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British Journal of Oral and Maxillofacial Surgery 47 (2009) 598–601

A survey of consultant members of the British Association of


Oral and Maxillofacial Surgeons regarding
bisphosphonate-induced osteonecrosis of the jaws
S.N. Rogers a,b,∗ , J. Hung a , A.J. Barber a , D. Lowe a,b
a Regional Maxillofacial Unit, University Hospital Aintree, Longmoor Lane, Liverpool L9 7LN, UK
b Evidence-Based Practice Research Centre (EPRC), Faculty of Health, Edge Hill University, St Helens Road, Ormskirk L39 4QP, UK

Accepted 27 July 2009


Available online 12 September 2009

Abstract

The aims of this survey of consultants in the British Association of Oral and Maxillofacial Surgeons were threefold. Firstly, to estimate the
number of patients screened for oral health before starting intravenous bisphosphonate medication, secondly, to indicate the use of antibiotics
in patients on bisphosphonates who need routine extraction of a lower first molar tooth, and finally to estimate the number of new and currently
managed cases of bisphosphonate-induced osteonecrosis of the jaw (BONJ) in the last year, and approximately how many of those currently
being managed had healed.
A questionnaire was mailed to 322 consultants working at 154 hospitals in the summer of 2008. There were responses from 184 consultants
(57%) and from 111 hospitals (72%). Screening patients before starting intravenous bisphosphonates was uncommon (15%). Almost all
consultants would prescribe antibiotics for molar extraction and in about two-thirds this was both before and after extraction. Relatively few
would stop bisphosphonates. Nearly two-thirds of consultants had seen new cases of BONJ from intravenous treatment in the last year, and a
quarter had seen three or more. A similar proportion had patients on intravenous bisphosphonates under review for BONJ, and it was estimated
that in a fifth of patients the lesion had healed.
This survey indicates current practice among oral and maxillofacial surgeons in the UK. A national project for the registration of new
patients will provide a stronger evidence base with respect to incidence, risk factors, and management of BONJ.
© 2009 Published by Elsevier Ltd on behalf of The British Association of Oral and Maxillofacial Surgeons.

Keywords: Bisphosphonates; Bisphosphonate-induced osteonecrosis of the jaws; Survey; British Association of Oral and Maxillofacial Surgeons

Introduction indications include treatment for Paget disease, ankylos-


ing spondylitis, and even bone diseases in children such as
Bisphosphonates are some of the most commonly prescribed osteogenesis imperfecta.9 The side effect of bisphosphonate-
drugs in the world,1,2 and are prescribed for patients with induced osteonecrosis of the jaw (BONJ) in medical care
osteoporosis,3 and for bone metastasis such as that in prostate was reported by Marx in 2003.10 Since then there have
cancer,4 multiple myeloma,5–7 and breast cancer.8 Other been numerous case reports, patient series, and review
statements.11–14
∗ Corresponding author at: Regional Maxillofacial Unit, University Hos- The incidence of BONJ is not clear and varies between
pital Aintree, Longmoor Lane, Liverpool L9 7LN, UK. reports, but it is much higher in patients on intravenous prepa-
Tel.: +44 0151 529 5287; fax: +44 0151 529 5288. rations. Incidence from cumulative exposure in patients on
E-mail addresses: snrogers@doctors.co.uk (S.N. Rogers), long-term oral bisphosphonates is yet to be fully realised.
janitrix@gmail.com (J. Hung), andrewbarber2@nhs.net (A.J. Barber),
astraglobeltd@btconnect.com (D. Lowe).
Hoff et al.15 recently published a report of a large series of

0266-4356/$ – see front matter © 2009 Published by Elsevier Ltd on behalf of The British Association of Oral and Maxillofacial Surgeons.
doi:10.1016/j.bjoms.2009.07.020
S.N. Rogers et al. / British Journal of Oral and Maxillofacial Surgery 47 (2009) 598–601 599

