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Odontogenic tumours, a collaborative retrospective study of 75 cases covering more than 25 years from Estonia
ARTICLE IN PRESS Journal of Cranio-Maxillofacial Surgery (2004) 32, 161–165 r 2004 European Association for Cranio-Maxillofacial Surgery. doi:10.1016/S1010-5182(04)00007-1, available online at http://www.sciencedirect.com
Odontogenic tumours, a collaborative retrospective study of 75 cases covering more than 25 years from Estonia Tiia Tamme1, Marianne Soots1, Andres Kulla2, Kert Karu3, Siiri-Mai Hanstein3, Airi Sokk3, 4 * Enn Joeste , Edvitar Leibur1 Department of Maxillofacial Surgery (Chairman: Dr. Peeter Mu. ursepp), University of Tartu, Tartu . 51014, Estonia; 2 Department of Pathology (Chairman: Dr. Andres Kulla), University of Tartu, Tartu, Estonia; 3 Department of Maxillofacial Surgery (Chairman: Dr. Hamor Kaha), Tallinn, Estonia; 4 Department of Pathology (Chairman: Dr. Enn Joeste), * Mustamae . Hospital, Tallinn, Estonia 1
SUMMARY. Introduction: The aim of the present collaborative study was to analyse retrospectively the character of odontogenic tumours in Estonia, involving the entire Estonian population (1.4 million), and to compare their prevalence with the figures presented in similar reports from other countries. Material and methods: All material for the retrospective study was retrieved from the files of the Departments of Maxillofacial Surgery in Tartu and Tallinn, Estonia, where all in/out-patients are treated from the whole country. The final diagnosis in each case of odontogenic tumour was based on the 1992 WHO histological criteria. Results: A total of 75 odontogenic tumours was found, 74 (98.6%) of which were benign, and 1 (1.3%) was malignant. The frequency of odontogenic tumours in this study was the lowest ever reported. The most common tumours were odontoma (34.3%), followed by ameloblastoma with different subtypes (25.3%), ameloblastic fibroma (16%), odontogenic myxoma (12%) and benign cementoblastoma (8%). Conclusion: Odontogenic tumours are relatively rare in Estonia compared with the data from other countries. r 2004 European Association for Cranio-Maxillofacial Surgery.
Keywords: Odontogenic tumours; Retrospective study; Prevalence
By taking into account that all in- and outpatients with pathology in the maxillofacial region were treated in the only two Departments of Maxillofacial Surgery in Tartu and in Tallinn, the aim of the present collaborative study was to analyse retrospectively the character of odontogenic tumours in Estonia and to compare their prevalence with the figures presented in similar reports from other countries.
INTRODUCTION Odontogenic tumours occur as a result of disturbances in the development of teeth and associated structures (Eversole et al., 1971; Gold, 1991). They share two major characteristics, namely they arise from the tissue with the potential for differentiation into tooth or periodontal structures, and therefore found exclusively in the mandible and maxilla and, on rare occasions, the gingiva. Another variable but distinctive feature includes formation of tooth-related extracellular substances some of which may calcify and be visible on radiographs; they are a product of epithelial–mesenchymal interactions (Gallagher and Shklar, 2000). The biological behaviour of these lesions ranges from hamartoma-like lesions and benign neoplasms to rare, aggressive, malignant tumours. The most common sites are the mandibular molar region and the maxillary cuspid region. Odontogenic tumours are usually slow growing and asymptomatic. Certain odontogenic tumours have a predilection for particular ages, gender, geographic location, and race (Sawyer et al., 1985; Assael, 1992). To our knowledge, there are no reports on the frequency of these lesions either from Estonia or from any other Baltic State. Some reports deal with the prevalence in neighbouring countries (Finland, Happonen et al., 1982; and Poland, Stypulkowska, 1998).
MATERIAL AND METHODS This collaborative retrospective study is based on data from the following institutions: Departments of Maxillofacial Surgery and of Pathology, Tartu University Hospital, Tartu (42 cases; 1977–2001) and Departments of Maxillofacial Surgery and of Pathology, Mustam.ae Hospital, Tallinn (33 cases, 1981–2001). Haematoxylin and eosin stained sections were reviewed to confirm or to correct a previous histologic diagnosis according to the criteria suggested for the revised World Health Organization (WHO) classification (Kramer et al., 1992). The necessary clinical information, including patient age and gender, and tumour location was obtained from records when available. 161
ARTICLE IN PRESS 162 Journal of Cranio-Maxillofacial Surgery
For tumour location the following scheme was used. The maxilla was divided into 6 anatomical regions, 3 on either side: anterior (from the midline to the distal surface of the canine), premolar (from the mesial aspect of the first premolar to the distal side of the second premolar), and molar (from the mesial aspect of the first molar distally). The mandible was divided into 5 anatomical regions on each side: anterior and premolar as described above, molar (from the mesial aspect of the first molar to the distal side), angle (distal side of third molar to inferior portion of ramus, beneath the occlusal plane), and ramus (upper portion of ramus above the occlusal plane).
RESULTS The sources of odontogenic tumours are given in Table 1. It shows the frequency of odontogenic tumours found among all biopsy specimens, including all other benign and malignant tumours of the oral and maxillofacial regions. The distribution of histological types and frequency of odontogenic tumours is presented in Table 2. There were altogether 75 odontogenic tumours. Of these, 74 (98.6%) were benign, and 1 (1.3%) was malignant.
