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Stratospheric ozone depletion and the risk of non-melanoma skin cancer in a British population
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Php. Mod. Biol., 1992, Vol. 37, NO 12, 2267-2279. Printed in the UK
Stratospheric ozone depletion and the risk of non-melanoma skin cancer in a British population B L Diffey Regional Medical Physics Department, Drybum Hospital, Durham DHI .Try UK Received 24 July 1992 Abstract Quanlitative estimation of the increased dsk of non-melanoma skin cancer (NMX) in British people that may result from depletion of the stratospheric m n e layer is given for the w e n t generation of British people. For adults alive today mntinuing ozone depletion at wrrent rates is predicted to m u l l in a relatively small additional lifetime risk (C 5%) of N m , asuming no changes in climate, lime spent outdoors, behaviour or clothing habits. The lifetime risk incurred lq loday's children, however, is 1 0 9 ~ 4 5 %greater than expected in the absence of m n e depletion. However, if lhe produclion and Use of substances which deplete ozone are reduced, as expected under lhe arrent provisions of the Montreal Pralocol, the increased lifetime lisk of skin cancer is tikely U, be less than this estimate. n e s e predicled increases in ri&, resulting h m grealer salar ultraviolet exposure, can be offset bj adopting changes to behaviour during the summer months which may involve spending Igs time outdoors, wearing appropriate clothing including widc-brimmed hats, applying topical Sunscreens, or a combination of these.
1. Introduction
Skin cancers are the most common human cancer and their incidence is increasing in many countries, including the UK. Each year about 30aM people in Britain are said to develop skin cancers (CRC 1991), although because of under-recording of non-melanoma skin cancerb (NMSC) in the LJK, the incidence may be as much as three times this figure (Lloyd Roberts 1990). It is well recognized that chronic exposure to sunlight is a causal factor in the development of human skin cancer, particularly non-melanoma skin cancers (NMsC). Concern has been expressed widely that depletion of stratospheric ozone by chemical reactions involving the degradation products of chlorofluorocarbons will lead to a rise in the incidence of skin cancers as a consequence of increased levels of solar ultraviolet radiation (UVR) at the Earth's surface (UNEP 1991, Russell Jones 1987, MacKie and Rycroft 1988). 2. Ozone and terrestrial ultraviolet radiation
Significant global scale decreases in total ozone occurred during the period 1979-1989 (UNEP 1991, Science and Policy Associates, Inc 1992) and the loss of ozone in the northern hemisphere is now proceeding faster than previously thought with a rate of loss over mid-latitudes (3O06OoN)seen in winter and early spring of about 8% 0031-9155/92/lU267+13sO7.S0 @ 1992 IOP Publishing I l d
2267
2268
B L Diffq
per decade (SORG 1991). Measurements of total column ozone at several ground stations in Europe during the period November 1991 to February 1992 reported values ranging from 0% to 20% below average for the winter months (EASOE 1992). The loss in summer months, when uv levels are much higher and people are exposed more frequently to the sun, is less at about 2 % 4 % per decade. Calculations for the northern hemisphere based on the measured ozone trends for the period 1979-1989 indicate that, all other factors being constant, the terrestrial carcinogeniceffective W R (which lies mainly within the ultraviolet B waveband of 280-315 nm) should have increased by about 1.3% to 4.7% during this decade (Madronich 1992). Paradoxically these predictions have not been borne out by ground-based W monitoring programmes. Analysis of a 12 y record of ambient WB measured at eight stations in the USA showed a slight downward trend of -0.4% to -1.1% per year (Scotto el of 1988). The largest contribution to annually averaged ultraviolet levels occurs during the summer when stratospheric ozone depletion is at its least. firthermore year-to-year fluctuations in cloud cover and an increase in ozone present in the lower atmosphere due to pollution (Bruhl and Crutzen 1989) make it not surprising that no statistically significant increase in ambient WB has yet been demonstrated. However, measurements of ambient UVB in the Swiss Alps at an altitude of 3576 m above sea level, and where the atmosphere is much clearer than in urban areas at lower altitudes, indicate that there has been a slight increase of about 0.7% per year during the 1980s (Blumthaler and Ambach 1990). The authors ;:::',bated this smi!! i!creae to n n n e depletion. In the southern hemisphere the influence of Antarctic ozone depletion on ambient UVB in Melbourne (latitude 38'S) has been reported by Roy and Gies (1992). Continuous monitoring of ambient WB showed that the levels recorded in February 1991 were 37% and 27% higher than for the Same month in 1990 and 1989, respectively. February 1991 had the lowest ozone values recorded for this period, but also very low cloud cover compared with recent years. These two important factors reinforce each other and illustrate the difficulty of separating the effects of ozone depletion from climate on ambient WB. Long-term stability of monitoring equipment is essential if reliable estimates of terrestrial WR are to be obtained. The Robertson-Berger meter (Berger 1976), which is most frequently used for monitoring, has been subject recently to examination of its spectral response after long-term use (DeLuisi et al 1992), and a review of calibration procedures (Kennedy and Sharp 1992). In both cases it was concluded (Frederick 1992) that it is unlikely that the mean trend of -0.7% per year from the field measurements of Scotto CI al (1988) can be attributed to instrumental effects. 3. Human exposure to solar ultraviolet radiation
Experimental work in animals has shown that the action spectrum for photocarcinogenesis resembles that for ultraviolet-induced erythema in human skin (de Gruijl and van der Leun 1992). For this reason carcinogenic-effective exposure to sunlight is often expressed in units of 'minimal erythema dose' or MED; one MED is that dose of solar ultraviolet radiation (uVR) which produces a just perceptible reddening of the skin 8-24 h after exposure in unacclimatized white skin and in the following calculations is taken to be equivalent to an erythemally weighted radiant exposure of 200 J m-z (McKinlay and Diffey 1987). The solar UVR exposure received by an individual depends on three factors:
2269
Orone and skin cancer
(i) ambient solar ultraviolet radiation; (ii) the fraction of ambient exposure received on appropriate anatomical sites; (iii) exposuse habits outdoors. The model used to estimate annual personal exposure combines these variables to calculate exposure to the face in a manner similar to that described by Rosenthal er a1 (1991). The face is chosen since about 80% of NMSC in British people occur on the head and neck (Lloyd Roberts 1990). Time spent outdoors each month is considered in four periods. For each day within a given period exposure outdoors is assumed to be the same. The first and second periods comprise the weekdays (Monday to Friday) and weekend days (Saturday and Sunday) during the first half of the month, respectively. The third and fourth periods are the corresponding weekdays and weekends for the second half of the month. The choice of dividing the month into four periods is somewhat arbitrary. It does allow for an individual to be outdoors on holiday for one half of a month and mainly indoors at work for the other half. Decreasing the number of periods per month would not permit this, whilst increasing the number may give the unjustified impression that behaviour can be modelled with greater precision than is warranted. The exposure dose ( H ( m ) ) to an unprotected face in month m (January m = 1, Rbruary m = 2 etc) is calculated as:
=cc 4
H(m)
18
FE(i,h)
MED
i = l h=O
where FE( i, h) is the exposure received on the face in a one hour interval around time of day h multiplied by the number of days in the ith period, and is expressed by:
FE(i,h)= AE(i,h)FO(i,h)ER
MED
A E ( i , h ) is the ambient exposure (MED) on an unshaded, horizontal surface in the one hour interval around time of day h multiplied by the number of days in the ith period; F O ( i , h ) is the fraction of the one hour interval around time of day h spent out of doors during each day in the ith period; ER is the exposure ratio-the fraction of ambient radiation received on the face. The cumulative ambient exposure in the one hour interval around time of day h summed over each of the weekdays in the first and second halves of the month are A E ( 1 , h ) and A E ( 3 , h), respectively. Both quantities are equal to
( 1 0 / 2 8 ) M AE( t n ) H A F ( m , h )
MED
where M A E ( 7 n ) is the ambient exposure (in MED) incident on an unshaded, horizontal surface during month m, and H A F ( m , A ) is the fraction of diurnal ambient erythemally effective exposure occurring in a one hour interval around time of day h during month m. Similarly weekend ambient exposure, expressed by the even-numbered periods (i = 2 and 4 ) is given as
A E ( i , h )= ( 4 / 2 8 ) M A E ( m ) H A F ( m , h )
MED
2270
B L Diffey
3.1. Monthly ambient erpmure W ( m ) in the UK There exist no long-term measurements of ambient erythemally effective exposure for the tJK Continuous monitoring of erythemally effective solar UVR on an unshaded, horizontal roof at Durham (latitude SON) has been carried out by the author using a solar blind photomultiplier tube optically filtered to give a spectral sensitivity closely resembling the reference action spectrum for erythema in human skin (McKinlay and D#ey 1987). Unfortunately instrumental and other problems have meant that reliable data were available only for the period December 1988 to September 1989. Similar monitoring has been carried out by the National Radiological Protection Board at three sites in the UK since May 1988, but again problems occurring with instrumentation led to uncertainties in experimental data particularly in the period prior to 1990 (Driscoll et a1 1989). As a consequence of the paucity of measured ambient exposures in the UK, the values employed here, and shown in table 1, are derived from graphical data based on a radiative transfer model for clear skies (Frederick el a1 1991) and modified by the author by a factor which accounts for cloud cover. Values of average cloud m e r as a function of month for different locations in the UK (Laing and Grant 1980) were used to calculate the factor by which clear sky values need to be multiplied. This 'cloudiness factor' is given by (Cutchis 1980) as 1- 0.5C(m)
where C ( m ) is the average cloud cover in month m (unity for completely overcast). The weather in the UK is such that the calculated cloudiness factor is between 0.64 and 0.68 for all months and so an average value of 0.66 was applied to clear sky values for each month. Also shown in table 1 are the monthly ambient exposures measured at Durham during the period December 1988 to September 1989, where it may be seen that there is generally good agreement between the theoretical and measured values. Table 1. Average monthly ambient mposure (MED) for the UK (.50'N-6OoN)
Calculated ambient
Month January February
March April May June July August September October November December Annual
expure MAE( m) 14 38 84
Measured at Durham (55") during a single l0-month period
21 40 98
201
138
323 396
332 396 3M 287 1.56
394 302 165 ho 20 11 zM)8
-
12
2271
Ozone and skin cancer
%bk Z Mean fraction of diurnal ambient aythemally effective UVR occurring during t h periods of the day in the UK. Note: British Summer l l m e fmm April (0 October when solar noon m n at 13M.
