Skin cancer in Puerto Rico: a multiannual incidence comparative study.
Abstract: Background: The incidence of skin cancer continues to increase worldwide. The purpose of this study was to determine the incidence of skin cancer in Puerto Rico in a selected year (2005) and to compare these findings with those previously reported for Puerto Rico in 1974 and 1981 and with other countries.

Methods: The data was collected from the pathology reports corresponding to the period of January to December 2005 of 21 participating Pathology Laboratories throughout Puerto Rico. The rate and distribution of the main types of skin cancer was calculated based on sex, age, anatomic location and laterality.

Results: The incidence of skin cancer in Puerto Rico for 2005 was 6,568 cases, which represent a rate of 167.9 per 100,000 inhabitants. The most common type of skin cancer was basal-cell carcinoma. Skin cancer was more common in males except for melanoma, which was more common in females. The incidence increases with age on all types of skin cancer. The head and neck area was the most frequent location, except for melanoma in women, which was more common on the legs. The incidence rate was 41.5/100,000 in 1974, 52.5/100,000 in 1981 and 167.9/100,000 in 2005, a 305% increase.

Conclusions: We found an increasing incidence of skin cancer in Puerto Rico when compared with previous reported data. This analysis provides a comprehensive evaluation of the epidemiology of skin cancer in Puerto Rico. [P R Health Sci J 2010;3:312-316]

Key words: Skin Cancer, Incidence, Puerto Rico

Contexto: La incidencia de cancer de piel continua aumentando en todo el mundo. El proposito de este estudio fue determinar la incidencia de cancer de piel en Puerto Rico en un ano seleccionado (2005) y comparar nuestros resultados con los reportados para Puerto Rico en 1974 y 1981 y con otros paises. Metodos: Los datos fueron reunidos de los informes de patologia correspondientes al periodo de enero a diciembre 2005, de 21 Laboratorios del Patologia en Puerto Rico. La tasa y la distribucion de los principales tipos de cancer de piel fueron calculadas basadas en el sexo, la edad, la ubicacion anatomica y la lateralidad. Resultados: La incidencia de cancer de piel en Puerto Rico para 2005 fue 6,568 casos, que representan una tasa de 167.9 por 100,000 habitantes. El tipo mas comun de cancer de piel fue carcinoma baso-celular. El cancer de piel fue mas comun en hombres menos melanoma, que fue mas comun en mujeres. La incidencia aumenta con la edad en toda clase de cancer de piel. La area de la cabeza y el cuello fue la ubicacion mas frecuente, menos melanoma en mujeres que fue mas comun en las piernas. La tasa de la incidencia fue 41.5/100,000 en 1974, 52.5/100,000 en 1981 y 167.9/100,000 en 2005, un aumento de 305%. Conclusion: Encontramos una incidencia creciente de cancer de piel en Puerto Rico cuando comparamos con los datos antes reportados. Este analisis proporciona una evaluacion completa de la epidemiologia de cancer de piel en Puerto Rico.
Article Type: Perspectiva general de la enfermedad/trastorno
Subject: Cancer de la piel (Investigacion cientifica)
Cancer de la piel (Causas)
Cancer de la piel (Cuidado y tratamiento)
Authors: De La Torre-Lugo, Eneida M.
Figueroa, Luz D.
Sanchez, Jorge L.
Morales-Burgos, Adisbeth
Conde, Daniel
Pub Date: 09/01/2010
Publication: Name: Puerto Rico Health Sciences Journal Publisher: Universidad de Puerto Rico, Recinto de Ciencias Medicas Audience: Academic Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2010 Universidad de Puerto Rico, Recinto de Ciencias Medicas ISSN: 0738-0658
Issue: Date: Sept, 2010 Source Volume: 29 Source Issue: 3
Geographic: Geographic Name: Puerto Rico
Accession Number: 234999047
Full Text: Cancer of the skin refers to those neoplasms that are intrinsic to the skin and which originate from the different components of the epidermis, dermis or adnexal structures. It is the most common of all types of cancer in the United States (1). It is estimated that more than 1 million of skin cancers are diagnosed each year in the United States (1) and that 1 out of 5 Americans will develop skin cancer in the course of a lifetime (2). Most of these (about 800,000 to 900,000) are basal-cell carcinoma (BCC), squamous-cell carcinoma (SCC) occurs less often (about 200,000 to 300,000 per year) (3). Malignant melanoma (MM) is far less frequent than nonmelanoma skin cancer (NMSC) but is responsible for the majority of skin cancer deaths (4).

