Percutaneous computed tomography fluoroscopy–guided conformal ultrasonic ablation of vertebral tumors in a rabbit tumor model

Laboratory investigation

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  • 1 Departments of Neurosurgery and
  • 2 Interventional Radiology, Johns Hopkins University, Baltimore, Maryland;
  • 3 Systems Research Division, Acoustic MedSystems, Inc., Champaign, Illinois;
  • 4 Department of Radiation Oncology, University of California, San Francisco, California; and
  • 5 Department of Computing, Queen's University, Kingston, Ontario, Canada
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Object

Radiofrequency ablation (RFA) has proven to be effective for treatment of malignant and benign tumors in numerous anatomical sites outside the spine. The major challenge of using RFA for spinal tumors is difficulty protecting the spinal cord and nerves from damage. However, conforming ultrasound energy to match the exact anatomy of the tumor may provide successful ablation in such sensitive locations. In a rabbit model of vertebral body tumor, the authors have successfully ablated tumors using an acoustic ablator placed percutaneously via computed tomography fluoroscopic (CTF) guidance.

Methods

Using CTF guidance, 12 adult male New Zealand White rabbits were injected with VX2 carcinoma cells in the lowest lumbar vertebral body. At 21 days, a bone biopsy needle was placed into the geographical center of the lesion, down which an acoustic ablator was inserted. Three multisensor thermocouple arrays were placed around the lesion to provide measurement of tissue temperature during ablation, at thermal doses ranging from 100 to 1,000,000 TEM (thermal equivalent minutes at 43°C), and tumor volumes were given a tumoricidal dose of acoustic energy. Animals were monitored for 24 hours and then sacrificed. Pathological specimens were obtained to determine the extent of tumor death and surrounding tissue damage. Measured temperature distributions were used to reconstruct volumetric doses of energy delivered to tumor tissue, and such data were correlated with pathological findings.

Results

All rabbits were successfully implanted with VX2 cells, leading to a grossly apparent spinal and paraspinal tissue mass. The CTF guidance provided accurate placement of the acoustic ablator in all tumors, as corroborated through gross and microscopic histology. Significant tumor death was noted in all specimens without collateral damage to nearby nerve tissue. Tissue destruction just beyond the margin of the tumor was noted in some but not all specimens. No neurological deficits occurred in response to ablation. Reconstruction of measured temperature data allowed accurate assessment of volumetric dose delivered to tissues.

Conclusions

Using a rabbit intravertebral tumor model, the authors have successfully delivered tumoricidal doses of acoustic energy via a therapeutic ultrasound ablation probe placed percutaneously with CTF guidance. The authors have thus established the first technical and preclinical feasibility study of controlled ultrasound ablation of spinal tumors in vivo.

Abbreviations used in this paper: CTF = CT fluoroscopic; HIFU = high-intensity focused ultrasound; HIIU = high-intensity interstitial ultrasound; RFA = radiofrequency ablation.

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Contributor Notes

Address correspondence to: Daniel M. Sciubba, M.D., Department of Neurosurgery, Johns Hopkins University, 600 North Wolfe Street, Meyer Building 8-161, Baltimore, Maryland 21287. email: dsciubb1@jhmi.edu.
  • 1

    Amundson E, , Pradilla G, , Brastianos P, , Bagley C, , Riley LH III, & Garonzik IM, : A novel intravertebral tumor model in rabbits. Neurosurgery 57:341346, 2005

    • Search Google Scholar
    • Export Citation
  • 2

    Bilsky MH, , Boland PJ, , Panageas KS, , Woodruff JM, , Brennan MF, & Healey JH: Intralesional resection of primary and metastatic sarcoma involving the spine: outcome analysis of 59 patients. Neurosurgery 49:12771286, 2001

    • Search Google Scholar
    • Export Citation
  • 3

    Burak WE Jr, , Agnese DM, , Povoski SP, , Yanssens TL, , Bloom KJ, & Wakely PE, : Radiofrequency ablation of invasive breast carcinoma followed by delayed surgical excision. Cancer 98:13691376, 2003

    • Search Google Scholar
    • Export Citation
  • 4

    Callstrom MR, , Charboneau JW, , Goetz MP, , Rubin J, , Wong GY, & Sloan JA, : Painful metastases involving bone: feasibility of percutaneous CT- and US-guided radio-frequency ablation. Radiology 224:8797, 2002

