate vertebral bone marrow, reflecting the cellular components. The routine spine evaluation on MRI includes T1-weighted and T2-weighted sequences [10Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol 2011; 197(6): 1298-308.[PMID: 22109283] ]. The T1-weighted image intensity of red bone marrow is low but is higher than that of the intervertebral discs and paraspinal muscles [11Carroll KW, Feller JF, Tirman PF. Useful internal standards for distinguishing infiltrative marrow pathology from hematopoietic marrow at MRI. J Magn Reson Imaging 1997; 7(2): 394-8.[PMID: 9090597] ]. On the other hand, the T1-weighted image intensity of yellow bone marrow is comparable to that of the subcutaneous fat [6Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875] , 10Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol 2011; 197(6): 1298-308.[PMID: 22109283] , 11Carroll KW, Feller JF, Tirman PF. Useful internal standards for distinguishing infiltrative marrow pathology from hematopoietic marrow at MRI. J Magn Reson Imaging 1997; 7(2): 394-8.[PMID: 9090597] ].

In the current series, we report the diffuse appearance of red bone marrow on MRI mimicking cancer metastasis. MRI characteristics and clinical findings were compared.

2. MATERIALS AND METHODS

Diffuse appearance of red bone marrow on MRI was identified from medical files. All patients were referred for evaluation of abnormal bone marrow on MRI, with a working diagnosis of cancer metastasis. However, a final diagnosis of bone marrow reconversion was made in all patients. All patients were evaluated for a history of cancer, smoking, and anemia. Characteristic MRI signal intensity on T1-weighted and T2-weighted spinal images was assessed and compared to normal tissue, including spinal cord or conus for identification of red bone marrow and retroperitoneal fat for identification of yellow bone marrow.

3. RESULTS

A clinical summary is shown in Table 1. The patients included five males and two females, with a mean age of 71.4 ±13.6 years old, ranging from 47 to 86. All patients had a history of low back pain for which MRI was performed. The exact course of the low back pain and the medication used for it was not fully assessed, because the low back pain was non-specific and the degree of the pain was not severe in all cases. All patients were referred to our institute because MRI abnormality was noted following image analysis, and the disappearance of the low back pain was confirmed at the MRI examination. An association with back pain was excluded because the pain resolved in all patients. Spinal assessment included the lumbar spine in three cases. In the other four cases, spinal assessment included the entire cervical, thoracic and lumbar spine. Four out of seven cases had a history of cancer, including 2 stomach cancers and 2 bladder cancers. Smoking was seen in six cases. All smokers were heavy smokers, consuming more than 20 cigarettes per day. At the initial assessment, hematology analysis showed slight anemia with low hemoglobin values in four cases. Two cases were close to the lower limit of normal (within 1mg/dl).

Table 1
Summary of diffuse reconversion of spinal bone marrow.


On MRI, all cases demonstrated a well-demarcated diffuse appearance of red marrow, with low signal intensity in both the T1- and T2-weighted images in either whole vertebrae or near the endplate and center of the vertebra (Figs. 1-6). There was no evidence of cortex destruction in any patient. A summary of MRI signal intensity is shown in Table 2. The signal intensity of the red bone marrow on T1-weighted images was iso to the spinal cord or conus in four cases (58%), slightly lower in one case (14%) and slightly higher in two cases (29%)(Figs. 1-3). On T2-weighted images, the signal intensity of the red bone marrow was iso in three cases (43%), slightly lower in two case (29%) and slightly higher in two cases (29%) (Figs. 1-4). The signal intensity of yellow bone marrow was the same as the retroperitoneal fat in all seven cases. Follow-up MRI was performed in six cases from 8 months to 8 years. On follow up imaging, all cases except one had no change or a slight decrease in the size of the low signal area (Fig. 5). In one case treated with radiation, the red bone marrow converted into yellow bone marrow on follow up (Fig. 6).

Fig. (1)
Bone marrow reconversion in the lumber spine of a 66-year-old male. MRI demonstrates a diffuse lesion with low signal intensity in the whole spine on the T1 weighted image (left) and high signal intensity on the T2 weighted image (middle). High signal intensity on the T2 weighted image is suppressed on fat suppression image (right). The signal intensity is almost the same as that of the spinal cord.


Fig. (2)
Bone marrow reconversion in an 83-year-old male. MRI demonstrates a well-circumscribed diffuse lesion with low signal intensity in the whole spine on the T1 weighted image (left) and high signal intensity on the T2 weighted image (right). The signal intensity is almost the same as that of the spinal cord.


