Review Article · Übersichtsarbeit Forsch Komplementmed 2013;20:454–460 DOI: 10.1159/000357413

Published online: December 16, 2013

Too Much Salt and How We Can Get Rid of It Cem Ekmekcioglua   Gerhard Blaschea   Thomas E. Dornerb a

Institute of Environmental Health, Institute of Social Medicine, Centre for Public Health, Medical University of Vienna, Austria

Keywords Salt ⋅ Sodium ⋅ Food ⋅ Cardiovascular diseases ⋅ Food industry ⋅ Behavioral change

Schlüsselwörter Salz ⋅ Natrium ⋅ Lebensmittel ⋅ Herz-Kreislauf-Erkrankungen ⋅ Lebensmittelindustrie ⋅ Verhaltensänderung

Summary Humans evolved on potassium-rich diets containing only small amounts of sodium. Nowadays, sodium intake considerably exceeds potassium intake. However, from the evolutionary point of view we are not accustomed to such high salt (sodium chloride) ingestion. The consequences of a high dietary salt intake are primarily elevated blood pressure with a higher risk for cardiovascular diseases, but also a higher probability of developing kidney diseases and stomach cancer. High sodium consumption is favored by an extremely ‘salty’ environment, where palatable salty food is frequently available promoting a dietary salt overload of the human body. To efficiently achieve a consistent reduction in dietary salt intake, sodium content of food should be reduced and eating ­behavior modified. This review covers both of these ­aspects, including the reasons why we are not ‘programmed’ to cope with high salt loads, the clinical consequences of a high salt consumption and the possibilities of reducing dietary salt intake and getting rid of the ‘salty’ environment.

Zusammenfassung Menschen entwickelten sich auf Grundlage einer kaliumreichen Ernährung, die nur geringe Mengen an Natrium enthielt. Heutzutage überwiegt die Natriumaufnahme gegenüber der Kaliumzufuhr erheblich. Aus evolutiver Sichtweise sind wir jedoch an eine derart hohe Aufnahme von Salz (Natriumchlorid) nicht angepasst. Die Folgen einer hohen Salzaufnahme durch Nahrung sind in erster Linie erhöhter Blutdruck mit einem erhöhten Risiko für Herz-Kreislauf-Erkrankungen. Zudem steigt die Wahrscheinlichkeit von Nierenerkrankungen und Magenkrebs. Eine hohe Natriumaufnahme wird durch eine ­extrem «salzhaltige» Umgebung begünstigt, in der schmackhafte salzige Nahrung häufig verfügbar ist und eine Übersalzung des menschlichen Körpers fördert. Um effizient eine konsequente Reduzierung der Salzaufnahme zu erreichen, sollten sowohl der Natriumgehalt von Lebensmitteln reduziert als auch die Ernährungs­gewohnheiten geändert werden. Diese Übersichtsarbeit greift beide Aspekte auf und beschäftigt sich mit den Gründen, warum unsere Körper nicht darauf ausgerichtet sind, eine hohe Salzbelastung zu kompensieren, und mit den klinischen Folgen eines hohen Salzverbrauchs; darüber hinaus werden Möglichkeiten aufgezeigt, die Salzzufuhr zu reduzieren und die salzhaltige Um­gebung loszuwerden.

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Accessible online at: www.karger.com/fok

Cem Ekmekcioglu, MD Institute of Environmental Health Centre for Public Health Medical University Vienna Kinderspitalgasse 15, 1090 Vienna, Austria [email protected]

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Sodium chloride (NaCl), in this manuscript termed simply as salt, is essential to human life. However in the last 5–6 decades it became also increasingly evident that a high salt intake is associated with diseases, especially those affecting the cardiovascular system [1–3]. Many reviews, especially in the last decade, have summarized the detrimental effects of a high salt intake on humans [2, 4–6], and, e.g., the World Health Organization (WHO) has prioritized the reduction of dietary salt intake around the globe [7]. This review gives a general overview of the ‘salt disaster’, which affects several hundreds of million people worldwide and causes high costs in health systems of many countries. It is discussed, why we are not accustomed to higher salt intake, and the negative consequences of a high salt intake on human health are outlined. A‘salty’ environment and the possibilities of how consumers are able to reduce their salt intake are further topics of this paper.

