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Dental caries is a chronic, infectious, and transmissible disease that affects children and adults throughout life.1 Primary cariogenic bacteria can easily thwart a dentist's best restorative efforts, interfere with the precision of the impression and restorations, and diminish the capacities of restorative materials or luting agents. The prevailing assumption in dentistry has generally been that placing a restoration "fixes" dental caries; however, this is not true. Unfortunately, placing a restoration does not remove the cariogenic bacteria load in the oral cavity and, thus, does not stop the disease process.2 The cycle of caries, restoration, and new caries does not change. The cycle of restorations, with each new restoration being less prophylactic and more iatrogenic than the previous one, continues indefinitely.3
First presented to the dental profession in 2003, the principles of CAries Management By Risk Assessment (CAMBRA®) (University of California San Francisco Office of Innovation, Technology & Alliances Division, ita.ucsf.edu) represented a major change in dealing with caries.4,5 CAMBRA provides clinicians with scientific, evidence-based solutions for the prevention and, consequently, treatment of the disease dental caries.6
Fortunately, modern-day dentistry has generally been accepting of the tendency to treat caries lesions early at the non-cavitated stage without drilling.7,8 The integration of CAMBRA into the office routine requires dentists to identify the caries risk of the individualby evaluating his or her disease indicators, risk factors, and preventive factors. A classification of low, moderate, high, or extreme caries risk is made. Changes in the patient's lifestyle and use of preventive chemical measures are then recommended.6,9-14
For moderate or high caries risk the goal is to reduce the patient's risk level and prevent further caries development. Lesions that are already cavitated may require invasive conventional restorative treatment. In contrast, non-cavitated caries lesions that show demineralization of enamel but still present an intact mineral surface layer can be treated with remineralization efforts. Remineralization can be achieved directly by providing different levels of fluoride treatment (eg, prescription fluoride toothpaste, fluoride rinse, fluoride varnishes) or indirectly through efforts to enhance saliva flow (eg, xylitol mints/gums) or reduce bacteria (eg, chlorhexidine applications, xylitol mints/gums).11,13,15,16
In summary, the CAMBRA philosophy consists of assessing the caries risk of the individual, suggesting treatment plans that include chemical therapy, use of fluoride and/or antibacterial therapy based on observations, performing minimally invasive restorative procedures to conserve tooth structure, and finally, recall and review.17
The Caries Balance Concept: Pathological Versus Protective Factors
Dental caries is a highly dynamic process in the oral cavity that is not at all static. Cycles of demineralization and remineralization occur daily in the presence of cariogenic bacteria, fermentable carbohydrates, and saliva. The balance between pathological factors and protective factors determines this process. Caries can either be arrested or progress if any of the components change.
Understanding the balance of caries risk, giving consideration to both pathological and protective factors (Figure 1), enables the clinician to implement patient-specific treatment protocols that can arrest and even reverse the disease process. However, this knowledge has still not been implemented in most clinical practices.18As the legal standard of care evolves, this knowledge should be of primary concern and, thus, interest to practitioners.
Caries pathological factors include acid-producing, cariogenic bacteria; frequent consumption of fermentable carbohydrates; and subnormal saliva flow. The two major groups of cariogenic bacteria in the oral cavity are mutans streptococci and the lactobacillus species. They produce organic acids during the metabolism of fermentable carbohydrates.1,5 On the opposite side of the caries balance are the protective factors, which consist of normal saliva flow and protective saliva components, such as fluoride, calcium, and phosphate for remineralization, along with antibacterials, such as chlorhexidine, xylitol, and potentially others, which are intended to reduce the bacteria load (Figure 1).
If the pathological factors outweigh the protective factors, a net loss of calcium and phosphate minerals will occur, first from the enamel and/or exposed root dentin. This demineralization process causes a caries lesion, which is initially non-cavitated.19 However, this process can be reversed if the balance changes and protective factors outweigh the pathological factors. The mineral can rebuild and the process of remineralization occurs. If demineralization is not stopped, non-cavitated lesions will progress into cavitated lesions.
