Abstract
Introduction
Despite being a benign pathology, ameloblastoma is considered to be locally-aggressive and has a high recurrence-rate. The following study describes the experience in a tertiary care hospital to manage ameloblastoma using treatment modalities based on the site of occurrence and histologic-type and to evaluate recurrence in long term.
Material and methods
In this 21-year-long retrospective study, 92 patients were followed-up for a minimum period of 5-years (range 5–21 years) to assess the clinical and demographic characteristics, treatment-procedure performed, and outcomes including the recurrence-rate associated with different treatment-strategies for treating ameloblastoma.
Results
Out of 92 cases, 90 had mandibular involvement, with the most frequent site being Body (B), and Angle and Ramus (AR) region. The most prevalent histological-subtype was plexiform ameloblastoma. Five cases had mixed histopathologic-presentations in which more than one histological variant was found simultaneously. Segmental resection with reconstruction using a reconstruction plate was the most commonly employed surgical procedure for all histologic types. One case of plexiform ameloblastoma that underwent marginal resection presented with a recurrence at 189 months.
Conclusions
Based on the observed results, it is concluded that adequate surgical planning along with long-term follow-up may provide the desired results and reduce the rate of recurrence.
Supplementary Information
The online version contains supplementary material available at 10.1007/s12663-024-02197-2.
Keywords: Ameloblastoma, Odontogenic tumors, Mandibular neoplasms, Oral pathology, Recurrence, Retrospective studies
Introduction
Ameloblastoma, the second most common odontogenic tumor, is also one of the most documented and extensively researched benign tumor affecting the maxillofacial region. Usually diagnosed between 30 and 60 years of age, it accounts for about 1% of all head and neck tumors and about 9–11% of all odontogenic tumors. While both jaws are affected, it is most frequently encountered in the lower jaw, especially in the mandibular posterior region. Although considered benign and usually non-fatal, it shows a locally invasive growth pattern with destruction of the jaws and the surrounding tissues, causing a profound impact on the quality of life [1–4]. Fatality due to ameloblastoma is a rare occurrence and is usually associated with delayed treatment, particularly in cases with intracerebral extension or due to its malignant variant metastasizing to vital organs [5–8].
In the 2005 WHO classification, they were classified as solid/multicystic, extraosseous/peripheral, desmoplastic, and unicystic types. Solid/multicystic ameloblastomas were again sub-classified histopathologically into follicular, plexiform, acanthomatous, granular cell, and basal cell variants. But in 2017, WHO reviewed this and narrowed it to Solid/multicystic ameloblastoma, unicystic ameloblastoma, and extraosseous/peripheral types [9, 10]. With simple enucleation, solid and multicystic ameloblastomas have a high recurrence rate (60–80%) and necessitate more aggressive therapy [11]. Recurrence can occur from 1 to 18 years after surgery, with most occurring between the second and fifth years postoperatively [12, 13]. Among the histopathologic types, desmoplastic ameloblastoma is considered to be the most aggressive with high a recurrence rate [14].
Though the most effective treatment for ameloblastoma remains a topic of debate, the evidence favors radical treatment for both unicystic and solid or multicystic variants [15–17]. Radical treatment comes at a cost as it can lead to severe disfigurement and associated functional sequelae, which necessitate additional reconstructive and rehabilitative procedures. Resection with safety margins and immediate reconstruction can provide good oral function and high quality of life while reducing the incidence of recurrence [18–20].
The author’s institute, being a tertiary care center, is frequented by numerous referrals for the management of maxillofacial pathologies [21]. Among them, one of the most prevalent pathology is ameloblastoma. This retrospective study aimed to assess the clinical and demographic characteristics, treatment procedure performed, and outcomes including the recurrence rate associated with different treatment strategies for treating ameloblastoma in a tertiary care hospital spanning a period of almost two decades.
Materials and Methods
This retrospective study was conducted by collecting the records of patients who were operated on for the management of maxillary/ mandibular ameloblastoma by a single surgeon from January 2002 to March 2018. The data collected included demographic data, site and extent of tumor, type of Ameloblastoma, time of surgery, treatment strategy used, duration of follow-up, and recurrence, if any, during the follow-up period. Patients were followed up for at least 5 years, with the most recent follow-up occurring in May 2023.
All the cases included in the study were biopsy-proven intraosseous ameloblastoma in which treatment was decided according to the evidence-based data available in the literature. Extraosseous/peripheral ameloblastomas were excluded from the study. Patients were grouped into cases that underwent Conservative treatment (curettage/enucleation followed by peripheral ostectomy and/or physicochemical treatment with liquid nitrogen or Carnoy’s solution) or Radical treatment (marginal or segmental resection with or without disarticulation) depending on the extent and histological variant. The method of reconstruction, if any, was also noted. The postoperative histopathologic diagnosis of each case was also included in the data. The duration of follow-up was noted in months, and instances of recurrence were recorded during the follow-up period. Patients lost to follow-up within 5 years following surgery were excluded from the study.
