Professional Documents
Culture Documents
Osteoporosis is a skeletal disorder characterized by are more than 5 million prescriptions written for
decreased bone density, a condition that predisposes in- osteoporosis per year in North America, and the
dividuals to an increased risk of fracture. This particular overwhelming medication of choice for more
medical condition is most frequent in people older than than 95% of patients with osteoporosis is a
45 years, with a probable prevalence ratio of up to 1 in bisphosphonate (BP).1 BPs also are used in oncologic pa-
4 women and 1 in 8 men in North America. There tients to decrease bone metastasis, fractures, and pain.
Received from the Faculty of Dentistry, University of Toronto, Address correspondence and reprint requests to Dr Azarpaz-
Toronto, ON, Canada. hooh: Faculty of Dentistry, University of Toronto, Room 515-C,
*Former Resident. 124 Edward Street, Toronto, ON, Canada M5G 1G6; e-mail: amir.
yAssistant Professor. azarpazhooh@dentistry.utoronto.ca
zAssistant Professor. Received September 9 2014
xProfessor. Accepted December 11 2014
kAssistant Professor. Ó 2015 American Association of Oral and Maxillofacial Surgeons
This study was supported in part by the Ronald E. Warren Award 0278-2391/15/00023-3
from the Canadian Association of Oral and Maxillofacial Surgeons. http://dx.doi.org/10.1016/j.joms.2014.12.040
1095
1096 DENTISTS TREATING PATIENTS ON BISPHOSPHONATES
Despite the many benefits of BPs, in the early 2000s, and opinions of Ontario dentists about BRONJ when
several patients presented to dental offices with treating patients receiving BPs by measuring their
exposed necrotic bone in the maxilla or mandible of knowledge of BPs and BRONJ and to identify how
then-unknown etiology. Further investigations identi- they manage patients on BP therapy.
fied a common feature in these patients: they were
taking BPs and most of them had recently undergone
a surgical dental procedure.2 In 2003, Marx2 was the
Materials and Methods
first to describe the relation of treatment with BPs to DESIGN
the occurrence of osteonecrosis of the jaw (ONJ). This study is a cross-sectional Web-based survey
Subsequently, Ruggiero et al3 published a case series that was conducted over a period of 2 months and
of ONJ related to the use of BPs. This realization led was approved by the research ethics board at the
to numerous studies2,4,5 that examined the relation University of Toronto (Toronto, ON, Canada; protocol
between BPs and exposed necrotic bone in the 27571). A list of the members of the Royal College of
mouth, a clinical scenario that is now known as Dental Surgeons of Ontario (RCDSO) was obtained
BP-related ONJ (BRONJ). through the membership directory. Potential partici-
BRONJ is defined as an area of exposed bone that pants were defined as those who might perform
persists longer than 8 weeks in a patient taking a dentoalveolar surgeries based on their professional
BP.3 It is a severe but extremely rare complication of RCDSO registration (general dentists, oral and maxillo-
prolonged treatment with BPs.3,6 Studies have not yet facial surgeons, periodontists, prosthodontists, and
conclusively established a mechanism by which BPs endodontists). They were approached by e-mail and
are responsible for causing BRONJ. However, one directed by link to an online interface (SurveyGizmo,
hypothesis is that BPs prevent osteoclastic activity by Boulder, CO) displaying the survey instrument.
inhibiting farnesyl pyro-phosphonate synthase, a key Follow-up e-mail reminders were sent 4 times during
amino acid in the mevalonate pathway.5,7 This action a period of 2 months. No gift or remuneration was
can lead to a decrease in bone absorption. It also has provided to the participants in the study.
