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(Radiology. 2000;215:910-916.)
© RSNA, 2000

Technical Developments

Normal Lumbar Vertebrae: Anatomic, Age, and Sex Variance in Subjects at Proton MR Spectroscopy-Initial Experience1

Dieter Schellinger, MD, Chin Shoou Lin, PhD, Djamil Fertikh, MD, Jacob S. Lee, MD, MS, William C. Lauerman, MD, Fraser Henderson, MD and Bolivia Davis, MD

1 From the Departments of Radiology (D.S., C.S.L., D.F., J.S.L., B.D.), Orthopedic Surgery (W.C.L.), and Neurosurgery (F.H.), Georgetown University Medical Center, 3800 Reservoir Rd NW, Washington, DC 20007. From the 1998 RSNA scientific assembly. Received January 25, 1999; revision requested March 24; final revision received September 27; accepted October 20. Address correspondence to D.S. (e-mail: dschell37@aol.com).


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Fifty-seven subjects underwent proton magnetic resonance (MR) spectroscopy of the second lumbar vertebra to evaluate single-voxel and multivoxel techniques. Measurements included lipid-to-water ratios, lipid fractions, and line width. These data provide information about vertebral fat content. There was an age-dependent linear increase in fat content and sex dependence. A higher fat concentration was found in men. The observed spectra provide a basis for future study to determine clinical utility of vertebral proton MR spectroscopy.

Index terms: Bone marrow, MR, 30.12145 • Magnetic resonance (MR), chemical shift, 30.12145 • Magnetic resonance (MR), spectroscopy, 30.12145 • Spine, MR, 30.12145


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
In conventional magnetic resonance (MR) imaging, the signal emanating from vertebrae is a signal composite of its major tissue constituents: bone (cortical or cancellous) and bone marrow (hematopoietic or fatty) (1). Image analysis based on the relative MR signal intensity can be specific, but a quantitative evaluation of tissue components requires additional methods (1–9).

Proton MR spectroscopy, a quantitative method considered in this study, separates the total bulk MR signal into its components of distinct lipid and water signals (10–13). Schick et al (10,13) used proton MR spectroscopy to quantify marrow-based pathologic conditions. Schick et al (2) also performed proton MR spectroscopy of the lower femur in one volunteer to investigate bone density (MR densitometry). Therefore, proton MR spectroscopy has the potential to quantify all major vertebral tissue components (ie, bone and marrow). The quality and quantity of these tissues change with age and may also be sex dependent (6,14). Consequently, corresponding proton MR spectroscopic changes are expected.

To use proton MR spectroscopy as a diagnostic tool for vertebral bone and marrow analysis, it is important to know whether the spectral composition differs at various sites. Our first aim was to evaluate spectral dependency in anatomic locations within a vertebral body and to identify a volume of interest to serve as a representative tissue sample. This could make bone analysis with proton MR spectroscopy an easy and quick adjunct to routine spinal MR imaging.

Our second aim was to analyze proton MR spectroscopic spectra among healthy men and women at various ages. Baseline data are needed for meaningful interpretation of spectra, and the possible normal variation in spectra with respect to age and sex needs to be investigated. To our knowledge, such data are not available at this time (14,15).


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Fifty-seven subjects (27 male and 30 female subjects; age range, 15–87 years; mean age, 43 years ± 18 [SD]) underwent proton MR spectroscopy of the second lumbar vertebral body. Eleven subjects (eight men and three women; age range, 19–59 years; mean age, 35 years ± 14) were healthy volunteers. Forty-six subjects (19 male and 27 female subjects; age range, 15–87 years; mean age, 44 years ± 19) had undergone lumbar MR imaging for low back pain, but no bone abnormalities were seen. A normal L2 vertebra was a precondition for inclusion in the study. Subjects with MR images that showed pathologic bone conditions were excluded. We excluded patients with known diffuse marrow disease, focal lesions, compression fractures, and a history of radiation treatment or steroid therapy. L2 was chosen because it is less likely to be affected by degenerative changes when compared with lower lumbar vertebrae. All subjects gave informed consent. The study was conducted with a protocol approved by the institutional review board.

