- Email: [email protected]
A multidisciplinary approach to treating maxillofacial arteriovenous malformations in children
A multidisciplinary approach to treating maxillofacial arteriovenous malformations in children Wei-liang Chen, DDS, MD, MBA,a Jian-tao Ye, DDS, MD,b Lin-feng Xu, MD,c Zhi-quan Huang, DDS, MD,d and Da-ming Zhang, DDS, MS,e Guangzhou, China SECOND AFFILIATED HOSPITAL, SUN YAT-SEN UNIVERSITY
Objective. Congenital arteriovenous malformations (AVMs) in the maxillofacial region are rare, potentially lifethreatening, vascular lesions. This study reviewed our experience with a multidisciplinary approach to treating maxillofacial AVMs in children. Study design. Thirteen patients (10 boys and 3 girls) with AVMs involving the facial soft tissues or jaws were treated using a multidisciplinary approach that included: 1) superselective intra-arterial embolization (SIAE); 2) bone wax packing (BWP) of the bone cavity and curettage; and 3) compartmentalization and sclerotherapy. Results. The mean follow-up was 13.5 months, with a range of 6-22 months. The following outcomes were obtained: 9 lesions (69.2%) were completely involuted, 3 lesions (23.1%) were mostly involuted, and 1 lesion (7.7%) was partially involuted. The rates of completely and mostly involuted AVMs involving the jaws treated using SIAE, BWP, and curettage were 80% and 20%, respectively. The rates of completely, mostly, and partially involuted AVMs involving soft tissues treated by compartmentalization and sclerotherapy were 60%, 30%, and 10%, respectively. Conclusion. SIAE was reliable for controlling bleeding and as adjunctive treatment for maxillofacial AVMs in children. SIAE followed by BWP of the bone cavity and curettage was a simple, safe, and effective method for treating AVMs of the jaws; SIAE followed by compartmentalization and the injection of OK-432 and pingyangmycin was a reliable alternative treatment for AVMs of the soft tissues in the maxillofacial region. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:41-47)
Maxillofacial arteriovenous malformations (AVMs) can cause facial asymmetry, loose teeth, tinnitus, headaches, and bruits, and they can be complicated by life-threatening conditions such as hemorrhage, highoutput heart failure, and ischemic necrosis due to the “steal” phenomenon. Despite medical advances, the treatment of congenital AVMs of the maxillofacial region remains a challenge. Treatment with radiotherapy and sclerotherapy (the injection of 5% sodium morrhuate) may not be effective for AVMs.1 Proximal ligation is contraindicated, because it requires the recruitment of vessels from adjacent vascular territories that may be inaccessible surgically and it may compromise subsequent attempts at highly selective embolization.2 The nidus of the AVM should be removed completely to achieve a complete cure. The remnant AVM may grow quickly, becoming bigger than before treata
Professor and Director, Department of Oral and Maxillofacial Surgery. Assistant Professor, Department of Oral and Maxillofacial Surgery. c Assistant Professor, Department of Radiology. d Lecturer, Department of Oral and Maxillofacial Surgery. e Resident, Department of Oral and Maxillofacial Surgery. Received for publication Dec 19, 2008; returned for revision Feb 9, 2009; accepted for publication Mar 3, 2009. 1079-2104/$ - see front matter © 2009 Published by Mosby, Inc. doi:10.1016/j.tripleo.2009.03.006 b
ment.3 Kohout et al.4 believed that complete excision of the nidus is critical, but surgical treatment alone can result in massive life-threatening bleeding during the surgery.5 Some investigators state that reconstructing complex defects of the soft and hard tissues remains challenging after successful selective embolization and surgical resection.6 With the recent progress in interventional radiologic techniques, such as superselective intra-arterial embolization (SIAE), comprehensive treatment including SIAE has been reported to be effective in treating maxillofacial AVMs.1 The present study reviewed the clinical outcomes in children with maxillofacial AVMs treated using a multidisciplinary approach that included: 1) SIAE; 2) bone wax packing (BWP) of the bone cavity and curettage; and 3) compartmentalization and sclerotherapy. MATERIALS AND METHODS Materials Thirteen patients with AVMs in the maxillofacial region were referred to the Department of Oral and Maxillofacial Surgery, Second Affiliated Hospital of Sun Yat-sen University (Guangzhou, China) from October 2004 to April 2006. There were 10 boys and 3 girls. Their mean age was 9.1 (range 4-13) years. Ten AVMs were located in soft tissues (lip, cheek, parotid gland, or floor of mouth) and caused clinical symptoms 41
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Table I. Demographic, clinical, and outcome characteristics of 13 patients treated for arteriovenous malformations (AVMs) Case/age (yr)/gender
Location of AVM
1/8/M 2/11/F 3/5/M 4/13/M 5/13/F 6/9/M
Mandible Cheek, mandible Cheek, mandible Lip, cheek Mandible Parotid gland, cheek Cheek, mandible Lip, cheek, mandible Mandible Floor of mouth Cheek, maxilla Cheek, mandible Cheek, mandible
7/7/M 8/10/M 9/12/M 10/6/M 11/8/F 12/9/F 13/7/M
Schoebinger Feeding artery BWP/ No. of injections, clinical stage embolized curettage dose of OK/PY III III III III III II
IAA,* LA* IAA,* FA* IAA,* FA* IAA, FA IAA* MA, FA, STA
⫹/⫹ ⫹/⫹ ⫹/⫹ ⫺ ⫹/⫹ ⫺
III II
IAA,* FA* IAA, FA, LA
III II II III II
IAA* IAA, LA MA, FA IAA,* FA* IAA, FA
Complications
Follow-up Outcome for soft (mos) tissue/jaw† 11 8 20 14 19 6
—/1 1/1 1/2 1/— —/1 3/—
⫹/⫹ ⫹/⫹
— — 8, 16 KE/64 mg — 6, 6 KE/24 mg Scarring 8, 16 KE/64 mg Hyperpigmentation — — 6, 12 KE/36 mg Transient facial paresis 7, 7 KE/28 mg — 6, 12 KE/36 mg —
20 8
1/1 2/1
⫹/⫹ ⫺ ⫾ ⫹/⫹ ⫹/⫹
— — 6, 6 KE/24 mg — 6, 12 KE/36 mg — 8, 16 KE/48 mg Scarring 6, 6 KE/42 mg —
10 7 14 16 22
—/1 2/— 2/1 1/2 1/1
F, Female; M, male; IAA, inferior alveolar artery; LA, lingual artery; FA, facial artery; MA, maxillary artery; STA, superior temporal artery; OK, OK-432; PY, pingyangmycin. *Emergency control of hemorrhage. †Outcome for soft tissue/jaw: 1 ⫽ completely involuted; 2 ⫽ mostly involuted; 3 ⫽ partially involuted.