Results
The retrospective analysis spanning 21 years (2002–2023) showed that 92 cases underwent definitive surgery for ameloblastoma. The mean age of the study subjects was 32.30 ± 15.06 and consisted of 30 (32.61%) females and 62 (67.39%) males, i.e., the female: male ratio was 1:2.07. The data showed that 90 (97.83%) cases out of a total of 92 cases had mandibular involvement, while only two (2.17%) had maxillary involvement. Both sides of the mandible were almost equally involved, with 39 (42.39%) cases on the right side and 42 (45.65%) cases on the left side. It was found that the lesion crossed midline in 13 (14.13%) patients with exclusive Symphysis (S) involvement, representing only 8 (8.70%) cases. Within the mandible, the lesion was mostly located in the Body (B), Angle and Ramus (AR) regions. However, Coronoid and Condylar (CC) involvement was also not uncommon. 26 (28.26%) cases had a combination of B + AR regions, while 22 (23.91%) and 15 (16.30%) cases had pathology in isolated B and AR regions respectively. 14 (15.22%) cases showed CC involvement, with 10 (10.87%) having AR and 4 (4.35%) having B + AR + CC extension (Fig. 1 and Table 1).
Fig. 1.
Diagrammatic representation of the distribution of Ameloblastoma within the mandible as recorded in the study. S, Symphysis and parasymphysis of mandible; B, Body of mandible; AR, Angle and ramus region; CC, Coronoid and condylar region
Table 1.
Incidence of histopathologic types of ameloblastoma and their distribution within the mandible as recorded in the study
With 33 (35.87%) cases out of 92, Plexiform ameloblastoma was the most predominant histopathologic variant in the current study. Follicular type was found to be the second most common and constituted 19 (20.65%) cases, one of which was a recurrent case. There were 15 (16.30%) cases of Acanthomatous type, followed closely by 13 (14.13%) cases of Unicystic ameloblastoma. Granular Cell variant constituted 5 (5.44%) cases, while there were 2 (2.17%) cases of Desmoplastic variant. No Basal Cell variant of ameloblastoma was identified in this retrospective analysis. There were 5 (5.44%) cases of mixed histopathologic presentation, among which 3 (3.26%) were a combination of Acanthomatous and Plexiform ameloblastoma. A combination of Follicular with Plexiform and Follicular with Granular Cell ameloblastoma represented 1 (1.09%) of each of the mixed variants (Table 1).
Conservative treatment, which involved rigorous curettage/ enucleation of the lesion followed by peripheral ostectomy and/or physicochemical treatment with liquid nitrogen or Carnoy’s solution, was done in 11 (11.96%) of the cases, while the rest of the 81 (88.04%) cases were treated by radical approach. Conservative approach was employed in six (6.52%) cases of Unicystic ameloblastoma and in two (2.17%) instances of Follicular and Acanthomatous variants respectively. It was also done in one case of plexiform variant. Marginal resection was done in two (2.17%) cases, and 79 (85.87%) cases underwent Segmental resection with or without reconstruction. Among the patients who underwent segmental resection of the mandible, 7 (7.61%) cases didn’t undergo any reconstruction, while 55 (59.78%) cases underwent reconstruction only with a reconstruction plate (RP). Reconstruction using iliac crest graft (ICG) was done in 7 (7.61%) cases while costochondral graft (CCG) was used in 4 (4.35%) cases involving the mandible. Two (2.17%) patients underwent mandibular reconstruction with non-vascularized free fibular graft (NVFFG), and in three cases (3.26%) transport distraction osteogenesis (TDO) was performed to reconstruct the defect. The left maxillary defect caused by segmental resection was reconstructed by temporalis myofascial flap (TF). Segmental resection with reconstruction using a reconstruction plate was the most commonly used surgical procedure in all histologic types (Fig. 2 and Table 2).
Fig. 2.
Details of treatment approach provided to the ameloblastoma cases. C, Conservative treatment (curettage/enucleation followed by peripheral ostectomy and/or physicochemical treatment with liquid nitrogen or Carnoy’s solution); MR, Marginal resection; SR, Segmental resection; RP, Reconstruction plate; ICG, Iliac crest graft; CCG, Costochondral graft; TDO, Transport distraction osteogenesis; NVFFG, Non vascularized free fibular graft; TF, Temporalis myofascial flap
Table 2.
