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J Periodont Res 2014; 49: 143–163 © 2013 John Wiley & Sons A/S.

All rights reserved Published by John Wiley & Sons Ltd

JOURNAL OF PERIODONTAL RESEARCH


doi:10.1111/jre.12094
Review Article
I. Bignozzi1, A. Crea1, D. Capri1,
Root caries: a periodontal C. Littarru2, C. Lajolo2,
D. N. Tatakis3

perspective
1
EduPERIO Periodontal Education and
Research International Organization, Rome,
Italy, 2Catholic University of Sacred Heart,
Rome, Italy and 3The Ohio State University,
Columbus, OH, USA
Bignozzi I, Crea A, Capri D, Littarru C, Lajolo C, Tatakis DN. Root caries: a
periodontal perspective. J Periodont Res 2014; 49: 143–163. © 2013 John Wiley
& Sons A/S. Published by John Wiley & Sons Ltd

Background and objective: A prevailing dental problem in the periodontal


patient is root caries. Specifically, periodontal involvement often results in root
surfaces becoming exposed and at risk for this condition. Periodontal therapy
often leads to increased gingival recession as well, and the associated increased
root caries risk may compromise the long-term success and survival of periodon-
tally treated teeth.This narrative review will address the topic of root caries in
the periodontal patient, focusing on unmet research needs.
Material and Methods: The Medline database was searched to identify items
dealing with root caries, in terms of clinical features, diagnosis, pathogenic
mechanisms and histopathology, as well as epidemiology, focusing then on the
relationship between root caries and periodontal disorders.
Results: Although there is extensive literature on root caries, consensus is lack-
ing regarding certain aspects, such as diagnostic criteria, prevalence within pop-
ulations and indisputable risk factors. Advancing age could be an aggravating
factor in susceptibility to root caries for the periodontal patient; however, defini-
tive evidence in this regard is still missing. Similarly, full awareness of the
increased risk of root caries in patients with periodontal disease or long-term
periodontal treatment appears to be still lacking. Isabella Bignozzi, DDS, PhD, EduPERIO
Periodontal Education and Research
Conclusion: Research regarding root caries in age-specific (elderly) periodontal International Organization, Rome, Via
patients is needed. Improved oral hygiene practices, locally applied preventive Germanico 99, 00192, Italy
Tel: +39 065572211
measures, good dietary habits and regular dental check-ups are crucial Fax: +39 06636208
approaches to prevent both periodontal disease progression and root caries. e-mail: i.bignozzi@tiscali.it
Periodontal patients with root exposure should follow a strict root caries pre- Key words: periodontal disease; prevention and
vention protocol, as an integral component of their periodontal maintenance control; root caries
therapy. Accepted for publication March 30, 2013

Gingival recession (GR) is defined as The purpose of this narrative apy as risk factors for tooth root
“the apical migration of the gingival review is to provide a periodontal per- exposure and RC; the benefits and
margin beyond the cemento-enamel spective on RC in the periodontal limitations of periodontal surgical
junction” (1). This condition is inevita- patient; specifically, this article will procedures, with or without adjunc-
bly associated with exposed root sur- provide an overview of the main path- tive restorative treatments, as a viable
faces and the consequently increased ogenic mechanisms leading to RC and prevention and treatment strategy for
risk of root caries (RC). GR is a multi- of the preventive and therapeutic RC; and the significance of RC as a
factorial condition, with periodontal approaches to address these tooth factor complicating or reducing the
disease and inappropriate dental root lesions in periodontally involved long-term prognosis of teeth treated
therapy being common contributing patients. The review focuses on: the with resective periodontal surgery. In
factors (2). role of periodontal disease and ther- addition, relevant aspects of RC in
144 Bignozzi et al.

age-specific (elderly) populations are tive differences in prevalence among noncavitated lesions (29). The ICDAS
addressed. The review also highlights sites and tooth type, RC can affect visual detection codes have been pro-
areas of unmet research needs in the entire dentition. Although RC ven effective for assessing enamel and
relation to RC and periodontal lesions tend to spread along the CEJ dentinal coronal caries in a reliable,
involvement. and, in general, along the root sur- valid and reproducible manner in
face, more aggressive RC lesions may both permanent and deciduous teeth
progress toward the pulp similarly to (30,31). Unfortunately, despite the
Root caries: general features
dentinal caries of the crown (14). fact that ICDAS includes diagnostic
RC commonly presents as a progres- Investigators have based the diag- criteria and decision trees specifically
sive lesion found on a tooth root that, nosis and staging of RC lesions on designed for RCs, data on the valid-
due to some degree of periodontal location (3,8,15,16), color (17–19), ity and reliability of this ICDAS sec-
attachment loss, has become exposed texture (6,16,20,21), cavitation (21,22) tion are not yet available, because no
to the oral environment (3,4). Sumney and contour (15,23,24) of the involved clinical, laboratory or epidemiological
et al. (3) defined RC as a cavitation surface. Investigators have also tried studies have been reported to date in
below the cemento-enamel junction to distinguish between active and this respect (32). Moreover, RC diag-
(CEJ), not including the adjacent inactive RC lesions based on charac- nosis may present unique clinical
enamel, usually discolored, softened, teristics cited above (20,25,26). Gaen- issues, such as the unreliability of
ill-defined and involving both cemen- gler et al. (27) classified RC into three color (33) and texture (28) as refer-
tum and underlying dentin. RC main categories, based on clinical and ence diagnostic criteria or the reduced
lesions have been variously described histopathological features. Specifi- accessibility of the affected area to
in the literature, where some authors cally, depth and progression of the direct view in case of interproximal
proposed distinctive criteria such as lesion as well as degree of demineral- (6) or subgingival (8) lesions, espe-
location at the CEJ, position entirely ization were considered to distinguish cially if complicated by the presence
on the root surface (5), spread to initial, stagnating and progressing of prosthetic crowns (34).
undermine the adjacent enamel (6) or lesions. As clinical examination may be not
extension to more than half on the Diagnosis of RC is based primarily sensitive enough to identify RC at the
root cementum (7). on traditional visual–tactile methods, very early clinical stages, several tech-
RC lesions are most often located although some reservations have been nologies have been proposed to give
on exposed root surfaces, although it raised regarding the reliability and the clinician the possibility to identify
has been reported that up to 10–20% repeatability of this RC screening subclinical, noncavitated lesions. The
of lesions may occur subgingivally (8). method (26). In this context, radio- use of emerging technologies aims to
Banting et al. (9) reported that the graphs and existing microbiological anticipate the diagnostic time, allow-
most frequent RC location is close to tests may supplement the clinical ing clinicians to manage the caries
the gingival margin, but Ravald et al. evaluation to increase sensitivity and process at an earlier stage of its natu-
(10) identified the margin of previous specificity of the RC diagnostic pro- ral history and take preventive rather
restorations (51%), the CEJ (25%), cess (28), which remains an issue. than therapeutic measures. These
and points of confluence with other The difficulty in rapid screening and technologies range from fluorescence-
lesions (17%) as areas at risk for RC early detection of carious lesions is a based or electrical caries monitors
in periodontally treated patients. Katz general concern in cariology. The (35,36) to optical coherence tomogra-
et al. (6) reported that RC are found clinical detection of dental caries at phy (37). These technologies remain
– in descending order of frequency – the early stages, which precede cavi- to be conclusively validated before
at buccal and interproximal surfaces tation, has always been a challenge. their use on a large scale to serve epi-
of mandibular posterior teeth, inter- The majority of caries detection sys- demiologic or dental practice needs.
proximal surfaces of maxillary ante- tems proposed over the years, both In the context of RC diagnosis,
rior teeth, lingual and interproximal for coronal and RC, used a dichoto- conclusive validation of a RC clinical
surfaces of maxillary posterior teeth mous system (cavitation/not) that did diagnostic system that is comprehen-
and buccal and interproximal surfaces not measure the disease process at sive of all clinical signs, but also
of mandibular anterior teeth. In con- different stages, but only identified rapid, feasible and repeatable, as
trast, Heegaard et al. (11) reported carious lesions at an advanced ICDAS has been shown to be for
that RCs are frequently found on stage of their natural history (29). coronal caries, appears to be neces-
labial surfaces and evenly distributed Recently, the International Caries sary. Future research should address
within the dentition. Imazato et al. Detection and Assessment System the in vitro and in vivo validation of
(12) reported canines and first premo- (ICDAS) has been developed from ICDAS for RCs, taking into consider-
lars as the most frequently involved the best aspects of previously pub- ation intra- and inter-examiner agree-
teeth, while Kularatne and Ekanayake lished systems to address and over- ment, to pursue standardization in
(13) indicated instead the molars of come inconsistencies, set diagnostic diagnosis and staging; studies that
both arches as most frequently threshold and criteria, as well as reli- address the specific challenges of RC
involved. Regardless of possible rela- ably and repeatedly identify and stage diagnosis should be encouraged.
Root caries: a periodontal perspective 145

