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Review
Squamous cell carcinoma in solid organ transplant recipients: Review of the literature
Carcinoma escamoso cutáneo en pacientes trasplantados de órgano sólido: revisión de la literatura
Inés Oteiza Rius, Ana Morelló Vicente
Corresponding author
amorellovic@unav.es

Corresponding author.
, Leyre Aguado Gil
Departamento de Dermatología, Clínica Universidad de Navarra, Pamplona, Spain
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Summary of the main recommendations on prevention&#44; treatment and follow-up of solid organ transplant patients diagnosed with cutaneous squamous cell carcinoma&#46;</p> <p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">SCC&#58; squamous cell carcinoma&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The incidence of cutaneous squamous cell carcinoma &#40;SCC&#41; is progressively increasing&#46; Although high photoexposure is the main associated risk factor for this type of tumour in the general population&#44; solid organ transplant recipients &#40;SOTRs&#41; have been found to have a higher susceptibility and&#44; therefore&#44; a higher incidence of SCC&#46; In addition&#44; their characteristics differ from SCC developed in the general population&#44; as they are more aggressive tumours&#44; with a 5&#8211;10 times higher probability of metastasis and a higher prevalence of associated death&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Given the scarcity of studies on this type of tumour in the context of immunosuppression due to transplantation&#44; this article aims to review the evidence collected to date on the main differences in the development of SCC in SOTRs compared to immunocompetent patients and specific recommendations regarding treatment&#44; management and follow-up in this group of patients &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Epidemiology</span><p id="par0010" class="elsevierStylePara elsevierViewall">SOTRs are at high risk of developing SCC due to decreased immune monitoring as a result of the immunosuppressive drugs required to prevent transplant rejection&#46; This risk is estimated to be approximately 65 times higher compared to the general population&#44;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> and varies according to the degree of immunosuppression&#44; the duration and type of treatment and the organ transplanted&#44; with heart transplants being the highest risk&#44; followed by kidney and then liver transplants&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> Some studies report an incidence of up to 75&#37; of at least one SCC in the first 20 years after transplantation&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> In addition&#44; these tumours have a higher risk of lymphatic metastasis &#40;up to 8&#37; compared to 2&#46;1&#37; in the general population&#41;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> and higher recurrence rates&#46; It is estimated that after a first diagnosis of SCC&#44; the risk of developing another tumour within 3 years is up to 80&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> Therefore&#44; prevention&#44; follow-up and the choice of appropriate treatment in SOTRs is crucial in this type of tumour&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Prevention</span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Retinoids</span><p id="par0015" class="elsevierStylePara elsevierViewall">Systemic retinoids &#40;acitretin&#44; isotretinoin and etretinate&#41; have been used in the systemic chemoprevention of SCC in SOTRs&#46; These drugs have been shown to be safe and effective for SOTRs with an active history of developing multiple SCC &#40;more than 5 per year&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;5&#44;6</span></a> Despite evidence of their effectiveness in reducing the development of these tumours&#44; these drugs need to be maintained for long periods to achieve efficacy&#44; and discontinuation can lead to a significant rebound in these tumours&#46; Prospective studies have recently been published evaluating the role of long-term acitretin &#40;10 to 35&#8239;mg&#47;day depending on tolerance&#41; in the prevention of SCC in SOTRs&#46; Both studies show a significant long-term reduction&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;8</span></a> However&#44; further studies are needed to determine their long-term efficacy as chemopreventive agents in SOTRs&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Nicotinamide</span><p id="par0020" class="elsevierStylePara elsevierViewall">Nicotinamide is an amide form of vitamin B3 that prevents ATP depletion and enhances DNA repair&#46; This drug reduces ultraviolet radiation-induced immunosuppression and has been shown to reduce the incidence of actinic keratosis and non-melanoma skin cancers &#40;NMSC&#41; at a dose of 500&#8239;mg&#47;12&#8239;h in immunocompetent patients in a phase III clinical trial&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> In addition&#44; it has a good tolerability profile with minimal side effects&#44; although there are no long-term safety data in SOTR&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> However&#44; a recent clinical trial found no statistically significant difference in the reduction of the number of keratinocytic cancers in SOTRs with and without nicotinamide treatment over 12 months&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Therefore&#44; further