Increased Burden of Melanoma and Nonmelanoma Skin Cancer in Young Women Sarah S. Evans, MD,* Ming H. Jih, MD, PhD,† Leonard H. Goldberg, MD,† and Arash Kimyai-Asadi, MD†

BACKGROUND A higher and increasing incidence of skin cancer has been noted in younger women as compared with men. OBJECTIVE To assess the relative gender burden of basal cell carcinoma, squamous cell carcinoma, and malignant melanoma in various age groups, particularly in young adult women. MATERIALS AND METHODS A total of 16,994 biopsy-proven skin cancers in 9,376 patients in a single private dermatologic surgery practice was included in this study. RESULTS Men constituted the majority (63.7%, p < .0001) of patients, accounting for 68.7% of squamous cell carcinomas (p < .0001), 60.8% of basal cell carcinomas (p < .0001), and 57.5% of malignant melanomas (p < .0001). However, a statistically significant majority of melanomas (67.3%, p < .0001) and basal cell carcinomas (60.4%, p < .0001) were seen in women in patients aged 10 to 49 years. There was also a statistically significant increase in the female representation in patients aged 10 to 49 years as compared with those aged 50 to 99 years with respect to squamous cell carcinoma. CONCLUSION Women comprise a statistically significant majority of patients with melanoma and basal cell carcinoma in the younger (10–49 years) age groups. This raises a concern regarding an increased future incidence of skin cancer in this population group and a demographic shift to increased female representation among patients with skin cancer. The authors have indicated no significant interest with commercial supporters.

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here is an epidemiologic interest in the high and rising incidence of both melanoma and nonmelanoma skin cancer in the United States.1–3 The incidence of skin cancer is associated with fair complexion and advancing age, and the incidence of skin cancer in the general population is higher in men than in women. However, studies have noted a worrisome new trend toward an increased incidence of melanoma and basal cell carcinoma in younger adult women.4,5 The purpose of this study was to elucidate whether there is an association between patient’s age and gender for the 3 most common types of skin cancer: basal cell carcinoma, squamous cell carcinoma, and malignant melanoma. In particular, this study was

designed to assess the relative gender burden of these malignancies in various age groups in this patient population. Methods A prospectively compiled database of all tumors treated by a dermatologic surgeon (A.K.-A.) in a private referral dermatologic surgery practice in Houston, Texas, was used to retrospectively extract the data for this study. The inclusion criteria included every basal cell carcinoma, squamous cell carcinoma (including squamous cell carcinoma in situ and keratoacanthoma), or malignant melanoma in a patient between the ages of 10 and 99 years who was treated between June 2006 and January 2013. A total of 16,994 biopsy-proven skin cancers met the inclusion

*University of Texas Medical School at Houston, Houston, Texas; †DermSurgery Associates, Houston, Texas

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© 2014 by the American Society for Dermatologic Surgery, Inc. Published by Lippincott Williams & Wilkins ISSN: 1076-0512 Dermatol Surg 2014;40:1385–1389 DOI: 10.1097/DSS.0000000000000188

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criteria for this study. Exclusion criteria included age younger than 10 or older than 100 years, because the number of tumors in each category would be too low for meaningful data analysis. Similarly, tumors other than basal cell carcinoma, squamous cell carcinoma, and malignant melanoma were excluded because of rarity, and stratification based on ethnicity and skin type was not performed because of the relative paucity of higher Fitzpatrick skin types in this population. For each tumor, the following data were extracted: the histopathologic diagnosis of the tumor, the age of the patient at the time the cancer was treated, and the patient’s gender. The age of the patients was divided into 9 age categories based on 10-year increments (10–19, 20–29, 30–39, 40–49, 50–59, 60–69, 70–79, 80–89, and 90– 99 years). Ten-year increments were chosen to allow better visualization of trends in Figures 1–3 and for the analysis of variance testing. Comparisons were also made between patients in the age categories of 10 to 49 years and 50 to 99 years. Statistics were performed using the binomial test, t-test for proportions, chi-square test, and analysis of variance. Calculations were performed using

Statistics Calculator (StatPac, Inc., Bloomington, MN). A statistically significant majority was defined as a statistically significant (p < .05) difference between female and male representation in a given age group for a particular tumor or a group of tumors, because a statistically significant difference would imply comparisons performed between 2 distinct populations which would require a populationbased study.