Caries Risk Assessment
Caries risk is the likelihood of a person having new or extended tooth decay in the future. When performing an individual caries risk assessment (CRA), three categories are considered: disease indicators, risk factors, and protective factors. Figure 2 shows a typical CRA form.
Disease Indicators
The disease indicators are best described as clinical or radiographic observations consistent with the presence of the disease caries. They indicate the presence of disease, which is a strong indication of disease continuing into the future; however, disease indicators are not risk factors themselves. Disease indicators include visible cavities or lesions into the dentin, as detected radiographically; approximal lesions in the enamel, as detected radiographically; and active smooth-surface white-spot lesions detected visually. For new patients, restorations placed in the preceding 3 years due to caries also are disease indicators. For patients of record, during a periodic oral examination and being under CAMBRA treatment, restorations placed in the previous year due to caries are disease indicators.
Risk Factors
Risk factors enhance the likelihood of increased acid production or prolong the amount of time the acids are in the mouth. These factors include high counts of mutans streptococci and lactobacilli, visible heavy plaque on teeth, deep pits and fissures that allow retention of fermentable carbohydrates, and exposed root surfaces. Frequent snacking (ie, more than three times daily between meals of all sorts of fermentable carbohydrates, including frequent sipping of carbohydrate-containing sodas and drinks) and recreational drug use (not including an occasional social drink) are also risk factors. Additional risk factors are inadequate saliva flow (by observation or measurement), saliva-reducing influences from medications (eg, blood pressure-reducing drugs, anti-anxiety drugs, etc), radiation that incapacitates the saliva glands, and systemic diseases. Finally, orthodontic appliances and other appliances that may allow heavy microbial plaque retention are also risk factors.
Protective Factors
Any influence that enhances protection against demineralization, supports remineralization, or reduces the amount of cariogenic bacteria in the oral cavity is considered a protective factor. For example, living, working, or attending school in a community that has fluoridated water is a protective factor. Other protective factors are: the use of fluoridated toothpaste once or twice a day; daily usage of an over-the-counter fluoridated mouth rinse; use of prescribed 5,000-ppm fluoride toothpaste; in-office topical application of fluoride varnish and/or other in-office fluoride topicals in the past 6 months; use of a chlorhexidine rinse 1 week per month in the past 6 months or any adequate antibacterial; use of xylitol four times a day over the past 6 months; and application of a calcium and phosphate paste during the past 6 months. An adequate saliva flow also serves as a protective factor.
How Protective Factors Work
It must be emphasized that no product listed in this section is successful in prevention of caries in patients with moderate, high, or extreme caries risk when used as a sole treatment. Only a combination of multiple products, as listed in Table 1, has been successful in reducing disease indicators, caries increments, and caries risk.2,20
Function of Fluoride
Fluoride works primarily and most effectively via topical (surface) mechanisms whether it is delivered in drinking water, foods, or beverages, or through oral healthcare products such as toothpastes and mouth rinses. Fluoride inhibits demineralization, enhances remineralization, and, in high concentrations, inhibits plaque bacteria.