The incidence of all types of skin cancer is increasing rapidly (1-8). The incidence of skin cancer reported for Puerto Rico in 1974 was 41.5 per 100,0005 habitants and in 1981 52.5 per 100,000 habitants (6). The reported increase of skin cancer, especially keratinocytic and melanocytic, is thought to be from a combination of increased sun exposure (ultraviolet light), increased outdoor activities, infrequent use of sunscreen, indoor tanning, changes in clothing styles, increased longevity and ozone depletion (8-9). Incidence also increases with age and male sex (8, 10). The incidence of basal-cell carcinoma in individual over 75 years is approximately 5 times higher than that of individuals between 50 and 55 years old and for squamous-cell carcinoma approximately 35 times higher.8 This means that the association between age and incidence is stronger for squamous than for basal-cell carcinoma. Recent studies have also found an association between the use of psoralen plus ultraviolet (UV) light A phototherapy and biologic therapies with an increase risk of cutaneous malignancies (11-12).

Results of this study are essential for the evaluation of the disease burden and demand for health care related services, and also for the development of public health prevention and care giving strategies.

Materials and Methods

This study was approved by the Oncology Hospital and Veterans Affairs Caribbean Healthcare System Institutional Review Boards. The study was conducted in accordance with the guidelines for good clinical practice. The data was collected from the pathology reports corresponding to the period of January to December 2005 of 21 participating Pathology Laboratories throughout Puerto Rico. Two pathology laboratories did not participate in the study. The potencial percentage of missed cases from these laboratories was estimated to be low. The data of each case included age and gender, type (histopathologic diagnosis), anatomical location and side of the tumor. The data was analyzed in terms of rate and distribution for type of skin cancer, sex, age, anatomic location and laterality.

The inclusion criteria consisted of a complete pathological report with a diagnosis of skin cancer during the year 2005. The following histopathologic diagnoses were included: malignant melanoma, basal-cell carcinoma, squamous-cell carcinoma, keratoacanthoma, Merkel-cell carcinoma, apocrine carcinoma and variants, eccrine carcinoma and variants, sebaceous carcinoma, and trichocarcinoma and variants. Bowen's disease and squamous-cell carcinoma in-situ were included under the diagnosis of squamous-cell carcinoma. Basosquamous carcinoma was included under the diagnosis of basal-cell carcinoma. The exclusion diagnoses were cutaneous lymphoma, Kaposi's sarcoma, other sarcomas, metastases to skin and recurrent malignancies. The exclusion criterion was the unavailability of the pathology report and incomplete data. In patients with multiple skin cancers, statistical adjustment was done to count these cases as individual lesions.

The incidence rates were calculated based on the Puerto Rico population estimates for 2005 which was 3,912,054 and multiplied by 100.000 (13). The statistical analysis use for comparing rates between age and sex was the Z test with a 95% confidence intervals and frequency distribution for %. P < 0.05 was considered statistically significant.

Results

A total of 6,568 new skin cancer cases were reported in Puerto Rico for 2005. The most common type of skin cancer was basal-cell carcinoma (BCC) with 4,164 cases (rate 106.4, 63.4%), followed by squamous-cell carcinoma (SCC) 2,042 cases (rate 52.2, 31.1%), keratoacanthoma (KA) 235 cases (rate 6.0, 3.6%) and melanoma 100 cases (rate 2.6, 1.5%) (Table 1). Other reported skin cancers correspond to 0.7% and included: sebaceous carcinoma, adnexal carcinoma, porocarcinoma, adenoid cystic carcinoma, apocrine carcinoma, Merkel-cell carcinoma, malignant nodular hidradenoma, and malignant proliferating trichilemmal tumor.

Skin cancer was more common in males than in females and was statistically significant (p<0.05) for basal-cell carcinoma 53.9% vs. 46.1%, squamous-cell carcinoma 58.1% vs. 41.9% and keratoacanthoma 55.8% vs. 44.2%. This difference was not observed in melanoma which was found to be more common in females 48.0% vs. 52.0% (Table 2). Mean age for the main types of skin cancer was 69.8 in basal-cell carcinoma, 73.5 in squamous-cell carcinoma and keratoacanthoma and 64.1 in melanoma patients (Table 1). The incidence rates by age and sex were higher for the age group of 85 years and older (rate per 100,000 inhabitants) for both basal-cell carcinoma (860.0) (Table 3) and squamous-cell carcinoma (616.0) (Table 4). The distribution by age for melanoma was different between males and females because in males the majority of the cases reported were between the age group of 64-84 years, but in females the majority of the cases were in the age groups of 35-59 and 60-84 (data not shown).

