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ADRXXX10.1177/0022034517736500Advances in Dental ResearchFeatherstone and Chaffee

Advances
Advances in Dental Research
2018, Vol. 29(1) 9­–14
The Evidence for Caries Management by © International & American Associations
for Dental Research 2018

Risk Assessment (CAMBRA®) Reprints and permissions:


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DOI: 10.1177/0022034517736500
https://doi.org/10.1177/0022034517736500
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J.D.B. Featherstone1 and B.W. Chaffee1

Abstract
A system for Caries Management by Risk Assessment (CAMBRA®) has been developed in California. The purpose of this article is to
summarize the science behind the methodology, the history of the development of CAMBRA, and the outcomes of clinical application.
The CAMBRA caries risk assessment (CRA) tool for ages 6 y through adult has been used at the University of California, San Francisco
(UCSF), for 14 y, and outcome studies involving thousands of patients have been conducted. Three outcomes assessments, each on
different patient cohorts, demonstrated a clear relationship between CAMBRA-CRA risk levels of low, moderate, high, and extreme
with cavitation or lesions into dentin (by radiograph) at follow-up. This validated risk prediction tool has been updated with time and
is now routinely used at UCSF and in other settings worldwide as part of normal clinical practice. The CAMBRA-CRA tool for 0- to
5-y-olds has demonstrated similar predictive validity and is in routine use. The addition of chemical therapy (antibacterial plus fluoride)
to the traditional restorative treatment plan, based on caries risk status, has been shown to reduce the caries increment by about 20%
to 38% in high-caries-risk adult patients. The chemical therapy used for high-risk patients is a combination of daily antibacterial therapy
(0.12% w/v chlorhexidine gluconate mouth rinse) and twice-daily high-concentration fluoride toothpaste (5,000 ppm F), both for home
use. These outcomes assessments provide the evidence to use these CRA tools with confidence. Caries can be managed by adding
chemical therapy, based on the assessed caries risk level, coupled with necessary restorative procedures. For high- and extreme-risk
patients, a combination of antibacterial and fluoride therapy is necessary. The fluoride therapy must be supplemented by antibacterial
therapy to reduce the bacterial challenge, modify the biofilm, and provide prevention rather than continued caries progression.

Keywords: dental caries, fluoride, chlorhexidine, disease indicators, caries risk assessment, dental plaque

Background the roles of fluoride and other agents in the management of the
disease. Based on decades of research on dental caries by many
For decades, there have been numerous attempts to provide investigators, we published a clinically oriented summary that
methodology to predict future dental caries or to assess caries described the balance between pathological factors and protec-
risk and to manage the disease (Krasse 1985; Disney et al. tive factors and how this might be dealt with in the clinical
1992). There are many publications related to these topics. It is setting (Featherstone 1999, 2000, 2003). In summary, dental
not the aim of this article to review these published works. The caries is demineralization of tooth mineral caused by acid gen-
purpose of the present article is simply to review the history of erated when cariogenic bacteria in the plaque (biofilm) on the
the development of a system for caries risk assessment and car- teeth metabolize fermentable carbohydrates. The demineral-
ies management that has been developed in California and ization can be inhibited by salivary components, antibacterial
used for 14 y in the teaching clinics of the School of Dentistry agents, and fluoride or reversed by remineralization that
at the University of California San Francisco (UCSF). The pro- requires calcium, phosphate, and fluoride. We proposed that
cedures and philosophy are known as “Caries Management by the progression or reversal of dental caries was driven by the
Risk Assessment” and abbreviated to CAMBRA. This article “caries balance,” namely, the balance between the pathological
will briefly summarize the science behind the methodology, factors, primarily (1) cariogenic bacteria, (2) fermentable car-
the history of the development of CAMBRA®, and the out- bohydrates, and (3) salivary dysfunction, and protective
comes of 14 y of clinical application in thousands of patients.