that included facial asymmetry, skin discoloration, overlying skin warmth, pulsation, and a noise like blowing wind. In all cases, digital subtraction angiography (DSA) confirmed the diagnosis, and computerized tomography (CT) or 3-dimensional CT (3D-CT) reconstruction showed that 7 cases were located in the jaws (6 mandibles, 1 maxilla). Three cases were located in the mandible without soft tissue involvement (Table I). The clinical symptoms included recurrent spontaneous gingival bleeding or sudden uncontrollable hemorrhage following tooth extraction (Fig. 1, A). Computerized tomography showed expansion of the mandibular body and bony absorption, most commonly in the body, angle, and ramus. According to the Schoebinger clinical stages, 5 AVMs were stage II (expansion) and 8 were stage III (destruction); there were no patients with stage I (quiescence) or IV (decompensation) malformations.4 Stage I lesions remain stable for a long time. Expansion (stage
II) is usually followed by recurrent spontaneous gingival bleeding or sudden uncontrollable hemorrhage and ulceration (stage III) (Table I). Surgical techniques SIAE. The DSA Seldinger catheterization technique was performed through the femoral artery, using a 3F-6F guide wire (Cordis, Miami Lakes, FL). The catheter was passed into the common carotid artery, and angiographs of the external and internal carotid arteries were taken (Fig. 1, B) to show the AVM in the maxillofacial region (Fig. 1, C). For the lesions, the origin of each feeding artery (e.g., inferior alveolar, facial, maxillary, superior temporal, or lingual artery) was embolized individually. The embolization materials used included polyvinyl alcohol particles (500-700 m) and metal coils. The postembolization angiograph showed obviously reduced blood flow (Fig. 1, D), and the skin color over the AVMs was clinically normal.
™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3 Fig. 1. An 8-year-old boy presenting with an arteriovenous malformation (AVM) involving the mandible (case 1). A, Uncontrolled hemorrhage from the left lower gingiva. B, The digital subtraction angiography (DSA) Seldinger catheterization technique being used. C, DSA examination before superselective intra-arterial embolization (SIAE), showing the nidus of the AVM in the left maxillofacial region. D, The nidus is absent after SIAE of the nidus of the AVM. E, Preoperative panoramic radiograph, showing an AVM involving the body and ramus of the mandible and embolization coils in the maxillofacial region. F, Bone wax with iodoform being prepared for packing. G, The bone wax being packed into the bone cavity. H, Finishing bone wax packing of 4 bony cavities. I, The bone cavity of the mandible exposed for curettage. J, The removed bone wax. K, The bone cavity of the mandible was filled with inorganic bovine bone mineral. L, Postoperative panoramic radiograph, showing preservation of the tooth embryon and erupted teeth, and the defects filled with inorganic bovine bone mineral.
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Any hemorrhage in the gingiva was controlled immediately. The soft tissue pulsation decreased. The catheter was removed after embolization, and the puncture site was compressed with a bandage. BWP of the bone cavity and curettage. This technique should be performed under general anesthesia about 1 week after SIAE (Fig. 1, E). A bony window was made in the area of gingival bleeding. The involved teeth were extracted, and an 8.0-cm incision was made 1.5 cm beneath the lower margin of the mandible. The soft tissues were separated from the surface of the bone, and 1.0-cm bur holes were made in the bone. Any bleeding at this point was controlled by digital pressure over the hole in the alveolar bone or buccal cortex. Simultaneously, a 1.0-cm plug of bone wax with iodoform (Fig. 1, F) was packed in the bone cavity or AVM though the bur holes. This procedure was repeated until the bone cavity was filled with bone wax. Consequently, the bleeding in the bone or the alveolar socket ceased. The soft tissues were then sutured. If necessary, several mobile teeth were extracted and several holes were made in the bone to ensure that every bone cavity was filled with bone wax (Fig. 1, G and H). Four weeks after BWP of the bone cavity, an external incision was made and the mandible was exposed (Fig. 1, I). The bone cavity caused by the AVM was opened, which usually caused a slight hemorrhage. The AVM was observed to have formed a fibrous capsule, and the bone wax was removed without difficulty (Fig. 1, J). The inferior alveolar nerve should be preserved, and any tooth embryon and erupted teeth should be preserved if possible. The bone cavity was filled with inorganic bovine bone mineral (Bio-Oss; Osteohealth, Shirley, NY) (Fig. 1, K and L), and the soft tissues were sutured. Compartmentalization and sclerotherapy. This procedure is performed under general anesthesia about 1
Chen et al. 45
week after SIAE (Fig. 2, A and B) in patients with an AVM of the cheek. The AVM was treated by compartmentalization using #7 nonabsorbable sutures [back braided silk, Mersilk; Johnson Medical (China), Guangzhou, China]. An awl (zygomatic arch awl; Medicon, Tuttlingen, Germany) was used to place the sutures in a circumferential manner around the lesion. The first pass of the awl went deep; the second pass came up and into the intradermal region, passed out through the same entrance puncture as the previous suture, and was then ligated (Fig. 2, C and D). This was followed by the injection of the percutaneous sclerosing agents OK-432 (streptococcal pyrogenic exotoxin A; Shandong Lukuang Pharmaceutical Group, Luya, Jinan, China) and pingyangmycin (bleomycin A5 hydrochloride; Harbin Bolai Pharmaceutics, Harbin, China). All patients with AVMs were treated with a standard 0.1 mg (1 KE) injection of OK-432 and a 0.3-0.6 mg/kg injection of pingyangmycin into each compartment (Fig. 2, E). The needle was introduced through normal skin and was advanced into the lesion, and then the sclerosing agents were injected in a radial fashion. The needle was withdrawn, and the lesion was compressed for at least 1 minute. Initially, the injected solutions were prepared by dissolving lyophilized OK-432 to a concentration of 0.1 mg (1 KE) in 10 mL normal saline (NS) and dissolving lyophilized pingyangmycin to a concentration of 8 mg in 10 mL NS. Intravenous dexamethasone (0.1 mg/kg) and NS (60 mL/kg) were given for 3 days after surgery. Evaluating the results The outcomes were assessed by a panel of three surgeons, and the response rate was graded as follows: 1 ⫽ completely controlled, implying a ⬎90% reduction in size or absence of the lesion, normal skin temperature, and absence of pulsation and noise (Fig. 2, F-P);