microbial species not previously identi- but also the ability to survive and
Root caries: etiologic factors
fied in the oral cavity (47). Culture- grow in a low pH environment (acid-
The main etiologic factors for onset independent, open-ended approaches uricity) might be a virulence determi-
and progression of RC are the presence comparing the biofilm of patients/sites nant crucial for inducing RC. The
of bacteria and fermentable carbohy- with or without RC are advocated. The authors proposed a dynamic model of
drates on the root surface (38) [Correc- microbiological profile of patients with bacterial etiology, with a progressive
tion added on 20 May 2013, after first RC with periodontal disease or sub- selection for a bacterial biofilm* with
online publication: Reference of jected to long-term periodontal treat- significant acidogenic and aciduric
progression of RC ‘in the elderly’ was ment should be characterized as well, to properties, that seems to include (but
removed]. Lactobacillus, Streptococcus clarify the possible impact of periodon- is not limited to) bacteria commonly
mutans and Actinomyces salivary tal status on root surface bacterial believed to be involved, such as
counts have been significantly corre- biofilm and its role in RC pathogenesis. S. mutans and lactobacilli.
lated with RC occurrence (39). Scan- Recently, Hashimoto et al. (56) per-
ning electron microscopy observations formed a pilot study in six subjects
Root caries: pathogenic
revealed various patterns of bacterial aged 48–73 years and used 16S rRNA
mechanism and relevant
coaggregation in RC lesions (40), while sequencing analysis and anaerobic cul-
bacterial metabolic pathways
synergistic growth was observed in co- ture on blood agar plates to identify
cultures of Lactobacillus acidophilus Bacteria metabolize sugar into organic the proportions of protein-degrading
with Streptococcus mutans, Actinomy- acids, which initiate root surface and protein-coagulating bacteria in
ces israelii with Lactobacillus acidophi- demineralization by removing calcium plaque samples collected from RC
lus and Actinomyces israelii with and phosphate ions from surface apa- lesions, healthy supragingival sites and
Lactobacillus acidophilus and Strepto- tite crystals. For enamel, this process periodontal pockets  5 mm deep. In
coccus mutans, seemingly resulting in takes place as the pH reaches the crit- RC sites, a predominance of Propioni-
greater acidogenic and cariogenic ical value of 5.5; however, pH 6.4 is bacterium, Actinomyces, Streptococcus,
effects on the root surface (39). sufficient for cementum and dentin Lactobacillus and Bifidobacterium was
Although Candida albicans has been demineralization, due to their lower found, with evidence of prevailing pro-
identified in root surface soft lesions, it degree of mineralization (48). Under tein-coagulating metabolic pathways,
is not considered an etiologic factor in normal circumstances, this loss of cal- and less represented protein-degrading
RC onset (41–43). cium and phosphate ions is balanced activities. Subgingival periodontitis
Subjects with unaffected root sur- by the uptake of minerals from the sites had the highest proportion of pro-
faces show a more nonspecific micro- surrounding microenvironment. An tein-denaturing bacterial strains, with
flora, with greater interindividual unfavorable oral environment, with specific predominance of protein-
differences in biofilm composition, high levels of pathogenic bacteria and degrading ones, in agreement with pre-
while in patients with RC the bacterial rate of carbohydrate fermentation, vious findings (57). The authors noted
biofilm* of root surfaces tends to have may alter the balance of this deminer- that periodontally involved root sur-
lower interpatient diversity, decreasing alizing–remineralizing cycle in favor faces, exposed to oral environment and
further at affected roots (44). Although of caries development. challenged by organic acids derived
these findings corroborate the hypoth- In brief, some characteristics of from fermentable carbohydrates are
esis of a plaque-specific RC etiology, dental biofilm* have been considered likely to have their organic compo-
presently the microbiological agents to be relevant with regard to cario- nents denatured and then degraded
causing this condition have not been genic potential in several studies over through the synergistic action of pro-
conclusively identified (44). The oral the years; these include the dynamics tein-degrading and protein-coagulating
microflora is highly diversified and of pH and free calcium concentration bacterial strains, resulting in the onset
may comprise up to 600 bacterial spe- in the bacterial biofilm fluids after and progression of RC (56). In this set-
cies, many of which have not yet been exposure to fermentable carbohydrate ting, robust host-derived proteolytic/
cultured (45,46). Because of their (49) and collagenase activity (50) with collagenolytic activity (from periodon-
inherent limitations, culture-dependent consequent organic matrix degrada- tally involved gingival tissues) might
identification techniques pose the risk tion (51), long-lasting glycogen syn- play a contributory role in the RC pro-
of limited or even misleading informa- thetic and degradative activities at cess in patients with periodontitis.
tion, particularly when single site anal- acidic pH levels (52,53), and the abil- Although the various pathogenic
ysis is performed, given the site- ity to induce significant concentra- activities summarized above have been
specificity of microflora (44). tions of microbial-derived organic reported in the issue-focused litera-
The use of culture-independent meth- acids with high dissociation constants ture, the complete RC pathogenetic
ods has allowed the discovery of – such as formic and pyruvic acids – puzzle has not yet been solved. Given
in dentin matrix (54). the apparent significance of proteoly-
*Corrections added on 20 May 2013, after Brailsford et al. (55) suggested that sis as a pathogenic mechanism in RC
first online publication: References to plaque not only the ability to produce acid it appears that targeted studies, on lar-
have been corrected to biofilm. from carbohydrates (acidogenicity), ger patient samples, with specific
146 Bignozzi et al.

attention to protein-denaturing bacte- and intratubular dentin deposition clinically distinguished from stagnating
rial activities, as well as their potential and an underlying layer of translucent ones by their surface texture and color:
association or synergism with host- dentin (60). Dentinal tubules appear progressing RC lesions are commonly
derived proteases, could be helpful in to be sclerosed by precipitation of cal- characterized by a soft and yellowish
elucidating the significance of the vari- cium and phosphate ions, and tubules discolored surface, while in stagnating
ous mechanisms presently implicated containing ghosts of bacteria and RC lesions a hard, brown to black sur-
in RC pathogenesis. In this context, fine-granular crystals may be observed face may be observed (17,66). In more
intervention studies targeting host- as well (61). Stagnating RC lesions advanced lesions, the surface zone and
derived proteolytic enzymes could be are characterized by a surface layer demineralizing dentin are commonly
of help in illuminating the contribu- with high mineral content (62), not well demarcated, and a massive lat-
tion of periodontally involved tissues absence of viable bacteria in dentin eral spread of bacteria into intertubu-
to RC pathogenesis. tubules (59,63), impermeability to lar dentin may be observed, with
dyes and isotopes (64) and high resis- unaffected dentinal areas becoming
tance to acid and proteolytic enzymes continuously undermined. Notably,
Root caries: histopathology
(65) suggesting that arrest and remin- the mineral content in different zones
Root cementum and dentin are struc- eralization of active lesions may within the lesion may vary consider-
turally different from enamel and depend upon the balance between ably, and this aspect could result in
coronal dentin and react differently severity of cariogenic bacterial infec- underestimation of lesion depth (67).
to cariogenic challenges (Table 1) tion of dentin and degree of active
(14,28,58,59). As mentioned above, sclerosis of dentinal tubules in areas
Root caries: epidemiology
Gaengler et al. (27) classified RC into underlying the lesion.
(prevalence, incidence and
initial, stagnating and progressing Conversely, in progressing RC
risk indicators)
lesions, based on clinical and histo- lesions a superficial layer with diffuse
pathological features. Microstructural bacterial penetration and an intermedi- The apparent lack of unanimous con-
observations of initial RC lesions ate area of demineralizing dentin may sensus on the criteria to diagnose RC
reveal an external layer with dentinal be observed above the translucent den- lesions and the variability of RC
tubules partly occluded by peritubular tin (14). Progressing lesions may be descriptors used in the literature (28)

