The Natural History of Dental Caries Lesions A 4 Year
The Natural History of Dental Caries Lesions A 4 Year
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Abstract Introduction
Dental caries is a ubiquitous disease affecting all age
groups and segments of the population. It is known
that not all caries lesions progress to cavitation, but
little is known regarding the progression pattern of
D espite our knowledge of the basic concepts of dental caries, little is known
regarding the progression of dental caries lesions. It has long been known
that not all lesions progress to cavitation (Backer Dirks, 1966). The challenge
caries lesions. This study’s purpose was to evaluate has been to determine which white-spot lesions will progress to cavitation.
the natural history of dental caries using a standard- Unfortunately, despite all the efforts in caries detection in the past couple
ized, visually based system, the International Caries
Detection and Assessment System (ICDAS). The of decades, assessment of caries lesion activity at the time of examination
study population consisted of 565 consenting chil- is not usually part of the clinical examination (Zero et al., 2011). Thus, the
dren, who were enrolled and examined at baseline only option available to dentists is to monitor caries lesions longitudinally
and at regular intervals over 48 months with ICDAS before deciding on a restorative intervention. Once a tooth surface is restored,
and yearly bitewing radiographs. Of these, 338 chil- it enters a repetitive restorative cycle (Elderton, 1990), leading to a cascade
dren completed all examinations. Not all lesions of costly restorative treatments (Zero et al., 2011); therefore, minimizing the
cavitated at the same rate, differing by surface type
need for surgical intervention is the key to improving clinical outcomes.
and baseline ICDAS severity score and activity sta-
tus. With increasing severity, the percentage of The International Caries Detection and Assessment System (ICDAS; Pitts,
lesions progressing to cavitation increased: 19%, 2004) has been shown to be reproducible and accurate (Jablonski-Momeni et al.,
32%, 68%, and 66% for ICDAS scores 1, 2, 3, and 4, 2008) and provides the ability for dentists to visually detect and assess early
respectively. Lesions on occlusal surfaces were more lesions and provide longitudinal follow-up (Burt et al., 2006; Ekstrand et al.,
likely to cavitate, followed by buccal pits, lingual 2007; Finlayson et al., 2007; Ismail et al., 2007, 2008; Sohn et al., 2007; Cook
grooves, proximal surfaces, and buccal and lingual et al., 2008; Jablonski-Momeni et al., 2008; Varma et al., 2008).
surfaces. Cavitation was more likely on molars, fol-
lowed by pre-molars and anterior teeth. Predictors of
The objective of this study was to determine if characteristics of non-
cavitation included age, gender, surfaces and tooth cavitated lesions can be used as surrogates for cavitated lesions by longitudi-
types, and ICDAS severity/activity at baseline. In nal evaluation of tooth surfaces with the ICDAS criteria.
conclusion, characterization of lesion severity with
ICDAS can be a strong predictor of lesion progres-
sion to cavitation. Materials & Methods
As previously described (Ferreira Zandona et al., 2010; Fontana et al., 2011),
KEY WORDS: longitudinal study, dental caries, a convenience sample of 565 children (kindergarten to 9th grade) from public
ICDAS, activity, lesion progression, Hispanic. schools in Aguas Buenas, Puerto Rico, was recruited in January 2007, as
approved by the institutional review board committees from Indiana University
DOI: 10.1177/0022034512455030 (IU-IRB #0608-15) and the University of Puerto Rico (UPR-IRB#A1340107).