We Are Not Accustomed to Higher Salt Intake For about 5 millions of years the ancestors of the Homo sapiens ate natural plants and animals to which no salt was added [1]. Thus, humans evolved on diets consisting of only small amounts of salt, typically less than 2 g/day [8, 9]. In a comprehensive review by Karppanen and Mervaala [4] it was stated that ‘it is almost impossible to compose a diet consisting of unprocessed natural foodstuffs to provide sodium in excess of 50 mmol (1.2 g) a day.’ However, today our salt intake considerably exceeds the estimated 2–3 g. The average salt intake in most countries around the world is approximately 8–12 g/day. [2]. It is particularly worrying that salt intake in children is also very high, commonly more than 6 g/day in children older than 5 years of age, and that it increases with age [10]. Our ancestors and hunter-gatherers not only had a low sodium diet but also a diet which was rich in potassium by consuming large quantities of vegetables and fruits. Anthropological and epidemiological studies suggest that the daily intake ratio of potassium and sodium is estimated to be 5:1 in ancestral and isolated societies and more or less 1:5 in industrialized societies that consume prepared foods containing a high sodium ratio and drastically fewer fruits and vegetables that are rich in potassium [11]. Over a long period, efficient mechanisms for conserving salt in our bodies were developed to live within a low salt environment. The renin-angiotensin-aldosterone (RAA) system plays a pivotal role in sodium balance by secreting mineralcorticoid aldosterone primarily from the adrenal glands. Aldosterone is the principal hormone of sodium regulation. Its major function is to increase sodium reabsorption in the distale tubules and to collect ducts of the nephrons. One additional function of aldosterone is to sensitize certain specific areas of the brain

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to the circulating levels of angiotensin II that increases thirst and sodium appetite [12]. Although the secretion of aldosterone is considerably suppressed by high sodium levels [13], recent studies also hypothesized that a high-salt diet increases central hypothalamic aldosterone content in Dahl salt-sensitive rats, which, in combination with enhanced endogenous ouabain release, angiotensin II activity, and stimulation of the sympathetic nervous system can contribute to salt-sensitive hypertension, at least in rats [14, 15]. Aldosterone does not only conserve sodium, but also induces the excretion of potassium in order to prevent dangerous hyperkalemias, especially in cases of potassium rich diets, e.g., the paleolithic diet [16]. Studies on the RAA system evolution suggest its emergence about 400 million years ago [17]. A highly active RAA system was important for survival of our ancestors as it ensured salt and volume homeostasis during the different stages of evolution, up until the Homo sapiens appeared. The Homo sapiens lived in a hot African climate where some salt is lost in sweat, although it should also be considered that the human body can efficiently acclimatize to a hot climate by reducing the sodium content of sweat [18]. Furthermore, black people show increased sodium retention compared to white people after high dietary sodium intake [19], which, from an evolutionary perspective, makes sense in terms of conserving salt in a low-salt, hot environment. However, with the use of salt to spice up food, combined with low potassium levels, the RAA system might possibly have functionally altered or be somehow in ‘constant overdrive’, as Fournier and co-workers stated in a recent publication [17]. In evolutionary terms, we are ‘programmed’ to rather conserve sodium and to cope efficiently with high dietary level of potassium. It took millions of years to develop this system, and since a negligible short time span in the history of mankind we are disturbing this system and confronting the body with high amounts of salt our bodies are not used to cope with – it is a challenge to reduce this excess. It is likely that 100,000 years ago the ‘out of Africa’ diaspora of humans began [20, 21]. ­Afterwards, except for some alleles that have been added to the human genome, such as those for protection against sunlight [22] and those for new diets such as milk consumption at adult age [22], the genome has probably not changed significantly. This indicates that clinically relevant genomic changes which may make us salt-resistant to hypertension are not expected in the next decades. Therefore, one important way to reduce risk for hypertension is the reduction of dietary salt intake in nearly all populations around the world.