Table 1. Comparison between coronal and root caries, adapted from Banting (28)
Coronal caries Root caries

Etiology Cariogenic bacteria (S. mutans, Lactobacilli) Cariogenic bacteria (S. mutans, Lactobacilli,
Fermentable carbohydrates Actinomyces) (39)
Fermentable carbohydrates (38)
Predisposing factors Plaque index Plaque index (80,88,89)
Frequency of carbohydrate intake Frequency of carbohydrate intake (79)
Reduced salivary flow Reduced salivary flow (90,228)
Fluoride exposure ( ) Fluoride exposure ( ) (8)
GR/CAL (69,79,94,95,97–99)
Advanced age (81,206,207)
Low socio-economic status (95)
Reduced manual dexterity (93)
Cognitive decline (229)
Surface tissue Enamel/dentin Cementum/dentin
Tissue composition Enamel: Dentin:
(by weight) 95–97% mineral 65–70% mineral
3–5% organic and water 30–35% organic and water
Dentin: Cementum
65–70% mineral 45%–55% mineral
30–35% organic and water 45–55% organic and water
Demineralization onset pH  5.5 pH  6.4 (48)
Carious process In enamel: In cementum:
Bacterial invasion followed by demineralization Bacterial invasion followed by simultaneous
demineralization and proteolysis (14,58,59)
In dentin: In dentin:
Bacterial penetration of tubules; demineralization Bacterial penetration of tubules; demineralization of
of intertubular dentin and proteolysis of organic intertubular dentin and proteolysis of organic component;
component; Sclerosis of dentin tubules, destruction of lumens and
Sclerosis of dentin tubules, destruction of lumens peritubular dentin deposition (14,28,58–60)
and peritubular dentin deposition

GR, gingival recession; CAL, clinical attachment loss.


Root caries: a periodontal perspective 147

result in subjectivity impacted esti- seemed to be a greater likelihood to subgroups having different social class
mates of prevalence, incidence and develop RC for patients with a higher and education. In two other studies
severity of RC in the studied pop- mean frequency of sugar intake, with involving similar populations of com-
ulations (8,68). The inclusion or an odds ratio (OR) of 2.4, infrequent munity-dwelling individuals aged
exclusion of restored root surfaces tooth cleaning (OR = 4.7) and ineffec- 80 years or older, cognitive decline,
and/or recurrent lesions in any tive tooth cleaning in presence of a reduced functional ability as well as
assessment introduce further variabil- partial denture (OR = 1.6). The most unsatisfactory social relations were sig-
ity on reported prevalence rates (21). relevant background risk variables nificantly related to higher risk of
Several population characteristics were severe (  9 mm) loss of clinical active coronal caries and RC and, in
have been investigated as putative RC attachment (OR = 2.4) and exposed general, poorer oral health and infre-
risk indicators in cross-sectional and roots (OR = 1.05, per “vulnerable” quent use of dental services (85,86).
longitudinal studies (41,69–77); unfor- tooth), while having sound coronal Therefore, on the basis of the avail-
tunately, the considerable heterogene- restorations was somehow protective able literature, the following variables
ity among studies in terms of (OR = 0.94 per restored tooth). A should be considered among the main
analyzed variables (e.g. sample size, further stepwise multiple regression local factors involved in RC patho-
follow-up period and analytical tech- analysis was carried out considering genesis: high salivary counts of patho-
niques) has prevented conclusive vali- as dependent variable the root caries genic microorganisms (41,87); high
dation of a risk model and index for decay, calculated as the pro- percentage of dental surfaces harbor-
identification of population features portion of all vulnerable teeth, ing plaque (43,88,89); unrestored
that may significantly increase the risk i.e. with some degree of exposed root coronal caries and RC (69,75,88); and
of RC occurrence (78). surface, being affected by active factors promoting plaque accumula-
In general, all the identified predis- decay. Under such analysis, the habit tion, such as presence of restorations
posing conditions have to be consid- of sucking sweets to relieve dry mouth (10) and reduced salivary flow (90).
ered risk indicators rather than actual (b = 0.101, p = 0.037), living in an The population’s systemic and behav-
risk factors for RC occurrence, institution (b = 0.172, p = 0.000) or ioral conditions that might play a role
because of the inability to establish not attending regular dental check- in RC occurrence or progression
cause–effect relationships through the ups (b = 0.098, p = 0.002) were the include advanced age (41,72–74), low
available descriptive, cross-sectional behavioral conditions associated with socio-economic status and educational
studies and the limited agreement RC occurrence, in addition to the pre- level (84), discontinuity in oral health
among reported longitudinal investi- viously identified variables of wearing care and dental check-up (79,86),
gations. Table 2 summarizes the a partial denture and having infre- frequency of carbohydrate intake
results of longitudinal studies, report- quent personal tooth cleaning. (91,92), impaired manual dexterity
ing the calculated incidence rates and The potential contribution of some and cognitive decline (85,93). It must
the variables identified as putative risk sociodemographic parameters to RC be recognized that, despite the fact
factors for RC occurrence. prevalence may be hypothesized but it that disease prevalence is frequently
Among the numerous variables that is not easily evaluable due to lack of used as a rough estimate of risk, inci-
have been investigated over the years homogeneity among the relevant dence data from longitudinal studies
as putative RC risk indicators, 30 studies. Several cohort studies have (i.e. cohort studies) may provide a
have been shown to be significantly revealed a wide range of incidence higher level of evidence and more reli-
associated with increased RC inci- rates, varying by population charac- able risk estimates.
dence in at least one study. Specifi- teristics, sample size and study length. Surprisingly, the contribution of
cally, RC prevalence at baseline, Despite such differences in incidence periodontal parameters to RC has
number of teeth at baseline, patient rate, older, medically compromised or received limited attention. Only a few
age, plaque index and salivary counts institutionalized subjects and subjects studies (69,94,95) considered clinical
of Lactobacillus and S. mutans are with advanced periodontal disease attachment loss (CAL) and/or GR
independent variables that have been commonly exhibit higher RC inci- among the targeted putative risk indi-
repeatedly shown to have a positive dence compared to the general adult cators. Nevertheless, considering that
association with new RC occurrence population (9,22,41,42,70,75,80–83). GR is almost endemic in the adult
during a 1–10 year (median = 3) inci- Social, psychological and cogni- population, as well as a supposedly
dence period (78). tive status also seems to affect oral necessary condition for RC occur-
Steele et al. (79) conducted a multi- health conditions in noninstitutional- rence in the majority of cases, it may
variate analysis on 462 patients (405 ized elderly subjects. Avlund et al. (84) not be proper, from a methodological
community-living; 57 institutionalized) examined 157 independently living point of view, to include GR as an
aged  65 years; they used the pres- subjects, aged over 80 years, and independent variable in a risk model
ence of primary RC as dependent var- reported substantial differences in oral (78). However, it is undeniable that,
iable and behavioral or background health – measured as active coronal due to the unique spatial relationship
characteristics as independent vari- caries, active RC, edentulism and between root surface and marginal
ables. Based on this study, there regular use of dental services – in two periodontium, RC and periodontal
148
Table 2. Summary of cohort longitudinal studies reporting incidence rates and risk modelling (continued)
Observation RC incidence
Sample period Population (% subjects Significant
Study size (N) (months) characteristics affected) Risk model predictors

Powell et al., 23 12  65 years old 61.9% Logistic Variables Regr Coeff (SE)
1991 (230) instituzionalized regression Gender 1.06 [0.41]
Bignozzi et al.

