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Climate change, ozone depletion and the impact on ultraviolet exposure of human skin

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2004 Phys. Med. Biol. 49 R1

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INSTITUTE OF PHYSICS PUBLISHING PHYSICS IN MEDICINE AND BIOLOGY
Phys. Med. Biol. 49 (2004) R1–R11 PII: S0031-9155(04)68692-1

TOPICAL REVIEW

Climate change, ozone depletion and the impact on

ultraviolet exposure of human skin
Brian Diffey
Regional Medical Physics Department, Newcastle General Hospital, Newcastle NE4 6BE, UK

E-mail: b.l.diffey@ncl.ac.uk

Received 4 September 2003

Published 15 December 2003
Online at stacks.iop.org/PMB/49/R1 (DOI: 10.1088/0031-9155/49/1/R01)

Abstract
For 30 years there has been concern that anthropogenic damage to the Earth’s
stratospheric ozone layer will lead to an increase of solar ultraviolet (UV)
radiation reaching the Earth’s surface, with a consequent adverse impact on
human health, especially to the skin. More recently, there has been an increased
awareness of the interactions between ozone depletion and climate change
(global warming), which could also impact on human exposure to terrestrial
UV. The most serious effect of changing UV exposure of human skin is the
potential rise in incidence of skin cancers. Risk estimates of this disease
associated with ozone depletion suggest that an additional peak incidence of
5000 cases of skin cancer per year in the UK would occur around the mid-part
of this century. Climate change, which is predicted to lead to an increased
frequency of extreme temperature events and high summer temperatures, will
become more frequent in the UK. This could impact on human UV exposure
by encouraging people to spend more time in the sun. Whilst future social
trends remain uncertain, it is likely that over this century behaviour associated
with climate change, rather than ozone depletion, will be the largest
determinant of sun exposure, and consequent impact on skin cancer, of the
UK population.

1. Introduction

The sun is responsible for the development and continued existence of life on Earth. The sun’s
infrared rays warm us and we can see with eyes that respond to the visible part of the sun’s
spectrum. More importantly, visible light is essential for photosynthesis, the process whereby
plants, necessary for our nutrition, derive their energy. Besides serving as the ultimate source
of our food and our energy, sunlight also acts on us to alter our chemical composition, control
the rate of our maturation and drive our biological rhythms (Wurtman 1975). However the
0031-9155/04/010001+11$30.00 © 2004 IOP Publishing Ltd Printed in the UK R1
R2 Topical Review

ultraviolet (UV) component, which comprises approximately 5% of terrestrial solar radiation,

is largely responsible for the deleterious effects associated with sun exposure. In particular, the
shorter wavelengths of terrestrial UV radiation (UVB waveband: 280–315 nm) are especially
damaging. A major influence on the spectral irradiance of this waveband reaching the Earth’s
surface is stratospheric ozone. More recently, there has been an increased awareness of
the interactions between ozone depletion and climate change (global warming), which could
impact on human exposure to terrestrial UV.

