(Radiology. 2000;217:863-868.)
© RSNA, 2000
Reactive Bone Marrow Changes in Infectious Spondylitis: Quantitative Assessment with MR Imaging1
Axel Stäbler, MD,
Ahmed B. Doma, MD,
Andrea Baur, MD,
Andreas Krüger, MD and
Maximilian F. Reiser, MD
1 From the Department of Clinical Radiology (A.S., A.B., M.F.R.) and Clinic for Orthopedic Surgery (A.K.), University of Munich, Grosshadern, Marchioninistrasse 15, D-81377 Munich, Germany; and the Radiodiagnostic Department, Research Institute of Ophthalmology, Giza, Egypt (A.B.D.). Received February 24, 1999; revision requested April 23; final revision received April 14, 2000; accepted May 5. Address correspondence to A.S. (e-mail: axel.staebler@ikra.med.uni-muenchen.de).
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ABSTRACT
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PURPOSE: To evaluate diffuse, reactive bone marrow changes in unaffected vertebrae on magnetic resonance (MR) images in patients with proved infectious spondylitis.
MATERIALS AND METHODS: Percentage signal intensity increase of the unaffected bone marrow on contrast material–enhanced MR images (percentage enhancement) was calculated retrospectively in 22 cases of infectious spondylitis and 86 cases without bone marrow disease. Multiple regression analysis and Student t test statistics were performed.
RESULTS: Multiple regression analysis showed a significant influence of age and the presence of spondylitis on the values of percentage enhancement (P < .001). For those aged 35 years or younger, the mean percentage enhancement was 43.2% ± 4.0 for patients with infectious spondylitis (n = 3) and was 26.4% ± 8.6 for the control group (n = 23). For those older than 35 years, the mean percentage enhancement was 28.2% ± 12.2 for patients with infectious spondylitis (n = 19) and 17.5% ± 7.9 (P < .001) for the control group (n = 63). Six (27%) of 22 patients with infectious spondylitis showed abnormal percentage enhancement values in unaffected bone marrow when the upper limit of the normal value was 2 SDs above the mean of the control group.
CONCLUSION: On MR images, reactive bone marrow changes can be found in unaffected vertebrae in patients with infectious spondylitis. The signal intensity changes and increased percentage enhancement associated with this disease are similar to those of myeloproliferative and diffuse neoplastic disorders and bone marrow stimulation in hemolytic anemia.
Index terms: Bone marrow, diseases • Magnetic resonance (MR), contrast enhancement, 30.12143 • Spine, infection, 30.201 • Spine, MR, 30.12143 • Spondylitis, 30.29
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INTRODUCTION
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Bone marrow signal intensity abnormalities due to diffuse myeloproliferative disease (eg, myelopathic polycythemia), hematologic neoplasia such as leukemia or multiple myeloma, diffuse bone marrow infiltration in cancer patients (eg, breast cancer), and stimulation of hematopoiesis in hemolytic anemia are detectable on magnetic resonance (MR) images (1–6). In these patients, the signal intensity of bone marrow is decreased on T1-weighted images and increased on T2-weighted or short inversion time inversion-recovery (STIR) images, and enhancement following injection of a gadolinium-based contrast medium is increased. We have observed similar signal intensity changes in patients with infectious spondylitis (Fig 1).
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Figure 1a. Infectious spondylitis at the level of the L1 and L2 vertebrae in a 54-year-old man. (a) Sagittal nonenhanced T1-weighted MR image (repetition time msec/echo time msec, 642/12) shows that the bone marrow signal intensity, which is normally higher than that of the disk on T1-weighted images (Fig 3a), is relatively decreased (circles 1 and 2) when compared to the signal intensity of the disk (solid arrow). Open arrow indicates the level of L1 and L2. (b) Sagittal gadolinium-enhanced T1-weighted MR image (642/12) exhibits marked enhancement of the area of involved bone marrow (L1 to L2) and unaffected bone marrow (circles 1 and 2), Circles indicate regions of interest for the measurements of unaffected bone marrow. Mean percentage enhancement was 32.7%.
