Michael Dieckmeyer1,2, Stefan Ruschke2, Alexander Rohrmeier2, Jan Syväri2, Ingo Einspieler2, Jan S. Kirschke1, Ernst J. Rummeny2, Claus Zimmer1, Dimitrios C. Karampinos2, and Thomas Baum1
1Department of Diagnostic and Interventional Neuroradiology, Technical University of Munich, München, Germany, 2Department of Diagnostic and Interventional Radiology, Technical University of Munich, München, Germany
Synopsis
In recent years in-vivo
assessment of vertebral bone marrow (VBM) fat composition has been increasingly
used in the investigation of osteoporosis and bone metabolism. Postmenopausal
women represent a population of particular interest because they are at higher
risk for osteoporosis resulting from estrogen deficiency which can be potentially
aggravated by aromatase inhibitor (AI) therapy. The present study demonstrated
a relative increase in vertebral bone marrow fat content quantified by chemical
shift encoding-based water-fat MRI in patients receiving simultaneous AI and bisphosphonate
(BP) therapy, contradicting
previous findings reported in the literature.
Purpose
Quantification of vertebral bone marrow (VBM)
water–fat composition has been proposed as advanced imaging biomarker for
osteoporosis associated fracture risk prediction1,2. Estrogen is known to play an important role in
the pathogenesis of osteoporosis and estrogen deficiency is the primary reason
for trabecular bone loss in postmenopausal women3,4. By reducing
estrogen levels aromatase inhibitor (AI) therapy as part of breast cancer
traetment can promote bone loss. The additional administration of
bisphosphonates (BP) is recommended to counteract this adverse drug effect of
AI therapy. The purpose of our study was to quantify VBM proton density fat
fraction (PDFF) changes in the lumbar spine related to AI and BP treatment over
a 12-month period using chemical shift encoding-based water-fat MRI (CSE-MRI) and
magnetic resonance spectroscopy (MRS) as well as bone mineral density (BMD)
changes using dual energy X-ray absorptiometry (DEXA).Methods
Subjects: 27 postmenopausal
female estrogen receptor positive breast cancer patients (age = 63.3±6.4 years) receiving AI therapy were
recruited for this study. Inclusion criteria were no history of chemotherapy or
vertebral fractures. 5 subjects were lost to follow-up resulting in a total of
22 subjects completing the 1-year study. 14 subjects received AI and BP (zoledronic
acid) therapy (AI+BP), 8 subjects received AI without BP therapy (AI).
MR Imaging and Spectroscopy: All subjects underwent 3T MRI
(Ingenia, Philips Healthcare). An eight-echo 3D spoiled gradient-echo sequence
was used for CSE-based water-fat separation at the lumbar spine using the
built-in-the-table posterior coil elements (12-channel array). 8 echoes were
acquired in a single TR using non-flyback (bipolar) read-out gradients and the
following imaging parameters: TR/TE1/ΔTE = 11/1.4/1.1 ms,
FOV = 220×220x80 mm3, acquisition matrix = 124×121, voxel size =
1.8x1.8x4.0 mm³, receiver bandwidth = 1527 Hz/pixel, frequency direction = A/P
(to minimize breathing artifacts), 1 average, scan time = 1min 17s. A
flip angle of 3° was used to minimize T1-bias effects. Additionally, all
subjects underwent multi-TE STEAM MRS using the following parameters: TE1/ TE2/
TE3/ TE4 = 11/15/20/25 ms, TM = 16 ms, TR = 6000 ms, 8 averages per TE, 4096 sampling points, 5 kHz acquisition
bandwidth. The 15x15x15 mm3 MRS voxel was placed in the L3, L4 or L5
vertebral body depending on vertebral body size and avoiding severe
degenerative alterations and vascular structures.
Fat Quantification: The gradient echo
imaging data was processed online using the fat quantification routine of the
vendor. The routine first performs a phase error correction and then a
complex-based water–fat decomposition using a pre-calibrated seven-peak fat
spectrum and a single T2* to model the signal variation with echo
time and compute PDFF maps. Segmentation of the vertebral bodies L1-L5 was performed
manually on the PDFF maps using the open-source software
Medical Imaging Interaction Toolkit (Fig. 3). PDFF values were extracted at
each vertebral level from L1-L5 and averaged for each subject.
MRS spectra were fitted using
dedicated in-house routines built with MATLAB5. PDFF was computed as
the ratio of the T2‐corrected fat peak area over the sum
of the T2‐corrected fat peak area and T2‐corrected
water peak area.
BMD measurements: All subjects underwent DEXA (Lunar Prodigy, GE
Healthcare) of the lumbar spine measuring the average BMD of L1 to L4.
Results
Baseline age, BMD, CSE-based PDFF and MRS-based PDFF
showed no significant (p>0.05) difference between the two groups. There was
a relative longitudinal increase (∆rel) in
mean CSE-MRI-based PDFF averaged over L1-L5 in both groups (AI+BP: 5.93%; AI:
3.11%), however it was only significant (p=0.006) in the AI+BP group. There was
also a relative longitudinal increase in mean MRS-based PDFF in both groups
(AI+BP: 9.33%. AI: 7.55%), however not significant in either group (p>0.05).
∆rel of both CSE-MRI-based and MRS-based PDFF showed no significant
difference between the two groups. There was no significant longitudinal change
in BMD.Discussion & Conclusion
Over a 12-month period
VBM PDFF assessed with CSE-MRI significantly increased in subjects receiving combined AI
and BP therapy. The present results contradict previous results regarding the
effect of only BP therapy on bone marrow fat content quantified by MRS6 as
well as bone biopsies7. However, there is no previous study on the
combined effect of AI and BP therapy on VBM fat after one year. The reported
increase in VBM PDFF in subjects receiving combined AI and BP therapy was verified
by MRS measurements. Increasing the number of subjects and performing
additional follow-up measurements to assess longitudinal effects over a longer time period might help to further characterize the longer-term effects of combined AI and BP therapy on VBM PDFF.Acknowledgements
The present work was supported by the European
Research Council (grant agreement No 677661 – ProFatMRI and grant agreement No
637164 – iBack), TUM Faculty of Medicine KKF grant H01 and Philips Healthcare. This work reflects only the author's view and the EU is not responsible for any use that may be made of the information it contains.References
-
Patsch et al.: Bone marrow fat composition as a
novel imaging biomarker in postmenopausal women with prevalent fragility
fractures. J Bone Miner Res 2013; 28:1721.
- Schwartz et al.: Vertebral bone marrow fat associated
with lower trabecular BMD and prevalent vertebral fracture in older adults. J Clin Endocrinol Metab. 2013; 98:2294.
- Riggs et
al.: A Unitary Model for Involutional Osteoporosis: Estrogen Deficiency Causes
Both Type I and Type II Osteoporosis in Postmenopausal Women and Contributes to
Bone Loss in Aging Men. J Bone Miner Res. 1998; 13:763.
- Khosla et al.: The unitary model for estrogen deficiency and the pathogenesis of osteoporosis: is a revision needed? J Bone Miner Res. 2011; 26:441.
- Dieckmeyer
et al.: The need for T₂ correction on MRS-based vertebral bone marrow fat
quantification: implications for bone marrow fat fraction age dependence. NMR Biomed. 2015; 28:432.
- Yang et al.: Effect
of zoledronic acid on vertebral marrow adiposity in postmenopausal osteoporosis
assessed by MR spectroscopy. Skeletal Radiol. 2015; 44:1499.
- Duque et al.: Effects of risedronate on
bone marrow adipocytes in postmenopausal women.
Osteoporos Int. 2011; 22:1547.