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Int. J. Cancer: 67,24-28 (1996)
0 1996 Wiley-Liss, Inc.
Publication of the International Union Against Cancer
Publication de I’Union InternationaleContre le Cancel
SITE DISTRIBUTION OF DIFFERENT TYPES OF SKIN CANCER:
NEW AETIOLOGICAL CLUES
Silvia FRANCESCHI’,
Fabio L E V I ~Lalao
, ~ , RANDIMBISON’
and Carlo LA vECCHIA3
lServizio di Epidemiologia, Centro di Riferimento Oncologico, Aviano, Italy; 2Registre vaudois des tumeurs, Institut universitaire
de mCdecine sociale et priventive, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland; and 31stitutodi Ricerche
Farmacologiche “Mario Negri; ” and Istituto di Statistica Medica e Biometria, Universita degli Studi di Milano, Milan, Italy.
Since the investigation, at an individual level, of lifetime sun
exposure remains difficult, the site distribution of different
types of skin cancer can be an important source of aetiological
clues. The present report deals with I, 149 cases of cutaneous
malignant melanoma (CMM), 7,685 of basal-cell carcinoma
(BCC) and 3,049 of squamous-cell carcinoma (SCC) reported
between 1976 and 1992 to the Vaud Cancer Registry, in
Switzerland. Site- and type-specific age-standardized (on the
world population) incidence rates per IOO.000 population and
per IOO.000 unit surface were computed, together with relative
age-standardized incidence rates (i.e., rates per 100,000 surface
unit in each anatomical site relative to rates for the body as a
whole). The highest rates per unit surface were seen for both
genders in the face, thus indicating some role of cumulative sun
exposure in all skin-cancer types. Relative to the incidence in
the whole body, the excess on the face was, however, more than
20-fold for BCC and SCC, but only 4-fold for CMM. The relative
incidence in males was very much higher for SCC than for CMM
and BCC in the neck, ears and scalp, a heavily sun-exposed area
in men but not in women. Conversely, a substantial lack of SCC
was seen in the trunk. In conclusion, site distribution of different
skin-cancer types suggests that short-duration UV-light exposure is sufficient to increase CMM risk substantially, but has
little influence on SCC risk. With the increase of exposure,
however, SCC rises more steeply than BCC. Age-related behaviour (i.e., another indirect indicator of duration of exposure to
UV light) is consistent with the anatomical distribution of skin
cancer.
o 1996 Wiley-Liss, Inc.
Exposure to ultra-violet (UV) radiation plays a major role in
the aetiology of various skin-cancer types, i.e., cutaneous
malignant melanoma (CMM), basal-cell carcinoma (BCC) and
squamous-cell carcinoma (SCC). The incidence of all major
types of skin cancer has appreciably increased in most white
populations over the last few decades, in parallel with the
increase of sun exposure, chiefly for tanning purposes (Parkin
et al., 1992; Levi et al., 1995). The doses and patterns of sun
exposure most strongly related to the risk of various skincancer types seem, however, to vary substantially.
While SCC is believed to rise steadily with continuous
intense sun exposure (such as occupational exposure) up to
high cumulative dose, the strongest evidence for CMM has
been for recreational or intermittent exposure, and history of
early sunburn (Armstrong, 1988; IARC? 1992). BCC has been
less often studied, but some data indicate that the risk of BCC
may not increase beyond a certain level of sun exposure
(Kaldor et aL, 1993; Kricker et al., 1995a) and may be maximal,
as for CMM, for intermittent exposure (Kricker et al., 19956).
Since the investigation, at an individual level, of various
aspects of lifetime sun exposure, however, remains difficult,
comparison of the site distribution and age pattern of different
types of skin cancer can be an important source of aetiological
clues, especially if based on a large and unselected populationbased series (Levi et al., 1995).
