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The oral health status of IN BRIEF • Reports the first UK data published on RESEARCH this subject. pre-treatment head and neck • Highlights the poor oral health of head and neck patients at the time of diagnosis and the potential impact on long-term oral health. cancer patients • Emphasises the need for comprehensive preventive regimes in this group of S. B. Critchlow,*1 C. Morgan2 and T. Leung2 patients.

Background It is sometimes stated anecdotally that patients with have poor oral health at the time of oncology diagnosis; however, there is little data in the literature to confirm or refute this claim.Aim To assess, in the first UK study of its type, the oral health status of 100 patients attending for a dental assessment at a single centre before head and neck cancer treatment was commenced. Subjects Sixty-six male patients and 34 female patients were included. Results Of all 100 patients, 2% (2/100) were edentulous. Of the dentate patients, 71% (70/98) were clinically diagnosed with . Fifty-one percent (50/98) had a maximum probing pocket depth in excess of 6 mm. The mean number of carious teeth per dentate subject was 2.4 (95% C.I. 1.6‑3.1). Sixty-one percent (60/98) of dentate patients presented with one or more carious teeth. Conclusions Within this cohort, head and neck cancer patients had poor oral health at the time of oncology diagnosis, with caries and periodontal disease being important clinical issues. The implications for the dental management of these patients are discussed.

INTRODUCTION with either radiotherapy alone, surgery alone, The term head and neck cancer (HANC) or a combination of the two, sometimes with refers to a wide variety of tumours adjuvant chemotherapy.11,12 Radiotherapy has presenting in the aero-digestive tract of a number of side effects relevant to the oral the head and neck region.1 Due to the way cavity, which are shown in Table 1. that cancer statistics are compiled, exact Xerostomia and leave patients incidence figures for HANC as a whole are who have had radiotherapy at significantly difficult to obtain; however, it has been increased risk of dental caries and they can reported that there are approximately suffer rapid deterioration of their remaining 670,000 new cases worldwide annually, dentition (Fig. 1).13–15 This is of particular Fig. 1 A classic pattern of radiation caries amounting to approximately 6% of all relevance as many will be prescribed dietary with frothy, viscous saliva in a patient who malignant .2 supplements high in refined sugars in order underwent radiotherapy Specifically regarding , there to meet their nutritional requirements were 6,236 recorded new cases in the UK in around the treatment period. 2009, amounting to 2% of all new cancer Guidelines from the National Institute cases.3 Histologically, 95% of oral cancers for Health and Care Excellence (NICE) state are squamous cell carcinomas (SCC).4,5 that all HANC patients should be seen for The primary risk factors include smoking, dental assessment before their oncology alcohol, chewing of bettle nut/paan, the treatment.16 Due to the complex nature of human papilloma virus, immune status, the decision making and the subsequent genetics and socioeconomic factors.6–10 oral rehabilitation that is often required for The management of HANC in the UK is HANC patients, consultants in restorative carried out by multi-disciplinary teams dentistry are the people best trained and comprising multiple specialists from across best placed to carry out this assessment.16 Fig. 2 Osteoradionecrosis of the maxilla the healthcare spectrum. HANC can be treated The role of the restorative consultant can following radiotherapy for a squamous cell carcinoma of the nasal septum. Providing oral be summarised as follows: 1Specialist Registrar in Restorative Dentistry, rehabilitation for this patient was challenging 2Consultant in Restorative Dentistry, Department of • Optimise oral health before treatment Restorative Dentistry, Royal London Hospital Dental • Institute prevention Institute, New Road, Whitechapel, London, E1 1BB • Plan and facilitate extractions It is of particular importance that patients *Correspondence to Simon Bryan Critchlow Email: [email protected] before radiotherapy are seen for their dental assessment before • Provide support during treatment radiotherapy so a risk assessment can be Online article number E1 • Provide oral rehabilitation following carried out and teeth of reduced prognosis Refereed Paper - accepted 25 September 2013 DOI: 10.1038/sj.bdj.2013.1246 treatment can be extracted before radiation exposure. ©British Dental Journal 2014; 216: E1 • Facilitate maintenance. Extraction of teeth following radiotherapy

