ORIGINAL ARTICLE
Radiofrequency Ablation Near the Bone-Muscle Interface Alters Soft Tissue Lesion Dimensions Maxim S. Eckmann, MD,* Marte A. Martinez, MD,† Steven Lindauer, MD,* Asif Khan, BA,* and Somayaji Ramamurthy, MD* Background and Objectives: Radiofrequency (RF) lesions are safe and effective in the treatment of spine pain; however, models developed to study factors affecting lesion dimensions have been performed in homogeneous media that may not accurately simulate human anatomy and electrophysiology. We present a novel ex vivo porcine model for performing RF lesion studies and report the influence of bone on projection of RF ablation lesions into soft tissue. Methods: Radiofrequency lesions were performed in porcine rib specimens using monopolar 18-gauge, 10-mm straight active tip cannula, with a lesion temperature of 80°C for 150 seconds. Ten lesions were performed in pure porcine muscle tissue and abutting porcine rib bone with surrounding muscle. Lesions were exposed with dissection and measured with digital calipers. Results: Maximal effective lesion radius approximately doubled against the bone compared with the pure muscle group (mean, 5.65 mm [95% CI, 5.43–5.87 mm] vs 2.68 mm [95% CI, 2.55–2.81 mm], P < .0001), although this was seen only in a vertical direction and not horizontally. In addition, the prelesion and postlesion impedance of the bone-muscle interface was consistently higher than the muscle-only interface (mean, 165.6 Ohm [95% CI, 146.6–184.6 Ohm] vs 137.8 Ohm [95% CI, 135.5– 140.1 Ohm], P = 0.004; 144.3 Ohm [95% CI, 134.3–154.3 Ohm] vs 124.3 Ohm [95% CI, 119.3–129.3 Ohm], P = 0.001). Other dimensions and estimated volume were not significantly different. Conclusions: Bone adjacent to RF lesions alters the surrounding electrophysiological environment causing RF lesions to project further perpendicularly from the needle axis, vertically to bone, than previously expected. This phenomenon should be considered in the future modeling and clinical practice of RF. (Reg Anesth Pain Med 2015;40: 270–275)
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adiofrequency (RF) ablation of medial and lateral branch nerves is an established treatment for spine pain emanating from zygapophysial and sacroiliac joints.1–3 The coagulated tissue of RF lesions is not directly visualized in the clinical setting; however, the extents of the RF lesion are more likely to produce a therapeutic effect if the lesion is placed properly along the usual
From the *Department of Anesthesiology, The University of Texas Health Science Center at San Antonio (UTHSCSA), San Antonio; and †Advanced Spine Pain Solutions, Laredo, TX. Accepted for publication January 2, 2015. Address correspondence to: Maxim S. Eckmann, MD, Department of Anesthesiology, The University of Texas Health Science Center at San Antonio, Mail Code 7838, 7703 Floyd Curl Dr, San Antonio, TX 78229 (e‐mail: [email protected]). Institutional review board status: institutional exemption. This work was supported with funding from the Department of Anesthesiology, The University of Texas Health Science Center at San Antonio, Texas. Pilot data were presented at the American Society of Anesthesiologists 2013 Annual Meeting held October 12 to 16, in San Francisco, California. The authors declare no conflict of interest. Copyright © 2015 by American Society of Regional Anesthesia and Pain Medicine ISSN: 1098-7339 DOI: 10.1097/AAP.0000000000000221
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course of the nerve.4 The strategies for RF lesion placement are based on knowledge of the neurologic and bony anatomy of the spine,5,6 as well as studies of the factors that shape RF lesions.7–9 The predominance of studies on RF lesion dimensions has been conducted in a homogeneous media, such as egg-white liquid, chicken breast muscle, or hepatic tissue.4,10–15 Unfortunately, these models have yielded unpredictable and varying results. For example, the egg-white model can produce underestimation and inconsistency of lesion sizes due to the electrical, thermal, and physical properties of egg white.9 With varying albumin protein density and absent cellular matrix, an egg-white model for RF lesions remains unreliable.9 Despite this, investigators have worked to find factors that can affect (increase) lesion dimensions, such as bipolar versus monopolar probe orientations, lesion duration and current intensity, concurrent tip cooling, and fluid injection.10–15 While these models were instrumental in elucidating factors that affect RF lesions generally, most did not closely simulate anatomical conditions about the spine in clinical interventional pain practice. Exceptions include the ex vivo cooled RF experiments for the development of lumbar disk biacuplasty.16 Considering that RF lesions for spine pain occur adjacently or in close proximity1–4 to bony surfaces, current models have not elucidated differences in shape or dimension of tissue denaturation when RF is applied adjacently to periosteum with surrounding soft tissue. Electrical conductivity differences17,18 between the surrounding soft tissue and bone possibly alter the local electrical current density and resulting RF lesion shape. Finite-element models and in vitro experiments have demonstrated atypical extension of denaturation along tissue strands much more distant than would be expected; this is possibly due to an electrical insulating effect from surrounding fat.19 In addition, thermal conductivity differences20,21 at tissue-type interfaces may also alter the dissolution of heat, which may in turn affect lesion dimensions.19,21 We demonstrate an ex vivo model to evaluate RF lesion dimensions produced by interventional pain management equipment in relation to a bone–soft tissue interface. We refer to this interface as “bone-muscle,” reflecting the predominance of that type of soft tissue in our medium, although it contains fat and connective tissue as well.
METHODS This protocol received institutional review board exemption from our host institution.
RF Ablation System A commercially available RF generator (Pain Management Generator: REF PMG-115-TD; Baylis Medical Company, Montreal, Quebec, Canada) was set to deliver continuous (monopolar) RF at 80°C. Straight 18-gauge, 10-mm active tip RF cannulas (with matching probes) (PMF18-100-10, lot PFFA170113; Baylis Medical Company) were utilized to perform RF lesions. The generator was operated at 460 kHz, delivering variable a power output up to 50 W. A dual dispersive electrode (REF 410–200; Conmed,
Regional Anesthesia and Pain Medicine • Volume 40, Number 3, May-June 2015
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RF Lesion Changes Near Bone
Utica, New York) was secured at the base of a temperatureequilibrated 0.9% saline bath (1250 mL) to complete the electrical circuit. A saline bath, allowed to equilibrate to room temperature, was used to ensure electrical conductivity between the return electrode and entirety of the exterior of the tissue sample; tissue samples were only exposed to the bath for the duration of the lesion and were not stored in the bath to reduce any osmotic tissue changes.
