Article_5_3_5
MAXILLOFACIAL SURGERY
EFFICACY OF A DENTAL EXTRACTION POLICY DESIGNED TO PREVENT
Original Article
OSTEORADIONECROSIS: A RETROSPECTIVE STUDY IN 100 ORAL CANCER PATIENTS
TREATED WITH INTENSITY-MODULATED RADIOTHERAPY
Constantinus Politis1a* , Paul Deckers1b, Matthias Schol1b, Daan Nevens2c, Sandra Nuyts2d, Joseph Schoenaers1e,
Reinhilde Jacobs1f
1
OMFS-IMPATH research group, Department of Imaging & Pathology, Faculty of Medicine, KU Leuven and Oral and Maxillofacial Surgery, University Hospitals
Leuven, BE-3000 Leuven, Belgium
2
Department of Oncology, KULeuven - University of Leuven, University Hospitals Leuven - Radiation Oncology, BE-3000, Leuven, Belgium
a
MD, DDS, MHA, MM, PhD, Professor
b
DDS
c
MD
d
MD, PhD, Professor
e
MD, DDS, Professor
f
DDS,PhD, Professor
ABSTRACT DOI: 10.25241/stomaeduj.2018.5(3).art.5
Introduction: The aim was to determine the efficacy of an extraction policy OPEN ACCESS This is an Open Access
article under the CC BY-NC 4.0 license.
designed to prevent osteoradionecrosis (ORN) in dentate areas of the jaw after
Peer-Reviewed Article
intensity-modulated radiotherapy (IMRT). A secondary aim was to establish whether
our extraction policy risked unnecessary tooth extractions for areas designated to Citation: Politis C, Deckers P, Schol M, Nevens D, Nuyts
S, Schoenaers J, Jacobs R. Efficacy of a dental extraction
be not-at-risk of ORN. policy designed to prevent osteoradionecrosis: a
Methodology: Data were retrospectively collected from 100 oral cancer patients, retrospective study in 100 oral cancer patients treated
with intensity-modulated radiotherapy. Stoma Edu J.
including the fate of 1430 individual teeth, from diagnosis to follow-up. 2018;5(3):173-178
Results: Eight percent of IMRT-treated patients developed ORN; spontaneous cases Academic Editor: Nardi Casap-Caspi, DMD, MD,
(5) outnumbered those provoked by dental issues (3). All cases of ORN arose in regions Professor and Head, Hebrew University Hadassah
Jerusalem, Jerusalem, Israel
irradiated with > 60 Gy, with the posterior mandible as preferred location, with non-
spontaneous cases primarily due to progressive periodontitis. No correlation was Received: September 03, 2018
Revised: September 19, 2018
found between the likelihood of extraction and cancer stage. Acccepted: September 24, 2018
Conclusions: A more robust extraction policy of teeth affected with periodontitis Published: September 25, 2018
and pocket depths of 4 - 5 mm might be advocated in molar areas predicted to *Corresponding author: Prof. Dr. Constantinus
receive > 60 Gy. Unfortunately, our study's retrospective design precluded any Politis, MD, DDS, MHA, MM, PhD, Department of Oral
and Maxillofacial Surgery, University Hospitals Leuven,
detailed analyses of the underlying reasons for the 88 extractions that occurred at Kapucijnenvoer 33, Leuven, BE-3000 Belgium
Tel: +32 16 332464; Fax: +32 16 332437, e-mail:
lower radiation dose thresholds; a more conservative approach may therefore be constantinus.politis@uzleuven.be
warranted for these low-risk areas. orcid.org/0000-0003-4772-9897
Keywords: osteoradionecrosis, intensity-modulated radiotherapy, dosimetric Copyright: © 2018 the Editorial Council for the
distribution, tooth extraction, oral cancer. Stomatology Edu Journal.
