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174]

Review Article
Maxillofacial osteoradionecrosis
Amit T. Suryawanshi, S. N. Santhosh Kumar, R. S. Dolas, Ruchi Khindria,
Vivek Pawar, Manju Singh

ABSTRACT
Department of Oral and Osteoradionecrosis is a severe and delayed radiation‑induced injury, characterized by bone tissue necrosis and
Maxillofacial Surgery, failure to heal. Cases of osteoradionecrosis present to the clinician with features of pain, drainage, and fistulation
DPU, Dr. D. Y. Patil of the mucosa or skin related to exposed bone in the previously irradiated area. The tumour size and location,
Dental College and radiation dose, occurrence of local trauma, dental extractions, infection, immune defects, and malnutrition are
Hospital, Pimpri, Pune,
predisposing factors. A better understanding of risk factors leading to the development osteoradionecrosis
Maharashtra, India
and of the underlying pathophysiology may improve the ability of the clinician to prevent the occurrence and
help improve the prognosis of this complication. Although the frequency of osteoradionecrosis has declined
since the introduction of newer methods of radiotherapy, this review focuses on the etiology, pathophysiology,
Address for correspondence: clinical features, radiological features, diagnosis, and treatment modalities including the newer modalities.
Dr. Amit Suryawanshi,
E‑mail: amitsuryawanshi999
@gmail.com KEY WORDS: Jaws, management, osteoradionecrosis, physiopathology, risk factors

Introduction Historical perspective

T he global incidence of oral cancer is 5,00,000 cases

per year with mortality of 2,70,000 cases per year. The
incidence of oral cancer in India is 40% among all cancers and
In 1922, Regaud published the first report about osteoradionecrosis
of jaws after radiotherapy.[4] In 1926, further description of
osteoradionecrosis was given by Ewing under the name Radiation
about 1,00,000 patients suffer from oral cancer in any year. Osteitis.[5] In 1970, Meyer classified osteoradionecrosis as one
Oral cancer is responsible for 7% of all cancer deaths in males special type of osteomyelitis. In 1975, Mainous advocated the
and 3% in females.[1] use of hyperbaric oxygen therapy (HBO) for late radiation tissue
injury. In 1983, Robert Marx proposed the hypoxic, hypocellular,
The recent protocol for management of oral cancer includes and hypovascular theory as a new way of understanding
multimodal therapy, such as surgery with radiotherapy and/or the pathophysiology of osteoradionecrosis. In 1992, Harris
chemotherapy. Radiation therapy is one of the major treatment introduced the use of Ultrasound as one of the modes to treat
modalities for the management of oral malignancies. Like with osteoradionecrosis.[6] In 1998, Marx gave the 30/10 protocol that
any treatment modality, even radiation therapy is associated with was employed in the treatment of established osteoradionecrosis.
various complications. A long‑term side effect of radiotherapy In 2004, Delanian and Lefaix put forward a new theory named
that is also the most serious is osteoradionecrosis.[2,3] Literature radiation‑induced fibrosis that accounts for the damage to
reveals many terminologies to represent the same disease, such normal tissues, including bone after radiotherapy.[7]
as radiation osteitis, radio‑osteonecrosis, radiation osteomyelitis,
osteomyelitis of irradiated bone, osteonecrosis, radio‑osteomyelitis, Definitions
septic osteoradionecrosis, and post‑radiotherapy osteonecrosis.[4]
In literature, osteoradionecrosis has been defined in many
This review focuses on the general information on maxillofacial ways [Table 1].[8,9] However, the authors feel that the definition
osteoradionecrosis for general practitioners. given by Wong, Wood, and McLean (1997)[8] is the most
appropriate and complete:
Access this article online
Quick Response Code: “A slow‑healing radiation‑induced ischemic necrosis of bone
Website:
with associated soft tissue necrosis of variable extent occurring
www.jdrr.org
in the absence of local primary tumour necrosis, recurrence, or
metastatic disease that may or may not:
DOI: i. Be superinfected (and accompanied by fistulation or cellulitis)
10.4103/2348-3172.126171 ii. End in pathologic fracture
iii. Resolve without surgery, hyperbaric oxygen therapy or both.”

