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Mechanical changes induced by thermal stimulation in collagenous tissue
Mechanical changes induced by thermal stimulation in collagenous tissue Joa˜o Ellera Gomes, MD, PhD,a Andre´ Kruel, MD,b and Luiz Marcelo Mu¨ller, MD,b Porto Alegre, Rio Grande do Sul, Brazil
Radiofrequency thermal stimulation is used as a therapeutic procedure for joint laxity, but its thermal effects are still controversial. Although collagen shrinkage may be expected, this conclusion is empirical and not universally accepted. The purpose of this study was to investigate the mechanical response of collagen to thermal stimulation. A longitudinal cut was made in rabbit Achilles tendons previously marked with monofilament sutures. The distance between the sutures was measured before the cut, just after it was made, and after 8 weeks. The results did not show any shrinkage or significant change in tendon resistance to traction 8 weeks after thermal stimulation; however, comparison with the opposite, normal tendon revealed a statistically significant increase in tendon stiffness. (J Shoulder Elbow Surg 2008;17:93S-95S.)
C
auterization of tendons and periarticular soft tissues to correct posttraumatic joint instability has been used since ancient times, as described in Hippocrates’ writings.1 Cauterization techniques to treat recurrent glenohumeral instability were commonly complicated by extensive tissue necrosis and, consequently, unacceptable degrees of infection, restriction of joint mobility, and marked esthetic impairment. Despite the high failure rate obtained by his predecessors, Hippocrates, using a more selective, biochemically better technique, successfully applied cauterization to the lower third of the glenohumeral joint in his patients with recurrent shoulder dislocation. The effects of heat on capsular and periarticular ligament collagen were first described a few decades ago.4-9,12,13 The heat sources currently used for ablation of collagen are laser and radiofrequency energy, which From the aSchool of Medicine, Universidade Federal do Rio Grande do Sul; bOrthopaedic surgeon, private practice. Reprint requests: Joa ˜ o Ellera Gomes, Universidade Federal do Rio Grande do Sul, Faculdade de Medicina, Departamento de Cirurgia, Rua Ramiro Barcelos, 2400 - 4 andar, CEP 90035-003 Porto Alegre, RS, Brazil (E-mail: [email protected]). Copyright ª 2008 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2008/$34.00 doi:10.1016/j.jse.2007.06.015
have different mechanisms of action. Laser produces thermal energy through absorption of light energy by the water content found in tissues, whereas the thermal energy produced by radiofrequency results from molecular friction caused by the rapid change in cell polarity.7,10,11 Despite the different mechanisms, Wallace et al14 and Osmond et al10 showed that the thermal effects of laser and radiofrequency energy on collagen are similar and that the choice of method should be determined by availability, cost, and operator experience. This study investigated the biomechanical changes caused by radiofrequency thermal stimulation applied to collagenous tissue. The effect of connective tissue thermal therapy on resistance to stress and elasticity was evaluated to determine its usefulness in joint stabilization. The objective of this study was to evaluate Achilles tendon resistance to stress in a rabbit model using radiofrequency energy thermal treatment of the longitudinal fibers and compare results with those obtained for the normal tendon. MATERIALS AND METHODS The study used 12 New Zealand White rabbits supplied by the same breeder. The animals were 4 to 6 months old, and their mean weight was 2.5 kg. The study was conducted in the Biological Research Institute of the Health and Environment State Department in the State of Rio Grande do Sul (Instituto de Pesquisas Biolo´gicas da Secretaria Estadual da Sau´de e do Meio Ambiente do Rio Grande do Sul), Brazil. Animal care followed ethical norms and animal experimentation legislation established by Brazilian Federal Law No. 6638, passed on May 8, 1979. The animals were anesthetized with 0.25-mg/mL atropine (0.05 mg subcutaneously) and preanesthetic medication, followed by anesthetic induction with 2% xylazine hydrochloride (2 mg/kg, deep intramuscularly) and 5% ketamine (50 mg/kg, deep intramuscularly). After antisepsis with 5% iodinated alcohol solution, the posterior aspect of the distal right hind leg was shaved. A posterior longitudinal incision was made over the Achilles tendon, followed by dissection of the subcutaneous tissue and isolation of the tendon. The Achilles tendon was chosen because it is longer and more flexible than knee collateral ligaments, so the possible shrinkage caused by thermal stimulation would be more easily measured.