MATERIAL AND METHODS
The data included in the present analysis were derived from
the Vaud Cancer Registry datafile, which includes information
concerning incident cases of malignant neoplasms in the
canton (whose population, according to the 1990 census, was
about 580,000 inhabitants; Levi et al., 1992). Population
estimates were based on decennial censuses (1970, 1980,
1990), and on estimates by the Cantonal Office of Statistics for
each calendar year and 5-year age group, based on official
numbers of births, deaths, immigrations and emigrations.
Notification is based on a voluntary agreement between the
recording medical institutions of the canton and the Registry.
All hospital, pathology laboratories (including those specializing in dermatopathology) and most practitioners are asked to
report all cases of cancer. In this population, specific attention
has traditionally been paid to diagnosis, pathological confirmation and registration of skin neoplasms (Levi et al., 1988,1995).
Most cases are notified repeatedly and from different institutions to the Registry, thus increasing completeness and accuracy of notification.
Information collected by the registry includes general demographic characteristics of the patient (age, gender, municipality of residence), site and histological type according to the
standard International Classification of Diseases for Oncology
(ICD-0; WHO Health Organization, 1976), and time of
diagnostic confirmation.
The present series comprises 11,883 incident, histologically
verified skin-cancer primaries (6,046 males and 5,837 females)
registered from 1976 to 1992. Multiple skin tumours (either
synchronous or metachronous) are classified by the site of the
first recognized tumour of the same morphological type. For
the present report, cases were grouped into the following 3
morphological categories: (1) malignant melanoma (ICD-0
M: 8720-8790, excluding 8742.2, lentigo maligna, but including
8742.3, lentigo maligna melanoma, n = 1,149); (2) basal-cell
(ICD-0 M: 809CL8095, n = 7,685), and (3) squamous-cell
(ICD-0 M: 8070-8076, n = 3,049) carcinoma. Cancers whose
histological type was other or unspecified (n = 378, 3.1%)
were not considered, nor were cancers arising from skin of
genital organs (e.g., labia majora or minora, vulva, penis or
scrotum (ICD-0 T: 184, 187). The following 5 topographical
categories were considered: (1) face (ICD-0 T: 173.0-.l, .3);
(2) neck, ears and scalp (ICD-0 T: 173.2, .4); (3) trunk
(ICD-0 T: 173.5); (4) upper limbs, including shoulders (ICD-0
T: 173.6, and (5) lower limbs (ICD-0 T: 173.7). Skin cancers
whose anatomical sub-site was not specified (2%) were not
considered.
Site- and type-specific, age-standardized (world standard
population as reference population) incidence rates per 100,000
population were calculated. Site-specific rates were also computed per 100,000 unit surface, where the unit is the proportion of total skin surface area for each anatomical site (Green
jTo whom correspondence and reprint requests should be sent, at
Registre vaudois des tumeurs, Institut universitaire de mkdecine
sociale et prtventive, Centre Hospitalier Universitaire Vaudois, Falaises l, 1011 Lausanne, Switzerland. Fax: (41) 21 323-03-03.
Received: January 6,1996 and in revised form March 11,1996.
25
SITE DISTRIBUTION OF SKIN CANCER
TABLE I - NUMBER OF CASES AND AGE-STANDARDIZED (WORLD) INCIDENCE RATES OF DIFFERENT
TYPES OF SKIN CANCER PER 100 000 POPULATION AND PER UNIT SURFACE AREA PER 100,000IN VAUD,
SWITZERLAND, IN 1976-1992. BY GENDER AND ANATOMICAL SITE
Males
Females
Site
Cutaneous
malignant
meIanoma
Face
Neck, ears
and scalp
Upper limbs
and shoulders
Trunk
Lower limbs
Whole body*
Basal-cell carcinoma
Face
Neck, ears
and scalp
Upper limbs
and shoulders
Trunk
Lower limbs
Whole body*
Squamous-cell
carcinoma
Face
Neck, ears
and scalp
Upper limbs
and shoulders
Trunk
Lower limbs
Whole body*
60
44
0.9
0.6
37.4
9.7
104
26
1.o
0.3
42.5
4.7
0.9
2.1
78
1.3
6.7
124
1.8
9.3
0.7
252
73
507
4.2
1.3
8.3
13.0
3.3
132
256
642
2.2
3.9
9.1
6.7
9.8
1.9
0.3
0.9
2247
517
33.3
7.4
1449.4
112.2
2520
377
28.5
3.9
1237.6
59.0
1.2
1.9
20 1
3.1
16.1
131
1.7
8.9
1.8
798
93
3856
12.0
1.3
57.1
37.4
3.3
639
162
3829
8.4
1.8
44.3
26.3
4.6
1.4
0.7
1.3
852
500
11.6
6.3
504.4
95.0
896
102
8.1
1.0
352.7
15.3
1.4
6.2
191
2.5
13.2
188
1.7
9.1
1.5
93
47
1.3
0.7
4.2
1.7
76
104
1366
0.8
1.0
12.7
2.6
2.6
1.6
0.7
1.8
1683
~...