1. Introduction Frequently, these screens are based on the presumption
Osteoradionecrosis (ORN) of the jaw is a serious that conventional external beam radiation therapy will
complication that can arise following radiotherapy for be used, as is the case in our Department of Oral and
head and neck cancers [1]. ORN is defined as a slow- Maxillofacial Surgery, University Hospitals of Leuven
healing radiation-induced ischemic necrosis of the (Leuven, Belgium). However, with the introduction
bone, associated with varying degrees of soft tissue of intensity-modulated radiotherapy (IMRT), a
necrosis in the absence of local primary tumor necrosis, significantly higher proportion of normal tissue is
recurrent, or metastatic disease [1]. When radiation is spared from high-dose radiation [4], with these high
delivered in standard fractions, bone irradiated at doses doses restricted to a smaller area. This leads us to
in excess of 60 Gy appears to be the most vulnerable suggest that a modified extraction policy might be
to ORN lesions [1]. However, occasionally, lesions arise appropriate for IMRT patients [5].
in bone exposed to lower doses (usually above 50 Gy To determine which teeth should be left in situ versus
but below 60) [2]. Furthermore, ORN lesions may occur those that should be extracted (as a precautionary
spontaneously after radiotherapy, or after trauma, measure in terms of ORN prevention), clinicians in
particularly after dental extractions [1]. our department base their decision-making on the
Pre-treatment dental screens aim to reduce the risk outcome of a "single tooth risk assessment" (Table 1),
of developing ORN following radiation therapy by which is used for areas of the mouth at a low risk of
removing teeth predicted to be at an increased risk developing ORN (i.e. areas < 50 Gy).
of harboring infection or becoming infected [3]. Teeth which are designated "irrational to treat" in Table
Stomatology Edu Journal 173
EFFICACY OF A DENTAL EXTRACTION POLICY DESIGNED TO PREVENT OSTEORADIONECROSIS: A RETROSPECTIVE
STUDY IN 100 ORAL CANCER PATIENTS TREATED WITH INTENSITY-MODULATED RADIOTHERAPY
1) are extracted (leaving those with good prognoses in-
Original Article situ. The fates of teeth with doubtful prognoses are then
Table 1. Single tooth risk assessment.
Prognosis Dental field Criteria
based on levels of oral hygiene, any limitation in the
Good - -
ability to open the mouth, and the clinical experience
of the supervising surgeon: whenever possible these Furcation involvement (levels II and III)
teeth are treated and retained. Periodontal
Angular bone defects
For those areas at a high risk of developing ORN (> 50 “Horizontal” bone loss exceeding 2/3 of
Gy), extractions are completed whenever the tooth the root
Doubtful Incomplete root canal therapy
demonstrates one of the signs/conditions listed in
Table 2 [6]. Some teeth are also necessarily sacrificed as Endodontal Periapical pathology
part of the surgical resection procedure. Presence of voluminous posts/screws
The main objective of this study was to determine the Dental Extensive root caries
efficacy of the tooth extraction policy in preventing ORN Recurrent periodontal abscesses
at the Department of Oral and Maxillofacial Surgery,
Periodontal Periodontic-endodontic lesions
University Hospitals of Leuven (Leuven, Belgium). A high-
Attachment loss to the apex
performance extraction policy would accurately target
Root perforation in the apical half of
only those teeth that constitute a risk of promoting the root
ORN. However, two other scenarios, should they be Endodontic
Periapical pathology in the presence of
identified, would be of concern as these would indicate Irrational to obturating post and core
failings in the current preventative extraction protocol. treat Vertical fracture of the root
These scenarios include a failure to extract teeth that Oblique fracture in the middle third of
subsequently provoke ORN, or the identification of Dental the root
extractions in the absence of risk (i.e. non irradiated Caries lesions that extend into the root
teeth, teeth irradiated with < 50 Gy radiation, or teeth canal
with none of the indications in Table 1). Functional Third molars without antagonist and
with periodontitis/caries
2. Materials and Methods Table 2. Tooth extraction policy for areas predicted to receive a radiation
dose > 50 Gy.