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Figure 1b. Infectious spondylitis at the level of the L1 and L2 vertebrae in a 54-year-old man. (a) Sagittal nonenhanced T1-weighted MR image (repetition time msec/echo time msec, 642/12) shows that the bone marrow signal intensity, which is normally higher than that of the disk on T1-weighted images (Fig 3a), is relatively decreased (circles 1 and 2) when compared to the signal intensity of the disk (solid arrow). Open arrow indicates the level of L1 and L2. (b) Sagittal gadolinium-enhanced T1-weighted MR image (642/12) exhibits marked enhancement of the area of involved bone marrow (L1 to L2) and unaffected bone marrow (circles 1 and 2), Circles indicate regions of interest for the measurements of unaffected bone marrow. Mean percentage enhancement was 32.7%.
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Quantitative estimation of diffuse bone marrow disease with MR imaging can be achieved with estimation of the bulk T1 (7–12), chemical shift opposed-phase gradient-echo imaging (13–15), or calculation of the percentage enhancement (6,16). Measurement of percentage enhancement has been shown to be a reliable method to quantify diffuse bone marrow changes in malignant infiltration of plasmocytoma and breast cancer (6,16). A standardized dose of a gadolinium-based contrast medium and the use of identical imaging parameters for the nonenhanced and contrast material–enhanced T1-weighted spin-echo images are required. This retrospective study was undertaken to evaluate reactive bone marrow changes in unaffected normal or apparently normal vertebrae on T1-weighted MR images in patients with proved infectious spondylitis.
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MATERIALS AND METHODS
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Nonenhanced and contrast-enhanced MR images obtained at our institution in 22 patients with infectious spondylitis were retrospectively evaluated for quantitative analysis of unaffected bone marrow. During 4 years (July 1994 to August 1998), of 33 consecutive patients with the suspected diagnosis of infectious spondylitis, 22 patients (17 men, five women; mean age, 53 years; age range, 27–79 years) were identified in whom the existence of infectious spondylitis was proved by means of abnormal results of leukocyte count and C-reactive protein tests in connection with a characteristic bone marrow involvement of two adjacent vertebrae with decreased signal intensity on T1-weighted images and increased signal intensity on T2-weighted or STIR images. Patients with only one vertebra involved or without elevated values of C-reactive protein were excluded. The mean value of leukocyte counts was 13.61 x 109 per liter (range, 6.7–34.4 x 109 per liter; normal range, 4.0–11.0 x 109 per liter), and the mean value for C-reactive protein was 14.6 mg/dL (range, 3.7–38.5 mg/dL; normal value, <0.5 mg/dL). Eight patients had leukocyte counts that were within normal limits but clearly had elevated levels of C-reactive protein.
A positive test result for organisms was present in 14 of 22 patients: Staphylococcus aureus was found in 11, and streptococci were found in three. Testing was performed by means of blood culture in 10 patients, specimens from an operation in three, and biopsy in one. One patient showed serologic evidence for a Yersinia infection, and an organism could not be cultured in this case. Twelve patients had undergone surgery with use of an anterior and posterior approach to the involved segments. Ten patients were treated conservatively; two of these underwent computed tomographically guided biopsy. Antibiotic treatment in five of eight patients with negative test results probably explains why no organisms were found in their culture.
We also retrospectively evaluated the MR images of an age-matched control group that consisted of 86 persons (48 men, 38 women; mean age, 51 years; age range, 24–81 years) without known bone marrow disease. These persons were examined with enhanced MR imaging to prove or rule out disk disease. The MR imaging protocol was identical to that of the patients with infectious spondylitis, with a gadolinium-based contrast material applied routinely. In these patients, no clinical suspicion for chronic or acute infection was present.
