COMMENT ECOLOGY How elephants NEUROSCIENCE The LITERATURE How Charles OBITUARY Philip Lawley and the could reduce fire risk in source of the self in Dickens drew on science, but discovery that DNA damage Australia p.30 the brain’s wiring p.31 left room for wonder p.32 can cause cancer p.36 ILLUSTRATION BY MARK SMITH BY ILLUSTRATION

The toxic truth about Added sweeteners pose dangers to health that justify controlling them like alcohol, argue Robert H. Lustig, Laura A. Schmidt and Claire D. Brindis.

ast September, the United Nations will have a normal lifespan. Conversely, up declared that, for the first time in SUMMARY to 40% of normal-weight people develop human history, chronic non-commu- ● Sugar consumption is linked to a rise the diseases that constitute the metabolic Lnicable diseases such as heart disease, cancer in non-communicable disease syndrome: diabetes, hypertension, lipid and diabetes pose a greater health burden ● Sugar’s effects on the body can be problems, cardio­vascular disease and worldwide than do infectious diseases, similar to those of alcohol non-alcoholic fatty liver disease. Obesity contributing to 35 million deaths annually. ● Regulation could include tax, limiting is not the cause; rather, it is a marker for This is not just a problem of the developed sales during school hours and placing metabolic dysfunction, which is even more world. Every country that has adopted the age limits on purchase prevalent. Western diet — one dominated by low-cost, The UN announcement targets tobacco, highly processed — has witnessed rising alcohol and diet as the central risk factors rates of obesity and related diseases. There susceptible to non-communicable diseases; in non-communicable disease. Two of these are now 30% more people who are obese 80% of deaths attributable to them occur in three — tobacco and alcohol — are regulated than who are undernourished. Economic these countries. by governments to protect public health, development means that the populations Many people think that obesity is the leaving one of the primary culprits behind of low- and middle-income countries root cause of these diseases. But 20% of this worldwide health crisis unchecked. are living longer, and therefore are more obese people have normal metabolism and Of course, regulating food is more