Received April 2, 2012; Last revision June 25, 2012; Parental consent was obtained along with assent from the child for children
Accepted June 25, 2012 older than 7 yrs. This sample size, based on preliminary data, allowed for a
A supplemental appendix to this article is published electroni- sufficient number of clinically significant lesions at the end of the four-year
cally only at [Link] study. For inclusion in the study, children had to be between 5 and 13 yrs of
© International & American Associations for Dental Research age, have no medical problem that contraindicated participation, and allow
1
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examination of the oral cavity, including radiographs and digital (18.6%) and in the older age group. The vast majority of children
photographs. Caries-free and caries-active children were were Hispanic (91%), and 51% were boys. Despite over 99% of
included. All children were required to have at least 1 permanent children having dental insurance, at 48 mos there was only a slight
molar with at least 1 unrestored surface, with no upper limit to increase in the number of fillings (4.9 ± 6.0 at baseline vs. 5.4 ± 6.7
the number of carious surfaces. at 48 mos). There were no differences between children who com-
All children received (at baseline, 8, 12, 20, 24, 28, 32, 36, pleted the 48-month examinations and those who did not in terms
40, 44, and 48 mos) an oral soft-tissue examination and an of ethnicity, race, gender, and combined DMFS/dmfs counts. On
examination by a calibrated examiner using the ICDAS criteria, average, DMFS/dmfs at threshold ICDAS 1 (initial lesions) was
which range from 0 to 6 (Ferreira Zandona et al., 2010). 16.3 ± 13.2, that at threshold ICDAS 3 (moderate lesion) was 8.5 ±
Additionally, each lesion was given an activity score (active/ 9.2, and that at threshold ICDAS 5 (extensive lesion cavitated into
inactive) at each examination period. The activity score was dentin) was 7.6 ± 8.7. Children who completed the 48-month
subjective, based on surface luster (opaque or translucent), tex- examinations were 1.3 yrs younger than those who did not (p <
ture (rough or smooth), and location (in a plaque stagnation area 0.001) and had significantly lower DMFS scores at all thresholds
or not). At each visit, teeth were brushed and flossed by study (ICDAS 1, 3, and 5, DMFS scores 8.7, 3.2, and 2.7, respectively,
personnel, air-dried, and assessed under light, without magnifi- p ≤ 0.0002) and higher dmfs scores (7.0, 5.4, and 5.0, respectively,
cation, according to the ICDAS criteria and following ICDAS p < 0.01). Two calibrated examiners conducted all the examina-
guidelines (Ismail et al., 2007) and the activity criteria. At base- tions, one from baseline to 24 mos and another from 28 to 48 mos.
line and yearly examinations (12, 24, 36, and 48 mos), full- Intra-examiner weighted kappa repeatability ranged from 0.77 to
mouth examinations were conducted and up to 4 bite-wing 0.81, and inter-examiner repeatability ranged from 0.54 to 0.62.
radiographs obtained. Radiographs were independently ana- Analyses of cavitation included only primary lesions on permanent
lyzed by a modified version of the ICDAS criteria (0 = sound teeth with no fillings at baseline and used both ICDAS and radio-
surface; 1 = outer ½ of enamel; 2 = inner ½ of enamel including graph scores.
DEJ; 3 = outer 1/3 of dentin; 4 = middle 1/3 of dentin; 5 = Progression of lesions to cavitation varied according to surface
middle 1/3 of dentin; 6 = into the pulp). At the interim examina- type and lesion severity and activity status at baseline (Tables 1
tions (8, 20, 28, 32, 40, and 44 mos), only posterior teeth (pre- and 2). Only 3% of surfaces that were sound at baseline pro-
molars and molars) were examined. The data were collected on gressed during the study period, and 1% progressed within the
tablet PCs equipped with custom-made software (Optiform, first 2 yrs. Of the teeth that were unerupted at baseline that
Indianapolis, IN, USA). At the yearly examinations, the primary erupted during the study period, 1% of the surfaces cavitated.
examiner repeated the examination on 10% of the children to Almost 19% of the surfaces scored as ICDAS 1 cavitated, 8%
assess intra-examiner repeatability, and a back-up examiner during the first 2 yrs. Over 32% of the surfaces scored as ICDAS
examined 10% of the children to evaluate inter-examiner agree- 2 lesions cavitated, 17% within the first 2 yrs. Almost 68% of the
ment. At every examination, children received a referral form lesions scored as ICDAS 3 cavitated, 46% within the first 2 yrs.
for dental care. This study complied with STROBE guidelines. All of the ICDAS 4 lesions were considered active and were most
Repeatability of the ICDAS examinations was assessed by likely to cavitate during the study. Significance tests indicated
weighted kappa statistics. DMFS/dmfs counts at baseline were cavitation differences for (in order) ICDAS 4 or 3, 2-active,
calculated with ICDAS 1, 3, and 5 as thresholds for the decay 2-inactive/1-active/1-inactive, sound, and unerupted (significant
portion of the counts. Comparisons between children who p values were p ≤ 0.001, 1-inactive vs. 1-active vs. 2-inactive,
attended the final study visit and those who did not were made p = 1.00, 2-inactive vs. 2-active, p = 0.07, and 3 vs. 4, p = 1.00).
