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Musculoskeletal Imaging |
1 From the Department of Radiology, Taipei Municipal Jen-Ai Hospital, Taipei, Taiwan (W.T.C., R.C.C., C.T.C., J.M.L., H.Y.T.); the Department of Radiology, National Taiwan University, Medical College and Hospital, No. 7 Chung-Shan S Rd, Taipei 100, Taiwan (T.T.F.S.); and the Department of Radiology, Taipei Municipal Chun-Shau Hospital, Taipei, Taiwan (S.Y.L.). Received September 29, 2000; revision requested November 14; final revision received January 29, 2001; accepted February 26. Address correspondence to T.T.F.S. (e-mail: ttfshih@ha.mc.ntu.edu.tw).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Dynamic magnetic resonance imaging (160 images obtained in 80 seconds) was performed from T10 to L5 in 66 patients. Patients were assigned to three groups: group 1, those 50 years or younger without compression fracture; group 2, those older than 50 years without compression fracture; or group 3, those older than 50 years with compression fracture. Peak enhancement percentage and enhancement slope were determined from the time-intensity curve of normal (nonfractured) vertebral body. Comparisons were made between groups, and the effect of age and sex interaction was analyzed.
RESULTS: Higher peak enhancement percentage was demonstrated for group 1 compared with group 2 (58.21 ± 44.65 [SD] vs 21.88 ± 14.77, P < .005). Group 1 women revealed a higher enhancement percentage compared with group 1 men (87.17 ± 54.13 vs 38.16 ± 21.69, P < .05), which significantly decreased in those older than 50 years (from 87.17 ± 54.13 to 17.98 ± 13.80, P < .005). For men, this decrease in those older than 50 years was not as pronounced (from 38.16 ± 21.69 to 25.38 ± 15.43, P > .05). Presence of compression fracture at other levels of the spine (group 3) was not associated with a different enhancement percentage for normal vertebrae.
CONCLUSION: Rate of vertebral bone marrow perfusion revealed a significant decrease in subjects older than 50 years. Women demonstrated a higher marrow perfusion rate than men younger than 50 years and a more marked decrease than men older than 50 years.
Index terms: Aging • Bone marrow, 321.10, 331.10 • Bone marrow, MR, 321.12144, 331.12144 • Magnetic resonance (MR), contrast enhancement, 321.12143, 331.12143 • Magnetic resonance (MR), perfusion study, 321.12144, 331.12144 • Osteoporosis, 30.562 • Spine, 30.562
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Laroche (5), in 1996, proposed vascular aging and arteriosclerosis within the bone as possible causes of osteoporotic change through an ischemic mechanism; however, the pathophysiologic characteristics of this ischemic mechanism are not fully understood. It is generally accepted that vascular degeneration associated with aging and arteriosclerosis may alter blood perfusion for the heart, brain, kidneys, and muscles. Thus, it seems reasonable to assume that blood perfusion for bone and marrow also decreases with age, possibly resulting in ischemia. If we accept this hypothesis, an understanding of bone and marrow blood perfusion, in vivo, is especially important.
In 1991, Cova et al (6) evaluated bone marrow perfusion of the proximal femur with gadolinium-enhanced dynamic fast magnetic resonance (MR) imaging in an animal model. There was a strong correlation between MR imaging data and microsphere blood-flow measurements (r = 0.81). These researchers also concluded that contrast material–enhanced dynamic MR imaging may facilitate early detection of abnormal bone marrow flow.
Bluemke et al (7), in 1995, also evaluated hip perfusion by using gadolinium-enhanced T1-weighted MR imaging in patients at risk for avascular necrosis and in healthy control subjects. These researchers demonstrated that the perfusion of the femoral head is inversely related to marrow fat content for healthy subjects and is higher in patients who have systemic lupus erythromatosus without hip avascular necrosis.
Dynamic MR imaging is commonly used for evaluating musculoskeletal neoplasms (8) and for monitoring the response to chemotherapy (9). In 1994, Verstraete et al (10) concluded that first-pass data from dynamic contrast-enhanced MR imaging depicted tissue vascularization and perfusion, although an overlap in the slope values was demonstrated for the highly vascular benign and malignant lesions. Van Der Woude et al (11), in 1995, also used dynamic MR imaging to detect residual viable tumor before surgery. In 1997, Bollow et al (12) used dynamic MR imaging findings for comparison of normal and malignant bone marrow infiltrations. Thus, dynamic MR imaging has proved to be an effective and noninvasive method for evaluation of in vivo blood perfusion of bone, marrow, and tumors.