How to cite this article: Suryawanshi AT, Kumar SS, Dolas RS, Khindria R, Pawar V, Singh M. Maxillofacial osteoradionecrosis. J Dent Res Rev 2014;1:42-9.

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Suryawanshi, et al.: Maxillofacial osteoradionecrosis

Classification and staging systems • Marx’s Hypoxic, hypocellular, and hypovascular theory[20]
• Delanian’s Radiation‑induced fibroatrophic theory.[21]
There have been several staging or scoring systems that have
been proposed. These systems are based on response to HBO Meyer’s radiation, trauma, and infection theory
therapy, degree of bone damage, clinical–radiological findings,
length of bone exposure through the overlying skin or mucosa, In 1970, in an excellent monograph on infectious disease of the
and treatment needed [Tables 2 and 3].[8‑15] jaws, Meyer defined the classic triad of osteoradionecrosis as
radiation, trauma, and infection [Figure 1].[19] Meyer portrayed that
Risk factors the trauma provided the portal for invasion by oral microbiological
flora into the underlying irradiated bone. Meyer’s theory lasted
The existing articles in literature fail to give an exact etiology
for a decade and became the foundation for the popular use of
for osteoradionecrosis. The etiology of osteoradionecrosis is
antibiotics with surgery to treat osteoradionecrosis.[19]
considered to be multifactorial. These factors may increase the risk
of the patient for development of osteoradionecrosis. The factors
are classified into four groups as shown in Table 4.[15‑18] Marx’s hypoxic, hypocellular, and hypovascular theory

Pathophysiology Robert E Marx in his landmark study noted that there was no
injury before the onset of osteoradionecrosis in 35% of his cases.
The pathophysiology of osteoradionecrosis is not very clear till He also found that composite irradiated tissues were more hypoxic
date. However, literature reveals three theories that have been than those that had not been irradiated [Figure 2].[20] Marx
put forward since 1970, as mentioned in the following: concluded that “Osteoradionecrosis is not a primary infection
• Meyer’s Radiation, trauma and infection theory[19]
Table 2: Classification systems of osteoradionecrosis
Table 1: Definitions of osteoradionecrosis Year Authors Basis for classification
Year Author(s) Definition 1983 Coffin’s classification[10] Based on the extent of involvement
1983 Marx[8] An area of exposed bone greater Minor and Major
than 1 cm in a field of irradiation 1983 Marx classification[8] Based on time period between
that had failed to show any evidence radiation therapy and occurrence of
of healing for at least 6 months osteoradionecrosis
1983 BeumerIII, Harrison, An exposure of bone of the maxilla Type I-III
Sanders and Kurrasch[9] or mandible within the radiation 1983 Marx staging[8] Based on the treatment modalities
treatment volume persisting for involved along with HBO therapy
more than 3 months or longer Stage I-III
1986 Morton and Simpson[9] A loss of soft tissue integrity and 1986 Morton and simpson’s Based on the duration of occurrence
exposure of radiation damaged bone Classification[11] of osteoradionecrosis
1987 Marx and Johnson[9] An exposure of nonvital irradiated Minor, Moderate and Major
bone, which fails to heal without 1987 Epstein’s stages[10] Based on the progress of the disease
intervention Stage I-III
1987 Epstein, Rea, An ulceration or necrosis of the 1995 Late effects of normal Based on subjective symptoms and
Wong, Spinelli and mucous membrane (In the absence tissue/ Somatic objective signs of osteoradionecrosis
Stevenson-Moore[9] of recurrent or metastatic disease), objective management Grade 1-4
with exposure of necrotic bone for analytic (SOMA) scale[12]
more than 3 months 1997 Clayman’s Based on the presence/absence of
1989 Widmark, Sagne and A non healing mucous or cutaneous classification[13] soft tissue break down
Heikel[9] ulcer with denuded bone, lasting for Type I and II
more than 3 months 1998 Radiation therapy Based on the severity of bone
1990 Koka, Deo, Lusinichi, A persistent ulceration with oncology group morbidity
Roland and Schwaab[9] exposure of devitalised bone, scoring[12] Grade 0-5
cellulitis, fistula and a pathologic 2000 Store and Boysen’s Based on the extent of involvement
mandibular fracture. Patients staging[11] of soft and hard tissues
tumour free at primary site Stage 0-3
1992 Harris[9] Exposed and necrotic bone 2002 Kagan and Schwartz’s Based on the clinical assessment
associated with ulcerated or staging[14] and physical findings of
necrotic surrounding soft tissue osteoradionecrosis
which persists for greater 3 months Stage I-III
in an area that had been previously 2003 Notani et al’s For mandibular osteoradionecrosis
irradiated (not caused by tumor Classification[12] after clinical examination and
recurrence) orthopantogram
1993 Mirante and A loss of viable bone resulting from Class I-III
Urken et al.[9] radiation therapy 2009 National cancer institute Based on clinical presentation of
1995 Van Merkesteyn, Bakker A bone and soft tissue necrosis common terminology osteoradionecrosis
and Borgmeijer-Hoelen[9] of 6 months duration excluding criteria (version-IV)[12] Grade 1-5
radiation-induced periodontal
LENT: Late effects of normal tissue, SOMA: Somatic objective
breakdown
management analytic

