VETERINARY DENTISTRY AT WORK Odontoameloblastoma in a Calf A 6-month-old Chianina calf was referred for a large (5 x
4-cm), firm, ulcerated oval mass in the rostral portion of the mandible. The mass had been rapidly growing for 1-month, however no apparent involvement of the mandibular bone was observed. After deep sedation and local anesthesia, the mass was surgically excised and submitted for histopathology. On cut surface, the mass was fleshy to fibrous, white to
light red, with white, chalky, gritty streaks. Furthermore, the mass recurred 1-month after excision, and the owner opted for slaughter. Unfortunately, the head of the animal was not submitted for pathological examination. Samples from the mass were fixed in 10% neutral buffered formalin, routinely processed, and stained with hematoxylin and eosin (H&E), PAS, and Masson’s trichrome. Histologically,
Figure 1
Figure 2
Figure 3
Figure 4
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows epithelial ridges and anastomosing cords originating from overlying ulcerated gingival epithelium and extending into the fibrous stroma indicative of the bud stage. [Original magnification = 4X, H&E]
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows islets of fully developed enamel organ, composed of inner peripherial palisading cuboidal ameloblasts, flattened outer epithelium, and central dendritic cells of the stellate reticulum indicative of the bell stage. [Original magnification = 10X, H&E]
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Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows epithelial sheets of the developing enamel organ encircling a mass of undifferentiated mesenchymal stroma indicative of the cap stage. [Original magnification = 20X, H&E]
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows several sections of developing denticles composed of concentrically arranged dental hard tissues (eosinophilic osteodentin, deeply basophilic tubular dentin and enamel) interspersed in a fibrous stroma with little residual epithelial cords indicative of the appositional stage. [Original magnification = 10X, H&E]
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the tumor was composed of a dense, mature fibrous stroma with epithelial islands and anastomosing cords originating from the gingival epithelium, which was widely ulcerated (Fig.1). In the peripheral areas, epithelial cords were composed of 2 to 3 layers of cuboidal to flattened epithelial cells with oval nuclei and scant lightly basophilic cytoplasm, focally enclosing buds of undifferentiated mesenchymal cells (Fig.2). In the central areas of the mass, epithelial islands were wider with a peripheral rim of cuboidal cells arranged in a palisade pattern, with apical oval nuclei and scanty basal vacuolated cytoplasm (reverse polarity), consistent with differentiated ameloblasts. These peripheral palisades enclosed large islets of dendritic epithelial cells, which showed a clear cytoplasm and long processes, similar to that of the stellate reticulum of a normal enamel system (Fig.3). The epithelial structures were irregularly admixed with stromal polyhedric mesenchymal cells embedded in a strongly eosinophilic acellular “tubular-like” material (dentin) or bone-like, cell-rich, slightly eosinophilic substance (osteodentin) (Fig.4). The dental hard tissue was focally organized in arranged structures, mimicking developing denticles (Fig. 5). In some foci, palisades of cylindrical odontoblasts were also observed. Both the epithelial and the mesenchymal components of this tumor showed a low degree of anaplasia and no mitotic figures were found. In some areas, epithelial and mesenchymal components were interspersed, while in others they were unrelated and showed infiltrative growth (Fig.6). Based on the presence of both complex odontoma (disarrayed dental hard tissues) and ameloblastoma-like patterns, the tumor was diagnosed as an odontoameloblastoma (OA). The histological appearance of an OA recapitulates normal tooth development, which goes through a precise sequence of phases: the bud (Fig. 1), cap (Fig. 2), bell (Fig. 3), appositional (Fig. 4), and maturation (Fig. 5) stages.
