Awareness of The Risk of Radiation-Related Caries in Patients With Head and Neck Cancer: A Survey of Physicians, Dentists, and Patients

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Vol. 00 No. 00 && 2021

Awareness of the risk of radiation-related caries in


patients with head and neck cancer: A survey of
physicians, dentists, and patients
Beatriz Nascimento Figueiredo Lebre Martins, DDS,a Natalia Rangel Palmier, DDS, MSc,a,b
Ana Carolina Prado-Ribeiro, DDS, MSc, PhD,a,b Mario Fernando de Goes, DDS, MSc, PhD,c
Marcio Ajudarte Lopes, DDS, MSc, PhD,a Thais Bianca Brand~ao, DDS, MSc, PhD,b
Cesar Rivera, DDS, MSc, PhD,d Cesar Augusto Migliorati, DDS, MSc, PhD,e
Joel B. Epstein, DMD, MSD, FRCD, FDS RCS (E),f,g and Alan Roger Santos-Silva, DDS, MSc, PhDa

Objectives. Radiation-related caries (RRC) is one of the most aggressive complications of radiotherapy (RT) in survivors of head
and neck cancer (HNC). Lack of RRC awareness may contribute to the occurrence of this oral cavity complication. RRC may be
considered a “forgotten oral complication” by patients with HNC, oncologists, and dentists. The present study aimed to assess the
level of awareness of RRC among physicians, dentists, and patients.
Study Design. Physicians (group 1, G1), dentists (group 2, G2), and patients with HNC undergoing RT (group 3, G3) answered
questionnaires concerning their awareness of RRC. Physicians (G1) were divided into group 1A (oncological experience) and
group 1B (general physicians/other specialties). Dentists (G2) were divided into group 2A (oncological experience) and group 2B
(general dentists/other specialties). Personalized questionnaires were designed for each group.
Results. Recruitment was as follows: physicians (n = 124): 1A (n = 64), 1B (n = 60); dentists: (n = 280), 2A (n = 160), 2B (n = 120).
In addition, 58 patients answered the questionnaire. In terms of RRC awareness, 46.77% of physicians, 81.78% of dentists, and
24.13% of patients had some knowledge of the problem.
Conclusion. Patient awareness of RRC was poor. The heterogeneity of answers among physicians and dentists suggests an oppor-
tunity to improve patient education and prevention of this serious oral complication of RT. (Oral Surg Oral Med Oral Pathol Oral
Radiol 2021;000:1 11)

In 2018, approximately 888,000 new cases of head for HNC and can be used alone or combined with sur-
and neck cancer (HNC) were diagnosed worldwide. gery and chemotherapy.2 Worldwide it is estimated
Despite improvement in early diagnosis and therapy, that around 75% of patients with HNC and squamous
there were 453,000 deaths attributed to the disease.1 cell carcinoma (SCC) will be submitted to RT proto-
Radiotherapy (RT) is an important treatment modality cols as primary of adjuvant treatment modality.3
Regardless of the treatment success, it can have damag-
ing effects on normal tissue4,5 surrounding the tumoral
Beatriz Nascimento Figueiredo Lebre Martins and Natalia Rangel targeted areas and lead to a series of acute and chronic
Palmier are co-first authors.This study was financed in part by the toxicities that have been documented in the literature.6
Coordenaç~ao de Aperfeiçoamento de Pessoal de Nıvel Superior
One serious complication of RT in survivors of HNC
Brasil (CAPES) (Finance Code 001). The authors thank S~ao Paulo
Research Foundation (FAPESP) for financial support (Process Nos. is radiation-related caries (RRC). This complication
2018/04657-8, 2018/02233-6, 2016/22862-2, 2013/18402-8, and affects up to 29% of patients irradiated for HNC, which
2012/06138-1), as well as the National Council for Scientific and can increase to 37% after 2 years after RT.7 RRC can
Technological Development (CNPq), Brazil. lead to generalized destruction of teeth, loss of mastica-
a
University of Campinas (UNICAMP), Oral Diagnosis Department,
tory efficiency, chronic infection, and increased risk of
Piracicaba Dental School, Piracicaba, SP, Brazil.
b
Instituto do C^ancer do Estado de S~ao Paulo (ICESP-FMUSP), Den- developing osteoradionecrosis,7,8 which affects patients’
tal Oncology Service, S~ao Paulo, SP, Brazil. quality of life.7-9 RRC differs from conventional caries
c
University of Campinas (UNICAMP), Oral Rehabilitation Depart- in nonirradiated patients, in terms of both onset and
ment, Piracicaba Dental School, Piracicaba, SP, Brazil.
d
Department of Basic Biomedical Sciences, Universidad de Talca,
Talca, Chile.
e
Statement of Clinical Relevance
College of Dentistry, University of Florida, Gainesville, FL, USA.
f
Samuel Oschin Comprehensive Cancer Center, Cedars-Sinai Health Radiation-related caries (RRC) may be considered a
System, Los Angeles, CA, USA. “forgotten oral complication” of radiotherapy. Lack
g
City of Hope Comprehensive Cancer Center, Duarte, CA, USA.
Received for publication Mar 11, 2021; returned for revision May 27,
of RRC awareness by physicians and dentists in the
2021; accepted for publication Jun 13, 2021. oncology field could impair the provision of accu-
Ó 2021 Elsevier Inc. All rights reserved. rate information to patients, consequently, affecting
2212-4403/$-see front matter patients’ understanding of RRC.
https://doi.org/10.1016/j.oooo.2021.06.011