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Suryawanshi, et al.: Maxillofacial osteoradionecrosis

Table 3: Classification of osteoradionecrosis

Year Classification Stages/ Description Management
grades
2002 Kagan and Schwartz’s Stage I Minimal soft tissue ulceration and limited exposed Conservative management
staging[15] cortical bone
Stage II Localized involvement of the mandibular cortex and Conservative management or minor
underlying medullary bone surgical procedures
Stage II a Minimal soft tissue ulceration
Stage II b Presence of an oro-cutaneous fistula and mild soft tissue
necrosis
Stage III Full thickness involvement of the bone, including the Surgical intervention, including bone and/
inferior border. Pathological fracture may also be present or soft-tissue replacement
2009 Bone toxicity according Grade 1 Asymptomatic Clinical or diagnostic observations only;
to the National Cancer intervention not indicated
Institute Common
Terminology Criteria[12]
Grade 2 Symptomatic Medical intervention indicated (e.g.,
topical agents); limiting instrumental ADL
Grade 3 Severe symptoms Limiting self-care ADL; elective operative
intervention indicated
Grade 4 Life-threatening consequences Urgent intervention indicated
Grade 5 Death
ADL: Activities of daily living

Table 4: Risk factors of osteoradionecrosis

Type of risk factors Risk factors Description of risk factors
[15]
Patient related Gender Male predominance (male:female=1.6:1)
factors Age[16] Common in elderly patients
Race[15] Common in whites (74%)
Tumour-related Site[15] The oral cavity and oropharynx comprised the vast majority of primary tumors leading to
factors osteoradionecrosis of the jaws
Histopathology[17] Squamous cell carcinoma is more prone to lead to the occurrence of osteoradionecrosis
Stage[18] As the stage of carcinoma increases the risk for development of osteoradionecrosis increases
Size[16,17] Larger tumours were associated with higher incidence of osteoradionecrosis
Treatment-related Radiotherapy setting[15,18] Patients undergoing adjuvant radiotherapy had more risk for developing osteoradionecrosis
factors Radiotherapy modality[15,17] 3D-CRT or IMRT, have reduced the risk of developing osteoradionecrosis
Radiotherapy dose[17,18] Risk of developing osteoradionecrosis increases with higher RT doses
Chemotherapy[16,17] Increases acute toxicity especially mucositis, but its effect on late toxicity is less clear
Surgery[17,18] Ablative surgical procedures increased risk of developing osteoradionecrosis after radiation
Miscellaneous Active smoking[15-18] Tobacco smoking as a risk factor for osteoradionecrosis
factors[15-18] Alcohol[16] Alcohol consumption during and after radiotherapy is one of the risk factors for developing
osteoradionecrosis
Inadequate oral hygiene[17] Poor oral hygiene increases the risk for development of osteoradionecrosis
Steroids and Steroid and anticoagulants use before or after radiation reduced the risk of
anticoagulants[15] osteoradionecrosis
Dental diseases[15] Positive association between presence of dental disease pre-radiation therapy and
osteoradionecrosis
Body-mass index[16] For every one point increase in BMI, osteoradionecrosis risk decreased by 27%
Secondary infection[17] Secondary infection in post-radiotherapy phase correlated with severe mandibular
osteoradionecrosis
Dental extraction[18] Dentoalveolar surgery in post-radiotherapy phase is an established predisposing factor for
the development of osteoradionecrosis
Nutritional status[15] Poor nutritional status increases the risk of osteoradionecrosis