studies are needed to validate its usefulness in the prevention of SCC in SOTRs&#46; In addition&#44; its potential long-term benefits&#44; its safety in patients with co-morbidities such as chronic kidney disease and its effect after discontinuation need to be further evaluated&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Capecitabine</span><p id="par0025" class="elsevierStylePara elsevierViewall">It is a 5-fluorouracil &#40;5-FU&#41; prodrug used orally at low doses for chemoprevention in SOTRs who develop more than two SCC in 6 months&#46; In a small case series&#44; Endrizzi et al&#46; demonstrated a reduction in SCC associated with low-dose capecitabine &#40;0&#46;5&#8211;1&#46;5&#8239;g&#47;m<span class="elsevierStyleSup">2</span> per day&#41; over a 12-month period in liver and kidney transplant recipients&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Side effects include fatigue&#44; nausea&#44; palmar-plantar erythrodysaesthesia and impaired renal function&#46; The latter should be taken into consideration especially in renal transplant recipients&#44; in whom it will be necessary to start with low doses&#44; closely monitor renal function and assess risk-benefit on an individual basis&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> However&#44; more randomised studies are needed to determine long-term efficacy and safety in SOTRs&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Actinic keratosis and cancerisation field treatment</span><p id="par0030" class="elsevierStylePara elsevierViewall">We refer to areas of chronic sun damage with a high number of actinic keratosis&#44; and therefore a higher risk of developing SCC&#44; as field cancerisation&#46; For this reason&#44; in transplant patients it is essential to treat these areas in order to prevent the development of these tumours&#46; Different topical therapies are available for this purpose&#44; such as photodynamic therapy &#40;PDT&#41;&#44; 5-FU&#44; imiquimod&#44; tirbanibulin and cryotherapy&#46; The efficacy of PDT for the prevention and treatment of SCC in SOTRs has recently been demonstrated in a meta-analysis&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> Moreover&#44; it is an option that is well tolerated by patients and has few side effects&#44; apart from local adverse effects&#46; There are clinical trials that demonstrate the effectiveness of both conventional PDT<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> and daylight PDT<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> in the prevention of SCC in SOTRs&#44; however&#44; there are no studies in this population subgroup that compare both treatment modalities&#46; Regarding the use of 5-FU and imiquimod&#44; both are valid options in transplant patients and should be selected on a patient-by-patient basis&#44; however&#44; a recent study demonstrates the superiority of 5-FU &#40;partial response rates of 58&#37; vs&#46; 29&#37;&#41; over imiquimod in 40 SOTR&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> As for tirbanibulin&#44; there are currently no studies in transplant recipients&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a></p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Beta-HPV vaccination</span><p id="par0035" class="elsevierStylePara elsevierViewall">Human papillomaviruses &#40;HPV&#41; constitute a group of more than 170 subsets with 5 main genera&#44; the most important of which are &#945; and &#946;&#46; The genus &#946; seems to be involved in the development of SCC in immunocompromised patients&#46; However&#44; the varying sensitivity and specificity of the methods used to detect it leads to ambiguous and controversial results between different studies&#46; In addition&#44; current vaccines target high-risk HPV-&#945;&#44; responsible for cervical&#44; anogenital and oropharyngeal cancers&#46; Despite a possible partial cross-protection against the other HPV-&#945; types&#44; their cross-protective efficacy against HPV-&#946; types is not fully established&#46; New vaccines are currently being developed that offer reactivity against HPV-&#946; types&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Topical sirolimus</span><p id="par0040" class="elsevierStylePara elsevierViewall">Based on the indications for substitution of oral immunosuppressive therapy in transplant recipients&#44; which recommend switching from calcineurin inhibitors to sirolimus&#44; the authors Chong et al&#46; studied the role of topical sirolimus 1&#37; for 12 months as a preventive treatment of SCC in transplant recipients&#46; The results showed a three-fold decrease in <span class="elsevierStyleItalic">in situ</span> SCC&#44; with no difference in the number of SCCs&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Despite being a drug with several indications and no evidence of serious adverse effects&#44; further studies are needed to substantiate its role in the prevention of SCC in this group of patients&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Diet</span><p id="par0045" class="elsevierStylePara elsevierViewall">There is a recent study on the preventive effects of omega-3 polyunsaturated fatty acid intake on the development of NMSC in kidney and liver transplant recipients&#46; The results showed a lower risk of SCC in patients with a high intake of long-chain omega-3 polyunsaturated fatty acids&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> In contrast&#44; there is