Dimensional Evaluation of Root Resorption Areas in Differing Severity of Chronic Periodontitis: A Scanning Electron Microscopic Study.

AIM: The aim of this study was to evaluate root surface alterations in terms of location, length, and depth of root resorption in the gingival, middle, and apical third of the mesial and distal surfaces of the root in healthy and periodontally affected teeth with chronic periodontitis.
MATERIALS AND METHODS: Teeth diagnosed with differing severity of chronic periodontitis, as assessed by clinical and radiographic parameters of bone destruction, were observed under a scanning electron microscope. Existence and location of root resorption areas, as well as length and depth of the resorption on each radicular third of the teeth, were determined.
RESULTS: Totally 27 teeth (60%) among all the groups exhibited root resorption. The number of teeth showing root resorption in each group was divided into the following groups; Group I: 2 teeth (13.33%); Group II: 11 teeth (73.33%); and Group III: 14 teeth (93.33%). The most affected teeth were the mandibular incisors. The apical one-third of the root was the most affected and the gingival third of the root was the least affected with respect to the length and depth of the root resorption. The mesial surface of the root was more commonly affected when compared to the distal surface of the root.
CONCLUSION: It may thus be concluded that the existence and extent of root resorption depend on the severity of periodontal destruction.

Introduction

In humans and other mammals, the teeth are not attached rigidly to the alveolar bone, but interposed between the two is a soft connective tissue, referred to as the periodontal ligament. At the soft–hard tissue borders of the periodontal ligament, principal fibers are embedded in the alveolar bone and radicular cementum on either sides. The embedded terminations of these collagen fibers are referred to as Sharpey's fibers. Due to its intermediary position between the radicular dentin and the periodontal ligament, cementum is a component of the tooth itself, but belongs functionally to dental attachment apparatus, the periodontium. One of the main functions of cementum is to anchor the periodontal ligament fibers to the root surface. Besides its indispensable role in tooth attachment to the surrounding alveolar bone, root cementum has important adaptive and reparative functions. The dynamic and highly responsive features of cementum are crucial for maintaining occlusal relationship and for the integrity of the root surface and its function in tooth support.

Chronic periodontitis is the most common form of destructive periodontal disease.[1] It is characterized by an inflammatory process that gradually spreads in an apical direction, causing resorption of the alveolar bone as well as the loss of the soft tissue attached to the tooth. The disease usually begins at around the age of 40 years and progresses slowly with the periods of exacerbation and remission.[23]

Root resorption may result in shortening or blunting of the root with loss of cementum and/or dentin. Although physiological root resorption is a normal phenomenon of deciduous teeth during tooth shedding, permanent teeth do not undergo physiological resorption. When resorption of permanent teeth is observed, the resorption is usually the result of trauma, chronic inflammation of the pulp, periodontal tissues, or both, induced pressure in the periodontal ligament associated with orthodontic tooth movement, traumatic injuries, tumors, replantation of teeth, or tooth eruption.[45] In the vast majority of cases, however, idiopathic resorption does occur.[6] Current literature indicates the prevalence of root resorption in teeth as high as 90%, while another study reports that resorption of teeth in Indians was five times more often than that in the United States.[78] Root resorption in the presence of periodontal diseases is found three times more often than that in uninvolved teeth. Although studies are done to detect the presence of resorption in periodontally affected teeth, only a few studies classified teeth according to the severity of chronic periodontitis.[910] These studies observed that, the more severe the periodontal infection, the greater the number of transient external resorption. In addition, there are some studies which examined the presence of root resorption on the different locations on the root surface, however the results are very inconsistent.[911] Limited information available in the literature necessitated this study, which was planned to evaluate root surface alterations in terms of location, length, and depth of root resorption in the gingival, middle, and apical third of the mesial and distal surfaces of the root in healthy and periodontally affected teeth with differing severity of periodontal destruction under a scanning electron microscope (SEM).

Materials and Methods

The study was carried out in the Department of Periodontics and Implantology, VSPM Dental College and Research Centre, Nagpur, India, from where patients indicated for extraction of single-rooted teeth were recruited. The study was initiated after the clearance from the Institutional Ethics Committee of our institute and adhered to the principles outlined in the Declaration of Helsinki on experimentation involving humans. The patients were enrolled after having signed an informed consent. The present study was done on 45 teeth extracted and then segregated into three groups as follows.

