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174]

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

Department of Oral and
Maxillofacial Surgery,
DPU, Dr.D. Y. Patil
Dental College and
Hospital, Pimpri, Pune,
Maharashtra, India
Address for correspondence:
Dr.Amit Suryawanshi,
Email: amitsuryawanshi999
@gmail.com
ABSTRACT
Osteoradionecrosis is a severe and delayed radiationinduced injury, characterized by bone tissue necrosis and
failure to heal. Cases of osteoradionecrosis present to the clinician with features of pain, drainage, and fistulation
of the mucosa or skin related to exposed bone in the previously irradiated area. The tumour size and location,
radiation dose, occurrence of local trauma, dental extractions, infection, immune defects, and malnutrition are
predisposing factors. Abetter understanding of risk factors leading to the development osteoradionecrosis
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,
clinical features, radiological features, diagnosis, and treatment modalities including the newer modalities.
KEY WORDS: Jaws, management, osteoradionecrosis, physiopathology, risk factors

Introduction Historical perspective

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

per year with mortality of 2,70,000cases per year. The
incidence of oral cancer in India is 40% among all cancers and
about 1,00,000patients suffer from oral cancer in any year.
Oral cancer is responsible for 7% of all cancer deaths in males
and 3% in females.[1]
The recent protocol for management of oral cancer includes
multimodal therapy, such as surgery with radiotherapy and/or
chemotherapy. Radiation therapy is one of the major treatment
modalities for the management of oral malignancies. Like with
any treatment modality, even radiation therapy is associated with
various complications. Alongterm side effect of radiotherapy
that is also the most serious is osteoradionecrosis.[2,3] Literature
reveals many terminologies to represent the same disease, such
as radiation osteitis, radioosteonecrosis, radiation osteomyelitis,
osteomyelitis of irradiated bone, osteonecrosis, radioosteomyelitis,
septicosteoradionecrosis, and postradiotherapy osteonecrosis.[4]
This review focuses on the general information on maxillofacial
osteoradionecrosis for general practitioners.
Access this article online
Quick Response Code:
Website:
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DOI:
10.4103/2348-3172.126171
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
Osteitis.[5] In 1970, Meyer classified osteoradionecrosis as one
special type of osteomyelitis. In 1975, Mainous advocated the
use of hyperbaric oxygen therapy(HBO) for late radiation tissue
injury. In 1983, Robert Marx proposed the hypoxic, hypocellular,
and hypovascular theory as a new way of understanding
the pathophysiology of osteoradionecrosis. In 1992, Harris
introduced the use of Ultrasound as one of the modes to treat
osteoradionecrosis.[6] In 1998, Marx gave the 30/10 protocol that
was employed in the treatment of established osteoradionecrosis.
In 2004, Delanian and Lefaix put forward a new theory named
radiationinduced fibrosis that accounts for the damage to
normal tissues, including bone after radiotherapy.[7]
Definitions
In literature, osteoradionecrosis has been defined in many
ways[Table1].[8,9] However, the authors feel that the definition
given by Wong, Wood, and McLean(1997)[8] is the most
appropriate and complete:
A slowhealing radiationinduced ischemic necrosis of bone
with associated soft tissue necrosis of variable extent occurring
in the absence of local primary tumour necrosis, recurrence, or
metastatic disease that may or may not:
i. Be superinfected(and accompanied by fistulation or cellulitis)
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, etal.: Maxillofacial osteoradionecrosis

