Association between coronal caries and malocclusion in an adult population

Purpose Only a few but conflicting results have been reported on the association between malocclusions and caries. We investigated this association using data from the population-based cross-sectional Study of Health in Pomerania (SHIP). Methods Sagittal, vertical and transversal intermaxillary relationship, space conditions and sociodemographic parameters of 1210 dentate subjects (median age 30 years, interquartile range 25–35 years) were collected. Caries was assessed with the Decayed-Missing-Filled Surfaces index but analyzed as ordered outcome (four levels: sound, enamel caries, caries, tooth loss) in ordinal multilevel models, taking into account subject, jaw, and tooth level simultaneously. Results Anterior open bite ≤3 mm (odds ratio [OR] = 2.08, 95% confidence interval [CI]: 1.19–3.61), increased sagittal overjet of 4–6 mm (OR = 1.31, CI: 1.05–1.64), distal occlusion of ½ premolar width (OR = 1.27, CI: 1.05–1.53) and distal 1 premolar width (OR = 1.31, CI: 1.06–1.63) were associated with adjusted increased odds for a higher outcome level (caries). Anterior spacing (OR = 0.24, CI: 0.17–0.33), posterior spacing, (OR = 0.69, CI: 0.5–0.95), posterior crowding (OR = 0.57, CI: 0.49–0.66) and buccal nonocclusion (OR = 0.54, CI: 0.33–0.87) were associated with a lower outcome level (caries). Conclusion The results from this population-based study suggest that a connection between caries and malocclusion exists to a limited extent in young adults. The associations with caries are contradictory for several malocclusion variables. Distal occlusion (OR = 1.31, CI: 1.06–1.63) and related skeletal anomalies displayed positive associations with caries whereas crowding did not. Orthodontic treatment of anterior crowding would probably not interfere with caries experience. These aspects should be considered for patient information and in treatment decisions.


Introduction
Proper alignment and function of teeth as well as neutral occlusion are primary goals of orthodontic treatment. This should lead to an appealing aesthetic appearance, ensure chewing efficiency and last but not least, has been proposed to be associated with periodontal and dental health [3]. There has been a long-lasting debate about the impact of malocclusion on the progression of caries and periodontal disease [23,24]. Although an association between malocclusion and periodontitis was established and does not seem to be negligible [4], periodontal health after orthodontic treatment does not seem to improve [6]. Regarding caries, the association with malocclusion seems to be even smaller [12].
Conflicting data have been reported in the past as to whether dental crowding increases caries scores [20]. Some studies reported higher interproximal caries prevalence, whereas others did not. Most of the studies focused on anterior teeth [2]. Differences in caries risk were also found between the upper and lower jaws [20]. Regarding caries, results from intervention studies are also heterogeneous [5,12]. A recent publication on caries prevalence and former orthodontic treatment on 448 Australians at the age of 30 years did not provide any measurable benefits from orthodontic treatment with respect to improved den-tal health later in life [12]. No distinction was made in that study, however, for different forms of malocclusion, which was established with the Dental Aesthetic Index and orthodontic treatment had been performed mainly to resolve aesthetic problems [12]. In a retrospective German evaluation, 75 former Angle class II patients seemed to benefit from orthodontic treatment based on Decayed-Missing-Filled Surfaces (DMFS) values when compared to a population-based age cohort [5].
In contrast to crowding, much less is known about the relationship between overjet, overbite, crossbite, and spacing to caries. Studies in primary and mixed dentitions delivered inconsistent results [15,19,35,40]. In an early study, Helm and Petersen considered different forms of malocclusion but did not find any association with caries prevalence in an adult sample [23].
To the best of our knowledge, there are no epidemiological data on the association between caries and the different forms of malocclusion including sagittal intermaxillary relationships in an adult population. Thus, we aimed to analyze cross-sectional data from the Study of Health of Pomerania (SHIP) to assess the association between caries prevalence and various forms of malocclusion in a statistical model on tooth, jaw and subject levels.
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Study participants
The aim of the population-based SHIP was to estimate the prevalence of a broad range of diseases, risk factors, and health-related factors for the Northeast German population. The baseline examination SHIP-0, whose sampling method was adopted from the World Health Organization MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Project in Augsburg, Germany, was approved by the local ethics committee and performed between 1997 and 2001 [28]. The net sample (without migrated or deceased subjects) comprised 6265 subjects with an age range from 20 to 79 years. Finally, 4308 subjects-all were Caucasian-gave written, informed consent and participated in SHIP-0, which corresponded to a response rate of 68.8%. SHIP-0 comprised a medical examination, a clinical dental examination (including periodontal, orthodontic, functional, and cariologic components), an interview, and a questionnaire completed by each participant [26,28].

