J Clin Oncol 25: by American Society of Clinical Oncology INTRODUCTION

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1 VOLUME 25 NUMBER 19 JULY JOURNAL OF CLINICAL ONCOLOGY O R I G I N A L R E P O R T From the Department of Oncology- Pathology, Karolinska Institutet and Karolinska University Hospital Solna, Stockholm; Department of Dermatology and Pathology, University Hospital, Umeå; Department of Dermatology, Linköping University Hospital, Linköping; Consultant Group Histopathology, Capio Diagnostics; and the Department of Dermatology, Sahlgrenska University Hospital, Gothenburg, Sweden. Submitted February 21, 2007; accepted April 9, Supported by grants from the Swedish Cancer Society and the Research Funds of Radiumhemmet, Stockholm, Sweden. Presented in part at the 3rd EUROSKIN Conference, Stockholm, Sweden, September 16-19, Authors disclosures of potential conflicts of interest and author contributions are found at the end of this article. Address reprint requests to Johan Hansson, MD, PhD, Department of Oncology-Pathology, Karolinska Institutet, Karolinska University Hospital Solna, S Stockholm, Sweden; johan.hansson@ki.se. Monitoring of Kindreds With Hereditary Predisposition for Cutaneous Melanoma and Dysplastic Nevus Syndrome: Results of a Swedish Preventive Program Johan Hansson, Mia Bergenmar, Per-Åke Hofer, Göran Lundell, Eva Månsson-Brahme, Ulrik Ringborg, Ingrid Synnerstad, Annika Ternesten Bratel, Ann-Marie Wennberg, and Inger Rosdahl A B S T R A C T Purpose To evaluate a program initiated in 1987 by the Swedish Melanoma Study Group aiming to provide preventive surveillance to kindreds with hereditary cutaneous melanoma and dysplastic nevus syndrome. Patients and Methods Overall, 2,080 individuals belonging to 280 melanoma families were followed for 14 years between 1987 and 2001 at 12 participating centers. Data were registered in a central database. Results Among 1,912 skin lesions excised during follow-up, 41 melanomas were removed in 32 individuals. Of these, 15 (37%) were in situ melanomas and 26 (63%) invasive melanomas. The median tumor thickness of invasive melanomas was 0.5 mm. Ulceration was absent in 24 of 26 invasive melanomas (92%) and 12 (46%) lacked vertical growth phase. Compared with melanomas in the general Swedish population, the melanomas identified in these kindreds during follow-up had better prognostic characteristics. All melanomas except one were diagnosed in families with two or more first-degree relatives with melanoma. Diagnosis of melanoma occurred in three of eight kindreds with germline CDKN2A mutations, supporting that families with such mutations are at increased risk for melanoma development. Of the 32 individuals who developed melanoma during follow-up, 21 (66%) had had at least one previously diagnosed melanoma. Conclusion This study shows that a coordinated program aimed at detecting and offering skin surveillance in kindreds with hereditary cutaneous melanoma results in a low incidence of melanomas during the follow-up period and that the tumors that do arise have favorable prognostic characteristics. J Clin Oncol 25: by American Society of Clinical Oncology 2007 by American Society of Clinical Oncology X/07/ /$20.00 DOI: /JCO INTRODUCTION Up to 10% of all cases of cutaneous malignant melanoma (CMM) occur in kindreds with hereditary CMM predisposition. 1 In the first description of CMM, Norris 2 reported a family in which two members had CMM and several had large moles. In 1978, Clark 3 reported six melanoma-prone families in which members had large nevi designated as potential precursors of CMM. This syndrome has several eponyms: dysplastic nevus syndrome (DNS), 4 familial atypical multiple mole melanoma syndrome, 5 and atypical mole syndrome 6 ; and the nevi are called dysplastic nevi (DN) or atypical moles. In an early report of 14 DNS families, 95% of CMM patients and 50% of relatives had DN. 7 During follow-up, new CMMs were diagnosed only in individuals with DN. In an another early report D-2 kindreds were defined, with at least two family members with CMM and two or more with DN. 8 In a study of 23 D-2 kindreds, individuals with DN had a 89-fold increased CMM risk and those with a previous CMM a 229-fold increased risk for a second CMM 9 In 1994, germline mutations in the CDKN2A tumor suppressor gene in kindreds with hereditary CMM (HCMM) were demonstrated. 10,11 Worldwide, germline CDKN2A mutations are found in approximately 20% of HCMM kindreds. 1 However, such mutations are present in less than 10% of Swedish HCMM kindreds. 12,13 In Sweden, one CDKN2A founder mutation (insertion of an extra arginine in codon 113, p.r112_l113insr) is predominant. 14 Thus, the genetic background remains unknown in most kindreds. 1 GenoMEL (The Melanoma Genetics Consortium), has published 2819