93S
94S
Gomes, Kruel, and Mu¨ller
A 2-cm area of the distal tendon was demarcated with 2 nonabsorbable sutures and cauterized in the direction of the tendon fibers using an electrocautery device developed by the Biomedical Engineering Service (Servic¸o de Engenharia Biome´dica) of Hospital de Clı´nicas de Porto Alegre. Power was set at 100 W. The surgical field was then washed with saline, and the skin was sutured with monofilament nylon suture. The animals were monitored for 8 weeks and then were euthanized using an anesthetic overdose. Both hind legs were dissected, and the Achilles tendons were detached from their insertion on the calcaneus to their proximal musculotendinous junction. Specimens were divided into 2 groups: group 1—noncauterized, control tendons; and group 2—cauterized tendons. The distance between the monofilament, nonabsorbable sutures was measured again and compared with that recorded at the time of cauterization. The tendons were immediately submitted to stress test trials. They were fixed with metal pincers to a tension and compression-testing machine (K-1000, Kratos, New York, NY, USA) connected to a computer-controlled data acquisition system (AMD K5 133-MHz computer [Port Alegre, Brazil] with an Eagle [Cape Town, South Africa] data acquisition board). The software DIAdem 3.02 (GsFmbH, Aachen University, Germany) was used to generate graphs that were later exported to Excel 6.0 (Microsoft, Redmond, WA). Statistical analysis was conducted with the EpiInfo 6.03 software (Centers for Disease Control and Prevention, Atlanta, GA) using the Student t test and the Cohen criteria for effect size.2
RESULTS No significant differences were found in the measurements of the area between the monofilament nylon sutures at cauterization and at 8 weeks. The data in the load vs deformation graph obtained from the stress tests (Figure 1) provided the tendon rupture point (TRP), which represents the load (N) necessary for tendon rupture, and the tendon elasticity coefficient (TEC), calculated according to the curve slope in the area of elastic deformation (N/mm). The results described in Table I were obtained from Figure 1 for each group. Data are presented as mean 6 standard deviation. The tendon rupture point was not significantly different between groups. The elasticity coefficient, however, was statistically different between the groups, and the Cohen criteria for effect size revealed a great effect size between the difference of the elasticity coefficient means in the control and in the electrocautery groups, as the tendon elasticity coefficient shows below. Effect size ¼ Difference between group means/ mean standard deviation ¼ 7.0/7.55 ¼ 0.9. DISCUSSION The laxity of capsule and ligament structures and the consequent joint instability are difficult to resolve post-
J Shoulder Elbow Surg January/February 2008
Figure 1 Standard load versus deformation graph.
traumatic sequelae, even for an experienced orthopedist. The large number of surgical techniques reported in the literature reinforces the idea that the results of treatment of these tissues are not always as expected, and clinical outcomes can be unsatisfactory. Moreover, several of these techniques cause an initial weakening of these capsular and ligament structures, which requires the use of casts or braces for immobilization for long periods of time.6,8,15 However, if a technique could be developed in which retraction and connective tissue stiffness caused by accidental burns was controlled so that protective immobilization was not required, the therapeutic effect of localized and controlled burns of connective tissue theoretically could be used in the treatment of capsular and ligament laxity. Although our understanding of the mechanism of action of heat on connective tissue has improved, no measurable retraction has been observed in the progression of the healing process after planned burns.14 No increase in resistance to stress has been found that could be assigned to fibrous tissue in the development of scar tissue. At the same time, we found a significant reduction in the elasticity coefficient of tissues that undergo cauterization compared with contralateral controls.3,7 These findings do not provide evidence to support the hypothesis that the resistance to stress of the periarticular ligament and capsule is increased by cauterization alone.3,5,15 When increased resistance to stress has to be achieved, an additional technique will have to be used. We also have not found any evidence to support the inference that cauterization may resolve complaints of instability by decreasing joint amplitude through tissue retraction. Therefore, the only property achieved by cauterization, the decrease in capsular elasticity, only benefits patients with mild instability. In more
Gomes, Kruel, and Mu¨ller
J Shoulder Elbow Surg Volume 17, Number 1S
95S
Table I Achilles tendon rupture point and elasticity coefficient in New Zealand rabbits: comparison of results for electrocautery and control groups Properties
Control (n ¼ 12)
Electrocautery (n ¼ 12)
Difference
95% CI
P
TRP (N) TEC (N/mm)
181.4 6 40.6 21.4 6 7.6
163.8 6 57.9 14.4 6 7.5
17.7 7.0
24.6 to 60.0 0.6 to 13.4
.40 .03
CI, Confidence interval; TRP, tendon rupture point; TEC, elasticity coefficient.