Figure 5
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows a developing denticle composed of inner mesenchymal connective tissue of dental papilla, and concentric layers of osteodentin, tubular dentin, and enamel, with regression of enamel organ indicative of the maturation stage. [Original magnification = 10X, H&E]
OA is an extremely rare neoplasm, with about 20 confirmed cases in humans.1 It is defined by the World Health Organization (WHO) as “a neoplasm that includes odontogenic ectomesenchyme in addition to odontogenic epithelium and resembles an ameloblastoma in both structure and behavior. Because of the presence of odontogenic ectomesenchyme, inductive changes take place leading to the formation of dentin and enamel in parts of the tumor”. It is characterized by simultaneous occurrence of ameloblastoma and complex or compound odontoma patterns.2 OA is very rare in animals, with single cases reported in a ewe3, Japanese monkey4, and rat5. Most of odontogenic tumors in animals are reported to be benign.6 However, in some cases, they can be locally aggressive7, suggesting a poor prognosis due to mechanical interference with food intake and mastication, as we observed in the case reported here. In farm animals, it is difficult to speculate on the biological behavior of tumors, as they are often slaughtered before the tumor reaches its full development. OA shares some morphological features with other odontogenic tumors, such as the ameloblastic odontoma and ameloblastic fibroma/fibro-odontoma. Ameloblastic odontoma is a tumor similar to OA reported in many species including cattle.8 This term has been widely used as a synonym of OA and is still used in veterinary medicine, but it has been replaced in human pathology by ameloblastic fibro-odontoma and odontoameloblastoma, and should therefore be avoided.4 Ameloblastic fibro-odontoma (AFO) is an inductive odontogenic tumor composed of a loose stroma with poorly differentiated epithelial structures and dental hard tissues.9 Histologically, both OA and AFO contain a mixture of variably arranged and variably mature odontogenic epithelium and dental hard tissues (enamel, dentin, and cementum). The odontogenic epithelium is well differentiated in odontoameloblastoma and composed of peripheral palisading ameloblasts with “reverse
Figure 6
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows irregularly arranged epithelial sheets of fully developed enamel organ (upper left) and disarrayed dental hard tissue in a fibrous stroma (lower right), typical of odontoameloblastoma. [Original magnification = 4X, H&E]
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polarity”, circumscribing large areas of stellate reticulumlike tissue (fully developed enamel system)2, which fulfils the histological criteria of ameloblastoma.10 The odontogenic epithelium is less differentiated for AFO and composed of epithelial cords with peripheral palisading but scant to absent stellate reticulum-like tissue. Also, the stromal component differs between the two tumors. It is well differentiated, mature, dense and fibrous in OA, while in AFO it is highly cellular and immature, similar to embryonic mesenchyme of the dental papilla.11 Oral tumors reported in the literature including adamantinomas, ameloblastic odontomas, squamous cell carcinomas, and odontomas were reviewed and re-classified as ameloblastic fibromas/fibro-odontoma. Subsequently, ameloblastic fibro-odontoma (AFO) was reported as the most common odontogenic tumor in cattle.12 In humans, AFO and OA are considered two distinct tumors with different prognoses: the former allows a good prognosis after excision, while the latter is considered to be a more aggressive tumor. OA expands by infiltrating bony trabeculae, has a high rate of recurrence, and should be treated aggressively, like conventional ameloblastoma.1 Due to the rare incidence of this tumor, it is not known if a different clinical course occurs in domestic animals. Additional cases are required to evaluate the biological behavior of these tumors. The histological features and aggressive nature of the tumor reported here was consistent with odontoameloblastoma rather than the more common bovine ameloblastic fibroodontoma. To the best of our knowledge, this is the first odontoameloblastoma reported in a calf, suggesting a critical review of bovine odontogenic tumors formerly diagnosed as ameloblastic fibro-odontomas.
Acknowledgement
The authors thank Professor Paola Roccabianca for scientific support.
