Case and Research Letters
Mitotic Rate as a Prognostic Factor in Melanoma: Implications for Disease Management
El índice mitótico como factor pronóstico y sus implicancias en el manejo del melanoma
a Departamento de Dermatología, Hospital General de Agudos Dr. Cosme Argerich, Buenos Aires, Argentina
b Departamento de Dermatología, Melanoma Group IDIBAPS, Hospital Clínic, Universitat de Barcelona, Barcelona, Spain
c Departamento de Dermatología, HIGA Prof. Dr. Rodolfo Rossi, La Plata, Argentina
d Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Barcelona, Spain
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Predictors of nodal involvement include Breslow thickness, ulceration, and mitotic rate.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The eight edition of the American Joint Committee on Cancer (AJCC-8) melanoma staging system removed mitotic rate as a predictive factor in melanoma because of its poor reproducibility secondary to low intraobserver and interobserver reliability.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> The National Comprehensive Cancer Network Guidelines (version 1.2018), by contrast, suggest that SLN biopsy should be considered in patients with T1a melanoma (<0.8 mm, nonulcerated) and a mitotic rate of > 2 mitoses/mm<span class="elsevierStyleSup">2</span>, particularly if they are young. There is ample evidence that mitotic rate is predictive of SLN positivity (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a><span class="elsevierStyleBold">)</span>. According to a multicenter European study, SLN positivity was the most important prognostic factor in thin melanomas (n = 4249, Breslow thickness < 1 mm), and the only predictor of this positivity was a mitotic rate of > 2 mitoses/mm<span class="elsevierStyleSup">2</span>. T1a melanoma was associated with an overall risk of SLN positivity of 3.4% (or 1.2% for patients with a mitotic rate of 0 mitoses/mm<span class="elsevierStyleSup">2</span>), but this risk was 20% for > 2 mitoses/mm<span class="elsevierStyleSup">2</span>, which is even higher than that observed for T1b melanoma (8%).<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> In melanoma patients downstaged to T1a under the AJCC-8 criteria, the 3-year disease-free survival rate was 95%. This rate was significantly lower, however, at 80%, in those with a mitotic rate of > 3 mitoses/mm.<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> A US study of 17 204 patients with melanoma with a Breslow thickness of 0.01-1 mm reported a linear relationship between mitotic rate and SLN involvement. After adjustment for known prognostic factors, patients with a rate of > 1 mitoses/mm<span class="elsevierStyleSup">2</span> were twice as likely to have SLN involvement than those with < 1 mitoses/mm<span class="elsevierStyleSup">2</span>. The risk of SLN involvement was 7.9% in patients with 1 mitosis/mm<span class="elsevierStyleSup">2</span>, but 21.8% and 44.5% for those with 5 and > 10 mitoses/mm<span class="elsevierStyleSup">2</span>, respectively. A recent European study that included a large cohort for the development (n = 3666) and validation (n = 4227) of a nomogram to improve the selection of patients with thin melanoma (Breslow thickness, < 1 mm) for SLN biopsy showed that age, Breslow thickness, a mitotic rate of > 1 mitosis/mm<span class="elsevierStyleSup">2</span>, ulceration, lymphovascular invasion, and regression > 75% were all significant predictors of SLN involvement. The resulting nomogram performed better than models based on current international recommendations at identifying which patients with thin melanomas should undergo SLN biopsy and showed that the higher the number of mitoses, the greater the likelihood of SLN involvement.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> Based on these studies, we strongly recommend rigorous assessment of patients with thin melanomas and a high mitotic rate and consider that SLN biopsy should always be contemplated.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">The predictive value of mitotic rate is not limited to thin melanomas. One Italian study of 1524 patients with melanoma with a Breslow thickness > 1 mm found a significant association between mitotic rate and SLN involvement. In particular, a rate of > 1 mitosis/mm<span class="elsevierStyleSup">2</span> was associated with worse disease-free survival (hazard ratio, 1.82; 95% CI, 1.02-3.24; <span class="elsevierStyleItalic">P</span> = .043).<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Similar results were obtained in a Canadian study of thin melanomas (n = 1072), where a mitotic rate of > 1 mitosis/mm<span class="elsevierStyleSup">2</span> was the only associated factor for SLN involvement in patients with a Breslow thickness of 1.01-2.0 mm.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> A Spanish study of 141 patients with a mean Breslow thickness of 2.6 mm reported that ≥ 2 mitoses/mm<span class="elsevierStyleSup">2</span> was associated with worse disease-free and overall survival rates.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> Another study of 128 patients attempting to explain the paradoxically worse survival rates observed in patients with stage IIC versus IIIA melanoma found that an age of 55 years or older and a mitotic rate of > 5 mitoses/mm<span class="elsevierStyleSup">2</span> were independent predictors of overall survival.