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Research

JAMA Dermatology | Original Investigation

Anatomical Distributions of Basal Cell Carcinoma and


Squamous Cell Carcinoma in a Population-Based Study
in Queensland, Australia
Padmini Subramaniam, MBBS, MSc, MClinSc; Catherine M. Olsen, PhD, MPH; Bridie S. Thompson, PhD;
David C. Whiteman, MBBS, PhD; Rachel E. Neale, BVSc, PhD; for the QSkin Sun and Health Study Investigators

Supplemental content
IMPORTANCE Keratinocyte cancers (KCs), including basal cell carcinoma (BCC) and squamous
cell carcinoma (SCC), are the most common cancers among fair-skinned populations
worldwide. Although studies have indicated that the anatomical distribution of BCC and SCC
differ, few have compared them directly in well-defined population samples.

OBJECTIVES To describe and compare the anatomical distribution of BCC and SCC in a
population-based sample in Queensland, Australia.

DESIGN, SETTING, AND PARTICIPANTS This study was nested within the population-based
QSkin Sun and Health Study in Queensland, Australia. Of 37 103 study participants linked to
national medical insurance records, 3398 diagnosed with KCs from September 1, 2010, to
September 30, 2012, were identified, and information about their KCs was extracted from
pathology reports. Data were analyzed from January 1, 2013, to March 30, 2016.

MAIN OUTCOMES AND MEASURES The relative tumor densities (RTDs) on defined body sites,
calculated by dividing the proportion of tumors occurring at a specified site by the proportion
of skin area of that site.

RESULTS A total of 5150 KCs with complete data were identified in 2374 study participants
(1339 men [56.4%] and 1035 women [43.6%]; mean [SD] age, 59.7 [7.4] years). Of these,
3846 KCs (74.7%) were BCCs. Most BCCs were on the head and/or neck (1547 [40.2%]) and
the trunk (1305 [33.9%]); most SCCs were on the head and/or neck (435 [33.4%]) and upper
limbs (455 [34.9%]). The greatest differences in RTDs between BCC and SCC were on the
hand (BCC:SCC ratio, 1:14) and the back and/or buttocks (BCC:SCC ratio, 8:1). Relative tumor
densities of KCs were higher on the scalp and ear in men compared with women, and on the
upper arm in women compared with men. The pattern of RTDs did not differ with age for
BCC. Compared with younger adults (40-54 years), the RTDs in older adults (55-69 years)
were 2-fold higher for SCC on the scalp (0.38 [95% CI, 0.00-0.81] vs 1.07 [95% CI, 0.75-1.38])
and the back and/or buttocks (0.05 [95% CI, 0.00-0.12] vs 0.12 [95% CI, 0.07-0.16]).

CONCLUSIONS AND RELEVANCE The high RTDs on sun-exposed body sites for BCC and SCC
are in keeping with sun exposure as the primary etiologic factor for both tumors. However, for
BCC, the low RTD on the hand and high RTDs on less sun-exposed sites suggest a complex
association between sun exposure and occurrence of BCC. Knowledge about the anatomical
distribution of BCC and SCC may provide insight into their diagnoses and causes. Author Affiliations: Author
affiliations are listed at the end of this
article.
Group Information: Members of the
QSkin Sun and Health Study are listed
at the end of the article.
Corresponding Author: Padmini
Subramaniam, MBBS, MSc, MClinSc,
Department of Population Health,
QIMR Berghofer Medical Research
Institute, Locked Bag 2000, Royal
Brisbane Hospital, Brisbane,
QLD 4029, Australia
JAMA Dermatol. 2017;153(2):175-182. doi:10.1001/jamadermatol.2016.4070 (padmini.subramaniam
Published online November 23, 2016. @qimrberghofer.edu.au).

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Research Original Investigation Anatomical Distributions of Skin Cancers in Queensland, Australia