Classification and staging systems
There have been several staging or scoring systems that have
been proposed. These systems are based on response to HBO
therapy, degree of bone damage, clinicalradiological findings,
length of bone exposure through the overlying skin or mucosa,
and treatment needed[Tables2 and 3].[8-15]
Risk factors
The existing articles in literature fail to give an exact etiology
for osteoradionecrosis. The etiology of osteoradionecrosis is
considered to be multifactorial. These factors may increase the risk
of the patient for development of osteoradionecrosis.Thefactors
are classified into four groups as shown in Table4.[15-18]
Marxs Hypoxic, hypocellular, and hypovascular theory[20]
Delanians Radiationinduced fibroatrophic theory.[21]
Meyers radiation, trauma, and infection theory
In 1970, in an excellent monograph on infectious disease of the
jaws, Meyer defined the classic triad of osteoradionecrosis as
radiation, trauma, and infection[Figure1].[19] Meyer portrayed that
the trauma provided the portal for invasion by oral microbiological
flora into the underlying irradiated bone. Meyers theory lasted
for a decade and became the foundation for the popular use of
antibiotics with surgery to treat osteoradionecrosis.[19]
Marxs 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 morehypoxic
date. However, literature reveals three theories that have been than those that had not been irradiated [Figure2].[20] Marx
put forward since 1970, as mentioned in the following: concluded that Osteoradionecrosisis not a primary infection
Meyers Radiation, trauma and infection theory[19]
Table2: Classification systems of osteoradionecrosis
Table1: Definitions of osteoradionecrosis Year Authors Basis for classification
Year Author(s) Definition 1983 Coffins 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 simpsons 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 Epsteins 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
StevensonMoore[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 Claymans 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 Boysens 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 Schwartzs 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 etals 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 etal.[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(versionIV)[12] Grade 1-5
radiationinduced periodontal
LENT: Late effects of normal tissue, SOMA: Somatic objective
breakdown
management analytic

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Suryawanshi, etal.: Maxillofacial osteoradionecrosis

Table3: Classification of osteoradionecrosis

Year Classification
2002 Kagan and Schwartzs
staging[15]
2009 Bone toxicity according
to the National Cancer
Institute Common
Terminology Criteria[12]
ADL: Activities of daily living
Stages/ Description Management
grades
Stage I Minimal soft tissue ulceration and limited exposed Conservative management
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 orocutaneous 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 softtissue replacement
Grade 1 Asymptomatic Clinical or diagnostic observations only;
intervention not indicated
Grade 2 Symptomatic Medical intervention indicated(e.g.,
topical agents); limiting instrumental ADL
Grade 3 Severe symptoms Limiting selfcare ADL; elective operative
intervention indicated
Grade 4 Lifethreatening consequences Urgent intervention indicated
Grade 5 Death

Table4: Risk factors of osteoradionecrosis

Type of risk factors Risk factors Description of risk factors
Patient related Gender [15]
Male predominance(male:female=1.6:1)
factors Age[16] Common in elderly patients
Race[15] Common in whites(74%)
Tumourrelated 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
Treatmentrelated Radiotherapy setting[15,18] Patients undergoing adjuvant radiotherapy had more risk for developing osteoradionecrosis
factors Radiotherapy modality[15,17] 3DCRT 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[1518] 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 preradiation therapy and
osteoradionecrosis
Bodymass index[16] For every one point increase in BMI, osteoradionecrosis risk decreased by 27%
Secondary infection[17] Secondary infection in postradiotherapy phase correlated with severe mandibular
osteoradionecrosis
Dental extraction[18] Dentoalveolar surgery in postradiotherapy 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
deficiency of tissue that is created by radiationinduced cellular
injury; microorganisms play only a contaminating role in
osteoradionecrosis; and traumamay ormay not be an initiating
factor.[20]
Delanians radiationinduced fibroatrophic theory
Radiationinduced fibrosis is a new theory that accounts for the
damage to normal tissues, including bone, after radiotherapy.
It was introduced in 2004 when recent advances in cellular and
molecular biology explained the progression of microscopically
observed osteoradionecrosis[Figure3].[21] Three distinct phases
are seen:
The initial prefibrotic phase in which changes in endothelial
cells predominate together with the acute inflammatory
response
The constitutive organised phase in which abnormal
fibroblastic activity predominates, and there is disorganisation
of the extracellular matrix

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Suryawanshi, etal.: Maxillofacial osteoradionecrosis

