Photodermatology, Photoimmunology & Photomedicine

ORIGINAL ARTICLE

The incidence and body site of skin cancers in the population groups of South Africa Mary Norval1, Patricia Kellett2 & Caradee Yael Wright3

1 Biomedical Sciences, University of Edinburgh, Edinburgh, Scotland. 2 National Cancer Registry, National Health Laboratory Service, Johannesburg, South Africa. 3 Climate Studies, Modelling and Environmental Health Research Group, Council for Scientific and Industrial Research, Natural Resources and the Environment, Pretoria, South Africa.

SUMMARY Background/Purpose Data regarding basal cell carcinoma (BCC), squamous cell carcinoma of the skin (SSCC) and cutaneous melanoma (CM) in multiracial populations are sparse. Here the incidence and body site of these tumours in the South African population in 2000–2004 were analysed. Methods Annual age-standardized incidences and body sites of BCC, SSCC and CM in black, coloured, Asian and white groups were obtained from histological confirmed cases, reported to the National Cancer Registry.

Key words: basal cell carcinoma; cutaneous melanoma; South Africa; squamous cell carcinoma of the skin

Correspondence: Professor Mary Norval, B.Sc., PhD, D.Sc., Biomedical Sciences, University of Edinburgh Medical School, Teviot Place, Edinburgh EH8 9AG, UK. Tel: +44 1316503167 e-mail: [email protected]

Accepted for publication: 20 December 2013

Results Highest annual incidences of BCC, SSCC and CM occurred in the white group, followed by coloured, then Asian and then black. BCCs and SSCCs were about twice as common in males than females. CM was the least frequent skin tumour, and BCC the most frequent, except in black people. The head was the commonest body site for SSCC and BCC in all groups and both sexes, whereas the lower limb was the predominant site for CM in black people. Mean age at diagnosis was generally mid-50s for CM, and mid-60s for BCC and SSCC. Conclusions In South Africa, differences in reported incidence rates and body sites of skin tumours by population group and sex occur. Host characteristics, particularly skin phototype, and personal behaviour are likely to affect the risk of these cancers.

Funding sources: None.

Conflicts of interest: None declared.

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Photodermatol Photoimmunol Photomed 2014; 30: 262–265

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd doi:10.1111/phpp.12106

Skin cancers in South Africa

The majority of surveys monitoring the prevalence and annual incidence of the three commonest skin cancers, basal cell carcinoma (BCC), squamous cell carcinoma of the skin (SSCC) and cutaneous melanoma (CM) have used data from populations with predominantly white skin. Limited information, mainly from the United States, indicates that that these tumours occur less frequently and sometimes on different body sites in subjects with black skin compared with white skin (1–4). Similar investigations in countries where the majority of people have black skin and a minority fair or brown skin are sparse. South Africa represents one such country. Also, due to its latitude (22–35°S), high altitude in the interior, annual average daytime temperature of 22°C and high UV index almost all year round, intense personal exposure to solar ultraviolet radiation (UVR), recognized as the major environmental risk factor for skin cancer, is likely. South Africans are divided into four populations, largely reflecting pre-1994 legislated groupings: black, white, coloured (mixed European [white] and African [black] or Asian ancestry and Cape Malays, with skin colour ranging from pale to dark brown) and Asian/Indian (called Asian in South Africa). The groups reflect those used in the census data collected by the South African Government. The 2001 census indicated that 79.4% were black, 9.2% white, 8.8% coloured and 2.6% Asian. There is a considerable range of skin phototypes within each group.

METHODS Histologically confirmed cases of BCC, SSCC and CM, reported to the National Cancer Registry (NCR) in 2000– 2004, were analysed. The NCR is a pathology-based registry that receives reports on patients diagnosed with cancer from all public and private sector histology, cytology and haematology laboratories in South Africa. The cancers are coded by organ site and morphological type using the International Classification of Diseases for Oncology. Each multiple primary cancer is recorded as an additional case, using the International Agency for Research on Cancer guidelines (5), and duplicate entries are deleted. Duplicate cancers include those that were diagnosed in previous years and already existed on the NCR database. The population group of the patients was unspecified in 93% of cases: these subjects were assigned to a group by comparing their surnames with a reference database of approximately 1.4 million surnames of known race. A hot-deck imputation method was employed to allocate the surnames whose validity was proved using data collected prior to the mid1990s when the group was routinely reported (6). This method was constructed for the NCR as a SAS program by Photodermatol Photoimmunol Photomed 2014; 30: 262–265 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Table 1. Mean age-standardized annual incidence of reported squamous cell carcinoma of the skin (SSCC), basal cell carcinoma (BCC) and cutaneous melanoma (CM) per 100 000 persons in the black, Asian, coloured and white populations of South Africa, 2000–2004