severe cases, it will only work as a complementary procedure. Within these limitations, low-cost procedures that do not require implants may be developed if this method is systematized. The benefits of this therapeutic approach may be even greater and more relevant in developing countries, where high costs of modern medicine have a much greater social impact. Despite this potentially therapeutic use, our findings should be seen as a warning against the indiscriminate use of electrothermal shrinkage in orthopedic surgical procedures because its use may lead to unexpected damaging effects on connective tissue with postoperative joint stiffness. REFERENCES
1. Brockbank W, Griffiths DL. Orthopaedic surgery in the 16th and 17th centuries: 1. Luxations of the shoulder. J Bone Joint Surg 1948;30:365-75. 2. Cohen J. Statistical power analysis for the behavioral sciences. 7th ed. Mahwah, NJ: Lawrence Erlbaum Associates; 1988. 3. Hayashi K, Markel MD, Thabit G 3rd, Bogdanske JJ, Thielke RJ. The effect of nonablative laser energy on joint capsular properties: an in vivo mechanical study using a rabbit model. Am J Sports Med 1995;23:482-7. 4. Hayashi K, Thabit G 3rd, Massa KL, et al. The effect of thermal heating on the length and histologic properties of the glenohumeral joint capsule. Am J Sports Med 1997;25:107-12. 5. Hecht P, Hayashi K, Cooley AJ, et al. The thermal effect of monopolar radiofrequency energy on the properties of joint capsule. Am J Sports Med 1998;26:808-14.
6. Hecht P, Hayashi K, Lu Y, et al. Monopolar radiofrequency energy effects on joint capsular tissue: potential treatment for joint instability: an in vivo mechanical, morphological, and biomechanical study using an ovine model. Am J Sports Med 1999;27:761-71. 7. Ilhami K, Eray BM, Gokhan M, Ulukan I, Levent A. Comparative effects of monopolar radiofrequency energy and conservative management of mechanical properties of elongated lateral collateral ligament in rabbits: an experimental study. J Clin Biomech 2004;19:184-9. 8. Indelli PF, Dillingham MF, Fanton GS, Schurman DJ. Monopolar thermal treatment of symptomatic anterior cruciate ligament instability. Clin Orthop 2003;407:139-47. 9. Lopez MJ, Hayashi K, Vanderby R Jr, Thabit G 3rd, Fanton GS, Markel MD. Effects of monopolar radiofrequency energy on ovine joint capsular mechanical properties. Clin Orthop 2000;374: 286-97. 10. Osmond C, Hecht P, Hayashi K, et al. Comparative effects of laser and radiofrequency energy on joint capsule. Clin Orthop 2000; 375:286-94. 11. Selecky MT, Vangsness CT Jr, Liao WL, Saadat V, Hedman TP. The effects of laser-induced collagen shortening on the biomechanical properties of the inferior glenohumeral ligament complex. Am J Sports Med 1999;27:168-72. 12. Sherk HH. The use of lasers in orthopaedic procedures. J Bone Joint Surg Am 1993;75:768-76. 13. 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. 14. Wallace AL, Hollinshead RM, Frank CB. The scientific basis of thermal capsular shrinkage. J Shoulder Elbow Surg 2000;9: 354-60. 15. Wallace AL, Hollinshead RM, Frank CB. Electrothermal shrinkage reduces laxity but alters creep behavior in lapin ligament model. J Shoulder Elbow Surg 2001;10:1-6.
