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Update on surgical treatment of primary and metastatic cutaneous melanoma
Actualización en el tratamiento quirúrgico del melanoma cutáneo primario y metastásico
María Alejandra Zuluaga-Sepúlvedaa, Ivonne Arellano-Mendozab, Jorge Ocampo-Candiania,
Corresponding author
jocampo2000@yahoo.com.mx

Corresponding author at: Universidad Autónoma de Nuevo León, Av. Madero y Gonzalitos s/n, Col.: Mitras Centro, C.P. 64000, Monterrey, Nuevo León, Mexico. Tel.: +52 (81) 8363 5635; fax: +52 (81) 8363 5337.
a Servicio de Dermatología, Hospital Universitario Dr. José E. González, Monterrey, Nuevo León, Mexico
b Servicio de Dermatología, Hospital General de México Dr. Eduardo Liceaga, México, D.F., Mexico
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Background</span><p id="par0005" class="elsevierStylePara elsevierViewall">Primary cutaneous melanoma is one of the most common skin cancers&#46; It is the fifth most common malignant neoplasm in men and the sixth most common in women&#59; it is associated with high morbimortality due to its aggressive behaviour&#44; its high risk of regional and distant lymph node metastases&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">1</span></a> It is estimated that in the United States approximately 76&#44;000 people will have been diagnosed with melanoma in 2014&#44; and 9710 deaths will be attributed to this cancer&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">2</span></a> Seventy-five percent of skin cancer-related deaths are due to melanoma&#46; However&#44; it is believed that these figures are an underestimation of reality&#44; as a considerable number of <span class="elsevierStyleItalic">in situ</span> or superficial melanomas are not reported&#46; The risk during life of acquiring an <span class="elsevierStyleItalic">in situ</span> or superficial melanoma has considerably increased&#44; at 1 in 30 from 1 in 1500 in 1935&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">3</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Epidemiology</span><p id="par0010" class="elsevierStylePara elsevierViewall">Although melanoma has a peak of presentation between the fifth and sixth decades of life&#44;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">4</span></a> its incidence in people aged between 25 and 29 has increased to become the most common cancer in this age group&#46; Ninety-five percent of cases start on the skin&#44; the remainder originate from the eyes and mucosa &#40;oral&#44; vagina or anus&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">5</span></a> and from 3&#37; to 10&#37; of people present with metastatic disease with no clinically evident primary lesion&#46;<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">6</span></a></p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Diagnostic approach</span><p id="par0015" class="elsevierStylePara elsevierViewall">If a melanoma is suspected a complete physical examination of all of the skin should be made&#44; including the oral and anogenital mucosa&#44; the palms of the hands&#44; and the soles of the feet&#46; There is increasing interest in dermatoscopy<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">7</span></a> as a diagnostic technique in the study of skin tumours&#44; especially pigmented tumours&#46; Advanced digital computed imaging techniques are also used&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Once the pigmented lesions suspicious of melanoma have been detected&#44; an excisional biopsy should be performed &#40;margin of 1&#8211;3<span class="elsevierStyleHsp" style=""></span>mm&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">8</span></a> ideally with negative margins&#46; On the limbs&#44; it should be directed longitudinally in order not to subsequently alter the sentinel node result&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">An appropriate biopsy should enable the Breslow&#39;s depth to be assessed&#44; since the extension tests that are required&#44; the final surgical margin&#44; and the patient&#39;s prognosis will depend on this Breslow&#39;s depth&#44; which is the depth of the melanoma measured in millimetres from the most superficial layer of the epidermis to the deepest point of penetration&#46; The greater the Breslow depth the poorer the patient&#39;s prognosis&#44; and the lower the cure rates&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Excisional biopsy is not appropriate on&#58; the palms of the hands&#44; the soles of the feet&#44; the face&#44; fingers&#44; subungual region&#44; outer ear or on very large lesions&#59; and in these cases it is indicated that an incisional biopsy is acceptable&#44; taking the portion which has been clinically shown to be deeper&#46; If the incisional biopsy does not allow accurate microstaging of the patient &#8211; which is frequent due to underestimating the thickness of the lesion &#8211; it is appropriate to repeat the procedure&#44; and preferably go on to perform an excisional biopsy&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Preoperative staging</span><p id="par0035" class="elsevierStylePara elsevierViewall">When the diagnosis of melanoma has been confirmed&#44; the patient needs to be staged&#46; This is determined by the thickness&#44; the histological features of the melanoma and the locoregional spread of the disease&#46; Staging enables the risk of lymph node and systemic metastasis of the melanoma to be evaluated&#44; which increases according to the thickness of the lesions&#46; The recommendation&#44; according to NCCN guidelines &#40;National Comprehensive Cancer Network&#41;&#44; 2014&#44;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a> is that routine testing for spread should not be undertaken in patients with stages I and II&#44; unless the patient presents symptoms or signs of disease distant from the primary tumour&#46; By contrast&#44; they do stress that there should be a complete physical examination of the skin&#44; the regional lymphatic