It has been shown that an initial high dose of fluoride as a burst effect increases enamel resistance against decalcification21,22 and, thus, prevents lesion formation. Lower fluoride concentrations appear more effective in remineralizing enamel and preventing lesion progression.23 A fluoride varnish application forms a reservoir of fluoride ions as calcium fluoride-like deposits on tooth surfaces and in the plaque layer. The fluoride ions are then slowly released over time and continuously enhance remineralization as they react with the carbonated hydroxyapatite crystals in carious lesions.21
During the demineralization process the enamel/dentin crystals (carbonated apatite) are attacked by organic acid, resulting in partially dissolved crystals.24 When enamel crystals remineralize in the presence of calcium, phosphate, and fluoride a low-soluble, fluorapatite-like veneer over the original defective crystal forms. The fluorapatite-coated crystal is much less soluble in acid and more caries resistant.6
CPP-ACP and Fluoride
The casein phosphopeptide-amorphous calcium phosphate (CPP-ACP) complex uses casein phosphopeptides to stabilize calcium and phosphate (and fluoride) ions at high concentrations as ACP or with fluoride as amorphous calcium fluoride phosphate (ACFP). CPP is needed as the carrier molecule for the ACP/ACFP, which concentrates the calcium-phosphate phase, increases its solubility, and prevents mineral precipitation.25-27 The CPP allows high concentrations of calcium, phosphate, and fluoride ions to be stabilized in a metastable solution in a form that is bioavailable for the promotion of remineralization.28
When CPP-ACP is applied to tooth surfaces, the incorporation of fluoride into plaque is actually increased, which again promotes enamel remineralization.26,29,30 The combination of CPP-ACP and fluoride can have a synergistic, enhanced effect on enamel remineralization due to the formation of stabilized ACFP.29,31 In the presence of fluoride, CPP-ACP has been shown to promote the formation of fluorapatite deep within the lesion.27,29
Chlorhexidine
Chlorhexidine gluconate is a broad-spectrum antibacterial agent that works by opening up the cell membranes of the bacteria. It is available in the United States as 0.12% chlorhexidine gluconate antibacterial mouth rinse. For patients with high or extreme caries risk, a chlorhexidine rinse for 1 minute daily for 1 week each month to reduce mutans streptococci and lactobacilli levels in the plaque biofilm is recommended. This regimen was developed and shown to be effective in reducing caries incidence in a randomized clinical trial.2 Subsequently, its use as part of a CAMBRA regimen was shown to be effective in reducing cares incidence in an outcomes study in thousands of patients (as discussed below).32
Xylitol
Xylitol is a natural sugar that is non-fermentable by oral bacteria. It reduces the levels of mutans streptococci in plaque and saliva by disrupting their energy production processes, leading to cell death.33 In addition, xylitol diminishes the bacteria acid production potential and decreases the adhesion of these microorganisms to tooth surfaces, consequently reducing the amount of plaque on teeth.34,35 Xylitol has been shown to disrupt the vertical transmission of pathogens from caregiver to child.36 The reported effective xylitol dose is 6 to 10 grams per day.35,37
Results of the First CAMBRA Clinical Trial
The CAMBRA randomized, prospective, controlled 2-year clinical trial at the University of California at San Francisco (UCSF) was performed between 1999 and 2004.2 The trial showed that a therapy combination of an antibacterial agent (chlorhexidine) and fluoride (over-the-counter fluoride toothpaste and rinse) significantly reduced the bacterial load over the test period.
This study also showed that placing restorations in the control group at baseline did not significantly reduce the mutans streptococci bacterial challenge. These restorations did not significantly change the caries risk status of subjects in the control group. However, for the intervention group the applied treatment resulted in a significantly lower percentage of subjects at high caries risk. The change in mutans streptococci bacterial challenge was also significantly different between the two groups. The antibacterial and fluoride therapy had successfully altered the balance between pathological and protective caries risk factors.
The clinical trial reported a reduced caries increment over 2 years in patients with a high caries risk, who at baseline examination had one to seven cavitated teeth. The intervention group had a statistically significantly 24% lower increase in DMFS (decayed, missing, filled surfaces) than the control group over time. In summary, the CAMBRA study demonstrated that for patients with high caries risk, applying bactericidal and fluoride agents reduced the caries risk, and less cavitated lesions occurred over the ensuing 2 years.2
CAMBRA Validation Studies
The CAMBRA system and philosophy was developed following two consensus conferences in 2003 and 2007.5,38 The CAMBRA caries risk assessment (CRA) system was subsequently validated in two outcomes studies.12,39 The first outcomes study, presented by Doméjean and coworkers, followed 2,571 patients at the UCSF School of Dentistry clinics who had been categorized at baseline as low, moderate, high, or extreme caries risk.39 At a follow-up examination on average 16 ± 13 months after risk level assignment, new cavitated lesions, radiographic lesion penetration into dentin, or approximal enamel lesions on x-rays were found related to the assigned risk level in 24%, 39%, 69%, and 88%, respectively (Figure 3). Importantly, those patients at high or extreme caries risk due to multiple reasons had not received the appropriate preventive measures.39 Consequently, they developed new caries lesions.