In 11 healthy volunteers, a multivoxel two-dimensional (2D) chemical shift imaging method was used. For 2D chemical shift imaging, a 1-cm-thick transverse center section of the L2 lumbar vertebral body was sampled, consisting of eight contiguous 1-cm3 voxels. The transverse slab was centered at the middle third of the vertebral body. It was placed by referring to the lateral localizer image. In the transverse plane, these voxels were aligned in two parallel transverse-voxel bands, four anterior and four posterior to the vertebral center (Fig 1). This position was chosen because it places the voxel away from the endplates, which often harbor secondary degenerative changes. Vertebral tissue texture closer to the endplates consists of more densely woven bone and represents a transitional zone between central trabecular and peripheral cortical bone. Bone architecture in this transitional zone is expected to be less consistent than that in the center section, which contains more loosely woven trabeculae. Also, center sections are easier landmarks for repetitive scanning.



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  		Figure 1. Schematics depict voxel positions. Top: In transverse view of L2, squares 1-8 represent 1-cm3 voxels in a multivoxel array. Bottom: Lateral view of L2 shows the position of the central slab for the multivoxel acquisition, which consists of an anterior and a posterior row of voxels. SV indicates the position of the single voxel used in the single-voxel technique.

 
Five of these 11 subjects also underwent a separate spectroscopic examination with the single-voxel method. The single voxel was placed anterior to the center of L2. The proper precentral voxel position was achieved by referencing the voxel to the anterior and sagittal localizer images. On the sagittal localizer image, the center of the voxel was approximately between the middle and anterior third of the vertebral body (Fig 1). The remaining 46 subjects underwent imaging with only the single-voxel method, with the voxel placed in the same location as in the first group (ie, anterocentral) (Fig 1).

The total subject base allowed (a) intrasubject comparison of single-voxel spectra with corresponding spectra obtained with multivoxel technique and (b) evaluation of sex and age dependence. Voxel positioning was always performed by the same individual (C.S.L.).

All measurements were performed with a 1.5-T system (Vision; Siemens, Erlangen, Germany). The body coil was used for transmitting radio-frequency power, and a quadrature spine phased-array coil served for signal reception. Unlike in cerebral proton MR spectroscopy, water suppression is not needed in vertebral proton MR spectroscopy. The water signal is fully exploited by manually setting the water suppression voltage to zero before data acquisition. Spectroscopic data were acquired with stimulated echo acquisition mode, or STEAM, sequences in both the single-voxel and 2D chemical shift imaging methods. The stimulated echo acquisition mode was used because it appeared superior to point-resolved spectroscopy, or PRESS, in several ways. It provides better spacial resolution and concomitant reduction of partial volume effects while also allowing the use of shorter echo times (16,17). The sequence characteristics of the stimulated echo acquisition mode benefit T1 measurements (10), which are crucial for the evaluation of lipids. The applied software is approved by the U.S. Food and Drug Administration and commercially available with the standard proton MR spectroscopic package for this system. To our knowledge, other major vendors offer similar capabilities.

Single-voxel imaging parameters included repetition time of 5,000 msec and echo time of 20 msec (5,000/20), voxel size of 1 cm, 32 signals acquired, 1,024 data points, spectral bandwidth of 1,000 Hz, and total scanning time of 2 minutes 40 seconds. Two-dimensional chemical shift imaging parameters included 5,000/20, 16 x 16 partitions, 1-cm voxel size, one signal acquired, 1,024 data points, spectral bandwidth of 1,000 Hz, and total scanning time of 21 minutes.

The use of repetition time of 5,000 msec allowed observation of fully T1-relaxed MR. Keeping echo time at 20 msec minimized MR signal reduction due to the T2 effect. The imaging parameters for both the single-voxel and 2D chemical shift imaging methods were kept the same to ensure comparability of the spectra.