4™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™ Fig. 2. An 11-year-old girl presenting with an arteriovenous malformation (AVM) involving the cheek and mandible (case 2). A, Digital subtraction angiography (DSA) examination before superselective intra-arterial embolization (SIAE), showing the nidus of the AVM in the left maxillofacial region. B, The nidus is absent after SIAE. C, Using an awl, silk sutures were placed circumferentially around the base; the first pass of the awl was deep. The second pass of the awl came up into the intradermal region and exited through the entrance puncture of the previous suture. D, The sutures were ligated. E, The percutaneous sclerosing agents OK-432 and pingyangmycin were injected into each compartment. F, Preoperative panoramic radiograph, showing an AVM involving the body and ramus of the mandible and the teeth. G, Postoperative panoramic radiograph, showing the defects in the mandible packed with bone wax with iodoform, the loss of the involved teeth, and the embolization coils in the maxillofacial region. H, Postoperative panoramic radiograph, showing complete absence of the lesion. I, Three-dimensional computerized tomography (3D-CT) reconstruction, showing an AVM involving the left cheek before compartmentalization and sclerotherapy. J, 3D-CT reconstruction, showing absence of the AVM involving the cheek after compartmentalization and sclerotherapy after SIAE (8-month follow-up). K, 3D-CT reconstruction, showing an AVM involving the left mandible before bone wax packing (BWP) of the bone cavity and curettage. L, 3D-CT reconstruction, showing a normal mandible after BWP of the bone cavity and curettage after SIAE (8-month follow-up). M, Before using a multidisciplinary approach to treat the AVM. N, After using a multidisciplinary approach to treat the AVM (8-month follow-up). O, Before dental prosthetic rehabilitation. P, After dental prosthetic rehabilitation.
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2 ⫽ mostly controlled, implying a 75%-90% reduction in size or a mostly improved facial deformity and mostly reduced skin temperature, pulsation, and noise; 3 ⫽ partially controlled, implying a 50%-75% reduction in size or a partly improved facial deformity and partly reduced skin temperature, pulsation, and noise; 4 ⫽ slightly controlled, implying a 25%-50% reduction in size or little improved facial deformity and no change in pulsation and noise; and 5 ⫽ not controlled, implying a ⬍25% reduction in size or no change in size, pulsation, and noise of the AVM. RESULTS All of the patients had significant swelling and mild pain for up to 1 week after SIAE, BWP of the bone cavity, and sclerotherapy, but no major complications occurred. One patient developed transient facial paresis, which resolved spontaneously within 2 weeks. Hypopigmentation occurred in 1 patient, and scarring in 2 patients. The mean follow-up time was 13.5 months, with a range of 6-22 months. Nine (69.2%) of the lesions were completely controlled, 3 (23.1%) were mostly controlled, and 1 (7.7%) was partially controlled. The rates of completely and mostly controlled AVMs involving the jaws treated by SIAE, BWP, and curettage were 80% and 20%, respectively. The rates of completely, mostly, and partially controlled AVMs involving soft tissues treated by compartmentalization and sclerotherapy were 60%, 30%, and 10%, respectively (Table I). All of the patients had normal liver and kidney functions and normal lung fields on chest radiographs. DISCUSSION In this study, there were no patients with stage I or IV AVMs. We believe that stage I AVMs do not need to be treated, whereas stage II AVMs should be treated, because they often cause problems such as cosmetic concerns and compression of adjacent structures. Hemorrhage is the most common and serious symptom of stage III AVMs in the maxillofacial region, and controlling hemorrhage is the most important step in the treatment of maxillofacial AVMs.1 Subtotal excision or proximal ligation frequently results in rapid progression of the arteriovenous malformation. Thus, ligation of the feeding artery without removing the nidus should be avoided because other collateral vessels and quiescent AVMs will grow rapidly, possibly becoming bigger than before. Moreover, if the feeding artery of the AVM is ligated, further embolotherapy/sclerotherapy may be impossible because of the lack of a route for embolotherapy/sclerotherapy.3 Digital subtraction angiography can demonstrate the nidus, feeding vessels, and flow characteristics of
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AVMs and can determine the site of bleeding. SIAE involves selective embolization of the nidus of the AVM. First the minimal artery is embolized, and then the embolization proceeds from inside to outside the AVM. In the present study, 7 cases of stage III AVM of the mandible resulted in gingiva bleeding or uncontrollable hemorrhage in the alveolar socket; these patients underwent emergency SIAE, and the bleeding was controlled quickly and effectively. In this study, there were no major complications, such as facial nerve palsy, pulmonary embolism, deep vein thrombosis, and massive tissue necrosis. During SIAE, metal coils were used to block the artery supplying the AVMs to reduce its vascularity. Alternatively, polyvinyl alcohol particles can be used to cause blood to coagulate in the vessel lumen. Following partial obstruction of the vascular lumen, the blood flow was blocked, which resulted in necrosis of the endoepithelial cells of the vessel and proliferation of the fibrous tissue of the AVM. Motamedi et al.7 found that simple embolization was not successful in treating AVMs of the mandible and that surgical treatment was also needed. No patients with AVMs were cured by simple embolization.1 Computerized tomography can delineate the bony involvement of AVMs, and 3D-CT reconstruction may enhance the accuracy of preoperative planning, such as planning the approach to the lesion. We performed BWP