2 Hansson et al consensus statements on counseling and genetic testing of individuals perceived to be genetically predisposed to CMM. 15,16 In 1987 The Swedish Melanoma Study Group initiated a national preventive program for kindreds with HCMM-DNS. The aim is to reduce the risk of CMM by regular skin examinations, excision of suspicious lesions, and information about skin self-examination and behavior to avoid harmful exposure to ultraviolet irradiation. We now present a 14-year follow-up of 280 Swedish HCMM-DNS families to our knowledge, the largest prospectively followed populationbased cohort of such kindreds so far reported. PATIENTS AND METHODS We used the original definition of D-2 kindreds: CMM in at least two blood relatives as well as clinical DN in two or more relatives. 8 The program was carried out in 12 clinics, covering 7.3 million inhabitants, 82% of the Swedish population. 17 Data was collected in a central database. The project was approved by the ethics committee of the Karolinska Institutet, Stockholm, Sweden. HCMM-DNS kindreds were identified through questioning of newly diagnosed CMM patients regarding relatives with CMM. CMM in relatives was verified by pathology reports and/or clinical records. Melanoma in situ (Tis) was included in the diagnosis of CMM. A pedigree was established and blood relatives contacted by the proband and invited to participate in the program. At the initial visit, participants received written and oral information regarding protection from damaging sunlight and skin self-examination. A skin examination was performed. For diagnosis of DN, ABCD criteria 18 were used and nevi not fulfilling these criteria were registered as common nevi (CN). Photographic documentation included whole-body photographs and detailed pictures of all DN. Dermoscopy was performed, and in many centers computerized digital image systems were used for documentation. Individuals who were diagnosed with melanoma and unaffected individuals with DN were followed-up at 6-month intervals. Patients with newly diagnosed CMM were followed-up on more frequently, according to guidelines for CMM follow-up. Nevi with changing appearance, and lesions raising suspicion of melanoma for other reasons, were excised for histopathologic examination. At the initial visit information on previous CMM and other malignant tumors, skin type, hair and eye color, and number and sites of CN and DN were registered. At follow-up visits, new or changing DN and histopathology of excised skin lesions were registered. In the present study, data on members of all HCMM-DNS kindreds entered in the database between 1987 and 2001 were analyzed. Melanomas excised during follow-up were reevaluated by a reference pathologist (A.T.B.). In some kindreds, screening of germline CDKN2A mutations was performed in a separate project. 13 Statistical analyses were performed using the 2 test and t test as appropriate. RESULTS Characteristics of HCMM-DNS Kindreds The present report is based on 280 kindreds with 2,080 individuals registered 1987 to In these kindreds, 614 index CM cases were identified before or at the initial examination. The median age at diagnosis of index melanomas was 45 years (range, 12 to 90 years). The number of CMM cases in kindreds ranged between two and nine, whereas 88% had only two CMM cases (Table 1). In 193 families (69%), at least two first-degree relatives had CMM; in 52 families (19%), CMM was diagnosed in second-degree relatives only; and in 35 kindreds (12%), in third-degree or more distant family members. Table 1. Characterization of 280 Swedish Kindreds With HCMM-DNS Included in the Analysis With Respect to Number of Index Cases per Family No. of CMM Cases Kindreds CMM Cases per Kindred No. % No. % Total Abbreviations: HCMM-DNS, hereditary cutaneous malignant melanoma dysplastic nevus system; CMM, cutaneous malignant melanoma. Characteristics of HCMM-DNS Family Members Among the 2,080 family members, 614 (29%) had a CMM before follow-up (Table 2). Among 1,466 unaffected individuals, 866 (59%) had DN, whereas 600 (41%) lacked DN. There were more women than men among melanoma patients and unaffected individuals without DN, and