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The effect of pulsed electromagnetic fields on flexor tendon healing in chickens
THE EFFECT OF PULSED ELECTROMAGNETIC FIELDS FLEXOR TENDON HEALING IN CHICKENS
ON
E. ROBOTTI, A. G. ZIMBLER, D. KENNA and J. A. I. GROSSMAN
From the Miami C7fildren's Hospital, Miami, USA
This study was designed as a pilot investigation of the effect of pulsed electromagnetic fields (PEMF) stimulation on early flexor tendon healing in a chicken model using a similar stimulus to that used clinically. The PEMF used caused a decrease in tensile strength and an increase in peritendinous adhesions.
Journal of Hand Surgery (British and European Volurne, 1999) 24B: 1:56-58 Pulsed electromagnetic fields (PEMF) delivered by opposing coils of wire mounted on the external surface of the skin have well-established clinical applications in the treatment of fracture nonunions and as a stimulus for bone healing (Bassett, 1985; De Haas et al., 1985; Downes and Watson, 1984; Dunn and Rush, 1984; Haupt, 1984; Wahlstrom, 1982). The external pulsing electromagnetic field bone growth system creates an electrical current within the bone by electromagnetic field induction (Bassett, 1985). Experimental evidence further suggests that both collagen producing cells and/or collagen itself may be affected by electromagnetic fields (Lee et al., 1993). Responses have been associated experimentally with a variety of soft tissues, including skin, tendon, and ligament (Black, 1985; Lee et al., 1993). The effect of electrical stimulation on soft-tissue is, however, still poorly understood. Studies have demonstrated some beneficial effects of electrotherapy in the healing of skin ulcers (Wolcott et al., 1969), ankle sprains (Wilson, 1972), rotator cuff tendinitis (Binder et al., 1984), and injured ligaments in rabbits (Frank et al., 1983). Pulsed electromagnetic field stimulation also appears to stimulate nerve regeneration in vivo and in vitro (Orgel et al., 1984; Sisken et al., 1989). This study was designed as a pilot investigation of the effect of PEMF on early flexor tendon healing in an established chicken model (Farkas et al., 1974). We were interested in finding out whether PEMF treatment could increase strength of the repaired tendons and whether such treatment would influence adhesion formation and range of motion.
extremity was immobilized by a plaster cast holding the central toe in its normal extended position and the adjacent toes in hyperextension. All animals received perioperative antibiotics. Initially, two groups of animals were studied. Group 1 consisted of animals with tendons repaired as described above. Group 2 consisted of animals with repaired tendons and a PEMF coil applied to the cast for 8 hours daily. A commercially available PEMF therapy unit was used to provide a standardized burst signal repeating at 15 Hz with 19 quasirectangular pulses per burst and a 5.1 msec burst duration. The peak amplitude was 12 mV in the positive direction and 4 mV in the negative direction. Using an inductive sensing probe, the field strength was estimated at 0.2 gauss. Animals were sacrificed at 3 weeks, and the tendons tested using an lnstron apparatus for tensile strength. Additionally, range of motion was measured by traction on the proximal end of the profundus tendon stump after disarticulation. Selected specimens were evaluated histologically. Subsequently, three additional control groups were studied. Group 3 consisted of unoperated casted extremities. Group 4 consisted of unoperated casted extremities that received PEMF therapy for 8 hours per day. Group 5 consisted of normal unoperated tendons. All data were analysed to obtain means, standard deviations, and significance determined by one-way analysis of variance. RESULTS
As might be expected, all operated tendons had significantly decreased breaking strength as compared to nonoperated tendons. Operated control tendons showed a breaking strength of 1.3 kg versus 0.6 kg (P<0.05) for tendons treated with PEMF stimulation (Table 1). Joint flexion at the three chicken toe joints were noted to be essentially the same in both the operated tendon groups, treated or not treated with PEMF (Table 2). Histology revealed no difference in collagen deposition or wound healing characteristics, although there appeared to be an increase in adhesions in PEMF treated operated animals.
