Abstract
Background:
Odontogenic cysts have the potential to transform into neoplasms. However, the characteristics of those which transformed to neoplastic tissues have not been well described and the exact causes of that phenomenon are not yet clear.
Objectives:
This study aims to describe characteristics of odontogenic cysts that transformed into neoplasms and to look for their potential etiologies.
Data Sources:
English-written studies indexed in PubMed, Science Direct, and Proquest were assessed using keywords verified by Medical Subject Headings: ‘Odontogenic Cyst’ and ‘Neoplastic Cell Transformation’.
Study Eligibility Criteria:
Preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) guidelines were used as guidance.
Participants:
Following steps in PRISMA guidelines, 19 articles were fully reviewed (three case series and 16 case reports) with 27 subjects of 16 males (59%) and 11 females (41%) from 15 to 86 years old.
Results:
Cystic origins were eight dentigerous cysts, four odontogenic keratocysts, two residual cysts, one radicular cyst, one calcifying odontogenic cyst, one follicular cyst, one glandular odontogenic cyst, and nine unspecified odontogenic cysts that transformed to ameloblastoma (3 cases) and carcinoma (24 cases).
Limitations:
Neoplastic transformations of odontogenic cysts arose from epithelial remnants of inadequate odontogenic cyst removal and chronic inflammation due to infection. However, the exact causes of their transformations remain unclear.
Conclusions:
Therefore, careful removal of odontogenic cysts and regular postoperative follow-ups are key to prevent recurrence and neoplastic transformation. Future studies are needed to investigate potential causes of neoplastic transformation of odontogenic cysts.
Keywords: Odontogenic cyst, neoplastic cell transformation, neoplasm
INTRODUCTION
The jaw acts as the ‘host’ for cysts and tumours because its tissues are involved in tooth formation.[1] Odontogenic cysts are pathological cavities lined with epithelium and filled with fluid, semisolid, or gaseous material, which develop from the remnants of odontogenic apparatus, while odontogenic tumours are solid tissue masses, which are not necessarily neoplastic.[2,3] A considerable amount of odontogenic lesions have been reported in the literature globally.[3] Among all cysts, odontogenic cysts had a prevalence of 15.31%, with radicular cysts being the most frequently found odontogenic cysts (48.67%), then dentigerous cysts, odontogenic keratocysts, and calcifying odontogenic cysts.[3]
In addition to their high prevalence, odontogenic cysts have the potential to transform into neoplastic lesions.[4] Several studies stated the epithelial remnants of odontogenic cysts as the main origin of odontogenic cysts transforming into neoplastic lesions, such as ameloblastomas, adenomatoid odontogenic tumours, and even nonodontogenic malignant tumours.[4] However, the frequency of these neoplastic transformations are known to be low.[4] In the literature, studies that purposefully investigated the characteristics of those cystic lesions that transformed into neoplastic tissues and the causes of those transformations have not been reported.
In this systematic review, we assessed 19 studies reporting the transformation of odontogenic cysts to neoplasms to systematically review the characteristics of odontogenic cysts that transformed into neoplastic lesions and to look for potential etiologies of those phenomena.
METHODS
An electronic search was performed using Science Direct, ProQuest, and PubMed databases for English-written scientific literatures published between April 2012 and April 2022 on odontogenic cyst transformation to neoplasms using keywords specified as shown in Table 1.
Table 1.