patients on intravenous treatment in which 16 of 1338 with Methods


breast cancer (1%), and 13 of 548 with multiple myeloma
(2%) developed osteonecrosis of the jaw (ONJ). The inci- A questionnaire was mailed in June 2008 to all consultants
dence of BONJ in osteoporotic patients has been reported (excluding SAS grades) on the May 2007 mailing list (white
to be in the region of 1 in 2260–8470 (0.04–0.01%).16 book) of the British Association of Oral and Maxillofacial
Sedghizadeh et al.17 recently published an estimate by the Surgeons (BAOMS) at each hospital where they worked. A
University of Southern California that about 4% of their postage-paid reply envelope was included. Members of the
patient population had BONJ secondary to oral treatment BAOMS who work at more than one hospital were asked
with alendronate sodium. There is very little data on patients to complete the questionnaire only once unless they had a
in the UK. different practice in another hospital. Reminders were sent
Risk factors for BONJ are becoming recognised and broad after 3 weeks to consultants who did not respond.
guidelines for the oral and dental management of patients on
bisphosphonates have been developed, such as those by the
Canadian Association of Oral and Maxillofacial Surgeons,18 Results
and the American Association of Oral and Maxillofacial
Surgeons.19 These multidisciplinary guidelines were devel- A total of 443 questionnaires were sent to 322 consultants
oped for medical and dental practitioners as well as for oral at 154 hospitals. Responses were received from 184 of 322
pathologists and related specialists. They suggest that all consultants (57%) (7 responded from two different hospitals),
oncology patients should have a thorough dental examina- and from 111 of 154 hospitals (72%). Fourteen blank returns
tion that includes radiographs before initiation of intravenous were omitted, which left 177 responses for analysis. Missing
treatment with bisphosphonates. Patients with osteoporosis data is reflected by variations in denominator.
on oral or intravenous bisphosphonates do not require a dental In the previous 3 months 26 of 177 consultants (15%)
examination before initiating treatment if they have appro- had screened at least one patient before starting intravenous
priate dental care and good oral hygiene. Malden et al.20 bisphosphonates. Responses to the question “What would
proposed an algorithm for low and high-risk patients who normally be done if a patient taking oral or intravenous bis-
require extractions. Although suggested, there is a lack of phosphonates required “routine” extraction of a lower first
evidence for stopping bisphosphonates before invasive den- molar tooth?” are shown in Tables 1 and 2.
tal procedures.18,21 There are several treatment guidelines for Forty-seven of 163 (29%) had protocols in their hospital or
the management of BONJ, but the evidence base is weak.21–23 unit for the management of patients taking oral or intravenous
In 2007 a survey of oral and maxillofacial surgeons in bisphosphonates who need minor operations. Management of
Australia was published.16 A hundred and fifty-eight cases such patients depended on duration of medication for 55 of
of BONJ were identified primarily in patients with bone 156 (35%), on requirements for surgical extraction for 65 of
malignancy (72%), and the main trigger was dental extrac- 154 (42%), for coexisting diseases such as diabetes and use
tion (73%). Other factors were untreated periodontal disease, of steroids for 62 of 154 (40%), on patients being elderly for
mucosal trauma, or ill-fitting dentures. Immunocompromised 38 of 155 (25%), and on the presence of infection for 77 of
patients seem to have the highest risk. The reported num- 151 (51%).
ber of cases varied between different Australian states with A hundred and twenty-four of 168 consultants (74%) had
the highest incidence being reported in states with the best seen new cases of BONJ from oral bisphosphonates in the last
integrated health systems. year, and 40 of 168 (24%) had seen at least four. A hundred
In view of the absence of a survey of opinion amongst oral and eleven of 164 (68%) were currently managing patients
and maxillofacial consultants, and the paucity of data with with BONJ from oral bisphosphonates, and 38 of 164 (23%)
respect to the screening of patients commencing bisphos- were managing at least five. The total was 486, of which 190
phonate treatment, prescription of antibiotics for extractions, (39%) were stated to be, or were estimated to be healed.
and the incidence of BONJ in the UK, a national survey was In the last year 103 of 162 (64%) had seen new cases
undertaken. Consultants were asked to estimate numbers of of BONJ from intravenous bisphosphonates, and 43 of 162
patients in the previous 3 months that they had screened for (27%) had seen at least three. Ninety-six of 155 (62%) were
oral health before starting intravenous bisphosphonate medi- currently managing BONJ cases from intravenous bisphos-
cation, and to describe their usual management of patients on phonates, and 35 of 155 (23%) were managing at least four.
bisphosphonates who required routine extraction of a lower The total was 449, of which 90 (20%) were stated to be, or
first molar tooth. They were also asked if their hospital or were estimated to be healed.
unit had a protocol for managing such patients for minor
oral surgery, and whether such management varied accord-
ing to certain factors. Finally they were asked to estimate Discussion
numbers of new and currently managed cases of BONJ in
the last year, and how many of those currently managed had This survey gives an insight into the views of consultant
healed. oral and maxillofacial surgeons with respect to the screening
600 S.N. Rogers et al. / British Journal of Oral and Maxillofacial Surgery 47 (2009) 598–601

