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BJD

E P ID EMIOL O GY AN D HE AL TH S ER VI CE S R ESEA RCH British Journal of Dermatology

A systematic review of worldwide incidence of


nonmelanoma skin cancer
A. Lomas, J. Leonardi-Bee and F. Bath-Hextall*
Epidemiology and Public Health, and *Centre for Evidence Based Dermatology, University of Nottingham, Queen’s Medical Centre, Nottingham
NG7 2UH, U.K.

Summary

Correspondence Background Nonmelanoma skin cancer (NMSC) is the most common cancer affect-
Alexander Lomas. ing white-skinned individuals and the incidence is increasing worldwide.
E-mail: mzybawl@nottingham.ac.uk Objectives This systematic review brings together 75 studies conducted over the
past half century to look at geographical variations and trends worldwide in
Accepted for publication
7 January 2012
NMSC, and specifically incidence data are compared with recent U.K. cancer
registry data.
Funding sources Methods Following the development of a comprehensive search strategy, an assess-
None. ment tool was adapted to look at the methodological quality of the eligible
studies.
Conflicts of interest
Results Most of the studies focused on white populations in Europe, the U.S.A.
None declared.
and Australia; however, limited data were available for other skin types in
DOI 10.1111/j.1365-2133.2012.10830.x regions such as Africa. Worldwide the incidence for NMSC varies widely with
the highest rates in Australia [> 1000 ⁄100 000 person-years for basal cell carci-
noma (BCC)] and the lowest rates in parts of Africa (< 1 ⁄100 000 person-years
for BCC). The average incidence rates in England were 76Æ21 ⁄100 000 person-
years and 22Æ65 ⁄100 000 person-years for BCC and squamous cell carcinoma
(SCC), respectively, with highest rates in the South-West of England
(121Æ29 ⁄100 000 person-years for BCC and 33Æ02 ⁄100 000 person-years for
SCC) and lowest rates by far in London (0Æ24 ⁄100 000 person-years for BCC and
14Æ98 ⁄100 000 person-years for SCC). The incidence rates in the U.K. appear to
be increasing at a greater rate when compared with the rest of Europe.
Conclusions NMSC is an increasing problem for health care services worldwide.
This review highlights a requirement for prevention studies in this area and the
issues surrounding incomplete NMSC registration. Registration standards of
NMSC should be improved to the level of other invasive disease.

Basal cell carcinoma (BCC) and squamous cell carcinoma such the older population currently being diagnosed used very
(SCC) are the two most common subtypes of nonmelanoma little sun protection and received very little education regard-
skin cancer (NMSC). Although they share many similarities, ing the effects of ultraviolet radiation (UVR). A primary
they have different incidence rates and important aetiological prevention study in Australia ran for 20 years before beneficial
differences. BCC is the most common cancer in many coun- effects were observed.6,7
tries worldwide1 and although the mortality rate is exception- The main difficulty in measuring the incidence comes from
ally low,2 NMSC represents both a significant economic poor registration practice in the majority of countries. Usually
burden to health services and can cause significant morbidity only the first case of NMSC in a patient is registered, any sub-
especially as most NMSCs occur on highly visible areas such as sequent tumours are not included and multiple tumours are
the head and neck and face. not differentiated. The majority of data on NMSC incidence
In comparison with other malignancies, little is known comes from local studies of incidence in a certain geographical
about the incidence. The rate is increasing in many coun- location.
tries3–6 and although the reason for this is unclear, it may be The recently updated National Institute for Health and Clini-
linked to increased sun-seeking behaviours and improved reg- cal Excellence (NICE) guidelines state a need to establish the
istration procedures. It is important to realize that NMSC inci- true nature of the epidemiology of BCC.8 This systematic
dence is based on a lifetime of exposure to risk factors and as review aims to summarize all the existing literature regarding

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080 1069
1070 Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al.

the incidence of not only BCC but also SCC worldwide and Table 1 Quality assessment criteria
for the U.K. to make comparisons between that literature and
incidence data from U.K. cancer registries. Internal validity
Data collection
(a) Did the study directly sample the population, as opposed to
Materials and methods using cancer registries?
Description of methods
Inclusion and exclusion criteria (b) Is the method of counting tumours stated?
• Number of tumours or number of patients
Any epidemiological study that assessed the incidence rate of (c) Is there histological verification?
BCC, SCC or both subtypes combined was included. In order Reporting of incidence rates
to improve the chance a study was sufficiently rigorous to deal (d) Were separate rates reported for BCC and SCC?
accurately with the complexities of NMSC epidemiology, the (e) Are gender-specific incidence rates reported?
(f) Are age-specific incidence rates reported?
studies needed to examine the incidence of NMSC exclusively,
(g) Were the rates age standardized?
as opposed to all malignancies. Incidence rates had to be sta-
(h) Are confidence intervals used?
ted or sufficient data provided to allow the calculation of inci- External validity
dence rates. If two papers reported results in the same (i) Is there information about the ethnicity or skin type of the
population at the same point in time (such as provisional population?
rates) the data were compared and counted only once. Studies • Must state actual proportions
which focused solely on genetic syndromes were excluded. (j) Were the data standardized to a major population?
• U.S. population, European population or world population

Search strategy BCC, basal cell carcinoma; SCC, squamous cell carcinoma.