Table 1 – Sources of odontogenic tumours Source (years)
Biopsies
Departments of Maxillofacial Surgery and of Pathology, Tartu University Clinics (1977–2001)
4089
Departments of Maxillofacial Surgery and of Pathology, Mustam.ae Hospital, Tallinn (1981–2001)
6052
Total
Odontogenic tumours (%) 42 (1.03)
The most frequent benign tumour was odontoma (compound, complex; 34.3%), followed by ameloblastoma with different subtypes (25.3%), ameloblastic fibroma (16%), odontogenic myxoma (12%) and benign cementoblastoma (8%). The other, less common types were calcifying epithelial odontogenic tumour and adenomatoid odontogenic tumour, accounting for 1.3% each. There was only one malignant odontogenic tumour, namely primary intraosseous carcinoma (1.3%). The nineteen ameloblastomas were subdivided into 2 biologic-microscopic subtypes: 13 solid or multicystic ameloblastomas and 6 unicystic ameloblastomas. The 75 lesions were found in 28 males and in 47 females. The overall male to female ratio was 1:1.7. The gender distribution is listed in Table 3 and the age distribution in Table 4. Fifty-one cases (68%) were found during the second, third and fourth decades and, in the sixth
Table 2 – Histologic type and frequency of odontogenic tumours Tumours type
No. of tumours
Benign 1. Odontoma Compound Complex 2. Ameloblastoma Multicystic Unicystic 3. Ameloblastic fibroma 4. Odontogenic myxoma 5. Benign cementoblastoma 6. Calcifying epithelial odontogenic tumour 7. Adenomatoid odontogenic tumour
26
12 9 6 1
34.6 16 18.6 25.3 17.3 8 16 12 8 1.3
1
1.3
1
1.3
12 14 19 13 6
33 (0.55) Malignant 9. Primary intra-osseous carcinoma
10,141
Percentage
75 (0.74)
Total
75
100
Table 3 – Gender distribution of odontogenic tumour cases Type of tumour
Number
Male
Female
Male:female ratio
Odontoma Compound Complex Ameloblastoma Multicystic Unicystic Ameloblastic fibroma Odontogenic myxoma Benign cementoblastoma Calcifying epithelial odontogenic tumour Adenomatoid odontogenic tumour Primary intraosseous carcinoma
26 12 14 19 13 6 12 9 6 1 1 1
8 3 5 10 7 3 5 4 1 0 0 0
18 9 9 9 6 3 7 5 5 1 1 1
1.0:2.3 1.0:3.0 1.0:1.8 1.1:1.0 1.0:1.0 1.0:1.0 1.0:1.4 1.0:1.3 1.0:5.0 NA NA NA
Total
75
28
47
1:1.7
NA, not applicable.
ARTICLE IN PRESS Odontogenic tumours 163 Table 4 – Age distribution of odontogenic tumour cases Type of tumour
Number of cases
Age (years) 0–10
11–20
21–30
31–40
41–50
51–60
61–70
71–80
Mean
— — — 2 2
Odontoma Compound Complex Ameloblastoma Multicystic Unicystic Ameloblastic fibroma Odontogenic myxoma Benign cementoblastoma Calcifying epithelial odontogenic tumour Adenomatoid odontogenic tumour Primary intra-osseous carcinoma
26 12 14 19 13 6 12 9 6 1 1 1
4 3 1 1 — 1 — 4 — — — —
8 4 4 3 1 2 2 — 2 — — —
8 3 5 2 1 1 1 3 — — — —
4 1 3 2 1 1 1 1 1 — 1 —
— — — — — — 7 1 1 — — —
1 — 1 7 6 1 — — 2 1 — 1
1 1 — 2 2 — 1 — — — — —
— — — — — —
23.7 21.8 25.4 44.7 48.7 38.5 39.2 18.0 36.6 (51.0) (38.0) (58.0)
Total
75
9
15
14
10
9
12
4
2
32.5
decade of life. The members in the sixth decade can be attributed mainly to the high prevalence of (multicystic) ameloblastomas in elderly people. The site distribution is summarized in Table 5. In general, there was a predilection for mandibular tumours (mandibular to maxillary ratio 1.6:1), which was particularly marked for ameloblastomas (mandible to maxilla 2.8:1). In contrast, 2 (out of 6) benign cementoblastomas occurred in the maxilla (!), the maxilla to mandible ratio being 1:2. The most frequently affected areas were the premolar (20%) and molar regions (21.3%) in the mandible and the most common location in the maxilla was the premolar region (17.3%). DISCUSSION Odontogenic tumours are relatively uncommon lesions. The present study comprised all odontogenic tumours taken care of in Estonia during 1977–2001. Estonia is a small Baltic State with a population of 1.4 million (German, 2001) and the treatment of all odontogenic tumours is concentrated at two medical institutions with their in- and out-patient clinics. The study period involved profound changes in the political situation in Estonia (transition from socialist economy to free market economy), while the organization of the treatment of odontogenic tumours was not altered. The frequency of odontogenic tumours among all oral and maxillofacial biopsy specimens was 0.74%, ranging from 0.55% at Mustam.ae Hospital to 1.03% at Tartu University Clinics. Despite the obvious need to know the prevalence of odontogenic tumours, there are surprisingly few relevant reports. Bhaskar examined benign and malignant odontogenic tumours in 1969, and Regezi et al., in 1978, both among American populations. More recently, additional case series have been reported from Turkey (Gunham et al., 1990), Germany (Mothes . et al., 1991), Canada (Daley et al., 1994), Zimbabwe (Chidzonga et al., 1996a, b), Nigeria (Arotiba et al.,