rime of day
Jan
Feb
hlsr
Apr
May
Juo
Jul
Aug
Sep
Oct
Nov
Dec
530-630
0
0
0
o
aoi
0.01
0 0.01
0
0
7:30-8:30 8 : ~ 3 0 9:%10:30 1030-11:30
0 0.06 0.13 0.19 0.24 0.19 0.13
Cl02
a02
0.04 0.06
0.03
0.02 0.05
0.08 0.11 0.12
0.08 0.11
am
0.04 0.08 a12 0.16 0.18 0.16 0.12 0.08
0.01 0.02 0.04 0.06 0.08
0
o
0.01 0.02 0.04 0.06 0.08 0.11 0.12 0.14 0.12
0
6:x~wo
0 0.01
0.02
0.04
0.08
0
0.01
0.M O.M
11:30-1230 1230-1330 1330-1430
14:30-m0 15:30-16:30
o
16:30-17:30
0
17:w-18:30
0.06
o
am 0.13 0.18 0.20 0.18 0.13
o
o
0.05 0.08 0.12 0.14
0.16 0.14
an
0.11 0.08 0.06 0.04
all 0.12 0.14
a12 0.11 0.0s 0.06
aw
0.02
0.14 0.12 0.11 0.08 0.06 0.04
0.05
0.14 0.16 0.14
0.11 0.08 0.05 0.03
o a07 0.12 0.15 0.18 0.15 0.12
am 0.05 0.02
o
o
0
0 0.06 0.13
0.03 0.07 0.13 0.17 0.20 0.17 0.13 0.07 0.03
o
o 0
0.0s
0.22 0.20 0.13 0.06
0.13 0.20 0.24 0.20 0.13 0.05
o
o
0.20
0
0
o
o
3.2. Hourly ambient fraction .WF(m,h) These data, given in table 2, were derived mainly from ambient monitoring at Durham and supplemented with values calculated from a computer model of terrestrial ultraviolet radiation (Diffey 1977).
3.3. Exposure mtio ER A number of workers have used ultraviolet sensitive film badges to measure solar W R exposure on the face relative to ambient exposure on both human subjects (Holman et a1 1983, Rosenthal et al 1990, Melville et a1 1991, Gies et al 1992) and manikins (Diffey et a/ 1977, 1979, Gies et al 1988, Diffey and Cheeseman 1992). There is considerable variation in these data, reflecting factors such as positioning of film badges a t different sites on the face,behaviour of individuals, solar altitude and the influence of shade. The fractions of ambient exposure recorded around the nose and cheeks have ranged from 0.08 to 0.6 but most studies have yielded values clustering between 0.2 and 0.3. A representative value of 0.25 is used here.
3.4. Lfeslyle scenarios The numerical wlues assigned to the fractions of hourly intervals spent outdoors FO( i, h ) lie between 0 and 1. A value of 0 implies the subject remains indoors during the hourly interval around time of day h on each of the days during the ith period, whereas a value of 1 indicates outdoor exposure throughout the entire hourly interval on each day. An intermediate value reflects the fraction of the hourly interval spent outdoors on each day in the ith period. nV0 hypothetical individuals are considered: (i) Child aged 10; walks for 10 min to and from school; in the playground three times a day for a total of 1 h; plays outdoon after school each day during the summer for 1 h; plays outdoors for up to 6 h on Saturdays and Sundays, depending on season. (ii) Adult indoor worker aged 35; travels to work by car; spends 3 0 4 0 min outside at lunchtime from April to August; enjoys outdoor pursuits at weekends.
2272
B L Difey
Each person takes a summer holiday in the UK during the first two weeks in August when they are outside for 6 h a day but indoors at lunchtime between 1230 and 1.30 pm. It is assumed that no measures are used to protect the face from sun exposure (e.g. hats or sunscreens) throughout the year. Neither subject is outdoors before 8.30 am or after 4.30 pm. The number of hours spent outdoors each year by the child and indoor worker are 700 and 332 of which 35% and 60% are at weekends, respectively. The carcinogenic-effective exposure to the face ( H ( m ) )based on these behaviour patterns are summarized in table 3. These data show that about 80% of annual personal exposure for each individual occurs between May and August yet the ambient solar UVR in this period (table 1) is 70% of the annual. The difference is accounted for by the fact that most people are likely to spend more time outdoors in the summer than at other rimes of the year. Table 3. Estimated monthly mlar UMI aposure dose to the
Month
Janualy Febmaly March April May lune
4. The
Exposure Dose to Face (MED) Child
Adult
0.3 1
0.2 0.5
3
1
6.4
August September October November Decemkr
14 21 28 34 42 10 3.5 1 0.2
Annual
157
July
Llce of each subjed
12
IS a0 31 5 1.6
0.2 0.1
93
risk of NMSC from sunlight
Application of multivariate analysis to the epidemiology of skin cancer has shown that, for a goup of subject, with a given genetic susceptibility, age and environmental ultraviolet exposure are the two most important factors in determining the relative risk (Fears et a1 1977). Other epidemiological studies have confirmed these findings, and this has led to a simple power law relationship which expresses the cumulative risk in terms of these factors (Schothorst ef al 1985):
Risk a (annual solar uv dose)@(age)" The symbols a and p are numerical constants associated with the age dependence of the cumulative incidence and the biological amplification factor, respectively. This equation is applicable to situations where the annual exposure received by an individual remains unaltered throughout life. In most instances changes in lifestyle
Orone and shin cancer
2273
with age mean that the annual UV exposure does not remain constant. For example, table 3 suggests that children receive greater sun exposure than adults. The situation of changes in annual exposure was examined in a series of experiments with mice (de Gruijl 1982), and led Slaper and van der Leun (1987) to modify the above equation to estimate the risk of NMSC at age, T , as T
Risk a (cumulative
UV
dose at age T ) ' - ' ~ [ a n n u a l dose at age (T - t)]t"-O. fdJ
Values of the exponents a and p are normally derived from surveys of skin cancer incidence and UV climatology. Results from a survey by the National Cancer Institute in the USA during the period June 1977 to May 1978 (Scotto et a1 1981) estimated a U) be 5.7 and 4.9 for squamous cell and basal cell carcinomas, respectively, and p to be 2.9 and 1.7 for these two cancers. More recent estimates (UNEP 1991) give p to be 2 5 and 1.4 for squamous and basal cell cancers, respectively. Combining the data for basal and squamous cell cancers, and noting that the former are about four times more common than the latter, exemplary values for a and p of 5 and 2, respectively, are often adopted in risk estimates of NMSC (Schothorst et al 1985, van der Leun 1984, Diffey 1987), and will he used here.