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can be contraindicated due to the risk of a consultant in restorative dentistry (CM Table 1 Side effects of radiotherapy. Many developing osteoradionecrosis, which can or TL). The following demographic details of the acute side effects of radiotherapy be severe and debilitating (Fig. 2).17–20 were recorded: become chronic over time14,15 The decision to recommend extractions • Date of birth Acute Chronic is one that must be made with great care • Sex and is influenced by a number of factors. • Oncology diagnosis Dysphagia Dysphagia These include oncology factors such as • Details of planned surgery, Taste disturbances Taste disturbances prognosis for curative treatment and the radiotherapy or chemotherapy specific planned surgical approach; and • Presence of gastro-oesophageal reflux Trismus Trismus the proposed radiotherapy fields, including disease (GORD) Mucositis Xerostomia doses to individual teeth. Patient factors such • General dental practitioner (GDP) status as oral hygiene and patient expectations; • Alcohol consumption Neck/cheek fibrosis toothwear and existing patterns of tooth • Smoking status Osteoradionecrosis loss; as well as individual tooth factors • Smokeless tobacco use (betel nut/paan). including any existing restorations, caries, periodontal and endodontic status and Patients were categorised as having RESULTS where each individual tooth sits in an GORD if they had ticked the relevant box Sixty-six male patients and 34 female overall strategic plan for oral rehabilitation on the medical history questionnaire at patients were included. Age ranged from post-operatively; must also be considered. their assessment visit. As part of the initial 20 years to 88 years with a mean age of Anecdotally, HANC patients have poor assessment, patients were asked if they visit 61 (95% CI 58.2‑63.4) years at the time dental health at the time of their cancer a dentist regularly or irregularly. Alcohol of presentation. Tobacco and alcohol diagnosis; however, there is no UK data consumption was self-reported in number of consumption is shown in Tables 2 and 3. currently available regarding this specific units per week. Smoking status was recorded Of the 100 patients, 3% (3/100) of patients group of patients. In a Brazilian study of by asking patients whether they were a reported using betel nut/paan. Self-reported 207 pre-radiotherapy patients it was found current smoker, ex-smoker or non-smoker. GORD was 9% (9/100) in this cohort. that 12% had caries, 41% periodontal The use of smokeless tobacco products or Ninety-one percent (91/100) of patients disease and 21% had one or more retained betel nut/paan was also recorded. presented with a squamous cell carcinoma roots.21 Katsura et al. found a mean probing As regards clinical data, BPE scores were (SCC). The tumour sites are shown in Figure 3. pocket depth of 4.82 mm in a group recorded. In addition, probing pocket depths The TNM staging of the tumours is shown in of 242 patients before radiotherapy.22 (PPD) of 4 mm or more were recorded on Figure 4.Ninety percent (90/100) of patients Lockhart and Clark found a high incidence individual teeth. On teeth where multiple were planned to have radiotherapy as part of alveolar bone loss (66%), clinical caries PPD were measured, the deepest pocket was of their oncology treatment. Sixteen percent (71%) and failing restorations (91%) in recorded. A standard dental chart was used (16/100) were planned for radiotherapy 131 pre-radiotherapy patients.23 to record the DMFT and type of restoration alone, 27% (17/100) were planned for The aim of this study is to present data present. Caries was diagnosed using both chemoradiotherapy, 26% (26/100) were regarding the levels of dental disease in clinical and radiographic findings. The planned for surgery and radiotherapy and head and neck cancer patients attending dental diagnoses made at the time of 20% (20/100) were planned for surgery and a UK dental hospital for assessment initial presentation were recorded, as was chemoradiotherapy. Six percent (6/100) before commencement of their oncology the treatment plan including the number were planned for surgery alone. In 2% treatment. of planned tooth extractions. (2/100) of cases it was undecided as to MATERIALS AND METHODS Before oncology treatment, all whether radiotherapy would be needed patients received thorough oral hygiene post-operatively. A further 3% (3/100) were Records from 100 patients who were instruction and diet advice. In addition, planned for surgery and chemotherapy referred from the Barts Health HANC all patients were given an information and one patient was planned for multi-disciplinary team (MDT) for pre- leaflet and a letter to take to their general chemotherapy alone. oncology treatment dental assessments medical practitioner for the prescription Forty-three percent (43/100) of patients at the Royal London Hospital Dental of Duraphat® toothpaste 5,000 ppm reported visiting a dentist regularly. Institute, Whitechapel, London from fluoride and fluoride mouth rinse for life Two percent (2/100) of patients were January 2008 were reviewed. Case notes in accordance with NICE guidelines.16 edentulous and 64% (64/100) had 21 or were examined consecutively by date of Patients undergoing surgery had their more natural teeth. The mean decayed/ dental assessment until a convenience extractions carried out at the same time as missing/filled teeth (DMFT) score was 19.6 sample of 100 was reached. No power their oncology surgery. Those undergoing (95% CI 17.0‑21.1). calculation was possible. Inclusion radiotherapy had their extractions carried Regarding the 98 dentate patients, 71% criteria in the study were a diagnosis out within two weeks of their dental (70/98) were clinically diagnosed with of HANC at the time of assessment and assessment. Socket healing was reviewed periodontal disease. Fifty-one percent a complete data set in the case notes. before commencement of radiotherapy to (50/98) had a maximum probing pocket Exclusion criteria were no diagnosis of ensure soft tissue healing. The minimum depth in excess of 6 mm. A further 26% HANC, previous diagnosis and treatment time period between completion of (25/98) presented with a maximum probing for HANC and incomplete data in the extractions and commencement of pocket depths of 4-6 mm. case notes. Dental assessments took place radiotherapy was two weeks. The mean number of carious teeth per within two weeks of the patients receiving Statistical analysis was carried out using dentate patient was 2.4 (95% CI 1.6‑3.1). their oncology diagnosis and all patients SPSS statistical software package (SPSS Sixty-one percent (60/98) of patients were seen for their dental assessment by v. 18.0. SPSS Inc. Chicago Ill). presented with one or more carious