with chi-square tests for differences in ethnicity, race, and sex, Lesions on occlusal surfaces were more likely to cavitate, ranging
and with two-sample t tests for differences in baseline DMFS/ from 7% (surfaces unerupted at baseline) to 78% (ICDAS 3 at
dmfs counts. Lesion cavitation was considered as lesions going baseline), followed by cavitation on buccal pits and lingual
from ICDAS score 0-4 to ICDAS 5-6 or filled or missing due to grooves, proximal surfaces, and buccal and lingual surfaces.
caries. Surfaces with orthodontic bands and surfaces on which Some important findings were related to how fast lesions
sealants were placed were evaluated up to banding/sealant progressed (Figs. 1a, 1b). A greater percentage of lesions scored
placement. The associations of age, sex, tooth type, surface, and as ICDAS 3 and 4 progressed within 1 yr of baseline examina-
baseline ICDAS severity/activity scores with time to cavitation tions. Cavitation of lesions initially scored as ICDAS 1 was
were analyzed by Cox proportional hazards survival analysis, spread throughout the 4 yrs, while cavitation of lesions initially
with a frailty term to account for multiple observations per scored ICDAS 2 was more concentrated in the first 2 yrs of the
child. The associations of age, sex, tooth type, surface, and base- study (Fig. 1). Lesions cavitated more quickly and more fre-
line ICDAS severity/activity scores with the presence of cavita- quently in girls and in younger children (Fig. 2). Lesions on
tion during follow-up or within the first 2 yrs of follow-up were occlusal surfaces cavitated sooner than lesions on other sur-
analyzed by generalized estimating equation (GEE) methods faces, followed by buccal pits, lingual grooves, and interproxi-
applied to logistic regression models. mal sites, with time to cavitation longest on smooth surfaces
(significant p values were p ≤ 0.001, and B vs. L, p = 0.31, D vs.
M vs. LG surfaces, p > 0.08). Molar teeth progressed the fastest,
Results
followed by premolars and then anteriors. In contrast to the
In total, 338 children completed the 48-month examination. frequency of cavitation, time to cavitation was significantly
Attrition was, on average, 10% per yr, with higher attrition in yr 1 shortest for ICDAS 3 and also shorter for 2-active than for
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Table 1. Percentage (%) of Lesions Progressing to Cavitation According to ICDAS and Activity Scores at Baseline
Baseline ICDAS Active Lesion Total Number of Surfaces Ever Progressed, N (%) Progressed within First 2 yrs, N (%)
ICDAS 4 (Fig. 2). Also of interest is that when cavitation was ICDAS is a set of visual criteria based on the examination of
limited to within 2 yrs, age and gender were no longer signifi- clean, dry surfaces. ICDAS 0 is for sound surfaces, ICDAS 1 and
cant predictors. 2 are scores for initial lesions (or early, white-spot lesions), and
ICDAS 3 and 4 are moderate or established lesions. These
lesions do not have frank cavitations exposing the dentin,
Discussion
although they might have microcavitations (ICDAS 3/4), and
Modern management of dental caries involves: detecting and histologically have reached the dentin (ICDAS 2/3/4). ICDAS
assessing caries lesions at an earlier stage; making a diagnosis scores 5 and 6 are extensive, frank cavitations, with dentin expo-
as to whether the disease is actually present; determining the sure and different levels of surface destruction. Traditionally,
caries risk status of the patient; establishing a prognosis; apply- dentists do not detect ICDAS score 1 (it requires focused surface-
ing intervention strategies focused on preventing, arresting, and drying) and place a “watch” on lesions with ICDAS scores of 2
possibly reversing the caries process; and delaying restorative and 3. Although a greater percentage of lesions scored as ICDAS
treatment until absolutely necessary (Zero et al., 2011). 4 progressed to cavitation, lesions scored as ICDAS 3 progressed
Identification of at-risk active sites is a core component for the at a faster rate. The clinical implications of these findings are that
principles for the modern management of dental caries, and it is in younger children, especially girls, on occlusal surfaces with
one of the biggest challenges faced by dentists. To date, the lesions scored as ICDAS 4 and 3, an intervention strategy (thera-
practice has been mostly to characterize lesions as a “watch” peutic sealant) should be instituted sooner rather than later. If
until it is deemed that progression warrants surgical interven- these lesions show on bite-wing radiographs as affecting the
tion. There is a tendency to opt for early restorative intervention middle third of the dentin, the dentin is heavily infected, and thus
of many lesions (Doméjean-Orliaguet et al., 2004; Tellez et al., minimal surgical intervention is indicated (Ricketts et al., 2002).