Assessment of malocclusion
The occlusal status was assessed according to selected occlusal parameters including the sagittal intermaxillary relationship in the canine region. This relationship was registered separately for the right and left canine regions and determined as neutral, distal by the width of ½ premolar and 1 premolar, and mesial by at least a ½ premolar width [25]. The following signs were recorded as being either present or absent: frontal and lateral crowding, ectopic position of canines, widely spaced teeth without approximal tooth contact, frontal and lateral crossbite, buccal nonocclusion, excessive overjet and overbite, edge-to-edge bite, open bite, negative overjet and retruded position of maxillary incisors. Orthodontic status was not recordable when in 2 or more sextants of the dentition (2 anterior and 4 posterior tooth regions), 3 or more teeth per sextant were missing, regardless of whether the gaps were restored or not. Third molars were not included in the evaluation.

Dental examination
According to the WHO recommendations [42], coronal caries findings (cavitated carious defects into the enamel and dentine), fillings, secondary caries on the surface level, and missing teeth, were registered by surface with the exception of third molars according to the half-mouth method (quadrants 1 and 4, or quadrants 2 and 3 in alternating sequence) using a periodontal probe (PCP 11, Hu Friedy, Frankfurt am Main, Germany) [26,39]. Cavitated carious lesions (D component) were subdivided into lesions confined to enamel and those involving dentine. The number of cavitated lesion solely in enamel was absolutely minimal (n = 72). Initial caries lesions without cavitation were not recorded or counted for the caries scores. In detail, caries was defined in the manual of SHIP-0 as follows: and crowns 5. Secondary caries: visible or detectable caries at the margin of fillings 6. Missing: all missing teeth except third molars 7. Others: missing anterior teeth due to trauma, missing premolars due to orthodontic treatment, crowns due to trauma (probands were ask for the reason of tooth loss), persistent teeth of the first dentition This was the basis for the calculation of the DMFS index to characterize the SHIP sample in Tables 1 and 2, and to analyze the data using four ordered outcome levels on tooth level as described in more detail in the statistical analyses section.
Visual inspection and probing with the dental probe PCP11 determined the presence or absence of plaque and calculus on test teeth 1, 3, and 6 in the selected quadrants, and the proportion of sites with plaque was calculated per participant. If a test tooth was missing, the distal adjacent tooth was examined instead. Each of these teeth was scored at four sites: distobuccal, midbuccal, mesiobuccal, midlingual.

Quality control
Eight experienced and calibrated dentists performed the dental examinations. Training of examiners and consensus discussions were carried out before the study started and training/calibration sessions were repeated twice yearly while the study was ongoing. Orthodontic calibration of the examiners was based on the examination of 30 pairs of casts showing complex symptoms of malocclusion, examination was repeated after several days. Intra-and interexaminer agreement were measured by Cohen's kappa (κ) [25,26]. Cohen's κ values ranged from 0.66-0.81, meaning "good agreement" [41]. The calibration exercises for the caries scores consisted of each examiner performing two examinations on each of 10 and 5 test participants one to two weeks apart. Examiners applied the eight categories for caries as described in the manual for SHIP-0. On surface level, which was the basis for calibration and certification, very good Cohen's κ values were reached for intra-and interexaminer reliability (0.9-1.0 and 0.93-0.96, respectively [26,39]). On the tooth level as used herein, good κ values were reached for intra-and interexaminer reliability (0.69-1.0 and 0.70-1.0, respectively).