1
Department of Preventive and Restorative Dental Sciences, School of
Caries Mechanism and Its Application Dentistry, University of California San Francisco, San Francisco, CA,
to Caries Risk Assessment and Caries USA

Management Corresponding Author:


J.D.B. Featherstone, School of Dentistry, University of California at San
There are hundreds of articles that have contributed to our Francisco, 513 Parnassus Avenue, San Francisco, CA 94143-0430, USA.
understanding of the overall mechanism of dental caries and Email: [email protected]
10 Advances in Dental Research 29(1)

4. Preliminary studies that used detailed microbiological


assessments over short periods had established that the
chlorhexidine rinse should be used once a day for 1 wk
every month. This regimen was then used in the clini-
cal trial and was shown to markedly reduce the levels
of cariogenic bacteria in the patients (Fig. 1). Other
studies that reported no effect on dental caries by
chlorhexidine used very different regimens, such as
rinsing daily for 2 wk every 3 mo. The sustained
marked reduction in cariogenic bacterial levels in the
intervention group in this high-risk population coin-
cided with the reduction in caries increment.
5. A reanalysis of the trial findings (Cheng et al. 2015)
Figure 1. Mean (SE) log of mutans streptococci counts in saliva showed that caries reduction was mediated by com-
(colony-forming units per milliliter) at baseline and at follow-up visits bined action of changes in salivary bacterial levels and
every 6 mo in a randomized controlled clinical trial that examined fluoride concentration, as well as additional unmea-
caries management by risk assessment using chemical intervention
therapy (Featherstone et al. 2012). Between sampling visits 1 and 3, all sured factors.
restorative work was completed. Visits 3 to 7 represent the 2-y period 6. The results of the study clearly showed the need for
between “restorations complete” and the final examination. The upper antibacterial therapy as well as fluoride therapy in order
line is the control group (conventional dental and restorative treatment). to alter the balance in these high-risk individuals.
The lower line is the intervention group that received chlorhexidine
rinse and fluoride toothpaste.

Development of the CAMBRA


factors, primarily (1) sufficient saliva; (2) remineralization that Philosophy and Practice
requires calcium, phosphate, and fluoride; and (3) antibacterial The Caries Management By Risk Assessment (CAMBRA) phi-
agents. losophy was developed in California following 2 consensus con-
ferences (Featherstone et al. 2003, 2007). The full proceedings,
Randomized Controlled Clinical Trial including all manuscripts, of these 2 conferences are available
online at http://www.cdafoundation.org/education/resources-library.
on Caries Management
Representatives from most of the California dental schools and
A randomized controlled clinical trial was conducted during several others across the United States were present and contrib-
1999 to 2005 that examined the concept of the caries balance uted to these proceedings. The newly designed caries risk assess-
and whether altering that balance could reduce new dental car- ment form was piloted in several dental schools. UCSF and
ies (Featherstone et al. 2012). This controlled clinical trial was University of the Pacific implemented particularly comprehen-
conducted in the predoctoral teaching clinic at UCSF. The sive, large-scale pilots, starting in 2003. The forms and proce-
study included adults aged 18 to 65 y who had 1 to 7 cavities. dures were modified over time, and the modified versions were
Details are given elsewhere (Featherstone et al. 2012). The published in the California Dental Association Journal in 2007
control group was patients who continued with conventional (Featherstone et al. 2007; Jenson et al. 2007) in 2 special issues
treatment, and the test group had an intervention that consisted (available online as described above).
of a combination of fluoride mouth rinse, fluoride toothpaste, The following summarizes the steps in the caries manage-
and 0.12% chlorhexidine gluconate mouth rinse. ment process that were implemented and remain in place in
The trial produced several key results. these university clinics:

1. The trial demonstrated a statistically significant 24% 1. Take dental and medical history.
reduction in 2-y caries increment in initially high- 2. Conduct clinical examination.
caries-risk patients provided with the combined thera- 3. Detect caries lesions early enough to reverse or prevent
peutic intervention. progression.
2. The study also showed that placing restorations had no 4. Assess the caries risk as low, high, moderate, or
statistically significant effect on mean bacterial levels extreme using data from 1, 2, and 3 and a short
in the whole mouth, either initially or over a 2-y questionnaire.
follow-up period after the restorative work was com- 5. Produce a treatment plan that includes chemical ther-
plete. In the control group, approximately 70% of the apy appropriate to the caries risk level.
subjects returned within 2 y with new cavities. 6. Use chemical therapy that includes fluoride and/or
3. High numbers of decayed surfaces at baseline were antibacterial agents based on risk level.
strongly related to a combination of high levels of 7. Use minimally invasive restorative procedures to con-
mutans streptococci and lactobacilli. serve tooth structure and function.
Featherstone and Chaffee 11

Table. Cross-Tabulation of Disease Indicators, Caries Risk Factors, and Protective Factors with Cavitation or Caries into Dentin by Radiograph at
Baseline for 2 Studies (Doméjean-Orliaguet et al. 2006; Doméjean et al. 2011).