Results This study included 16,994 tumors in 9,376 patients. Of these, 9,837 (57.9%) were basal cell carcinoma, 6,508 (38.3%) were squamous cell carcinoma, and 649 (3.8%) were malignant melanoma. Overall, men comprised of the majority (63.7%, p < .0001) of patients with all 3 tumor types, accounting for 68.7% of squamous cell carcinomas (p < .0001), 60.8% of basal cell carcinomas (p < .0001), and 57.5% of malignant melanomas (p < .0001). The male majority, however, was reversed in younger age groups, with women accounting for a statistical majority of patients (p < .0001), comprising of 58.9% of the 1,808 tumors in patients aged 10 to 49 years. This reversal in gender burden was particularly

Figure 1. Malignant melanoma. Percentage of female and male patients is indicated for each age range. The overall number of patients in each age category (n) and the p-value are included. NS, not statistically significant.

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Figure 2. Basal cell carcinoma. Percentage of female and male patients is indicated for each age range. The overall number of patients in each age category (n) and the p-value are included. NS, not statistically significant.

notable for malignant melanoma (Figure 1). Overall, 67.3% of melanomas in patients aged 10 to 49 years were in women, which represented a statistically significant difference with men (p < .0001). This was followed by a drastic drop in female representation in the patients with melanoma in subsequent deciles, with women accounting for only 34.8% of

melanomas in patients between the ages of 50 and 99 years (p < .0001 as compared with men). Women comprised of the majority (60.4%) of patients with basal cell carcinoma between the ages of 10 and 49 years (p < .0001), as opposed to only 36.0% of patients between the ages of 50 and 99 years

Figure 3. Squamous cell carcinoma. Percentage of female and male patients is indicated for each age range. The overall number of patients in each age category (n) and the p-value are included. NS, not statistically significant.

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(p < .0001). The reversal in the gender burden between the groups aged 10 to 49 years and 60 to 99 years is statistically significant (p < .0001). For squamous cell carcinoma (Figure 3), women comprised of a nearly equal proportion (49.4%) of patients in the 10- to 49-year age groups. This is in contrast to the statistically significant male majority (p < .0001), comprising of 69.8% of patients between the ages of 50 and 99 years. Indeed, women comprise of a significantly higher percentage of squamous cell carcinoma in patients aged 10 to 49 years as compared with patients aged 50 to 99 years (p < .0001). One-way analysis of variance confirmed statistically significant differences in mean gender prevalence in the 9 age groups analyzed for each of the 3 tumor types (p < .0001).

Conclusion The authors’ data are consistent with the overall increase in skin cancer incidence with advancing age, as well as the increased overall incidence of melanoma and nonmelanoma skin cancer in men. In this study population, however, women comprise of a statistically significant majority of patients with malignant melanoma and basal cell carcinoma in younger age groups. This is consistent with other studies, in particular a study by Weir and colleagues,4 which reported the incidence of melanoma among women aged 15 to 39 years as 9.74 per 100,000 as compared with 5.77 per 100,000 in men. Similarly, a study by Christenson and colleagues5 using data from 1976 to 2003 found the age-adjusted incidence of basal cell carcinoma among the population under age 40 years in Olmsted County, Minnesota to be 25.9 per 100,000 in women and 20.9 per 100,000 in men, with the incidence of basal cell carcinoma rising over the study period only in women. An important question that is left unanswered by this study is whether the cancers in younger women are caused by ultraviolet exposure (e.g., tanning beds and sunbathing) or by other factors. Although, it is recognized that female gender is associated with more frequent sun tanning and sunbed use,6,7 there has also

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been a controversial link between melanoma and pregnancy and gender-specific hormones, raising the possibility that hormonal factors may play a role in the etiology of skin cancer.8–10 This study was not designed to answer the question of causality. However, the data showing the increased incidence of melanoma in young women over the past decades are more consistent with behavioral changes with respect to ultraviolet exposure rather than hormonal factors, because the latter would be more constant over time. Based on data from the Surveillance, Epidemiology, and End Results Program, Purdue and colleagues found that the age-adjusted annual incidence of melanoma among men aged 15 to 39 years increased from 4.7 cases per 100,000 in 1973 to 7.7 cases per 100,000 in 2004. Among women, the incidence increased from 5.5 per 100,000 to 13.9 per 100,000 over the same time period.11 Similarly, Quatresooz and colleagues12 reported a 24% rise in the female-to-male ratio of malignant melanoma in southeast Belgium between the years 1988 and 2002. In Spain, the annual increase in melanoma mortality between 1975 and 1998 was found to be 13% among men and 33% among women.13 The increased mortality also makes it less likely that the increase in melanoma incidence in younger women is due simply to their increased dermatologic vigilance as compared with men. It should be noted, however, that because these studies are conducted across different countries and cultures, the exact applicability of the results to other populations is questionable. One notable finding in this study, which to the authors’ knowledge has not been previously reported, is that there is an inflection point around age 50 years, where melanoma and basal cell carcinoma go from being a predominantly female disease to a predominantly male one (Figures 1 and 2). It is noteworthy that tanning beds were introduced in the United States in 1979, therefore women who were in their late teens and 20s at that time would be in their late 40s and 50s, which corresponds to the inflection point observed in this study. The main limitation of this study is that it is not a population-based study but rather a single-surgeon

