Indices for the assessment of radiation-related caries

Abstract

Radiation therapy, either used alone or in combination with surgery and or chemotherapy, is the most commonly utilized modality for treating head and neck cancers. Patients undergoing radiation therapy usually experience significant early and late-onset toxicities/adverse effects. Radiation-related caries (RRC) is a common complication that detrimentally affects patients' quality of life (QoL). A clearer understanding and more uniform approach to scoring systems help provide a more accurate diagnosis, form treatment protocols, plan, and evaluate outcomes of preventive initiatives and create scientific databases. Many indices have been used to assess and quantify the dental caries experience after radiotherapy. Considering the need for uniform standards for measuring radiation caries, indices specific to radiation caries have been proposed in the literature to capture postradiation damage to the dentition accurately. This narrative review aims to consolidate the evolution of different indices used for scoring RRC to improve the understanding of radiation caries assessment.

INTRODUCTION

Cancers of the head and neck region are the sixth most common form of cancer worldwide and rank among the top three types in India.[1,2] This condition often requires a multidisciplinary approach. Depending on the presentation stage, radiotherapy (RT) alone or in combination with surgery or chemotherapy is used as a significant treatment modality.[3] RT involves the use of ionizing radiation to target cancerous cells. However, the normal tissues in the zone of radiation therapy are inadvertently affected. The plausibility and severity of radiation-related adverse effects are multifactorial and depend on the site, extent of the tumor, total radiation dose, and precision of the radiation machine. Complication rates are higher in patients with concurrent chemotherapy and preexisting systemic diseases such as diabetes, cardiovascular conditions, and neurological problems.

The adverse effects of RT can be categorized as early and late onset.[4] Early or acute side effects occur during and immediately (approximately 2–3 weeks) after completing a course of radiation therapy. These include mucositis, loss of taste or altered taste sensation, candidiasis, dermatitis of irradiated skin, odynophagia, laryngeal edema accompanied by hoarseness of voice. Late effects can manifest at any time thereafter, from weeks to years later, and have profound, long-lasting consequences on the QoL. These include xerostomia, trismus, carious breakdown of dentition, and osteoradionecrosis.

Radiation-related caries (RRC) is well-documented and one of the most common complications, affecting approximately 25% of patients after HNRT.[5] RRC has a rapid onset, quick progression and is an essentially destructive form of dental decay. This can lead to persistent infection, pain, and an increased risk of the development of osteoradionecrosis. RRC generally occurs between 6 and 12 months after the conclusion of HNRT.

RRC manifests a characteristic clinical course that starts as discrete enamel cracks and fractures and progresses to brown or blackish discoloration of the enamel. Due to its presentation as a cervical, annular lesions typically involving more than one surface RRC are also referred to as the “caries circularis.”[6] If not treated promptly, RRC can rapidly progress to the underlying dentin and cause complete amputation of the tooth crown. RRC is distinguished from ordinary smooth surface dental caries by its characteristic involvement of areas of teeth that are often resistant to decay (lingual surfaces of incisors and premolars, incisal edges, and cusp tips), rapid progression, and absence of acute pain in even advanced lesions.

The etiopathogenesis of RRC is considered multifactorial. It is primarily attributed to indirect effects of radiation therapy. Salivary glands undergo dose-dependent degenerative changes after radiation therapy. Radiation-induced salivary gland damage primarily affects the serous cells, with minor effects on the mucous cells and ductal epithelium. Changes in salivary production begin within the 1^st week of radiation therapy for doses around 20 Gray (Gy). Salivary secretions decrease up to 50% at 4–5 fractions The decreased salivary flow rate leads to thick and ropey saliva with low pH and reduced buffering capacity.[7,8] Oral saliva pH 5.3 increases the risk for RRCs, and patients with low pH for a long time recover slowly.[9] With impaired oral clearance and compromised oral hygiene due to mucositis, trismus, and oral discomfort, acidogenic and cariogenic bacteria such as Streptococcus mutans, Lactobacillus, and Candida species tend to grow.[10,11,12] All these things manifest as “clustering of oral symptoms,” leading to the development of a conducive environment for dental caries.[13] Besides indirect damage, radiation caries is also a product of direct radiation-induced effects on dental hard tissues.[14] The damage to the mineralized structure of the tooth is minimal at doses <30 Gy (salivary gland threshold) but the damage increases two to three folds for radiation doses between 30 and 60 Gy.[15,16,17] These are reflected in the reduction of microhardness and modulus of elasticity of enamel near DEJ, destabilization of DEJ, decreased crystallinity and loss of mineral and protein content in both enamel and dentin.[14,15]