been suggested that BPs can prevent normal bone
turnover remodeling. Microfractures of the bone are
no longer repaired and angiogenesis might be SURVEY INSTRUMENT
inhibited, which leads to weakening of the bone The survey tool included questions about partici-
structure.5,7 More recently, cases of ONJ have been pants’ knowledge of BPs, their experiences treating
reported in patients taking medications other than patients presenting with ONJ, any treatment modifica-
BPs, including the antiresorptive drug denosumab and tion in performing different surgical procedures
the antiangiogenic drugs bevacizumab and sunitinib,8 (eg, tooth extraction, dental implant placement, peri-
suggesting that the mechanism of action is most likely odontal surgery, or endodontic surgery) in patients
related to antiresorptive and antiangiogenic effects taking IV or oral BPs, and their awareness of the BRONJ
rather than effects on a specific pathway. guidelines suggested by the AAOMS.3 For validation
The incidence of oral BRONJ has been discussed and adjustment, the survey instrument was pilot
in some studies, with important differences being tested among 15 specialists and dentists at the Faculty
reported.5,9 The incidence of BRONJ associated of Dentistry, University of Toronto. Pilot testing aimed
with oral BPs ranges from 0.001 to 0.1%, and that to evaluate the clarity of the survey questions, respon-
associated with intravenous (IV) BPs ranges from 1 to dent burden (time needed to respond and level of
12%. Longer duration of exposure results in increased understanding), face validity, and feasibility of the
risk.10 There has been no report of BRONJ associated planned data analysis. Further, each respondent was
with the less active BPs etidronate and clodronate, asked follow-up questions to ensure that all sections
although they are used in oncologic studies.11 were easy to understand. This field test resulted in
The American Association of Oral and Maxillofacial revisions to the original questionnaire, from which a
Surgeons (AAOMS) produced a guideline in 2009 that final questionnaire was drafted based on the following
categorized patients into at-risk and stage 0, 1, 2, and 3 4 principal domains.
categories with specific treatment recommendations
for each group.3 Contrary to the established guideline, Domain 1—Perception and Current Practice
there are anecdotal reports of some dentists refusing Included in this domain were questions that mea-
to treat patients who previously received or are sure participants’ general knowledge about BRONJ.
currently receiving BPs. Barriers to a dentist’s adher- They were asked 9 key knowledge questions about
ence to practice guidelines include lack of awareness BP use, route of administration, incidence, and treat-
of the guideline and their attitudes and behaviors.12 ment for a patient with BRONJ based on the AAOMS
This study aimed to evaluate the knowledge, practices, 2009 position paper.3 They also were asked about
ALHUSSAIN ET AL 1097
the volume of patients they see with BRONJ symp- historically low response rates of dentists, the authors
toms, at which stage of BRONJ they would refer the selected all 6,920 dentists with available e-mail ad-
patient to a specialist, and their treatment. dresses who would have direct surgical interventions
(Fig 1).
Domain 2—Scenario Cases
In this domain, the participants were provided with DATA ANALYSIS
a scenario of a patient who takes BPs and presents for a
Data from the online survey were downloaded from
surgical procedure relevant to the field of specialty of
the SurveyGizmo Web site as an Excel file (Microsoft,
the participant. Six scenarios were presented for
Redmond, WA). After recoding the variables, the data-
simple, complicated, and impacted tooth extraction,
base was imported to SAS 9.2 (SAS Institute, Cary, NC)
placing dental implants, or performing periodontal
for management and analysis. Responses to the ques-
or endodontic surgeries. The scenarios differed based
tions in this survey were summarized using descriptive
on duration (#3 or >3 yr) and route of BPs given (oral
statistics (percentages for categorical data and means
or IV). The participants were asked about their man-
and standard deviations for continuous variables).
agement plan for these different scenarios: whether
Descriptive analyses were conducted for the entire
they would perform the surgical procedure; or would
sample and for subgroups of participants (general den-
discontinue BPs for 3 months and then perform the
tists, periodontists, prosthodontists, oral surgeons,
procedure; or would not perform the procedure; or
and endodontists). Responses were compared among
would refer to a specialist.
these subgroups using the c2 test and the Fisher exact
test for categorical variables and the Student t test for
Domain 3—Demographics
continuous variables. A score of 9 of 9 was given if the
Included in this domain were questions pertaining
participant answered all knowledge questions
to participants’ age, gender, pattern of practice
correctly in the first domain. A series of bivariate and
(currently practicing vs retired or not practicing),
linear regression analyses were conducted to identify
primary professional activity (eg, general dentist,
the characteristics of those with good knowledge of
specialist, military dentist, or academic instructor),
the guideline. Moreover, the results of the 6 scenario
location and years of practice, specialty field, and
questions in domain 2 were divided into right or
population of town or city where they practice.
wrong treatment answers based on the AAOMS guide-
line3 or referral. The percentage of each category was
Domain 4—Knowledge Acquisition
Included in this domain were questions that asked
about the resources participants use to stay current
in their knowledge (educational courses, scientific
meetings, journal articles, or Internet), where they
first learned about BRONJ, whether they feel comfort-
able treating patients with BRONJ, and their preferred
method for continuing education related to BRONJ.
derived for each practitioner. Multivariate regression Table 1. DESCRIPTION OF THE DENTISTS PARTICI-
analyses were applied to analyze the association of PATING IN THE SURVEY
the frequency of scenario responses with the practi-
tioner characteristics. All tests were conducted at a sig- Demographics n (%)
nificance level of .05.
