March 26, 2010

Carole Davis CoRExecutive Secretary of the Dietary Guidelines Advisory Committee Center of Nutrition Policy and Promotion U.S. Department of Agriculture 3101 Park Center Drive, Room 1034 Alexandria, VA 22303

RE: 2010 Dietary Guidelines for Americans

Dear Ms. Davis and the Dietary Guidelines Advisory Committee:

The American Meat Institute (AMI) is the nation's oldest and largest meat packing and processing industry trade association. AMI members slaughter and process more than 90 percent of the nation's beef, pork, lamb, veal, and a majority of the turkey produced in the United States. On behalf of AMI and its member companies, we appreciate the opportunity to comment on the 2010 Dietary Guidelines for Americans (or the Guidelines). AMI has and will continue to support the use of sound science as the foundation for nutritional public policy.

AMI would like to commend the Dietary Guidelines Advisory Committee (the Committee) for its structured approach in compiling the data, modifying proposed nutritional targets, and working with the industry in a partnered approach to improve consumer . The health of our customers is the driving force in the production of meat and poultry products, not only with respect to improving the safety of meat and poultry products, but also in offering diverse nutritional products to consumers so they can make an educated decision in choosing the food that best fits their personal lifestyle and family needs. The following comments address specific concerns that require further clarification and/or additional consideration prior to finalizing the Guidelines.

Sodium Plays an Important Role in Meat Production and Safety

Salt or plays a critical role in the production of meat products -- whether used by large commercial processors, local butchers, or even within the consumer’s home -- to improve the , texture, and safety of those products. Specifically, adding improves the functionality of the muscle proteins. The change in ionic strength increases hydration of the proteins, improving the binding of fat by the muscle protein in products like bologna and . Sodium chloride also improves tenderness during cooking. The binding of meat proteins caused by sodium stabilizes the delicate protein matrix during cooking, thus producing a final product that has improved texture, tenderness, and palatability.

Consumer health is paramount to successfully processing meat and poultry products. Sodium reduction is an issue the meat and poultry industry has been actively working on since the 1980s. In the last 20 years, the industry has learned much through its efforts to reduce sodium in meat and poultry products, including a greater understanding of pathogenic bacterial risks presented by Listeria monocytogenes, Salmonella, and pathogenic Escherichia coli in processed meat and poultry items.

Listeria monocytogenes is of particular concern in ready-to-eat processed meat and poultry items because it is very difficult to eradicate from the environment and if products are contaminated, the organism will survive and grow (even at refrigerated temperatures) unless growth inhibitor systems are used. Three common ingredients used for this purpose are sodium chloride, sodium or lactate, and sodium diacetate. These inhibitors are used in up to 70% of processed items in the U.S. marketplace. Reduction in the use of one requires a concomitant increase in another in order to maintain the same degree of safety. Alternatives to these ingredient approaches exist, but are not widespread due to ease of use, economic, and product quality reasons.

As an ingredient in meat products, sodium is used as a preservative, which is one aspect of a multi-hurdle approach toward maintaining the safety of products. Sodium also contributes to the overall palatability of a food product. Reductions in sodium would produce meat products that would be unacceptable in texture, tenderness, and flavor to consumers. These products may ultimately never be purchased, or of greater concern, purchased with consumers adding ad libim, thus defeating any recommendations the Committee might make regarding daily sodium intake.

For the foregoing reasons, with respect to the decision-making process regarding sodium intake recommendations, AMI respectfully requests that the Committee consider the unforeseen possible food safety consequences of those recommendations.

Protein-Based Diet is a Component of a Healthy Diet

It is in Americans’ best health interest to encourage them to consume meat and poultry products as a dense food that complements a varied and balanced diet, which includes fruits, vegetables, nuts, dairy products, legumes, and grains. AMI is concerned that the Committee is overemphasizing its recommendations to make grains, fruits, and vegetables the core of a plant-based diet as the foundation of a “healthy” diet for Americans.

Although each of those food groups play an important and critical part in a healthy diet, AMI is concerned that there may be a negative bias by the Committee toward animal proteins and more specifically beef and pork products. Regardless that the studies evaluated found limited data to support the hypothesized better health outcomes for plant-based and vegan diets, the Carbohydrate and Protein subcommittee appears to be actively seeking a link between adverse health outcomes and animal proteins. Meat and poultry products are an excellent source of high-quality protein, B-vitamins, zinc, and iron, all of which play a critical role in meeting the daily nutritional needs of Americans.

AMI strongly recommends that the Committee evaluate its data based on sound science and a scientifically based risk assessment, not nutrition publication bias, as the foundation for nutrition public policy. AMI recommends that the guidelines be worded to include a fair and balanced recommendation for inclusion of an animal-based diet as a foundation for a healthy American diet.

Consuming Animal-based Proteins as Part of a Healthy Diet is Not a Health Risk

A number of submissions have commented on the controversial discussion concerning whether red meats and processed meats pose an increased public health risk for Americans, specifically as to development of cancer. AMI ardently supports the submissions of Dr. Dominik Alexander (#000539, 06/30/2009), Dr. Andy Milkowski (#000765, 11/23/2009), and Dr. Douglass Weed (#000510, 05/58/2009).

During the April 2009 meeting, the Committee stated it would defer to the WCRF/AICR Expert Report, Food, Nutrition, Physical Activity and the Prevention of Cancer: A Global Perspective (or the WCRF report) for a variety of diet and cancer research questions. Drs. Weed and Alexander, however, have highlighted significant errors, omissions, and flaws in the analysis and conclusions of the WCRF report. Dr. Milkowski eloquently describes inaccuracies inherent in the myths regarding red meat and processed meat products being the dietary sources of the carcinogenic polycyclic aromatic hydrocarbons and heterocyclic amines, nitrosamines and of nitrite, which despite popular belief is not a carcinogen. The common concern of meat-acquired nitrite consumption as a carcinogen is unwarranted, which was supported by the 2000 National Toxicology Program Report TR495 that found nitrite levels typically used in meat products are not toxic or carcinogenic.

These errors concerning the inaccurate causal relationship between red meats, processed meats, and cancer are the basis for the WCRF report, which recommends limiting intake of red meats and processed meat in the human diet. AMI strongly believes that the WCRF report does not accurately reflect the body of scientific evidence in this area and should not be used as a default resource and source for diet and cancer research questions.

