Report Omari Skin Report cancer etUK al. inJournal northern Jordan Oxford, International IJD Blackwell 1365-4632 45 Publishing, Publishing Ltd, of Ltd. Dermatology 2004
Skin cancer trends in northern Jordan Abdel K. Omari, MD, Muhammad R. Khammash, MD, and Ismail Matalka, MD
From the Jordan University of Science and Technology, Irbid, Jordan Correspondence Muhammad R. Khammash, MD Jordan University of Science and Technology PO Box 3030 Irbid Jordan E-mail:
[email protected]
Abstract Background The Jordan Cancer Registry was established in 1996, since which time all cases of cancer have been reported and registered. We have used this registry to perform the first analysis of skin cancer in northern Jordan and to compare our findings with those of published reports from other regions. Methods All histopathologically proven cases of skin cancer, reported during the years 1997 through 2001, were reviewed. Information regarding tumor type, age, gender, and anatomical location was collected. Results A total of 272 cases of malignant skin tumors were diagnosed between the years 1997 and 2001. Basal cell carcinoma (BCC) was the commonest type, representing 52.9% of all skin cancers. Females were more frequently affected than males, with age-adjusted incidence rates of 23.3 and 19.7 per 100,000 of population, respectively. Squamous cell carcinoma (SCC) comprised 26.4% of the total, its age-adjusted incidence rate per 100,000 of population being 14.2 for males and 6.18 for females. the incidence rate increased in males and decreased in females during the study period. The incidence of both BCC and SCC increased with age. The head and neck region was the commonest site affected by both types of cancer. Malignant melanoma (MM) comprised 11.39% of all skin cancer cases, with a female to male ratio of 1.2 : 1. The median age at onset for female patients was 49 years while that for males was 70 years, and the commonest site affected was the lower limbs, followed by the trunk. Conclusions In Jordan, sun-related skin cancers have relatively low incidences and a rather stable pattern, compared with other areas with similar climate and skin phenotypes.
Introduction
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Jordan is an Eastern Mediterranean country lying along lines of latitude 31°31′ N and longitude 37°38′ E. The climate is that of the eastern Middle East, with nine sunny months in the year. The north of Jordan consists of four geographic regions, each with a slightly different climate: generally hot in the Jordan valley (420 m below sea level), moderate in the plains of Irbid, cold in the Ajlun mountains and hot and dry in the semi-desert area of Mafrak. The regions have a population of about 1.4 million, mostly of Arab origin, with skin phenotype mainly Fitzpatric type IV.1 Seventy per cent of the people are farmers, the rest are working in business and the civil service. The sun-related skin cancers basal cell carcinoma (BCC), squamous cell carcinoma (SCC) and malignant melanoma (MM) are the commonest cancers in Caucasians world-wide. Their incidence varies among geographic regions. This retrospective study aimed to investigate sun-related skin cancers in the north of Jordan, to determine their incidences and trends, and to compare these findings with those from other areas of International Journal of Dermatology 2006, 45, 384–388
the world. Data were retrieved from the Jordan Cancer Registry office, which was established in 1996. Materials and Methods A total of 272 cases of malignant skin tumors were reported in the north of Jordan during the years 1997 through 2001. Patient and tumor data were taken from the Jordan Cancer Registry. Data were completed from the patients’ charts whenever necessary. Incident cancer cases were defined as the first presentation of the tumor and the rates were calculated for each year, age group, and sex by using the total number of incident cases as the numerator and corresponding population estimates as the denominator. The population rates were based on census data for the years 1997– 2000, while that for 2001 was an estimate. Age-adjusted incidence and age/gender-specific incidence were calculated and 95% confidence intervals (CI) were calculated on the basis of the Poisson distribution. The anatomical location of the tumor was categorized as head and neck, upper limbs, trunk or lower limbs. The per cent © 2004 The International Society of Dermatology
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Skin cancer in northern Jordan Report
distribution of each tumor type by these anatomical sites was calculated for males and females for the entire time period.