Experimental Protocol Ex vivo porcine ribs obtained from local commercial supply, freshly butchered and without chemical processing, were allowed to equilibrate to ambient room temperature (21°C) for a minimum of 2 hours, outside the saline bath. The tissue temperature was verified via the thermocouple in the RF probe, as was impedance. Muscle tissue in both groups was trimmed to 50 30 30 mm. The bone-muscle samples retained the lower rib (trimmed to the same length) and superiorly adjoining muscles, whereas the next (upper) rib was removed from the intercostal segment. For the pure muscle group, an RF cannula was placed into the center of the bulk of the tissue sample, the stylette removed, and the RF probe inserted into the cannula. The sample was lowered into the saline bath overlying the dispersive electrode. A temperaturecontrolled RF ablation was performed at 80°C for a cycle time of 150 seconds, chosen to be analogous to total coagulation times reported in studies of monopolar RF in spinal structures25 and to ensure truly maximal monopolar lesion size.4 It should also be noted that this selected cycle time includes ramp-up, which is common in RF generators. The sample was removed, and a dissection was performed to expose the extents of the denatured tissue about the active cannula tip. For RF lesions performed against porcine rib bone, a similar process was performed, except that the entire active tip was placed flush (and bevel up) to the bony surface, parallel to the long axis of the bone, and embedded within the longitudinal center of overlying muscle tissue (Fig. 1). Samples and cannulas were stabilized. Then, 10 individual lesions each were performed in 10 individual pure muscle tissue specimens and bone-muscle interface specimens, respectively.
FIGURE 2. Representation of lesion measurements. Legend: d = vertical lesion depth (or height); w = horizontal width (Dh); l = length (Dv); Merv = maximum effective vertical radius from the outer wall of the needle. The bone surface was used as the perpendicular reference to the lesion depth. Where lesions were performed in pure muscle, the depth axis was considered to be perpendicular to the open face of the needle bevel, so that both groups would be subject to the same dissection and measurement process.
FIGURE 1. Placement of RF needle against bone. Bone is left unshortened for purposes of demonstrating plane of approach.
surface), and a horizontal width or Dh (Fig. 2) using white to tan lesion area corresponding to the zone of coagulation. Maximal effective radius (Mer) was measured as well, denoting the farthest extent of coagulated tissue radially from the needle. Of note, in other RF studies,15 the lesion shape has been denoted by “vertical diameter (Dv),” and we have elected to use “length” to avoid confusion with the vertical axis reference to the bone surface in 3 dimensions. To remain internally consistent in our nomenclature, we have used width similarly to mean “horizontal diameter (Dh).” Distal extension radius from the active tip (T ) and proximal extension from the active tip base (Tp) were measured. A second investigator confirmed digital caliper placement at the color transitions by the investigator performing the dissection. The vertical axis was defined as perpendicular to the bone surface for the bone-muscle group. Two dissections with surgical blades were performed after the lesion was complete (Fig. 3). The first dissection was clean cut vertically, perpendicular to bone, and down to the needle itself to split the lesion along the long axis of the needle. One-half was then folded laterally, with care not to exert any tension on the other half, which was then exposed for measurement of vertical lesion extents. The Merv was considered to originate from the outer wall of the needle. Lesion length along the needle axis was also measured. Then, a horizontal dissection (parallel to the plane of bone) was performed just over the top wall of the needle on each split half, again along the long axis of the needle, to expose a thin portion of denatured soft tissue still overlying the bone representing the thickness of the needle. The tissue, still intact, could then be reflected upward and away to allow for horizontal measures, such as width, with the needle still in place. Maximal effective radius would be the largest effective radius observed among any visualized plane available. For lesions performed in pure muscle, the vertical axis was defined as oriented perpendicular to the open surface of the needle bevel. The exact same process was used to dissect and identify lesion dimensions, even though a bone surface was not present. Significant practice was required on the part of the investigators to perfect the dissections in pilot lesions, and 2 investigators were solely responsible for performing them. Measurements were made using a digital caliper (Neiko 01407A) accurate to the nearest 0.01 mm using color transition of the coagulation zone as the end point. Although it is established that RF lesions formed by linear probes are actually somewhat pear-shaped,22 most published studies have approximated the shape closest to that of a spheroid or ellipsoid11,12,14 for the purposes of volume calculation. The volume
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Determination of Lesion Size Lesions were measured in 3 dimensions along a length or Dv, maximal effective vertical radius (Merv, with reference to bone
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was from our pilot experiments, which revealed an overall shape consistent with an ellipsoid about the active tip but bisected by the equatorial plane of bone. Because d = 2r, and a factor of 2 is added to the denominator for a half-ellipsoid, the equation for the bone-muscle interface lesion condenses to the following: πðr l wÞ 6
Statistical Analysis Based on prior pilot data in regard to lesion dimension means and SDs for both groups, power analysis estimated that 10 experiments per group were necessary to have 95% power to detect a difference at an α level of 0.01. The data were presented as mean (95% confidence interval [CI]) and analyzed with single-factor analysis of variance performed in IBM SPSS version 22 (Armonk, New York). We considered α < 0.01 to be statistically significant.
