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
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.
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)
No standardization used
No standardization used
nonmelanoma skin cancer (NMSC), basal cell carcinoma (BCC) and
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
Not specified
confirmation
Partly
Partly
Partly
Partly
Yes
Yes
No
Network of physicians
Cancer Survey
Cancer registry
Cancer registry
Cancer registry
Cancer registry
1971–1980
1958–1995
1961–1995
1988–2005
2001
4923¢N
5125¢N
1942¢N
3904¢N
5919¢N
6007¢N
5126¢N
2516¢S
2516¢S
1942¢S
latitude
121¢N
Whole country
Whole country
Whole country
One hospital
Stockholm
Qld
Australia
Country
Sweden
Sweden
Greece
the two regional studies are not likely to represent the whole
U.S.A.
Wassberg74
Wallberg73
Stenbeck69
Valery71
Staples6
Staples7
Stang67
Stang68
where else in the world. The national surveys showed that the
Sng66
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
Denmark, Osterlind A.
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.
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.
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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