Results In total, 272 cases of malignant skin tumors were recorded during the study period: 144 cases of BCC, 72 cases of SCC, 31 cases of MM and 25 cases of other skin tumors such as B-cell lymphoma (three cases), Kaposi’s sarcoma (three cases), malignant histiocytoma (five cases), dermato-fibrosarcoma (nine cases) and adnexial malignant tumors (five cases). Table 1 shows the yearly age-adjusted incidence rates and 95% CIs for all malignant skin tumors. Table 2 presents the age/gender-specific incidence rates for all men and women during the period of study. In males, the incidence was highest (374.4/100,000) in the age group > 80 years, while in females, it was highest in the age group 61–70 years (178.2/ 100,000). Basal cell carcinoma
A total of 144 cases of BCC were diagnosed (69 males and 75 females), constituting 52.9% of the total. The yearly adjusted incidence rates were 19.7 and 23.34 per 100,000 population for males and females, respectively, with no specific pattern of change during the period. Analysis of the age/gender-specific
incidence of BCC showed that the incidence of BCC increased with age in males to reach a maximum (16.22) in the age group above 80 years; while for females the maximum incidence was found in the age group 61–70 years (Table 3). The anatomical distribution of BCC is illustrated in Fig. 1. The majority of tumors were located in the head and neck region (95.83%), followed by the trunk (2.78%) and the upper and lower limbs (each 0.69%), with no significant differences between males and females. Squamous cell carcinoma
The second most common type of skin cancer was SCC, with 72 cases (50 males and 22 females). Its age-adjusted incidence was 14.24 for males and 4.18 for females. The incidence increased in males over the study period (9.7 in 1997 to 12.13 in 2001), while in females it decreased (8.13 in 1997 to 4.47 in 2001). Analysis of the age/gender-specific incidence (Table 4) showed that the incidence of SCC increased with age in males to reach 216.27 in the age group > 80 years. For females, it also increased with age to a maximum of 44.85 in the age group 71–80 years. There were no cases reported below 30 years of age in either sex. The head and neck region was mostly affected (72.22%). The tumor distribution on the body was different in the two sexes: in males the head and neck region was most commonly affected, followed by the
Table 1 Yearly age-adjusted incidence of skin tumors in northern Jordan Total
Males
Females
Year
No.
Rate (95% CI)
No.
Rate (95% CI)
No.
Rate (95% CI)
1997 1998 1999 2000 2001
47 62 52 55 56
36.83 (32.28 – 49.82) 47.23 (41.40 – 58.93) 38.44 (33.69 – 51.22) 39.53 (34.65 – 52.18) 39.14 (34.31– 51.84)
21 36 27 31 30
31.77 (27.85 – 45.38) 52.91 (46.38 – 63.91) 38.50 (33.75 – 51.28) 42.98 (37.67 – 55.20) 40.44 (35.44 – 52.98)
26 26 25 24 26
42.28 (37.05 – 54.59) 41.12 (36.04 – 53.57) 38.36 (33.63 – 51.16) 35.82 (31.40 – 48.93) 38.81 (34.01 – 51.55)
CI, confidence interval. Table 2 Age/gender-specific incidence (per 100,000) of malignant skin tumors in northern Jordan Total Age (years) < 20 21– 30 31– 40 41–50 51– 60 61–70 71– 80 > 80 Total
No.
Males Rate (95% CI)
No.
Females Rate (95% CI)
No.
Rate (95% CI)
2 7 21 49 71 75 30 17
0.3 (0.20 – 0.93) 2.6 (1.94 – 2.68) 15.3 (11.31–18.72) 60.3 (44.65–118.73) 112.0 (82.97–157.05) 208.0 (194.11–228.19) 173.6 (148.64 –202.72) 228.5 (169.29 –243.36)
1 1 12 23 34 42 18 14
0.3 (0.18 – 0.94) 0.8 (0.60 –1.34) 18.2 (13.48 – 20.89) 57.1 (42.29 –116.37) 109.9 (81.44 –155.52) 239.6 (177.49–251.57) 201.8 (149.50–223.58) 374.4 (277.33–351.41)
1 6 9 26 37 33 12 3
0.2 (0.17–0.92) 4.2 (3.11–3.85) 12.6 (9.31–16.72) 63.4 (46.98 –121.06) 114.0 (84.43–158.51) 178.2 (131.98 –206.06) 143.6 (106.41–180.48) 81.1 (60.08 –208.24)
272
195.5 (144.83 –218.91)
145
216.4 (160.32–234.40)
127
176.1 (130.44 –278.60)
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Table 3 The age/gender-specific incidence (per 100,000) of BCC (1997–2001) Males
Females
Total
Age (years)
No.
Rate (95% CI)
No.