5. Human exposure as a consequence of ozone loss
In the absence of ozone depletion the adult indoor worker continues to receive
an annual facial exposure dose of 93 MED. The child receives 157 MED per year until the age of 18 and thereafter 93 MED each year (assuming he/she becomes an indoor worker). However, if ozone depletion continues indefinitely at the rates shown in table 4, it is possible to calculate the expected lifetime exposure, and hence the increased risk of developing skin cancer, for each subject compared with that expected if ozone levels remained at present values. Implicit in these estimates is that behaviour, time spent outdoors and climate remain unchanged. Table A 'Ibtal ozone trends for UK latitudes (from Stolarski U d (1991)).
Monrh Janualy February March April May June July
August September October November December
7% ozone decrease per year 0.6 0.8
0.8 0.7 0.5 a4 0.3 0.2 0.3 0.4 0.4 0.4
2274
B L Diffey
The facial exposure dose received by each subject during the 12-month period t years from now would be 12
MED
H(m){l+RAF[1-(1-6(m))‘]) m=1
where H ( m ) is the monthly exposure from the relevant column in table 4, h ( m ) is the fractional ozone depletion in month m (i.e. U100 of the values given in table 4) and R A F is the radiation amplification factor defined such that a 1% decrease in ozone results in a R A F % increase in carcinogenic-effective radiation at the Earth’s surface. Using the most recent action spectrum for photocarcinogenesis in hairless mice a factor of 1.4 for R A F is obtained (UNEP 1991); this B slightly lower than the value of 1.6 used previously (UNEP 1989). Computations based upon the reference erythema action spectrum (McKinlay and Diffey 1987) as a surrogate for a carcinogenic action spectrum yield a R A F of 1.15 (Kelfkens et RI 1990). Use of this R A F is likely to underestimate the risk and so the value of 1.4 given above was used in the calculations. By incorporating annual exposure doses into the model for skin cancer risk, it is possible to estimate the increased risk at different ages throughout life (table 5). Tabk 5. Cumulative wlar w exposure Jure io faax a i d iiie reiatile dsk of k i n ianier assuming m n e depletion mntinues indefinitely at current rates. Ozone depletion at ~ r r e n t
No Ozone depletion
Child (presently 10)I when aeed -U aged
Cumulative dose hlED
Relative risk
of skin cancer
Cumulative dose MED
of skin cancer
50 60
58u) 6750
70
7680
1.00 1.00 1.W
6184 7302 8457
1.08 1.10 1.13
~
Addl (presently aged 35) when aged
No Ozone depletion Relative risk
ratCS
Relative risk
Ozone depletion at “ e n 1 rates
Cumulative dose MED
of skin cancer
Cumulative dose MBD
50
5820
1.00
60 70
6750 7680
1.00
5873 6892
1.00
7952
Relative risk
of skin cancer 1.01 1.02 1.04
The above calculations of the lifetime risk of skin cancer assume that ozone depletion continues indefinitely at present rates. However, if there is global adherence to international undertakings for the phasing out of ozone depleting chemicals, as agreed in the Montreal Protocol (UNEP 1987) ozone levels should begin to recover slowly in the next century. Models of atmospheric chemistry and transport are not capable of predicting reliably the details of any future ozone depletion resulting from the increasing concentrations of chlorine compounds which are largely responsible (SORG 1990). There will also be a time lag of several years before stratospheric chlorine
Ozone and skin cancer
2275
concentrations respond to a decrease in chlorine loading. The implication is that stratospheric ozone destruction may continue to increase for several years after the chlorine loading of the troposphere has passed its peak value (SORG 1991). Given these uncertainties the approach used here is to assume that ozone depletion continues at present rates for a period T, years from now and thereafter the ambient ultraviolet levels at that time return exponentially to present levels with a half recovery time of T years. The child’s risk at age 60 and 70 years for a range of T, and T have k e n calculated and the results are shown in table 6 where it can he seen that if ozone depletion continues at present rates for another U) years, say, and then recovers with a half recovery time of 20 years, the risk by age 60 will be 1.06 compared with 1.10 if ozone depletion continues indefinitely at present rates. NMSC in a child presently aged 10 when aged 64 and 70 yean relative ta that under an intact mone layer. W t a are given assuming that ozone depletion mntinues at present rates until a period T,yean from now and thereafter the ambient ultraviolet levels at that time ~ t u m exponentially ta present levels with a half recovery time of r years.
lhbk 6 ?he risk of
Relative risk at age 60 years
T,
r years
years 5
10
15
20
25
30
1.02
1.03
1.05 1.07 1.09
1.05 1.07
50
1.10
1.10
1.03 1.06 1.08 1.09 1.10
1.03 1.06 1.08 1.09 1.10
1.03
30 40
1.02 1.04 1.06 1.09
1.06 1.08 1.09 1.10
10 U)
1.09 1.10
Relative risk at age 70 yean
TC
r yean
yeam 10 U)
30 40 50
6a
5
to
15
20
25
30
1.02 1.04 1.06 1.09 1.11 1.13
1.02 1.05 1.07 1.10 1.12 1.13
1.03 1.05 1.08 1.10 1.12 1.13
1.03 1.06 1.08 1.10 1.12 1.13
1.03
1.04 1.06 1.09 1.11 1.12 1.13
1.06 1.09 1.11 1.12 1.13
Previous estimates of the expected increase in skin cancer incidence have assumed a steady state scenario in which stratospheric ozone is depleted by a tixed amaunt (Kelfkens et a1 1990, Henriksen et a1 1990). The most recent report by UNEP (1991)
predicts that a 1% ozone depletion will result in a 23%&0.4%increase in nonmelanoma skin cancer. In the UK there are about moo0 new cases a year (CRC 1991) and so each 1% decrease in ozone would, in theory, lead to an additional 700 cases per year. It must be stressed, however, that this estimate assumes there will be no long-term changes in cloud cover, time spent outdoors, behaviour or clothing habits. 6. Strategies for reducing sun exposure
Unlike agricultural and marine ecosystems which are also at risk from the potential
2276
B L Difley
effects of increased terrestrial solar UVR, humans have the opportunity to modify their behaviour and so their exposure (Diffey 1992). In the absence of ozone depletion table 5 indicates that the adult d l have a lifetime facial exposure dose (at age 70 y) of 7680 MED. Ozone depletion at current rates is estimated to increase this lifetime exposure to 7952 MED. Only simple measures with minimal effect on lifestyle, such as remaining indoors one extra hour at lunchtime from 1.30 pm until 2.30 pm on each day of hisher two-week summer holiday, need to he adopted to reduce this figure to below 7680 MED. In the case of the child, however, more severe sun protection measures are required to maintain his lifetime exposure below 7680 MED. These would include staying indoors between 11.30 am and 2.30 pm on each day of his six-week school summer holiday and again during this period on every day of his hvoweek summer holiday as an adult As an alternative to reducing time spent outdoors, wearing a hat with a wide brim (at least 3 inches) whenever outdoors during July and August for the remainder of his life would achieve a similar reduction in lifetime facial exposure dose (Diffey and Cheeseman 1992), as would application of topical sunscreens. Any one of these measures alone is probably unduly restrictive and is unlikely to meet with compliance. A more rational approach to sun protection is to encourage adoption of a combination of measures such as avoiding sun exposure around solar noon on clear, sunny summer days by staying indoors or seeking shade, and where this is not practicable to make use of clothing, hats and sunscreens. An important aim, particularly with sun exposure of children, is to avoid sunburn.
7. Discussion
The model described above incorporates climatological data with personal behaviour to estimate the annual burden of ultraviolet radiation in subjects taken to be representative of different population groups. It must be stressed, however, that there will be large variations in the annual exposure doses received by individuals within a given population group depending upon propensity for outdoor activities. The greater leisure time available to children is reflected in an annual exposure dose which may be SO% higher than for adults. The model predicts that a typical annual exposure dose of an indoor worker in the UK (excluding vacational exposure) is about 80 MED, or 4% of ambient. This estimate is in good agreement with those obtained by personal monitoring (Challoner t ? ~nl 1976, Leach et a1 1978, Larko and Diffey 1983, Slaper 1987) and gives support to the validity of the model, despite the inherent assumptions and simplifications regarding behaviour. For British adults alive today ozone depletion continuing indefinitely at current rates is predicted to result in a relatively small additional lifetime risk (< 5%; table 5) of non-melanoma skin cancer, assuming no changes in climate, time spent outdoors, behaviour or clothing habits. The lifetime risk incurred by today’s children, however, is 10%15% greater than expected in the absence of ozone depletion. However, if the production and use of substances which deplete ozone are reduced as expected under the current provisions of the Montreal Protocol (UNEP 1987) the increased lifetime risk of skin cancer is likely to be less than this estimate (table 6). These predicted increases in risk, resulting from greater solar ultraviolet exposure, can be offset by adopting changes to behaviour during the summer months which may involve spending less time outdoors, wearing wide-brimmed hats, applying topical sunscreens, or a combination of these. It is to be hoped that public awareness
2277
Ozone and skin cancer
about potential environmental and health effects of ozone depletion will achieve these changes, which could lead to a reduction-rather than the anticipated increase-in skin cancer incidence. If there is no change in sun exposure habits and the rate of ozone depletion, the calculations suggest that 50 years from now the number of skin cancers occurring each year in the UK will increase from the present number of about 30000 to around 33000. This is a much smaller increase than has occurred over the previous 50 years and illustrates that changes in leisure time, fashion and activities in the sun have had a much greater effect on skin cancer rates than expected as a consequence of ozone depletion. Clearly it will prove difficult to identily the real effect of ozone depletion on skin cancer incidence over the next few decades.