A comprehensive search strategy was developed, and EMBASE


(from 1980) and Medline (from 1950) were searched to
March 2011 using the following search string to identify rele- which was developed and based on existing assessment
vant papers: carcinoma, basal cell, basal cell nevus syndrom ⁄, tools.10,11 The criteria listed in Table 1 were assessed, with
carcinoma, squamous cell non melanoma or nonmelanoma or each point equally weighted.
non-melanoma, skin, cutaneous, incidence, epidemiology. No Incidence rates are presented as rates per 100 000 person-
restrictions on language were imposed during the search strat- years. The incidence rates from studies which standardized to
egy. A second author independently reviewed titles and the same population were compared directly. Graphs were
abstracts and disagreements were resolved through discussion constructed using data from male incidence rates because these
with a third author. maximized the number of comparable figures, as few studies
reported overall standardized incidence rates for male and
females combined.
Data acquisition
Two of the authors (A.L. and J.L.-B.) independently extracted
Results
the following data for each study: author, country and region,
study period, reported rates of NMSC, BCC or SCC, source of The search strategy identified 3083 papers of which 275 were
the study’s population (e.g. cancer registry, histology labora- deemed potentially eligible based on abstracts, and 75 were
tory etc.), whether histological confirmation was obtained, finally included in the review (Fig. 1).3–7,12–81 Thirty-one
unit of analysis (i.e. number of patients or number of studies were excluded as they did not focus exclusively on
tumours) and method of standardization for incidence rates. NMSC. These papers were all cancer incidence reviews and in
Disagreements were resolved through discussions with a third the majority of cases did not report NMSC incidence at all.
author (F.B.-H.). Values for approximate latitude were Fifteen papers were excluded as no translation was available.
obtained using Google Earth.9 The included papers provide data on 38 different countries
The South West Cancer Intelligence Service provided stan- worldwide over the period 1955–2007. Twelve incidence
dardized data from all cancer registries in England. Northern studies were based on Australian populations, more than any
Ireland and Scotland provided standardized data. No data were other country. Most of the papers reported age-standardized
available from the Welsh cancer registry. The data for England incidence rates. Thirty-eight were standardized to the world-
were entered into ArcGIS for Windows (Esri, Redlands, CA, wide population, eight to the U.S. population and eight to the
U.S.A.) and displayed on a map of England. European population. Fifteen papers did not age-standardize
incidence rates to any population.
The methodological quality of the studies varied with a
Quality assessment
range of scores between 1 and 9. Forty-eight (64%) studies
The included studies were assessed for methodological quality were deemed of high quality (score ‡ 6); however, no study
using a modified methodological quality-assessment tool met all the criteria and only 19 provided information about

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080
Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al. 1071

rates dropping from 104Æ12 ⁄100 000 person-years in York-


Studies from search strategy
shire to 90Æ4 ⁄100 000 person-years in Scotland as a whole.
n = 3083
Scotland has a similar incidence to Northern Ireland
Titles reviewed (86Æ8 ⁄100 000 person-years).
Excluded: n = 2808