Summary

Meat is an important component of a healthy human diet because it provides essential amino acids, minerals such as iron, vitamins, and other dietary requirements. Processed and enhanced meat products in the market place today are available to consumers at very affordable prices. As previously stated, the health of consumers is the driving force in the production of our products. AMI looks forward to working with the Committee to set achievable, practical, and meaningful nutrition policy for the American people and in that regard, AMI appreciates the opportunity to comment on the development of the 2010 Dietary Guidelines for Americans. AMI would be pleased to work with the Committee regarding each of these concerns and requests that AMI’s recommendations be considered before finalizing the 2010 Dietary Guidelines for Americans.

Thank you for your consideration of the comments provided above. If there are any questions about the above comments, please do not hesitate to contact me at [email protected] or 202-587-4249.

Sincerely,

Betsy Booren, Ph.D. Director, Scientific Affairs

cc: J. Patrick Boyle Jim Hodges Susan Backus March 31, 2010

Carole Davis CoRExecutive Secretary of the Dietary Guidelines Advisory Committee Center of Nutrition Policy and Promotion U.S. Department of Agriculture 3101 Park Center Drive, Room 1034 Alexandria, VA 22303

RE: 2010 Dietary Guidelines for Americans

Dear Ms. Davis and the Dietary Guidelines Advisory Committee:

The American Meat Institute (AMI) is the nation's oldest and largest meat packing and processing industry trade association whose members slaughter and process more than 90 percent of the nation's beef, pork, lamb, veal, and a majority of the turkey produced in the United States. The U.S. meat and poultry industry offers a diverse array of products to consumers, so they can make an educated decision in choosing the that best fits their personal nutritional lifestyle and family needs.

During the November 2009 meeting of the Dietary Guidelines Advisory Committee, the Sodium, Potassium, and Water Subcommittee discussed the inclusion of sodium in meat products, the adverse effect it may have on human health, and the necessity of sodium intake reduction. The health of our customers is the driving force in the production of meat and poultry products, which not only includes the offering nutrient dense protein food products, but also in respect to improving and maintaining the safety of the food the meat and poultry industry produces.

The role of sodium in meat and poultry products is primarily for food safety, not the common misperception of improving product palatability. AMI respectfully requests the Dietary Guidelines Advisory Committee include the following articles in the evidence-based review of this topic in the development of the 2010 Dietary Guidelines for Americans.

Taormina has eloquently summarized the critical food safety necessity of sodium chloride in the production food products in his article “Implications of Salt and Sodium Reduction on Microbial Food Safety” in Critical Reviews in Food Science and Nutrition. Taormina concluded

…sufficient research has not been conducted to remove and/or reduce NaCl in processed and restaurant foods to the extent being proposed by various stakeholders through biomedical journals and other media. Governments and food protection groups must convene to weigh the societal risks versus benefits and potential economic burdens associated with imposing further restrictions on use of NaCl in food formulations. Epidemiological and clinical evidence indicates that long-term public health benefits would result from reducing NaCl in human diets. However, short-term unintended consequences related to the impact on microorganisms have not been fully explored. Regulatory action on reducing NaCl in foods without first obtaining thorough predictions on the behavior of foodborne pathogens and spoilage organisms in the food supply could lead to significant disruptions to international food commerce at best. These disruptions would be caused by microbial survival, growth, and spoilage when and where previously unexpected using processing and distribution parameters developed for the current amounts of sodium in foods. At worst, a rush to significantly reduce NaCl without research and careful planning could lead to significant increase in exposure of humans to foodborne pathogens.” 1

Doyle and Glass (2010) have published “Sodium Reduction and Its Effect on Food Safety, , and Human Health” in the January issue of Comprehensive Reviews in Food Science and Food Safety. 2 The Doyle and Glass review considers the published data on the effect on health due to excess salt consumption, the functionality of sodium in the production of processed foods and possible reformulation strategies for sodium reduction while maintaining critical food safety standards.

On behalf of AMI and its member companies, we appreciate your consideration and addition of these articles to the evidence-based review of this topic in the development of the 2010 Dietary Guidelines for Americans. AMI looks forward to working with the Committee to set achievable, practical, and meaningful nutrition policy for the American people through the use of sound science.

If there are any questions about these articles, please do not hesitate to contact me at [email protected] or 202-587-4249.

Sincerely,

Betsy Booren, Ph.D. Director, Scientific Affairs

1 Taormina, P. 2010. Implications of Salt and Sodium Reduction on Microbial Food Safety. Critical Reviews in Food Science and Nutrition. 50(3): 209-227. DOI: 10.1080/10408391003626207. http://dx.doi.org/10.1080/10408391003626207 2 Doyle, M; Glass, K. 2010. Sodium Reduction and Its Effect on Food Safety, Food Quality, and Human Health. Comprehensive Reviews in Food Science and Food Safety. 9(1):44-56. DOI: 10.1111/j.1541-4337.2009.00096. http://www3.interscience.wiley.com/journal/123221587/abstract Critical Reviews in Food Science and Nutrition, 50:209–227 (2010) Copyright C Taylor and Francis Group, LLC ISSN: 1040-8398 DOI: 10.1080/10408391003626207

Implications of Salt and Sodium Reduction on Microbial Food Safety

PETER J. TAORMINA John Morrell Food Group, Cincinnati, OH, USA

Excess sodium consumption has been cited as a primary cause of and cardiovascular diseases. Salt (sodium chloride) is considered the main source of sodium in the human diet, and it is estimated that processed foods and restaurant foods contribute 80% of the daily intake of sodium in most of the Western world. However, ample research demonstrates the efficacy of sodium chloride against pathogenic and spoilage microorganisms in a variety of food systems. Notable examples of the utility and necessity of sodium chloride include the inhibition of growth and toxin production by Clostridium botulinum in processed meats and cheeses. Other sodium contributing to the overall sodium consumption are also very important in the prevention of spoilage and/or growth of microorganisms in foods. For example, sodium lactate and sodium diacetate are widely used in conjunction with sodium chloride to prevent the growth of Listeria monocytogenes and lactic acid bacteria in ready-to-eat meats. These and other examples underscore the necessity of sodium salts, particularly sodium chloride, for the production of safe, wholesome foods. Key literature on the antimicrobial properties of sodium chloride in foods is reviewed here to address the impact of salt and sodium reduction or replacement on microbiological food safety and quality.