Group I (control)

The control group consisted of 15 teeth of periodontally healthy patients with no signs of radiographic bone loss and probing pocket depth (PPD) <3 mm with respect to the concerned tooth and were indicated for extractions for orthodontic treatment.

Group II

This group consisted of 15 teeth of chronic periodontitis patients exhibiting <50% radiographic bone loss of the total root length, PPD of 3–5 mm, clinical attachment level (CAL) of 3–5 mm with respect to the concerned tooth, and were indicated for total extraction.

Group III

This group consisted of 15 teeth of chronic periodontitis patients exhibiting >50% radiographic bone loss of the total root length, PPD and CAL >5 mm with respect to the concerned tooth, and were indicated for total extraction.

Patients with a history of systemic diseases, allergies, or drug usage, have undergone periodontal treatment in the previous 6 months, and those having teeth with restorations or caries were excluded from the study. Clinical parameters such as PPD and CAL were measured using a William's graduated periodontal probe (Hu-Friedy, Chicago, IL, USA) on four sites of the concerned tooth. Plaque index (PI)[12] and papillary bleeding index (PBI)[13] were recorded, which provided information on the periodontal condition of the patients.

Preparation of samples for scanning electron microscope analysis

A periapical radiograph using grid was taken prior to extraction for evaluating the amount of alveolar bone destruction. After extraction, the specimens for SEM were fixed in buffered formol-saline solution for 7 days. The teeth were later sectioned in a mesiodistal direction at low speeds with a carborundum disc (0.5 mm diameter). The buccal half of the tooth was then dehydrated using a series of ascending grades of acetone up to 100% and dried in a critical point drying apparatus in liquid carbon dioxide at 1080 psi at 31°C. The samples were coated with gold-palladium, examined with a scanning electronic microscope (Joel – Made in Japan, Model No: JSM 5400) at 10 kv. The images with a magnification of ×35 were photographed with a Polaroid camera set on the microscope.

Measurement of root resorption

The SEM image of the concerned tooth was printed on a paper. A reference bar scale of 500 μm (0.5 mm) was provided with the image. Measurement errors were minimized by allowing a single examiner (RK) to perform the measurements three times for each area and the most frequently measured readings were selected as the final measurement.

Length of root resorption

The images were observed visually for irregularities (resorption areas) on the root surface. The normal contour of the resorbed root was drawn with a pencil on the printed SEM image. The most superior and inferior extent of this resorption area was marked on the image and this distance was measured with the help of a steel ruler calibrated at 0.5 mm [Figure 1].

Figure 1

Schematic representation of measurement of length and depth of root resorption

Depth of root resorption

The deepest extent of the resorption area was marked on the image. The distance from the marked contour of cementum surface to the deepest point on the image was measured [Figure 1].

Calculation

The bar scale on the image when measured with the help of the steel ruler was calibrated at 0.5 mm and was 25 mm in length.

Statistical analysis

Statistical software STATA Version 12.0 (StataCorp. 2011. Stata Statistical Software: Release 12. College Station, TX: StataCorp LP) was used for data analysis. Clinical parameters such as PPD, CAL, PI, PBI, and the presence of root resorption on the gingival, middle, and apical one-third were compared across the three groups by performing one-way parametric ANOVA. Multiple comparisons between the groups were done by Bonferroni test for normalized data.

Length and depth of root resorption on gingival, middle, and apical one-third of the root on mesial and distal surfaces and total length and depth on mesial and distal surfaces were compared between three groups by performing one-way nonparametric Kruskal–Wallis ANOVA. Multiple comparisons between the groups were done by Wilcoxon rank-sum test for nonnormalized data. P < 0.05 was considered statistically significant.

Results

The mean age of patients in Group I was 23.5 ± 2.66 years, in Group II was 50 ± 15.52 years, and in Group III was 53.33 ± 9.07 years. Intergroup comparison of mean values of PI, PBI, PPD, and CAL showed highly significant differences between the groups, which indicated appropriate patient selection in respective groups.