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progression and clinical presentation. RRC usually starts and treatment aimed at better dental prognosis and
as blackish-brown color alteration and the development improved quality of life for survivors.
of enamel cracks that promote enamel breakage or frac-
ture and, consequently, rapid destruction of the underly- MATERIALS AND METHODS
ing dentin. It mainly affects areas of the cusp, incisal The present study was a collaboration between dental
border, and cervical region leading, in more severe professionals of Piracicaba Dental School, University of
cases, to amputation of the dental crown.2,10-13 Campinas (UNICAMP), Brazil, and of the Dental Oncol-
The etiology of RRC is still not fully understood, and ogy Service of the S~ao Paulo State Cancer Institute
the ability of RT to cause direct radiogenic damage to the (ICESP-FMUSP), Brazil. This study was approved by
dentition leading to RRC has been discussed in the litera- the Ethics Committee for Human Studies at Piracicaba
ture.14,15 However, studies have shown that the clustering Dental School (UNICAMP), according to the recommen-
of oral symptoms using contemporary concepts has led to dations of the National Health Council Ministry of
new ideas for the analysis of RRC pathogenesis.16 This Health of Brazil for research in human patients (Protocol
clustering includes concurrent mucositis, taste changes, No. 88571818.8.0000.5418) and was developed accord-
oral infections, oral pain, trismus, hyposalivation, altered ing to the Strengthening the Reporting of Observational
saliva composition, and shifts in the composition of the Studies in Epidemiology statement guidelines.31
oral microbiota, which, associated with dietary changes
and deficient oral hygiene, lead to the development of a Sample and data collection
highly cariogenic oral environment, working in synergy to This was a cross-sectional study using questionnaires
increase the risk for RRC development and progres- developed to assess the level of awareness of RRC among
sion.4,16-18 RRC restorative treatment can be challenging physicians, dentists, and patients . Physicians (oncolo-
owing to altered dental substrate and a hostile oral envi- gists, head and neck surgeons, radiation oncologists, and
ronment. A recent systematic review showed that resin general practitioners), dentists (general practitioners, oral
composite restorations and fluoride supplementation may medicine specialists, and oral oncologists working in can-
be the best alternative for the treatment of RRC; neverthe- cer centers), and patients treated with RT for oral-oropha-
less, the longevity of dental restorations post head and ryngeal SCC were recruited for the study.
neck radiotherapy (HNRT) is still remarkably lower com-
pared with conventional restorations in nonirradiated Physicians. Physicians were divided into groups as fol-
patients.19 Counseling patients before, during, and after lows: group 1A: oncologists, head and neck surgeons,
RT could improve awareness of the complications of RT and radiation oncologists; group 1B: physicians with no
and, consequently, improve patients’ compliance with experience with patients with HNC. The locations for
RRC preventive measures.2,20-23 recruitment of physicians included hospitals that offered
Awareness studies are widely used to assess knowl- clinical oncology services and medical professionals in
edge or perception of a specific health issue or dis- private clinics or offices. Contact with health professio-
ease.24 Orfei et al.25 reported that lack of awareness nals was made through an active search by sharing the
can significantly affect the course of a disease and con- questionnaire weblink to professionals at different hos-
sequently its prognosis. Hence, awareness is essential pitals, clinics, and locations to reduce bias in the results.
to encourage more proactive behavior toward disease Clinical data, such as training time, residency, and/or
prevention and health promotion.26 This scientifically specialty and areas of expertise, were obtained for later
based strategy also provides the recognition of critical comparison of results. All physicians who agreed to par-
points that must be improved on a given health topic, ticipate answered the same questionnaire with 8 ques-
in addition to improving communication between pro- tions related to RRC using SurveyMonkey
fessionals and their patients. (SurveyMonkey Inc., San Mateo, CA, USA).32,33
Previously published studies have been carried out to
assess the level of knowledge of physicians,27 dentists,28 Dentists. Dentists were recruited as follows: group 2A:
and patients29,30 concerning awareness of the develop- oral medicine practitioners or dentists working in can-
ment of oral complications secondary to cancer treatment. cer treatment facilities and group 2B: dentists who do
In this context, studies have shown that RRC as an not focus their activities on the management of oncol-
adverse effect of RT is unknown by patients.8,30 Thus, ogy patients. The locations for recruitment of dentists
RRC still poses a major challenge for multi-professional were Piracicaba Dental School, University of Campi-
teams in the oncology setting. Thus, we investigated the nas, Brazil; cancer hospitals with dentistry services;
level of awareness of RRC among physicians, dentists, and dentists working in private practice. Contact with
and survivors of HNC. We considered knowledge in early health professionals was made via e-mail after an
diagnosis, referral for dental evaluation before initiation active search of the Brazilian Society of Oral Medicine
of cancer therapy, assessment of adequate prevention, and Oral Pathology databases. Selection was carried
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out in different hospitals, clinics, and locations to incomplete elementary education; 3B: complete ele-
reduce bias in the results. Clinical data, such as training mentary and/or high school and incomplete higher edu-
time, residency, and/or specialization courses and areas cation; 3C: complete higher education (university
of expertise, were obtained for later comparison of education).34 Patients were also divided into 2 groups
results. All selected dentists received the same ques- according to their clinical stage of disease (I/II and III/
tionnaire with 13 questions related to RRC ussinng IV), according to the American Joint Committee on
SurveyMonkey (SurveyMonkey).32,33 Cancer Staging System35,36 and further divided into 2
groups according to the number of teeth present in the
Patients. Patients with oral and oropharyngeal SCC mouth at the time of assessment: group 3D (3-17 teeth)
subjected to RT at ICESP-FMUSP were recruited. and group 3E (18-32 teeth).
Inclusion criteria included patients who underwent
dental evaluation, including oral hygiene and mouth Statistical analysis
conditioning protocols, before the beginning of onco- Answers to the 3 questionnaires were grouped in
logic treatment, where patients were instructed both Microsoft Office Excel 2019 (Microsoft 365; Microsoft
verbally and in written form of the adverse effects of Corp) for descriptive statistical analysis. Demographic
RT. Additionally, all patients were evaluated daily by profile data and questionnaire answers for the 3 groups
the dentists’ team throughout RT and the orientation were descriptively analyzed, and the results were
regarding oral complications of RT were reinforced assessed using absolute values and percentages. Mean
throughout the treatment course.8,21 values were used to analyze patient age. The effect of
The questionnaire was administered in the last week time in the specialty and awareness of RRC was ana-
of HNRT between the 30th and 35th RT sessions. All lyzed. Chi-square tests were used to correlate the data
patients received the same questionnaire with 7 ques- within the physician (1A and 2A), dentist (1B and 2B),
tions related to RRC. Patient questionnaires were pre- and patient (3A-3E) groups. Chi-square tests were used
sented by the same trained dental surgeon (N.R.P.). to correlate the data between physicians, dentists, and
When patients could not read or did not fully understand patients.
any of the questions, the dental surgeon responsible for Because the contact with health professionals (physi-
presenting the questionnaire explained the questions cians and dentists) was made through an active search,
(Supplemental Material S1). different hospitals, clinics, and locations, it was not
For data analysis, the patients were divided into 3 possible to measure how many professionals declined
groups according to their education level: group 3A: to participate in the present study. All contacted