    • Search Google Scholar
    • Export Citation
  • 5

    Carlson SK, , Bender CE, , Classic KL, , Zink FE, , Quam JP, & Ward EM, : Benefits and safety of CT fluoroscopy in interventional radiologic procedures. Radiology 219:515520, 2001

    • Search Google Scholar
    • Export Citation
  • 6

    Caudana R, , Renzi Brivio L, , Ventura L, , Aitini E, , Rozzanigo U, & Barai G: CT-guided percutaneous vertebroplasty: personal experience in the treatment of osteoporotic fractures and dorsolumbar metastases. Radiol Med (Torino) 113:114133, 2008

    • Search Google Scholar
    • Export Citation
  • 7

    Chi JH, , Bydon A, , Hsieh P, , Witham T, , Wolinsky JP, & Gokaslan ZL: Epidemiology and demographics for primary vertebral tumors. Neurosurg Clin N Am 19:14, 2008

    • Search Google Scholar
    • Export Citation
  • 8

    Chi JH, , Sciubba DM, , Rhines LD, & Gokaslan ZL: Surgery for primary vertebral tumors: en bloc versus intralesional resection. Neurosurg Clin N Am 19:111117, 2008

    • Search Google Scholar
    • Export Citation
  • 9

    Chiras J, , Depriester C, , Weill A, , Sola-Martinez MT, & Deramond H: [Percutaneous vertebral surgery. Technics and indications.]. J Neuroradiol 24:4559, 1997. (Fr)

    • Search Google Scholar
    • Export Citation
  • 10

    Cook AM, , Lau TN, , Tomlinson MJ, , Vaidya M, , Wakeley CJ, & Goddard P: Magnetic resonance imaging of the whole spine in suspected malignant spinal cord compression: impact on management. Clin Oncol (R Coll Radiol) 10:3943, 1998

    • Search Google Scholar
    • Export Citation
  • 11

    Cooper PR, , Errico TJ, , Martin R, , Crawford B, & DiBartolo T: A systematic approach to spinal reconstruction after anterior decompression for neoplastic disease of the thoracic and lumbar spine. Neurosurgery 32:18, 1993

    • Search Google Scholar
    • Export Citation
  • 12

    Cotten A, , Dewatre F, , Cortet B, , Assaker R, , Leblond D, & Duquesnoy B, : Percutaneous vertebroplasty for osteolytic metastases and myeloma: effects of the percentage of lesion filling and the leakage of methyl methacrylate at clinical follow-up. Radiology 200:525530, 1996

    • Search Google Scholar
    • Export Citation
  • 13

    Deardorff DL, & Diederich CJ: Angular directivity of thermal coagulation using air-cooled direct-coupled interstitial ultrasound applicators. Ultrasound Med Biol 25:609622, 1999

    • Search Google Scholar
    • Export Citation
  • 14

    Deardorff DL, & Diederich CJ: Axial control of thermal coagulation using a multi-element interstitial ultrasound applicator with internal cooling. IEEE Trans Ultrason Ferroelectr Freq Control 47:170178, 2000

    • Search Google Scholar
    • Export Citation
  • 15

    Delabrousse E, , Mithieux F, , Birer A, , Salomir R, , Chapelon J, & Lafon C: [Ultrasound interstitial mini invasive probes for thermal ablation in liver: feasibility study in vivo.]. J Radiol 88:18171822, 2007. (Fr)

    • Search Google Scholar
    • Export Citation
  • 16

    Diederich CJ, , Nau WH, , Burdette EC, , Bustany IS, , Deardorff DL, & Stauffer PR: Combination of transurethral and interstitial ultrasound applicators for high-temperature prostate thermal therapy. Int J Hyperthermia 16:385403, 2000

    • Search Google Scholar
    • Export Citation
  • 17

    Diederich CJ, , Stafford RJ, , Nau WH, , Burdette EC, , Price RE, & Hazle JD: Transurethral ultrasound applicators with directional heating patterns for prostate thermal therapy: in vivo evaluation using magnetic resonance thermometry. Med Phys 31:405413, 2004

    • Search Google Scholar
    • Export Citation
  • 18

    Dupuy DE, , Hong R, , Oliver B, & Goldberg SN: Radiofrequency ablation of spinal tumors: temperature distribution in the spinal canal. AJR Am J Roentgenol 175:12631266, 2000