Odds Ratio

Doméjean et al. (2006), N = 2,351 Doméjean et al. (2011), N = 12,954

Disease indicators
Approximal lesions in enamel, by radiograph 13.6 8.2
Restorations in the past 3 y 1.6 1.5
White spot lesions 3.3 2.8
Risk factors/pathological factors
Visible heavy plaque on the teeth 2.8 2.6
Frequent snacking 1.9 1.8
Inadequate saliva 1.4 1.3
Deep pits and fissures 1.9 1.8
Recreational drug use 2.0 2.0
Protective factors
Fluoride toothpaste 0.67 0.81
Fluoride mouth rinse 0.74 0.80
Fluoridated community 0.81 (not statistically significant) 0.85
a
Odds ratios are for the relationship of each individual item. All items shown here were statistically significantly related. Odds ratios greater than 1.0
indicate a positive relationship and odds ratios less than 1.0 a negative relationship.

8. Recall and review at intervals appropriate to the caries studies showed that in our clinics, approximately 5% of our
risk status. patients are at extreme risk (Doméjean et al. 2011).
9. Reassess caries risk level at recall and modify the treat- An example of a patient at extreme risk would be the
ment plan as necessary. following:

Disease indicators: Visible cavity, numerous approximal


Caries Risk Assessment Procedure
lesions by radiograph, numerous restorations in the past 3 y.
Development and Validation Biological risk factors: Visible heavy plaque on the teeth,
Following the pilot introduction of caries risk assessment pro- frequent snacking, inadequate saliva flow by measure-
cedures into our clinics in early 2003, we made the decision to ment and signs of dry mouth, more than 1 medication
conduct caries risk assessments on all new UCSF patients that has hyposalivatory side effects.
starting in July 2003. As time progressed, the caries risk assess- Protective factors: Once-daily fluoride toothpaste use.
ment items included in the form were paired with the goal of
retaining only risk items that were the strongest predictors of In this case, the assessment would be 7 disease indicators and
caries outcomes and clinically relevant to disease progression pathological factors, including hyposalivation and only 1 pro-
and management (Doméjean-Orliaguet et al. 2006). Outcomes tective factor, leading to a definite extreme risk patient
studies specifically related to the predictive validity of the car- assessment.
ies risk assessment form were conducted and published in The 2011 outcomes assessment (Doméjean et al. 2011)
2006 and 2011 (Doméjean-Orliaguet et al. 2006; Doméjean clearly showed a relationship between assessed risk level and
et al. 2011). As a result of these outcomes studies, the items new cavities at follow-up, as illustrated in Figure 2 for 2,571
used in the caries risk assessment for patients aged 6 y through returning patients. Although 24% of patients classified at low
adult were grouped into (1) disease indicators (clinical obser- risk had cavities at follow-up, 76% did not. Refinement of the
vations), (2) biological risk factors (expanded to pathological tool, such as addition of accurate chairside microbiological
factors), and (3) protective factors. These are shown in the assessment in the future, may further improve the negative pre-
Table, together with the odds ratios relating each risk factor to dictive value of a designation of low caries risk. Close to 70% at
visible cavities or caries into dentin by radiograph for the 2006 high risk had new cavities at follow-up, and 88% at extreme risk
and the 2011 studies. The number of patient records used was had new cavities, demonstrating very good predictive validity.
2,351 in the 2006 study and 12,954 in the 2011 study. These numbers were similar to those observed in a smaller
The caries risk level was determined by the individual pro- patient cohort in the 2006 outcomes assessment (Doméjean et al.
viders based on an assessment of the balance between the dis- 2006) and were repeated recently in a new cohort of patients
ease indicators, the risk factors, and the protective factors, as (Chaffee et al. 2015a, 2015b). Undoubtedly, the tool can be fur-
per detailed instructions previously published (Featherstone ther refined and improved, but in its current form, it is an excel-
et al. 2007). Risk levels were assigned as low, moderate, high, lent predictor of low, high, and extreme caries risk.
or extreme. Extreme was defined as high risk plus hyposaliva- One recent modification to the caries risk assessment
tion, as assessed by visual inspection, medical history, and, if (CRA) form clarifies the item about recent restorations. For
in doubt, measurement of salivary flow rate. Our outcomes new patients (6 y through adult), we use “restorations in the
12 Advances in Dental Research 29(1)