Imaging included sagittal T1-weighted spin-echo sequences (repetition time msec/echo time msec, 450–750/12–15; field of view, 250 x 250–500 mm; section thickness, 3–4 mm; number of signals acquired, two to three) before and after intravenous bolus injection (3–5 seconds; rate, 2–3 mL/sec) of 0.1 mmol of gadopentetate dimeglumine per kilogram of body weight (Magnevist; Schering, Berlin, Germany). Imaging was performed with a 1.0 or 1.5-T scanner (Magnetom Impact or Harmony, Magnetom Vision; Siemens, Erlangen, Germany), with use of a spinal surface or phased-array coil. Contrast-enhanced imaging was started approximately 1 minute following injection of contrast material. The acquisition time was 3 minutes 29 seconds to 4 minutes 35 seconds for the spin-echo T1-weighted sequences for three acquisitions and 2 minutes 45 seconds for the fast spin-echo sequence with three acquisitions. The imaging parameters for the nonenhanced and contrast-enhanced acquisitions were identical.
Signal intensity measurements were made over a circled region of interest (mean diameter, 1.2 cm; minimum, 0.8 cm; maximum, 2.5 cm). Two to three regions of interest were placed on unaffected vertebral bodies of each patient in the same location on nonenhanced and contrast-enhanced T1-weighted spin-echo images; all regions of interest were placed by the same author (A.B.D.), and measurements were controlled by a second author (A.S.). Only vertebral bodies in the center of the spinal surface coil were measured. The midsagittal section with the basivertebral vein, complete or incomplete vertebral hemangiomas, fatty marrow replacement, and cortical borders was excluded from the measurements. Areas with signal degradation caused by pulsation artifacts (eg, cardiac pulsation) were also excluded. For each pair of nonenhanced and contrast-enhanced regions of interest, the percentage of signal intensity increase was calculated and the mean percentage enhancement determined by using the following formula: [(SIpost - SIpre)/SIpre]100%, where SI is signal intensity and "pre" and "post" are before and after injection of gadopentetate dimeglumine, respectively.
Since there were two variables, age (continuous variable) and the presence or absence of spinal infection (dichotomous variable), that had influence on the measured values of percentage enhancement, a multiple regression analysis was performed. In addition, as patients with bone marrow disorders are in general older than 35 years and to create distinct values for the percentage enhancement, the patient and control populations were divided into two groups, those 35 years or younger and those older than 35 years, and evaluated independently with use of the Student t test. Uptake of a gadolinium-based contrast material is higher in younger than in older persons (6). This finding correlates with the decrease of cellular marrow and increase of fat cells in hematopoietic marrow observed during aging.
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RESULTS
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A multiple linear regression technique was used to determine the correlation between the two independent variables, age and group (ie, patients with infectious spondylitis or control subjects), and the measured values of percentage enhancement, which was significant for both covariates (P < .001) (Table). The presence of an infectious spondylitis significantly increased the values for percentage enhancement. The negative association between age and the increase in signal intensity following injection of gadopentetate dimeglumine demonstrate the influence of the increased amount of fat cells in hematopoietic marrow during aging. Only 25% of the variation in percentage enhancement was explained by the combination of age and group (model r2 = 0.2463), so the existence of other important influencing factors can be suspected.
The values for the percentage enhancement for the spondylitis and control groups are given in a scatterplot diagram (Fig 2). The mean percentage enhancement in patients aged 27–35 years with infectious spondylitis (n = 3) was 43.2% ± 4.0, whereas in the control group (24–35 years; n = 23), the mean percentage enhancement was 26.4% ± 8.6. No statistical test was conducted for this group because of the small sample size. For patients older than 35 years in the infectious spondylitis group (n = 19), the mean percentage of gadolinium–related signal intensity increase (percentage enhancement) in unaffected bone marrow of the spine was 28.2% ± 12.2. In the control group (>35 years; n = 63), the mean percentage enhancement in bone marrow signal intensity was 17.5% ± 7.9. This difference was significant for those older than 35 years (P < .001, Student t test).
