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Bring me sunshine

The sun's UV rays cause skin cancer, no doubt about it. But what if they also help ward off other cancers? Celeste Biever finds out what the doctors don't tell you about sunshine

THE sight of three young children with badly sunburnt faces was all it took. An Ohio county sheriff charged their mother, Eve Hibbits, with the felony of “child endangerment” and had her thrown into jail. Though she was released a week later when the felony charges were dropped, the case attracted widespread media attention. The message to the public was clear: neglecting to apply sunscreen to your kids is a form of child abuse.

Few can plead ignorance of the risks. Every summer we are bombarded with official warnings to avoid all exposure to the sun’s cancer-causing rays. But what if the official advice is wrong? A handful of dissidents around the world say that shunning sunshine actually increases our risk of cancer. They argue for a more balanced approach: as long as people don’t go over the top, moderate sun exposure is beneficial, they say.

It’s a controversial message that angers most health professionals who have spent the past 20 years exhorting people to keep out of the sun. Now one of the sunshine advocates is preparing to stoke the argument by publishing detailed guidelines on how much sun we should soak up each week. With research likely to be published soon on the risks of sun phobia, and a major conference in October, sunshine is becoming a hot topic.

Years ago we never used to worry about how much sun we got. Many readers will recall childhood summers when they tore about half-naked without so much as a smear of sunscreen. Clued-up parents would urge their kids to get outside and make some vitamin D, referring to the way skin cells use the energy of sunlight to make this essential chemical.

But times have changed. Convincing evidence that the sun’s rays cause skin cancer began to emerge in the 1970s, and now the case against it appears overwhelming. UV radiation damages skin cells’ DNA, and this can lead to three types of skin cancer, including the deadliest form, malignant melanoma.

Many western countries saw rising rates of skin cancer, but it was in Australia in the early 1980s that the sun avoidance campaign really took off. There, a mix of fair-skinned immigrants, plentiful sunshine and a growing hole in the UV-absorbing ozone layer was causing the highest per capita incidence of skin cancer in the world. In response, Cancer Council Australia launched its “Slip Slop Slap” crusade, urging people to slip on a shirt, slop on sunscreen and slap on a hat. Other countries followed with their own campaigns, and official advice has gradually become more insistent.

Of course some people ignore the warnings. But many of us now find it hard to step outside in summer without worrying about skin cancer. We are exhorted to buy high-factor sunscreen and tightly woven clothing. On the beach children swathed in head-to-toe sun suits are a common sight, and some Australian and American playgrounds now have protective canopies. “The message is getting out there,” says dermatologist Sandra Read at Georgetown University in Washington DC. “People are paying attention.”

With sunshine clearly the enemy, why would anyone think we need more of it? The answer is the vitamin D that our parents knew about. The body has two sources of this important chemical: foods such as oily fish and dairy products, and skin cells, which use those same cancer-causing UV rays to convert a precursor chemical into vitamin D3. Further processing in the liver and kidneys results in “active vitamin D”.

Active vitamin D’s best-known function is enabling calcium to be absorbed from the gut. Calcium plays a key role in nerve, muscle and metabolic signalling, as well as cementing bone cells together. When calcium blood levels fall, the substance is stolen from bones to stop nerves and muscles seizing up. That is why the most obvious sign of vitamin D deficiency is rickets, the weak-bone disease.

But calcium metabolism is not the vitamin’s only vital role. Cells are subject to a multitude of different chemical signals, whose balance determines whether the cells should multiply or stay as they are. Over the past couple of decades, suspicions have grown that active vitamin D is an important brake on cell proliferation. If so, lack of it could predispose people to cancer, the result of cells multiplying out of control.

It has been more than 20 years since active vitamin D was shown to have an anti-proliferative effect, in the lab, at least. In an experiment in 1979, leukaemia cells cultured with the vitamin matured and stopped dividing. Since then several groups have shown a similar effect with cells from cancer of the colon, prostate, breast, lung and even skin. Now several drug firms, such as the Danish company Leo Pharmaceuticals, are developing vitamin D analogues as anti-cancer drugs.

But it takes epidemiological studies, which look at disease patterns in populations, to show if lack of vitamin D can cause cancer in the real world. The pioneer in this field is Cedric Garland of the University of California, San Diego. In 1985 his team published the results of a 19-year study that compared rates of colorectal cancer and vitamin D dietary intake in nearly 2000 middle-aged white men. The 1000 with the highest vitamin D intake had half the incidence of the disease. In 1989 Garland’s team published a larger study, this time spanning 8 years, which seemed to confirm the finding.