Keywords salt, sodium chloride, foodborne pathogens, spoilage, hypertension

INTRODUCTION (2008) recently theorized that habitual sodium consumption in the Western diet, leading to amounts of sodium chloride (NaCl) In recent years there has been a renewal of interest in sodium far above evolutionary norms and potassium far below those reduction in the human diet, particularly in the United States norms, increases and sustains acidity in body fluids, which con- and Europe. Such interest has been fueled by rather compelling tributes net loss of body calcium and could lead to the develop- evidence that excess sodium intake is a major cause of high ment of osteoporosis and renal stones, loss of muscle mass, and

Downloaded By: [[email protected]] At: 20:44 17 March 2010 levels (Dickinson and Havas, 2007; Karppanen age-related renal insufficiency. These and other data have been and Mervaala, 2006; He and MacGregor, 2008), and that hyper- cited by certain public health professionals in their characteri- tension leading to can be prevented by zation of the need to reduce sodium content in foods as “urgent” decreasing dietary sodium intake (Cutler and Roccella, 2006; (Havas et al., 2007). Cook et al., 2007). The World Health Organization (WHO) has Various campaigns for “salt” reduction in the human diet have deemed the evidence “conclusive” that excess sodium causes been organized or reinvigorated to address what is perceived as a hypertension and has advocated world-wide reformulation of serious threat to human health and a burden on healthcare. World processed and prepared foods to achieve the lowest possible Action on Salt and Health (WASH) has set a goal of reduction in sodium content (WHO, 2006). It should be noted that sensi- dietary salt intake of 10–15 g/day to the WHO target of 5 g/day tivity to sodium can vary amongst individuals. For instance, (2009b), while the governmental body for food regulations in some studies suggest that metabolic syndrome enhances blood the United Kingdom, the , has a stated pressure response to sodium so that sufferers are more salt sensi- goal of consumption of no more than 6 g/day (2009a). In the tive than those without the syndrome (Hoffmann and Cubeddu, United States, the Center for Science and the Public Interest 2007; Chen et al., 2009), and that adverse cardiovascular events (CSPI) has petitioned the U.S. Food and Drug Administration can occur more frequently in patients with sodium-sensitive (FDA) to revoke the GRAS status of NaCl and reclassify the hypertension (Morimoto et al.,1997). Frassetto and others molecule as a food additive (FDA, 2007). The microbiological food safety and quality implications of NaCl reduction in foods has received little recent attention both Address correspondence to: P. J. Taormina, 805 East Kemper Road, Cincinnati, OH, 45246. Phone: 513-346-7558. Fax: 513-346-7674. E-mail: in peer-reviewed literature and media relative to that devoted to [email protected] potentially beneficial cardiovascular health impacts. This may 209 210 P. J. TAORMINA

be due to a perception that “refrigeration has largely replaced the number of days or months achieved since the early years of the need for sodium salts as food preservatives” as suggested by this debate. These technologies were designed for present levels Flegel and Magner (2009). Although food microbiologists and of NaCl and other food ingredients. Leistner (1992) purported food scientists can certainly agree that refrigeration is of utmost the theory that even small enhancements of individual hurdles importance in modern food production and distribution, the idea in a food, in summation, have a definite effect on the microbial that refrigeration alone can replace the need to formulate food stability of a product. Conversely, it was also recently reported products for safety and quality is erroneous. One need merely to that even a small 3-gram–a-day reduction in salt intake (about consider the growth potential of the psychrotrophic foodborne 1200 mg of sodium) would result in 6 percent fewer cases of pathogens Listeria monocytogenes, Yersinia enterocolitica, and new heart disease, 8 percent fewer heart attacks, and 3 percent Aeromonas hydrophila in refrigerated foods to realize the im- fewer deaths (Bibbins-Domingo et al., 2009). It is not unrea- portance of formulating food safety into products as part of an sonable to expect small reductions in hurdles, such as through overall risk mitigation system. Among the foodborne bacterial increase in water activity (aw) due to reduction or replacement of pathogens, L. monocytogenes is exceeded in tolerance to NaCl NaCl, could likely tip the balance from microbiologically safe only by Staphylococcus aureus (Nolan et al., 1992). Haphazard to unsafe, and these are the minutia of the debate that warrant elimination of NaCl from processed foods may not only en- careful consideration and validation. able enhanced pathogen growth and survival, it may also permit This review in part attempts to answer some key questions more accelerated spoilage of certain foods causing a negative posed by the U.S. Food and Drug Administration (FDA, 2007) economic impact to producers, distributors, retailers, and con- concerning reducing the salt content of food: sumers. Sofos (1983) thoroughly reviewed the antimicrobial prop- “would reducing the salt content of food, even in a modest way, erties of NaCl in foods and concluded that the removal or the impact the safety or quality of various foods given the wide variety of reduction from processed foods should be based on the results technical functions for which salt is used in food? How feasible would it of appropriate research. A subsequent review by Reddy and be to mitigate this impact if true? Could it be mitigated by, for example, the addition of other ingredients?” Marth (1991) on the subject also summarized foods that were commercially available at the time with less than the normal Another key point of this present review is that of all the amounts of NaCl. While the latter review focused on main- sodium containing molecules used in food, NaCl is among the taining the functional properties of foods with salt-replacement most efficacious in regard to the preservative properties against molecules, summary data justifying the microbiological stabil- foodborne pathogens and spoilage organisms, and therefore has ity and safety of reduced sodium products was reported for the greatest impact on the microbiological safety and quality of Clostridium botulinum and S. aureus in cheeses with some cov- foods. Consequently, if the goal is to reduce the sodium content erage of spoilage organisms in meat, fish, and produce products. in the human diet while maintaining food safety and quality, Their review also summarized data on C. botulinum in meat and other molecules should be considered for their contribution to seafood, and Trichinella spiralis in dry cured ham. Although overall sodium content. Achieving a human diet that is safer both reviews have dealt with preservative properties of NaCl from a nutritional standpoint due to the reduction of NaCl should in foods, there have been related research reports on the topic not outweigh the more immediate possible negative implications since, and an updated and expanded review is in order. As those Downloaded By: [[email protected]] At: 20:44 17 March 2010 of growth or survival of foodborne pathogens in formulated reviews well covered the historical use of NaCl, it will not be foods that were previously less supportive of microbial growth reviewed here. From these past reviews, one can easily conclude and survival. These potential consequences of the removal and that in addition to its necessary functional attributes in complex the reduction of NaCl from foods has received too little research food formulations and recipes, NaCl is perhaps the most ef- given the myriad synergies and influences involving NaCl in fective and versatile antimicrobial ingredient used in foods and food systems and processes. remains one of the most effective tools for the development of safe and wholesome food products. Diminished food safety could be an unintended consequence of salt and sodium reduction in processed foods due to the low- PRESENCE OF SODIUM IN FOODS ering of a key hurdle against foodborne pathogens. The removal or reduction of NaCl as a key hurdle in many of the microbio- The functions of sodium in foods and beverages are as logically sensitive foods and beverages could have far reaching an essential nutrient, flavor modifier, preservative, and leav- effects that may not be evident until well after system-wide ening agent (Miller, 1996). Sodium in the form of NaCl has implementation. Pathogens that otherwise do not overcome the many important technological and processing contributions, intrinsic properties of food systems may grow or persist during such as altering meat and moisture binding in processed meat processing. Advances in food science and technology mani- products (Desmond, 2006). NaCl alters the nutrient availabil- fested in optimization of food product formulations, food pro- ity and texture and consistency of foods, and aides in malt- cessing and engineering conditions, , and han- ing and the fermentation of various foods. The wide array of dling have led to extensions of the shelf life of foods well beyond technological functions of sodium salts and sodium chloride SALT REDUCTION AND FOOD SAFETY 211

