Introduction

Periodontitis, an inflammatory disease primarily instigated by opportunistic bacteria, leads to the destruction of tooth-supporting structures, including the alveolar bone, cementum, and the periodontal ligament. As the disease progresses, loss of attachment occurs, potentially resulting in tooth loss if not promptly and effectively managed1.

The importance of early diagnosis of periodontal disease cannot be overstated. If not treated soon after its onset at an early age, rapid destruction of the periodontal apparatus may lead to the consequent spontaneous exfoliation of primary teeth without the normal root resorption process, or necessitate early extraction2. Furthermore, periodontitis in primary teeth not only threatens the integrity of these temporary teeth but also poses risks to the subsequent permanent dentition3,4,5.

Thus, precise and early diagnostic techniques are critical. They not only facilitate timely intervention but also mitigate risks associated with the natural progression of periodontal disease, which can lead to early tooth loss or complex dental procedures at a young age. Radiographic evaluation appears to provide essential information for diagnosing alveolar bone loss, a key feature of periodontal disease6. It is also indispensable for diagnosing other oral conditions, as bitewing radiographs are the primary tool for detecting carious lesions in both clinical practice and research7. In summary, radiographic evaluation is a fundamental component of dental examinations.

However, there is limited research on the prevalence of radiographic alveolar bone loss in deciduous dentition, an indicator that warrants further investigation. Furthermore, existing studies vary, indicating a need for further research on the prevalence of radiographic alveolar bone loss in primary dentition.8,9,10,11,12,13,14,15

The aim of this retrospective study was to evaluate the incidence of early alveolar bone loss in primary teeth among an Israeli pediatric population through radiographic analysis. Correlations between bone loss and factors such as age, gender, and dental history, including the presence of decay and restorations, were further examined. By exploring these relationships, another objective of this study was to enhance the understanding of early alveolar bone loss in primary dentition and its potential implications for long-term dental health.

Materials and methods

The present study was approved by the Tel Aviv University Institutional Review Board (IRB) (IEC No. 0001704-2) and all methods were performed in accordance with the relevant guidelines. The need for informed consent was waived by the Tel Aviv University IRB. Bitewing radiographs were collected from the clinical files of patients who attended the Department of Paediatric Dentistry at Tel Aviv University between 1999 and 2014 and were screened for early alveolar bone loss in deciduous teeth during the primary and mixed dentition stages. Inclusion criteria included patients born before 2002, clinical files containing bitewing radiographs taken before 2014, and patients aged 12 years or younger at the time the radiographs were taken. Radiographs presenting partially erupted teeth were excluded from the study. For each included patient, gender, age, and socioeconomic level were recorded. The latter was based on the socioeconomic grade (1-low level to 10-high level) of the residence, as defined by Israel’s Central Bureau of Statistics (CBS)16.

Radiographic analysis

Radiographs of all patients from the study population were captured using a Canon EOS 550D camera (Canon Inc., Tokyo, Japan) on a viewing box, alongside a millimeter ruler for standardization of measurements (Fig. 1). The images were then scanned into a computer and analyzed using ImageJ software (version 1.52a; ImageJ, RRID: SCR_003070). Calibration was conducted using the markings on the millimeter ruler.

Fig. 1
figure 1

Right bitewing radiograph analysis using a millimetric ruler on ImageJ software shows definite bone loss (≥ 2 mm) measurements, demonstrated as red lines (at the mesial surface of tooth 54 and at the distal surfaces of teeth 53 and 84).

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In order to assess alveolar bone loss, the distance from the CEJ to the alveolar bone crest was measured at both mesial and distal sites for all primary teeth. The number, corresponding jaw (upper or lower), and the distance from the CEJ to the alveolar bone crest at each site of all examined teeth were recorded. Sites with values of 2 mm or more were considered as having ‘definite’ bone loss13 (Fig. 1). Additionally, the presence of caries or any type of restoration (e.g., filling, crown, pulpotomy/pulpectomy) was recorded. Furthermore, differentiation between faulty and proper restorations was performed and documented.

Statistical analysis

Data were imported from the original dataset into SPSS version 27 for statistical analysis. Descriptive statistics, including frequencies, means, and standard deviations, were computed. Additionally, statistical analyses were conducted to test research hypotheses: independent samples t-tests, Pearson correlations for relationships between quantitative variables, Chi-square tests for independence to examine relationships between categorical variables, regression for predicting case outcomes, and One-Way ANOVA for testing differences between groups.

Furthermore, data integration was performed in Excel after SPSS analysis. Some results were transferred to Excel spreadsheets for further processing or graphical representation.