Fig. (3)
Bone marrow reconversion in a 47-year-old female. MRI demonstrates a diffuse lesion with low signal intensity in the whole spine on the T1 weighted image (left) and on the T2 weighted image (right). The signal intensity is slightly lower than that of the spinal cord on T1- and T2-weighted images.


Fig. (4)
Bone marrow reconversion in an 86-year-old male. MRI demonstrates a diffuse lesion with low signal intensity on the T1- weighted image (left) and high signal intensity on the T2-weighted image (right). The signal intensity is almost the same as the spinal cord on the T1-weighed image and slightly higher on the T2 weighted image.


Fig. (5)
Bone marrow reconversion in an 82-year-old female. MRI demonstrates a diffuse lesion on the initial assessment (A) and 8 years later (B) with low signal intensity in the whole spine on the T1-weighted image (top) and high signal intensity on the T2 weighted image (bottom). MRI after 8 years demonstrated a slightly decreased area of red bone marrow (yellow arrow) (B).


Fig. (6)
Bone marrow reconversion in a 66-year-old male. MRI demonstrates a diffuse lesion with low signal intensity on the T1-weighted image and high signal intensity on the T2-weighted image. After radiation to the posterior portion, the red bone marrow disappeared (12 month interval) (B). (top: T1 weighted image, bottom: T2 weighted image).


Table 2
MRI signal intensity of diffuse reconversion of spinal bone marrow.


4. DISCUSSION

In the current case series, we report the unique MRI appearance of a mixture of red and yellow bone marrow. With aging, the bone marrow becomes increasingly replaced with fatty marrow [10Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol 2011; 197(6): 1298-308.[PMID: 22109283] ]. Red bone marrow tends to be diffused in the axial bone marrow in patients under the age of 40 years, with only small areas of yellow marrow around the basivertebral plexus [3Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, et al. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 1990; 177(1): 83-.[PMID: 2399343] ]. The pattern of spinal bone marrow conversion is centripetal, starting in the subcortical and subendplate regions and proceeding to the center of the vertebral body [6Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875] ]. Three patterns have been reported, including a band-like pattern of fatty replacement along the endplates, small foci of fatty marrow replacement, and large globular areas of fat replacement [3Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, et al. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 1990; 177(1): 83-.[PMID: 2399343] ]. Red bone marrow reconversion from yellow bone marrow may occur when there is an increased oxygen requirement [5Hanrahan CJ, Shah LM. MRI of spinal bone marrow: part 2, T1-weighted imaging-based differential diagnosis. AJR Am J Roentgenol 2011; 197(6): 1309-21.[http://dx.doi.org/10.2214/AJR.11.7420] [PMID: 22109284] , 6Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875] ]. The pattern of reconversion occurs in the opposite sequence of bone marrow conversion [7Poulton TB, Murphy WD, Duerk JL, Chapek CC, Feiglin DH. Bone marrow reconversion in adults who are smokers: MR Imaging findings. AJR Am J Roentgenol 1993; 161(6): 1217-21.[http://dx.doi.org/10.2214/ajr.161.6.8249729] [PMID: 8249729] ]. In this series, we identified variations in the location of red bone marrow, which was seen in whole vertebrae, in endplates, and at the center of vertebrae. These patterns appear to be typical of red bone marrow reconversion.

The signal intensity of red bone marrow on T1-weighted images is low, but is higher than that of the intervertebral discs and paraspinal muscles [11Carroll KW, Feller JF, Tirman PF. Useful internal standards for distinguishing infiltrative marrow pathology from hematopoietic marrow at MRI. J Magn Reson Imaging 1997; 7(2): 394-8.[PMID: 9090597] ]. Intervertebral discs degenerate with aging and signal intensity in degenerative discs tends to decrease. Therefore, it may be misleading to compare the signal intensity of bone marrow to that of the intervertebral discs, especially in the elderly. In our series, the spinal cord or conus was used for comparison to red bone marrow. In about half of the cases, the red bone marrow was iso intense to the spinal cord or conus. Furthermore, the other cases had only slightly lower or higher intensity as the spinal cord or conus. Hence, comparison to the spinal cord or conus is useful in the diagnosis of bone marrow reconversion. On the other hand, the signal intensity of yellow bone marrow is reported to be similar to that of the subcutaneous fat [6Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875] , 10Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol 2011; 197(6): 1298-308.[PMID: 22109283] , 11Carroll KW, Feller JF, Tirman PF. Useful internal standards for distinguishing infiltrative marrow pathology from hematopoietic marrow at MRI. J Magn Reson Imaging 1997; 7(2): 394-8.[PMID: 9090597] ]. In our series, we found that retroperitoneal fat had the similar signal intensity to the yellow bone marrow. Hence, comparison to the retroperitoneal fat is useful in the diagnosis of yellow bone marrow. The natural history of reconverted red bone marrow appears to be stable, as five out of six cases had no change or slightly decreased area during a maximum follow up period of 8 years.