Existence of root resorption

Totally 27 teeth (60%) exhibited root resorption (19 teeth, i.e., 42.22% of the mandibular teeth and 8 teeth, i.e., 17.77% of the maxillary teeth). The number of teeth showing root resorption in each group was divided into the following groups; Group I: 2 teeth (13.33%); Group II: 11 teeth (73.33%); and Group III: 14 teeth (93.33%).

In the diseased teeth (Group II and III; n = 30), the most affected teeth were the mandibular incisors (n = 11; 36.66%), followed by maxillary incisors (n = 5; 16.66%), mandibular first premolar (n = 4; 13.33%), maxillary canine (n = 3; 10%), mandibular canine (n = 2; 6.66%), and mandibular second premolar (n = 2; 6.66%).

Root resorption location

The predominant location of root resorption in all teeth was the apical third of the root. With respect to the total sample size (n = 45), Group I: apical third, 2.22%; middle third 2.22%, and gingival third 0%. For Group II, the values were 22.22%, 8.88%, and 8.88%, respectively; and in Group III, it was 33.33%, 22.22%, and 11.11% for apical, middle, and gingival one-third, respectively, for the above-mentioned locations [Figure 2].

Figure 2

(a) Scanning electron microscopic images of gingival one-third of the root in all the three groups. (b) Scanning electron microscopic images of middle one-third of the root in all the three groups. (c) Scanning electron microscopic images of apical one-third of the root in all the three groups

Length and depth of root resorption

In all the three locations (gingival, middle, and apical one-third), the length and depth of root resorption increased with increasing severity in the three groups. The extent of root resorption with multiple comparisons is summarized in Tables 1–4.

Table 1

Total length and depth of root resorption (mm) on all aspects (mean±standard deviation)

Table 4

Multiple comparisons of observed root resorption depth (mesial and distal depths) in different locations of teeth

Dentin invasion

With respect to the total number of resorbed teeth (n = 27), the dentin was invaded in 12 teeth (44.44%) with root resorption, and the number increasing with the severity of periodontitis. No teeth in Group I exhibited resorption invading the dentin, only 2 teeth (7.40%) in Group II were affected with dentin invasion, but 10 (37.03%) teeth in Group III were affected with dentin invasion. In Group II, the invaded dentin occurred on the mesio-apical third aspects on both the teeth. In Group III, the dentin was invaded in 4 teeth (14.81%) on the mesio-gingival third, 4 teeth (14.81%) on the mesio-apical third, and 2 teeth (7.40%) on the disto-apical third.

Discussion

Root resorption is one of the complications in periodontal diseases, which in severe cases may be indicated for tooth extraction. The denuded mineralized tissue is colonized by multinucleated cells, which are known to initiate the process of resorption. Repair within the cemental tissues occurs within a few weeks, but does not cover large surface areas. Owing to the regular stimulus in periodontal disease, the resorption areas are likely to increase in extent.[14]

The main purpose of this study was to quantify the length and depth of root-resorbed region on each radicular third of root showing differing levels of periodontal disease severity by SEM. Group III patients had a mean age of 53.33 years, which coincides with the understanding that severe periodontal destruction is often evident with increasing age, especially above the fourth decade of life. The clinical parameters recorded showed significant differences in PI, PBI, PPD, and CAL among the groups.

In the present study, the most affected teeth exhibiting root resorption areas were mandibular incisors, which have also been reported by Bossert and Marks and Crespo Abelleira et al. to be the commonly affected teeth.[15] Among the total sample size of 45 teeth, 11 were mandibular incisors and belonged to only Group II and Group III, indicating that, within the total sample size of 30 teeth in these groups, 13 teeth, i.e., 43.33% were mandibular incisors, 11 of them showed root resorption amounting to 84.61% which was far more as compared to the other teeth. Massler and Malone have also found that mandibular incisors were the most susceptible teeth but have attributed it to idiopathic root resorption.[6] We differ with the author's view in terms of cause of resorption, because in our study, we had only two teeth out of the total in the Group I, which exhibited root resorption and which could be assigned to idiopathic reasons. Whereas the other teeth showing root resorption amounting to 90% could very well be assigned to periodontal disease conditions. It has been mentioned in the literature that root resorption location may not be always cervical, but it is related to the level of marginal tissues and pocket depth present in the periodontal diseases.[16] With regard to the mandibular incisors being the commonly affected teeth, it is believed that, since these are single-rooted teeth, with a slender anatomy and having lesser amount of surrounding periodontal structures, they are more prone toward periodontal destruction, as compared to the other teeth, especially molars.

