Sunlight Information: Skin Cancers and Vitamin D

Introduction

For the past several decades the numbers of skin cancers, and particularly the deadly one, malignant melanoma, have risen dramatically among Caucasian populations throughout the world. In the USA melanoma is the seventh most commonly diagnosed cancer with a rate of 14.2 cases per 100,000 population, ⁽¹⁾ while in 1987 Queensland, Australia, had 55.8 cases per 100,000, the world’s highest rate. ⁽²⁾ The incidence of the various types of skin cancer in the general British population has been increasing at an annual rate of two to eight percent over the past 2 decades. ⁽³⁾ The contributory factors seem to be a light-skinned, northern European population living in areas of high ambient sunlight, and the incidence of the disease is seasonal, with more cases reported in summer than winter. Yet several clinical and epidemiological aspects of cutaneous melanoma seem anomalous because they contrast with other sunlight-associated skin cancers. For example, persons with the greatest risk of melanoma are not those with the greatest cumulative solar exposure; the anatomic areas that receive the most solar exposure are not preferentially affected; and not all light-skinned people suffer the same – albino Africans who have no pigmentation, are more likely to get sunburn and a number of other skin complaints as a result of exposure to the sun, but they don’t get melanomas. ⁽⁴⁾

In the 1960s I lived with my family in Singapore, just 1.5 degrees from the Equator. I have blond hair, fair skin and blue eyes. It is a combination not believed to be suited to the harsh sun of the tropics. Nevertheless, I regularly went on the beach, to the swimming pool or sailing on the South China Sea with little or nothing on, in the heat of the midday sun. I don’t go brown, the best I can manage by way of a tan is a dark golden colour. I remember, in an effort to deepen my tan, I would lie out for hours with the sun to one side of me and its reflection in a mirror of cooking foil on the other to increase my exposure. Like everyone else in the ex-patriot Singapore community, I didn’t give skin cancer a thought in those days; the phrase ‘malignant melanoma’ was unheard of.

I didn’t use a sunscreen. They too were unavailable. If we used anything at all, which most of the time we did not, it was usually a well-shaken mixture of coconut oil and vinegar. This was a concoction used at the time by naturists. We smelt like a fish and chip shop, but we didn’t get burnt in the years we lived there.

Today, it seems, all that has changed. Why? What has changed in the last forty years?

Skin cancers

There are three major forms of skin cancer:

• Basal cell carcinoma is the most common form of skin cancer. It forms small, fleshy bumps or lumps on the head, neck, and hands. Named for the lowest layer of the epidermis (top layer of skin) where the cancer originates. It occurs most frequently in men who spend a great deal of time outdoors and is usually found on the head and neck. ⁽⁵⁾ Basal cell carcinoma is not particularly dangerous as it rarely spreads throughout the body, although it can extend below the skin to the bone.
• Squamous cell carcinoma is the second most common skin cancer. It usually affects people who sunburn easily, tan poorly, and have blue eyes and red or blond hair. Squamous cell carcinoma often develops from actinic keratoses and can metastasise (spread) if left untreated. ⁽⁶⁾
• Malignant melanoma is the rarest form of skin cancer but it is the most deadly. It originates in the melanocytes – the cells that produce the skin colouring or pigment known as melanin – and can be recognised by its black or grey colour. It usually grows from an existing mole, which may enlarge, become lumpy, bleed, change colour, develop a spreading black edge, turn into a scab, or begin to itch. It is more prevalent among city and office workers than among people who work out-of-doors and is thought to be linked to brief, intense periods of sun exposure such as one might get on annual holidays on sunny beaches and a history of severe sunburn in childhood or adolescence. Malignant melanoma metastasises readily and is almost always fatal if not caught in time ⁽⁷⁾ as it responds poorly to conventional therapy. ⁽⁸⁾ Malignant melanoma is growing at a rate of seven percent per year in the United States. In 1991 cancer experts estimated that there would be about 32,000 cases during the year of which 6,500 would be fatal. ⁽⁹⁾ In Canada melanoma incidence rose by six percent per year for men and by 4.6 percent per year for women during the period 1970 to 1986. ⁽¹⁰⁾ In Australia the rate for men doubled between 1980 and 1987 and for women it increased by more than fifty percent. ⁽¹¹⁾ It is now estimated that, by the age of 75, two out of three Australians will have been treated for some form of skin cancer. ⁽¹²⁾

Who’s at risk?