Table I. Demographic characteristics of physicians included in this study.


Demographic features Physicians group Physicians group Total, n (%)
1A, n (%) 1B, n (%)
Sex
Male 43 (67.18) 33 (55) 76 (61.29)
Female 21 (32.81) 27 (45) 48 (38.70)
Age (years)
20-30 9 (14.06) 38 (63.33) 47 (37.90)
31-40 23 (35.93) 9 (15) 32 (25.80)
41-50 16 (25) 7 (11.6) 23 (18.54)
51-60 8 (12.5) 4 (6.6) 12 (9.67)
>60 8 (12.5) 2 (3.33) 10 (8.06)
Specialty
Head and neck surgeons 40 (62.50) 0 40 (32.25)
Radiotherapists 17 (26.56) 0 17 (13.7)
Oncologists 7 (10.95) 0 7 (5.64)
General physicians 0 49 (81.66) 49 (39.51)
Others 0 11 (18.34) 11 (8.87)
Time in the specialty
(years)
<5 14 (21.87) 41 (68.33) 55 (44.35)
5-10 15 (23.43) 4 (6.66) 19 (15.32)
10-20 15 (23.43) 7 (11.66) 22 (17.74)
>20 20 (31.25) 8 (13.3) 28 (22.58)
Physicians group 1A: head and neck surgeons, radiotherapists, or oncologists; physicians group 1B: general practice physicians, cardiologists, dermatolo-
gists, endoscopists, army or occupational physicians, neurologists, otorhinolaryngologists, pediatricians, psychiatrists, radiologists, and urologists.
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Table II. Demographic characteristics of dentists included in this study.


