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Treatment With UV-B for Psoriasis and Nonmelanoma Skin Cancer
A Systematic Review of the Literature
Pieternel C. M. Pasker-de Jong, PhD;
Gina Wielink, PhD;
Pieter G. M. van der Valk, MD;
Gert-Jan van der Wilt, PhD
Arch Dermatol. 1999;135:834-840.
ABSTRACT
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Background In a cost-effectiveness study currently being conducted of short-contact anthralin treatment for psoriasis in an outpatient setting as compared with the standard treatment with UV-B radiation, the excess incidence (IDD) of skin cancer due to exposure to UV-B could not be ascertained because the study did not last long enough. A meta-analysis of published data was deemed appropriate.
Objective To quantify the IDD of nonmelanoma skin cancer as a function of the total dose of UV-B and specific for time since first exposure, age at first treatment, and other treatments received.
Methods Systematic review of the literature with meta-analysis of all available evidence published in English, French, German, or Dutch between 1980 and 1996.
Results Four articles contained information that enabled us to calculate an overall IDD of nonmelanoma skin cancer. The estimates varied between -0.6 and 2 extra skin cancers per 100 patients with psoriasis treated with UV-B phototherapy per year. However, these estimates were calculated under several assumptions, and do not allow for the construction of a dose-response model specific for time since exposure or age at first treatment. A model based on animal data suggests that a total of 5 excess skin cancers can be expected per 100 treated in the 60 years after the start of treatment with 500 minimum effective doses of UV-B per year from age 25 years.
Conclusions The available evidence is insufficient for quantifying the IDD of nonmelanoma skin cancer in patients with psoriasis treated with UV-B radiation. However, it seems unlikely that the excess risk exceeds 2% per year. As yet, it is not possible to assess at what level of exposure this IDD occurs, or how long after exposure excess risk is present.
INTRODUCTION
PSORIASIS IS a multifactorial skin disease with a hereditary component that affects 1% to 3% of the world population.1 It can manifest at any age with variable severity, and when it interferes with patients' social and relational activities, treatment is indicated.1 Frequently used treatments include phototherapy with UV-B, photochemotherapy with UV-A and psoralens, and clinical treatment with anthralin.2 Phototherapy/chemotherapy combination is assumed to cause nonmelanoma skin cancer (NMSC), and clinical treatment with anthralin is expensive. Ambulatory short-contact treatment with anthralin was suggested to be a safe and cost-effective alternative.3
We are currently conducting a randomized controlled trial that includes a cost-effectiveness analysis in which ambulatory short-contact treatment with anthralin is being compared with clinical anthralin treatment and with UV-B phototherapy. As NMSC is one of the potential adverse effects of phototherapy, the costs of diagnosis and treatment of additional cancers due to phototherapy need to be taken into account in the cost-effectiveness analysis. However, the size and duration of the study do not allow for assessment of these related costs within the project. We therefore carried out a systematic review of the literature and a meta-analysis of available evidence to determine a dose-response relation considering the excess incidence (IDD) of NMSC as a function of the total dose of UV-B specific for time since first exposure, age at first treatment, and other treatments for psoriasis used. The estimated IDD was combined with cost data to compute additional costs of diagnosis and treatment for NMSC.
MATERIALS AND METHODS
SEARCH STRATEGIES
Searches in MEDLINE, BIOSIS, and ONLINE CONTENTS were carried out in June 1998 for articles published between 1980 and 1996. Both free-word searches and searches with thesaurus and index words were used Each search combined 2 or 3 of the following terms: UV light (UV-B), phototherapy, psoriasis, and skin-cancer/carcinoma. References of the selected articles were scanned for potentially relevant titles.