of the bone cavity within 1 week after embolization, because if the interval is too long, the embolization materials would be absorbed and the AVMs might recanalize. The AVMs had formed a fibrous capsule in the bone cavity of the mandible by about 4 weeks after BWP of the bone cavity.1 After curettage, the bone cavity was filled with exogenous bone to induce osteogenesis and to maintain the architecture of the mandible while sparing the inferior alveolar nerve. The teeth, dental follicles, and erupted teeth can be preserved in most cases. Dissection of the jaws should be avoided. In the present study, we used BWP of bone cavities to control hemorrhage of the lesions in emergencies, and we performed curettage 4 weeks later. This markedly reduced the bleeding and allowed complete removal of the AVM without complications. The rates of completely and mostly involuted AVMs involving the jaws were 80% and 20%, respectively. Our experience with BWP of the bone cavity and curettage after SIAE demonstrates that this is safe and effective therapy. We believe that the technique saves the jaws while ensuring function, without complications. Chen et al.8 reported that compartmentalization followed by the injection of OK-432 and pingyangmycin into each compartment was a simple, safe, and reliable alternative treatment for massive venous malformations of the face and neck, and they used SIAE was an
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adjunct treatment for AVMs of the soft tissues.1 We performed compartmentalization and sclerotherapy after SIAE to interrupt the blood supply from the regional vascular network and to divide the AVMs into compartments by isolating blocks of tissue with considerably reduced flow. Subsequently, large doses of OK-432 and pingyangmycin were injected into each compartment, allowing “pooling” of the agents followed by thrombosis and solidification. Pooling ensures that the highly concentrated sclerosing agents have prolonged contact with the endothelial lining to maximize effectiveness. Sclerosing agents provoke a severe intimal inflammatory reaction that leads to thrombosis and shrinks the vascular anomaly.9 In the present study, the treatment of maxillofacial AVMs with OK-432 and pingyangmycin after compartmentalization was effective, with 6 lesions (60%) achieving complete control, 3 lesions (30%) becoming mostly controlled, and 1 lesion (10%) becoming partially controlled. For intralesional injection, OK-432 and pingyangmycin (bleomycin A5 hydrochloride) are preferable to other sclerosing agents such as absolute alcohol, sodium tetradecyl sulphate, and sodium morrhuate, because they are antineoplastic drugs in addition to sclerosing agents. OK-432 and bleomycin have been used to treat lymphatic and venous malformations.8,10 OK432 is secreted by some strains of Streptococcus pyogenes and possesses pyrogenic toxin superantigenicity. Superantigenic activation of T cells and monocytes stimulates the release of cytokines such as tumor necrosis factors alpha and beta, interleukin 1, and gammainterferon. OK-432 interacts directly with endothelial cells.11 Several inflammatory cytokines increase cellular immunity, leading to tumor eradication, and cause local inflammation, the formation of granulation tissue, and the disappearance of the vessel due to obliteration of its lumen. Pingyangmycin has an apoptotic effect on rapidly growing immature cells.12 The intralesional injection of pingyangmycin results in the detachment of endothelial cells and thickening of the vessel wall, which leads to lumen narrowing and occlusion. The theoretic reasoning behind choosing OK-432 and pingyangmycin for the intralesional injection of AVMs is sound. We speculated that compartmentalization after SIAE would allow high doses of OK-432 and pingyangmycin to be used, would allow the sclerosing agents to remain active in the lesions for a long time, and would allow the agents to have a synergistic effect on the AVM. No major complications occurred after the injection of OK-432 and pingyangmycin. Intravenous dexamethasone (0.1 mg/kg) and NS (60 mL/kg) were given for 3 days after surgery to control inflammation
Chen et al. 47
and prevent pulmonary fibrosis, which is a serious potential complication of pingyangmycin. Our multidisciplinary approach to the treatment of maxillofacial AVMs is reliable. SIAE was effective for controlling bleeding and as an adjunctive treatment for maxillofacial AVMs in children. SIAE followed by BWP of the bone cavity and curettage was a simple, safe, and effective method for treating AVMs of the jaws. SIAE followed by compartmentalization and the injection of OK-432 and pingyangmycin was a reliable alternative treatment for AVMs of the soft tissues in the maxillofacial region. REFERENCES 1. Chen W, Wang J, Li J, Xu L. Comprehensive treatment of arteriovenous malformations in the oral and maxillofacial region. J Oral Maxillofac Surg 2005;63:1484-8. 2. Niechajev I, Clodius L. Histologic investigation of vascular malformations of the face after transarterial embolization with Ethibloc and other agents. Plast Reconstr Surg 1990;86:664-71. 3. Rockman CB, Rosen RJ, Jacobowitz GR, Weiswasser J, Hofstee DJ, Fioole B, et al. Transcatheter embolization of extremity vascular malformations: the long-term success of multiple interventions. Ann Vasc Surg 2003;17:417-23. 4. Kohout MP, Hansen M, Pribaz JJ, Mulliken JB. Arteriovenous malformations of the head and neck: natural history and management. Plast Reconstr Surg 1998;102:643-54. 5. Lee BB, Bergan JJ. Advanced management of congenital vascular malformations: a multidisciplinary approach. Cardiovasc Surg 2002;10:523-33. 6. Loose DA. Surgical correction of vascular malformations of the lower extremity. Kongressbd Dtsch Ges Chir Kongr 2001;118: 507-15. 7. Motamedi MH, Behnia H, Motamedi MR. Surgical technique for the treatment of high-flow arteriovenous malformations of the mandible. J Craniomaxillofac Surg 2000;28:238-42. 8. Chen WL, Yang ZH, Bai ZB, Wang YY, Huang ZQ, Wang YJ. A pilot study on combination compartmentalisation and sclerotherapy for the treatment of massive venous malformations of the face and neck. J Plast Reconstr Aesthet Surg 2008;61:486-92. 9. Jackson IT, Keskin M, Yavuzer R, Kelly CP. Compartmentalisation of massive vascular malformations. Plast Reconstr Surg 2005;115:10-21. 10. Ogita S, Tsuto T, Tokiwa K, Takahashi T. Intracystic injection of OK-432: a new sclerosing therapy for cystic hygroma in children. Br J Surg 1987;74:690-1. 11. Roggiani M, Stoehr JA, Leonard BA, Schlievert PM. Analysis of toxicity of streptococcal pyrogenic exotoxin A mutants. Infect Immun 1997;65:2868-75. 12. Kullendorff CM. Efficacy of bleomycin treatment for symptomatic hemangiomas in children. Pediatr Surg Int 1997;12:526-8. Reprint requests: Dr. Wei-liang Chen Oral and Maxillofacial Surgeon Department of Oral and Maxillofacial Surgery Second Affiliated Hospital of Sun Yat-sen University 107 Yan-jiang Road 510120 Guangzhou [email protected]