2. Trends in atmospheric ozone and ambient ultraviolet radiation

Significant global scale decreases in total ozone have been occurring since the late 1970s,
and the loss of ozone in the northern hemisphere in the 1990s was proceeding with a rate of
loss over mid-latitudes (30–50 ◦ N) seen in winter and early spring of about 6% per decade.
The loss in summer months, when UV levels are much higher and people are exposed more
frequently to the sun, is less at about 3% per decade (United Nations Environment Programme
1998). At mid-latitudes ozone depletion now appears to be levelling off with losses reported
in the northern mid-latitudes of about 4% in winter/spring and 2% in summer/autumn (WMO
2003). Evidence continues to appear indicating that the rate at which ozone is being destroyed
in the upper stratosphere is slowing (Newchurch et al 2003).
Calculations for the northern hemisphere based on the measured ozone trends for the
period 1979–1992 indicate that, all other factors being constant, the terrestrial erythemally-
effective UV radiation (which lies mainly within the UVB waveband) should have increased
by less than 1% per decade at 15 ◦ N to about 3% per decade at 30–40 ◦ N and 5% per decade
at 50–60 ◦ N decade (United Nations Environment Programme 1998).
Paradoxically these predictions have not generally been borne out by ground based UV
monitoring programmes (Diffey 1996, Kerr and Seckmeyer 2003). Reasons (Weatherhead
1996) offered to account for this apparent discrepancy include the limited period of most UV
monitoring networks, accuracy of instrument calibration and long-term stability of monitoring
equipment, year-to-year fluctuations in cloud cover, and an increase in ozone and aerosols
present in the lower atmosphere due to pollution. However, international inter-comparisons
between instrumentation are improving data quality and reliability (McKenzie et al 2003).
As an example of the uncertainty concerning long-term trends, ground-based measurement
data of erythemal UV radiation1 using broad-band filter radiometers obtained in the period
1989–2002 by the UK National Radiological Protection Board (Driscoll 2003) at Chilton
(latitude 51.5 ◦ N) indicate an upward trend of 12% per decade with a 95% confidence interval of
3–20% encompassing the predicted (United Nations Environment Programme 1998) increase
of 5% per decade (see figure 1). The observed upward trend may simply be a consequence
of the confounding factors, especially cloud cover, described above rather than a result of
increasing terrestrial UV as a direct result of ozone depletion, or possibly a combination of
both.
As a surrogate for cloud cover, figure 1 also shows the annual number of hours of bright
sunshine recorded at the Radcliffe Meteorological Station in Oxford (30 km distance from
NRPB’s station at Clinton) for the same period. There is a weak association (P = 0.19;
Spearman’s rank correlation coefficient) between annual ambient UV and hours of bright
sunshine, suggesting that the rising trend of UV is only partly explained by similar changes in
1 The unit of erythemal radiation is the SED (standard erythema dose) (CIE Standard 1998); it requires an exposure

of about 3 SED to produce just perceptible reddening of skin (erythema) in the unacclimatized white skin of the most
common northern European skin types (Harrison and Young 2002). An exposure of 5–8 SED will result in moderate
sunburn and 10 SED or more can result in a painful, blistering sunburn.
Topical Review R3

Figure 1. Ambient annual erythemal UV measured at Chilton, UK (solid line) (Driscoll 2003)
and hours of bright sunshine (broken line) recorded at the Radcliffe Meterological Station 30 km
distant for the same period (http://www.geog.ox.ac.uk/research/rms/series.html).

cloud cover and so, in part, might well be a manifestation of changes expected as a consequence
of ozone depletion.
Just how the climatology of terrestrial UV is predicted to change in the future as
a consequence of changes not only in total ozone but also other atmospheric variables
that are influenced by changes in climate, is addressed in a recent UNEP/WMO report
(Kerr and Seckmeyer 2003). Results of model calculations indicate that generally there will
be small changes in ambient UV over the next decade. By the mid-part of this century, UV
levels will return to values close to those in 1980, provided all other factors remain constant.
This assumption is unlikely and factors that could influence recovery include non-compliance
with the Montreal protocol and subsequent amendments, interactions between ozone depletion
and global warming, and future volcanic eruptions.

3. Effects of ultraviolet radiation on skin

Whilst the normal responses of skin to UV radiation are largely deleterious to health, there are
some real and perceived benefits of solar UV exposure.

3.1. Production of vitamin D

The only well-established beneficial effect of solar UV on the skin is the production of
vitamin D3 required for skeletal health. The skin absorbs UVB radiation in sunlight to convert
sterol precursors in the skin, such as 7-dehydrocholesterol, to vitamin D3. Vitamin D3 is
further transformed by the liver and kidneys to form 1,25-hydroxyvitamin D, the biologically
active form of vitamin D that is responsible for increasing the efficiency of intestinal calcium
absorption (Holick 2001). There is some suggestion that increased production of 1,25-
hydroxyvitamin D may protect against colon, breast and prostate cancer (Holick 2001) and
that exposure to UVB with subsequent effects on vitamin D levels may protect against acute
myocardial infarction (Ness et al 1999), reduce blood pressure (Kraus et al 1998) and reduce
the risk of multiple sclerosis (van der Mei et al 2003).
R4 Topical Review