B
asal cell carcinoma (BCC) and squamous cell carci-
noma (SCC), collectively termed keratinocyte cancers Key Points
(KCs), are the most common cancers among fair-
Question How great are the differences in anatomical
skinned populations worldwide. Australia has the highest distributions of basal cell carcinoma (BCC) and squamous cell
incidence,1 with approximately 434 000 people (or nearly 2% carcinoma (SCC)?
of the population) estimated to have been diagnosed with KCs
Findings In this population-based study, the anatomical
in the calendar year 2008.2 The cost of managing KCs in Aus-
distribution of 3398 keratinocyte cancers arising during 2 years of
tralia was projected to reach A$703 million (US $536 million) follow-up of 37 103 Australians consisted of BCCs primarily on the
in 2015.3 head and neck and trunk and SCCs predominantly on the upper
Although UV radiation is the major risk factor for BCC and limbs and head and neck. Sites with the greatest discrepancy in
SCC, their anatomical distributions differ. Squamous cell car- relative tumor densities between BCC and SCC were the hand and
cinoma occurs primarily on sites habitually exposed to sun- back and buttocks.
light, such as the face and exposed parts of the upper and lower Meaning Basal cell carcinoma and SCC have high relative tumor
limbs, whereas BCC occurs on these sites and those less fre- densities on the head, consistent with sun exposure as the primary
quently exposed to sunlight, such as the trunk.4-15 etiologic factor; however, for BCC, the low relative tumor densities
Most studies report the proportion of tumors on speci- on the hand and high relative tumor densities on less sun-exposed
sites suggest a complex association with sun exposure.
fied body sites without taking into account the proportion of
surface area of the defined body site, which prevents direct
comparison of tumor burden across different anatomical sites.
A few studies have reported the relative tumor density held by Medicare Australia records medical billing events for
(RTD),5,6,16-19 calculated as the ratio of the proportion of tu- KCs and the type of procedure undertaken, but no details about
mors at a specific anatomical site to the proportion of skin sur- histologic type or specific anatomical site are recorded. We
face area at that site, or have reported surface area–adjusted therefore obtained the corresponding pathology reports for
incidence rates.5-7 These studies5,6,17,18 showed that the high- each treatment event by linking our QSkin data set to pathol-
est RTDs occurred on the face for both cancers, but analysis ogy service providers for those participants identified from the
of facial subsites has been limited. Medicare Australia data as having had KC treatments.
Some studies suggest that the body site distribution of BCC The diagnosis, treatment procedures, and anatomical site
and SCC varies with age and sex,5,17,18 although few studies have of each tumor were manually abstracted from the pathology
compared both tumor types from 1 population sample. Given reports. We included only primary BCCs and SCCs; recurrent
the relatively small number of studies reported to date, the aim lesions, defined as the regrowth of a previously treated ma-
of our study was to compare the anatomical distribution of BCC lignant neoplasm, were excluded. Thus, we cross-checked all
and SCC arising in participants from a large, population- biopsies, excisions, and reexcisions of apparently multiple BCC
based cohort in Queensland, Australia, and to investigate or SCC lesions diagnosed within a 6-month period on the same
differences according to age and sex. anatomical site in the same person in Medicare Australia rec-
ords and pathology reports and omitted verified recurrent le-
sions from our analysis.

Methods
Analysis
This study is nested within the QSkin Sun and Health Study, Data were analyzed from January 31, 2013, to March 30, 2016.
which consists of 43 794 residents of Queensland, Australia. We were able to match 65% of individual Medicare Australia
Participants aged 40 to 69 years were randomly selected from claims for KC treatment (72.1% of people) with pathology re-
the Australian electoral roll (enrollment to vote is compul- ports. The median follow-up duration of the participants was
sory) and recruited in 2010. They completed a survey that in- 12.6 (range, 4.0-19.8) months. Almost all lesions for which we
cluded questions about ancestry, lifestyle, skin phenotype, past had pathology reports (99.5%) had complete information on
treatment of skin lesions, and sun exposure history. Details of body site and histologic findings and were included in the
the survey have been published previously.20 This study was analysis. To allow for differences in the skin surface area at dif-
approved by the human ethics committees of the QIMR Berg- ferent body sites, the RTD for each body site was calculated
hofer Medical Research Institute and Queensland University by dividing the proportion of tumors at a defined anatomical
of Technology, Brisbane, Queensland. All participants pro- site by the mean proportion of the skin surface area of that
vided written informed consent for linkage of records with the site.16 An RTD of 1 corresponds to the density of tumors on the
Medicare Australia database. whole body.
Through record linkage to Medicare Australia, Australia’s The proportion of the surface area of skin attributed to each
national health insurance scheme, we identified participants body site was based on the estimated proportion of surface area
in the QSkin cohort who had been treated for skin cancer from described by Lund and Browder.21 We classified body sites into
September 1, 2010, to September 30, 2012. Medicare Austra- 4 broad areas—head and/or neck, trunk (including shoul-
lia subsidizes health care for all Australians and records infor- ders), upper limbs, and lower limbs—that constituted 9.0%,
mation about medical services to Australian residents, ex- 32.0%, 19.0%, and 40.0% of the skin surface, respectively.
cept for some services delivered in public hospitals. The data These 4 body sites were further subdivided into subsites as

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Anatomical Distributions of Skin Cancers in Queensland, Australia Original Investigation Research