Too Much Salt, Hypertension, and Beyond Cardiovascular System According to the WHO hypertension is the number one risk factor for mortality worldwide [23]. High blood pressure is a

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Introduction

Stomach Cancer Relating to human observational data and also animal experiments, the 2003 report of the joint WHO/Food and Agriculture Organization (FAO) expert consultation concluded that salt-preserved food and salt might increase the risk of gastric cancer [38]. This statement was also confirmed by the World Cancer Research Fund (WCRF) report from 2007 [39]. In a review from 2011 [40] it was concluded that approximately 24% of stomach cancer cases in the UK in 2010 can be attributed to high salt consumption. Also in a recent meta-analysis of prospective population studies it was found that dietary salt intake is directly associated with the risk of gastric cancer, with progressively increasing risk across consumption levels [41]. Several mechanisms, such as increased gastric Helicobacter pylori colonization, endogenous mutations, or exposure to carcinogens such as N-nitroso compounds from certain salty

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foods, are hypothesized to play a role in increasing the risk of gastric cancer related to high salt intake [42]. However no consistent conclusion can be drawn [42]. Kidney Disease Urinary albumin levels are not only a risk factor for the development and progression of renal disease, but also are strong predictors for cardiovascular risk [43]. Epidemiological studies have shown a direct association between salt intake and urinary albumin excretion, independent of blood pressure [44]. Additionally, a modest reduction of salt intake of about 3.2 g/day (9.7–6.5 g) causes not only significant decreases in blood pressure in certain ethnic groups, but also reduces urinary albumin excretion [45]. Furthermore, it was demonstrated that reduced salt intake may lower the risk of estimated glomerular filtration rate decline [46]. Further Potential Harms by High Salt Consumption Salt fosters thirst. The temporary hyperosmolality in the postprandial phase stimulates the thirst centers in the hypo­ thalamic areas and thus induces the individual to drink. Early studies on animals provided evidence that a high salt intake leads to higher water intake and renal water excretion [47]. Also in humans higher salt intake results in considerably higher urinary volumes [2, 48]. It was estimated that a 100 mmol daily reduction of salt intake would decrease 24-hour urinary volume by 454 ml in untreated hypertensives. Additionally, data analyses from the International Study of Salt and Blood Pressure (Intersalt) [49], including 1,731 hypertensives and 8,343 normotensives, showed that a 100 mmol daily reduction in salt intake would decrease 24-hour urinary volume to 379 ml in hypertensives and 399 ml in normotensives. A reduction of salt intake to 5 g/day would possibly reduce fluid intake in the population by approximately 350 ml/day per person. Reduction of salt intake could be highly relevant in preventing childhood obesity, since the problem is not the thirst itself but the kind of drinks children consume. Thirsty people do not solely drink tap water or other energy-free drinks. Many people, especially children and adolescents, prefer energy-dense beverages to satisfy their thirst. This has been shown for example in a multi-center, cross-sectional observational study in lifestyle and nutrition among European adolescents located in 8 different countries [50]. The energy intake by sugar-sweetened beverages was 489 kJ/day per person. In a cross-sectional study [51] in British children and adolescents salt and fluid intake were assessed in 1,688 participants by using dietary records. It was shown that 31% of total fluid intake is made up of sugar-sweetened soft drinks. After controlling for potentially confounding factors, a significant correlation between intake of salt and total intake of fluid as well as sugar-sweetened soft drink consumption was found. A difference of 1 g/day in salt intake went hand in hand with a difference of 100 g/day in total fluid and 27 g/day in sugar-sweetened soft drink consumption. The authors estimated that a