Results

General findings

Out of 2878 clinical records from individuals who attended the Department of Paediatric Dentistry at Tel Aviv University between 1999 and 2014, only 216 met the inclusion criteria. Of these, 120 records were deemed eligible for the study, as they included comprehensive data on age, gender, and socioeconomic status, along with satisfactory bitewing radiographs that allowed for measurements and analysis while excluding partially erupted teeth. Only the most recent radiographic images of each patient were assessed. Overall, radiographic measurements were carried out on 1,845 sites, in 1305 teeth. The study sample consisted of 69 males (57.7%) and 51 females (42.5%). The mean age of the participants was 7.36 ± 1.73 years. The mean age for females was 7.46 ± 1.61 years, while males appeared to be slightly younger, at 7.15 ± 1.86 years; however, these differences were not statistically significant (p = 0.4). The mean socioeconomic grade was 6.59 ± 2.21.

Radiographic bone related findings

The mean CEJ-bone crest radiographic distance (CBRD) on the distal aspect of maxillary canine 63 was found to be the most prominent at 1.88 ± 0.36 mm (range: 0.95–2.63 mm), while the minimal CBRD was found on the distal aspect site of the mandibular second primary molar 75, measuring 1.18 ± 0.43 mm. Mean CBRD at each site is presented in Table 1.

Table 1 Mean radiographic distance from the CEJ to the bone crest.
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Definite bone loss distribution

Sites that demonstrated CBRD greater than or equal to 2 mm were defined as definite bone loss sites. These definite bone loss sites were identified in 12.8% of the inspected teeth. Definite bone loss sites were more common in males than in females, occurring at rates of 13.5% and 11.9%, respectively; however, this difference was not significant (p = 0.563). Among the 120 participants, 63 were diagnosed with at least one definite bone loss site. Twenty-one participants had one definite bone loss site, although four participants had six sites or more (Table 2).

Table 2 The number of participants diagnosed with definite bone loss according to the number of affected sites.
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The tooth site with the highest incidence of definite bone loss was the left maxillary canine 63, with a 36% incidence rate, while no cases of definite bone loss were found in the mandibular canines (Fig. 2). Definite bone loss sites were significantly more frequent in the upper jaw, with a mean incidence rate of 1.35 ± 2.08 sites per jaw. In contrast, the mandible had a mean incidence rate of 0.41 ± 0.84 sites per jaw (p < 0.001).

Fig. 2
figure 2

Histogram demonstrating the incidence of definite bone loss according to tooth site.

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To examine whether there is a correlation between age and bone loss and to identify potential patterns of bone loss progression with age, definite bone loss was evaluated across three equally sized age groups: 6.8 years or younger, 6.9–8.3 years, and 8.4 years or older. The occurrence of definite bone loss in each age group increased gradually with age, from 11.9% in the youngest group to 13.8% and 15.9% in the older age groups, respectively. This pattern of definite bone loss occurrence had a weak, yet statistically significant, correlation with age (Pearson correlation, r = 0.1, p = 0.04). Moreover, it was also found that the severity of bone loss was weakly correlated with an increase in age, yet this too was statistically significant (Pearson’s correlation, r = 0.17, p = 0.04).

The occurrence of definite bone loss across different socioeconomic levels was examined by dividing the cohort according to their residence socioeconomic grade level (1–10). The highest incidence of definite bone loss was observed in the 9th socioeconomic level, at 17.9%, with a mean CBRD of 2.22 ± 0.11 mm, while the lowest incidence was found in the group at the 8th socioeconomic level, at 11%, with a mean CBRD of 2.35 ± 0.41 mm. The occurrence of definite bone loss across different socioeconomic levels is presented in Table 3. No significant correlation was found between socioeconomic level and definite bone loss incidence (Pearson’s correlation, r = 0.028, p = 0.545).

Table 3 The occurrence of definite bone loss across different socioeconomic levels.
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Crown condition related parameters

An intact crown was observed in 891 sites. Proper amalgam restorations were found in 394 sites. Radiographic diagnosis of caries lesions was found in 292 sites. The distribution of crown condition and the propriety of treatments are presented in Table 4.

Table 4 Distribution of crown conditions and appropriateness of treatments.
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Dental treatments were significantly more frequent in the lower jaw, with a mean incidence rate of 3.54 ± 3.72 sites per jaw, while in the maxilla, the mean incidence rate was 3.00 ± 3.69 sites per jaw (p < 0.005).

In the maxilla, the mean CBRD for treated sites was 1.64 ± 2.15 mm, significantly higher than the CBRD for untreated sites, which was 0.65 ± 1.73 mm (p < 0.05). This kind of correlation was not significant in the mandible or when both jaws were pooled together.

The number of dental treatments had a weak correlation with mean CBRD (Pearson’s correlation, r = 0.322, p < 0.05). Amalgam restorations, regardless of their propriety, had a weak correlation with CBRD (Pearson’s correlation, r = 0.24, p < 0.01). Similar findings were observed in crowned teeth, which presented a weak correlation with CBRD (Pearson’s correlation, r = 0.22, p < 0.05).