Table 1. Proportions, RTDs, and BCC:SCC Ratio by Body Site


BCC Lesions SCC Lesions
(n = 3846) (n = 1304)
Body Surface BCC to SCC Ratio
Body Site Area, % No. (%) [95% CI] RTD (95% CI)a No. (%) [95% CI] RTD (95% CI)a (95% CI)
Head and/or neck 9.0 1547 (40.2) [39-42] 4.47 (4.30-4.64) 435 (33.4) [31-36] 3.71 (3.42-3.99) 1.2 (1.1-1.3)
Scalp 3.7 89 (2.2) [2-3] 0.63 (0.50-0.75) 46 (3.5) [3-5] 0.95 (0.68-1.22) 0.7 (0.5-0.9)
Ears 0.5 138 (3.6) [3-4] 7.18 (6.00-8.35) 54 (4.1) [3-5] 8.28 (6.12-10.45) 0.9 (0.6-1.2)
Face 2.4 1086 (28.2) [27-30] 11.77 (11.17-12.36) 295 (22.6) [20-25] 9.43 (8.48-10.37) 1.3 (1.1-1.4)
Most exposedb 1.3 712 (18.5) [17-20] 14.24 (13.30-15.18) 213 (16.6) [14-18] 12.56 (11.02-14.11) 1.1 (1.0-1.3)
Less exposedc 1.3 384 (10.0) [9-11] 7.68 (6.95-8.41) 107 (8.2) [7-10] 6.31 (5.17-7.46) 1.2 (1.0-1.5)
Least exposedd 0.3 129 (3.4) [3-4] 11.18 (9.28-13.08) 29 (2.2) [1-3] 7.41 (4.75-10.08) 1.5 (1.0-2.2)
Neck 2.4 234 (6.1) [5-7] 2.54 (2.22-2.85) 40 (3.1) [2-4] 1.28 (0.89-1.67) 2.0 (1.4-2.8)
Trunk 32.0 1305 (33.9) [32-35] 1.06 (1.01-1.11) 109 (8.4) [7-10] 0.26 (0.21-0.31) 4.1 (3.4-4.9)
Chest and/or 13.0 647 (16.8) [15-18] 1.29 (1.20-1.38) 83 (6.4) [5-8] 0.49 (0.39-0.59) 2.6 (2.1-3.3)
abdomen
Back and/or 19.0 658 (17.1) [16-18] 0.90 (0.84-0.96) 26 (2.0) [1-3] 0.10 (0.07-0.14) 8.6 (5.8-12.6)
buttocks
Upper limbs 19.0 528 (13.7) [13-15] 0.72 (0.67-0.78) 455 (34.9) [32-37] 1.84 (1.70-1.97) 0.4 (0.4-0.4)
Upper arm 8.0 234 (6.1) [5-7] 0.76 (0.67-0.85) 56 (4.3) [3-5] 0.54 (0.40-0.67) 1.4 (1.1-1.9)
Forearm 6.0 257 (6.7) [6-8] 1.11 (0.98-1.25) 223 (17.1) [15-19] 2.85 (2.51-3.19) 0.4 (0.3-0.5)
Hande 5.0 37 (1.0) [1-1] 0.19 (0.13-0.25) 176 (13.5) [12-15] 2.70 (2.33-3.07) 0.1 (0.1-0.1)
Lower limbs 40.0 466 (12.1) [11-13] 0.30 (0.28-0.33) 305 (23.4) [21-26] 0.58 (0.53-0.64) 0.5 (0.5-0.6)
Thigh 19.0 67 (1.7) [1-2] 0.09 (0.07-0.11) 30 (2.3) [1-3] 0.12 (0.08-0.16) 0.8 (0.5-1.2)
Lower leg 14.0 377 (9.8) [9-11] 0.70 (0.63-0.77) 258 (19.8) [18-22] 1.41 (1.26-1.57) 0.5 (0.4-0.6)
Footf 7.0 22 (0.6) [0-1] 0.08 (0.05-0.12) 17 (1.3) [1-2] 0.19 (0.10-0.27) 0.4 (0.2-0.8)
All 100 NA NA NA NA NA
d
Abbreviations: BCC, basal cell carcinoma; NA, not applicable; RTD, relative Includes under eyebrow, upper and lower eyelids, medial and lateral canthus,
tumor density; SCC, squamous cell carcionoma. and nasolabial fold.
a e
Calculated as the ratio of the proportion of tumors at a specific anatomical site Includes back of hand, palmar skin, and fingernail.
to the proportion of skin surface area at that site. f
Includes dorsum of foot, toes, plantar skin, and toenail.
b
Includes ears, nose, cheeks, and lips.
c
Includes forehead, eyebrows, chin, jaw, temple, and preauricular area.

shown in Table 1. The classification of facial subsites accord- (1346 men [56.4%] and 1041 women [43.6%]; mean [SD] age,
ing to their sun exposure was adapted and modified from 59.7 [7.4] years). Participants with available histopathologic
previous studies5,6 as follows: most exposed included the data were similar with respect to age and sex to those with-
ears, nose, cheeks, and lips; less exposed, the forehead, eye- out available data.
brows, chin, jaw, temple, and preauricular area; and least ex- Most participants reported having white European ances-
posed, under the eyebrow, upper and lower eyelids, medial and try (2327 [97.5%]) and 1473 (68.3%) had lived longest as a
lateral canthus, and nasolabial fold. child or youth in the north and central regions (10°S-30° S
We calculated the RTDs and 95% CIs for BCC and SCC over- parallels) of Australia. For skin characteristics, 1820 partici-
all and within the strata of sex and age groups (40-54 and 55-69 pants (76.3%) had fair skin, 2265 (94.9%) reported that their
years). We calculated the ratio of RTDs for BCC to SCC for each skin burned after exposure to 30 minutes of midday sun, and
anatomical site and 95% CIs of these ratios, overall and within 2079 (87.1%) reported that they tanned after long-term sun
strata of age and sex.22 Statistical analysis was conducted using exposure.
SAS (version 9.4; SAS Institute, Inc) and Excel (Microsoft) From the pathology reports, we identified 5189 primary
software. KC lesions in 2387 participants. We excluded 39 BCCs and SCCs
from 13 participants with missing site information. Of the 5150
KCs from 2374 participants included in the final analysis, 3846
(74.7%) were BCCs. Of these, 3233 lesions (62.8%) were treated
Results in men and 2891 (57.3%) were treated in people aged 60 to 69
Of the 43 794 QSkin participants, 39 033 consented to link- years. Among the participants with a histologically con-
age with Medicare and 37 103 were linked to the Medicare firmed BCC or SCC, 806 (42.6%) had multiple BCCs (range, 2-40
Australia database (Figure 1). Of these, we identified 3398 lesions), and 223 (28.1%) had multiple SCCs (range 2-8 le-
participants who were treated for KCs during the study sions). Three hundred eight participants (12.9% of those with
period. Histopathology reports for at least 1 KC lesion were KC) had both BCC and SCC. Of those with BCC, 16.3% also had
retrieved and matched for 2387 of these participants (70.2%) SCC, and of those with SCC, 38.7% also had BCC.