22.4
~~
*Sites "other or unspecified" excluded.
et al., 1993). Briefly, for a specific site, rates per unit surface
were calculated by dividing the rates for each 5-year age group
and each gender group by the proportion of the total surface
area of the body occupied by that site (Pearl and Scott, 1986).
For example, for trunk, each age-specific rate was divided by
0.29 because the trunk (comprising trunk/back, trunk/front
and buttocks) is estimated as 29% of the total body surface
area. In addition, age-standardized incidence rates per 100,000
units were also calculated, separately for each gender, topographical category and morphologic group, relative to incidence rate for the body as a whole (set to unity) (Doll and
Smith, 1982; Green et al., 1993).
RESULTS
Table I gives the number of cases, and the corresponding
age-standardized (world population) incidence rate per unit
surface for each histotype, site and gender. Obviously, for
whole body, rates per los and per unit surface per los are
identical. CMM rates per 100,000 were highest in the trunk for
males (4.2/100,000) and in the lower limbs for females (3.9/
100,000). However, when expressed per unit surface, the
highest rates were in the face for both genders (37.4/100,000
males, 42.5/100,000 females). In females, rates per unit surface in lower and upper limbs were similar (9.8 and 9.3 per unit
surface per 100,000 respectively), whereas in males the rates
TABLE 11 - IIAI'IOS 01, AGt:-STASDARDIZED (WORLD) IIVC'IDESC'E
IIAI'ES OF l)lI.'I:FRFKTTYPF.S O F SKIK ('AKC'EK I'EK UNIT SUKk'ACL:
AIIEA AND 100.000 POPUl ATION IN VAI'D. SWIl'ZEKLAND. I N l Y 7 h - l Y Y ? .
BY GENDER AND ANATOMICAL SITE
Site
Face
Neck, ears and scalp
Upper limbs and
shoulders
Trunk
Lower limbs
Whole bodv
Males
Females
CMMISCC BCCiSCC CMMISCC BCCISCC
0.07
0.10
0.51
2.9
1.2
1.2
0.12
0.31
1.0
3.5
3.9
1.0
3.1
1.9
0.37
8.9
1.9
2.6
2.6
3.8
0.73
10.1
1.8
3.5
were higher in the upper limb. With reference to BCC, by far
the highest incidence was observed in the face for both genders
(1449/100,000 and 1238/100,000 per unit surface per 100,000
in males and females respectively), followed by neck, ears and
scalp (112.2 and 59.0 per unit surface per 100,OOO in males and
females respectively) and the trunk. Also for SCC the highest
incidence site was the face in both genders (504.4 and 352.7,
respectively, per unit surface per lOO,OOO), followed in both
genders by the neck, ears and scalp (95.0 and 15.3 per unit surface
per 100,000 in males and females), and by the upper limbs and
shoulders. Site-specific male-to-female ratios were rather consistent in different skin-cancer types except for cancers of the
26
FRANCESCHI ETAL.