RESULTS
FIGURE 3. Dissection and visualization of lesions. Both muscle and bone-muscle groups underwent the same process. With open face of bevel denoting vertical axis (and perpendicular to plane of bone), cut made to bisect lesion and expose vertical extents above the needle. After measurement, a horizontal plane is made to reveal a small thickness of coagulated tissue about 1.4 mm deep to bone representing a tissue plane the thickness of the needle, or the remaining tissue in pure muscle samples. With now 2 planes of dissection, the tissue is reflected upward and out of the way to allow horizontal plane measurements. Maximal effective radius is found among the several planes as the largest effective radius from the needle wall.
of the ablation zone in muscle was approximated to an ellipsoid using the following equation:
Radiofrequency-induced lesions created a well-defined zone of coagulation necrosis compared with areas of nontreated tissue. Results are summarized in Table 1. Baseline sample temperature was equivalent in both groups. The bone-muscle interface groups did reliably show higher prelesion and postlesion impedance than the muscle-only groups (mean [95% CI], 165.6 Ohm [146.6–184.6 Ohm] vs 137.8 Ohm [135.5–140.1 Ohm], P = 0.004; 144.3 Ohm [134.3–154.3 Ohm] vs 124.3 Ohm [119.3– 129.3 Ohm], P = 0.001). We found with high statistical significance that the lesion Mer projecting outward from the bony surface was consistently much larger, almost double, than the Mer in pure muscle (mean [95% CI], 5.65 mm [5.43–5.87 mm] vs 2.68 mm [2.55– 2.81 mm], P < .0001). In addition, Merv projection perpendicular to the bone surface was always found to be the Mer of the bonemuscle lesions in any direction. Other lesion dimensions, including total vertical depth, width (Dh), length (Dv), distal and proximal tip radii (T, Tp), Dh/Dv, and estimated volume, were not different.
πðd l wÞ 6
DISCUSSION
The volume of the ablation zone adjacent to bone was approximated using an ellipsoid cut in half. The basis for this estimation
To our knowledge, this is the first ex vivo study quantifying lesion shape in 3 dimensions when RF is performed at the bone-muscle interface using monopolar RF interventional pain
TABLE 1. Summary of 18-gauge, 10-mm Straight Active Tip Lesion Dimensions Represented as Means (95% CI) Measure Mer or *Merv, mm Total depth, mm Width (Dh), mm Length (Dv), mm Distal radius from tip (T), mm Proximal Radius From Tip(Tp), mm Dh/Dv Volume, μL Prelesion impedance, Ohm Postlesion impedance, Ohm Prelesion temperature, °C
Muscle (n = 10)
Bone-Muscle (n = 10)*
P
2.68 (2.55–2.81) 6.99 (6.66–7.31) 7.25 (7.09–7.42) 12.71 (12.3–13.1) 1.37 (1.17–1.56) 0.83 (0.72–0.95) 0.57 (0.55–0.59) 337.4 (314–361) 137.8 (135.5–140.1) 124.3 (119.3–129.3) 20.7 (20.1–21.3)
5.65 (5.43–5.87) 7.01 (6.79–7.23) 6.96 (6.34–7.59) 12.09 (11.5–12.7) 1.42 (1.15–1.70) 0.96 (0.72–1.20) 0.58 (0.52–0.64) 309.9 (272–348) 165.6 (146.6–184.6) 144.3 (134.3–154.3) 20.7 (20.1–21.3)
Mer1. The radius from bone was nearly double that in pure muscle, on average.
equipment. The Mer is essentially doubled in the bone-muscle interface group; however, the projection is directly outward from the bone and perpendicular to the needle axis in the vertical plane, creating a “taller” lesion (Fig. 4). The width and length and Dh/Dv ratio appear conserved in reference to the parallel plane to bone compared with pure muscle. Volume is similar, although caution should be used in interpreting volume, as the value is calculated based on estimation of an ellipsoid shape and not a direct measure. Importantly, distal extension of the lesion axially from the needle tip does not appear to be influenced by the presence of bone. Notably, the finding of vertical lesion extension is novel, considering the preponderance of interventional pain RF studies performed in chicken breast tissue or egg-white media yielded relatively circumferentially uniform lesions. We developed this porcine rib model as we felt it would be practical for examining and dissecting lesions near a relatively flat, consistent, and smooth bone surface, with ample overlying muscle tissue, which is easy to visualize and target. We hypothesize that the cortical bone, which has a significantly higher electrical impedance than muscle and other deep soft tissues,17,18 serves as an insulator that directs the current return path further outward into the surrounding soft tissue. Indeed, our data indicate that starting and ending impedances are increased near the bone, although we did not track impedance throughout the lesion cycle or the resulting power output. There may be a thermal insulating effect as well, preventing heat loss, as bone has a lower thermal conductivity than muscle.20 The resulting RF lesion projection is directly in the vertical plane perpendicularly away from the bone surface and axis of the needle, but not distally from the needle tip or horizontally along the plane of the bone surface. There are some weaknesses of our model. The bone surface regularity and surrounding tissue composition (eg, muscle, tendon, ligament, fat, vessels) in our model probably differ somewhat © 2015 American Society of Regional Anesthesia and Pain Medicine
RF Lesion Changes Near Bone
from those in the spine. Porcine rib bone and muscle may have a different density than human vertebral bone and spine tissues as well, although the model is at least mammalian. The relative compositions of muscle, fat, and connective tissue may systematically differ near the bone than in other parts of the muscle in our own samples (although all were obtained from intercostal segments) and might account for some of the lesion size difference due to soft tissue changes alone. Therefore, caution must be used in inferring direct effects of the bone surface. However, this model is arguably closer to physiologic conditions—where these factors are present in clinical practice—than any purely uniform medium. The tissue dissection must be carefully performed to avoid disruption and loss of information. Performing the same measures with an irregular bone surface, such as is present around the dorsal elements of the lumbar spine, will prove more challenging, although investigation in homogeneous isolated spine tissue has been possible.26 We cannot account for any cooling effects of circulating blood in perfused living tissue21; however, other models have not demonstrated this either. Using previous estimates for lesion extents made by commonly available interventional pain management RF probes may underestimate the projection of RF lesions performed on the spine away from the surface of the periosteum. However, absence of any additional projection from the needle tip with the presence of bone is reassuring with respect to concern for avoidance of spinal