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Original article
Incidence of non-melanoma skin cancer in patients treated with psoralen and ultraviolet A therapy
Incidencia de cáncer cutáneo distinto del melanoma en pacientes tratados con PUVA oral
José María Ortiz Salvadora,
Corresponding author
josema.ortiz.salvador@gmail.com

Corresponding author.
, Amparo Pérez-Ferriolsa,b, Víctor Alegre de Miquela,b, Martina Saneleuterio Temporalc, Juan José Vilata Corella,b
a Servicio de Dermatología, Hospital General Universitario de Valencia, Valencia, Spain
b Facultad de Medicina, Universitat de València, Valencia, Spain
c Hospital Universitario y Politécnico La Fe, Valencia, Spain
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This is mostly because of the variability in the typical risk factors of this neoplasm &#40;environmental UV irradiance&#44; cutaneous phototype&#44; sun exposure habits&#44; etc&#46;&#41;&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The different incidence rate of NMSC in the different published studies makes it difficult to extrapolate results to populations with characteristics that vary from those studied&#46; However&#44; by using standardised rates adjusted to a common population&#44; we are able to compare the results obtained in different populations&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">2</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">The main objective of this study is to determine the gross and age-adjusted incidence of NMSC in patients treated with PUVA therapy&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Materials and method</span><p id="par0030" class="elsevierStylePara elsevierViewall">A longitudinal retrospective follow-up study was conducted&#44; which included a cohort of patients treated with systemic PUVA between 1982 and 1996 in the Photobiology and Phototherapy Unit of the Valencia University General Hospital&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The inclusion criteria were&#58;<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8211;</span><p id="par0040" class="elsevierStylePara elsevierViewall">Patients with dermatological diseases treated by oral PUVA in the Photobiology and Phototherapy Unit of the Valencia University General Hospital between 1982 and 1996&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8211;</span><p id="par0045" class="elsevierStylePara elsevierViewall">Availability of at least four years&#8217; follow-up data&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8211;</span><p id="par0050" class="elsevierStylePara elsevierViewall">Not having received phototherapy regimes other than oral PUVA at any time before treatment or during the study period&#46;</p></li></ul></p><p id="par0055" class="elsevierStylePara elsevierViewall">Between 1982 and 1996&#44; 1&#44;012 patients were treated with oral PUVA&#44; of which 234 &#40;23&#46;1&#37;&#41; met the relevant criteria and were thus included in the study&#46; The different exclusions criteria are shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#46; Patients with incomplete or absent data in the registry were excluded from the study&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">Patients with psoriasis or mycosis fungoides were treated with oral PUVA therapy according to clinical indications and following the protocols established by Carrascosa et al&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">3</span></a> The eligibility of patients to receive treatment was considered by the health professional in charge of the Photobiology and Phototherapy Unit during the study period&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Patients&#8217; clinical history was accessed and follow-up was carried out until the patient&#39;s last registered visit to the Photobiology Unit&#44; with the last access being made in May 2017&#46; The information regarding cutaneous cancer was collected by professionals not involved in this study and sourced from the Valencia General Hospital &#40;reference centre for the entire population served&#41; dermatopathology database and the Valencian Community ABUCASIS II unified clinical database&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Cases of cutaneous neoplasms were considered to be patients with basal cell carcinoma &#40;BCC&#41; or cutaneous epidermoid carcinoma &#40;CEC&#41; included in the clinical database and for whom histologic confirmation was confirmed by biopsy or extirpation&#46; Recommendations from the <span class="elsevierStyleItalic">International Agency for Research on Cancer</span> were followed&#44; defining cases as the first tumour of each histological type in each patient&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The variables registered in the study were sex&#44; age phototherapy was initiated&#44; dermatological pathology&#44; reason for treatment and duration of follow-up&#46; The outcome variables were&#44; prevalence of cutaneous neoplasms according to histological type at the end of the observation period&#44; incidence of NMSC and its subtypes&#44; location of neoplasms&#44; age at the