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SCIENTIFIC A R T I C L E

Australian Dental Journal 1999;44:(3):187-194

Incidence of complicated healing and osteoradionecrosis following tooth extraction in patients receiving radiotherapy for treatment of nasopharyngeal carcinoma

Antonio Chi-kit Tong, BDS, FRACDS, FFDRCSI* Albert Chun-fung Leung , BDS, FRACDS Jason Chi-fung Cheng, BDS, FFDRCSI Jonathan Sham, MBBS, MD, DMRT, FRCR§

Introduction Osteoradionecrosis (ORN) of the jaw bones is a well known complication following tooth extraction in patients who have received radiotherapy to the head and neck region. In 1983, Marx identified the specific pathophysiology of ORN as being a defect of wound healing following tissue breakdown (trauma-induced or spontaneous) in hypovascularhypocellular-hypoxic tissue. The process not only affects irradiated bone, but radionecrosis of the soft tissue occurs concomitantly.1 It is generally accepted that meticulous preventive dental treatment should be planned for patients receiving radiotherapy to the head and neck region. However, it is not uncommon to encounter patients with poor dental conditions necessitating tooth extraction after radiotherapy. Under such circumstances,surgical trauma is kept to a minimum with antibiotic cover until adequate wound healing occurs. Despite these precautionary measures, ORN can still occur. In general, mandibular tooth extraction results in a greater risk of ORN compared with maxillary tooth extraction because of better vasculature of the maxilla. In Hong Kong and southern China, nasopharyngeal carcinoma (NPC) is one of the most common head and neck neoplasms. It was the third most common neoplasm in Hong Kong males in 1994/1995.2 In the Chinese population, there is an increasing incidence of NPC from the second decade of life and the peak incidence occurs in the fifth and sixth decades of life. Radiotherapy is the mainstay of treatment for NPC and this group of patients constitutes the majority of patients receiving radiotherapy to the head and neck region.

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Abstract A group of 43 patients requiring tooth extraction after radiotherapy for nasopharyngeal carcinoma (NPC) was studied retrospectively to determine the incidence of post-extraction complications. It was found that because of the method used in the delivery of radiation, extraction of maxillary posterior teeth resulted in the greatest risk of complications (28.9 per cent), including a 10.5 per cent risk of osteoradionecrosis (ORN). Based on the findings, a protocol was established for the dental care of such patients. It was concluded that when extraction of maxillary posterior teeth was necessary, prophylactic antibiotics were not sufficient to prevent the complication of delayed healing. The risk of ORN was 10.5 per cent within the field of maximal radiation dose. Hyperbaric oxygen may be the better choice of preventive measures. However, in view of the low risk of ORN, wholesale prescription of hyperbaric oxygen therapy may not be indicated. An additional patient who had tooth extraction two weeks prior to radiotherapy was included to show that if adequate time for wound healing was not allowed, ORN could develop.

Key words: Nasopharyngeal carcinoma, radiotherapy, tooth extraction, osteoradionecrosis. (Received for publication June 1997. Revised March 1998. Accepted March 1998.)

*Senior Dental Officer, Department of Health, Hong Kong Government, Hong Kong. Dental Officer, Department of Health, Oral Maxillofacial Surgery and Dental Unit, Pamela Youde Eastern Nethersole Hospital, Hong Kong. Consultant Oral and Maxillofacial Surgeon,Department of Health, Oral Maxillofacial Surgery and Dental Unit, Pamela Youde Eastern Nethersole Hospital, Hong Kong. §Department of Radiation Oncology, The University of Hong Kong, Queen Mary Hospital,Hong Kong.

Australian Dental Journal 1999;44:3.

Lateral Wedged Fields ­ Nasopharyngeal Treatment Field ­ Cervical Shielding Field ­ Cervical and orbital

Fig. 1. ­ Split field technique for radiotherapy of NPC.