evidence for an increased risk of SCC in patients following a pro-inflammatory diet&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a></p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Photoprotection and health education</span><p id="par0050" class="elsevierStylePara elsevierViewall">Of course&#44; health education and photoprotection measures are key elements in the prevention of SCC in SOTRs&#46; However&#44; a recent systematic review of randomised clinical trials demonstrated the lack of evidence to date regarding photoprotection measures in this subgroup of patients&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> Therefore&#44; further studies are needed to support the true efficacy of photoprotection in SOTRs&#46;</p></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Treatment</span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Surgical treatment</span><p id="par0055" class="elsevierStylePara elsevierViewall">As in immunocompetent patients&#44; the choice of appropriate treatment will depend on both the characteristics of the tumour &#40;anatomical location&#44; size and stage&#41; and the characteristics of the patient &#40;comorbidities and patient preferences&#41;&#46; This implies that in infiltrating tumours the treatment of choice will be mainly surgical&#46; In addition&#44; it is important to determine the stage of the tumour and to rule out the presence of features that determine whether it is a high-risk tumour&#46; The eighth and latest edition of the American Joint Committee on Cancer &#40;AJCC&#41; states that the characteristics of a high-risk tumour include tumours equal to or larger than 4&#8239;cm in size&#44; a thickness &#62;&#8239;6&#8239;mm or invasion beyond the subcutaneous fat&#44; the presence of perineural invasion &#40;nerves greater than 0&#46;1&#8239;mm&#44; deeper than the dermis&#44; or clinical or radiological involvement of nerves&#41; and bone involvement&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> To date&#44; there are no prognostic classifications of these tumours specific to transplant patients&#46; For tumours classified as high risk&#44; Mohs Micrographic Surgery &#40;MMS&#41; is the most recommended modality as it offers higher cure rates&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> It is important to note that although several studies consider immunosuppression&#44; especially in transplant recipients&#44; as a poor prognostic factor in these tumours &#40;higher rates of local recurrence&#44; higher likelihood of metastatic disease and higher prevalence of death&#41;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> and therefore amenable to MMS&#44; there is a paucity of data in the literature on cure rates after MMS in SOTR&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> In cases where MMS is not available&#44; surgical excision with postoperative margin assessment is a valid alternative&#46; In these cases&#44; the recommended optimal surgical margins in SOTRs are described in the literature with variations between 4 to 10&#8239;mm&#44;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> with no clinical data on the proportion of residual or recurrent SCC depending on the recommended margins&#46; However&#44; it is important to bear in mind that immunosuppressed patients&#44; especially SOTRs and those with haematological malignancies&#44; are at increased risk of having a microscopically larger SCC compared to what is clinically and even dermoscopically visible&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> For this reason&#44; MMS should be considered as first-line treatment in SOTRs&#44; whenever circumstances allow&#46; Likewise&#44; after surgical treatment&#44; it is essential to treat the cancerisation field where the tumour is located using topical therapies such as PDT&#44; 5-FU or imiquimod&#44; in order to prevent the development of other tumours in at-risk locations&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a></p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Sentinel node</span><p id="par0060" class="elsevierStylePara elsevierViewall">The indication for sentinel node biopsy &#40;SNB&#41; in patients diagnosed with SCC is not fully established in the guidelines for the management of these tumours&#46; Despite a higher incidence of metastasis in high-risk patients&#44; there are studies that question its cost-effectiveness compared to clinical follow-up&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> It is also important to consider that the cost-effectiveness of SCC in the head and neck is particularly controversial due to the complexity of lymphatic drainage&#44; the proximity of the primary tumour to the lymph nodes and the presence of anatomical structures such as the facial nerve&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> In contrast&#44; several studies consider it necessary to perform this diagnostic test in the presence of several poor prognostic factors according to the Brigham and Women&#39;s &#40;BWH&#41; staging system&#46; These factors include a diameter greater than 2&#8239;cm&#44; poor histological differentiation&#44; perineural invasion of a nerve greater than or equal to 1&#8239;mm&#44; or tumour invasion beyond the subcutaneous cellular tissue&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> Although immunosuppression is not considered&#44; several studies postulate the need to include it among these factors and&#44; according