Evaluation of MRI protocols for the assessment of lumbar facet joints after MR-guided focused ultrasound treatment

Roland Krug, Loi Do, Viola Rieke, Mark W Wilson, Maythem Saeed, Roland Krug, Loi Do, Viola Rieke, Mark W Wilson, Maythem Saeed

Abstract

Background: MR-guided focused ultrasound (MRgFUS) might be a very safe and effective minimally invasive technique to treat facet joint pain caused by arthritis and other degenerative changes. However, there are still safety concerns for this treatment and challenges regarding MR imaging and temperature mapping due to susceptibility effects between the bone and soft tissue near the joint, which has resulted in poor MR image quality. The goal of this research was to evaluate multiple magnetic resonance imaging (MRI) pulse sequences for characterizing ablated lumbar facet joint lesions created by high-intensity focused ultrasound (FUS) and compare the findings to histological tissue assessment. In particular, we investigated the use of T2-weighted MRI to assess treatment effects without contrast administration.

Methods: An IACUC approved study (n = 6 pigs) was performed using a 3T widebore MRI system equipped with an MRgFUS system. Facet joints of the lumbar vertebra were ablated using 1-MHz frequency and multiple sonication energies (300-800 J). In addition to T2-weighted MRI for treatment planning, T1-, T2-, and T2*-weighted and perfusion MRI sequences were applied. Signal intensity ratios of the lesions were determined. Histopathology was used to characterize cellular changes.

Results: Ablation of the facet joint, using MRgFUS, was successful in all animals. T2-weighted images showed high signal intensity in the edematous facet joint and adjacent muscle, while delayed contrast-enhanced T1-weighted images showed an enhanced ring surrounding the target volume. T2*-weighted GRE images revealed inconsistent lesion visualization. Histopathology confirmed the presence of cellular coagulation (shrinkage), extracellular expansion (edema), and hemorrhage in the bone marrow.

Conclusions: MRgFUS provided sufficient precision and image quality for visualization and characterization of ablated facet joints directly after ablation. MRI may help in monitoring the efficacy of FUS ablation without contrast after treating patients with back pain.

Keywords: Delayed contrast-enhanced MRI; Facet joint; MRgFUS; T2-weighted FSE.

Figures

Fig. 1
Fig. 1
T2-weighted planning images are shown with the focal spot on the facet joint (left image). The beam orientation was chosen to best protect the spinal nerve roots, the spinal canal, and the spinal process as outlined in green. After HIFU treatment, the area of ablation is shown in blue (dose overlay) on the right image
Fig. 2
Fig. 2
Coronal T1-FSE images. a Baseline. b After FUS ablation. c After both FUS and contrast injection. The lesions were delineated, as hypoenhanced zone, after administration of 0.15 mmol/kg Gd-DTPA, suggesting lack of delivery of the contrast media due to the damage of microvessels
Fig. 3
Fig. 3
Coronal T2-FSE (left) and DCE T1-FSE (right) after FUS treatment. The T2-FSE image shows a positive contrast of the lesions. The DCE T1-FSE image shows the hyperenhancement of the border zone, but not the core of ablated lesion. The following energies were applied (from top to bottom): 650, 300, 500, and 800 J, and the arrows indicate ablated lesions. A positive relationship between energy and lesion size can be appreciated in both images
Fig. 4
Fig. 4
Axial T2-FSE (left) and DCE T1-FSE (right) after FUS treatment. The T2-FSE image shows a positive contrast of the lesions. The DCE T1-FSE image shows the hyperenhancement of the border zone, but not the core of ablated lesion
Fig. 5
Fig. 5
Axial T2-weighted images. a Acquired before FUS. b After FUS treatment. The lesion is clearly visible as hyperintense signal, suggesting the presence of edema. The sonication energy used for the depicted joint was 800 J. Smaller lesion sizes were generated with smaller sonication energies
Fig. 6
Fig. 6
Sagittal MR images of the paraventricular muscles obtained on T2-FSE (left) and DCE T1-FSE. T2-FSE image shows the hyperintense edematous ablated lesion, while T1-FSE image shows the donut pattern enhancement after administration of Gd-DTPA
Fig. 7
Fig. 7
Representative axial T2*-weighted images acquired before (a) and after (b) FUS ablation. The slice location corresponds to the slices depicted in Fig. 4. A small hyperintense lesion is visible after ablation (arrow)
Fig. 8
Fig. 8
Sagittal image and histopathological section through the paravertebral muscles show the wedge shape-ablated lesion on DCE (left) and microscopy (right). Arrows denote the necrotic core with damaged tissue. Note the border edematous hyperenhanced zone (arrowheads) surrounding the ablated core on DCE (scale shows the SI range in arbitrary units). The border edematous zone is also seen on microscopy (arrowheads, calibration bar = 100 μm)
Fig. 9
Fig. 9
Microscopic sections of dorsal root ganglion after 800-J sonication showing no evidence of injury in neural cells or axons. Magnifications are ×10, ×40, and ×100
Fig. 10
Fig. 10
Histological sections of facet joint. a Control side with zoom ×2. b Control side with zoom ×40. c Ablated side with ×2. d Ablated side with ×40. Evidence of hemorrhage is clearly demonstrated in the treated facet joint. There was no change in the architecture of the osteoblast, most likely due to the short period of exam after ablation