• Whites at greater risk than other groups.
• People who have had excessive exposure to UV radiation from the sun without protection.
• People with fair skin are at more than twenty-times greater risk.
• Men are two to three times more likely than women to have basal cell and squamous cell cancers.
• People with a family history of skin cancer.
• Workers exposed to arsenic, industrial tar, coal, paraffin, and certain types of heavy oils.

How to detect skin cancer

Consult a dermatologist immediately if you have moles or pigmented spots with these characteristics:

• Asymmetrical (one half is not identical to the other)
• Borders that are irregular, uneven, or ragged
• Colour varies from one area to another
• Diameter is larger than 6 mm

Ultraviolet radiation

All types of skin cancer are attributed to exposure to the ultraviolet (UV) part of the spectrum of sunlight. UV is classified as three distinct wavebands: A, B and C. They are all believed to contribute to the development of skin cancer. ⁽⁵⁾

• UVA rays constitute between ninety and ninety-five percent of the ultraviolet light that reaches the earth. It is not absorbed by the ozone layer. UVA light penetrates furthest into the skin and is involved in the initial stages of suntanning. UVA tends to suppress the immune function and is implicated in premature aging of the skin. ^{(5) (13)}
• UVB rays are partially absorbed by the ozone layer. They do not penetrate the skin as far as the UVA rays but are the primary cause of sunburn. They are also responsible for most of the tissue damage which results in wrinkles and aging of the skin and are implicated in cataract formation ⁽⁵⁾ .
• UVC rays are almost completely absorbed by the ozone layer. However, it is thought that as the ozone layer thins UVC rays may begin to contribute to sunburning and premature aging of the skin ⁽⁵⁾ .

How strong is the evidence linking exposure to sunlight with melanoma?

During the 1980s and early ’90s more than a dozen studies compared histories of sunburn in patients with melanoma and controls. But differences in design and definition of sunburn make it difficult to quantify a single estimate of risk.

The most complete data on melanoma and sunburn come from six studies from Australia, Europe and North America. These studies suggest an association but say that the effect is modest. They emphasise the point that episodic exposure seems to be more risky than constant exposure. ⁽¹⁴⁾

British doctors R Marks and D Whiteman are unconvinced of the sunlight/melanoma link. They point out that:

• Melanoma can be found on ovaries
• Melanoma occurs less frequently on sun-exposed areas
• In Japan forty percent of pedal melanomas are on the soles of the feet
• There is 5-times more melanoma in Scotland on the feet than on the hands
• And melanoma in Orkney and Shetland is ten times that of the Mediterranean islands.

Other clinicians agree. Karnauchow says: “The simplistic idea of a sun/melanoma relationship is based more on a belief than science.”. . . “As with other neoplasms, the cause of melanoma remains an enigma and most probably the sun has little, if anything, to do with it.” ⁽¹⁵⁾ And Newcastle dermatology professor, Sam Shuster states that the main reason for the supposed increase in melanomas was a change in diagnostic beliefs: lesions previously regarded as benign became classified first as dubious then as malignant. “Melanomas are being invented, not found,” he says, ” . . . exposure to screening and pigmented lesion clinics is a greater cause of melanoma than sun exposure.” ⁽¹⁶⁾

Dr Anne Kricker and colleagues, looking at studies into skin cancer other than malignant melanoma and exposure to sunlight, also say that the evidence linking skin cancers with sun exposure is weak. They note that most studies have not found statistically significant positive associations, while the few that have lacked empirical evidence that sun exposure was the cause.

“Many questions remain about the relationship between sun exposure and skin cancer,” they say. ⁽¹⁷⁾

The ozone hole

The stratospheric ozone layer is a delicate umbrella guarding us from the worst effects of solar radiation. One suggested cause of the recent increase in skin cancers is our use of chemicals which interact with protective layers in our atmosphere that screen us from the sun’s ultraviolet rays, of which the best example is a hole in the ozone layer which appeared over the Antarctic a few years ago.

The history of skin cancers follows the increase in the use of many chemicals now known to be harmful to the environment. Manufacturing processes which use or generate such synthetic chemicals as chlorofluorocarbons (CFCs), hydrochlorofluorocarbons (HCFCs), and other perfluorinated compounds (PFCs) all of which tend to destroy the ozone layer as well as having other deleterious effects on our atmosphere, have proliferated over the past half century.