to the authors Pride et al&#46;&#44; SNB should be considered in all immunosuppressed patients with tumours at stage T2b or greater &#40;BWH&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> However&#44; there are insufficient data on the benefit of SNB in SOTRs with high-risk SCC and prospective studies are needed to clarify its true efficacy&#46;</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Radiotherapy</span><p id="par0065" class="elsevierStylePara elsevierViewall">Radiotherapy is a well-accepted alternative for SOTRs with inoperable head and neck SCC or patients who are not candidates for surgical treatment&#46; It is also recommended as adjuvant therapy in high-risk SCC or in cases of incomplete resection&#46; For non-head and neck SCC&#44; there is limited clinical evidence&#44; particularly in SOTR&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> On the other hand&#44; recent studies have shown the effectiveness of a type of radiotherapy called volumetric modulated arc therapy &#40;VMAT&#41; in the treatment of actinic keratosis and SCC<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a> but there are no data yet in transplanted patients&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Systemic therapy</span><p id="par0070" class="elsevierStylePara elsevierViewall">For patients with advanced metastatic or locoregional disease&#44; there is no current agreement on specific management in SOTR&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> To date&#44; the guidelines are the same for the general population&#58; radiation&#44; chemotherapy and targeted therapy&#46; However&#44; despite the increasing use of targeted therapies &#40;anti-PD-1&#47;PDL-1 and EGFR inhibitors predominantly&#41; in patients with advanced disease or unsuitable for surgical treatment&#44; it is essential to note that anti-PD1 drugs have been associated with irreversible allograft rejection&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">36</span></a> Despite this&#44; there are cases described in the literature with good response to anti-PD-1&#44; without associated rejection of the transplanted organ&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">37</span></a> To date&#44; there is more evidence in kidney transplant patients because of the possibility of dialysis in the event of kidney failure&#44; as opposed to heart and liver transplant patients&#44; who have a higher risk of death in the event of organ rejection&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> However&#44; there are studies showing satisfactory results in the latter&#44; the largest series reported to date being a retrospective study of 39 patients in whom the prevalence of rejection was 40&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a> In addition&#44; Tsung et al&#46; propose the use of oral glucocorticoid therapy before and after immunotherapy infusion &#40;40&#8239;mg the day before&#44; 20&#8239;mg&#47;day for 5 days after infusion and 10&#8239;mg&#47;day until 20 days after infusion&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> Unfortunately&#44; there are currently no clinical trial data to determine the management of these patients&#46; On the other hand&#44; the immunosuppression of SOTRs casts doubt on the efficacy of these drugs in terms of tumour shrinkage&#46; However&#44; a recent systematic review shows that a significant tumour response is observed in most SCC patients&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> On the other hand&#44; there are new alternatives which are the subject of isolated descriptions in the literature&#46; Recently&#44; a case of complete response of metastatic SCC to treatment with talimogene laherparepvec &#40;T-VEC&#41; in SOTRs has been published&#46; T-VEC is a genetically modified herpes simplex virus engineered to express granulocyte-macrophage colony-stimulating factor &#40;GM-CSF&#41;&#46; T-VEC is thought to exert its effects through 2 pathways&#58; direct lysis of tumour cells at the injection site and induction of local and systemic immune responses&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> In addition&#44; there are other cases described in the literature in patients transplanted for treatment of other tumours &#40;Merkel carcinoma and melanoma&#41;&#44; in which no damage to the transplanted organ is described&#46; However&#44; it is important to take into account the potential risk of encephalitis due to virus dissemination after the use of this therapy&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> Another novelty described in the treatment of multifocal disease in SOTRs is a case of disease-free response after weekly injections of intralesional IL-2 combined with topical imiquimod&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a></p></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Modification of immunosuppression</span><p id="par0075" class="elsevierStylePara elsevierViewall">The diagnosis of aggressive SCC or the presence of multiple SCC suggests a review of immunosuppressive therapy in SOTR&#46;<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">43&#8211;45</span></a> In recent years&#44; there has been increasing evidence to support switching from mTOR inhibitors to calcineurin inhibitors &#40;tacrolimus&#41;&#46; This substitution appears to be effective after the first post-transplant diagnosis of SCC&#46; However&#44; such a switch in patients without a history of SCC