References

    1. Hynynen K, Freund WR, Cline HE, Chung AH, Watkins RD, Vetro JP, et al. A clinical, noninvasive, MR imaging-monitored ultrasound surgery method. Radiographics: a review publication of the Radiological Society of North America, Inc. 1996;16(1):185–95. doi: 10.1148/radiographics.16.1.185.
    1. Hectors SJ, Jacobs I, Heijman E, Keupp J, Berben M, Strijkers GJ, et al. Multiparametric MRI analysis for the evaluation of MR-guided high intensity focused ultrasound tumor treatment. NMR Biomed. 2015;28(9):1125–40. doi: 10.1002/nbm.3350.
    1. Hectors SJ, Jacobs I, Moonen CT, Strijkers GJ, Nicolay K. MRI methods for the evaluation of high intensity focused ultrasound tumor treatment: current status and future needs. Magn Reson Med. 2016;75(1):302–17. doi: 10.1002/mrm.25758.
    1. Hectors SJ, Jacobs I, Strijkers GJ, Nicolay K. Multiparametric MRI analysis for the identification of high intensity focused ultrasound-treated tumor tissue. PLoS One. 2014;9(6):e99936. doi: 10.1371/journal.pone.0099936.
    1. Keshavarzi A, Vaezy S, Noble ML, Paun MK, Fujimoto VY. Treatment of uterine fibroid tumors in an in situ rat model using high-intensity focused ultrasound. Fertil Steril. 2003;80(Suppl 2):761–7. doi: 10.1016/S0015-0282(03)00783-0.
    1. Machtinger R, Tempany CM, Kanan Roddy A, Fennessy FM. Successful MRI-guided focused ultrasound uterine fibroid treatment despite an ostomy and significant abdominal wall scarring. ISRN obstetrics and gynecology. 2011;2011:962621. doi: 10.5402/2011/962621.
    1. Mahmoud MZ, Alkhorayef M, Alzimami KS, Aljuhani MS, Sulieman A. High-intensity focused ultrasound (HIFU) in uterine fibroid treatment: review study. Polish journal of radiology / Polish Medical Society of Radiology. 2014;79:384–90.
    1. Stewart EA, Gedroyc WM, Tempany CM, Quade BJ, Inbar Y, Ehrenstein T, et al. Focused ultrasound treatment of uterine fibroid tumors: safety and feasibility of a noninvasive thermoablative technique. Am J Obstet Gynecol. 2003;189(1):48–54. doi: 10.1067/mob.2003.345.
    1. Vaezy S, Fujimoto VY, Walker C, Martin RW, Chi EY, Crum LA. Treatment of uterine fibroid tumors in a nude mouse model using high-intensity focused ultrasound. Am J Obstet Gynecol. 2000;183(1):6–11.
    1. Zhang J, Feng L, Zhang B, Ren J, Li Z, Hu D, et al. Ultrasound-guided percutaneous microwave ablation for symptomatic uterine fibroid treatment—a clinical study. Int J Hyperthermia. 2011;27(5):510–6. doi: 10.3109/02656736.2011.562872.
    1. Catane R, Beck A, Inbar Y, Rabin T, Shabshin N, Hengst S, et al. MR-guided focused ultrasound surgery (MRgFUS) for the palliation of pain in patients with bone metastases—preliminary clinical experience. Ann Oncol. 2007;18(1):163–7. doi: 10.1093/annonc/mdl335.
    1. Zippel DB, Papa MZ. The use of MR imaging guided focused ultrasound in breast cancer patients: a preliminary phase one study and review. Breast Cancer. 2005;12(1):32–8. doi: 10.2325/jbcs.12.32.
    1. Okada A, Murakami T, Mikami K, Onishi H, Tanigawa N, Marukawa T, et al. A case of hepatocellular carcinoma treated by MR-guided focused ultrasound ablation with respiratory gating. Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine. 2006;5(3):167–71. doi: 10.2463/mrms.5.167.
    1. Hynynen K, McDannold N, Clement G, Jolesz FA, Zadicario E, Killiany R, et al. Pre-clinical testing of a phased array ultrasound system for MRI-guided noninvasive surgery of the brain—a primate study. Eur J Radiol. 2006;59(2):149–56. doi: 10.1016/j.ejrad.2006.04.007.
    1. Vykhodtseva N, McDannold N, Hynynen K. Progress and problems in the application of focused ultrasound for blood-brain barrier disruption. Ultrasonics. 2008;48(4):279–96. doi: 10.1016/j.ultras.2008.04.004.
    1. Harnof S, Zibly Z, Shay L, Dogadkin O, Hanannel A, Inbar Y, et al. Magnetic resonance-guided focused ultrasound treatment of facet joint pain: summary of preclinical phase. J Ther Ultrasound. 2014;2:9. doi: 10.1186/2050-5736-2-9.