Figure 3. Percentage of children, aged 0 to 5 y, with evident dental


decay at follow-up, stratified by caries risk status at baseline (Chaffee
et al. 2016): n = 3,810 at baseline and n = 1,315 at the follow-up
Figure 2. Percentage of adult patients with evident cavitation or caries examination.
into dentin (by radiograph) at follow-up, stratified by risk level assessed
at baseline: n = 12,954 at baseline and n = 2,571 at the follow-up
examination.
intensive preventive interventions are targeted at high-risk and
extreme-risk patients, delaying or preventing decay and restor-
past 3 years,” whereas for patients of record, we use “new caries- ative treatment needs.
related restorations in the past 12 months.” This allows the Over the first decade of CAMBRA implementation at
compliant patient to get “out of the penalty box” in that a patient UCSF, we had accumulated meaningful data on caries risk
under continuing care is not relegated to high-risk status for 3 y assessment and caries management based on risk assessment.
following restoration placement if the balance of risk and pro- The age 6 to adult multicomponent CAMBRA caries risk
tective factors is otherwise favorable. The fact that caries risk assessment tool, described above, was confirmed as strongly
level can be lowered with behavior change and therapeutic inter- associated with future treatment needs (Chaffee et al. 2015a),
vention may be motivating for patients. The feasibility of lower- and the first CAMBRA clinical trial had yielded promising
ing caries risk was illustrated in a practice-based research study results (Featherstone et al. 2012). Less information was avail-
reported by Rechmann et al., as reported in the present publica- able regarding the effectiveness of risk-based caries manage-
tion (Rechmann et al. 2017), where the authors demonstrated ment in practice. We recently conducted an outcomes
dramatic reductions in caries risk status within 18 to 24 mo. assessment (Chaffee et al. 2015b) based on patient records for
A second CAMBRA caries risk assessment tool (Ramos- 18,004 eligible patients from 2007 to 2012 in our predoctoral
Gomez et al. 2007) was developed in parallel with the age 6 y to teaching clinic. Caries risk assessment was conducted at base-
adult form for use with young children aged 0 to 5 y. This form line as a routine part of clinical care using the CRA methodol-
was introduced in the UCSF postgraduate pediatric teaching ogy summarized above (Featherstone et al. 2007). At their
clinics in 2009. An outcomes assessment was conducted (Chaffee initial visit, 11,900 adult patients were assessed as high risk by
et al. 2016) to assess the predictive validity of this additional student providers under the supervision of faculty dentists. Of
CRA tool. Very few extreme-risk children were identified, so these patients 2,724 were examined at follow-up after an aver-
this assessment was confined to low-, moderate-, and high-risk age of 18 mo. Full details of the methodology, patient charac-
patients. Very similar results to the adult studies described above teristics, statistical analyses, and so forth are given elsewhere
were found and are summarized in Figure 3. As was the case (Chaffee et al. 2015b).
with older patients, approximately 70% of patients assessed as The recommended chemical therapy for these high-caries-
high risk had new decay at follow-up visits. risk patients consisted of (1) fluoride varnish at the initial visit,
(2) twice-daily use of prescription fluoride toothpaste (5,000
ppm F), (3) chlorhexidine gluconate 0.12% mouthrinse (once
Caries Management Outcomes daily for 1 wk every month), and (4) xylitol gum or mints daily.
Under the CAMBRA philosophy, minimal intervention den- All patients were offered this therapy, but many opted not to
tistry is carried out as needed, and invasive restorative treat- receive or use the anticaries products.
ments may be delayed and performed at more advanced caries To assess the efficacy of the regimen, caries outcomes in 3
lesion stages if they develop over time (Vidnes-Kopperud et al. patient groups were compared, namely, (1) never received the
2011; Doméjean et al. 2015; Rechmann et al. 2016). A central anticaries products (n = 1,501), (2) took the products once and
tenant of CAMBRA is that patient risk assessment levels dic- never returned for refills (n = 900), (3) took the anticaries prod-
tate appropriate, patient-tailored noninvasive therapy: the most ucts and returned at least once for more (n = 323). Although
Featherstone and Chaffee 13