CMM . MALES
w
. FEMALES
T
v
Q
CMM
5
4.57
4.40
Lower limb
Upper limb
Neck
Trunk
Neck
F2Ce
Trunk
Upper Limb
BCC FEMALES
BCC - MALES
Trunk
Neck
SCC MALES
~
Lower Limb
FW3
-
27.56
r
T
v
U p p r Limb
Face
~
22.20
Lower Limb
Lower Limb
Upper Limb
Trunk
Neck
SCC .FEMALES
FUa
27.55
22.20
4.19
5
4
3
2
1
0.07
0
Lower Limb
Trunk
Upper Limb
Neck
FKa
BODY SITE
Lower Limb
Trunk
Upper Limb
Neck
FaCe
BODY S I E
FIGURE
1 - Incidence rates of CMM, BCC and SCC by body site relative to those for the whole body, by gender. Vaud, Switzerland,
1976-1992. Site-specific rates are age-adjusted (world population); those for the whole body are set to 1 for each gender.
neck, ears and scalp, where the male-to-female ratio was approximately 2 for CMM and BCC, but over 6 for SCC (Table I).
The ratios of age-standardized incidence rates per unit
surface between CMM and SCC and between BCC and SCC in
each sex are given in Table 11. For the whole body the ratio
CMM/SCC was 0.37 for males but 0.73 for females. At specific
sites, it ranged between 0.07 in the face and 3.1 in the trunk for
males, and between 0.12 in the face and 3.8 in the lower limbs
in females. The overall BCC/SCC ratio was 2.6 for males and
3.5 for females. In specific sites, it ranged for males between
SITE DISTRIBUTION OF SKIN CANCER
1.2 in the neck, ears and scalp and the upper limbs and
shoulders and 8.9 in the trunk, and, for females, between 1.0 in
the upper limbs and shoulder and 10.1 in the trunk.
Figure 1gives the age-standardized incidence rates per unit
surface per 100,000 in specific body sites relative to the whole
body for each gender, site and histotype. Relative incidence of
BCC and SCC shows very similar patterns, with more than
20-fold excess in the face compared with total body. Relative
incidence rates per unit surface below 1 were found for all
other sites except neck and ears and scalp. With respect to
these latter sites, however, a 4-fold higher incidence of SCC in
the male neck was observed. Rates per unit showed a much
smaller variation for CMM, with rates in the face about 4-fold
higher than in the whole body in both genders. Relative CMM
incidence below 1 could be found for lower and upper limbs in
males, and neck, ears and scalp and trunk in females, whereas
trunk in males showed a 53% excess.
Figure 2 illustrates the age- and gender-specific incidence
curves for each skin-cancer histological type and gender. CMM
increased much less steeply than BCC and SCC with age.
Absence of SCC, as compared with BCC, emerged in young
and middle-aged adults of both genders. At older age, SCC
incidence in males approached that of BCC, and, in contrast to
BCC, showed no tendency to plateau. Site-specific age curves
were also examined. They were consistent with those of the
whole-body curves and are, therefore, not shown.
DISCUSSION
The present incidence rates are consistent with previous
reports (i.e., highest frequency of CMM in the trunk in males
and lower limbs in females, and on the face for BCC and SCC
in both genders) (Magnus, 1991). Incidence rates per unit
surface have rarely been assessed (Pearl and Scott, 1986;
0sterlind et al., 1988; Green et al., 1993), but disclose a
somewhat different pattern, with face being the highest incidence area also for CMM, although to a lesser extent than for
BCC and SCC. This cannot be attributed to the high frequency
on the face of lentigo-maligna lesions (which were excluded)
or lentigo-maligna melanomas (which represented only 8% of
CMM), and indicates some role of cumulative sun exposure for
all 3 major skin-cancer types.
In terms of relative incidence per unit surface, as compared
with total body incidence (for which, obviously, incidence per
lo5 and incidence per unit surface coincide), not only do the 3
major types of skin cancer differ substantially with respect to
the face, where BCC and SCC relative excess is about 5-fold
BCC - M
l0O0T
SCC F
~
100
=
CMM - F
10
1
l-
27
greater than that of CMM, but also to the neck, ears and scalp,
sites more frequently sun-exposed in males than in females. In
males, the relative excess compared with other body sites is
similar for CMM and BCC, but 2-to-3 fold greater for SCC.