3.2. Tanning and hyperplasia

A consequence of exposure to solar UV, which at present still seems to be socially desirable,
is the delayed pigmentation of the skin known as tanning, or melanin pigmentation. Melanin
pigmentation of skin is of two types:
• constitutive—the colour of the skin seen in different races and determined by genetic
factors only;
• facultative—the reversible increase in tanning in response to sun exposure.
In addition to tanning, the skin is capable of another perhaps even more important adaptive
response that limits damage from further UV exposure—epidermal thickening or hyperplasia.
This begins to occur around 72 h after exposure, is a result of an increased rate of cell division
in the lower epidermis, and eventually results in thickening of both epidermis and stratum
corneum (the outermost layer of the epidermis) that persists for several weeks. This adaptive
process, unlike tanning, does not depend on a genetic predisposition and is the major factor
that protects those who tan poorly in sunlight.
Whilst these processes are, or may be perceived to be, a desirable consequence of
sun exposure, the remaining three—sunburn, skin cancer and photoageing—are universally
recognized to be adverse effects of sun exposure.

3.3. Sunburn
Erythema, or redness of the skin due to dilatation of superficial dermal blood vessels, is the
commonest and most obvious effect of UV exposure (‘sunburn’). Following exposure to solar
UV radiation, there is usually a latent period of 2–4 h before erythema develops. Erythema
reaches maximum intensity between 8 and 24 h after exposure, but may take several days to
resolve completely. If a high enough exposure has occurred, the skin will also become painful
and oedematous, and blistering may result.

3.4. Skin cancer

The three common forms of skin cancer, listed in order of seriousness are basal cell carcinoma
(BCC), squamous cell carcinoma (SCC) and malignant melanoma (MM). Around 90% of skin
cancer cases are of the non-melanoma variety (BCC and SCC) with BCCs being approximately
four times as common as SCCs. Exposure to UV radiation is considered to be a major
etiological factor for all three forms of cancer (International Agency for Research on Cancer
1992). For basal cell carcinoma and malignant melanoma, neither the wavelengths involved
nor the exposure pattern that results in risk have been established with confidence; whereas
for squamous cell carcinoma, both UVB and UVA are implicated and the major risk factors
seem to be cumulative lifetime exposure to UV radiation and a poor tanning response.
Squamous cell cancer. The evidence that exposure to sunlight, even without ozone depletion, is
the predominant cause of squamous cell cancer in man is very convincing. These cancers occur
almost exclusively on sun-exposed skin such as the face, neck and arms, and the incidence
is clearly correlated with geographical latitude, being higher in the more sunny areas of the
world (Kricker et al 1994). Epidemiological studies suggest that sun exposure in the 10 years
prior to diagnosis may be important in accounting for individual risk of SCC (Gallagher et al
1995a).
Basal cell cancer. The relationship between basal cell carcinoma and sunlight is less
compelling, but the evidence is sufficiently strong to consider it also to be a consequence
Topical Review R5

of exposure to sunlight. Whilst SCC is strongly related to cumulative lifetime exposure to

sunlight, this relationship is not so convincing for BCC (Gallagher et al 1995b, Kricker et al
1995), and it may be that sun exposure in childhood and adolescence may be critical periods
for establishing adult risk for BCC (Gallagher et al 1995b).
Malignant melanoma. During the past 50 years or so there has been an increase in the
incidence of malignant melanoma in white populations in several countries. There exists
an inverse relationship between latitude and melanoma incidence and this has been taken as
evidence for a possible role of sunlight as a cause of malignant melanoma. However, this
pattern is not always consistent. In Europe, for example, the incidence and the mortality rates in
Scandinavia are considerably higher than those in Mediterranean countries. This inconsistency
may reflect ethnic differences in constitutional factors and customs. Also, the unexpectedly
low incidence in outdoor workers, the sex and age distribution, and the anatomical distribution
have pointed to a more complex association (Armstrong and Kricker 1994).
There is now growing evidence that intermittent sun exposure—mainly from recreational
activities—rather than cumulative or chronic exposure associated with occupation is associated
with increased risk of developing malignant melanoma. Several studies have established a
history of sunburn as an important risk factor for melanoma development, although in these
studies a potential for recall bias exists. Migration studies have led to the suggestion that sun
exposure in childhood is a particularly critical period in terms of melanoma risk.