Table 1 of patients on intravenous bisphosphonates, use of antibi-


Results of questionnaire to the question “What would normally be done otics for lower molar extractions, and the number of cases of
if a patient taking oral or intravenous bisphosphonates required “routine”
extraction of a lower first molar tooth? Data are number (%).
BONJ. Nearly three-quarters of units responded. Although
it is acknowledged that postal surveys have limitations, this
Patients taking bisphosphonates
raises some interesting points.
Orally Intravenously Few consultants screened patients before starting intra-
Normally do you stop bisphosphonate medication preoperatively? venous bisphosphonates. The guidelines for starting patients
Yes 29/175 (17) 62/161 (39) on this treatment are that they should have a dental assess-
If yes, for how many months? ment and be rendered dentally fit.23 The fact that consultant
Less than 1 month 5/29 (17) 9/62 (15)
1–2 months 7/29 (24) 20/62 (32)
oral and maxillofacial surgeons are not really involved in
3–4 months 13/29 (45) 13/62 (21) screening should be seen as appropriate use of their time and
More than 4 months 3/29 (10) 5/62 (8) expertise, but it raises the question of how many patients are
Not stated 1/29 (3) 15/62 (24) actually being screened and by whom. Some patients will not
If yes, when do you suggest the bisphosphonates are restarted? be referred by the clinician, and a proportion will have a regu-
Immediately 2/29 (7) 4/62 (6) lar dental practitioner. Further studies are needed to evaluate
Only when socket has healed 16/29 (55) 39/62 (63) the screening pathway for this high-risk group. In a recent
Other (see Table 2) 6/29 (21) 8/62 (13)
survey of general dental practitioners with respect to osteo-
Not stated 5/29 (17) 11/62 (18)
radionecrosis, McLeod et al.24 reported that only 35% asked
Do you prescribe antibiotics for the extraction? specifically about head and neck cancer or radiotherapy as
Yes 147/170 (86) 143/157 (91)
If yes, when?
part of the medical history. If this relatively low awareness of
Before extraction only 13/147 (9) 6/143 (4) the patient’s history was seen for bisphosphonates it would
After extraction only 40/147 (27) 30/143 (21) imply that potentially there are many patients who are not
Before and after extraction 85/147 (58) 95/143 (66) recognised to be at risk from cumulative oral exposure or
Not stated 9/147 (6) 12/143 (8) intravenous treatment.
If yes, which antibiotic(s) Most consultants used antibiotics for the extraction of
Amoxicillin alone 43/147 (29) 38/143 (27) a lower molar tooth. The type of antibiotics being pre-
Metronidazole alone 14/147 (10) 10/143 (7)
scribed varied greatly in duration and frequency of dose.
Co-amoxiclav (Augmentin) alone 45/147 (31) 45/143 (31)
Amoxicillin and metronidazole 4/147 (3) 4/143 (3) Chlorhexidine mouthwash was commonly used as an adjunc-
Other alone 20/147 (14) 22/143 (15) tive measure. Clinical management was also influenced by
Other combinations 13/147 (9) 14/143 (10) factors such as existing infection (51%), coexisting disease
Not stated 8/147 (5) 10/143 (7) (40%), age (25%), duration of treatment with bisphospho-
Do you use a chlorhexidene mouthwash for the extraction? nates (35%), and the need for surgical extraction (42%).
Yes 117/170 (69) 116/159 (73) Evidence for use of prophylactic antibiotics is weak. There is
If yes, when? a need for greater understanding of the risk factors of BONJ
Before extraction only 21/117 (18) 16/116 (14)
After extraction only 21/117 (18) 17/116 (15)
as this should allow better selection of patients who might
Before and after extraction 72/117 (62) 76/116 (66) benefit from antibiotic prophylaxis.
Not stated 3/117 (3) 7/116 (6) This survey did not attempt to address which patients
Do you ask for a restorative dentist’s opinion? should be treated specifically by oral and maxillofacial
Yes 53/153 (35) 60/155 (39) surgeons, and it would not be appropriate to make any defi-
nite recommendations from the evidence presented because
Table 2 patients on intravenous bisphosphonates have a considerably
Breakdown of responses marked as “other” in reply to the question “When higher risk of BONJ, and it is suggested that they are seen
do you suggest the bisphosphonates are restarted?”.
by clinical teams familiar with the problems in management
Patients taking bisphosphonates associated with them.
Orally Intravenously The survey showed a lack of consistency with respect to
6 weeks postoperatively 1 1 the stopping of bisphosphonates before extractions. About
2–3 months postoperatively 4 3 39% of consultants would stop intravenous use, and 17%
Assessing urgent clinical 1 – would stop oral medications. This difference in practice
need reflects a deficit in understanding the risks of developing
On recommendation of – 1
physician
BONJ and the lack of robust evidence for guidelines.
Leave up to oncologist – 1 During the last year three quarters of consultants had seen
As late as possible in liaison – 1 new cases of BONJ in patients taking oral medication and
with haematology or two-thirds had seen new cases in those on intravenous medi-
oncology, or other specialty cation. Data on actual numbers and rates of healing from the
Leave up to prescriber or – 1
oncologist
survey is limited, but it does support the premise that BONJ
is a growing clinical problem.
S.N. Rogers et al. / British Journal of Oral and Maxillofacial Surgery 47 (2009) 598–601 601

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