Not only do these gases have a strong environmental effect, their chlorine and fluorine bonds make them exceptionally long-lived in the environment. For example, data show that sulphur hexafluoride may persist in the atmosphere for up to 3,200 years.

Could our increasing release of these chemicals into the atmosphere be the cause of the dramatic increase in skin cancers? Unfortunately, it seems not. In 1991 Professor Johan Moan of the Norwegian Cancer Institute made an astounding discovery: He found that between 1957 and 1984 the annual incidence of melanoma in Norway had increased by 350 percent for men and by 440 percent for women. But he also determined that there had been no change in the ozone layer over this period. His report concluded that: “Ozone depletion is not the cause of the increase in skin cancers”. ⁽¹⁸⁾

But if the ozone layer has not yet changed significantly, except at the poles, then what is causing the recent, enormous increase in skin cancer?

The sunscreen connection

The Australian experience might provide the first clue. The medical establishment in Queensland has vigorously promoted the use of sunscreens for many years – and today, Queensland has more cases of melanoma per capita than any other place in the world. This is a trend seen worldwide.

Incidence rates of melanoma have risen especially steeply since the mid-1970s. The two principal strategies for reduction of risk of melanoma and other skin cancers during this period were sun avoidance and use of chemical sunscreens. Rising trends in the incidence of and mortality from melanoma have continued since the 1970s and 1980s, when sunscreens with high sun protection factors became widely used.

Sunscreens are designed to protect against sunburn which is caused by UVB; they generally provide little protection against UVA rays. There are two types of sunscreen:

• Physical sunscreens contain inert minerals such as titanium dioxide, zinc oxide, or talc and work by reflecting the ultraviolet (UVA and UVB) rays away from the skin. This is the type seen as white or coloured bands on the lips and faces of sportsmen.
• Chemical sunscreens contain chemicals such as benzophenone or psoralen as the active ingredient. They prevent sunburn by absorbing the (mainly UVB) ultraviolet rays. These are the sunscreens used by those on the beaches wishing to tan. A sunscreen with a sun protection factor (SPF) of 15 filters out approximately ninety-four percent of the UVB rays. Using one with a SPF of 30 does not double to protection – filtering out ninety-seven percent means that it only increases protection by about three percent. And this quoted SPF applies to UVB rays only. The protection provided against UVA rays in chemical sunscreens is much less at about ten percent of the UVB rating. ⁽¹⁹⁾ Drs Cedric and Frank Garland of the University of California are the foremost opponents of the use of chemical sunscreens. They point out that the greatest rises in melanoma are in countries where chemical sunscreens have been heavily promoted. ⁽²⁰⁾ They say that, while sunscreens do protect against sunburn, there is no scientific proof that they protect against melanoma or basal cell carcinoma in humans.

Indeed, the Garland brothers strongly believe that the increased use of chemical sunscreens is the primary cause of the skin cancer epidemic. Recent studies by them have shown a higher rate of melanoma among men who regularly use sunscreens and a higher rate of basal cell carcinoma among women using sunscreens. ^{(21) (22)} This was confirmed by another study group who found that ‘always users’ of sunscreens had 3.7 times as many malignant melanomas as those ‘never using’.

The Garland brothers suggest that this is because people using sunscreens develop a false sense of security; that because they do not get a sunburn they are encouraged to stay longer in the sun, but there may be other reasons why chemical sunscreens can be dangerous:

