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Experimental study of epithelialization of the muscle-only flap in the oral cavity
KLAUS-DIETRICH
J Oral Maxillofac 55:1431-1432,1997
1431
WOLFF
Surg
Discussion Experimental Study of Epithelialiration of the Muscle-Only Flap in the Oral Cavity
Klaus-Dietrich
Wolff; MD, DMD
Benjamin Germany
Medical
Franklin
Center,
Free
University
of Berlin,
Compared with conventional myocutaneous, cutaneous, or jejunum transplants, the use of free muscle flaps for defect coverage in the oral cavity is relatively uncommon because the missing epithelial coat must be actively formed by local mucosa. Although this necessary substitution of the epithelial coat should primarily be considered a disadvantage, it does lead to physiologic covering of the defect, that is, coating with local mucosa. In this regard, free muscle transplantations come very close to fulfilling the requirement of “replacing tissue with tissue of the same kind.” Muscle transplantations for defect coverage in the oral cavity are also unique in that they are functionally diverted far more than any other transplantation type. Muscles with active motor innervation stemming from their original function will be denervated by the transplantation process or are subject to disuse atrophy because of their passive embedding in the oral cavity. Both features, secondary epithelization and muscle atrophy, make the use of free muscle flaps a method with low outcome predictability. In their experimental study, Elshal et al were especially concerned with the question of epithelization, for which they used a rabbit model with a cranially pedicled cleidomastoid flap. As the authors showed, the muscle is well perfused into the periphery by a dominant artery entering cranially. Thus, muscle fiber fragmentation and peripheral muscle replacement by granulation tissue beginning 10 days after transplantation cannot be attributed to transplant ischemia. Why is there a loss of muscle tissue that subsequently leads to a contraction in the transplant area? In a histologic and immunohistochemical workup, the authors determined that, with the granulation tissue, the muscle surface is colonized by myofibroblasts that cause muscle atrophy by forming a contractile organ. The authors make no mention of the fact that the motor innervation of the flap also must be be considered in direct relation to muscle atrophy. If the muscle transplant is denervated, neurogenic atrophy sets in shortly thereafter, causing considerable volume loss. Even if the cleidomastoid flap is placed in the oral cavity with preserved innervation via the accessory nerve, the altered basic tension and the lack of functional use of the transplant will also result in disuse atrophy of unknown severity.’ The question of what quantitative contribution each of the described mechanisms makes with regard to transplant atrophy cannot yet be decisively answered. In one of our own experimental studies on microneurovascular anastomosed muscle flaps in rats, the muscle transplant had already lost 20% of its initial size and weight by the third postoperative week. After 8 weeks, the transplant had decreased by 40% of its original weight. After 5 months, there was less than one third of the original muscle mass without motor reinnervation. The role of function and thus motor innervation was made clear in this study, because the muscle transplant regained 80% of its original weight after 5 months with successful motor reinnervation. The dis-
use atrophy of noninnervated muscle transplants could also be determined by 3’P spectroscopy, which already showed a clear reduction of the energy-rich phosphate in the muscles 24 hours after transplantation.2 All muscle reduction processes are only caused neurogenically and occur without granulation and epithelization. We also clinically investigated the phenomenon of atrophy in free muscle flaps used for tongue reconstruction, which were reinnervated by anastomosis with the hypoglossal nerve. In five patients, despite reinnervation, there was a 50% to 75% long-term loss of transplant volume.3 In contrast to the experiments in rats, this disappointing result can be explained by the granulation and epithelization process taking place in these transplants. As the authors showed, epithelization of the muscles is associated with a decline in myofibrils and the formation of collagen fibers, which reduces muscle mass and impairs the reinnervation process. The exact description of the type and temporal course of epithelization is one strength of the current study, particularly because it is supported by long-term studies. The authors showed that epithelization is initiated by the presence of inflammatory cells and the formation of granulation tissue. Moreover, the local epithelium slides over the granulation tissue from the periphery in a “tongue-like” manner. The numerous fibroblasts occurring with the granulation tissue originate from the lamina propria of the surrounding mucosa and are the prerequisite for the proliferation and the further maturation of the epithelial cells. During transformation of the peripheral muscle tissue into granulation tissue, there is a gradual confluence of the epithelial tongue. Thus, all flaps in the selected transplant model were completely covered with layered parakeratinized squamous epithelium by the 21st day. Islandlike growth of desquamated epithelial cells was excluded. A similar temporal course of the centripetal epithelization pattern, especially granulation tissue formation on the muscle surface, also can be observed clinically. With the transformation of epithelium-covered granulation tissue into mature connective tissue there is shrinkage of the flap region with flattening of the buccal sulcus starting on the 28th day. After 6 months, the outcome of the epithelization