1997), Mexico (Mosqueda-Taylor et al., 1997), China (Lu et al., 1998), and Poland (Stypulkowska,1998). We recorded 75 cases of odontogenic tumours for the period of 25 years (1977–2001) in Estonia, from the database of University Clinics (1977–2001 and from the database of Mustam.ae Hospital which opened in 1981 (1981–2001). Inasmuch as Estonia is a small Baltic State with a population of 1.4 million, it is difficult to perform a comparative analysis of different populations. However, the frequency of odontogenic tumours among all biopsy cases in our series was 0.74%, which is the lowest ever reported in the literature, being as high as 30% in a Nigerian study (Arotiba et al., 1997) and as low as 1.1% in a Finnish study (Happonen et al., 1982) and in a Canadian study (Daley et al., 1994). Although the vast majority of odontogenic tumours were benign, there were some interesting differences regarding their prevalence that should be mentioned: The most frequent tumours in the present study were compound and complex odontomas (34.3%), the result being similar to that of a Mexican study (Mosqueda-Taylor et al., 1997). The prevalence for the Estonian population was almost twice as high as that recorded for a Turkish (18%) population (Gunham et al., 1990). . In most other series from Canada, Finland, America and Germany, compound and complex odontomas accounted for 51.5% to 74% of odontogenic tumours (Bhaskar, 1969; Regezi et al., 1978; Happonen et al., 1982; Mothes et al., 1991; Daley et al., 1994). In contrast, the incidence of compound and complex odontomas was low in the series involving Chinese (6.2%) and Nigerian populations (Chung et al., 1969; Wu and Chan, 1985; Arotiba et al., 1997; Lu et al., 1998). It is difficult to perform a comparative analysis of the frequency of odontomas, because these tumours are interpreted as developmental malformations or hamartomas rather than true neoplasms (Gallagher and Shklar, 2000; Assael, 1992). This lesion is usually
ARTICLE IN PRESS
1.0:1. 6 45 2 8 16 15 6 28 7 13 8 75
— 1
Total
— 1 — — — 1 — — —
—
—
— 1 — — — 1 — — —
13 5 8 14 9 5 9 5 4 —
1
—
Ramus
— — — 2 1 1 — — — — 1 1 — 4 3 1 1 1 1 —
Angle Molar
2 — 2 6 4 2 5 1 2 — 6 2 4 1 — 1 3 2 1 —
Premolar Anterior
4 2 2 1 1 — — 1 — — 13 7 6 5 4 1 3 4 2 1
Total Molar Premolar
7 3 4 1 1 — — — — — 26 12 14 19 13 6 12 9 6 1
Odontoma Compound Complex Ameloblastoma Multicystic Unicystic Ameloblastic fibroma Odontogenic myxoma Benign cementoblastoma Calcifying epithelial odontogenic tumour Adenomatoid odontogenic tumour Primary intra-osseous carcinoma
Anterior
1 1 — 3 2 1 1 1 1 —
Mandible Maxilla Number Type of tumour
Table 5 – Distribution of odontogenic tumours by location
5 3 2 1 1 — 2 3 1 1
Total
1.0:1.0 1.0:0.7 1.0:1.3 1.0:2.8 1.0:2.3 1.0:5.0 1.0:3.0 1.0:1.3 1.0:2.0 —
Maxilla:mandible
164 Journal of Cranio-Maxillofacial Surgery
discovered on routine radiographic examination and it does not produce pain; treatment is generally provided by dentists or oral surgeons in Western countries. Only problematic odontomas commonly require hospital management. In Estonia, the treatment of all odontogenic tumour cases is concentrated at two institutions and is documented in their databases, which is related to tradition (referral by dentists) and to the small population. Hence, the institutional background and the specific features of the country appear essential in assessment of compound and complex odontomas. Ameloblastoma with its different subtypes appears to be particularly frequent in Africa (Mosadomi, 1975; Odukoya, 1995; Chidzonga et al., 1996a, b; Arotiba et al., 1997), and some Asian populations (Kovi and Laing, 1966; Chung et al., 1969; Reddy, 1974; Wu and Chan, 1985; Lu et al., 1998; Tay, 1999). In the present series, ameloblastoma was the second most common tumour, accounting for 25.3% of all cases, which is similar to the corresponding figure in a German study (Mothes et al., 1991). We compared our data to those from Finland and Poland, both in close geographic proximity to Estonia, where the respective data were 8.8% and 36.6% (Happonen et al., 1982; Stypulkowska, 1998). In the present study, the age distribution of ameloblastoma was higher (mean age 44.7 years) than that reported by other researchers, but consistent with the results of Reichart et al. (1995) who compared 3677 ameloblastomas in a metaanalysis from different continents and found that the patients mean age, 42.3 years, was considerably higher in European countries than the other