of irradiated bone, but a complex metabolic and homeostatic It was introduced in 2004 when recent advances in cellular and
deficiency of tissue that is created by radiation‑induced cellular molecular biology explained the progression of microscopically
injury; micro‑organisms play only a contaminating role in observed osteoradionecrosis [Figure 3].[21] Three distinct phases
osteoradionecrosis; and trauma may or may not be an initiating are seen:
factor.”[20] • The initial prefibrotic phase in which changes in endothelial
cells predominate together with the acute inflammatory
Delanian’s radiation‑induced fibroatrophic theory response
• The constitutive organised phase in which abnormal
Radiation‑induced fibrosis is a new theory that accounts for the fibroblastic activity predominates, and there is disorganisation
damage to normal tissues, including bone, after radiotherapy. of the extracellular matrix

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Suryawanshi, et al.: Maxillofacial osteoradionecrosis

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Suryawanshi, et al.: Maxillofacial osteoradionecrosis

• The late fibroatrophic phase, when attempted tissue difficult to differentiate from recurrent tumour if bone changes
remodelling occurs with the formation of fragile healed are not visible on CT.[28]
tissues that carry a serious inherent risk of late reactivated
inflammation in the event of local injury.[10] PET scan is helpful to differentiate between osteoradionecrosis
and recurrent tumour.[28]
Microbiology
Radionuclide bone scanning with technetium methylene
Osteoradionecrosis was earlier attributed to secondary infection diphosphonate (99mTc‑MDP) can identify pathophysiologic
in the traumatized irradiated tissue following the nonhealing
wounds and exposed bone. However, this was challenged by Table 5: Microbiology of osteoradionecrosis
Robert Marx in 1983.[20] The detailed description of various Year Author(s) Microorganisms isolated
microorganisms detected in osteoradionecrosis is given in [8]
1983 Marx Surface contaminants
Table 5.[8,22‑27] Further studies on bacterial flora associated with 2005 Store and Polymicrobial bacterial infection-rods,
osteoradionecrosis are required, which may contribute to a more Olsen[22] spirochetes and cocci. Rods were the
precise use of antibiotics. predominant
2005 Støre, Eribe Porphyromonas gingivalis
and Olsen[22] Actinomyces species
Clinical features 2006 Hansen, Actinomyces species
Wagner,
The incidence of osteoradionecrosis varies from 0.95% to 35% Kirkpatrick
as shown in Table 6.[28‑36] The patient is usually asymptomatic. and Kunkel[23]
Pain and evidence of exposed bone are the most common chief 2007 Nason and 50% of the oral and 80% of the
Chole[24] intestinal indigenous bacterial flora
complaints. Trismus, fetor oris, and elevated body temperature
consist of uncultured phylotypes
are usually present during the initial period although acute 2005 Aas, Paster, Firmicutes
infection is usually not present. Other clinical features of Stokes, Olsen Actinobacteria
osteoradionecrosis are swelling, nonresolving painful mucosal and Dewhirst[25] Proteobacteria
ulcer, dysgeusia, dysguesia, xerostomia, food impaction, Fusobacteria-Fusobacterium nucleatum
Spirochaetes
malocclusion, telangiectasia, orocutaneous fistula, and missing
Bacteroidetes
hair follicles. The tissues surrounding the bone may be Campylobacter gracilis
indurated. Surface texture changes such as cutaneous flaking and Streptococcus intermedius
keratinisation may be present. Surface colour changes may also Peptostreptococcus sp. oral clone FG014
be seen. Pathologic fracture of the jaws may be evident in severe Uncultured bacterium clone RL178
cases. Rarely, Deep cellulitis of face and neck may be present.[28] Prevotella spp
1988 Calhoun, Streptococcus sp.
Shapiro, Bacteroides sp.
Radiological features Stiernberg, Lactobacillus sp.
Calhoun and Eubacterium sp.
The presence of osteoradionecrosis cannot always be diagnosed Mader[26] Klebsiella sp.
Actinomyces
radiographically and often clinically obvious signs of exposed
2006 Kjetil Treponema spp
necrotic may not be accompanied by significant radiologic Pedersen[27] Porphyromonas gingivalis
changes.

