By Darrell Brooks, MD
In 1970 Tamai1 transplanted the biceps brachii and rectus femoris muscles from the hind limb to the contralateral hind limb in a dog along with an artery, vein, and motor nerve repair. Four months after transplantation and microneurovascular repair, early degenerative changes and fibrillation potentials were replaced by normal muscle architecture and M-wave potentials consistent with healthy functioning neuromuscular units. From this seminal scientific study, reconstructive surgeons were able to envision muscle transplantation for restoration of function and not simply for provision of soft tissue coverage. Since then, experimental2-5 and clinical6-10 studies have combined to make functional microvascular muscle transplantation (FMMT) a reliable technique in reconstructive surgery of the extremities and in facial reanimation.
Muscle groups in the arms and legs work in a synergistic fashion to perform specific motions such as extension or flexion across a joint. When all muscles in a synergistic group are denervated or destroyed, motion is lost. When available, tendons can be transferred (tendon transfer) from an adjacent muscle compartment to restore lost function. When local muscles are also affected, as in limb replantation, or when major soft tissue or major nerve crush/avulsion injury is present, a functional microvascular muscle transplant can be utilized to overcome the barriers presented by extensive injury.
Our approach to muscle transplantation to restore function is based on the work of the other major microsurgical centers in the world as well as the evolution of our clinical experience and research. The goal of FMMTs is to restore active motion and satisfy a patient's particular functional need. To be successful, this requires that certain criteria be met:
Criteria for the microsurgeon:
Criteria for appropriate patient selection:
Selection of appropriate donor muscle:
depends on the circumstance for which it is being used. The functional muscle can be transplanted acutely for non-traumatic muscle deficits after Volkmann's ischemic contracture11,12 and compartmental surgical resection for malignant tumors.13-14 In these situations, the zone of injury is limited. However, functional muscle transplantation must be staged in situations where patients have sustained traumatic loss. These include muscle compartment destruction after limb amputation, mechanical crush/avulsion, and major nerve avulsion. In these situations, the wound is dynamic and can be characterized by infection or ongoing muscle/nerve demarcation. Because of this, intervention is usually separated into acute, sub acute, and late - each with specific goals.
The acute period can be defined as the time of injury until the initial effects of the trauma such as limb compromise and open wounds with exposure of vital structures have been addressed. The goal in this period is to revascularize the limb, provide stabilization or skeletal support, and provide stable coverage of the wounds. Of course the first priority is saving the patient's life. Only after that has been addressed should attention be directed towards salvage of a limb.
Limb salvage can begin with either revascularization or bony stabilization. Despite advances in microsurgical technique, prolonged tissue ischemia is a contraindication to replantation and a concern in revascularization. Upon return of blood flow, ischemic tissue generates toxins, which can threaten the replanted or revascularized tissue and even the patient. This is referred to as "re-perfusion syndrome".15,16 The duration of ischemia that tissue will tolerate is dependent on the amount of muscle present. Muscle has a much higher metabolic requirement and is therefore much more sensitive to ischemia. Multiple studies have shown that lowering the metabolic requirement by hypothermic ischemia protects it from enzyme leakage, histologic changes, and adverse re-flow patterns. This protection is limited to 4-5 hours if ischemia is normothermic (body temperature) and 8-10 hours if hypothermic. Surviving muscle will have greater return of function the shorter the ischemic period. Tissues close to their ischemic limit can have vascular shunts placed initially so that the limb can perfuse while time consuming procedures such as bony reduction and stabilization are being undertaken. Thereafter, vein grafts to the inflow artery and outflow vein can be done. Testing the venous blood prior to vein repair has been reported as a way to reduce or prevent reperfusion syndrome.17 An implantable doppler is then placed to monitor the patency of this vascular circuit.
Once blood flow has been reestablished all tissues are inspected for reperfusion injury or non-viable elements. Compartments can be opened (fasciotomy) to allow for muscle swelling and decrease progressive muscle loss. Serial debridements continue until the wound is clean. Vascular tissue such as muscle can be transplanted to close the wound, cover vital structures and decrease infection risk.18 Grafts to damaged structures such as nerve, bone, and tendon should be deferred until control of the wound is achieved.
The sub acute period begins after limb salvage, stable cover has been provided, and there is no evidence of infection. At that point, the patient can be returned to the operating room where structures not repaired acutely can be addressed. In certain injuries, there is loss of bone from comminution, and nerve, or muscle from crush/avulsion. In these situations, nerve gaps can be grafted to restore sensation/motor function or offer a target for muscle transplantation, and stabilized bone defects can be grafted. If the bone has been shortened, the Ilizarov distraction technique can be employed to lengthen the residual bone. Ulnar or median nerve grafting should be performed as early as possible (usually within 3 weeks) to restore sensation and salvage the intrinsic muscles of the hand.