this was a retrospective study and not a controlled randomized been conducted (Doméjean-Orliaguet et al. 2006; Doméjean
clinical trial, these 3 groups provide evidence whether or not et al. 2011; Chaffee et al. 2015a). These 3 outcomes assess-
the regimen worked to reduce caries increment. ments, each on different cohorts of thousands of patients, dem-
The results of this outcomes assessment, reported as onstrated a clear relationship between CAMBRA-CRA risk
adjusted decayed, filled teeth (DFT) increment, after 18 mo of levels of low, moderate, high, and extreme with cavitation or
follow-up were as follows: lesions into dentin (by radiograph) at follow-up. This risk pre-
diction tool has been updated with time and is now routinely
1. Never took the products: DFT increment = 1.82.* used in these clinics as part of normal clinical practice. The
2. Took the products only once: DFT increment = 1.78.* CAMBRA-CRA tool for 0- to 5-y-olds (Ramos-Gomez et al.
3. Took the products twice or more: DFT increment = 2007) has demonstrated similar predictive validity (Chaffee
1.47.** et al. 2016) and is in routine use in the UCSF postgraduate
pediatric dentistry clinics. These CRA tools can be used with
Groups 1 and 2* were not statistically significantly different, confidence. Additions and modifications should not be made
but group 3 was statistically significantly** less than groups 1 unless there is evidence to support such changes.
and 2 by approximately 20%. This lesser DFT increment rep-
resents a major change in caries increment for a university
clinic that serves a largely high-caries, mostly poorly compli- Caries Reduction
ant, mostly low socioeconomic status population. Implementation, assessment, and utilization of the CRA tool
A subgroup of these patients was on a public assistance pro- took several years to fully embrace in the UCSF teaching clinics.
gram, and their products were available at no cost to them. Addition of chemical therapy to the traditional restorative treat-
Even then, many did not accept or use the anticaries products, ment plan, based on caries risk status, has been shown to reduce
or took them only once, which presumably indicated they did the caries increment by about 20% in high-caries-risk adult
not use them regularly. Comparing the same 3 groupings of patients. The biggest barriers are the need for patients to pay for
none, 1, and 2 or more times, the group that took the products the therapy, coupled with patient and provider acceptance. In a
twice or more had 38% lower DFT increment than the group subset of these patients, a group whose therapy was covered by
that never received the products. However, because of rela- insurance showed a 38% reduction in caries increment.
tively small numbers (n = 335, 238, and 167, respectively, for The chemical therapy used for high-risk patients (6 y
the 3 groups), this difference was not statistically significant. through adult) is a combination of antibacterial therapy (0.12%
The next question is whether these reductions in caries w/v chlorhexidine gluconate mouthrinse) and high-concentration
increment in an academic teaching clinic setting can be twice-daily fluoride toothpaste (5,000 ppm F), both for home
achieved, or improved upon, in a private practice setting. A use. The chlorhexidine is used as a daily rinse for 1 wk each
practice-based research network clinical trial was recently month and is continued until the risk level has been reduced for
completed, and the preliminary results are reported elsewhere 1 y. Looking ahead, chlorhexidine products can be substituted
in this issue (Rechmann et al. 2017). The study used 18 private by equivalent, or better, antibacterial agents as these become
practices, 3 community clinics, and 460 patients, each patient available and are clinically proven to be effective. As our
followed for up to 2 y. Marked reductions in caries risk status understanding of the microbiome, and the best ways to modify
were observed. the biofilm, evolves and improves, there will undoubtedly be
The evidence for the CAMBRA approach includes the 2 better therapies that can be substituted for chlorhexidine so that
randomized, controlled, clinical trials summarized above as altering the caries balance can be even more effectively done.
well as several outcomes studies involving thousands of Modifications to diet may also be shown to be powerful ways
patients. In the ideal world, further randomized clinical trials to positively alter the biofilm in the future. All of these
should be conducted that include other possible chemical ther- approaches together will provide more successful caries man-
apeutic regimens, perhaps with lower dropout rates and pediat- agement of high- and extreme-risk patients.
ric participants as well as adults. However, it is very challenging The results of the clinical trial described above (Featherstone
to get funding for such studies that are expensive and take sev- et al. 2012), together with the several years of outcomes assess-
eral years to conduct. ment results summarized here, clearly show that for high-car-
ies-risk individuals, even with access to community water
fluoridation and topical fluorides, new cavities will continue to
Summary and Conclusions
develop. The fluoride therapy must be supplemented by anti-
Caries Risk Assessment Tools bacterial therapy to reduce the bacterial challenge, modify the
biofilm, and swing the caries balance (Featherstone 2000) to
The CAMBRA (Caries Management by Risk Assessment) provide prevention rather than caries progression.
CRA procedure for the age group 6 y through adult
(Featherstone et al. 2007) was developed over a period of years
and followed the suggestions of a consensus conference. These Author Contributions
CRA procedures have been used in the predoctoral teaching J.D.B. Featherstone, contributed to conception, design, data analy-
clinics at UCSF for 14 y, and several outcome studies have sis, and interpretation and drafted and critically revised the
14 Advances in Dental Research 29(1)