2.1. Subjects
Our 100-patient cohort (with 1430 individual teeth under Lesions induced by deep caries that could expose the pulp during
treatment
consideration) comprised patients diagnosed with cancer
pockets > 6 mm
of the oral cavity between January 2012 and September
furcation involvement > = level I
2016, at the Department of Oral and Maxillofacial Surgery,
mobility > level I
University Hospitals of Leuven (Leuven, Belgium). These
gingival recession > = 6 mm
patients were subsequently treated with IMRT at the Active periodontitis
Department of Radiotherapy and Oncology, University with: any combination of these periodontal
criteria
Hospitals of Leuven (Leuven, Belgium).
in patients that demonstrate poor
All patients underwent pre-IMRT dental screening, cooperation, any tooth with active
after which extractions of compromised teeth were periodontitis in the field of radiation is
extracted
performed: the “irrational to treat” as listed in Table 1, the
indications as listed in Table 2, and extractions deemed Non-restorable teeth with large and/or subgingival restorations
necessary because of the planned resection procedure. Root caries
Since clinical, radiographic, and radiotherapeutic Teeth with large restorations, combined with severe erosion and
documentation were available for all patients, we could abrasion
retrospectively determine which teeth remained in- Teeth with a periapical granuloma
situ and were present at the time of IMRT. These teeth Avital teeth
were subsequently denoted as "not being considered a
Partially impacted or partially erupted teeth that are not fully
risk factor for ORN development after IMRT". covered by bone, or those showing a radiolucency above the crown
Using the individual IMRT plans for each patient, all teeth
Teeth with cyst formation
(including those that were, and were not extracted)
were subdivided according to maximum dose, with Teeth showing radiographic abnormalities
categories of < 50 Gy (1), 50 - 60 Gy (2), and > 60 Gy (3). Teeth with cracked tooth syndrome
This distinction was made because there is still a risk of
ORN, albeit reduced [2], even if the total radiation dose
delivered by standard fractionation is below 60 Gy [1]. 2.2. Statistical Analyses
Patients who developed ORN prior to February 2017 The primary objective of this study was analyzed
were categorized according to two types of ORN: statistically by evaluating patient subsets with
spontaneous ORN that occurred post IMRT, and ORN percentages and confidence intervals, as well as plots
caused by a dental issue. of an empirical distribution function. Statistical analyses
The following data were also collected: patient were supervised by a certified statistician.
identification number, date of cancer diagnosis,
start date for IMRT, the cause of ORN and its date of Ethical Approval
diagnosis. To avoid bias, clinicians involved in gathering This study was approved by the ethical committee of
and processing data were not involved in treatment. UH Leuven (S54701).
174 Stoma Edu J. 2018;5(3):173-178 http://www.stomaeduj.com
EFFICACY OF A DENTAL EXTRACTION POLICY DESIGNED TO PREVENT OSTEORADIONECROSIS: A RETROSPECTIVE
STUDY IN 100 ORAL CANCER PATIENTS TREATED WITH INTENSITY-MODULATED RADIOTHERAPY
Original Article
Table 3. Details of all extractions.
3. Results Number of
In 100 patients, 1770 teeth were absent at intake (Table Area Tooth status teeth
3). Management decisions for the 1430 remaining Absent at intake 1770
teeth were then made prior to surgery and/or radiation Present at intake 1430
therapy. In total 1031 teeth were left in situ, with 399 Peroperative removal in
Resection site 136
extractions. The respective dose predictions for the 399 the resection specimen
extracted teeth were as follows: 156 were destined to Irradiated area > Left in situ 397
50 Gy
receive a radiation dose of < 50Gy; 59 were projected
Irradiated area > Extracted for ORN
to receive > 50Gy but < 60 Gy; and 48 extractions 50 Gy prevention 76
were in an area that would receive a dose of > 60 Gy. Irradiated area > Extracted for a dental
Another 136 teeth were removed during the surgical 31
50 Gy reason
procedure due to their position in the resection zone or Non-irradiated or Left in situ 634
immediately opposite the free flap. <50 Gy
In those areas predicted to receive a radiation dose of Non-irradiated or Extracted for a dental 75
<50 Gy reason
less than 50 Gy, 156 teeth were also extracted: 75 for
dental reasons (indications listed in Table 1), and 81 for Noni-rradiated or Extracted, reasons not 81
<50 Gy specified
(other) reasons that could not be established following
review of the medical files. Due to the retrospective
character of this study, it was impossible to identify the
relevant decision-making criteria for these 81 extractions
(i.e. limited cooperation of the patient, predictions of
poor oral hygiene, or limited ability to open the mouth).