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study at a referral dermatologic surgery practice, creating the possibility of referral bias that is difficult to quantify; this may be reflected in the higher proportion of squamous cell carcinomas in this study. Furthermore, this study is limited by the lack of other demographic information (race, ethnicity, socioeconomic status, and marital status), health variables (e.g., immunosuppression), and exposure variables, all of which may affect the trends noted. However, the fact that the authors’ data are corroborated by other studies, including population-based ones, somewhat mitigates this concern. Furthermore, the authors did not demographically adjust the data, which may affect the data in the 80- to 99-year age groups where women significantly outnumber men in the general population. However, some of the convergence seen in the 80- to 99-year age groups (Figures 1–3) may be due to increased female representation in the elderly population. Furthermore, because the authors’ data capture a snapshot in time, no conclusion regarding trends can be deduced from their data, and because it is not a population-based study, estimates of incidence and prevalence and comparisons with population-based studies cannot be made. In addition, skin cancers treated nonsurgically are not included in this study, and that may affect some of the findings. The results of this study and other cited studies raise potential long-term public health concerns. First, over the ensuing decades, as the current population of young adults ages, women may continue to develop more skin cancers than men, drastically increasing the skin cancer incidence in the overall population. Second, reversal of this trend will require concerted public health efforts, including population-based education, particularly among young women. The educational and health care systems have vital roles to play in the public education campaigns. Third, the results of a study like this, if properly publicized, can help spread the message that skin cancer does affect younger

patients, and that young women are particularly vulnerable, and that their tanning and sunbathing behaviors may be contributory behavioral factors that can be altered.

References 1. Stern RS. Prevalence of a history of skin cancer in 2007: results of an incidence-based model. Arch Dermatol 2010;146:279–82. 2. Rogers HW, Weinstock MA, Harris AR, Hinckley MR, et al. Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch Dermatol 2010;146:283–7. 3. Garbe C, Leiter U. Melanoma epidemiology and trends. Clin Dermatol 2009;27:3–9. 4. Weir HK, Marrett LD, Cokkinides V, Barnholtz-Sloan J, et al. Melanoma in adolescents and young adults (ages 15–39 years): United States, 1999–2006. J Am Acad Dermatol 2011;65:S38–49. 5. Christenson LJ, Borrowman TA, Vachon CM, Tollefson MM, et al. Incidence of basal cell and squamous cell carcinomas in a population younger than 40 years. JAMA 2005;294:681–90. 6. Falk M, Anderson CD. Influence of age, gender, educational level and self-estimation of skin type on sun exposure habits and readiness to increase sun protection. Cancer Epidemiol 2013;37:127–32. 7. Centers for Disease Control and Prevention (CDC). Use of indoor tanning devices by adults—United States, 2010. MMWR Morb Mortal Wkly Rep 2012;61:323–6. 8. Wiggins CL, Berwick M, Bishop JA. Malignant melanoma in pregnancy. Obstet Gynecol Clin North Am 2005;32:559–68. 9. Grin CM, Driscoll MS, Grant-Kels JM. The relationship of pregnancy, hormones, and melanoma. Semin Cutan Med Surg 1998; 17:167–71. 10. Driscoll MS, Grant-Kels JM. Nevi and melanoma in pregnancy. Dermatol Clin 2006;24:199–204. 11. Purdue MP, Freeman LE, Anderson WF, Tucker MA. Recent trends in incidence of cutaneous melanoma among US Caucasian young adults. J Invest Dermatol 2008;128:2905–8. 12. Quatresooz P, Uhoda I, Fumal I, Piérard-Franchimont C, et al. Revisiting the gender-linked melanoma burden. Dermatology 2004;209: 197–201. 13. Nieto A, Ruiz-Ramos M, Abdel-Kader L, Conde M, et al. Gender differences in rising trends in cutaneous malignant melanoma in Spain, 1975–98. Br J Dermatol 2003;148:110–6.

Address correspondence and reprint requests to: Arash Kimyai-Asadi, MD, DermSurgery Associates, 7515 Main Street, Suite 290, Houston, TX 77030, or e-mail: [email protected]

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Increased burden of melanoma and nonmelanoma skin cancer in young women.

A higher and increasing incidence of skin cancer has been noted in younger women as compared with men...
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