Details of treatment provided according to histopathologic type of ameloblastoma
| Treatment approach | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| C | MR | SR | SR + RP | SR + ICG | SR + CCG | SR + TDO | SR + NVFFG | SR + TF | Total | ||
| Histopathologic variant | Mixed | 0 | 0 | 1 | 4 | 0 | 0 | 0 | 0 | 0 | 5 |
| Plexiform | 1 | 1* | 2 | 20 | 3 | 4 | 1 | 0 | 1 | 33 | |
| Follicular | 2 | 0 | 1 | 12 | 0 | 0 | 2 | 2 | 0 | 19 | |
| Acanthomatous | 2 | 0 | 2 | 8 | 3 | 0 | 0 | 0 | 0 | 15 | |
| Unicystic | 6 | 1 | 0 | 5 | 1 | 0 | 0 | 0 | 0 | 13 | |
| Granular Cell | 0 | 0 | 1 | 4 | 0 | 0 | 0 | 0 | 0 | 5 | |
| Desmoplastic | 0 | 0 | 0 | 2 | 0 | 0 | 0 | 0 | 0 | 2 | |
| Total | 11 | 2 | 7 | 55 | 7 | 4 | 3 | 2 | 1 | 92 | |
C, Conservative treatment (curettage/enucleation followed by peripheral ostectomy and/or physicochemical treatment with liquid nitrogen or Carnoy’s solution); MR, Marginal resection; SR, Segmental resection; RP, Reconstruction plate; ICG, Iliac crest graft; CCG, Costochondral graft; TDO, Transport distraction osteogenesis; NVFFG, Non vascularized free fibular graft; TF, Temporalis myofascial flap
*Recurrence
The location and extent of the lesion also influenced the treatment approach; e.g., in four cases where the lesion extended into the CC region, SR + CCG was employed so as to reconstruct the temporomandibular joint. The details of the treatment approach according to the location of ameloblastoma are given in Table 3. The follow-up period of these patients ranged from 5 to 21 years, with the mean follow-up period being 156.25 ± 54.43 months (13.02 ± 4.54 years). Among these cases, only one (1.09%) patient who underwent marginal resection for plexiform ameloblastoma in the right AR region of the mandible presented with recurrence at 189 months.
Table 3.
Details of treatment provided according to location of ameloblastoma
| Treatment Approach | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| C | MR | SR | SR + RP | SR + ICG | SR + CCG | SR + TDO | SR + NVFFG | SR + TF | TOTAL | ||
| Site | S | 2 | 0 | 0 | 3 | 2 | 0 | 1 | 0 | 0 | 8 |
| S + B | 0 | 0 | 0 | 3 | 0 | 0 | 0 | 0 | 0 | 3 | |
| S + B + AR | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | |
| B + S + B | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | |
| B | 5 | 1 | 4 | 8 | 2 | 0 | 2 | 0 | 0 | 22 | |
| AR | 3 | 1* | 2 | 9 | 0 | 0 | 0 | 0 | 0 | 15 | |
| B + AR | 0 | 0 | 0 | 22 | 2 | 0 | 0 | 2 | 0 | 26 | |
| AR + CC | 0 | 0 | 1 | 4 | 1 | 4 | 0 | 0 | 0 | 10 | |
| B + AR + CC | 0 | 0 | 0 | 4 | 0 | 0 | 0 | 0 | 0 | 4 | |
| Maxilla | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 2 | |
| Total | 11 | 2 | 7 | 55 | 7 | 4 | 3 | 2 | 1 | 92 | |
C, Conservative treatment (curettage/enucleation followed by peripheral ostectomy and/or physicochemical treatment with liquid nitrogen or Carnoy’s solution); MR, Marginal resection; SR, Segmental resection; RP, Reconstruction plate; ICG, Iliac crest graft; CCG, Costochondral graft; TDO, Transport distraction osteogenesis; NVFFG, Non vascularized free fibular graft; TF, Temporalis myofascial flap; S, Symphysis and parasymphysis of mandible; B, Body of mandible; AR, Angle and ramus region; CC, Coronoid and condylar region
*Recurrence
Discussion
Ameloblastoma has been a topic of considerable interest and is one of the most extensively researched and catalogued pathology associated with the oral and maxillofacial region. They are aggressive benign neoplasms of odontogenic origin, principally of the enamel organ and usually occur between 30 and 60 years of age, with equal predilection for both genders. Though this study reported a mean age of incidence comparable to the available literature, it showed more of a male predilection with a female: male ratio of 1:2.07, contrary to the 1:1 ratio reported in most of the literatures [2, 4]. Approximately 80% of all ameloblastoma are found in the mandible, especially in the posterior region [2, 4, 22]. Similarly, our series also showed a striking 97.83% mandibular involvement with a strong predilection for the posterior mandible. Only two cases of maxillary ameloblastoma were reported in this series.