Studies on the impact of radiation therapy on dental development reported that at therapeutic radiation doses in children in addition to salivary gland dysfunction, the formation of “osteodentin” is observed due to the interference with the mitotic activity of the rapidly dividing preodontoblasts, resulting in impaired nucleation of enamel following mineralization.[18,19] The odontogenic cells in performative and differentiative phases are more sensitive to radiation than cells in the secretory or maturation stage. Exposure to radiation before calcification leads to the destruction of tooth bud, while exposure at later stages results in defective enamel and dentin formation with shortened roots.[20,21] The age-related changes in dentine and the exposure of root surface due to gingival recession increases the risk of RRC in the elderly. However, irrespective of age, the alteration in composition and mechanical changes in the tooth structures makes the restoration of RRC a daunting task for dentists. A study on the clinical performance of different restorative materials reported that conventional glass ionomer cement (GIC) appears to show better sealing ability, while composite resin presented better long-term integrity and marginal adaptation. Based on the findings, it is suggested to use convention GIC as a base under composite resin.[22]

The detrimental effect of RRC on the QoL of head and neck cancer patients has been well accepted and documented.[23] Epidemiological investigations require accurate measurement and quantification of the disease to study its burden. A clearer understanding and more uniform approach to scoring systems help provide a more accurate diagnosis, treatment protocols, forming a scientific database, planning, and evaluating outcomes of preventive initiatives taken. Many indices have been used to assess and quantify the dental caries experience after RT. Considering the need for uniform standards for measuring radiation, caries-specific indices have been proposed in the literature to accurately capture post-radiation damage to the dentition. This narrative review consolidates the evolution of different indices used for scoring RRCs.

NONSPECIFIC DENTAL CARIES INDICES USED TO MEASURE RADIATION-RELATED CARIES

The Decayed Missing Filled Teeth (DMFT) and Decayed, Missing, filled surface (DMFS) indices were developed by Henry Klein, Palmer, and Knutson in 1938 to determine the prevalence of coronal caries.[24] Both DMFT and DMFS require evaluation of 28 permanent teeth, excluding retained primary teeth and third molars. If the occlusal surface of a tooth is exposed or may be exposed by the manual reflection of the gingiva, it is considered to have erupted. The DMFS requires the evaluation of four surfaces (buccal, palatal, mesial, and distal) in anterior teeth and five surfaces (buccal, lingual, mesial, distal, and occlusal) in posterior teeth. No tooth or surface is counted more than once, and missing is only reported for teeth or surfaces lost attributable to caries. Congenitally missing or unerupted teeth and teeth lost due to traumatic dental injury are excluded. Restorations due to reasons other than caries (e.g., hypoplastic teeth, abutments, and preventive fissure sealants) are also excluded from evaluation.

Initially used to describe the dental status and treatment need in preelementary school children, DMFT and DMFS soon became a tool to describe caries experience in epidemiologic studies due to its simplicity, ease of performance, and versatility. However, these indices lacked discrete differentiation between diseased state or treated condition and arrested carious lesion thus can overestimate caries experience in teeth with preventive restorations. In addition, they lose validity in population groups such as the elderly, people with motor difficulties, and others who may lose teeth for reasons other than caries. When used for the evaluation of RRC, the use of DMFT and DMFS underestimates the degree of RRC due to failure to capture incisal edge caries.

The international caries detection and assessment system (ICDAS) was developed by a team of researchers, epidemiologists, and restorative dentists with their first meeting held in 2002, integrating several criteria and combining evidence received from various studies into one standard system of caries detection and assessment.[25] ICDAS estimates changes on the surface and potential histological depth of carious lesions by relying on surface characteristics. It detects six stages of the carious process ranging from early visible changes in enamel to extensive distinct cavitation.[25] The index includes two components: The 'D' stands for detection of dental caries by stage of the carious process, the topography of lesion (pit and fissures or smooth surfaces), anatomy (crown or root status), and restoration or sealant. Component 'A' stands for assessment by analyzing whether the carious lesion is cavitated or non cavitated and active or arrested caries. The major shortcoming was that in the initial ICDAS criteria, detection and assessment of only coronal carious lesion activity and radicular caries were not included. In 2005, the IACDS coordination committee modified the initial assessment criteria to include caries associated with sealants and root caries along with coronal caries, and the ICDAS II system [Table 1] was developed.[26,27,28] The principal advantage of ICDAS is the ability to evaluate noncavitated lesions. Braga et al. evaluated the feasibility of using ICDAS II criteria in an epidemiological survey to assess its correlation with the WHO criteria.[29] WHO criteria classify tooth surfaces as sound, decayed, filled, or indicated for extraction.[30] They observed that ICDAS II took twice as long the application time when compared with WHO criteria. It may lead to an overestimation of the seriousness of dental caries experience.[17] and requires a longer application time when compared with WHO criteria.[15,18,19] When used for assessment of RRC, it underestimates the degree of RRC due to a failure to capture incisal edge and cusp tip decay, enamel delamination, and crown amputation.