Men 678 (68.0)
Oral surgeons 48 (85.7)
Results Periodontists 30 (73.2)
From a total of 6,920 RCDSO dentists with e-mail ad- Prosthodontists 13 (68.4)
dresses who might perform dentoalveolar surgeries, Endodontists 18 (78.3)
General practitioners 555 (66.5)
the authors achieved a database of 5,255 members
Age (yr)
with valid e-mail addresses. From this pool, a total of
25-34 131 (12.9)
1,579 survey responses were collected, resulting in a 35-44 233 (22.9)
response rate of 30%. The demographic characteristics 45-54 297 (29.2)
of survey participants are listed in Table 1. Most partic- 55-64 271 (26.6)
ipants were men (68%) and general practitioners (GPs; >65 86 (8.4)
86.2%) with more than 20 years of experience as a Dental specialty
general dentist (56.1%) or as a specialist (50%). Almost Oral surgeons 57 (4.9)
half (45.7%) the participants were working in areas Periodontists 42 (3.6)
that have a population of more than 500,000 people. Prosthodontists 20 (1.7)
Endodontists 26 (2.2)
GPs 1,003 (86.2)
KNOWLEDGE QUESTIONS
Other 16 (1.4)
Table 2 presents the results of the knowledge ques- Working years
tions in the survey. Most participants (66.4%) correctly As a GP
identified osteoporosis as the indication for BP use. 1-5 125 (13.5)
Very few participants identified wrong indications for 6-10 89 (9.6)
BP (2.3% for diabetes and 0.5% for hypertension). 11-20 193 (20.8)
More than 80% of participants correctly selected the >20 521 (56.1)
BP route to be oral or IV. Almost one fourth of partici- As a specialist
1-5 24 (20.3)
pants did not know the answer to the question on
6-10 12 (10.2)
the incidence of BRONJ in patients taking oral or IV 11-20 23 (19.5)
BPs. The remaining knowledge questions (questions >20 59 (50.0)
5 to 9) pertained to the assessment of the knowledge Local population
of participants on treatment strategies of BRONJ in <5,000 45 (4.5)
different stages of risk. The least aggressive strategies 5,000-50,000 161 (16.1)
was selected for the lower degrees of risk, that is, pa- 50,000-500,000 338 (33.7)
tient education, treating symptoms, and mouth rinse >500,000 458 (45.7)
were mostly selected for patients at risk, at stage 0,
Abbreviation: GP, general practitioner.
and at stage 1, respectively. Most participants selected
antibiotics and in particular surgical debridement for Alhussain et al. Dentists Treating Patients on Bisphosphonates.
J Oral Maxillofac Surg 2015.
the higher stages of risk, with 70.1% recommending
antibiotics for stage 2 treatment and 68.3% recom-
mending surgical debridement fort stage 3. Conversely, edge score compared with other age groups. Being
for the patient in stage 1, almost 12.3 and 66.4% of par- a specialist and in particular being an oral and maxillo-
ticipants selected the wrong choices of no treatment facial surgeon, being comfortable treating patients
and antibiotics, respectively, as their approach to treat- with BRONJ, having some exposure to BRONJ cases
ment. This pattern of incorrect answers was similar for in a given month, and practicing in large urban centers
the scenario of a patient in stage 2. were associated with higher knowledge scores
Table 3 presents the impact of participants’ charac- (P < .05). All these significant variables were analyzed
teristics on their knowledge score. Overall, the mean in a linear regression model (Table 3). Only 2 factors
( standard deviation) knowledge score for all partic- remained important. 1) A pattern of a better knowl-
ipants was 5.6 1.9. No statistical difference was edge score was found in those 25 to 34 years old
found between participants’ knowledge score and compared with other groups. In particular, those 45
their gender or years in practice. However, there was to 54 years old had a statistically lower knowledge
a statistical difference in knowledge score with age, score compared with younger practitioners 25 to
in which those 45 to 54 years old had a lower knowl- 34 years old (b = 0.73; 95% CI, 1.07 to 0.30). 2)
ALHUSSAIN ET AL 1099
Note: Table presents the percentages of participants’ answers for each knowledge question. Percentages might not add up to
100% because the participants could choose all options that were applicable.
Abbreviations: BP, bisphosphonate; BRONJ, bisphosphonate-related osteonecrosis of the jaw; IM, intramuscular; IV, intrave-
nous; Q, question.
* Correct answers.