The purpose of our study was to investigate blood perfusion of noncollapsed, normal-appearing vertebral bodies with regard to age and sex.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The patients were assigned to three groups. Group 1 included 22 patients (13 men, nine women; mean age, 40.1 years; SD, 7.5; age range, 22–49 years) 50 years of age or younger with no vertebral fracture or abnormal marrow signal intensity. Group 2 included 19 patients (10 men, nine women; mean age, 72.5 years; SD, 6.4; age range, 50–84 years) older than 50 years with no evidence of vertebral fracture or abnormal marrow signal intensity. Signal intensity of marrow for the vertebrae in subjects in groups 1 and 2 was high on T1-weighted images. Group 3 included 25 patients (five men, 20 women; mean age, 72.3 years; SD, 8.4; age range, 50–84 years) older than 50 years with one or more vertebral compression fractures. Patients with acute burst or traumatic fractures of the spine were not included. Patients in group 3 were classified according to symptom duration of less than or longer than 1 month. All three groups of patients were followed up for at least 6 months after they underwent the spinal MR study and they showed no clinical or radiologic evidence of progressive deterioration.
All patients in groups 1 or 2 and 13 patients in group 3 underwent an MR study without contrast enhancement to aid in the diagnosis of their back pain or sciatica. They agreed to receive an additional intravenous injection of contrast agent and to undergo one more study with a dynamic pulse sequence, and they provided written informed consent before participation. The remaining 12 patients in group 3 underwent both nonenhanced and enhanced imaging of the spine to help in the diagnosis of their back problems. They also provided written informed consent. Our study was conducted according to the principles of the Declaration of Helsinki.
MR Imaging
A routine MR study of the spine was performed by using a 1.5-T superconducting system (Powertrak 6000; Philips, Best, the Netherlands). A synergy spine coil was used. The routinely used nonenhanced MR sequences included a sagittal turbo spin-echo T1-weighted sequence, with a repetition time msec/echo time msec of 450/12, turbo factor of 4, section thickness of 4 mm, gap of 0.4 mm, and field of view (FOV) of 35 cm. The same sequence was also used to obtain images in the transverse plane with a smaller FOV (20 cm). Another MR sequence included a sagittal turbo spin-echo T2-weighted sequence, with 3,000/120, a turbo factor of 4, section thickness of 4 mm, gap of 0.4 mm, and FOV of 35 cm. The same sequence was also used to obtain images in the transverse plane with a smaller FOV (20 cm).
A dynamic contrast-enhanced MR image was then obtained with a section thickness of 10 mm and a 35-cm FOV in the midsagittal plane of the vertebral body. This FOV could cover the imaging range from T8 through T9 to the sacrum. Short T1-weighted gradient-echo sequences (turbo field echo; Philips), with 4/1.5, a prepulse inversion time of 400 msec, flip angle of 15°, and 179 x 256 acquisition matrix, were used. In total, 160 dynamic images were obtained within 80 seconds (2 frames per second) in each of the patients. A bolus of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany; 0.1 mmol per kilogram of body weight) was rapidly administered manually with an injection rate of approximately 2.5 mL/sec through a 21-gauge intravenous catheter previously inserted in the right antecubital vein. This injection was immediately followed by a 20-mL saline flush at the same injection rate. The dynamic imaging started as soon as the injection of the contrast medium commenced.
In those 12 patients in group 3 who underwent enhanced MR imaging, two more studies were performed after dynamic imaging: sagittal T1-weighted imaging with fat saturation and transverse T1-weighted imaging.
Data Analysis
Signal intensity values were measured in operator-defined regions of interest (ROIs). The ROIs were placed by one investigator (W.J.C.), with the aid of a cursor and graphic display device, and covered whole vertebral bodies, starting from the subchondral bone inside the cortex (Fig 1). Signal intensity was measured for nonfractured vertebral bodies in all three groups. The signal intensity values derived from the ROIs were plotted against time as a time-intensity curve by using a software system (Gyroview; Philips). The baseline value for signal intensity (SIbase) on a time-intensity curve was defined as the mean signal intensity from the first three images. The maximum signal intensity (SImax) was defined as the peak enhancement value for the first pass of contrast material. The contrast enhancement rise time (Trise) was defined as the time between SIbase and SImax. The peak enhancement percentage ([SImax - SIbase/SIbase] x 100%) and enhancement slope (SImax - SIbase/Trise) for each ROI were calculated and compared with those of other groups by using the t test. Peak enhancement percentage was calculated as (SImax - SIbase/SIbase) x 100%. Enhancement slope was calculated as SImax - SIbase/Trise.