more men among unaffected individuals with DN ( 2 7.3; P.026). The comparison regarding phenotype between categories of family members was hampered by lacking information in some melanoma patients. Many of these individuals were dead before the program started, and data regarding the melanoma diagnosis were obtained from pathology reports and clinical records. Only 369 of the 597 melanoma patients were examined at a participating center (Table 2). There were significant differences in skin and pigmentation characteristics, between the three categories of family members. Melanoma patients had a significantly more sensitive skin type than did unaffected individuals both with and without DN (P.008). Likewise, there was a significantly increased proportion of individuals with red hair and fewer persons with dark hair among melanoma patients compared with unaffected individuals with or without DN (P.013). No significant differences in eye color were seen. There was a wide variation in both CN and DN between individuals at the initial examination (Table 3). Unaffected individuals without DN had significantly fewer CN than did those with DN and melanoma patients (P.001). Melanoma patients had a small but significantly (P.004) increased number of DN compared with the group of unaffected individuals with DN, whereas there was no significant difference in CN between these two groups. Screening for germline CDKN2A mutations in at least one family member affected with melanoma was performed in 169 kindreds. 16 Of these, eight families (4.7%) had germline CDKN2A mutations. The Swedish p.r112_l113insr mutation was detected in seven kindreds, whereas one family exhibited a proline to leucine missense mutation in codon 48 (p.p48l). Results of the Follow-Up Program Overall, 1,784 family members visited the participating centers for examination, and only melanoma patients and individuals with DN were followed regularly, whereas unaffected individuals without 2820 JOURNAL OF CLINICAL ONCOLOGY

3 Monitoring Familial Melanoma Characteristic All Individuals (N 2,080) Table 2. Characteristics of Members of HCMM-DNS Kindreds Individuals Without DN (n 600) Individuals With DN (n 866) Melanoma Patients (n 614) No. % No. % No. % No. % Sex Male Female 1, Total 2, Skin type I II III 1, IV Total 1, Hair color Red Blond Brown Dark Total 1, Eye color Blue 1, Gray Green Brown Mixed colors Total 1, NOTE. Family members without a melanoma diagnosis have been categorized according to the presence or absence of DN. Abbreviations: HCMM-DNS, hereditary cutaneous malignant melanoma dysplastic nevus system; DN, dysplastic nevi. Information lacking for 20 individuals: 3 individuals without DN and 17 melanoma patients. Information lacking for 302 individuals: 36 individuals without DN, 18 individuals with DN and 248 melanoma patients. Information lacking for 297 individuals: 35 individuals without DN, 16 individuals with DN and 246 melanoma patients. Information lacking for 297 individuals: 35 individuals without DN, 17 individuals with DN and 245 melanoma patients. 2 P clinical DN were not followed. In total, 13,113 visits by members of the HCMM-DNS kindreds were registered, corresponding to an observation time of 17,539 person-years (Table 4). The larger number of visits and longer median follow-up in melanoma patients is probably explained by more frequent and prolonged follow-up after treatment for CMM. New DN were registered during follow-up in a large proportion of melanoma patients (46%) and unaffected individuals (54%; Table 5). Overall, an average of 3.3 new DN were registered. A significant correlation was found between the total number of DN registered in each individual and hair color: individuals with red or blond hair had higher number of DN than did those with brown or dark hair (P.014). No correlation was found between the total number of DN and age, skin type, or eye color. Changes in appearance of DN were frequent in both melanoma patients (37%) and unaffected individuals (40%; Table 5). The risk of developing changes in DN during follow-up was significantly correlated to the number of DN at the initial examination (coefficient of correlation 0.33; P.0001). Table 3. Nevus Phenotype in Members of HCMM-DNS Kindreds at Initial Examination Category No. of CN No. of DN Median Range Median Range All individuals Individuals without DN Individuals with DN Melanoma patients NOTE. Family members without a melanoma diagnosis have been categorized according to the presence or absence of dysplastic nevi. Abbreviations: HCMM-DNS, hereditary cutaneous malignant melanoma dysplastic nevus system; CN, common nevi; DN, dysplastic nevi. Table 4. Number of Visits to Outpatient Clinics, Median Observation Time, and Total Person-Years Observed in Members of HCMM-DNS Kindreds Who Were Included in the Follow-Up Program Individuals With DN Melanoma Patients Factor No. % No. % No. of visits 3,871 9,242 Observation time, years Median Range Total person-years observed 5, , NOTE. Unaffected family members without DN were not followed. Abbreviations: HCMM-DNS, hereditary cutaneous malignant melanoma dysplastic nevus system; DN, dysplastic nevi