pathways&#44; and of the nodal basin&#46; If there are any doubts on physical examination of the lymph nodes&#44; it is suggested that an ultrasound should be performed of the nodal basin before sentinel node biopsy&#46; If a suspicious lesion is found on ultrasound&#44; this should be confirmed histologically&#46; For stage III patients with positive sentinel nodes &#40;clinically negative&#41; the panellists leave the decision to treating physician whether to undertake a computed tomography &#40;CT&#41; scan or a positron emissions scan &#40;PET&#47;CT&#41;&#46; They consider that histological confirmation of lymph node spread is appropriate by fine needle aspiration&#44; core needle biopsy or open biopsy&#44; and imaging studies for the purpose of staging&#44; and evaluating specific signs and symptoms in patients with stage III melanoma with clinically positive lymph nodes&#46; For patients with stage IV melanoma with distant metastasis&#44; the consensus recommends confirming the metastasis histologically&#44; and ideally perform a genetic study &#40;BRAF or c-Kit mutation&#41; to start targeted therapy&#44; lactic dehydrogenase &#40;prognostic marker&#41; in addition to imaging studies &#40;CT with or without PE&#47;CT&#41;&#44; including magnetic resonance &#40;MRI&#41; or contrasted CT of the central nervous system due to the high incidence of brain metastasis in stage IV patients&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Surgical management</span><p id="par0040" class="elsevierStylePara elsevierViewall">The surgery recommended to remove this tumour&#44; also known as wide radical excision&#44; is the appropriate way to manage primary cutaneous melanoma in stages I&#8211;III&#44; and including cases with regional nodal metastasis&#46; The fundamental objective is to excise both the visible and microscopic tumour&#44; and micro- and macroscopic satellites&#46; This type of surgery must meet 2 criteria&#58; the resection of the primary tumour should include a peripheral margin of normal skin measured from the visible edge of any residual pigmentation&#44; tumour tissue or biopsy scar&#44; and the deep margin of the excision should extend to the muscular fascia&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a> However&#44; it has not been demonstrated that including the muscular fascia in the resection is sufficient for the procedure to be successful&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">12</span></a> The appropriate excision margins have been widely investigated in randomised clinical studies&#44;<a class="elsevierStyleCrossRefs" href="#bib0285"><span class="elsevierStyleSup">13&#44;14</span></a> and it has been found necessary to widen the margins as the Breslow depth of the melanoma increases<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a> &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; It is considered unlikely that margins greater than 2<span class="elsevierStyleHsp" style=""></span>cm have a significant impact on local recurrence &#40;12&#37;&#41; and the poor 5-year survival rate &#40;55&#37;&#41; of patients with melanomas with a Breslow depth greater than 4<span class="elsevierStyleHsp" style=""></span>mm&#44; therefore offering appropriate management which&#44; functionally and aesthetically&#44; is more acceptable for the patient&#46;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">15</span></a> The evidence shows that the failure of the most radical procedures&#44; such as margins of 3&#8211;5<span class="elsevierStyleHsp" style=""></span>cm and limb amputation&#44; is due to the melanoma&#39;s intrinsic aggressive behaviour and not to inadequate primary surgical management&#46; Persistence of melanoma-positive margins&#44; on histological examination of the excision&#44; requires a second excision to be made&#46; In cases when it is not possible to achieve tumour-free negative margins&#44; complementary radiotherapy has been suggested&#44; which has demonstrated a decrease in local recurrence rates of some histological types of melanoma&#46;<a class="elsevierStyleCrossRefs" href="#bib0300"><span class="elsevierStyleSup">16&#44;17</span></a></p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0045" class="elsevierStylePara elsevierViewall">Melanomas located on the palms of the hands&#44; soles of the feet&#44; head&#44; neck and those which are histologically associated with ulceration&#44; angiolymphatic invasion&#44; satellitosis or high Breslow depth have a greater risk of local recurrence after wide radical excision&#46; In Balch et al&#46; study of 2001<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">18</span></a> it was demonstrated that for melanomas of 1&#8211;4<span class="elsevierStyleHsp" style=""></span>mm thickness&#44; local recurrence is associated with high mortality&#44; and that ulceration on the primary melanoma is the most important prognostic factor which should alert us to the high risk of local recurrence and metastasis&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">For the majority of cases it is recommended that the residual defect should be reconstructed with primary closure or a total or partial thickness graft&#46; Flaps are only indicated in cases where the primary defects are too large to perform the abovementioned procedures&#46; If a graft is the best option for reconstructing a defect on a limb&#44; it should not be collected from the proximal limb&#44; as this could potentially reintroduce tumour cells into the reconstructed wound&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Most guidelines recommend managing melanomas with margins of 0&#46;5<span class="elsevierStyleHsp" style=""></span>cm <span class="elsevierStyleItalic">in situ</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a> However&#44; applying these margins has been demonstrated to be insufficient for managing lentigo maligna located in the head and neck due to the principally radial growth of this melanoma subtype&#46; For this reason&#44; it is better approached