Alhussain et al. Dentists Treating Patients on Bisphosphonates. J Oral Maxillofac Surg 2015.
Those who described themselves as being comfortable likely to refer the patient. In an aggregate of all sce-
with their current level of knowledge treating patients narios combined together, 23.8% of participants
with BRONJ had a statistically higher knowledge score answered correctly to all 6 scenarios, 15.9% answered
compared with those who were not comfortable treat- wrong, and 60.3% referred.
ing such patients (b = 0.34; 95% CI, 0.06-0.62). To understand the impact of practitioners’ charac-
teristics, 2 regression models were constructed. The
first model identified the characteristics of those
SCENARIO QUESTIONS who referred versus those who selected the right treat-
Table 4 presents the frequency distribution for ment strategy (Table 6) and showed that women, GPs,
responses of the 6 scenario questions. In general, no those working in urban locations with a population of
matter the surgical intervention, participants tended 50,000 to 500,000, and those who are not comfortable
to select referral if the patient had been taking oral with their current knowledge were more likely to
BPs for more than 3 years or if they have been taking refer. The second model aimed to identify the charac-
IV BPs regardless of duration. Among the 3 scenarios teristics of those who selected the wrong treatment
of tooth extraction (simple, complex, and impacted), strategy versus those who selected the right treatment
participants tended not to extract and refer as the strategy or who would refer the patient and showed
complexity of extraction increased. no statistical differences between participants who
Table 5 presents the aggregated responses, catego- gave wrong answers and those who gave correct an-
rized as the percentages of right answer, wrong swers or referred the patient (data not shown).
answer, and referral answer. Participants more Knowledge score also predicts when practitioners
frequently chose the correct management for patients would refer their patients. As presented in Table 7,
receiving oral BP for less than 3 years; in contrast, in those with a lower knowledge score would refer pa-
scenarios in which patients were given oral BP for tients from a lower risk category compared with those
more than 3 years, they more frequently chose the with a higher knowledge score who would tend to
wrong management. When patients in these scenarios refer later. For example, those with 1 unit more knowl-
were given IV BP, participants were frequently more edge score would be 1.42 times (95% CI, 1.23-1.64)
1100 DENTISTS TREATING PATIENTS ON BISPHOSPHONATES
Table 3. SUMMARY OF MULTIVARIATE ANALYSES FOR PREDICTORS OF GENERAL KNOWLEDGE SCORE ABOUT BRONJ
Abbreviations: BRONJ, bisphosphonate-related osteonecrosis of the jaw; CI, confidence interval; GP, general practitioner;
SD, standard deviation.
Alhussain et al. Dentists Treating Patients on Bisphosphonates. J Oral Maxillofac Surg 2015.
more likely to treat patients who are at risk and only Internet browsing (63%). Most participants (56%)
refer a patient when they are showing some early signs learned about BRONJ through journal articles. Almost
of BRONJ (stage 0). half (49%) reported that they are not comfortable treat-
ing patients with BRONJ with their current knowledge.
Further inquiry identified participants as preferring
KNOWLEDGE ACQUISITION journal articles (55%) or full- or half-day courses (51%)
The last part of the survey asked participants how as their source of information about BPs and BRONJ.
they obtained their knowledge related to BRONJ
(Table 8). Most participants (87%) identified continuing
Discussion
education courses as the leading resource to stay cur-
rent in dentistry. Other primary resources included This cross-sectional study was designed to investi-
journal articles (86%), scientific meetings (72%), and gate the knowledge, practices, and opinions of
ALHUSSAIN ET AL 1101
Table 4. FREQUENCY OF MANAGEMENT PLANS FOR THE 6 SCENARIO PROCEDURES DIFFERING BY ROUTE AND
DURATION OF BP ADMINISTRATION
Ontario dentists when treating patients receiving the AAOMS 2009 position paper provide detailed guid-
BPs. The interest was in whether participants’ knowl- ance regarding the use of dental devices and selection
edge and approach to care of BRONJ was consistent of appropriate antibiotic therapy.3,13
with the established guidelines. The AAOMS 2009 This present study found that despite the existence