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Comparisons were made between groups 1 and 2 by using the t test for evaluation of the effect of age and then between groups 2 and 3 also by using the t test for evaluation of the effect of compression fracture. Groups 1 and 3 were not compared, since group 3 included patients who were older than 50 years and who had a compression fracture and group 1 included patients who were 50 years of age and younger who did not have a compression fracture. We further stratified each group into men and women. Linear regression was performed to assess the potential age effect on both sexes.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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We further stratified each group into men and women (Table 3) and made comparisons by using the t test, with the following significant differences revealed: (a) Women in group 1 had a higher peak enhancement percentage than women in group 2 (87.17 ± 54.13 vs 17.98 ± 13.80, P < .005). (b) Men in group 1 had a lower peak enhancement percentage than women in group 1 (38.16 ± 21.69 vs 87.17 ± 54.13, P < .05). No significant difference in peak enhancement percentage was noted for men in group 1 versus men in group 2 (P > .05).
The influence of age and sex interaction on peak percentage enhancement in subjects in groups 1 and 2 was analyzed with linear regression. Since the regression for age and sex interaction on bone marrow perfusion and age was significant (P < .05), we plotted separately for male and female subjects (Fig 3). The slope for female subjects was higher than that for male subjects. We considered that the male and female subjects had decreasing peak percentage enhancement along with increasing age, and the female subjects had a more marked decrease.
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The means for enhancement slope and SD for the subjects in different groups are listed in Tables 2 and 4. Subjects in group 1 had a higher enhancement slope than subjects in group 2 (1.85 ± 1.59 vs 1.07 ± 0.72, P < .05). Women in group 1 had a higher enhancement slope than women in group 2 (2.31 ± 1.84 vs 0.82 ± 0.72, P < .05). The comparison was also made for the remaining groups, and no significant difference was noted.
Data for patients in group 3 (n = 25) were further analyzed according to the disease durations of their compression fractures. Eleven patients had recent compression fractures with symptom durations of less than 1 month, while the remaining 14 patients had chronic compression fractures with symptom durations of longer than 1 month. No significant difference was noted between the two subgroups; however, the group with more recent manifestation of symptoms demonstrated higher enhancement percentage and slope for normal nonfractured vertebrae (26.73 ± 20.64 vs 20.49 ± 17.42, P > .05; and 1.26 ± 1.38 vs 1.10 ± 1.34, P > .05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In our study, the blood perfusion of bone marrow was evaluated in the lower thoracic (T10 to T12) and lumbar (L1 to L5) vertebrae by using dynamic contrast-enhanced MR imaging. We demonstrated a decrease (from 58.21 to 21.88, 62.4%) in vertebral bone marrow perfusion in subjects older than age 50 years (Table 1, mean peak enhancement percentage decreased from 58.21 in group 1 to 21.88 in group 2, P < .005). This alteration may be explained by aging and arteriosclerosis, in our opinion. As proposed by Hui et al (15) in 1988, age and bone mass act as predictors of fracture; when the subsets were examined, it was demonstrated that age was a stronger predictor of fracture. Thus, vascular aging is an important factor in bone metabolism as a consequence of degeneration of bone marrow blood perfusion.
When subsets of bone marrow perfusion were examined according to age and sex (Table 3), a stronger association was demonstrated for sex. In male subjects, bone marrow perfusion decreased 33.5% (from 38.16 to 25.38) in those older than age 50 years. (Mean enhancement percentage decreased from 38.16 in men in group 1 to 25.38 in men in group 2; the difference between these two groups was not significant, P > .05.)
In female subjects, bone marrow perfusion decreased 79.4% (from 87.17 to 17.98) in those older than age 50 years. (Mean enhancement percentage decreased from 87.17 in women in group 1 to 17.98 in women in group 2; the difference between these two groups was significant, P < .005.) This finding may be related not only to aging but also to the change in female sex hormone level in women older than age 50 years.
Tsai et al (16) noted decreasing bone density associated with increasing age for the lumbar vertebrae in postmenopausal women but no significant age-related change in men. They also measured the levels of bone markers (bone alkaline phosphate isoenzymes, procollagen I C-terminal propeptide, osteocalcin, and N-terminal telopeptide of type I collagen) and found that bone markers increased with age in postmenopausal women but decreased in men (16). In addition, Tsai et al (17) mentioned that the prevalence for vertebral fracture was low in women younger than age 50 years, with a steady increase thereafter; in men, vertebral fracture increased at a lower rate. An increased bone turnover rate is associated with lowered bone mineral density in both men and postmenopausal women, although, with aging, the rate seems to increase in women but decrease in men (18).