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Table 2 Smoking status were molar teeth, 16% (78/494) were premolars and 17% (84/494) were incisors Study cohort Nationally24 and canines. Which teeth to extract are Smoker 25% 20% influenced considerably by radiotherapy Non-smoker 43% 47% being planned as part of the treatment. However, when those patients not Ex-smoker 41% 33% undergoing radiotherapy were discounted, the mean number of teeth planned for Table 3 Alcohol intake extraction was unchanged.

This cohort Nationally25 DISCUSSION

Males >28 units per week 14% 27% This cohort of HANC patients had poor oral health at the time of presentation. Caries Females >21 units per week 4% 13% and moderate-advanced periodontitis were significant clinical issues. In order to put these findings into context it is important to consider how the patients in this study compare to the general population. Tongue The demographics of this cohort are Tonsil consistent with national data in terms of 2,4,5 Tongue base, larynx sex, age and oncology diagnosis. The Supraglottis data on smoking is interesting as it seems Unknown, naso pharynx that within this cohort of patients there Maxilla are fewer smokers than in the general 24 Parotid, glottis, buccal mucosa population. It is the experience of the Hypopharynx authors that a number of patients will Soft , retromolar and pharynx report quitting smoking at the time of their cancer diagnosis, usually a few days Scalp, pre-auricular, posterior cricoid, piriform fossa, palate, oesophagus, mandibular, nasal, epiglotis before their dental assessment. Therefore, the number of ex-smokers may be overestimated in this group. East London has a large South Asian population for which the chewing of betel nut/paan is Fig. 3 Tumour sites by frequency culturally important. Three percent of this cohort reported chewing betel nut/ 40 pann, highlighting the importance of routinely asking about smokeless tobacco 35 use (Fig. 5). Alcohol consumption was also reported 30 to be less in this cohort of patients when compared with national data.25 It is unclear 25 why this is the case. Possibilities include patients cutting down on their alcohol 20 intake following cancer diagnosis or difficulties in accurately estimating the 15 number of units consumed per week. Data from the 2009 Adult Dental Health 10 Survey (ADHS) indicates that 8% of the adult population have periodontal probing 5 pocket depths in excess of 6 mm.26 In contrast, 51% of dentate patients in this 0 cohort had periodontal probing pocket Tx T1 T2 T3 T4 depths in excess of 6 mm. While it is Fig. 4 Tumour staging. Sixty-two patients presented with positive nodal disease and two had important to recognise the differences distant metastases. The TNM classification was not used in six cases between the nature of the adult dental health survey and this study, moderate teeth. The mean number of filled teeth CI 4.2‑6.1). In 15% (15/98) of dentate cases to advanced periodontal disease is a per dentate patient was 4.9 (95% CI no extractions were planned. Sixty percent significant issue for this group of patients. 4.‑5.8). 37% (36/98) of dentate patients (59/98) of dentate patients were planned This may be due to a combination of had crowned teeth and 12% (12/98) had for five or fewer extractions; the remaining smoking, poor oral hygiene practices and fixed bridgework. 40% (39/98) were planned for more than lack of regular attendance at a general The mean number of dental extractions five extractions. Sixty-seven percent dental practitioner. Table 4 shows how planned per dentate patient was five (95% (332/494) of teeth planned for extraction the findings from this study compare to

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Table 4 Summary of the relevant literature Number of Percentage of Percentage of Mean number patients patients with patients with of missing carious teeth periodontal disease teeth

Lockhart and Clarke 131 (75 dentate) 35 66 (flashlight and 21.9 (1994) USA23 tongue spatula)

Jham et al. (2008) 209 (135 dentate) 12 41 (criteria Not recorded Brazil21 not clear)