RCIlog 0.42 [0.15]


Ravald and 99 24 33–76 years old 50% Stepwise Variables R2 Partial correlation p-value
Birkhed, 1992 community-dwelling, multiple Baseline RC 0.18 0.43 p = 0.0002
(88) periodontally treated regression Plaque score 0.23 0.24 p = 0.0069
No. teeth 0.28 0.24 p = 0.0246
Joshi et al., 130 9–24 Middle-aged/older 50.7% Stepwise Variables Estimate (SE) OR (95% CI) p-value
1993 (89) (median = 16) community-dwelling logistic Baseline RC 0.13 [0.04] 1.14 (1.05–1.23) p = 0.004
regression No. teeth 0.97 [0.39] 2.63 (1.22–5.66) p = 0.01
Plaque score 0.99 [0.45] 2.69 (1.11–6.50) p = 0.02
Ravald et al., 27 144  46 years old 88.9% Stepwise Variables p-value
1993 (80) community-dwelling multiple Plaque score p = 0.00
periodontally treated regression Smoking p < 0.05
Scheinin et al., 96 36 47–79 years old 51% Logistic Variables OR (95% CI)
1994 (43) community-dwelling regression rDFS 12.8 [2.8–58.5]
Candida 2.8 [0.9–8.1]
Lactobacilli 8.6 [2.4–31.2]
Lawrence et al., 55 36  65 years old 29% (blacks) Logistic Variables OR (95% CI)
1995 (95) community-dwelling 39% (whites) regression Blacks:
234 blacks RPD 3.43 [1.52–7.76]
218 whites Root fragments 3.31 [1.28–8.58]
Average GR 1.75 [0.75–4.12]
P. Intermedia 2.74 [1.27–5.92]
Impact on appearance 2.24 [1.09–4.60]
Daily activities 1.67 [1.12–2.5]
Whites:
Worst GR 4.5 [1.95–10.39]
Average PD 3.81 [1.24–11.69]
Worst GR + average PD 3.35 [1.28–8.76]
Antihistamines 4 [1.45–11.07]
Calcium therapy 2.45 [1.08–5.57]
Age-related problems (> 40) 4.99 [2.17–11.47]
Employement status 3.17 [1.32–7.61]
Locker, 1996 493 36  50 years old 27.4% Logistic Variables OR p-value
(81) community-dwelling regression DFS model:
Baseline RC 2.3 p < 0.001
DS model
Age 2.5 p < 0.05
Regular check-up 1.9 p < 0.05
Baseline RC 2.2 p < 0.05
Table 2. (continued)

Observation RC incidence
Sample period Population (% subjects Significant
Study size (N) (months) characteristics affected) Risk model predictors

Lawrence et al., 702 60  65 years old 39% (blacks) Logistic NR NR


1996 (22) community-dwelling 52% (whites) regression
379 blacks
323 whites
Powell et al., 55 36  60 years old 77% Poisson Variables Regr Coeff (SE) Rel Risk (95% C) p-value
1998 (42) community-dwelling regression Bacterial countslog 0.258 [0.085] 1.29 [1.10–1.53] p = 0.002
Asian ethnicity 0.617 [0.237] 1.85 [1.16–2.95] p = 0.009
Gilbert et al., 723 24  45 years old 36% Logistic Variables OR (95% CI) Estimate (SE) p-value
2001 (75) community-dwelling regression Baseline RC 2.3 [1.4–3.7] 0.83 [0.24] p = 0.01
Baseline FS 3.6 [2.4–5.7] 1.29 [0.22] p = 0.01
No. teeth 1.9 [1.1–3.4] 0.64 [0.30] p = 0.03
No. lost teeth 1.6 [1.0–2.5] 0.46 [0.22] p = 0.04
Chalmers et al., 216 12 Older, institutionalized 62.1% (dementia) Linear Variables b (SE) F p-value
2002 (229) 103 dementia affected 44.2 (control) regression Gender (male) 0.071[0.291] 0.059 p < 0.8
113 control Dementia 0.945[0.287] 10.824 p = 0.001
Takano et al., 373 24 70 years old community- 35.9% Logistic Variables OR (95% CI) p-value
2003 (69) dwelling regression Baseline RC 3.71[2.07–6.67] p = 0.00
Prosthetic crow 2.33[1.24–4.39] p = 0.009
CAL 2.32[1.31–4.12] p = 0.004
OH habits 2.05[1.26–3.35] p = 0.004
Fure et al., 102 120 65–85 years old 12.4% Stepwise Variables Partial correlation b-coefficient
2004 (41) community-dwelling regression Lactobacilli log 0.37 2.78
No. teeth 0.45 0.85
Drugs/day 0.27 1.76
S
anchez-Garcıa 531 12  60 years old 21.7% Bivariate and Variables Bivariate OR Multivariate
et al., 2011 multivariate (95% CI) OR (95% CI)
(94) logistic Limitations in BDLA 2.2 [0.9–5.0] 3.1 [1.0–9.5]
regression Smoking 2.0 [1.1–3.7] 2.0 [1.0–4.1]
Self-perceived oral 1.6 [1.0–2.7] 1.4 [0.8–2.5]
health
Dental mouthwash 1.6 [1.0–2.5] 1.7 [1.0–2.8]
(no)
Mutans streptococci 1.6 [1.0–2.7] 2.1 [1.1–4.0]
(‡105 CFU⁄ ml)
DMFT index (  17) 1.6 [1.0–2.5] 1.3 [0.8–2.3]
Exposed root 5.1 [3.2–8.2] 5.4 [3.2–9.1]
surfaces (  6)
RCI  8% 1.6 [1.1–2.5] 1.8 [1.1–3.1]
CAL  4 mm 1.6 [1.0–2.5] 0.8 [0.5–1.4]
Root caries: a periodontal perspective

RCI, Root Caries Index; Regr Coeff, Regression Coefficient; SE, Standard Error; CI, Confidence Interval; RC, Root Caries; rDFS, root Decayed Filled Surface; RPD, Removable Partial
Denture; GR, Gingival recession; PD, Probing Depth; DFS, Decayed Filled Surface; DS, Decayed Surface; NR, Not Reported; Rel Risk, Relative Risk; DMFT, Decayed Missing Filled
Teeth; FS, Filled Surface; CAL, Clinical Attachment Loss; OH habits, Oral Hygiene habits; BDLA, Basic Daily Life Activity.
149
150 Bignozzi et al.