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complicated — food is required, whereas world, people are consuming an average of the individual to consume more1,6. tobacco and alcohol are non-essential con- more than 500 calories per day from added Finally, consider the negative effects of sumables. The key question is: what aspects sugar alone (see ‘The global sugar glut’). sugar on society. Passive smoking and - of the Western diet should be the focus of Now, let’s consider toxicity. A growing driving fatalities provided strong arguments intervention? body of epidemiological and mechanistic for tobacco and alcohol control, respec- In October 2011, Denmark chose to tax evidence argues that excessive sugar con- tively. The long-term economic, health-care high in saturated fat, despite the fact sumption affects human health beyond and human costs of metabolic syndrome that most medical professionals no longer simply adding calories4. Importantly, sugar place sugar overconsumption in the same believe that fat is the primary culprit. But induces all of the diseases associated with category7. The United States spends $65 bill­ now, the country is considering taxing sugar metabolic syndrome1,5. This includes: hyper- ion in lost productivity and $150 billion on as well — a more plausible and defensible tension ( increases uric acid, which health-care resources annually for morbidi- step. Indeed, rather than focusing on fat and raises blood pressure); high triglycerides ties associated with metabolic syndrome. salt — the current dietary ‘bogeymen’ of the and insulin resistance through synthesis of Seventy-five per cent of all US health-care US Department of Agriculture (USDA) and fat in the liver; diabetes from increased liver dollars are now spent on treating these dis- the European Food Safety Authority — we production eases and their resultant disabilities. Because believe that attention should be turned to “Sugar is combined with insu- about 25% of military applicants are now ‘added sugar’, defined as any sweetener con- cheap, sugar lin resistance; and rejected for obesity-related reasons, the past taining the molecule fructose that is added tastes good and the ageing process, three US surgeons general and the chairman to food in processing. sugar sells, caused by damage to of the US Joint Chiefs of Staff have declared Over the past 50 years, consumption of so companies lipids, proteins and obesity a “threat to national security”. sugar has tripled worldwide. In the United have little DNA through non- States, there is fierce controversy over the incentive to enzymatic bind­ing HOW TO INTERVENE pervasive use of one particular added sugar change.” of fructose to these How can we reduce sugar consumption? — high-fructose corn (HFCS). It is molecules. It can also After all, sugar is natural. Sugar is a nutrient. manufactured from (glucose), be argued that fructose exerts toxic effects Sugar is pleasure. So too is alcohol, but in processed to yield a roughly equal mixture of on the liver that are similar to those of alco- both cases, too much of a good thing is toxic. glucose and fructose. Most other developed hol1. This is no surprise, because alcohol It may be helpful to look to the many genera- countries eschew HFCS, relying on natu- is derived from the fermentation of sugar. tions of international experience with alcohol rally occurring as an added sugar, Some early studies have also linked sugar and tobacco to find models that work8,9. So which also consists of equal parts glucose consumption to human cancer and cogni- far, evidence shows that individually focused and fructose. tive decline. approaches, such as school-based interven- Authorities consider sugar as ‘empty Sugar also has clear potential for abuse. tions that teach children about diet and exer- calories’ — but there is nothing empty about Like tobacco and alcohol, it acts on the cise, demonstrate little efficacy. Conversely, these calories. A growing body of scientific brain to encourage subsequent intake. for both alcohol and tobacco, there is robust evidence is showing that fructose can trig- There are now numerous studies examin- evidence that gentle ‘supply side’ control ger processes that lead to liver toxicity and ing the dependence-producing properties strategies which stop far short of all-out pro- a host of other chronic diseases1. A little is of sugar in humans6. Specifically, sugar hibition — taxation, distribution controls, not a problem, but a lot kills — slowly (see dampens the suppression of the hormone age limits — lower both consumption of the ‘Deadly effect’). If international bodies are ghrelin, which signals hunger to the brain. product and the accompanying health harms. truly concerned about public health, they It also interferes with the normal transport Successful interventions share a common must consider limiting fructose — and its and signalling of the hormone leptin, which end-point: curbing availability2,8,9. main delivery vehicles, the added helps to produce the feeling of satiety. And Taxing alcohol and tobacco products HFCS and sucrose — which pose dangers it reduces dopamine signalling in the brain’s — in the form of special excise duties, to individuals and to society as a whole. reward centre, thereby decreasing the pleas- value-added taxes and sales taxes — are ure derived from food and compelling the most popular and effective ways to NO ORDINARY COMMODITY In 2003, social psychologist Thomas Babor DEADLY EFFECT and his colleagues published a landmark Excessive consumption of fructose can cause many of the same health problems as alcohol. book called Alcohol: No Ordinary Commod- Chronic ethanol exposure Chronic fructose exposure ity, in which they established four criteria, Haematological disorders now largely accepted by the public-health community, that justify the regulation of Electrolyte abnormalities alcohol — unavoidability (or pervasiveness Hypertension Hypertension (uric acid) throughout society), toxicity, potential for Cardiac dilatation abuse and negative impact on society2. Sugar Cardiomyopathy Myocardial infarction (dyslipidaemia, insulin resistance) meets the same criteria, and we believe that it similarly warrants some form of societal Dyslipidaemia Dyslipidaemia (de novo lipogenesis) intervention. Pancreatitis Pancreatitis (hypertriglyceridaemia) First, consider unavoidability. Evolution- Obesity (insulin resistance) Obesity (insulin resistance) arily, sugar was available to our ancestors as for only a few months a year (at har- Malnutrition Malnutrition (obesity) vest time), or as , which was guarded Hepatic dysfunction (alcoholic steatohepatitis) Hepatic dysfunction (non-alcoholic steatohepatitis) by bees. But in recent years, sugar has been Fetal alcohol syndrome added to nearly all processed foods, limiting Addiction Habituation, if not addiction consumer choice3. Nature made sugar hard to get; man made it easy. In many parts of the Source: ref. 1

