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The scientific basis of thermal capsular shrinkage
REVIEW ARTICLE The scientific basis of thermal capsular shrinkage Andrew L. Wallace, MBBS, PhD, FRACS, Robert M. Hollinshead, MD, FRCS(C), and Cyril B. Frank, MD, FRCS(C), Calgary, Alberta, Canada
With advances in technology, arthroscopic manage-
ment of glenohumeral instability has increased in popularity over recent years. However, the short-term attractions of a minimally invasive technique that offers reduced hospital stay and the potential for accelerated rehabilitation should be balanced against the longer term functional outcome. Unfortunately, published reports of arthroscopic stabilization have thus far yielded disappointing results when compared with those of conventional open procedures.43 In a recent study higher rates of symptomatic recurrence, residual signs of instability, and the need for revision surgery were found in those patients treated with arthroscopy.18 Although repair of a labral detachment is technically feasible, eliminating excess capsular laxity has proven more difficult and has been cited as a major factor in failure of the arthroscopic procedure.34,55 Thermal capsular shrinkage holds considerable promise for dealing with redundant capsule and therefore may enhance the outcome of arthroscopic stabilization. Heat lability of the collagen triple helix has long been recognized; recent developments have allowed this phenomenon to be harnessed to treat the unstable joint. Thermal energy may be delivered to the tissue by the application of either laser light or radiofrequency electrical current. At present there are no published prospective randomized studies with either modality with sufficient follow-up to establish clinical From the McCaig Centre for Joint Injury and Arthritis Research, University of Calgary, and the Division of Orthopaedic Surgery, Department of Surgery, University of Calgary. Supported by the Alberta Heritage Foundation for Medical Research. Reprint requests: A. L. Wallace, MBBS, PhD, FRACS, Senior Lecturer in Orthopaedic Surgery, Imperial College School of Medicine, Charing Cross Hospital, Fulham Palace Rd, London W6 8RF, England. J Shoulder Elbow Surg 2000;9:354-60. Copyright © 2000 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2000/$12.00 + 0 32/1/103659 doi:10.1067/mse.2000.103659
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outcome. The purpose of this review is to examine the evidence available from basic science studies to determine the biologic and biomechanical effects of thermal capsular shrinkage, which may assist in the development of guidelines for clinical use.
PHYSICAL ASPECTS OF HEAT TRANSFER Thermal energy may be transferred to tissues by direct conduction, by fluid convection currents, or by radiation. The transfer of radiant heat depends on the temperature differential at the surface and the absorption properties of the tissue.13 Once transferred, the heat is diffused throughout the tissue by random motion of the molecules; it may also be conducted to other tissue planes and subject to convection by local blood flow and the flow of irrigation fluid. Laser light is a collimated beam of finite wavelength, usually in the infrared region of the electromagnetic spectrum for clinical use. It may be transmitted, refracted, scattered, or absorbed; it is absorption of light by water that results in tissue heating.1,51 The temperature achieved is related to the power of the laser, the duration of application, and the area irradiated. The distance of the laser from the tissue surface and the color of the tissue are also factors that affect energy absorption.3 Most clinical lasers such as the carbon dioxide laser have been used for ablation of tissue, in which the objective is to remove the target lesion with minimal adjacent thermal damage. Theoretically, pulsatile delivery of laser energy allows for some tissue cooling between pulses (thermal relaxation time) and therefore less residual damage than continuous delivery. Histologically, 3 zones of collagen damage of varying extent have been described after ablative use in skin: (1) charring (1 to 5 µm), (2) loss of fibrillar appearance (5 to 15 µm), and (3) increased fibril diameter (50 to 100 µm).63 In a study with the Holmium-Yttrium-Aluminum-Garnet (Hol-YAG) laser, which may be used with flexible fiberoptic cables in a fluid environment and is therefore suited for arthroscopic use, varying the pulsewidth did not appear to affect thermal damage in human meniscal tissue.61
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When an alternating electrical current is applied to tissue, heat may be generated by friction as a result of the oscillation of electrons and molecules as the polarity changes; this is termed ohmic resistance. As with the laser, this “resistive” heat may be further distributed by conduction and convection. With electrical energy the degree of tissue damage depends on the power and the waveform: damping and separation of wavetrains result in tissue destruction or coagulation, whereas very high frequencies of 350 kHz to 1 MHz (radiofrequency) result only in a heating effect.12 Thermal ablation with radiofrequency energy has been used for treatment of experimental chondromalacia in the ovine knee59 and for various nonorthopaedic surgical indications such as prostatic hypertrophy7 and cardiac arrhythmias.41 The extent of a radiofrequency lesion is dictated by the magnitude of power delivered, the size of the electrode tip, the duration of application, and the temperature at the electrode-tissue interface. Because the volume of tissue heated is related to the fourth power of the distance from the electrode, only a very narrow rim (approximately 1 mm) of heating typically occurs.19 Temperature monitoring has been proposed as a practical means of controlling lesion size,14,19 and commercially available RF electrodes now incorporate temperature-sensing devices.37 In myocardium in vitro studies have shown good correlation between lesion size and tip temperature,30 but in ligaments measured tissue temperatures may be different from those at the probe tip.42 These discrepancies have been attributed to a convective cooling effect of the surrounding fluid flow,39 but the design and orientation of the electrode tip may also be implicated.30 In a recent study with an RF probe in the ovine knee joint, the thermal effect (lesion area and depth) was found to be proportional to the power delivered by the RF generator when the temperature was held constant at 65°C.28 The ability to measure temperature at the RF probe tip may prove to be a relative advantage over laser devices in controlling the extent of thermal shrinkage.
