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AJR 2004; 183:1761-1765
© American Roentgen Ray Society

Bone Marrow Fat and Bone Mineral Density on Proton MR Spectroscopy and Dual-Energy X-Ray Absorptiometry: Their Ratio as a New Indicator of Bone Weakening

D. Schellinger1, C. S. Lin1, J. Lim2, H. G. Hatipoglu1, J. C. Pezzullo3 and A. J. Singer2

1 Department of Radiology, Georgetown University Hospital and Georgetown University, 3800 Reservoir Rd., NW, Washington, DC 20007.
2 Department of Obstetrics and Gynecology, Georgetown University Hospital and Georgetown University, Washington, DC 20007.
3 School of Nursing and Health Sciences, Georgetown University Hospital and Georgetown University, Washington, DC 20007.

Received December 11, 2003; accepted after revision March 26, 2004.

 
Address correspondence to D. Schellinger.


Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. Bone weakening can be affected by agents other than bone mineral density (BMD). Increased bone marrow fat may have a direct link to bone loss. This pilot study analyzes the relationship between bone marrow fat and BMD in subjects with normal and structurally weakened vertebrae.

SUBJECTS AND METHODS. Twenty-six subjects underwent both dual-energy X-ray absorptiometry and proton MR spectroscopy of 71 lumbar vertebrae. Fifteen subjects had normal-appearing vertebrae on MRI, and 11 had signs of bone weakening.

RESULTS. We found that high bone marrow fat did not consistently equate with low BMD. Bone marrow fat can indicate bone weakening nearly as well as BMD, but neither parameter alone is suitable to be used independently as an indicator. The bone marrow fat/BMD ratio showed significant diagnostic power to detect bone weakening, even in this relatively small subject sample.

CONCLUSION. An inverse relationship between bone marrow fat and BMD could not be confirmed. Bone marrow fat can be used to diagnose reduced bone strength nearly as well as BMD. The bone marrow fat/BMD ratio is a significant diagnostic indicator of bone weakening.


Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Bone mineral density (BMD) is commonly viewed as a bone signature that measures mechanical strength. A large portion of bone strength is not explained by bone density alone. Many suggest that BMD is only one of several elements responsible for the mechanical competence of bone [1–4]. During the First Consensus Conference on Osteoporosis of the New Millennium [5], it was concluded that BMD and bone quality are two primary contributors to bone strength and weakness. The term "bone quality" was coined to describe bone characteristics that are independent of BMD but that contribute to bone strength.

The diagnostic limitations of BMD have stimulated interest in bone microstructure and microchemical composition [6–8]. More recently, bone marrow fat was scrutinized for its potential diagnostic value [9–13]. Some believe that increased bone marrow fat has an etiologic link to osteopenia and that inhibiting marrow adipogenesis could affect bone strength [14].

Until recently, researchers had to assess bone marrow fat with invasive methods. Now, a new technique, proton MR spectroscopy (1H MR spectroscopy), can gauge bone marrow fat noninvasively and serially [15–18]. Our group used 1H MR spectroscopy for measuring bone marrow fat. The percentage fat fraction is used as a measuring standard. In prior work, researchers showed that increased bone marrow fat may present a fracture risk [17]. Whether high bone marrow fat is an independent risk factor or whether it simply connotes fat replacement for bone loss is still unclear.

The goal of this work was to analyze carefully the relationship between BMD and bone marrow fat in subjects with normal and structurally weakened vertebrae. The results can bring about new knowledge in various ways. First, if BMD and bone marrow fat are shown to be related directly, bone marrow fat can be validated as a substitute measure for BMD: abnormal bone marrow fat infers abnormal BMD. Second, if BMD and bone marrow fat are not interrelated, bone marrow fat can be viewed as an independent marker of bone quality. Third, studying bone marrow fat and BMD in subjects with weakened vertebrae can help determine the diagnostic power of each.


Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Patients who were referred for a dual-energy X-ray absorptiometry (DEXA) study as part of a routine workup were offered the opportunity to undergo lumbar spine MRI free of charge. Informed consent was obtained from all subjects. The study was conducted under a protocol that was approved by the institutional review board. Many disease states—that is, myelo- and lymphoproliferative disorders, anemia, AIDS, metastatic disease—and steroid therapy are known to change the abundance of bone marrow fat [19–22]. Therefore, subjects in these categories were excluded from this series.

Twenty-six subjects (three men and 23 women; age range, 32–70 years; mean, 57 ± 9 [SD] years) underwent both DEXA and 1H MR spectroscopy of lumbar vertebral bodies. Specific 1H MR spectroscopy measuring parameters are described in the next section of this article. Fifteen subjects (two men and 13 women; age range, 44–65 years; mean, 55 ± 6 years) had normal-appearing vertebrae on MRI. Eleven subjects (one man and 10 women; age range, 32–70 years; mean, 60 ± 12 years) had MRI stigmata of bone weakening.