if a method with control of the margin is used&#44; deferring reconstruction of the defect until complete excision of the tumour has been confirmed&#46;<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">19</span></a> For melanoma <span class="elsevierStyleItalic">in situ</span> in anatomical areas other than the head and neck&#44; it is useful to make a wide radical excision with margins of 0&#46;5&#8211;1<span class="elsevierStyleHsp" style=""></span>cm&#44; better cure rates have been reported with margins of 1<span class="elsevierStyleHsp" style=""></span>cm&#44; without considerable differences in morbidity&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a></p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Approach to the patient with clinically negative metastasis-sentinel lymph node biopsy</span><p id="par0060" class="elsevierStylePara elsevierViewall">After surgical management of the melanoma&#44; the next step is to stage the regional lymph nodes&#46; Melanoma <span class="elsevierStyleItalic">in situ</span> has a metastatic potential that is not significant&#44; as do melanomas with a Breslow depth of less than 1<span class="elsevierStyleHsp" style=""></span>mm which are not associated with other histological factors with a poor prognosis &#40;&#60;<span class="elsevierStyleHsp" style=""></span>5&#37;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">20</span></a> For melanomas with a Breslow depth of between 1 and 4<span class="elsevierStyleHsp" style=""></span>mm the risk of micrometastasis to regional lymph nodes is 20&#8211;25&#37;&#44; and 3&#8211;5&#37; for distant metastasis&#44;<a class="elsevierStyleCrossRefs" href="#bib0325"><span class="elsevierStyleSup">21&#44;22</span></a> and considered as the principal prognostic factor for long-term survival in patients with stage I and III melanoma&#46; These are not easily detectable with imaging techniques such as ultrasound&#44;<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">23</span></a> or even PET&#47;TC&#44;<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">24</span></a> which is one of the diagnostic tools suggested to define the presence or otherwise of metastasis in melanoma patients&#46; Sentinel lymph node biopsy is a minimally invasive procedure which is highly accurate in detecting lymph node micrometastasis&#44; and it has replaced elective lymphadenectomy in staging patients with clinically negative lymph nodes&#46; A randomised study revealed that sentinel lymph node biopsy provides important prognostic information&#44; in identifying patients with primary melanomas with an intermediate or thick Breslow depth&#44; with nodal metastasis who would benefit from immediate completion lymphadenectomy&#44; which prolongs disease-free survival and distant spread of the disease&#44; in patients with melanomas of intermediate thickness&#46;<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">25</span></a> The ideal candidate for sentinel lymph node biopsy is a patient with a melanoma of a Breslow depth of at least 1<span class="elsevierStyleHsp" style=""></span>mm and with no clinical or radiological regional lymph node metastases&#46; The indications for sentinel lymph node biopsy were recently broadened&#44; and it is recommended in patients with a Breslow depth of 1&#8211;4<span class="elsevierStyleHsp" style=""></span>mm in any anatomical location&#44; in staging regional disease in patients with a Breslow &#62;<span class="elsevierStyleHsp" style=""></span>4<span class="elsevierStyleHsp" style=""></span>mm&#44; and in patients with a Breslow depth of 0&#46;75&#8211;1<span class="elsevierStyleHsp" style=""></span>mm associated with adverse histological factors such as ulceration&#44; mitotic rate<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>1&#44; angiolymphatic invasion or sattelitosis&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">26</span></a> It is also recommended that a sentinel lymph node biopsy should be routine in paediatric patients with a melanoma of a Breslow depth of 1<span class="elsevierStyleHsp" style=""></span>mm or larger&#44; because these patients have a greater risk of lymph node metastasis than adults&#44; despite their better prognosis&#46; Atypical melanocytic nevi in children and adolescents have a high rate of positive sentinel lymph nodes&#46; Therefore&#44; sentinel lymph node biopsy could be indicated in paediatric patients in whom a melanoma is included as a differential diagnosis&#46;<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">27</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">The use of sentinel lymph node biopsy in some melanoma subtypes is controversial&#59; in pure desmoplasic melanoma&#44; for example&#44; a low incidence of nodal metastases has been demonstrated &#40;0&#8211;4&#37;&#41;<a class="elsevierStyleCrossRefs" href="#bib0360"><span class="elsevierStyleSup">28&#44;29</span></a>&#59; however in others&#44; rates of regional metastases of up to 14&#37; have been found&#44; and for mixed desmoplasic melanoma the incidence is higher &#40;25&#37;&#41; than for pure desmoplasic melanoma&#44; similar to that of non-desmoplasic melanoma&#46;<a class="elsevierStyleCrossRefs" href="#bib0370"><span class="elsevierStyleSup">30&#44;31</span></a> Some authors&#44; however&#44; consider that the risk of lymph node metastasis of desmoplasic melanoma is sufficient justification for undertaking a sentinel lymph node biopsy if a Breslow depth of 1<span class="elsevierStyleHsp" style=""></span>mm or more is found in these tumours&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">Despite the high precision of sentinel lymph node biopsy in detecting lymph node micrometastasis&#44; there are some cases where the use of this technique is suboptimal&#44; in patients who have already undergone wide radical excision and defect closure&#44; for example&#44; when lymphogammagraphy has revealed more than 2 lymph node drainage basins&#44; in melanomas near or on the lymph node drainage basin&#44; melanomas