Data from systematic review


Potentially relevant papers
n = 275
U.K. One study conducted in the North Humberside region,
Based on abstracts: between the years 1978 and 1991, showed an increase in BCC
Study irrelevant: n = 40
Not a study (i.e. a review): n = 35
incidence from 38Æ8 ⁄100 000 person-years to 115Æ6 ⁄100 000
NMSC was not the main focus: n = 31 person-years.42 A study using a primary care database (The
Unable to calculate incidence: n = 16
Duplicates: n = 13 Health Improvement Network) found the European age-
Others: n = 6
Total excluded = 141 standardized rate of BCC across the U.K. to be 89 ⁄100 000
person-years between 1996 and 2003.15 Only two studies
Full text located: were found that looked at BCC in Wales and reported the inci-
n = 134
dence to be 75Æ1 ⁄100 000 person-years5 and 83Æ1 ⁄100 000
person-years,64 respectively, in 1988. Ten years later in 1998,
Based on full texts:
No incidence calculated: n = 34 the rate had increased to 114Æ2 ⁄100 000 person-years.5 A
Foreign language: n = 15
Non-representative population: n = 4
study in Scotland reported rates increasing from
Unavailable: n =2 35Æ6 ⁄100 000 person-years in 1979 to 97Æ5 ⁄100 000 person-
Same dataset: n = 2
Not an original study: n = 1 years in 2003 (standardized to the European population).81
Indirectly standardized: n = 1
Total excluded = 59
Europe Figure 3 shows data from males from 14 comparable
Studies included: studies assessing the incidence of BCC in Eur-
N = 75
ope.5,15,17,18,25,34,41,48,50,56,57,64,67,68 All of the studies show
that the rates of BCC have increased at a similar rate over the
Fig 1. Results of search strategy and reasons for exclusion. NMSC, past four decades, on average increasing by 20 ⁄100 000 per-
nonmelanoma skin cancer. son-years every 15 years, a 5Æ5% increase per year.34 The two
South Wales-based studies report a higher incidence than in
other European countries.5,64 A further study conducted in the
the skin types or ethnicity of the study population. The major- North Humberside region of the U.K.42 could not be included
ity (65%) of studies used histological verification. Fifty-three in this graph due to data being standardized to a different
studies used records from sources such as cancer registries and standard population (England and Wales); however, this study
hospitals with the remaining 22 studies obtaining their own showed that the U.K. incidence rates could be increasing
data from sources such as questionnaires. Table 2 includes much faster than in other European countries: an increase
methodological information about each of the studies included from 38Æ8 ⁄100 000 person-years in 1978 to 115Æ6 ⁄100 000
in this review. person-years in 1991 was seen.42 Incidence rates in the Neth-
erlands are also not shown due to differing populations where
the male and female combined incidence rate was
U.K. registry data
87Æ5 ⁄100 000 person-years in 2003 (standardized to the
The data provided by the cancer registries are shown in European population).77 Elsewhere in Europe, Switzerland and
Table 3. As the incidence of BCC is much higher than SCC in Italy appear to have the highest incidence rates at around
the U.K., the distribution of NMSC appears the same as BCC. 70 ⁄100 000 person-years in 1995;17,48,50 for comparison, the
The incidence for BCC and SCC is shown diagrammatically in incidence of BCC in Slovakia was only 38 ⁄100 000 person-
Figure 2. years in 1994,57 even though Slovakia lies at a similar latitude
to Switzerland and Italy. In Denmark, the male incidence rate
increased from 34Æ2 ⁄100 000 person-years to 91Æ2 ⁄100 000
Basal cell carcinoma
person-years between 1978 and 2007.79 In the same study, an
even greater increase was reported in female incidence rates
U.K. registry data
(27Æ1 ⁄100 000 person-years in 1978 to 96Æ6 ⁄100 000 per-
The South-East regions of the U.K., including London, the son-years in 2007). The lowest rates were observed in Croatia
South-East coast and East Anglia, have lower rates of BCC than at 33Æ6 ⁄100 000 person-years between 2003 and 2005.80
more Northern regions of the country where the incidence is
similar at around 100 ⁄100 000 person-years. There appears to North America Manitoba (Canada) lies at a similar latitude to
be a divide between the North of England and Scotland with Europe and hence is exposed to comparable levels of UVR.

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080
Table 2 Study characteristics

Approximate Histological Direct or indirect


First author Country Region latitude Study period Data source confirmation Coding (population)
Abarca12 Chile South: Punta Arenas 5308¢S 1987–2000 Sole dermatologist Yes By patient Direct (Chile)
Athas13 U.S.A. North central NM 3458¢N 1977–1999 Cancer registry Partly By patient Direct (U.S.A.)
Bariani14 Brazil Sao Paulo 2332¢S 2001–2003 One hospital’s records Yes By patient No standardization used
Bath-Hextall15 U.K. Whole country 5522¢N 1996–2003 THIN database of all No By patient Direct (world)
patient records
Battistini3 Italy Pisa 4342¢N 1997–2002 Hospital presentations Yes By patient Crude
Bernard16 France Whole country 4613¢N 2004 Dermatologists Partly By tumour No standardization used
Birch-Johansen79 Denmark Whole country 5615¢N 1978–2007 Cancer registry Yes By patient Direct (world)
Boi17 Italy Province of Trento 4604¢N 1992–1997 Interviews of patients Yes By patient Direct (world)
from cancer registry
Brewster18 Scotland East 5629¢N 1992–2003 Cancer registry Yes By patient Direct (world)
Buettner19 Australia Townsville, Qld 1915¢S 1996–1997 Laboratories Yes By patient Direct (world)
Cheng20 Hong Kong Whole country 2223¢N 1990–1999 Clinics run by Yes By patient No standardization used
dermatology department
Chuang21 U.S.A. Rochester, MN 4401¢N 1976–1984 Mayo Clinic presentations Yes By patient Direct (U.S.A. 1980)
Chuang22 U.S.A. Rochester, MN 4401¢N 1976 Mayo Clinic presentations Yes By patient Direct (U.S.A. 1980)
Chuang23 U.S.A. Kauai, HI 2205¢N 1983–1987 Laboratory Yes By patient Direct (world)
1072 Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al.