    • Search Google Scholar
    • Export Citation
  • 19

    Finelli A, , Rewcastle JC, & Jewett MA: Cryotherapy and radiofrequency ablation: pathophysiologic basis and laboratory studies. Curr Opin Urol 13:187191, 2003

    • Search Google Scholar
    • Export Citation
  • 20

    Fourney DR, , Schomer DF, , Nader R, , Chlan-Fourney J, , Suki D, & Ahrar K, : Percutaneous vertebroplasty and kyphoplasty for painful vertebral body fractures in cancer patients. J Neurosurg 98:1 Suppl 2130, 2003

    • Search Google Scholar
    • Export Citation
  • 21

    Fowl RJ, , Patterson RB, , Gewirtz RJ, & Anderson DK: Protection against postischemic spinal cord injury using a new 21-aminosteroid. J Surg Res 48:597600, 1990

    • Search Google Scholar
    • Export Citation
  • 22

    Froelich JJ, & Wagner HJ: CT-fluoroscopy: Tool or gimmick?. Cardiovasc Intervent Radiol 24:297305, 2001

  • 23

    Fry WJ, & Fry FJ: Fundamental neurological research and human neurosurgery using intense ultrasound. IRE Trans Med Electron ME-7 166181, 1960

    • Search Google Scholar
    • Export Citation
  • 24

    Garrean S, , Hering J, , Saied A, , Helton WS, & Espat NJ: Radiofrequency ablation of primary and metastatic liver tumors: a critical review of the literature. Am J Surg 195:508520, 2008

    • Search Google Scholar
    • Export Citation
  • 25

    Gianfelice D, , Lepanto L, , Perreault P, , Chartrand-Lefebvre C, & Milette PC: Value of CT fluoroscopy for percutaneous biopsy procedures. J Vasc Interv Radiol 11:879884, 2000

    • Search Google Scholar
    • Export Citation
  • 26

    Goetz MP, , Callstrom MR, , Charboneau JW, , Farrell MA, , Maus TP, & Welch TJ, : Percutaneous image-guided radiofrequency ablation of painful metastases involving bone: a multicenter study. J Clin Oncol 22:300306, 2004

    • Search Google Scholar
    • Export Citation
  • 27

    Gokaslan ZL, , York JE, , Walsh GL, , McCutcheon IE, , Lang FF, & Putnam JB Jr, : Transthoracic vertebrectomy for metastatic spinal tumors. J Neurosurg 89:599609, 1998

    • Search Google Scholar
    • Export Citation
  • 28

    Hsu TH, , Fidler ME, & Gill IS: Radiofrequency ablation of the kidney: acute and chronic histology in porcine model. Urology 56:872875, 2000

    • Search Google Scholar
    • Export Citation
  • 29

    Itoh T, , Orba Y, , Takei H, , Ishida Y, , Saitoh M, & Nakamura H, : Immunohistochemical detection of hepatocellular carcinoma in the setting of ongoing necrosis after radiofrequency ablation. Mod Pathol 15:110115, 2002

    • Search Google Scholar
    • Export Citation
  • 30

    Katada K, , Anno H, , Takeshita G, , Ogura Y, , Koga S, & Ida Y, : [Development of real-time CT fluoroscopy.]. Nippon Igaku Hoshasen Gakkai Zasshi 54:11721174, 1994. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 31

    Katada K, , Kato R, , Anno H, , Ogura Y, , Koga S, & Ida Y, : Guidance with real-time CT fluoroscopy: early clinical experience. Radiology 200:851856, 1996

    • Search Google Scholar
    • Export Citation
  • 32

    Kirchner J, , Kickuth R, , Laufer U, , Schilling EM, , Adams S, & Liermann D: CT fluoroscopy-assisted puncture of thoracic and abdominal masses: a randomized trial. Clin Radiol 57:188192, 2002

    • Search Google Scholar
    • Export Citation
  • 33

    Klimo P Jr, & Schmidt MH: Surgical management of spinal metastases. Oncologist 9:188196, 2004

  • 34

    Kyle RA, & Rajkumar SV: Epidemiology of the plasma-cell disorders. Best Pract Res Clin Haematol 20:637664, 2007

  • 35

    Lafon C, , Chapelon JY, , Prat F, , Gorry F, , Margonari J, & Theillère Y, : Design and preliminary results of an ultrasound applicator for interstitial thermal coagulation. Ultrasound Med Biol 24:113122, 1998