Results of the present study revealed that the percentage of teeth with root resorption increased with the severity of periodontal disease ranging from 13.33% to 93.33%. These findings are similar to those of López et al.,[14] Harvey and Zander[10] who showed 77% and up to 90% of root resorption, respectively, in periodontally diseased teeth and Crespo Abelleira et al.[9] who showed 100% resorption in severe cases of periodontally affected teeth. The differences can be due to different classification criteria for periodontal disease diagnosis and did not include the radiographic quantum of bone destruction as was used in the present study. The methods of sample preparation were also different, as the authors made horizontal sections, 20 μm thick, at 80 μm intervals, for only four areas of each tooth, while we screened the entire root surface, which yielded comprehensive information.

The majority of the resorption were located in the radicular apical third followed by middle third and least in gingival third in our study. Similar findings were observed by Kurol et al. and Rodriguez-Pato,[1117] and the authors opined that mechanical irritation, trauma, inflammation, or systemic disturbances have been considered the causative factors for external resorption. The presence of resorption in healthy and unhealthy teeth seemed to show that the inflammation was not the only etiology of resorption as it was believed. We observed that, with regard to the gingival third, the control group did not show any resorption, while the diseased teeth did; the percentage of teeth with resorption areas was smaller in Group I than that in Group II and III. These differences seem to suggest that resorption in the gingival third occurred when it was exposed to inflammation. Furthermore, the intergroup differences are probably due to the fact that only teeth in Group II and III had the entire length of the gingival third exposed to inflammation.

In our study, the average length of root resorption decreased from apical third to gingival third. These findings are somewhat dissimilar to those of Rodriguez-Pato who found the highest length of resorption being in the middle third.[11] These variations may be due to the difference in the methods used to measure the amount of resorption. In our study, we used SEM to study the presence of resorption and the measurements were done manually, whereas the authors observed the resorption under a light microscope.[11] In fact, SEM is more sensitive in identifying surface alterations.

In our study, the length and depth of resorption were significantly more on the mesial surface as compared to the distal surface, which is similar to findings obtained by Dastmalchi et al. and Stamfelj et al. on multirooted molars.[1819]

Periodontal disease implies alveolar bone loss, attachment loss, and leads to considerable tooth mobility. In mobile teeth, it is possible that occlusion could lead to mechanical irritation on the radicular surface and the formation of cementum lesions, which would probably be more frequent and more serious in relation to tooth mobility associated with periodontal disease as microorganisms from gingival sulcus penetrate patent dentinal tubules at a coronal level and exit apically. Consequently, area of the root surface, which is damaged, is colonized by hard tissue-resorbing cells that penetrate into dentin leading to further resorption. This resorption spreads in an irregular manner into the dentinal surfaces.[202122]

In our study, the resorption areas affecting both the cementum and the dentin and their presence in the apical third increased depending on the severity of the periodontal disease. Without underestimating the fact that the inflammation per se could be acting directly, it is considered that teeth in a more advanced stage of the disease have had the apical third exposed to a more intense mechanical trauma. In severely affected teeth which have mobility and limited support, there would neither be sufficient periodontal fibers nor alveolar bone to absorb the forces of occlusion, which would facilitate the formation of deeper lesions of invasion.

Conclusion

The results of our study indicate that root resorption is commonly seen in periodontally diseased teeth when compared with healthy controls. The resorption areas increased with the increase in the severity of periodontal disease. The resorption changes occurring over the root surface are predominantly located at the apical one-third portion, while the gingival one-third portion was the least affected. Hence, within the limits of the present study, a strong association between the severity of periodontal disease and root resorption is evident. Further detailed studies are required to unfurl the exact mechanisms and understand the other intricacies of this association.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Table 2

Multiple comparisons of observed root resorption length (mesial and distal lengths) in different locations of teeth

Table 3

Comparison of total length and depth of root resorption in different areas