MATERIALS AND M E T H O D S
The experimental model used the flexor profundus tendon of the central toe in adult White Leghorn chickens weighing 1100-1600 g. All animals were housed in individual cages with stable conditions and diet. Surgery was performed under ketamine anaesthesia supplemented by digital block using 1% xylocaine. Under loupe magnification, a midlateral incision was used to expose the flexor tendon sheath. The flexor tendon was isolated proximal to the proximal joint, sharply divided, stabilized with a Keith needle, and carefully repaired with a 5/0 nylon mattress suture. After wound closure, the 56
57
EFFECT OF PEMF ON FLEXOR TENDON HEALING
Table l--Breaking strength. Mean (SD) Group
Breaking strength (kg)
1
Operated, casted, n o P E M F
1.3 (0.15)
2
Operated, casted, P E M F
0.6 (0.04)
3
U n o p e r a t e d , casted, n o P E M F
8.4 (0.95)
4
U n o p e r a t e d , casted, P E M F
7.8 (0.80)
5
N o r m a l , untreated
7.8 (0.80)
Table 2 Joint Flexion. Mean (SD) Group
Joint 1
Joint 2
Joint 3
!
51 ° (2)
47 ° (2)
1° (0)
2
50 ° (2)
42 ° (2)
2 ° (0)
DISCUSSION This study examined the effect of a PEMF of particular configuration as an adjunctive therapy to surgical repair of tendons. No benefit, and possibly a small decrease in tensile strength, was observed in the PEMF treated group after 3 weeks of healing. The signal used was a pulsed-burst configuration that has been used with clinical success in the treatment of nonunions (Bassett, 1985; De Haas et al., 1985; Downes and Watson, 1984; Dunn and Rush, 1984; Haupt, 1984;) and has been shown to increase endochondral bone formation experimentally (Aaron et al., 1989). Other studies have demonstrated an increase in collagen synthesis by cultured fibroblasts (Lee et al., 1993) and an enhanced repair of ligaments and tendons in vivo in models treated with PEMF in vivo (Binder et al., 1984; Frank et al., 1983). Frank et al. (1983) demonstrated an increase in ligament healing at 3 weeks after surgical repair using a very low frequency field (1 Hz). Their study also demonstrated an increase in collagen content of the tissue treated with PEMF. In contrast, Watkins et al. (1985), demonstrated a significant delay in maturation of scar tissue in surgically created defects in equine flexor tendons, and a slightly detrimental effect on collagen composition. One difference between these studies and our own is that the gain in tensile strength was examined at different times. Clinically, a gain in tensile strength is important by 6 weeks following repair, and the value of any additional treatment should be seen by this time. Another important difference between these studies is the various types of the signals used. Signal frequencies have varied from 1 Hz to the megaherz range with field strengths varying by three orders of magnitude. These studies suggest that certain connective tissue cells will respond to a restricted frequency and amplitude range and that the biological response depends upon the position of cells in the cell cycle, the differentiation and activity of tissue, and the electromagnetic field. Clearly the optimum field
configurations for enhancing soft tissue repair have not yet been established and dose-response modalities are not yet understood. Neither the breaking strength nor the range of motion were improved by PEMF application. Direct application of ultrasound seems more promising than PEMF, at least in softening postoperative peritendinous adhesions (Stevenson et al., 1986). In a recent study using a chicken flexor tendon model, Gan et al. (1995) reported a 67% increase in range of motion over controls in animals treated by early application of ultrasound using a coupling gel. These animals showed no decrease in tensile strength. The signal used in this study is similar to that used to stimulate bone healing. There is a large volume of literature indicating that fracture nonunions may be successfully stimulated with a 15 Hz pulse burst signal. This signal has been