Demographic features Dentists group 2A, n (%) Dentists group 2B, n (%) Total, n (%)
Sex
Male 54 (33.75) 31 (25.83) 85 (30.35)
Female 106 (66.25) 89 (74.16) 195 (69.64)
Age (years)
20-30 62 (38.75) 53 (44.16) 115 (41.07)
31-40 57 (35.62) 40 (33.33) 97 (34.64)
41-50 28 (17.5) 12 (10) 40 (14.28)
51-60 8 (5) 11 (9.16) 19 (6.7)
>60 5 (3.12) 4 (3.33) 9 (3.21)
Specialty
Oral medicine or dentists working with oncological dentistry 160 (100) 0 160 (57.14)
Oral and maxillofacial surgery* 0 25 (20.83) 25 (8.93)
Orthodontics 0 21 (17.5) 21 (7.5)
Oral rehabilitation 0 20 (16.66) 20 (7.14)
Pediatric dentistry 0 14 (11.66) 14 (5)
Endodontics 0 13 (10.83) 13 (4.64)
Dentistry 0 11 (9.16) 11 (3.93)
Periodontics 0 10 (8.33) 10 (3.57)
Social/legal dentistry 0 6 (5) 6 (2.14)
Time in the specialty (years)
<5 68 (42.5) 55 (45.83) 123 (43.92)
5-10 19 (11.87) 17 (14.16) 36 (12.85)
10-20 30 (18.75) 21 (17.5) 51 (18.21)
>20 43 (26.87) 27 (22.5) 70 (25)
Dentists group 2A: Oral medicine or dentists working with oncological dentistry; dentists group 2B: oral and maxillofacial surgery (*with no
experience in oncological centers or patients with head and neck cancer patients), orthodontics, oral rehabilitation, pediatric dentistry, endodon-
tics, dentistry, periodontics, and social/legal dentistry.