disorders often coexist, not only as can occur subgingivally (8), in most after appropriate periodontal plastic
concurrent events, but also as condi- cases GR might be considered a nec- surgery procedures (106).
tions linked by two-way cause–effect essary condition for RC development Conversely, GR that manifests as a
relationships. (101,102). GR is highly prevalent in component of inflammatory periodon-
patients with either high (2,103) or titis is associated with interproximal
poor (104,105) oral hygiene standard, CAL (105), and may involve buccal,
Root caries: relationship with
but presents with different characteris- lingual and interproximal surfaces
periodontal disorders
tics. Miller (106) categorized GR (2,105) (Fig. 1B). This type of GR
In the context of RC predisposing defects into four classes, based on the lesion typically belongs to Miller III
clinical factors, particular attention relation of the gingival margin to the or IV class (103), and is, therefore,
should be paid to patients with peri- mucogingival junction and the degree unlikely to be completely resolved fol-
odontal diseases. CAL and GR have of interproximal CAL, highlighting lowing regenerative periodontal surgi-
been recognized as relevant predispos- how these clinical variables concern- cal intervention (106,115). Regardless
ing factors in the onset of RC, given ing GR are significant for root cover- of the underlying etiology or associ-
the increased vulnerability of exposed age outcomes (106). ated attachment loss, GR lesions
root surfaces. RC is considered a Notably, in patients with good oral predispose to several different compli-
serious problem affecting the long- hygiene and without signs of inflamma- cations, such as hypersensitivity (116),
term prognosis of both treated and tory periodontal disease, GR is com- loss of esthetic appearance (117),
untreated periodontally involved teeth monly located at buccal tooth surfaces tooth abrasion (118), plaque retention
(96). Epidemiologic as well as large and putative causative factors include (119) and RC (120). The RC preva-
clinical trials agree that presence of traumatic tooth-brushing (107–109), lence rate in subjects with GR was
GR and CAL are associated with a eccentric orthodontic movement (110), significantly higher (90%) than that
higher incidence of RC (79,97–99). tooth malposition (111), presence of (20–40%) reported in matched reces-
Fadel et al. in a recent cross- alveolar bone dehiscence (112), or high sion-free subjects (120).
sectional study (100) reported a high frenal attachment (113). In this sub-
prevalence of RC lesions and high group of patients, GR defects are not
Root caries: relationship with
caries risk rates in 20% of patients associated with interproximal CAL
nonsurgical periodontal
referred for periodontal treatment, and are typically classified as either
therapy
whether affected by gingivitis (mean Miller I or Miller II (2,103,114)
age 25.8), mild-to-moderate periodon- (Fig. 1A); these types of GR defects The interrelationship between RC and
titis (mean age 41.9), or severe peri- are much more likely to fully resolve periodontal disease extends beyond
odontitis (mean age 49.7); the (i.e. to exhibit complete root coverage) the pathological entities per se.
prevalence of root lesions (caries and/
or fillings) was 9%, 15% and 29% for
each group, respectively. However, A B
estimated RC risk profiles appeared
correlated with a combination of sev-
eral factors and not specifically with
periodontal disease severity. The
undeniable correlation between peri-
odontal disorders and RC incidence
rate emerged also from a RC predic-
tion model involving a population of
698 subjects aged  60 years, where
it has been shown that having C
 75 years of age (OR = 1.3, CI
95% 0.8–2.0),  6 exposed roots
(OR = 5.1, CI 95%: 3.2–8.2) or
 4 mm CAL (OR = 1.6, CI 95%:
1.0–2.5) are significant risk predictors
for RC development in a 12-month
period (94).

Root caries: relationship with


Fig. 1. (A) Patient with good oral hygiene and multiple deep Miller I and Miller II gingi-
gingival recession
val recession defects. (B) Severe Miller III and Miller IV gingival recession defects in a
As discussed above, despite the fact patient with periodontitis. (C) Severe periodontitis treated by osseous surgery (left panel);
that a small proportion of RC lesions the resulting gingival recession is evident at the 1 wk postoperative visit (right panel).
Root caries: a periodontal perspective 151

Periodontal therapy alone may lead breakdown was the main cause of tooth worst probing depth/GR ratio in sites
to GR and thus to an increased vul- loss during the period of observation. of medium (5–6 mm) and shallow
nerability of the root surface to caries. However, a combination of periodon- (1–4 mm) probing depth. Even
While the crucial role of subgingival tal problems and RC was evident in though it is important to emphasize
mechanical debridement (scaling and 20% of the considered population, and that sites treated by resective surgery
root planing) in the treatment of peri- RC lesions alone accounted for 13% of seem to have the least incidence of
odontitis is undisputed (121), the failing teeth (129). It should be empha- breakdown during long-term follow-
occurrence of GR development or sized that subgingival mechanical up (139), it is fair to point out that
increase following mechanical instru- debridement is indicated, and must be the potential significant amount of
mentation has been widely reported performed, only in pathologically GR resulting from this surgical
(122–124). GR development or pro- involved periodontal sites; subgingival approach (Fig. 1C) may constitute a
gression following scaling and root instrumentation performed on physio- limit of the obvious and generally
planing, especially for initially shallow logic crevices, with shallow probing recognized clinical benefit of osseous
or moderately deep probing depths depth values and absence of bleeding surgery in certain cases.
(125), is particularly evident in on probing, may result in iatrogenic In this context, when surgical inter-
patients with thin gingiva (126). CAL and GR, which could promote vention is deemed necessary, an alter-
Cause-related periodontal therapy, long-term RC occurrence. native to osseous surgery, such as
through ultrasonic or hand instru- The nonsurgical therapy of peri- open flap debridement, may be con-
mentation, acts on the root surface by odontitis may include systemic and/or sidered to gain access to the affected
removing or exposing cementum and local chemotherapeutic agents that root surfaces without drastically
dentin; these tissues are characterized target either the pathogenic biofilm or changing the periodontal tissue archi-
by a lower degree of mineralization, host-derived catabolic processes (130– tectural relationships, thus minimizing
limited amount of fluoride and poorer 133). Although most of the chemo- post-surgical GR occurrence. Further-
caries resistance than enamel (48). therapeutic drug studies are of short more, as two determining factors for
Furthermore, repeated professional duration, which precludes consider- the prognosis of surgically treated
oral hygiene procedures may lead to ation of RC development, even stud- sites are the quality of the patient’s
an imbalance of normal competitive ies of sufficient duration (  12 mo) postoperative plaque control and the
microflora, promoting the growth of have not included RC assessment frequency of maintenance care
cariogenic bacterial colonies on the (134–137). Therefore, the potential appointments (140,141), patients who
root surface (127). impact of periodontal chemotherapeu- have difficulty in maintaining a high
Ravald et al. (10,80,128,129) studied tics to RC incidence or prevention standard of self-performed daily oral
longitudinally the incidence of RC and remains to be investigated. hygiene and/or regular attendance for
the main reasons for tooth loss in a dental check-ups are not the best can-
population of periodontally treated didates for resective periodontal sur-
Root caries: relationship with
patients at four (128), eight (10), 12 gery (or any periodontal surgical
surgical periodontal therapy
(80) and 14 (129) years of maintenance therapy, for that matter).
periodontal therapy. The mean age of Although surgical pocket elimination
patients was 52  10.6 years (range remains an important component of
Other site-specific putative
30–78) at baseline and 64  8.3 years periodontal treatment, it can be antic-
predisposing factors;
(range 49–91) at the final examination. ipated that periodontal surgery, espe-
noncarious cervical lesions
During the first 4 years of follow-up, cially when incorporating resective
approximately two-thirds of patients procedures, will have an even greater In sites affected by GR, it is not
developed RC lesions. This incidence impact than nonsurgical therapy in uncommon to observe an associated
of new RC lesions was confirmed promoting increased RC incidence. noncarious cervical lesion (NCCL) on
during all observation periods, exhibit- Kaldahl et al. (138,139) followed 82 the exposed root surface. NCCL is
ing a certain degree of clustering in patients with chronic periodontitis defined as the wear of tooth substance
some patients and sporadic or (initial mean age 43.5 years) treated along the gingival margin of the
recurrent correlation with advanced by either coronal scaling, root plan- tooth, due to mechanical abrasion,
age (10,80,128,129), salivary counts of ing, modified Widman surgery, or erosion or abfraction. The different
S. mutans and Lactobacilli osseous resection surgery in a four- underlying etiologies result in NCCL
(10,80,128,129), plaque score (10,80), quadrant split-mouth design, evaluat- with diverse clinical characteristics.
dietary habits (10), previous RC experi- ing probing depth, CAL and GR after Dental abrasion is frequently asso-
ence (10,128), low saliva secretion rates 2 (138) and 7 (139) years of mainte- ciated with repeated mechanical
(128) and smoking habit (80,129). In nance therapy. In general, osseous trauma from compulsive, excessive
these studies, patients with ongoing resective surgery produced both the toothbrushing and use of abrasive
periodontal problems were more preva- greatest probing depth decrease and toothpaste or hard toothbrush. The
lent (49%) than patients with RC alone the greatest amount of GR compared frequency and duration of tooth-
(3%), and recurrence of periodontal with other therapies, showing the brushing, force applied and structure
152 Bignozzi et al.