THERMAL STABILITY OF COLLAGEN The collagen in ligamentous tissues is predominantly type I, which assumes a triple-helical configuration in the extracellular matrix. The 3 polypeptide chains that form the molecule are stabilized in this coiled-coil arrangement by interchain hydrogen bonding between adjacent glycine residues and reinforced by hydrogen bonding based on the sidechains of hydroxyproline residues.5 The individual molecules are aggregated laterally in a quarter-stagger array to form a linear polymer, which is stabilized in turn by covalent cross-linking. The most prevalent form of this cross-linking is derived from lysine residues, forming aldehyde cross-links that are “reducible” under the action of borohydride. As a tissue ages, these are progressively replaced with irre-
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ducible multivalent cross-links such as pyridinoline and nonenzymatic glycosylation.5,54 In essence, intramolecular bonding stabilizes the triple helix; intermolecular cross-linking maintains the fibrillar arrangement that contributes to tissue tensile properties. As collagen is heated to a critical temperature, the heat-labile intramolecular hydrogen bonds break, and the protein undergoes a phase transition from a highly ordered crystalline structure to a random-coil state, similar to melting.16,38 Typically, this “denaturation” occurs at approximately 55° to 60°C, the “shrinkage temperature,”56 although the temperature varies between tissues and species and is higher with increased collagen concentration and increased tensile load on the tissue.10,16,29 The shrinkage temperature has also been found to increase with age, possibly because of an increased proportion of heat-stable irreducible crosslinks.54 In vitro studies have demonstrated shrinkage at lower temperatures (42° to 45°C) in purified collagen-I films, which was attributed to the absence of a stabilizing effect of matrix proteoglycans.53 The thermal denaturation process is essentially irreversible.20,38,53 Histologic studies have shown loss of fiber striations, which is manifest under electron microscopy as loss of the classic 67-nm periodicity of the collagen-I fibril. The fibrils appear enlarged, with blurred margins and interdigitation with adjacent fibrils.23,33,48 Early investigations of experimental vascular “welding” with lasers at temperatures less than 60°C suggested that there was annealing of collagen molecules, either by reestablishment of physicochemical bonds64 or by formation of new cross-links.31 Subsequently, it has been shown that the helical structure does not reform, and there is no evidence of novel covalent bonds; rather, it is more likely that noncovalent bonds form between adjacent denatured strands.4
BIOMECHANICAL EFFECTS OF THERMAL TREATMENT The acute changes in tissues after thermal treatment have been investigated in vitro with a temperaturecontrolled saline solution bath, which eliminates some of the variables related to energy delivery. In an experiment with bovine knee joint capsule, no shrinkage was demonstrated at temperatures less than 60°C.40 Isolated human Achilles tendon specimens shrank up to 50% of their original length at 69°C, but there was no further shrinkage when the temperature exceeded 72°C.60 Thermal shrinkage was found to depend not just on temperature but also on the duration of treatment, although at 65°C most of the shrinkage occurred within the first minute. These results have been confirmed with cadaveric human glenohumeral joint capsule, although maximal shortening was found at 80°C.27 An earlier study with an isometric preparation of rat skin found a sudden increase
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in longitudinal tension when the temperature was raised from 62° to 65°C.2 In vitro studies with the Hol-YAG laser at nonablative doses have shown similar findings, with up to 50% shrinkage of the lased area of isolated canine patellar tendon. However, mechanical testing immediately after treatment showed a significant reduction in tissue stiffness, even when the tissue was stretched back to its original length.6 In another study with specimens of capsule from the rabbit knee joint, the extent of shrinkage (10% to 50%) was shown to be quantitatively related to the energy density of the laser dose. With higher doses of energy delivered (10 to 15 W), there was a 77% to 90% decrease in tissue stiffness after lasing, although viscoelastic properties (assessed by load relaxation) were not altered.23 In human tissue laser treatment effectively reduced translation of the glenohumeral joint subjected to low “physiological” loads.49,58 However, in another human cadaveric study performed under similar conditions, the inferior glenohumeral ligament complex underwent significantly greater deformation after lasing than did nonlased specimens.50 In one of the few studies to investigate failure behavior immediately after nonablative Neodymium-YAG (Nd-YAG) treatment, tensile failure loads of human patellar tendon specimens were reduced by approximately 30%.61 When laser-induced thermal shrinkage has been applied in vivo, however, the response of tissues appears to be different. In one study there was less than 10% shrinkage of the rabbit patellar tendon at the time of surgery.47 The authors attributed this finding to the fact that the tissue was relatively more constrained by its bony attachments when treated in situ, tending to resist shrinkage, together with a lower penetration depth of laser energy, when compared with the specimens used in previous studies. Subsequently, under physiological loads the patellar tendon began to stretch at 4 weeks, so that it was approximately 5% longer than its original length by 8 weeks, when the experiment concluded. These findings were associated with a 20% reduction in stiffness and a 25% increase in crosssectional area.47 However, in this study length was assessed with a radiographic technique in the anesthetized animal without measurement of the load on the tendon, and therefore it is difficult to compare with other in vitro studies. Longer term effects of laser energy have recently been investigated. After 12 weeks tensile strength of the lapine patellofemoral joint capsule had recovered to control values, although the degree of recovery varied with the site of treatment within the joint.46 After arthroscopically applied laser shrinkage of the normal ovine knee joint capsule occurred, mechanical properties were assessed at multiple intervals up to 180 days after surgery.22 Tissue stiffness was reduced immedi-
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ately after surgery but had returned to control values by 14 days and remained similar for the duration of the experiment. Viscoelastic properties (measured by stress relaxation) were unchanged at any time point, and remarkably, no statistically significant differences were found in failure strength either. Conversely, in a model of surgically created abnormal laxity of the rabbit medial collateral ligament, viscoelastic properties (assessed by measurement of creep deformation) were found to be dramatically altered after radiofrequency electrothermal shrinkage treatment. Although joint laxity was effectively restored, creep strains remained elevated even at 12 weeks after surgery. At 3 weeks some specimens failed at less than 5% of the strength of intact normal ligaments.62 In summary, the biomechanical data available indicate that although significant alterations in length of capsular and ligamentous tissues may be achieved at the time of thermal treatment in vitro and to a lesser extent in vivo, the shrinkage may not be maintained once physical activity resumes. At this time the effects on the structural and material properties also provide cause for concern, because in some studies the technique appears to result in substantial reductions in strength and stiffness of the tissue in the acute phase. It should also be remembered that these biomechanical investigations have been based on normal tissues, which are likely to behave quite differently from the tissues found in pathologically unstable joints or joints subjected to previous surgery; the relative importance of collagen fibril orientation and extent or type of crosslinking have yet to be determined.