nerve damage (from overly anterior lesions approaching the foramen) when the RF cannula is oriented in the proper position along the course of the medial branch nerve,6 particularly considering that our finding of 1.4-mm distal tip lesion projection is identical to previous work by Bogduk et al4 in meat samples with 18-gauge cannulas. We also find that horizontal lesion width along the bone surface and total volume are not significantly altered. Therefore, we cannot conclude any expected change to the maximal tolerable margin of error28 of needle proximity in parallel to the path of the nerve to ensure full denaturation, and clinicians should continue to place the needle as closely as previously recommended so that a radius of about 2 mm can encompass the diameter of the medial branch nerve fully.5,6,27 Overall, using pure muscle tissue for modeling RF lesions as has been done previously appears to be both practical and comparatively accurate with the exception of vertical lesion extension from the bone surface. Further elaboration of our model using a curved, especially concave, bone surface as encountered on the spine may be warranted to evaluate possible effects of bone surface geometry. Although RF has proven to be a safe and effective method of producing controlled lesions in clinical practice,23 the unanticipated extension of RF lesions near bone could incorporate tissues that were unintended for denaturation, including skin in regions where tissue overlying the spine is thin, or possibly vascular structures where they are closely associated with the cervical spine. A third-degree burn has been reported in the application of cooled RF for thoracic medial branch neurotomy,28 although it is not possible to conclude that vertical extension due to bone was the cause because multiple technical factors such as current leakage, inadvertent cannula migration, or cooled RF increased lesion size relative to thin anatomic conditions might also result in superficial burns. Transient blindness has been reported during a cervical RF procedure,29 although the phenomenon was attributed to local anesthetic injection of the deep ascending cervical artery in proximity to the articular pillar; adverse clinical consequences of coagulating this artery are otherwise unknown. Further cadaveric spine and mammalian spine studies, although likely challenging, should
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be considered to investigate these potential safety issues. Incorporating imaging technology (such as infrared) may be useful to augment measures obtained by dissection and direct visualization. Although cooled RF technologies are now available for significant lesion enhancement in the lumbosacral and thoracic spine, there should be careful consideration and testing before such strategies are applied to the cervical spine considering the proximity of critical neurologic and vascular structures and the additional possible but untested effect of bone projection in the setting of cooled RF. In tumor ablation RF techniques, excessive necrosis has been reported from overexpansion of saline-enhanced RF lesions; however, saline in these applications is usually continuously infused throughout the procedure.24 Fluid injection against bone may be a logical next area of investigation as it has been shown to enhance lesion size in soft tissue.15 Currently, the majority of research aimed at determining the effect of variables on RF lesion dimensions is seen in the cardiology or interventional radiology literature and performed in homogenous media relevant, for example, to the destruction of solid organ tumors. These principles are being successfully applied to interventional pain medicine, yet current studies do not factor in the effects of nearby bone, which we believe to be relevant to clinical use of RF about the spine in some select conditions. The bone-muscle interface should be evaluated in many applications including pulsed and continuous RF, bipolar and monopolar RF, lesion properties with fluid injection, and effects of active cooling. Similarly, there is a lack of literature on RF near metallic spine hardware despite this very relevant challenge in patients with chronic facetogenic spine pain and prior fusion. More research is warranted to confirm the mechanism of lesion extension into soft tissue when RF is applied near a bony surface and to determine any potential impact on clinical practice. In addition, we should work to refine models that can test this phenomenon.
5. Bogduk N. The clinical anatomy of the cervical dorsal rami. Spine (Phila Pa 1976). 1982;7:319–330. 6. Lau P, Mercer S, Govind J, Bogduk N. The surgical anatomy of lumbar medial branch neurotomy (facet denervation). Pain Med. 2004;5:289–298. 7. Organ LW. Electrophysiologic principles of radiofrequency lesion making. Appl Neurophysiol. 1977;39:69–76. 8. Cosman ER, Nashold BS, Ovelman-Levitt J. Theoretical aspects of radiofrequency lesions in the dorsal root entry zone. Neurosurgery. 1984;15:945–950. 9. Cosman ER Jr, Gonzalez CD. Bipolar radiofrequency lesion geometry: implications for palisade treatment of sacroiliac joint pain. Pain Pract. 2011;11:3–22. 10. Lee CH, Derby R, Choi HS, Lee SH, Kim SH, Kang YK. The efficacy of two electrodes radiofrequency technique: comparison study using a cadaveric interspinous ligament and temperature measurement using egg white. Pain Physician. 2010;13:43–49. 11. Watanabe I, Masaki R, Min N, et al. Cooled-tip ablation results in increased radiofrequency power delivery and lesion size in the canine heart: importance of catheter-tip temperature monitoring for prevention of popping and impedance rise. J Interv Card Electrophysiol. 2002;6:9–16. 12. Lee JM, Han JK, Kim SH, et al. Bipolar radiofrequency ablation using wet-cooled electrodes: an in vitro experimental study in bovine liver. AJR Am J Roentgenol. 2005;184:391–397. 13. Lubienski A, Düx M, Lubienski K, Grenacher L, Kauffmann G. Radiofrequency thermal ablation: increase in lesion diameter with continuous acetic acid infusion. Cardiovasc Intervent Radiol. 2005;28:789–794. 14. Bruners P, Müller H, Günther RW, Schmitz-Rode T, Mahnken AH. Fluid-modulated bipolar radiofrequency ablation: an ex-vivo evaluation study. Acta Radiol. 2008;49:258–266. 15. Provenzano DA, Lassila HC, Somers D. The effect of fluid injection on lesion size during radiofrequency treatment. Reg Anesth Pain Med. 2010;35:338–342.
ACKNOWLEDGMENTS The authors thank the following individuals for their contributions to this work: Dr Kun Zhang, PhD, MD, UTHSCSA, for review of style and statistical methodology; Dr Joshua Hay, MD, Spine Works Institute, North Richland Hills, Texas, for preliminary experimental protocol development; and Jimmy Tai, BS, UTHSCSA, for assistance performing the experiments.