Table 1.

International caries detection and assessment system II

Code	Criteria
Caries on pits and fissures, smooth surface, free smooth surface
0	Sound tooth surface
1	First visual change in enamel
2	Distinct visual change in enamel when viewed wet
3	Initial breakdown in enamel due to caries with no visible dentin
4	Underlying dark shadow from dentin with or without localized enamel breakdown
5	Distinct cavity with visible dentin, visual evidence of demineralization and dentin exposed
6	Extensive distinct cavity with visible dentine involving at least half of the tooth surface and possibly reaching pulp
CARS
0	Sound tooth surface with restoration and sealant
1	First visual change in enamel
2	Distinct visual change in enamel/dentin adjacent to restoration/sealant margin
3	Carious defect of<0.5 mm, with sign of code 2
4	Marginal caries in enamel/dentin/cementum adjacent to restoration/sealant with underlying dark shadow from dentin
5	Distinct cavity adjacent to restoration/sealant. There is interfacial gap>0.5 mm either appreciable visually or by insertion of>0.5 mm ball-ended probe
6	Extensive distinct cavity adjacent to restoration/sealant with visible dentin in interfacial space with sign of code 5, gap>0.5 mm
Carious lesions on the root surfaces
E	Root surface cannot be visualized as result of gingival recession or gentle air drying
0	Root surface does not exhibit unusual discoloration at CEJ or wholly on root surface, root surface with natural anatomic contour or loss of root contour not associated with caries processes such as abfractions or erosions
1	There is a clearly demarcated area on the root surface or at the cementoenamel junction that is discolored (light/dark brown, black) but there is no cavitation (loss of anatomical contour<0.5 mm) present
2	A clearly demarcated area on the root surface or at the CEJ that is discolored (light/dark brown, black) and there is cavitation (loss of anatomical contour=0.5 mm) present

CARS: Caries associated with restoration and sealants, CEJ: Cementoenamel junction

SPECIFIC INDICES FOR THE MEASUREMENT OF THE RADIATION-RELATED CARIES

Post-radiation dental index

Walker et al. in 2008, developed the post-radiation dental index (PRDI) as a measure to assess the pattern and severity of lost tooth structure after radiation therapy.[31] It was the first caries index designed specifically to assess RRC. Each tooth crown is divided into three surfaces (buccal, lingual, and occlusal for posterior teeth) or two surfaces (buccal and lingual for anterior teeth). A six-point (0–5) semiquantitative ordinal scale, based on the changes in the tooth surface and the extent of surface covered with restoration, is used to score individual tooth surfaces [Table 2]. The sum of each tooth surface score (SS) or restoration score (RS) is divided by the number of evaluated surfaces (3 for posterior teeth and 2 for anterior teeth) to calculate the Mean Restorative Score and Mean SS.

Table 2.

Postradiation dental index surface score and restorative score

Score	Description
SS
0	No change in tooth surface. appearance is smooth, shiny, and intact
1	White line or brown stain. intact enamel, surface is smooth and shiny
2	Single focal area of enamel/tooth structure loss (≤2 mm); surface may have white line or brown stain
3	Single focal area of enamel/tooth structure loss (>2 mm); or>1 focal area of enamel/tooth. Total tooth structure lost <1/3 of surface area
4	Enamel/tooth structure lost >1/3 but<2/3 of surface area
5	Enamel/tooth structure lost >2/3 of surface area
RS
0	No restoration
1	≤2 mm×≤2 mm restoration
2	>2 mm×>2 mm restoration but restored surface<1/3 surface area
3	Restored surface≥1/3 but <2/3 surface area
4	Restored surface≥2/3 but <100% surface area
5	Restored surface=100% surface area

SS: Surface score, RS: Restorative score

Advantage

PRDI is the first index designed specifically to assess RRC.