After the sub-acute period, a rehabilitation protocol is instituted to optimize return of function. This can require up to one year. Regular exams through this period identify what function has returned and what is lost. Only with this understanding can the appropriate strategy for reconstruction be formulated. After conservative approaches have been exhausted and functional deficiencies persist, a FMMT can be considered. One or more FMMTs can be transplanted to restore function. Each requires a nutrient vessel and a healthy motor nerve. An angiogram can be used to determine the adequacy of the target vessel. Assessment of the adequacy of the motor nerve target is difficult prior to surgical exploration. Fascicles usually sprout from the proximal nerve stump to form a neuroma by the third week after nerve injury. At this time exploration can reveal a neuroma and help define the appropriate nerve level.19,20 The vessel and nerve, which supplied the original muscle group, should be used preferentially. If the original vessel cannot be utilized, vein can be harvested and grafted to supply blood flow to the transplant. If the original nerve cannot be utilized, a nerve can be borrowed from another muscle group. The nerve selected should not result in significant disability and must have a similar function to that which it is replacing or be under voluntary control such that the patient can relearn and control that function.
Several muscles potentially meet the criteria for FMMT. The most commonly used muscles include the gracilis, latissimus, rectus femoris, and the tensor fascia lata (TFL) muscles. The muscle selected should offer the strength required to restore a desired function and a contractile excursion longer than that of the muscle or muscles it is replacing.21,22 The gracilis and latissimus muscles are strap muscles meaning that their muscle fibers are arranged longitudinal to their direction of contraction. These muscles usually shorten between 40 to 60% of their stretched length. In the case of a 30 cm gracilis muscle, that would be at least 12 cm of excursion. Finger range of motion requires 6-7 cm of excursion. The rectus femoris and TFL muscles are bipennate muscles meaning that their fibers are oriented at an angle to the direction of muscle contraction. They shorten 40% of their average fascicule length. Because of their fascicular orientation and the fact that they are shorter, maximum excursion is limited to about 3cm. Muscle strength is proportional to the cross sectional area of the muscle. Therefore, the bipennate transplants provide increased strength but sacrifice excursion or range of motion.
The gracilis muscle is most often used as a FMMT. Its size, length, and shape most closely approximates that of the muscles, which provide flexion and extension in the hand, flexion at the elbow, as well as, dorsiflexion at the ankle. The latissimus muscle
is an excellent alternative to the gracilis. It has excellent excursion and strength. However, it is bulkier than the gracilis muscle, fans out at its distal insertion, and does not have a distal tendon for weave or repair making it technically more difficult to apply to the forearm and lower leg. However, we prefer its use in restoration of function in the anterior and posterior compartments of the thigh for restoration of function at the knee.
Even when care is taken to follow a specific algorithm functional muscle transplanted for traumatic injuries is less reliable. The poor quality of the recipient bed and motor nerve are believed to be responsible. Techniques to optimize the wound bed and motor nerve are being employed with success in our clinic.
Facial paralysis can result from mutiple causes, most commonly from trauma, congenital malformation, tumor resection or Bell's palsy. Early diagnosis is important, to rule out correctible causes and to act before facial muscle degeneration. In children, elective reconstruction can be considered after 2 years of age. Facial reanimation is covered in detail here.
When an arm is replanted care is taken to return all structures to their normal positions and then repair them. Often, depending on the mechanism of amputation additional vascularized tissue is needed to provide soft tissue cover of vital structures. Unfortunately, this does not result in adequate function is all cases.
Limb amputation obviously involves all muscle compartments at the level of injury. Because of this, local muscles are not always appropriate for transfer. One option available for patients with upper arm replantation and loss of elbow flexion is distant muscle transfer. If available, the ipsilateral latissimus muscle can be transferred from the back onto the arm to restore elbow flexion. No vessel or nerve repair is required in this situation. When this is not an option or when function is lost below the elbow, a muscle has to be transplanted with microneurovascular anastomosis to restore function.
FMMTs can be used to restore elbow flexion, wrist extension, wrist flexion, finger extension, finger flexion or a combination thereof. Even if the FMMT is successful in the upper extremity replant, injury to the ulnar nerve often dictates the ultimate functional return of the hand. If the ulnar nerve is irreparable, additional surgeries will be required to rebalance the hand. Review ulnar nerve palsy for details.
Synergistic muscle compartments can be mechanically lost secondary to traumatic crush/avulsion, Volkmann's ischemic contracture, or after surgical resection for malignant tumors. Acute care for these injuries entails bony stabilization, revascularization, and possible compartment release or fasciotomy. Given the nature of the injury, serial debridement is necessary until all questionable tissue is removed. Grafting of nerve or bone is deferred until control of the wound. Often vascularized tissues need to be transplanted to accomplish this.
When the wounds are healed and FMMT criteria are met, a functional muscle can be transplanted to restore active motion across the joints of the upper and lower extremities.
Major peripheral nerve injury will result in loss of synergistic muscle function. The first approach is primary nerve repair or nerve grafting. When this is not possible, or repair has failed and resultant muscle atrophy has occurred, a FMMT can be employed.