of dental tissues influence the degree face (Fig. 2A). Dental erosion is tooth erosion lesions appear as not well-
of tooth wear in each individual structure dissolution without bacterial demarcated, hard and quite smooth
(142). Root surface abrasion lesions involvement, due to intrinsic (e.g. gas- areas (Fig. 2B). Abfraction lesions
appear as well-demarcated cervical tro-esophageal reflux) or extrinsic appear to be the consequence of tooth
concavities, usually more broad than (e.g. acidic foods such as fruit juices) bending and strain, possibly due to
deep, showing a hard and smooth sur- acid sources (143). Root surface eccentric occlusal forces (144). They
commonly present as deep, narrow,
v-shaped notches on the facial aspect
A B of the cervical area (Fig. 2C).
Recent clinical and experimental
findings suggest that it is the synergis-
tic action of the various processes
cited above, with mechanical causes
such as abrasion and abfraction being
potentiated by chemical dental ero-
sion, which results in tooth structure
wear, as opposed to the action of a
single damaging mechanism (145).
C NCCLs have the potential to evolve
and in later stages result in dentin
hypersensitivity (146), severe loss of
tooth structure integrity and pulpal
involvement (Fig. 2D). More impor-
tantly, for the context of the present
topic, NCCLs may be complicated by
superimposed RCs (147) (Fig. 2E).
It is widely recognized that NCCL
and RC are distinct nosologic entities,
D E and risk models generally do not con-
sider NCCL as a predisposing factor
for RC (78). Nevertheless, these two
pathological conditions share some
clinical features (such as progressive
impaired structural integrity of cervi-
cal dental hard tissues), pathogenic
factors (such as cavitation from inter-
mittent demineralization processes
(148) and long-term consequences, as
F mentioned above; these shared traits
establish a conceptual link between
NCCL and RC. In this context, it is
reasonable to postulate that the pres-
ence of NCCL, i.e. concave area near
the gingival margin, may promote
bacterial biofilm* accumulation on
tissues with decreased microstructural
resistance and thus result in RC
development (149).
Fig 2. (A) Patient with multiple noncarious cervical lesions, likely due to mechanical
trauma from horizontal toothbrushing (abrasion lesions). (B) Gingival recession defects
Specifically focusing on dental
associated with noncarious cervical lesions apparently due to erosion from acidic foods erosion, long-term high intake of
and drinks. (C) Noncarious cervical lesions probably related to occlusal imbalance (abfrac- acidic drinks or foods has been shown
tions). Frontal view (left panel) and lateral view (right panel); note the wear facets on to reduce surface hardness of enamel
canines and premolars. (D) Advanced noncarious cervical lesion resulting in pulpal expo- and dentin (150). Frequent exposure to
sure (endodontically treated left central incisor) in elderly patient; note the good level of erosive substances, in the presence of
oral hygiene and superimposed inactive carious lesion. (E) Carious cervical lesion superim- good oral hygiene, results primarily in
posed on noncarious cervical lesion. (F) Multiple restored noncarious cervical lesions and dental erosion without caries. Hard tis-
coexisting buccal and interproximal root caries, under conditions of suboptimal oral sue loss after acid exposure and imme-
hygiene, in an elderly patient. diate toothbrushing is significantly
Root caries: a periodontal perspective 153

greater than acid erosion alone program (91). Nevertheless, sugar proposed, although their use may be
(151,152) and, paradoxically, it would restriction may be a difficult goal to questioned due to unfavorable cost–
be advisable to avoid toothbrushing achieve for most individuals (156), con- benefit ratio (164).
for at least 30 min after an erosive sidering that sweet taste may be Griffin et al. (165), analyzing thro-
attack to protect dentin (153). Never- responsible for addictive-like behaviors ugh a systematic review with meta-
theless, in a patient who presents with (157). A possible support strategy to analysis the effectiveness of various
multiple NCCLs a decline in self- address this concern is to replace fer- forms of fluorides in preventing caries
performed oral hygiene standard can mentable carbohydrates with noncario- in adults, reported that any form of
quickly lead to the onset of deep RC genic sugar alcohols such as sorbitol or fluoride administration (self- and pro-
lesions superimposed on the previous xylitol, to decrease sugar intake and fessional application or water fluori-
inactive ones (154) (Fig. 2F). thus reduce caries risk (158). The dation) results in a RC prevented
replacement of sugar with xylitol was fraction of 22% per year. There is
able to produce a substantial (85%) some evidence (166) of a synergistic
Root caries: preventive and
decrease in caries incidence in an adult effect of amorphous calcium phos-
therapeutic considerations
Finnish population during a 2-year phate and casein amorphous calcium
From a clinical standpoint, there is observation period (159). phosphate complexes with fluoride,
general agreement in the literature Furthermore, when polyol sweeten- through the induction of a favorable
that deep cervical lesions, regardless ers are delivered in the form of chew- chemical gradient of calcium and
of their carious or noncarious nature, ing gum, the chewing action in itself phosphorous at the tooth surface able
require a full understanding of their and the resulting salivary flow stimu- to induce remineralization and
etiology; this will allow the clinician lation may provide further protective reduced incidence of RC even in
to provide the patient with appropri- effects (160). Accordingly, xylitol and patients at particular risk (167).
ate information on lifestyle changes sorbitol in chewing gum or candies Recently, encouraging in vitro
and adoption of preventive measures were able to significantly reduce RC results have been obtained testing a
(145), as well as proper restorative incidence in a geriatric patient popu- proanthocyanidin-rich grape extract, a
treatment to preclude further damage lation sample over a 6–30 month per- widely available naturally occurring
(154). iod (161). Although the widespread plant metabolite, in reducing root
adoption of a xylitol regimen for dentin demineralization during a
caries prevention appears to be non- pH cycling artificial caries protocol
Preventive measures
sustainable, because of low cost-effec- (168,169). Based on the principle that
Proper preventive measures should be tiveness (160), this prevention strategy proper mineralization of a collagen-
taken based on the estimated level of remains viable when applied to high- based tissue (i.e. root dentin) strictly
risk for the individual patient. In gen- risk populations such as disabled, depends on structure and stability of
eral, all modifiable behaviors that elderly and most frail individuals its extracellular organic matrix, the
have been implicated, as outlined (155). mechanism of action hypothesized for
above, in the multifactorial model of Fluorides are widely recognized to a proanthocyanidin-rich grape extract
pathogenesis should be addressed, to be a key factor in the prevention and in inhibiting RC relies on increased
the extent possible. Particularly, pre- control of dental caries, through collagen cross-links and reduced enzy-
vention of RC, similar to coronal car- inhibition of demineralization and matic degradation of the root collagen
ies, is based on modification of enhancement of remineralization. matrix (168). A synergistic effect with
harmful dietary habits, inhibition of Topical fluoride treatments may be fluoride has been speculated, but fur-
demineralization, promotion of remin- indicated, especially in patients with ther studies are needed to deepen the
eralization and reduction of the cario- reduced salivary flow or impaired self- knowledge about this promising natu-
genic dental biofilm (155). performed oral hygiene ability (162), ral agent.
The high consumption of low molec- but higher fluoride concentrations Moreover, as already underlined, it
ular weight carbohydrates, especially in seem to be required for remineraliza- is essential to motivate the patient to
industrialized countries, appears to be tion of RC in comparison with coro- perform satisfactory oral hygiene rou-
strongly implicated in the observed nal caries (163). There are several tines and attend regular dental check-
high caries prevalence, as organic acids options available, such as daily ups, as a good standard of oral hygiene
resulting from the anaerobic metabo- 5000 ppm sodium fluoride toothpaste is a necessary condition in any caries
lism of fermentable dietary sugars is or 0.025–0.1% fluoride mouth rinses, prevention program, but especially
the main cause of demineralization and neutral 1.2% sodium fluoride gel (in a when addressing RC prevention (170)
cavity development (91). Accordingly, 5-min tray), as well as sodium fluoride in the periodontal patient. Focusing on
patient education regarding diet, i.e. or silver diamine fluoride varnishes patients with a history of periodontal
avoiding high-sugar containing foods applied on to the exposed root sur- disease and therapy, typically exhibit-
and snacks and limiting the frequency faces three to four times a year; ing generalized CAL and numerous
of sugar intake, should be an essential finally, fluoride tablets, chewing gum, tooth surfaces with GR, the resulting
component of a caries prevention toothpick and flossing have been anatomical complications must be
154 Bignozzi et al.