3.5. Photoageing
The clinical signs of a photo-aged skin are: dryness, deep wrinkles, accentuated skin furrows,
sagging, loss of elasticity, mottled pigmentation and telangiectasia (Leyden 1990). Chronic
solar exposure is the major environmental insult that contributes to photoageing, and is quite
distinct from chronological, or intrinsic, ageing. Extrapolating from experimental studies
using animal models of photodamage (Kligman 1995), the action spectrum for photoageing in
human skin probably encompasses the UVB and UVA wavelengths, and so changes in UVB
as a consequence of ozone depletion may have some impact.

4. Risk estimates of human skin cancer associated with ozone depletion

The most sophisticated attempt to estimate the impact of ozone depletion on skin cancer
incidence was given by Slaper et al (1996) and subsequently reported in the 1998 UNEP
assessment (United Nations Environment Programme 1998). These estimates suggest that
the increased risk of skin cancer due to ozone depletion would not have been adequately
controlled by implementation of the Montreal Protocol alone, but can be achieved through
implementation of its later amendments. They indicate that under the Montreal Amendments,
incidences of skin cancer (all types) in north-west Europe will peak around the mid-part of
this century at an additional incidence of about 90 per million. For the UK population of
approximately 60 million this would imply about 5000 additional cases of skin cancer per
year, which represents a relative increase in risk of about 8% compared to current incidence
of around 60 000. Thereafter the increase in disease rates attributable to ozone depletion is
expected to return almost to zero by the end of the next century; as skin cancer typically results
from several decades of UV exposure the response of the disease follows later than changes
in exposure.
It should be noted that the calculated risks do imply full compliance with restrictions on
the production and consumption of ozone-depleting chemicals throughout the world. If, in
R6 Topical Review

Figure 2. Overseas holidays taken by British residents in the period 1971–1998 (Office of National
Statistics 1998a) (closed squares) and skin cancer incidence in England and Wales in the period
1980–1992 (open triangles).

the future, compliance does not continue, damage to the ozone layer could be greater than
hitherto expected and biological impacts could be more severe (UNEP 1998).
These quantitative risk estimates for skin cancer are only valid if all other factors that
determine risk, notably human behaviour, remain unchanged. This is extremely unlikely given
that skin cancer rates in the UK have been rising through the 1980s and 1990s with a doubling
time of 16 years (figure 2), presumably as a consequence of changes in outdoor exposure and
fashion over the preceding 50 years or so. If the same trend should continue then by 2050, the
peak of the predicted effect of ozone depletion on skin cancer incidence (Slaper et al 1996),
the additional cases due to this effect will only be 1% of the naturally occurring incidence at
that time. Given the uncertainties that exist with regard not only to atmospheric change but
equally to human behaviour, it is likely to prove impossible to look back at the end of this
century and be certain what effect ozone depletion had on skin cancer incidence worldwide.

5. Climate change and UV exposure

Most attention has been given to the effects of changes in terrestrial UV radiation as a result
of stratospheric ozone depletion. What has frequently been overlooked is that greenhouse-gas
induced climate change can also influence ambient UV through the indirect influence of global
warming on total ozone, and the effect of climate changes that modify ambient UV through
influences on other variables such as clouds and aerosols (Kerr and Seckmeyer 2003).
More significantly, the impact of changes in ambient temperature will influence people’s
behaviour and the time they spend outdoors. A change to warmer conditions is predicted
to occur in the UK (Hulme et al 2002), for example, where the average annual temperatures
may rise by between 2 ◦ C and 3.5 ◦ C by the 2080s. These average temperature changes will
be accompanied by an increased frequency of extreme temperature events and high summer
temperatures, such as experienced in the summer of 2003, will become more frequent. Also,
it is not just temperatures that will change in the UK, but also rainfall amounts and frequency.
Winters will become wetter and summers may become drier across all of the UK.
Clearly such changes in climate could encourage behaviour that would increase population
exposure to sunlight and the health risks associated with it. For example, a study that reported
Topical Review R7