time of appearance of the first neoplasm and time until the development of the first neoplasm&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">The prevalence of skin cancer was determined at the end of the follow-up period and the standardised incidence density of cutaneous neoplasms during the follow-up period&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The incidence standardised by age and sex was made by direct adjustment to the world population&#44; as studied by Segi et al&#46; for 18 age groups and both sexes&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">4</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">The study was approved by the Valencia General Hospital&#44; Clinical Investigation Ethical Committee&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Results</span><p id="par0095" class="elsevierStylePara elsevierViewall">Of the 234 patients included in the study&#44; 131 &#40;56&#37;&#41; were male and 103 &#40;44&#37;&#41; female&#46; Patients&#8217; age &#40;mean &#91;standard deviation&#93;&#41; at start of treatment was 41&#46;8 &#40;17&#46;4&#41;&#46; Their age at the end of the follow-up period was 62&#46;8 &#40;15&#46;5&#41;&#46; Mean follow-up time was 21 years &#40;range between 4&#46;1 and 34&#46;5 years&#41; with an accumulated follow-up period of 4&#46;912<span class="elsevierStyleHsp" style=""></span>patients&#47;year&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Fifty neoplasms were diagnosed in 22 patients&#46; The prevalence of NMSC in patients treated with phototherapy was 10&#46;3&#37;&#44; accounting for a single tumour by histological type and patient&#44; and 22&#46;2&#37; considering all tumours&#46; The 50 neoplasms corresponded to 23 BCC and 27 CEC&#46; Considering a tumour by histological type and patient&#44; the prevalence of BCC in the sample was 7&#46;3&#37; and the prevalence of CEC was 4&#46;7&#37;&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">Regarding the location of the lesions&#44; the most frequent location was lower limbs &#40;52&#46;8&#37;&#41; followed by the head and neck &#40;34&#37;&#41;&#44; the trunk &#40;11&#46;3&#37;&#41; and the lower limb &#40;1&#46;9&#37;&#41;&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Considering only one case per tumour and histological type&#44; the incidence density of NMSC in our study &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41; was 554&#46;4 cases&#47;100&#44;000 patients treated per year &#40;95&#37; CI&#58; 345&#46;3&#8211;763&#46;5&#41;&#46; The incidence density of BCC was 352&#46;3 cases&#47;100&#44;000 patients treated per year &#40;95&#37; CI&#58; 184&#46;8&#8211;519&#46;8 cases&#47;100&#44;000 patients treated per year&#41;&#46; The incidence density of CEC was 229 cases&#47;100&#44;000 patients treated per year &#40;95&#37; CI&#58; 93&#46;7&#8211;364&#46;3 cases&#47;100&#44;000 patients treated per year&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0115" class="elsevierStylePara elsevierViewall">After making a direct standardisation adjusted to the age of the world population&#44; the adjusted incidence density of NSCLC was 183&#46;9 cases&#47;100&#44;000 patients treated per year&#46; The adjusted incidence density of BCC was 111&#46;2 cases&#47;100&#44;000 patients treated per year&#46; The adjusted incidence density of CEC was 77&#46;7 cases&#47;100&#44;000 patients treated per year&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">The age of appearance of the first lesion in patients who presented neoplasias and the latency time until its development is shown in <a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#46; The median time until appearance of the first lesion was 18 years for NMSC in general&#44; 18&#46;3 years for BCC and 12&#46;6 years for CEC&#46; The median age of appearance of the first neoplasm was 67&#46;5 years for NMSC in general&#44; 67&#46;5 years for BCC and 68&#46;4 years for CEC&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0125" class="elsevierStylePara elsevierViewall">To our knowledge&#44; our study&#44; which included 234 patients and a mean follow-up period of 21 years&#44; constitutes the largest known registry in the Mediterranean area&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">It is also the first study to define the standardised incidence density of NMSC&#44; which is a much more reliable measure of the risk of carcinogenesis and facilitates comparability with other studies into skin cancer incidence&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">From Stern&#39;s 1979 study until today&#44; numerous countries have published studies to discern the potential risk of cutaneous tumours in patients who have received PUVA therapy to treat various cutaneous diseases&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">2</span></a> In the United States&#44; most prospective studies have found a direct association between PUVA therapy and a risk of carcinogenesis&#46;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">5&#8211;9</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">The risk was greater for the development of