studied extensively in an experimental model of endochondral bone formation and has been shown to increase collagen and proteoglycan synthesis and enhance cell differentiation in early bone formation. Most studies of the duration and exposure to stimulation indicate that it is most effective when applied for 8 hours over a 3-week period. Our study indicated that this signal had no effect on tendon repair, lending further support to the concept of signal specificity of PEME The frequency and amplitude of PEMF for improving tendon repair appear to be different from those for endochondral bone formation. References Aaron RK, Ciombor DM, Jolly G (1989). Stimulation of experimental endochondral ossification by low-energy pulsing electromagnetic fields. Journal of Bone and Mineral Research, 4:227 233. Bassett CAL (1985). The development and application of pulsed electromagnetic fields (PEMFs) for ununited fractures and arthrodeses. Clinics in Plastic Surgery, 12: 259-277. Binder A, Parr G, Hasleman B, Fitton-Jackson S (1984). Pulsed electromagnetic field therapy of persistent rotator cuff tendinitis. Lancet, 1: 695 698. Black J (1985). Electrical stimulation of hard and soft tissues in animal models. Clinics in Plastic Surgery, 12: 243-257. De Haas WG, Beaupre A, Cameron H, English E (1985). The Canadian experience with pulsed magnetic fields in the treatment of ununited tibial fractures. Clinical Orthopaedics and Related Research, 208: 55-58. Downes EM, Watson J (1984). Development of the iron-cored electromagnet for the treatment of non-union and delayed union. Journal of Bone and Joint Surgery British, 66B: 754-759. Dunn AW, Rush GA (1984). Electrical stimulation in the treatment of delayed union and nonunion of fractures and osteotomies. Southern Medical Journal, 77: 1530-1534. Farkas LF, Thomson HG, Martin R (1974). Some practical notes on the anatomy of the chicken toe for surgeon investigators. Plastic and Reconstructive Surgery, 54: 452458. Frank C, Schachar N, Dittrich D, Shrive N, Phil D, deHaas W, Edwards G (1983). Electromagnetic stimulation of ligament healing in rabbits. Clinical Orthopaedics and Related Research, 175:263 272. Gan BS. Huys S, Sherebrin MH, Scilley CG (1995). The effects of ultrasound treatment on flexor tendon healing in the chicken limb. Journal of Hand Surgery, 20B: 809 814. Haupt HA (1984). Electrical stimulation of osteogenesis. Southern Medical Journal, 77: 56-64. Lee RC, Canaday DJ, Doong H (1993). A review of the biophysical basis for the clinical application of electric fields in soft-tissue repair. Journal of Burn Care and Rehabilitation, 14: 319-335. Orgel MG, O'Brien WJ, Murray HM (1984). Pulsing electromagnetic field therapy in nerve regeneration: an experimental study in the cat. Plastic and Reconstructive Surgery, 73:173 183. Sisken BF, Kanje M, Lundborg G, Kurtz W (1989). Stimulation of rat sciatic
58 nerve regeneration with pulsed electromagnetic fields. Brain Research, 485: 309-316. Stevenson JH, Pang CY, Lindsay WK, Zuker RM (1986). Functional, mechanical and biochemical assessment of ultrasound therapy on tendon healing in the chicken toe. Plastic and Reconstructive Surgery. 77: 965--972. Wahlstrom O (1982). Stimulation of fracture healing with electromagnetic fields of extremely low frequency (EMF of ELF). Clinical Orthopaedics and Related Research, 186:293 301. Watkins JR Auer JA, Morgan SL Gay S (1985). Healing of surgically created defects in the equine superficial digital flexor tendon: effects of pulsing electromagnetic field therapy on collagen-type transformation and tissue morphologic reorganization. American Journal of Veterinary Research, 46:2097 2103.
THE J O U R N A L OF H A N D SURGERY VOL. 24B No. l FEBRUARY 1999 Wilson DH (1972). Treatment of soft4tissue injuries by pulsed electrical energy. British Medical Journal, 2:269 270. Wolcott LE, Wheeler PC, Hardwicke HM, Rowley BA (1969). Accelerated healing of skin ulcers by electrotherapy. Southern Medical Journal, 62: 795 80I.
