Introduction

Head and neck cancer comprises 3% of all new cancer cases, making it the eighth most common cancer in the UK, and has increased in prevalence by 31% over the last three decades.1 Treatment modality depends on both the tumour size and location, with up to 85% of patients receiving radiotherapy, with or without a combination of surgery and chemotherapy.1 Head and neck cancers do respond to radiotherapy; however, there are several acute and chronic side effects that can occur in the oral cavity, which should be planned for and discussed with head and neck cancer (HANC) patients before treatment. The acute symptoms can include but are not limited to: oral mucositis, changes to salivary production/consistency, radiation caries and fibrosis. These symptoms can be very debilitating for a HANC patient.

Osteoradionecrosis of the jaw (ORNJ) is a chronic complication which can develop after radiotherapy to the head and neck, being both difficult to manage and sometimes painful to patients who have developed osteoradionecrosis (ORN). Various risk factors have been commonly documented for developing ORN including local factors such as: radiation dose, tumour location, tumour stage and dental extractions, and systemic factors including smoking and alcohol consumption.

Owing to the seriousness and chronic nature of ORN, it is important that dental extractions are timed effectively to minimise the local risks while other risk factors are brought under control and taken into consideration. The current Royal College of Surgeons (RCS) guidelines state that a minimum period of ten days should be given to allow for adequate healing pre-radiotherapy, although some other references state an ideal period would be 21 days.2,3

The aims of this audit were as follows:

  1. 1.

    Determine the number of HANC patients being assessed pre-radiotherapy

  2. 2.

    Determine the average waiting time between assessment and extraction

  3. 3.

    Determine how many patients are meeting the set standard for timing between dental extractions and the start of radiotherapy

  4. 4.

    Determine the prevalence of ORN post-radiotherapy and associated risk factors for ORNJ at Portsmouth Hospital University NHS Trust.

Standards

  1. 1.

    One hundred percent of patients should be given ten days' healing between dental extractions and radiotherapy

  2. 2.

    One hundred percent of patients should be dentally assessed before commencing radiotherapy.

Materials and methods

This audit retrospectively reviewed the records of 154 patients who received radiotherapy treatment to the head and neck between July 2016 and August 2017 at Queen Alexandra Hospital in Portsmouth. The audit was registered with the local audit department within the Hospital Trust. All patients who underwent radiotherapy to the head and neck region during this period were included in the audit, with data being collected from patients' notes, radiographic reports, clinicians' letters and general anaesthetic records within the hospital.

Results

Portsmouth Hospital's NHS Trust protocol (Fig. 1) shows the general pathway of HANC patients from their initial referral onto the two-week fast-track pathway through to their start of treatment. The guidelines give a target of 52 days from the initial referral to the first treatment, which includes treatment modalities of surgery, radiotherapy or chemotherapy. Following the trust pathway, once a multidisciplinary team (MDT) meeting has decided on the optimum treatment modalities for HANC patients, there is a 19-day window to complete dental extractions before the first cancer treatment. Following the RCS guidelines of ten days' minimum healing time before radiotherapy, this gives nine days to complete any dental extractions.

Fig. 1
figure 1

Portsmouth Hospital NHS Trust protocol

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The demographics of the 154 patients identified 29 (18.8%) female and 125 (81.2%) male patients, which was slightly higher than the national distribution of the HANC male-to-female ratio.2 The age range (Fig. 2) showed an expected peak in incidence from 60-69 years, although the youngest patient identified was just 32 years old. The mortality rate for this group of patients was 24.7% at 2-3 years, depending on the start date of their radiotherapy.

Fig. 2
figure 2

Age of patients receiving radiotherapy to the head and neck region

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Of the 154 patients, the most common tumour, nodes and metastases (TNM) staging was T4 N2 M0, closely followed by T2 N2 M0 and T2 N0 M0, as shown in Figure 3. A total of three patients had distant metastases (M1).

Fig. 3
figure 3

Tumour, nodes and metastases staging of head and neck cancer patients

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A total of 42 patients (33.8%) were under the management of the oral and maxillofacial surgery unit, with the location of primary tumours in the oral cavity seen in Figure 4. The floor of mouth had the highest incidence rate as a primary tumour site in the oral cavity (33.3%), followed closely by the base of tongue (26.2%) and salivary glands (26.2%), although it should be noted that these accounted for just 23.4% of the total primary tumours.

