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is extremely rare&#44; accounting for 0&#46;2&#37;&#8210;1&#46;1&#37; of all extranodal lymphomas&#44; with an estimated number of 165 new cases annually in the USA&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Secondary involvement by nodal lymphoma is more frequent&#46; The most commonly affected site is the ovary&#44; followed by the uterine cervix&#44; and the most common histopathological subtype is diffuse large B-cell lymphoma&#44; followed by follicular lymphoma&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;5&#44;6</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Regarding the risk factors&#44; it is suggested that a possible chronic antigenic stimulus may have a causal role&#44; but no factor has been well established yet&#46; In cutaneous B-cell marginal zone lymphomas&#44; a relationship with <span class="elsevierStyleItalic">Borrelia burgdorferi</span> has been suggested&#44; but this association has not been confirmed&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Regarding transgender individuals&#44; the question of the role of hormonal stimulation in the development of neoplasms is important&#46; For hormone-dependent neoplasms&#44; such as breast cancer&#44; this risk exists&#59; for NHL there is a hypothesis of a hormonal role in some studies&#44; but this relationship is suggested for female hormone replacement&#44; but is not described for male hormones&#44; as would be the case in transgender men&#44; as in the case described below&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">The authors describe a 42-year-old male transgender patient&#44; without comorbidities&#44; who presented to the Dermatology Outpatient Clinic with an asymptomatic&#44; slow-growing&#44; infiltrated&#44; erythematous tumor&#44; measuring 3&#8239;cm in the left preauricular region &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Histopathology disclosed an infiltrate of small lymphocytes&#44; with a &#8220;bottom-heavy&#8221; nodular growth pattern&#44; and no epidermal alterations&#46; The neoplastic cells were CD20&#43; and CD10 and MUM1 negative&#59; with CD21 staining in the lymphoid follicles&#59; BCL6&#43; both inside &#40;more evident&#41; and outside the follicles&#59; BCL2&#43; in B and T cells&#59; CD3 and CD5 revealed a background of reactive T cells but were negative in atypical cells &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Polymerase chain reaction &#40;PCR&#41; showed monoclonality for the IgH gene in the B cell population&#46; A diagnosis of FCL was made and no evidence of extracutaneous disease was found after staging with CT scans of the chest&#44; abdomen&#44; pelvis and cervix&#44; and a bone marrow biopsy&#46; The patient was treated with intralesional corticosteroids with a complete response &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">Regarding gender identity&#44; the patient started a hormonal transition &#40;with testosterone&#41; at the age of 40 years&#46; Two years after the diagnosis of cutaneous lymphoma&#44; the patient continued the transition by undergoing a total hystero-salpingo-oophorectomy&#46; Histopathology of the uterine cervix disclosed lymphoid aggregates in a nodular&#44; follicular pattern&#44; with a phenotype similar to that of the skin lesion &#40;CD20&#43;&#44; CD23 highlighting nodules&#44; in a background rich in T CD3&#43; and CD5&#43; cells&#44; weak BCL6&#43;&#44; with a strong similarity to the distribution of CD20&#43;&#44; CD10-&#44; MUM-&#44; Bcl2- cells in the germinal center&#44; and resembling the distribution of CD3&#43; and KI67 cells&#44; with lack of polarization inside the neoplastic follicles&#59; <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; PCR analysis for immunoglobulin was inconclusive&#46; The investigation of the t&#40;14&#59;18&#41; translocation in paraffin-embedded tissue&#44; both in the cervix and the skin of the face&#44; was negative&#46; The patient had no B symptoms and no signs of residual disease on PET-CT staging and a new bone marrow biopsy&#44; thus&#44; clinical follow-up without additional treatment was chosen&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">Two years later&#44; a new cutaneous nodule on the right thorax&#44; with the same clinical aspect as the one on the face&#44; was surgically excised&#44; and presented histopathologic findings again compatible with the diagnosis of FCL &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Figs&#46; 1</a> C and D&#41;&#46; The patient has been in complete remission for two years&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">After several multidisciplinary