Recently, in another outcomes study Chaffee and coworkers again showed that the baseline caries risk is strongly associated with future caries.40 From electronic patient records at the UCSF student dental clinic, the group drew clinical data from 18,004 patients with assigned caries risk. Of these patients, 4,468 visited on average 18 ± 9 months later for an oral examination. Patients with low caries risk developed on average 0.94 decayed or filled teeth (DFT), while patients with moderate risk showed a 0.32 higher DFT than the low-risk group, those with high risk showed a 0.85 increased DFT, and extreme risk patients demonstrated a 2.32 increased DFT over the low caries risk patients. Between each risk category the difference in mean DFT increment was statistically significant. It was concluded that, after adjustment for other patients characteristics, the predictive validity of the multicomponent caries risk assessment approach on which CAMBRA is based was again confirmed.40
In 2015 Chaffee and colleagues validated the efficiency of anticaries agents that included high-concentration fluoride toothpaste, chlorhexidine rinse, and xylitol products. The electronic records of 2,724 patients with follow-up at the UCSF School of Dentistry revealed a significant difference in new DFT for those patients who had received anticaries agents at least twice compared to those patients who had never or only once received these products. On average, over 18 months, patients with two-time deliveries of anticaries agents developed 20% less DFT (Figure 4).32
In 2018 Rechmann and colleagues demonstrated that CAMBRA can be successfully implemented into dental practice. They recruited 30 dentists to perform a 2-year CAMBRA trial. The randomized, controlled, parallel-arm, double-blinded clinical trial with individual-level caries risk assignment of 460 patients to standard of care (control) versus active CAMBRA treatment (intervention) demonstrated that caries risk level as well as disease indicators, reflecting the existence of caries, were significantly reduced in the CAMBRA intervention group compared to the controls at all recall time points.20
Caries Risk Assessment: Assigning Caries Levels
A UCSF study in 2014 tested the reliability and reproducibility of caries risk level assignments by different clinical teachers who completed CRA forms for simulated patients.41 When presented with the same set of CRA forms 6 months later the intra-examiner reliability was very high. In contrast, when compared to a gold standard, the average reliability to accurately assign the correct caries risk level was only moderate. In total, 20% of the presented high caries risk cases were underestimated at caries levels too low, even in the presence of obvious caries disease indicators.
From a treatment standpoint, overestimating caries risk may be inefficient but protective for the patient, while underestimating caries risk could have serious consequences. In this context it is important to note that Doméjean et al found in their study that 23.6% of the 2,571 patients assessed at baseline as low caries risk had developed new cavities 16 months later.39
Goolsby and coworkers in 2016 tested 55 faculty members on CRAs from simulated patients before and after an instructional lecture was given. They showed a statistically significant increase in the proportion of faculty members responding correctly for five of the seven cases on the pre- and post-calibration tests.42
In 2017 Young et al performed a similar study involving students and clinical faculty. They tested the correct caries risk assignment levels between a gold standard (a group of three CAMBRA experts) and the study participants using 22 CRAs from simulated patients. They found significant improvements after face-to-face calibration sessions but also after PowerPoint self studies.43 Less than a quarter of the students and only half of the faculty assigned "high caries risk" correctly. Furthermore, the extreme caries risk level was the lowest accurate assignment for students and faculty and still remained low after calibration. These disappointing outcomes occurred despite "A Simplified Guide to Use the CRA Form" guidelines being provided to students and faculty.43
In the present article, the CRA form (Figure 2) delineates the disease indicators as color coded in red, the risk factors in yellow, and the protective factors in green. This color coding was designed to help dentists correctly assign the risk balance, illustrating the weight of the risk and protective factors, and leading to a caries balance in favor of caries progression or no caries. If any of the disease indicators (red zone) are marked, the patient is immediately categorized as having high caries risk. A high caries risk patient with inadequate saliva flow moves the scale further down to the left (caries progression) and denotes extreme risk. Three or more risk factors (yellow zone) in the absence of a disease indicator might also indicate high risk.