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(GRAS) list, which allows food manufactur- THE GLOBAL SUGAR GLUT ers to add unlimited amounts to any food. Global sugar supply (in the form of sugar and sugar crops, excluding fruit Opponents will argue that other nutrients SOURCE: FAO and wine) expressed as calories per person per day, for the year 2007. on the GRAS list, such as iron and vitamins A and D, can also be toxic when over-con- sumed. However, unlike sugar, these sub- stances have no abuse potential. Removal from the GRAS list would send a powerful signal to the European Food Safety Author- ity and the rest of the world. Regulating sugar will not be easy — particularly in the ‘emerging markets’ of developing countries where soft Calories per are often cheaper than potable water or person per day >600 milk. We recognize that societal interven- 500–600 tion to reduce the supply and demand for 400–500 300–400 sugar faces an uphill political battle against 200–300 a powerful sugar lobby, and will require 100–200 <100 active engagement from all stakeholders. No data Still, the food industry knows that it has a problem — even vigorous lobbying by fast- food companies couldn’t defeat the toy ban reduce smoking and drinking, and in Another option would be to limit sales in San Francisco. With enough clamour for turn, substance abuse and related harms2. during school operation, or to designate change, tectonic shifts in policy become pos- Consequently, we propose adding taxes to an age limit (such as 17) for the purchase of sible. Take, for instance, bans on smoking in processed foods that contain any form of drinks with added sugar, particularly soda. public places and the use of designated driv- added sugars. This would include sweetened Indeed, parents in South Philadelphia, Penn- ers, not to mention airbags in cars and con- fizzy drinks (soda), other sugar-sweetened sylvania, recently took this upon themselves dom dispensers in public bathrooms. These beverages (for example, , sports drinks by lining up outside convenience stores and simple measures — which have all been on and milk) and sugared cereal. blocking children from entering them after the battleground of American politics — are Already, Canada and some European coun- school. Why couldn’t a public-health direc- now taken for granted as essential tools for tries impose small additional taxes on some tive do the same? our public health and well-being. It’s time to sweetened foods. The United States is cur- turn our attention to sugar. ■ rently considering a penny-per-ounce soda THE POSSIBLE DREAM tax (about 34 cents per litre), which would Government-imposed regulations on Robert H. Lustig is in the Department raise the price of a can by 10–12 cents. Cur- the marketing of alcohol to young people of Pediatrics and the Center for Obesity rently, a US citizen consumes an average have been quite effective, but there is no such Assessment, Study and Treatment at the of 216 litres of soda per year, of which 58% approach to sugar-laden products. Even so, University of California, San Francisco, contains sugar. Taxing at a penny an ounce the city of San Francisco, California, recently California 94143, USA. Laura A. Schmidt could provide annual revenue in excess of banned the inclusion of toys with unhealthy and Claire D. Brindis are at the Clinical $45 per capita (roughly $14 billion per year); meals such as some types of fast food. A limit and Translational Science Institute and however, this would be unlikely to reduce — or, ideally, ban — on television commer- the Philip R. Lee Institute for Health Policy total consumption. Statistical modelling cials for products with added sugars could Studies, University of California, San suggests that the price would have to double further protect children’s health. Francisco, California 94118, USA. to significantly reduce soda consumption — Reduced fructose consumption could e-mail: [email protected] so a $1 can should cost $2 (ref. 10). also be fostered through changes in sub- Other successful tobacco- and alcohol- sidization. Promotion of healthy foods in 1. Lustig, R. H. J. Am. Diet. Assoc. 110, 1307–1321 (2010). control strategies limit availability, such as US low-income programmes, such as the 2. Babor, T. et al. Alcohol: No Ordinary Commodity: reducing the hours that retailers are open, Special Supplemental Nutrition Program Research and Public Policy (Oxford Univ. Press, controlling the location and density of retail for Women, Infants and Children and the 2003). markets and limiting who can legally pur- Supplemental Nutrition Assistance Pro- 3. Vio, F. & Uauy, R. in Food Policy for Developing 2,9 Countries: Case Studies (eds Pinstrup-Andersen, P. chase the products . A reasonable parallel gram (also known as the food-stamps & Cheng, F.) No. 9-5 (2007); available at http:// for sugar would tighten licensing require- programme) is an obvious place to start. go.nature.com/prjsk4 ments on vending machines and snack bars Unfortunately, the petition by New York City 4. Joint WHO/FAO Expert Consultation. Diet, Nutrition and the Prevention of Chronic Diseases that sell sugary products in schools and to remove soft drinks from the food-stamp WHO Technical Report Series 916 (WHO; 2003). workplaces. Many schools have removed programme was denied by the USDA. 5. Tappy, L., Lê, K. A., Tran, C. & Paquot, N. Nutrition unhealthy fizzy drinks and from Ultimately, food producers and distribu- 26, 1044–1049 (2010). 6. Garber, A. K. & Lustig, R. H. Curr. Drug Abuse Rev. vending machines, but often replaced them tors must reduce the amount of sugar added 4, 146–162 (2011). with juice and sports drinks, which also to foods. But sugar is cheap, sugar tastes 7. Finkelstein, E. A., Fiebelkorn, I. C. & Wang, G. contain added sugar. States could apply good and sugar sells, so companies have Health Aff. W3 (suppl.), 219–226 (2003). 8. Engelhard, C. L., Garson, A. Jr & Dorn, S. zoning ordinances to control the number little incentive to change. Although one Reducing Obesity: Policy Strategies from the of fast-food outlets and convenience stores institution alone can’t turn this juggernaut Tobacco Wars (Urban Institute, 2009); available in low-income communities, and especially around, the US Food and Drug Adminis- at http://go.nature.com/w4o5uk 8 9. Room, R., Schmidt, L. A., Rehm, J. & Mäkela P. around schools, while providing incentives tration could “set the table” for change . Br. Med. J. 337, a2364 (2008). for the establishment of grocery stores and To start, it should consider removing fruc- 10. Sturm, R., Powell L. M., Chriqui, J. F. & Chaloupka, farmer’s markets. tose from the Generally Regarded as Safe F. J. Health Aff. 29, 1052–1058 (2010).

2 FEBRUARY 2012 | VOL 482 | NATURE | 29 © 2012 Macmillan Publishers Limited. All rights reserved