Keywords used in the literature search in PubMed, Science Direct and Proquest databases
| Databases | Keywords |
|---|---|
| PubMed | ((((((odontogenic cyst[MeSH Terms]) OR (Cyst, Odontogenic)) OR (Cysts, Odontogenic)) OR (Odontogenic Cyst)) OR (Keratocysts)) OR (Keratocyst)) AND (((((((((((((((Cell Transformation, Neoplastic[MeSH Terms]) OR (Transformation, Neoplastic Cell)) OR (Neoplastic Transformation, Cell)) OR (Cell Neoplastic Transformation)) OR (Cell Neoplastic Transformations)) OR (Neoplastic Transformations, Cell)) OR (Transformation, Cell Neoplastic)) OR (Transformations, Cell Neoplastic)) OR (Tumorigenic Transformation)) OR (Transformation, Tumorigenic)) OR (Transformations, Tumorigenic)) OR (Tumorigenic Transformations)) OR (Cell Transformations, Neoplastic)) OR (Neoplastic Cell Transformations)) OR (Transformations, Neoplastic Cell)) |
| Science Direct | Odontogenic cyst neoplastic transformation |
| Proquest | Odontogenic cyst neoplastic transformation |
Inclusion criteria were analysed based on the PICOS components as follows:
P = population = all odontogenic cyst lesions
I = intervention = analysis of neoplastic transformation of odontogenic cysts
C = comparison = comparison of various types of odontogenic cysts and transformed neoplastic lesions
O = outcomes = clinical, radiological, histopathological, and genetic analysis
S = study type = all English-written research articles, case reports and case series, except review articles.
Research questions being asked are as follows:
How are the characteristics of odontogenic cysts that underwent transformation to neoplasms?
What causes odontogenic cyst transformation to neoplastic tissues?
The title of each article was independently reviewed by four researchers. The papers assessed were clinical trials, randomised controlled trials, case reports, case series, and prospective and retrospective cohort studies reporting odontogenic cysts that transformed into neoplasms. Studies reporting irrelevant topics were not included. Papers that met the inclusion criteria were retrieved in full for eligibility assessment and further review.
After planning the search and review strategy, this study was registered in PROSPERO with registration number: CRD42022340739 on June 30, 2022. The data extracted from eligible papers were: Titles, authors, year, study design, total samples, age, sex, clinical appearance, radiographic appearance, histologic appearance, diagnosis, differential diagnosis, and recurrence.
An independent risk of bias assessment was conducted by two reviewers using Quality Assessment Tool for Case Series Studies by the US National Institutes of Health. We categorised 0–1 not reported (NR) items as good quality, 2–3 NR as fair quality, and 4–5 NR as poor quality. The data obtained in this study were then analysed and reported with descriptive statistics.
RESULTS
Preferred Reporting Items for Systematic Review and Meta-Analysis guidelines were used in selecting the articles [Figure 1]. In the identification stage, 346 records, 26 from PubMed, 179 from ScienceDirect, and 141 from ProQuest were identified, then 320 records were removed due to duplicates and irrelevant titles. In the screening stage, 26 articles were obtained. The full paper of one article was not found, full paper of one article was not available in English, two were review articles, and three of them apparently were out of topic. Finally, only 19 articles were included in this review.
Figure 1.
PRISMA flow of this study. PRISMA = Preferred Reporting Items for Systematic Review and Meta-analysis
The complete description of selected studies is shown in Annexure (1.1MB, pdf) . The types of the studies found were three case series and 16 case reports. Within the 19 articles, there were 27 subjects assessed in total, consisted of 16 males (59%) and 11 females (41%), ranging from 15 to 86 years old. Meanwhile, types of the cystic origins were classified as dentigerous cysts (8 cases), odontogenic keratocysts (4 cases), residual cysts (2 cases), radicular cyst (1 case), calcifying odontogenic cyst (1 case), follicular cyst (1 case), glandular odontogenic cyst (1 case), and many were unspecified odontogenic cysts (9 cases). Meanwhile, the cases show that odontogenic cysts could transform into ameloblastoma (3 cases) and carcinoma (24 cases), ranging from ameloblastic carcinoma (1 case), mucoepidermoid carcinoma (3 cases), primary intraosseous squamous cell carcinoma (13 cases), and other squamous cell carcinoma (7 cases). The quality assessments for the risk of bias of each reviewed paper were conducted based on the nine questions in the Quality Assessment Tool for Case Series Studies by the US National Institutes of Health. Assessment results rated all studies as good quality [Table 2].
Table 2.