Plain radiography shows an ill‑defined cortical destruction Table 6: Incidence of osteoradionecrosis

without sequestration. The periphery may be ill‑defined as in Year Author(s) Incidence (%)
osteomyelitis. Bone pattern can be granular. Scattered regions 1972 Carl, Schaaf, Chen, and Tak Yee[28] 4
of radiolucency may be seen, with or without central sequestra. 1972 Daley, Drane, and Mc Comb[29] 22
The most common effect on surrounding bone is stimulation 1974 Wang[30] 17
of sclerosis. 1976 Bedwinck[31] 14
1980 Murray, Herson, Daly, and 19
Zimmerman[32]
Computed tomography plays an important role in diagnosis 1995 Constantino, Friedman and 5 to 15
of osteoradionecrosis since it is hard tissue lesion. Anterior– Steinberg[33]
posterior and supero–inferior extent of the osteolytic lesion is best 1997 Epstein and van der Meij et al.[34] 5 to 15
judged with CT scans comparatively. Hence, from diagnostic 1997 Clayman[35] Before 1968-11.8
purpose to the surgical intervention, CT is recommended as After 1968-5.4
2000 Thorn, Sand Hansen, Specht and 5 to 15
far as osteoradionecrosis is concerned.[29] Bastholt[36]
2003 Vissink, Jansma, Spijkervet, 2.6 to 22
MRI reveals development of new heterogeneous signal within Burlage and Coppes[37]
the marrow of an irradiated area (intermediate or low T1 signal, 2004 Reuther, Schuster, Mende, and 1 to 37.5
intermediate or high T2 signal). Adjacent muscles may appear Kübler[38]
2006 Wahl[39] 3 to 3.5
oedematous and show intense enhancement, which can be

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changes in bone earlier than conventional radiography because at sites of osteoradionecrosis, confirming that it is a hypovascular
scan changes reflect osteoblastic activity and good blood flow.[28] and hypoxic tissue with decreased metabolic rate.[28]