the exposure of schoolchildren to sunlight in different regions of the UK (Diffey et al 1996)

showed that differences in personal UV exposure were greater than differences in ambient
UV, with children in the south-west of England receiving recreational UV exposures that
were a higher percentage of ambient than children living in the colder north-east of England.
This suggests that factors other than ambient UV, such as climate and ambient temperature,
influence behaviour and hence skin exposure.
In a behavioral study in Australia (Hill and Boulter 1996), it was observed that the
likelihood of sunburn approximately doubled when the ambient temperature was 19–27 ◦ C,
compared to temperatures of 18 ◦ C or lower (currently typical average maximum summer
temperatures in the UK). The reason for this is presumably because warmer temperatures
encourage people to spend more time in direct sunlight with the increased risk of sunburn.
Interestingly, the study found that at temperatures in excess of 27 ◦ C, the likelihood of sunburn
fell again as people sought shade for comfort reasons.

6. Climate change and skin cancer

Studies in experimental animals have shown that elevated temperatures enhance UV-induced
skin cancer in comparison with that at room temperature. In an intriguing analysis, assuming
that ambient temperature would have a similar effect in humans, van der Leun and de Gruijl
(2002) speculated that long-term elevation of temperature by 2 ◦ C as a consequence of climate
change would increase the carcinogenic effectiveness of solar UV by 10%. The resulting
increase in skin cancer would be steeper since the incidence of skin cancer increases in an
approximately quadratic manner with UV exposure (van der Leun 1984).
Hence this synergistic interaction between ozone depletion and global warming would
enhance the excess incidence by about 20%, which would result in the excess skin cancers in
the UK increasing from an estimated 5000 to 6000 cases per year by 2050.
The authors discuss the underlying assumptions in their calculations but conclude that
with the protection of the ozone layer now well-established, the effect of rising temperatures
on skin cancer incidence may soon be greater than that of ozone depletion, and that this effect
will increase with further rises in temperature. Clearly efforts analogous to the Montreal
protocol are needed to mitigate the adverse consequences of climate change on human skin.

7. Behavioural influences on exposure to solar ultraviolet radiation

The solar UV radiation to which an individual is exposed depends upon (Diffey 1999):

• ambient solar UV radiation,

• behaviour and time spent outdoors,
• use of photoprotective agents, such as sunscreens, that modify exposure.

From a number of studies measuring personal exposure to solar UV in northern Europe, it

can be inferred that adult indoor workers receive an annual exposure of around 200 SED
mainly from summer weekend and holiday exposure (International Agency for Research on
Cancer 2001), and principally to the hands, forearms and face. How this exposure is received
during different times of the year and activities is shown in figure 3. During adult life an
indoor worker in the UK might typically receive 30% of their annual UV exposure from sun-
seeking holidays, 40% from summer weekends, 20% from casual weekday exposure between
April and September, and just 10% from sun exposure during the 6-month period October to
March.
R8 Topical Review

Figure 3. Typical daily UV exposure of adult indoor workers in Northern Europe.

Children have more opportunities to be outside than adults and dosimetric studies (Diffey
1999) indicate northern European children typically receive around 300 SED per year. Hence,
sun exposure up to the age of 18 years constitutes roughly one-third of lifetime exposure.
However, with the trend for earlier retirement, greater life expectancy and higher disposable
income with opportunities for overseas travel, we may see this fraction diminish as the sun
exposure in late middle age and onwards contributes a larger fraction than hitherto of lifetime
UV exposure.