continents. When comparing the age distribution among the two subtypes of ameloblastomas in this study, an obvious contrast between multicystic and unicystic ameloblastomas was found. The mean age of the patients with unicystic ameloblastoma (23.3 years) was much lower than that of the patients with classical (solid or multicystic) ameloblastomas (49.3 years). The average age of the patients with unicystic ameloblastoma was similar to that reported by Ackermann et al. (1988; 23.8 years). Regarding the other types of odontogenic tumours, the most significant difference in this study was found in the frequency of ameloblastic fibroma in this study (16%), which was significantly higher than that presented in other reports (Daley et al., 1994; Lu et al., 1998; Chidzonga et al., 1996b; MosquedaTaylor et al., 1997; 8%, Happonen et al., 1982, 53%). The gender, age and site distributions of this neoplasm were also different from those presented in other reports. This finding requires further attention, as the authors cannot provide an explanation for this difference at present. Odontogenic myxoma constituted 12% of all odontogenic tumours in the present study. This figure is considerably higher than that presented in German (Mothes et al., 1991) and North American (Bhaskar, 1969; Regezi et al., 1978) studies but is similar to that
ARTICLE IN PRESS Odontogenic tumours 165
reported for African populations (Chidzonga et al., 1996a; Odukoya, 1995; Arotiba et al., 1997). Six cases (8%) met the recent WHO criteria for the diagnosis of benign cementoblastoma. The proportion of benign cementoblastomas in this series is larger than in North American (Regezi et al., 1978; Daley et al., 1994), Mexican (Mosqueda-Taylor et al., 1997) and African studies (Odukoya, 1995; Arotiba et al., 1997) but is similar to the proportions reported from Poland (Stypulkowska, 1998) and Finland (Happonen et al., 1982), both geographically close to Estonia. The site distribution of benign cementoblastoma was different from that found in other studies. In the present study, two out of six benign cementoblastomas were located in the upper jaw, the maxilla to mandible ratio being 1:2. However, our results were similar to those of Minderjahn (1979). This tumour displayed a remarkable topographic affinity for the premolar and molar regions (nearly 100% were located here). The other odontogenic tumours included calcifying epithelial odontogenic tumour, adenomatoid odontogenic tumour and primary intraosseous carcinoma. However, all these were only represented by one case each, which is a number too small for analysis.
CONCLUSION Based on this collaborative retrospective study which involved the entire Estonian population it was concluded: Odontogenic tumours are relatively rare in Estonia compared with other countries. There were differences in the prevalence of certain odontogenic tumours in comparison with data from other countries.
References Ackermann GL, Altini M, Shear M: The unicystic ameloblastoma: a clinicopathological study of 57 cases. J Oral Pathol 17: 541–546, 1988 Arotiba JT, Ogunbiyi JO, Obiechina AE: Odontogenic tumours: a 15-year review from Ibadan, Nigeria. Br J Oral Maxillofac Surg 35: 363–367, 1997 Assael LA: Surgical management of odontogenic cysts and tumors. In: Peterson LJ, Indresana AT, Marciani RD, Roser SM, (eds.), Principles of Oral and Maxillofacial Surgery. Philadephia: Lippincott, 1992; 692–711 Bhaskar SN: Synopsis of oral pathology. St Louis: CV Mosby, 1969; 225–258 Chidzonga MM, Lopez VM, Alverez PP: Odontogenic tumors: analysis of 148 cases in Zimbabwe. Central Afr J Med 42: 158–161, 1996a Chidzonga MM, Lopez Perez VM, Portilla Alvarez AL: Ameloblastoma: the Zimbabwean experience over 10 years. Oral Surg Oral Med Oral Pathol 82: 38–41, 1996b Chung DH, Kinnman JEG, Lee BC, Lee YT: Tumors of the jaws in Korea: report of 157 cases. Oral Surg Oral Med Oral Pathol 27: 716–728, 1969
Daley TD, Wysocki GP, Pringle GA: Relative incidence of odontogenic tumors and oral and jaw cysts in a Canadian population. Oral Surg Oral Med Oral Pathol 77: 276–280, 1994 Eversole LR, Tomich CE, Cherrick HM: Histogenesis of odontogenic tumors. J Oral Surg 32: 569–581, 1971 Gallagher GT, Shklar G: Odontogenic tumors. In: Cancer Medicine, Holland JF, Frei E (eds.), Neoplasms of Head and Neck, 5th edition. London: B.C. Decker, 2000; 1221–226 German G: There is One Estonia. Tallinn: Gustav German, 2001 Gold L: Biologic behavior of ameloblastoma. Oral Maxillofac Surg Clin North Am 3: 21–71, 1991 Gunham . O, Erseven G, Ruacan S, Celasun B, Aydintug Y, Ergun E: Odontogenic tumors: a series of 409 cases. Aust Dent J 35: 518–522, 1990 Happonen