Chuang24 U.S.A. Kauai, HI 2205¢N 1983–1987 Laboratory Yes By patient Direct (world)
Coebergh25 Netherlands Southeast (Eindhoven area) 5126¢N 1975–1988 Cancer registry Yes By patient Direct (world)
Dahl26 Sweden Malmö 5536¢N 1970–1986 Laboratory Yes By patient Direct (U.S.A. rates)
Dal27 Sweden Whole country 6007¢N 1960–2004 Cancer registry Not specified Unknown Direct (European)
De Vries28 Netherlands Southeast (Eindhoven area) 5126¢N 2000 Cancer registry Yes By patient Direct (European)
De Vries29 Netherlands Southeast (Eindhoven area) 5126¢N 1973–2000 Cancer registry No By patient Direct (European)
Demers4 Canada MB 5345¢ N 1960–2000 Cancer registry No By patient Direct (world)
Doherty81 Scotland Whole country 5629¢N 1978–2004 Cancer registry Not specified By patient Direct (European)
Foster30 Papua New Guinea North Solomon Islands 930¢S 1960–1980 Cancer registry Yes By tumour Crude
Freeman31 New Zealand Waikato, Tauranga, Bay 3811¢S 1977–1978 Doctor reporting Partly By patient Direct (U.S.A. 1970)
of Plenty and Taumarunui area
Giles32 Australia Whole country 2516¢S 1985 Commercial research No By patient Direct (world)
face to face interviews
Green33 Australia Nambour, Qld 2637¢S 1985–1992 Sample of electoral roll No By patient Direct (world)
Hannuksela-Svahn34 Finland Whole country 6155¢N 1956–1995 Cancer registry Yes By patient Direct (world)
Harris35 U.S.A. Southeast AZ 3402¢N 1985–1996 Cancer registry Yes By patient Direct (U.S.A.)
Hayes36 Canada NB 4029¢N 1992–2001 Cancer registry Yes By patient Direct (world)
Hoey37 Northern Ireland Whole country 5417¢N 1993–2002 Cancer registry Yes By patient Direct (European)
Holme5 Wales West Glamorgan 5149¢N 1988–1998 Cancer treatment and Partly By patient Direct (world)
outcomes registry service
(CANTORIS)

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080
Table 2 (Continued)

Approximate Histological Direct or indirect


First author Country Region latitude Study period Data source confirmation Coding (population)
Holterhues77 Netherlands Whole country 5207¢N 2001–2005 Cancer registry Yes By tumour Direct (European)
Hussain76 Sweden Whole country 6007¢N 1990–2005 Cancer registry Yes Not specified Direct (Sweden)

 2012 The Authors


Ichihashi38 Japan Whole country 3612¢N 1976–1980 Hospitals Yes By tumour Age standardized
Iversen75 Norway Whole country 6028¢N 1966–1995 Cancer registry Yes By patient Direct (world)
Jung78 Canada AB 5355¢N 1988–2007 Cancer registry No By patient Direct (Canada)
Kaldor39 Australia Tas. 4142¢S 1978–1987 Cancer registry Partly By patient Direct (world)
Karagas40 U.S.A. NH 4311¢N 1979–1980 Dermatologist and No By patient Direct (U.S.A.)
laboratory reporting
Katalinic41 Germany Schleswig-Holstein 5413¢N 1998–2001 Cancer registry Yes By patient Direct (world)
Ko42 U.K. North Humberside 5355¢N 1978–1991 Histology laboratory Yes Not specified Direct
(England and Wales)
Koh43 Singapore Whole country 121¢N 1968–1997 Cancer registry Yes Not specified Direct (world)
Kricker44 Australia Geraldton, WA 2846¢N 1986–1987 Postal questionnaire Yes By patient Crude
Kromann45 Greenland Whole country 7019¢N 1955–1974 Hospitals Yes By patient Direct (world)
Kubeyinje46 Saudi Arabia North: Arar 3058¢N 1988–1995 Hospital Yes By patient Crude
Leong47 U.S.A. Kauai, HI 2205¢N 1983–1985 Physicians and laboratory Yes By patient Crude
Levi49 Switzerland Neuchatel 4659¢N 1976–1998 Cancer registry Yes By patient Direct (world)
Levi48 Switzerland Vaud 4633¢N 1976–1992 Cancer registry Yes By patient Direct (world)

BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080


Levi50 Switzerland Vaud 4633¢N 1993–1998 Cancer registry Yes By patient Direct (world)
Lipozencic80 Croatia Whole country 4506¢N 2003–2005 Cancer registry Yes Not specified Direct (world)
Marks51 Australia Maryborough, Vic. 2532¢S 1982–1986 Postal survey No By tumour Direct (world)
Marks52 Australia Whole country 2516¢S 1990 Commercial research No By patient Direct (world)
face to face interviews
Munyao53 Kenya Whole country 001¢S 1968–1997 Cancer registry Not specified Not specified Crude
Nunes54 Brazil Tubarao 2828¢S 2000–2006 Laboratory records Yes Not specified Crude
Omari55 Jordan North 3035¢N 1997–2000 Cancer registry Yes By patient Direct (Jordan)
Østerlind56 Denmark East 5615¢N 1978–1982 Cancer registry Yes By patient Direct (world)
Plesko57 Slovakia Whole country 4840¢N 1978–1995 Cancer registry Yes By patient Direct (world)
Raasch58 Australia Townsville, Qld 1915¢S 1997–1999 Laboratories Yes By patient Direct (world)
Radespiel-Tröger59 Germany Bavaria 4847¢N 2001–2005 Cancer registry Not specified By patient Direct (European)
Rawashdeh60 Jordan North 3140¢N 1991–2000 Laboratory Yes By patient Direct (world)
Reizner61 U.S.A. Kauai, HI 2205¢N 1983–1987 Laboratory Yes By patient Crude
Revenga Arranz62 Spain Northeast: Soria 4145¢N 1998–2000 Clinical records at the Yes By patient Direct (world)
sole dermatological
hospital in the area
Richmond-Sinclair63 Australia Nambour, Qld 2637¢N 1997–2006 Cohort, histologically Yes By patient Direct (world)
confirmed, of Nambour
Skin Cancer Survey
Roberts64 Wales West Glamorgan 5149¢N 1988 Reports from clinicians Not specified By patient Direct (world)
Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al. 1073
1074 Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al.