of the head and neck where lymphogammagraphy has mapped an intraparotid sentinel lymph node&#44; when there are confirmed distant lymph node metastases&#44; when lymphogammagraphy is negative&#44; and when life expectancy is limited&#44; due to advanced melanoma&#44; or other comorbidities&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">Although sentinel lymph node biopsy is not a very invasive procedure&#44; it is not complication-free&#46; Complications include those of the surgical wound &#40;infections&#44; dehiscence&#44; etc&#46;&#41; lymphoedema &#40;&#60;<span class="elsevierStyleHsp" style=""></span>5&#37;&#41;&#44; the formation of seroma&#44; reactions to the contrast medium &#40;&#60;1&#37;&#41; and false-negative results &#40;5&#8211;15&#37;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">32</span></a></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Approach to the patient with clinically positive lymph node metastasis</span><p id="par0080" class="elsevierStylePara elsevierViewall">When patients present with a primary melanoma&#44; and with clinically palpable lymph nodes&#44; lymph node metastasis of the melanoma should be staged and confirmed by fine needle aspiration biopsy &#40;FNAB&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">33</span></a> FNAB is a fast&#44; precise and clinically useful technique for evaluating patients with a suspected metastatic melanoma&#46; In the event that the tissue obtained with FNAB is not sufficient for a diagnosis or that the resource is not available&#44; excisional lymph node biopsy is suggested&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The survival rates of patients who present with clinically palpable lymph node metastasis reduce significantly &#40;10&#8211;50&#37;&#41;&#44; according to the number of lymph nodes affected&#44; the extent of spread to the lymph nodes&#44; and the Breslow depth of the primary melanoma&#46;<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">34</span></a></p><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Surgical treatment of lymph node metastasis</span><p id="par0090" class="elsevierStylePara elsevierViewall">After regional lymph node metastasis of the melanoma has been confirmed&#44; the standard treatment is radical lymphadenectomy&#46; This in turn is known by 3 different terms according to the method used for diagnosis&#44; and whether or not it has been confirmed histologically&#46; Thus&#44; completion lymphadenectomy refers to surgery after a positive sentinel lymph node biopsy&#58; elective lymphadenectomy when surgery is performed on clinically negative lymph node basins&#44; and when nodal involvement has not been confirmed histologically&#44; and finally&#44; the procedure performed on clinically positive lymph node basins after histological confirmation&#44; which is known as therapeutic lymphadenectomy&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">11</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">Therapeutic lymphadenectomy is indicated in all patients with clinically evident lymph node metastases&#44; and should not be replaced by radiotherapy or systemic adjuvant therapy&#44; although they can be used as coadjuvant treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">35</span></a> Therapeutic lymphadenectomy is not indicated for patients in whom extensive distant metastasis and&#47;or large lymph node metastasis&#44; fixed to adjacent structures&#44; has been confirmed&#46; These patients have a poor prognosis and might benefit from other treatments&#44; such as palliative radiotherapy or systemic therapy&#46; Elective lymphadenectomy is not routinely performed&#44; and as mentioned above&#44; has been substituted by sentinel lymph node biopsy&#46; There is some controversy with regard to the function and indications of completion lymphadenectomy after positive sentinel lymph node biopsy&#46; To date&#44; it has not been confirmed that completion lympadenectomy improves patient survival compared with observation after positive sentinel lymph node biopsy&#44; or that all patients with a positive sentinel lymph node biopsy would benefit from completion lymphadenectomy&#44; as they do not all develop clinically evident lymph node metastasis&#44; and sentinel lymph node biopsy might have resected the only focus of nodal metastasis&#46; Furthermore&#44; for the moment&#44; there is no evidence from patients with positive sentinel lymph node biopsy who do not have at least a 5&#37; probability of other non-sentinel lymph node involvement&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">26</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">At present&#44; the conclusion of the guidelines from the American Society of Clinical Oncology-Society of Surgical Oncology &#40;ASCO-SSO&#41;&#44; is to perform completion lymphadenectomy on all patients with a positive sentinel lymph node biopsy&#44; and if the patient refuses lymphadenectomy&#44; strict follow-up is recommended to enable the detection and early treatment of lymph node recurrence&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">26</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Treatment of local recurrence</span><p id="par0105" class="elsevierStylePara elsevierViewall">Locally recurring melanoma is associated in most cases with systemic metastasis&#44; which dramatically reduces these patients&#8217; 10 year survival &#40;5&#37;&#41;&#46; The initial Breslow thickness is the greatest prognostic indicator of local recurrence&#44; and death in patients with melanoma&#44; associated with other adverse histological factors such as ulceration and mitosis&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a> Clinically it presents as a blue subcutaneous nodule&#44; of variable size but usually from 2 to 5<span class="elsevierStyleHsp" style=""></span>cm in diameter&#44; which commonly presents in the neighbourhood of the excision of the primary melanoma &#40;satellite metastasis&#41; or en route to the regional lymphatic drainage