To the authors' knowledge, there is currently no available information from the literature regarding the incidence of ORN following tooth extraction for NPC patients receiving radiotherapy. Local dental practitioners and oral surgeons generally follow the guidelines from the English literature for management of patients who have received radiotherapy, mainly for other head and neck tumours. In the present study, a group of patients was reviewed who had received radiotherapy for NPC and required tooth extraction. The study aimed at identifying the incidence of complications, correlating the occurrence of complications in wound healing with the method of radiotherapy, and considering possible treatment measures besides the use of hyperbaric oxygen which was not available for medical treatment in Hong Kong until early 1995. Although Marx demonstrated that hyperbaric oxygen therapy was the most cost-effective means of treating ORN,3 the problem with hyperbaric oxygen therapy was that of manpower.The hyperbaric oxygen facilities in Hong Kong are owned and manned by the Fire Services Department which is located in a military base with restricted access. An occupational health doctor is required to supervise the treatment and nursing staff is required to accompany the patient before, during and after the treatment. Transportation of the patient and the nurse is usually by ambulance which is in heavy demand. Only three patients under the authors' care have been sent for hyperbaric oxygen because of the extensive manpower involved and liaison between different departments. Despite all of these difficulties, the authors are of the opinion that hyperbaric oxygen therapy has an important role to play in the management of ORN but its use should not be indiscriminate.

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In the present study, the authors aim to establish a protocol that will be of practical relevance for dental practitioners and oral surgeons having to deal with patients with NPC, especially when hyperbaric oxygen is not readily available. This will also be useful for dentists who do not encounter such patients routinely. Materials and methods A group of 43 patients having radiotherapy for NPC who required post-irradiation tooth extraction was studied retrospectively. One additional patient who had undergone extractions of left maxillary molars two weeks before radiotherapy and subsequently developed extensive ORN of the left posterior maxilla was also included. This particular case is discussed later in this paper. The patients were treated with one of two radiotherapy techniques,4 and the tumour dose was 6600 to 7000 cGy except for two patients who received two courses of radiotherapy. Technique 1 was a split field technique (Fig. 1). The primary tumour in the nasopharynx was treated with two lateral opposing facial fields and one anterior facial field, and the neck lymphatics were treated with matching anterior cervical fields. The aim of using the three-field technique was to spare the laterally situated structures from high dose irradiation, so that the parotid glands, lateral part of temporal lobes, the masseter muscles and the ascending ramus of the mandible received a lower dose than the tumour (about 70-80 per cent of the tumour dose), while the posterior part of maxilla received the full tumour dose.

Australian Dental Journal 1999;44:3.

Treatment Field Shielding Field

Fig. 2. ­ (a), (b) Two-phased technique for radiotherapy of NPC.

For Technique 2 (Fig. 2), the primary tumour and the neck lymphatics were initially treated in one volume with a pair of lateral opposing faciocervical fields, with Phase 2 of the treatment being changed to split field as used in Technique 1 when the spinal cord tolerance dose was being reached. Technique 1 was designed for small tumours, as the high dose zone was the area of cross-firing of the three beams (two lateral and one anterior where the anterior was usually 80 mm wide) and was considered a better technique in terms of oral hygiene. In contrast, Technique 2 was designed for more extensive tumours where the initial part of treatment covered most of the structures adjacent to the nasopharynx by two lateral beams, while the second part of the treatment was the same as Technique 1. In essence, the ascending ramus of the mandible, the masseter muscles and the temporomandibular joints were exposed more to radiation in

Technique 2 and thus may be considered inferior to Technique 1 in terms of prevention of ORN. When post-irradiation tooth extraction was considered absolutely necessary (due to advanced dental caries or periodontal disease), the extraction was carried out with as little trauma as possible. For single tooth extraction, suturing was performed to decrease the soft tissue defect; primary closure was not attempted. For multiple tooth extractions, the interseptal bone was trimmed to allow buccol-lingual compression of the alveolus to achieve primary closure. Post-operatively, antibiotics (usually oral penicillin 250 mg four times a day) were prescribed for at least one week or even longer until complete epithelization of the socket. A 0.2 per cent chlorhexidine gluconate mouthrinse was prescribed for one to two weeks after the extraction. The patients were closely followed up after the extraction. When healing was considered not satisfactory as

Table 1. Incidence of complicated wound healing (including ORN) in different areas of the maxilla and the mandible following tooth extraction

No of teeth extracted Total Location Anterior maxilla Maxillary premolars Maxillary molars Anterior mandible Mandibular premolars Mandibular molars