Shortcomings

• The index does not include incisal surfaces of anterior teeth as reasoned by the authors to avoid artificially inflating the tooth destruction scores due to wear (attrition and abrasion), thus limiting its validity and practical applicability

• The qualitative elements of RRC, such as brownish/back discoloration, enamel cracks and fissures, enamel delamination, and crown alteration, were not taken into account.

DMFS160

Watson et al. in 2020, proposed this novel index for RRC assessment.[32] It allows for the rapid identification of the degree of RRC along with treatment strategies. This index takes into consideration 32 sets of teeth, and each tooth is divided into five surfaces. Thus, a healthy mouth consists of a total of 160 (32 × 5) tooth surfaces. The missing surface (MS) value is calculated by counting all the missing teeth surfaces (number of missing teeth X 5) irrespective of the etiology (extraction or congenitally missing). All the DMFSs (except the one with attrition and abrasion) comprise the total DMFS value. The DMF value is calculated by subtracting the MS value from the DMFS value. The visual changes in the tooth surface are used to determine the stage of severity, and the percentage of teeth involved in the most severe stage is used for grading. A treatment algorithm is proposed for managed of teeth based on the stage and grade of RRC [Table 3].

Table 3.

Staging and grading in DMFS160 index and treatment recommendations

Staging and grading based on clinical presentation and extent of RRC
Stage	Visual changes		Grade		The extent of tooth involvement
1	Early decalcification (chalky white or brown decalcification lines)		1		<25% of teeth affected by the worst stage
2	Cervical decay and/or incisal/cusp tip decay		2		Between 25%-50% of teeth affected by the worst stage
3	Enamel delamination		3		Between 50%-75% of teeth affected by the worst stage
4	Crown amputation		4		>75% of teeth affected by the worst stage
Treatment recommendations based on the stage and grade of RRC
Stage	Stage 1	Stage 2	Stage 3	Stage 3	Stage 4	Stage 4
Grade	Any grade	Any grade	Grade 1-3	Grade 4	Grade 1-2	Grade 3-4
Treatment recommendations	Oral hygiene instructions Daily application of topical fluoride Oral hygiene assessment every 3-4 months initially, after every 6 months on achieving stability	As per Stage 1 Avoid restoring teeth that are cleansable and are able to remineralize through use of topical fluoride SDF should be considered for circumferential lesions or root lesions Restorations to be done where appropriate, favoring amalgam, composite resin or resin-modified GIC in patients compliant with topical fluoride regimens, convention GIC to be given in noncomplaint patients	As per Stage 1 and 2 and In motivated patients and congenital conditions involving the enamel/dentin to teeth with enamel delamination, consider application of restorative techniques from pediatric dentistry Extraction of nonrestorable teeth in fields >50 Gy Within high-dose fields (>50 Gy), prophylactic endodontics and/or extractions	Consider use of SDF to maintain teeth as long as possible for mastication Extraction of nonrestorable teeth in fields below 50 Gy Within high-dose fields (>50 Gy), consider prophylactic endodontics and/or extractions as teeth become symptomatic	Maintain teeth with Stage 1, 2 or 3 lesions as per above Extraction of nonrestorable teeth in fields below 50 Gy Within high-dose fields (>50 Gy), consider prophylactic endodontics and/or extractions as teeth become symptomatic	Extraction of nonrestorable teeth in fields below 50 Gy Within high-dose fields (>50 Gy), consider prophylactic endodontics and/or extractions as teeth become symptomatic. Consider removable prosthodontic rehabilitation in motivated patients

GIC: Glass ionomer cements, SDF: Silver diamine fluoride, RRC: Radiation-related caries

Advantages

• This allows for accurate capturing of the unique pattern of RRC in the anterior region

• It eliminates the need for hypothesizing reasons for missing teeth

• Provide directions regarding the treatment of affected teeth.

Shortcomings

• The index does not provide information about caries progression

• The grading system does not include diffused punctate defects, which is one of the characteristic clinical patterns of RRC.

DISCUSSION

Dental indices can be used to measure the severity of dental disease and the effectiveness of therapy, allowing for cross-sectional comparisons. Dental caries, “a biofilm-mediated, diet modulated, multifactorial, noncommunicable, dynamic disease resulting in net mineral loss of dental hard tissues,” is a widely prevalent dental disease. RRC are characterized by caries lesions on otherwise resistant tooth surfaces driven by biomechanical changes in tooth structure and xerostomia associated with radiation therapy. RRC differs from conventional caries in clinical appearance, development, and progression. However, the majority of epidemiologic studies have used indices proposed for conventional caries to study the incidence and prevalence of RRCs.