process is a dense network of collagen fibers and a poorly organized, very strongly keratinized, epithelium over the thinned, original muscles of the transplant. Only a few capillaries were noted in the immunohistologic examination, so that a hypoxic metabolic situation may be responsible for the configuration of the new epithelium. What is the status of free muscle transplants for defect coverage in the oral cavity? The key to answering this question lies in finding the correct indication for this transplant type, and this study has made a considerable contribution. Because of the regular occurrence of cicatrization applying free muscle flaps in the area of mobile mucosa is out of the question; this especially includes the anterior floor of the mouth, the buccal plane, the tongue, and the vestibule. A muscle transplant would restrict the mobility of the mucosa in all of these locations and lead to ankyloglossia, obstruction of the oral aperture, and impairment in wearing a mucosaborned prosthesis. Because epithelization is an active function of the local mucosa, muscle transplants should not be used if irradiation is planned postoperatively because the
1432 resultant delay in the epithelization process may increase the risk of a wound healing disorder. However, in areas with osseous support, especially the hard palate, muscle transplants are particularly useful and are superior to all other transplant types because they become firmly attached to bone, are covered by local epithelium, and adjust well to the bone level. Thus, defect coverage with the temporalis muscle flap is the ideal reconstruction method on the hard palate. The iliac crest osseomyocutaneous transplant, which may involve using the internal oblique muscle for intraoral lining in mandibular reconstruction, is also indicated as a free muscle flap in the oral cavity.4 Muscles atrophying on the bone transplant change into relatively thin, firmly fixed and epithelialized, fibrous tissue, which is similar to the clinical pattern of the attached gingiva; for this reason, this also creates good conditions for the insertion of dental implants. The indications for free muscle transplants can be more precisely
DISCUSSION
determined by knowing more about the histologic pattern of this transplant type. For this reason, the authors should be congratulated on their study.
References 1. Turk AE, Ishida K, Kobayashi M, et al: The effects of dynamic tension and reduced graft size on muscle regeneration in rabbit free muscle grafts. Plast Reconstr Surg 88:299, 1991 2. Wolff K-D, Stiller D: Functional aspects of free muscle transplantation: Atrophy, reinnervation and metabolism. J Reconstr Microsurg 8:137, 1992 3. Wolff K-D, Dienemann D, Hoffmeister B: Intraoral defect coverage with free muscle flaps. J Oral Maxillofac Surg 53:680, 1995 4. Urken M, Vickery C, Weiberg H, et al: The internal oblique iliac crest osseomyocutaneous free flap in head and neck reconstruction. Reconstruct Microsurg 5:203, 1989
J Oral Maxillofac 55:1431-1432,1997
1431
WOLFF
Surg
Discussion Experimental Study of Epithelialiration of the Muscle-Only Flap in the Oral Cavity
Klaus-Dietrich
Wolff; MD, DMD
Benjamin Germany
Medical
Franklin
Center,
Free
University
of Berlin,
Compared with conventional myocutaneous, cutaneous, or jejunum transplants, the use of free muscle flaps for defect coverage in the oral cavity is relatively uncommon because the missing epithelial coat must be actively formed by local mucosa. Although this necessary substitution of the epithelial coat should primarily be considered a disadvantage, it does lead to physiologic covering of the defect, that is, coating with local mucosa. In this regard, free muscle transplantations come very close to fulfilling the requirement of “replacing tissue with tissue of the same kind.” Muscle transplantations for defect coverage in the oral cavity are also unique in that they are functionally diverted far more than any other transplantation type. Muscles with active motor innervation stemming from their original function will be denervated by the transplantation process or are subject to disuse atrophy because of their passive embedding in the oral cavity. Both features, secondary epithelization and muscle atrophy, make the use of free muscle flaps a method with low outcome predictability. In their experimental study, Elshal et al were especially concerned with the question of epithelization, for which they used a rabbit model with a cranially pedicled cleidomastoid flap. As the authors showed, the muscle is well perfused into the periphery by a dominant artery entering cranially. Thus, muscle fiber fragmentation and peripheral muscle replacement by granulation tissue beginning 10 days after transplantation cannot be attributed to transplant ischemia. Why is there a loss of muscle tissue that subsequently leads to a contraction in the transplant area? In a histologic and immunohistochemical workup, the authors determined that, with the granulation tissue, the muscle surface is colonized by myofibroblasts that cause muscle atrophy by forming a contractile organ. The authors make no mention of the fact that the motor innervation of the flap also must be be considered in direct relation to muscle atrophy. If the muscle transplant is denervated, neurogenic atrophy sets in shortly thereafter, causing considerable volume loss. Even if the cleidomastoid flap is placed in the oral cavity with preserved innervation via the accessory nerve, the altered basic tension and the lack of functional use of the transplant will also result in disuse atrophy of unknown severity.’ The question of what quantitative contribution each of the described mechanisms makes with regard to transplant atrophy cannot yet be decisively answered. In one of our own experimental studies on microneurovascular anastomosed muscle flaps in rats, the muscle transplant had already lost 20% of its initial size and weight by the third postoperative week. After 8 weeks, the transplant had decreased by 40% of its original weight. After 5 months, there was less than one third of the original muscle mass without motor reinnervation. The role of function and thus motor innervation was made clear in this study, because the muscle transplant regained 80% of its original weight after 5 months with successful motor reinnervation. The dis-