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No and percentage with healing problem 15 (6.3%) 0 0 11 (28.9%) 0 2 (5.3%) 2 (7.4%)

No and percentage of sockets with ORN 4 (1.7%)

237 42 36 38 56 38 27

4 (10.5%)

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Table 2. Age, sex distribution and timing of post-radiotherapy extractions

Case 1 2 3 4 5 6 7 8 9 10 Age 64 75 41 68 59 58 54 48 73 55 Sex F F F M F M M M M F Timing of extraction* (Related to time of RT) 11 years post-RT 5 years post-RT 1 year post-RT 3 years post-RT 4 years post-RT 2 years post-RT 5 years post-RT 4 years post-RT 2 years post-RT 2 weeks pre-RT

*Most of the extractions were performed within 2 to 5 years after radiotherapy. Patient who had tooth extraction 2 weeks before radiotherapy.

judged by the presence of exposed bone or incomplete soft tissue healing one month or more after the tooth extraction, surgical intervention for debridement and primary wound closure was instituted. Osteoradionecrosis was considered to be present when failure of wound healing with exposed bone persisted beyond six months. Results Of the 43 patients, nine (21 per cent) developed complications in wound healing necessitating further intervention. The majority of these patients presented with delayed socket healing. The overall incidence of complication was 6.3 per cent (15 out of 237) when individual tooth extraction was considered, while the incidence of ORN (based on the definition of unhealed exposed bone persisting beyond six months) was 1.7 per cent overall and 10.5 per cent for extraction of posterior maxillary teeth. The incidence of complicated healing in different areas of the jaws is outlined in Table 1. For the nine patients with complicated healing, all the extractions were performed non-surgically either with forceps or elevators under local anaesthesia.

The age, sex distribution and timing of postradiotherapy extractions are set out in Table 2. Case 10 was a patient who had tooth extraction from the left posterior maxilla two weeks before radiotherapy and who subsequently developed ORN of the extraction site after radiotherapy. The extracted teeth, method and dosage of radiotherapy, together with post-extraction complications, are set out in Table 3. The results indicate that extraction of anterior teeth (incisors and canines) in both the maxilla and the mandible was not associated with any risk of complicated healing when a prophylactic antibiotic (penicillin 250 mg four times a day for a week) was used.The risk associated with extraction of maxillary and mandibular premolars and mandibular molars is small and the problems were manageable with relatively simple measures of wound debridement and closure. There is a significant risk associated with the extraction of maxillary molars which received directly the full dose of radiation. Moreover, the further posterior the tooth lies in the maxilla, the greater the risk. The major complications in this series were related to the upper third molars. The two patients with delayed healing after extractions of mandibular posterior teeth were noted to have Technique 2 as the method of radiotherapy and the dosages were both 6100 cGy. Discussion Considerable variation in the incidence of ORN is noted among surveys from different centres, ranging from 2 to 85 per cent.5 It is understandable that a correlation exists between the incidence of ORN and the total radiation received.The overall incidence of ORN decreased from around 12 per cent to 5.4 per cent after 1968 when megavoltage therapy became available.6 Direct comparison of the figures appeared inappropriate in view of the existence of other

Table 3. The extracted teeth, method and dosage of radiotherapy together with post-extraction complications

Case 1 2 3 4 5 6 7 8 9 10 Teeth extracted 13, 14,18, 21,22,23, 24,25, 31, 32 35,37, 38, 41,42, 43,44, 45,46, 47 36,37,46, 47 11,17,21, 22,27,43, 47 32,33, 34, 35,44 16,17,18, 26,27, 28,37,38, 44 24,25, 26, 27,44 21,23, 31, 32,34, 35,36, 44,45, 46 18 27,28, 13, 17, 33 11, 16,17, 21, 23,27, 37,46 Radiotherapy technique 1 2 1 2 2 2 2 2 2 1 Dosage (cGy) 5950 6100 7350* 6100 6100 6100 11 250* 6100 6100 7000 Complications 18 wound healing incomplete 2 months after extraction 46, 47 wound infection 1 month after extraction Bilateral oronasal fistulae over 18 and 28 regions (2 3 cm) diagnosed 2 years after extraction Delayed wound healing of 34, 35 sockets 16, 17,18 sockets healed very slowly ORN over 26, 27 sockets Sequestrum in 18 region Wound healing incomplete 1 month after extraction Sharp bony edge buccal side of 27 socket Oronasal fistula present in left maxilla

*Denotes 2 courses of radiotherapy given altogether. Patient who had tooth extraction 2 weeks before radiotherapy.