R-P, Ylipaavalniemi P, Calonius B: A survey of 15,758 oral biopsies in Finland. Proc Finn Dent Soc 78: 201–206, 1982 Kovi J, Laing WN: Tumors of the mandible and maxilla in Accra, Ghana. Cancer 19: 1301–1307, 1966 Kramer IRH, Pindborg JJ, Shear M: Histological Typing of Odontogenic Tumours, 2nd edition. Berlin: Springer, 1992 Lu Y, Xuan M, Takata T, Wang C, He Z, Zhou Z, Mock D, Nikai H: Odontogenic tumors. A demographic study of 759 cases in a Chinese population. Oral Surg Oral Med Oral Pathol 86: 707–714, 1998 Minderjahn A: Incidence and clinical differentiation of odontogenic tumours. J Maxillofac Surg 7: 142–150, 1979 Mosadomi A: Odontogenic tumors in an African population. Oral Surg Oral Med Oral Pathol 40: 502–512, 1975 Mosqueda-Taylor A, Ledesama-Montes C, Caballero-Sandoval S, Portilla-Robertson J, Ruiz-Godoy Rivera L, Meneses-Garcia A: Odontogenic tumors in Mexico. A collaborative retrospective study of 349 cases. Oral Surg Oral Med Oral Pathol 84: 672–675, 1997 Mothes P, Kreusch T, Harms D, Donath K, Schmelzle R: Die Ha¨ufigkeit odontogener Tumoren in Wachstumsalter. Dtsch Zahna¨rztl Z 46: 18–19, 1991 Odukoya O: Odontogenic tumors: analysis of 289 Nigerian cases. J Oral Pathol Med 24: 454–457, 1995 Reddy CRRM: Incidence of jaw tumors on the East coast of South India. Int Surg 59: 400–4001, 1974 Regezi JA, Kerr DA, Courtney RM: Odontogenic tumors: an analysis of 706 cases. J Oral Surg 36: 771–778, 1978 Reichart PA, Philipsen HP, Sonner S: Ameloblastoma: biological profile of 3677 cases. Oral Oncol Eur J Cancer 31: 86–99, 1995 Sawyer DR, Mosadomi A, Page DG, Svirsky JA, Kekere-Ekun A: Racial predilection of ameloblastoma? A probable answer from Lagos (Nigeria) and Richmond, Virginia (USA). J Oral Med 40: 27–31, 1985 Stypulkowska J: Odontogenic tumors and neoplastic-like changes of the jaw bones. Clinical study and evaluation of treatment results (in Polish). Folia Medica Cracoviensia 39: 135–141, 1998 Tay AB: A 5-year survey of oral biopsies in an oral surgical unit in Singapore. Ann Acad Med, Singapore 28: 665–671, 1999 Wu PC, Chan KW: A survey of tumorus of the jawbones in Hong Kong Chinese: 1963–1982. Br J Oral Maxillofac Surg 23: 92–102, 1985 Dr. T. Tamme Department of Maxillofacial Surgery 8 L.Puusepa Street Tartu, 51014 Estonia Tel.: +372 7 318237 Fax: +372 7 318224 E-mail: [email protected] Paper received 25 March 2003 Accepted 10 December 2003
Odontogenic tumours, a collaborative retrospective study of 75 cases covering more than 25 years from Estonia Tiia Tamme1, Marianne Soots1, Andres Kulla2, Kert Karu3, Siiri-Mai Hanstein3, Airi Sokk3, 4 * Enn Joeste , Edvitar Leibur1 Department of Maxillofacial Surgery (Chairman: Dr. Peeter Mu. ursepp), University of Tartu, Tartu . 51014, Estonia; 2 Department of Pathology (Chairman: Dr. Andres Kulla), University of Tartu, Tartu, Estonia; 3 Department of Maxillofacial Surgery (Chairman: Dr. Hamor Kaha), Tallinn, Estonia; 4 Department of Pathology (Chairman: Dr. Enn Joeste), * Mustamae . Hospital, Tallinn, Estonia 1
SUMMARY. Introduction: The aim of the present collaborative study was to analyse retrospectively the character of odontogenic tumours in Estonia, involving the entire Estonian population (1.4 million), and to compare their prevalence with the figures presented in similar reports from other countries. Material and methods: All material for the retrospective study was retrieved from the files of the Departments of Maxillofacial Surgery in Tartu and Tallinn, Estonia, where all in/out-patients are treated from the whole country. The final diagnosis in each case of odontogenic tumour was based on the 1992 WHO histological criteria. Results: A total of 75 odontogenic tumours was found, 74 (98.6%) of which were benign, and 1 (1.3%) was malignant. The frequency of odontogenic tumours in this study was the lowest ever reported. The most common tumours were odontoma (34.3%), followed by ameloblastoma with different subtypes (25.3%), ameloblastic fibroma (16%), odontogenic myxoma (12%) and benign cementoblastoma (8%). Conclusion: Odontogenic tumours are relatively rare in Estonia compared with the data from other countries. r 2004 European Association for Cranio-Maxillofacial Surgery.
Keywords: Odontogenic tumours; Retrospective study; Prevalence
By taking into account that all in- and outpatients with pathology in the maxillofacial region were treated in the only two Departments of Maxillofacial Surgery in Tartu and in Tallinn, the aim of the present collaborative study was to analyse retrospectively the character of odontogenic tumours in Estonia and to compare their prevalence with the figures presented in similar reports from other countries.