• Chemical sunscreens do little to stop UVA rays. These rays penetrate deeper into the skin where they are strongly absorbed by the melanocytes which are involved not only in the production of the skin-tanning pigment, melanin, but also in the formation of melanoma. ⁽²⁰⁾ UVA rays also have a depressing effect on the immune system. ⁽²³⁾
• More importantly, however, may be the fact that most chemical sunscreens contain up to five percent of benzophenone or its derivatives oxybenzone or benzophenone-3 as their active ingredient. And benzophenone, used in industrial processes to initiate chemical reactions and promote cross-linking. ⁽²⁴⁾ is one of the most powerful free radical generators known to man. Moreover, benzophenone is activated by ultraviolet light. UV breaks benzophenone’s double bond to produce two free radical sites. These free radicals desperately look for a hydrogen atom to make them “feel whole again”. While they may find this hydrogen atom, harmlessly, in the sunscreen, they could equally find it on the surface of the skin and thereby initiate a chain reaction which could ultimately lead to melanoma and other skin cancers.
• Harvard Medical School researchers also discovered that psoralen, another ultraviolet light-activated free radical generator, is an extremely efficient carcinogen. They found that the rate of squamous cell carcinoma among patients with psoriasis, who had been repeatedly treated with UVA light after an application of psoralen to their skin, was eighty-three times higher than among the general population. ⁽²⁵⁾ This added weight to a study in 1991-2, in which scientists at the European Organisation for Research and Treatment of Cancer (EORTC) found that regular use of sunscreens increased cancer risk by fifty percent but sunscreens containing psoralen multiplied the risk by 228 percent. They also showed that in people with a poor ability to tan, psoralen users had almost four-and-a-half times the risk of malignant melanoma compared to regular sunscreen users. There was no increase of risk for those using self-tanning cosmetics. They say: “Serious doubts are raised regarding the safety of sunscreens containing psoralens”. ⁽²⁶⁾

There is, however, some evidence that regular use of sunscreens helps prevent the formation of actinic keratoses, the precursors of squamous cell carcinoma. ⁽²⁷⁾

The dietary connection

In the 1970s, when kidney transplantation was pioneered, doctors first encountered the problem of tissue rejection. To combat it, they gave their transplant patients linoleic acid. This suppressed their immune systems very effectively, preventing their transplanted kidneys being rejected. But it also caused a large increase in cancers and this treatment was stopped.

Since then, linoleic acid and oils that contain it, have been shown time and again to increase the risk of several types of cancer, including skin cancers.

Linoleic acid is the major fatty acid in all polyunsaturated vegetable margarines and cooking oils:

• Polyunsaturated margarines are around 40% linoleic acid
• Sunflower, safflower, corn and soya oils are all more than 50% linoleic acid.

Drs B S and L E Mackie, working on Australia’s Sunshine Coast have a great deal of experience in skin cancers. They say: “In view of the work of Black and Erickson in mice and our own work in humans, we believe that human subjects who are at high risk of melanomas and other solar-induced forms of skin cancer should be advised to be moderate in their intake of dietary polyunsaturated fats.” ⁽²⁸⁾

Patricia Holborrow also points out that the increase in melanomas could be a result of dietary changes to PUFs.”Recently, I followed up four families that started in 1976 to use a diet with preferred oils as safflower and sunflower oil and low in salicylates and additives (that interfere with the metabolic pathway of these fats). There had been three cases of cancer resulting in two deaths in these families.” ⁽²⁹⁾ “The issue is further complicated by dietary factors that are cofactors for the metabolic pathways for the fatty acids and which may in addition favour or have a negative effect on the anticancer or cancer enhancing properties of the various prostaglandins (eg the negative effects of vitamin E and the positive effects of vitamin C).” ⁽³⁰⁾

The Australians are as paranoid about heart disease as the Americans. I was in Australia in 1995 and noticed that it is even their custom to remove the cream from milk and replace it with polyunsaturated vegetable oil.

One of the recommendations for reducing the risk of skin and other cancers is to reduce intakes of fats and take vitamin supplements. But this approach doesn’t seem to work. The findings of a huge study by scientists at the Departments of Nutrition and Epidemiology, Harvard School of Public Health, Boston; the Division of Human Nutrition and Epidemiology, Wageningen Agricultural University, Wageningen, Netherlands; the Department of Community and Preventive Medicine, Mount Sinai School of Medicine, New York; and the Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, of 43,217 male participants of the Health Professionals Follow-up Study, did not support the hypothesis that diets low in fat or high in specific vitamins lower risk of basal cell carcinoma. ⁽³¹⁾

It’s usually saturated animal fats that get the blame for all diseases today. They are not the culprits — ‘healthy’ vegetable oils are (see Polyunsaturated Fats in The Cholesterol Myth)

The benefits of sunlight

Although the medical establishment still strongly supports the use of sunscreens there is a growing consensus among progressive researchers that the use of sunscreens and heeding the current advice to cover up when out doors may promote not only skin cancers but other cancers as well.