Received: 9 March 1998 Accepted after revision: 13 July 1998 J. A, I. Grossmann MD FACS, 8940 N. Kendall Drive, Suite # 904E, Miami, Florida 33176, USA. ~', 1999The British Society for Surgery of Ihe Hand Article no. jhsb. 1998.0027
ON
E. ROBOTTI, A. G. ZIMBLER, D. KENNA and J. A. I. GROSSMAN
From the Miami C7fildren's Hospital, Miami, USA
This study was designed as a pilot investigation of the effect of pulsed electromagnetic fields (PEMF) stimulation on early flexor tendon healing in a chicken model using a similar stimulus to that used clinically. The PEMF used caused a decrease in tensile strength and an increase in peritendinous adhesions.
Journal of Hand Surgery (British and European Volurne, 1999) 24B: 1:56-58 Pulsed electromagnetic fields (PEMF) delivered by opposing coils of wire mounted on the external surface of the skin have well-established clinical applications in the treatment of fracture nonunions and as a stimulus for bone healing (Bassett, 1985; De Haas et al., 1985; Downes and Watson, 1984; Dunn and Rush, 1984; Haupt, 1984; Wahlstrom, 1982). The external pulsing electromagnetic field bone growth system creates an electrical current within the bone by electromagnetic field induction (Bassett, 1985). Experimental evidence further suggests that both collagen producing cells and/or collagen itself may be affected by electromagnetic fields (Lee et al., 1993). Responses have been associated experimentally with a variety of soft tissues, including skin, tendon, and ligament (Black, 1985; Lee et al., 1993). The effect of electrical stimulation on soft-tissue is, however, still poorly understood. Studies have demonstrated some beneficial effects of electrotherapy in the healing of skin ulcers (Wolcott et al., 1969), ankle sprains (Wilson, 1972), rotator cuff tendinitis (Binder et al., 1984), and injured ligaments in rabbits (Frank et al., 1983). Pulsed electromagnetic field stimulation also appears to stimulate nerve regeneration in vivo and in vitro (Orgel et al., 1984; Sisken et al., 1989). This study was designed as a pilot investigation of the effect of PEMF on early flexor tendon healing in an established chicken model (Farkas et al., 1974). We were interested in finding out whether PEMF treatment could increase strength of the repaired tendons and whether such treatment would influence adhesion formation and range of motion.
extremity was immobilized by a plaster cast holding the central toe in its normal extended position and the adjacent toes in hyperextension. All animals received perioperative antibiotics. Initially, two groups of animals were studied. Group 1 consisted of animals with tendons repaired as described above. Group 2 consisted of animals with repaired tendons and a PEMF coil applied to the cast for 8 hours daily. A commercially available PEMF therapy unit was used to provide a standardized burst signal repeating at 15 Hz with 19 quasirectangular pulses per burst and a 5.1 msec burst duration. The peak amplitude was 12 mV in the positive direction and 4 mV in the negative direction. Using an inductive sensing probe, the field strength was estimated at 0.2 gauss. Animals were sacrificed at 3 weeks, and the tendons tested using an lnstron apparatus for tensile strength. Additionally, range of motion was measured by traction on the proximal end of the profundus tendon stump after disarticulation. Selected specimens were evaluated histologically. Subsequently, three additional control groups were studied. Group 3 consisted of unoperated casted extremities. Group 4 consisted of unoperated casted extremities that received PEMF therapy for 8 hours per day. Group 5 consisted of normal unoperated tendons. All data were analysed to obtain means, standard deviations, and significance determined by one-way analysis of variance. RESULTS
As might be expected, all operated tendons had significantly decreased breaking strength as compared to nonoperated tendons. Operated control tendons showed a breaking strength of 1.3 kg versus 0.6 kg (P<0.05) for tendons treated with PEMF stimulation (Table 1). Joint flexion at the three chicken toe joints were noted to be essentially the same in both the operated tendon groups, treated or not treated with PEMF (Table 2). Histology revealed no difference in collagen deposition or wound healing characteristics, although there appeared to be an increase in adhesions in PEMF treated operated animals.