Radiofrequency thermal stimulation is used as a therapeutic procedure for joint laxity, but its thermal effects are still controversial. Although collagen shrinkage may be expected, this conclusion is empirical and not universally accepted. The purpose of this study was to investigate the mechanical response of collagen to thermal stimulation. A longitudinal cut was made in rabbit Achilles tendons previously marked with monofilament sutures. The distance between the sutures was measured before the cut, just after it was made, and after 8 weeks. The results did not show any shrinkage or significant change in tendon resistance to traction 8 weeks after thermal stimulation; however, comparison with the opposite, normal tendon revealed a statistically significant increase in tendon stiffness. (J Shoulder Elbow Surg 2008;17:93S-95S.)
C
auterization of tendons and periarticular soft tissues to correct posttraumatic joint instability has been used since ancient times, as described in Hippocrates’ writings.1 Cauterization techniques to treat recurrent glenohumeral instability were commonly complicated by extensive tissue necrosis and, consequently, unacceptable degrees of infection, restriction of joint mobility, and marked esthetic impairment. Despite the high failure rate obtained by his predecessors, Hippocrates, using a more selective, biochemically better technique, successfully applied cauterization to the lower third of the glenohumeral joint in his patients with recurrent shoulder dislocation. The effects of heat on capsular and periarticular ligament collagen were first described a few decades ago.4-9,12,13 The heat sources currently used for ablation of collagen are laser and radiofrequency energy, which From the aSchool of Medicine, Universidade Federal do Rio Grande do Sul; bOrthopaedic surgeon, private practice. Reprint requests: Joa ˜ o Ellera Gomes, Universidade Federal do Rio Grande do Sul, Faculdade de Medicina, Departamento de Cirurgia, Rua Ramiro Barcelos, 2400 - 4 andar, CEP 90035-003 Porto Alegre, RS, Brazil (E-mail: [email protected]). Copyright ª 2008 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2008/$34.00 doi:10.1016/j.jse.2007.06.015
have different mechanisms of action. Laser produces thermal energy through absorption of light energy by the water content found in tissues, whereas the thermal energy produced by radiofrequency results from molecular friction caused by the rapid change in cell polarity.7,10,11 Despite the different mechanisms, Wallace et al14 and Osmond et al10 showed that the thermal effects of laser and radiofrequency energy on collagen are similar and that the choice of method should be determined by availability, cost, and operator experience. This study investigated the biomechanical changes caused by radiofrequency thermal stimulation applied to collagenous tissue. The effect of connective tissue thermal therapy on resistance to stress and elasticity was evaluated to determine its usefulness in joint stabilization. The objective of this study was to evaluate Achilles tendon resistance to stress in a rabbit model using radiofrequency energy thermal treatment of the longitudinal fibers and compare results with those obtained for the normal tendon. MATERIALS AND METHODS The study used 12 New Zealand White rabbits supplied by the same breeder. The animals were 4 to 6 months old, and their mean weight was 2.5 kg. The study was conducted in the Biological Research Institute of the Health and Environment State Department in the State of Rio Grande do Sul (Instituto de Pesquisas Biolo´gicas da Secretaria Estadual da Sau´de e do Meio Ambiente do Rio Grande do Sul), Brazil. Animal care followed ethical norms and animal experimentation legislation established by Brazilian Federal Law No. 6638, passed on May 8, 1979. The animals were anesthetized with 0.25-mg/mL atropine (0.05 mg subcutaneously) and preanesthetic medication, followed by anesthetic induction with 2% xylazine hydrochloride (2 mg/kg, deep intramuscularly) and 5% ketamine (50 mg/kg, deep intramuscularly). After antisepsis with 5% iodinated alcohol solution, the posterior aspect of the distal right hind leg was shaved. A posterior longitudinal incision was made over the Achilles tendon, followed by dissection of the subcutaneous tissue and isolation of the tendon. The Achilles tendon was chosen because it is longer and more flexible than knee collateral ligaments, so the possible shrinkage caused by thermal stimulation would be more easily measured.