Diminution de I'owne stratosphCrique et risque de cancers mtanb la population britannique.
,
(A
Vexclusion des milanomes) dans
Eauteur pdsente "ne estimation quantilalive de I'accroissement du risque des ancen cutanb, B I'exdusion des milanomes (NMSC), susceptible #etre provoqut dans la population britannique par la diminution de I'ozone slratosphCrique. Ces don"& son1 p-es pour la &nCration actuelle de la population britannique. Pour les adultes vivant acfuellement, I'estimalion prhoit que la diminution de I'ozone, penistant au niveau m u d , n'entrainerait qu'un risque additionnel relativement faible pour toute la durCe de vie (< 5%), en supposant aucun changement de climal, de mmportement gCntral, vis b vis du temps pa& B I'interieur ou #habitudes vestimentaires. Le risque, pour la du& de vie, relatif b des enfants d'aujourd'hui, est apendant de 10% B 15% plus imponant que d u i attcndu en I'aknce de diminution de I'omne. Cependant. si la production et I'utilisation de substances qui panent atteinte B I'ozone wnt &uita, mmme on peut I'attendre Cap& Ies plans du protwole de Montdal, I.acmissement du risque de cancer cutani ( ~ r aprobablement plus bible que celui indiquC ddessus Ces prhisions daccmissement du risque liC B une plus grande exposition au rayonnement ultraviolet peuvent susciter une compensation par Un changement de mmponement au mum des mois de M i , lel que la dduction du temps pa& B I'exlirieur, le pon de dtemenu adaptis, y mmpris de chapeau b larges bords, I'application de d m e s solaires, ou une mmbinaison de ccs pratiques.
Zusammenfassung Die Veningerung des Ozons in der Wratospha~ und das Risiko w n nicht-melanomen Hautkrebserkrankungen in einer britischen Beviilkeerungsgmppe.
Eine quantitative Bestimmung des erhohten Risikos w n nieht-melanomen Hautkreberkrankungen (NMSC) in der britischen Bevolkerung, das durch die Veningerung der stratospharischen Ozonschicht mstandekommt, wurde Fir die heutige Generation durchgefiihn. For heme lebende Envachsene wid bei anhaltender Ozonvemngerung im gegenwiriigen AusmaO ein ,,relativ kleines msiitzlicha Lebenslcilrisiko (< 5%) tiir NMSC emanet, unter der Annahme, da0 k i n e Anderungen auftreten im Klima. in der im Freien verbrachten &it, im Verhalten d e r in den Kleidungsgnvohnheiten. Das kbenszeitrisikc, ki heutigen Kindern kt jedoch 10?&15% gn30er ah man ohne Ozonvemngerung emanen wiirde. Wiirde die Pmduktion und die Vemendung w n Substanzen. die das Ozon zentoren wrringen, wie dies in den Vorkehrungen des Montrealer Pmtokolls wrgesehen kt. a) kt das erhohte Lebenszeilrisiko hum kleiner als dieser Wn. Die berechneten Risikocrhohungen ergeben sich aus der hoheren Exposition dumh solares ullranoletta Licht und kdnnen nur verringen werden durch VerhaltenSndemngen Mhrend der Sommermonale, LE. weniger &it im Freien zu verbringen, entsprechende Kleidung, w r allem geeignete Koptbedeckungen zu uagen. m i e Uvpischen Sonnenschuu zu vetwenden.
B L Diffey
2278 References
Berger D S 1976 I h e sunburning ultraviolet meter design and performance Phorockm PhotobioL 24
587-93 Blumthaler M and Ambach W 1990 Indication of increasing solar ultraviolet8 radiation flux in alpine regions Science 248 20M Bmhl C and O m e n P J 1989 On the disproportionate rule of tmppheric ozone as a filter against solar W - B radiation Geophys. b. Len 16 703-6 Cancer Research Campaign 1991 Skin C m c q lhe Sun rmd You: YOW Questions Anwered (London: Cancer Rssearch Campaign) Challoner A V J, Corlas D, Davis A, Deane G H W Diffey B l, Gupla S P and Magnus I A 1976 Personnel monitoring of exposure to ultraviolel radiation Clin Ep. DemoroL 1 175-9 Cutchis P 1980 A formula for "paring annual damaging ultraviolet (DUV) radiation doses at tropical and mid-latitude sites US applmmsu of Pmponi~tioq Isdeml Aviatbn Admiiimarion W c e of Envumrnmr m d Energy Fino1 Repon No FAA-EE 80-21 (Washington Dc: FAA-EE) de GNijl F R 1982 The dose-response relationship for W tumorigenesisPhD 7h-is University of Utrecht de GNijl F R and van der Leu" J C 1592 Action spectra for carcinogenesis Biolo&ol Respowes ro Ulwm'aler A &dation ed F Urbach (Overland Park, Ks: Valdenmar) pp 91-7 DeLuisi J, Wendell J and Kreiner F 1992 An examination of the spectral response characteristics of w e n Robenson-Berger meten after long-term field use Phorochmn PhorobioL 56 115-22 Diffey B L 1977 The calculation of the spectral distribution of natural ultraviolet radiation under clear sky conditions Phys. Med Bid 22 %%I6 1987 Analysis of the risk of skin cancer from sunlight and solaria in subjects living in Noonhem Europe PhorodenmroL 4 11&26 - I" Asi1nti-n "-r.a-4 &in -n_r R. M r l ..I _u?d !!7&7 Diiey B L and Cheeseman J 1992 Sun Protection with Hats &. 1. DmnaroL U7 1 M 2 Diffey B L Kemin M and Davis A 1977 Ihe anatomical distribution of sunlight B,: 1. DennnroL 97
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__I.._
407-10 Diffey B 1 %le T J and Davis A 1979 Solar dosimetry of the face: the relationship of natural ultraviolet radialion aposure to basal cell carcinoma localisation Phys. Mcd BioL 24 931-9 Driscoll C M H, Whillock M 1, Gall A, Clark IE, Peatson A J, Blackwell R E Strong J C and McKinlay A F 1989 Solar radiation measuremenls at three sites in the LIK May 198aApril 1989 Nmbnol Rodiological Rorection Board Repon NRPM-M184 European Arctic Sratospheric Ozone Fxperiment (EASOE) 1992 News Release 7 April 1 9 2 Fears T R, Scotlo J and Schneiderman M A 1977 Mathematical models of age and ultraviolet effects on the incidence of skin cancer among whites in the United Slates Am . l EpidonwL 105 42C-7 Frederick J E I992 An a-men1 of the Robertson-Berger ultraviolet meter and measurements: intrcduclory mmments Phorochem PhotabioL 56 113-14 Fnderick J E, Weatherhead E C and H a y m d E K 1991 Long-term variations in ultraviolet sunlight reaching the biosphere: calculations for the past three decades Photochon Photobwl 54 781-8 Gies H P, Herlihy E and Riven J 1992 Pemnal dosimetry of solar WB using wlysulphone film Roc. IRPA 8 Congr: (Monnca4 1992) unpublished Gies 8 Roy C and Elliott G 1988 me anatomical distribution of solar UVR with emphasis on the y e Roc.7rh hr. Cong of the lnrmational Radarion Rolection Rrsociotion (Sydvq, 1988) (Sydney: Pergamon) pp 341-4 Henriksen T Dahlback A, Larsen S H H and Moan J 1990 Ultraviolet radiation and skin cancer effect of an ozone layer depletion Phorochmn. PhorobioL 51 579-82 Holman C D 1, Gibson I M, Stephenson M and Armstrong B K 1983 Ultraviolet irradiation of human body sites in relation to arupation and outdoor activity: field studies using penonal W R dosimeters Clin Ep. DennatoL 8 269-77 Kelfkens G, de GNgl F R and van der k u n J C 1 9 0 Ozone depletion and increase in annual carcinogenic ullraviolet dose Phorochem PhorobioL 52 819-23 Kennedy B C and Sharp W E 1992 A validation study of the Robertson-Berger meter Phorochem PhorobioL 56 13341 Laing J and Grant K 1980 Bbles of total doud amount for the United Kingdom 1957-76 BrackteY Merewological office, CIinaroIogical Memormdwn NO 110 Lark6 0 and Diffey B L 1983 Natural W-B radiation received by people With outdmr, indoor and mixed arupations and W - B treatment of psoriasis C h h a l o L 8 279-35
e.