Maps of mortality

And it is not just dietary vitamin D that seems to ward off cancer. William Grant, a relative outsider to the cancer research community, says the effect extends to vitamin D made by the skin. Grant’s day job is as an atmospheric ozone physicist at NASA’s Langley Research Center in Hampton, Virginia. While analysing correlations between atmospheric ozone and tree health in the late 1990s, he stumbled upon National Cancer Institute maps of cancer death rates across the US. He noticed that mortality from many common cancers, including that of colon, breast and prostate, was noticeably higher in the north-east than most of the rest of the country (see Map).

Bring me sunshine

The accepted reason was that people in the colder north have a fattier diet, which is known to be a risk factor for cancer. But Grant found that diet only varied by about 10 to 20 per cent between the north-east and south-west, while cancer incidence varied by about 150 per cent. “It was way beyond what can be explained by diet,” he says. “The American diet is very homogeneous now.”

Grant considered another possibility – that people in the southern states, and those who live in rural areas and spend more time outside, are making more cancer-preventing vitamin D. He carried out a huge analysis, comparing the cancer maps with regional UV intensity. There was a statistically significant correlation between low UV and deaths from 13 cancers. He published the research last year, concluding that every year at least 23,600 Americans die of cancer through lack of sunshine (Cancer, vol 94, p 1867). To put that into context, about 9800 die each year from skin cancer.

The paper has drawn a lot of flak. Michael Thun, the American Cancer Society’s vice-president of epidemiology, brands Grant’s conclusion a “wild leap”. “He went rapidly from the geographic rates of cancer to the recommendation that you could prevent large numbers of cancer incidences,” Thun says.

Grant has been criticised for excluding the five states with the highest immigration rates from his analysis, as migration confounds studies of diseases that take a lifetime to develop. The five include the sunny states of California, Arizona, Florida and Nevada, which have high cancer rates, as well as Alaska. Frank De Gruijl, a leading expert on skin cancer at the University of Leiden in the Netherlands, interprets that as “anything that correlates is included, anything that does not is rejected”.

Sunshine phobia

Another criticism of Grant’s approach is that using regional variations in the sun’s strength is too crude a tool for gauging UV exposure. But his findings were borne out by three smaller, more detailed studies by Richard Strange and colleagues at Keele University in the UK. In one, the team recorded details on lifetime sun exposure from 355 men, about half of whom had prostate cancer. The quarter who got the least sun were three times as likely to be in the cancer group as the quarter who got the most (The Lancet, vol 358, p 641).

Grant was also condemned for failing to take into account known cancer risk factors that vary regionally. In response, he has repeated the analysis, this time factoring in urban living, smoking, alcohol, Hispanic race and poverty. The UV correlation was still there. The other risk factors also affected cancer incidence, but nothing correlated as strongly as UV, except smoking when it came to lung cancer. Adding in urban living actually strengthened the conclusion that UV was key. “I would challenge any critic to find another explanation for the distribution,” Grant says.

In the new analysis, Grant has raised his estimate of the yearly toll from lack of sunshine to 100,000 people developing the disease and 40,000 deaths – four times the mortality from skin cancer. The research is still undergoing peer review for publication, but Cedric Garland, for one, finds the figures plausible. “In my opinion, in terms of lives that could have been saved, Grant’s findings are conservative,” he says.

If the vitamin D advocates are right, is there any evidence to suggest our growing sunshine-phobia is reducing the amount we get? According to 5 studies over the past 5 years, rickets is making a comeback in the US. The problem is seen with breastfed infants, as formula milk is fortified with vitamins, but no-one wants to discourage breastfeeding as it is so beneficial in other ways. Instead, the American Academy of Pediatrics warned in April that all breastfed infants should be given vitamin D drops.

Frank Greer, a member of the Academy’s nutrition committee and lead author of the report, says: “We very carefully avoided making the suggestion that babies should get more sun because there is a whole coalition of organisations who recommend that babies should get no sun.” But Michael Holick, a vitamin D expert based at Boston University. has no such reservations. Part of the reason for the resurgence in rickets is, he complains, “a campaign that encourages people to avoid sunlight at all costs”. Holick is particularly concerned for black infants, who are most likely to be deficient in vitamin D. That’s because the pigment melanin, present in higher levels in black people’s skin, helps block UV rays – so black people make vitamin D more slowly than Caucasians.

