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Neuroepithelial structures associated with neurogenous subgemmal plaque of the tongue: an autopsy finding
Vol. 120 No. 1 July 2015
LETTERS TO THE EDITOR Neuroepithelial structures associated with neurogenous subgemmal plaque of the tongue: an autopsy finding To the Editor: We have read with great interest the article published by Palazzolo et al. (2014),1 where the authors described for the first time the presence of neuroepithelial structures consistent with the juxtaoral organs of Chievitz in the tongue of four patients. We agreed with the authors when they highlighted the importance of the appropriate recognition of this remnant structure because of its close and frequent association with neural plexus that could cause an erroneous interpretation of a neoplastic neural invasion, especially in patients with history of oral squamous cell carcinoma. Concerning the anatomic neural aggregate present in the posterior border of the tongue, termed by the authors as “subepithelial nerve plexus,” our group has previously documented the clinical relevance of this structure, which we preferred to call “subgemmal neurogenous plaque,” in patients complaining of a burning sensation in the posterior border of the tongue. In addition to this clinical association, we further emphasized the importance of distinguishing this neural plexus from other benign neural tumors or lesions of the oral cavity, such as ganglioneuroma, ganglioneurofibroma, neurofibroma, and traumatic neuroma. However, we could not identify the neuroepithelial structures in any of the nine cases reported.2,3 An important line of investigation by our group refers to the study of the oral alterations found during autopsy in patients who had died due to complications of human immunodeficiency virus infection.4,5 Although not a common field of study by oral pathologists, autopsybased investigations represent an unmeasured source of data for better understanding the oral manifestations of systemic diseases, especially in developing countries, where infections still represent major causes of death. The microscopic analysis of autopsies can also provide a better comprehension of normal structures not commonly evaluated in regular oral biopsies, such as the posterior area or the base of the tongue. Hence, in this letter, we would like to contribute to the original description of Palazzolo et al. by describing an additional case containing neuroepithelial structures consistent with the juxtaoral organ of Chievitz in the posterior area of the oral tongue identified through microscopic analysis during the autopsy of a 73-yearold female patient who had died due to cardiovascular 94
complications. No relevant clinical data were available with regard to oral abnormalities, and no alteration in the patient’s tongue was evident during the autopsy. Histologic analysis of the tongue specimens depicted the presence of several foliate papillae covered by normal surface epithelium. Aggregates of epithelial islands were superficially dispersed in the connective tissue surrounded by an extensive neural structure consistent with the subgemmal neurogenous plaque. These epithelial nests were composed by central squamous cells with an abundant eosinophilic cytoplasm and a peripheral cellular layer arranged in palisade. No atypia or mitotic figures were present, and in smaller islands, the cellular disposal occasionally gave rise to a rosette-like pattern. Immunohistochemical reactions demonstrated a strong expression for pan-cytokeratin (AE1/AE3) and CK5, moderate for CK19, and a faint reactivity for CK7 in the neuroepithelial nests. Some islands stained diffusely for CD56, whereas in others the positivity was restricted to the peripheral cells. A strong nuclear positivity for p63 was found in all nests. S100 evidenced the surrounding neural structures, whereas neurofilament strongly stained ganglion cells. Epithelial membrane antigen (EMA) was positive in the perineurium and demonstrated only a focal and weak positivity in the neuroepithelial cells (Figure 1). In conclusion, by documenting this rare presentation of neuroepithelial structures consistent with the justaoral organs of Chievitz in the tongue, which would represent the fifth description in the literature, we further emphasize Palazzolo et al. advise not to misinterpret such an embryologic remnant as neural invasion of a squamous cell carcinoma. Moreover, the current case also clearly illustrates the importance of autopsy-based studies for oral pathologists. Thais Mauad is supported by the National Council for Scientific and Technological Development (CNPq/Brazil).