190 Australian Dental Journal 1999;44:3.

variables (such as site of malignancy, patients' dental status and awareness, and the radiotherapeutic mode and technique). However, there is a general consensus that a higher incidence is found when the tumour has a close proximity to bone. Moreover,the mandible is more frequently affected than the maxilla and dentate patients more often than edentulous patients. To a certain extent, the factors mentioned above affected the treatment philosophy of the dental practitioners in the preparation of the mouth for irradiation. Daland7 favoured rendering the patient edentulous and so did Watson and Scarborough8 before the days of antibiotics. Less drastically, some clinicians recently advocated removal of those teeth in the primary field of irradiation. A third and more current school of thought is the conservation of as many functional teeth as possible for the patient. Provided continuous preventive, restorative and periodontal care are available, sound teeth in the path of irradiation ought to be maintained in suitable patients when dental rehabilitation after radiotherapy is taken into consideration. Post-irradiation dental extraction has generally been considered a potentially hazardous procedure. Murray and co-workers9,10 found that seven out of eight patients who had post-irradiation extractions were subsequently afflicted with ORN; and so were the 11 out of 18 patients described by Morrish et al.11 Beumer et al.12 reported a 22 per cent incidence of bone exposure for three months or longer in 72 postradiation extraction episodes. They reported that the mandible sustained a significantly higher risk of ORN than the maxilla (29 per cent against 11 per cent); the risk was further increased when the radiation dose exceeded 6500 cGy and the treatment volume covered not less than 75 per cent of the body of the mandible.The authors concluded that in view of the undesirably high rate of ORN, root canal therapy was preferable to dental extraction in the management of dental infection after radiotherapy. Epstein et al.13 compared the incidence of ORN in relation to extractions before and after radiotherapy. They were able to demonstrate a higher risk in postirradiation extraction than pre-irradiation extraction, which was in accordance with the results reported by Beumer et al.14 On the other hand, there were clinicians who claimed the use of antibiotics enabled post-irradiation extraction to be accomplished with minimal risk. Carl et al.15 reported uneventful healing in the majority of their group of 47 irradiated patients requiring extraction of 187 teeth. They emphasized atraumatic extraction of no more than two or three teeth at one time. Solomon and co-workers16 described similar f avourable results. Traditionally, different treatment modalities of ORN are categorized into either non-surgical or

Australian Dental Journal 1999;44:3.

surgical means. In real practice, the management of patients afflicted with ORN of the jaws usually consists of a combination of different modalities and will be determined by factors such as the size of the defect, the signs and symptoms of the patient and the cosmetic and functional derangement consequent to the complication. In addition to oral hygiene maintenance with routine dental follow-up, non-surgical or `conservative' therapy includes nutritional support, topical medicaments, systemic antibiotics and hyperbaric oxygen. Rankow and Weissman17 further emphasized the importance of avoiding irritation from prosthetic appliances and hot, cold, rough or spicy foods. Besides aiding in prevention of sepsis of the radionecrotic wound, topical medicaments can provide symptomatic relief for the patient. A variety of mouthwashes has been recommended by different authors. Those commonly accepted include warm saline, sodium bicarbonate and 0.2 per cent chlorhexidine solution.The use of medicated packs has also been advocated. Application of BIPP (bismuth iodoform paraffin paste) on ribbon gauze is emphasized as a valuable short-term measure in patients prior to definitive treatment. 18 Since Marx re-investigated the role of bacteria in the pathogenesis of ORN, the use of systemic antibiotics as the principal therapeutic component has been questioned. High doses of penicillin or tetracycline had been prescribed for prolonged periods. While not all cases of ORN are infected, long-term antibiotics carry the risk of development of resistant strains. Attainment of a high therapeutic level of drug can also be impeded by the extent of necrosis and the poor vascularity of the surrounding tissues resulting from the post-irradiation endarteritis obliterans. Nevertheless, antibiotic therapy is useful as an adjunctive treatment modality and it is a common practice to provide antibiotic cover for post-irradiation extractions. Recent treatment concepts have focused on revascularization of the irradiated tissues. No doubt hyperbaric oxygen therapy has been the greatest advance. By stimulating angiogenesis, promoting fibroblastic activity and collagen synthesis, hyperbaric oxygen (HBO) enhances the healing of ischaemic wounds. The research of Hohn19 further demonstrated its promotion of leukocytic antibacterial activity which would be advantageous in the presence of infection. Hyperbaric oxygen has been effectively employed as an adjunctive treatment of ORN of the jaw bones. Marx et al. even demonstrated its successful use as a preventive measure in a clinical study.20 Their study showed that when mandibular teeth within the radiation field were extracted, the use of pre- and post-operative antibiotics with an atraumatic extraction technique