Objective. Congenital arteriovenous malformations (AVMs) in the maxillofacial region are rare, potentially lifethreatening, vascular lesions. This study reviewed our experience with a multidisciplinary approach to treating maxillofacial AVMs in children. Study design. Thirteen patients (10 boys and 3 girls) with AVMs involving the facial soft tissues or jaws were treated using a multidisciplinary approach that included: 1) superselective intra-arterial embolization (SIAE); 2) bone wax packing (BWP) of the bone cavity and curettage; and 3) compartmentalization and sclerotherapy. Results. The mean follow-up was 13.5 months, with a range of 6-22 months. The following outcomes were obtained: 9 lesions (69.2%) were completely involuted, 3 lesions (23.1%) were mostly involuted, and 1 lesion (7.7%) was partially involuted. The rates of completely and mostly involuted AVMs involving the jaws treated using SIAE, BWP, and curettage were 80% and 20%, respectively. The rates of completely, mostly, and partially involuted AVMs involving soft tissues treated by compartmentalization and sclerotherapy were 60%, 30%, and 10%, respectively. Conclusion. SIAE was reliable for controlling bleeding and as adjunctive treatment for maxillofacial AVMs in children. SIAE followed by BWP of the bone cavity and curettage was a simple, safe, and effective method for treating AVMs of the jaws; SIAE followed by compartmentalization and the injection of OK-432 and pingyangmycin was a reliable alternative treatment for AVMs of the soft tissues in the maxillofacial region. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:41-47)
Maxillofacial arteriovenous malformations (AVMs) can cause facial asymmetry, loose teeth, tinnitus, headaches, and bruits, and they can be complicated by life-threatening conditions such as hemorrhage, highoutput heart failure, and ischemic necrosis due to the “steal” phenomenon. Despite medical advances, the treatment of congenital AVMs of the maxillofacial region remains a challenge. Treatment with radiotherapy and sclerotherapy (the injection of 5% sodium morrhuate) may not be effective for AVMs.1 Proximal ligation is contraindicated, because it requires the recruitment of vessels from adjacent vascular territories that may be inaccessible surgically and it may compromise subsequent attempts at highly selective embolization.2 The nidus of the AVM should be removed completely to achieve a complete cure. The remnant AVM may grow quickly, becoming bigger than before treata
Professor and Director, Department of Oral and Maxillofacial Surgery. Assistant Professor, Department of Oral and Maxillofacial Surgery. c Assistant Professor, Department of Radiology. d Lecturer, Department of Oral and Maxillofacial Surgery. e Resident, Department of Oral and Maxillofacial Surgery. Received for publication Dec 19, 2008; returned for revision Feb 9, 2009; accepted for publication Mar 3, 2009. 1079-2104/$ - see front matter © 2009 Published by Mosby, Inc. doi:10.1016/j.tripleo.2009.03.006 b
ment.3 Kohout et al.4 believed that complete excision of the nidus is critical, but surgical treatment alone can result in massive life-threatening bleeding during the surgery.5 Some investigators state that reconstructing complex defects of the soft and hard tissues remains challenging after successful selective embolization and surgical resection.6 With the recent progress in interventional radiologic techniques, such as superselective intra-arterial embolization (SIAE), comprehensive treatment including SIAE has been reported to be effective in treating maxillofacial AVMs.1 The present study reviewed the clinical outcomes in children with maxillofacial AVMs treated using a multidisciplinary approach that included: 1) SIAE; 2) bone wax packing (BWP) of the bone cavity and curettage; and 3) compartmentalization and sclerotherapy. MATERIALS AND METHODS Materials Thirteen patients with AVMs in the maxillofacial region were referred to the Department of Oral and Maxillofacial Surgery, Second Affiliated Hospital of Sun Yat-sen University (Guangzhou, China) from October 2004 to April 2006. There were 10 boys and 3 girls. Their mean age was 9.1 (range 4-13) years. Ten AVMs were located in soft tissues (lip, cheek, parotid gland, or floor of mouth) and caused clinical symptoms 41
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Table I. Demographic, clinical, and outcome characteristics of 13 patients treated for arteriovenous malformations (AVMs) Case/age (yr)/gender
Location of AVM
1/8/M 2/11/F 3/5/M 4/13/M 5/13/F 6/9/M
Mandible Cheek, mandible Cheek, mandible Lip, cheek Mandible Parotid gland, cheek Cheek, mandible Lip, cheek, mandible Mandible Floor of mouth Cheek, maxilla Cheek, mandible Cheek, mandible
7/7/M 8/10/M 9/12/M 10/6/M 11/8/F 12/9/F 13/7/M
Schoebinger Feeding artery BWP/ No. of injections, clinical stage embolized curettage dose of OK/PY III III III III III II
IAA,* LA* IAA,* FA* IAA,* FA* IAA, FA IAA* MA, FA, STA
⫹/⫹ ⫹/⫹ ⫹/⫹ ⫺ ⫹/⫹ ⫺
III II
IAA,* FA* IAA, FA, LA
III II II III II
IAA* IAA, LA MA, FA IAA,* FA* IAA, FA
Complications
Follow-up Outcome for soft (mos) tissue/jaw† 11 8 20 14 19 6
—/1 1/1 1/2 1/— —/1 3/—
⫹/⫹ ⫹/⫹
— — 8, 16 KE/64 mg — 6, 6 KE/24 mg Scarring 8, 16 KE/64 mg Hyperpigmentation — — 6, 12 KE/36 mg Transient facial paresis 7, 7 KE/28 mg — 6, 12 KE/36 mg —
20 8
1/1 2/1
⫹/⫹ ⫺ ⫾ ⫹/⫹ ⫹/⫹
— — 6, 6 KE/24 mg — 6, 12 KE/36 mg — 8, 16 KE/48 mg Scarring 6, 6 KE/42 mg —
10 7 14 16 22
—/1 2/— 2/1 1/2 1/1
F, Female; M, male; IAA, inferior alveolar artery; LA, lingual artery; FA, facial artery; MA, maxillary artery; STA, superior temporal artery; OK, OK-432; PY, pingyangmycin. *Emergency control of hemorrhage. †Outcome for soft tissue/jaw: 1 ⫽ completely involuted; 2 ⫽ mostly involuted; 3 ⫽ partially involuted.