Felipe Paiva Fonseca, DDS, MSca Johanna Pamela Latta Moreira, MDb O.P. Almeida, DDS, PhDa Pablo Agustin Vargas, DDS, PhDa,* Thais Mauad, MD, PhDb a Department of Oral Diagnosis, Piracicaba Dental School, University of Campinas, Brazil b Department of Pathology, Medical School, University of São Paulo, Brazil *
Correspondence: [email protected]
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Fig. 1. Histopathologic and immunohistochemical findings. A, Low-power view of the foliate papilla with aggregates of epithelial nests below the overlying epithelium and surrounded by the subgemmal neurogenous plaque that extends deeper in the connective tissue (H&E; 50). B, The neuroepithelial islands were closely associated to the neural fibers of the subgemmal neurogenous plaque (left side) (H&E; 100). C, Under higher magnification, the epithelial structures were seen to be composed of larger nests containing central squamous cells with abundant eosinophilic cytoplasm and a peripheral layer organized in palisade (arrow), as well as smaller nests occasionally demonstrating a rosette-like pattern (arrowhead) (H&E; 200). D, The neuroepithelial nests were strongly positive for cytokeratin (AE1/AE3) (streptavidin-biotin; 200). E, The neuroepithelial nests were variably positive for CK19 (streptavidin-biotin; 100). F, The neuroepithelial nests were faintly positive for CK7 (streptavidin-biotin; 100). G, In some larger islands, CD56 staining was present in the peripheral cells only (arrow), but in other nests, both central and peripheral cells stained intensely for the protein (streptavidin-biotin; 100). H, S100 protein was negative in the neuroepithelial cells, but it clearly illustrated the surrounding subgemmal neurogenous plaque (streptavidin-biotin; 100).
LETTERS TO THE EDITOR
OOOO July 2015
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REFERENCES 1. Palazzolo MJ, Fowler CB, Magliocca KR, Gnepp DR. Neuroepithelial structures associated with the subepithelial nerve plexus of taste buds: a fortuitous finding resembling the juxtaoral organ of Chievitz. Oral Surg Oral Med Oral Pathol Oral Radiol. 2014;117:497-501. 2. Gueiros LA, Leon JE, Lopes MA, Almeida OP, Jorge J. Subgemmal neurogenous plaque associated with burning tongue: report of two cases and review of the literature. Int J Oral Maxillofac Surg. 2008;37:773-776. 3. Gueiros LA, León JE, Leão JC, Lopes MA, Jorge J, Almeida OP. Subgemmal neurogenous plaque: clinical and microscopic evaluation of 7 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108:920-924. 4. Gondak R, Mauad T, Schultz L, Soares F, Kowalski LP, Vargas PA. Decreased CD1aþ, CD83þ and factor XIIIaþ dendritic cells in cervical lymph nodes and palatine tonsils of AIDS patients. Histopathology. 2014;64:234-241. 5. De Faria PR, Vargas PA, Saldiva PH, Böhm GM, Mauad T, Almeida OP. Tongue disease in advanced AIDS. Oral Dis. 2005;11:72-80.
http://dx.doi.org/10.1016/j.oooo.2015.02.487
Response to “Neuroepithelial structures associated with neurogenous subgemmal plaque of the tongue: an autopsy finding” To the Editor: This case is an interesting example of the recently described finding, initially published by our group, with regard to the posterior tongue. We described the posterior tongue exhibiting neuroepithelial structures resembling the juxtaoral organ of Chievitz associated with the subepithelial nerve plexus of taste buds. As noted by our group, the subepithelial nerve plexus of taste buds was
initially described by McDaniel in 1999.1 However, the term “subgemmal nerve plexus” or “subgemmal neurogenous plaque” has been used interchangeably in the literature. Gueiros et al. described the presence of this plexus in patients complaining of burning sensation of the tongue. As outlined by the authors, none of these previously reported cases were associated with the presence of neuroepithelial structures resembling the organ of Chievitz. This may give some credence to the thought that these neuroepithelial structures are perhaps embryologic remnants that fail to involute. However, the exact origin and function of these neuroepithelial structures and their association with the above-mentioned nerve plexus, whether fortuitous or not, has yet to be completely elucidated. We agree that the potential for misinterpretation of these structures as invasive squamous cell carcinoma or neural invasion remain an important diagnostic challenge for pathologists. Mitzi J. Palazzolo, DDS, MS Associate Professor Uniformed University of the Health Sciences (USUHS), Oral and Maxillofacial Pathology-Staff JBSA-Lackland WHASC/SAMMC San Antonio, Texas USA