BIOLOGIC RESPONSE TO THERMAL SHRINKAGE At present little information is available on the morphologic, ultrastructural, and biochemical changes that underlie the alterations in connective tissue mechanics resulting from thermal treatment. Some insight as to possible mechanisms involved may be gained from observations made after dermal burn injuries. In the burn zone cell death is inevitable, because most enzyme systems are inactivated at temperatures greater than 45°C, and proteins other than collagen are also denatured.35 Collagen in burned tissue also shows increased solubility and susceptibility to degradation by proteolytic enzymes.21 The local microvasculature also undergoes profound changes, which have been characterized into 3 zones: (1) coagulation, where all flow has ceased, (2) stasis, where there is partial occlusion of vessels caused by platelet aggregation, and (3) hyperemia, where there is initial vasoconstriction followed by a rebound increase in flow resulting from release of vasoactive mediators from damaged endothelial cells.8 The repair of a full-thickness skin burn has been well
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studied and follows a predictable sequence of reepithelialization, in-growth of granulation tissue, and contraction.45 Studies of the contraction process have shown clinically and experimentally that excision of a full-thickness burn enhances contraction and that treatment with partial-thickness grafts results in greater contraction than that with full-thickness grafts. Conversely, little contraction occurs after a freezing injury.32 These observations are consistent with the idea that the greater the quantity and quality are of matrix preserved after a thermal injury, the greater the inhibitory influence on the contraction process is. The lack of a contractile response may play a role in the “stretching out” of the ligamentous tissue seen in one in vivo model after laser thermal shrinkage.47 Histologic analysis of laser-treated tissues has generally concentrated on the changes in the first few weeks after surgery, and little information is available on longer term response. The extent of repair by scar formation is controversial. In a comparison of vascular anastomosis with the argon laser or conventional suture techniques, laser-treated tissue was found to have less evidence of inflammation, with minimal change in collagen content or synthesis after 4 weeks.65 In a porcine model of cutaneous resurfacing, Fitzpatrick et al15 assessed the tissue response from 2 days to 6 weeks and found that although dermal thickness was increased (which was attributed to thermal shrinkage of collagen), there was no evidence of scarring despite initial thermal necrosis. However, in human skin biopsy specimens assessed 90 days after laser surgery, a distinct “dermal repair zone” was seen with newly synthesized collagen and reorientation of elastin fibers.11 Furthermore, in a comparative study of wounds caused by either scalpel or laser, no difference was found in the expression of a range of growth factors in the acute phase after surgery, although in the lased wounds inflammatory cells appeared slightly earlier.66 In ligament tissue several short-term histologic studies provide some qualitative evidence for scar formation after laser thermal treatment. In a canine model in which thermal treatment was applied to the glenohumeral capsule with an arthroscopic technique, the authors found that the extent of thermal injury was difficult to control, resulting in some areas where full-thickness necrosis of the capsule occurred. At 6 weeks after surgery, there was marked synovitis, extensive fibrosis, and neovascularization, with a prominent inflammatory cell infiltrate in the thickened capsule.44 Similar changes were found in the rabbit knee capsule, with fibroblasts actively synthesizing new collagen matrix 30 days after laser treatment. It was concluded that the newly arrived fibroblasts used the acellular “hyalinized” collagen as a framework for migration and matrix synthesis.25 Electron microscopic analysis of these tissues has shown a high proportion of small-
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diameter (30 to 50 nm) collagen fibrils.47 Loss of the normal bimodal distribution of large- and small-diameter fibrils and replacement by a homogeneous population of small-diameter fibrils is typical of scar tissue.17 In a longer term report after laser thermal shrinkage, Hayashi et al22 found little histologic evidence of inflammation at any time point up to 180 days after surgery. Collagen fibrils assessed with transmission electron microscopy were “normal-looking” by 90 days. Although this was a purely qualitative assessment, the authors speculated that remodeling was mainly dependent on the residual population of fibroblasts. In another study from the same laboratory, biopsy specimens of human glenohumeral capsule were obtained from patients undergoing treatment for the contralateral shoulder between 3 and 38 months after the initial laser shrinkage procedure. No inflammation was seen in the specimens, although overall cellularity remained greater than normal, even after 3 years. The periodic “crimp” pattern of collagen fibers seen in normal ligaments began to reappear 12 months after surgery.24 There have been few direct comparisons of the effects of lasers with electrothermal energy on tissues. Previously, lasers have been compared with electrosurgery (cautery) in investigations of ablative properties. In fresh human menisci electrosurgical incisions produced a greater zone of residual thermal damage than a range of different lasers.52 Similar patterns were found in porcine palatal tissue.36 In a study using porcine skin, both the Nd-YAG laser and cautery created a similar depth of injury, but 60 days after treatment collagen concentration and synthesis were lower in the laser wound, leading the authors to conclude that the effects on collagen metabolism were different.9 However, in mechanical terms there may not be any particular advantage of one modality over the other. In the only report to date comparing the Hol:YAG laser with radiofrequency shrinkage, the acute reduction of glenohumeral translation in a cadaveric model was the same.58 A preliminary report of RF effects on joint capsular tissue has recently been presented.28 At 7 days after arthroscopic treatment of the ovine knee capsule, the extent of the lesion was found to be related to the magnitude of power delivery. The lesions were well circumscribed, with avascular necrotic centers of fused collagen fibrils surrounded by thrombotic vessels. There was a definite increase in vascularity and inflammation. It is interesting that in the higher-power lesions in which there was evidence of damage to underlying muscle, the synovial layer was preserved, suggesting that the arthroscopic irrigation fluid had some protective effect in moderating heat generation at the tissue surface.