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major cause of cardiovascular disease (CVD) and responsible for 62% of cerebrovascular diseases and 49% of ischemic heart diseases [24]. Clinically relevant and important is that the risk of CVD increases already at a blood pressure beyond 115/75 mm Hg [25]. Although genetic and pathological factors contribute to the development of hypertension, it undoubtedly can be classified primarily as a lifestyle disease, which is exacerbated by negative chronic stress, obesity, low physical activity, high alcohol intake, and unhealthy diet [26]. Leading national and international societies, e.g., the WHO, have highlighted the important role of sodium intake on blood pressure levels, and diets rich in salt are now widely seen as one of the main causes leading to CVD worldwide [7]. Modest reductions in dietary sodium intake are associated with significant decreases in blood pressure in especially hypertensives but to a lesser degree also in normotensives [27, 28]. Furthermore, a reduced salt intake leads to a decreased cardiovascular morbidity and mortality. Recent meta-analyses calculated a reduced risk of approximately 10– 20% reduction in cardiovascular events [29, 30]. Also children could benefit from salt reduction. In a large study with 650 children, a sodium intake reduction of 15–20% induced a significant decrease in blood pressure after 6 months [31], and in a meta-analysis of controlled trials by He and MacGregor it was concluded that a median reduction of salt intake (42%) in children and adolescents results in immediate decreases in blood pressure and, if continued, may prevent the subsequent rise in blood pressure with age [32]. Furthermore, cross-sectional studies showed a positive correlation between urinary sodium excretion and left ventricular mass, independent of blood pressure [33]. Additionally, it was found that in hypertensive individuals a reduction of salt intake leads to a decrease in left ventricular mass [34]. Since left ventricular hypertrophy is an important independent predictor of cardiovascular events and mortality [35], a reduction of salt intake is highly relevant for cardiac medicine. Finally, in the last years increasing evidence linked a high sodium/salt intake to endothelial dysfunction [36, 37].

The Salty Environment Our environment is not only obesogenic but also extremely rich in salty food. The basic salt needs of a human are around 1–2 g/day; in case of sweating casually more. The intake levels worldwide are even much higher. Salty foods make a high percentage of our daily food supply. Especially in Western countries, salt added in food preparation accounts for the lion’s share of the daily dietary salt intake with estimated 75–80% of total salt intake [57, 58]. The remaining 20–25% of salt occurs naturally in foods or is added at the table or during cooking. One problem is that the access to salty (but also sweet) food for fast and easy consumption, especially when dining out, is generally easy, whereas access to low-salt food is far more than difficult. Fast food restaurants providing lots of salty food can be frequently found in large cities, whereas the access to lowsalt foods, especially fruits and vegetables, is mainly restricted to markets and supermarkets. Furthermore, in the last decades, the portions of commercial energy-dense food and beverages have increased remarkably in the USA [59] and probably also in other countries. Humans have a hereditary affinity to eat when food is visible and easily available; the more is served and the larger portions are served, the more we eat. This trend is associated with an increased intake of energy which in turn favors the development of obesity [60]. Since the salt content of food has not been reduced yet in most countries in the last years, the increasing portions also probably lead to increased intake of salt.

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A review [61] of cost-effectiveness studies from different countries showed considerable economic evidence in favor of population-based interventions to reduce sodium intake. For example, Smith-Spangler et al. [62] found that for US adults aged 40–85 years, collaboration with the food industry that decreases the mean intake of sodium by 9.5% was estimated to avert 513,885 strokes and 480,358 myocardial infarctions over their lifetimes and to save USD 32.1 billion in medical costs. In the course of intensive efforts to improve public health which has been undertaken in Finland since the late 1970s, several companies have reduced the sodium content and increased the potassium and magnesium content of their food products by replacing common salt by sodium-reduced, potassium-, and magnesium-enriched mineral salt [4]. This measure resulted in a decrease of general sodium intake in Finland in the extend of about 4–5 g/d salt with a subsequent decrease in mean diastolic blood pressure of more than 10 mm Hg and a 80% decrease in mortality rate related to heart disease and stroke. Another example is UK, where reductions in the amount of salt added to manufactured food products, in addition to a broad marketing campaign, have been associated with a reduction of salt intake to about 0.9 g/day per person within 7–8 years [63]. There are even more strategies and initiatives in several other countries around the world to reduce salt intake, especially in Europe [64]. An analysis published in 2011 [64] showed that 28 out of 32 countries were working with the food industry to reduce salt load in food. Because of the ubiquity of salt in processed and prepared food it is very difficult for the consumers to control and to reduce their own sodium intake. Therefore joint efforts of the food industry, restaurants, canteens, and similar institutions are very important in order to reduce the salt load in the population.