    1. Weeks EM, Platt MW, Gedroyc W. MRI-guided focused ultrasound (MRgFUS) to treat facet joint osteoarthritis low back pain—case series of an innovative new technique. Eur Radiol. 2012;22(12):2822–35. doi: 10.1007/s00330-012-2628-6.
    1. De Poorter J, De Wagter C, De Deene Y, Thomsen C, Stahlberg F, Achten E. Noninvasive MRI thermometry with the proton resonance frequency (PRF) method: in vivo results in human muscle. Magnetic resonance in medicine : official journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine. 1995;33(1):74–81. doi: 10.1002/mrm.1910330111.
    1. Pauly KB, Rieke V, Holbrook AB, Grissom W, Chen J, Kaye E. MR-guidance of HIFU therapy. Conference proceedings : Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Conference. 2009;2009:141–4.
    1. Rieke V, Butts PK. MR thermometry. J Magn Reson Imaging. 2008;27(2):376–90. doi: 10.1002/jmri.21265.
    1. Bazzocchi A, Napoli A, Sacconi B, Battista G, Guglielmi G, Catalano C, et al. MRI-guided focused ultrasound surgery in musculoskeletal diseases: the hot topics. Br J Radiol. 2016;89(1057):20150358. doi: 10.1259/bjr.20150358.
    1. Hijnen NM, Elevelt A, Grull H. Stability and trapping of magnetic resonance imaging contrast agents during high-intensity focused ultrasound ablation therapy. Invest Radiol. 2013;48(7):517–24. doi: 10.1097/RLI.0b013e31829aae98.
    1. Bucknor MD, Rieke V, Do L, Majumdar S, Link TM, Saeed M. MRI-guided high-intensity focused ultrasound ablation of bone: evaluation of acute findings with MR and CT imaging in a swine model. J Magn Reson Imaging. 2014;40(5):1174–80. doi: 10.1002/jmri.24451.
    1. Fukunishi H, Funaki K, Ikuma K, Kaji Y, Sugimura K, Kitazawa R, et al. Unsuspected uterine leiomyosarcoma: magnetic resonance imaging findings before and after focused ultrasound surgery. International journal of gynecological cancer : official journal of the International Gynecological Cancer Society. 2007;17(3):724–8. doi: 10.1111/j.1525-1438.2007.00818.x.
    1. Kirkham AP, Emberton M, Hoh IM, Illing RO, Freeman AA, Allen C. MR imaging of prostate after treatment with high-intensity focused ultrasound. Radiology. 2008;246(3):833–44. doi: 10.1148/radiol.2463062080.
    1. Sung HY, Jung SE, Cho SH, Zhou K, Han JY, Han ST, et al. Long-term outcome of high-intensity focused ultrasound in advanced pancreatic cancer. Pancreas. 2011;40(7):1080–6. doi: 10.1097/MPA.0b013e31821fde24.
    1. Li X, Ma BC, Bolbos RI, Stahl R, Lozano J, Zuo J, et al. Quantitative assessment of bone marrow edema-like lesion and overlying cartilage in knees with osteoarthritis and anterior cruciate ligament tear using MR imaging and spectroscopic imaging at 3 tesla. J Magn Reson Imaging. 2008;28(2):453–61. doi: 10.1002/jmri.21437.
    1. Voogt MJ, Arntz MJ, Lohle PN, Mali WP, Lampmann LE. Uterine fibroid embolisation for symptomatic uterine fibroids: a survey of clinical practice in Europe. Cardiovasc Intervent Radiol. 2011;34(4):765–73. doi: 10.1007/s00270-010-9978-8.
    1. Wu F, Chen WZ, Bai J, Zou JZ, Wang ZL, Zhu H, et al. Tumor vessel destruction resulting from high-intensity focused ultrasound in patients with solid malignancies. Ultrasound Med Biol. 2002;28(4):535–42. doi: 10.1016/S0301-5629(01)00515-4.
    1. Hellerstein S. Fluids and electrolytes: physiology. Pediatrics in review / American Academy of Pediatrics. 1993;14(2):70–9. doi: 10.1542/pir.14-2-70.
    1. Vandenberg JI, Rees SA, Wright AR, Powell T. Cell swelling and ion transport pathways in cardiac myocytes. Cardiovasc Res. 1996;32(1):85–97. doi: 10.1016/S0008-6363(96)00048-X.
    1. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Solares J, Soler J. The role of Na+–H+ exchange occurring during hypoxia in the genesis of reoxygenation-induced myocardial oedema. J Mol Cell Cardiol. 1997;29(4):1167–75. doi: 10.1006/jmcc.1996.0352.
    1. Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys. 1984;10(6):787–800. doi: 10.1016/0360-3016(84)90379-1.
    1. Düx M. MRgFUS Frankfurt experience. 3. London, U.K: European Symposium on Focused Ultrasound Therapy; 2015.

Source: PubMed

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