    • Search Google Scholar
    • Export Citation
  • 36

    Lafon C, , Chapelon JY, , Prat F, , Gorry F, , Theillère Y, & Cathignol D: Design and in vitro results of a high intensity ultrasound interstitial applicator. Ultrasonics 36:683687, 1998

    • Search Google Scholar
    • Export Citation
  • 37

    Lafon C, , Chavrier F, , Prat F, , Chapelon JY, & Cathignol D: Theoretical comparison of two interstitial ultrasound applicators designed to induce cylindrical zones of tissue ablation. Med Biol Eng Comput 37:298303, 1999

    • Search Google Scholar
    • Export Citation
  • 38

    Lafon C, , Melo de Lima D, , Theillère Y, , Prat F, , Chapelon JY, & Cathignol D: Optimizing the shape of ultrasound transducers for interstitial thermal ablation. Med Phys 29:290297, 2002

    • Search Google Scholar
    • Export Citation
  • 39

    Lafon C, , Melodelima D, , Salomir R, & Chapelon JY: Interstitial devices for minimally invasive thermal ablation by high-intensity ultrasound. Int J Hyperthermia 23:153163, 2007

    • Search Google Scholar
    • Export Citation
  • 40

    Lafon C, , Salomir R, , Bouchoux G, , Birer A, , Owen N, & Delabrousse E, : Ultrasound interstitial applicators for thermal ablation in liver. J Acoust Soc Am 123:2996, 2008

    • Search Google Scholar
    • Export Citation
  • 41

    Lafon C, , Theillére Y, , Prat F, , Arefiev A, , Chapelon JY, & Cathignol D: Development of an interstitial ultrasound applicator for endoscopic procedures: animal experimentation. Ultrasound Med Biol 26:669675, 2000

    • Search Google Scholar
    • Export Citation
  • 42

    Levine SA, , Perin LA, , Hayes D, & Hayes WS: An evidence-based evaluation of percutaneous vertebroplasty. Manag Care 9:5660, 63, 2000

  • 43

    Lindner NJ, , Ozaki T, , Roedl R, , Gosheger G, , Winkelmann W, & Wörtler K: Percutaneous radiofrequency ablation in osteoid osteoma. J Bone Joint Surg Br 83:391396, 2001

    • Search Google Scholar
    • Export Citation
  • 44

    Martin JB, , Jean B, , Sugiu K, , San Millán Ruíz D, , Piotin M, & Murphy K, : Vertebroplasty: clinical experience and follow-up results. Bone 25:2 Suppl 11S15S, 1999

    • Search Google Scholar
    • Export Citation
  • 45

    Maruyama M, , Asano T, , Kenmochi T, , Kainuma O, , Iwasaki K, & Miyauchi H, : Radiofrequency ablation therapy for bone metastasis from hepatocellular carcinoma: case report. Anticancer Res 23:3C 29872989, 2003

    • Search Google Scholar
    • Export Citation
  • 46

    Melcher I, , Disch AC, , Khodadadyan-Klostermann C, , Tohtz S, , Smolny M, & Stöckle U, : Primary malignant bone tumors and solitary metastases of the thoracolumbar spine: results by management with total en bloc spondylectomy. Eur Spine J 16:11931202, 2007

    • Search Google Scholar
    • Export Citation
  • 47

    Murphy KJ, & Deramond H: Percutaneous vertebroplasty in benign and malignant disease. Neuroimaging Clin N Am 10:535545, 2000

  • 48

    Nau WH, , Diederich CJ, & Burdette EC: Evaluation of multielement catheter-cooled interstitial ultrasound applicators for high-temperature thermal therapy. Med Phys 28:15251534, 2001

    • Search Google Scholar
    • Export Citation
  • 49

    Nau WH, , Diederich CJ, & Shu R: Feasibility of using interstitial ultrasound for intradiscal thermal therapy: a study in human cadaver lumbar discs. Phys Med Biol 50:28072821, 2005

    • Search Google Scholar
    • Export Citation
  • 50

    Neeman Z, & Wood BJ: Radiofrequency ablation beyond the liver. Tech Vasc Interv Radiol 5:156163, 2002

  • 51

    Olsen MA, , Mayfield J, , Lauryssen C, , Polish LB, , Jones M, & Vest J, : Risk factors for surgical site infection in spinal surgery. J Neurosurg 98:2 Suppl 149155, 2003