In the majority of patients (16 [73%] of 22) with infectious spondylitis, signal intensity and percentage enhancement of the unaffected bone marrow were normal (Fig 3). Six (27%) of the 22 patients with infectious spondylitis showed abnormal values for gadopentetate dimeglumine uptake in areas of unaffected bone marrow when the upper limit for the normal percentage enhancement value was 2 SDs above the mean percentage enhancement of the control group (Fig 4). The defined cutoff values for normal were 43.6% for those 35 years old and younger and 33.3% for those older than 35 years. No person in the control group 35 years old or younger (zero [0%] of 23) showed an abnormal value greater than 2 SDs above the mean value of this group for the percentage enhancement. One person in the control group older than 35 years (one [2%] of 63) showed an abnormal value greater than 2 SDs above the mean value.
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Figure 3a. Infectious spondylitis at the level of the L4 and L5 vertebrae in a 41-year-old man. Sagittal T1-weighted (a) nonenhanced and (b) gadolinium-enhanced MR images (750/12) show decreased signal intensity in a with marked enhancement in b of the infected bone marrow at this level, with enhancing granulation tissue anteriorly at the level of the spondylitis (arrow) and no abnormal enhancement of unaffected bone marrow. Areas of unaffected bone marrow, which were taken for measurement, are indicated by circles 1, 2, and 3. Enhancement was 15.9%.
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Figure 3b. Infectious spondylitis at the level of the L4 and L5 vertebrae in a 41-year-old man. Sagittal T1-weighted (a) nonenhanced and (b) gadolinium-enhanced MR images (750/12) show decreased signal intensity in a with marked enhancement in b of the infected bone marrow at this level, with enhancing granulation tissue anteriorly at the level of the spondylitis (arrow) and no abnormal enhancement of unaffected bone marrow. Areas of unaffected bone marrow, which were taken for measurement, are indicated by circles 1, 2, and 3. Enhancement was 15.9%.
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Figure 4a. Infectious spondylitis (S aureus) at the level of the T12 and L1 vertebrae in a 60-year-old man. Sagittal T1-weighted (a) nonenhanced and (b) gadolinium-enhanced MR images (450/12). At the level of the spondylitis, signal intensity of the infected bone marrow is decreased in a. The low-signal-intensity endplate is focally invisible (arrow), and there is epidural extension of the infective granulation tissue. In b, affected bone marrow, infective granulation tissue, and epidural space exhibit strong enhancement. Unaffected bone marrow also shows abnormal enhancement compared with the nonenhancing disk. Circled regions of interest for the measurements of the unaffected bone marrow are numbered 1, 2, and 3. Enhancement was 55.8%.
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Figure 4b. Infectious spondylitis (S aureus) at the level of the T12 and L1 vertebrae in a 60-year-old man. Sagittal T1-weighted (a) nonenhanced and (b) gadolinium-enhanced MR images (450/12). At the level of the spondylitis, signal intensity of the infected bone marrow is decreased in a. The low-signal-intensity endplate is focally invisible (arrow), and there is epidural extension of the infective granulation tissue. In b, affected bone marrow, infective granulation tissue, and epidural space exhibit strong enhancement. Unaffected bone marrow also shows abnormal enhancement compared with the nonenhancing disk. Circled regions of interest for the measurements of the unaffected bone marrow are numbered 1, 2, and 3. Enhancement was 55.8%.
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No statistically significant correlation was found between the enhancement percentages and the values for leukocyte count, C-reactive protein, or duration of spondylitis. A problem was that we were unable to define the precise duration of the infectious process because no reliable data were available on this from the clinical reports.
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DISCUSSION
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Direct visualization of the bone marrow makes MR imaging the method of choice for the diagnosis and staging of infectious and neoplastic diseases of the spine. In this respect, MR imaging is most valuable for focal diseases, such as metastasis or infectious spondylitis. When diffuse abnormalities of the bone marrow in hematologic neoplasias and myeloproliferative diseases are present without focal disease, an abnormal signal intensity of the bone marrow can be overlooked (16–20). In this situation, a homogeneous diffuse decrease in signal intensity over all vertebral bodies on T1-weighted spin-echo images results from a homogeneous replacement of fat cells by cellular marrow or an accumulation of iron in the bone marrow in hemolytic disorders. A replacement of fat cells by tumor cells or nonneoplastic cells in hemolytic disorders with stimulation of the bone marrow cells increases the amount of water-bound protons (4–6,11,15,18,21–23). A diffuse decrease in signal intensity of bone marrow can be found in uncontrolled stem cell proliferation in cases of myelodysplastic syndrome or malignant transformation and stem cell stimulation in hemolytic anemia. Also, fibrosis results in a decreased signal intensity on T1-weighted images.