Ozone and skin cancer
2219
Leach 1F, M c L e d V E, Pingstone A R, Davis A and m a n e G H W 1978 Measurement of the ultraviolet d o s s received by omce workers c h @. M O L 3 77-9 Uoyd Rokrls D 1990 Incidence of non-melanoma skin cancer in West Glamorgan, South Wales B1: J DatnotoL U2 399403 MacKie R M and Rymft M J 1988 Health and the mane layer: skin cancers may increase dramaticaliy Bc Med J 197 369-70 Madmnich S 1592 Implications of =en1 total atmospheric raone measurements for tiologically active ultraviolet radiation reaching the Earth’s surface Geophp Rex . L a 19 37-40 McKinlav A F and DER, B L 1987 A reference action s w t r u m for UIlravioiet induced avthema in human skin CIE 3. 6 17-22 Melville S K. Rosenthal F S, Luckmann R and Inu R A 1991 Quantitative ultraviolet skin exwsure in children during selected outdoor actinties PhotodemaroL PhotobnmrrnoL Phoromed 8 s i 0 4 Rwnthal F S, Lw R A, Rouleau L J and ‘Ihomson M 1990 Ultraviolet exposure to children h m sunlight: a study using personal dosimetry Photodemrorol PhotoimmunoL Phorwned 7 77-81 Rosenthal F S, West S K, Munoz B, Emmett E A, Stickland P T and ’Lhylor H R 1991 Ocular and facial skin exposure to ultraviolet radiation in sunlight: a pemnal exposure model with application lo a worker population Health Phys. 61 77-86 Roy C Rand G i a H P 1592 Resulrr from an Australian mlar W R measurement network and implications for radiation protection policy Rm.IRPA 8 C o n s (MonrreaJ 1992) unpublished Russell Jones R 1987 Ozone depletion and mncer risk Lancer ii 4436 Schothont A A, Slaper H, Schouten R and Suurmond D 1985 UVB doses in maintenance p n a s i s phototherapy versus solar UVB exposure Pho~ode”tok?g~2 21>u) Science and Policy Associates, Inc. 1992 UV-B Monitoring Workhop: (I review of he xience mad d a w of measwing mid mniroring p o q m (Washington, DC Science and Policj Associates Inc.) Scotlo I, Cotton G, Urbacb, F, Berger D and Fears T 1988 Biologically effeclive ultraviolet radiation: surface measurements i lhe United Stales 1974 to 1985 Science U9 7624 Scotto J, Fears T R and Fraument J F 1981 h i c i a k c of Non-melanoma Skin Cmrco h he Lhrircd Sraucr (Washington, D C US Department of Health and Human Sciences (NIH)) Slaper H 1987 Skin a n e r and W exposure: investigations on lhe estimation of risks PhLl 7h-a University of Uvecht Slaper H and van der k u n J C 1987 Human exposure to Ultraviolet radiation: quantitative modelling of g i n cancer incidence Human @ o m to Ularaviolet Rodlalion: Risks a d Regulations ed W F P a s h i e r and B F M Bosnjakowc (Amsterdam: Elsevier) pp 155-71 Stolalski R S, Blaomfield e McPetels R D and Herman J R 1591 l b t a l cuone wends deduced from Nimbus 7 TOMS data Geophy Res. Lett 18 1015-18 United Kingdom Stratospheric Ozone Rwiew Gmup 1990 Slratospheric Ozone B u d Report (London:
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Stratospheric ozone depletion and the risk of non-melanoma skin cancer in a British population
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Php. Mod. Biol., 1992, Vol. 37, NO 12, 2267-2279. Printed in the UK
Stratospheric ozone depletion and the risk of non-melanoma skin cancer in a British population B L Diffey Regional Medical Physics Department, Drybum Hospital, Durham DHI .Try UK Received 24 July 1992 Abstract Quanlitative estimation of the increased dsk of non-melanoma skin cancer (NMX) in British people that may result from depletion of the stratospheric m n e layer is given for the w e n t generation of British people. For adults alive today mntinuing ozone depletion at wrrent rates is predicted to m u l l in a relatively small additional lifetime risk (C 5%) of N m , asuming no changes in climate, lime spent outdoors, behaviour or clothing habits. The lifetime risk incurred lq loday's children, however, is 1 0 9 ~ 4 5 %greater than expected in the absence of m n e depletion. However, if lhe produclion and Use of substances which deplete ozone are reduced, as expected under lhe arrent provisions of the Montreal Pralocol, the increased lifetime lisk of skin cancer is tikely U, be less than this estimate. n e s e predicled increases in ri&, resulting h m grealer salar ultraviolet exposure, can be offset bj adopting changes to behaviour during the summer months which may involve spending Igs time outdoors, wearing appropriate clothing including widc-brimmed hats, applying topical Sunscreens, or a combination of these.
1. Introduction
Skin cancers are the most common human cancer and their incidence is increasing in many countries, including the UK. Each year about 30aM people in Britain are said to develop skin cancers (CRC 1991), although because of under-recording of non-melanoma skin cancerb (NMSC) in the LJK, the incidence may be as much as three times this figure (Lloyd Roberts 1990). It is well recognized that chronic exposure to sunlight is a causal factor in the development of human skin cancer, particularly non-melanoma skin cancers (NMsC). Concern has been expressed widely that depletion of stratospheric ozone by chemical reactions involving the degradation products of chlorofluorocarbons will lead to a rise in the incidence of skin cancers as a consequence of increased levels of solar ultraviolet radiation (UVR) at the Earth's surface (UNEP 1991, Russell Jones 1987, MacKie and Rycroft 1988). 2. Ozone and terrestrial ultraviolet radiation
Significant global scale decreases in total ozone occurred during the period 1979-1989 (UNEP 1991, Science and Policy Associates, Inc 1992) and the loss of ozone in the northern hemisphere is now proceeding faster than previously thought with a rate of loss over mid-latitudes (3O06OoN)seen in winter and early spring of about 8% 0031-9155/92/lU267+13sO7.S0 @ 1992 IOP Publishing I l d
2267
2268
B L Diffq
per decade (SORG 1991). Measurements of total column ozone at several ground stations in Europe during the period November 1991 to February 1992 reported values ranging from 0% to 20% below average for the winter months (EASOE 1992). The loss in summer months, when uv levels are much higher and people are exposed more frequently to the sun, is less at about 2 % 4 % per decade. Calculations for the northern hemisphere based on the measured ozone trends for the period 1979-1989 indicate that, all other factors being constant, the terrestrial carcinogeniceffective W R (which lies mainly within the ultraviolet B waveband of 280-315 nm) should have increased by about 1.3% to 4.7% during this decade (Madronich 1992). Paradoxically these predictions have not been borne out by ground-based W monitoring programmes. Analysis of a 12 y record of ambient WB measured at eight stations in the USA showed a slight downward trend of -0.4% to -1.1% per year (Scotto el of 1988). The largest contribution to annually averaged ultraviolet levels occurs during the summer when stratospheric ozone depletion is at its least. firthermore year-to-year fluctuations in cloud cover and an increase in ozone present in the lower atmosphere due to pollution (Bruhl and Crutzen 1989) make it not surprising that no statistically significant increase in ambient WB has yet been demonstrated. However, measurements of ambient UVB in the Swiss Alps at an altitude of 3576 m above sea level, and where the atmosphere is much clearer than in urban areas at lower altitudes, indicate that there has been a slight increase of about 0.7% per year during the 1980s (Blumthaler and Ambach 1990). The authors ;:::',bated this smi!! i!creae to n n n e depletion. In the southern hemisphere the influence of Antarctic ozone depletion on ambient UVB in Melbourne (latitude 38'S) has been reported by Roy and Gies (1992). Continuous monitoring of ambient WB showed that the levels recorded in February 1991 were 37% and 27% higher than for the Same month in 1990 and 1989, respectively. February 1991 had the lowest ozone values recorded for this period, but also very low cloud cover compared with recent years. These two important factors reinforce each other and illustrate the difficulty of separating the effects of ozone depletion from climate on ambient WB. Long-term stability of monitoring equipment is essential if reliable estimates of terrestrial WR are to be obtained. The Robertson-Berger meter (Berger 1976), which is most frequently used for monitoring, has been subject recently to examination of its spectral response after long-term use (DeLuisi et al 1992), and a review of calibration procedures (Kennedy and Sharp 1992). In both cases it was concluded (Frederick 1992) that it is unlikely that the mean trend of -0.7% per year from the field measurements of Scotto CI al (1988) can be attributed to instrumental effects. 3. Human exposure to solar ultraviolet radiation