2011; Traebert et al., 2011), despite evidence that early lesions On surfaces with lesions considered active and scored as ICDAS
on occlusal surfaces can often be sealed (Beauchamp et al., 1 and 2, the treatment plan should not be a “watch” but rather a
2008), hampering further progression. This leads to an irrevers- therapeutic intervention, such as therapeutic sealant placement
ible restorative cycle (Tellez et al., 2011). Analysis of the data on occlusal surfaces, fluoride varnishes on smooth surfaces, and/
in this study indicates that careful monitoring of dental surfaces or infiltrants. For lesions that are progressing faster (within 2
by the ICDAS criteria can identify predictors of progression and yrs), which were mostly the lesions scored ICDAS 4, 3, and 2,
rate of progression. This can be a valuable tool for dentists to age and gender were not significant predictors. This indicates
use to determine treatment decisions and surface prognosis. To that, for these more established lesions, surface, tooth type,
our knowledge, the only other study that examined the natural ICDAS score, and activity status are more important predictors
history of dental caries longitudinally using detailed criteria was than age and gender. This knowledge should support the imple-
the study by Backer Dirks in 1966. Despite the subjectivity of mentation of these non-surgical approaches to caries manage-
the activity criteria used in the current study, it is notable that, ment, since the careful monitoring of the lesions allows for delay
for all ICDAS scores, a greater percentage of lesions that were or elimination of the need for restorative intervention. Additional
considered active at baseline progressed to cavitation. analyses of these data on outcomes of restorative interventions
We confirmed some findings that had been previously based on ICDAS scores at baseline can provide greater insight
reported: Molars are more susceptible to caries, followed by into intervention thresholds.
premolars and anterior teeth (Mejàre and Stenlund, 2000); and We acknowledge that these results are based on a high-risk,
occlusal surfaces are more susceptible to dental caries than other rather uniform rural population of Hispanic schoolchildren in
surfaces (Richardson and McIntyre, 1996). In this population, Puerto Rico, and the results many not be applicable to other
lesions in younger children progressed faster, likely due to erup- populations. However, there are certainly implications for clinical
tion stage (Carlos and Gittelsohn, 1965). Gender, as previously research on preventive/therapeutic interventions for high-risk
reported (Lukacs and Largaespada, 2006), was also found to be populations in whom detailed criteria such as ICDAS can be used
a predictor of the rate and odds of progression. to determine outcomes at shorter intervals than in traditional
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Table 2. Percentage (%) of Lesions Progressing to Cavitation According to Surface Type and ICDAS and Activity Scores at Baseline
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Acknowledgments
This study was supported by the National
Institute of Dental and Craniofacial
Research, National Institutes of Health,
Bethesda, MD 20892, USA (NIH-RO1
DEO17890). The authors thank the fol-
lowing individuals for their assistance:
Ms. Gwinn, Ms. Hernandez, Ms. Riviera,
Ms. Tran, Drs. Delgado, Eggertsson,
Hernandez, and Gomez and the support-
ing staff at OHRI and the University of
Puerto Rico. The authors declare no
potential conflicts of interest with respect
to the authorship and/or publication of
this article.
Figure 2. Hazard ratio and odds ratio of progression to cavitation by predictors.
References
Backer Dirks O (1966). Posteruptive changes in dentaldEnamel. J Dent Res Carlos JP, Gittelsohn AM (1965). Longitudinal studies of the natural history
45:503-510. of caries. II. A life-table study of caries incidence in the permanent
Beauchamp J, Caufield PW, Crall JJ, Donly K, Feigal R, Gooch B, et al. teeth. Arch Oral Biol 10:739-751.
(2008). Evidence-based clinical recommendations for the use of pit- Cook SL, Martinez-Mier EA, Dean JA, Weddell JA, Sanders BJ, Eggertsson
and-fissure sealants: a report of the American Dental Association H, et al. (2008). Dental caries experience and association to risk indica-
Council on Scientific Affairs. J Am Dent Assoc 139:257-268. tors of remote rural populations. Int J Paediatr Dent 18:275-283.
