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| ORIGINAL ARTICLE |
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| Year : 2022 | Volume
: 49
| Issue : 3 | Page : 339-346 |
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Correlation of pericoronal radiographic width with histopathology of dental follicle of impacted teeth using modified gallego's and H and E stain
Sandhya Tamgadge1, Treville Pereira1, Gokul Venkateshwar2, Mandavi Waghmare3, Hemant Bhutani3, Charu Girotra2, Siddharth Acharya4
1 Department of Oral and Maxillofacial Pathology and Microbiology, School of Dentistry, D. Y. Patil Deemed to be University, School of Dentistry, Navi Mumbai, Maharashtra, India
2 Department of Oral and Maxillofacial Surgery, School of Dentistry, D. Y. Patil Deemed to be University, School of Dentistry, Navi Mumbai, Maharashtra, India
3 Department of Oral and Maxillofacial Radiology, School of Dentistry, D. Y. Patil Deemed to be University, School of Dentistry, Navi Mumbai, Maharashtra, India
4 Department of Public Health Dentistry, School of Dentistry, D. Y. Patil Deemed to be University, School of Dentistry, Navi Mumbai, Maharashtra, India
| Date of Submission | 28-May-2022 |
| Date of Acceptance | 11-Sep-2022 |
| Date of Web Publication | 27-Dec-2022 |
Correspondence Address:
Dr. Sandhya Tamgadge
Department of Oral and Maxillofacial Pathology and Microbiology, School of Dentistry, D. Y. Patil University, Sector 7, Nerul, Navi Mumbai - 400 706, Maharashtra
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/jss.jss_105_22
Background: Dental follicles are involved the development of tooth and periodontal structures. Dental follicles are known for pleuripotency and inductive changes but are also known for origin for various pathologies. Materials and Methods: Fifty eight asymptomatic dental follicle tissues were examined histologically and radiographically wherein orthopantomogram radiographic width was correlated with various histological parameters of dental follicle and evaluated for the presence of various pathologies using modified Gallego's stain. Observation and Results: There was evidence of pathological changes associated with asymptomatic dental follicle. We also found variations in epithelial lining, stromal calcifications, and variable compositions. Conclusion: We encourage researchers to examine this peculiar tissue as a unique model and explore its potential to avoid future complications.
Keywords: Calcifications, epithelium, follicle, modified Gallego's stain, orthopantomogram, pathologies, width
How to cite this article:
Tamgadge S, Pereira T, Venkateshwar G, Waghmare M, Bhutani H, Girotra C, Acharya S. Correlation of pericoronal radiographic width with histopathology of dental follicle of impacted teeth using modified gallego's and H and E stain. J Sci Soc 2022;49:339-46 |
How to cite this URL:
Tamgadge S, Pereira T, Venkateshwar G, Waghmare M, Bhutani H, Girotra C, Acharya S. Correlation of pericoronal radiographic width with histopathology of dental follicle of impacted teeth using modified gallego's and H and E stain. J Sci Soc [serial online] 2022 [cited 2023 Mar 31];49:339-46. Available from: https://www.jscisociety.com/text.asp?2022/49/3/339/365163 |
| Introduction | |  |
Pericoronal sac or follicle occasionally persists adjacent to the crown of unerupted or impacted teeth. It is composed of fibrous connective tissue and frequently contains epithelial residues of odontogenesis, which could be the starting point of pathology. Radiographically, it appears as a thin pericoronal radiolucency considered normal by some authors when it is <3 mm thick and by others when it is no thicker than 2.5 mm.[1]
Data on pathological changes in follicle are scant due to the fact that following removal of asymptomatic impacted teeth, the pericoronal tissue is often discarded rather than being submitted for histopathological evaluation. However there are follicles of impacted teeth associated with cyst and tumor development.[2]
The aim of this study was to determine the pathologic alterations in follicular tissues where radiographic pericoronal radiolucency is <3 mm, thus stressing the need for routine removal of unerupted third molars as advocated by some investigators. Unlike previous studies, the present study was carried out to microscopically evaluate the dental follicular tissues for pathological changes using H and E and modified Gallego's stain, and to correlate with pericoronal radiolucency using orthopantomogram.