Definite bone loss incidence was found to have a moderate positive correlation with the number of treatments in the assessed teeth (Pearson’s correlation, r = 0.35, p < 0.01). When we examined the same correlation according to the different jaws, we found a moderate positive correlation between definite bone loss incidence in the upper jaw and the number of treatments (Pearson’s correlation, r = 0.44, p < 0.01). However, this pattern was not evident in both jaws, as no significant correlation was found between definite bone loss incidence in the lower jaw and the number of treatments.

Intervariable correlation

Linear regression analysis for CBRD in tooth site 53D revealed that definite bone loss prediction was statistically significant [F(3,12) = 3.63, p < 0.05]. The variance explained by age, gender, and socioeconomic level for definite bone loss in site 53D was 47.6%. Age was the only parameter that had a moderate positive correlation with CBRD in site 53D (r = 0.53, p < 0.05); as age increases, CBRD increases accordingly by 0.22 mm per year. Stepwise regression analysis for CBRD in tooth site 53D revealed that definite bone loss prediction was statistically significant [F(1,14) = 5.46, p < 0.05]. Age was the single contributing factor for 28.1% of the variance.

Discussion

According to the current study, the mean CBRD was highest at the distal aspect of the maxillary canine 63, measuring 1.88 ± 0.36 mm, and lowest at the distal aspect of the mandibular second primary molar 75, measuring 1.18 ± 0.43 mm. We speculate that the distal morphology of the canine, particularly its anatomical contour and the nature of its contact point with the adjacent tooth, might contribute to localized plaque accumulation or food impaction. These factors could, in turn, predispose this site to a higher risk of focal bone loss. Additionally, it is possible that mechanical forces during mastication or occlusion may concentrate stress on the distal aspect of the canine, further exacerbating bone resorption in this area. Further investigations would be needed to confirm these hypotheses. Additionally, definite bone loss, defined as a CBRD ≥ 2 mm, was observed in 12.8% of inspected sites, with the highest incidence at the left maxillary canine 63 (36%). The results seem to be in accordance with a study by Bimstein (2018), who conducted a radiographic evaluation of 29 children with primary or mixed dentition diagnosed with aggressive periodontitis (AgP)2. According to his study, the most prevalent definite bone loss site, which appeared in 89.8% of the children, was the distal aspect of maxillary canines. Other definite bone loss sites were also in the maxilla: the distal aspect of the first primary molar and the mesial aspect of the same tooth (83.9% and 83.3%, respectively). On the other hand, Miller et al. (2018), based on a study of 33 localized AgP African American children, demonstrated definite bone loss in 30 cases involving both first and second primary molars while only 1 case also affected a canine17. This difference in bone loss pattern can be explained by ethnic variances. In a Swedish study comparing 26 children with marginal bone loss in the primary dentition to 20 children in an equivalent matching control group, it was found that 27% of the children in the test group were of Asian origin18. This group of Asian children comprised an even higher portion of cases with 3 or more definite bone loss sites. In another study by the same group, comparing Vietnamese immigrant and Swedish age- and sex-matched children, it was found that 28% of the Vietnamese and 5% of the Swedish children, aged 4–11 years, had bone loss in their primary dentition19. In the current study of the Israeli pediatric population, 63 out of 120 participants (52.5%) were found to have at least one site with definite bone loss (CBRD ≥ 2 mm). To the best of our knowledge, this is the first study to evaluate bone loss in primary teeth within the Israeli pediatric population.

In the following studies, marginal alveolar bone loss has been found to affect the primary dentition of 5–11-year-olds with frequencies ranging from 0.9 to 4.5% of subjects8,9,10. However, in the study of Darby et al. (2005), which examined radiographs of 542 Australian children aged 5–12, the incidence of bone loss amounted to 13%11. Mainly, the second primary molars were affected, particularly in the distal aspect.

Several reasons may account for the wide differences between these studies, including genetic and methodological factors. Therefore, further investigation into the prevalence of early alveolar bone loss affecting the primary dentition and the implications for permanent teeth is required.

When it comes to diagnosing periodontal disease, and particularly bone loss, periodontal pocket probing has been found to be the most sensitive examination12. However, this may be difficult to perform effectively in primary, mixed, and erupting dentitions. Therefore, a radiographic measurement of the distance from the cemento-enamel junction (CEJ) to the alveolar bone crest has been suggested as a surrogate for assessing bone loss. Sjödin et al. (1992) reported that the physiological limit for this distance should be less than 2 mm13. Any measurement exceeding 2 mm might be suspected of indicating periodontal disease in primary dentition. Later publications found that the CEJ-alveolar bone radiographic distance varies between the upper and lower jaws and also tends to change with age14,15.