One or two risk factors (in the absence of any disease indicator) may classify the patient as moderate caries risk. If no disease indicators and also no risk factors are marked the patient is at low caries risk.
If patients use their prescribed products and show improved oral healthcare outcomes at their follow-up visits, each protective factor (green zone) can override one risk factor. In that case the balance scale slides to the right "no caries" side.
An electronic system (MyCAMBRA® App) that assigns the caries risk level has recently been developed at UCSF to aid the private practitioner.41 The digital system inputs clinical findings and questions that require an answer on the California Dental Association's CRA form similar to the form in Figure 2. Offering treatment protocol recommendations, this digital option for CRA provides visual and descriptive representations of the caries risk and protective factors within the app. Once the caries balance is determined, the patient's caries risk level and the appropriate corrective course of treatments are emailed to the patient as well as to the dentist for documentation purposes using HIPAA-compliant encryption. CAMBRA results that show improvement are sent to the patient, which may encourage continued patient participation in a personalized CAMBRA program.
CAMBRA Treatment Recommendations
Table 1 summarizes treatment recommendations differentiated by the risk levels.11 In addition to the listed fluoride and antibacterial products, patients should receive adult prophylaxis treatment, oral hygiene instructions, and bitewing x-rays at appropriate time intervals. Visits for re-evaluation for extreme caries risk patients should occur every 3 to 6 months, and for high caries risk patients every 4 to 6 months.
Restorative Treatment Thresholds and Minimally Invasive Dentistry
The CAMBRA philosophy emphasizes the preservation of as much natural tooth structure as possible while simultaneously encouraging remineralization of early lesions to inhibit further progression. Non-cavitated lesions have lost mineral, but no physical loss of enamel prisms and no localized enamel breakdown has occurred yet.19 The philosophy of minimal intervention commands that operative intervention should be performed only when cavitation is present.44 Some enamel lesions never penetrate into dentin, and up to 60% of lesions in the outer one-half of dentin are not cavitated and, thus, can be arrested and remineralized.45-48 Some remineralized approximal lesions are no longer apparent in follow-up bitewing x-rays, and others become smaller or are arrested with no further progression. For non-cavitated lesions, monitoring the success of topical fluoride applications and pit-and-fissure sealants is considered best practice and should become standard treatment.15,49,50
A recent report addressed approximal and occlusal caries lesion management, detection, and restorative thresholds of California dentists. A plurality would restore approximal lesions at the dentin-enamel junction, while 39% would wait until the lesion reached the outer third of dentin. Newly graduated dentists and pediatric dentists were found to be more likely to delay restorations.8 This may portend a change in long-held restorative decision-making philosophy.
Implementation of CAMBRA Into Clinical Practice
A team approach is essential for a successful caries management program, and the role of the dental hygienist can be critical in the overall supervision of the program. Following initial CRA by the dentist, the hygienist can monitor and educate the patient during the prophylaxis appointment.18,51,52
Although research overwhelmingly supports the importance of caries risk assessments and supportive/corrective treatment, general acceptance in private practice has not occurred. Impediments include insufficient education, dentists' calibration of CRAs for accurate results, altering the "drill and fill" mindset, and the absence of or reduced dental insurance reimbursements for CAMBRA-based services.
About the Authors
Peter Rechmann, PhD, DMD
Professor and Director, Clinical Sciences Research Group, Department of Preventive and Restorative Dental Sciences, School of Dentistry, University of California at San Francisco, San Francisco, California
Richard Kinsel, DDS
Health Science Associate Clinical Professor, Department of Preventive and Restorative Dental Sciences, School of Dentistry, University of California at San Francisco, San Francisco, California
John D.B. Featherstone, PhD, MSc
Professor Emeritus and Dean Emeritus, School of Dentistry, University of California at San Francisco, San Francisco, California
Queries to the author regarding this course may be submitted to authorqueries@aegiscomm.com.
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