Irrespective of the underlying reasons, the extraction
policy in these areas more closely resembled the
extraction policy used to prevent ORN. Collectively, 22
patients underwent 81 extractions from areas that were
either not destined for irradiation, or were destined to
be irradiated with a dose of < 50 Gy. One hypothesis
that was tested was whether patients with an advanced
stage of cancer would undergo more extractions in
areas not prone to exhibit ORN of dental origin? Figure
1 shows a scatterplot depicting the correlation between Figure 1. Scatter plot showing the relationship between the number of
tooth extraction (in each patient) and cancer staging at teeth removed and tumor size.
the tumor level. A linear correlation could not be found.
The Spearman’s rank correlation coefficient was -0.0314
(p-value = 0.7557). If only those patients that underwent
tooth extractions were included, the Spearman’s rank
correlation coefficient was 0.285 (p-value = 0.1465).
Consequently, no correlation was found to exist between
the stage of the oral cancer and the tooth extraction
policy.
The patients in this study had an average follow-up
period of 815 days, or close to 2 years and 3 months after
starting IMRT. In total, 8 out of 100 patients developed an
ORN lesion, 5 spontaneously, and 3 after an extraction.
For the five spontaneous cases (with no link to dental
problems), 1 lesion occurred in the maxilla and the other
4 cases were in the mandible. All lesions arose in the
body of the mandible, in areas where radiation levels Figure 2. Empirical distribution function showing the follow-up period
exceeded 60 Gy. Lesion incidence showed a preference prior to developing ORN.
for the posterior parts of the jaw in areas corresponding or higher. The causal teeth for these lesions were canine
to (6) molars, (3) bicuspids, and (1) canine. (1), bicuspid (3), and molar (2). The medical files did
Three patients developed ORN lesions caused by not mention any specific pathological findings at the
dental problems from the retention of 6 teeth that canine or bicuspids at intake. The molars showed signs
were presumed to pose (at the time of the extraction of periodontitis with pocket depths of 4 and 5 mm,
decision-making) no risk of ORN. respectively, at intake. Eventually, these teeth had to be
The average period between commencing IMRT and removed as periodontitis had progressed. Either this
developing ORN was 438 days, or just over 1 year and infection, or the subsequent extraction, triggered ORN.
2 months; onset data for individuals (all 8 patients that
developed ORN) with follow-up periods for the entire
cohort are shown in Figure 2. 4. Discussion
All three ORN lesions of dental origin arose in the As early as 1922, the first case of ORN was described
mandible in areas exposed to a radiation dose of 60 Gy by Regaud [7]. In 1926, Ewing followed with an article
Stomatology Edu Journal 175
EFFICACY OF A DENTAL EXTRACTION POLICY DESIGNED TO PREVENT OSTEORADIONECROSIS: A RETROSPECTIVE
STUDY IN 100 ORAL CANCER PATIENTS TREATED WITH INTENSITY-MODULATED RADIOTHERAPY
describing bone changes associated with radiation clarify this aspect of the decision-making process. For
Original Article therapy that were termed “radiation osteitis" [8]. those areas not destined to receive > 60 Gy by IMRT, a
Despite the extensive research provoked by these early more heuristic approach might be beneficial in terms
reports, ORN still poses a substantial threat in patients of improving decision-making without bias.