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resulted in a complication rate of 29.9 per cent whereas the use of hyperbaric oxygen reduced the risk of development of ORN to 5.4 per cent. Surgical procedures range from simple sequestrectomy to radical resection with or without reconstruction. In general, severe, intractable pain and refractory, progressive ORN which fails to respond to non-surgical measures are regarded as primary indications for surgical intervention. In 1983, Marx proposed a staging protocol (which was modified subsequently)21 combining surgery and hyperbaric oxygen for more aggressive treatment of ORN. He was able to achieve complete resolution in all 58 cases.22 Marx's protocol consists of three treatment stages of advancing clinical severity. All patients who meet the criteria of ORN (exposed bone present for six months or longer with no healing) begin Stage 1 treatment. Stage 2 treatment is begun if the disease does not resolve. More advanced diseases, for example, pathologic fractures, fistulas or radiographic evidence of osteolysis to the inferior border, begin directly with Stage 3 treatment and usually require resection. In Stage 1, each patient receives 30 HBO treatments at 2.4 ATA (atmospheres absolute) for 90 minutes each. If clinical improvement is seen, the patient receives another 10 treatments. In Stage 2, the patient receives 30 treatments, followed by a transoral alveolar sequestrectomy; while in Stage 3, the patient undergoes a transoral partial jaw resection after the initial 30 treatments and reconstruction and rehabilitation is carried out as early as possible. A more recent study23 reported successful treatment of 20 patients out of a group of 29. While addressing the underlying pathophysiologic problem of the radionecrotic tissues, hyperbaric oxygen therapy in combination with moderate surgical procedures may spare the less severely affected patients the need for major surgical procedures. The present study showed that the risk of complicated wound healing and ORN after extraction can be explained by the radiation dose received by the bone and socket in which the teeth were situated. Extraction of teeth in areas outside the high radiation dose areas can be safely undertaken with antibiotic cover. Extraction of teeth in those areas irradiated to a high dose needs to be undertaken with care. The findings of the present study are at variance with the reported experience that the mandible is the higher risk area for development of ORN and other wound complications. The difference between the present findings and the reported experience is in the location of the tumour and the radiation technique that delivered a high dose to different parts of the maxilla and mandible. The findings of the present study are similar to those of Marx20 in that when teeth directly within the

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field of radiation therapy were extracted, prophylactic antibiotic treatment alone was associated with a significant risk of delayed wound healing. However, the incidence of frank ORN was lower than that of Marx's study (10.5 per cent in this study compared with 29.9 per cent in Marx's study).Although hyperbaric oxygen may be a better preventive measure, this was not available in the local community for medical purposes before early 1995.The finding that most of the complications of delayed wound healing (even in the posterior maxilla which received the maximal radiation dose) could be managed by simple wound debridement and primary closure, questions the desirability of routine hyperbaric oxygen treatment which is not without side effects and may not be economical. The authors had to resort to the use of antibiotics and careful monitoring and tended to intervene at an early stage by closing any delayed healing wound by local flaps (for example, buccal advancement flaps). The patient who underwent tooth extraction two weeks before radiotherapy and subsequently developed extensive ORN of the left posterior maxilla was included to show that perhaps a longer period of healing should be allowed before the commencement of radiotherapy. Marx and Johnson24 suggested a minimum of 21 days based on a study in 1987. In daily practice, this optimum waiting time is often compromised by the urge of both the patients and the Radiotherapy and Oncology Department to start treatment of the tumour as soon as possible. In the cases of established ORN with extensive oronasal fistulae (Cases 2 and 4), the use of the buccal f at pad was limited by the size of the defect and atrophy of the fat following irradiation. Therefore, this may not be the ideal tissue to use when the defect is large. Even though the defect could be closed initially with the buccal fat pad in Case 2, breakdown of the fatty tissue ensued. The defect was subsequently closed with satisfactory healing under peri-operative antibiotic cover after extensive sequestrectomy using the ipselateral temporalis muscle flap. Based on the findings of this study, the following protocol for the dental care of patients receiving radiotherapy for NPC was established: Before radiotherapy 1. Dental examination, institution of preventive measures,including instructions on oral hygiene and the use of a fluoride mouthrinse. 2. Completion of restorative treatment. 3. Extraction of all third molars (functional or non-functional) and any other teeth of questionable prognosis. Deeply impacted teeth which are completely covered by bone and without any associated pathosis are left undisturbed.