Common examples include brachial plexus or common peroneal nerve injury. Surgical intervention such as nerve exploration and repair or grafting has resulted in less than optimal restoration of function. The reason for this is unclear. However, it is believed that their "mixed" sensory and motor character results in fascicle mismatching. Specific nerve stains have been employed to identify the motor component for transplant innervation.23 The gracilis transplant to the anterior compartment has restored foot dorsiflexion and the ability to walk without dependence on ankle splints in a selected group of our patients.
Patients with devastating injuries to their upper and lower extremities should be evaluated by a reconstructive microsurgeon as well as a prosthetist. A complete understanding of the functional potential provided by each must be understood before embarking on either. In selected patients functional microvascular muscle transplants can restore function and allow patients to return to their daily activities.
1. Tamai S. Free muscle transplantation in dogs with microsurgical neurovascular anastomoses. Plast Reconstr Surg 1970;46:219-225.
2. Terzis J K, Sweet R C, Dykes R W, Williams H B. Recovery of function in free muscle transplants using microvascular anastomoses. Hand 1987;3:37.
3. Zalewski A A. Effects of reinnervation on denervated skeletal muscle by axons of motor, sensory, and sympathetic neurons. Am J Physiol 1970;219:1675.
4. Sorbie C, Porter T L. Reinnervation of paralysed muscles by direct motor nerve implantation: an experimental study in the dog. J Bone Joint Surg 1969;51B:156.
5. Kanaya F, Tajima T. Effect of electrostimulation on denervated muscle. Clin Orthop 1992;283:296.
6. Manktelow R T, Zuker M, McKee N H. Functioning free muscle transplantation. J Hand Surg 1984;9A:32-39.
7. McKee NH, Kuzon WM. Functioning free muscle: Making it work? What is known? Ann Plast Surg 1989;23:249-254.
8. Manktelow RT, Zucker RM. The principles of functional muscle transplantation: applications to the upper arm. Ann Plast Surg 1989;22:275-282.
9. Doi K, Sakai K, Ihara K, et al. Reinnervated free muscle transplantation for extremity reconstruction. Plast Reconstr Surg 1993;91:872-883.
10. Chuang DCC. Functioning free muscle transplantation for the upper extremity. Hand Clin 1997;13:279-289.
11. Zuker R M, Egerzegi E P, Manktelow R T, McLeod A, Candlish S. Volkmann's ischemic contracture in children: the results of free vascularized muscle transplantation. Microsurgery 1991;12:341-345.
12. Ikuta Y, Kubo T, Tsuge K. Free muscle transplantation by microvascular technique to treat severe Volkmann's contracture. Plast Reconstr Surg. 1976;53:407-411.
13. Doi K, Kuwata N, Kawakami F, Hattori Y, Otsuka K, Ihara K. Limb-sparing surgery with reinnervated free muscle transfer following radial escision of soft tissue sarcoma in the extremity. Plast Reconstr Surg 1999;104:1679-1688.
14. Ihara K, Shigetomi M, Kawai S, Doi K, Yamamoto M. Functioning muscle transplantation after wide excision of sarcomas in the extremity. Clin Orthop 1999;358:140-148.
15. al-Qattan, M.N., Ischemia-reperfusion injury. Implications for the hand surgeon. J Hand Surg [Br], Oct;23(5):570-3, 1998
16. Usui M, Ishii S, Muramatsu I, Takahata N. An experimental study on "replantation toxemia". The effect of hypothermia on an amputated limb. J Hand Surg [Am]. 1978 Nov;3(6):589-96.
17. Waikakul S, Vanadurongwan V, Unnanuntana A. Prognostic factors for major limb re-implantation at both immediate and long-term follow-up. J Bone Joint Surg Br. 1998 Nov;80(6):1024-30.
18. Chuang DCC, Lai JB, Cheng SL, Jain V, Lin CH, Chen HC. Traction avulsion amputation of the major upper limb: a proposed new classification, guidelines for acute management, and strategies for secondary reconstruction. Plast Reconstr Surg 2001;108:1624-1638.
19. MacKinnon SE, Dellon AL. Nerve repair and nerve grafting. In MacKinnon SE, Dellon Al. (eds): Surgery of the peripheral nerve. New York, Thieme Medical Publishers, 1988:pp 89-129.
20. Meyer VE, Stallmach TH, Burg D. Assessment of the nerve quality at the coaptation site by nerve function evaluation. In Frey M, Giovanoli P, Koller R. (eds): 5th International Muscle Symposium May 19-21, 2000. Vienna, Austria, Proceedings. Vienna, Austria, Division of Plastic and Reconstructive Surgery, University of Vienna, Medical School, 2000, pp 23-26.
21. Brand P W, Beach R B, Thompson D E. Relative tension and potential excursion of muscles in the forearm and hand. J Hnad Surg 1981;6A:209-219.
22. Manktelow RT, McKee NH. Free muscle transplantation to provide active finger flexion. J Hand Surg 1978;3:416-426.