discussions&#44; no conclusion could be reached on the unification of the cutaneous and uterine findings&#46; Initially&#44; the diagnosis of FCL was made&#46; However&#44; extracutaneous spread of FCL is rare and&#44; when present&#44; is more frequent to local lymph nodes&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> No previous description of spread to the uterine cervix was found&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">One possibility would be a primary nodal lymphoma secondarily affecting the skin and cervix&#46; However&#44; no signs of nodal involvement were found when staging with tomography and later through PET-CT&#44; nor disease in the bone marrow biopsy&#44; at the time of the diagnosis in the skin and cervix&#46; Additionally&#44; nodal lymphomas are usually Bcl2 positive in germinal centers&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">This led to a third proposition of two different primary extranodal follicular B-cell lymphomas&#58; an FCL and a PFGSL&#46; Also&#44; for this association&#44; no previous description was found&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Another possibility would be that the involvement of the uterine cervix represents a pseudolymphoma&#46; Lymphoma-like lesions of the cervix were first described in 1985&#44; and there are other rare reports&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#44;10</span></a> Au et al&#46; described three cases of uterine cervix B-cell lymphomas&#44; but upon review concluded that two of the three were&#44; in fact&#44; pseudolymphomas&#46; The reported cases usually regressed spontaneously when the biopsy was repeated&#46; As possible diagnostic clues for pseudolymphoma&#44; a more superficial distribution of the infiltrate is suggested&#44; with heterogeneity of lymphoid cells and absence of masses or ulcerations&#44; but this can also occur in indolent lymphomas&#46; It can be suggested that the detection of the immunoglobulin gene rearrangement by PCR helps to differentiate these two diseases since the lymphoma is usually clonal while the pseudolymphoma&#44; as a reactional and non-neoplastic process&#44; is expected to be polyclonal&#46; However&#44; previous studies have shown that clonal rearrangement can also be detected in benign conditions&#44; reported&#44; for instance&#44; in 50&#37; of benign gastric lymphoid hyperplasia cases and 41&#37; of benign lymphoepithelial lesions of the salivary glands&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;12</span></a> Thus&#44; even though it is not conclusive&#44; it could be one more tool to help &#40;but not define&#41; the diagnosis&#46; Unfortunately&#44; in the current case&#44; clonal detection in the paraffin-embedded uterine cervix sample was inconclusive&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Although a definitive diagnosis was not possible&#44; the authors describe the association of two rare lymphoproliferative diseases and the diagnostic pitfalls of this group of diseases&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Financial support</span><p id="par0065" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Authors&#39; contributions</span><p id="par0070" class="elsevierStylePara elsevierViewall">Jade Cury-Martins&#58; Approval of the final version of the manuscript&#59; design and planning of the study&#59; drafting and editing of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; effective participation in research orientation&#59; critical review of the literature&#59; critical review of the manuscript&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Marcelo Abrante Giannotti&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; critical review of the manuscript&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Denis Miyashiro&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; critical review of the manuscript&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Juliana Pereira&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; critical review of the manuscript&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Jose Antonio Sanches&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; effective participation in research orientation&#59; critical review of the manuscript&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Conflicts of interest</span><p id="par0095" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span></span>"
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Letter - Dermatopathology
A unique case of a lymphoproliferative disorder affecting the skin and uterine cervix on a male transgender
Jade Cury-Martinsa,
Autor para correspondência
jadecury@yahoo.com.br

Corresponding author.