Radiographically, multicystic ameloblastoma usually appears as a multilocular radiolucency with well-defined, corticated, scalloped margins and has a pronounced tendency to cause extensive root resorption, tooth migration, and displacement [23, 24]. Histopathologically, the most common variants are follicular and plexiform accounting for an incidence of 32.5% and 28.2% respectively while desmoplastic is extremely rare with incidence ranging from 4–13% [25, 26]. Most of the studies emphasized that the histological subtypes and radiographic features have a prognostic value, considering granular cell and desmoplastic variants as more aggressive [9, 20, 27, 28]. Plexiform ameloblastoma (35.87%) was the most predominant histopathologic type in this study, followed by follicular variant (20.65%). Mixed or Hybrid ameloblastoma displaying a combination of the histological variants, though rare, is well documented in the literature [25, 26, 29, 30]. Only five such cases involving the mandible were encountered in this study.
Unicystic and peripheral ameloblastomas are usually managed conservatively, while solid/multicystic variants require a more radical approach [11, 27, 28]. In children and young adults, a conservative approach with regular follow-ups can be advocated owing to their growth potential and to alleviate the psychological impact of radical treatment. In this study, Radical resection with 0.5 to 1 cm margins was the most commonly employed method, as it is associated with a lower recurrence rate [18, 21]. In our center, conservative treatment was chosen only after considering the patient’s age, histologic type, and extent of ameloblastoma. This included curettage/enucleation followed by peripheral ostectomy and/or physicochemical treatment with liquid nitrogen or Carnoy’s solution and primary closure.
Few authors, like Vayvada et al. [18] and Pappalardo et al. [19] have advocated immediate reconstruction with graft or vascularized bone flap following segmental resection, as reconstruction is considered to have significantly better functional outcomes, less post-operative aesthetic concerns, and improved quality of life [21]. However, in our institute, most of the cases underwent immediate jaw reconstruction with the application of a reconstruction plate only, owing to the fact that most of the patients came from a low-literacy background and were not willing to additional surgical site exposure for procurement of graft. In this study, apart from use of the ICG and CCG, NVFFG and DO were also utilized successfully for immediate jaw reconstruction. Most of the patients underwent prosthodontic rehabilitation to facilitate function and improve their quality of life. The authors suggested an algorithm for the management and follow-up of ameloblastoma based on their experience and study findings. (Fig. 3).
Fig. 3.
Proposed algorithm for management and follow-up of maxillary and mandibular ameloblastoma
According to the available literature, recurrence in ameloblastoma is common and more than 50% of all recurrences occur within 5 years postoperatively. It is usually seen more frequently in the solid type, with the recurrence rate significantly higher in the Desmoplastic variant and the follicular variant has more recurrence rate than that of the plexiform variant [12, 15, 27, 28]. In this study, only one case of plexiform ameloblastoma treated by marginal resection had recurrence at 189 months of review, which was addressed by segmental resection and reconstruction with ICG and reconstruction plate.
The drawback of the study is that none of the patients underwent free flap reconstruction, as this treatment modality is unavailable at the author’s institute. But those who underwent reconstruction with autogenous grafts showed good results with prosthetic rehabilitation using dentures or dental implants. Nevertheless, in most of the patients, reconstruction was done with a reconstruction plate only, thus compromising their quality of life.
Conclusion
This retrospective analysis documented the experience of treating ameloblastoma in a tertiary care hospital over a period of two decades. Patients were followed up for at least five years (range: five to twenty-one years) during the study's twenty-one-year duration in order to assess recurrence. In 90 of the 92 cases, the mandibular region was involved, with the Body (B), Angle, and Ramus (AR) regions being the most frequently affected areas. Plexiform ameloblastoma represented the most typical histological subtype. There were multiple histological variants identified simultaneously in five patients with mixed histopathologic presentations. All histologic groups were treated with the most frequent surgical technique i.e., segmental excision with reconstruction using a reconstruction plate. According to the data of the study, it can be concluded that careful surgical planning backed by a proper radiological and histopathological assessment and long-term monitoring could deliver the desired outcomes while reducing the recurrence rates. Nevertheless, the surgeon should be prepared to modify the surgical plan based on their professional judgement. A multidisciplinary team involving competent maxillofacial surgeons, prosthodontists, and reconstructive surgeons can considerably improve the quality of life of the patients.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
We acknowledge the support provided by the Department of Oral Pathology and Microbiology and the Department of Prosthodontics for assessment and treatment planning.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declarations
Conflict of interest
None.
Footnotes
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