patients agreed to participate in the study by answering medicine practitioners or dental surgeons working in
the questionnaire. oral oncology and group 2B included 120 dental pro-
fessionals (42.86%): 25 oral and maxillofacial sur-
RESULTS geons (8.93%), 21 orthodontists (7.5%), 20
In a total, 458 individuals participated in the surveys, prosthodontics and oral rehabilitation specialists
as follows: 124 physicians: oncologists, head and neck (7.16%), 14 pediatric dentists (5%), 13 endodontists
surgeons, and radiation oncologists (n = 64) and gen- (4.6%), 11 dentistry specialists (3.92%), 10 periodont-
eral physicians (n = 60); 280 dentists: oral medicine ists (3.57%), and 6 forensic dentistry specialists
practitioners or dentists working in cancer treatment (2.14%). Most dental specialists were practicing their
facilities (n = 160) and general dentists (n = 120); and specialty for <5 years (123; 43.93%) (Table II). The
58 patients who received RT for treatment of oral-oro- estimated age of dentists was 25 to 60 years, with an
pharyngeal SCC. equal distribution between male and female dentists.
The demographic profile of physicians is shown in Owing to the age range options on the objective ques-
Table I. Seventy-six physicians were male (61.3%) and tionnaire, it was not possible to calculate mean age
48 were female (38.7%). Of these 124 physicians, data for this group. Nevertheless, there was a concen-
group 1A included 40 head and neck surgeons tration of dentists between 20 and 30 years old (115;
(62.50%), 17 radiation oncologists (26.56%), and 7 41.07%) and between 31 and 40 years old (97;
medical oncologists (10.95%), and group 1B included 34.64%).
physicians who had no experience with patients with The patient group included 58 participants, of whom
HNC (60; 48.38%). Most physicians (55; 44.35%) 51 were male (87.93%) and 7 were female (12.07%).
were in the specialty for <5 years. The estimated age Their mean age was 57.3 years (range, 39-72). Primary
of physicians ranged from 25 to 60 years (mean, 38.35 tumors were located on the tongue (14, 24.13%), oro-
years), with an equal distribution between male and pharynx (13, 22.41%), retromolar area (5, 8.62%), pal-
female physicians. ate (4, 6.89), lip (4, 6.89%), larynx (3, 5.17%), and
Of the 280 dentists who replied to the questionnaire, other sites (13, 25.89%). Most patients were diagnosed
195 were female (69.64%) and 85 were male as having advanced clinical stage III (13, 22.41%) and
(30.36%). Group 2A included 160 (57.14%) oral stage IV (29, 50%) disease. The most frequent
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Table III. Demographic characteristics of patients the 2 groups. Group 2A (78, 48.45%) and group 2B
included in this study. (61, 50.83%) responded approximately 20%, but
among 51.55% of dentists in group 2A and 49.17% in
Variables n (%)
group 2B, answers varied between 5%, 75%, and 90%.
Age (years), mean (range) 57.3 (39-72) Two hundred and sixteen dentists (77.14%) advised
Sex
Male 51 (87.9)
their patients undergoing HNC RT to be evaluated by a
Female 7 (12.1) dentist trained in the field. In addition, 209 (74.64%)
Primary tumor site believed that RRC can lead to osteoradionecrosis.
Tongue 14 (24.13) Patients were grouped according to education level,
Oropharynx 13 (22.41) clinical stage of the disease, and number of teeth pres-
Retromolar trigone 5 (8.62)
Lip 4 (6.89)
ent (Table VI). Most patients (44, 75.86%) were not
Palate 4 (6.89) aware of RRC. Additionally, 38 patients (65.5%)
Larynx 3 (5.17) believed that the decrease in saliva caused by RT could
Other sites 13 (25.89) be associated with RRC (Table VI). Patients with a
Clinical stage higher education level (group 3C) had better overall
Stage I (3.44)
Stage II 7 (12.06)
results relating to their comprehension of the effects of
Stage III 13 (22.41) RT leading to the development of RRC (74.07%).
Stage IV 29 (50) Group 3C also reported being advised by physicians
Unavailable* 7 (12.06) (55.5%) and dentists (77.8%) to see a dental specialist
Treatment in the field at higher frequency than patients with lower
Surgery + RT 13 (22.41)
RCT 28 (48.27)
education levels (groups 3A and 3B) (Table VI).
Surgery + RCT 9 (15.51) More patients (66.66%) in initial stages I/II of disease
Exclusive RT 8 (13.79) reported being advised by their dentists of the possibility
HNRT modality of developing caries after RT than were patients in
3DRT 36 (62.06) advanced clinical stages III/IV (59.52%). This correlation
VMAT 18 (31.03),
IMRT 4 (6.89).
was also observed regarding orientation from the physi-
Mean radiation dose 63.92 Gy cians, where more patients in stages I/II (55.55%) reported
being advised about RRC by their physicians compared
3DRT, 3D conformal radiotherapy; HNRT, Head and neckl radiother-
apy; IMRT, intensity-modulated radiotherapy; RCT, radiochemother-
with patients in stages III/IV (45.23%) (Table VI).
apy; RT, radiotherapy; VMAT, volumetric modulated arc therapy. Patients with a greater number of teeth (group 3E)
*Patients’ cancer staging information was not available in medical had an increased awareness of RRC (30%). They were
charts. more often informed of the effects of RT on RRC
(80%) and were better informed by their physicians
(50%) and dentists (66.6%) that hyposalivation could
oncologic treatment was concomitant radiochemother- lead to the development of RRC (73.3%). All patients
apy (RCT) (28, 48.27%) (Table III). in groups 3D and 3E understood that oral hygiene
The data obtained from physicians are presented in affected the risk of RRC. Similarly, the effect of RRC
Table IV. Regarding RRC awareness, 58 physicians on osteoradionecrosis (ORN) development was under-
(46.77%) were aware of this toxicity. Most physicians stood in both groups (89.28% in group 3D and 86.66%
in group 1A (36; 56.25%) and group 1B (41; 68.33%) in group 3E, respectively) (Table VI).
groups believed that the percentage of patients postirra-
diation who will develop RRC is 20% (P < .03). DISCUSSION
Regarding the approximate time for the development The present study assessed the level of awareness of
of RRC, professionals in group 1A (29, 45.31%) and physicians who work with patients with HNC and gen-
group 1B (29, 48.33%) responded 12 months (P < eral physicians; dentists who work with patients with
0,03), but for 54.69% in group 1A and 51.67% in group cancer and general dentists, and patients with HNC with
1B answered varied from 1 month, 3 months, and 36 a focus on RRC clinical characteristics. Based on recent
months as the time for the development of RRC post- published studies in the field, to our knowledge, this is
HNRT. Seventy-seven physicians advised patients the first study to evaluate awareness of RRC from the
undergoing RT for HNC to be evaluated by dentists perspective of physicians, dentists, and patients.1,7,8,30
(62.09%). RRC is an adverse effect of RT that can lead to wide-
Data obtained from dentists are shown in Table V. spread destruction of teeth, loss of masticatory effi-
Regarding RRC awareness, 229 dentists (81.78%) ciency, and chronic infection and increase the risk for
were aware of this toxicity. Knowledge regarding the the development of osteoradionecrosis, with a direct
approximate incidence of RRC post-RT varied between effect on patients’ quality of life.8,9 These patients may
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Table IV. Physicians’ questionnaire answers.


Questions Physicians group 1A, n (%) Physicians group 1B, n (%) Total, n (%)
Are you aware of the concept of RRC?
Yes 50 (78.12) 8 (13.33) 58 (46.77)
No 14 (21.87) 52 (86.66) 66 (53.22)
Which patients are susceptible to RRC?
Head and neck cancer 63 (98.43) 58 (96.66) 121 (97.58)
Multiple myeloma 1 (1.56) 1 (1.66) 2 (1.61)
Graft vs host disease 0 1 (1.66) 1 (0.80)
Bone marrow transplant 0 0 0
How long (approximately) until the development of RRC (after RT)?
1 month 4 (6.25) 6 (10) 10 (0.80)
3 months 18 (28.12) 20 (33.33) 38 (30.64)
12 months 29 (45.31) 29 (48.33) 58 (46.77)
36 months 13 (20.31) 5 (8.3) 18 (14.51)
Do you believe that RRC can be more aggressive than conventional caries?
Yes 63 (98.43) 52 (86.66) 115 (92.74)
No 1 (1.56) 8 (13.33) 9 (7.25)
What is the approximate percentage of post-RT patients who will develop RRC?
5% 9 (14.06) 15 (25) 24 (19.35)
20% 36 (56.25) 41 (68.33) 77 (62.09)
75% 14 (21.87) 4 (6.66) 18 (14.51)
90% 5 (7.81) 0 5 (4.03)
Do you advise your patients with head and neck cancer undergoing RT to be evaluated by a dentist?
Yes 61 (95.31) 16 (26.66) 77 (62.09)
No 2 (3.12) 14 (23.33) 16 (12.90)
Not applicable 1 (1.56) 30 (50) 31 (25)
Do you advise your patients with head and neck cancer undergoing RT of the risk of developing RRC?
Yes 43 (67.18) 8 (13.33) 51 (41.12)
No 18 (28.12) 22 (36.66) 40 (32.25)
Not applicable 3 (4.68) 30 (50) 33 (26.61)
Do you believe that RRC can lead to osteoradionecrosis?
Yes 60 (93.75) 58 (96.66) 118 (95.16)
No 4 (6.25 2 (3.33) 6 (4.83)