considered a nonmodifiable risk factor; involvement. Therefore, clinical stud- (192). Tal et al. (193) considered in a
however, the patient’s motivation to ies focusing on the periodontal man- beagle dog model class V cavities pre-
achieve a high standard of oral hygiene, agement of GR in this class of pared so that the apical margin was
along with close monitoring of at-risk patients are warranted. Given the pro- in close spatial relationship with the
sites, integrated with the patient’s peri- gressing aging of the population, such alveolar crest (test) and other cavities
odontal maintenance program, may be studies will be particularly applicable not exceeding the CEJ (control). All
useful in preventing RC occurrence to periodontal practice. cavities were restored and, at 1 year
(171). Antimicrobial agents, such as following treatment, GR and bone
chlorhexidine, have been investigated loss were significantly greater at test
Restorative therapeutic approaches
as additional tools in reducing cario- sites in comparison with controls.
genic oral biofilm (172), but – specifi- The potential consequences of both More recently, G€ unay et al. (194)
cally considering RC prevention – the RC and NCCL, e.g. dental pulp and/ reported increased inflammatory
current lack of evidence on long-term or marginal periodontal tissue involve- parameters and periodontal attach-
clinical outcomes and ascertained side ment, hypersensitivity and compro- ment loss at prosthetic restorative
effects makes chlorhexidine devoid of mised aesthetics, demand a timely and margins placed in proximity of the
any added clinical benefit compared to comprehensive therapeutic approach bone crest, i.e. within the biologic
conventional and well-established for each lesion. Such a site-specific width. There is general agreement in
preventive measures, i.e. diet modifica- approach may include the use of res- recommending that when RC extends
tion, fluoride delivery and improved torations (Fig. 3). Glass ionomer, below the gingival margin the restora-
oral hygiene (173). In patients with resin-modified glass ionomer, resin tion must be preceded by, or be part
impaired salivary gland function, due composite, fluoride-containing resin of, a crown lengthening procedure
to aging, radiotherapy, diseases or composite or compomer restorations (Fig. 4) to re-establish a proper bio-
medications, the administration of sali- may be recommended based on indi- logic width apical to the proposed res-
vary substitutes to buffer the acidic vidual patient risk (187). In this con- toration margin (195).
environment and inhibit adhesion and text, it should be emphasized that
growth of bacteria might also be of unique aspects of the tooth cervical
Root caries: a risk factor for
help (174,175). area, i.e. less than ideal characteristics
tooth loss after periodontal
The general preventive measures as adhesion substrate (188), concentra-
therapy
considered above are useful and effec- tion of biomechanical stress (189),
tive in preventing RC by reducing the spatial relationship with the marginal From a periodontal perspective RC is
impact of risk factors throughout the periodontium and difficulties in access significant not only because periodon-
oral cavity. In addition to general pre- and field isolation, may render chal- tal disease (attachment loss) and ther-
vention, it is possible to implement lenging the achievement of perfect apy lead to conditions (i.e. GR) that
site-specific measures that, from a marginal seal and long-term success of favor RC development, as outlined in
periodontal standpoint, could repre- composite restorations used to treat the previous paragraphs, but also
sent an important clinical strategy to RC. However, as restorative issues are because RC can be a leading factor
prevent and arrest RC (176–178). not the focus of this review, the reader compromising the long-term outcomes
Whenever possible, the ideal site- is referred to specific sources on this of definitive periodontal therapy. Lon-
specific approach to RC prevention in topic (154,190). gitudinal studies have shown that in
GR cases, with or without initial RC cases of advanced periodontal disease,
or NCCL, is the restitutio ad integrum where resective therapeutic approaches
Periodontal therapeutic approaches
of the root–periodontium complex (such as osseous surgery combined
(102). Complete root coverage will Deep RC may occur, involving deep with root amputation, hemisection or
significantly diminish, if not eliminate, layers of dentin and/or affecting the tunneling procedures) have been
the possibility of RC development root at a more apical level than the employed, it is not uncommon for the
and progression for the specific site. cervical area or the marginal gingiva. initially successful therapeutic out-
State of the art of root coverage peri- In such cases, the maximum apical come to be compromised long-term,
odontal techniques have been the sub- extension of RC should be carefully primarily because of complications
ject of several clinical trials (179–183) considered to achieve complete other than periodontal ones, and espe-
and systematic reviews (184–186). removal of the decayed tissue and cially because of RC (196). In this
Although great progress has been proper cavity restoration. RC that regard, several authors reported RC
made in the surgical treatment of GR, extends below the gingival margin occurrence to account for 7.9% (202)
and the available techniques show may impinge on the biologic width to 25% (203), and up to 50% (204) of
excellent results (185,186), it must be and interfere with the gingival attach- the nonsalvageable complications
emphasized that most, if not all, of ment apparatus (191). leading to tooth extraction.
the published studies have not consid- A deeply placed restorative margin, The frequency of periodontally
ered specifically the patient with a his- violating the biologic width, will involved teeth treated by resective sur-
tory of inflammatory periodontal result in loss of periodontal support gery and subsequently condemned
Root caries: a periodontal perspective 155

A B dexterity and altered oral anatomical


structures, which can hinder the
performance of proper oral hygiene.
Senescence is also associated with
reduced salivary flow, because of age-
related structural salivary gland
changes (199,200) or functional impair
ment induced by various systemic dis-
orders and medications. Hyposaliva-
tion is a debilitating condition that can
C D potentially induce difficulty in chewing
and speaking, as well as taste loss, dys-
phagia, and increased incidence of den-
tal caries and soft tissue pathologies
(201,202). Furthermore, other factors
can also contribute to deficiencies in
the structural integrity of teeth in
elderly people through an incremental
effect over the years: dietary acid
exposure, oral parafunctional habits,
E F occlusal trauma, attrition, abrasion
from toothpastes or powders, erosion
by alteration of oral pH due to medi-
cations or gastro-esophageal reflux
(145).
Consistently, the prevalence of RC
in adults has been shown to progres-
sively increase with age (203–205).
The 1988–1991 NHANES III national
G H survey (203) provided evidence for
RC prevalence among nearly 6726
people; 55.9% of patients aged
 75 years had one or more RC
lesions, with severity being age-
dependent. The NHANES III study
established that, past the age of
34 years, the expected probability for
a person of having one or more
decayed or filled root surface will be
Fig. 3. Root caries occurrence in patient with periodontitis treated with resective surgery 20–22% less than his age. This means
and root amputation; clinical view at baseline (A) and at 3 mo (B), 2 years (C), 3 years that for a person aged 65 years, a 43–
(D) and 6 years (E, F) postoperatively. Recommended restorative procedure was per- 45% probability of having one or
formed (G, H) following the long-awaited patient consent. more RC may be assumed.
More recently, different prevalence
because of RC suggests that patients free of RC and retain the function rates in the elderly have been reported
with periodontitis who are candidates of his/her periodontally treated denti- in the literature, ranging from 28.4%
for osseous surgery must undergo a tion. to 96.5% (12,13,206–210). This wide
stringent assessment for all endodon- range of RC prevalence probably
tics, prosthetic and periodontal prog- reflects the highly diverse ethnic, cul-
Root caries and periodontal
nostic factors before implementing tural and social background of the
issues in the elderly
such a treatment approach (197). populations examined in the afore-
Ultimately, the level of patient com- Longer life expectancy and decreased mentioned studies; such differences
pliance and feasibility of an adequate edentulism result in an ever-increasing are likely to represent different dietary
maintenance program, in conjunction number of elderly patients retaining habits, standards of oral hygiene, and
with an individualized caries preven- their natural dentition in advanced age other relevant parameters, such as
tion protocol during follow-up, will and being in need of special dental ser- availability of water fluoridation,
allow the patient who received resec- vices (198). Aging is associated with community-dwelling or institutional-
tive periodontal therapy to remain changes, such as reduced manual ized subjects, and urban or rural
156 Bignozzi et al.