What Can the Consumer Do? Because of plenty of food available everywhere and anytime and the possibility to choose what, when and how much to eat, it is more than difficult for the consumer to consciously reduce calorie and salt intake. To trigger dietary change, people’s food availability and choices must be changed first. On the one hand, this falls under the remit of the food industry and government, on the other hand the consumer himself must change his/her behavior. Most public health and health promotion interventions aim at changing health behavior by improving health education and attitudes toward nutrition [65]. Behavior change is probably the most important requirement for a more healthy diet and salt reduction [66]. Therefore, both sides have to act and react: the food industry, restaurants, and other food promoters by voluntarily reducing their use of salt and the consumers by changing their behavior. Hence, by doing small steps the salt intake of the population can be decreased gradually to the optimum level (fig.1).

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mean decrease of salt intake of 3 g/day would lead to an average reduction of approximately 2.3 sugar-sweetened soft drinks (assuming ca. 250 g per soft drink) per week and child. Additionally, in 499 German children and adolescents a positive association was found between urinary sodium excretion and beverage consumption [52]. Another recent study in Australian children also showed that high dietary salt intake predicted a higher total fluid as well as sugar-sweetened beverage consumption [53]. Each additional salt intake of 1 g/day was associated with a 46 g/day higher intake of fluid; this remains true also after adjusting for various factors. In summary, the negative effects of a high sodium/salt intake are not only restricted to the cardiovascular and renal systems, but may also adversely affect our metabolism and ­energy intake. It should also be mentioned that not only a low dietary intake of salt but also a higher consumption of potassium-rich fruit and vegetables, as important components of a healthy diet, have preventive potential in chronic diseases [54]. Several publications in the last years provided a high degree of evidence that a Dietary Approaches to Stop Hypertension (DASH)-style diet (which is based on fruits and vegetables as well as on low-fat dairy products) is low in saturated and total fat, and has blood pressure-lowering and cardioprotective ­effects [26, 55, 56].

More information Better information (e.g. nutrient labeling)

Marketing strategies

Changing the environment

Government regulation

Education/Coaching

Food Industry

Consumers Awareness own salt intake

Production change

Reduction of salt in food

Reduced intake level

Reduction of salt intake Awareness low-salt products

Consumers reassurance

Adaptation to

on taste

lower salt levels

Intention to change

Behavioral change

Habituation Further reduction of salt in food

Further reduction of salt intake

Optimal Intake Level Continue to work on consumer motivation

Fig. 1. A simple model of how dietary salt intake can be reduced in population.

In general, behavioral change begins with an intention to change something. One important theory on human health behavior, which is used to promote healthy diet, is the theory of planned behavior [67, 68]. This theory sees behavioral decision or intention as the primary determinant of behavior [67]. Intentions are fuelled by motivations. It is half the battle if someone can be motivated to reduce salt. Concrete and realistic goals addressing the ‘where’, ‘when’, and ‘how’ are necessary for an efficient motivation [69]. Motivations are influenced by the individual perception of how easy or difficult it would be to adopt certain behavior [70]. The degree of intention in turn is influenced by the attitude whether a certain behavior is positively or negatively connoted. Attitudes are based on a subjective calculation of the cost-benefit analysis, which is an important hallmark of the health belief model [71]. What are my profits? How much do I have to invest? Is it realistic? These are classical questions at the onset of a dietary change. If a person realizes that high salt consumption can favor the development of hypertension she/he would be more inclined to change her/his salt use, despite of the subjectively sensed constraints in taste during the first weeks – awareness is the key accelerator of behavior change. One problem is that the consumer associates salt primarily with taste and not with disease. People should be aware not only of the relation between high salt and high blood pressure