Table 1 Some sodium-containing preservative molecules used in processed foods and their contribution to total sodium per serving

Sodium-Containing Molar Mass Molar Ratio Typical Addition Levels Ingredient Formula (g/mole) of Na+ (g / 100 g serving) mg Na+ / 100 g

- chloride NaCl 58.44 0.3934 2.0 78.6790 trisodium phosphate Na3PO4 163.94 0.4207 1.0 42.0703 disodium phosphate Na2HPO4 141.96 0.3239 1.0 32.3894 sodium tripolyphosphate Na5P3O10 367.86 0.3125 1.0 31.2483 - lactate NaC3H5O3 112.06 0.2052 1.5 30.7737 monosodiurn phosphate NaH2PO4 119.98 0.1916 1.0 19.1615 - hexametaphosphate (NaPO3)6 611.77 0.2255 0.75 16.9108 - metabisulfite Na2S2O5 190.11 0.2419 0.2 4.8372 - citrate Na3C6H5O7 258.07 0.2673 0.15 4.0088 - acetate NaC2H3O2 136.08 0.1689 0.15 2.5342 - diacetate NaC4H7O4 142.09 0.1618 0.15 2.4270 - propionate NaC3H5O2 96.07 0.2393 0.025 0.5983 - eryihorbate NaC6H7O6 198.11 0.1160 0.05 0.5802 - nitrite NaNO2 68.99 0.3332 0.017 0.5665 - benzoate NaC6H5CO2 144.11 0.1595 0.025 0.3988 - ascorbate NaC6H7O6 198.11 0.1160 0.01 0.1160 calcium disodium EDTA Na2C10H12CaN2O8 374.27 0.1229 0.005 0.0614

in foods and beverages have been summarized elsewhere to calculate brine concentrations, which equals [% NaCl / % (Miller, 2008; Ravishankar and Juneja, 2000; Anonymous, NaCl + %H2O] × 100 (Cerveny, 1980). Brine concentration, 2005; Sanchez-Castillo´ et al., 2005). It is not surprising that also known as water-phase salt (WPS), along with aw,isakey sodium intake is high given these multiple functions. In a measurement for assessing microbial stability of intermediate seven day study of 62 U.S. adults it was estimated that moisture foods like meats made by drying, fermenting, and/or sodium added to foods during processing contributes 77% smoking (Ingham et al., 2004a), salted smoked fish (Cornu of total intake compared to 6.2% and 5.1% contributed by et al., 2006), and cheeses (Perez´ Elortondo et al., 1999). the use of salt at the table and during cooking, respectively (Mattes and Donnelly, 1991). While NaCl generally occurs at higher levels than most other sodium-containing ingredi- ANTIMICROBIAL ACTIVITY OF NACL IN FOODS ents, it is certainly not the sole contributor of sodium to the diet. Typical sodium-containing molecules used in foods with Table 2 lists examples of foods for which the addition of NaCl preservative properties against microorganisms are listed in Ta- does and does not contribute to the overall microbiological sta- ble 1. While NaCl contributes the most sodium, the combined bility of the product under normal conditions of storage in the

Downloaded By: [[email protected]] At: 20:44 17 March 2010 contribution from other molecules often used in perserving uncompromised, final, marketed form. Many of these classifica- the same formulation must be noted. Some non-preservative, tions would be altered if the food items were to become exposed Na+ -containing molecules commonly used in foods include to conditions considered abusive, such as through elevation of sodium metasilicate, the leavening agents (sodium bicarbon- temperature, loss of package integrity leading to post-processing ate, sodium aluminum sulfate, and sodium acid pyrophosphate), contamination, or loss of barrier to moisture. For instance, most sodium caseinate, and monosodium glutamate (MSG), to name a of the baked products listed in the left column would be essen- few. tially microbiologically inert unless they became damp, leading Analysis of food and beverage products for total sodium is to an increase of aw sufficient for microbial growth. Similarly, required practice for developing the nutritional panels on prod- frozen foods could become highly sensitive microbiologically if uct labels. Sodium and NaCl analyses are also made at various allowed to thaw, and NaCl levels would become a very important points during product development and scale-up and as part factor at that point. The need to understand freezing implica- of ongoing product quality and safety assessments. NaCl and tions on pathogens has already been pointed out (Archer, 2004), the moisture contents of foods have long been important in the and reduction of NaCl in frozen foods should be included in assessment of microbiological stability, but water activity (aw) such future research. Designations of antimicrobial efficacy of serves as a better general indicator of microbial stability than NaCl in these foods are based on bacteria, yeast, and mold. moisture content (Sperber, 1983). The term aw is defined as Viruses that may inadvertently contaminate foods are generally the vapor pressure of a food divided by the vapor pressure of not impacted by the levels of NaCl seen in foods and beverage pure water, or the equivalent relative humidity / 100. The aw products. of foods is greatly influenced by the presence of NaCl (Chirife Aside from flavor enhancement, it is clear that NaCl plays and del Pilar Buera, 1996). Sodium chloride levels are also used a critical role controlling microbial growth, particularly in 212 P. J. TAORMINA

Table 2 Summary of impact of NaCl addition on microbiological stability of some food products

Foods Not Microbiologically Preserved by Added NaCla Foods for which Added NaCl Contributes to Microbiological Stabilityb