All spectra exhibited a water peak and one dominant lipid peak, methylene, separated by 3.1 ppm. Global shimming was performed before each data acquisition (MAPSHIM; Siemens). The peak amplitude of the methylene and water signals were measured and used to calculate the peak lipid-to-water ratio (LWR) for each voxel. Peak LWR can be used to measure lipid fractions and percentage volume of fat and water within the voxel (2,13). We used ratios rather than direct signal measurements because the absolute amplitude of a signal peak can vary from patient to patient and from one anatomic zone to another. Signal peaks are also influenced by the surface coil in use, patient body habitus, and the geometric relationship of voxel and the surface coil. The LWR is not affected by these factors and is, therefore, the preferred mode of quantification.

Peak LWR is obtained by dividing the lipid peak amplitude by the water peak amplitude. For example, a spectrum with a lipid peak amplitude of 35 mm and a water peak amplitude of 40 mm has a peak LWR of 35/40 or 0.88. The lipid fraction (LF) is derived from this formula: LF = peak LWR/(peak LWR + 1). The percentage lipid fraction equals LF x 100. Since studies in the literature often use lipid fraction or percentage lipid fraction, it was also used in this study to allow comparison with data in other publications.

For signal assessment, some investigators use measurements of peak area rather than peak amplitude. In 37 subjects (22 men and 15 women; age range, 19–79 years; mean age, 40 years ± 17), we were able to make signal area measurements and determine area and peak LWRs. Signal area measurements were made by charting the area covered by the water and lipid signals by means of a spectroscopic processing software. The water peak area was measured first, followed by the total area of the entire spectrum. The lipid peak area was derived from the difference between the two measurements. Peak and area LWRs were compared in all 37 subjects. This comparison was made to determine whether concordant data are achieved with these two methods. If concordance was found, use of the much simpler peak measurement would be preferable.

In these 37 subjects, we also determined the signal line width by measuring the full width at half maximum of each signal. Line width is commonly measured in hertz (2,4,13). Line width depends on the distribution of the static magnetic field, which influences water and lipid peaks in the same way. We used the water peak for this data set. Since the water peak always consists of a single peak, it is more suitable for measurement of full width at half maximum (2). Line width is influenced by magnetic field inhomogeneities, which stem largely from bone trabeculae (2,4,6,13). LWR provides information about the bone marrow, but line width may be a function of bone density.

Peak and area LWR data were analyzed with the linear regression method. Additionally, the paired Student t test was used to compare the sex difference regarding line width and peak LWR. The statistical evaluation was conducted with commercially available software (EXCEL; Microsoft, Redmond, Wash).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The spectra show a water peak on the left side of the spectrum and a lipid peak on the right (Fig 2). The signals are separated by approximately 3.1 ppm. In most cases, the lipid signals were unstructured, with the various lipid fragments generally not resolved. The line shape of the water signals was usually unstructured.



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  		Figure 2a. Volume-selected proton MR spectroscopy of the body of L2 in (a) 37- and (b) 65-year-old healthy men. In each spectrum, signals of water (left peak) and lipid (right peak) are clearly seen and are separated by approximately 3 ppm. Peak LWR was 0.73 in a and 3.18 in b.

 


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  		Figure 2b. Volume-selected proton MR spectroscopy of the body of L2 in (a) 37- and (b) 65-year-old healthy men. In each spectrum, signals of water (left peak) and lipid (right peak) are clearly seen and are separated by approximately 3 ppm. Peak LWR was 0.73 in a and 3.18 in b.

 
Anatomic Region Dependence
The peak LWRs for 11 subjects are listed in Table 1. Each voxel row consisted of two central and two peripheral voxels. Inner voxels 2 and 3 or 6 and 7 denote antero- and posterocentral voxels, respectively. Outer voxels 1 and 5 or 4 and 8 are right and left peripheral voxels, respectively. The anterocentral voxels showed peak LWRs that were 15%–120% higher than those of the posterocentral voxels (ie, their fat content was always higher). Conversely, in posterocentral voxels, the water content was consistently higher. The peripheral-voxel groups (voxels 1 and 5 or 4 and 8) showed variable and inconsistent peak LWRs.