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Research Original Investigation Anatomical Distributions of Skin Cancers in Queensland, Australia

Anatomical Distribution of BCC and SCC limbs (34.9%) and head and/or neck (33.4%) (Table 1 and
The most commonly diagnosed sites of the 3846 identified Figure 2). Although the differences in the proportion of le-
BCCs were on the head and/or neck (40.2%) and trunk (33.9%). sions on the most commonly affected sites were small, we
The 1304 SCCs occurred with similar frequency on the upper found marked differences in the RTDs once we accounted for
the surface area of these sites (Table 1, Figure 2, and Figure 3).
Figure 1. Outline of Data Collection Process for the Study Participants For BCCs, highest RTDs were observed on the head and/or neck
(RTD, 4.47; 95% CI, 4.30-4.64), which was 4 times higher than
43 794 Participants in QSkin cohort on the trunk, the second most commonly affected site (RTD,
1.06; 95% CI, 1.01-1.11). Similarly, SCCs occurred at highest
39 033 (89.1%) Consent for Medicare density on the head and/or neck region (RTD, 3.71; 95% CI, 3.42-
Australia linkage
3.99), which was twice as high as that on the upper limbs (RTD,
1.84; 95% CI, 1.70-1.97).
37 103 (95.1%) Linkage with Medicare
Australia data
Subsites with the highest RTDs for BCC were the most
(14.24; 95% CI, 13.30-15.18) and least (11.18; 95% CI, 9.28-
13.08) sun- exposed face. The lowest RTD s for BCC
3398 (9.2%) Treated for keratinocyte
cancersa, b were observed on the foot (0.08; 95% CI, 0.05-0.12), thigh
(0.09; 95% CI, 0.07-0.11), and hand (0.19; 95% CI,
2387 Participants (5189 lesions) with 0.13-0.25). Sites with the highest RTDs for SCC were the
histology reports diagnosing most sun-exposed face (12.56; 95% CI, 11.02-14.11) and ears
keratinocyte cancersc
(8.28; 95% CI, 6.12-10.45). The lowest RTDs of SCC were
observed on the back and/or buttocks (0.10; 95% CI, 0.07-
2374 Participants (5150 lesions) 13 Participants (39 lesions) with 0.14), thigh (0.12; 95% CI, 0.08-0.16), and foot (0.19; 95%
with complete data incomplete data (not included) CI, 0.10-0.27).
The greatest disparity in RTD was seen on the hand, for
which the RTD for SCC was 14 times higher than that for BCC
3846 (74.7%) Lesions are BCC 1304 (25.3%) Lesions are SCC
(2.70 [95% CI, 2.33-3.07] vs 0.19 [95% CI, 0.13-0.25]). At the
other extreme, BCCs occurred on the back and/or buttocks at
The number of basal cell carcinoma (BCC) (n = 3846) and squamous cell
a more than 8-fold higher RTD (0.90; 95% CI, 0.84-0.96) than
carcinoma (SCC) (n = 1304) lesions included in the analysis was derived from
participants recruited for the QSkin Sun and Health Study, who gave consent for SCCs (0.10; 95% CI, 0.07-0.14) (Table 1). Overall, RTDs for SCC
linkage with Medicare Australia, were treated for keratinocyte cancers, and had on the upper and lower limbs were almost twice those of BCC,
histologic verification of BCC and SCC. whereas BCCs were twice as dense as SCCs on the neck and
a
Includes excision and destructive therapies. chest and/or abdomen. For participants with multiple le-
b
Includes treatment for BCC, SCC, intraepidermal carcinoma, and sions, the RTDs on the body sites followed a similar pattern of
keratoacanthoma.
c
distribution to the overall distribution of lesions (eTable 1 in
Includes BCC and SCC only.
the Supplement).