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Contributed by: Lepri Elvio, DVM, PhD Avallone Giancarlo, DVM, PhD Mandara Maria Teresa, DVM Vitellozzi Giovanni, DVM Department of Veterinary Medicine, University of Perugia, Via S.Costanzo 4, Perugia, Italy, and the Department of Veterinary Sciences and Public Health (Avallone), University of Milano, Via Celoria 10, Milano, Italy. Dr. Avallone’s current address is Department of Veterinary Medical Sciences, University of Bologna, via tolara di sopra 50, Ozzano dell’Emilia, Bologna, Italy. Email: elvio. [email protected]
References 1. Dive A, Khandekar S, et al. Odontoameloblastoma. J Oral Maxillofac Pathol 2011; 15:60 -64. 2. Mosqueda-Taylor A, Carlos-Bregni R, et al. Odontoameloblastoma. Clinico-pathological study of three cases and critical review of the literature. Oral Oncol 2002; 38: 800-805. 3. Dubielzig RR, Griffith JW. An odontoameloblastoma in an adult sheep. Vet Pathol 1982; 19:318-20. 4. Yanai T, Masegi T, et al. Odontoameloblastoma in a Japanese monkey (Macuaca fuscata). Vet Pathol 1995; 32: 57-59. 5. Burrough ER, Myers RK, Whitley EM. Spontaneous odontoameloblastoma in a female Sprague Dawley rat. J Vet Diagn Invest 2010; 22: 998 - 1001. 6. Poulet FM, Valentine BA, Summers BA. A survey of epithelial odontogenic tumors and cysts in dogs and cats. Vet Pathol 1992; 29: 369-380. 7. Binnington JA, Adkins, KF. Ameloblastic odontosarcoma in a bovine mandible. J Pathol 1972; 108: 169-72. 8. Chalmers GA, Shacklady EM. Ameloblastic odontoma in a calf. Can Vet J 1991; 32: 365-366. 9. Head KW. Tumors of the alimentary tract. In: Meuten J, ed. Tumors in domestic animals, 4th ed., Iowa States Press:Ames, 2002. 10. Vickers RA, Gorlin RJ. Ameloblastoma. Delineation of early histopathological features of neoplasia. Cancer 1970; 26: 699-710. 11. Dubielzig RR. Odontogenic tumors and cysts. In: Moulton JE, ed. Tumors of domestic animals. 3rd ed., University of California Press:Berkley, 1990. 12. Gardner DJ. Ameloblastic fibromas and related tumors in cattle. J Oral Pathol Med 1996; 25: 119-124.
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4-cm), firm, ulcerated oval mass in the rostral portion of the mandible. The mass had been rapidly growing for 1-month, however no apparent involvement of the mandibular bone was observed. After deep sedation and local anesthesia, the mass was surgically excised and submitted for histopathology. On cut surface, the mass was fleshy to fibrous, white to
light red, with white, chalky, gritty streaks. Furthermore, the mass recurred 1-month after excision, and the owner opted for slaughter. Unfortunately, the head of the animal was not submitted for pathological examination. Samples from the mass were fixed in 10% neutral buffered formalin, routinely processed, and stained with hematoxylin and eosin (H&E), PAS, and Masson’s trichrome. Histologically,
Figure 1
Figure 2
Figure 3
Figure 4
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows epithelial ridges and anastomosing cords originating from overlying ulcerated gingival epithelium and extending into the fibrous stroma indicative of the bud stage. [Original magnification = 4X, H&E]
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows islets of fully developed enamel organ, composed of inner peripherial palisading cuboidal ameloblasts, flattened outer epithelium, and central dendritic cells of the stellate reticulum indicative of the bell stage. [Original magnification = 10X, H&E]
248
JOV_2013_Winter_30_4.indd 248
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows epithelial sheets of the developing enamel organ encircling a mass of undifferentiated mesenchymal stroma indicative of the cap stage. [Original magnification = 20X, H&E]
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows several sections of developing denticles composed of concentrically arranged dental hard tissues (eosinophilic osteodentin, deeply basophilic tubular dentin and enamel) interspersed in a fibrous stroma with little residual epithelial cords indicative of the appositional stage. [Original magnification = 10X, H&E]