In both sexes, the most frequent location of basal-cell carcinoma and squamous-cell carcinoma was the head and neck area (data not shown). Melanoma in males was more common also in the head and neck area, but in females the legs was most frequent location (Table 5). The results of this study show a small but generally consistent excess of left-sided skin cancer (data not shown), but no statistically significant difference was reach because of the high number of reports were the laterality was not specified.

We found an increase in the incidence of skin cancer in Puerto Rico when compared with previous reported data, for 1974 the incidence rate was 41.5/100,000, in 1981 was 52.5/100,000 and in 2005 was 167.9/100,000, a 305% increase in incidence.

Comment

The incidence of skin cancer in Puerto Rico has substantially increased from 1941 to 2005, and it is estimated that will continue to increase (6).

The age-adjusted incidence rates per 100,000 persons were as follow: BCC (males) 117.5, BCC (females) 93.1, SCC (males) 62.8, SCC (females) 41.9 (Table 2). These are lower when compared to the estimated (lowest and highest) age-adjusted incidence rates per 100,000 whites for the year 1994 in the United States (14): BCC (males) 407-485, BCC (females) 212-253, SCC (males) 81-136, SCC (females) 26-59. Although the incidence rates of the US are higher than those of Puerto Rico, they do not approach the rates described from Australia where the incidence is 1000-2000 per 100,000 per year (14). The age-standardized incidence rates in Townsville, Australia between December 1996 and December 1997 were: BCC (males) 2058.3, BCC (females) 1194.5, SCC (males) 1332.3, SCC (females) 754.8 (15). In Scotland, the incidence of SCC between 1995-1997 was 34.7/100,000 which is lower than in Puerto Rico (16). In Canada, the age-standardized rate of NMSC per 100.000 persons was 36 in 1960 and 99 in 2000, lower than the rates in Puerto Rico (17). In Sweden, SCC rates increase in men from 4.4/100,000 in 1961 to 23.1/100,000 in 1995 and among women from 4.1 to 10.1 respectively, but still are lower when compare with the rates of SCC in Puerto Rico (18).

The incidence of skin cancer depends on the geographical region, those living at latitudes closer to the equator have higher incidence rates (8, 10). The highest increases in the incidence of BCC has been reported in Australia with incidence rates between 1 and 2% per year, followed by the US and Europe (10). There is an increased risk of NMSC in white populations, especially those with blue eyes, skin types I and II (sunburn easily, suntan poorly, freckle with sun exposure) and red or blond hair (8). The protective role of skin pigmentation is underlined by the fact of low incidence rates of BCCs in individuals of African descent (10). Malignant melanoma occurs among all racial and ethnic groups, but the frequency of its occurrence is closely associated with the color of the skin, and depends on the geographical zone (8). The risk factors for melanoma occurring in an individual include a combination of constitutional predisposition (skin color, tendency to freckle, family history of melanoma, presence of a large number of nevi, increasing age) and exposure to environmental factors (UV light). Sun exposure in childhood and intense intermittent sun exposures are suggested to be the major environmental risk factors (19).

Most of the skin cancers in Puerto Rico were basal-cell carcinoma, followed by squamous-cell carcinoma. There was a statistically significant difference between sexes for BCC and SCC, being most common in males. This difference was not held true for melanoma for which the majority of the cases were reported in women. This finding is very similar to that described by Valentin et al. in 2007 (7). They reported 48.2% of males cases and 51.8% of females cases between 1987 and 2002, with a mean of 98 melanoma cases per year. We found 48% of male cases and 52% of female cases with a total of 100 melanoma cases for the year 2005. Also the distribution by age for melanoma was different between males and females because for males the majority of the cases reported were between the age group of 64-84 years, but for females the majority of the cases were in the age groups of35-59 and 60-84. In both sexes, the most frequent location of skin cancer was the head and neck area, except for melanoma in women were the most common anatomic area reported was the legs. For women 4.2% of SCC occurred on the genitalia, but the etiology for the cancer in this area is multifactorial and includes the human papillomavirus but not sun exposure (20).

Anatomical asymmetry (laterality) in skin cancer incidence has been observed for malignant melanoma in Australia, England, Finland, Netherlands, Scotland and US from 19982003 (21). More recently Butler and Fosko found significantly more skin cancers formed on the left side of the body than the right in men and especially of the exposed areas of the head and neck (22). Our results reflect a small but generally consistent excess of left-sided skin cancers, but not statistically significant due to the high numbers of cases where laterality of skin cancers was not specified in the pathology reports. The suggested explanations to the left-sided skin cancer excess are due to increased exposure to UV rays during driving may lead to the development of more skin cancers on the left side of the body, (22) and asymmetry of melanocyte distribution during embryogenesis (21).