Figure 2. Relative Tumor Densities of Basal Cell Carcinoma (BCC) and Squamous Cell Carcinoma (SCC) by Body Sites

15
14
BCC broad area
13
12 BCC subsite
11
Relative Tumor Density

SCC broad area


10
SCC subsite
9
8
7
6
5
4
3
2
1
0
All Scalp Ears Overall Most Less Least Neck All Chest Back All Upper Forearm Hand All Thigh Lower Foot
Subsites Face Exposed Exposed Exposed Subsites and/or and/or Subsites Arm Subsites Leg
Faces Face Face Abdomen Buttocks

Head and/or Neck Trunk Upper Limb Lower Limb

Body Sites

Relative tumor density is calculated as the ratio of the proportion of tumors at a trunk, upper limbs, and lower limbs) for BCC and SCC and for their respective
specific anatomical site to the proportion of skin surface area at that site. subsites.
Distribution is shown for the 4 broad areas of body sites (head and/or neck,

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Anatomical Distributions of Skin Cancers in Queensland, Australia Original Investigation Research

Figure 3. Relative Tumor Densities (95% CIs) of Basal Cell Carcinoma (BCC) and Squamous Cell Carcinoma (SCC)
at Different Body Sites

A Basal cell carcinoma B Squamous cell carcinoma


Head and/or neck
Upper limbs

4.47 (95% CI, 4.30-4.64) 3.71 (95% CI, 3.42-3.99) Trunk


Lower limbs
1.06 (95% CI, 1.01-1.11) 0.26 (95% CI, 0.21-0.31)

0.72 (95% CI, 0.67-0.78) 1.84 (95% CI, 1.70-1.97)


Relative tumor density is calculated
as the ratio of the proportion of
tumors at a specific anatomical site to
the proportion of skin surface area at
that site. Body maps show the
0.30 (95% CI, 0.28-0.33) 0.58 (95% CI, 0.53-0.64) relative tumor densities of BCC and
SCC according to the following body
site classifications: head and/or neck
(total body surface area, 9.0%), trunk
(total body surface area, 32.0%),
upper limbs (total body surface area,
19.0%), and lower limbs (total body
surface area, 40.0%).

Sex Differences in the Anatomical Distribution Among younger participants, the RTD of BCC on the scalp
of BCC and SCC was higher than the RTD of SCC on the scalp (0.84 [95% CI,
For BCC, we found little difference between men and women 0.56-1.13] vs 0.38 [95% CI, 0.00-0.81]), whereas the opposite
in the RTDs overall, except that the relative density of BCCs was observed among older participants (0.54 [95% CI, 0.40-
on the ears and scalp were 3.7-fold (2.68 [95% CI, 1.51-3.84] vs 0.68] vs 1.07 [95% CI, 0.75-1.38]). On the back and buttocks,
10.03 [95% CI, 8.27-11.80]) and 1.6-fold (0.45 [95% CI, 0.28- the RTD of BCC compared with SCC was 18-fold higher among
0.63] vs 0.74 [95% CI, 0.56-0.91]), respectively, higher in men younger participants (0.91 [95% CI, 0.79-1.03] vs 0.05 [95% CI,
than in women. In contrast, BCCs occurred 80% more fre- 0.00-0.12]), but just more than 7-fold higher among older
quently (in relative terms) on the upper arms of women than participants (0.90 [95% CI, 0.82-0.97] vs 0.12 [95% CI,
men (RTDs, 1.05 [95% CI, 0.87-1.22] vs 0.58 [95% CI, 0.47- 0.07-0.16]).
0.69]). The occurrence of BCC on the face was marginally higher
in women than men (13.61 [95% CI, 12.14-14.49] vs 10.60 [95%
CI, 9.68-11.33]); this was most marked on the least exposed
areas of the face (13.83 [95% CI, 10.46-17.20]vs 9.50 [95% CI,
Discussion
7.25-11.74]; 1.5-fold higher) (eTable 2 in the Supplement). In this study, we analyzed the anatomical site distributions of
In contrast, the site distribution of SCC differed markedly BCC and SCC and compared them within strata of age and sex.
between men and women, with RTDs in men 10 times higher This study is, to our knowledge, one of the largest population-
on the scalp (1.35 [95% CI, 0.96-1.74] vs 0.13 [95% CI, 0.00- based studies to compare the site distribution of BCC and SCC
0.30]) and 5 times higher on the ears (11.12 [95% CI, 8.10- within the same sample of participants.
14.15] vs 2.36 [95% CI, 0.30-4.42]) compared with women. With Compared with the whole body, the head and/or neck re-
the exception of the forearm, the RTDs of SCC on the trunk gion (face, ears, and neck) had a higher RTD of BCC than the
(0.23 [95% CI, 0.18-0.28] vs 0.33 [95% CI, 0.23-0.42]) and up- mean. Although the RTD of BCC was highest on sites of fre-
per (1.74 [95% CI, 1.57-1.90] vs 2.04 [95% CI, 1.80-2.28]) and quent sun exposure, a large number of lesions also occurred
lower (0.52 [95% CI, 0.45-0.59] vs 0.72 [95% CI, 0.61-0.83]) on body sites less frequently exposed to sunlight, particu-
limbs was higher in women than in men. larly the trunk. For SCC, RTDs higher than the mean were seen
on the frequently sun-exposed parts of the body, with the head
Age Differences in the Anatomical Distribution and/or neck region (face, ears, and neck), upper limbs (fore-
of BCC and SCC arm and hands), and lower legs all exhibiting high RTDs. The
The distributions of BCC were similar among younger and older highest RTDs were present on the most sun-exposed facial
participants (Table 2) at all anatomical sites. For SCC, higher sites, followed by the ears.
RTDs were seen on the scalp (0.38 [95% CI, 0.00-0.81] vs 1.07 The pattern of distribution5,6,18 and the absolute tumor
[95% CI, 0.75-1.38]), ears (5.63 [95% CI, 1.19-10.08] vs 8.80 [95% densities17 of BCC and SCC were consistent with other Austra-
CI, 6.37-11.23]), and back and/or buttocks (0.05 [95% CI, 0.00- lian studies. However, studies from other countries have found
0.12] vs 0.12 [95% CI, 0.07-0.16]) in the older compared with a much higher proportion of both cancer types on the head
the younger participants. Although numbers were small, some and/or neck region, with as many as 80% of BCCs and SCCs
evidence suggested that the RTD of SCCs on the face was higher occurring on this site.7-15,23,24 A number of possible reasons
among younger than older people, especially on the least sun- may explain this frequency. First, these studies differed in
exposed facial sites. age range of the participants and methodologic approach.