MATERIALS AND M E T H O D S
The experimental model used the flexor profundus tendon of the central toe in adult White Leghorn chickens weighing 1100-1600 g. All animals were housed in individual cages with stable conditions and diet. Surgery was performed under ketamine anaesthesia supplemented by digital block using 1% xylocaine. Under loupe magnification, a midlateral incision was used to expose the flexor tendon sheath. The flexor tendon was isolated proximal to the proximal joint, sharply divided, stabilized with a Keith needle, and carefully repaired with a 5/0 nylon mattress suture. After wound closure, the 56
57
EFFECT OF PEMF ON FLEXOR TENDON HEALING
Table l--Breaking strength. Mean (SD) Group
Breaking strength (kg)
1
Operated, casted, n o P E M F
1.3 (0.15)
2
Operated, casted, P E M F
0.6 (0.04)
3
U n o p e r a t e d , casted, n o P E M F
8.4 (0.95)
4
U n o p e r a t e d , casted, P E M F
7.8 (0.80)
5
N o r m a l , untreated
7.8 (0.80)
Table 2 Joint Flexion. Mean (SD) Group
Joint 1
Joint 2
Joint 3
!
51 ° (2)
47 ° (2)
1° (0)
2
50 ° (2)
42 ° (2)
2 ° (0)
DISCUSSION This study examined the effect of a PEMF of particular configuration as an adjunctive therapy to surgical repair of tendons. No benefit, and possibly a small decrease in tensile strength, was observed in the PEMF treated group after 3 weeks of healing. The signal used was a pulsed-burst configuration that has been used with clinical success in the treatment of nonunions (Bassett, 1985; De Haas et al., 1985; Downes and Watson, 1984; Dunn and Rush, 1984; Haupt, 1984;) and has been shown to increase endochondral bone formation experimentally (Aaron et al., 1989). Other studies have demonstrated an increase in collagen synthesis by cultured fibroblasts (Lee et al., 1993) and an enhanced repair of ligaments and tendons in vivo in models treated with PEMF in vivo (Binder et al., 1984; Frank et al., 1983). Frank et al. (1983) demonstrated an increase in ligament healing at 3 weeks after surgical repair using a very low frequency field (1 Hz). Their study also demonstrated an increase in collagen content of the tissue treated with PEMF. In contrast, Watkins et al. (1985), demonstrated a significant delay in maturation of scar tissue in surgically created defects in equine flexor tendons, and a slightly detrimental effect on collagen composition. One difference between these studies and our own is that the gain in tensile strength was examined at different times. Clinically, a gain in tensile strength is important by 6 weeks following repair, and the value of any additional treatment should be seen by this time. Another important difference between these studies is the various types of the signals used. Signal frequencies have varied from 1 Hz to the megaherz range with field strengths varying by three orders of magnitude. These studies suggest that certain connective tissue cells will respond to a restricted frequency and amplitude range and that the biological response depends upon the position of cells in the cell cycle, the differentiation and activity of tissue, and the electromagnetic field. Clearly the optimum field
configurations for enhancing soft tissue repair have not yet been established and dose-response modalities are not yet understood. Neither the breaking strength nor the range of motion were improved by PEMF application. Direct application of ultrasound seems more promising than PEMF, at least in softening postoperative peritendinous adhesions (Stevenson et al., 1986). In a recent study using a chicken flexor tendon model, Gan et al. (1995) reported a 67% increase in range of motion over controls in animals treated by early application of ultrasound using a coupling gel. These animals showed no decrease in tensile strength. The signal used in this study is similar to that used to stimulate bone healing. There is a large volume of literature indicating that fracture nonunions may be successfully stimulated with a 15 Hz pulse burst signal. This signal has been studied extensively in an experimental model of endochondral bone formation and has been shown to increase collagen