A limitation to our study was the two Pathology Laboratories that did not participated in the study, but potential percentage of missed cases was estimated to be low. Other limitation is the cases not reported due to patients lacking access to physicians, patient not seeking care, patients dying from other causes before diagnosis, and diagnostic accuracy of primary and/or pathologist. The rising in the incidence can be secondary to the increase in life expectancy, earlier detection and higher surveillance.

When compared with previous reported data, the incidence of skin cancer in Puerto Rico has increased from 41.5/100,000 in 1974, to 52.5/100,000 in 1981 and 167.9/100,000 in 2005. These results are valuable for the public health care system to encourage the importance of skin cancer preventive strategies such as: use of sunscreen with sun protection factor of 30 or higher; wearing protective clothing and sunglasses; and avoidance of sunbathing as well as tanning beds which provide an additional source of UV radiation (1). Early detection is essential through regular skin exam by the patient and promptly visiting a physician if new or unusual lesions or a progressive change in a lesion's appearance (size, shape or color, etc) occurs.

For all suspicious lesions removal and microscopic examination is necessary. Although NMSC has a low mortality, its incidence is more common than all other cancers combined (23) and in view of the already mentioned increase in incidence, the cost of care to health insurance is likely to increase. Regulations or legislations that will positively impact the management of skin cancer are needed.

References

(1.) American Cancer Society. Cancer Facts & Figures 2009. Atlanta: American Cancer Society; 2009.

(2.) Robinson JK. Sun Exposure, Sun Protection and Vitamin D. JAMA 2005; 294: 1541-43.

(3.) American Cancer Society (ACS). Skin Cancer--Basal and Squamous Cell. Altanta GA: ACS 2008.

(4.) de Vries E, van de Poll-Franse LV, Louwman WJ, de Gruijl FR, Coebergh JW. Predictions of skin cancer incidence in the Netherlands up to 2015. Br J Dermatol. 2005 Mar;152(3):481-8.

(5.) Cancer Control Program, Central Cancer Registry, Department of Health, 1984.

(6.) Quintero, AL, Torres SM, Sanchez, JL. Skin Cancer in Puerto Rico. Bol. Asoc. Med. P. Rico. 1985; 77; 502-503.

(7.) Valentin SM, Sanchez JL, Figueroa LD, Nazario CM. Epidemiology of melanoma in Puerto Rico. 1987-2002. PR Health Sci J. 2007 Dec;26(4): 343-8.

(8.) Diepgen TL, Mahler V The epidemiology of skin cancer. Br J Dermatol. 2002 Apr; 146 Suppl 61:1-6.

(9.) Coups EJ, Manne SL, Heckman CJ. Multiple skin cancer risk behaviors in the U.S. population. Am J Prev Med. 2008 Feb;34(2):87-93.

(10.) Roewert-Huber J, Lange-Asschenfeldt B, Stockfleth E, Kerl H. Epidemiology and aetiology of basal cell carcinoma. Br J Dermatol. 2007 Dec;157 Suppl 2:47-51.

(11.) Patel RV, Clark LN, Lebwohl M, Weinberg JM. 2009. Treatments for psoriasis and the risk of malignancy. J Am Acad Dermatol. Jun;60(6): 1001-17.

(12.) Wolfe F, Michaud K. Biologic treatment of rheumatoid arthritis and the risk of malignancy: analyses from a large US observational study. Arthritis Rheum. 2007 Sep; 56(9):2886-95.

(13.) Federal-State Cooperative for Population Estimates. Annual Estimates of the Population for the United States and for Puerto Rico. Available at: http://www.gobierno.pr/Censo/EstimacionPoblacion/ EstimacionesNegociado/. Accessed June 25, 2010.

(14.) Miller DL, Weinstock MA. Nonmelanoma skin cancer in the United States: incidence. J Am Acad Dermatol. 1994 May;30(5 Pt 1):774-8.

(15.) Buettner PG, Raasch BA. Incidence rates of skin cancer in Townsville, Australia. Int J Cancer. 1998 Nov 23;78(5):587-93.

(16.) Brewster DH, Bhatti LA, Inglis JH, Nairn ER, Doherty VR. Recent trends in incidence of nonmelanoma skin cancers in the East of Scotland, 19922003. Br J Dermatol. 2007;156(6):1295-1300.

(17.) Demers AA, Nugent Z, Mihalcioiu C, Wiseman MC, Kliewer EV. Trends of nonmelanoma skin cancer from 1960 through 2000 in a Canadian population. J Am Acad Dermatol. 2005;53(2):320-328.