So can’t everyone follow the paediatricians’ advice, and ensure they get enough dietary vitamin D? This is harder than it sounds, as it would take about four portions of salmon or mackerel a week to get Holick’s recommended dose. “So go to the health food store and take a pill,” says James Spencer, a dermatologist at the Mount Sinai School of Medicine in New York. But that isn’t such a simple solution either. Many people can’t be bothered or actively dislike taking pills every day. Poorer people, whose health is usually worse, are unlikely to spend what money they have on vitamins. In any case, few people realise that obeying doctors’ orders about avoiding sunshine means that they ought to start taking vitamin pills.

There is also controversy over the correct dose. The current recommended daily allowance (RDA, or “adequate intake” as it is starting to be called) of 5 micrograms was calculated assuming that the sole role of the chemical is calcium regulation. Holick, an acknowledged expert on the subject, says that adults getting no sunshine need five times that amount. Taking more than one multivitamin daily is a no-no, as the quantities of the other vitamins, particularly A, quickly reach toxic levels. And taking your vitamins individually is too costly and tiresome for most people. Even vitamin D can be harmful if you consume too much. In contrast, it’s impossible to overdose on sunlight because the skin’s manufacturing process has built-in feedback pathways that prevent this.

There may even be benefits from sunshine that are not available from vitamin D pills, says Holick. Skin cells use UV to make at least two other chemicals, lumisterol and tachysterol. Their function is still unknown, but some people think they could be beneficial. This theory is speculative, but if true it would parallel the accepted idea that people who pop vitamin pills instead of eating healthily miss out on the hundreds of other beneficial compounds in fruit and vegetables.

So how much time in the sun does the vitamin D lobby advocate? It varies greatly, depending on where you are and the time of year, as the more oblique the sun’s rays, the weaker they are. In addition, more oblique rays pass through more of the ozone layer which absorbs more UV. Michael Holick has carried out extensive fieldwork to measure the rate at which the skin makes vitamin D at various latitudes. He has used this to draw up tables showing exactly how long is needed, according to skin colour, location, the time of year and the time of day – in other words, an RDA for sunshine.

It works out at one-quarter of the exposure that would cause redness, on the hands, face and arms, two to three times a week. For example, in London in July between 11 am and 2 pm, this is about 8 to 12 minutes for a Caucasian with medium-fair skin. A black person who never burns would need 45 minutes. The equivalents in Boston would be 5 to 8 minutes and 20 to 30 minutes, and Sydney, 3 to 5 minutes, and 15 to 20 minutes. The periods would be longer at times of the day or year when the sun’s rays are less intense.

Some people would still need dietary vitamin D in winter, but following these guidelines would at least minimise that need, says Holick. The tables are due to appear early next year in his book The UV Advantage.

Meanwhile, many mainstream doctors and scientists continue to vehemently deny that they should change their advice. They point to the mountain of evidence that sunshine causes skin cancer, compared with the scattering of results that link a lack of it to internal cancers. Dermatologist Sandra Read says: “We know that sun is a carcinogen and melanoma is rapidly increasing, whereas the evidence linking a lack of sunlight to cancer is very preliminary.”

Thinking the unthinkable

With many people failing to follow even existing advice to stay out of the sun, dermatologists fear the message that moderate sun exposure is good but excessive amounts are bad would only encourage sunbathers in their dangerous habit. “People who sun themselves on the beach are not at risk of vitamin D deficiency – they are at risk of skin cancer,” says Rebecca Mason, a physiologist at the University of Sydney in Australia.

“People don’t do what you tell them,” agrees Thun. “They don’t go out for 10 minutes and then go in again.” But maybe this view is too pessimistic. At least one other public health message is no longer couched in terms of black and white: many people have come to understand that while binge-drinking is bad for you, moderate amounts of alcohol may do you some good. And there are signs that the health establishment is starting to at least consider the vitamin D lobby’s arguments. In October, the US National Institutes of ҹ1000 will be holding a meeting under the heading “Vitamin D: Bone and Beyond” at which Holick and Grant have been invited to speak.

Even in Australia, melanoma capital of the world, a few doctors are thinking the unthinkable. For the past year, Mason has been helping to raise awareness among certain vulnerable groups of the benefits of moderate exposure to sunshine. The target groups include elderly people, those with dark skin, children who do not play outside, and people who cover up for religious reasons.

Before there can be any consensus, the dermatologists will have to at least consider whether the pendulum has swung too far. Grant says: “I will admit that there are adverse impacts of UV radiation. If dermatologists would admit to the benefits, we would have common ground to go on to the next stage – developing guidelines for UV exposure for optimal health.”

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