Rate (95% CI)
< 20 21–30 31– 40 41–50 51–60 61–70 71– 80 > 80
1 1 3 15 17 19 7 6
0.25 (0.23 – 0.97) 0.70 (0.60 –1.31) 4.19 (3.11–3.85) 36.59 (30.24 – 47.36) 52.37 (45.42 – 62.81) 102.58 (89.25 –138.32) 83.79 (69.54 –192.45) 162.21 (141.84 – 201.64)
0 1 1 14 24 25 7 3
0 0.81 (0.59 –1.69) 1.52 (0.94 – 2.58) 34.75 (24.27– 63.47) 77.60 (49.72 –184.36) 142.62 (87.62–187.65) 78.48 (41.24 –159.48) 80.21 (59.45 –178.95)
1 2 4 29 41 44 14 9
0.13 (0.12 –1.09) 0.75 (0.42–2.15) 2.91 (1.13 – 4.15) 35.68 (13.08–79.62) 64.68 (32.04–113.09) 122.05 (79.09–201.91) 81.04 (39.82–102.92) 120.98 (82.66 –182.06)
Total
69
95.66 (58.11–168.57)
75
111.94 (78.08 –186.13)
144
103.50 (69.15 –192.06)
No.
Rate (95% CI)
Figure 1 Anatomical distribution of BCC
and SCC in males and females Table 4 Age/gender-specific incidence (per 100,000) of SCC Males
Females
Age (years)
No.
Rate (95% CI)
< 20 21–30 31– 40 41–50 51–60 61–70 71– 80 > 80
0 0 6 4 11 16 5 8
0 0 8.38 (4.31–14.53) 9.76 (6.85 –14.63) 33.89 (18.48– 68.24) 86.38 (54.98–119.64) 59.85 (41.58–98.62) 216.27 (173.92–258.64)
Total
50
69.32 (39.86–99.68)
No.
Total Rate (95% CI)
No.
Rate (95% CI)
0 0 3 2 9 4 4 0
0 0 4.55 (2.12–7.82) 4.96 (1.95 –9.54) 29.10 (24.12–55.36) 22.82 (12.03 – 41.95) 44.85 (28.09–86.15) 0
0 0 9 6 20 20 9 8
0 0 6.54 (2.16 –10.12) 7.38 (3.51–16.45) 31.55 (17.62–73.25) 55.48 (34.05–95.36) 52.10 (29.15–86.45) 107.54 (82.12–148.31)
22
32.84 (19.25–72.06)
72
51.75 (24.32–86.54)
trunk and the lower limbs (72, 12 and 10%, respectively), while in females the lower limbs were the second most commonly affected region (22.7%) (Fig. 1).
found on the lower limbs, followed by the trunk (29.73%), the head and neck (8.11%) and the upper limbs (5.41%). Other skin tumors
Malignant melanoma
Thirty-one cases of MM were seen during the study period (14 males and 17 females), comprising 11.39% of all skin cancers (with female to male ratio of 1.2 : 1). The mean age at presentation was 70 and 49 years for males and females, respectively. The anatomical distribution of MM differed from that of the nonmelanoma group, as 40.54% of the tumors were International Journal of Dermatology 2006, 45, 384–388
Twenty-five cases of other skin tumors were diagnosed: three cases of B-cell lymphoma, five cases of malignant histiocytoma, nine cases of dermatofibrosarcoma, five cases of adnexial carcinomas, and three cases of Kaposi’s sarcoma (13 males and 12 females). The mean age of male patients was 54 years and that of females was 48 years. The commonest anatomical site affected was the trunk (44%), followed by the © 2004 The International Society of Dermatology
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Skin cancer in northern Jordan Report
head and neck (32%), the upper limbs (16%) and the lower limbs (8%). Discussion Skin cancers are the commonest types of cancer in Caucasians, with incidences reaching epidemic proportions.2 They are uncommon in black people, Hispanics and Asians.3–6 Their incidence shows considerable geographic and racial variation.4 The incidence of nonmelanoma skin cancers (BCC and SCC) is more than three times that of other cancers in Australia,15 and is higher than that of any other cancer in the USA,16 while in Finland BCC alone is the second most common type of cancer.17 In Jordan, according to the Jordan National Cancer Registry Book in the year 2000, skin cancer comprised 6.3% of all cancers. This was the sixth most common type of cancer in males and the fourth most common type in females. During the study period (1997–2001), BCC was the most frequently diagnosed skin cancer in our group of patients (53%), with a slightly decreasing age-adjusted incidence from 18.15 per 100,000 of population to 16.17 in 2001 for males, while for females it decreased from 29.27 to 19.4. This incidence is much lower than that found in Australia, the USA and Europe, but higher than that found in the Chinese of Singapore14 (Table 5). It is lower than that reported from the nearby region of Izmir in Turkey.18 The female to male ratio of 1.08 and the maximum age incidence in the age group 60– 70 years were close to those reported in Izmir; however, these results differ from those obtained in other regions, where males were found to be more affected and the maximum incidence was found in an older age group.15–17 Like others, we
Table 5 Comparison of age-adjusted skin cancer incidence/
100,000 population for BCC and SCC in males and females in various geographic locations of the world Age-adjusted skin cancer incidence/ 100,000 population (male/female)
Country/region and reference Slovakia7 Finland8 UK (Scotland)9 UK (Wales)10 Canada11 USA12 Southern Arizona4 Australia13 Singapore14 Northern Jordan (present study)
Basal cell carcinoma (male/female)
Squamous cell carcinoma (male/female)
39/29 49/45 50/37 128/105 120/92 407/212 935.9/497.1 955/629 6.5/5.8 17.18/24.33
6.7/6.8 9/5 18/8 25/9 31/17 65/24 270.6/112.1 419/228 3.2/1.8 14.24/4.18
© 2004 The International Society of Dermatology