DEXA and Proton MR Spectroscopy
DEXA, used to measure BMD, and 1-H MR spectroscopy, used to measure bone marrow fat, data for each subject represent the average of all lumbar vertebrae, usually L1–L4. All data are summarized in Table 1. The list includes patient sex, age, BMD, bone marrow fat, and bone marrow fat/BMD ratios.


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  		TABLE 1 Bone Mineral Density (BMD), Bone Marrow Fat (BMF), and BMF/BMD Ratios of Lumbar Vertebrae

 

BMD and bone marrow fat were compared in 75 lumbar vertebrae of 26 patients who were referred to this institution for DEXA scanning.

BMD data were obtained on a scanner (4000W, Hologic) that is capable of scanning vertebrae and hip DEXA. This unit is in routine clinical use and provides BMD service for the entire hospital. The L1 through L4 vertebrae were scanned and measured in the anteroposterior direction. Subjects were positioned supine with the lower part of the legs elevated to reduce lordosis of the lumbar region. After completion of DEXA scanning, BMD (g/cm2) as well as T and Z scores for individual lumbar vertebrae (L1–L4) were calculated using online software. These measurements were fed into the data comparison pool. The World Health Organization considers a T score of less than –2.5 as indicative of osteoporosis [23, 24]. Osteopenia denotes bone loss in the range of –1.0 to –2.5. Subjects with an average T score above –1.0 are considered normal.

The technique used for performing 1-H MR spectroscopy was published previously [17, 18]: 1-H MR spectroscopy is preceded by a survey that consists of sagittal T1- and T2-weighted MRI of the lumbar spine. All MRI evaluations were performed on a 1.5-T system (Vision, Siemens Medical Solutions). The body coil was used for transmitting radiofrequency power, and a quadrature spine array was used for signal reception. Images were obtained using a section thickness of 5 mm. Localized 1-H MR spectroscopy of unfractured lumbar vertebrae was performed using a single-voxel stimulated-echo acquisition mode (termed "STEAM") sequence. The parameters for this sequence were TR/TE, 5,000/20; voxel size, 1 x 1 x 1 cm3; 1,024 data points; spectral width, 1,000 Hz; and number of signals averaged, 1. The use of a TR of 5,000 msec allows observation of fully T1-relaxed MR signal.

Keeping the TE at 20 msec minimizes MR signal reduction due to the T2 effect. This set of parameters has proved to be sufficient to derive the quantitative bone marrow fat fraction in prior work. Examination time for the MRI portion of the test was approximately 15 min and 10–15 min for MR spectroscopy. The total examination time was about 30 min for each subject.

Proton MR spectroscopy bone marrow spectra have two dominant peaks: water and lipid (methylene). In this article, bone marrow fat is expressed as a percentage fat fraction. This value denotes relative vertebral fat content and can be derived from the lipid–water ratio (LWR). For example, assuming that the water peak of a spectrum measures 4 cm and the lipid (methylene) peak is 1 cm in height, the LWR would be 1/4, which is 0.25. The fat fraction (FF) is derived as follows:

Therefore, in this example, the FF is 0.20.

The percentage FF is the fat fraction multiplied by 100. In this example, the percentage FF is 20%. Other examples are as follows: For an LWR of 0.5, the percentage FF is 33%; for an LWR of 1.0, the percentage FF is 50%; for an LWR of 2.0, the percentage FF is 66%; and for an LWR of 3.0, the percentage FF is 75%.

MR images of the lumbar spine were reviewed by a senior neuroradiologist and screened for structural changes. The radiologist's review focused mainly on vertebral changes that could reflect bone weakening. These included Schmorl's nodes, endplate depressions, wedge deformities, and obvious compression fractures (Fig. 1A, 1B, 1C). The same criteria also were used in a prior study [17]. Schmorl's nodes are thought to represent intraosseous disk herniation secondary to weakened vertebral endplates. Endplate depression and wedge deformities are sequelae of vertebral compression. Vertebrae with fracture lines and gross anatomic distortion were considered recent fractures. Vertebrae with signs of recent fractures were not included in the DEXA and 1H MR spectroscopy analyses, because bone tissue may be contaminated with bone edema, bone fibrosis, and granulation tissue. Although these vertebrae were not used for bone marrow fat measurements, the unfractured lumbar vertebrae of the subjects were. They constitute the bone environment of the fractured vertebra and were considered valuable sources of data.