All study patients were referred to our institute with a working diagnosis of cancer metastasis. The differential diagnosis of bone marrow abnormalities includes malignancies such as multiple myeloma, non-Hodgkins lymphoma, metastatic non-small cell lung cancer, and metastatic adenocarcinoma [12Shah GL, Rosenberg AS, Jarboe J, Klein A, Cossor F. Incidence and evaluation of incidental abnormal bone marrow signal on magnetic resonance imaging. Scientific World J 2014; 2014: 380814.[http://dx.doi.org/10.1155/2014/380814] [PMID: 25374938] ]. The diagnosis of reconversion and the exclusion of cancer metastasis was made not only with MRI findings but also with follow up imaging. Metastatic lesions are usually brighter than normal bone marrow on T2-weighted images. However, it can be difficult to differentiate metastatic lesions from normal marrow on T2-weighted sequences [10Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol 2011; 197(6): 1298-308.[PMID: 22109283] , 13Mirowitz SA, Apicella P, Reinus WR, Hammerman AM, et al. MR imaging of bone marrow lesions: relative conspicuousness on T1-weighted, fat-suppressed T2-weighted, and STIR images. AJR Am J Roentgenol 1994; 162(1): 215-.[PMID: 8273669] ]. The halo sign, characterized by a rim of bright signal intensity on T2-weighted images, may indicate the presence of malignancy [14Schweitzer ME, Levine C, Mitchell DG, Gannon FH, Gomella LG. Bull's-eyes and halos: useful MR discriminators of osseous metastases. Radiology 1993; 188(1): 249-52.[PMID: 8511306] ]. Infection (i.e., osteomyelitis) is also part of the differential diagnosis of abnormal bone marrow signal intensity [12Shah GL, Rosenberg AS, Jarboe J, Klein A, Cossor F. Incidence and evaluation of incidental abnormal bone marrow signal on magnetic resonance imaging. Scientific World J 2014; 2014: 380814.[http://dx.doi.org/10.1155/2014/380814] [PMID: 25374938] ]. In the current series, multi vertebral signal intensity and the absence of clinical signs of infection excluded infection in all seven patients.

Several clinical characteristics were associated with the diffuse appearance of red bone marrow in this series. Most patients in this series were elderly, with an average age of 71.4 years old, and the youngest age of 47 years old. Although, all patients had a history of back pain, the pain resolved and was thus not considered in the association analysis. Moreover, non-specific low back pain might not explain MRI abnormality in the whole spine. Four patients had a history of cancer. The association between cancer and reconversion is unknown, because patients with a history of cancer tend to have extensive investigations, and thus have a higher probability of identifying reconversion. Most patients in this series had mild anemia. Red bone marrow reconversion occurs when oxygen requirements increase [5Hanrahan CJ, Shah LM. MRI of spinal bone marrow: part 2, T1-weighted imaging-based differential diagnosis. AJR Am J Roentgenol 2011; 197(6): 1309-21.[http://dx.doi.org/10.2214/AJR.11.7420] [PMID: 22109284] , 6Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875] ]; hence, compensation by reconversion may have occurred leading to mild anemia. A heavy smoking history has been significantly associated with marrow reconversion [7Poulton TB, Murphy WD, Duerk JL, Chapek CC, Feiglin DH. Bone marrow reconversion in adults who are smokers: MR Imaging findings. AJR Am J Roentgenol 1993; 161(6): 1217-21.[http://dx.doi.org/10.2214/ajr.161.6.8249729] [PMID: 8249729] ]. Chronic smoking may result in tissue hypoxia because of elevated carboxyhemoglobin levels [7Poulton TB, Murphy WD, Duerk JL, Chapek CC, Feiglin DH. Bone marrow reconversion in adults who are smokers: MR Imaging findings. AJR Am J Roentgenol 1993; 161(6): 1217-21.[http://dx.doi.org/10.2214/ajr.161.6.8249729] [PMID: 8249729] ]. In our series, heavy smoking, having more than 20 cigarettes a day, was seen in six out of seven cases. Thus, heavy smoking appears to be associated with reconversion. However, one female patient had no history of smoking, and was otherwise healthy. Further investigation of such cases is required to understand the as-yet-unidentified factors associated with reconversion.