CONCLUSIONS Capsular shrinkage induced by thermal denatura-
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tion of the collagen triple helix represents a novel development in the evolving management of shoulder instability. From the data available, both laser and radiofrequency electrical modalities appear to provide satisfactory modes of delivery; the clinical choice will be determined by practical issues such as availability, cost, safety concerns, and the ability to quantitatively control the extent of treatment. The latter factor deserves special consideration, because overzealous application of heat may be conducted to deeper planes, posing a risk to adjacent structures such as the axillary nerve. The acute shortening of ligament tissues that may be produced by the application of thermal energy in vitro is impressive, but the extent of shrinkage and outcome after recovery in vivo remains uncertain. Evidence from study of human tissues and from animal models suggests that normal capsule is significantly weakened and made more compliant immediately after treatment and may subsequently be remodeled by the in-growth of scar tissue at a new, shortened length. However, if this repair tissue stretches out under physiological loading conditions, the excess laxity may recur or may even be made worse. Fortunately, there seems to be potential for recovery of mechanical properties toward normal by approximately 12 weeks after surgery. Therefore from both basic science and clinical perspectives much remains to be done. To provide a more relevant clinical analog, the underlying pathologic condition of capsular laxity must be further investigated. The physiological, morphologic, and biochemical abnormalities that give rise to capsular laxity across the clinical spectrum from atraumatic multidirectional to post-traumatic unidirectional instability require definition. Once more information regarding these abnormalities is known, more appropriate in vivo models can be developed on which to evaluate new therapies such as thermal shrinkage. The biomechanical behavior of thermally treated ligament tissue under low “physiological” and high “failure” loads can then be ascertained at clinically relevant intervals and compared with existing data on healing ligaments. At the present time, thermal capsular shrinkage should be regarded as a developmental technique in the arthroscopic management of instability. It is conceivable that the final result might still be comparable to open surgical capsulorraphy, but prospective clinical studies with validated outcome measures are necessary to answer this question. Continued close collaboration between clinicians and research scientists will determine the precise role for thermal shrinkage in the armamentarium of the shoulder surgeon, with the ultimate goal of restoring stability with low morbidity and predictable early return of function for the patient with an unstable shoulder.
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60. Vangsness CT, Mitchell W, Nimni M, Erlich M, Saadat V, Schmotzer H. Collagen shortening: an experimental approach with heat. Clin Orthop 1997;337:267-71. 61. Vangsness CT, Watson T, Saadatmanesh V, Moran K. Pulsed Ho:YAG laser meniscectomy: effect of pulsewidth on tissue penetration rate and lateral thermal damage. Lasers Surg Med 1995;16:61-5. 62. Wallace AL, Sutherland CA, Marchuk LL, Waddell M, Hollinshead RM, Shrive NG, Frank CB. Early in vivo effects of electrothermal shrinkage on viscoelastic properties and cellular responses in a model of ligament laxity. Trans Orthop Res Soc 1999;306.
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63. Walsh JT, Flotte TJ, Anderson RR, Deutsch TF. Pulsed CO2 laser tissue ablation: Effect of tissue type and pulse duration on thermal damage. Lasers Surg Med 1988;8:108-18. 64. White RA, Kopchok G, Peng S-K, Fujitani R, White G, Klein S, Uitto J. Laser vascular welding: How does it work? Ann Vasc Surg 1986;1:461-4. 65. White RA, Kopchok GE, Donayre CE, Peng S-K, Fujitani RM, White GH, Uitto J. Mechanism of tissue fusion in argon laser-welded vein-artery anastomoses. Lasers Surg Med 1988;8:83-9. 66. Yu W, Naim JO, Lanzafame RJ. Expression of growth factors in early wound healing in rat skin. Lasers Surg Med 1994;15:281-9.
With advances in technology, arthroscopic manage-
ment of glenohumeral instability has increased in popularity over recent years. However, the short-term attractions of a minimally invasive technique that offers reduced hospital stay and the potential for accelerated rehabilitation should be balanced against the longer term functional outcome. Unfortunately, published reports of arthroscopic stabilization have thus far yielded disappointing results when compared with those of conventional open procedures.43 In a recent study higher rates of symptomatic recurrence, residual signs of instability, and the need for revision surgery were found in those patients treated with arthroscopy.18 Although repair of a labral detachment is technically feasible, eliminating excess capsular laxity has proven more difficult and has been cited as a major factor in failure of the arthroscopic procedure.34,55 Thermal capsular shrinkage holds considerable promise for dealing with redundant capsule and therefore may enhance the outcome of arthroscopic stabilization. Heat lability of the collagen triple helix has long been recognized; recent developments have allowed this phenomenon to be harnessed to treat the unstable joint. Thermal energy may be delivered to the tissue by the application of either laser light or radiofrequency electrical current. At present there are no published prospective randomized studies with either modality with sufficient follow-up to establish clinical From the McCaig Centre for Joint Injury and Arthritis Research, University of Calgary, and the Division of Orthopaedic Surgery, Department of Surgery, University of Calgary. Supported by the Alberta Heritage Foundation for Medical Research. Reprint requests: A. L. Wallace, MBBS, PhD, FRACS, Senior Lecturer in Orthopaedic Surgery, Imperial College School of Medicine, Charing Cross Hospital, Fulham Palace Rd, London W6 8RF, England. J Shoulder Elbow Surg 2000;9:354-60. Copyright © 2000 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2000/$12.00 + 0 32/1/103659 doi:10.1067/mse.2000.103659
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outcome. The purpose of this review is to examine the evidence available from basic science studies to determine the biologic and biomechanical effects of thermal capsular shrinkage, which may assist in the development of guidelines for clinical use.