Fig. 4
figure 4

Graph showing distribution of primary tumours in the oral cavity

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Figure 5 shows the treatment modalities that were used for this group of HANC patients. The most common treatment was a combination of chemotherapy and radiotherapy (70 patients), followed by 49 patients that had radiotherapy alone. All patients had intensity-modulated radiotherapy.

Fig. 5
figure 5

Graph showing treatment modalities used for head and neck cancer patients

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One hundred percent of patients underwent masking before radiotherapy and treatment was not commenced until the mask fit satisfactorily. In terms of radiotherapy dose, 64.2% of patients had a dosage of 65 Gy 30 F with curative intent and 18.8% had 55 Gy 20 F either post-surgery or palliative, usually for five days a week for a period of six weeks.

Of 154 patients undergoing head and neck radiotherapy, 81.2% were seen for dental assessments before their initial treatment. This falls below the current British Association of Head & Neck Oncologists guidelines4 stating 100% of patients should be dentally assessed before radiotherapy. Despite this, it should be noted this audit has seen improvement from just 51.1% of patients previously being assessed the last time this audit was undertaken in 2017.

Of the 125 patients undergoing dental assessments, 102 (81.6%) required dental extractions. There is no set standard for the interval between the initial assessment and dental extractions, but this ideally should be as quick as possible to avoid delay in start of radiotherapy treatment. A target of seven days was set (including for patients undergoing extractions under general anaesthesia), with 78.4% of patients falling within this target (Fig. 6), and a mean time of 5.7 days was recorded.

Fig. 6
figure 6

Assessment to extraction waiting time (X = extraction)

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A total of 101 patients (99%) adhered to the RCS guidelines, with a minimum of ten days' healing time between their dental extractions and first radiotherapy treatment. Of these patients, 79 (77.5%) had over 21 days between their dental extractions and first radiotherapy, falling within the timeframe outlined by Vissink et al.3 A mean time of 32 days was recorded, although this was somewhat offset by several extractions in palliative cases which may have been some months after the initial assessment, with problems requiring extractions arising post-radiotherapy.

Out of the sample, 12 patients had full clearance of their remaining dentition. Most of the patients had their remaining molar teeth removed, with most being periodontally involved or heavily restored. Ten patients, excluding the full clearances, had teeth removed in the anterior region. Fifty-three patients had no extractions.

The rate of ORN was found to be just 1.3%, with two patients being diagnosed with the condition. Patient A had malignant neoplasm of the larynx, TNM staging T4a N2b M0 and the dose of radiotherapy given was 65 Gy in 30 fractions. This patient required multiple extractions and was given 23 days between these extractions and their first radiotherapy. This patient used to be a heavy smoker and was diagnosed with an impacted molar tooth associated with a cystic lesion on the left angle of the mandible. Figures 7, 8 and 9 show the progression of ORNJ in Patient A where guidelines for pre-radiotherapy extractions were followed, over 21 days before initial radiotherapy. Interestingly this patient adhered to the RCS guidelines as well as the ideal timeframe outlined by Vissink et al.,3 yet still developed ORN. This was managed via a surgical bone debridement and plating of the mandible.

Fig. 7
figure 7

Initial management for Patient A (August 2017)

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Fig. 8
figure 8

ORN left mandible for Patient A (March 2018)

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Fig. 9
figure 9

Mandibular resection and plating for Patient A (March 2019)

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Patient B had a right neck recurrence of a right soft palate squamous cell carcinoma. This patient refused dental extractions before radiotherapy and underwent neck dissection followed by radiotherapy 63 Gy in 30 fractions. Dental extractions were only completed when the patient developed pain during treatment and the patient smoked 10-12 cigarettes per day. The patient developed ORN in the right mandible, which was treated with a rim resection and nasolabial flap. Figures 10 and 11 show the initial presentation and subsequent ORN post-extractions in Patient B.