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the tumor was composed of a dense, mature fibrous stroma with epithelial islands and anastomosing cords originating from the gingival epithelium, which was widely ulcerated (Fig.1). In the peripheral areas, epithelial cords were composed of 2 to 3 layers of cuboidal to flattened epithelial cells with oval nuclei and scant lightly basophilic cytoplasm, focally enclosing buds of undifferentiated mesenchymal cells (Fig.2). In the central areas of the mass, epithelial islands were wider with a peripheral rim of cuboidal cells arranged in a palisade pattern, with apical oval nuclei and scanty basal vacuolated cytoplasm (reverse polarity), consistent with differentiated ameloblasts. These peripheral palisades enclosed large islets of dendritic epithelial cells, which showed a clear cytoplasm and long processes, similar to that of the stellate reticulum of a normal enamel system (Fig.3). The epithelial structures were irregularly admixed with stromal polyhedric mesenchymal cells embedded in a strongly eosinophilic acellular “tubular-like” material (dentin) or bone-like, cell-rich, slightly eosinophilic substance (osteodentin) (Fig.4). The dental hard tissue was focally organized in arranged structures, mimicking developing denticles (Fig. 5). In some foci, palisades of cylindrical odontoblasts were also observed. Both the epithelial and the mesenchymal components of this tumor showed a low degree of anaplasia and no mitotic figures were found. In some areas, epithelial and mesenchymal components were interspersed, while in others they were unrelated and showed infiltrative growth (Fig.6). Based on the presence of both complex odontoma (disarrayed dental hard tissues) and ameloblastoma-like patterns, the tumor was diagnosed as an odontoameloblastoma (OA). The histological appearance of an OA recapitulates normal tooth development, which goes through a precise sequence of phases: the bud (Fig. 1), cap (Fig. 2), bell (Fig. 3), appositional (Fig. 4), and maturation (Fig. 5) stages.
Figure 5
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows a developing denticle composed of inner mesenchymal connective tissue of dental papilla, and concentric layers of osteodentin, tubular dentin, and enamel, with regression of enamel organ indicative of the maturation stage. [Original magnification = 10X, H&E]
OA is an extremely rare neoplasm, with about 20 confirmed cases in humans.1 It is defined by the World Health Organization (WHO) as “a neoplasm that includes odontogenic ectomesenchyme in addition to odontogenic epithelium and resembles an ameloblastoma in both structure and behavior. Because of the presence of odontogenic ectomesenchyme, inductive changes take place leading to the formation of dentin and enamel in parts of the tumor”. It is characterized by simultaneous occurrence of ameloblastoma and complex or compound odontoma patterns.2 OA is very rare in animals, with single cases reported in a ewe3, Japanese monkey4, and rat5. Most of odontogenic tumors in animals are reported to be benign.6 However, in some cases, they can be locally aggressive7, suggesting a poor prognosis due to mechanical interference with food intake and mastication, as we observed in the case reported here. In farm animals, it is difficult to speculate on the biological behavior of tumors, as they are often slaughtered before the tumor reaches its full development. OA shares some morphological features with other odontogenic tumors, such as the ameloblastic odontoma and ameloblastic fibroma/fibro-odontoma. Ameloblastic odontoma is a tumor similar to OA reported in many species including cattle.8 This term has been widely used as a synonym of OA and is still used in veterinary medicine, but it has been replaced in human pathology by ameloblastic fibro-odontoma and odontoameloblastoma, and should therefore be avoided.4 Ameloblastic fibro-odontoma (AFO) is an inductive odontogenic tumor composed of a loose stroma with poorly differentiated epithelial structures and dental hard tissues.9 Histologically, both OA and AFO contain a mixture of variably arranged and variably mature odontogenic epithelium and dental hard tissues (enamel, dentin, and cementum). The odontogenic epithelium is well differentiated in odontoameloblastoma and composed of peripheral palisading ameloblasts with “reverse
Figure 6