Odontogenic tissues have unique epithelial-mesenchymal interactions in spite of being derived from ectoderm which leads to various types of calcified tissue deposits. This study additionally involves analysis of such deposits using modified Gallego's stain as H and E stain can't differentiate the true nature of such deposits.[3]
There are various histochemical stains to detect calcifications such as methylene blue-acid fuchsin (MB-AF) and von Kossa etc. Modified Gallego's stain is a variant of Lille's stain that uses basic reagents hematoxylin, carbol fuchsin, and aniline blue.[4] The advantage of modified Gallego's stain is that it differentially stains the hard tissues.[5]
A study on few samples has been reported earlier. However, the current research is with larger sample size with additional new findings. Dhouskar et al. have conducted a study on fibro-osseous lesions using the same stain,[6]
Satheesan et al. in 2016 reported that the dental follicle surrounding an impacted tooth has the potential to differentiate into a wide variety of tissue types, and thus shows the potential for cyst and tumor development which was observed in this study in most of the specimens with normal follicular width radiographically.[2]
Bi, R.; Lyu summarized, in 2021, the current knowledge of dental follicle, including their stem cell properties, physiological functions, and clinical application potential. A deep understanding of DFPCs can thus inspire novel perspectives in regenerative medicine in the future.[4]
Tao Zhou 2019 reviewed the roles of DFCs in tooth development, their properties, and clinical application potentials, thus providing a novel guidance for tissue engineering.[7]
| Materials and Methods | | |
The study was conducted in the Department of Oral and Maxillofacial Pathology of D.Y. Patil University, School of Dentistry. Nerul Navi Mumbai, Sector 7, Nerul, Navi Mumbai, Maharashtra, from 2017 to 2018. Patients requiring removal of mandibular or maxillary impacted teeth under local anesthesia were enrolled in the study. Fifty-eight dental follicles of impacted teeth were submitted for histopathologic examination.
Orthopantamograph was considered for analysis for measurement of pericoronal space using the software “Kodak Dental Imaging Software-6.12.26.0-Measuring tool.”
H and E stain was used to evaluate the presence of odontogenic epithelial tissue, type of epithelium, presence of inflammation, type of stroma, and nature of calcification evaluated through modified Gallego's stain[5] using Leica research microscope (Model No. DM1000 LED).
Patients with at least one impacted teeth covered by mucosa and partially or completely covered by bone with minimum pericoronal follicular space <3 mm were included in the study. Cases with follicular space >3.1 mm and follicular tissue insufficient for histopathological analysis were excluded from the study.
Patients with impacted third molar with established pathosis were excluded. The pericoronal space was measured from the mesial, distal, and occlusal surfaces, and the largest width was recorded disregarding the manufacturer's reported magnification factor. The width measured was color coded as pink for mesial, blue for occlusal, and green for distal dimension. The control group included 5 cases. Out of which three tooth germs demonstrating dentin and cementum depositions and two were ground section of bone and cementum, respectively. They served as a positive control for staining specificity of calcifications using modified Gallego's stain.
Microscopic examination of epithelial and mesenchymal components of all the dental follicular specimens was performed. Additional pathological features if found were assessed. Data were tabulated statistically and associations between the attributes were tested using Pearson Chi-square test. The Pearson Chi-square test with a significance level of 5% was employed to assess the correlation between the radiographic and morphological features. For all the tests, P = 0.05 or less was considered for statistical significance.
| Observation and Results | | |
Epithelium was present in 55.7%, out of which stratified squamous epithelium was 31.1%, reduced enamel epithelium 18.0%, and ameloblastomatous epithelium was present in very few. The type of stroma was also analyzed. Myxoid stroma was present in 3.3%, and cellular stroma was in 9.8% of samples. Inflammation was found as mild, moderate, and severe as 55.7%, 24.6%, and 3.3%, respectively. Odontogenic cell rests were very common and present in 31.1%.