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Suryawanshi, etal.: 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(99mTcMDP) can identify pathophysiologic
in the traumatized irradiated tissue following the nonhealing
wounds and exposed bone. However, this was challenged by Table5: 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
1983 Marx [8]
Surface contaminants
Table5.[8,22-27] Further studies on bacterial flora associated with 2005 Store and Polymicrobial bacterial infectionrods,
osteoradionecrosis are required, which may contribute to a more Olsen[22] spirochetes and cocci. Rods were the
precise use of antibiotics. predominant
2005 Stre, 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 Table6.[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, FusobacteriaFusobacterium 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 illdefined cortical destruction Table6: Incidence of osteoradionecrosis

without sequestration. The periphery may be illdefined 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 superoinferior extent of the osteolytic lesion is best 1997 Epstein and van der Meij etal.[34] 5 to 15
judged with CT scans comparatively. Hence,fromdiagnostic 1997 Clayman[35] Before 1968-11.8
purpose to the surgical intervention, CT is recommended as After 19685.4
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 Kbler[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

showsareduction of the amount of deoxygenated haemoglobin
Table7: Preventive management of osteoradionecrosis
Measures to be taken
Preradiation protocol
A thorough clinical and radiographic examination is recommended for
patient scheduled for radiotherapy
Teeth with poor prognosis should be removed
Oral hygiene regimen should be started as soon as possible. This
includes.
Teeth brushing with soft brush with the frequency of four times daily
Warm saline(NaCl and NaHC03) mouth wash daily especially after
brushing
Fluoride treatment either 0.4% stannous fluoride gel, 1% sodium
fluoride or 1% acidulated fluorophosphate gel in a custom tray for
15min twice daily
Intraradiation protocol
Weekly prophylaxis with fluoridated polishing paste
Analgesics, dietary supplements, antifungal and antibiotics prescription
Postradiation protocol
Patients who have completed radiotherapy should not wear dentures for
at least a year to maximize tissue healing
Fluoride treatment and oral hygiene care should be continued. Artificial
saliva may have to be prescribed
Lifelong followup
The histological findings noted by Marx showed endothelial
death, hyalinisation, and thrombosis of vessels with a fibrotic
periosteum.[25]
Diagnostic criteria
In 1997, Wong, Wood, and McLean have given diagnostic
criteria for osteoradionecrosis that seem to be agreed by the
majority of the authors:
The affected site should have been previously irradiated
There should be absence of recurrent tumour on the affected
site
Mucosal breakdown or failure to heal should occur, resulting
in bone exposure
The overlying bone should be dead, usually due to a hypoxic
necrosis
Cellulitis, fistulation, or pathologic fracture need not be
present to be considered as osteoradionecrosis.[30]
Osteoradionecrosis usually develops after 3-6months having
bone exposure at least for 3months.[30]

Table8: 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 4weeks be reviewed by the multidisciplinary team consisting of
The interval period between extraction and radiotherapy is extremely
crucial Table9: 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 3weeks to form Analgesics
Teeth with questionable prognosis should be carefully discussed with the Antifungal therapy
patient Antiviral therapy
Postradiotherapy 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 recontouring 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, etal.: Maxillofacial osteoradionecrosis
a dentist/oral and maxillofacial surgeon. The measures taken
to prevent osteoradionecrosis, as per Donoffs protocol, are
mentioned in Table7.[37] The precautions that are to be taken
during dental extraction are summarized in Table8.[38]
Therapeutic management
The nonsurgical and surgical management with a note on recent
medications are summarized in Table9.[39]
Conclusion
Osteoradionecrosis can be a cruel blow to patients and
their families who have been enduring radiotherapy for
the treatment of cancer. Prevention of osteoradionecrosis
by regular followup and early diagnosis should be the
goal of every health care professional managing head and
neck cancer patients. Improved radiotherapy protocols,
multidisciplinary preventive care and reconstructive surgery
can help to improve the quality of life of patients suffering
from osteoradionecrosis.
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Source of Support: Nil, Conflict of Interest: None declared.

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Journal of Dental Research and Review Jan-Apr 2014 Vol. 1 Issue 1 49