7.1. Trends in sun exposure

Whilst climatological factors may influence the levels of UV radiation at the Earth’s surface,
it is the behaviour of people outside which will have a much greater impact on personal
UV exposure. Consequently, efforts are being made in a number of countries to understand
people’s behaviour in the sun with a view to developing strategies to encourage them to limit
their exposure to acceptable values (Morris and Elwood 1995).
Lifestyles are changing in a way that impact on personal exposure to the sun and the use of
photoprotective measures. The number of overseas holidays has increased dramatically with
a 7-fold increase in the number of overseas holidays taken by British residents in the period
1971–98 (Office of National Statistics 1998a) (figure 2). Furthermore, in recent years the most
rapid increases in foreign holiday travel have been to long-haul destinations at low-latitude
destinations where UV levels are typically high. For example, holiday visits to the USA
(where Florida is the most popular destination) increased 15-fold in the 20 years up to 1997.
It, therefore, seems likely that changing patterns of holidaymaking continue to be an important
factor tending to increase the overall UV doses received by the UK population and associated
health risks. Coupled with this is the growth in outdoor leisure activities with consequential
increases in sunlight exposure (Office of National Statistics 1998b).
Public health campaigns aimed at encouraging people to reduce their sun exposure by sun
avoidance and the use of photoprotective measures such as sunscreens, clothing and shade,
may achieve a reduction in average population UVB exposures, and presumably skin cancer
rates, which could more than offset the adverse effects of ozone depletion (Hill and Boulter
1996).
Topical Review R9

7.2. Global solar UV index

An internationally-agreed mechanism for informing the public about UV levels is the global
solar UV index (World Health Organization 2002), which estimates the average maximum
solar UV at the Earth’s surface. While the intensity of UV reaching the ground varies during
the day, it reaches a maximum, when there is no cloud cover, around midday. The calculation
of the UV index allows for the wavelength-dependant nature of UV erythema and averages out
variations over a 10–30 min time span. The index is generally presented as a forecast of the
maximum amount of erythemal UV expected to reach the Earth’s surface at solar noon.
The values of the index range from zero upward and the higher the index number, the greater
the likelihood of skin damaging exposure to UV, and the less time it takes for damage to occur.
In many countries close to the equator, summer-time values can range up to 20. During the
European summer the index is generally not more than about 8, but can be higher, especially at
beach resorts where there may be less urban tropospheric pollution. The following descriptions
are usually associated with various values of the index: low UV exposure—1 and 2; moderate
exposure—3 and 4; high exposure—5 and 6; very high exposure—7 and 8; extreme exposure—
greater than 9.
In a survey carried out in the UK in 1999 by the Office of National Statistics (Office of
National Statistics 1999), 64% of respondents had heard of the UV index, the television weather
forecast being the most common source of information, although only 7% of respondents were
able to correctly interpret the index. Yet despite this there was encouraging evidence to indicate
that hearing about the UV index, even though understanding was poor, did encourage greater
use of sun protective measures, especially sunscreens.

7.3. Sunscreens
Some preventive measures may not be as effective as commonly believed; this is especially
true of sunscreens. In April 2000, a Working Group of 23 international experts convened at the
International Agency for Research on Cancer in Lyon to evaluate published data on the cancer-
preventive effect of sunscreens. The conclusions of the Working Group were (International
Agency for Research on Cancer 2001):
• Sunscreens probably prevent squamous cell carcinomas of the skin when used mainly
during unintentional sun exposure.
• No conclusion can be drawn about the cancer preventive activity of topical use of
sunscreens against basal cell carcinoma and cutaneous melanoma.
Of concern is that the majority of case-control studies suggest that sunscreen use is
associated with an increased risk of melanoma (International Agency for Research on Cancer
2001). The reasons for this observation are not fully understood. One of several possibilities is
that sunscreen use encourages people to stay in the sun longer coupled with fact that inadequate
amounts of sunscreen are normally applied and/or areas of the body are missed (Diffey 2001).
However, these studies are difficult to interpret because of problems of positive confounding
(e.g. people who are at most risk of burning and most likely to develop melanoma are also
most likely to use sunscreens) and negative confounding (e.g. sunscreen users may also use
other methods of sun protection such as clothing and shade).

8. Conclusion

In conclusion, climate change could have a greater impact on future skin cancer incidence
in northern Europe than ozone depletion. This would be due more to changes in behaviour
R10 Topical Review

encouraging more time in the sun than increases in ambient UV. Future social trends remain
uncertain but the sun exposure of northern Europeans is likely to continue to increase due to
sun-seeking holidays coupled with over-reliance on the efficacy of sunscreens. As a result, skin
cancer incidence is likely to continue to rise, but as a result of behavioural factors consequent
to, rather than directly attributable to, environmental changes.

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