Baked breads Ready-to-eat, refrigerated •Pre-packaged bread and rolls •Deli meats, hot dogs and sausages, roasts, and hams •Pitta, focaccia, tortillas •Prepared salads and spreads Dry snack products •Soft cheese: cottage, white (cream) •Savory snacks, crackers, chips, popcorn, etc. •Hard cheese: Cheddar, Jack, aged Prepared foods (boxed) •Pickles, olives •Spice and cheeses packets in rice meals, macaroni and cheese packages •Butters Cereals Ready-to-cook, refrigerated Beverages (shelf stable or refrigerated) •, fresh sausages, meat patties, moisture enhanced beef, pork, and poultry cuts Flavorings •Dough, par-baked bread •Spice packets Read-to-eat, ambient Frozen foods •Baked pastries with filling •Raw (ready to cook) meat, produce, prepared foods, etc. •Pies, cakes •Precooked (ready to heat and eat) pot pies, pizza toppings Ready-to-eat, shelf stable •Dry and semi-dry sausages, dry cured ham, pre-cooked bacon, smoked fish •Processed cheese foods and spreads •Pre-cooked bacon •Canned foods (soups, broths, chilies, sauces, beans, vegetables) •Pre-cooked rice pouches •Oil and salt preserved delicacies (olives, anchovies, •Salad dressings, ketchup, mayonnaise, other condiments

a When stored according to manufacturer recommendations in final packaged form. Does not account for microbial preservation properties during food preparation, handling, and storage. b Foods capable of supporting growth of spoilage and/or pathogenic microorganisms.

refrigerated ready-to-eat (RTE) foods. Also, many shelf-stable MECHANISMS OF ACTION OF NaCl AGAINST RTE foods are classified as such primarily due to NaCl and MICROORGANISMS moisture content. NaCl provides flavor and acts as a functional agent in baked goods (Miller, 2008) and as an osmoregulant in Various terms have been used to describe degrees of mi- sports beverages (Merson et al., 2008), but does not contribute crobial tolerance or resistance to NaCl, including “obligate to the microbiological stability of such products. Sodium re- ,” “salt tolerant,” “salt resistant,” and “facultative duction initiatives targeting NaCl in foods in the left column halophile” (Jensen, 1944). The term, “halotoerant” might be of Table 2 would not greatly alter the ultimate microbiological considered synonymous with “salt tolerant” and both terms are food safety or quality outcomes. interchangeable with “facultative halophile.” Examples of food-

Downloaded By: [[email protected]] At: 20:44 17 March 2010 As stated above, a caveat to the microbiological stability borne bacterial pathogens that are salt tolerant, salt resistant, classification is that they apply under the conditions of rec- and halophilic are L. monocytogenes, Staphylococcus aureus, ommended storage and use and do not account for the con- and Vibrio parahaemolyticus, respectively. Fungi are more apt ditions to which foods could be exposed after processing and than bacteria to thrive and survive in low aw foods. Examples prior to consumption. These classifications also do not apply of salt tolerant fungi include Torula, Hemispora, Oospora, and in instances where food products are mishandled, abused, or Sporendonema. Salt tolerant and halophilic microorganisms are otherwise altered from their intended state. It should be noted also referred to as xerotolerant or xerophilic, but these terms are that food handling is a major contributing factor to foodborne used more often in reference to low aw conditions created by outbreaks, and that in many instances temperature abuse has high levels of . Salt-tolerant yeast such as Debaryomyces caused microbial hurdles to be overcome leading to pathogen hansenii, Hansenula anomala, and Candida pseudotropicalis growth and outbreaks (Greig et al., 2007). The microbiological may grow at concentrations of NaCl up to 11% (aw 0.93) (Farkas, stability impact of NaCl content on restaurant foods consumed 2007). Microorganisms that become reversibly adapted to NaCl shortly (<2 hr) after preparation or prepared but not consumed are classified as salt resistant. immediately after preparation are particularly difficult to clas- Early research concluded that the preserving effect of NaCl sify. The effects of heating, cooling, and reheating would not be involves more than dehydrating capacity. Magnesium sulfate known without extensive research on the behavior of foodborne was shown to have greater dehydrating effect on proteins than pathogens and spoilage organisms in these various products sub- NaCl, but was not as bacteriostatic as NaCl against S. aureus jected to simulated conditions at normal and reduced levels of (Rockwell and Ebertz, 1924). This research concluded that the NaCl. factors involved in preservative properties of NaCl include the SALT REDUCTION AND FOOD SAFETY 213

− direct toxicity of Cl , removal of oxygen from the medium, Table 3 Influence of solute on minimum aw for bacterial growth sensitization of the organisms to CO , and interference with the 2 Min. aw for growth in rapid action of proteolytic enzymes. Organism NaCl Glucose* Glycerol

Clostridium perfringens 0.97 0.96 0.95 Clostridium botulinum type E 0.97 - 0.94 Lowering of aw in Foods and Plasmolysis Lactobacillus helveticus 0.963 0.966 0.928 Streptococcus lactis 0.965 0.949 0.924 Pseudomonas fluorescens 0.957 - 0.940 Csonka (1989) thoroughly reviewed osmotic regulation in Vibrio parahaemolyticus 0.948 0.984 0.937

bacteria and described the hyperosmotic shock imposed on cells ∗ by NaCl. Hyperosmotic shock, he concluded, causes shrinkage Glucose not sterilized separately from media; inhibitory nonenzymatic brown- ing products may have been present [adapted from Sperber (1983)]. of the cytoplasmic volume, a process known as plasmolysis. If solutes that create hyperosmotic conditions are excluded from the plasma membrane, plasmolysis is dependent upon the mag- Miller (1992) later found that the minimum aw levels for growth nitude of increase in the osmolarity of the medium but not on of L. monocytogenes occurred at 0.90, 0.92, and 0.97 for glyc- the solute used (Csonka, 1989). Lowering of aw was viewed erol, NaCl, and propylene glycol, respectively. Survival was by some researchers as most likely the primary cause for mi- longest in glycerol and shortest in propylene glycol, with sur- crobial growth inhibition by NaCl (Shelef and Seiter, 1993). vival in NaCl being intermediate. The general solute-independent effect of low aw is lethal to Figure 1 shows the effects of 5 and 10% NaCl on morphology microorganisms (Gutierrez et al.,1995). However, among other of Gram-negative and Gram-positive bacterial cells (Hajmeer solutes present in the water-phase of foods, NaCl appears to con- et al., 2006). Extra coarse grade NaCl, such as would be found trol the growth of bacteria to the greatest degree. As shown in in , seemed to have a milder effect compared to fine grade Table 3, the minimum aw for the growth of various bacteria with respect to cell damage, and 24 h cells were more affected is higher when NaCl, compared to other humectants, is used. than 12 h cells. Visual evidence of the plasmolysis theory was in Downloaded By: [[email protected]] At: 20:44 17 March 2010