REFERENCE 1. McDaniel RK. Subepithelial nerve plexus (with ganglion cells) associated with taste buds. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1999;87:605-609. http://dx.doi.org/10.1016/j.oooo.2015.03.010
LETTERS TO THE EDITOR Neuroepithelial structures associated with neurogenous subgemmal plaque of the tongue: an autopsy finding To the Editor: We have read with great interest the article published by Palazzolo et al. (2014),1 where the authors described for the first time the presence of neuroepithelial structures consistent with the juxtaoral organs of Chievitz in the tongue of four patients. We agreed with the authors when they highlighted the importance of the appropriate recognition of this remnant structure because of its close and frequent association with neural plexus that could cause an erroneous interpretation of a neoplastic neural invasion, especially in patients with history of oral squamous cell carcinoma. Concerning the anatomic neural aggregate present in the posterior border of the tongue, termed by the authors as “subepithelial nerve plexus,” our group has previously documented the clinical relevance of this structure, which we preferred to call “subgemmal neurogenous plaque,” in patients complaining of a burning sensation in the posterior border of the tongue. In addition to this clinical association, we further emphasized the importance of distinguishing this neural plexus from other benign neural tumors or lesions of the oral cavity, such as ganglioneuroma, ganglioneurofibroma, neurofibroma, and traumatic neuroma. However, we could not identify the neuroepithelial structures in any of the nine cases reported.2,3 An important line of investigation by our group refers to the study of the oral alterations found during autopsy in patients who had died due to complications of human immunodeficiency virus infection.4,5 Although not a common field of study by oral pathologists, autopsybased investigations represent an unmeasured source of data for better understanding the oral manifestations of systemic diseases, especially in developing countries, where infections still represent major causes of death. The microscopic analysis of autopsies can also provide a better comprehension of normal structures not commonly evaluated in regular oral biopsies, such as the posterior area or the base of the tongue. Hence, in this letter, we would like to contribute to the original description of Palazzolo et al. by describing an additional case containing neuroepithelial structures consistent with the juxtaoral organ of Chievitz in the posterior area of the oral tongue identified through microscopic analysis during the autopsy of a 73-yearold female patient who had died due to cardiovascular 94
complications. No relevant clinical data were available with regard to oral abnormalities, and no alteration in the patient’s tongue was evident during the autopsy. Histologic analysis of the tongue specimens depicted the presence of several foliate papillae covered by normal surface epithelium. Aggregates of epithelial islands were superficially dispersed in the connective tissue surrounded by an extensive neural structure consistent with the subgemmal neurogenous plaque. These epithelial nests were composed by central squamous cells with an abundant eosinophilic cytoplasm and a peripheral cellular layer arranged in palisade. No atypia or mitotic figures were present, and in smaller islands, the cellular disposal occasionally gave rise to a rosette-like pattern. Immunohistochemical reactions demonstrated a strong expression for pan-cytokeratin (AE1/AE3) and CK5, moderate for CK19, and a faint reactivity for CK7 in the neuroepithelial nests. Some islands stained diffusely for CD56, whereas in others the positivity was restricted to the peripheral cells. A strong nuclear positivity for p63 was found in all nests. S100 evidenced the surrounding neural structures, whereas neurofilament strongly stained ganglion cells. Epithelial membrane antigen (EMA) was positive in the perineurium and demonstrated only a focal and weak positivity in the neuroepithelial cells (Figure 1). In conclusion, by documenting this rare presentation of neuroepithelial structures consistent with the justaoral organs of Chievitz in the tongue, which would represent the fifth description in the literature, we further emphasize Palazzolo et al. advise not to misinterpret such an embryologic remnant as neural invasion of a squamous cell carcinoma. Moreover, the current case also clearly illustrates the importance of autopsy-based studies for oral pathologists. Thais Mauad is supported by the National Council for Scientific and Technological Development (CNPq/Brazil).