Experimental work in animals has shown that the action spectrum for photocarcinogenesis resembles that for ultraviolet-induced erythema in human skin (de Gruijl and van der Leun 1992). For this reason carcinogenic-effective exposure to sunlight is often expressed in units of 'minimal erythema dose' or MED; one MED is that dose of solar ultraviolet radiation (uVR) which produces a just perceptible reddening of the skin 8-24 h after exposure in unacclimatized white skin and in the following calculations is taken to be equivalent to an erythemally weighted radiant exposure of 200 J m-z (McKinlay and Diffey 1987). The solar UVR exposure received by an individual depends on three factors:
2269
Orone and skin cancer
(i) ambient solar ultraviolet radiation; (ii) the fraction of ambient exposure received on appropriate anatomical sites; (iii) exposuse habits outdoors. The model used to estimate annual personal exposure combines these variables to calculate exposure to the face in a manner similar to that described by Rosenthal er a1 (1991). The face is chosen since about 80% of NMSC in British people occur on the head and neck (Lloyd Roberts 1990). Time spent outdoors each month is considered in four periods. For each day within a given period exposure outdoors is assumed to be the same. The first and second periods comprise the weekdays (Monday to Friday) and weekend days (Saturday and Sunday) during the first half of the month, respectively. The third and fourth periods are the corresponding weekdays and weekends for the second half of the month. The choice of dividing the month into four periods is somewhat arbitrary. It does allow for an individual to be outdoors on holiday for one half of a month and mainly indoors at work for the other half. Decreasing the number of periods per month would not permit this, whilst increasing the number may give the unjustified impression that behaviour can be modelled with greater precision than is warranted. The exposure dose ( H ( m ) ) to an unprotected face in month m (January m = 1, Rbruary m = 2 etc) is calculated as:
=cc 4
H(m)
18
FE(i,h)
MED
i = l h=O
where FE( i, h) is the exposure received on the face in a one hour interval around time of day h multiplied by the number of days in the ith period, and is expressed by:
FE(i,h)= AE(i,h)FO(i,h)ER
MED
A E ( i , h ) is the ambient exposure (MED) on an unshaded, horizontal surface in the one hour interval around time of day h multiplied by the number of days in the ith period; F O ( i , h ) is the fraction of the one hour interval around time of day h spent out of doors during each day in the ith period; ER is the exposure ratio-the fraction of ambient radiation received on the face. The cumulative ambient exposure in the one hour interval around time of day h summed over each of the weekdays in the first and second halves of the month are A E ( 1 , h ) and A E ( 3 , h), respectively. Both quantities are equal to
( 1 0 / 2 8 ) M AE( t n ) H A F ( m , h )
MED
where M A E ( 7 n ) is the ambient exposure (in MED) incident on an unshaded, horizontal surface during month m, and H A F ( m , A ) is the fraction of diurnal ambient erythemally effective exposure occurring in a one hour interval around time of day h during month m. Similarly weekend ambient exposure, expressed by the even-numbered periods (i = 2 and 4 ) is given as
A E ( i , h )= ( 4 / 2 8 ) M A E ( m ) H A F ( m , h )
MED
2270
B L Diffey
3.1. Monthly ambient erpmure W ( m ) in the UK There exist no long-term measurements of ambient erythemally effective exposure for the tJK Continuous monitoring of erythemally effective solar UVR on an unshaded, horizontal roof at Durham (latitude SON) has been carried out by the author using a solar blind photomultiplier tube optically filtered to give a spectral sensitivity closely resembling the reference action spectrum for erythema in human skin (McKinlay and D#ey 1987). Unfortunately instrumental and other problems have meant that reliable data were available only for the period December 1988 to September 1989. Similar monitoring has been carried out by the National Radiological Protection Board at three sites in the UK since May 1988, but again problems occurring with instrumentation led to uncertainties in experimental data particularly in the period prior to 1990 (Driscoll et a1 1989). As a consequence of the paucity of measured ambient exposures in the UK, the values employed here, and shown in table 1, are derived from graphical data based on a radiative transfer model for clear skies (Frederick el a1 1991) and modified by the author by a factor which accounts for cloud cover. Values of average cloud m e r as a function of month for different locations in the UK (Laing and Grant 1980) were used to calculate the factor by which clear sky values need to be multiplied. This 'cloudiness factor' is given by (Cutchis 1980) as 1- 0.5C(m)
where C ( m ) is the average cloud cover in month m (unity for completely overcast). The weather in the UK is such that the calculated cloudiness factor is between 0.64 and 0.68 for all months and so an average value of 0.66 was applied to clear sky values for each month. Also shown in table 1 are the monthly ambient exposures measured at Durham during the period December 1988 to September 1989, where it may be seen that there is generally good agreement between the theoretical and measured values. Table 1. Average monthly ambient mposure (MED) for the UK (.50'N-6OoN)
Calculated ambient
Month January February
March April May June July August September October November December Annual
expure MAE( m) 14 38 84
Measured at Durham (55") during a single l0-month period
21 40 98
201
138
323 396
332 396 3M 287 1.56
394 302 165 ho 20 11 zM)8
-
12
2271
Ozone and skin cancer
%bk Z Mean fraction of diurnal ambient aythemally effective UVR occurring during t h periods of the day in the UK. Note: British Summer l l m e fmm April (0 October when solar noon m n at 13M.
rime of day
Jan
Feb
hlsr
Apr
May
Juo
Jul
Aug
Sep
Oct
Nov
Dec
530-630
0
0
0
o
aoi
0.01
0 0.01
0
0
7:30-8:30 8 : ~ 3 0 9:%10:30 1030-11:30
0 0.06 0.13 0.19 0.24 0.19 0.13
Cl02
a02
0.04 0.06
0.03
0.02 0.05
0.08 0.11 0.12
0.08 0.11
am
0.04 0.08 a12 0.16 0.18 0.16 0.12 0.08
0.01 0.02 0.04 0.06 0.08
0
o
0.01 0.02 0.04 0.06 0.08 0.11 0.12 0.14 0.12
0
6:x~wo
0 0.01
0.02
0.04
0.08
0
0.01
0.M O.M
11:30-1230 1230-1330 1330-1430
14:30-m0 15:30-16:30
o
16:30-17:30
0
17:w-18:30
0.06
o
am 0.13 0.18 0.20 0.18 0.13
o
o
0.05 0.08 0.12 0.14
0.16 0.14
an
0.11 0.08 0.06 0.04
all 0.12 0.14
a12 0.11 0.0s 0.06
aw
0.02
0.14 0.12 0.11 0.08 0.06 0.04
0.05
0.14 0.16 0.14
0.11 0.08 0.05 0.03
o a07 0.12 0.15 0.18 0.15 0.12
am 0.05 0.02
o
o
0
0 0.06 0.13
0.03 0.07 0.13 0.17 0.20 0.17 0.13 0.07 0.03
o
o 0
0.0s
0.22 0.20 0.13 0.06
0.13 0.20 0.24 0.20 0.13 0.05
o
o
0.20
0
0
o
o
3.2. Hourly ambient fraction .WF(m,h) These data, given in table 2, were derived mainly from ambient monitoring at Durham and supplemented with values calculated from a computer model of terrestrial ultraviolet radiation (Diffey 1977).
3.3. Exposure mtio ER A number of workers have used ultraviolet sensitive film badges to measure solar W R exposure on the face relative to ambient exposure on both human subjects (Holman et a1 1983, Rosenthal et al 1990, Melville et a1 1991, Gies et al 1992) and manikins (Diffey et a/ 1977, 1979, Gies et al 1988, Diffey and Cheeseman 1992). There is considerable variation in these data, reflecting factors such as positioning of film badges a t different sites on the face,behaviour of individuals, solar altitude and the influence of shade. The fractions of ambient exposure recorded around the nose and cheeks have ranged from 0.08 to 0.6 but most studies have yielded values clustering between 0.2 and 0.3. A representative value of 0.25 is used here.