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  		TABLE 1. Peak LWRs with Multivoxel and Single-Voxel Techniques
 
Multivoxel (2D Chemical Shift Imaging) versus Single-Voxel Proton MR Spectroscopy
In five subjects, single-voxel proton MR spectroscopy was performed in addition to the multivoxel scheme (Table 1). An effort was made to place the single voxel in the anterocentral region, close to voxels 2 and 3 (Fig 1). In two subjects, the peak LWRs of the single voxels matched those of voxels 2 and 3 almost perfectly (3%–4% variance). In three subjects, the peak LWRs deviated by 19%–25%. In these subjects, peak LWRs of single voxels more closely approximated those of posterocentral voxels (2%–13% variance). The differences in peak LWR were probably caused by imprecise placement of the single voxels and by bleeding artifacts seen on 2D chemical shift images with central-voxel spectra contaminated by peripheral-voxel spectra.

Age and Sex Dependence
Fifty-seven subjects underwent proton MR spectroscopy for evaluation of their vertebral bone marrow profile. In the 11 subjects who underwent 2D chemical shift imaging, the mean values for voxels 2 and 3 were used for this analysis. In all other patients, single-voxel data were used.

Peak LWRs for 57 subjects and area LWRs for 37 subjects are depicted in Figure 3 and listed in Table 2. Peak and area LWRs progressed with age in a linear fashion for both sexes. Values of peak and area LWRs, percentage lipid fractions, and lipid fractions (Fig 3, Table 2) are interdependent and therefore run parallel.



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  		Figure 3a. Scatterplots depict (a) peak and (b) area LWRs, which show a continuous increase with age. Peak and area LWRs are higher in men ({block}) than in women ({blacklozenge}). Note that data for fewer subjects were analyzed for area LWRs (Table 2).

 


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  		Figure 3b. Scatterplots depict (a) peak and (b) area LWRs, which show a continuous increase with age. Peak and area LWRs are higher in men ({block}) than in women ({blacklozenge}). Note that data for fewer subjects were analyzed for area LWRs (Table 2).

 

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  		TABLE 2. Summary of Lipid Fractions, LWRs, and Line Width
 
With the linear regression method, peak LWRs in women show age progression. The slope for peak LWR was 0.175 (intercept, - 0.108; r = 0.974). For men, the age progression of peak LWR had a slope of 0.247 (intercept, - 0.05; r = 0.91). There was a clear trend for higher peak LWRs in the male group for all decades. For the male group as a whole, the t test showed that the difference in peak LWR between the sexes was significant (P < .005). The greatest peak LWR differential between sexes was found during the 4th decade (peak LWR, P < .01). Decade by decade (Table 2), peak LWRs and related values (area LWR, lipid fraction, percentage lipid fraction) are consistently higher in the male group.

In 37 subjects, line width varied between 25.7 and 50.0 Hz (Fig 4, Table 2). In the 3rd and 4th decades, line width was significantly larger in the male group than in the female group (P < .005). The remaining age groups were sparsely represented, and no meaningful conclusions could be drawn at this time.



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  		Figure 4. Scatterplot depicts line width by age and sex. Line width is highest in the 3rd and 4th decades, when men ({block}) exhibit values higher than those in women ({blacklozenge}). In the groups older than 50 years, the data are too sparse to allow meaningful conclusions.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Bone marrow is composed mainly of water and lipid. Accurate determination of these two key fractions can be achieved with proton MR spectroscopy, which has the ability to transform bulk MR imaging data into these two distinct components (Fig 2). To our knowledge, there have been only few publications on vertebral proton MR spectroscopy. Schick et al (10,18) obtained vertebral proton spectra in patients with bone pathologic conditions and healthy volunteers. The number of subjects in their test series (10,13) was limited. No attempt was made in their series to examine sex or age dependence.