Figure 1 Transmission electron micrographs (28,500x) of 24-h cultures of E. coli O157:H7 (top) and S. aureus (bottom) in BHI broth supplemented with NaCl at 0%, 5%, and 10% subset f, g, and h, respectively - Reprinted from Hajmeer et al. (2006) with permission from Elsevier. 214 P. J. TAORMINA

lutes accumulate to high intracellular concentrations without impeding core and can balance the osmotic poten- tial of the surrounding medium, enabling the cell to maintain turgor pressure (Welsh, 2000). Although a conserved response in microorganisms, compatible solute uptake may have differ- ent limits of utility for different microorganisms depending on the degree of halotoerance. For instance, the production of the compatible solute tyramine by Carnobacterium divergens,a common meat spoilage bacterium, was inhibited by 10% NaCl (Masson et al., 1997). Other adaptations to growth in high-NaCl environments include changes to the composition of lipid mem- branes and alterations in global gene expressions (Galinski and Truper, 1994).

Figure 2 Minimum water activity for growth of S. aureus at near optimum Effects of the Chloride Ion temperature as influenced by solute. PEG is polyethylene glycol - from Chirife (1994) with permission from Elsevier. Toxicity of halogens to biological systems is a well known paradigm, but definitive effects of the Cl− itself on foodborne agreement with research that confirmed plasmolysis in L. mono- microorganisms remain somewhat unclear. Forty-four different cytogenes when morphological changes were observed due to Gram-negative and Gram-positive bacteria were tested for a growth in media supplemented with NaCl (Zaika and Fanelli, chloride dependence or chloride stimulation of growth (Roeßler 2003). et al., 2003). None required chloride for growth at their optimal growth (salt) conditions. However, in hyperosmotic media con- taining elevated concentrations of Na+, 11 bacteria (Aeromonas Interference with Substrate Utilization hydrophila, Bacillus megaterium, Bacillus subtilis, Corynebac- terium glutamicum, Escherichia coli, P. denitrificans, Proteus A sudden onset of plasmolysis causes inhibition of nutrient mirabilis, Proteus vulgaris, S. aureus, Thermus thermophilus, uptake and deoxyribonucleic acid (DNA) replication and trig- and V. fischeri) exhibited strict chloride dependence for growth gers an increase in the (ATP) levels of or were significantly stimulated by chloride. It was concluded cells, which could lead to inhibition of macromolecular biosyn- that chloride is essential for growth at high salt concentrations − thesis (Csonka, 1989). Phosphohexose isomerase, isocitrate de- in these various species. Others have observed that Cl contain- hydrogenase, and aldolase enzymes appear to be inhibited when ing minerals slightly enhanced sporulation in C. sporogenes,but microorganisms are in the presence of between 3 and 7% NaCl. not as much as CaCO2 (Mah et al., 2008), which may be cause A progressive decrease in glucose utilization and loss of intracel- for some concern regarding use of CaCl2 for NaCl replacement. −

Downloaded By: [[email protected]] At: 20:44 17 March 2010 lular ATP over a 90 minute period concomitant with increasing Observations of Cl toxicity in bacteria are expanded upon in concentrations of NaCl was observed in C. sporogenes (Woods, more applied research (reviewed below), in which some suc- 1982). The rate of respiration and uptake of α-aminoisobutyrate cess is demonstrated with controlling microorganisms in food by Paracoccus denitrificans decreased with progressively more systems with salts containing sodium replacement cations and − NaCl (Erecinska and Deutsch, 1985). Research on the effects of Cl . NaCl on S. aureus revealed that a number of cellular processes were inhibited by its presence (Smith et al., 1987). NaCl inhib- ited staphylococcal enterotoxin A synthesis, glucose utilization, Broth Studies with NaCl and other Factors and respiratory activity with a number of substrates. The break- down of o-nitrophenyl-ß-galactoside (ONPG) by lactose-grown A higher ratio of NaCl to water accounts for the preservative S. aureus was inhibited by NaCl other solutes, indicating that effect of NaCl in meats as compared to liquid culture media the inhibitory effect generally occurs due to nonspecific solutes. (Jensen, 1944). Nonetheless, liquid culture microbiological me- Generally, it was concluded that NaCl and perhaps other solutes dia, or broth, can be excellent for screening large numbers of inhibit the transport of substrates into cells of the particular variables for antagonistic, additive, or synergistic interactions strain of S. aureus. with NaCl. The interactions of pH (5.0, 6.0, and 7.0), tempera- When bacteria are subjected to osmotic stress, a conserved ture (19, 28, and 37◦C), and atmosphere (aerobic versus anaero- response is uptaking potassium ions or accumulating or syn- bic) with NaCl (0, 1, 2, 3, 4, and 5%) on the growth of Salmonella thesizing compatible solutes, such as glycine betaine, proline, Typhimurium ATCC14028 in defined glucose-mineral salts cul- glutamine, ectoine, η-acetylornithine, and trehalose (Galinski ture medium were evaluated (Thayer et al., 1987). Response and Truper,1994; Gutierrez et al., 1995). These compatible so- surface methodology was used to develop equations describing SALT REDUCTION AND FOOD SAFETY 215