According to a systematic review and meta-analysis by Moghaddam et al. (2020), dental caries and periodontal diseases are associated with poor health-related quality of life in children20. In the current study, no significant correlation between socioeconomic level and the incidence of definite bone loss was found. With a mean socioeconomic grade of 6.59 ± 2.21, this may suggest that most of the eligible patients belonged to middle socioeconomic classes. The smaller differences in socioeconomic levels among Israeli children can be explained by the fact that since 2010, dental care for Israeli children has been provided free of charge by the public health system. According to Natapov et al. (2016), the reform in Israeli children’s dental care resulted in a marked increase in treatments and a significant decline in untreated dental disease21. Consequently, the ratio of treated to untreated teeth has increased. Since most of the eligible patients in the study were within a relatively homogeneous age range (mean age: 7.36 ± 1.73 years), the majority would qualify for inclusion in the reform.

In the current study, a significantly higher CBRD was found in maxillary treated teeth compared to untreated teeth. The number of dental treatments, amalgam restorations, and crowned teeth had weak correlations with the mean CBRD increase. The propriety of restorations did not affect CBRD. Moreover, definite bone loss incidence was found to have a moderate positive correlation with the number of treatments. Similar findings were reported by Albandar et al. (1995), who conducted a 3-year longitudinal study on 227 school children22. Their follow-up findings suggest that untreated caries lesions and both proper and defective dental restorations lead to the progression of periodontal support loss. A possible explanation for this phenomenon could be a plaque-induced inflammatory reaction. A study conducted on young adolescents, Swiss Army recruits, reported that Plaque Index and Gingival Index increased at restored sites, while the indices at non-filled sites remained relatively low23. Clinical attachment loss was associated with the presence of overhangs. Similar results were found by other studies focused on the effect of overhanging restorations on periodontal attachment in the permanent dentition. Jansson et al. (1994), found radiographic attachment loss and deeper periodontal pockets at proximal sites with marginal overhangs compared to adequately restored sites24. A recent study evaluated the effect of overhang on bone loss using cone beam computed tomography (CBCT). The study reported a higher incidence of bone loss in sites with overhanging surfaces than in control sites, and bone loss was greater adjacent to overhanging restorations compared to control sites (2.28 ± 1.69 mm and 1.53 ± 1.73 mm, respectively)25. It seems that there is a marked difference between the primary and permanent dentitions, as restorations affected CBRD without association with restoration propriety22. This pattern of attachment loss next to both adequate and inadequate restorations can be explained by restoration margins violating the biologic width26,27. According to Sardana et al. (2014), the mean CBRD in children with primary dentition is 1 ± 0.5 mm28. Such a short distance between the restoration margin and the alveolar crest may result in biologic width violation, which can explain the current observations of radiographic attachment loss.

This study, being a retrospective analysis based on radiographic data without clinical examination, has certain limitations. First, in the absence of a clinical evaluation, it is not possible to confirm whether the radiographic bone loss observed on bite-wing radiographs of children is a sign of early periodontal disease or a result of other factors, such as the condition of deciduous teeth or the eruption of permanent teeth. Furthermore, according to a review by Jenkins et al. (1992), radiographic data from epidemiological studies evaluating periodontal diseases in the primary dentition should be interpreted with caution29. The accuracy of radiographs might be affected by multiple factors, such as X-ray beam angulation and the ability to properly recognize the cemento-enamel junction. Inadequate radiograph quality and missing data lead to the loss of valuable information, which may affect conclusions. Nevertheless, most of the published literature is based on retrospective studies. Longitudinal and large-scale cross-sectional studies are needed for further investigation.

The manuscript offers several novel perspectives on periodontal health in primary dentition, notably finding higher bone loss rates in maxillary canines (36% incidence) rather than molars, and revealing that dental treatments in the assessed teeth correlate with increased bone loss regardless of restoration quality, likely due to biological width violations. Surprisingly, despite previous literature, no correlation was found between socioeconomic status and bone loss in this Israeli population, potentially due to universal children’s dental care implementation in 2010. Additionally, this study identifies a weak but statistically significant correlation between age and the occurrence and severity of bone loss, suggesting that as children grow older, the risk of bone loss increases slightly. These insights emphasize the need for further research to understand better and address alveolar bone loss in primary dentition, considering its implications for future dental health.

Conclusions

Pediatric dentists may observe early alveolar bone loss in the primary dentition of up to 52.5% of the Israeli pediatric population as an initial sign of periodontal disease. This condition most frequently occurs in the maxillary arch, particularly at the distal sites of canines and restored teeth. Among the 120 participants, 63 were found to have at least one site with definite bone loss. The left maxillary canine was the most affected tooth, with a 36% occurrence rate of definite bone loss. No correlation was found between socioeconomic level and the incidence of definite bone loss in the primary dentition of the Israeli pediatric population.