SELECTION OF ARTICLES
Selection of relevant articles was based on a checklist derived from our research question: only articles that presented information based on histopathological reports of NMSC incidence as a function of UV-B monotherapy in patients with psoriasis were eligible for inclusion in the meta-analysis. For practical reasons, only studies published in English, French, German, or Dutch were included. Articles were selected in 2 steps. First, the relevance of all retrieved references was evaluated by the first author (P.C.M.P.) on the basis of title, abstract, and keywords. Articles were retrieved only if they satisfied the inclusion criteria. To examine the reproducibility of the selection of relevant articles, a second reviewer (G.W.) evaluated a sample of all references. Second, both reviewers read the selected articles, and relevance was assessed once again. Furthermore, the articles were evaluated for various sources of bias. Articles were included in the meta-analysis only if they presented original data, confounders were adequately adjusted for, and selection and information bias were deemed unlikely by the epidemiologist (P.C.M.P.). Case series and case reports were excluded altogether because the occurrence of selection and information bias is generally high in these types of studies. Data on the incidence of skin cancer, if available, were extracted from the articles independently by the 2 reviewers. Moreover, all selected articles were thoroughly read by the medical expert (P.G.M.V.) to assess the medical qualities of the presented research.
RESULTS
ARTICLES
The 9 search strategies performed (see Appendix) resulted in a total of 810 references. Overlaps between the results of the various search strategies included 168 of these (130 references were found twice; 24, three times; 9, four times; and 5, five times). Fifty-nine references were not in Dutch, English, French, or German. From the remaining 751 references, 104 were selected for reading by the first author (P.C.M.P.). Although most of these were not expected to provide useful data, lack of relevant articles made us decide not to be too stringent. Agreement on selection between the 2 reviewers was 99%. Only 1 article selected by the first reviewer would not have been selected by the second. Thirteen articles were not retrieved. A list of the selected articles can be obtained from the first author.
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Appendix. Search Strategies and Sources
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None of the 91 articles satisfied the postulated criteria. Only 10 articles contained information about the incidence of NMSC in patients with psoriasis following UV-B phototherapy. Of the remaining 81, 31 contained data on other treatments, notably psoralen–UV-A (PUVA) photochemotherapy and not UV-B phototherapy; 21 were reviews with no original data; 16 described animal experiments; 6 were letters and editorials; 5 described a theoretical dose-response model for skin cancer resulting from exposure to UV-B radiation based on animal data; 1 described the UV treatments and doses received in a hospital; and 1 case report was accidentally requested.
INFORMATION
Of the articles with information about the effects of UV-B on the incidence of NMSC, 1 was thought to be so confounded that the results should not be used. Five more contained insufficient information to calculate the IDD of NMSC. This left 4 articles for analysis. One described research on the effects of UV-B monotherapy; 2 dealt with skin cancer in relation to treatment with UV-B and coal tar combined; and the fourth did not show what treatment combinations had occurred. Treatment dose and time since first exposure were insufficiently specified in all 4 articles. We used these 4 articles to estimate the IDD of skin cancer due to the treatment with UV-B. Table 1 presents some of the relevant parameters of the design of these studies.
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Summary and Results of the Informative Studies Included in the Meta-analysis of Excess Incidence of NMSC* After UV-B Phototherapy
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STUDIES
Only Larkö and Swanbeck4 describe the change in incidence of skin cancer among patients with psoriasis treated with UV-B alone. Patients who received more than 100 treatments with UV-B monotherapy were compared with population controls. Confounding due to contraindication cannot be ruled out because patients who may have stopped treatment because of anticipated high risk of skin cancer were not included in the study. Of the study population of 120 patients with psoriasis who received over 100 UV-B treatments, 85 were examined. Controls matched for age, sex, and address were randomly selected from the birth and address register, and 338 of 510 invited were also examined. The prevalence of malignant skin lesions was found to be lower in the patients with psoriasis than in the population control group. No information was given about the time between treatment with UV-B phototherapy and the physical examination.
Pittelkow et al5 studied 280 patients with psoriasis up to 25 years after their first treatment with UV-B and coal tar. They selected these patients from hospital records and collected information on diagnoses of skin cancer from 260 of the patients. The patients did not have more NMSCs than would have been expected on the basis of the age-specific incidence rates in the area. Pittelkow et al also carried out a case-control analysis with the 280 patients. The 19 patients in whom NMSC had developed were compared with the 261 patients who remained free from skin cancer. Cases did not differ from controls in the median number of days of exposure to UV-B (13 vs 14 in 5 years). There was no information on the dose.