Single-Voxel versus Multivoxel Techniques
Acquisition time per voxel was almost equal for both techniques. Since preparation time was similar for both methods, 2D chemical shift imaging offered a net time saving per voxel. The use of 2D chemical shift imaging for bone analysis is new. Our data suggest spectral dependency on anatomic location. Two-dimensional chemical shift imaging has the advantage of allowing selection among several voxels of the most representative voxel for signal analysis. This could be important for bone marrow evaluation in myelo- or lymphoproliferative disorders, in which involvement can be focal and spotty. It may also be useful for selection from several voxels of a signature voxel for LWR measurements. The single-voxel method appears ideal for serial bone analysis and screening because of the much shorter acquisition time. This technique requires greater attention to proper voxel placement.

Validity of Multivoxel Technique
In five subjects, we placed a single voxel in the anterocentral position and compared its spectrum with that of a correlating voxel in the multivoxel array (Table 1). We found a very close match in two subjects with a peak LWR spread of only plus or minus 3%–4%. In three subjects, the spectrum of the single voxel more closely matched that of the posterocentral 2D chemical shift imaging voxels (2%–13% variance) than that of the anterocentral 2D chemical shift imaging voxels (19%–25% variance). We believe that imprecise placement of the single voxels was responsible for the small disparities.

Anatomic Variance
In 11 subjects, 2D chemical shift imaging data indicated variability in spectral composition among the eight voxels (Table 1). The LWRs of the anterocentral voxels (voxels 2 and 3) were 15%–120% higher than those of the posterocentral voxels (voxels 6 and 7). Schick et al (10) compared spectra from different locations inside the same vertebral body measured with the single-voxel method; they also noted that the LWR of anterior voxels was higher than that of voxels in more posterior positions (0.95 vs 0.45). We believe that spectra of the dorsal moiety are contaminated by venous blood from the basivertebral vein. Its large dorsal trunk runs in midline and likely influences the spectral composition in favor of water. Findings in the peripheral voxels were highly variable and inconsistent. This is probably caused by partial volume effects from tightly woven cancellous bone, cortical bone, or perivertebral fat. Schick et al (10) also observed variance in lipid signals of as much as 30% among voxels at different sites in the L3 vertebral body.

Spectral Analysis
For clinical use, it is essential to define the range of proton MR spectroscopic variations in healthy subjects. Fifty-seven healthy subjects showed a clear linear age progression of peak and area LWRs and percentage lipid fractions (Fig 3, Table 2). In 37 subjects, peak and area LWRs could be compared. Since the two parameters run parallel, we recommend signal evaluation with peak amplitude measurement, which is easy and quick. Men had higher LWRs and, therefore, higher percentage lipid fractions than did women (Fig 3, Table 2). The sex difference was present in all age groups and was most significant for the 4th decade (P < .01).

The adult bone marrow is composed of 30% lipid and 70% water (1). Since the lipid fraction is contained primarily within fatty (yellow) bone marrow, the rising percentage lipid fraction with age (11%–63%) (Table 2) indicates an age-related increase in fatty marrow , which is supported by Dunnill et al (14). Schick et al (10) found the percentage lipid fractions of healthy volunteers (n = 15) with mean age of 36 years ± 7.6 to be in the range of 22%–79%. In our study, we found percentage lipid fractions of 22%–45% in a similar age group. In another study by Schick et al (13), which included 26 healthy volunteers aged 20–68 years, the percentage lipid fractions were 26%–85%. This compares with 22%–64% in our study. Schick et al did not look into sex differences.

The water fraction approximates the percentage volume of hematopoietic (red) marrow. It declined with age from 81%–89% in the 2nd decade to 37%–45% in subjects older than 70 years (Table 2, Fig 2). In a quantitative histologic study of vertebrae in 95 healthy subjects (14), a decline in hematopoietic marrow was reported with age. It dropped from 57.9% (11st decade) to 29.2% (8th decade) and showed no sex difference. Dooms et al (6) evaluated bone marrow of vertebrae by measuring T1 and T2 in patients aged 4–80 years. They concluded that there was a progressive conversion of hematopoietic marrow to fatty marrow.