that have undergone radiation therapy in the head Due to the elevated incidence of oropharyngeal cancers
and neck region, especially given the absence of any caused by the human papilloma virus (HPV) [17,18], the
standard conservative treatment [9], and the frequent number of patients at risk of ORN is predicted to rise.
requirement for extensive surgery [10]. The highest doses of radiation will be in the oropharynx
The first category of ORN that should be addressed itself [19], with a smaller amount affecting the anterior
is the spontaneous lesion. These can, by definition, area of the mandible. Therefore, there should be a focus
not be prevented, even with an adequate extraction on maintaining the strict extraction criteria for ORN
policy, as their origin is unrelated to trauma [1]. In this prevention [6] for posterior teeth, particularly those
study, all but one spontaneous lesion arose in the in the mandible, whereas areas with a low risk of ORN
mandible, with these results in line with the higher should be treated with the less austere general practice
susceptibility of the mandible to ORN versus (vs.) the guidelines as outlined in Table 1.
maxilla [1, 10]. The overall ratio for ORN incidence for In total, 8 out of 100 patients developed an ORN lesion.
the mandible vs. maxilla was 24:1 [11]. All spontaneous Recent studies have reported an overall incidence
lesions in this study were found in the alveolar ridge, of ORN in IMRT patients treated for oral cavity and
with a preference for more posterior regions. The oropharyngeal cancer of 25.5% (mean follow-up of 41
lesions occurred in areas corresponding to 6 molars, 3 months) [20] and 40% (after 5 years of follow-up) [21].
bicuspids, and 1 canine. These findings are also in line The 8% incidence reported in this study is therefore
with the general consensus that the posterior regions much lower than average. However, the short average
of the jaw are more susceptible to developing ORN follow-up period of 815 days (just under 2 years and
lesions [1, 10]. 3 months) may explain this low incidence rate that is
The second category of ORN lesion would appear to be predicted to increase with lengthier follow-up.
preventable given that this category arises following
an extraction or by dental infection that occurs in areas
of bone exposed to a high level of radiation [1]. The 5. Conclusions
risk of developing ORN because of dental problems This study revealed that, in spite of an existing
in highly irradiated alveolar bone persists for life [12]. extraction policy, ORN lesions caused by dental
Furthermore, there is an increased risk of developing problems still occurred. Since ORN in these patients
dental caries [13], and periodontal defects [14] after only developed in areas in receipt of > 60 Gy, primarily
radiation therapy. Teeth predicted to lie in the path of in the molar areas, a more robust extraction policy
high doses of radiation (> 50 Gy) should be in good could be warranted for these areas.
condition in order to satisfy the criteria for being left in This study made a distinction between areas receiving
situ without posing a risk of developing ORN [6, 15, 16]. a radiation dose of between 50 and 60 Gy, and those
In this study, ORN caused by dental problems still areas that received a higher radiation dose. The results
developed, with three cases identified. This finding show that all ORN lesions caused by a dental problem
indicates that more teeth should have been extracted occurred in areas of 60 Gy or higher. As such, a cut-off
from the area of high radiation in order to prevent value of 60 Gy of radiation may be a good guideline to
ORN. These findings point to periodontal disease as establish for decision-making processes. The overall
the greatest hazard, with periodontal pockets of 4-5 incidence of 8% (8/100) ORN after IMRT for oral and
mm present at dental screening that subsequently oropharyngeal cancer, after a follow-up period of 2.3
progressed during follow-up. yrs., is considered to be low, although this figure is
It was noted that ORN lesions caused by extractions expected to increase with time. Spontaneous ORN
showed a slight preference to develop in the posterior (5 patients) was more common than ORN caused by
regions of the alveolar bone, although not to the dental problems (3 patients).
same extent as spontaneous ORN lesions. The teeth As for extractions in areas not destined for irradiation,
that provoked ORN in the 3 patients were a canine, 3 or predicted to receive less than 50 Gy, a heuristic
bicuspids, and 2 molars. approach to extraction decision-making is warranted.