Statistical analyses
To avoid selection bias, subject's age range was restricted to 20-39 years; older subjects have a higher proportion of missing orthodontic variables due to missing teeth. As shown for the relationship between malocclusion and periodontal disease [4], confounding by tooth type across jaws required modelling on subject, jaw, and tooth levels. As is common in multilevel analyses [16], the outcome (caries) is measured on the tooth level, whereas some covariates are at the subject level, for example gender, and other covariates are at the tooth level, including all malocclusion variables except distal and mesial occlusion [4]. Thus, the 33 malocclusion variables on the subject level were transformed into 18 corresponding variables on the tooth level [4]. Thus, ectopic canines on the tooth level could occur only at 13, 23, 33, or 43 [4]. For crowding (and spacing as well), a single variable instead of two variables for anterior and posterior regions may be desirable. We addressed this coding scheme only in sensitivity analyses because the six joint tests for the global malocclusion conditions, including space conditions in the anterior region and lateral malocclusions, were clearly of clinical and statistical interest. Moreover, crowding was assessed differently in the anterior and posterior regions. The malocclusion variables were simultaneously fitted in ordinal logistic multilevel models using the "meologit" procedure (Stata software, release 14.2; Stata Corporation, College Station, TX, USA). The four ordered outcome levels were (1) sound, (2) carious defects into the enamel, (3) caries (dentine caries ≤3 mm, dentine caries >3 mm, filling, or secondary caries), and (4) tooth loss. Because pitfalls of ignoring the hierarchy in dental research (subject, tooth, surface; subject, jaw, tooth) have been well-known for 20 years [17], multilevel models have been widely used for answering complex research questions, especially when the tooth type is a confounder on a level different from the subject level [4,18]. Herein, the three hierarchical levels subject, jaw, and tooth were included as random effects [36]; age, gender, school education (3 levels in accordance with the former east German   IQR interquartile range school system), marital status (5 categories), jaw, tooth type (7 levels), the interaction between jaw and tooth type [21], and monthly household equivalence income (1 C = 1.956 German marks) were included as fixed effects [30]. Restricted cubic splines with three knots were used to allow for departures from linearity for age and income. Income was considered only in additional analyses because, unlike school education, it was linked with adulthood rather than childhood and, therefore, not assumed to be a confounder.
As orthodontic treatment is part of the effect to be studied, it was not included into the model because "a confounder must not be an effect of the exposure" [37]. Odds ratios (OR) with 95% confidence intervals (CI) and p-values are provided. For any cut point of the outcome on four lev-els, ORs in ordinal logistic regression models can be interpreted as those in binary logistic regression models; note that the ordinal logistic regression model has fewer assumptions than the ordinary least squares regression model [22].

Results
The analysis sample consisted of 1210 participants with a median age of 30 years (interquartile range [IQR] 25-35 years). Of these patients, 30% had previously undergone orthodontic treatment. Four patients (<0.5%) were under treatment at the time of examination. (Fig. 1). The median DMFT half mouth was 7 (IQR 5-9 teeth). Partici-  Table 1. Notably, the difference in plaque was very small comparing never and former orthodontic treatment (median: 40 and 38%, respectively). The orthodontic characteristics are shown in Table 2. The most common malocclusion was anterior crowding of the lower jaw in 766 of the 1210 subjects. Lateral open bite was observed in 12 subjects and was the least common malocclusion. According to intermaxillary relationships in the canine area, 44.3% of the subjects showed a neutral occlusion on both sides. Table 3 displays malocclusion in relation to orthodontic treatment for nontreated participants and participants who had previously undergone orthodontic treatment.

Caries model
On the tooth level, the following malocclusions were associated with an increased odds ratio for caries, or more exactly, for tooth loss versus no tooth loos; or tooth loss or caries versus no caries; or tooth loss, caries, or enamel caries versus sound (     Table 4), space conditions in the posterior region (p < 0.0001), vertical overbite (p = 0.0412), sagittal overjet (p = 0.0325), lateral malocclusions (p = 0.0051), and sagittal intermaxillary relationship in the canine region (p = 0.0200). The joint effect for increased sagittal overjet and distal oc-clusion, which were correlated, was statistically significant (p = 0.0011 for the global test with 4 degrees of freedom).

Sensitivity analyses using a single variable for crowding and spacing, respectively
Whereas anterior and posterior spacing can be combined into a single spacing variable in a natural way, posterior crowding can be combined with different levels of anterior crowding. Counting posterior crowding as the lowest level of the presence of anterior crowding, the ORs were 0.65 (95% CI: 0.58-0.74; p < 0.0001), 0.64 (95% CI: 0.43-0.95; p < 0.0255), and 0.60 (95% CI: 0.17-2.14; p = 0.4348) from the lowest to the highest crowding level, respectively. The K OR of spacing was 0.38 (95% CI: 0.30-0.48; p < 0.0001). Counting posterior crowding as the middle level of anterior crowding, the OR of the middle level was 0.56 (95% CI: 0.49-0.65; p < 0.0001). Of note, the 95% CIs for anterior and posterior spacing did not overlap in the main analysis (Table 4).