Several studies in the literature examine sex-related differences in fatty marrow content of bone (19–26). The issue remains unresolved, however, as equal bodies of data support or contradict the notion of sex dependence. Findings in studies that support sex differences (23–26) suggest that bone marrow in men has a higher lipid fraction, which supports our findings. None of these studies involve vertebral proton MR spectroscopy. Instead, marrow quantification was based on inspection at MR imaging (20,21), T1 or T2 analysis (19,22,23,26), or chemical shift MR imaging (24,25,27,28).

Line width of bone is reported to stem mainly from the inhomogeneity in the magnetic field produced by bone trabeculae (2,6,13). Other factors, such as inhomogeneity in the static magnetic field and in the surface coil radio-frequency magnetic induction field can influence line width. Schick et al (2) found that the spectral line width of a normal calcaneus bone was much larger than that of an osteoporotic calcaneus bone (47.2 vs 25.1 Hz) and proposed proton MR spectroscopy as a method for quantitative MR bone densitometry, with line width as the key parameter. Therefore, we included line width measurements in our study (Fig 4) and expected the values to decline with age as an expression of progressive bone loss. This could not be substantiated in our subject group for lack of data points, particularly in the groups older than 50 years. Line widths in the 3rd and 4th decades were significantly different between the sexes (P < .005), but meaningful conclusions can not be derived at this time.

Prospects of Proton MR Spectroscopy for Assessment of Bone Quality
At this time, there is not enough evidence to suggest that line width can serve as a measure of bone mass, but LWRs and lipid fractions are potentially useful. Osteoporosis yields loss of trabecular bone and produces widened spaces between the remaining trabeculae (29,30). In one study (31), increased trabecular spacing accounted for 67% of the decrease in bone volume that occurred with age. Bone loss creates resorption cavities (32). Fatty marrow expands into the widened marrow spaces (6,29,33). Dunnill et al (14) observed that fatty marrow increases with age "which is even more marked than the fall in cellular marrow, presumably because fatty marrow is replacing bone and hematopoietic tissue." The disproportionate increase in fatty marrow was attributed to the additional fat cells necessary to replace trabecular bone loss. This concept is also supported by others (9). If bone quality and the quantity of fatty marrow were inversely related, the lipid fraction could become an indirect measure of bone mass.

Why is the LWR higher in men than in women? We believe that increased fat marrow content in healthy men may be a physiologic phenomenon that has no effect on the bone mineral density or overall bone strength. In both men and women, however, marrow fat increased beyond a critical point may affect bone strength. This hypothesis awaits confirmation. The role of line width in determining bone density is uncertain at this time.

The possibility of using proton MR spectroscopy for diagnosis and quantification of osteoporosis represents a challenge. Since the spine is particularly prone to osteoporosis and compression fractures (11,33), direct analysis of bone quality would be important at the vertebral level (29,33,34). Proton MR spectroscopy, an easy add-on to routine spinal MR imaging, could fill an important diagnostic void. More studies are needed, however, to determine whether proton MR spectroscopy is a useful method in the evaluation of osteoporosis. Comparison with current methods, particularly absorptiometry (1–4,6,35), is needed to test this component of proton MR spectroscopy.


   Footnotes
 
Abbreviations: LWR = lipid-to-water ratio, 2D = two-dimensional

Author contributions: Guarantors of integrity of entire study, D.S., C.S.L.; study concepts and design, D.S., C.S.L.; definition of intellectual content, D.S., C.S.L.; literature research, D.S., C.S.L., D.F., J.S.L.; clinical studies, D.S., C.S.L., D.F.; experimental studies, D.S., C.S.L., D.F.; data acquisition, D.S., C.S.L., D.F.; data analysis, D.S., C.S.L., D.F., J.S.L.; statistical analysis, C.S.L., D.F., J.S.L.; manuscript preparation, D.S., C.S.L., D.F., J.S.L.; manuscript editing and review, all authors.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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