found BCC to affect mainly the head and neck region of the body (95.83%), with no significant differences between the sexes. SCC was the second most common cancer diagnosed (26.27%). Its age-adjusted incidence was 14.24 and 4.18 for males and females, respectively. The male to female ratio of 2.27 was higher than that for BCC, and the maximum incidence was found in an older age group, similar to findings reported from other regions. The anatomical distribution of SCC was slightly different from that of BCC, the head and neck being affected in 72% of males and 63.6% of females, and the second most affected area being the lower limbs in females and the trunk in males. The incidences of both BCC and SCC seem low for a country with nine sunny months per year where most of the population are farmers. The traditional head covering (Kofeyya), which farmers wind round the face during field work to reduce dust inhalation, and also the long dresses and veils wore by women might be responsible for these low incidences as they decrease the sun-exposed areas of the body. The true incidence of skin cancer is difficult to measure exactly, as unknown numbers of patients may never seek medical advice because skin cancer is a disease of elderly people who may have important concerns other than a nodule on the skin. In addition, some cases may have been treated using ablative procedures, without being submitted to histopathological examination. In females, the highest incidences of both BCC and SCC were found in younger age groups than in males, a finding also reported by Giles, who considered it puzzling and attributed it to inadequate sampling of women in this age group or to real differences between sexes.19 In our area, the minimal outdoor activities of elderly women could be another factor decreasing the duration of sun exposure. It is clear that the likelihood of developing BCC and SCC in any person depends on constitutional predisposition (genotypic and phenotypic characteristics). The most important of these is skin color and its reaction to sunlight and ultraviolet ray exposure (Fitzpatric skin types).1 This decreases with an increase in the natural darkness of the skin.20,21 Besides skin phenotypes, geographic factors are also important in increasing the risk of non melanoma skin cancer (NMSC), the incidence of which increases in areas nearer to the equator.22 In Jordan there are no exact statistics on skin phenotypes, but generally most of the population have skin type IV, with a small percentage of fair skin type III, and most of the Jordan valley people being of type V. Our incidence is close to that found for type IV Chinese patients in Singapore.14 Malignant melanoma was the third most common skin cancer in our patients (11.39%). The male to female ratio of 1 : 1.2 was close to those reported from Japan (1 : 1.06) and Singapore (1 : 1.5).14,23 In contrast to NMSC, which affected mainly older individuals, MM in white people affected younger age groups (29–45 years of age).8 In our patients it affected mostly the lower limbs, followed by the trunk, a distribution International Journal of Dermatology 2006, 45, 384–388
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similar to that generally reported, but with different mean ages of 49 and 70 years for females and males, respectively. The nature of the exposure to sunlight necessary for the development of melanoma appears to differ from that for NMSC. It has been shown that the risk of melanoma increases with history of sunburn, particularly in childhood, and migration to sunny areas, especially during childhood, was seen to increase its incidence.20 Others have reported the incidence of melanoma to be higher in higher socioeconomic groups and in indoor workers, and less in areas of maximum light exposure like the face, being most common on the back in men and on the lower limbs in women.24,25 Our findings are consistent in terms of distribution over the body, but the number of cases is too small to allow conclusions regarding other factors that may be implicated. Conclusions
This study investigated the incidence of skin cancer in the north of Jordan, in a sample reflecting the incidence in the country as a whole. The 5-year period studied may not be long enough to reveal trends for different types of skin cancer in Jordan. However, a relatively low incidence and stable trends were found, in comparison to areas with similar climates and skin phenotypes. The study highlights the importance of establishing a cancer registry office, which is vital in providing information about the incidence of the disease and in enabling planning of educational programs. References 1 Fitzpatrick TB. The validity and practicality of sun-reactive skin types I through VI. Estimating increase in skin cancer morbidity due to increase in ultraviolet radiation exposure. Arch Dermatol 1988; 124: 829 – 871. 2 Diepgen TL, Mahler V. The epidemiology of skin cancer. Br J Dermatol 2002; 146: 1– 6. 3 Pennello G, Devesa S, Gail M. Association of surface ultraviolet B radiation levels with melanoma and nonmelanoma skin cancer in United States blacks. Cancer Epidemiol Biomarkers Prev 2000; 9: 291–297. 4 Harris RB, Griffith K, Moon TE. Trends in the incidence of nonmelanoma skin cancers in southeastern Arizona, 1985–96. J Am Acad Dermatol 2001; 45: 528 –536. 5 Leong GK, Stone JL, Farmer ER, et al. Nonmelanoma skin cancer in Japanese residents of Kauai, Hawaii. J Am Acad Dermatol 1987; 17: 233–238. 6 Cheng SY, Luk NM, Chong LY. Special features of non-melanoma skin cancer in Hong Kong Chinese patients: 10-year retrospective study. Hong Kong Med J 2001; 7: 22–28. 7 Plescko I, Severi G, Obsitnikova A, et al. Trends in the incidence of non-melanoma skin cancer in Slovakia, 1978–95. Neoplasma 2000; 47: 137–142.