CONCLUSION

In the current series, we report the diffuse appearance of red bone marrow on MRI mimicking cancer metastasis. The diagnosis of bone marrow reconversion on MRI can be made by comparison of red bone marrow intensity to that of the spinal cord and by comparison of the yellow bone marrow intensity to that of the retroperitoneal fat. Mild anemia was seen in most cases and may be a compensated condition. The association of bone marrow reconversion with cancer is unknown, but heavy smoking might be related to the condition.

ABBREVIATION

MRI = Magnetic Resonance Imaging

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.

HUMAN AND ANIMAL RIGHTS

No animals/humans were used for studies that are the basis of this research.

CONSENT FOR PUBLICATION

All patients represented in this study were informed that the data from their case would be de-identified and used in a journal publication.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

[1] Nouh MR, Eid AF. Magnetic resonance imaging of the spinal marrow: Basic understanding of the normal marrow pattern and its variant. World J Radiol 2015; 7(12): 448-58.[http://dx.doi.org/10.4329/wjr.v7.i12.448] [PMID: 26753060]
[2] Vande Berg BC, Malghem J, Lecouvet FE, Maldague B. Magnetic resonance imaging of normal bone marrow. Eur Radiol 1998; 8(8): 1327-34.[PMID: 9853209]
[3] Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, et al. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 1990; 177(1): 83-.[PMID: 2399343]
[4] Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Normal bone marrow: dynamic aspects in magnetic resonance imaging. J Radiol 2001; 82(2): 127-35.[PMID: 11428207]
[5] Hanrahan CJ, Shah LM. MRI of spinal bone marrow: part 2, T1-weighted imaging-based differential diagnosis. AJR Am J Roentgenol 2011; 197(6): 1309-21.[http://dx.doi.org/10.2214/AJR.11.7420] [PMID: 22109284]
[6] Vande Berg BC, Malghem J, Lecouvet FE, Maldague B, et al. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998; 27(9): 471-83.[PMID: 9809875]
[7] Poulton TB, Murphy WD, Duerk JL, Chapek CC, Feiglin DH. Bone marrow reconversion in adults who are smokers: MR Imaging findings. AJR Am J Roentgenol 1993; 161(6): 1217-21.[http://dx.doi.org/10.2214/ajr.161.6.8249729] [PMID: 8249729]
[8] Vande Berg BC, Lecouvet FE, Galant C, Maldague BE, Malghem J. Normal variants and frequent marrow alterations that simulate bone marrow lesions at MR imaging. Radiol Clin North Am 2005; 43(4): 761-70.[http://dx.doi.org/10.1016/j.rcl.2005.01.007]
[9] Tall MA, Thompson AK, Vertinsky T, Palka PS. MR imaging of the spinal bone marrow. Magn Reson Imaging Clin N Am 2007; 15(2): 175-98.[http://dx.doi.org/10.1016/j.mric.2007.01.001] [PMID: 17599639]
[10] Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol 2011; 197(6): 1298-308.[PMID: 22109283]
[11] Carroll KW, Feller JF, Tirman PF. Useful internal standards for distinguishing infiltrative marrow pathology from hematopoietic marrow at MRI. J Magn Reson Imaging 1997; 7(2): 394-8.[PMID: 9090597]
[12] Shah GL, Rosenberg AS, Jarboe J, Klein A, Cossor F. Incidence and evaluation of incidental abnormal bone marrow signal on magnetic resonance imaging. Scientific World J 2014; 2014: 380814.[http://dx.doi.org/10.1155/2014/380814] [PMID: 25374938]
[13] Mirowitz SA, Apicella P, Reinus WR, Hammerman AM, et al. MR imaging of bone marrow lesions: relative conspicuousness on T1-weighted, fat-suppressed T2-weighted, and STIR images. AJR Am J Roentgenol 1994; 162(1): 215-.[PMID: 8273669]
[14] Schweitzer ME, Levine C, Mitchell DG, Gannon FH, Gomella LG. Bull's-eyes and halos: useful MR discriminators of osseous metastases. Radiology 1993; 188(1): 249-52.[PMID: 8511306]

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"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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