does not seem to extend the time to first diagnosis and therefore does not have any beneficial effect&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">46</span></a> As for mTOR inhibitors&#44; their use is limited by a relatively high discontinuation rate &#40;25&#8211;40&#37;&#41; due to side effects&#46; These include hyperlipidaemia&#44; glucose intolerance&#44; interstitial pneumonias and lymphoedema&#46; In addition&#44; it is important to note an increased risk of death due to infections and cardiovascular diseases&#46; On the other hand&#44; mTOR inhibitors may affect the healing process&#44; which needs to be taken into account for an appropriate post-operative approach and follow-up in these patients&#46; Nevertheless&#44; it is essential to consider that the use of low-dose sirolimus reduces the risk of SCC without increasing the risk of death from other causes and&#44; for this reason&#44; guidelines recommend its use in patients with very high-risk tumours or with rapid onset of multiple SCC&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a> As for the use of everolimus&#44; although there is less evidence&#44; it seems to have similar results&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">48</span></a> On the other hand&#44; older immunosuppressants&#44; such as azathioprine or cyclosporine&#44; have been associated with an increased risk of developing these tumours&#46; It is true that this evidence has been more documented for azathioprine than for cyclosporine&#46; Currently&#44; both drugs are rarely used as maintenance immunosuppressive therapy&#44; but in patients on such therapy with a history of multiple SCC&#44; a switch to mycophenolate should be considered&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">49</span></a> Belatacept &#40;selective CD80 and CD86 blocker&#41; is another immunosuppressant approved for use in kidney transplantation for which the data on the relative risk of developing skin cancer compared with calcineurin inhibitors is inconclusive&#46;<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">50</span></a></p></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Treatment of squamous carcinoma <span class="elsevierStyleItalic">in situ</span></span><p id="par0080" class="elsevierStylePara elsevierViewall">The optimal treatment of SCC <span class="elsevierStyleItalic">in situ</span> in SOTRs is controversial and more long-term prospective studies comparing surgical treatment with other types of therapies indicated in immunocompetent patients&#44; such as cryotherapy&#44; curettage or topical chemotherapy&#44; are needed&#46; Among the latter&#44; imiquimod has demonstrated efficacy and safety in the treatment of SCC <span class="elsevierStyleItalic">in situ</span> in transplant recipients&#44; despite initial suggestions of a potential risk of organ rejection in transplant recipients due to its immune-enhancing effect&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">51</span></a> Even so&#44; there are studies that demonstrate a superiority of 5-FU over imiquimod in this population subgroup in the treatment of actinic keratosis and&#44; therefore&#44; in the prevention of SCC&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> Recently&#44; a study was published postulating the safety and efficacy of cryoimmunotherapy &#40;5 weeks of daily imiquimod and cryosurgery on day 14&#41; in renal transplant patients&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">52</span></a> On the other hand&#44; there are studies showing a higher prevalence of residual SCC after shave biopsy compared to non-immunosuppressed controls&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">53</span></a></p></span></span><span id="sec0095" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Follow-up</span><span id="sec0100" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Time intervals</span><p id="par0085" class="elsevierStylePara elsevierViewall">The main objectives of follow-up in SOTRs are early detection and prevention of actinic keratosis and NMSCs&#44; in order to try to improve their prognosis&#46; There is controversy about the monitoring interval&#46; Given the growing population of transplant recipients&#44; this should be short enough to detect precursors of malignant lesions and long enough to avoid overuse of available resources&#46; According to the American Society of Transplantation &#40;AST&#41;&#44; these patients should undergo skin examinations by a qualified healthcare professional with expertise in skin tumours on an annual basis&#44; or even more frequently in case of a history of skin cancer&#46; In addition&#44; there are expert consensus guidelines&#44; mainly based on retrospective studies&#44; that recommend full-body skin examinations annually in patients with no history of NMSCs&#44; every 6 months if actinic keratosis or NMSC is present&#44; every 3 months if there is a history of multiple NMSCs or high-risk SCC&#44; and every 1&#8211;3 months for metastatic SCC&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> Although more evidence is needed to determine the frequency of follow-up in SOTRs&#44; there are some prospective studies that suggest the need to consider other risk factors such as age&#44; phototype or previous history of sunburn&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">54</span></a> In addition&#44; it is important to consider that these risk factors may differ between