that included facial asymmetry, skin discoloration, overlying skin warmth, pulsation, and a noise like blowing wind. In all cases, digital subtraction angiography (DSA) confirmed the diagnosis, and computerized tomography (CT) or 3-dimensional CT (3D-CT) reconstruction showed that 7 cases were located in the jaws (6 mandibles, 1 maxilla). Three cases were located in the mandible without soft tissue involvement (Table I). The clinical symptoms included recurrent spontaneous gingival bleeding or sudden uncontrollable hemorrhage following tooth extraction (Fig. 1, A). Computerized tomography showed expansion of the mandibular body and bony absorption, most commonly in the body, angle, and ramus. According to the Schoebinger clinical stages, 5 AVMs were stage II (expansion) and 8 were stage III (destruction); there were no patients with stage I (quiescence) or IV (decompensation) malformations.4 Stage I lesions remain stable for a long time. Expansion (stage
II) is usually followed by recurrent spontaneous gingival bleeding or sudden uncontrollable hemorrhage and ulceration (stage III) (Table I). Surgical techniques SIAE. The DSA Seldinger catheterization technique was performed through the femoral artery, using a 3F-6F guide wire (Cordis, Miami Lakes, FL). The catheter was passed into the common carotid artery, and angiographs of the external and internal carotid arteries were taken (Fig. 1, B) to show the AVM in the maxillofacial region (Fig. 1, C). For the lesions, the origin of each feeding artery (e.g., inferior alveolar, facial, maxillary, superior temporal, or lingual artery) was embolized individually. The embolization materials used included polyvinyl alcohol particles (500-700 m) and metal coils. The postembolization angiograph showed obviously reduced blood flow (Fig. 1, D), and the skin color over the AVMs was clinically normal.
™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3 Fig. 1. An 8-year-old boy presenting with an arteriovenous malformation (AVM) involving the mandible (case 1). A, Uncontrolled hemorrhage from the left lower gingiva. B, The digital subtraction angiography (DSA) Seldinger catheterization technique being used. C, DSA examination before superselective intra-arterial embolization (SIAE), showing the nidus of the AVM in the left maxillofacial region. D, The nidus is absent after SIAE of the nidus of the AVM. E, Preoperative panoramic radiograph, showing an AVM involving the body and ramus of the mandible and embolization coils in the maxillofacial region. F, Bone wax with iodoform being prepared for packing. G, The bone wax being packed into the bone cavity. H, Finishing bone wax packing of 4 bony cavities. I, The bone cavity of the mandible exposed for curettage. J, The removed bone wax. K, The bone cavity of the mandible was filled with inorganic bovine bone mineral. L, Postoperative panoramic radiograph, showing preservation of the tooth embryon and erupted teeth, and the defects filled with inorganic bovine bone mineral.
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Any hemorrhage in the gingiva was controlled immediately. The soft tissue pulsation decreased. The catheter was removed after embolization, and the puncture site was compressed with a bandage. BWP of the bone cavity and curettage. This technique should be performed under general anesthesia about 1 week after SIAE (Fig. 1, E). A bony window was made in the area of gingival bleeding. The involved teeth were extracted, and an 8.0-cm incision was made 1.5 cm beneath the lower margin of the mandible. The soft tissues were separated from the surface of the bone, and 1.0-cm bur holes were made in the bone. Any bleeding at this point was controlled by digital pressure over the hole in the alveolar bone or buccal cortex. Simultaneously, a 1.0-cm plug of bone wax with iodoform (Fig. 1, F) was packed in the bone cavity or AVM though the bur holes. This procedure was repeated until the bone cavity was filled with bone wax. Consequently, the bleeding in the bone or the alveolar socket ceased. The soft tissues were then sutured. If necessary, several mobile teeth were extracted and several holes were made in the bone to ensure that every bone cavity was filled with bone wax (Fig. 1, G and H). Four weeks after BWP of the bone cavity, an external incision was made and the mandible was exposed (Fig. 1, I). The bone cavity caused by the AVM was opened, which usually caused a slight hemorrhage. The AVM was observed to have formed a fibrous capsule, and the bone wax was removed without difficulty (Fig. 1, J). The inferior alveolar nerve should be preserved, and any tooth embryon and erupted teeth should be preserved if possible. The bone cavity was filled with inorganic bovine bone mineral (Bio-Oss; Osteohealth, Shirley, NY) (Fig. 1, K and L), and the soft tissues were sutured. Compartmentalization and sclerotherapy. This procedure is performed under general anesthesia about 1
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week after SIAE (Fig. 2, A and B) in patients with an AVM of the cheek. The AVM was treated by compartmentalization using #7 nonabsorbable sutures [back braided silk, Mersilk; Johnson Medical (China), Guangzhou, China]. An awl (zygomatic arch awl; Medicon, Tuttlingen, Germany) was used to place the sutures in a circumferential manner around the lesion. The first pass of the awl went deep; the second pass came up and into the intradermal region, passed out through the same entrance puncture as the previous suture, and was then ligated (Fig. 2, C and D). This was followed by the injection of the percutaneous sclerosing agents OK-432 (streptococcal pyrogenic exotoxin A; Shandong Lukuang Pharmaceutical Group, Luya, Jinan, China) and pingyangmycin (bleomycin A5 hydrochloride; Harbin Bolai Pharmaceutics, Harbin, China). All patients with AVMs were treated with a standard 0.1 mg (1 KE) injection of OK-432 and a 0.3-0.6 mg/kg injection of pingyangmycin into each compartment (Fig. 2, E). The needle was introduced through normal skin and was advanced into the lesion, and then the sclerosing agents were injected in a radial fashion. The needle was withdrawn, and the lesion was compressed for at least 1 minute. Initially, the injected solutions were prepared by dissolving lyophilized OK-432 to a concentration of 0.1 mg (1 KE) in 10 mL normal saline (NS) and dissolving lyophilized pingyangmycin to a concentration of 8 mg in 10 mL NS. Intravenous dexamethasone (0.1 mg/kg) and NS (60 mL/kg) were given for 3 days after surgery. Evaluating the results The outcomes were assessed by a panel of three surgeons, and the response rate was graded as follows: 1 ⫽ completely controlled, implying a ⬎90% reduction in size or absence of the lesion, normal skin temperature, and absence of pulsation and noise (Fig. 2, F-P);