A B mainly on studies of young and mid-


dle-aged adults. Bacterial species other
than those commonly found have been
isolated in RC lesions of elderly
patients (214), suggesting that the
putative RC etiologic agents in older
adults belong to microbial communi-
ties more complex than previously
presumed (44,87). Recently Preza
et al. (215), using an rRNA-based,
C D culture-independent, microarray tech-
nique in a sample of 41 patients aged
70 or older, did not find specific
strains to be consistently associated
with RC, suggesting the possibility of
a certain degree of intersubject vari-
ability regarding RC bacterial etiology
in this age-specific setting and the need
for additional research. Moreover,
although the caries process is endemic
Fig. 4. Root caries under fixed dental prosthesis; note the extension of the carious lesion in the elderly and more than 50% of
apical to the gingival margin. Clinical view at initial presentation (A), during crown all individuals retaining their dentition
lengthening surgery (B), intraoperative restoration application (C), and 3 mo postopera- after age 65 have at least one RC
tively (D). lesion (205,216,217), clustering has
been observed so that only a third of
inhabitants. Nevertheless, it is clear tion for this approach, which – when the older adults account for the
that RC in the elderly is a problem used in older adults – seems to provide majority of RC cases (218–220); the
with a global impact. In older adults clinical outcomes similar to those latter observation suggests the possible
it is not unusual to find RC, espe- obtained in younger patients (140). contribution of yet unknown genetic
cially at the margin of previous pros- However, careful consideration con- factors (90). Specifically focusing on
thetic restorations, which often extend cerning the advisability of performing patients with periodontitis, the inte-
below the gingival margin. resective surgery in the elderly patient is nse protein-degrading activity found
Increased RC susceptibility of the necessary (211). Considering the docu- at RC-affected and periodontally
elderly may be due to age-specific mented increased RC risk with advanc- involved sites may suggest the possi-
behavioral and socio-demographic ing age (41,69,80) and greater GR bility of a special role for protein-
characteristics, as mentioned above. (79,97,99), the overall therapeutic degrading and protein-coagulating
However, from a clinical point of view, advantage of radical surgical pocket bacterial strains in the onset and pro-
the main local factor that may be asso- elimination should be carefully weighed gression of RC (56). This putative
ciated with increased RC prevalence is in the context of the overall dental pathogenic mechanism deserves fur-
root surfaces becoming exposed simply health management of the older adult. ther investigation, with special empha-
due to aging or progressive periodontal As previously mentioned, furcation- sis on the elderly.
disease (41,69). Coherently, in peri- involved molars treated with flap sur- Other special issues of RC in the
odontal patients the estimated RC risk gery and root resection are prone to aging patient should be considered as
profile appears correlated with a the development of a series of compli- well. RC diagnosis in elderly people
number of predisposing factors but cations, including RC (197,212,213). may be complicated by the necessity to
as reported above, the prevalence It is reasonable to assume that in perform examinations under nonideal
increases with the amount of CAL and elderly populations the coexistence of clinical settings (221) and the reduced
with advancing age (108). A correlation several predisposing factors, such as ability to maintain a good standard of
with advanced age recurs also in stud- hyposalivation or impaired manual oral hygiene, resulting in greater bac-
ies, including periodontally involved dexterity may result in increased post- terial biofilm accumulation [Correction
patients receiving long-term supportive operative RC incidence; nevertheless, added on 20 May 2013, after first
periodontal therapy (10,80,128,129). In targeted studies on age-specific popu- online publication: The phrase ‘result-
this regard, the cumulative effect over lations, which may corroborate this ing in greater plaque deposits’ has been
time of repeated professional root assumption, are still lacking (196). corrected to ‘resulting in greater bac-
instrumentation procedures should be Similarly, knowledge on some other terial biofilm accumulation’.] on the
considered. issues regarding RC in the elderly is root surfaces (222). Such diagnostic
With respect to resective periodontal still scarce. Current models of RC difficulties lessen the reliability of the
surgery, age per se is not a contraindica- microbiological etiology are based reported epidemiological data in the
Root caries: a periodontal perspective 157

age-specific populations and, more well established, it appears that impli- role of RC in compromising the long-
importantly, may result in inadequate cations of the interrelationship term survival of the dentition of peri-
patient care. between these two clinical entities have odontal patients. RC appears to be
As regards prevention, a good stan- not been routinely considered in the an underestimated clinical problem,
dard of oral hygiene may be a chal- course of RC investigations. Despite despite its high prevalence and contri-
lenge for the elderly, because of the fact that GR and, in general, peri- bution to tooth loss in this patient
physical and mental disabilities. odontal attachment loss are biological population. The exposure of root sur-
Changes in dietary habits and gravita- factors essential for RC onset and pro- faces to the oral environment due to
tion towards softer foods rich in sim- gression, often these variables are not aging, i.e. progressive GR, makes
ple sugars – typical of the elderly investigated in the proposed risk mod- them prone to carious involvement.
population – may complicate further els (78). The inclusion of these param- The risk of RC in patients with a his-
prevention efforts. Therefore, elderly eters in future investigations should tory of periodontitis and resective sur-
patients need to receive adequate help determine further the significance gery, especially in multi-rooted teeth,
motivation and support for the neces- of the periodontal component in RC is of particular concern. Therefore,
sary changes in diet, with particular pathophysiology. general preventive measures such as
emphasis on the frequency of ferment- Despite the recognition of the signif- noncariogenic diet and fluoride appli-
able carbohydrate ingestion and the icance of RC prevention protocols as cation together with plaque control,
possible replacement with noncario- integral parts of a periodontal mainte- must be regarded as mandatory com-
genic sweeteners (161). Moreover, nance program (80,225), it appears ponents of any periodontal mainte-
instructions to maintain the best pos- that RC prevention is commonly not nance program. Careful assessment of
sible plaque control using electric or given due weight and importance dur- each individual case is needed to out-
manual toothbrush, floss, interdental ing periodontal supportive therapy line a patient-centered comprehensive
brush and adjuvants such as chlorhex- (226). Given that high patient compli- preventive and therapeutic approach
idine and fluoride mouthwashes, and ance with periodontal maintenance has for RC lesions. The high prevalence
fluoride or anti-plaque dentifrices been shown to result in protection of periodontitis in older adults,
(223) should be provided, especially in from further attachment loss and the increasing life expectancy and decreas-
elderly patients with a history of peri- onset of new RC (227), a fact that ing edentulism of the population, and
odontal involvement. Unfortunately, underscores again the interrelationship apparent coexistence of RC with
other age-specific socio-demographic between the two conditions, it is evi- advanced age and periodontitis, col-
characteristics, such as institutionali- dent that periodontists, hygienists or lectively suggest that RC could
zation, lower socio-economic status other oral healthcare providers respon- become an increasingly frequent chal-
and age-related cognitive decline, may sible for periodontal maintenance, can lenge for periodontal care providers.
severely impair effective patient com- play a key role in RC prevention. From this standpoint, future studies
munication or essentially curtail the Specifically emerging from this are needed to address special diagnos-
patient’s ability to comply with peri- review, future research should assess tic, preventive and therapeutic mea-
odontal maintenance. provider awareness about the impact sures to best meet the needs of the
In conclusion, advanced age, peri- of RC as a risk factor for further elderly periodontal patient.
odontitis and RC are a triad of condi- tooth loss in periodontally compro-
tions frequently interrelated. The mised patients of advanced age, with
Acknowledgements
recent epidemiological data indicating the inevitable consequences of edentu-
that moderate or severe periodontitis lism and reduced quality of life. Clini- We gratefully acknowledge Dr Luca
affects 64% of adults aged  65 years cal studies regarding the effect of Landi and Dr Takuichi Sato for the
in the United States (224) underscores specific RC prevention protocols – scientific material provided.
the relevance of periodontal disease for possibly based on targeted check-ups,
the older adult. Therefore, future stud- dietary advice, improved oral hygiene
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