Fig. 10
figure 10

Initial presentation for Patient B (July 2013)

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Fig. 11
figure 11

ORN right mandible for Patient B (December 2016)

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Discussion

With 81.2% of patients being dentally assessed before their first radiotherapy, the audit fell below the set standard. The majority of those who were not dentally assessed were either edentulous or had been placed under a palliative treatment plan and therefore it was incorrectly assumed these individuals did not require an assessment. Despite this, no justification of why these patients were not scheduled for a dental assessment was ever recorded and at least one incidence of ORNJ could have potentially been avoided if the hospital's protocol had been followed accordingly. Even under a palliative treatment plan, dental assessments should still be carried out as it is still necessary that dental disease should not impact on the patient's remaining quality of life. A large systematic review on the prevalence and risk factors associated with ORNJ revealed that excessive alcohol consumption and poor dental health places patients receiving radiotherapy at an increased risk of developing ORNJ, with patients undergoing extractions post-radiotherapy demonstrating an increased prevalence of the disease.5 Despite this, teeth are often monitored rather than extracted in palliative patients, but this does not mean assessments should be abandoned.

Unfortunately, ORNJ cannot always be avoided, even when guidelines and protocols are strictly adhered to, which is why teeth must be carefully selected for extraction during dental assessments. Figures 7, 8 and 9 show the progression of ORNJ in Patient A. Despite following the protocols, this patient went on to develop ORNJ in their mandible which eventually resulted in a mandibular resection. As seen in Figure 8, this patient's dentition is now also beginning to deteriorate with evidence of extensive carious lesions. This is likely secondary to xerostomia and could potentially result in further extractions, leaving this patient prone to further ORNJ. This particular case shows why dental assessments and appropriate extractions are so important before radiotherapy. Further teeth could possibly have been extracted before this individual's radiotherapy but this could have caused further ORNJ, showing why a careful balance needs to be struck.

There was no set standard for waiting times between dental assessments and extractions, only that it should be minimised to reduce delays in treatment. The departmental average time was found to be 5.7 days (Fig. 6), which certainly fell within the hospital protocol for keeping treatment delays to a minimum waiting time. Specific time slots were kept free during the week for the dental assessment and treatment of HANC patients, and if these were full, other patients scheduled for routine treatment would be re-arranged to accommodate this group. Overall, 78.4% of patients were treated in ≤1 week and only 6.9% of patients took ≥2 weeks to treat. Again, these results were affected by the inclusion of patients undergoing palliative treatment. These individuals frequently underwent dental extractions several months after their initial dental assessment, as teeth with questionable prognoses were more likely to be monitored in these individuals.

Only one patient failed to meet the minimum standard set by the RCS guidelines between their extractions and first course of radiotherapy. This patient was given a five-day interval between these two dates owing to the seriousness of their diagnosis, which allowed for no delay in treatment. Fortunately, this patient did not develop ORN despite undergoing a total of eight extractions and their dentition was recently restored to replace the teeth lost before their radiotherapy. The first radiotherapy date is planned at MDT meetings in order to ensure patients always follow the RCS guidelines wherever possible.

Owing to the small pool of patients who developed ORN from this cohort, it is not possible to accurately discuss any relevant risk factors. Recognised risk factors for the development of ORN include: higher radiation dose, alcohol use and poor periodontal status.6 It is worth noting that these individuals did not receive an abnormally large dose of radiation and had minimised their alcohol consumption before treatment. It is important that every patient, whether their treatment is palliative or curative, should be dentally assessed before radiation of the head and neck as this can prevent unfortunate incidences of ORNJ due to extractions during or after radiotherapy. The case of Patient B highlights the importance of informing the patient of the inherent risks of ORNJ if dental extractions are not carried out before radiotherapy.

Conclusion

In summary, 1.3% of 154 HANC patients treated with radiotherapy between July 2016 and August 2017 developed ORNJ after a follow-up of at least 20 months, with no apparent correlation with healing time between extractions and first radiotherapy. The prevalence of ORN is lower than figures reported in other studies6 but the sample size is not large enough to render these results reliable; further audits and wider national studies are required. RCS guidelines are being used and followed well but we still need further improvement to ensure all patients are appropriately dentally assessed before receiving radiotherapy to the head and neck region. The action plan includes updating the MDT pro forma to include earliest radiotherapy start date and to highlight 'dental assessment', justification to be given if a dental assessment is not required, and improved channels of communication to ensure the head and neck team are aware of dental assessment slots. A further audit cycle would assess the outcome of these changes and investigate any further improvements required.