Physicians group 1A: Head and neck surgeons, radiotherapists, or oncologists; physicians group 1B: general practice physicians, cardiologists,
dermatologists, endoscopists, army or occupational physicians, neurologists, otorhinolaryngologists, pediatricians, psychiatrists, radiologists, and
urologists.
RRC, radiation-related caries; RT, radiotherapy.

choose to avoid social interaction, eating, conversation, the development of RRC, where group 1A (45.31%) and
laughing, smiling, and engaging in relationship behav- group 1B (48.33%) reported that the approximate time
iors such as kissing because of the embarrassment asso- for the development of RRC is 12 months, but answers
ciated with the appearance of their teeth.9,37-39 from 54.69% in group 1A and 51.67% in group 1B varied
Although RRC was first described more than between 1 month, 3 months, and 36 months, showing that
80 years ago,40 our results showed that only 46.77% of less than half knew the time for onset and progression of
physicians were aware of it in relation to HNC treat- RRC. It is known that RRC begins within the first year
ment. This lack of awareness can compromise the (6-12 months) after HNRT. The first clinical changes in
safety of their patients and expose them to serious tooth structure include demineralization of enamel and
problems that could be prevented.41 dentin, the development of cracks and fissures that pro-
Overall, physicians and dentists answered most of mote enamel breakage or fracture, cavitation with struc-
the questions correctly. Previous studies regarding ture loss, discoloration of tooth structure, and, with the
other oral complications of head and neck RT reported progression of tooth structure, destruction leading to
that this high rate of correct answers could be amputation of the dental crown.8,13 Thus, the lack of
explained by the way the data collection was carried knowledge among physicians treating this patient popula-
out because the questionnaires were designed to be tion may lead to a delay in diagnosis of RRC and
completed in approximately 5 minutes.27 increased risk of additional complications after the devel-
When comparing the answers within physician groups opment and progression of structural damage that may
1A and 1B, the answers varied. This divergence stands lead to dental fracture, dental abscess, high of risk of
out for the question regarding the approximate time for osteoradionecrosis, and decreased quality of life.8,9
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Table V. Dentists’ questionnaire answers.


Questions Dentists group 2A, n (%) Dentists group 2B, n (%) Total, n (%)
Are you aware of the concept of RRC?
Yes 155 (97) 74 (46) 229 (81.78)
No 5 (3) 46 (29) 51 (18.21)
Which patients are susceptible to RRC?
Head and neck cancer 160 (100) 119 (99) 279 (99.64)
Multiple myeloma 0 1 (1) 1 (0.35)
Graft vs host disease 0 0 0
Bone marrow transplant 0 0 0
How long (approximately) until the development of RRC (after RT)?
1 month 31 (19.37) 21 (17.5) 52 (18.57)
3 months 62 (38.75) 55 (45.83) 117 (41.78)
12 months 60 (37.5) 37 (30.83) 97 (34.64)
36 months 7 (4.37) 7 (5.83) 14 (5)
Do you believe that RRC can be more aggressive than conventional caries?
Yes 145 (90.62) 102 (85) 247 (88.21)
No 15 (9.37) 18 (15) 33 (11.79)
What is the approximate percentage of post-RT patients who will develop RRC?
5% 8 (5) 17 (14.17) 25 (8.92)
20% 78 (48.45) 61 (50.83) 139 (49.64)
75% 66 (41.25) 35 (29.17) 101 (36.07)
90% 8 (5) 7 (5.83) 15 (5.35)
Do you believe that RRC develops:
Proximal region, scars, and fissures? 11 (6.87) 27 (22.5) 38 (13.57)
Cervical region, incisal edge, and cusp tip? 149 (93.12) 93 (77.5) 242 (86.42)
Do you advise your patients with head and neck cancer undergoing RT o be evaluated by a specialist dentist in the field?
Yes 129 (80.62) 87 (72.5) 216 (77.14)
No 7 (4.3) 17 (14.16) 24 (8.57)
Not applicable 24 (15) 16 (13.33) 40 (14.28)
Do you advise your patients with head and neck cancer undergoing RT of the risk of developing RRC?
Yes 147 (91.87) 77 (64.16) 224 (80)
No 2 (1.25) 23 (19.16) 25 (8.92)
Not applicable 11 (6.87) 20 (16.66) 31 (11.07)
Do you believe that RRC can present as blackish-brown spots?
Yes 155 (96.87) 99 (82.5) 254 (90.71)
No 5 (3.12) 21(17.5) 26 (9.28)
Do you believe that cracks and enamel cracks can be part of the spectrum of RRC?
Yes 98 (61.25) 70 (58.33) 168 (60)
No 62 (38.75) 50 (41.66) 112 (40)
Do you believe that RRC can lead to enamel delamination or amputation of the dental crown?
Yes 148 (92.5) 107 (89.16) 255 (91.07)
No 12 (7.5) 13 (10.83) 25 (8.92)
Do you believe that RRC can lead to osteoradionecrosis?
Yes 129 (80.62) 80 (66.66) 209 (74.64)
No 31 (19.37) 40 (33.33) 71 (25.35)
Do you believe that the RRC restorative treatment has the same longevity as conventional caries restorative treatment?
Yes 25 (15.62) 41 (34.16) 66 (23.57)
No 135 (84.37) 79 (65.83) 214 (76.42)