Stern et al6 described an analysis of the men in the PUVA follow-up study. Men with psoriasis with exposure to UV-B and coal tar had 4.6 times more invasive squamous cell carcinomas of the genitals than men with psoriasis with no exposure to UV-B or coal tar but with similar exposure to PUVA. In this study, exposure to UV-B and coal tar was defined as more than 300 treatments with UV-B and/or more than 90 months of coal tar use as estimated by the patient. Time since first exposure was not available.
Stern et al7 also presented the results of a case-control study among the patients with psoriasis who participated in the PUVA follow-up study. Among the 1373 participants, 75 cases of skin cancer became known. The case history of 59 of them was complete. All patients with psoriasis who did not develop skin cancer, who were at least 30 years old, and whose case history was complete were included in the control group (n=924). Furthermore, a matched control group was constructed with a maximum of 4 controls per case (n=126). The patients with psoriasis were classified according to their exposure to both coal tar and UV-B, as both treatment modalities were highly correlated. High exposure to coal tar or UV-B was defined as exposure to over 300 treatments with UV-B and/or over 90 months of treatment with coal tar compared with low exposure, or fewer than 300 treatments with UV-B and fewer than 90 months of treatment with coal tar. Analysis of the data of the nonmatched patients revealed a crude odds ratio of 2.4 (95% confidence limits, 1.4, 4.2); the matched analysis (that controlled for age, sex, skin type, address, and exposure to ionizing radiation and PUVA) showed an odds ratio of 4.7 (95% confidence limits, 2.2, 10.0). Information about time since exposure or about the presence of other confounders or effect modifiers in the data was not available.
UNINFORMATIVE STUDIES
Bhate et al8 studied the incidence of skin cancer among 2247 patients with psoriasis by evaluating the case notes from the general practitioners of these patients for information on skin cancer diagnoses and exposure information. They found a cumulative incidence of 34 carcinomas in 2247 patients at a mean age of 41 years. They refrained from analyzing the available data for evidence of carcinogenicity of treatments for psoriasis, but they presented information that can be used to calculate crude cumulative incidences of NMSC for those exposed to UV-B and to coal tar. The cumulative incidence of NMSC was 1.2% in patients with psoriasis treated with UV-B and 1.8% in patients with psoriasis not treated with UV-B. For coal tar, the figures were 1.7% and 0.8%, respectively. However, no information on the amount of exposure, duration of follow-up, confounders, or joint exposure was available.
In 1994, Stern and Laird9 published further results of the PUVA follow-up study for which the patients had been observed an average of 13 years. In this report they focused on the association between PUVA and squamous cell carcinoma, finding no relation between exposure to UV-B and/or coal tar and squamous cell carcinoma after correction for all potential confounders. Data were not presented. As the squamous cell carcinomas developed long after both the UV-B and PUVA treatments, it seems possible that the effects of UV-B treatment were drowned in the effects of PUVA treatment, which seem much stronger.
Halprin et al10 studied 150 patients with psoriasis who had been admitted to the hospital at least once between 1976 and 1980 but had never been treated with PUVA. Patients with diabetes admitted to the hospital during the same period were selected as the control group. All skin malignancies were counted in both groups in 1981. Ninety-five of the 150 patients with psoriasis had been treated with UV-B and coal tar, and in 13 (14%) of them skin cancer was diagnosed. Furthermore, in 7 (13%) of the nonexposed patients with psoriasis, skin cancer was diagnosed. Skin cancer had been diagnosed in only 7 (5%) of the patients with diabetes. Information about the duration of follow-up was not available, and excess risks therefore cannot be calculated.
Maier et al11 described 496 patients with psoriasis of 1149 treated with more than 5 exposures to PUVA before 1987. Among 111 patients treated with UV-B, 2 cases of skin cancer occurred. Among the 384 not exposed to UV-B, 11 cases occurred. Duration of follow-up is not available, and other treatments were prevalent. The authors performed a multivariate analysis in which all other treatments were included, as well as skin type, age, and sex. The relative risk for NMSC after UV-B treatment was 0.36. For treatment with coal tar, the relative risk was 3.83.