INTRODUCTION Odontogenic tumours occur as a result of disturbances in the development of teeth and associated structures (Eversole et al., 1971; Gold, 1991). They share two major characteristics, namely they arise from the tissue with the potential for differentiation into tooth or periodontal structures, and therefore found exclusively in the mandible and maxilla and, on rare occasions, the gingiva. Another variable but distinctive feature includes formation of tooth-related extracellular substances some of which may calcify and be visible on radiographs; they are a product of epithelial–mesenchymal interactions (Gallagher and Shklar, 2000). The biological behaviour of these lesions ranges from hamartoma-like lesions and benign neoplasms to rare, aggressive, malignant tumours. The most common sites are the mandibular molar region and the maxillary cuspid region. Odontogenic tumours are usually slow growing and asymptomatic. Certain odontogenic tumours have a predilection for particular ages, gender, geographic location, and race (Sawyer et al., 1985; Assael, 1992). To our knowledge, there are no reports on the frequency of these lesions either from Estonia or from any other Baltic State. Some reports deal with the prevalence in neighbouring countries (Finland, Happonen et al., 1982; and Poland, Stypulkowska, 1998).
MATERIAL AND METHODS This collaborative retrospective study is based on data from the following institutions: Departments of Maxillofacial Surgery and of Pathology, Tartu University Hospital, Tartu (42 cases; 1977–2001) and Departments of Maxillofacial Surgery and of Pathology, Mustam.ae Hospital, Tallinn (33 cases, 1981–2001). Haematoxylin and eosin stained sections were reviewed to confirm or to correct a previous histologic diagnosis according to the criteria suggested for the revised World Health Organization (WHO) classification (Kramer et al., 1992). The necessary clinical information, including patient age and gender, and tumour location was obtained from records when available. 161
ARTICLE IN PRESS 162 Journal of Cranio-Maxillofacial Surgery
For tumour location the following scheme was used. The maxilla was divided into 6 anatomical regions, 3 on either side: anterior (from the midline to the distal surface of the canine), premolar (from the mesial aspect of the first premolar to the distal side of the second premolar), and molar (from the mesial aspect of the first molar distally). The mandible was divided into 5 anatomical regions on each side: anterior and premolar as described above, molar (from the mesial aspect of the first molar to the distal side), angle (distal side of third molar to inferior portion of ramus, beneath the occlusal plane), and ramus (upper portion of ramus above the occlusal plane).
RESULTS The sources of odontogenic tumours are given in Table 1. It shows the frequency of odontogenic tumours found among all biopsy specimens, including all other benign and malignant tumours of the oral and maxillofacial regions. The distribution of histological types and frequency of odontogenic tumours is presented in Table 2. There were altogether 75 odontogenic tumours. Of these, 74 (98.6%) were benign, and 1 (1.3%) was malignant.
Table 1 – Sources of odontogenic tumours Source (years)
Biopsies
Departments of Maxillofacial Surgery and of Pathology, Tartu University Clinics (1977–2001)
4089
Departments of Maxillofacial Surgery and of Pathology, Mustam.ae Hospital, Tallinn (1981–2001)
6052
Total
Odontogenic tumours (%) 42 (1.03)
The most frequent benign tumour was odontoma (compound, complex; 34.3%), followed by ameloblastoma with different subtypes (25.3%), ameloblastic fibroma (16%), odontogenic myxoma (12%) and benign cementoblastoma (8%). The other, less common types were calcifying epithelial odontogenic tumour and adenomatoid odontogenic tumour, accounting for 1.3% each. There was only one malignant odontogenic tumour, namely primary intraosseous carcinoma (1.3%). The nineteen ameloblastomas were subdivided into 2 biologic-microscopic subtypes: 13 solid or multicystic ameloblastomas and 6 unicystic ameloblastomas. The 75 lesions were found in 28 males and in 47 females. The overall male to female ratio was 1:1.7. The gender distribution is listed in Table 3 and the age distribution in Table 4. Fifty-one cases (68%) were found during the second, third and fourth decades and, in the sixth
Table 2 – Histologic type and frequency of odontogenic tumours Tumours type
No. of tumours
Benign 1. Odontoma Compound Complex 2. Ameloblastoma Multicystic Unicystic 3. Ameloblastic fibroma 4. Odontogenic myxoma 5. Benign cementoblastoma 6. Calcifying epithelial odontogenic tumour 7. Adenomatoid odontogenic tumour
26
12 9 6 1
34.6 16 18.6 25.3 17.3 8 16 12 8 1.3
1
1.3
1
1.3
12 14 19 13 6
33 (0.55) Malignant 9. Primary intra-osseous carcinoma
10,141
Percentage
75 (0.74)
Total
75
100
Table 3 – Gender distribution of odontogenic tumour cases Type of tumour
Number
Male
Female
Male:female ratio
Odontoma Compound Complex Ameloblastoma Multicystic Unicystic Ameloblastic fibroma Odontogenic myxoma Benign cementoblastoma Calcifying epithelial odontogenic tumour Adenomatoid odontogenic tumour Primary intraosseous carcinoma
26 12 14 19 13 6 12 9 6 1 1 1
8 3 5 10 7 3 5 4 1 0 0 0
18 9 9 9 6 3 7 5 5 1 1 1
1.0:2.3 1.0:3.0 1.0:1.8 1.1:1.0 1.0:1.0 1.0:1.0 1.0:1.4 1.0:1.3 1.0:5.0 NA NA NA
Total
75
28
47
1:1.7
NA, not applicable.