regions&#44; depending on different ethnic distributions and geographic location&#59; therefore&#44; it is essential to validate the follow-up interval in each country&#46; On the other hand&#44; the efficacy of periodic skin self-examinations has not been demonstrated in the early detection of SCC in OTR&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> To date&#44; there is no specific indication to differentiate follow-up intervals according to the type of transplant or degree of immunosuppression&#46;</p></span><span id="sec0105" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Previous rejections</span><p id="par0090" class="elsevierStylePara elsevierViewall">Another factor to consider in the follow-up of these patients is the existence of previous episodes of rejection&#46; This is a factor associated with a higher incidence of SCC&#44; as well as a shorter time to the development of the first SCC&#44; in kidney transplant recipients&#46; This implies the need for closer monitoring in kidney transplant recipients after a rejection episode&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">55</span></a> To date&#44; the importance of previous rejection has not been confirmed in other studies with other types of solid organ transplantation&#46;</p></span><span id="sec0110" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">CD57 expression on TCD8 cells</span><p id="par0095" class="elsevierStylePara elsevierViewall">CD57 expression on TCD8 cells has also been considered as a possible risk factor in some studies&#46; This marker is measured on cells obtained from peripheral blood and identifies cells that have undergone repeated rounds of antigenic stimulation&#44; have shorter telomeres and impaired proliferation and cytokine production&#46; CD57 expression may therefore represent a marker of T-cell exhaustion&#46; There is a study comparing the incidence of SCC in SOTRs showing &#8805;&#8239;50&#37; CD8 with CD57 expression &#40;flow cytometry&#41; with those showing &#60;&#8239;50&#37; expression&#46; A follow-up of 522 &#40;434&#8211;607&#41; days was carried out and statistically significant results were obtained regarding an increased likelihood of developing SCC &#40;hazard ratio&#58; 2&#46;9&#59; 95&#37; CI&#58; 1&#46;0&#8211;8&#46;0&#41; and earlier recurrence in patients with higher CD57 expression&#44; adjusted for age and previous history of SCC&#46; Furthermore&#44; stability of this marker over time and an association with older age and CMV seropositivity were observed&#46; These results imply that this test could help identify high-risk SOTRs who require intensive dermatological screening and a reduction of their immunosuppression&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">56</span></a></p></span><span id="sec0115" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">Polymorphisms</span><p id="par0100" class="elsevierStylePara elsevierViewall">In relation to genetic predisposition&#44; a non-coding nucleotide polymorphism &#40;rs34567942&#41; has been identified as a predisposing factor for SCC in transplant recipients&#46; This polymorphism has a deleterious effect on the FBXO25 gene&#44; whose mutation is associated with head and neck SCC&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">57</span></a> While it is true that genetic variants alone can have virtually imperceptible effects&#44; the combination of different variables can have more significant consequences&#46; Thus&#44; Stapleton et al&#46; suggest the usefulness of polygenetic risk estimation in renal transplant patients&#46; These findings could suggest a role for genomics in risk stratification of these patients&#44; allowing the development of personalised treatment regimens in the future&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">58</span></a></p></span><span id="sec0120" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Painful lesions</span><p id="par0105" class="elsevierStylePara elsevierViewall">The sensation of pain in skin tumours should raise suspicion of invasive SCC in transplant recipients&#46; There is evidence of increased overall mortality in SOTRs with painful skin lesions regardless of histological diagnosis&#46; Despite the absence of a relationship between pain and perineural invasion in these tumours&#44; there is an association between the number of painful lesions and overall mortality&#46; For this reason&#44; painful skin lesions should be used as a clinical indicator of increased risk&#46;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">59</span></a></p></span></span><span id="sec0125" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0145">Pre-transplant screening</span><p id="par0110" class="elsevierStylePara elsevierViewall">To date&#44; there are no data validating the role of skin cancer screening and&#47;or actinic keratosis screening prior to transplantation&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a></p></span><span id="sec0130" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0150">Paediatric patients</span><p id="par0115" class="elsevierStylePara elsevierViewall">In paediatric patients&#44; the development of NMSCs occurs several years after transplantation &#40;6 to 20 years after transplantation&#41;&#46; For this reason&#44; in paediatric transplant recipients these tumours occur at an earlier age than in the general population&#46; To date&#44; there are no guidelines on skin cancer screening for paediatric patients or publications