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16. Pauza K. Cadaveric intervertebral disc temperature mapping during disc biacuplasty. Pain Physician. 2008;11:669–676. 17. Saha S, Williams PA. Electric and dielectric properties of wet human cortical bone as a function of frequency. IEEE Trans Biomed Eng. 1992;39:1298–1304. 18. Faes TJ, van der Meij HA, de Munck JC, Heethaar RM. The electric resistivity of human tissues (100 Hz–10 MHz): a meta-analysis of review studies. Physiol Meas. 1999;20:R1–R10. 19. Ekstrand V, Wiksell H, Schultz I, Sandstedt B, Rotstein S, Eriksson A. Influence of electrical and thermal properties on RF ablation of breast cancer: is the tumour preferentially heated? Biomed Eng Online. 2005;4:41. 20. El-Brawany MA, Nassiri DK, Terhaar G, Shaw A, Rivens I, Lozhken K. Measurement of thermal and ultrasonic properties of some biological tissues. J Med Eng Technol. 2009;33:249–256. 21. Tamaki K, Shimizu I, Oshio A, et al. Influence of large intrahepatic blood vessels on the gross and histological characteristics of lesions produced by radiofrequency ablation in a pig liver model. Liver Int. 2004;24:696–701. 22. Ahadian FM. Pulsed radiofrequency neurotomy: advances in pain medicine. Curr Pain Headache Rep. 2004;8:34–40. 23. Kornick C, Kramarich SS, Lamer TJ, Todd Sitzman B. Complications of lumbar facet radiofrequency denervation. Spine (Phila Pa 1976). 2004;29:1352–1354. 24. Kim TS, Lim HK, Kim H. Excessive hyperthermic necrosis of a pulmonary lobe after hypertonic saline-enhanced monopolar
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radiofrequency ablation. Cardiovasc Intervent Radiol. 2006;29:160–163. 25. Podhajsky RJ, Belous A, Johnson K, Maul DH, Finch PM. Effects of monopolar radiofrequency heating on intradiscal pressure in sheep. Spine J. 2007;7:229–234. 26. Lee CH, Derby R, Choi HS, Lee SH, Kim SH, Kang YK. The efficacy of two electrodes radiofrequency technique: comparison study using a cadaveric interspinous ligament and temperature measurement using egg white. Pain Physician. 2010; 13:43–49.
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27. Lord SM, Barnsley L, Bogduk N. Percutaneous radiofrequency neurotomy in the treatment of cervical zygapophysial joint pain: a caution. Neurosurgery. 1995;36:732–739. 28. Walega D, Roussis C. Third-degree burn from cooled radiofrequency ablation of medial branch nerves for treatment of thoracic facet syndrome. Pain Pract. 2014;14:e154–e158. 29. Swain AR, Njalamimba M, Head D. Transient vision loss during cervical medial branch nerve radiofrequency. Abstract presented at: American Society of Regional Anesthesia and Pain Medicine; November 2010; Phoenix, AZ.
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Radiofrequency Ablation Near the Bone-Muscle Interface Alters Soft Tissue Lesion Dimensions Maxim S. Eckmann, MD,* Marte A. Martinez, MD,† Steven Lindauer, MD,* Asif Khan, BA,* and Somayaji Ramamurthy, MD* Background and Objectives: Radiofrequency (RF) lesions are safe and effective in the treatment of spine pain; however, models developed to study factors affecting lesion dimensions have been performed in homogeneous media that may not accurately simulate human anatomy and electrophysiology. We present a novel ex vivo porcine model for performing RF lesion studies and report the influence of bone on projection of RF ablation lesions into soft tissue. Methods: Radiofrequency lesions were performed in porcine rib specimens using monopolar 18-gauge, 10-mm straight active tip cannula, with a lesion temperature of 80°C for 150 seconds. Ten lesions were performed in pure porcine muscle tissue and abutting porcine rib bone with surrounding muscle. Lesions were exposed with dissection and measured with digital calipers. Results: Maximal effective lesion radius approximately doubled against the bone compared with the pure muscle group (mean, 5.65 mm [95% CI, 5.43–5.87 mm] vs 2.68 mm [95% CI, 2.55–2.81 mm], P < .0001), although this was seen only in a vertical direction and not horizontally. In addition, the prelesion and postlesion impedance of the bone-muscle interface was consistently higher than the muscle-only interface (mean, 165.6 Ohm [95% CI, 146.6–184.6 Ohm] vs 137.8 Ohm [95% CI, 135.5– 140.1 Ohm], P = 0.004; 144.3 Ohm [95% CI, 134.3–154.3 Ohm] vs 124.3 Ohm [95% CI, 119.3–129.3 Ohm], P = 0.001). Other dimensions and estimated volume were not significantly different. Conclusions: Bone adjacent to RF lesions alters the surrounding electrophysiological environment causing RF lesions to project further perpendicularly from the needle axis, vertically to bone, than previously expected. This phenomenon should be considered in the future modeling and clinical practice of RF. (Reg Anesth Pain Med 2015;40: 270–275)
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adiofrequency (RF) ablation of medial and lateral branch nerves is an established treatment for spine pain emanating from zygapophysial and sacroiliac joints.1–3 The coagulated tissue of RF lesions is not directly visualized in the clinical setting; however, the extents of the RF lesion are more likely to produce a therapeutic effect if the lesion is placed properly along the usual
From the *Department of Anesthesiology, The University of Texas Health Science Center at San Antonio (UTHSCSA), San Antonio; and †Advanced Spine Pain Solutions, Laredo, TX. Accepted for publication January 2, 2015. Address correspondence to: Maxim S. Eckmann, MD, Department of Anesthesiology, The University of Texas Health Science Center at San Antonio, Mail Code 7838, 7703 Floyd Curl Dr, San Antonio, TX 78229 (e‐mail: [email protected]). Institutional review board status: institutional exemption. This work was supported with funding from the Department of Anesthesiology, The University of Texas Health Science Center at San Antonio, Texas. Pilot data were presented at the American Society of Anesthesiologists 2013 Annual Meeting held October 12 to 16, in San Francisco, California. The authors declare no conflict of interest. Copyright © 2015 by American Society of Regional Anesthesia and Pain Medicine ISSN: 1098-7339 DOI: 10.1097/AAP.0000000000000221