Infrared spectroscopy is a noninvasive method. This Histologic features

shows a reduction of the amount of deoxygenated haemoglobin
The histological findings noted by Marx showed endothelial
Table 7: Preventive management of osteoradionecrosis death, hyalinisation, and thrombosis of vessels with a fibrotic
Measures to be taken periosteum.[25]
Preradiation protocol
A thorough clinical and radiographic examination is recommended for Diagnostic criteria
patient scheduled for radiotherapy
Teeth with poor prognosis should be removed
Oral hygiene regimen should be started as soon as possible. This In 1997, Wong, Wood, and McLean have given diagnostic
includes. criteria for osteoradionecrosis that seem to be agreed by the
Teeth brushing with soft brush with the frequency of four times daily majority of the authors:
Warm saline (NaCl and NaHC03) mouth wash daily especially after • The affected site should have been previously irradiated
brushing
Fluoride treatment either 0.4% stannous fluoride gel, 1% sodium • There should be absence of recurrent tumour on the affected
fluoride or 1% acidulated fluorophosphate gel in a custom tray for site
15 min twice daily • Mucosal breakdown or failure to heal should occur, resulting
Intraradiation protocol in bone exposure
Weekly prophylaxis with fluoridated polishing paste • The overlying bone should be ‘dead’, usually due to a hypoxic
Analgesics, dietary supplements, antifungal and antibiotics prescription
Postradiation protocol necrosis
Patients who have completed radiotherapy should not wear dentures for • Cellulitis, fistulation, or pathologic fracture need not be
at least a year to maximize tissue healing present to be considered as osteoradionecrosis.[30]
Fluoride treatment and oral hygiene care should be continued. Artificial
saliva may have to be prescribed Osteoradionecrosis usually develops after 3‑6 months having
Life-long follow-up
bone exposure at least for 3 months.[30]

Table 8: Precautions to be taken for dental extractions in Management

osteoradionecrosis
Precautions to be taken The management of osteoradionecrosis is divided into two methods.
Preradiotherapy dental extractions 1. Preventive management
The policy followed in most institutions is to remove unrestorable teeth 2. Therapeutic management.
prior to radiotherapy
The mandibular teeth in the bone to be radiated above 6,000 cGy are
indicated for extraction Preventive management
The extractions should be carried out in a nontraumatic manner with
minimal damaged to the surrounding tissues. Planned preradiotherapy The prevention of osteoradionecrosis begins as early as the
extractions include alveoloplasty and primary closure with minimal head and neck malignancy is diagnosed. The patient should
periosteal elevation
Antibiotic therapy is usually prescribed for 1 to 4 weeks be reviewed by the multidisciplinary team consisting of
The interval period between extraction and radiotherapy is extremely
crucial Table 9: Therapeutic management of osteoradionecrosis
Beumer III and Curtis and Maxymiw, Wood & Liu stated that at
least two weeks interval is required in order not to delay the radiation Methods
therapy Nonsurgical management
Marx and Johnson recommended an interval of three weeks before Pharmacological
commencing radiotherapy, based on experimental studies that show Antibiotic therapy
osteoid takes 3 weeks to form Analgesics
Teeth with questionable prognosis should be carefully discussed with the Antifungal therapy
patient Antiviral therapy
Post-radiotherapy dental extractions Newer agents: Pentoxyphilline, tocopherol, clodronate and
Extractions should be limited to one or two teeth at a time combination therapy
The techniques should be as Atraumatic and aseptic as possible Nonpharmacological
Flaps should be raised conservatively to minimize displacement of Local wound care
mucoperiosteum Hyperbaric oxygen therapy
Sharp projections of bone require· re-contouring or minor alveoloplasty Ultrasound therapy
followed by primary closure Electrotherapy
Hyperbaric oxygen therapy can be considered as prophylaxis against Ozone therapy
ORN Surgical management
The prophylactic use of ultrasound as an alternative to hyperbaric Sequestrectomy
oxygen is recommended by Reher and Harris Resection with continuity defect
Prophylactic antibiotics for extractions are required Reconstruction
Rehabilitation
ORN: Osteoradionecrosis

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Suryawanshi, et al.: Maxillofacial osteoradionecrosis

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14. Van Merkesteyn JP, Bakker DJ, Borgmeijer-Hoelen AM. Hyperbaric
to prevent osteoradionecrosis, as per Donoff’s protocol, are
oxygen treatment of osteoradionecrosis of the mandible: experience
mentioned in Table 7.[37] The precautions that are to be taken in 29 patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod
during dental extraction are summarized in Table 8.[38] 1995;80:12-6.
15. Regaud C (1922a) Sur la necrose des os attenté par un processus
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