The percentage of calcifications was analyzed in the form of dentinoid and cementoid. Such calcifications were present as individually or in combinations, which were confirmed with modified Gallego's stain. These clinically asymptomatic follicles revealed multiple pathological changes on histopathological examinations such as multiple odontogenic islands, acanthomatous ameloblastoma, CEOT-like changes, mucoid change and Rushton bodies like changes [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]. | Figure 1: (a-c) Dental follicle dimensions, odontogenic islands with stellate reticulum change, reduced enamel epithelium, respectively. (d-f)- dental follicle, dimensions epithelial lining, lining with pseudostratified epithelium respectively
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 | Figure 2: Photomicrograph: (a) Histopathology of follicle showing reduced enamel epithelium and odontogenic islands in connective tissue capsule. (b) Dimensions of follicle in OPG. (c and d) Dentinoid-like calcifications in Hematoxylene and eosin stain and modified Gallego's stain. (e) Odontogenic rests. OPG: Orthopantomogram
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 | Figure 3: (a, c, and f) Odontogenic islands. (b) Odontogenic islands showing acanthomatous change. (d) Modified Gallego's stain. (e) Dental follicle dimensions
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 | Figure 4: (a-d) Dental follicle showing myxoma-like change. (e) Dimensions of follicle in OPG. OPG: Orthopantomogram
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 | Figure 5: (a and b) Epithelial lining is of stratified squamous type with focal collections of eosinophilic bodies resembling Rushton bodies above the epithelial surface. (c) Modified Gallego's stain. (d) Mucous metaplasia in odontogenic rests
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 | Figure 6: Follicle: (a) Stratified, reduced enamel epithelium, and developing odontogenic epithelium. (b) Developing odontogenic epithelium under higher magnification. (c) Dental follicle in OPD. OPD: Outpatient department
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 | Figure 7: (a and b) Dentinoid-like calcification. (c) Modified Gallego's stain. (d) Reduced enamel epithelium
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 | Figure 8: (a) Epithelial lining and odontogenic islands. (b) Epithelial lining has pseudostratified epithelium and calcification. (c) Modified Gallego's stain. (d) Odontogenic islands showing cells resembling CEOT features. CEOT: Calcifying epithelial odontogenic tumor
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 | Figure 9: (a and b) Odontogenic islands showing features resembling Vicker's and Gorlin's criteria
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The largest radiographic width of dental follicle was compared with various histopathological parameters. Such as (1) pericoronal radiographic width with inflammation, stratified squamous epithelium and inflammation, fibrocellular stroma with inflammation, odontogenic cells rests with pathologic changes, and calcification with modified Gallego's stain [Table 1], [Table 2], [Table 3]. Positive Correlation between Radiographic Width Largest and Myxoid Stroma was significant at p>0.05. | Table 1: Correlation between inflammation and largest radiographic width
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 | Table 2: Correlation between stratified squamous epithelium and inflammation
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 | Table 3: Correlation between presence of calcifications and modified Gallego's stain
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Radiographic width was ranging from a minimum value of 0.4 mm to maximum 5.6 mm.
| Discussion | | |
Radiographically
The pericoronal radiolucency surrounding the crown of an impacted tooth is interpreted as follicular sac.[8] The width of this radiolucency is of utmost importance to differentiate between a normal and an abnormal dental follicle as it is the source of odontogenic cysts and tumors.