In our study, bone marrow perfusion decreased in both sexes with increasing age; however, women had a more marked decrease than men. The influence of age and sex interaction on bone marrow perfusion was analyzed and is demonstrated in Figure 3; in women in groups 1 and 2, regression coefficients were higher than in men. The vertebral bone marrow perfusion in female subjects was high at a younger age, with a steady decrease thereafter; in male subjects, vertebral bone marrow perfusion decreased at a lower rate, without significant age-related change. Thus, our study findings were consistent with those of the previously mentioned articles, which demonstrated similar changes in age, sex, and age and sex interaction, indicating that bone marrow perfusion change or ischemia would be influenced by age and sex.
Our study, however, focused on the relationship between bone marrow perfusion change and aging and sex, with bone mineral density, bone markers, and sex hormone level not analyzed. This is the limitation of our study. However, the significant change demonstrated by this research, showing decreased bone marrow perfusion in subjects older than age 50 years, indicates the role of perfusion in the aging process and the effects on ischemia and bone metabolism. We considered that the study of bone marrow perfusion change may be an important research direction in investigating the pathogenesis of osteoporosis and the aging process of the bone.
The histologic study of bone marrow by Dunnill et al (19), in 1967, demonstrated that the volume of red marrow in vertebral bodies decreases from a mean of 58% in the 1st decade of life to a mean of 29% in the 8th decade of life. Concomitantly, there is an even greater increase in the percentage of fatty marrow with age. Ricci et al (20), in 1990, also demonstrated similar findings for fatty bone marrow distribution by using in vivo MR imaging. The histomorphometric measurements performed by Demmler et al (4), in 1983, also demonstrated that reduced hematopoietic elements in bone marrow are accompanied by a corresponding increase in fat cells and a decrease in arterial capillary and sinus numbers. These pieces of evidence further support our finding that decreased bone marrow perfusion is associated with increased age and fatty marrow percentage.
Vertebral body bone marrow perfusion was significantly higher in female subjects than in male subjects younger than age 50 years (Table 3) (group 1 women vs men, 87.17 vs 36.16, P < .05). This finding is not replicated in previous histologic studies of bone marrow, however, and no difference was demonstrated in our study in either sex in subjects older than age 50 years.
We assumed that the female menstrual cycle and sex hormones were important factors in higher bone marrow perfusion in women younger than age 50 years. The regular associated blood loss from menstration may stimulate erythropoietin secretion, also activating the hematopoietic marrow and promoting red marrow perfusion. However, the female sex hormone was not evaluated in our study, and the marrow perfusion was analyzed according to age, either older or younger than 50 years, and the age for menopause varies in each woman. The higher bone marrow perfusion in women younger than age 50 years noted in our study may suggest a possible relationship between blood perfusion and the female sex hormone and deserves further investigation.
Comparing bone marrow perfusion of normal vertebrae, no differences were demonstrated for either sex in groups 2 and 3 (P > .05). Our study did not, however, demonstrate a correlation between bone marrow perfusion change and the presence of fractures. Although the presence of fractures had a strong correlation with bone mineral density (15), bone mineral density was not measured in our study. When compression fracture occurs, the additional mechanical stresses associated with compression fracture may be transferred to the adjacent, nonfractured normal vertebrae, increasing vascularity in the endplates (21,22), and the adjacent normal vertebrae may compensate the blood perfusion. On the other hand, the relative ischemia for bone marrow in subjects older than age 50 years may be a precursor to, or associated with, the aging process before bone density decreases or the risk of fracture increases.
In conclusion, our study revealed a significant decrease in vertebral bone marrow perfusion in subjects older than age 50 years. The female subjects demonstrated a higher marrow perfusion than did the male subjects younger than age 50 years, with a more marked decrease in those older than age 50 years compared with the male subjects.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, T.T.F.S.; study concepts, T.T.F.S.; study design, T.T.F.S., W.T.C.; literature research, R.C.C., W.T.C.; clinical studies, W.T.C.; data acquisition, W.T.C., S.Y.L.; data analysis/interpretation, T.T.F.S., S.Y.L., W.T.C.; statistical analysis, W.T.C., C.T.C., S.Y.L.; manuscript preparation, J.M.L., W.T.C., C.T.C.; manuscript definition of intellectual content, T.T.F.S., W.T.C.; manuscript editing, T.T.F.S.; manuscript revision/review, W.T.C., T.T.F.S., H.Y.T., J.M.L., C.T.C.; manuscript final version approval, T.T.F.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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) and data from measurement (
) are shown.