Bajdik et al12 conducted a case-control study in the general population in which they studied exposure to nonsolar UV radiation and the risk of NMSC. The odds ratio for exposure to UV lamp treatments was 0.9 after correction for age, skin and hair color, and occupational exposure to the sun. The study was not conducted specifically among patients with psoriasis. Furthermore, no information about time since exposure was available.
BIASED STUDY
Lindelof and Sigurgeirsson13 conducted a case-control study of risk factors for NMSC in patients with psoriasis treated with PUVA. They matched the controls to the cases on sex, age, diagnosis, PUVA dose, number of treatments, site of treatment, and skin type. However, they did not analyze the data on prior therapies in a matched way. Therefore, the results cannot be used to estimate the effect of UV-B phototherapy on the risk of NMSC.
ESTIMATING THE EXCESS INCIDENCE
For carcinomas and keratoses combined, the cumulative incidence difference between patients with psoriasis and the general population reported by Larkö and Swanbeck4 was -4.2% with a confidence interval of -10.1% to 1.8%. For carcinomas only, the cumulative incidence difference can be calculated from the information in their article. Among the patients with psoriasis, 4 (4.7%) of 85 were found to have or have had a carcinoma. Among the 338 controls matched on age and sex, there were 14 carcinomas (4.1%). The difference in cumulative incidence is 0.6% in 16.2 years on average. The IDD is 0.04% per year under the assumption of constancy of this excess over time. This IDD is calculated under the assumption of no difference in sensitivity to UV-B between those with more than 100 treatments and those with fewer treatments.
Pittelkow et al5 found 19 carcinomas in 260 patients with psoriasis treated with UV-B and coal tar in a total of 5222 person-years. The incidence density amounted to 0.36% per year. The incidence density calculated from population data in the area where the study was conducted varied between 0.30% and 0.94% per year. The IDD was therefore estimated between -0.58% and 0.06% per year.
Stern6 reported an expected cumulative incidence of 0.285 genital squamous cell carcinomas in 892 patients with psoriasis treated with PUVA who were observed for 12.3 years on average based on population figures. The incidence density among those not exposed to UV-B was 0.0026% per year, assuming constant rates. With an odds ratio of 4.6, the incidence density among those exposed to treatment with UV-B and/or coal tar would be 0.0119% per year. The IDD would then amount to 0.0093% per year for genital carcinomas.
Among the 59 cases of skin cancer reported by Stern et al,7 there were 34 new cases in 958 patients in 2.7 years of follow-up on average. The incidence density of skin carcinomas was 1.3% per year in exposed and nonexposed subjects combined. There were 19 cases of skin carcinoma among the 751 patients who underwent low-exposure treatment with UV-B and/or coal tar (an incidence rate of 0.9% per year, assuming equal follow-up on average). There were 15 cases among the 207 patients treated with high exposure to UV-B and/or coal tar (incidence rate, 2.7% per year). The IDD was approximately 1.8% per year. There is no information on time since exposure to treatment with UV-B and/or coal tar. Furthermore, these figures were crude rates, with control neither for mutual confounding of UV-B and coal tar nor for confounding by other treatments.
SUMMARY AND DISCUSSION OF THE DATA
The IDD data calculated from the studies and given in the Table 1 varied between -0.58% and 1.8% per year. These IDDs cannot be interpreted as excess risks due to a certain total number of UV-B treatments because information about the total dose received is unavailable in all of the studies. At what time after exposure the maximum effects of UV-B phototherapy can be expected is unclear as well. We assumed constancy of the incidence to calculate IDDs. We also assumed absence of sources of bias or confounding. However, in 3 of the studies patients were treated with the Goeckerman regimen. The concomitant exposure to coal coal tar has been neglected in the calculations, although reports have been published from animal data that suggest a relation between coal by-products and NMSC.14 A recent review concluded that insufficient human data are available to evaluate the carcinogenic effects of coal tar.15 In the present analysis, the effect of treatment seemed larger in the studies where UV-B phototherapy and coal tar were jointly evaluated than in the study where UV-B was evaluated separately. Furthermore, treatment with PUVA was not always controlled for. It is likely that other treatments were used more frequently in those also treated with higher doses of UV-B because these are the patients with more severe psoriasis. Lack of sufficient information made controlling for this source of bias impossible.