3.4. Lfeslyle scenarios The numerical wlues assigned to the fractions of hourly intervals spent outdoors FO( i, h ) lie between 0 and 1. A value of 0 implies the subject remains indoors during the hourly interval around time of day h on each of the days during the ith period, whereas a value of 1 indicates outdoor exposure throughout the entire hourly interval on each day. An intermediate value reflects the fraction of the hourly interval spent outdoors on each day in the ith period. nV0 hypothetical individuals are considered: (i) Child aged 10; walks for 10 min to and from school; in the playground three times a day for a total of 1 h; plays outdoon after school each day during the summer for 1 h; plays outdoors for up to 6 h on Saturdays and Sundays, depending on season. (ii) Adult indoor worker aged 35; travels to work by car; spends 3 0 4 0 min outside at lunchtime from April to August; enjoys outdoor pursuits at weekends.
2272
B L Difey
Each person takes a summer holiday in the UK during the first two weeks in August when they are outside for 6 h a day but indoors at lunchtime between 1230 and 1.30 pm. It is assumed that no measures are used to protect the face from sun exposure (e.g. hats or sunscreens) throughout the year. Neither subject is outdoors before 8.30 am or after 4.30 pm. The number of hours spent outdoors each year by the child and indoor worker are 700 and 332 of which 35% and 60% are at weekends, respectively. The carcinogenic-effective exposure to the face ( H ( m ) )based on these behaviour patterns are summarized in table 3. These data show that about 80% of annual personal exposure for each individual occurs between May and August yet the ambient solar UVR in this period (table 1) is 70% of the annual. The difference is accounted for by the fact that most people are likely to spend more time outdoors in the summer than at other rimes of the year. Table 3. Estimated monthly mlar UMI aposure dose to the
Month
Janualy Febmaly March April May lune
4. The
Exposure Dose to Face (MED) Child
Adult
0.3 1
0.2 0.5
3
1
6.4
August September October November Decemkr
14 21 28 34 42 10 3.5 1 0.2
Annual
157
July
Llce of each subjed
12
IS a0 31 5 1.6
0.2 0.1
93
risk of NMSC from sunlight
Application of multivariate analysis to the epidemiology of skin cancer has shown that, for a goup of subject, with a given genetic susceptibility, age and environmental ultraviolet exposure are the two most important factors in determining the relative risk (Fears et a1 1977). Other epidemiological studies have confirmed these findings, and this has led to a simple power law relationship which expresses the cumulative risk in terms of these factors (Schothorst ef al 1985):
Risk a (annual solar uv dose)@(age)" The symbols a and p are numerical constants associated with the age dependence of the cumulative incidence and the biological amplification factor, respectively. This equation is applicable to situations where the annual exposure received by an individual remains unaltered throughout life. In most instances changes in lifestyle
Orone and shin cancer
2273
with age mean that the annual UV exposure does not remain constant. For example, table 3 suggests that children receive greater sun exposure than adults. The situation of changes in annual exposure was examined in a series of experiments with mice (de Gruijl 1982), and led Slaper and van der Leun (1987) to modify the above equation to estimate the risk of NMSC at age, T , as T
Risk a (cumulative
UV
dose at age T ) ' - ' ~ [ a n n u a l dose at age (T - t)]t"-O. fdJ
Values of the exponents a and p are normally derived from surveys of skin cancer incidence and UV climatology. Results from a survey by the National Cancer Institute in the USA during the period June 1977 to May 1978 (Scotto et a1 1981) estimated a U) be 5.7 and 4.9 for squamous cell and basal cell carcinomas, respectively, and p to be 2.9 and 1.7 for these two cancers. More recent estimates (UNEP 1991) give p to be 2 5 and 1.4 for squamous and basal cell cancers, respectively. Combining the data for basal and squamous cell cancers, and noting that the former are about four times more common than the latter, exemplary values for a and p of 5 and 2, respectively, are often adopted in risk estimates of NMSC (Schothorst et al 1985, van der Leun 1984, Diffey 1987), and will he used here.
5. Human exposure as a consequence of ozone loss
In the absence of ozone depletion the adult indoor worker continues to receive
an annual facial exposure dose of 93 MED. The child receives 157 MED per year until the age of 18 and thereafter 93 MED each year (assuming he/she becomes an indoor worker). However, if ozone depletion continues indefinitely at the rates shown in table 4, it is possible to calculate the expected lifetime exposure, and hence the increased risk of developing skin cancer, for each subject compared with that expected if ozone levels remained at present values. Implicit in these estimates is that behaviour, time spent outdoors and climate remain unchanged. Table A 'Ibtal ozone trends for UK latitudes (from Stolarski U d (1991)).
Monrh Janualy February March April May June July
August September October November December
7% ozone decrease per year 0.6 0.8
0.8 0.7 0.5 a4 0.3 0.2 0.3 0.4 0.4 0.4
2274
B L Diffey
The facial exposure dose received by each subject during the 12-month period t years from now would be 12
MED
H(m){l+RAF[1-(1-6(m))‘]) m=1
where H ( m ) is the monthly exposure from the relevant column in table 4, h ( m ) is the fractional ozone depletion in month m (i.e. U100 of the values given in table 4) and R A F is the radiation amplification factor defined such that a 1% decrease in ozone results in a R A F % increase in carcinogenic-effective radiation at the Earth’s surface. Using the most recent action spectrum for photocarcinogenesis in hairless mice a factor of 1.4 for R A F is obtained (UNEP 1991); this B slightly lower than the value of 1.6 used previously (UNEP 1989). Computations based upon the reference erythema action spectrum (McKinlay and Diffey 1987) as a surrogate for a carcinogenic action spectrum yield a R A F of 1.15 (Kelfkens et RI 1990). Use of this R A F is likely to underestimate the risk and so the value of 1.4 given above was used in the calculations. By incorporating annual exposure doses into the model for skin cancer risk, it is possible to estimate the increased risk at different ages throughout life (table 5). Tabk 5. Cumulative wlar w exposure Jure io faax a i d iiie reiatile dsk of k i n ianier assuming m n e depletion mntinues indefinitely at current rates. Ozone depletion at ~ r r e n t
No Ozone depletion
Child (presently 10)I when aeed -U aged
Cumulative dose hlED
Relative risk
of skin cancer
Cumulative dose MED
of skin cancer
50 60
58u) 6750
70
7680
1.00 1.00 1.W
6184 7302 8457
1.08 1.10 1.13
~
Addl (presently aged 35) when aged
No Ozone depletion Relative risk
ratCS
Relative risk
Ozone depletion at “ e n 1 rates
Cumulative dose MED
of skin cancer
Cumulative dose MBD
50
5820
1.00
60 70
6750 7680
1.00
5873 6892
1.00
7952
Relative risk
of skin cancer 1.01 1.02 1.04
The above calculations of the lifetime risk of skin cancer assume that ozone depletion continues indefinitely at present rates. However, if there is global adherence to international undertakings for the phasing out of ozone depleting chemicals, as agreed in the Montreal Protocol (UNEP 1987) ozone levels should begin to recover slowly in the next century. Models of atmospheric chemistry and transport are not capable of predicting reliably the details of any future ozone depletion resulting from the increasing concentrations of chlorine compounds which are largely responsible (SORG 1990). There will also be a time lag of several years before stratospheric chlorine
Ozone and skin cancer
2275
concentrations respond to a decrease in chlorine loading. The implication is that stratospheric ozone destruction may continue to increase for several years after the chlorine loading of the troposphere has passed its peak value (SORG 1991). Given these uncertainties the approach used here is to assume that ozone depletion continues at present rates for a period T, years from now and thereafter the ambient ultraviolet levels at that time return exponentially to present levels with a half recovery time of T years. The child’s risk at age 60 and 70 years for a range of T, and T have k e n calculated and the results are shown in table 6 where it can he seen that if ozone depletion continues at present rates for another U) years, say, and then recovers with a half recovery time of 20 years, the risk by age 60 will be 1.06 compared with 1.10 if ozone depletion continues indefinitely at present rates. NMSC in a child presently aged 10 when aged 64 and 70 yean relative ta that under an intact mone layer. W t a are given assuming that ozone depletion mntinues at present rates until a period T,yean from now and thereafter the ambient ultraviolet levels at that time ~ t u m exponentially ta present levels with a half recovery time of r years.