manuscript; B.W. Chaffee, contributed to conception, design, data further developments in caries risk prediction. Community Dent Oral
analysis, and interpretation and critically revised the manuscript. Epidemiol. 20(2):64–75.
Doméjean S, Léger S, Rechmann P, White JM, Featherstone JD. 2015. How do
Both authors gave final approval and agree to be accountable for dental students determine patients’ caries risk level using the caries manage-
all aspects of the work. ment by risk assessment (CAMBRA) system? J Dent Educ. 79(3):278–285.
Doméjean S, White JM, Featherstone JD. 2011. Validation of the CDA
CAMBRA caries risk assessment—a six-year retrospective study. J Calif
Acknowledgments Dent Assoc. 39(10):709–715.
Doméjean-Orliaguet S, Gansky SA, Featherstone JD. 2006. Caries risk assess-
The authors would like to acknowledge the many people involved ment in an educational environment. J Dent Educ. 70(12):1346–1354.
Featherstone JD. 1999. Prevention and reversal of dental caries: role of low
in these studies and in developing the CAMBRA caries manage- level fluoride. Community Dent Oral Epidemiol. 27(1):31–40.
ment procedures. It is not possible to list them all. We wish to Featherstone JD. 2000. The science and practice of caries prevention. J Am
particularly acknowledge Jane Weintraub, Charles Hoover, Stuart Dent Assoc. 131(7):887–899.
Gansky, Francisco Ramos-Gomez, Ling Zhan, Peter Rechmann, Featherstone JD. 2003. The caries balance: contributing factors and early detec-
tion. J Calif Dent Assoc. 31(2):129–133.
Beate Rechmann, Charles Le, Marcia Rapozo-Hilo, Joel White, Featherstone JD, Adair SM, Anderson MH, Berkowitz RJ, Bird WF, Crall JJ,
Sophie Doméjean, Jing Cheng, Douglas Young, Larry Jenson, and Den Besten PK, Donly KJ, Glassman P, Milgrom P, et al. 2003. Caries
Stephan Eakle. We also thank the California Dental Association management by risk assessment: consensus statement, April 2002. J Calif
Dent Assoc. 31(3):257–269.
for support with the consensus conferences that contributed a great Featherstone JD, Doméjean-Orliaguet S, Jenson L, Wolff M, Young DA. 2007.
deal to this work. Support by various National Institutes of Health Caries risk assessment in practice for age 6 through adult. J Calif Dent
grants is acknowledged in the respective papers reviewed in this Assoc. 35(10):703–707, 710–703.
article but in particular R01-DE12455 and KL2TR000143. The Featherstone JD, White JM, Hoover CI, Rapozo-Hilo M, Weintraub JA, Wilson
RS, Zhan L, Gansky SA. 2012. A randomized clinical trial of anticaries
authors declare no potential conflicts of interest with respect to the therapies targeted according to risk assessment (caries management by risk
authorship and/or publication of this article. assessment). Caries Res. 46(2):118–129.
Jenson L, Budenz AW, Featherstone JD, Ramos-Gomez FJ, Spolsky VW,
Young DA. 2007. Clinical protocols for caries management by risk assess-
ment. J Calif Dent Assoc. 35(10):714–723.
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