ARTICLE IN PRESS Odontogenic tumours 163 Table 4 – Age distribution of odontogenic tumour cases Type of tumour
Number of cases
Age (years) 0–10
11–20
21–30
31–40
41–50
51–60
61–70
71–80
Mean
— — — 2 2
Odontoma Compound Complex Ameloblastoma Multicystic Unicystic Ameloblastic fibroma Odontogenic myxoma Benign cementoblastoma Calcifying epithelial odontogenic tumour Adenomatoid odontogenic tumour Primary intra-osseous carcinoma
26 12 14 19 13 6 12 9 6 1 1 1
4 3 1 1 — 1 — 4 — — — —
8 4 4 3 1 2 2 — 2 — — —
8 3 5 2 1 1 1 3 — — — —
4 1 3 2 1 1 1 1 1 — 1 —
— — — — — — 7 1 1 — — —
1 — 1 7 6 1 — — 2 1 — 1
1 1 — 2 2 — 1 — — — — —
— — — — — —
23.7 21.8 25.4 44.7 48.7 38.5 39.2 18.0 36.6 (51.0) (38.0) (58.0)
Total
75
9
15
14
10
9
12
4
2
32.5
decade of life. The members in the sixth decade can be attributed mainly to the high prevalence of (multicystic) ameloblastomas in elderly people. The site distribution is summarized in Table 5. In general, there was a predilection for mandibular tumours (mandibular to maxillary ratio 1.6:1), which was particularly marked for ameloblastomas (mandible to maxilla 2.8:1). In contrast, 2 (out of 6) benign cementoblastomas occurred in the maxilla (!), the maxilla to mandible ratio being 1:2. The most frequently affected areas were the premolar (20%) and molar regions (21.3%) in the mandible and the most common location in the maxilla was the premolar region (17.3%). DISCUSSION Odontogenic tumours are relatively uncommon lesions. The present study comprised all odontogenic tumours taken care of in Estonia during 1977–2001. Estonia is a small Baltic State with a population of 1.4 million (German, 2001) and the treatment of all odontogenic tumours is concentrated at two medical institutions with their in- and out-patient clinics. The study period involved profound changes in the political situation in Estonia (transition from socialist economy to free market economy), while the organization of the treatment of odontogenic tumours was not altered. The frequency of odontogenic tumours among all oral and maxillofacial biopsy specimens was 0.74%, ranging from 0.55% at Mustam.ae Hospital to 1.03% at Tartu University Clinics. Despite the obvious need to know the prevalence of odontogenic tumours, there are surprisingly few relevant reports. Bhaskar examined benign and malignant odontogenic tumours in 1969, and Regezi et al., in 1978, both among American populations. More recently, additional case series have been reported from Turkey (Gunham et al., 1990), Germany (Mothes . et al., 1991), Canada (Daley et al., 1994), Zimbabwe (Chidzonga et al., 1996a, b), Nigeria (Arotiba et al.,
1997), Mexico (Mosqueda-Taylor et al., 1997), China (Lu et al., 1998), and Poland (Stypulkowska,1998). We recorded 75 cases of odontogenic tumours for the period of 25 years (1977–2001) in Estonia, from the database of University Clinics (1977–2001 and from the database of Mustam.ae Hospital which opened in 1981 (1981–2001). Inasmuch as Estonia is a small Baltic State with a population of 1.4 million, it is difficult to perform a comparative analysis of different populations. However, the frequency of odontogenic tumours among all biopsy cases in our series was 0.74%, which is the lowest ever reported in the literature, being as high as 30% in a Nigerian study (Arotiba et al., 1997) and as low as 1.1% in a Finnish study (Happonen et al., 1982) and in a Canadian study (Daley et al., 1994). Although the vast majority of odontogenic tumours were benign, there were some interesting differences regarding their prevalence that should be mentioned: The most frequent tumours in the present study were compound and complex odontomas (34.3%), the result being similar to that of a Mexican study (Mosqueda-Taylor et al., 1997). The prevalence for the Estonian population was almost twice as high as that recorded for a Turkish (18%) population (Gunham et al., 1990). . In most other series from Canada, Finland, America and Germany, compound and complex odontomas accounted for 51.5% to 74% of odontogenic tumours (Bhaskar, 1969; Regezi et al., 1978; Happonen et al., 1982; Mothes et al., 1991; Daley et al., 1994). In contrast, the incidence of compound and complex odontomas was low in the series involving Chinese (6.2%) and Nigerian populations (Chung et al., 1969; Wu and Chan, 1985; Arotiba et al., 1997; Lu et al., 1998). It is difficult to perform a comparative analysis of the frequency of odontomas, because these tumours are interpreted as developmental malformations or hamartomas rather than true neoplasms (Gallagher and Shklar, 2000; Assael, 1992). This lesion is usually
ARTICLE IN PRESS
1.0:1. 6 45 2 8 16 15 6 28 7 13 8 75
— 1
Total
— 1 — — — 1 — — —
—
—
— 1 — — — 1 — — —
13 5 8 14 9 5 9 5 4 —
1
—
Ramus
— — — 2 1 1 — — — — 1 1 — 4 3 1 1 1 1 —
Angle Molar
2 — 2 6 4 2 5 1 2 — 6 2 4 1 — 1 3 2 1 —
Premolar Anterior
4 2 2 1 1 — — 1 — — 13 7 6 5 4 1 3 4 2 1
Total Molar Premolar
7 3 4 1 1 — — — — — 26 12 14 19 13 6 12 9 6 1