Australian Dental Journal 1999;44:3.

4. Extraction of all non-functional molars without opposing teeth. Formation of food traps following over-eruption of these teeth results in root surface caries in contact areas which are difficult to manage. 5. Extraction of all second molars unless the patient is keen to maintain meticulously good oral hygiene and has demonstrated the ability to do so. 6. Extraction of all molars if the patient's oral hygiene is judged to be unsatisfactory and is unlikely to change. 7. Reassessment immediately prior to radiotherapy to ensure that the patient is dentally fit. After radiotherapy Frequent dental follow-up to reinforce palliative and preventive measures. At each recall visit: 1. Check for mucositis. This will only last for two to three weeks after completion of radiotherapy. If present, prescribe Difflam (benzydamine hydrochloride) or thymol gargle. 2. Check for xerostomia. The effect of radiotherapy on salivary flow is usually long-lasting and xerostomia almost certainly will follow. 3. Watch for cervical caries. Encourage frequent sips of water. Patients have found non-sucrose based chewing gum helpful in improving xerostomia. 4. Check trismus. Jaw opening exercise should commence as soon as possible after radiotherapy to prevent fibrosis of the jaw muscles and the temporomandibular joint. 5. Check susceptibility to caries. Encourage more frequent fluoride mouthrinses. Apply fluoride varnish or gel where indicated. Restore if cavities are found. If tooth extraction is considered absolutely necessary, it will be quite safe to extract maxillary and mandibular anterior teeth. Extraction of premolars and mandibular molars are not associated with significant risk provided that an atraumatic technique and antibiotic cover are used. Careful follow-up until completed healing is necessary. Extraction of maxillary posterior teeth is best performed by specialist oral and maxillofacial surgeons. Antibiotic cover alone is not sufficient to prevent delayed healing or osteoradionecrosis. The protocol of Marx for giving hyperbaric oxygen should be considered.When complications in healing occur, early inter vention with an attempt at closing any defect with a local flap is indicated. Extensive defects will require sequestrectomy and major reconstructive surgery. Conclusions The risk of complicated healing and osteoradionecrosis following tooth extraction in patients who have had radiotherapy for nasopharyngeal carcinoma

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varies in different parts of the jaws. The greatest risk is associated with the extraction of maxillary posterior teeth especially the third molars. Prophylactic antibiotics and a careful technique are not sufficient to reduce the development of delayed healing or osteoradionecrosis. When the ideal treatment modality of hyperbaric oxygen is not available, it is advisable to monitor healing carefully and to intervene at an early stage when healing is judged to be compromised. Wound debridement and primary closure of soft tissue over the tooth socket by local flaps are able to prevent further wound breakdown. Acknowledgement The authors would like to acknowledge Dr S. W. Yan, Consultant In Charge, Dental Services, Department of Health, Hong Kong Government, for allowing the use of patient data in the preparation of this study. References