, Marcelo A. Giannottib, Denis Miyashiroa, Juliana Pereirac, José Antonio Sanchesa
a Department of Dermatology, Universidade de São Paulo, São Paulo, SP, Brazil
b Department of Pathology, Universidade de São Paulo, São Paulo, SP, Brazil
c Department of Hematology, Universidade de São Paulo, São Paulo, SP, Brazil
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Extranodal lymphomas account for 25&#37;-35&#37; of all Non-Hodgkin&#39;s lymphomas &#40;NHL&#41;&#46; The most common site of involvement is the gastrointestinal tract&#44; followed by the skin&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;2</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Primary cutaneous follicular center lymphoma &#40;FCL&#41; is the most common form of cutaneous B-cell lymphoma&#44; accounting for 50&#37;-60&#37; of cases&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;4</span></a> It affects mainly adults&#44; and has an excellent prognosis and a specific five-year survival of more than 95&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Extracutaneous spread is extremely rare&#44; but recurrences are frequent&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Primary female genital system lymphoma &#40;PFGSL&#41; is extremely rare&#44; accounting for 0&#46;2&#37;&#8210;1&#46;1&#37; of all extranodal lymphomas&#44; with an estimated number of 165 new cases annually in the USA&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Secondary involvement by nodal lymphoma is more frequent&#46; The most commonly affected site is the ovary&#44; followed by the uterine cervix&#44; and the most common histopathological subtype is diffuse large B-cell lymphoma&#44; followed by follicular lymphoma&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;5&#44;6</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Regarding the risk factors&#44; it is suggested that a possible chronic antigenic stimulus may have a causal role&#44; but no factor has been well established yet&#46; In cutaneous B-cell marginal zone lymphomas&#44; a relationship with <span class="elsevierStyleItalic">Borrelia burgdorferi</span> has been suggested&#44; but this association has not been confirmed&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Regarding transgender individuals&#44; the question of the role of hormonal stimulation in the development of neoplasms is important&#46; For hormone-dependent neoplasms&#44; such as breast cancer&#44; this risk exists&#59; for NHL there is a hypothesis of a hormonal role in some studies&#44; but this relationship is suggested for female hormone replacement&#44; but is not described for male hormones&#44; as would be the case in transgender men&#44; as in the case described below&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">The authors describe a 42-year-old male transgender patient&#44; without comorbidities&#44; who presented to the Dermatology Outpatient Clinic with an asymptomatic&#44; slow-growing&#44; infiltrated&#44; erythematous tumor&#44; measuring 3&#8239;cm in the left preauricular region &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Histopathology disclosed an infiltrate of small lymphocytes&#44; with a &#8220;bottom-heavy&#8221; nodular growth pattern&#44; and no epidermal alterations&#46; The neoplastic cells were CD20&#43; and CD10 and MUM1 negative&#59; with CD21 staining in the lymphoid follicles&#59; BCL6&#43; both inside &#40;more evident&#41; and outside the follicles&#59; BCL2&#43; in B and T cells&#59; CD3 and CD5 revealed a background of reactive T cells but were negative in atypical cells &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Polymerase chain reaction &#40;PCR&#41; showed monoclonality for the IgH gene in the B cell population&#46; A diagnosis of FCL was made and no evidence of extracutaneous disease was found after staging with CT scans of the chest&#44; abdomen&#44; pelvis and cervix&#44; and a bone marrow biopsy&#46; The patient was treated with intralesional corticosteroids with a complete response &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">Regarding gender identity&#44; the patient started a hormonal transition &#40;with testosterone&#41; at the age of 40 years&#46; Two years after the diagnosis of cutaneous lymphoma&#44; the patient continued the transition by undergoing a total hystero-salpingo-oophorectomy&#46; Histopathology of the uterine cervix disclosed lymphoid aggregates in a nodular&#44; follicular pattern&#44; with a phenotype similar to that of the skin lesion &#40;CD20&#43;&#44; CD23 highlighting nodules&#44; in a background rich in T CD3&#43; and CD5&#43; cells&#44; weak BCL6&#43;&#44; with a strong similarity to the distribution of CD20&#43;&#44; CD10-&#44; MUM-&#44; Bcl2- cells in the germinal center&#44; and resembling the distribution of CD3&#43; and KI67 cells&#44; with lack of polarization inside the neoplastic follicles&#59; <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; PCR analysis for immunoglobulin was inconclusive&#46; The investigation of the t&#40;14&#59;18&#41; translocation in paraffin-embedded tissue&#44; both in the cervix and the skin of the face&#44; was negative&#46; The patient had no B symptoms and no