Foci of calcifications also are seen as a normal finding in the stroma of dental follicles. Studies show that 13.7% of follicles have foci of dystrophic calcification. Kim and Ellis found 37% of follicles with dystrophic calcification whereas Stanley et al. found approximately one-third of the unerupted follicles with dystrophic calcification.[9]
It was proposed that removing these teeth in younger people might be a preventive measure for probable lesions in adulthood. On the other hand, Santosh stated that the risk of retained impacted teeth overexaggerated and their removal is to be done only in case of definitive pathology.[10] The 12-year follow-up study conducted by Alquist and Grondahl revealed minor changes in 15% of the impacted teeth,[11] whereas a study done by Khorasini and Samiezadeh did not reveal any pathologic changes in the follicle of impacted teeth.[12]
Therefore, numerous studies with conflicting results have been conducted on the potential of follicular tissues to undergo pathological alteration. Furthermore, not much attention was given to the presence of calcifications and its nature in the previous studies even though it is considered to be an important parameter in the WHO classification of odontogenic tumors. In a recent extensive review by Bastos et al. in 2021,[4] various studies have been compiled on dental follicle. A systemic review by Fernanda Weber Mello reported that odontogenic cysts and tumors were found in 5.3% of impacted third molar extracted. The most common lesions were the radicular cyst, dentigerous cyst, and odontogenic keratocyst.[13]
Mesgarzadeh et al. in 2007 concluded in their study that radiographically normal dental follicles surprisingly show multiple pathosis which was also seen in our study.[14]
Meleti and van der Waal in 2018 hypothesized in their study of 164 dental follicles that the presence of odontogenic islands in the stroma could be a sign of focal ameloblastoma.[15] Our study also showed the presence of odontogenic islands with minimum radiographic width.
Haghanifar et al. in 2014 studied a ratio of dental follicle diameter to the mesiodistal width of the teeth to be used as a diagnostic index to differentiate between normal and pathological dental follicles. However, the results were inconclusive. In this study, dental follicle was measured in three directions.[16]
An evaluation of pathologic changes in the follicle of impacted mandibular third molars was reported by Tambuwala et al. in 2015 and their findings were highly conclusive.[17]
Epithelial lining
In the present study, 32% of the samples showed cystic changes which had a pericoronal radiolucency lesser than 3 mm. This finding was consistent with studies by Vishal Mehrotra et al. who reported that 55% of follicles associated with impacted third molars, with pericoronal radiolucency <2.5 mm, actually showed the presence of stratified squamous epithelium. This result correlates with a study done by Baykul et al. who investigated the cystic changes in radiographically normal follicles associated with 94 impacted mandibular impacted third molars, and reported that 50% of the follicular specimens showed cystic changes as the only pathological condition.[18] Another study conducted by Satheesan et al. in 2015 on impacted teeth had associated dentigerous cysts.[2]
In this study, 34% of the follicular specimens were associated with epithelial layer.[19] In this study, we observed various types of epithelial lining such as reduced enamel epithelium, stratified squamous epithelium, ameloblastomatous epithelium pseudostratified epithelium, and one specimen showed the presence of eosinophilic Rushton bodies like changes on the surface of the epithelium. A zone of separation was clearly evident between the two suggesting that it is a part of the follicle and not the tissue tag coming from elsewhere.[20]
Eleven percent of cases in this present study showed reduced enamel epithelial lining.
Cystic changes according to Saravana, the presence of squamous epithelium in the lining of a tissue sac that invests the crown of an unerupted or impacted tooth defines progression from dental follicle to dentigerous cyst.[8] We also observed the transition of epithelium from reduced to stratified to ameloblastomatous in the same specimen.
Many investigators require a continuous lining of stratified squamous epithelium for the diagnosis of dentigerous cyst.[20] And therefore, for the purposes of this study, the dental follicles lined by continuous stratified squamous epithelium located around the crown of an unerupted tooth were considered to be “cystic” changes (dentigerous cyst-like changes). In the present study, around 19% of cases demonstrated stratified squamous epithelium which was indicative of cystic transformation of the dental follicle.[21] If the impacted teeth are overdue for eruption, then the reduced enamel epithelium and remnants of the dental follicle in the connective tissue have the potential for cystic or neoplastic transformation.[22] and mostly associated with inflammation.