1. Marx RE. Osteoradionecrosis: A new concept of its pathophysiology. J Oral Maxillofac Surg 1983;41:283-288. 2. Hong Kong Government, Department of Health.Annual report 1994/1995. Hong Kong: Hong Kong Government, Department of Health, 1995. 3. Marx RE. Osteoradionecrosis of the jaws:Review and update. Hyperbaric Oxygen Rev 1984;5:78. 4. Ho JHC. Nasopharynx. In: Halman KE, ed. Treatment of cancer. London: Chapman and Hall, 1982:249-267. 5. Lambert PM, Intriere N, Eichstaedt R. Management of dental extractions in irradiated jaws: A protocol with hyperbaric oxygen therapy. J Oral Maxillofac Surg 1997;55:268-274. 6. Clayman L.Management of dental extractions in irradiated jaws: a protocol without hyperbaric oxygen therapy. J Oral Maxillofac Surg 1997;55:275-281. 7. Daland EM. Radiation necrosis of the jaw. Radiology 1949;52:205-215. 8. Watson WL, Scarborough JE. Osteoradionecrosis in intraoral cancer. Am J Roentgenol 1938;40:524-534. 9. Murray CG, Herson J, Daly TE, Zimmerman S. Radiation necrosis of the mandible: a 10 year study. Part I. Factors influencing the onset of necrosis. Int J Radiat Oncol Biol Phys 1980;6:543-548. 10. Murray CG, Herson J, Daly TE, Zimmerman S. Radiation necrosis of the mandible: a 10-year study. Part II.Dental factors; onset, duration and management of necrosis. Int J Radiat Oncol Biol Phys 1980;6:549-553. 11. Morrish RB, Chan E, Silverman S Jr, Meyer J, Fu KK, Greenspan D. Osteonecrosis in patients irradiated for head and neck carcinoma. Cancer 1981;47:1980-1983. 12. Beumer J III, Harrison R, Sanders B, Kurrasch M.Preradiation dental extractions and the incidence of bone necrosis. Head Neck Surg 1983;5:514-521. 13. Epstein JB,Giuseppa R, Wong FLW, Spinelli J,Stevenson-Moore P. Osteonecrosis: Study of the relationship of dental extractions in patients receiving radiotherapy. Head Neck Surg 1987;10:48-54. 14. Beumer J III, Silverman S Jr, Benak SB Jr . Hard and soft tissue necroses following radiation therapy for oral cancer. J Prosthet Dent 1972;27:640-644. 15. Carl W, Schaef NG, Sako K. Oral surgery and the patient who has had radiation for head and neck cancer. Oral Surg Oral Med Oral Pathol 1973;36:651-657. 16. Solomon H, Marchetta F, Wilson R, Miller R, Detolla H. Extraction of teeth after cancericidal doses of radiotherapy to the head and neck.Am J Surg 1968;115:349-351.

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17. Rankow RM, Weissman B. Osteoradionecrosis of the mandible. Ann Otol Rhinol Laryngol 1971;80:603-611. 18. Morton ME, Simpson W. The management of osteoradionecrosis of the jaws. Br J Oral Maxillofac Surg 1986;24:332-341. 19. Hohn DC.Oxygen and leukocyte microbial killing.In: David JC, Hunt PK, eds. Hyperbaric oxygen therapy. Bethesda: Undersea Medical Society, 1977:101. 20. Marx RE, Johnson RP, Kline SN. Prevention of osteoradionecrosis: a randomized prospective clinical trial of hyperbaric oxygen versus penicillin. J Am Dent Assoc 1985;111:49-54. 21. Johnson RP, Marx RE, Buckley SB. Hyperbaric oxygen in oral and maxillofacial surgery. In: Worthington P, Evans JR, eds. Controversies in oral and maxillofacial surgery. Philadelphia: Saunders,1994:107-126. 22. Marx RE.A new concept in the treatment of osteoradionecrosis. J Oral Maxillofac Surg 1983;41:351-357.

23. van Merkesteyn JPR, Bakker DJ, Borgmeijer-Hoelen AMMJ. Hyperbaric oxygen treatment of osteoradionecrosis of the mandible. Experience in 29 patients. Oral Surg Oral Med Oral Pathol 1995;80:12-16. 24. Marx RE, Johnson RP. Studies in the radiobiology of osteoradionecrosis and their clinical significance.Oral Surg Oral Med Oral Pathol 1987;64:379-390.

Address for correspondence/reprints: Dr Antonio Tong Chi Kit, Oral Maxillofacial Surgery and Dental Unit, A1, Queen Mary Hospital, 102, Pokfulam Road, Hong Kong.

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