In the literature, it has been suggested that patients with psoriasis have a lower risk of malignant skin diseases.16 While this has been refuted,17-22 3 of the studies summarized above also suggested a protective effect of psoriasis against skin cancers.4-5,8 As multiple treatments, all potentially carcinogenic, are often used in patients with psoriasis, this may explain that the other studies did not show a protective effect of psoriasis.6-7,10
To calculate the long-term excess costs of NMSC due to UV-B phototherapy, the purpose of the present study was to quantify the dose-response relation of UV-B monotherapy to NMSC incidence. Because none of the studies gave appropriate information about the risk of NMSC as a function of the time since first exposure and/or the dose of the exposure, it is impossible to construct a valid dose-response relation from their results.
MODEL
A dose-response relation has been constructed by Schothorst et al23 and improved by Slaper et al24 on the basis of animal experiments. The model is capable of calculating the excess cumulative incidence of NMSC specific for age and average annual dose of UV-B treatment. These can be translated into IDD. The model needs estimates of some biological susceptibility factors. The model is CI= [AE D‘ a + AR Dth (a-as)], where CI is the cumulative incidence up to age a; , the genetic susceptibility factor to NMSC of the population; AE, the skin surface with the highest exposure to sunlight; AR, the skin surface with the lowest exposure to sunlight; D‘, the average annual dose of UV-B from sunlight and treatment combined, equal to D+(a-as/a)Dth; D, the annual dose of UV-B from sunlight; Dth, the annual dose of UV-B from treatment; a, age at the calculation of skin cancer risk (time since first exposure to sunlight); as, age at the start of treatment (a-as=time since first exposure to treatment); , biological amplification factor; and , the age effect on the incidence of skin cancer.
This model was validated in the lower-dose range for humans with incidence figures from countries at various latitudes. From these figures, the biological amplification factor was also estimated. According to the estimates of Slaper et al,24 it would be expected that after 30 years of therapy with 250 minimum effective doses (MEDs) per year starting at age 25 years, the cumulative incidence of basal cell carcinoma would be increased by a factor of 2 and that of squamous cell carcinoma by a factor of 4.
From this model, we calculated the IDD of NMSC specific for total yearly dose, age at start of treatment, and time since first treatment. We assumed that IDDa=(CIda-CI da-1)-(CIa-CIa-1), where CIdis the CI calculated from the model above and CI is the CI assuming no therapeutic exposure to UV-B.
The biological amplification factor was taken as 2.2; the genetic susceptibility factor, 1.6x10-17; and the age effect, 5.2; all figures as estimated by Slaper et al.24 A higher genetic susceptibility would increase the model results with the ratio of both susceptibilities. We calculated the IDD for 3 ages at first exposure (25, 45, and 65 years), although the model assumes that the effect of UV-B does not depend on age at first exposure. The skin surface with highest exposure to the sun was estimated at 15%. An average of 225 MEDs per year was taken as the background exposure.23 A higher background exposure would increase the estimated IDD because the model assumes that the total dose received is exponentially associated with the incidence of NMSC. We estimated the IDD for doses between 0 and 1000 MEDs. The mean dose of UV-B in patients from the Department of Dermatology of St Radboud University Hospital in Nijmegen, the Netherlands, was 10.57 J/cm2 per treatment with an average of 3.4 treatments per person between 1992 and 1995, for an average annual dose of about 8.98 J/cm2 or 449 MEDs per year (with 1 MED being 20 mJ/cm2).23 The maximum dose given in this period was 1875 MEDs per year. Age at the start and total duration of treatment were unknown for the patients.