on chemoprevention in this patient group&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">60</span></a></p></span><span id="sec0135" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0155">Conclusions</span><p id="par0120" class="elsevierStylePara elsevierViewall">SCC in SOTRs is more aggressive and more likely to metastasise&#44; requiring a specific approach to prevention&#44; treatment and follow-up for this group of patients&#46; In terms of treatment&#44; surgery is the treatment of choice in most cases&#44; preferably by paraffin-embedded margin control surgery&#44; although the availability and suitability of this technique may vary&#46; On the other hand&#44; modification of immunosuppression is an essential part of treatment in this group of patients&#44; and switching from calcineurin inhibitors to mTOR inhibitors is an effective strategy&#44; although with important side-effect considerations&#46; With regard to follow-up&#44; there is some controversy about specific monitoring intervals&#44; as various risk factors that have not yet been established&#44; such as previous rejections&#44; CD57 expression on TCD8 cells or genetic polymorphisms&#44; should be taken into account&#46; However&#44; these check-ups should be carried out regularly&#44; at least every 12 months&#44; and may be necessary every 3 months depending on the degree of immunosuppression and the presence of a history of NMSC&#46; In summary&#44; the management of SCC in SOTRs is an important challenge that requires a multidisciplinary approach&#44; taking into account the unique characteristics of these patients and the need for ongoing research to improve the prevention&#44; diagnosis and treatment of this disease in this population&#46;</p></span><span id="sec0140" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0160">Informed consent</span><p id="par0125" class="elsevierStylePara elsevierViewall">No informed consent was required due to the absence of patients in the study&#46;</p></span><span id="sec0145" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0165">Funding</span><p id="par0130" class="elsevierStylePara elsevierViewall">We have not received funding for this article&#46;</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Epidemiology"
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          "titulo" => "Prevention"
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              "titulo" => "Capecitabine"
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              "titulo" => "Actinic keratosis and cancerisation field treatment"
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              "titulo" => "Beta-HPV vaccination"
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              "titulo" => "Topical sirolimus"
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    "fechaRecibido" => "2024-01-16"
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            0 => "Squamous cell carcinoma"
            1 => "Solid organ transplant recipients"
            2 => "Immunosuppression"
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            0 => "Carcinoma escamoso cut&#225;neo"
            1 => "Trasplantados de &#243;rgano s&#243;lido"
            2 => "Inmunosupresi&#243;n"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Solid organ transplant recipients &#40;SOTRs&#41; exhibit an elevated incidence and aggressiveness of squamous cell carcinomas &#40;SCCs&#41; due to their immunosuppression&#46; These tumors are associated with a heightened risk of metastasis and increased mortality&#46; Therefore&#44; an appropriate management of these patients is essential to improve their prognosis&#46; Given the scarcity of studies on non-melanoma skin cancers &#40;NMSCs&#41; in SOTRs&#44; this article aims to summarize and analyze the evidence gathered to date regarding therapeutic approaches&#44; personalized monitoring&#44; and prevention strategies for SCCs in these patients&#46; Additionally&#44; recent advancements in understanding SCCs within this patient group are also documented&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Los pacientes trasplantados de &#243;rgano s&#243;lido &#40;PTOS&#41; presentan una mayor incidencia y agresividad de carcinomas escamosos &#40;CECs&#41; debido a su inmunosupresi&#243;n&#46; Estos tumores se asocian a un mayor riesgo de met&#225;stasis y a un aumento de la mortalidad&#46; Por lo tanto&#44; un adecuado manejo de estos pacientes resulta esencial para favorecer su pron&#243;stico&#46; Dada la escasez de estudios sobre los c&#225;nceres cut&#225;neos no melanoma &#40;CCNM&#41; en PTOS&#44; este art&#237;culo pretende resumir y analizar las evidencias recogidas hasta la fecha sobre el enfoque terap&#233;utico&#44; seguimiento personalizado y estrategias de prevenci&#243;n en estos pacientes en relaci&#243;n al CEC&#46; Asimismo&#44; se recogen las novedades sobre el CEC descritas en este grupo de pacientes durante los &#250;ltimos a&#241;os&#46;</p></span>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Summary of the main recommendations on prevention&#44; treatment and follow-up of solid organ transplant patients diagnosed with cutaneous squamous cell carcinoma&#46;</p> <p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">SCC&#58; squamous cell carcinoma&#46;</p>"
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ISSN: 23870206
Original language: English
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