In the present study, few cases demonstrated all the classical Vickers and Gorlin suggests that the retained dental follicle of asymptomatic impacted teeth has the potential to transform into a unicystic ameloblastoma.[22]
Few cases lined by stratified squamous epithelium (considered to be a cystic change in the follicle) along with ameloblastomatous epithelium are suggestive of the fact that the relatively harmless pericoronal follicle can show squamous metaplasia resembling a dentigerous cyst and can further progress into unicystic ameloblastoma which is a neoplastic change.
Cabbar et al. stated that the inflammation observed in the mesenchymal components of dental follicle upregulates the cell turnover of odontogenic epithelium and leads to proliferation.[23]
Inflammation
Khorasani and Samiezadeh found inflammation in 44% of their samples. The results of the present study showed that 24.6% of dental follicles were associated with severe inflammation.[12]
Inflammation acts as a stimulator on the lining epithelium of dental follicle and changes it from its normal cuboidal or columnar form to a squamous type. There is a significant correlation between severe inflammation and the presence of squamous epithelium.[24] Similar results were found in the present study also where 19 showed stratified squamous type of epithelium. The authors concluded that squamous metaplasia is not a normal sequela in follicle maturation but represents early signs of pathology. The hypothesis put forward by Browne is that since the attachment of the squamous epithelium to the enamel is inferior as compared to that of the reduced enamel epithelium, there is a high probability of cystic development in such cases.[25]
Lautenschläger Gde et al. suggested that severe inflammation may cause chronic irritation and stimulate the proliferation of epithelial cells. Whereas some researchers assert that the presence of squamous metaplasia in the lining of dental follicle is not sufficient to diagnose dentigerous cyst, others suggest that it is the early stage of the lesion since it presents high proliferation compared to healthy follicular tissue.[26] The inflammatory exudate may cause separation of reduced enamel epithelium from the enamel with resultant cyst formation.[1]
Odontogenic islands
Inactive odontogenic islands should be evaluated properly.[15] In the present study, 31% of cases demonstrated odontogenic island in the connective tissue stroma. This finding was similar to the results obtained by Khorasani and Samiezadeh (2008),[12] where 48% of the samples demonstrated odontogenic epithelial rests in their connective tissue. This was <79% reported by Kim and Ellis.[9] The odontogenic islands were correlated with clinical parameters. They were also evaluated for activity and any signs of neoplastic change. Odontogenic islands are normally considered to be inactive but have the potential to differentiate and give rise to various cysts and tumors. De Oliveira et al. observed that in 4.8% of the follicles, the following changes occurred that deviated from the pattern of normality: acanthomatous change, mucoid change, stellate reticulum change, Rushton bodies like changes, and CEOT-like changes.[27]
Follicular ameloblastomas are characterized by islands of odontogenic tissues within a fibrous stroma.[28] In the study by Kim and Ellis,[9] scattered epithelial rests were present in 79% of follicles. Features of ameloblastic differentiation were not observed.[29] In the current study, the odontogenic cell rests differentiated to show features of acanthomatous change and also mucous cell differentiation.
Few of the follicles had undergone squamous metaplasia where the central cells had lost their stellate appearance and resembled low cuboidal and squamous cells.