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course of the nerve.4 The strategies for RF lesion placement are based on knowledge of the neurologic and bony anatomy of the spine,5,6 as well as studies of the factors that shape RF lesions.7–9 The predominance of studies on RF lesion dimensions has been conducted in a homogeneous media, such as egg-white liquid, chicken breast muscle, or hepatic tissue.4,10–15 Unfortunately, these models have yielded unpredictable and varying results. For example, the egg-white model can produce underestimation and inconsistency of lesion sizes due to the electrical, thermal, and physical properties of egg white.9 With varying albumin protein density and absent cellular matrix, an egg-white model for RF lesions remains unreliable.9 Despite this, investigators have worked to find factors that can affect (increase) lesion dimensions, such as bipolar versus monopolar probe orientations, lesion duration and current intensity, concurrent tip cooling, and fluid injection.10–15 While these models were instrumental in elucidating factors that affect RF lesions generally, most did not closely simulate anatomical conditions about the spine in clinical interventional pain practice. Exceptions include the ex vivo cooled RF experiments for the development of lumbar disk biacuplasty.16 Considering that RF lesions for spine pain occur adjacently or in close proximity1–4 to bony surfaces, current models have not elucidated differences in shape or dimension of tissue denaturation when RF is applied adjacently to periosteum with surrounding soft tissue. Electrical conductivity differences17,18 between the surrounding soft tissue and bone possibly alter the local electrical current density and resulting RF lesion shape. Finite-element models and in vitro experiments have demonstrated atypical extension of denaturation along tissue strands much more distant than would be expected; this is possibly due to an electrical insulating effect from surrounding fat.19 In addition, thermal conductivity differences20,21 at tissue-type interfaces may also alter the dissolution of heat, which may in turn affect lesion dimensions.19,21 We demonstrate an ex vivo model to evaluate RF lesion dimensions produced by interventional pain management equipment in relation to a bone–soft tissue interface. We refer to this interface as “bone-muscle,” reflecting the predominance of that type of soft tissue in our medium, although it contains fat and connective tissue as well.
METHODS This protocol received institutional review board exemption from our host institution.
RF Ablation System A commercially available RF generator (Pain Management Generator: REF PMG-115-TD; Baylis Medical Company, Montreal, Quebec, Canada) was set to deliver continuous (monopolar) RF at 80°C. Straight 18-gauge, 10-mm active tip RF cannulas (with matching probes) (PMF18-100-10, lot PFFA170113; Baylis Medical Company) were utilized to perform RF lesions. The generator was operated at 460 kHz, delivering variable a power output up to 50 W. A dual dispersive electrode (REF 410–200; Conmed,
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RF Lesion Changes Near Bone
Utica, New York) was secured at the base of a temperatureequilibrated 0.9% saline bath (1250 mL) to complete the electrical circuit. A saline bath, allowed to equilibrate to room temperature, was used to ensure electrical conductivity between the return electrode and entirety of the exterior of the tissue sample; tissue samples were only exposed to the bath for the duration of the lesion and were not stored in the bath to reduce any osmotic tissue changes.
Experimental Protocol Ex vivo porcine ribs obtained from local commercial supply, freshly butchered and without chemical processing, were allowed to equilibrate to ambient room temperature (21°C) for a minimum of 2 hours, outside the saline bath. The tissue temperature was verified via the thermocouple in the RF probe, as was impedance. Muscle tissue in both groups was trimmed to 50 30 30 mm. The bone-muscle samples retained the lower rib (trimmed to the same length) and superiorly adjoining muscles, whereas the next (upper) rib was removed from the intercostal segment. For the pure muscle group, an RF cannula was placed into the center of the bulk of the tissue sample, the stylette removed, and the RF probe inserted into the cannula. The sample was lowered into the saline bath overlying the dispersive electrode. A temperaturecontrolled RF ablation was performed at 80°C for a cycle time of 150 seconds, chosen to be analogous to total coagulation times reported in studies of monopolar RF in spinal structures25 and to ensure truly maximal monopolar lesion size.4 It should also be noted that this selected cycle time includes ramp-up, which is common in RF generators. The sample was removed, and a dissection was performed to expose the extents of the denatured tissue about the active cannula tip. For RF lesions performed against porcine rib bone, a similar process was performed, except that the entire active tip was placed flush (and bevel up) to the bony surface, parallel to the long axis of the bone, and embedded within the longitudinal center of overlying muscle tissue (Fig. 1). Samples and cannulas were stabilized. Then, 10 individual lesions each were performed in 10 individual pure muscle tissue specimens and bone-muscle interface specimens, respectively.
FIGURE 2. Representation of lesion measurements. Legend: d = vertical lesion depth (or height); w = horizontal width (Dh); l = length (Dv); Merv = maximum effective vertical radius from the outer wall of the needle. The bone surface was used as the perpendicular reference to the lesion depth. Where lesions were performed in pure muscle, the depth axis was considered to be perpendicular to the open face of the needle bevel, so that both groups would be subject to the same dissection and measurement process.
FIGURE 1. Placement of RF needle against bone. Bone is left unshortened for purposes of demonstrating plane of approach.