4™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™ Fig. 2. An 11-year-old girl presenting with an arteriovenous malformation (AVM) involving the cheek and mandible (case 2). A, Digital subtraction angiography (DSA) examination before superselective intra-arterial embolization (SIAE), showing the nidus of the AVM in the left maxillofacial region. B, The nidus is absent after SIAE. C, Using an awl, silk sutures were placed circumferentially around the base; the first pass of the awl was deep. The second pass of the awl came up into the intradermal region and exited through the entrance puncture of the previous suture. D, The sutures were ligated. E, The percutaneous sclerosing agents OK-432 and pingyangmycin were injected into each compartment. F, Preoperative panoramic radiograph, showing an AVM involving the body and ramus of the mandible and the teeth. G, Postoperative panoramic radiograph, showing the defects in the mandible packed with bone wax with iodoform, the loss of the involved teeth, and the embolization coils in the maxillofacial region. H, Postoperative panoramic radiograph, showing complete absence of the lesion. I, Three-dimensional computerized tomography (3D-CT) reconstruction, showing an AVM involving the left cheek before compartmentalization and sclerotherapy. J, 3D-CT reconstruction, showing absence of the AVM involving the cheek after compartmentalization and sclerotherapy after SIAE (8-month follow-up). K, 3D-CT reconstruction, showing an AVM involving the left mandible before bone wax packing (BWP) of the bone cavity and curettage. L, 3D-CT reconstruction, showing a normal mandible after BWP of the bone cavity and curettage after SIAE (8-month follow-up). M, Before using a multidisciplinary approach to treat the AVM. N, After using a multidisciplinary approach to treat the AVM (8-month follow-up). O, Before dental prosthetic rehabilitation. P, After dental prosthetic rehabilitation.
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2 ⫽ mostly controlled, implying a 75%-90% reduction in size or a mostly improved facial deformity and mostly reduced skin temperature, pulsation, and noise; 3 ⫽ partially controlled, implying a 50%-75% reduction in size or a partly improved facial deformity and partly reduced skin temperature, pulsation, and noise; 4 ⫽ slightly controlled, implying a 25%-50% reduction in size or little improved facial deformity and no change in pulsation and noise; and 5 ⫽ not controlled, implying a ⬍25% reduction in size or no change in size, pulsation, and noise of the AVM. RESULTS All of the patients had significant swelling and mild pain for up to 1 week after SIAE, BWP of the bone cavity, and sclerotherapy, but no major complications occurred. One patient developed transient facial paresis, which resolved spontaneously within 2 weeks. Hypopigmentation occurred in 1 patient, and scarring in 2 patients. The mean follow-up time was 13.5 months, with a range of 6-22 months. Nine (69.2%) of the lesions were completely controlled, 3 (23.1%) were mostly controlled, and 1 (7.7%) was partially controlled. The rates of completely and mostly controlled AVMs involving the jaws treated by SIAE, BWP, and curettage were 80% and 20%, respectively. The rates of completely, mostly, and partially controlled AVMs involving soft tissues treated by compartmentalization and sclerotherapy were 60%, 30%, and 10%, respectively (Table I). All of the patients had normal liver and kidney functions and normal lung fields on chest radiographs. DISCUSSION In this study, there were no patients with stage I or IV AVMs. We believe that stage I AVMs do not need to be treated, whereas stage II AVMs should be treated, because they often cause problems such as cosmetic concerns and compression of adjacent structures. Hemorrhage is the most common and serious symptom of stage III AVMs in the maxillofacial region, and controlling hemorrhage is the most important step in the treatment of maxillofacial AVMs.1 Subtotal excision or proximal ligation frequently results in rapid progression of the arteriovenous malformation. Thus, ligation of the feeding artery without removing the nidus should be avoided because other collateral vessels and quiescent AVMs will grow rapidly, possibly becoming bigger than before. Moreover, if the feeding artery of the AVM is ligated, further embolotherapy/sclerotherapy may be impossible because of the lack of a route for embolotherapy/sclerotherapy.3 Digital subtraction angiography can demonstrate the nidus, feeding vessels, and flow characteristics of
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AVMs and can determine the site of bleeding. SIAE involves selective embolization of the nidus of the AVM. First the minimal artery is embolized, and then the embolization proceeds from inside to outside the AVM. In the present study, 7 cases of stage III AVM of the mandible resulted in gingiva bleeding or uncontrollable hemorrhage in the alveolar socket; these patients underwent emergency SIAE, and the bleeding was controlled quickly and effectively. In this study, there were no major complications, such as facial nerve palsy, pulmonary embolism, deep vein thrombosis, and massive tissue necrosis. During SIAE, metal coils were used to block the artery supplying the AVMs to reduce its vascularity. Alternatively, polyvinyl alcohol particles can be used to cause blood to coagulate in the vessel lumen. Following partial obstruction of the vascular lumen, the blood flow was blocked, which resulted in necrosis of the endoepithelial cells of the vessel and proliferation of the fibrous tissue of the AVM. Motamedi et al.7 found that simple embolization was not successful in treating AVMs of the mandible and that surgical treatment was also needed. No patients with AVMs were cured by simple embolization.1 Computerized tomography can delineate the bony involvement of AVMs, and 3D-CT reconstruction may enhance the accuracy of preoperative planning, such as planning the approach to the lesion. We performed BWP of the bone cavity within 1 week after embolization, because if the interval is too long, the embolization materials would be absorbed and the AVMs might recanalize. The AVMs had formed a fibrous capsule in the bone cavity of the mandible by about 4 weeks after BWP of the bone cavity.1 After curettage, the bone cavity was filled with exogenous bone to induce osteogenesis and to maintain the architecture of the mandible while sparing the inferior alveolar nerve. The teeth, dental follicles, and erupted teeth can be preserved in most cases. Dissection of the jaws should be avoided. In the present study, we used BWP of bone cavities to control hemorrhage of the lesions in emergencies, and we performed curettage 4 weeks later. This markedly reduced the bleeding and allowed complete removal of the AVM without complications. The rates of completely and mostly involuted AVMs involving the jaws were 80% and 20%, respectively. Our experience with BWP of the bone cavity and curettage after SIAE demonstrates that this is safe and effective therapy. We believe that the technique saves the jaws while ensuring function, without complications. Chen et al.8 reported that compartmentalization followed by the injection of OK-432 and pingyangmycin into each compartment was a simple, safe, and reliable alternative treatment for massive venous malformations of the face and neck, and they used SIAE was an