PHYSICAL ASPECTS OF HEAT TRANSFER Thermal energy may be transferred to tissues by direct conduction, by fluid convection currents, or by radiation. The transfer of radiant heat depends on the temperature differential at the surface and the absorption properties of the tissue.13 Once transferred, the heat is diffused throughout the tissue by random motion of the molecules; it may also be conducted to other tissue planes and subject to convection by local blood flow and the flow of irrigation fluid. Laser light is a collimated beam of finite wavelength, usually in the infrared region of the electromagnetic spectrum for clinical use. It may be transmitted, refracted, scattered, or absorbed; it is absorption of light by water that results in tissue heating.1,51 The temperature achieved is related to the power of the laser, the duration of application, and the area irradiated. The distance of the laser from the tissue surface and the color of the tissue are also factors that affect energy absorption.3 Most clinical lasers such as the carbon dioxide laser have been used for ablation of tissue, in which the objective is to remove the target lesion with minimal adjacent thermal damage. Theoretically, pulsatile delivery of laser energy allows for some tissue cooling between pulses (thermal relaxation time) and therefore less residual damage than continuous delivery. Histologically, 3 zones of collagen damage of varying extent have been described after ablative use in skin: (1) charring (1 to 5 µm), (2) loss of fibrillar appearance (5 to 15 µm), and (3) increased fibril diameter (50 to 100 µm).63 In a study with the Holmium-Yttrium-Aluminum-Garnet (Hol-YAG) laser, which may be used with flexible fiberoptic cables in a fluid environment and is therefore suited for arthroscopic use, varying the pulsewidth did not appear to affect thermal damage in human meniscal tissue.61
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When an alternating electrical current is applied to tissue, heat may be generated by friction as a result of the oscillation of electrons and molecules as the polarity changes; this is termed ohmic resistance. As with the laser, this “resistive” heat may be further distributed by conduction and convection. With electrical energy the degree of tissue damage depends on the power and the waveform: damping and separation of wavetrains result in tissue destruction or coagulation, whereas very high frequencies of 350 kHz to 1 MHz (radiofrequency) result only in a heating effect.12 Thermal ablation with radiofrequency energy has been used for treatment of experimental chondromalacia in the ovine knee59 and for various nonorthopaedic surgical indications such as prostatic hypertrophy7 and cardiac arrhythmias.41 The extent of a radiofrequency lesion is dictated by the magnitude of power delivered, the size of the electrode tip, the duration of application, and the temperature at the electrode-tissue interface. Because the volume of tissue heated is related to the fourth power of the distance from the electrode, only a very narrow rim (approximately 1 mm) of heating typically occurs.19 Temperature monitoring has been proposed as a practical means of controlling lesion size,14,19 and commercially available RF electrodes now incorporate temperature-sensing devices.37 In myocardium in vitro studies have shown good correlation between lesion size and tip temperature,30 but in ligaments measured tissue temperatures may be different from those at the probe tip.42 These discrepancies have been attributed to a convective cooling effect of the surrounding fluid flow,39 but the design and orientation of the electrode tip may also be implicated.30 In a recent study with an RF probe in the ovine knee joint, the thermal effect (lesion area and depth) was found to be proportional to the power delivered by the RF generator when the temperature was held constant at 65°C.28 The ability to measure temperature at the RF probe tip may prove to be a relative advantage over laser devices in controlling the extent of thermal shrinkage.