Dentists group 2A: Oral medicine or dentists working with oncological dentistry; dentists group 2B: oral and maxillofacial surgery, orthodontics,
oral rehabilitation, pediatric dentistry, endodontics, dentistry, periodontics, social/legal dentistry.
RRC, radiation-related caries; RT, radiotherapy.

Most dentists (81.78%) reported that they were knowledge of RRC varied between the groups of den-
aware of RRC. This was expected because dental care tists, reinforcing the need for better education of dental
programs for patients with HNC have been well docu- professionals on the unique aspects of RRC and how to
mented in the literature.42-44 In addition to decreasing best manage patients with HNC undergoing RT.52
the risk of oral toxicity, preventive dental care pro- Patients undergoing RT should receive intensive oral
grams can lower the cost of treatment in hospitalized hygiene instructions, high-potency fluoride applica-
patients.45-50 For instance, the global cost of RRC man- tions, salivary stimulation and antimicrobial therapy
agement ranges from $192 to $4500.51 However, when indicated, dietary advice, and regular dental
8 Martins et al.
ORAL MEDICINE
Table VI. Patient questionnaire answers by subgroup.
Level of education, n (%) Cancer staging, n (%) No. of teeth, n (%) Total, n (%)
Questions 3A 3B 3C I-II III-IV Unavailable* 3D 3E
Are you aware of the concept of RRC?
Yes 1 (25) 6 (22.22) 7 (25.92) 1 (11.11) 11 (26.19) 5 (17.85) 5 (17.85) 9 (30) 14 (24.13)
No 3 (75) 21 (77.78) 20 (74.07) 8 (88.88) 31 (73.80) 23 (82.14) 23 (82.14) 21 (70) 44 (75.86)

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Do you believe that radiation can affect teeth, leading to caries?
Yes 2 (50) 8 (29.62) 20 (74.07) 8 (88.89) 29 (69.04) 19 (67.85) 19 (67.85) 24 (80) 30 (51.72)
No 2 (50) 19 (70.37) 7 (25.92) 1 (11.11) 13 (30.95) 9 (32.14) 9 (32.14) 6 (20) 28 (48.27)
Were you advised by your physician of the possibility of developing caries after RT?
Yes 1 (25) 10 (37.03) 15 (55.55) 5 (55.55) 19 (45.23) 11 (39.28) 11 (39.28) 15 (50) 26 (44.82)
No 3 (75) 17 (62.96) 12 (44.45) 4 (44.44) 23 (54.76 17 (60.71) 17 (60.71) 15 (50) 32 (55.18)
Were you advised by your dentist of the possibility of developing caries after RT?
Yes 1 (25) 12 (44.45) 21 (77.78) 6 (66.66) 25 (59.52) 14 (50) 14 (50) 20 (66.66) 34 (58.62)
No 3 (75) 15 (55.55) 6 (22.22) 3 (33.33) 17 (40.47) 14 (50) 14 (50) 10 (33.33) 24 (41.37)
Do you believe that RT-related hyposalivation increases the risk of the development of RRC?
Yes 4 (100) 17 (62.96) 17 (62.96) 5 (55.55) 28 (66.66) 16 (57.14) 16 (57.14) 22 (73.33) 38 (65.51)
No 0 10 (37.04) 10 (37.04) 4 (44.44) 14 (33.33) 12 (42.85) 12 (42.85) 8 (26.66) 20 (34.49)
Do you believe that good oral hygiene can help prevent the development of RRC?
Yes 4 (100) 27 (100) 27 (100) 9 (100) 42 (100) 28 (100) 28 (100) 30 (100) 58 (100)
No 0 0 0 0 0 0 0 0 0
Do you believe that RRC can lead to osteoradionecrosis?
Yes 4 (100) 23 (85.18) 24 (88.88) 7 (77.77) 39 (92.85) 25 (89.28) 25 (89.28) 26 (86.66) 51 (87.94)
No 0 4 (14.82) 3 (11.12) 2 (22.22) 3 (7.14) 3 (10.71) 3 (10.71) 4 (13.33) 7 (12.06)
3A: complete elementary; 3B2: incomplete high school and complete high school or incomplete higher education; 3C: complete higher education university education; 3D: 3 to 17 teeth present in mouth; and
3E: 18 to 30 teeth present in mouth.
RRC, radiation-related caries; RT, radiotherapy.
*Patients’ cancer staging information was not available in medical charts.