Bone marrow cellularity may also be influenced by smoking, menstruation, hemolytic anemia, various drug therapies (especially hematopoietic growth factor during chemotherapy or enzyme therapy [eg, in Gaucher disease]), and endurance activities (24–31). Hematopoietic activity induced by growth factors can produce changes in bone marrow signal intensity that may simulate bone marrow involvement by musculoskeletal tumors (25). Hematopoietic bone marrow hyperplasia was also recognized in endurance athletes (26). Two articles (30,31) describe increased bone marrow reconversion or an elevated prevalence of red marrow around the knee in smokers. In the study by Poulton et al (30), no correlation between sex and marrow reconversion around the knee was obvious, whereas Wilson et al (31) reported an association between the presence of sex and red marrow. No association between smoking or sex and marrow celluarity of the spine was found in our search of the literature. Unfortunately, data concerning smoking habits or severity of menstruation from our control group were not available.
Our results indicate that in patients with chronic bacterial infectious spondylitis, MR imaging signal intensity alterations occur that are probably due to reactive bone marrow stimulation. The decreased signal intensity on T1-weighted images probably results from a replacement of fat cells by nonneoplastic, stimulated, proliferating bone marrow cells for the production of white blood cells in chronic infection. The signal intensity of this reaction is equal to that seen in myeloproliferative diseases, diffuse malignant bone marrow infiltration in carcinomas, and stimulation of the red bone marrow in hemolytic disorders. This reaction parallels the process of stimulation of hematopoiesis (red cells) and was found in six [27%] of 22 patients with infectious spondylitis.
Previously reported (7,10) quantitative estimations of bone marrow infiltration were performed by estimation of bulk T1. Our study findings confirm the usefulness of calculating the percentage enhancement for objective assessment of bone marrow alteration. A great variation in gadopentetate dimeglumine–related enhancement exists in normal bone marrow (3%–38%), with an age-dependent shift of the values for percentage enhancement to lower values with increasing age. Nevertheless, patients with infectious spondylitis can show pathologically increased values for percentage enhancement.
In conclusion, our results indicate that reactive bone marrow changes, which can occur in patients with infectious spondylitis, can be seen with MR imaging. Clearly visible changes in MR signal intensity in unaffected vertebrae are found in about 25% of patients with infectious spondylitis and are similar to those of bone marrow infiltration in malignant diseases, myeloproliferative diseases, hematologic neoplasia, and stimulation of cellular marrow in hemolytic anemias, with increased percentage enhancement following the administration of gadopentetate dimeglumine. In clinical practice, one should be aware of this phenomenon so as not to confuse diffuse bone marrow changes in infectious spondylitis with bone marrow diseases.
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ACKNOWLEDGMENTS
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The authors thank Michael Schmidt, PhD, of the Institute for Medical Information Processing, Biometry and Epidemiology of the University of Munich, Grosshadern, for the preparation of the statistics and his help in the evaluation of the data. We also thank Laurie Gauger for her assistance in preparing the manuscript.
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FOOTNOTES
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Abbreviation: STIR = short inversion time inversion recovery
Author contributions: Guarantor of integrity of entire study, A.S.; study concepts, A.S.; study design, A.S.; definition of intellectual content, A.S.; literature research, A.S., A.B.D.; clinical studies, A.K., A.B.; data acquisition, A.B.D., A.B.; data analysis, A.B.D., A.S.; statistical analysis, A.B., A.S.; manuscript preparation, A.B.D., A.S.; manuscript editing, A.S., M.F.R.; manuscript review, M.F.R.
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ABSTRACT
INTRODUCTION
) and the control group (
). Age is in years.