squamous cell carcinomas&#44; with increased incidence rates even at low doses of radiation and a directly proportional relationship between the number of sessions and the risk of developing NMSC&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">7</span></a> In Europe&#44; studies have been conducted in Sweden&#44; the United Kingdom&#44; France&#44; Finland&#44; Austria&#44; the Netherlands and Ireland&#44; among others&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">10&#8211;16</span></a> In four prospective studies and in most of the retrospective studies&#44; an increased risk of NMSC has not been found in patients undergoing treatment with PUVA&#46; Only the most recent cohort studies have found a somewhat higher incidence of NMSC in patients treated with PUVA compared to national tumour registries in each study&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">10&#44;11&#44;13</span></a> The risk of NMSC in our study is lower than that found in prospective US studies&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">The incidence of NMSC found in our study is higher than that found by Vilar-Coromina et al&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">17</span></a> in the general population of Girona&#44; with a standardised incidence density three times higher than that described in the population of this study &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; The risk was even greater for the development of CPB&#44; with an adjusted incidence in patients treated with PUVA seven times higher than in the unexposed population&#46; These findings are consistent with other studies that defend the carcinogenic risk of PUVA therapy&#44; especially in relation to CEC&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">9</span></a></p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0150" class="elsevierStylePara elsevierViewall">Our study has found a prevalence of NMSC similar to that of other cohorts of patients treated with PUVA in American studies&#44;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">5&#44;9</span></a> and higher than that found in the majority of patients in European studies&#46;<a class="elsevierStyleCrossRefs" href="#bib0200"><span class="elsevierStyleSup">18&#8211;20</span></a> Regarding the effect on the Mediterranean population&#44; the global prevalence of neoplasias adjusted to the follow-up time concurs with that found by Maiorino et al&#46; in the Italian population&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">21</span></a> However&#44; most of the carcinogenic risk studies associated with PUVA are aged &#8211; they have a different inclusion criteria and did not study the incidence rate associated with the follow-up time&#44; only the prevalence at the end of the period&#44; making them very sensitive to differences in the follow-up time&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">2</span></a></p><p id="par0155" class="elsevierStylePara elsevierViewall">The high average age of onset and time to the development of the neoplasm reveal the need for studies with a longer follow-up period&#46; In this sense&#44; these findings are consistent with previous studies&#44; in which the prolongation of observation time is accompanied by an increase in the prevalence of neoplasms&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">9</span></a> In the same way&#44; it validates the observation that the carcinogenic risk associated with PUVA is maintained years after the end of treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">22</span></a> The mean age of onset of NMSC in our study was lower than that found in the general population by Vilar-Coromina et al&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">17</span></a> This indicates that PUVA therapy not only increases the risk of developing NMSC&#44; but also advances the age of onset of cutaneous neoplasms&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">As shown in <a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#44; the incidence of cutaneous neoplasms was not homogeneous during the study period&#44; and was closely related to the age of the population&#46; For this reason&#44; caution should be used when defining the incidence of skin cancer as a single value&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">Although our study has found an incidence of MCNM higher than that described in the Mediterranean population&#44; this association does not necessarily imply a causal relationship with PUVA therapy has been demonstrated&#44; which may be due to differences not detected in the different study populations or to causal factors not related to UV radiation&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall">The main limitations of our study are loss of follow-up during the recruitment of patients and during the study period&#44; as well as the retrospective nature of the follow-up&#46; Similarly&#44; there was no cohort of patients not exposed to UV phototherapy with which the incidence of cutaneous neoplasms could have been directly compared and measures of strength of association