Sensitivity analyses including household income
Including household income did not lead to a change >10% in the ORs of malocclusion variables in the reduced sample of 1171 subjects.

Discussion
Capitalizing on a large sample size from the general population, this is the first study to investigate the association between malocclusions and caries on tooth, jaw and subject levels in adults in a single model. The benefit of orthodontic treatment on oral health including caries prevention is a matter of ongoing debate in the literature as well as in political demands for scientific proof [2,5,8,12]. The extensive dataset of SHIP enables analyses with multilevel Hier steht eine Anzeige. K models that consider the nested character of the data (tooth level under consideration of the jaw and subject level) [36]. Such extensive analyses including all forms of malocclusion have not been possible in the past.
Although a marked decline in caries has been noticed during the last 30 years in Western countries, caries still represents a relevant dental problem [29,38,39]. DMFT values of our subsample are not comparable to other population-based surveys due to the selection criteria described above. Caries prevalence of the sample from SHIP, which has been published previously, is higher compared to other nationwide data from Western European countries in the same decade [27,31,38,39]. Higher numbers of filled and missing teeth in seniors compared to Swedish and US surveys may be based on limited caries prevention programs or unavailability of fluoridated tooth paste before 1989 [39]. DMFT values in the comparable age group of the 35-44 year olds are slightly elevated compared to a German nationwide survey, which was conducted in 2005 [39,43]. The Fourth German Health Study also reported elevated values for the former East Germany [43].
Beside socioeconomic or cohort effects, several local factors such as improper tooth alignment have also been connected to an increased caries prevalence [1]. Although Fig. 2 Stacked bar chart of sound, enamel caries, dentine carious/ filled/secondary caries, and missing teeth according to tooth type and jaw (half mouth). "Other" includes missing due to trauma or due to orthodontic extraction. Differences between jaws regarding sound teeth justify the level "jaw" in the analysis Abb. 2 Balkendiagramm für gesunde Zähne, Zähne mit Schmelzkaries, kariöse und gefüllte Zähne, Zähne mit sekundärer Karies sowie fehlende Zähne geordnet nach Zahntyp und Kiefer (halbseitig). "Sonstige" umfasst das Fehlen von Zähnen aufgrund von Traumata oder kieferorthopädischen Extraktionen. Unterschiede zwischen Ober-und Unterkiefer in Bezug auf gesunde Zähne rechtfertigen die Ebene "Kiefer" in der Analyse policy makers have long demanded for a causal relationship between different forms of malocclusion and caries, these associations have been only insufficiently investigated [1,7].
Our analyses resulted in a heterogeneous picture with some positive and also inverse associations between malocclusion and caries which have not been investigated in detail before. We observed positive associations for caries and increased sagittal overjet, anterior open bite and distal occlusion. These associations have not been reported previously in adult samples of epidemiologic surveys. In spite of statistical significance, the strength of the association remained moderate. Just anterior open bite up to 3 mm displayed an OR of 2. It occurred, however, in only 0.8% of the relevant teeth. In adolescents, however, this association was previously reported. Reduced salivary flow and a mouth breathing habit may have enhanced susceptibility to dental caries [33]. In one of the few studies on adults that also included maxillary overjet, Helm and Petersen did not find associations of any malocclusion variable with caries incidence [23]. In pediatric epidemiological samples, an association to increased overjet and open bite could be established at least for the mixed dentition [33,40]. Whereas the study by Stahl and Grabowski displayed that mandibular overjet was associated with higher caries incidence, high plaque scores were found in 12-yearold children with extreme maxillary overjet. The authors assumed a more difficult tooth cleaning and prolonged plaque accumulation in these cases that might lead to higher caries values [11]. In a study by Feldens et al. on 509 Brazilian adolescents, higher caries scores were associated with handicapping malocclusion, maxillary irregularity and abnormal molar relationships. The authors also speculated that prolonged biofilm formation might have increased the caries risk [13].
Some studies that found an association between malocclusion and caries did not distinguish between malocclusion traits but used sum scores or indices [7,14,15], whereas several other studies did not confirm an increased risk [10,12,44]. An aspect to recognize here is the age differences between the studied populations, i.e., caries had a longer course to develop in adult subjects with certain malocclusion traits compared to the pediatric and adolescent populations with the same traits, where mixed or permanent dentitions in the latter had shorter periods of exposure to caries-inducing factors.