THERMAL STABILITY OF COLLAGEN The collagen in ligamentous tissues is predominantly type I, which assumes a triple-helical configuration in the extracellular matrix. The 3 polypeptide chains that form the molecule are stabilized in this coiled-coil arrangement by interchain hydrogen bonding between adjacent glycine residues and reinforced by hydrogen bonding based on the sidechains of hydroxyproline residues.5 The individual molecules are aggregated laterally in a quarter-stagger array to form a linear polymer, which is stabilized in turn by covalent cross-linking. The most prevalent form of this cross-linking is derived from lysine residues, forming aldehyde cross-links that are “reducible” under the action of borohydride. As a tissue ages, these are progressively replaced with irre-
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ducible multivalent cross-links such as pyridinoline and nonenzymatic glycosylation.5,54 In essence, intramolecular bonding stabilizes the triple helix; intermolecular cross-linking maintains the fibrillar arrangement that contributes to tissue tensile properties. As collagen is heated to a critical temperature, the heat-labile intramolecular hydrogen bonds break, and the protein undergoes a phase transition from a highly ordered crystalline structure to a random-coil state, similar to melting.16,38 Typically, this “denaturation” occurs at approximately 55° to 60°C, the “shrinkage temperature,”56 although the temperature varies between tissues and species and is higher with increased collagen concentration and increased tensile load on the tissue.10,16,29 The shrinkage temperature has also been found to increase with age, possibly because of an increased proportion of heat-stable irreducible crosslinks.54 In vitro studies have demonstrated shrinkage at lower temperatures (42° to 45°C) in purified collagen-I films, which was attributed to the absence of a stabilizing effect of matrix proteoglycans.53 The thermal denaturation process is essentially irreversible.20,38,53 Histologic studies have shown loss of fiber striations, which is manifest under electron microscopy as loss of the classic 67-nm periodicity of the collagen-I fibril. The fibrils appear enlarged, with blurred margins and interdigitation with adjacent fibrils.23,33,48 Early investigations of experimental vascular “welding” with lasers at temperatures less than 60°C suggested that there was annealing of collagen molecules, either by reestablishment of physicochemical bonds64 or by formation of new cross-links.31 Subsequently, it has been shown that the helical structure does not reform, and there is no evidence of novel covalent bonds; rather, it is more likely that noncovalent bonds form between adjacent denatured strands.4
BIOMECHANICAL EFFECTS OF THERMAL TREATMENT The acute changes in tissues after thermal treatment have been investigated in vitro with a temperaturecontrolled saline solution bath, which eliminates some of the variables related to energy delivery. In an experiment with bovine knee joint capsule, no shrinkage was demonstrated at temperatures less than 60°C.40 Isolated human Achilles tendon specimens shrank up to 50% of their original length at 69°C, but there was no further shrinkage when the temperature exceeded 72°C.60 Thermal shrinkage was found to depend not just on temperature but also on the duration of treatment, although at 65°C most of the shrinkage occurred within the first minute. These results have been confirmed with cadaveric human glenohumeral joint capsule, although maximal shortening was found at 80°C.27 An earlier study with an isometric preparation of rat skin found a sudden increase
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in longitudinal tension when the temperature was raised from 62° to 65°C.2 In vitro studies with the Hol-YAG laser at nonablative doses have shown similar findings, with up to 50% shrinkage of the lased area of isolated canine patellar tendon. However, mechanical testing immediately after treatment showed a significant reduction in tissue stiffness, even when the tissue was stretched back to its original length.6 In another study with specimens of capsule from the rabbit knee joint, the extent of shrinkage (10% to 50%) was shown to be quantitatively related to the energy density of the laser dose. With higher doses of energy delivered (10 to 15 W), there was a 77% to 90% decrease in tissue stiffness after lasing, although viscoelastic properties (assessed by load relaxation) were not altered.23 In human tissue laser treatment effectively reduced translation of the glenohumeral joint subjected to low “physiological” loads.49,58 However, in another human cadaveric study performed under similar conditions, the inferior glenohumeral ligament complex underwent significantly greater deformation after lasing than did nonlased specimens.50 In one of the few studies to investigate failure behavior immediately after nonablative Neodymium-YAG (Nd-YAG) treatment, tensile failure loads of human patellar tendon specimens were reduced by approximately 30%.61 When laser-induced thermal shrinkage has been applied in vivo, however, the response of tissues appears to be different. In one study there was less than 10% shrinkage of the rabbit patellar tendon at the time of surgery.47 The authors attributed this finding to the fact that the tissue was relatively more constrained by its bony attachments when treated in situ, tending to resist shrinkage, together with a lower penetration depth of laser energy, when compared with the specimens used in previous studies. Subsequently, under physiological loads the patellar tendon began to stretch at 4 weeks, so that it was approximately 5% longer than its original length by 8 weeks, when the experiment concluded. These findings were associated with a 20% reduction in stiffness and a 25% increase in crosssectional area.47 However, in this study length was assessed with a radiographic technique in the anesthetized animal without measurement of the load on the tendon, and therefore it is difficult to compare with other in vitro studies. Longer term effects of laser energy have recently been investigated. After 12 weeks tensile strength of the lapine patellofemoral joint capsule had recovered to control values, although the degree of recovery varied with the site of treatment within the joint.46 After arthroscopically applied laser shrinkage of the normal ovine knee joint capsule occurred, mechanical properties were assessed at multiple intervals up to 180 days after surgery.22 Tissue stiffness was reduced immedi-
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ately after surgery but had returned to control values by 14 days and remained similar for the duration of the experiment. Viscoelastic properties (measured by stress relaxation) were unchanged at any time point, and remarkably, no statistically significant differences were found in failure strength either. Conversely, in a model of surgically created abnormal laxity of the rabbit medial collateral ligament, viscoelastic properties (assessed by measurement of creep deformation) were found to be dramatically altered after radiofrequency electrothermal shrinkage treatment. Although joint laxity was effectively restored, creep strains remained elevated even at 12 weeks after surgery. At 3 weeks some specimens failed at less than 5% of the strength of intact normal ligaments.62 In summary, the biomechanical data available indicate that although significant alterations in length of capsular and ligamentous tissues may be achieved at the time of thermal treatment in vitro and to a lesser extent in vivo, the shrinkage may not be maintained once physical activity resumes. At this time the effects on the structural and material properties also provide cause for concern, because in some studies the technique appears to result in substantial reductions in strength and stiffness of the tissue in the acute phase. It should also be remembered that these biomechanical investigations have been based on normal tissues, which are likely to behave quite differently from the tissues found in pathologically unstable joints or joints subjected to previous surgery; the relative importance of collagen fibril orientation and extent or type of crosslinking have yet to be determined.