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8 Anna H-S, Eero P, Jaakko K. Basal cell skin carcinoma and other nonmelanoma skin cancers in Finland from 1956 through 1995. Arch Dermatol 1999; 135: 781–786. 9 Scottish Cancer Intelligence Unit ISD, National Health Service in Scotland. Cancer Registration Statistics Scotland 1990–95. Edinburgh: National Health Service, 1998. 10 Holme SA, Malinovszky K, Roberts DL. Changing trends in non-melanoma skin cancer in South Wales, 1988– 98. Br J Dermatol 2000; 143: 1224–1229. 11 Gallagher RP, Ma B, Mclean DI, et al. Trends in basal cell carcinoma, squamous cell carcinoma, and melanoma of the skin, 1973–87. J Am Acad Dermatol 1990; 23: 413–421. 12 Miller DL, Weinstock MA. Nonmelanoma skin cancer in the United States: incidence. J Am Acad Dermatol 1994; 30: 774–778. 13 Staples M, Marks R, Giles G. Trends in the incidence of non-melanoma skin cancer (NMSC) treated in Australia 1985–95: are primary prevention programs starting to have an effect? Int J Cancer 1998; 78: 144–148. 14 Koh D, Wang H, Lee J, et al. Basal cell carcinoma, squamous cell carcinoma and melanoma of the skin: analysis of the Singapore Cancer Registry data 1968–97. Br J Dermatol 2003; 148: 1161–1166. 15 Marks R. Epidemiology of non-melanoma skin cancer and solar keratosis in Australia: a tale of self-immolation in Elysian Fields. Australas J Dermatol 1997; 38: S26–S29. 16 Martinez JC, Otley CC. The management of melanoma and nonmelanoma skin cancer: a review for the primary care physician. Mayo Clinic Proc 2001; 76: 1253–1265. 17 Cancer incidence in Finland 1995. Cancer Statistics of the National Research and Development Center for Welfare and Health, Publication 58. Helsinki: Cancer Society of Finland, 1997. 18 Ceylan C, Ozturk G, Alper S. Non-melanoma skin cancers between the years of 1990 and 1999 in Izmir, Turkey: dermographic and clinicopathological characteristics. J Dermatol 2002; 30: 123–131. 19 Giles GG, Marks R, Foley P. Incidence of non-melanocytic skin cancer treated in Australia. Br Med J 1988; 296: 13–17. 20 Marks R. An overview of skin cancers. Incidence Causation Cancer 1995; 75: 607–612. 21 Hensin T. Genetics of nonmelanoma skin cancer. Arch Dermatol 2001; 137: 1486–1492. 22 Fears TR. Estimating increase in skin cancer morbidity due to increase in ultraviolet radiation exposure. Cancer Invest 1983; 1: 119–126. 23 Ishihara K, Saida T, Yamamoto A. Updated statistical data for malignant melanoma in Japan. Int J Clin Oncol 2001; 6: 109–116. 24 Holman CDJ, Mulroney CDD, Armstrong BK. Epidemiology of pre-invasive and invasive malignant melanoma in Western Australia. Int J Cancer 1980; 25: 317–323. 25 Cooke KR, Skegg DCG, Fraser J. Socioeconomic status, indoor and outdoor work, and malignant melanoma. Int J Cancer 1984; 34: 57– 62.
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