&& 2021
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Volume 00, Number 00 Martins et al. 9

follow-up before, during, and after treatment to prevent study, osteoradionecrosis was the most unknown toxic-
dental complications. Pre-RT dental evaluation and ity of RT, followed by RRC (43%).30 Patients in the
indicated treatment with a preventive program for car- present study presented a remarkably higher lack of
ies reduction to reduce the need for tooth extractions awareness of RRC (75.86%) compared with patients
post-RT and minimize the risk of osteoradionecrosis who were advised of RT complications with an educa-
should also be performed.53,54 tional video,30 which reinforces the need for better
RRC can lead to the destruction of teeth and associ- strategies for the delivery of information regarding pos-
ated dental infection.4,7,8 Dental extractions may need sible complications of HNRT. Results also corroborate
to be avoided in teeth in the high dose radiated volume the literature assessment of the level of awareness
owing to risk of osteoradionecrosis.8,51 Nevertheless, regarding other oral toxicities of cancer treatment, such
25.35% of dentists do not believe that RRC can lead to as oral mucositis, among physicians, dentists, and
osteoradionecrosis. This lack of knowledge can lead to patients, which also reported a low level of aware-
inappropriate treatment that can affect the course of the ness.59-63
disease and lead to complications of RT.25 All patients with HNC treated with RT should be
Awareness is essential to encourage proactive aware of the importance of oral hygiene. Epstein
behavior related to disease and promote health.26 How- et al.64 suggested that patients’ dental behaviors are
ever, studies have shown that without close interdisci- more positive when recommendations are delivered by
plinary cooperation, communication gaps may occur oncology professionals. However, the present study
between physicians, dentists, and patients. The lack of demonstrated that 55.18% of patients reported that
communication might increase the risk of complica- they were not advised by their physicians of the risk of
tions.29 Therefore, irradiated patients are at significant developing RRC. On the other hand, 58.62% of
risk of potentially debilitating oral complications, patients reported that they were advised by dentists of
which can be prevented or at least more appropriately the possibility of developing RRC. Nevertheless, both
managed if dental and medical health care providers results are low considering that only approximately
work together in an interprofessional fashion.55,56 half of patients reported being advised by a physician
As previously mentioned, all patients included in the or dentist of the risk of developing RRC. Even health
present study were instructed both verbally and in writ- care professionals who do not regularly work with
ten form of the adverse effects of RT. The guidelines patients with HNC should have knowledge regarding
covering RRC and other toxicities were reinforced at this complication of RT, considering that with advan-
every dental appointment.8,28 Nevertheless, 75% of ces in cancer treatment and increase in overall survival
patients were not aware of RRC. This lack of patient rates these patients may require assistance from a vari-
awareness may be explained in part by the inadequate ety of health care providers in addition to physicians
education of health professionals and the lack of inter- and dentists who work in oncology.65-68
est in the problem on the part of patients being treated
for cancer.29,30 Another reason could be the lack of
knowledge among health professionals who do not
CONCLUSIONS
educate patients on the effect of cancer therapy on den-
Patients with HNC had limited awareness of RRC.
tal health and the risk of RRC.27
Despite the percentage of correct answers, the hetero-
Patients’ level of education, as observed in Table VI,
geneity of answers among physicians and dentists may
may explain differences in the way patients answered the
be an important factor in how the information is pre-
questionnaires. Although not statistically significant,
sented to patients and caregivers. The lack of aware-
patients with a higher level of education (group 3C)
ness impairs the provision of accurate information to
answered more questions correctly compared with those
patients, consequently affecting patients’ understand-
with a lower level of education (groups 3A and 3B). Edu-
ing of RRC. Strategies for further dissemination and
cation contributes to the development of a range of skills
better communication between health care providers
and traits, such as cognitive skills, problem-solving abil-
and patients in addition to measures to prevent RRC
ity, learning effectiveness, and personal control.57
must be established to provide the best care for these
Table VI shows a trend that patients with a greater num-
patients.
ber of teeth (18-30) answered more questions correctly.
This suggests that patients with better oral health may be
more aware and maintain good oral and dental health.
These patients may also pay more attention to instructions ACKNOWLEDGMENTS
regarding necessary oral care during and after HNRT.58 We thank the Brazilian Society of Stomatology
Fernandes et al.30 reported similar results regarding (SOBEP) for their support in sending questionnaires to
the low level of awareness among patients. In their the participants.
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APPENDIX

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