BIOLOGIC RESPONSE TO THERMAL SHRINKAGE At present little information is available on the morphologic, ultrastructural, and biochemical changes that underlie the alterations in connective tissue mechanics resulting from thermal treatment. Some insight as to possible mechanisms involved may be gained from observations made after dermal burn injuries. In the burn zone cell death is inevitable, because most enzyme systems are inactivated at temperatures greater than 45°C, and proteins other than collagen are also denatured.35 Collagen in burned tissue also shows increased solubility and susceptibility to degradation by proteolytic enzymes.21 The local microvasculature also undergoes profound changes, which have been characterized into 3 zones: (1) coagulation, where all flow has ceased, (2) stasis, where there is partial occlusion of vessels caused by platelet aggregation, and (3) hyperemia, where there is initial vasoconstriction followed by a rebound increase in flow resulting from release of vasoactive mediators from damaged endothelial cells.8 The repair of a full-thickness skin burn has been well
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studied and follows a predictable sequence of reepithelialization, in-growth of granulation tissue, and contraction.45 Studies of the contraction process have shown clinically and experimentally that excision of a full-thickness burn enhances contraction and that treatment with partial-thickness grafts results in greater contraction than that with full-thickness grafts. Conversely, little contraction occurs after a freezing injury.32 These observations are consistent with the idea that the greater the quantity and quality are of matrix preserved after a thermal injury, the greater the inhibitory influence on the contraction process is. The lack of a contractile response may play a role in the “stretching out” of the ligamentous tissue seen in one in vivo model after laser thermal shrinkage.47 Histologic analysis of laser-treated tissues has generally concentrated on the changes in the first few weeks after surgery, and little information is available on longer term response. The extent of repair by scar formation is controversial. In a comparison of vascular anastomosis with the argon laser or conventional suture techniques, laser-treated tissue was found to have less evidence of inflammation, with minimal change in collagen content or synthesis after 4 weeks.65 In a porcine model of cutaneous resurfacing, Fitzpatrick et al15 assessed the tissue response from 2 days to 6 weeks and found that although dermal thickness was increased (which was attributed to thermal shrinkage of collagen), there was no evidence of scarring despite initial thermal necrosis. However, in human skin biopsy specimens assessed 90 days after laser surgery, a distinct “dermal repair zone” was seen with newly synthesized collagen and reorientation of elastin fibers.11 Furthermore, in a comparative study of wounds caused by either scalpel or laser, no difference was found in the expression of a range of growth factors in the acute phase after surgery, although in the lased wounds inflammatory cells appeared slightly earlier.66 In ligament tissue several short-term histologic studies provide some qualitative evidence for scar formation after laser thermal treatment. In a canine model in which thermal treatment was applied to the glenohumeral capsule with an arthroscopic technique, the authors found that the extent of thermal injury was difficult to control, resulting in some areas where full-thickness necrosis of the capsule occurred. At 6 weeks after surgery, there was marked synovitis, extensive fibrosis, and neovascularization, with a prominent inflammatory cell infiltrate in the thickened capsule.44 Similar changes were found in the rabbit knee capsule, with fibroblasts actively synthesizing new collagen matrix 30 days after laser treatment. It was concluded that the newly arrived fibroblasts used the acellular “hyalinized” collagen as a framework for migration and matrix synthesis.25 Electron microscopic analysis of these tissues has shown a high proportion of small-
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diameter (30 to 50 nm) collagen fibrils.47 Loss of the normal bimodal distribution of large- and small-diameter fibrils and replacement by a homogeneous population of small-diameter fibrils is typical of scar tissue.17 In a longer term report after laser thermal shrinkage, Hayashi et al22 found little histologic evidence of inflammation at any time point up to 180 days after surgery. Collagen fibrils assessed with transmission electron microscopy were “normal-looking” by 90 days. Although this was a purely qualitative assessment, the authors speculated that remodeling was mainly dependent on the residual population of fibroblasts. In another study from the same laboratory, biopsy specimens of human glenohumeral capsule were obtained from patients undergoing treatment for the contralateral shoulder between 3 and 38 months after the initial laser shrinkage procedure. No inflammation was seen in the specimens, although overall cellularity remained greater than normal, even after 3 years. The periodic “crimp” pattern of collagen fibers seen in normal ligaments began to reappear 12 months after surgery.24 There have been few direct comparisons of the effects of lasers with electrothermal energy on tissues. Previously, lasers have been compared with electrosurgery (cautery) in investigations of ablative properties. In fresh human menisci electrosurgical incisions produced a greater zone of residual thermal damage than a range of different lasers.52 Similar patterns were found in porcine palatal tissue.36 In a study using porcine skin, both the Nd-YAG laser and cautery created a similar depth of injury, but 60 days after treatment collagen concentration and synthesis were lower in the laser wound, leading the authors to conclude that the effects on collagen metabolism were different.9 However, in mechanical terms there may not be any particular advantage of one modality over the other. In the only report to date comparing the Hol:YAG laser with radiofrequency shrinkage, the acute reduction of glenohumeral translation in a cadaveric model was the same.58 A preliminary report of RF effects on joint capsular tissue has recently been presented.28 At 7 days after arthroscopic treatment of the ovine knee capsule, the extent of the lesion was found to be related to the magnitude of power delivery. The lesions were well circumscribed, with avascular necrotic centers of fused collagen fibrils surrounded by thrombotic vessels. There was a definite increase in vascularity and inflammation. It is interesting that in the higher-power lesions in which there was evidence of damage to underlying muscle, the synovial layer was preserved, suggesting that the arthroscopic irrigation fluid had some protective effect in moderating heat generation at the tissue surface.