(18.) Wassberg C, Thorn M, Johansson AM, Bergstrom R, Berne B, Ringborg U. Increasing incidence rates of squamous cell carcinoma of the skin in Sweden. Acta Derm Venereol. 2001;81(4):268-272.

(19.) Walter SD, King WD, Marrett LD. Association of cutaneous malignant melanoma with intermittent exposure to ultraviolet radiation: results of a case-control study in Ontario, Canada. Int J Epidemiol. 1999 Jun;28(3):418-27.

(20.) van der Avoort IA, et al. Vulvar squamous cell carcinoma is a multifactorial disease following two separate and independent pathways. Int J Gynecol Pathol. 2006 Jan;25(1):22-9.

(21.) Brewster DH, Horner MD, Rowan S, Jelfs P, de Vries E, Pukkala E. Left sided excess of invasive cutaneous melanoma in six countries. EJC 2007 2634-2637.

(22.) Butler ST, Fosko SW. Increased prevalence of left-sided skin cancers. J Am Acad Dermatol. 10.1016/j.jaad.2009.11.032.

(23.) Housman TS, Feldman SR, Williford PM, Fleischer AB Jr, Goldman ND, Acostamadiedo JM, et al. Skin cancer is among the most costly of all cancers to treat for the Medicare population. J Am Acad Dermatol. 2003 Mar;48(3):425-9.

Eneida M. De La Torre-Lugo, MD *; Luz D. Figueroa, MD ([dagger]); Jorge L. Sanchez, MD ([double dagger]); Adisbeth Morales-Burgos, MD ([section]); Daniel Conde, MD **

* Dermatology Resident; ([dagger]) Associate Professor; ([double dagger]) Professor; ([section]) Assistant Professor, Department of Dermatology, University of Puerto Rico School of Medicine, San Juan, Puerto Rico; ** Veterans Affairs Caribbean Healthcare System

The authors have no conflict of interest to disclose.

Address correspondence to: Eneida M. De La Torre-Lugo, MD, University of Puerto Rico School of Medicine, Department of Dermatology, PO Box 365067 San Juan, Puerto Rico 00936-5067. Tel: (787) 765-7950 * Fax: (787) 767-0467 * Email: eneida. delatorre@upr.edu
Table 1. Incidence rates and mean age for the main types of skin
cancer

Type of skin cancer   # of cases   Rate *   Mean Age

BCC                   4,164        106.4    69.8
SCC                   2,042        52.2     73.5
KA                    235          6.0      73.5
MELANOMA              100          2.6      64.1

* Rates per 100,000 inhabitants

The incidence of skin cancer in Puerto Rico
for 2005 was 6,568 cases (rate 167.9)

Table 2. Incidence rates by type of skin cancer and sex

                    Male                 Female
Type of
skin cancer   #cases   Rate    # cases   Rate   P-value

BCC           2,209    117.5   1,892     93.1   <0.0001
SCC           1,181    62.8    851       41.9   <0.0001
KA            130      6.9     103       5.1    0.0185
MELANOMA      48       2.6     52        2.6    0.9941

* Rates per 100,000 inhabitants

Table 3. Incidence rates of BCC by age and sex

            Male              Female            Total
Age group   cases    Rate *   cases    Rate *   cases    Rate *

0-19        4        0.7      1        0.2      5        0.4
20-34       19       4.6      34       7.9      53       6.3
35-59       402      69.5     388      58.5     790      63.6
60-84       1367     496.9    1124     327.3    2491     402.8
85+         280      1259.6   217      610.2    497      860.0
Age, not
specified   137               128               265
Total       2209     117.5    1892     93.1     4101     104.8

* Rates per 100,000 inhabitants

Table 4. Incidence rates of SCC by age and sex

            Male              Female            Total
Age group   cases    Rate *   cases    Rate *   cases    Rate *

0-19        1        0.2      0        0.0      1        0.1
20-34       14       3.4      2        0.5      16       1.9
35-59       155      26.8     82       12.4     237      19.1
60-84       657      238.8    425      123.8    1082     174.9
85+         170      764.8    186      523.0    356      616.0
Age, not
specified   184               156               340
Total       1181     62.8     851      41.9     2032     51.9

* Rates per 100,000 inhabitants

Table 5. Anatomic distribution for melanoma

Site      Male   Female   Total   %

back      7      7        14      15.6
foot      7      7        14      15.6
leg       0      12       12      13.3
arm       1      8        9       10.0
abdomen   6      0        6       6.7
ear       5      1        6       6.7
chest     3      2        5       5.6
neck      4      0        4       4.4
buttock   2      1        3       3.3
cheek     1      2        3       3.3
eyelid    1      2        3       3.3
others    7      4        11      12.2

Total     44     46       90      100
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