Felipe Paiva Fonseca, DDS, MSca Johanna Pamela Latta Moreira, MDb O.P. Almeida, DDS, PhDa Pablo Agustin Vargas, DDS, PhDa,* Thais Mauad, MD, PhDb a Department of Oral Diagnosis, Piracicaba Dental School, University of Campinas, Brazil b Department of Pathology, Medical School, University of São Paulo, Brazil *
Correspondence: [email protected]
OOOO Volume 120, Number 1
LETTERS TO THE EDITOR
95
Fig. 1. Histopathologic and immunohistochemical findings. A, Low-power view of the foliate papilla with aggregates of epithelial nests below the overlying epithelium and surrounded by the subgemmal neurogenous plaque that extends deeper in the connective tissue (H&E; 50). B, The neuroepithelial islands were closely associated to the neural fibers of the subgemmal neurogenous plaque (left side) (H&E; 100). C, Under higher magnification, the epithelial structures were seen to be composed of larger nests containing central squamous cells with abundant eosinophilic cytoplasm and a peripheral layer organized in palisade (arrow), as well as smaller nests occasionally demonstrating a rosette-like pattern (arrowhead) (H&E; 200). D, The neuroepithelial nests were strongly positive for cytokeratin (AE1/AE3) (streptavidin-biotin; 200). E, The neuroepithelial nests were variably positive for CK19 (streptavidin-biotin; 100). F, The neuroepithelial nests were faintly positive for CK7 (streptavidin-biotin; 100). G, In some larger islands, CD56 staining was present in the peripheral cells only (arrow), but in other nests, both central and peripheral cells stained intensely for the protein (streptavidin-biotin; 100). H, S100 protein was negative in the neuroepithelial cells, but it clearly illustrated the surrounding subgemmal neurogenous plaque (streptavidin-biotin; 100).
LETTERS TO THE EDITOR
OOOO July 2015
96
REFERENCES 1. Palazzolo MJ, Fowler CB, Magliocca KR, Gnepp DR. Neuroepithelial structures associated with the subepithelial nerve plexus of taste buds: a fortuitous finding resembling the juxtaoral organ of Chievitz. Oral Surg Oral Med Oral Pathol Oral Radiol. 2014;117:497-501. 2. Gueiros LA, Leon JE, Lopes MA, Almeida OP, Jorge J. Subgemmal neurogenous plaque associated with burning tongue: report of two cases and review of the literature. Int J Oral Maxillofac Surg. 2008;37:773-776. 3. Gueiros LA, León JE, Leão JC, Lopes MA, Jorge J, Almeida OP. Subgemmal neurogenous plaque: clinical and microscopic evaluation of 7 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009;108:920-924. 4. Gondak R, Mauad T, Schultz L, Soares F, Kowalski LP, Vargas PA. Decreased CD1aþ, CD83þ and factor XIIIaþ dendritic cells in cervical lymph nodes and palatine tonsils of AIDS patients. Histopathology. 2014;64:234-241. 5. De Faria PR, Vargas PA, Saldiva PH, Böhm GM, Mauad T, Almeida OP. Tongue disease in advanced AIDS. Oral Dis. 2005;11:72-80.
http://dx.doi.org/10.1016/j.oooo.2015.02.487
Response to “Neuroepithelial structures associated with neurogenous subgemmal plaque of the tongue: an autopsy finding” To the Editor: This case is an interesting example of the recently described finding, initially published by our group, with regard to the posterior tongue. We described the posterior tongue exhibiting neuroepithelial structures resembling the juxtaoral organ of Chievitz associated with the subepithelial nerve plexus of taste buds. As noted by our group, the subepithelial nerve plexus of taste buds was
initially described by McDaniel in 1999.1 However, the term “subgemmal nerve plexus” or “subgemmal neurogenous plaque” has been used interchangeably in the literature. Gueiros et al. described the presence of this plexus in patients complaining of burning sensation of the tongue. As outlined by the authors, none of these previously reported cases were associated with the presence of neuroepithelial structures resembling the organ of Chievitz. This may give some credence to the thought that these neuroepithelial structures are perhaps embryologic remnants that fail to involute. However, the exact origin and function of these neuroepithelial structures and their association with the above-mentioned nerve plexus, whether fortuitous or not, has yet to be completely elucidated. We agree that the potential for misinterpretation of these structures as invasive squamous cell carcinoma or neural invasion remain an important diagnostic challenge for pathologists. Mitzi J. Palazzolo, DDS, MS Associate Professor Uniformed University of the Health Sciences (USUHS), Oral and Maxillofacial Pathology-Staff JBSA-Lackland WHASC/SAMMC San Antonio, Texas USA
REFERENCE 1. McDaniel RK. Subepithelial nerve plexus (with ganglion cells) associated with taste buds. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1999;87:605-609. http://dx.doi.org/10.1016/j.oooo.2015.03.010