CONCLUSIONS Capsular shrinkage induced by thermal denatura-
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tion of the collagen triple helix represents a novel development in the evolving management of shoulder instability. From the data available, both laser and radiofrequency electrical modalities appear to provide satisfactory modes of delivery; the clinical choice will be determined by practical issues such as availability, cost, safety concerns, and the ability to quantitatively control the extent of treatment. The latter factor deserves special consideration, because overzealous application of heat may be conducted to deeper planes, posing a risk to adjacent structures such as the axillary nerve. The acute shortening of ligament tissues that may be produced by the application of thermal energy in vitro is impressive, but the extent of shrinkage and outcome after recovery in vivo remains uncertain. Evidence from study of human tissues and from animal models suggests that normal capsule is significantly weakened and made more compliant immediately after treatment and may subsequently be remodeled by the in-growth of scar tissue at a new, shortened length. However, if this repair tissue stretches out under physiological loading conditions, the excess laxity may recur or may even be made worse. Fortunately, there seems to be potential for recovery of mechanical properties toward normal by approximately 12 weeks after surgery. Therefore from both basic science and clinical perspectives much remains to be done. To provide a more relevant clinical analog, the underlying pathologic condition of capsular laxity must be further investigated. The physiological, morphologic, and biochemical abnormalities that give rise to capsular laxity across the clinical spectrum from atraumatic multidirectional to post-traumatic unidirectional instability require definition. Once more information regarding these abnormalities is known, more appropriate in vivo models can be developed on which to evaluate new therapies such as thermal shrinkage. The biomechanical behavior of thermally treated ligament tissue under low “physiological” and high “failure” loads can then be ascertained at clinically relevant intervals and compared with existing data on healing ligaments. At the present time, thermal capsular shrinkage should be regarded as a developmental technique in the arthroscopic management of instability. It is conceivable that the final result might still be comparable to open surgical capsulorraphy, but prospective clinical studies with validated outcome measures are necessary to answer this question. Continued close collaboration between clinicians and research scientists will determine the precise role for thermal shrinkage in the armamentarium of the shoulder surgeon, with the ultimate goal of restoring stability with low morbidity and predictable early return of function for the patient with an unstable shoulder.
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21. Hambleton J, Shakespeare PG. Thermal damage to skin collagen. Burns 1991;17:209-12. 22. Hayashi K, Hecht P, Vanderby R, Peters DM, Cooley AJ, Xiang Z, et al. The long term effect of laser energy on joint capsular tissue. Trans Orth Res Soc 1998:1026. 23. Hayashi K, Markel MD, Thabit G, Bogdanske JJ, Thielke RJ. The effect of nonablative laser energy on joint capsular properties: an in vitro mechanical study using a rabbit model. Am J Sports Med 1995;23:482-7. 24. Hayashi K, Massa KL, Thabit G, Fanton GS, Dillingham MF, Gilchrist KW, Markel MD. Histologic evaluation of the glenohumeral joint capsule after the laser-assisted capsular shift procedure for glenohumeral instability. Am J Sports Med 1999;27:162-7. 25. Hayashi K, Nieckarz JA, Thabit G, Bogdanske JJ, Cooley AJ, Markel MD. Effect of nonablative laser energy on the joint capsule: an in vivo rabbit study using a holmium:YAG laser. Lasers Surg Med 1997;20:164-71(b). 26. Hayashi K, Thabit G, Bogdanske JJ, Mascio LN, Markel MD. The effect of nonablative laser energy on the ultrastructure of joint capsular collagen. Arthroscopy 1996;12:474-81. 27. Hayashi K, Thabit G, Massa KL, Bogdanske JJ, Cooley AJ, Orwin JF, Markel MD. The effect of thermal heating on the length and histologic properties of the glenohumeral joint capsule. Am J Sports Med 1997;25:107-12(a). 28. Hecht P, Hayashi K, Cooley AJ, Lu Y, Fanton GS, Thabit G, Markel MD. The thermal effect of radiofrequency energy on the properties of joint capsule: an in vivo study using a sheep model. Am J Sports Med 1998;26:808-14. 29. Horgan DJ, King NL, Kurth LB, Kuypers R. Collagen crosslinks and their relationship to the thermal properties of calf tendons. Arch Bioch Biophys 1990;281:21-6. 30. Kongsgaard E, Steen T, Jensen O, Aass H, Amlie J. Temperature guided radiofrequency catheter ablation of myocardium: comparison of catheter tip and tissue temperatures in vitro. PACE 1997;20:1252-60. 31. Kopchok G, White RA, Grundfest WS, Fujitani RM, Litvack F, Klein SR, White GH. Thermal studies of in-vivo vascular tissue fusion by argon laser. J Invest Surg 1988;1:5-12. 32. Li AKC, Ehrlich HP, Trelstad RL, Koroly MJ, Schattenkerk ME, Malt RA. Differences in healing of skin wounds caused by burn and freeze injuries. Ann Surg 1980;191:244-8. 33. Lopez MJ, Hayashi K, Fanton GS, Thabit G, Markel MD. The effect of radiofrequency energy on the ultrastructure of joint capsular collagen. Arthroscopy 1998;14:495-501. 34. Manta JP, Organ S, Nirschl RP, Pettrone FA. Arthroscopic transglenoid suture capsulolabral repair: five year followup. Am J Sports Med 1997;25:614-8. 35. Matylevitch NP, Schuschereba ST, Mata JR, Gilligan GR, Lawlor DF, Goodwin CW, Bowman PD. Apoptosis and accidental cell death in cultured human keratinocytes after thermal injury. Am J Pathol 1998;153:567-77. 36. Mausberg R, Visser H, Aschoff T, Donath K, Kruger W. Histology of laser- and high-frequency-electrosurgical incisions in the palate of pigs. J Craniomaxillofac Surg 1993;21:130-2. 37. Mirotznik MS, Schwartzman D. Nonuniform heating patterns of commercial electrodes for radiofrequency catheter ablation. J Cardiovasc Electrophysiol 1996;7:1058-62. 38. Nagy IZ, Toth VN, Verzar F. High-resolution electron microscopy of thermal collagen denaturation in tail tendons of young, adult and old rats. Connect Tiss Res 1974;2:265-72. 39. Nakagawa H, Yamanishi WS, Pitha JV, Arruda M, Wang X, Ohtomo K, et al. Comparison of in vivo tissue temperature profile and lesion geometry for radiofrequency ablation with a saline-irrigated electrode versus temperature control in a canine thigh muscle preparation. Circulation 1995;91:2264-73.
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