Histomicrograph from a 6-month-old Chianina calf with mandibular odontoameloblastoma shows irregularly arranged epithelial sheets of fully developed enamel organ (upper left) and disarrayed dental hard tissue in a fibrous stroma (lower right), typical of odontoameloblastoma. [Original magnification = 4X, H&E]
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polarity”, circumscribing large areas of stellate reticulumlike tissue (fully developed enamel system)2, which fulfils the histological criteria of ameloblastoma.10 The odontogenic epithelium is less differentiated for AFO and composed of epithelial cords with peripheral palisading but scant to absent stellate reticulum-like tissue. Also, the stromal component differs between the two tumors. It is well differentiated, mature, dense and fibrous in OA, while in AFO it is highly cellular and immature, similar to embryonic mesenchyme of the dental papilla.11 Oral tumors reported in the literature including adamantinomas, ameloblastic odontomas, squamous cell carcinomas, and odontomas were reviewed and re-classified as ameloblastic fibromas/fibro-odontoma. Subsequently, ameloblastic fibro-odontoma (AFO) was reported as the most common odontogenic tumor in cattle.12 In humans, AFO and OA are considered two distinct tumors with different prognoses: the former allows a good prognosis after excision, while the latter is considered to be a more aggressive tumor. OA expands by infiltrating bony trabeculae, has a high rate of recurrence, and should be treated aggressively, like conventional ameloblastoma.1 Due to the rare incidence of this tumor, it is not known if a different clinical course occurs in domestic animals. Additional cases are required to evaluate the biological behavior of these tumors. The histological features and aggressive nature of the tumor reported here was consistent with odontoameloblastoma rather than the more common bovine ameloblastic fibroodontoma. To the best of our knowledge, this is the first odontoameloblastoma reported in a calf, suggesting a critical review of bovine odontogenic tumors formerly diagnosed as ameloblastic fibro-odontomas.
Acknowledgement
The authors thank Professor Paola Roccabianca for scientific support.
250
JOV_2013_Winter_30_4.indd 250
Contributed by: Lepri Elvio, DVM, PhD Avallone Giancarlo, DVM, PhD Mandara Maria Teresa, DVM Vitellozzi Giovanni, DVM Department of Veterinary Medicine, University of Perugia, Via S.Costanzo 4, Perugia, Italy, and the Department of Veterinary Sciences and Public Health (Avallone), University of Milano, Via Celoria 10, Milano, Italy. Dr. Avallone’s current address is Department of Veterinary Medical Sciences, University of Bologna, via tolara di sopra 50, Ozzano dell’Emilia, Bologna, Italy. Email: elvio. [email protected]
References 1. Dive A, Khandekar S, et al. Odontoameloblastoma. J Oral Maxillofac Pathol 2011; 15:60 -64. 2. Mosqueda-Taylor A, Carlos-Bregni R, et al. Odontoameloblastoma. Clinico-pathological study of three cases and critical review of the literature. Oral Oncol 2002; 38: 800-805. 3. Dubielzig RR, Griffith JW. An odontoameloblastoma in an adult sheep. Vet Pathol 1982; 19:318-20. 4. Yanai T, Masegi T, et al. Odontoameloblastoma in a Japanese monkey (Macuaca fuscata). Vet Pathol 1995; 32: 57-59. 5. Burrough ER, Myers RK, Whitley EM. Spontaneous odontoameloblastoma in a female Sprague Dawley rat. J Vet Diagn Invest 2010; 22: 998 - 1001. 6. Poulet FM, Valentine BA, Summers BA. A survey of epithelial odontogenic tumors and cysts in dogs and cats. Vet Pathol 1992; 29: 369-380. 7. Binnington JA, Adkins, KF. Ameloblastic odontosarcoma in a bovine mandible. J Pathol 1972; 108: 169-72. 8. Chalmers GA, Shacklady EM. Ameloblastic odontoma in a calf. Can Vet J 1991; 32: 365-366. 9. Head KW. Tumors of the alimentary tract. In: Meuten J, ed. Tumors in domestic animals, 4th ed., Iowa States Press:Ames, 2002. 10. Vickers RA, Gorlin RJ. Ameloblastoma. Delineation of early histopathological features of neoplasia. Cancer 1970; 26: 699-710. 11. Dubielzig RR. Odontogenic tumors and cysts. In: Moulton JE, ed. Tumors of domestic animals. 3rd ed., University of California Press:Berkley, 1990. 12. Gardner DJ. Ameloblastic fibromas and related tumors in cattle. J Oral Pathol Med 1996; 25: 119-124.
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