Squamous differentiation of the odontogenic islands may be attributed to chronic irritation.[30]
The reason for hybrid nature of lesions seen in this study could be due to pleuripotent nature of cells of dental follicle. Patients with such changes should be followed up radiographically. A further unusual finding noticed was the presence of mucous cells in few of the islands.[31] The mucous cell differentiation is attributed to the pleuripotent nature of dental follicle. The potential of stem cells of dental follicle to undergo osteogenic, adipogenic, and neurogenic differentiation was demonstrated using in vitro studies.[32]
In the WHO classification of odontogenic tumors, hard tissue formation has been considered a subclassification. However, studies on hard tissue formation and nature of calcification in dental follicle of impacted teeth have so far not been documented in dental literature. Calcifications are a part of the mesenchymal tissue and hence its presence in the follicle needs to be emphasized along with the epithelial component. Calcium deposits made by cells are produced by mesenchymal cells such as osteoblasts, odontoblasts, or ameloblasts.[33] The gross calcific depositions are easily seen in routine H- and E-stained sections, early minimal deposits are often easily missed out and differentiation between the nature of calcification to be osteoid, cementoid, or dentinoid type becomes difficult or impossible. Cementum under H and E stain is seen as round to ovoid basophilic globular depositions which are devoid of cells (i.e-acellular). Osteoid areas are eosinophilic with osteoblasts and osteocytes which are bone-forming cells.[34] There are various histochemical stains to detect calcifications such as MB-AF and von Kossa. Modified Gallego's stain is a variant of Lille's stain that uses basic reagents hematoxylin, carbol fuchsin, and aniline blue.[5] The advantage of this stain is that it differentially stains the hard tissues seen in teeth, dental follicle, and other oral lesions. It gives a clearer understanding of the histological picture of the hard tissue forming conditions of the oral cavity. When combinations of hard and soft tissues as well as multiple hard tissue components are evident in the same tissue, they pose diagnostic difficulties; also identification of types of calcified structures in their initial phase is crucial for diagnosis. In a well-stained slide of Modified Gallego's stain, cementum-like deposition shows red color whereas dentin and bone takes up green color. This helps in clearly distinguishing between the different hard tissues which are otherwise difficult to identify using routine H and E staining techniques. The advantage of this staining technique is that it can be applied in soft tissue specimens, decalcified sections, ground sections, and even frozen sections. Very few stains are mentioned in literature which can be used on ground sections of bone and teeth.[5]
Using modified Gallego's stain, we were able to confirm that 38% of dental follicle showed cementum-like depositions, 24% showed dentinoid/osteoid depositions, and 2% showed a mixture of more than one type of calcification. Enamel-like depositions were not seen in the current study.
In the present study, there was an increased incidence of calcifications as the pericoronal width increased. The calcifications are a part of the mesenchyme and therefore seen as an increased radiolucent width radiographically. The dental follicle that surrounds the developing tooth germ contains progenitor cells for the development of the periodontium. These progenitor (stem) cells have been shown to differentiate into various tissue types as mentioned by Handa et al.[35] Few cases in the present study showed calcifications which were present close to the epithelium (epithelial-connective tissue interface) whereas maximum calcifications were seen deep in the stroma. The presence of calcification adjacent to the epithelium can suggest an inductive activity. One case showed curvilinear eosinophilic bodies resembling Rushton bodies on the surface of the epithelium as focal collection. Few attached epithelial cells at the interface were suggestive of epithelial origin and not the dislodged connective tissue fragment. Few cases in this study showed the presence of dentinoid with tubule formation. The possible pathogenesis could be the inductive changes, leading to calcium deposits. Metaplasia can be regarded as another probable explanation for the presence of the cementum, bone, and dentinoid calcifications.[2],[6]
| Conclusion | | |
It can be concluded that the dental follicle surrounding an impacted teeth has the potential to differentiate into a wide variety of tissue types, and the potential for cyst and tumor development exists. One disturbing finding from this study is that many of the specimens with radiographically normal follicular radiolucency had developed pathological entities. Histopathological analysis in earlier studies has detected multiple changes, while some studies have reported dentigerous cysts as the only detected pathologic entity. Further studies with a larger sample size and long-term follow-up are required. The use of modified Gallego's stain with additional findings was the unique feature of the study. Indeed, new techniques such as immunochemical, new histochemical stains and cone-beam CT might provide further assistance in exploring new dimensions in the analysis of asymptomatic dental follicles.
Acknowledgment
The authors are grateful to senior lab technician of the Department of Oral Pathology and Microbiology, Mrs. Rajshree Dahale, of D. Y. Patil University School of Dentistry, Nerul, Navi Mumbai, for contributing in staining procedures.
This research has been funded by “Viridis Biopharma Pvt. Ltd.”
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
[Table 1], [Table 2], [Table 3]
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