4 Hansson et al Category Table 5. Number of Individuals With New and Changing DN Registered During Follow-Up New DN Individuals Individuals No. % Mean Range No. % Changing DN Individuals with DN (n 850) Melanoma patients (n 369) Abbreviation: DN, dysplastic nevi. Mean Range Skin Lesions Excised During Follow-Up During follow-up, 1,912 skin lesions were excised (Table 6). The most common histopathologic diagnoses were CN (53%) and DN (40%). Importantly, 41 CMMs (2.1%) were diagnosed in 32 patients, 18 male (56%) and 14 female (44%). Most patients, 25, had a single CMM, whereas six patients had two CMMs, and one patient four CMMs. The 32 individuals belonged to 25 different kindreds. Interestingly, all melanomas except one were diagnosed in members of families where two or more first-degree relatives had been previously diagnosed with CMM. The remaining melanoma occurred in a family with two second-degree relatives with CMM. Of the 32 individuals with CMM diagnosed during follow-up, 21 (66%) had at least one previous CMM diagnosis. Thus, 18 patients had a single previous CMM, one patient had two previous CMMs, one patient had three previous CMMs, and one patient had four previous CMMs. Interestingly, CMMs were diagnosed during follow-up in three of the eight families exhibiting germline CDKN2A mutations. Specifically, in the family with the p.p48l mutation, six CMMs were diagnosed in three family members (four CMMs in one and one CMM each in two individuals), whereas a single CMM was diagnosed in each of two kindreds with p.r112_l113insr mutations. Although the number of families with germline CDKN2A mutations is small, our results indicate that kindreds with such mutations are at particular risk for melanoma development The median age at diagnosis of CMM during follow-up was 43 years, which is slightly lower than the median age of 45 years for all CMMs registered in the families The median time from the first visit to the participating center to diagnosis of melanoma was 38 months (range, 0 to 126 months) and 10 (24%) of 41 tumors were diagnosed within the first year of follow-up. In 29 cases (71%), the patient did not report any signs or symptoms, and the tumor was identified by the examining physician. In 12 cases (29%), the patient reported signs or symptoms: in four cases the patient had Table 6. Histopathologic Diagnoses of 1,912 Skin Lesions Excised During Follow-Up of Family Members Diagnosis Lesions No. % No. of Patients Lesions per Patient Melanoma Dysplastic nevus Common nevus 1, Other NOTE. In some cases, pigmented lesions were not excised because of suspicion of melanoma, but rather at the patient s request for cosmetic or other reasons. discovered a new lesion, in five cases changing appearance of an existing lesion, and in three cases itching. Histopathologic examinations showed that 15 (37%) of the 41 tumors were noninvasive Tis (Table 7). As expected, a majority (85%) of invasive tumors were superficial spreading melanomas (SSMs). Of the invasive CMMs, most (77%) were Clark level II. Likewise, the majority of tumors were thin, with a median thickness of 0.5 mm, and only three tumors had a thickness above 1.0 mm. Histopathologic signs of ulceration were present in two tumors, and in one of those only punctuate ulceration was seen. Importantly, of the 26 invasive melanomas, 12 (46%) were pure radial growth phase tumors, thus lacking metastatic capacity. When Tis are included, 66% of all primary CMM detected during Table 7. Characteristics of 41 Cutaneous Melanomas Excised During Follow-Up Characteristic No. % Age at diagnosis, years (n 41) Median 43 Range Invasiveness (n 41) Melanoma in situ Invasive melanoma T-classification according to AJCC (n 41) Tis T1a T1b 1 2 T2a 2 5 T2b 1 2 Histogenetic type of invasive melanomas (n 26) Superficial spreading melanoma Nodular melanoma 3 11 Lentigo maligna melanoma 1 4 Level of invasion of invasive melanomas (n 26) II III 5 19 IV 1 4 Tumor thickness of invasive melanomas, mm (n 26) Median 0.5 Range Ulceration of primary melanoma (n 26) Absent Present 2 8 Vertical growth phase in invasive melanomas (n 26) Absent Present Abbreviation: AJCC, American Joint Committee on Cancer. In one of these, only punctuate ulceration was present JOURNAL OF CLINICAL ONCOLOGY