DMFT/S index is the most widely used caries assessment tool for radiation caries.[33,34] A systematic review reported the mean prevalence of radiation caries as 28.1%, where the mean DMFT of irradiated patients was 9.19.[5] A study by Konjhodzic-Prcic et al., in 2010, used the DMFT index and found that the incidence of radiation caries went from 19.4 to 23.9 following 6 months of radiation therapy, which is a significant increase.[35] de Pauli Paglioni et al. attempted to establish a link between radiation caries and QoL in their multicenter study. The patients were divided into two groups: The study group (patients with at least 1 year of RT completion who developed RRC) and the control group (patients with at least 1 year of RT completion who did not develop RRC). Physical and social-emotional functioning domains were used to calculate the QoL score. DMFT index was used for caries assessment. They discovered that the mean DMFT and QoL scores were 30.5 and 878.1 in the study group and 20.7 and 927.2 in the control group, respectively. They reported that RRC has a detrimental effect on the QoL of individuals with HNC.[23]

ICDAS index has been used widely in the assessment of conventional dental caries. However, limited literature is available for its use in the assessment of radiation caries. In 2008, Walker et al. developed the PRDI as a pioneering index designed specifically for RRC. The authors assessed the reliability of the clinical index and found that it demonstrated excellent intra- and inter-examiner reliability.[31] Palmier. et al. compared the validity of ICDAS and PRDI for the assessment of radiation caries.[36] They observed that both ICDAS and PRDI underestimate the clinical expressivity of post-radiation caries by not including the whole qualitative clinical spectrum of radiation caries, such as enamel cracks, delamination, crown amputation, atypical lesions topography (incisal/cuspal caries), and surface color alterations. They emphasized the dire need for a more comprehensive caries assessment tool that caters to the atypical pattern of radiation caries. Palmier et al., through a study on the reliability of PRDI and ICDAS, concluded that ICDAS is used for conventional caries rather than RRC, and PRDI is an ex vivo index that does not fully represent the true clinical picture of radiation caries.[37]

In an attempt to overcome the aforementioned issues, Watson et al. in 2020, developed a novel caries assessment index called DMFS160.[32] First, it focuses on the inclusion of incisal edge caries which allows for a more accurate representation of the damaged dentition. Second, the index acknowledges the qualitative component of radiation caries by addressing surface discoloration, enamel delamination, and crown amputation in its staging. Third, the index separates MSs and decayed/filled surfaces, which provides further context for the DMFS160 value. Furthermore, the staging and grading allow quick identification of the overalls state of the patient's dentition and making a required treatment decision. The DMFS 160 index looks promising and practical for use as it includes all the dental surfaces and proposes a treatment for the management of RRC. However, clinical studies are required to generate the data on its applicability and reliability in the clinical scenario.

Prevention and reduction of radiation-related side effects are essential for reducing the incidence of RRC and improving the oral health and QoL of patients. Intensity-modulated radiation therapy (IMRT) is a recently developed RT approach that provides for reduced induced damage and improved survival as compared to the conventional two-field radiation therapy. Duarte et al. compared the dental health of patients with head and neck cancer receiving IMRT versus conventional radiation therapy. They observed that patients treated with IMRT exhibited significantly lesser xerostomia, mucositis, and fewer required post treatment dental extraction as compared to those treated with conventional RT.[38] However, no studies were found in the literature using specific indices for measurement radiation caries after IMRT.

Restricted mouth opening is a challenge for dental evaluation of patients with head and neck cancers. This often leads to underreporting of the disease. With the advancements in technology, equipment like intraoral cameras can be used to overcome the constraint of limited visualization of dentition in these patients. Furthermore, the integration of artificial intelligence for caries detection and treatment planning can aid in objectively assessing and grading the RRC process, which presents a spectrum of clinical presentations.

CONCLUSION

PRDI and DMFS160 are the only two indices that have been specifically designed to assess RRC. Although DMFS160 being more comprehensive, appears to be promising and specific to radiation caries assessment compared to other indices used previously, more studies need to be done to assess its clinical viability.

Financial support and sponsorship

This study was supported by the Indian Council of Medical Research. (No. 5/4/2-8/OralHealth/2021-NCD-II).

Conflicts of interest

There are no conflicts of interest.