93S
94S
Gomes, Kruel, and Mu¨ller
A 2-cm area of the distal tendon was demarcated with 2 nonabsorbable sutures and cauterized in the direction of the tendon fibers using an electrocautery device developed by the Biomedical Engineering Service (Servic¸o de Engenharia Biome´dica) of Hospital de Clı´nicas de Porto Alegre. Power was set at 100 W. The surgical field was then washed with saline, and the skin was sutured with monofilament nylon suture. The animals were monitored for 8 weeks and then were euthanized using an anesthetic overdose. Both hind legs were dissected, and the Achilles tendons were detached from their insertion on the calcaneus to their proximal musculotendinous junction. Specimens were divided into 2 groups: group 1—noncauterized, control tendons; and group 2—cauterized tendons. The distance between the monofilament, nonabsorbable sutures was measured again and compared with that recorded at the time of cauterization. The tendons were immediately submitted to stress test trials. They were fixed with metal pincers to a tension and compression-testing machine (K-1000, Kratos, New York, NY, USA) connected to a computer-controlled data acquisition system (AMD K5 133-MHz computer [Port Alegre, Brazil] with an Eagle [Cape Town, South Africa] data acquisition board). The software DIAdem 3.02 (GsFmbH, Aachen University, Germany) was used to generate graphs that were later exported to Excel 6.0 (Microsoft, Redmond, WA). Statistical analysis was conducted with the EpiInfo 6.03 software (Centers for Disease Control and Prevention, Atlanta, GA) using the Student t test and the Cohen criteria for effect size.2
RESULTS No significant differences were found in the measurements of the area between the monofilament nylon sutures at cauterization and at 8 weeks. The data in the load vs deformation graph obtained from the stress tests (Figure 1) provided the tendon rupture point (TRP), which represents the load (N) necessary for tendon rupture, and the tendon elasticity coefficient (TEC), calculated according to the curve slope in the area of elastic deformation (N/mm). The results described in Table I were obtained from Figure 1 for each group. Data are presented as mean 6 standard deviation. The tendon rupture point was not significantly different between groups. The elasticity coefficient, however, was statistically different between the groups, and the Cohen criteria for effect size revealed a great effect size between the difference of the elasticity coefficient means in the control and in the electrocautery groups, as the tendon elasticity coefficient shows below. Effect size ¼ Difference between group means/ mean standard deviation ¼ 7.0/7.55 ¼ 0.9. DISCUSSION The laxity of capsule and ligament structures and the consequent joint instability are difficult to resolve post-
J Shoulder Elbow Surg January/February 2008
Figure 1 Standard load versus deformation graph.
traumatic sequelae, even for an experienced orthopedist. The large number of surgical techniques reported in the literature reinforces the idea that the results of treatment of these tissues are not always as expected, and clinical outcomes can be unsatisfactory. Moreover, several of these techniques cause an initial weakening of these capsular and ligament structures, which requires the use of casts or braces for immobilization for long periods of time.6,8,15 However, if a technique could be developed in which retraction and connective tissue stiffness caused by accidental burns was controlled so that protective immobilization was not required, the therapeutic effect of localized and controlled burns of connective tissue theoretically could be used in the treatment of capsular and ligament laxity. Although our understanding of the mechanism of action of heat on connective tissue has improved, no measurable retraction has been observed in the progression of the healing process after planned burns.14 No increase in resistance to stress has been found that could be assigned to fibrous tissue in the development of scar tissue. At the same time, we found a significant reduction in the elasticity coefficient of tissues that undergo cauterization compared with contralateral controls.3,7 These findings do not provide evidence to support the hypothesis that the resistance to stress of the periarticular ligament and capsule is increased by cauterization alone.3,5,15 When increased resistance to stress has to be achieved, an additional technique will have to be used. We also have not found any evidence to support the inference that cauterization may resolve complaints of instability by decreasing joint amplitude through tissue retraction. Therefore, the only property achieved by cauterization, the decrease in capsular elasticity, only benefits patients with mild instability. In more
Gomes, Kruel, and Mu¨ller
J Shoulder Elbow Surg Volume 17, Number 1S
95S
Table I Achilles tendon rupture point and elasticity coefficient in New Zealand rabbits: comparison of results for electrocautery and control groups Properties
Control (n ¼ 12)
Electrocautery (n ¼ 12)
Difference
95% CI
P
TRP (N) TEC (N/mm)
181.4 6 40.6 21.4 6 7.6
163.8 6 57.9 14.4 6 7.5
17.7 7.0
24.6 to 60.0 0.6 to 13.4
.40 .03
CI, Confidence interval; TRP, tendon rupture point; TEC, elasticity coefficient.