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but especially of the association of high salt and stroke, heart attack, or renal failure and the associated burden of hemodialysis. The awareness of a link between salt and high blood pressure will possibly not motivate too many people, since hypertension is mostly a silent disease which is not primarily associated with suffering and impairment. The awareness of pain and disability are possibly better arguments to change behavior. Hedonistic factors undoubtedly play a dominant role in our eating behavior [72]. Therefore the fear not to eat preferred food is probably one of the major barriers to consuming healthier low-salt diets. Reasonable arguments and regular motivation can strengthen one’s will. Therefore, it is necessary to help individuals discover other sources of taste pleasure. Behavioral change is also related to subjective norms, i.e. the perceived social pressure to perform as expected [67, 68]. Social factors appear to be important for different eating behavior, especially in youth where the personality is not fully developed yet. Parents play an important role for the eating behavior of their children and often provide a role model [73]. If a child or adolescent grows up in an environment where a healthy lifestyle, e.g., healthy food and physical activity, have priority the child will likely head toward this direction. On the other hand, an environment which provides unhealthy food negatively affects the child’s eating behavior. A recent study in more than 13,000 children from 9 European countries further supports the importance of family for eating behavior. It was shown that social cultural factors such as demands (parents demand from their children to eat fruit/vegetables) and modelling (mother / father / best friend eats fruits and vegetables) had a stronger effect on eating behavior than the mere availability of fruits and vegetables [74]. Probably one of the most important variables predicting eating behavior is self-efficacy. It relates to people’s beliefs about their capabilities to behave in a certain way [75]. The slogan ‘Yes, we can’ that was used by Barack Obama in his presidential campaign transfers the term self-efficacy into daily practice quite aptly. People with a high level of self-efficacy can usually deal with difficult tasks more easily, i.e. the more confident the person is about her/his abilities the more she/he will be inclined to have a healthy diet (e.g., a low-salt diet) [76]. Self-efficacy is influenced by performance and know-how being related to previous own successful attempts or observations of behavior of others as well as the impacts of this behavior [77]. Self-efficacy can be improved by verbal persuasion, i.e. motivating and encouraging people so that they will consis­ tently maintain a healthy diet according to their experiences [77]. In addition, appreciation and praise are very important to promote behavioral changes in every stage of life, especially in childhood [78]. Self-efficacy can be specific, which means that a person may feel confident to drink for example less sugar-sweetened soft drinks but not to reduce salt intake. Furthermore, self-efficacy is strongly related to abilities and knowledge. If a person is

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More information Expert consultations

informed about healthy nutrition and how to reduce salt, she/ he will probably change his/her eating behavior at least to some extent which is in contrast to someone who has acquired no information on this topic. The final and most sustainable goal of behavior change is to establish habits. A habit is an automatically driven activity including the unawareness to behave in a particular way or to control this behavior [79, 80]. Our life is organized by habits, such as brushing teeth, eating breakfast, and reading the newspaper every morning. Habit has been described as a strong determinant of nutritional behaviors in different settings [79, 81, 82]. It is hypothesized that habits occur when a certain behavior is frequently and consistently performed in a similar and stable manner for the same purpose [83, 84]. Eating is an important example for something which is strongly influenced by habit, and so is high salt consumption [85]. For example, adding salt during meal preparation is performed every day, unconsciously, and without the awareness of how much of it is used. Therefore, it is important to strengthen good and to minimize bad habits [79]. For example, great salt shakers could be substituted by small ones (with small holes), or natural spices could be used instead of salt [70].

Behavior change is a key determinant for an efficient and constituent way to reduce dietary salt intake. Motivation as well as adequate and easily understandable information from experts about health outcomes, salt sources, etc. and regular verbal persuasion are key factors to change behavior toward a low salt intake.

Conclusions In summary, when the food industry, the governments, and the consumers are willing to take the necessary steps and efforts, an efficient reduction in salt intake could be achieved in the population. This would have an enormous relevance for the health and quality of human life worldwide.

Dislcosure Statement The authors declare to have no conflict of interest.

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Too much salt and how we can get rid of it.

Humans evolved on potassium-rich diets containing only small amounts of sodium. Nowadays, sodium intake considerably exceeds potassium intake. However...
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