basin &#40;in-transit metastasis&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a> In these cases&#44; diagnosis should be made by FNAB or with excisional biopsy under local anaesthesia&#46; When a diagnosis of recurrent melanoma is confirmed&#44; the next step is to undertake further imaging studies &#40;CT&#44; MRI or PET&#47;CT&#41;&#44; and sentinel lymph node biopsy&#44; if the patient is a candidate&#44; for re-staging&#44; to evaluate symptoms&#44; and to define management&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">Ideally&#44; in patients with recurrent melanoma &#40;local&#44; satellite and&#47;or in-transit&#41;&#44; tissue should be taken for genetic analysis of the tumour&#44; which is particularly important in order to assess the use of targeted therapies&#44; or plan their inclusion in a clinical study&#46; If the absence is confirmed of regional nodal disease&#44; surgical excision is recommended with negative margins&#44; and primary closure of the defect&#44; where possible&#46; Patients with resectable in-transit recurrence might benefit from sentinel lymph-node biopsy&#44; in addition to wide radical excision&#44; and reconstruction of the defect with graft or flap&#46; Although it is still not clear whether resection margins should be wide in recurrences&#44; it is clear that a margin of normal skin should be left&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a></p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Special clinical situations</span><p id="par0115" class="elsevierStylePara elsevierViewall">There are still questions as to the correct management of patients with primary melanoma in some clinical situations&#44; such as subungual melanoma&#44; acral melanoma&#44; or the appropriate management of pregnant patients with a diagnosis of melanoma&#46; However&#44; expert recommendations are a tool on which management of these cases can be based&#46;</p><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Subungual melanoma</span><p id="par0120" class="elsevierStylePara elsevierViewall">This is a rare variant of melanoma in the white population&#44; with a prevalence of 3&#37;&#44; in contrast to its prevalence in black patients&#44; of 15&#8211;35&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">36</span></a> The most common location of this melanoma is the first finger and the first toe &#40;75&#37;&#41;&#46; It presents clinically as a longitudinal melanonychia&#44; de novo or pre-existing with recent changes&#46; Hutchinson&#39;s sign &#8211; pigmentation of the periungual skin &#8211; is highly suggestive of melanoma &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Amelanic melanoma presents atypically to conventional melanoma&#44; as an erythmatose&#44; frequently ulcerative nodule in the subungual region associated with onycholysis&#44; and dystrophy of the nail plate with an absence of pigment&#46; If there are any of these signs a biopsy should be taken for histological confirmation&#46; Longitudinal biopsy which includes where possible all the pigmentation &#40;excisional&#41;&#44; as with other types of melanoma&#44; is the ideal technique for studying a lesion for which melanoma is the differential diagnosis&#46; Biopsy should include tissue from the nail bed&#44; and reach the periosteum in depth&#46;<a class="elsevierStyleCrossRef" href="#bib0405"><span class="elsevierStyleSup">37</span></a></p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0125" class="elsevierStylePara elsevierViewall">The margins for wide radical excision are based on the guidelines according to Breslow thickness&#44; and adverse histological factors&#46; If the melanoma is <span class="elsevierStyleItalic">in situ</span>&#44; the recommended margins are 5<span class="elsevierStyleHsp" style=""></span>mm&#44; including the bed and proximal matrix&#44; and reconstruction with partial thickness graft&#46; The most appropriate management of an invasive subungual melanoma of a lower limb is amputation at the level of the metatarsophalangeal joint&#46; However&#44; for an invasive subungual melanoma affecting an upper limb&#44; amputation at the level of the joint distal to the lesion is preferred&#44; using margins of 1<span class="elsevierStyleHsp" style=""></span>cm&#44; with the objective of giving the patient more conservative management&#44; enabling better function of the hand&#46;<a class="elsevierStyleCrossRef" href="#bib0410"><span class="elsevierStyleSup">38</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">Indications for sentinel lymph node biopsy in subungual melanoma are based on the guidelines for managing conventional melanoma based on the thickness of the melanoma&#44; and the presence or otherwise of palpable lymph nodes&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">26</span></a></p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Plantar acral melanoma</span><p id="par0135" class="elsevierStylePara elsevierViewall">The importance of this clinical subtype of melanoma is the poor prognosis associated with it due to late diagnosis&#46;<a class="elsevierStyleCrossRef" href="#bib0415"><span class="elsevierStyleSup">39</span></a> High clinical suspicion on the part of the treating physician is required in addition to training in dermatoscopy&#44; as this tool is very useful in deciding whether to take a biopsy from a plantar melanocytic lesion&#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a></p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0140" class="elsevierStylePara elsevierViewall">Biopsy in these patients should be excisional&#46; However&#44; incisional biopsy can be used when the lesions are very large&#46; Definitive management is based on the stage of the disease and the management recommended by the established guidelines for melanoma for equivalents in thickness and histology in other skin locations&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a></p><p id="par0145" class="elsevierStylePara elsevierViewall">The decision to perform a sentinel lymph-node