Table 3 Directly standardized annual incidence rates for

No standardization used
No standardization used
nonmelanoma skin cancer (NMSC), basal cell carcinoma (BCC) and

Direct (U.S.A. 1970)


squamous cell carcinoma (SCC) in the U.K. per 100 000 person-years:

Direct (European)
Direct or indirect 2000–2006

Direct (Sweden)
Direct (world)
Direct (world)
Direct (world)
Direct (world)
Direct (world)

Direct (world)
(population)
Region NMSC BCC SCC

Crude
England 98Æ85 76Æ21 22Æ65
East Midlands 123Æ87 99Æ61 24Æ26
East of England 79Æ25 57Æ30 21Æ95
London 15Æ22 0Æ24 14Æ98
Not Specified

Not specified
North-East 121Æ48 97Æ11 24Æ36
By patient

By patient
By patient
By patient
By patient

By patient
By patient
By patient

By patient

By patient
Coding

North-West 121Æ94 99Æ08 22Æ86


South Central 130Æ81 108Æ73 22Æ08
South-East coast 20Æ47 0Æ43 20Æ04
South-West 154Æ31 121Æ29 33Æ02
Not specified

Not specified
confirmation

West Midlands 100Æ76 82Æ37 18Æ39


Histological

Yorkshire & the Humber 127Æ86 104Æ12 23Æ73


Partly

Partly

Partly
Partly
Partly

Scotland 118Æ9 90Æ4 27Æ0


Yes
Yes

Yes

Yes
No

North Scotland 111Æ0 83Æ5 26Æ2


South-East Scotland 122Æ9 89Æ8 30Æ5
West Scotland 121Æ0 94Æ6 25Æ2
Face to face interviews of sample
Face to face interviews of sample

Northern Ireland – 86Æ8 30Æ6


Cohort from Nambour Skin

All rates are directly standardized to the European population.


Reporting by clinicians

Network of physicians

Hospital and clinic


GP and hospitals

Cancer Survey
Cancer registry
Cancer registry

Cancer registry
Cancer registry

Despite this, a relatively high incidence of BCC was seen both


Data source

in Manitoba, where the male incidence was 93Æ9 ⁄100 000


Hospital

person-years in 2000,4 and in Alberta at 147Æ0 ⁄100 000 per-


son-years in 2006.78
Five comparable studies were found regarding BCC inci-
Study period
1979–1980
1968–2006
1995–1999
1998–2003

1971–1980
1958–1995

1961–1995
1988–2005

dence in the U.S.A.13,21,35,40,65 Arizona and New Mexico are


two adjacent states in the South-West of the U.S.A., lying at
2002
1995
1984

2001

approximately 34o N latitude. Both states appear to have simi-


lar incidence rates. A rate of 935Æ9 ⁄100 000 person-years was
reported for 1996 in Arizona.35 Two Northern states also
Approximate

share similar incidence rates. New Hampshire in New England


4351¢N

4923¢N
5125¢N

1942¢N
3904¢N

5919¢N
6007¢N
5126¢N
2516¢S
2516¢S

1942¢S
latitude

121¢N

lies at a latitude of 43o N. Minnesota lies more centrally but at


a very similar latitude of 44o N. The two states have nearly
THIN, The Health Improvement Network; GP, general practitioner.

identical BCC incidence rates at approximately 170 ⁄100 000


person-years in 1980.21,40,65 All studies were standardized to
Southeast (Eindhoven area)

the same population and appear to show a similar rate of


Northrhine-Westphalia

increase of approximately 2% per year.