lhbk 6 ?he risk of
Relative risk at age 60 years
T,
r years
years 5
10
15
20
25
30
1.02
1.03
1.05 1.07 1.09
1.05 1.07
50
1.10
1.10
1.03 1.06 1.08 1.09 1.10
1.03 1.06 1.08 1.09 1.10
1.03
30 40
1.02 1.04 1.06 1.09
1.06 1.08 1.09 1.10
10 U)
1.09 1.10
Relative risk at age 70 yean
TC
r yean
yeam 10 U)
30 40 50
6a
5
to
15
20
25
30
1.02 1.04 1.06 1.09 1.11 1.13
1.02 1.05 1.07 1.10 1.12 1.13
1.03 1.05 1.08 1.10 1.12 1.13
1.03 1.06 1.08 1.10 1.12 1.13
1.03
1.04 1.06 1.09 1.11 1.12 1.13
1.06 1.09 1.11 1.12 1.13
Previous estimates of the expected increase in skin cancer incidence have assumed a steady state scenario in which stratospheric ozone is depleted by a tixed amaunt (Kelfkens et a1 1990, Henriksen et a1 1990). The most recent report by UNEP (1991)
predicts that a 1% ozone depletion will result in a 23%&0.4%increase in nonmelanoma skin cancer. In the UK there are about moo0 new cases a year (CRC 1991) and so each 1% decrease in ozone would, in theory, lead to an additional 700 cases per year. It must be stressed, however, that this estimate assumes there will be no long-term changes in cloud cover, time spent outdoors, behaviour or clothing habits. 6. Strategies for reducing sun exposure
Unlike agricultural and marine ecosystems which are also at risk from the potential
2276
B L Difley
effects of increased terrestrial solar UVR, humans have the opportunity to modify their behaviour and so their exposure (Diffey 1992). In the absence of ozone depletion table 5 indicates that the adult d l have a lifetime facial exposure dose (at age 70 y) of 7680 MED. Ozone depletion at current rates is estimated to increase this lifetime exposure to 7952 MED. Only simple measures with minimal effect on lifestyle, such as remaining indoors one extra hour at lunchtime from 1.30 pm until 2.30 pm on each day of hisher two-week summer holiday, need to he adopted to reduce this figure to below 7680 MED. In the case of the child, however, more severe sun protection measures are required to maintain his lifetime exposure below 7680 MED. These would include staying indoors between 11.30 am and 2.30 pm on each day of his six-week school summer holiday and again during this period on every day of his hvoweek summer holiday as an adult As an alternative to reducing time spent outdoors, wearing a hat with a wide brim (at least 3 inches) whenever outdoors during July and August for the remainder of his life would achieve a similar reduction in lifetime facial exposure dose (Diffey and Cheeseman 1992), as would application of topical sunscreens. Any one of these measures alone is probably unduly restrictive and is unlikely to meet with compliance. A more rational approach to sun protection is to encourage adoption of a combination of measures such as avoiding sun exposure around solar noon on clear, sunny summer days by staying indoors or seeking shade, and where this is not practicable to make use of clothing, hats and sunscreens. An important aim, particularly with sun exposure of children, is to avoid sunburn.
7. Discussion
The model described above incorporates climatological data with personal behaviour to estimate the annual burden of ultraviolet radiation in subjects taken to be representative of different population groups. It must be stressed, however, that there will be large variations in the annual exposure doses received by individuals within a given population group depending upon propensity for outdoor activities. The greater leisure time available to children is reflected in an annual exposure dose which may be SO% higher than for adults. The model predicts that a typical annual exposure dose of an indoor worker in the UK (excluding vacational exposure) is about 80 MED, or 4% of ambient. This estimate is in good agreement with those obtained by personal monitoring (Challoner t ? ~nl 1976, Leach et a1 1978, Larko and Diffey 1983, Slaper 1987) and gives support to the validity of the model, despite the inherent assumptions and simplifications regarding behaviour. For British adults alive today ozone depletion continuing indefinitely at current rates is predicted to result in a relatively small additional lifetime risk (< 5%; table 5) of non-melanoma skin cancer, assuming no changes in climate, time spent outdoors, behaviour or clothing habits. The lifetime risk incurred by today’s children, however, is 10%15% greater than expected in the absence of ozone depletion. However, if the production and use of substances which deplete ozone are reduced as expected under the current provisions of the Montreal Protocol (UNEP 1987) the increased lifetime risk of skin cancer is likely to be less than this estimate (table 6). These predicted increases in risk, resulting from greater solar ultraviolet exposure, can be offset by adopting changes to behaviour during the summer months which may involve spending less time outdoors, wearing wide-brimmed hats, applying topical sunscreens, or a combination of these. It is to be hoped that public awareness
2277
Ozone and skin cancer
about potential environmental and health effects of ozone depletion will achieve these changes, which could lead to a reduction-rather than the anticipated increase-in skin cancer incidence. If there is no change in sun exposure habits and the rate of ozone depletion, the calculations suggest that 50 years from now the number of skin cancers occurring each year in the UK will increase from the present number of about 30000 to around 33000. This is a much smaller increase than has occurred over the previous 50 years and illustrates that changes in leisure time, fashion and activities in the sun have had a much greater effect on skin cancer rates than expected as a consequence of ozone depletion. Clearly it will prove difficult to identily the real effect of ozone depletion on skin cancer incidence over the next few decades.
Diminution de I'owne stratosphCrique et risque de cancers mtanb la population britannique.
,
(A
Vexclusion des milanomes) dans
Eauteur pdsente "ne estimation quantilalive de I'accroissement du risque des ancen cutanb, B I'exdusion des milanomes (NMSC), susceptible #etre provoqut dans la population britannique par la diminution de I'ozone slratosphCrique. Ces don"& son1 p-es pour la &nCration actuelle de la population britannique. Pour les adultes vivant acfuellement, I'estimalion prhoit que la diminution de I'ozone, penistant au niveau m u d , n'entrainerait qu'un risque additionnel relativement faible pour toute la durCe de vie (< 5%), en supposant aucun changement de climal, de mmportement gCntral, vis b vis du temps pa& B I'interieur ou #habitudes vestimentaires. Le risque, pour la du& de vie, relatif b des enfants d'aujourd'hui, est apendant de 10% B 15% plus imponant que d u i attcndu en I'aknce de diminution de I'omne. Cependant. si la production et I'utilisation de substances qui panent atteinte B I'ozone wnt &uita, mmme on peut I'attendre Cap& Ies plans du protwole de Montdal, I.acmissement du risque de cancer cutani ( ~ r aprobablement plus bible que celui indiquC ddessus Ces prhisions daccmissement du risque liC B une plus grande exposition au rayonnement ultraviolet peuvent susciter une compensation par Un changement de mmponement au mum des mois de M i , lel que la dduction du temps pa& B I'exlirieur, le pon de dtemenu adaptis, y mmpris de chapeau b larges bords, I'application de d m e s solaires, ou une mmbinaison de ccs pratiques.
Zusammenfassung Die Veningerung des Ozons in der Wratospha~ und das Risiko w n nicht-melanomen Hautkrebserkrankungen in einer britischen Beviilkeerungsgmppe.
Eine quantitative Bestimmung des erhohten Risikos w n nieht-melanomen Hautkreberkrankungen (NMSC) in der britischen Bevolkerung, das durch die Veningerung der stratospharischen Ozonschicht mstandekommt, wurde Fir die heutige Generation durchgefiihn. For heme lebende Envachsene wid bei anhaltender Ozonvemngerung im gegenwiriigen AusmaO ein ,,relativ kleines msiitzlicha Lebenslcilrisiko (< 5%) tiir NMSC emanet, unter der Annahme, da0 k i n e Anderungen auftreten im Klima. in der im Freien verbrachten &it, im Verhalten d e r in den Kleidungsgnvohnheiten. Das kbenszeitrisikc, ki heutigen Kindern kt jedoch 10?&15% gn30er ah man ohne Ozonvemngerung emanen wiirde. Wiirde die Pmduktion und die Vemendung w n Substanzen. die das Ozon zentoren wrringen, wie dies in den Vorkehrungen des Montrealer Pmtokolls wrgesehen kt. a) kt das erhohte Lebenszeilrisiko hum kleiner als dieser Wn. Die berechneten Risikocrhohungen ergeben sich aus der hoheren Exposition dumh solares ullranoletta Licht und kdnnen nur verringen werden durch VerhaltenSndemngen Mhrend der Sommermonale, LE. weniger &it im Freien zu verbringen, entsprechende Kleidung, w r allem geeignete Koptbedeckungen zu uagen. m i e Uvpischen Sonnenschuu zu vetwenden.
B L Diffey
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