Odontoma Compound Complex Ameloblastoma Multicystic Unicystic Ameloblastic fibroma Odontogenic myxoma Benign cementoblastoma Calcifying epithelial odontogenic tumour Adenomatoid odontogenic tumour Primary intra-osseous carcinoma
Anterior
1 1 — 3 2 1 1 1 1 —
Mandible Maxilla Number Type of tumour
Table 5 – Distribution of odontogenic tumours by location
5 3 2 1 1 — 2 3 1 1
Total
1.0:1.0 1.0:0.7 1.0:1.3 1.0:2.8 1.0:2.3 1.0:5.0 1.0:3.0 1.0:1.3 1.0:2.0 —
Maxilla:mandible
164 Journal of Cranio-Maxillofacial Surgery
discovered on routine radiographic examination and it does not produce pain; treatment is generally provided by dentists or oral surgeons in Western countries. Only problematic odontomas commonly require hospital management. In Estonia, the treatment of all odontogenic tumour cases is concentrated at two institutions and is documented in their databases, which is related to tradition (referral by dentists) and to the small population. Hence, the institutional background and the specific features of the country appear essential in assessment of compound and complex odontomas. Ameloblastoma with its different subtypes appears to be particularly frequent in Africa (Mosadomi, 1975; Odukoya, 1995; Chidzonga et al., 1996a, b; Arotiba et al., 1997), and some Asian populations (Kovi and Laing, 1966; Chung et al., 1969; Reddy, 1974; Wu and Chan, 1985; Lu et al., 1998; Tay, 1999). In the present series, ameloblastoma was the second most common tumour, accounting for 25.3% of all cases, which is similar to the corresponding figure in a German study (Mothes et al., 1991). We compared our data to those from Finland and Poland, both in close geographic proximity to Estonia, where the respective data were 8.8% and 36.6% (Happonen et al., 1982; Stypulkowska, 1998). In the present study, the age distribution of ameloblastoma was higher (mean age 44.7 years) than that reported by other researchers, but consistent with the results of Reichart et al. (1995) who compared 3677 ameloblastomas in a metaanalysis from different continents and found that the patients mean age, 42.3 years, was considerably higher in European countries than the other continents. When comparing the age distribution among the two subtypes of ameloblastomas in this study, an obvious contrast between multicystic and unicystic ameloblastomas was found. The mean age of the patients with unicystic ameloblastoma (23.3 years) was much lower than that of the patients with classical (solid or multicystic) ameloblastomas (49.3 years). The average age of the patients with unicystic ameloblastoma was similar to that reported by Ackermann et al. (1988; 23.8 years). Regarding the other types of odontogenic tumours, the most significant difference in this study was found in the frequency of ameloblastic fibroma in this study (16%), which was significantly higher than that presented in other reports (Daley et al., 1994; Lu et al., 1998; Chidzonga et al., 1996b; MosquedaTaylor et al., 1997; 8%, Happonen et al., 1982, 53%). The gender, age and site distributions of this neoplasm were also different from those presented in other reports. This finding requires further attention, as the authors cannot provide an explanation for this difference at present. Odontogenic myxoma constituted 12% of all odontogenic tumours in the present study. This figure is considerably higher than that presented in German (Mothes et al., 1991) and North American (Bhaskar, 1969; Regezi et al., 1978) studies but is similar to that
ARTICLE IN PRESS Odontogenic tumours 165
reported for African populations (Chidzonga et al., 1996a; Odukoya, 1995; Arotiba et al., 1997). Six cases (8%) met the recent WHO criteria for the diagnosis of benign cementoblastoma. The proportion of benign cementoblastomas in this series is larger than in North American (Regezi et al., 1978; Daley et al., 1994), Mexican (Mosqueda-Taylor et al., 1997) and African studies (Odukoya, 1995; Arotiba et al., 1997) but is similar to the proportions reported from Poland (Stypulkowska, 1998) and Finland (Happonen et al., 1982), both geographically close to Estonia. The site distribution of benign cementoblastoma was different from that found in other studies. In the present study, two out of six benign cementoblastomas were located in the upper jaw, the maxilla to mandible ratio being 1:2. However, our results were similar to those of Minderjahn (1979). This tumour displayed a remarkable topographic affinity for the premolar and molar regions (nearly 100% were located here). The other odontogenic tumours included calcifying epithelial odontogenic tumour, adenomatoid odontogenic tumour and primary intraosseous carcinoma. However, all these were only represented by one case each, which is a number too small for analysis.
CONCLUSION Based on this collaborative retrospective study which involved the entire Estonian population it was concluded: Odontogenic tumours are relatively rare in Estonia compared with other countries. There were differences in the prevalence of certain odontogenic tumours in comparison with data from other countries.
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