BCC: Male Female SSCC: Male Female CM: Male Female

Black

Asian

Coloured

White

All

3.0 1.7

7.7 5.3

59.2 26.5

198.3 112.8

51.3 25.4

3.0 1.6

4.3 2.7

26.1 15.4

69.5 31.8

20.8 8.5

1.0 1.2

0.7 1.1

5.9 4.1

20.5 16.5

5.3 3.9

the Data Management and Statistical Analysis Unit of the University of Witwatersrand. The database is continually updated with the addition of each new patient whose population group is known, and information from other sources is also used to improve quality and completeness. The incidence of each tumour type varied from 1 year to another by less than 10% over the 5 years of the study with no significant trends, and thus the mean values for the annual age-standardized incidence in the four population groups were calculated. The percentage of the three tumour types occurring on the head (lip, eyelid, ear, face, scalp and neck), trunk, upper limb/shoulder and lower limb/hip was calculated using all 26 695 case reports in men and 18 021 in women in 2000–2004. The body site was specified in about 55% of cases. Details relating to the dorsal or ventral side of the trunk and to acral or non-acral sites in the limbs were not recorded, except for CM in some instances. The average age at diagnosis of skin cancer was calculated from the first 300 cases reported in 2002 in white men and all cases in coloured, Asian and black men reported in 2002, and similarly in women in 2002.

RESULTS AND DISCUSSION Black people and Asians had a lower reported incidence of SSCC, BCC and CM than coloureds and a considerably lower incidence than white people (Table 1). The incidence of CM in white and black people was similar to that reported in the United States (1). Comparison of annual incidences of CM in white and black people with figures based on cases in Johannesburg in 1959–1970 (7) indicates substantial increases since that time. As far as we are aware, no more recent reports of skin cancers in South Africa are available to allow further comparisons. The photoprotection offered by 263

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Table 2. The percentage of basal cell carcinoma (BCC), squamous cell carcinoma of the skin (SSCC) and cutaneous melanoma (CM) reported to occur on four body sites in male and female black, Asian, coloured and white populations of South Africa, 2000–2004

BCC: Black Asian Coloured White SSCC: Black Asian Coloured White CM: Black Asian Coloured White

Head Male

Trunk Male

Upper limb/ shoulder Male

64.3 66.7 64.6 63.1

15.7 14.3 15.2 16.6

12.9 15.5 13.2 13.1

58.3 48.0 52.5 55.2

14.3 20.0 6.5 5.7

12.0 11.1 19.2 24.5

12.4 33.3 35.6 37.1

Lower limb/ hip Male

Head Female

Trunk Female

Upper limb/ shoulder Female

Lower limb/ hip Female

7.2 3.6 7.1 7.3

68.2 64.6 68.8 67.8

16.5 24.6 12.4 13.3

9.8 6.2 10.6 11.0

5.4 4.6 8.1 7.9

10.7 22.0 27.8 25.3

16.7 10.0 13.3 13.8

47.1 52.9 40.1 37.3

17.3 9.8 8.9 6.8

15.2 7.8 29.3 32.5

20.4 29.4 21.7 23.3

6.9 22.2 24.0 18.2

68.7 33.3 21.2 20.2

8.3 6.3 14.9 13.1

6.6 25.0 24.3 22.8

12.7 31.3 30.4 23.0

72.3 37.5 30.4 41.1

epidermal melanin provides an explanation of why the number of cases is fewer in those with pigmented skin. This endogenous sun protection factor has been calculated as up to 13.4 in African Americans (8). BCC was the most frequent skin tumour in white people, coloureds and Asians, whereas incidences of BCC and SCC were approximately equal in black people. SCCs represented 45% of skin tumours in black people in Kenya (9) and 37% in Nigeria (10), similar to the 40% in our study. It should be noted that oculocutaneous albinism, estimated as 1 in 3900 in the black population of South Africa (11), was not recorded by the NCR: such people are at particularly high risk of developing SCCs of the head and neck and rarely seek medical advice (11). BCCs and SSCCs were about twice as frequent in males as in females in all four groups. The higher incidence of these tumours in males compared with females has been reported previously (12) and could be due to higher sun exposure in men who tend to have more outdoor work and recreation with a larger area of skin exposed than women and who are less likely to use sun protection measures (13). The commonest site for BCCs was the head in all four groups in both sexes, as was also the case for SSCCs (Table 2). In contrast to the latter result, other studies have estimated that SCCs occur about eight times more frequently on non-exposed body sites in black people than in white people (2). In addition to sun exposure, cutaneous sites of chronic scarring and inflammation represent risk factors for the development of SSCC in black people, as