Whole country

Whole country
Whole country

Whole country
One hospital

Australia The search found eight studies which looked at inci-


NH and VT

Stockholm

dence of BCC in Australia.6,7,19,32,33,52,58,63 Four studies esti-


Saarland
Region

mated the incidence based on a national survey,6,7,32,52 two


Qld

Qld

papers focused on a population in Townsville, Queensland19,58


and a further two papers followed a population in Nam-
Netherlands

bour.33,63 Although all standardized to the world population,


Singapore
Germany
Germany
Australia
Australia
Australia

Australia
Country

Sweden
Sweden
Greece

the two regional studies are not likely to represent the whole
U.S.A.

country. As the Nambour study involved screening by experi-


Table 2 (Continued)

enced dermatologists, these results cannot be compared


directly with the national survey.
Van Hattem72
First author

Wassberg74
Wallberg73
Stenbeck69

The incidence of BCC in Australia was higher than any-


Stratigos70
Serrano65

Valery71
Staples6
Staples7
Stang67
Stang68

where else in the world. The national surveys showed that the
Sng66

incidence of BCC has been increasing gradually since 1985,


and appears to be reaching a plateau.6,7,32,52 The rate of

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080
Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al. 1075

Fig 2. Incidence of basal cell carcinoma and squamous cell carcinoma in England, data from cancer registries.

884 ⁄100 000 person-years (both sexes combined) in 2002 is with only a slight increase in incidence rate being seen 10 years
10 times the rate recorded in the U.K.15 The four studies that later (15Æ8 ⁄100 000 person-years in 19985). In Scotland, the
followed up the smaller populations show a decreasing inci- incidence rate of SCC increased from 16Æ1 ⁄100 000 person-
dence rate.19,33,58,63 In the case of the Nambour study group years in 1979 to 36Æ9 ⁄100 000 person-years in 2003.81
the male incidence rate decreased from an average incidence
of 2074 ⁄100 000 person-years between 1985 and 1992 to Europe For comparison, all European studies reporting male
1813 ⁄100 000 person-years between 1997 and 2006.33,63 SCC incidence rates standardized to the world population are
displayed in Figure 4.
Nineteen studies were identified that measured the incidence
Squamous cell carcinoma
of SCC in Europe.5,17,18,25,34,41,48,50,56,57,64,67,68,74–77,79,80
All studies suggested an increasing trend, although the rate of
U.K. registry data
increase varied from country to country. Like BCC, the South
Squamous cell carcinoma incidence data are listed in Table 3 Wales studies show the highest incidence rates of approxi-
and displayed in Figure 2. The incidence rates of SCC vary less mately 31Æ7 per 100 000 person-years.64 Switzerland had the
across the U.K. than those of BCC. The rate of 23Æ73 ⁄100 000 highest SCC incidence rate of all of mainland Europe, as well
person-years in Yorkshire is representative of most of the as showing the fastest increase from 14Æ2 ⁄100 000 person-
country north of London which, like BCC, has the lowest years in 1978 to 28Æ9 ⁄100 000 person-years in 1997.48,50
recorded SCC rate in the U.K. at 14Æ98 ⁄100 000 person-years. Northern European countries such as Norway, Finland and
The South-West counties again have a notably higher inci- Denmark reported very low rates of SCC of less than
dence rate at 33Æ02 ⁄100 000 person-years. 10 ⁄100 000 person-years, and the increase in incidence over
time is also much slower than in the other countries.34,56,75,79
Although Sweden has a similar geographical location to these
Data from systematic review
Northern European countries, the incidence of SCC has shown
a sharper increase.74 A second Swedish study between 1990
U.K. An increasing incidence rate of SCC from 15Æ9 ⁄100 000 and 2005 found that the average SCC incidence rate was
person-years in 1978 to 28Æ6 ⁄100 000 person-years in 1991 34Æ4 ⁄100 000 person-years for males and 15Æ4 ⁄100 000 per-
was reported in the North Humberside region.42 The two son-years for females.76 As for BCC, the incidence rate of SCC
Welsh studies reported rates of SCC at 19 ⁄100 000 person- in Croatia was lower than elsewhere in Europe at
years64 and 15Æ1 ⁄100 000 person-years5 in 1988, respectively, 8Æ9 ⁄100 000 person-years.80

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080
1076 Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al.

Incidence of BCC in European males


140

Denmark, Osterlind A.

Incidence of BCC per 100 000 persons


120
Finland, Hannuksela-Svahn A
Germany, Katalinic A
100
Germany, Stang A
Germany, Stang A. 1998
80
Italy, Boi S
Netherlands, Coebergh J
60
Scotland, Brewster D.

40 South Wales, Holme S.


Slovakia, Plesko I

20 Switzerland, Levi F
Switzerland, Levi F. 2001
0 UK, Bath-Hextall F.
1965 1970 1975 1980 1985 1990 1995 2000 2005
Wales, Roberts D
Year

Fig 3. The incidence of basal cell carcinoma (BCC) in European males over time. All incidence rates are standardized to the world population.

Incidence of SCC in European males


35
Denmark, Osterlind A

Finland, Hannuksela-Svahn A
30
Incidence of SCC per 100 000 persons

Germany, Schleswig-Holstein,
Katalinic A
25 Germany, Saarland, Stang A
Germany, Northrhine-Westphalia,
Stang A
20 Italy, Boi S
Netherlands, Coebergh J
15 Norway, Iversen T

Scotland, Brewster D
10
Slovakia, Plesko I

Sweden, Wassberg C
5
Switzerland, Levi F

0 Wales, Holme S
1950 1960 1970 1980 1990 2000 2010
Wales, Roberts D
Year

Fig 4. The incidence of squamous cell carcinoma (SCC) in European males over time. All incidence rates are standardized to the world population.