use atrophy of noninnervated muscle transplants could also be determined by 3’P spectroscopy, which already showed a clear reduction of the energy-rich phosphate in the muscles 24 hours after transplantation.2 All muscle reduction processes are only caused neurogenically and occur without granulation and epithelization. We also clinically investigated the phenomenon of atrophy in free muscle flaps used for tongue reconstruction, which were reinnervated by anastomosis with the hypoglossal nerve. In five patients, despite reinnervation, there was a 50% to 75% long-term loss of transplant volume.3 In contrast to the experiments in rats, this disappointing result can be explained by the granulation and epithelization process taking place in these transplants. As the authors showed, epithelization of the muscles is associated with a decline in myofibrils and the formation of collagen fibers, which reduces muscle mass and impairs the reinnervation process. The exact description of the type and temporal course of epithelization is one strength of the current study, particularly because it is supported by long-term studies. The authors showed that epithelization is initiated by the presence of inflammatory cells and the formation of granulation tissue. Moreover, the local epithelium slides over the granulation tissue from the periphery in a “tongue-like” manner. The numerous fibroblasts occurring with the granulation tissue originate from the lamina propria of the surrounding mucosa and are the prerequisite for the proliferation and the further maturation of the epithelial cells. During transformation of the peripheral muscle tissue into granulation tissue, there is a gradual confluence of the epithelial tongue. Thus, all flaps in the selected transplant model were completely covered with layered parakeratinized squamous epithelium by the 21st day. Islandlike growth of desquamated epithelial cells was excluded. A similar temporal course of the centripetal epithelization pattern, especially granulation tissue formation on the muscle surface, also can be observed clinically. With the transformation of epithelium-covered granulation tissue into mature connective tissue there is shrinkage of the flap region with flattening of the buccal sulcus starting on the 28th day. After 6 months, the outcome of the epithelization process is a dense network of collagen fibers and a poorly organized, very strongly keratinized, epithelium over the thinned, original muscles of the transplant. Only a few capillaries were noted in the immunohistologic examination, so that a hypoxic metabolic situation may be responsible for the configuration of the new epithelium. What is the status of free muscle transplants for defect coverage in the oral cavity? The key to answering this question lies in finding the correct indication for this transplant type, and this study has made a considerable contribution. Because of the regular occurrence of cicatrization applying free muscle flaps in the area of mobile mucosa is out of the question; this especially includes the anterior floor of the mouth, the buccal plane, the tongue, and the vestibule. A muscle transplant would restrict the mobility of the mucosa in all of these locations and lead to ankyloglossia, obstruction of the oral aperture, and impairment in wearing a mucosaborned prosthesis. Because epithelization is an active function of the local mucosa, muscle transplants should not be used if irradiation is planned postoperatively because the
1432 resultant delay in the epithelization process may increase the risk of a wound healing disorder. However, in areas with osseous support, especially the hard palate, muscle transplants are particularly useful and are superior to all other transplant types because they become firmly attached to bone, are covered by local epithelium, and adjust well to the bone level. Thus, defect coverage with the temporalis muscle flap is the ideal reconstruction method on the hard palate. The iliac crest osseomyocutaneous transplant, which may involve using the internal oblique muscle for intraoral lining in mandibular reconstruction, is also indicated as a free muscle flap in the oral cavity.4 Muscles atrophying on the bone transplant change into relatively thin, firmly fixed and epithelialized, fibrous tissue, which is similar to the clinical pattern of the attached gingiva; for this reason, this also creates good conditions for the insertion of dental implants. The indications for free muscle transplants can be more precisely
DISCUSSION
determined by knowing more about the histologic pattern of this transplant type. For this reason, the authors should be congratulated on their study.
References 1. Turk AE, Ishida K, Kobayashi M, et al: The effects of dynamic tension and reduced graft size on muscle regeneration in rabbit free muscle grafts. Plast Reconstr Surg 88:299, 1991 2. Wolff K-D, Stiller D: Functional aspects of free muscle transplantation: Atrophy, reinnervation and metabolism. J Reconstr Microsurg 8:137, 1992 3. Wolff K-D, Dienemann D, Hoffmeister B: Intraoral defect coverage with free muscle flaps. J Oral Maxillofac Surg 53:680, 1995 4. Urken M, Vickery C, Weiberg H, et al: The internal oblique iliac crest osseomyocutaneous free flap in head and neck reconstruction. Reconstruct Microsurg 5:203, 1989