5 Monitoring Familial Melanoma follow-up lacked vertical growth phase and are, therefore, expected to carry no risk of metastasis. DISCUSSION In this report, we describe the results of a Swedish national preventive program aimed to identify HCMM-DNS kindreds and to provide prevention, including skin surveillance to family members. We studied 280 such families, which is, to our knowledge, the largest prospectively followed material of HCMM kindreds so far reported. Our cohort of melanoma kindreds derives from a population-based screening for HCMM-DNS kindreds, whereas other sets of HCMM families usually have been collected by referral of high-risk kindreds to specialized centers. During follow-up of these 280 HCMM-DNS kindreds, 41 primary melanomas were excised. To compare these lesions to melanomas diagnosed in the general Swedish population, we used data from a Swedish national database on 12,533 invasive CMMs diagnosed in Sweden 1990 to The median age of diagnosis of CMM during follow-up of family members was 43 years, which is almost two decades below that of melanomas in the general Swedish population (61 years). This difference may be attributed both to the lower age at CMM development in HCMM kindreds 1 and possibly to earlier diagnoses resulting from the follow-up program. The latter is supported by the lower median age at diagnosis of melanomas in the follow-up program (43 years) compared with all melanomas in members of the participating kindreds (45 years). Moreover, a large proportion, 37%, of melanomas detected during follow-up were Tis, which is considerably higher than the proportion of Tis of 19.7% in the Stockholm- Gotland Regional Melanoma Registry, which contains 7,365 melanomas registered 1976 to 1999 (H. Hellborg, personal communication, October 2005). This suggests that the follow-up program has led to an early diagnosis of CMMs, which has been achieved already at the noninvasive stage in a many tumors. The median thickness of invasive CMMs detected during follow-up was 0.5 mm, considerably below the median CMM thickness of 0.9 mm in the Swedish population. 19 Of the invasive melanomas diagnosed during follow-up, most (77%) were limited to Clark level II, whereas five (19%) reached level III and one (4%) level IV. Again, this is in marked contrast to invasive melanomas in the Swedish population, of which 31% are level II, 36% level III, 29% level IV and 4% level V. Among the 26 invasive melanomas excised during follow-up of family members, 23 (88%) were T1 tumors and three (12%) T2 tumors, compared with 55% T1, 20% T2, 15% T3% and 10% T4 in the Swedish population. 19 Moreover, only two (8%) of the tumors detected during follow-up showed signs of ulceration, which was present in 24% of melanomas in the Swedish population. 23 Importantly, more than half of the invasive melanomas in the present study lacked vertical growth phase and should carry no risk of metastasis. There has also been no report of a disease recurrence that may be attributed to a CMM diagnosed during follow-up. Together, these data indicate that the preventive program has contributed to an early diagnosis of melanomas, preventing the development of metastatic disease. Results similar to ours have been reported from follow-up of 33 HCMM kindreds at the National Cancer Institute. Of 86 new CMMs identified, 72 were early (T1a) lesions, and 63 of the melanomas had only radial growth phase. 