guidelines were used to develop the knowledge and of guidelines, Ontario dentists had a poor understand-
scenario questions and score the answers given by ing of how or even whether to carry out surgical dental
the participants.3 This position paper was prepared treatment in patients taking BPs. In total, only 23.8% of
by clinicians based in multicenter hospitals and was 1,579 responding dentists followed the AAOMS guide-
approved by the AAOMS Board of Trustees in January line, and 49.7% were not comfortable treating patients
2009. The intent of the guidelines was to provide with BRONJ. The results show that in some scenarios
perspective on the risk of developing BRONJ and the almost 50% of participants, if they did not refer, would
risks and benefits of BPs to facilitate evidence-based select the wrong treatment strategy. This approach
decision making by the treating clinicians and the can exacerbate or fail to resolve the main dental condi-
patient and provide guidelines for treating BRONJ.3 tion, can lead to serious complications for the patient,
The recommendations of this multidisciplinary task or might lead them to develop BRONJ. In particular, it
force representing oral and maxillofacial surgery, oral has been shown that most patients taking BPs might
medicine, endocrinology, and medical oncology in be unfamiliar with the drug and its possible adverse
1102 DENTISTS TREATING PATIENTS ON BISPHOSPHONATES
Extraction
Simple oral <3 yr 73.4 6.8 19.8 836
oral >3 yr 18.1 47.2 34.7 834
IV <3 yr 13.7 8.75 77.6 840
IV >3 yr 10 9.9 80.1 809
Complicated oral <3 yr 52 7.8 39.5 833
oral >3 yr 16.7 30 53.4 828
IV <3 yr 9.1 6.3 84.6 824
IV >3 yr 5.9 8.4 85 826
Impacted oral <3 yr 26.5 6.3 67.3 831
oral >3 yr 10.1 15.2 74.7 829
IV <3 yr 5.6 6.7 87.8 826
IV >3 yr 3.8 8.7 87.5 819
Implant oral <3 yr 60.3 12.5 27.2 368
oral >3 yr 26.8 35.6 37.5 365
IV <3 yr 22.6 20.9 56.5 368
IV >3 yr 28.5 15.8 55.7 368
Periodontal oral <3 yr 81 10.2 8.8 294
oral >3 yr 16.8 61.6 21.6 292
IV <3 yr 27 17.7 55.3 293
IV >3 yr 23.1 16.7 60.2 294
Endodontic oral <3 yr 61.9 8.4 29.8 215
oral >3 yr 18.7 38.3 43 214
IV <3 yr 10.2 15.8 74 215
IV >3 yr 6.1 19.2 74.6 213
oral side effects. This would further highlight the re- 3 years or IV BP regardless of duration. This could be
sponsibility of the treating dentists to be prepared to related to the participants not knowing the differences
educate patients about the oral complications result- between oral and IV BPs, or the effect of extended
ing from BP use and the need for appropriate duration of use, or the benefits and disadvantages of
dental care.14 continuing or discontinuing BPs.
Participants more frequently gave correct answers When scenario patients were given IV BPs, partici-
for the scenarios of patients on oral BP for less than pants were more likely to refer the patient. The
3 years, but more frequently gave wrong answers for authors also noted a decreased comfort level and
the scenarios of patients on oral BP for more than increased referral when the complexity of the
Table 6. SUMMARY OF FINAL REGRESSION MODEL PRESENTING THE IMPACT OF SIGNIFICANT PRACTITIONERS’
CHARACTERISTICS ON DECISION MAKING OF REFERRAL VERSUS SELECTING A CORRECT TREATMENT STRATEGY
Abbreviations: BRONJ, bisphosphonate-related osteonecrosis of the jaw; CI, confidence interval; GP, general practitioner.
Alhussain et al. Dentists Treating Patients on Bisphosphonates. J Oral Maxillofac Surg 2015.
ALHUSSAIN ET AL 1103
What resources do you use (or would you use) to staycurrent in dentistry?
Browsing Internet, scientific meetings, 72.2% journal articles, 86.4% continuing education
63.6% courses, 87.6%
Where did you first learn about BRONJ?
Graduate residency, no knowledge, Internet, dental scientific continuing journal
program, 5.8% 13.8% 14.6% school, meetings, education articles,
3.3% 20.0% 34.6% courses, 43.0% 56.7%
Do you feel comfortable treating patients with BRONJ with your current knowledge?
Unsure, 12.2% yes, could use minor supplementation, 22.7% no, 49.7%
15.4%
Which would be your preference for continuing education related to BRONJ?
DVD or videos, 28.3% annual Internet-based courses, 36.4% Full- or half-day courses, 51.2% journal
meetings, article,
33.9% 55.3%
Abbreviation: BRONJ, bisphosphonate-related osteonecrosis of the jaw.
Alhussain et al. Dentists Treating Patients on Bisphosphonates. J Oral Maxillofac Surg 2015.
1104 DENTISTS TREATING PATIENTS ON BISPHOSPHONATES
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