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adjunct treatment for AVMs of the soft tissues.1 We performed compartmentalization and sclerotherapy after SIAE to interrupt the blood supply from the regional vascular network and to divide the AVMs into compartments by isolating blocks of tissue with considerably reduced flow. Subsequently, large doses of OK-432 and pingyangmycin were injected into each compartment, allowing “pooling” of the agents followed by thrombosis and solidification. Pooling ensures that the highly concentrated sclerosing agents have prolonged contact with the endothelial lining to maximize effectiveness. Sclerosing agents provoke a severe intimal inflammatory reaction that leads to thrombosis and shrinks the vascular anomaly.9 In the present study, the treatment of maxillofacial AVMs with OK-432 and pingyangmycin after compartmentalization was effective, with 6 lesions (60%) achieving complete control, 3 lesions (30%) becoming mostly controlled, and 1 lesion (10%) becoming partially controlled. For intralesional injection, OK-432 and pingyangmycin (bleomycin A5 hydrochloride) are preferable to other sclerosing agents such as absolute alcohol, sodium tetradecyl sulphate, and sodium morrhuate, because they are antineoplastic drugs in addition to sclerosing agents. OK-432 and bleomycin have been used to treat lymphatic and venous malformations.8,10 OK432 is secreted by some strains of Streptococcus pyogenes and possesses pyrogenic toxin superantigenicity. Superantigenic activation of T cells and monocytes stimulates the release of cytokines such as tumor necrosis factors alpha and beta, interleukin 1, and gammainterferon. OK-432 interacts directly with endothelial cells.11 Several inflammatory cytokines increase cellular immunity, leading to tumor eradication, and cause local inflammation, the formation of granulation tissue, and the disappearance of the vessel due to obliteration of its lumen. Pingyangmycin has an apoptotic effect on rapidly growing immature cells.12 The intralesional injection of pingyangmycin results in the detachment of endothelial cells and thickening of the vessel wall, which leads to lumen narrowing and occlusion. The theoretic reasoning behind choosing OK-432 and pingyangmycin for the intralesional injection of AVMs is sound. We speculated that compartmentalization after SIAE would allow high doses of OK-432 and pingyangmycin to be used, would allow the sclerosing agents to remain active in the lesions for a long time, and would allow the agents to have a synergistic effect on the AVM. No major complications occurred after the injection of OK-432 and pingyangmycin. Intravenous dexamethasone (0.1 mg/kg) and NS (60 mL/kg) were given for 3 days after surgery to control inflammation
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and prevent pulmonary fibrosis, which is a serious potential complication of pingyangmycin. Our multidisciplinary approach to the treatment of maxillofacial AVMs is reliable. SIAE was effective for controlling bleeding and as an adjunctive treatment for maxillofacial AVMs in children. SIAE followed by BWP of the bone cavity and curettage was a simple, safe, and effective method for treating AVMs of the jaws. SIAE followed by compartmentalization and the injection of OK-432 and pingyangmycin was a reliable alternative treatment for AVMs of the soft tissues in the maxillofacial region. REFERENCES 1. Chen W, Wang J, Li J, Xu L. Comprehensive treatment of arteriovenous malformations in the oral and maxillofacial region. J Oral Maxillofac Surg 2005;63:1484-8. 2. Niechajev I, Clodius L. Histologic investigation of vascular malformations of the face after transarterial embolization with Ethibloc and other agents. Plast Reconstr Surg 1990;86:664-71. 3. Rockman CB, Rosen RJ, Jacobowitz GR, Weiswasser J, Hofstee DJ, Fioole B, et al. Transcatheter embolization of extremity vascular malformations: the long-term success of multiple interventions. Ann Vasc Surg 2003;17:417-23. 4. Kohout MP, Hansen M, Pribaz JJ, Mulliken JB. Arteriovenous malformations of the head and neck: natural history and management. Plast Reconstr Surg 1998;102:643-54. 5. Lee BB, Bergan JJ. Advanced management of congenital vascular malformations: a multidisciplinary approach. Cardiovasc Surg 2002;10:523-33. 6. Loose DA. Surgical correction of vascular malformations of the lower extremity. Kongressbd Dtsch Ges Chir Kongr 2001;118: 507-15. 7. Motamedi MH, Behnia H, Motamedi MR. Surgical technique for the treatment of high-flow arteriovenous malformations of the mandible. J Craniomaxillofac Surg 2000;28:238-42. 8. Chen WL, Yang ZH, Bai ZB, Wang YY, Huang ZQ, Wang YJ. A pilot study on combination compartmentalisation and sclerotherapy for the treatment of massive venous malformations of the face and neck. J Plast Reconstr Aesthet Surg 2008;61:486-92. 9. Jackson IT, Keskin M, Yavuzer R, Kelly CP. Compartmentalisation of massive vascular malformations. Plast Reconstr Surg 2005;115:10-21. 10. Ogita S, Tsuto T, Tokiwa K, Takahashi T. Intracystic injection of OK-432: a new sclerosing therapy for cystic hygroma in children. Br J Surg 1987;74:690-1. 11. Roggiani M, Stoehr JA, Leonard BA, Schlievert PM. Analysis of toxicity of streptococcal pyrogenic exotoxin A mutants. Infect Immun 1997;65:2868-75. 12. Kullendorff CM. Efficacy of bleomycin treatment for symptomatic hemangiomas in children. Pediatr Surg Int 1997;12:526-8. Reprint requests: Dr. Wei-liang Chen Oral and Maxillofacial Surgeon Department of Oral and Maxillofacial Surgery Second Affiliated Hospital of Sun Yat-sen University 107 Yan-jiang Road 510120 Guangzhou [email protected]