North America Five studies standardized to the U.S. population postal survey found an almost identical pattern in
were found.13,22,35,40,65 A divide in incidence rate of SCC was SCC6,7,32,52 as was seen with BCC, relating to a gradual
seen according to latitude, although the overall trend is less increase since 1985, with the rate of increase slowing over
clear than that seen with BCC rates. A study in Arizona based time. In 2002, the rate of combined male and female SCC
on a histologically verified cancer registry showed a gradual was 387 ⁄100 000 person-years.6 Much higher incidence rates
decline in incidence of SCC from 1985 to 1991 to a steady of SCC were observed in the Nambour and Townsville study
level of approximately 290 ⁄100 000 person-years.35 New populations,19,33,58,63 with a world-standardized incidence
Mexico reported an increasing incidence of SCC,13 the rate of rate of 1035 ⁄100 000 person-years in males living in Nam-
increase being approximately the same as in the Northern state bour from 1985 to 1992.33 However, as with BCC, these
of New Hampshire.40 As with BCC, much lower incidence much smaller populations are not representative of the
rates were found in the Northern than in the Southern country as a whole.
states.13,22,35,40,65 In Alberta, Canada, rates increased from
45Æ0 ⁄100 000 person-years in 1988 to 60Æ2 ⁄100 000 person-
Discussion
years in 2006.78
This systematic review brings together 75 papers on the inci-
Australia Seven comparable studies were found that stated the dence of NMSC and is the largest systematic review to date on
incidence of SCC in Australia.6,7,19,32,33,52,58 The national the subject.

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Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al. 1077

The NICE guidelines to establish the true nature of NMSC wide. This theory is further supported by the very low inci-
epidemiology are complex. Cancer registries are certainly dence rates observed close to the equator in countries such as
improving practices following guidance but more should be Singapore.66
done to bring NMSC epidemiology in line with other invasive Australia has by far the highest incidence of BCC in the
diseases. A particular area of focus should be the encourage- world. Although intermittent UVR exposure is more important
ment of general practitioners to send all excised material for than total exposure in BCC aetiology,83 the very high UVR
histological confirmation. Incidence studies such as those com- levels in Australia are likely to be raising the incidence rates to
pared in this review should, as a minimum, standardize all the levels observed in this review. Support for this theory can
rates to a common population, use histological confirmation be found in the NMSC subtype proportions. The BCC : SCC
and provide basic information such as the unit of analysis (by ratio in Australia is approximately 5 : 2.7 In the U.K., the BCC
tumour or by patient). This will allow much more accurate : SCC ratio is 4 : 1.42 As Australians are exposed to long-term
comparison at both national and international levels. UVR, they are more likely to develop SCC than in other coun-
Variations in ethnicity may partly explain the BCC distribu- tries such as the U.K., where intermittent exposure is more
tion in the U.K. There is a comparatively large nonwhite common.
population in the South-East of England.82 Darker skin types The distribution of SCC in the U.K. is similar, but not iden-
have a much lower risk of BCC and this may be reflected by tical, to that of BCC, highlighting differences in the aetiology
the registry data. If the registries could divide the data by of the two tumours. London has the lowest SCC incidence in
county as opposed to Strategic Health Authority then the con- the U.K., although this is still not as low as the incidence of
tribution of ethnicity may be clearer. The South-West of Eng- BCC. According to the registry data, the South-West again
land is associated with the highest UVR exposure and also appears to report the highest incidence of SCC. Rates across
reports the highest incidence of BCC. the North of the country are generally similar, with the West
It is possible that the variation seen in the U.K. data is due Midlands reporting a slightly lower rate. The same registry
to variation in registration practice. Poor registration is highly also reported a lower than expected rate for BCC so it is possi-
likely to be the cause of the extremely low rates seen in the ble that this area is more affected by under-reporting than
South-East of England. Although this reduces the utility of the other areas.
comparisons here, it does highlight well the issues of NMSC The division between Northern and Southern states in the
registration in the U.K. and gives good evidence that registra- U.S.A. persists in the SCC data and again is almost certainly
tion procedures must be vastly improved and standardized. due to differences in UVR levels. According to the authors,
Although the different standard populations prevent direct the gradual decrease seen in Arizona35 may not be representa-
comparisons of incidence, the rate of increase can be exam- tive of the whole state and incidence may be increasing in
ined. BCC incidence is increasing by approximately other regions.13 As is the case in Europe, SCC rates are
1 ⁄100 000 persons per year in mainland Europe;34,48,57 how- increasing but not as rapidly as for BCC.
ever, the incidence in the U.K. is increasing at a rate of A potential area for future review is the variation in use of
approximately 6 ⁄100 000 persons per year.15,42 This differ- sun protection and sun exposure behaviour worldwide and
ence in the rate of increase is not discussed in the literature the correlation with NMSC incidence rates over time. These
and should be examined in the future. factors are highly likely to contribute to the geographical vari-
When comparing the incidence rates in mainland Europe, ation in rates reported here.
all countries appear to be similar with Switzerland and Italy This is the largest systematic review of incidence studies to
reporting slightly higher rates.17,50 Switzerland has the highest date regarding NMSC. The size and completeness is a key
average altitude in Europe and as such will have higher UVR strength that allows comparisons on a level not previously
levels. UVR levels in Italy are also likely to be high due to the possible. The inclusion and exclusion criteria also succeeded
low latitudes and high-altitude Northern regions bordering in providing enough studies to create a narrative without
Switzerland. Manitoba lies at a similar latitude to the U.K. and threatening validity. The U.K. registry data provide an interest-
should in theory have similar levels of UVR. In 2000, the ing comparison that other reviews do not include and help to
world-standardized male BCC incidence rate was highlight the rapidly increasing incidence rate in the U.K.
93Æ9 ⁄100 000 person-years4 which, although at the higher compared with Europe.
end of the European figures, fits the trend observed here. The main limitation encountered when making comparisons
The best evidence for increasing BCC incidence with was the different standard populations used. Although these
decreasing latitude is seen in North America where the divide different populations cannot account for large differences
between the Northern and Southern states is clear. Rawashdeh observed between countries, they do prevent comparisons
and Matalka60 conducted a U.S.-standardized BCC incidence between countries lying at similar latitudes. The main source
study in Jordan from 1991 to 2000 and reported incidence of error in this review is differences in data collection. Cancer
rates of just 8Æ8 ⁄100 000 person-years (both sexes combined). registries will be affected by under-reporting to a greater
Jordan lies at a similar latitude to North America. This large extent than studies performed in the community. Without
difference in incidence rate illustrates the effect that skin type histological confirmation, the incidence is also likely to be
has on the geographical distribution of incidence rates world- overestimated. Although these issues would present a problem