and proteoglycan synthesis and enhance cell differentiation in early bone formation. Most studies of the duration and exposure to stimulation indicate that it is most effective when applied for 8 hours over a 3-week period. Our study indicated that this signal had no effect on tendon repair, lending further support to the concept of signal specificity of PEME The frequency and amplitude of PEMF for improving tendon repair appear to be different from those for endochondral bone formation. References Aaron RK, Ciombor DM, Jolly G (1989). Stimulation of experimental endochondral ossification by low-energy pulsing electromagnetic fields. Journal of Bone and Mineral Research, 4:227 233. Bassett CAL (1985). The development and application of pulsed electromagnetic fields (PEMFs) for ununited fractures and arthrodeses. Clinics in Plastic Surgery, 12: 259-277. Binder A, Parr G, Hasleman B, Fitton-Jackson S (1984). Pulsed electromagnetic field therapy of persistent rotator cuff tendinitis. Lancet, 1: 695 698. Black J (1985). Electrical stimulation of hard and soft tissues in animal models. Clinics in Plastic Surgery, 12: 243-257. De Haas WG, Beaupre A, Cameron H, English E (1985). The Canadian experience with pulsed magnetic fields in the treatment of ununited tibial fractures. Clinical Orthopaedics and Related Research, 208: 55-58. Downes EM, Watson J (1984). Development of the iron-cored electromagnet for the treatment of non-union and delayed union. Journal of Bone and Joint Surgery British, 66B: 754-759. Dunn AW, Rush GA (1984). Electrical stimulation in the treatment of delayed union and nonunion of fractures and osteotomies. Southern Medical Journal, 77: 1530-1534. Farkas LF, Thomson HG, Martin R (1974). Some practical notes on the anatomy of the chicken toe for surgeon investigators. Plastic and Reconstructive Surgery, 54: 452458. Frank C, Schachar N, Dittrich D, Shrive N, Phil D, deHaas W, Edwards G (1983). Electromagnetic stimulation of ligament healing in rabbits. Clinical Orthopaedics and Related Research, 175:263 272. Gan BS. Huys S, Sherebrin MH, Scilley CG (1995). The effects of ultrasound treatment on flexor tendon healing in the chicken limb. Journal of Hand Surgery, 20B: 809 814. Haupt HA (1984). Electrical stimulation of osteogenesis. Southern Medical Journal, 77: 56-64. Lee RC, Canaday DJ, Doong H (1993). A review of the biophysical basis for the clinical application of electric fields in soft-tissue repair. Journal of Burn Care and Rehabilitation, 14: 319-335. Orgel MG, O'Brien WJ, Murray HM (1984). Pulsing electromagnetic field therapy in nerve regeneration: an experimental study in the cat. Plastic and Reconstructive Surgery, 73:173 183. Sisken BF, Kanje M, Lundborg G, Kurtz W (1989). Stimulation of rat sciatic
58 nerve regeneration with pulsed electromagnetic fields. Brain Research, 485: 309-316. Stevenson JH, Pang CY, Lindsay WK, Zuker RM (1986). Functional, mechanical and biochemical assessment of ultrasound therapy on tendon healing in the chicken toe. Plastic and Reconstructive Surgery. 77: 965--972. Wahlstrom O (1982). Stimulation of fracture healing with electromagnetic fields of extremely low frequency (EMF of ELF). Clinical Orthopaedics and Related Research, 186:293 301. Watkins JR Auer JA, Morgan SL Gay S (1985). Healing of surgically created defects in the equine superficial digital flexor tendon: effects of pulsing electromagnetic field therapy on collagen-type transformation and tissue morphologic reorganization. American Journal of Veterinary Research, 46:2097 2103.
THE J O U R N A L OF H A N D SURGERY VOL. 24B No. l FEBRUARY 1999 Wilson DH (1972). Treatment of soft4tissue injuries by pulsed electrical energy. British Medical Journal, 2:269 270. Wolcott LE, Wheeler PC, Hardwicke HM, Rowley BA (1969). Accelerated healing of skin ulcers by electrotherapy. Southern Medical Journal, 62: 795 80I.
Received: 9 March 1998 Accepted after revision: 13 July 1998 J. A, I. Grossmann MD FACS, 8940 N. Kendall Drive, Suite # 904E, Miami, Florida 33176, USA. ~', 1999The British Society for Surgery of Ihe Hand Article no. jhsb. 1998.0027