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  		Fig. 1A. —MR images of lumbar spine in three different subjects. 64-year-old woman with early anterior wedging of L2 and L3 (arrows). Bone marrow fat was 54 (mildly elevated for age), and dual-energy X-ray absorptiometry (DEXA) T score was –2.83.

 


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  		Fig. 1B. —MR images of lumbar spine in three different subjects. 61-year-old woman with prominent Schmorl's node at L1. Bone marrow fat was 61.4 (mildly elevated for age), and DEXA T score was –1.58.

 


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  		Fig. 1C. —MR images of lumbar spine in three different subjects. 70-year-old man with vertebral compression of L1. Bone marrow fat was 69.5 (moderately elevated for age), and DEXA T score was –2.67.

 

Data Evaluation
The relationship of bone marrow fat and BMD and their validity in the diagnosis of vertebral bone weakening were examined using logistic regression analysis [25], an unpaired Student's t test, and correlation coefficient calculations. All data elements are summarized in Table 1 and also are displayed as a graph in Figure 2.



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  		Fig. 2. —Graph shows comparison of bone marrow fat (percentage fat fraction ff) and bone mineral density (BMD [g/cm2]) of lumbar vertebrae from 26 subjects. Each data point represents an average value of BMF and BMD for 26 lumbar spines (71 vertebrae). Data points in the right box (dotted lines) represent subjects with BMD in the osteopenia range (0.75–0.9 g/cm2). Data points in left box represent BMD less than 0.75 g/cm2 and signify osteoporosis. Square gray boxes = subjects with weakened vertebrae, diamond-shaped black boxes = subjects with normal vertebrae.

 

First, logistic regression was used to determine the value of BMD, bone marrow fat, and the bone marrow fat/BMD ratio to evaluate for bone weakening. Second, an unpaired Student's t test was used to compare abnormal and normal data in terms of BMD, bone marrow fat, and bone marrow fat/BMD ratio. Third, all BMD and bone marrow fat data were paired, and correlations were calculated to determine the degree of relationship between the two. A p value of less than 0.05 was considered significant.


Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Bone Marrow Fat/BMD Relationship
To test the hypothesis that high fat concentration is accompanied by low bone density and that there may be an inverse relationship between bone marrow fat and BMD, we calculated a correlation coefficient from the data pool (Table 1). The data also are displayed in Figure 2. The calculated correlation coefficient (r) of –0.23 indicates that the bone marrow fat/BMD relationship is weak in this small sample.

Value for Diagnosing Bone Weakening
The logistic regression method was used to determine the diagnostic value of BMD and bone marrow fat. Findings showed that bone marrow fat can indicate bone weakening nearly as well as BMD (p = 0.1 vs p = 0.07, respectively). However, based on these data, neither of the parameters was suitable to be used as an independent indicator of bone weakening. Surprisingly, the bone marrow fat/BMD ratio was shown to have significant diagnostic power to detect bone weakening (p = 0.02) even in this limited data set. The Student's t test analysis also supports statistical data derived from the logistic regression analysis. When data of structurally normal and abnormal lumbar spines are compared, Student's t test analysis again shows that the degree of significance is escalated with the use of the bone marrow fat/BMD ratio. The p value for the bone marrow fat/BMD ratio was 0.005. The p values for BMD and bone marrow fat in isolation were 0.02 and 0.045, respectively.


Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Bone Marrow Evaluation with Proton MR Spectroscopy
In the past, bone marrow fat was investigated by in vitro tissue analysis. Today, 1H MR spectroscopy allows noninvasive quantitative bone marrow fat evaluation on all standard clinical MRI units with no magnet strength restrictions. Multiple vertebrae spectra can be acquired within a few minutes. Proton MR spectroscopy easily can be added to routine lumbar MRI with little time penalty. Patients undergoing diagnostic MRI evaluation of the spine can be screened simultaneously for bone marrow fat. The entire skeleton is accessible, and no ionizing radiation is involved. So far, most advanced MR applications for bone analysis have relied on magnetic susceptibility considerations, as expressed in T2* relaxation measurements [26, 27]. They require a number of postprocessing steps that make the technique impractical for routine clinical use. In this study and in prior work, we used 1H MR spectroscopy and focused on bone marrow fat. On the basis of the results of this research, we believe that the use of 1H MR spectroscopy for bone assessment represents a potentially powerful extension of diagnostic MRI.