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> The authors suggested that stage IIC and IIIA melanomas might be biologically distinct and that mitotic rate should be considered in this subgroup of patients. A large US study of 71 235 patients with melanoma that used 3 cutoff points for mitotic rate (0-3, 4-10 and > 10 mitoses/mm<span class="elsevierStyleSup">2</span>) found a linear association between mitotic rate and disease-specific survival for stages I, II, and III. In patients with stage I melanoma, the 5-year disease-specific survival rate was 98.3% for patients with a mitotic rate of 0-3 mitoses/mm<span class="elsevierStyleSup">2</span> versus 79.7% for those with a rate of > 10 mitoses/mm<span class="elsevierStyleSup">2</span>. The corresponding rates were 86.1% versus 72.9% for patients with stage II melanoma and 72.5% (0-3 mitoses/mm<span class="elsevierStyleSup">2</span>) versus 49.7% for those with stage III melanoma. Mortality risk increased by 23% for each unit increase in mitotic rate among patients with stage I disease, and the corresponding increases for patients with stage II and III disease were 5% and 3%, respectively. Patients with stage I disease and > 10 mitoses/mm<span class="elsevierStyleSup">2</span> had an almost 7-fold increased risk of mortality compared with those with 0-3 mitoses/mm<span class="elsevierStyleSup">2</span>.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> A recent Australian study of 156 children and adolescents younger than 20 years with a median Breslow thickness of 1 mm showed that mitotic rate had greater prognostic value than Breslow thickness, and was the only independent predictor of recurrence-free survival.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Mitotic rate is an important prognostic factor in melanoma. We recommend individualized management of patients with a high mitotic rate, and believe that those with a Breslow thickness of > 1 mm should be considered for SLN biopsy and undergo staging studies and close follow-up. Diagnostic procedures should also be optimized to increase the reproducibility of mitotic rate assessment.</p></span>" "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Please cite this article as: Bois MC, Morgado-Carrasco D, Barba PJ, Puig S. El índice mitótico como factor pronóstico y sus implicancias en el manejo del melanoma. Actas Dermosifiliogr. 2021;112:941–943.</p>" ] ] "multimedia" => array:1 [ 0 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:3 [ "leyenda" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Abbreviation: SLN, sentinel lymph node.</p>" "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleItalic">Melanomas with a Breslow thickness <1 mm</span> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A mitotic rate > 2 mitoses/mm<span class="elsevierStyleSup">2</span> appears to be the only risk factor for SLN involvement.<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>There is a linear association between number of mitoses and risk of SLN involvement (5.4% for 0 mitoses/mm2, 21.8% for 5 mitoses/mm<span class="elsevierStyleSup">2</span>, 38.3% for 10 mitoses/mm<span class="elsevierStyleSup">2</span>).<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>T1a melanoma with a mitotic rate > 2 mitoses/mm<span class="elsevierStyleSup">2</span> is associated with a higher risk of SLN involvement than T1b melanoma (20% vs. 8%).<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Three-year disease-free survival is worse in patients with a mitotic rate > 3 mitoses/mm.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,4</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A mitotic rate > 10 mitoses/mm2 is associated with an almost 7-fold increased risk of mortality compared with one of 0-3 mitoses/mm<span class="elsevierStyleSup">2</span>.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Mortality risk increases by 23% for each unit increase in mitotic rate.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_colgroup " colspan="1" align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleItalic">Melanomas with a Breslow thickness > 1 mm</span> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Mitotic rate is predictive of SLN involvement (34.4% of patients with mitosis had positive SLN status versus 12.8% of those without mitosis).<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A mitotic rate > 3 mitoses/mm2 is associated with significantly worse disease-free and overall survival.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a><span class="elsevierStyleSup">,</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A high mitotic rate may explain the worse survival observed in stage IIC compared with stage IIIA melanoma.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>For each unit increase in mitotic rate, mortality risk increases by 5% in patients with stage II melanoma and by 3% in those with stage III melanoma.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2740433.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">In another study with fewer patients (n = 141), a mitotic rate of ≥ 2 mitosis/mm<span class="elsevierStyleSup">2</span> was associated with significantly worse disease-free and overall survival.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Mitotic Rate as a Prognostic Factor in Melanoma.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:11 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "A retrospective, multicenter analysis of the predictive value of mitotic rate for sentinel lymph node (SLN) positivity in thin melanomas" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "H. 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