There is very little vitamin D in any of the food we eat. Most of the body’s vitamin D supply is manufactured by the action of UVB rays on lipids on the skin. ⁽³²⁾ Using a sunscreen drastically lowers this production. ⁽³³⁾

Researchers at the Occupational Medicine Department, School of Medicine, University of California, San Diego studied men in the US Navy during 1974-1984. They discovered that personnel working indoors had 10.6 cases of melanoma per 100,000 while those who worked in occupations that required spending time both indoors and outdoors had the lowest rate at 7.0 per 100,000. They also determined that there were more melanomas on the trunk than on the more commonly sunlight-exposed head and arms. Findings from this study suggest a protective role for brief, regular exposure to sunlight and fit with laboratory studies that showed that vitamin D suppressed the growth of malignant melanoma cells in tissue culture. ⁽²⁷⁾

The same team found that lack of exposure to ultraviolet sunlight may place some populations at higher risk of breast cancer. The association between total average annual sunlight energy striking the ground and age-adjusted breast cancer mortality rates in eighty-seven regions of the United States was evaluated. Annual age-adjusted mortality rates for breast cancer varied from 17-19 per 100,000 in the South and Southwest to 33 per 100,000 in the Northeast. Risk of fatal breast cancer in the major urban areas of the United States increased as intensity of local sunlight decreased. They conclude that “Vitamin D from sunlight exposure may be associated with low risk for fatal breast cancer, and differences in ultraviolet light reaching the United States population may account for the striking regional differences in breast cancer mortality”. ⁽³⁴⁾

They also evaluated the association between total average annual sunlight energy striking the ground and age-adjusted breast cancer incidence rates in the USSR and found that the pattern of increased breast cancer incidence in regions of low solar radiation in the USSR was consistent with the geographical pattern seen for breast cancer mortality in the USA and worldwide. ⁽³⁵⁾

A low blood level of vitamin D is known to increase the risk for the development of breast and colon cancer ⁽³⁶⁾ and may also accelerate the growth of melanoma. ^{(27) (28) (37)} Because of this, Dr Gordon Ainsleigh in California believes that the use of sunscreens causes more cancer deaths than it prevents. He estimates that the 17% increase in breast cancer observed between 1991 and 1992 may be the result of the pervasive use of sunscreens over the past decade. ⁽³⁰⁾ He also estimates that 30,000 cancer deaths in the United States alone could be prevented each year if people would adopt a regimen of regular, moderate sun exposure.

Prostate Cancer

That this could be so is confirmed by recent studies which have suggested that exposure to ultraviolet (UV) radiation may be protective to some internal cancers including that in the prostate. One such is by scientists working at the Department of Urology, North Staffordshire Hospital, Staffordshire, Stoke-on-Trent, UK. They studied 212 prostatic adenocarcinoma and 135 benign prostatic hypertrophy patients to determine whether previous findings showing a protective effect for UV exposure could be reproduced. Their data confirmed that higher levels of cumulative exposure, adult sunbathing, childhood sunburning and regular holidays in hot climates were each independently and significantly associated with a reduced risk of this cancer.⁽³⁸⁾

Cancer Prevention

So what should you do to protect yourself as much as possible against these cancers? Summarizing current research the following recommendations appear reasonable:

• Most important: the best protection is a natural suntan.
• DO try to develop a moderate natural suntan unless you have extremely sensitive skin and burn easily.
• DO build up a tan slowly over, say, a week. Aim for no more than a slight pinkness each day. You should never tan so much that your skin peels off.
• DO remember that sunlight is strongly reflected from sand, snow, ice, and concrete and can increase your direct sunlight exposure by 10 to 50%.
• DO cut down on the amount of polyunsaturated fat and oil in your diet.
• DO see your doctor if you spot any unusual moles or growth on your skin — particularly if they are irregular in shape, bleed, itch, or appear to be changing. Most skin cancers can be cured if caught in time.
• DO NOT sunbathe in the early morning or late afternoon sun as recommended by health authorities. If the sun is low in the sky, you will only receive UVA rays, which is counter-productive. Yes, UVA tans, but it also reduces the body’s vitamin D stores.
• DO NOT use a sunscreen but DO use a moisturiser on your skin. Put it on at least fifteen minutes before going into the sun to allow it to penetrate the skin. It is a good idea to put this on all over your body before you dress to go out. That way you don’t miss bits such as the ‘bikini line’.
• DO NOT shower in the morning before going out to sunbathe. The oils naturally produced by your body during the night are a good protection.
• DO NOT shower for at least an hour after you have sunbathed. Vitamin D formed by the action of the sun on oils on the skin need time to be absorbed.
• Forget ‘aftersun’ products. They are expensive and unnecessary if you have followed this advice and not allowed your skin to be burnt. But after you have showered, do use a moisturiser.
• DO NOT wear sunglasses that filter out 100% of the ultraviolet light. They may protect you against the development of cataracts, but they stop UV entering the eyes – and that is much more important as UV through the eyes prevents cancer.