the response of the pathogen to environmental changes. The such mechanisms allow the pathogen to adapt to NaCl in foods maximum growth of Salmonella Typhimurium was predicted to and processing environments. For example, cheese isolates of occur at an NaCl concentration of 0.5%, a temperature of 19◦C, L. monocytogenes exhibited higher growth rates than laboratory and an initial pH of 7.0 under aerobic growth conditions. The stocks when in the presence of NaCl (Ribeiro et al., 2006). relative amounts of aerobic growth at 19◦C, pH 7.0, and NaCl concentrations of 0, 0.5, 1, 2, 3, 4, and 5% were predicted to be 99.2, 100.0, 98.8, 90.2, 73.5, 48.6, and 15.6%, respectively. NaCl AGAINST MICROORGANISMS Anaerobic conditions repressed the amount of growth relative IN FOODS to growth under aerobic conditions, and the effects of NaCl and pH were additive at low NaCl concentrations. Interestingly, Jensen (1944) reviewed the preservative properties of NaCl anaerobiosis provided protection against the effects of higher in meats prior to full acceptance of sodium nitrite, and stated levels of NaCl (Thayer et al., 1987). The growth of L. monocy- that when >3.5% NaCl is used in curing whole meat pieces and togenes and L. innocua in media near the range of aw tolerance comminuted meats, the growth of most anaerobes is suppressed. as affected by humectant was thoroughly investigated (Nolan The noted exceptions were for certain strains of nonpathogenic, et al., 1992). The minimum aw for growth of L. monocytogenes in sporogenous anaerobes that can germinate and multiply when media adjusted with NaCl was between 0.924 and 0.921, while given heat treatments much greater than that necessary to destroy slightly higher for L. innocua at between 0.929 and 0.924. When C. botulinum. This statement has seemingly been verified many the medium was adjusted with sucrose, minimal aw for growth times since, including recently when a concentration of 3% of L. monocytogenes was between 0.925 and 0.920, while it NaCl completely inhibited growth of C. perfringens in cooked was again slightly higher for L. innocua at between 0.928 and beef and cured ham during exponentially declining temperatures 0.925. It takes roughly 4 times (w/w) as much sucrose as NaCl from54.4to8.5◦C in 21 h (Zaika, 2003). to adjust the aw to this range. It was concluded that among the Control of food product aw, particularly by addition of NaCl, foodborne bacterial pathogens, L. monocytogenes appears to be is of considerable utility for controlling C. botulinum (Johnson, resistant to deleterious osmotic conditions, and is exceeded in 2007). The formulated use of NaCl appears to have significant this regard only by S. aureus (Nolan et al., 1992). impact on the growth of C. botulinum in refrigerated processed A closer look at the response of L. monocytogenes to NaCl foods of extended shelf life. The growth from heated and un- stress is warranted given the pathogen’s ability to grow at refrig- heated spores of nonproteolytic C. botulinum type B at 10 and eration temperatures in salt-containing foods and it’s virulence 30◦C in broth supplemented with sodium chloride was studied relative to other foodborne pathogens. The genes involved in (Stringer and Peck, 1997). At 1.5 or 3.0% NaCl, time to tur- NaCl resistance by L. monocytogenes have been described (Gar- bidity from unheated spores was 1 to 2 weeks at 10◦C, while dan et al., 2003a). To tolerate osmotic stress L. monocytogenes the time to turbidity was delayed in the presence of 4.0% NaCl, undergoes changes in gene expression leading to an increased developing after 3 or 4 weeks. Also noted were visual differ- synthesis of about twelve salt shock proteins (Duche et al., ences in growth of C. botulinum in tubes of media as affected by 2002a). Eleven proteins were identified as capable of helping concentration of NaCl with turbidity and pellet formation being cells acclimate to osmotic stress including GbuA, which func- reduced by 3.0 and 4.0% NaCl. Spores that were heated to 75◦C tions as an osmoprotectant transporter for glycine betaine. The Downloaded By: [[email protected]] At: 20:44 17 March 2010 for up to 4 min were not less likely to grow in broth with 3.0% general stress protein Ctc was induced by salt stress (Duche NaCl at 10◦C compared to lower levels, but did increase the time et al., 2002a; Duche et al., 2002b), and was found to allow to turbidity. The effect of sodium chloride concentration (3, 4, resistance in the absence of osmoprotectants such as glycine be- 5, 6, 8, 10, and 12%) and storage temperatures (4, 10, 15, and taine and carnitine (Gardan et al., 2003b). The rel gene, which 30◦C) on toxin production by C. botulinum isolated from tropi- encodes for guanosine tetra- and pentaphosphate synthesis and cal fish was studied in anaerobic cooked meat medium (Lalitha hydrolysis protein, was shown to be involved in osmotolerance and Gopakumar, 2007). The combined effect of NaCl (3 or 5%), in L. monocytogenes (Okada et al., 2008). Further it was found low pH (5.5) and low temperature (15◦C) on toxin production that the rpoN gene was activated under high osmotic condi- by C. botulinum was also examined. An increase in lag phase tions achieved using NaCl (Okada et al., 2008). It is likely that was noticed by increasing the NaCl concentration. At 30◦C, spores of C. botulinum type E were able to grow and produce ◦ Table 4 Heat resistance (75 to 90 C), expressed as D-values in min and toxin at up to 3% NaCl (aw = 0.976), whereas for types C and ◦ Z-values in C for nonproteolytic C. botulinum type B in turkey slurry D the limiting salt concentration was 4–5% (aw = 0.97–0.974) (adapted from (Juneja and Eblen, 1995)) and for types A and B it was 8% (aw = 0.952). By lowering Temp (◦C) the storage temperature, an increase in lag phase and time to Heating Z-values toxicity was noticed for type E at 3% NaCl and for types A, C, Menstruum 75 80 85 90 and D at 5% NaCl level. The probability of growth and toxin Turkey + 1% NaCl 42.1 17.1 7.8 1.1 10.08 production at 5% NaCl decreased as the pH and storage tem- Turkey + 2% NaCl 25.7 15.1 5.5 0.6 8.82 perature was decreased. Two percent NaCl (equivalent to a + w Turkey 3% NaCl 17.7 13.1 3.2 0.5 8.47 0.988) was found in many foods to have relatively little effect 216 P. J. TAORMINA