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180
Table 2. Frequency Distribution and RTDs of BCC and SCC on Body Sites by Age Categories

BCC Age Group (n = 3846) SCC Age Group (n = 1304)


Young (n = 1055)a Old (n = 2791)b Young to Old Young (n = 213)a Old (n = 1091)b Young to Old
Frequency, % RTD Frequency, % RTD Ratio Frequency, % RTD Frequency, % RTD Ratio
Body Site (95% CI) (95% CI)c (95% CI) (95% CI)c (95% CI) (95% CI) (95% CI)c (95% CI) (95% CI)c (95% CI)
Head and/or neck 38 (35-41) 4.22 (3.88-4.53) 41 (39-43) 4.57 (4.37-4.77) 0.9 (0.8-1.0) 36 (30-43) 4.02 (3.30-4.73) 33 (30-36) 3.65 (3.34-3.96) 1.1 (0.9-1.3)
Scalp 3 (2-4) 0.84 (0.56-1.13) 2 (1-3) 0.54 (0.40-0.68) 1.6 (1.0-2.4) 1 (0-3) 0.38 (0.00-0.81) 4 (3-5) 1.07 (0.75-1.38) 0.4 (0.1-1.1)
Ears 4 (3-5) 7.57 (5.28-9.89) 4 (3-4) 7.02 (5.66-8.39) 1.1 (0.8-1.6) 3 (1-5) 5.63 (1.19-10.08) 4 (3-6) 8.80 (6.37-11.23) 0.6 (0.3-1.5)
Research Original Investigation

Face 25 (23-28) 10.53 (9.38-11.56) 29 (28-31) 12.26 (11.55-12.96) 0.9 (0.8-1.0) 29 (23-35) 11.93 (9.40-14.46) 21 (19-24) 8.94 (7.92-9.95) 1.3 (1.1-1.7)
Most exposedd 17 (15-20) 13.32 (11.45-14.95) 19 (18-20) 14.64 (13.51-15.76) 0.9 (0.8-1.1) 18 (13-23) 13.72 (9.77-17.68) 16 (14-18) 12.34 (10.66-14.01) 1.1 (0.8-1.5)
Less exposede 8 (6-10) 6.11 (4.87-7.38) 11 (10-12) 8.27 (7.38-9.15) 0.7 (0.6-0.9) 8 (5-12) 6.50 (3.63-9.37) 8 (7-10) 6.28 (5.03-7.52) 1.0 (0.6-1.7)
Least exposedf 4 (3-5) 12.93 (9.07-16.84) 3 (3-4) 10.51 (8.35-12.67) 1.2 (0.9-1.8) 5 (2-8) 17.21 (7.31-27.12) 2 (1-2) 5.50 (2.98-8.02) 3.1 (1.5-6.5)
Neck 6 (4-7) 2.40 (1.82-3.00) 6 (5-7) 2.58 (2.21-2.96) 0.9 (0.7-1.2) 3 (1-6) 1.37 (0.37-2.37) 3 (2-4) 1.26 (0.84-1.68) 1.1 (0.5-2.4)