MacCarthy et al. 590 (554 dentate) 68 31 (probing pocket Not recorded (2007 and 2010) Ireland: 287 dentate depth >6 mm) abstracts only 28,29 Fig. 5 SCC left lateral border of tongue. This patient chewed betel nut/paan regularly Sennhenn-Kirchner 36 (25 dentate) 10 47.3 (probing pocket 10.3 et al. (2009) German 27 depth >6 mm)

Adult Dental Health 6,469 examined 29 8 (probing pocket 6.3 Survey (2009) UK 26 depth >6 mm)

Critchlow et al. 100 (98 dentate) 61 51 (probing pocket 11.1 (2013) UK depth >6 mm) other studies in this area along with the position to provide this and also to facilitate ADHS. The periodontal diagnostic criterion the often challenging oral rehabilitation used varies significantly between studies, that will be necessary following treatment making direct comparisons difficult (Fig. 6).30 The need to liaise closely with Fig. 6 Severe xerostomia and cheek fibrosis although a high incidence was reported in colleagues, often at very short notice, from in an edentulous patient who underwent 20,22,27,28 radiotherapy. Providing complete dentures is several studies. In addition, the lack oral maxillofacial surgery, ear, nose and often difficult due to lack of saliva to provide of data from other UK centres regarding the throat, oncology, pathology, radiology and a peripheral seal and reduced inter-arch space oral health status of pre-treatment HANC general medical and dental practice further for the dentures patients makes it impossible to determine re-enforces the vital role played by the how representative this cohort is of the restorative dental team. in ensuring that these patients have national picture. The mean number of teeth planned for a chance to maintain their remaining The proportion of patients presenting extraction per patient in this cohort was dentitions in a healthy state following with one or more carious teeth was 61% five. Patients can be quite taken aback by their oncology treatment. Hygienists, after edentulous patients were discounted. the recommendation to remove a significant therapists and oral health educators all Caries incidence varies widely in the other number of their natural teeth, particularly play an important part in the management studies that have been published in this if they would under normal circumstances of HANC patients within a consultant- area.20,22,26,27,29 This heterogeneity in the data afford a reasonable prognosis. More molar lead service. GDPs have an invaluable is likely to be due to a variety of factors, not teeth were planned for extraction than any role as they are often the first healthcare least the fact that these studies come from a other tooth type, reflecting the difficulties professionals to see new cases of oral wide variety of different countries each with in maintaining molar teeth following cancer and form a key part of the long- individual dietary factors, habits and oral radiotherapy treatment due to trismus and term care of HANC patients since well- hygiene practices. Additionally, some studies the fact that it is often the molar teeth that maintained and dentally stable patients diagnosed caries clinically,23,26 whereas lie in the high dose radiotherapy fields, with are often discharged to primary care. others additionally used radiographs.27 In the posterior being at greatest Without intervention from the whole this study, caries was diagnosed using both risk of developing osteoradionecrosis if dental team, the consequences of allowing clinical and radiographic findings. future extractions are required.17,18,19,20 irradiated patient’s dentitions to deteriorate Ninety percent (90/100) of these patients Excellent communication skills are can be extreme. As previously stated, were planned to undergo radiotherapy as required to manage this difficult phase of extractions are often contraindicated part of their oncology treatment. Given the the consultation. due to the risk of osteoradionecrosis and side effects of radiotherapy, particularly Dental implants can provide patients with patients can be condemned to a terminal xerostomia, it is of vital importance that a fixed rehabilitation; however, placing dentition with no prospect of relief. This has these patients are assessed and risk factors implants in irradiated bone risks failure of implications for the patient’s quality of life addressed both in terms of diet and oral osseointegration due to a decreased vascular as a cancer survivor, not to mention the cost hygiene practices. Caries can progress supply, peri-implant infections and possible to the health service of trying to maintain rapidly and often affects the root surfaces osteoradionecrosis.31 This can, in selected teeth of a hopeless prognosis that may have of teeth at and beneath the gingival margin, patients, make a strong case for implant been better extracted following a thorough which can quickly undermine the crown placement at the time of oncology surgery specialist dental assessment.32 It is hoped of the tooth (Fig. 1). A high standard of (primary placement) although it has been that the data in this paper can be used to interproximal cleaning with tight recall reported that many such implants are either highlight to healthcare commissioners the intervals and careful examination of unusable or have a high failure rate.32 importance of prevention and ongoing these areas is required in these cases. This It is the opinion of the authors that support from the whole restorative team highlights the need for input from specialists a team approach involving professions when designing care pathways for head and in restorative dentistry who are in the complimentary to dentistry is invaluable neck cancer patients.

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