Given that IMRT spares many teeth from high doses Future prospective studies could clarify the reasoning
of radiation when compared to conventional external for those extractions that failed to meet the expected
beam radiation therapy [4], less teeth are predicted extraction criteria. We anticipate that this approach will
to be at risk to develop ORN lesions. However, the benefit patients given that the loss of multiple teeth is
findings of this study fail to account for the higher debilitating to the irradiated patient, both physically
number of extractions in areas considered to pose no and emotionally.
risk of developing ORN (81) vs. the 76 teeth that were
at risk (Table 3). It is unclear, due to the retrospective
design of this study, as to what triggered the extraction Author contributions
decisions in these scenarios. However, possibilities CP, PD, MS: Substantial contributions to the design of
include poor oral hygiene, future prospects of a limited the work; JS: Drafting the work; SN, DN: Substantial
ability to open the mouth, poor surgical access, an contributions to the acquisition of data; RJ: reviewed
uncooperative patient, or a mistaken evaluation of the the manuscript.
area of high radiation. A prospective study should now
176 Stoma Edu J. 2018;5(3):173-178 http://www.stomaeduj.com
EFFICACY OF A DENTAL EXTRACTION POLICY DESIGNED TO PREVENT OSTEORADIONECROSIS: A RETROSPECTIVE
STUDY IN 100 ORAL CANCER PATIENTS TREATED WITH INTENSITY-MODULATED RADIOTHERAPY
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Constantinus POLITIS
MD, DDS, MHA, MM, PhD, Professor and Chairperson
Department of Oral and Maxillofacial Surgery
University Hospitals Leuven
Kapucijnenvoer 33, Leuven, Belgium
CV
Constantinus Politis is an Oral and Maxillo-Facial Surgeon. He is currently Full Professor and Chairperson of the Department
of Oral and Maxillofacial Surgery at Leuven University Hospitals, KULeuven, Belgium. He is an invited Lecturer at the EHSAL in
Brussels. He graduated from the Catholic University of Leuven in medicine (MD, summa cum laude), in dentistry (DDS, magna
cum laude). He specialized in oral and maxillofacial surgery at the Catholic University of Leuven. His professional field of interest
is in orthognathic and orthodontic surgery and trigeminal nerve dysfunction. His clinical research projects include prevention
and repair of iatrogenic trigeminal nerve injury, transplantation of teeth and orthognathic surgery. He has been elected as
member of the Belgian Royal Academy of Medicine.
Stomatology Edu Journal 177
EFFICACY OF A DENTAL EXTRACTION POLICY DESIGNED TO PREVENT OSTEORADIONECROSIS: A RETROSPECTIVE
STUDY IN 100 ORAL CANCER PATIENTS TREATED WITH INTENSITY-MODULATED RADIOTHERAPY
Questions
Original Article
1. ORN occurred in areas irradiated with:
qa. < 40 Gy;
qb. < 50 Gy;
qc. < 60 Gy;
qd. > 60 Gy.
2. IMRT causes ORN in irradiation of oral and oropharyngeal cancer:
qa. within the first 3 months after irradiation;
qb. within the first 6 months after irradiation;
qc. within the first 12 months after irradiation;
qd. usually after the 1st year of irradiation.
3. ORN usually does not occur in:
qa. in the upper jaw;
qb. in the ascendic ramus of the lower jaw;
qc. in the dentate area of the lower jaw;
qd. in the area of the lower jaw where extractions have been done.
4. The following teeth need not to be extracted if they occur in a zone with 72 Gy
of irradiation:
qa. mobility > 6 mm;
qb. periodontal pocket of 2 mm;
qc. furcation > 1 mm;
qd. root caries.
https://2018acoms.com/cms-user/
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