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BJD  2012 British Association of Dermatologists 2012 166, pp1069–1080
1078 Worldwide incidence of nonmelanoma skin cancer, A. Lomas et al.

for a detailed statistical analysis, they are less of a problem for


a descriptive narrative such as this. Whenever studies were
compared, care was taken to ensure that the studies were What’s already known about this topic?
based on similar methodologies. For example, a study count- • The incidence rate of nonmelanoma skin cancer is high
ing number of patients would not be compared with a study compared with other malignancies and is increasing.
counting number of tumours. • The current best source of incidence data comes from
The data presented here provide a good representation of many observational studies of populations in a defined,
NMSC incidence in white populations. There have, however, often small, geographical location.
been very few good epidemiological studies undertaken in • Incidence rates vary geographically according to various
lower latitude regions such as Africa. These regions contain a factors including ultraviolet radiation exposure, sun-
very wide range of ethnicity resulting in a wide range of inci- seeking behaviours and skin type.
dence rates. The incidence studies that have been located all • Recent National Institute for Health and Clinical Excel-
use very different methodologies, rendering comparisons ex- lence guidelines recommend research in basal cell carci-
tremely difficult. Any future studies should aim to include the noma epidemiology and improved tumour registration
information discussed above in order to allow accurate com- practice.
parison internationally, particularly as NMSC incidence data
from cancer registries is likely to be highly limited.
This review focuses exclusively on nonmelanoma malignan- What does this study add?
cies and does not cover the incidence of melanoma. Melanoma
skin cancer receives a much higher level of registration and • This is the largest and most complete systematic review
was not included in the majority of the papers reviewed here. in this field to date.
The substantial variation between BCC and SCC incidence rates • This is the first review that has pulled together all obser-
is caused by the differences in their aetiology. Melanoma has vational studies in a systematic way.
a different aetiology again, rendering any comparisons • The review highlights the high and increasing incidence
between the diseases much less relevant. rates in the U.K. compared with other European coun-
In conclusion, in white populations, NMSC has the highest tries.
incidence of all cancers. Despite this it is rarely included in • These findings are important as they highlight the need
national cancer statistics and there are very few papers looking for early prevention.
at incidence rates in each country. Although NMSC does have
a low mortality rate, it still has a significant impact on quality
of life and is placing a large financial burden on health care
services. Acknowledgments
All the registry data were provided with warnings of under- The authors extend their thanks to Dr Sean McPhail of the South
reporting and problems with multiple tumour registration. West Cancer Intelligence Service for the provision of NMSC in-
The fact that Wales does not officially publish any NMSC data cidence data from every cancer registry in England. We also
indicates that current registry guidelines are not sufficient in acknowledge Mr Jeremy Hinds for his invaluable assistance in
obtaining accurate measurements. producing the maps displaying the U.K. incidence data.
A recent update to NICE guidelines8 highlighted the need
to establish the true epidemiology of NMSC. This review
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