Quality assessment for risks of bias of the 19 reviewed articles
| Study | Q1 | Q2 | Q3 | Q4 | Q5 | Q6 | Q7 | Q8 | Q9 | Quality rating |
|---|---|---|---|---|---|---|---|---|---|---|
| Isshiki-Murakami et al. (2021) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Garzino-Demo et al. (2020) | Yes | Yes | Yes | Yes | Yes | Yes | Yes | NR | Yes | Good |
| Nagasaki et al. (2018) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Kondamari et al. (2018) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Jalali et al. (2017) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Razavi et al. (2017) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Martinez et al. (2016) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Hino et al. (2016) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Singh et al. (2016) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Gurugubelli et al. (2016) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Morita et al. (2016) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Prasad et al. (2015) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Adachi et al. (2014) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Mahajan et al. (2014) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Bereket et al. (2013) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Zapala-Pospiech et al. (2013) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
| Jain et al. (2013) | Yes | Yes | Yes | Yes | Yes | Yes | Yes | NR | Yes | Good |
| Colbert et al. (2012) | Yes | Yes | Yes | Yes | Yes | Yes | Yes | NR | Yes | Good |
| Pirklbauer et al. (2012) | Yes | Yes | NA | NA | Yes | NA | Yes | NA | Yes | Good |
Rating criteria: 0–1 NR=Good quality, 2–3 NR=Fair quality and 4–5 NR=Poor quality, NA: Not applicable, NR: Not reported
DISCUSSION
Odontogenic cysts arise as a result of inflammation or development of the epithelium of the tooth-forming apparatus.[5] The epithelial lining of the odontogenic cysts arises from reduced enamel epithelium, the epithelial cell rest of Serres, and the epithelial cell rest of Malassez.[5] Reduced enamel epithelium is the covering epithelium of the developing tooth crown, the epithelial cell rest of Serres is remaining degenerated dental lamina which initiated tooth formation at the sixth week of embryonic development, while the epithelial cell rest of Malassez is remnants of Hertwig’s epithelial root sheath disintegration which plays a role in dental root formation.[2,6] All of these remnants will be trapped in the gingiva and embedded in bone.[6] The epithelium trapped in gingiva and bone can develop into odontogenic cysts and may undergo neoplastic transformation.[6,7,8] The incidence of neoplasms which developed from odontogenic cysts accounts for <3%.[9,10,11]
The neoplastic lesions that developed from odontogenic cysts most likely arose from epithelial remnants of the cysts.[9,12,13] Prolonged inflammation, persistent intracystic pressure, and incomplete removal of the cystic epithelium have been associated with the transformation of odontogenic cysts to neoplasms.[9,11,13,14,15,16,17] Jain et al. stated that signs of odontogenic cyst long-standing chronic inflammation, such as the development of a sinus tract and pus discharge are considered as a feature of carcinoma.[18] Chronic inflammation may trigger the instability of the cell genes due to reactive oxygen species (ROS) formation.[9,19] ROS, such as superoxide ions, hydrogen peroxide, and hydroxyl ions, are produced in cells and able to react with nitric oxide to form reactive nitrogen ions as intermediates.[18] These reactive nitrogen intermediates can trigger carcinogenesis by damaging DNA, proteins, and cell membranes.[18] Chronic inflammation also induces cell apoptosis, cytokine production, keratinisation of the cystic epithelium, and causes DNA, protein, and cell membrane aberration, thus stimulating the transformation of normal cells to neoplastic cells.[11,18,19] However, a study by Borrás-Ferreres et al. reported a neoplastic transformation from a follicular cyst without chronic inflammation, suggesting the presence of additional physiopathological mechanisms which may be associated with oncogenes.[9] The exact causes of those transformations are still unknown.