established&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">In conclusion&#44; the incidence of NMSC in patients treated with PUVA therapy was higher than that found in the general population&#46; The risk seems to be greater for the development of CEC than for the BCC&#46; Studies with a prolonged period of follow-up are essential to accurately determine the long-term carcinogenic effect of PUVA therapy&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Funding</span><p id="par0180" class="elsevierStylePara elsevierViewall">None of the authors report having received financial assistance for this manuscript&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflict of interest</span><p id="par0185" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interest in this manuscript&#46;</p></span></span>"
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    "fechaRecibido" => "2017-07-14"
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            0 => "PUVA therapy"
            1 => "Phototherapy"
            2 => "Skin cancer"
            3 => "Basal cell carcinoma"
            4 => "Squamous cell carcinoma"
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            0 => "PUVAterapia"
            1 => "Fototerapia"
            2 => "C&#225;ncer de piel"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Studies reporting incidences of non-melanoma skin cancer &#40;NMSC&#41; are heterogeneous&#44; depend on the geographic area of the studied population and are often short-term&#46; The aim of this study is to determine the incidence of NMSC in patients treated with oral PUVA therapy in the Mediterranean area&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Material and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A retrospective&#44; observational study was carried out with a sample of 234 patients treated with systemic PUVA between 1982 and 1996&#44; carrying out a historical follow-up until May 2017&#46; The incidence density rate of CCNM &#40;crude and adjusted&#41; was calculated by direct standardisation&#46; The incidence of CCNM was compared with that reported in the general population in a similar geographical area&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">50 neoplasms were diagnosed in 22 patients&#46; The prevalence of CCNM in patients treated with phototherapy was 10&#46;3&#37;&#46; The mean follow-up time was 21 years&#46; The crude-adjusted incidence density rate of CCNM was 554&#46;4&#8211;183&#46;9 cases&#47;100&#44;000 treated patients per year&#46; The crude-adjusted incidence density rate of basal cell carcinoma was 352&#46;3&#8211;111&#46;2 cases&#47;100&#46;000 patients and of squamous cell carcinoma was 229&#8211;77&#46;7 cases&#47;100&#44;000 patients&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">PUVA therapy is associated with an increased risk of CCNM in the Mediterranean population&#46;</p></span>"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Los trabajos que determinan la incidencia de c&#225;ncer cut&#225;neo no melanoma &#40;CCNM&#41; en la poblaci&#243;n tratada con psoralenos orales<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>UVA son heterog&#233;neos&#44; dependen de la localizaci&#243;n geogr&#225;fica de la poblaci&#243;n estudiada y tienen per&#237;odos de seguimiento cortos&#46; El objetivo del trabajo es determinar la seguridad a largo plazo de la PUVAterapia y en concreto determinar la incidencia de CCNM en los pacientes tratados con PUVAterapia oral en el &#225;rea mediterr&#225;nea&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Material y m&#233;todo</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se ha realizado un estudio longitudinal de seguimiento retrospectivo&#44; recogiendo 234 pacientes tratados con PUVA sist&#233;mico entre 1982 y 1996 con un seguimiento hasta mayo de 2017&#46; Se ha calculado la densidad de incidencia de CCNM bruta y ajustada por edad mediante estandarizaci&#243;n directa&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">En 22 pacientes se diagnosticaron 50 neoplasias&#46; La prevalencia de CCNM en pacientes tratados con fototerapia fue del 10&#44;3&#37;&#46; El tiempo medio de seguimiento fue de 21 a&#241;os&#46; la densidad de incidencia bruta-ajustada de CCNM fue de 554&#44;4-183&#44;9 casos&#47;100&#46;000 pacientes tratados-a&#241;o&#46; La densidad de incidencia bruta-ajustada de carcinoma basocelular fue de 352&#44;3-111&#44;2 casos&#47;100&#46;000 pacientes y la de carcinoma epidermoide de 229-77&#44;7 casos&#47;100&#46;000 pacientes&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La incidencia de c&#225;ncer cut&#225;neo en los pacientes tratados con PUVAterapia es superior a la descrita en la poblaci&#243;n mediterr&#225;nea&#46;</p></span>"
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          "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Crude incidence rate and adjusted age density of NMSC in the population treated with PUVA therapy&#46;</p>"
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      "titulo" => "References"
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