Crowding of the anterior or posterior teeth was not associated with an increased caries score. Posterior crowding was even significantly associated with lower caries prevalence, a result which has also been observed previously [20]. Our results strengthen the assumption that despite the irregular tooth alignment and potential plaque accumulation, these factors do not necessarily lead to a higher caries rate [2,23]. Our study followed the recommendations by Hafez et al. who did not confirm or refute a causal relationship between crowding and dental caries [20]. Until 2011, they found only eight reliable studies on that topic and claimed that well-controlled studies with larger sample sizes with standardized diagnostic tools would be necessary to resolve the question. Finally, the only plausible hypothesis on the link between malocclusion and caries that focus on plaque accumulation was also rejected in our large sample study.
We found inverse associations between caries and malocclusions as anterior and posterior spacing as well as posterior crowding and buccal nonocclusion, which were also observed in part by several studies in adolescents and adults [9,20]. Anterior and posterior spacing within the context of caries risk is assumed to play a protective role, as plaque removal would be easier to achieve with the absence of proximal contacts [32].
Traumatic events leading to increased caries values might also occur in persons with malocclusion as for instance increased sagittal overjet [34]. To avoid this influence, the examination in SHIP 0 did not count traumatic events and tooth loss due to trauma or orthodontic tooth extractions as missing teeth in assessing the DMFS. However, the caries risk was increased in persons with an overjet of more than 6 mm compared to an overjet of 4-6 mm. Furthermore, because periodontal disease that finally leads to tooth loss has been linked with increased sagittal overjet [4], we chose our sample within an age range of 20 to  For frequencies, each category is presented only if the variable (not the subgroup) has more than two levels. For variables on two levels, the frequency of the designated malocclusion category is presented; the frequency of the remaining category can be calculated (16,675 -frequency of the designated malocclusion category) Likewise, the frequency of the caries level "sound" can be calculated (sound = tooth frequency -(enamel caries + caries + tooth loss), for example, 5889 = 14,055 -(61 + 6915 + 1190) in the first row) 95% CI 95% confidence interval 39 years, to reduce the risk of complete tooth loss due to periodontal breakdown. Additional analyses (not shown) of our data on Decayed Filled Teeth (DFT) level resulted in lower OR values but yielded the same tendencies.
Our study has several strengths as the large sample size provided adequate statistical power. The target population was limited to ages within a certain range, reducing the risk of bias due to tooth loss or missing values. We performed a standardized data collection with a high degree of quality management, including calibration and certification of caries examiners on surface level. Clinical experience is reflected by modelling jaw differences in tooth types, which is important for incisors and canines. Moreover, tooth type is a key confounder for the relationship between malocclusion and caries, which can be dealt with in multilevel models as used herein, but not in classical regression models, which ignore the hierarchically structured data [16]. It is this hierarchical structure that can model caries and tooth loss on an ordinal scale, whereas this natural ordering is lost by using the DMFT in subject level analysis. Thus, the severe information loss accompanied with choosing DMFT and subject level analysis ignores basic principles in statistics-it is far from being the best "for the money".
Limitations are the cross-sectional analysis not allowing the establishment of causal relationships. A high prevalence of malocclusions was present in study participants who reported former orthodontic treatment. This was not unexpected since interviewing adult subjects about previous orthodontic treatments provides only orientational data. No information was given on orthodontic treatment length, applied methods and success rate [25].

Conclusion
The current results and reviews from the literature suggest that associations between caries and malocclusion depend on the kind of malformation. Anterior open bite (OR = 2.08, CI: 1.19-3.61), increased sagittal overjet (OR = 1.31, CI: 1.05-1.64) and distal occlusion (OR = 1.31, CI: 1.06-1.63) were positively associated with caries, whereas spacing, posterior crowing and buccal nonocclusion were negatively associated. Caries and malocclusion, however, were not far reaching associated. Anterior crowding was not associated with caries nor displayed higher plaque scores compared to no crowding. Causality of the detected associations have to be examined in longitudinal analyses.
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