20 Compared with the risk estimates of CMM development in HCMM-DNS kindreds in the literature, the number of melanomas in our families is unexpectedly small. The number of histologically dysplastic nevi excised during follow-up was much higher than the number of melanomas, indicating that the follow-up program led to early excisions of precursor lesions, thereby reducing the numbers of melanomas. This achievement has been reached through the excision of a large number of pigmented skin lesions. Of more than 1,900 lesions excised, 53% received a histopathologic diagnosis of CN. The high proportion of CN probably indicates a need for better clinical diagnosis of potential precursor lesions in order to avoid unnecessary excisions. However, the histopathologic criteria for diagnosis of DN are still controversial, and the high proportion of lesions diagnosed as CN may in part result from differences in criteria among pathologists. Moreover, excisions of nevi were sometimes made at the patients request for cosmetic or other reasons, and not solely because of suspicion of CMM. Our finding that 40 of 41 melanomas diagnosed during follow-up occurred in kindreds with at least two first-degree relatives with CMM confirms the need for monitoring of such families. Interestingly, diagnosis of CMM occurred in three of eight kindreds with germline CDKN2A mutations, supporting that these families have a particular risk for CMM development. This is in accordance with the high estimated penetrance of germline CDKN2A germline mutations for melanoma development, in affected kindreds, corresponding to a 67% risk of CMM development by age 80 years. 21 Moreover, the finding that 21 (66%) of 32 individuals with CMM during follow-up had a previous diagnosis of at least one melanoma, demonstrates that previously affected members of melanoma kindreds are at particular risk for developing further melanomas. All of these findings are of importance for the design of follow-up strategies in HCMM kindreds. A limitation in the reported data is that individuals without DN were not followed with skin examinations because, at the time of design of the program, we considered the presence of DN a marker for melanoma risk individuals. Also, we believed that surveillance should be aimed at following DN, and it seemed reasonable not to follow individuals without DN. All family members were, however, instructed in self-examination of the skin. Subsequently, it has been shown that DN is not an appropriate marker for mutation carrier status and CMM risk in families with germline CDKN2A mutations, 22 indicating that individuals without DN should also have the opportunity of skin examinations. To address the issue of whether melanomas have occurred in family members who have lacked DN and who, therefore, have not been followed with skin examinations, we will analyze the occurrence of tumors in all family members using the Swedish National Cancer Registry. This will also give information on other cancers in these families. It is important to improve primary prevention, because previous studies have shown disappointing results regarding harmful sun-related behavior in young members of Swedish HCMM-DNS families Our study cannot assess the cost effectiveness of the program. However, it is clear that individuals with a family history of CMM and who often have a large number of nevi would be frequent consumers of health care resources, requiring a large number of examinations and excisions of many pigmented lesions. Coordinated

6 Hansson et al programs such as ours represent a rational way to develop more cost-effective methods of identifying and defining high risk kindreds and designing optimal preventive interventions for the family members. In conclusion, our study shows that a coordinated program aimed at detecting CMM and performing preventive activities in HCMM-DNS kindreds results in a low number of diagnosed CMMs during follow-up among participating family members. Those tumors that do arise include a large proportion of Tis, and the invasive CMMs have considerably better prognostic characteristics than those in the general population. This indicates that the program efficiently prevents the development of high-risk melanomas in these CMMprone individuals. AUTHORS DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST The author(s) indicated no potential conflicts of interest. AUTHOR CONTRIBUTIONS Conception and design: Johan Hansson, Mia Bergenmar, Per-Åke Hofer, Eva Månsson-Brahme, Ulrik Ringborg, Inger Rosdahl Financial support: Johan Hansson, Ulrik Ringborg Administrative support: Johan Hansson Provision of study materials or patients: Johan Hansson, Per-Åke Hofer, Eva Månsson-Brahme, Ulrik Ringborg, Ann-Marie Wennberg, Inger Rosdahl Collection and assembly of data: Johan Hansson, Mia Bergenmar, Per-Åke Hofer, Eva Månsson-Brahme, Ingrid Synnerstad, Annika Ternesten Bratel, Ann-Marie Wennberg, Inger Rosdahl Data analysis and interpretation: Johan Hansson, Mia Bergenmar, Göran Lundell, Eva Månsson-Brahme, Ulrik Ringborg, Ingrid Synnerstad, Annika Ternesten Bratel, Ann-Marie Wennberg, Inger Rosdahl Manuscript