    • Search Google Scholar
    • Export Citation
  • 52

    Rosenthal DI, , Hornicek FJ, , Torriani M, , Gebhardt MC, & Mankin HJ: Osteoid osteoma: percutaneous treatment with radiofrequency energy. Radiology 229:171175, 2003

    • Search Google Scholar
    • Export Citation
  • 53

    Rouvière O, , Souchon R, , Salomir R, , Gelet A, , Chapelon JY, & Lyonnet D: Transrectal high-intensity focused ultrasound ablation of prostate cancer: effective treatment requiring accurate imaging. Eur J Radiol 63:317327, 2007

    • Search Google Scholar
    • Export Citation
  • 54

    Sciubba DM, , Wolinsky JP, , Than KD, , Gokaslan ZL, , Witham TF, & Murphy KP: CT fluoroscopically guided percutaneous placement of transiliosacral rod for sacral insufficiency fracture: case report and technique. AJNR Am J Neuroradiol 28:14511454, 2007

    • Search Google Scholar
    • Export Citation
  • 55

    Seket B, , Lafon C, , Mithieux F, , Goldenstedt C, , Paquet C, & Chapelon JY, : Developing an interstitial ultrasound applicator for thermal ablation in liver: results of animal experiments. J Surg Res 142:8189, 2007

    • Search Google Scholar
    • Export Citation
  • 56

    Silverman SG, , Tuncali K, , Adams DF, , Nawfel RD, , Zou KH, & Judy PF: CT fluoroscopy-guided abdominal interventions: techniques, results, and radiation exposure. Radiology 212:673681, 1999

    • Search Google Scholar
    • Export Citation
  • 57

    Solbiati L: New applications of ultrasonography: interventional ultrasound. Eur J Radiol 27:Suppl 2 S200S206, 1998

  • 58

    Stone MJ, , Venkatesan AM, , Locklin J, , Pinto P, , Linehan M, & Wood BJ: Radiofrequency ablation of renal tumors. Tech Vasc Interv Radiol 10:132139, 2007

    • Search Google Scholar
    • Export Citation
  • 59

    Sundaresan N, , Rothman A, , Manhart K, & Kelliher K: Surgery for solitary metastases of the spine: rationale and results of treatment. Spine 27:18021806, 2002

    • Search Google Scholar
    • Export Citation
  • 60

    Tomita K, , Kawahara N, , Murakami H, & Demura S: Total en bloc spondylectomy for spinal tumors: improvement of the technique and its associated basic background. J Orthop Sci 11:312, 2006

    • Search Google Scholar
    • Export Citation
  • 61

    Underwood HR, , Burdette EC, , Ocheltree KB, & Magin RL: A multi-element ultrasonic hyperthermia applicator with independent element control. Int J Hyperthermia 3:257267, 1987

    • Search Google Scholar
    • Export Citation
  • 62

    Venbrux AC, , Montague BJ, , Murphy KP, , Bobonis LA, , Washington SB, & Soltes AP, : Image-guided percutaneous radiofrequency ablation for osteoid osteomas. J Vasc Interv Radiol 14:375380, 2003

    • Search Google Scholar
    • Export Citation
  • 63

    Weber K, , Damron TA, , Frassica FJ, & Sim FH: Malignant bone tumors. Instr Course Lect 57:673688, 2008

  • 64

    Weill A, , Chiras J, , Simon JM, , Rose M, , Sola-Martinez T, & Enkaoua E: Spinal metastases: indications for and results of percutaneous injection of acrylic surgical cement. Radiology 199:241247, 1996

    • Search Google Scholar
    • Export Citation
  • 65

    Woertler K, , Vestring T, , Boettner F, , Winkelmann W, , Heindel W, & Lindner N: Osteoid osteoma: CT-guided percutaneous radiofrequency ablation and follow-up in 47 patients. J Vasc Interv Radiol 12:717722, 2001

    • Search Google Scholar
    • Export Citation
  • 66

    Wong DA, , Fornasier VL, & MacNab I: Spinal metastases: the obvious, the occult, and the impostors. Spine 15:14, 1990

  • 67

    Zhu JC, , Yan TD, & Morris DL: A systematic review of radiofrequency ablation for lung tumors. Ann Surg Oncol 15:17651774, 2008

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