Although relative incidence per unit surface is not a completely new measure, it has been rarely used. Site-specific rates
per 100,000 individuals have been generally preferred, leading,
however, for instance, to some under-estimation of the incidence of CMM on the face (the surface of which is relatively
small) as compared with the lower limbs.
Comparison of skin types at specific sites (with SCC as a
reference, on account of the better understood UV-lightrelated risk pattern; Council for Scientific Affairs, 1989)
showed that CMM/SCC ratios ranged from around 0.1 in the
face to around 4 in the limbs in females and 3 in the trunk in
males. The comparison between BCC and SCC showed ratios
between about 1 (neck, ears, and scalp in males and upper
limbs and shoulders in both genders) and 9-10 in the trunk.
Intermediate ratios of BCC/SCC were found for the face
(Moan and Dahlback, 1992; Kaldor et al., 1993).
Anatomic sites can be considered as indirect indicators of
different patterns of UV-light exposure, with respect to lifetime duration, intensity and intermittency of exposure. Age is
another indicator of duration of exposure. The relatively high
incidence rates of CMM in rarely sun-exposed areas and in
young individuals suggest that short-duration UV-light exposure is sufficient to increase cancer risk substantially. SCC risk
rises more steeply with age than BCC, also in the absence of a
major cohort effect (Marks et al., 1993; Levi et al., 1995). Very
low SCC incidence rates for short exposures ( e g , individuals
below age 30 and sites other than the face and, in males, scalp,
ears and neck) also suggest lack of tangible risk increase below
a certain threshold and/or latent period. The age-pattern of
SCC is consistent with that of most common non-cutaneous
cancers. Indeed, SCC may arise in any epithelium (Stoll and
Schwartz, 1987). Conversely, BCC virtually never arises from
stratified squamous epithelium other than the skin. It derives
from the immature basal cells of the epidermis and always
contains epidermal cellular and dermal stromal components
(Carter, 1987). Very often, BCC starts in the epithelium of
pilosebaceous follicles, thus partly explaining the anatomic
distribution of BCC (eg., relatively high frequency in the
trunk).
Unfortunately, the present descriptive data do not allow a
distinction to be made between short-duration exposure and
intermittent exposure, i.e., the type of exposure putatively
more dangerous for CMM (IARC, 1992) and BCC (Kricker et
al., 19956). Furthermore, some under-reporting of skin cancer
has probably occurred, although this cannot be quantified, and
may have been somewhat different for various histological
types, sites and age groups. Nevertheless, the present site- and
age-specific incidence rates are derived from a population
under particularly careful surveillance (Levi et al., 1988, 1995),
as confirmed by the comparatively high incidence of all types of
skin cancer in this population (Levi et aL, 1992, 1993). Apart
from important similarities in risk factors for all skin-cancer
types (ix.,skin phenotype, IARC, 1992; immunological deficiencies, Adami et al., 1995; exposure to chemicals, Stoll and
Schwartz, 1987; and, possibly, human papillomavirus, Shamanin and de Villiers, 1995), different sun-related risk patterns
are suggested by the site distribution, as well as type of
increase with age, of CMM, BCC and SCC.
-1'7-,*'
,.=..,,,'
,
;
:
;
;
:
:
:
:
:
:
20- 25- 30- 35- 4 0 - 4 5 - 5 0 - 5 5 - 6 0 - 6 5 - 7 0 - 75- 8 0 AGE GROUP
FIGURE
2 - Age-specific incidence curves for CMM, BCC and
SCC by gender. Vaud, Switzerland, 1976-1992.
ACKNOWLEDGEMENTS
The contributions of the Swiss League against Cancer
(Grant FOR 368.89.3), and of the Vaud Cancer Registry's staff
are gratefully acknowledged.
28
FRANCESCHI E T A L
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