writing: Johan Hansson, Mia Bergenmar, Per-Åke Hofer, Göran Lundell, Eva Månsson-Brahme, Ulrik Ringborg, Annika Ternesten Bratel, Ann-Marie Wennberg, Inger Rosdahl Final approval of manuscript: Johan Hansson, Mia Bergenmar, Per-Åke Hofer, Göran Lundell, Eva Månsson-Brahme, Ulrik Ringborg, Ingrid Synnerstad, Annika Ternesten Bratel, Ann-Marie Wennberg, Inger Rosdahl Other: Göran Lundell [provided database software] REFERENCES 1. Platz A, Ringborg U, Hansson J: Hereditary cutaneous melanoma. Semin Cancer Biol 10: , Norris W: Case of fungoid disease. Edinburgh Med Surg J 16: , Clark WH Jr, Reimer R, Greene M, et al: Origin of familial malignant melanoma from heritable melanocytic lesions: The B-K-mole syndrome. Arch Dermatol 114: , Greene M, Clark W Jr, Tucker M, et al: Precursor nevi in cutaneous malignant melanoma: A proposed nomenclature. Lancet 2:1024, Lynch H, Frichot B III, Lynch J: Familial atypical multiple mole melanoma (FAMMM) syndrome: Segregation analysis. J Med Genet 15: , Newton Bishop JA, Bataille V, Pinney E, et al: Family studies in melanoma: Identification of the atypical mole syndrome (AMS) phenotype. Melanoma Res 4: , Greene M, Clark W Jr, Tucker M, et al: High risk of malignant melanoma in melanoma-prone families with dysplastic nevi. Ann Intern Med 102: , Kraemer K, Greene M, Tarone R, et al: Dysplastic nevi and cutaneous melanoma risk. Lancet 2: , Tucker MA, Fraser MC, Goldstein AM, et al: Risk of melanoma and other cancers in melanomaprone families. J Invest Dermatol 100:350S-355S, Hussussian C, Struewing J, Goldstein A, et al: Germline p16 mutations in familial melanoma. Nat Genet 8:15-21, Kamb A, Gruis N, Weaver-Feldhaus J, et al: A cell cycle regulator potentially involved in genesis of many tumor types. Science 264: , Borg A, Johannsson U, Johannsson O, et al: Novel germline p16 mutation in familial malignant melanoma in southern Sweden. Cancer Res 56: , Platz A, Hansson J, Månsson Brahme E, et al: Screening of germline mutations in the CDKN2A and CDKN2B genes in Swedish families with hereditary cutaneous melanoma. J Natl Cancer Inst 89: , Hashemi J, Bendahl P-O, Sandberg T, et al: Haplotype analysis and age estimation of the 113 insr CDKN2A founder mutation in Swedish melanoma families. Genes Chromosomes Cancer 31: , Kefford RF, Newton Bishop JA, Bergman W, et al: Counseling and DNA testing for individuals perceived to be genetically predisposed t o melanoma: A consensus statement of the Melanoma Genetics Consortium. J Clin Oncol 17: , Kefford R, Newton Bishop J, Tucker M, et al: On behalf of the Melanoma Genetics Consortium: Genetic testing for melanoma. Lancet Oncol 3: , The National Board of Health and Welfare: Cancer Incidence in Sweden Stockholm, Sweden, The National Board of Health and Welfare, Friedman RJ, Rigel DS, Kopf AW: Early detection of malignant melanoma: The role of physician examination and self-examination of the skin. CA Cancer J Clin 35: , Lindholm C, Andersson R, Dufmats M, et al: Invasive cutaneous malignant melanoma in Sweden A prospective population based study of survival and prognostic factors. Cancer 101: , Tucker MA, Fraser MC, Goldstein AM, et al: A natural history of melanomas and dysplastic nevi: An atlas of lesions in melanoma-prone families. Cancer 94: , Bishop DT, Demenais F, Goldstein AM, et al: Geographical variation in the penetrance of CDKN2A mutations for melanoma. J Natl Cancer Inst 94: , Bishop JA, Wachsmut RC, Harland M, et al: Genotype/phenotype and penetrance studies in melanoma families with germline CDKN2A mutations. J Invest Dermatol 114:28-33, Brandberg Y, Rosdahl I, Jonell R, et al: Sunrelated behavior in individuals with dysplastic nevus syndrome. Acta Derm Venereol 76: , Brandberg Y, Sjödén P-O, Rosdahl I: Assessment of sun-related behavior in individuals with dysplastic nevus syndrome: A comparison between diary recordings and questionnaire responses. Melanoma Res 7: , Bergenmar M, Brandberg Y: Sunbathing and sun-protection behaviors and attitudes of young Swedish adults with hereditary risk for malignant melanoma. Cancer Nurs 24: , 2001 Acknowledgment The preventive program was organized as a collaboration within the Swedish Melanoma Study Group. We thank Diana Lindén for her excellent help with data management and analysis. Appendix The Appendix is included in the full-text version of this article, available online at It is not included in the PDF version (via Adobe Reader ) JOURNAL OF CLINICAL ONCOLOGY

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