Burt BA, Kolker JL, Sandretto AM, Yuan Y, Sohn W, Ismail AI (2006). Doméjean-Orliaguet S, Tubert-Jeannin S, Riordan PJ, Espelid I, Tveit AB
Dietary patterns related to caries in a low-income adult population [see (2004). French dentists’ restorative treatment decisions. Oral Health
comment]. Caries Res 40:473-480. Prev Dent 2:125-131.
Downloaded from [Link] at INDIANA UNIV MED CTR on July 24, 2012 For personal use only. No other uses without permission.
Ekstrand KR, Martignon S, Ricketts DJ, Qvist V (2007). Detection and Mejàre I, Stenlund H (2000). Caries rates for the mesial surface of the first
activity assessment of primary coronal caries lesions: a methodologic permanent molar and the distal surface of the second primary molar
study. Oper Dent 32:225-235. from 6 to 12 years of age in Sweden. Caries Res 34:454-461.
Elderton RJ (1990). Clinical studies concerning re-restoration of teeth. Adv Pitts N (2004). “ICDAS”—an international system for caries detection and
Dent Res 4:4-9. assessment being developed to facilitate caries epidemiology, research
Ferreira Zandona A, Santiago E, Eckert G, Fontana M, Ando M, Zero DT and appropriate clinical management. Community Dent Health 21:193-
(2010). Use of ICDAS combined with quantitative light-induced fluo- 198.
rescence as a caries detection method. Caries Res 44:317-322. Richardson PS, McIntyre IG (1996). Susceptibility of tooth surfaces to cari-
Finlayson TL, Siefert K, Ismail AI, Sohn W (2007). Psychosocial factors ous attack in young adults. Community Dent Health 13:163-168.
and early childhood caries among low-income African-American chil- Ricketts DN, Ekstrand KR, Kidd EA, Larsen T (2002). Relating visual and
dren in Detroit. Community Dent Oral Epidemiol 35:439-448. radiographic ranked scoring systems for occlusal caries detection to
Fontana M, Santiago E, Eckert GJ, Ferreira-Zandona AG (2011). Risk fac- histological and microbiological evidence. Oper Dent 27:231-237.
tors of caries progression in a Hispanic school-aged population. J Dent Sohn W, Ismail A, Amaya A, Lepkowski J (2007). Determinants of dental
Res 90:1189-1196. care visits among low-income African-American children. J Am Dent
Ismail AI, Sohn W, Tellez M, Amaya A, Sen A, Hasson H, et al. (2007). The Assoc 138:309-318.
International Caries Detection and Assessment System (ICDAS): an Tellez M, Gray SL, Gray S, Lim S, Ismail AI (2011). Sealants and dental
integrated system for measuring dental caries. Community Dent Oral caries: dentists’ perspectives on evidence-based recommendations. J
Epidemiol 35:170-178. Am Dent Assoc 142:1033-1040.
Ismail AI, Sohn W, Tellez M, Willem JM, Betz J, Lepkowski J (2008). Risk Traebert J, Jinbo Y, de Lacerda JT (2011). Association between maternal
indicators for dental caries using the International Caries Detection and schooling and caries prevalence: a cross-sectional study in southern
Assessment System (ICDAS). Community Dent Oral Epidemiol 36:55-68. Brazil. Oral Health Prev Dent 9:47-52.
Jablonski-Momeni A, Stachniss V, Ricketts DN, Heinzel-Gutenbrunner M, Varma S, Banerjee A, Bartlett D (2008). An in vivo investigation of associa-
Pieper K (2008). Reproducibility and accuracy of the ICDAS-II for tions between saliva properties, caries prevalence and potential lesion
detection of occlusal caries in vitro. Caries Res 42:79-87. activity in an adult UK population. J Dent 36:294-299.
Lukacs JR, Largaespada LL (2006). Explaining sex differences in dental Zero DT, Zandona AF, Vail MM, Spolnik KJ (2011). Dental caries and
caries prevalence: saliva, hormones, and “life-history” etiologies. Am J pulpal disease. Dent Clin North Am 55:29-46.
Hum Biol 18:540-555.
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