biopsy is based on the above-mentioned ASCO-SSO indications according to the stage of the melanoma&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">26</span></a> Therapeutic lymphadenectomy is recommended for primary melanoma with clinically positive lymph nodes&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">Reconstruction of defects on the sole of the foot depends on their location on the plantar surface&#44; the disease stage&#44; comorbidities&#44; and the patient&#39;s lifestyle&#46; In patients with defects in non-weight bearing sites&#44; sedentary patients&#44; comorbidities and&#47;or associated metastatic disease a primary closure of the defect is preferred with either partial or total skin graft&#46; For defects on weight-bearing sites on the plantar surface&#44; the reconstruction options are rotation or advance skin flaps or free musculocutaneous flaps&#44; preferably performed by a reconstructive plastic surgeon&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a></p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Lentigo maligna</span><p id="par0155" class="elsevierStylePara elsevierViewall">With a lesion on the face suggestive of lentigo where malignant changes are suspected&#44; a biopsy should be taken to confirm the diagnosis&#46; However&#44; the appropriate method for biopsy is a challenge&#44; as these are usually lesions with poorly defined edges&#44; which are large for such an aesthetically sensitive area as the face&#46; According to the guidelines for the management of melanoma&#44; the most appropriate method is excisional biopsy&#59; incisional or shave biopsy are often suboptimal&#46; However&#44; an acceptable option is a deep incisional biopsy&#44; or punch biopsy of the area which is seen clinically to be the deepest&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">10</span></a> Shave biopsy can compromise complete histological evaluation of the tumour&#44; and appropriate Breslow&#39;s depth measurement&#44; therefore we do not use this technique for diagnosing melanoma in our patients&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">When a diagnosis of lentigo maligna has been confirmed the tumour is resected&#44; 5<span class="elsevierStyleHsp" style=""></span>mm margins for lentigo maligna of the head and neck are usually suboptimal&#44; therefore a staged resection technique is recommended to enable thorough evaluation of the margins&#46;<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">19</span></a> On confirmation of the presence of an invasive lentigo maligna&#44; it is staged according to Breslow&#39;s depth&#46;<a class="elsevierStyleCrossRef" href="#bib0420"><span class="elsevierStyleSup">40</span></a> Lymph gammagraphy with technetium sulphur colloid is used to stage lentigo maligna melanoma&#46; This substance replaces the blue stains which are used routinely&#44; as they are unnecessary in this site&#44; and there is a remote risk of permanent dyschromia of the skin&#44; necrosis and anaphylaxis&#46;<a class="elsevierStyleCrossRef" href="#bib0425"><span class="elsevierStyleSup">41</span></a> If micrometastasis is confirmed&#44; a completion lymphadenectomy should be performed plus surface parotidectomy if the micrometastases are in the periparotid lymph nodes&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">9</span></a></p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Melanoma and pregnancy</span><p id="par0165" class="elsevierStylePara elsevierViewall">Melanoma in pregnancy has a prevalence of up to 31&#37;&#44; of all the cancers which present in this condition&#44;<a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">42</span></a> and is a neoplasm with high morbimorbidity&#44; and with a not insignificant risk of metastasis to the placenta and the foetus&#46; It is known that pregnancy does not significantly affect the aggressivity of the melanoma in terms of metastasis and survival&#59; however&#44; it is appropriate to be aware that they can occur in pregnancy&#44; and correct and fast management is required in this situation&#46;<a class="elsevierStyleCrossRefs" href="#bib0430"><span class="elsevierStyleSup">42&#44;43</span></a> Biopsy in pregnant patients with a suspected melanoma should be excisional as in all cases&#44; and local anaesthetic is recommended with lidocaine without epinephrine&#46; When the diagnosis has been confirmed&#44; staging can be undertaken safely with a chest X-ray and lactic dehydrogenase or MRI&#44; or abdominal ultrasound if the melanoma has a high Breslow&#39;s depth or palpable adenopathies&#46; The excision margins are the same as those for a woman who is not pregnant&#46;<a class="elsevierStyleCrossRef" href="#bib0440"><span class="elsevierStyleSup">44</span></a> Sentinel lymph node biopsy is safe with technetium sulphur colloid&#46;</p></span></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Conclusions</span><p id="par0170" class="elsevierStylePara elsevierViewall">Lesions suspicious of melanoma should be biopsied excisionally where possible in order to enable the pathologist to report the histological characteristics of the tumour as completely as possible&#44; which should include the presence or otherwise of ulceration&#44; the number of mitosis&#44; Breslow&#39;s depth and other adverse histological factors such as Clark level&#44; the presence of lymphovascular invasion&#44; satellitosis and regression of the melanoma&#46; Of these adverse histological factors&#44; the most associated with micrometastasis is ulceration&#44; followed by the presence of one or more mitoses&#46; Patients with stage I and II melanoma do not require routine testing&#46; In patients with regional lymph node involvement or in stage III of the disease&#44; the recommendation is histological confirmation by fine needle aspiration or open biopsy&#44; and it is left to the criteria of the physicians whether to perform imaging studies to find distant metastases&#46; Imaging studies such as CT and&#47;or PET&#44; plus brain MRI&#44; are indicated