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Trunk 36 (33-39) 1.13 (1.04-1.22) 33 (31-35) 1.03 (0.98-1.09) 1.1 (1.0-1.2) 12 (8-17) 0.38 (0.24-0.52) 8 (6-9) 0.24 (0.19-0.29) 1.6 (1.1-2.4)
Chest and/or abdomen 19 (16-21) 1.45 (1.27-1.63) 16 (15-17) 1.23 (1.13-1.34) 1.2 (1.0-1.4) 11 (7-16) 0.87 (0.54-1.19) 5 (4-7) 0.42 (0.31-0.52) 2.1 (1.3-3.3)
Back and/or buttocks 17 (15-20) 0.91 (0.79-1.03) 17 (16-18) 0.90 (0.82-0.97) 1.0 (0.9-1.2) 1 (0-2) 0.05 (0.00-0.12) 2 (1-3) 0.12 (0.07-0.16) 0.4 (0.1-1.8)
Upper limbs 16 (14-18) 0.84 (0.72-0.95) 13 (12-14) 0.68 (0.61-0.74) 1.2 (1.0-1.5) 32 (26-39) 1.70 (1.37-2.04) 35 (33-38) 1.86 (1.71-2.01) 0.9 (0.7-1.1)
Upper arm 8 (7-10) 1.03 (0.82-1.24) 5 (4-6) 0.66 (0.55-0.76) 1.6 (1.2-2.0) 4 (1-6) 0.47 (0.15-0.79) 4 (3-6) 0.55 (0.40-0.70) 0.9 (0.4-1.8)
Forearm 6 (5-8) 1.07 (0.83-1.32) 7 (6-8) 1.13 (0.97-1.28) 1.0 (0.7-1.2) 13 (9-18) 2.19 (1.43-2.95) 18 (16-20) 2.98 (2.60-3.36) 0.7 (0.5-1.1)

JAMA Dermatology February 2017 Volume 153, Number 2 (Reprinted)


Handg 1 (1-2) 0.25 (0.11- 0.38) 1 (1-1) 0.17 (0.10-0.24) 1.4 (0.7-2.8) 15 (11-20) 3.10 (2.13-4.07) 13 (11-15) 2.62 (2.22-3.02) 1.2 (0.8-1.7)
Lower limbs 10 (8-12) 0.25 (0.21-0.30) 13 (12-14) 0.32 (0.29-0.35) 0.8 (0.6-1.0) 19 (14-25) 0.48 (0.35-0.61) 24 (22-27) 0.60 (0.54-0.67) 0.8 (0.6-1.1)
Thigh 2 (1-3) 0.12 (0.07-0.17) 2 (1-2) 0.08 (0.06-0.11) 1.5 (0.9-2.4) 2 (0-4) 0.12 (0.02-0.23) 2 (1-3) 0.12 (0.07-0.17) 1.0 (0.4-2.7)
Lower leg 7 (6-9) 0.53 (0.42-0.65) 11 (10-12) 0.76 (0.68-0.84) 0.7 (0.6-0.9) 16 (11-21) 1.17 (0.82-1.53) 21 (18-23) 1.46 (1.29-1.63) 0.8 (0.6-1.1)
Footh 0 (0-1) 0.04 (0.00-0.09) 1 (0-1) 0.10 (0.05-0.14) 0.4 (0.1-1.4) 0 (0-1) 0.07 (0.00-0.20) 2 (1-2) 0.21 (0.11-0.31) 0.3 (0.0-2.4)
Total body 100 NA NA NA NA NA NA NA NA NA
d
Abbreviations: BCC, basal cell carcinoma; NA, not applicable; RTD, relative tumor density; SCC, squamous cell Includes ears, nose, cheeks, and lips.
carcinoma. e
Includes forehead, eyebrows, chin, jaw, temple, and preauricular area.
a
Indicates 40 to 54 years. f
Includes under eyebrow, upper and lower eyelids, medial and lateral canthus, and nasolabial fold.
b
Indicates 55 to 69 years. g
Includes back of hand, palmar skin, and fingernail.
c
Calculated as the ratio of the proportion of tumors at a specific anatomical site to the proportion of skin surface h
Includes dorsum of foot, toes, plantar skin, and toenail.

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Anatomical Distributions of Skin Cancers in Queensland, Australia
Anatomical Distributions of Skin Cancers in Queensland, Australia Original Investigation Research