signs of residual disease on PET-CT staging and a new bone marrow biopsy&#44; thus&#44; clinical follow-up without additional treatment was chosen&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">Two years later&#44; a new cutaneous nodule on the right thorax&#44; with the same clinical aspect as the one on the face&#44; was surgically excised&#44; and presented histopathologic findings again compatible with the diagnosis of FCL &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Figs&#46; 1</a> C and D&#41;&#46; The patient has been in complete remission for two years&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">After several multidisciplinary discussions&#44; no conclusion could be reached on the unification of the cutaneous and uterine findings&#46; Initially&#44; the diagnosis of FCL was made&#46; However&#44; extracutaneous spread of FCL is rare and&#44; when present&#44; is more frequent to local lymph nodes&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> No previous description of spread to the uterine cervix was found&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">One possibility would be a primary nodal lymphoma secondarily affecting the skin and cervix&#46; However&#44; no signs of nodal involvement were found when staging with tomography and later through PET-CT&#44; nor disease in the bone marrow biopsy&#44; at the time of the diagnosis in the skin and cervix&#46; Additionally&#44; nodal lymphomas are usually Bcl2 positive in germinal centers&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">This led to a third proposition of two different primary extranodal follicular B-cell lymphomas&#58; an FCL and a PFGSL&#46; Also&#44; for this association&#44; no previous description was found&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Another possibility would be that the involvement of the uterine cervix represents a pseudolymphoma&#46; Lymphoma-like lesions of the cervix were first described in 1985&#44; and there are other rare reports&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#44;10</span></a> Au et al&#46; described three cases of uterine cervix B-cell lymphomas&#44; but upon review concluded that two of the three were&#44; in fact&#44; pseudolymphomas&#46; The reported cases usually regressed spontaneously when the biopsy was repeated&#46; As possible diagnostic clues for pseudolymphoma&#44; a more superficial distribution of the infiltrate is suggested&#44; with heterogeneity of lymphoid cells and absence of masses or ulcerations&#44; but this can also occur in indolent lymphomas&#46; It can be suggested that the detection of the immunoglobulin gene rearrangement by PCR helps to differentiate these two diseases since the lymphoma is usually clonal while the pseudolymphoma&#44; as a reactional and non-neoplastic process&#44; is expected to be polyclonal&#46; However&#44; previous studies have shown that clonal rearrangement can also be detected in benign conditions&#44; reported&#44; for instance&#44; in 50&#37; of benign gastric lymphoid hyperplasia cases and 41&#37; of benign lymphoepithelial lesions of the salivary glands&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;12</span></a> Thus&#44; even though it is not conclusive&#44; it could be one more tool to help &#40;but not define&#41; the diagnosis&#46; Unfortunately&#44; in the current case&#44; clonal detection in the paraffin-embedded uterine cervix sample was inconclusive&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Although a definitive diagnosis was not possible&#44; the authors describe the association of two rare lymphoproliferative diseases and the diagnostic pitfalls of this group of diseases&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Financial support</span><p id="par0065" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Authors&#39; contributions</span><p id="par0070" class="elsevierStylePara elsevierViewall">Jade Cury-Martins&#58; Approval of the final version of the manuscript&#59; design and planning of the study&#59; drafting and editing of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; effective participation in research orientation&#59; critical review of the literature&#59; critical review of the manuscript&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Marcelo Abrante Giannotti&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; critical review of the manuscript&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Denis Miyashiro&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; critical review of the manuscript&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Juliana Pereira&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; critical review of the manuscript&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Jose Antonio Sanches&#58; Approval of the final version of the manuscript&#59; collection&#44; analysis&#44; and interpretation of data&#59; effective participation in research orientation&#59; critical review of the manuscript&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Conflicts of interest</span><p id="par0095" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span></span>"
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