in patients with stage <span class="elsevierStyleSmallCaps">IV</span>melanoma&#44; and LDH level&#44; which has prognostic significance for stage <span class="elsevierStyleSmallCaps">IV</span> melanomas&#46; Treatment for localised&#44; and regionally metastatic melanoma is essentially surgical&#46; The term local excision implies the use of peripheral margins of 1&#8211;2<span class="elsevierStyleHsp" style=""></span>cm from any residual pigmentation or scar&#44; according to the Breslow&#39;s depth and the anatomical location of the melanoma&#46; Sentinel lymph node biopsy is a minimally invasive procedure which provides information on the patient&#39;s prognosis&#44; and which also identifies the patients for whom completion lymphadenectomy is most useful&#44; therefore it has replaced scheduled lymphadenectomy&#44; which is currently not recommended routinely&#46; The patients who benefit most from sentinel lymph node biopsy are those with melanomas of 1&#8211;4<span class="elsevierStyleHsp" style=""></span>mm with no clinical or radiological evidence of regional lymph node involvement&#44; although the indications have extended to further clinical scenarios&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">Finally&#44; melanoma should be considered as one of the most aggressive skin cancers due to its high rates of regional&#44; and distant metastasis&#46; This cancer requires early diagnosis so as to offer appropriate treatment&#44; and reduce the morbimortality associated with it&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conflict of interests</span><p id="par0180" class="elsevierStylePara elsevierViewall">The authors have no conflict of interest to declare&#46;</p></span></span>"
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          "identificador" => "xres611326"
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          "titulo" => "Palabras clave"
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        4 => array:2 [
          "identificador" => "sec0005"
          "titulo" => "Background"
        ]
        5 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Epidemiology"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Diagnostic approach"
            ]
            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Preoperative staging"
            ]
            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Surgical management"
            ]
          ]
        ]
        6 => array:2 [
          "identificador" => "sec0030"
          "titulo" => "Approach to the patient with clinically negative metastasis-sentinel lymph node biopsy"
        ]
        7 => array:3 [
          "identificador" => "sec0035"
          "titulo" => "Approach to the patient with clinically positive lymph node metastasis"
          "secciones" => array:2 [
            0 => array:2 [
              "identificador" => "sec0040"
              "titulo" => "Surgical treatment of lymph node metastasis"
            ]
            1 => array:2 [
              "identificador" => "sec0045"
              "titulo" => "Treatment of local recurrence"
            ]
          ]
        ]
        8 => array:3 [
          "identificador" => "sec0050"
          "titulo" => "Special clinical situations"
          "secciones" => array:4 [
            0 => array:2 [
              "identificador" => "sec0055"
              "titulo" => "Subungual melanoma"
            ]
            1 => array:2 [
              "identificador" => "sec0060"
              "titulo" => "Plantar acral melanoma"
            ]
            2 => array:2 [
              "identificador" => "sec0065"
              "titulo" => "Lentigo maligna"
            ]
            3 => array:2 [
              "identificador" => "sec0070"
              "titulo" => "Melanoma and pregnancy"
            ]
          ]
        ]
        9 => array:2 [
          "identificador" => "sec0075"
          "titulo" => "Conclusions"
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        10 => array:2 [
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          "titulo" => "Conflict of interests"
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        11 => array:1 [
          "titulo" => "References"
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    "fechaRecibido" => "2014-10-14"
    "fechaAceptado" => "2014-12-10"
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            0 => "Cutaneous melanoma"
            1 => "Treatment"
            2 => "Surgical"
            3 => "Sentinel lymph node biopsy"
            4 => "Radical lymphadenectomy"
          ]
        ]
      ]
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          "clase" => "keyword"
          "titulo" => "Palabras clave"
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            0 => "Melanoma cut&#225;neo"
            1 => "Tratamiento"
            2 => "Quir&#250;rgico"
            3 => "Biopsia ganglio centinela"
            4 => "Linfadenectom&#237;a radical"
          ]
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      ]
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    "resumen" => array:2 [
      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Melanoma is a common cutaneous tumour&#46; It is of great importance due to its increasing incidence and aggressive behaviour&#44; with metastasis to lymph nodes and internal organs&#46; When suspecting melanoma&#44; excisional biopsy should be performed to obtain complete histological information in order to determine the adverse factors such as ulceration&#44; mitosis rate&#44; and Breslow depth&#44; which influence preoperative staging and provide data for sentinel lymph biopsy decision making&#46; The indicated management for melanoma is wide local excision&#44; observing recommended and well-established excision margins&#44; depending on Breslow depth and anatomical location of the tumour&#46; Therapeutic lymphadenectomy is recommended for patients with clinically or radiologically positive lymph nodes&#46;</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">This article reviews surgical treatment of melanoma&#44; adverse histological factors&#44; sentinel lymph node biopsy&#44; and radical lymphadenectomy&#46;</p><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Details are presented on special situations in which management of melanoma is different due to the anatomical location &#40;plantar&#44; subungual&#44; lentigo maligna&#41;&#44; or pregnancy&#46;</p></span>"