Second, variability in medical care, such as differences in op- is likely owing to sex differences in hair cover. Higher densi-
portunistic screening practice, may have led to fewer lesions ties of KCs occurring on the upper arm of women compared
being diagnosed on less habitually sun-exposed sites than in with men may be attributed to clothing choice, with more
Australia. This variability is particularly likely to influence the women than men choosing to wear short-sleeved or sleeve-
body site distribution of BCC.25 Finally, the relatively higher less shirts.
proportion of lesions on sites other than the head and/or neck Our findings did not show significant differences be-
in Australia is likely owing to lifestyle and sun exposure tween the younger and the older groups for BCC. Higher RTDs
practices. For example, the climate in Australia is conducive for SCCs seen on less exposed sites, such as the back and/or
to outdoor recreational pursuits that are commonly enjoyed buttocks region, in older compared with younger partici-
with minimal clothing, which would contribute to higher pants could be attributed to higher cumulative sun exposure
exposure on the trunk and limbs compared with other with increasing age. Differential treatment according to age (eg,
populations. older people having more regular full-body screening) may
The anatomical distribution of SCC corresponds closely partly explain the age differences in SCC RTDs but is unlikely
to the pattern of intensity of sun exposure, with the highest to be entirely responsible because the same differences are not
density of lesions occurring on body sites frequently observed for BCC.
exposed to sunlight. Basal cell carcinoma was less clearly This study has a number of strengths and weaknesses.
aligned with sun exposure patterns, with a relatively high We recruited a large community-based sample from the
RTD on less frequently exposed body sites. The infrequent compulsory voting register. Moreover, because we identi-
exposure of these sites results in less melanin protection, fied patients with KCs through linkage with the national
increasing the risk for sunburn. Basal cell carcinoma on less insurance scheme and confirmed the diagnoses with
exposed body sites may thus arise as a result of infrequent pathology reports, the information regarding diagnosis and
or intermittent high doses of UV radiation.26 Alternatively, anatomical distribution is likely to be accurate. Although we
the potential cells of origin of BCC on the trunk and but- did not capture services delivered in public hospitals, the
tocks may require a lower total dose of sun exposure to 2002 National Skin Cancer Survey reported that fewer than
become neoplastic. The relatively high RDT of BCC in the 2% of the survey participants underwent skin cancer treat-
periorbital region, which receives the least amount of ment in a hospital setting, indicating near-complete capture
sunlight among the facial subsites, also supports the theory of skin cancer events.30 A potential weakness in this analy-
that lower doses of UV radiation give rise to BCCs compared sis is the lack of histologic confirmation of all KCs identified
with SCCs. in the Medicare records. We obtained pathology records
The RTD of SCC on the hand was 14 times higher than the from the 2 largest and 2 smaller pathology service providers
RTD of BCC (2.70 [95% CI, 2.33-3.07] vs 0.19 [95% CI, 0.13- for the state of Queensland, but we were unable to obtain
0.25]). The relative paucity of BCC on the hands, which are pathology reports from all laboratories in the state. How-
chronically exposed to intense sunlight, has been reported in ever, we interrogated the Medicare data by item numbers
clinical and epidemiologic studies previously.16,27 We calcu- that broadly identify the site of the lesion, which showed
lated the BCC:SCC ratio in previous studies as 1:918 and 1:20.16 that the overall patterns of site distribution did not differ
The difference in RTDs between BCC and SCC on the hands between participants with and without pathology reports.
cannot be explained simply by sun-exposure patterns. The Therefore, the RTD estimates are likely to be representative
significantly greater thickness of the epidermis on the dor- of the fair-skinned population of Queensland, and by infer-
sum of the hand compared with the forearm28 may explain ence to other populations residing in low latitudes,
the relative lack of BCC on the hands but fails to explain the although they may not be applicable to other population
relative abundance of SCC. Basal cell carcinoma is postu- groups.
lated to arise from basal cells that are situated deeper in the
epidermis of the skin, in contrast to the more superficially
placed squamous cells, thought to be the origin of SCC.
Thus, one plausible explanation for the marked differences
Conclusions
in the occurrence of BCC and SCC on the dorsum of the The results from this large cohort study emphasized dif-
hand is that the depth of epidermis protects the deeply situ- ferences in the anatomical distributions of BCC and SCC.
ated basal cells from the UV rays compared with the expo- High densities of BCCs and SCCs observed on sun-exposed
sure received by the more superficial squamous cells. Stud- body sites confirm sun exposure as the primary etiologic
ies have also suggested that BCC may arise from follicular factor for both tumors; the differences in RTDs of SCCs
stem cells,29 so an alternate explanation for the lower RTD by age and sex underscore the association with cumulative
of BCC could be the relative lack of hair on the back of the sun exposure. In contrast, the observations that BCCs
hands compared with the forearm. occur relatively infrequently on the hand but relatively fre-
A limited number of studies have shown that the associa- quently on body sites that are only intermittently exposed
tion between the anatomical distributions of KC varies to UV radiation point to more complex associations
according to sex. We found that the RTDs of BCC and SCC on with sun exposure. Understanding the etiology and patho-
the scalp and ears were higher in men than in women, a pat- genesis of BCC may lead to new avenues for prevention and
tern that has been reported previously.6,7,18 This difference treatment.

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Research Original Investigation Anatomical Distributions of Skin Cancers in Queensland, Australia

ARTICLE INFORMATION Venn, PhD, Menzies Research Institute, Hobart, 15. Athas WF, Hunt WC, Key CR. Changes in
Accepted for Publication: September 2, 2016. Australia (scientific advisory board). nonmelanoma skin cancer incidence between
Previous Presentation: This study was presented 1977-1978 and 1998-1999 in northcentral New
Published Online: November 23, 2016. Mexico. Cancer Epidemiol Biomarkers Prev. 2003;12
doi:10.1001/jamadermatol.2016.4070 as an abstract at the 21st Australasian
Epidemiological Association Annual Scientific (10):1105-1108.
Author Affiliations: Department of Population Meeting; October 10, 2014; Auckland, New 16. Pearl DK, Scott EL. The anatomical distribution
Health, QIMR Berghofer Medical Research Institute, Zealand. of skin cancers. Int J Epidemiol. 1986;15(4):502-506.
Royal Brisbane Hospital, Queensland, Australia
(Subramaniam, Olsen, Thompson, Whiteman, 17. Staples MP, Elwood M, Burton RC, Williams JL,
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