Bone Marrow Fat/BMD Relationship
The intention of this pilot study was to explore a possible connection between bone marrow fat and BMD. This comparison has not, to our knowledge, been conducted thus far. It was advocated here that bone marrow fat and BMD may be inversely related. Such a reciprocal relationship appeared plausible on the basis of the published observation that BMD decreases and marrow fat steadily and progressively increases with age [28, 29]. At the cellular level, the number and size of adipocytes increase with age in a linear fashion [30]. A connection between bone density and marrow fat also could be constructed on the basis of the observation that bone resorption cavities are filled with yellow marrow [11, 14, 28, 29, 31].

An inverse relationship between bone marrow fat and BMD was not supported in this study. Only a weak inverse correlation existed between BMD and bone marrow fat, as expressed in a correlation coefficient of –0.23. Larger series will be needed to look further into this relationship. At present, recommending bone marrow fat as a proxy for BMD is not justified. The apparent mismatch between bone marrow fat and BMD suggests that bone marrow fat and BMD may be unrelated or only partially related.

Value for Diagnosing Mechanical Weakening of Vertebrae
In this segment, two subject groups are juxtaposed: a group with MRI features suggesting vertebral bone weakening and a group of subjects with structurally normal-appearing vertebrae (Table 1). These two groups are small and their makeup may appear arbitrary. Although intact vertebrae in the "healthy" subject group still may harbor osteoporosis, imaging stigmata of bone weakening probably signify a greater degree of bone loss. Thus, juxtaposition of these groups appeared justified.

Evaluating the data of Table 1 with the logistic regression method showed that bone marrow fat can be used to diagnose bone weakening nearly as well as BMD. Nevertheless, at the sample size of this study, neither BMD nor bone marrow fat alone was suitable reliably to show bone weakening (p = 0.1 and 0.07, respectively). Although BMD did not show sufficient diagnostic power in this study, the sample size clearly is too small to challenge the historical diagnostic role of BMD [16, 26, 27]. Measurement of bone marrow fat for diagnosing reduced bone strength also cannot be ignored in view of other important observations. In a prior 1H MR spectroscopy study [17], vertebrae with bone weakening significantly had increased bone marrow fat based on Student's t test analysis. Also, in our study, the majority of subjects (73%) with weakened vertebrae had a percentage bone marrow fat fraction of 54% or higher (Fig. 2). This is abnormal for the age categories under consideration (age range, 51–71 years) and should be approximately 42.6% (SD = 12%) [17]. These results await analysis on a larger scale.

In spite of the noted limitations, the results point to an interesting diagnostic opportunity that combines the diagnostic potential of bone marrow fat and that of BMD in a single expression: the bone marrow fat/BMD ratio. This ratio proved to be a valid indicator of bone weakening (p = 0.02), showing significant diagnostic value even at the present sample size.

Possible Relationship of Increased Bone Marrow Fat and Bone Weakening
Our findings buttress literature reports postulating that bone weakening can be affected by agents other than BMD [1–4] and that bone fat itself can be a contributor to diminished structural bone integrity [14, 28, 31–34]. Osteoporosis is reported to be associated with increased bone marrow fat [28, 31–33]. Nuttall and Gimble [14] consider increased bone marrow fat at least partially responsible for bone weakening and recognize a therapeutic opportunity for treatment of bone loss by pharmacologic inhibition of bone marrow fat.

The relationship of bone marrow fat to bone weakening could be explained by several factors: First, excessive amounts of bone marrow fat could reflect diminished bone mass. This, in turn, could cause reduced bone strength [28, 29, 31, 35]. Second, increased adipogenesis competes with osteogenesis by reducing the population of osteoblasts as adipogenesis and osteogenesis may be regulated independently. Bone loss results [36]. This theory is supported in an animal experiment: Growth hormone administration to hypophysectomized rats inhibited the differentiation of stromal cells into adipocytes [37]. Third, marrow fat can directly influence the quality of trabecula [12]. Fourth, some believe that vertebral marrow quality itself is an important determinant of mechanical vertebral strength and increased bone marrow fat negatively may affect the biomechanical strength of bone. Marrow-filled intertrabecular spaces function as energy dampers and act as biomechanical support structures for medullary bone. Yellow marrow is a weaker biomechanical support medium than red bone marrow [34]. Red marrow contributes to hydrostatic strengthening, and fatty marrow causes greater compressibility of vertebrae. The combination of hematopoietic marrow (red), collagen, and hydroxyapatite forms a comparatively tough material.

This pilot study leads to the following conclusions: First, an inverse relationship between bone marrow fat and BMD cannot be confirmed. Second, bone marrow fat can be used to diagnose reduced bone strength nearly as well as BMD but, individually, neither bone marrow fat nor BMD was validated as a reliable indicator. Third, the bone marrow fat/BMD ratio is shown to be a significant diagnostic indicator of bone weakening even in this small subject sample. These findings need to be confirmed in a larger series.


References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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