severe cases, it will only work as a complementary procedure. Within these limitations, low-cost procedures that do not require implants may be developed if this method is systematized. The benefits of this therapeutic approach may be even greater and more relevant in developing countries, where high costs of modern medicine have a much greater social impact. Despite this potentially therapeutic use, our findings should be seen as a warning against the indiscriminate use of electrothermal shrinkage in orthopedic surgical procedures because its use may lead to unexpected damaging effects on connective tissue with postoperative joint stiffness. REFERENCES
1. Brockbank W, Griffiths DL. Orthopaedic surgery in the 16th and 17th centuries: 1. Luxations of the shoulder. J Bone Joint Surg 1948;30:365-75. 2. Cohen J. Statistical power analysis for the behavioral sciences. 7th ed. Mahwah, NJ: Lawrence Erlbaum Associates; 1988. 3. Hayashi K, Markel MD, Thabit G 3rd, Bogdanske JJ, Thielke RJ. The effect of nonablative laser energy on joint capsular properties: an in vivo mechanical study using a rabbit model. Am J Sports Med 1995;23:482-7. 4. Hayashi K, Thabit G 3rd, Massa KL, et al. The effect of thermal heating on the length and histologic properties of the glenohumeral joint capsule. Am J Sports Med 1997;25:107-12. 5. Hecht P, Hayashi K, Cooley AJ, et al. The thermal effect of monopolar radiofrequency energy on the properties of joint capsule. Am J Sports Med 1998;26:808-14.
6. Hecht P, Hayashi K, Lu Y, et al. Monopolar radiofrequency energy effects on joint capsular tissue: potential treatment for joint instability: an in vivo mechanical, morphological, and biomechanical study using an ovine model. Am J Sports Med 1999;27:761-71. 7. Ilhami K, Eray BM, Gokhan M, Ulukan I, Levent A. Comparative effects of monopolar radiofrequency energy and conservative management of mechanical properties of elongated lateral collateral ligament in rabbits: an experimental study. J Clin Biomech 2004;19:184-9. 8. Indelli PF, Dillingham MF, Fanton GS, Schurman DJ. Monopolar thermal treatment of symptomatic anterior cruciate ligament instability. Clin Orthop 2003;407:139-47. 9. Lopez MJ, Hayashi K, Vanderby R Jr, Thabit G 3rd, Fanton GS, Markel MD. Effects of monopolar radiofrequency energy on ovine joint capsular mechanical properties. Clin Orthop 2000;374: 286-97. 10. Osmond C, Hecht P, Hayashi K, et al. Comparative effects of laser and radiofrequency energy on joint capsule. Clin Orthop 2000; 375:286-94. 11. Selecky MT, Vangsness CT Jr, Liao WL, Saadat V, Hedman TP. The effects of laser-induced collagen shortening on the biomechanical properties of the inferior glenohumeral ligament complex. Am J Sports Med 1999;27:168-72. 12. Sherk HH. The use of lasers in orthopaedic procedures. J Bone Joint Surg Am 1993;75:768-76. 13. 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. 14. Wallace AL, Hollinshead RM, Frank CB. The scientific basis of thermal capsular shrinkage. J Shoulder Elbow Surg 2000;9: 354-60. 15. Wallace AL, Hollinshead RM, Frank CB. Electrothermal shrinkage reduces laxity but alters creep behavior in lapin ligament model. J Shoulder Elbow Surg 2001;10:1-6.