Dermatologists recommend that you do periodic self-examinations for any changes in the number, size, shape, and colour of pigmented areas of your skin, such as freckles and moles.

However, consulting your doctor or a dermatologist may be the surest way to detect skin cancer early. Physicians are trained to recognise skin cancers and are more likely to detect thinner melanomas, the most dangerous type of skin cancer, than patients who do self-examinations, increasing the likelihood that the skin cancer can be detected early enough to be treated effectively.

Having said that, however, Christopher Del Mar, Professor of General Practice, University of Queensland, Australia, may disagree. He notes that a worried public are the initiators of surgery. Doctors perform excisions of benign pigmented tissue because of pressure from their patients. He says: “The benefits of early detection programs are uncertain; such programs need to be evaluated to determine whether there are any benefits and, if so, whether they outweigh the costs.” ⁽³⁹⁾

Conclusion

Johnathan Rees, Professor of dermatology, University Department of Dermatology, Newcastle upon Tyne, appraises the current melanoma “epidemic”, saying: “Once you excise a pigmented lesion and know its histology you forfeit the chance of knowing what would have happened if you had left it in situ”. “Cohort analyses show, perhaps surprisingly, that mortality from melanoma rose from the 1890s to the 1950s and then started to decline. Changes in leisure activity don’t explain the 3-7% pa increase in melanoma incidence from mid-1950s to early 1980s.

“. . . individuals with higher continuous sun exposure have lower rates than those exposed intermittently.”

“There is after all no robust empirical evidence to defend most health promotion in this area. It has been suggested that the antithesis of science is not art but politics; melanoma is perhaps an example of the two having become mistakenly intertwined. An amicable separation is required. The certainties of health of the Nation and “slip-slap-slop” already look a little shaded: molecules care little for consensus.” ⁽⁴⁰⁾

Some years ago, the vicar of a parish in Devon, who was not in favour of a nearby nudist beach, wrote in his parish magazine: “If God had meant us to walk around without clothes, we’d have been born naked”! Well, of course, He did and we are — perhaps it was for a very good reason.