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">El melanoma es una neoplasia cut&#225;nea com&#250;n que ha alcanzado gran importancia en las &#250;ltimas d&#233;cadas debido al aumento en su incidencia y a su comportamiento agresivo&#44; con met&#225;stasis ganglionares y a distancia frecuente&#46; La biopsia&#44; en caso de sospecharse melanoma&#44; debe ser escisional&#44; con el objetivo de obtener informaci&#243;n histol&#243;gica completa y analizar factores de mal pron&#243;stico&#44; como ulceraci&#243;n&#44; n&#250;mero de mitosis y el Breslow&#44; que influyen en la estadificaci&#243;n preoperatoria del paciente y en la decisi&#243;n de realizar biopsia de ganglio centinela o no&#46; La escisi&#243;n local amplia es el manejo indicado para el melanoma con m&#225;rgenes perif&#233;ricos de piel normal ya establecidos de acuerdo al Breslow y a la localizaci&#243;n del tumor&#46; La linfadenectom&#237;a terap&#233;utica es el tratamiento recomendado de los pacientes con melanoma que tienen ganglios linf&#225;ticos cl&#237;nica o radiol&#243;gicamente positivos&#46;</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">En este art&#237;culo se realiza una revisi&#243;n del tratamiento quir&#250;rgico del melanoma&#44; la toma adecuada de biopsia de lesiones sospechosas&#44; los factores histol&#243;gicos adversos&#44; las indicaciones de biopsia del ganglio centinela y de linfadenectom&#237;a radical&#46; Adem&#225;s se revisan situaciones especiales en las cuales el manejo del melanoma difiere por su localizaci&#243;n &#40;acral plantar&#44; subungueal&#44; lentigo maligno&#41; o diagn&#243;stico durante el embarazo&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Zuluaga-Sep&#250;lveda MA&#44; Arellano-Mendoza I&#44; Ocampo-Candiani J&#46; Actualizaci&#243;n en el tratamiento quir&#250;rgico del melanoma cut&#225;neo primario y metast&#225;sico&#46; Cir Cir&#46; 2016&#59;84&#58;77&#8211;84&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Subungual melanoma which started as longitudinal melanonychia&#46; Hutchinson&#39;s sign is present&#46;</p>"
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Breslow&#39;s depth of the melanoma &#40;mm&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Excision margin&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">In situ</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">5<span class="elsevierStyleHsp" style=""></span>mm&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>1&#46;00&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">1<span class="elsevierStyleHsp" style=""></span>cm &#40;in any anatomical area&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="2" align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>1&#46;01&#8211;2&#46;00</td><td class="td" title="table-entry  " align="left" valign="top">1<span class="elsevierStyleHsp" style=""></span>cm &#40;head&#47;neck&#44; distal limb&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">2<span class="elsevierStyleHsp" style=""></span>cm &#40;trunk and proximal limb&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="2" align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>2&#46;00</td><td class="td" title="table-entry  " align="left" valign="top">1<span class="elsevierStyleHsp" style=""></span>cm &#40;head&#47;neck&#44; distal limb&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">2<span class="elsevierStyleHsp" style=""></span>cm &#40;trunk and proximal limb&#41;&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Excision margins according to Breslow&#39;s depth&#46;</p>"
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      "titulo" => "References"
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          "identificador" => "bibs0005"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Epidemiology of melanoma"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => "D&#46;S&#46; Rigel"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.sder.2010.10.005"
                      "Revista" => array:6 [
                        "tituloSerie" => "Semin Cutan Med Surg"
                        "fecha" => "2010"
                        "volumen" => "29"
                        "paginaInicial" => "204"
                        "paginaFinal" => "209"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/21277533"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0230"
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              "referencia" => array:1 [
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                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24399786"
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            2 => array:3 [
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              "referencia" => array:1 [
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                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Trends in dermatology&#58; melanoma incidence"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
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                  "host" => array:1 [
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                      "doi" => "10.1001/archdermatol.2009.379"
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            3 => array:3 [
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                    0 => array:2 [
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                          "etal" => false
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ISSN: 24440507
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