surface), and a horizontal width or Dh (Fig. 2) using white to tan lesion area corresponding to the zone of coagulation. Maximal effective radius (Mer) was measured as well, denoting the farthest extent of coagulated tissue radially from the needle. Of note, in other RF studies,15 the lesion shape has been denoted by “vertical diameter (Dv),” and we have elected to use “length” to avoid confusion with the vertical axis reference to the bone surface in 3 dimensions. To remain internally consistent in our nomenclature, we have used width similarly to mean “horizontal diameter (Dh).” Distal extension radius from the active tip (T ) and proximal extension from the active tip base (Tp) were measured. A second investigator confirmed digital caliper placement at the color transitions by the investigator performing the dissection. The vertical axis was defined as perpendicular to the bone surface for the bone-muscle group. Two dissections with surgical blades were performed after the lesion was complete (Fig. 3). The first dissection was clean cut vertically, perpendicular to bone, and down to the needle itself to split the lesion along the long axis of the needle. One-half was then folded laterally, with care not to exert any tension on the other half, which was then exposed for measurement of vertical lesion extents. The Merv was considered to originate from the outer wall of the needle. Lesion length along the needle axis was also measured. Then, a horizontal dissection (parallel to the plane of bone) was performed just over the top wall of the needle on each split half, again along the long axis of the needle, to expose a thin portion of denatured soft tissue still overlying the bone representing the thickness of the needle. The tissue, still intact, could then be reflected upward and away to allow for horizontal measures, such as width, with the needle still in place. Maximal effective radius would be the largest effective radius observed among any visualized plane available. For lesions performed in pure muscle, the vertical axis was defined as oriented perpendicular to the open surface of the needle bevel. The exact same process was used to dissect and identify lesion dimensions, even though a bone surface was not present. Significant practice was required on the part of the investigators to perfect the dissections in pilot lesions, and 2 investigators were solely responsible for performing them. Measurements were made using a digital caliper (Neiko 01407A) accurate to the nearest 0.01 mm using color transition of the coagulation zone as the end point. Although it is established that RF lesions formed by linear probes are actually somewhat pear-shaped,22 most published studies have approximated the shape closest to that of a spheroid or ellipsoid11,12,14 for the purposes of volume calculation. The volume
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Determination of Lesion Size Lesions were measured in 3 dimensions along a length or Dv, maximal effective vertical radius (Merv, with reference to bone
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was from our pilot experiments, which revealed an overall shape consistent with an ellipsoid about the active tip but bisected by the equatorial plane of bone. Because d = 2r, and a factor of 2 is added to the denominator for a half-ellipsoid, the equation for the bone-muscle interface lesion condenses to the following: πðr l wÞ 6
Statistical Analysis Based on prior pilot data in regard to lesion dimension means and SDs for both groups, power analysis estimated that 10 experiments per group were necessary to have 95% power to detect a difference at an α level of 0.01. The data were presented as mean (95% confidence interval [CI]) and analyzed with single-factor analysis of variance performed in IBM SPSS version 22 (Armonk, New York). We considered α < 0.01 to be statistically significant.
RESULTS
FIGURE 3. Dissection and visualization of lesions. Both muscle and bone-muscle groups underwent the same process. With open face of bevel denoting vertical axis (and perpendicular to plane of bone), cut made to bisect lesion and expose vertical extents above the needle. After measurement, a horizontal plane is made to reveal a small thickness of coagulated tissue about 1.4 mm deep to bone representing a tissue plane the thickness of the needle, or the remaining tissue in pure muscle samples. With now 2 planes of dissection, the tissue is reflected upward and out of the way to allow horizontal plane measurements. Maximal effective radius is found among the several planes as the largest effective radius from the needle wall.
of the ablation zone in muscle was approximated to an ellipsoid using the following equation:
Radiofrequency-induced lesions created a well-defined zone of coagulation necrosis compared with areas of nontreated tissue. Results are summarized in Table 1. Baseline sample temperature was equivalent in both groups. The bone-muscle interface groups did reliably show higher prelesion and postlesion impedance than the muscle-only groups (mean [95% CI], 165.6 Ohm [146.6–184.6 Ohm] vs 137.8 Ohm [135.5–140.1 Ohm], P = 0.004; 144.3 Ohm [134.3–154.3 Ohm] vs 124.3 Ohm [119.3– 129.3 Ohm], P = 0.001). We found with high statistical significance that the lesion Mer projecting outward from the bony surface was consistently much larger, almost double, than the Mer in pure muscle (mean [95% CI], 5.65 mm [5.43–5.87 mm] vs 2.68 mm [2.55– 2.81 mm], P < .0001). In addition, Merv projection perpendicular to the bone surface was always found to be the Mer of the bonemuscle lesions in any direction. Other lesion dimensions, including total vertical depth, width (Dh), length (Dv), distal and proximal tip radii (T, Tp), Dh/Dv, and estimated volume, were not different.
πðd l wÞ 6
DISCUSSION
The volume of the ablation zone adjacent to bone was approximated using an ellipsoid cut in half. The basis for this estimation
To our knowledge, this is the first ex vivo study quantifying lesion shape in 3 dimensions when RF is performed at the bone-muscle interface using monopolar RF interventional pain
TABLE 1. Summary of 18-gauge, 10-mm Straight Active Tip Lesion Dimensions Represented as Means (95% CI) Measure Mer or *Merv, mm Total depth, mm Width (Dh), mm Length (Dv), mm Distal radius from tip (T), mm Proximal Radius From Tip(Tp), mm Dh/Dv Volume, μL Prelesion impedance, Ohm Postlesion impedance, Ohm Prelesion temperature, °C
Muscle (n = 10)
Bone-Muscle (n = 10)*
P
2.68 (2.55–2.81) 6.99 (6.66–7.31) 7.25 (7.09–7.42) 12.71 (12.3–13.1) 1.37 (1.17–1.56) 0.83 (0.72–0.95) 0.57 (0.55–0.59) 337.4 (314–361) 137.8 (135.5–140.1) 124.3 (119.3–129.3) 20.7 (20.1–21.3)
5.65 (5.43–5.87) 7.01 (6.79–7.23) 6.96 (6.34–7.59) 12.09 (11.5–12.7) 1.42 (1.15–1.70) 0.96 (0.72–1.20) 0.58 (0.52–0.64) 309.9 (272–348) 165.6 (146.6–184.6) 144.3 (134.3–154.3) 20.7 (20.1–21.3)
Mer1. The radius from bone was nearly double that in pure muscle, on average.