References

1. American Cancer Society. Cancer facts and figures 1998 . Atlanta, The Society, 1998.
2. MacLennan R, Green AC, McLeod GR, Martin NG. Increasing incidence of cutaneous melanoma in Queensland, Australia. J Natl Cancer Inst 1992; 84: 1427-32.
3. Potten CS, et al . DNA damage in UV-irradiated human skin in vivo: automated direct measurement by image analysis (thymine dimers) compared with indirect measurement (unscheduled DNA synthesis) and protection by 5-methoxypsoralen. Int J Radiat Biol . 1993; 63: 313-24.
4. Diffey BL, Healy E, Thody AJ, Rees JL. Melanin, melanocytes and melanoma. Lancet 1995; 346: 1713.
5. Harmful effects of ultraviolet radiation. JAMA 1989; 262: 380-84.
6. Hacker SM, Flowers FP. Squamous cell carcinoma of the skin. Postgraduate Medicine , 1993; 93: 115-26
7. Lee JAH. The relationship between malignant melanoma of skin and exposure to sunlight. Photochem Photobiol 1989; 50: 493-96
8. Malignant melanoma — Report of a meeting of physicians and scientists, University College, London Medical School. Lancet 1992; 340: 948-51.
9. Skolnick AA. Revised regulations for sunscreen labelling expected soon from FDA. JAMA 1991; 265: 3217-20.
10. Statistics Canada . Canadian Cancer Statistics, 1991.
11. Reynolds T. Sun plays havoc with light skin down under. J Natl Cancer Inst 1992; 84: 1392- 94.
12. Ozone depletion and health. Lancet 1988; ii: 1377.
13. Fitzpatrick TB, Haynes HA. Photosensitivity and other reactions to light . In Harrison’s Principles of Internal Medicine , 7th ed, McGraw-Hill, 1974, 281-84.
14. Marks R, Whiteman D. Sunburn and melanoma: how strong is the evidence? Br Med J 1994; 308: 75-6.
15. Karnauchow PN. Melanoma and sun exposure. Lancet 1995; 346: 915.
16. Shuster S. Melanoma and sun exposure. Lancet 1995; 346: 1224.
17. Kricker Anne, Armstrong B K, English D R. Sun exposure and non-melanocytic skin cancer. Cancer Causes and Controls 1994; 5: 367-392.
18. Moan J, Dahlback A. The relationship between skin cancers, solar radiation and ozone depletion. Br J Cancer 1992; 65: 916-21.
19. Kaidbey K, Gange RW. Comparison of methods of assessing photoprotection against ultraviolet A in vivo. J Am Acad Dermatol Vol. 16, No. 2, Pt. 1, February 1987, pp. 346-53
20. Garland CF, et al . Could sunscreens increase melanoma risk? Am J Publ Hlth 1992; 82: 614-15.
21. Garland CF, et al . Could sunscreens increase melanoma risk? Am J Publ Hlth 1992; 82: 614-15.
22. Garland CF, et al . Effect of sunscreens on UV radiation-induced enhancement of melanoma growth in mice. J Natl Cancer Inst 1994; 86: 798-801
23. Fuller, Cindy J., et al. Effect of beta-carotene supplementation on photosuppression of delayed-type hypersensitivity in normal young men. Am J Clin Nutr 1992; 56: 684-90.
24. Kirk-Othmer Encyclopedia of Chemical Technology. 1981; Vol 13, 3rd ed: 367-68.
25. Stern RS, Laid N. The carcinogenic risk of treatments for severe psoriasis. Cancer 1994; 73: 2759-64.
26. Autier P, et al . Melanoma and use of sunscreens: an EORTC case-control study in Germany, Belgium and France. Int J Cancer 1995; 61: 749-55.
27. Dover JS, Arndt KA. Dermatology. JAMA 1994; 271: 1662-63.
28. Mackie BS, Mackie LE. Dietary polyunsaturated fats. Med J Aust 1988; 149: 449.
29. Holborow P. Melanoma and polyunsaturated fat; cancer and diet. NZ Med J 1990; 103: 515-6.
30. Holborow P. Melanoma and fatty acids. NZ J Med 1991; 104: 19.
31. van Dam R M, et al. Diet and basal cell carcinoma of the skin in a prospective cohort of men. Am J Clin Nutr 2000; 71: 135-141
32. Garland FC, et al . Geographic variation in breast cancer mortality in the United States: a hypothesis involving exposure to solar radiation. Prev Med 1990; 19: 614-22
33. Koh HK, Lew RA. Sunscreens and melanoma: implications for prevention. J Natl Cancer Inst 1994; 86: 78-9
34. Garland FC, Garland CF, Gorham ED, Young JF. Geographic variation in breast cancer mortality in the United States: a hypothesis involving exposure to solar radiation. Prev Med 1990; 19: 614-22
35. Gorham ED, Garland FC, Garland CF. Sunlight and breast cancer incidence in the USSR . Int J Epidemiol. 1990; 19: 820-4
36. Martinez ME, Willett WC. Calcium, vitamin D, and colorectal cancer: a review of the epidemiologic evidence. Cancer Epidemiol Biomarkers Prev . 1998; 7: 163-8
37. Ainsleigh HG. Beneficial effects of sun exposure on cancer mortality. Prev Med 1993; 22: 132-40.
38. Bodiwala D, Luscombe CJ, Liu S, Saxby M, French M, Jones PW, Fryer AA, Strange RC. Prostate cancer risk and exposure to ultraviolet radiation: further support for the protective effect of sunlight. Cancer Lett 2003;192:145-9
39. Del Mar C. Slip, slop slap and wrap. Should we do more to prevent skin cancer? Med J Aust 1995; 163: 511-2.
40. Rees J L. The melanoma epidemic: reality or artefact. Br Med J 1996; 312: 137-8

http://www.second-opinions.co.uk/sunlight.html