MODEL RESULTS
Figure 1 shows the annual IDD and Figure 2, the cumulative IDD over time as a function of the yearly therapeutic dose in MEDs and duration of treatment (time since first exposure) for 3 ages at first exposure. The maximal cumulative number of excess cases of NMSC estimated from the model was 18.7 per 100 treated, after 1000 MEDs per year for 60 years starting at age 25 years, or a maximum excess risk of 1.4% per year. This excessive treatment will not occur in practice, however. At a mean annual dose of 500 MEDs and a duration of treatment of 20 years starting from age 45 years, the estimated total number of excess cases at age 65 was 0.2 per 100 treated. These figures are lower than those calculated from the published data.
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Figure 1. Graphic representation of the annual excess incidence of nonmelanoma skin cancer as a function of yearly dose of UV-B therapy in minimum effective doses (MEDs) and years since first exposure. A, Age at the start of treatment, 25 years; B, age at the start of treatment, 45 years; C, age at the start of treatment, 65 years.
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Figure 2. Graphic representation of the cumulative excess incidence of nonmelanoma skin cancer as a function of yearly dose of UV-B therapy in minimum effective doses (MEDs) and years since first exposure. A, Age at the start of treatment, 25 years; B, age at the start of treatment, 45 years; C, age at the start of treatment, 65 years.
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COMMENT
As there was inadequate information in the literature, it was impossible to quantify the IDD of NMSC as a function of total dose of UV-B and time since first exposure specific for age at first treatment and other treatments received from empirical data. From the studies published to date, the IDD of NMSC was estimated to be between 0% and 2% per year. The excess risk of NMSC due to the treatment with PUVA has been shown to be considerably higher.9, 24
The initial purpose of the present study was to construct a valid dose-response relation based on empirical data in humans. This was not possible. A theoretical model based on animal data was available, and its results were compatible with the empirical evidence. Model calculations showed that with a mean annual dose of 1000 MEDs, the maximum IDD was 1.4% per year, occurring after 60 years of exposure starting at age 25 years. This would result in 19 additional cases of skin cancer per 100 patients treated after 60 years of treatment. The IDD from the model is lower for all exposures of shorter duration than this.
The estimates from the model are somewhat lower than those from the literature. This may be a consequence of a higher baseline risk in the populations described in the literature. A higher genetic susceptibility factor would result in a multiplication of the model results with the ratio of the new and the old susceptibility factors. The lower estimates may also be a consequence of a higher background UV-B exposure, a larger part of the body exposed to sunlight, or an underestimated biological amplification factor or age effect. It is uncertain whether the model performs adequately at higher dose ranges. Furthermore, the model does not allow for a possible effect of age at first exposure. The calculated effects are a result of time since first exposure to treatment and total dose received only. Although the data from the literature were inadequate to estimate a dose-response relation, and the model results are sensitive to the estimates of several unknown quantities included in the model, we estimate the maximum number of excess skin cancers due to treatment with UV-B to be 2 per 100 treated per year. In general, in a comparison between UV-B and anthralin treatments for patients with psoriasis, the long-term effects of UV-B treatment may be of some importance. Long-term effects of treatment with anthralin have not been reported.
To construct a valid dose-response relation on the basis of epidemiological data, further research is necessary. However, it will be very hard to perform such research because multiple treatments are used in patients with psoriasis. Furthermore, patients are likely to be treated selectively based on their assumed susceptibility to NMSC, which creates confounding by contraindication and may lead to an earlier discontinuation of treatment among those patients assumed to be at higher risk for NMSC, eg, because of their skin color or occupational exposure to sunlight. A randomized controlled trial in which patients are assigned to either UV-B or a noncarcinogenic alternative will answer the question. The ongoing study that prompted the present review of the literature may be a valuable starting point for future research.
AUTHOR INFORMATION
Accepted for publication February 16, 1999.
This work was supported by a grant from the Reinier Post Foundation, Nijmegen, the Netherlands.
Corresponding author: Pieternel C.M. Pasker-de Jong, Department of Epidemiology 152, University of Nijmegen, PO Box 9101, 6500 HB Nijmegen, the Netherlands.
From the Departments of Epidemiology (Dr Pasker-de Jong) and Medical Technology Assessment (Drs Wielink and van der Wilt), and the Department of Dermatology, University Hospital St Radboud (Dr van der Valk), University of Nijmegen, Nijmegen, the Netherlands.
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