equipment. The Mer is essentially doubled in the bone-muscle interface group; however, the projection is directly outward from the bone and perpendicular to the needle axis in the vertical plane, creating a “taller” lesion (Fig. 4). The width and length and Dh/Dv ratio appear conserved in reference to the parallel plane to bone compared with pure muscle. Volume is similar, although caution should be used in interpreting volume, as the value is calculated based on estimation of an ellipsoid shape and not a direct measure. Importantly, distal extension of the lesion axially from the needle tip does not appear to be influenced by the presence of bone. Notably, the finding of vertical lesion extension is novel, considering the preponderance of interventional pain RF studies performed in chicken breast tissue or egg-white media yielded relatively circumferentially uniform lesions. We developed this porcine rib model as we felt it would be practical for examining and dissecting lesions near a relatively flat, consistent, and smooth bone surface, with ample overlying muscle tissue, which is easy to visualize and target. We hypothesize that the cortical bone, which has a significantly higher electrical impedance than muscle and other deep soft tissues,17,18 serves as an insulator that directs the current return path further outward into the surrounding soft tissue. Indeed, our data indicate that starting and ending impedances are increased near the bone, although we did not track impedance throughout the lesion cycle or the resulting power output. There may be a thermal insulating effect as well, preventing heat loss, as bone has a lower thermal conductivity than muscle.20 The resulting RF lesion projection is directly in the vertical plane perpendicularly away from the bone surface and axis of the needle, but not distally from the needle tip or horizontally along the plane of the bone surface. There are some weaknesses of our model. The bone surface regularity and surrounding tissue composition (eg, muscle, tendon, ligament, fat, vessels) in our model probably differ somewhat © 2015 American Society of Regional Anesthesia and Pain Medicine
RF Lesion Changes Near Bone
from those in the spine. Porcine rib bone and muscle may have a different density than human vertebral bone and spine tissues as well, although the model is at least mammalian. The relative compositions of muscle, fat, and connective tissue may systematically differ near the bone than in other parts of the muscle in our own samples (although all were obtained from intercostal segments) and might account for some of the lesion size difference due to soft tissue changes alone. Therefore, caution must be used in inferring direct effects of the bone surface. However, this model is arguably closer to physiologic conditions—where these factors are present in clinical practice—than any purely uniform medium. The tissue dissection must be carefully performed to avoid disruption and loss of information. Performing the same measures with an irregular bone surface, such as is present around the dorsal elements of the lumbar spine, will prove more challenging, although investigation in homogeneous isolated spine tissue has been possible.26 We cannot account for any cooling effects of circulating blood in perfused living tissue21; however, other models have not demonstrated this either. Using previous estimates for lesion extents made by commonly available interventional pain management RF probes may underestimate the projection of RF lesions performed on the spine away from the surface of the periosteum. However, absence of any additional projection from the needle tip with the presence of bone is reassuring with respect to concern for avoidance of spinal nerve damage (from overly anterior lesions approaching the foramen) when the RF cannula is oriented in the proper position along the course of the medial branch nerve,6 particularly considering that our finding of 1.4-mm distal tip lesion projection is identical to previous work by Bogduk et al4 in meat samples with 18-gauge cannulas. We also find that horizontal lesion width along the bone surface and total volume are not significantly altered. Therefore, we cannot conclude any expected change to the maximal tolerable margin of error28 of needle proximity in parallel to the path of the nerve to ensure full denaturation, and clinicians should continue to place the needle as closely as previously recommended so that a radius of about 2 mm can encompass the diameter of the medial branch nerve fully.5,6,27 Overall, using pure muscle tissue for modeling RF lesions as has been done previously appears to be both practical and comparatively accurate with the exception of vertical lesion extension from the bone surface. Further elaboration of our model using a curved, especially concave, bone surface as encountered on the spine may be warranted to evaluate possible effects of bone surface geometry. Although RF has proven to be a safe and effective method of producing controlled lesions in clinical practice,23 the unanticipated extension of RF lesions near bone could incorporate tissues that were unintended for denaturation, including skin in regions where tissue overlying the spine is thin, or possibly vascular structures where they are closely associated with the cervical spine. A third-degree burn has been reported in the application of cooled RF for thoracic medial branch neurotomy,28 although it is not possible to conclude that vertical extension due to bone was the cause because multiple technical factors such as current leakage, inadvertent cannula migration, or cooled RF increased lesion size relative to thin anatomic conditions might also result in superficial burns. Transient blindness has been reported during a cervical RF procedure,29 although the phenomenon was attributed to local anesthetic injection of the deep ascending cervical artery in proximity to the articular pillar; adverse clinical consequences of coagulating this artery are otherwise unknown. Further cadaveric spine and mammalian spine studies, although likely challenging, should
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be considered to investigate these potential safety issues. Incorporating imaging technology (such as infrared) may be useful to augment measures obtained by dissection and direct visualization. Although cooled RF technologies are now available for significant lesion enhancement in the lumbosacral and thoracic spine, there should be careful consideration and testing before such strategies are applied to the cervical spine considering the proximity of critical neurologic and vascular structures and the additional possible but untested effect of bone projection in the setting of cooled RF. In tumor ablation RF techniques, excessive necrosis has been reported from overexpansion of saline-enhanced RF lesions; however, saline in these applications is usually continuously infused throughout the procedure.24 Fluid injection against bone may be a logical next area of investigation as it has been shown to enhance lesion size in soft tissue.15 Currently, the majority of research aimed at determining the effect of variables on RF lesion dimensions is seen in the cardiology or interventional radiology literature and performed in homogenous media relevant, for example, to the destruction of solid organ tumors. These principles are being successfully applied to interventional pain medicine, yet current studies do not factor in the effects of nearby bone, which we believe to be relevant to clinical use of RF about the spine in some select conditions. The bone-muscle interface should be evaluated in many applications including pulsed and continuous RF, bipolar and monopolar RF, lesion properties with fluid injection, and effects of active cooling. Similarly, there is a lack of literature on RF near metallic spine hardware despite this very relevant challenge in patients with chronic facetogenic spine pain and prior fusion. More research is warranted to confirm the mechanism of lesion extension into soft tissue when RF is applied near a bony surface and to determine any potential impact on clinical practice. In addition, we should work to refine models that can test this phenomenon.
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ACKNOWLEDGMENTS The authors thank the following individuals for their contributions to this work: Dr Kun Zhang, PhD, MD, UTHSCSA, for review of style and statistical methodology; Dr Joshua Hay, MD, Spine Works Institute, North Richland Hills, Texas, for preliminary experimental protocol development; and Jimmy Tai, BS, UTHSCSA, for assistance performing the experiments.
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