There are characteristics that indicate the transformation of odontogenic cysts to neoplasms, one of which is the delay in healing after cystectomy (with or without dental extraction), swelling, pain, and the presence of the sinus tract.[9] Malignant changes are usually not seen radiographically in the early stages.[9] However, they will be seen as unilocular radiolucency with irregular scalloped and poorly defined edges, accompanied by eroded osseous cortical bone, indicating an invasive behavior.[9]
Among 19 studies reviewed in this study, the odontogenic cysts transformed into central mucoepidermoid carcinoma, primary intraosseous squamous cell carcinoma, ameloblastoma, squamous cell carcinoma, and ameloblastic carcinoma. Those neoplastic tissues originated from dentigerous cysts, odontogenic keratocysts, calcifying odontogenic cyst, glandular odontogenic cyst, residual cyst, radicular cyst, follicular cyst, and some unspecified odontogenic cysts. Some odontogenic cysts were unspecified due to late detection of the transformation, so it was difficult to trace the origin of the cystic lesions. In addition, the total samples from all cases were 27, consisted of 16 males (59%) and 11 females (41%), ranging from 15 to 86 years old. It can be noted that the transformation was slightly higher in male and irrespective of patients’ age. Young patients can also experience the transformation of odontogenic cysts into neoplasms, for example, in case report by Isshiki-Murakami et al., which reported an 18-year-old patient.[20]
These findings stress the importance of early diagnosis, early treatment, and long-term follow-ups.[13,20] Most reports suggest routine monitoring of odontogenic cysts, both clinically and radiographically, not only to avoid recurrence but also to monitor potential transformation to neoplasms. It is important to make an early diagnosis through an accurate radiological and histological examination, even if the lesion looks benign.[4,21,22,23,24] A histologic examination is considered as ‘sine qua non’ in diagnosing cystic and neoplastic lesions.[22] A thorough histologic examination is necessary to ensure that the patients are receiving adequate therapy.[25] Neoplasms that arise from cystic lesions were reported to have radiological ‘red flags’, such as bone erosion, large dimensions, and inferior alveolar nerve involvement,[26] that can help in early diagnosis. Other supporting examinations to confirm the diagnosis of neoplasms have been reported, such as MAML2 gene analysis[27] and immunohistochemistry examination.[28] Nagasaki et al. reported the first case of mucoepidermoid carcinoma from a glandular odontogenic cyst using MAML2 gene fusion analysis.[27] While Martinez et al. used immunohistochemistry in diagnosing odontogenic keratocysts that exhibit the potential for neoplastic transformation by detecting p53 gene.[28] This gene is usually negative in conventional odontogenic keratocysts, but p53 was positive in the primary intraosseous squamous cell carcinoma that developed from odontogenic keratocysts.[8,28] Moreover, Magic et al. also reported the association of genetic polymorphism of the PTCH1 IVS1-83 and GLI1 rs2228224 with the neoplastic transformation of odontogenic cysts.[29] These findings suggest that MAML2, p53, PTCH1 IVS1-83, and GLI1 rs2228224 can be useful to determine the potential for neoplastic transformation of odontogenic cysts, as well as pose as the target genes for potential treatment modalities.[27,28,30]
Treatments of odontogenic cysts to prevent neoplastic transformation were not yet standardised.[29,31] Many of the reports that we reviewed suggested that the treatment of odontogenic cysts should be carried out as conservatively as possible with sufficient margins. In the case of dentigerous cysts, the impacted tooth concerned should also be removed immediately to prevent the neoplastic transformation of the remnants of the cystic epithelium.[32,33,34] If the cyst is large, marsupialisation is recommended to prevent fracture or damage of important organs or tissues during enucleation. However, most literatures suggest that cyst enucleation is the preferred option as marsupialisation carries the risk of cystic cell retention and transformation to neoplasms.[35]
CONCLUSIONS
With the limit of this study, it can be concluded that most neoplastic transformation occurred from epithelial remnants of inadequate odontogenic cyst removal and from chronic inflammation due to infection, with or without predisposing genetic cofactors. Thus, the removal of odontogenic cysts must be carried out as optimally as possible to ensure the cystic lining is removed with sufficient margin to reduce the risk of neoplastic transformation from remnants of the cyst epithelium. In addition, monitoring odontogenic cysts both clinically and radiographically, before and after surgery, is essential to avoid recurrence and neoplastic transformation. Thorough radiological and histological examinations are keys for early diagnosis to determine accurate treatment plans for the patients. Although genetic mutation and the presence of some genes, such as MAML2 and p53 have been suspected to have crucial roles in the neoplastic transformation of odontogenic cysts, the exact causes of this phenomenon remain unclear. Further studies, especially randomised controlled trials are still needed to investigate potential etiologies and the exact mechanisms of the neoplastic transformation of odontogenic cysts.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
ANNEXURE
Data extraction of the 19 reviewed articles
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data extraction of the 19 reviewed articles