shown in reports from Nigeria and Tanzania (1). These sites may not be as common in black people living in South Africa as in more tropical African countries. Furthermore, the estimated prevalence of HIV-1 in South African black people was about 30% in 2004. Such an infection increases the risk of several cancers such as Kaposi’s sarcoma, and skin cancers are recognized to be more common in immunosuppressed renal transplant recipients than in the general population (14). In a study of HIV-associated cancers in a black population of South Africa, Stein et al. (15) found that there was a significantly increased risk of SSCC in HIV-infected individuals, with a suggested alteration in their site distribution. More than two-thirds of CMs occurred on the lower limb/hip in black males and females, whereas there was a more even distribution over the various body sites in white people, coloureds and Asians. However, as reported elsewhere (1, 2, 4), the lower limb/hip was the predominant site for CM in white women and the trunk in white men. It has been suggested that solar UVR may not be such a significant risk factor for CM in black people as in other phototypes, as shown by the frequent development of tumours on non-exposed sites (palmar, plantar and mucosal surfaces) in black people (2, 4). This was indeed found to be the case in the present study as, when the melanoma subtype was recorded (in about 40% of cases in each of the four population groups), the percentage of acral lentiginous melanoma in the black population was 16.6, compared with 5.4 in the Asian, 1.5 in the coloured and 0.8 in the white populations.

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Photodermatol Photoimmunol Photomed 2014; 30: 262–265 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Skin cancers in South Africa

The average age in years at diagnosis was mid-60s for BCC and SSCC for the four groups and both sexes, except for SSCC in Blacks where it was about 10 years younger in both men and women, perhaps explained by the high prevalence of HIV-1 in this group (15). The mean age for CM in all groups and both sexes was mid-50s. The percentage of cases of melanoma occurring in white people under the age of 40 was 13.9 compared with 11.3 in black people, indicating no substantial population differential in this younger age group. More recent trends in the incidence of BCC, SSCC and CM could not be investigated as the NCR has incomplete data from 2005 until 2011 when cancer became reportable with the formalization of new National Health Regulations. No information was collected on skin cancer deaths for the past 20 years, on the stage of melanoma at the time of diagnosis, and on the body site of the tumour in almost half

of the cases. Under-reporting of BCCs in particular is likely, and the provision of health services is scarce in some parts of South Africa, thus making the reporting of skin cancer uneven. However, despite the paucity of data available currently, it is clear that, although the risk of skin cancer is reduced in pigmented skin, it does exist and, as black people and coloureds comprise almost 90% of the South African population, a considerable health burden is implied. Sun protection and awareness programmes require to be tailored appropriately for all skin phototypes in South Africa (16).

ACKNOWLEDGEMENTS The authors thank the National Cancer Registry of South Africa for making the data for this paper available, and Margaret I. Urban for her review of the manuscript.

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7. Rippey JJ, Rippey E. Epidemiology of malignant melanoma of the skin in South Africa. S Afr Med J 1984; 65: 595– 598. 8. Halder RM, Bridgeman-Shah S. Skin cancer in African Americans. Cancer 1995; 75: s667–s673. 9. Nthumba PM, Cavadas PC, Landin L. Primary cutaneous malignancies in subSaharan Africa. Ann Plast Surg 2011; 66: 313–320. 10. Asuquo ME, Ngim O, Ugare G, Omotoso J, Ebughe G. Major dermatologic malignancies encountered in a teaching hospital surgical department in South Nigeria. Am J Clin Dermatol 2008; 9: 383–387. 11. Hong ES, Zeeb H, Repacholi MH. Albinism in Africa as a public health issue. BMC Public Health 2006; 6: 212. 12. Leiter U, Garbe C. Epidemiology of melanoma and nonmelanoma skin cancer – the role of sunlight. Adv Exp Med Biol 2008; 624: 89–103.

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13. Oberyszyn TM. Non-melanoma skin cancer: importance of gender, immunosuppressive status and vitamin D. Cancer Lett 2008; 18: 127–136. 14. Ho WL, Murphy GM. Update on the pathogenesis of post-transplant skin cancer in renal transplant recipients. Br J Dermatol 2008; 158: 217–224. 15. Stein L, Urban MI, O’Connell D et al. The spectrum of human immunodeficiencyassociated cancers in a South African black population: results from a casecontrol study, 1995–2004. Int J Cancer 2008; 122: 2260–2265. 16. Wright CY, Norval M, Summers B, Davids LM, Coetzee G, Oriowo M. Solar ultraviolet radiation exposure and human health in South Africa: finding a balance. S Afr Med J 2012; 102: 665–666.

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The incidence and body site of skin cancers in the population groups of South Africa.

Data regarding basal cell carcinoma (BCC), squamous cell carcinoma of the skin (SSCC) and cutaneous melanoma (CM) in multiracial populations are spars...
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