on the times to turbidity during growth from spores of nonpro- Also, a more recent investigation of the survival of pathogens teolytic C. botulinum (Whiting and Oriente, 1997). Although in butters and fat spreads revealed that Salmonella declined in nonproteolytic C. botulinum was able to multiply and sporu- unsalted butter, but grew in a similar salted butter with slightly late in media containing 3% NaCl, emerged cells had difficulty higher pH (Holliday et al., 2003). Growth was attributed to elongating into normal rod-shaped cells in media with 3% NaCl the very low levels of NaCl providing a stimulatory, rather (Webb et al., 2007). The addition of 2% NaCl to growth media than inhibitory, effect. Salmonella and E. coli O157:H7 in significantly reduced the probability of growth from nonprote- water-in-oil emulsions retained higher viability at 4.4◦C and olytic C. botulinum spores and significantly increased the lag grew in whipped salted butter but not in whipped unsalted butter times from individual spores, although these mechanisms were or salted light butter stored at 21◦C. These studies indicate a not elucidated (Webb et al., 2007). The concentration of NaCl degree of complexity with low moisture, high fat systems in necessary to prevent the growth of nonproteolytic C. botulinum regard to the stimulatory versus inhibitory effects of NaCl. under otherwise optimal conditions is considered to be 5.0% Beverages contribute a very minute quantity of sodium to (w/v) (Lund and Peck, 2000). the human diet relative to most foods. The presence of sodium Pasteurized process cheese spreads are matrices where the in beverages is primarily attributable to the use of NaCl as part amount of NaCl in water phase (brine concentration) is of ut- of an electrolytic balance system in sports beverages, sodium most importance. The brine concentration values for inhibiting polyphosphates as preservative enhancers, sodium benzoate and growth of group I and group II C. botulinum are 10 and 5%, calcium di-sodium EDTA as a preservative, and flavor sys- respectively (Hauschild, 1989). Tanaka et al. (1986) found that tems in non-caloric beverages. Response surface modeling made C. botulinum types A and B could not form toxin in processed clear that decreasing the pH of the beverage would permit less cheese when the aw was at or below 0.944, but did when aw was potassium sorbate and/or sodium benzoate while achieving the above 0.957. They concluded that the brine concentrations had same probability of yeast growth (Battey et al., 2002). Con- to be below 6.5% (3.75% NaCl in whole if moisture content versely, increasing preservative levels provides microbial sta- is 54%) for inoculated cheeses to produce toxic samples. Fur- bility at increased pH levels. Potassium benzoate is used al- ther, they reported that high moisture processed cheeses could ternatively to sodium benzoate for successful preservation in be produced safely if NaCl and disodium phosphate levels were reduced-calorie beverages mainly because it offsets the amount both high enough. Glycerol, organic polymers, ions such as of sodium per serving contributed by acidulants and sweeteners potassium, and other food components can bind free water and with the sodium cation. The effects of NaCl versus sucrose con- reduce aw, but the inhibition of C. botulinum is relatively poor centrations on the growth responses of various spoilage yeasts at on a weight/percent basis compared to NaCl (Johnson, 2007). pH 2, 3, 5, and 7 was investigated (Praphailong and Fleet, 1997). E. coli O157:H7 was able to grow in broth supplemented At pH near that of typical acidified soft drinks, the amount of with NaCl at 6.5%, while death occurred when cells were sus- sucrose necessary to inhibit yeast growth was roughly 4 times pended in 8.5% NaCl media (Glass et al., 1992). However, greater than the amount of NaCl necessary for inhibition. How- growth did not occur during fermentation and drying of ever, for several yeasts including Zygosaccharomyces bailii, Z. with an initial NaCl level of 3.5%. The combined effects of rouxii, Pichia anomala, and P. membranefaciens, the maximum salt, monosodium glutamate (MSG), and pH on cold storage NaCl concentration allowing growth at pH 7 was lower than at survival and subsequent acid tolerance of E. coli O157:H7 were acidic pH levels. Downloaded By: [[email protected]] At: 20:44 17 March 2010 determined (Campbell et al., 2004). Cold storage survival was evaluated in tryptic soy broth (TSB) with combinations of pH (7.2, 5.0, or 4.0), MSG (0, 0.5, 1%) and NaCl (0, 2, 4%). The NaCl and Food Fermentations impact of NaCl on cold storage survival was greater at pH 4.0 and 7.0 compared to pH 5.0. MSG did not enhance cold stor- Fermentation processes largely rely on NaCl and pH to inhibit age survival. Another Gram-negative enteric pathogen, Shigella undesirable spoilage microorganisms and pathogens while per- flexneri, was able to grow in media at pH 6 in the presence of mitting growth of a desirable native microflora or starter culture. ≤6% NaCl at 19 and 37◦C and in the presence of ≤7% NaCl at A thorough review of food fermentations is outside the scope 28◦C (Zaika, 2002). of this article, but it should be noted that NaCl is an integral Margarine has been described as a relatively inert product component of safe, quality fermentation processes for meats microbiologically in part due to the up to 2% NaCl that may be and fish (Ricke et al., 2007), vegetables (Breidt et al., 2007), added (Delamarre and Batt, 1999). Levels of NaCl in the water and cheese (Psoni et al., 2003). Cucumber fermentation, for in- phase of such products are higher than levels by the total weight stance, is completely inhibitory to undesirable microorganisms of the product, and migration of NaCl into the water phase at pH 3, but at higher pH levels NaCl must be >2% to enable a would enhance osmotic stress to cells. A bactericidal effect successful fermentation (Kim and Breidt, 2007). In combination of salt on “coli bacteria” in cultured and sweet cream butter with pH, NaCl also inhibits the formation of biogenic amines incubated at refrigeration temperatures was noted by Jensen et by bacteria that are undesirable to fermentation processes of al. (1983). However, L. monocytogenes is capable of growing at cheese (Gardini et al., 2001) and anchovies (Hernandez-Herrero 4◦C and 13◦C in butter containing 1.2% salt (Olsen et al., 1988). et al., 1999). SALT REDUCTION AND FOOD SAFETY 217

Others elucidated parameters of favorable fermentation of S. aureus was the same at each NaCl level, and L. monocyto- olives by Lc. mesenteroides, L. brevis, L. plantarum, and L. genes survived 30 days at aw 0.85. While inhibitory and lethal pentosus including optimal and detrimental NaCl levels (Tassou combinations of NaCl and temperature were defined for Y. ente- et al., 2002). At 25◦C and 18◦C in brines containing 4% and rocolitica and S. aureus, L. monocytogenes was shown to grow 6% NaCl, the growth of lactic acid bacteria was favored, as at 12◦C in 9% NaCl without significant injury and survived in indicated by the high free acidity levels and low pH values in 20% NaCl for 30 days at −12◦ (Miller et al., 1997). the brines. However, 8% NaCl in brine affected the growth of Dry salt application to animal-derived products appears par- lactic acid bacteria and enhanced the activity of fermentative ticularly lethal to bacterial, parasitic, and viral pathogens. Salt- yeasts, producing a final product with lower free acidity and cured hams are preserved from bacterial pathogen growth during higher pH value. At ambient temperature, the counts of lactic the curing and drying process largely due to NaCl (Reynolds acid bacteria followed the fluctuation of temperature regardless et al., 2001). NaCl alone did not destroy T. spiralis in dry- of NaCl concentration, while yeasts did not seem to be affected. cured hams through a curing process of 40 days, except in The best conditions for fermentation were shown to be at 25◦C surface muscles when the brine content approached 8% (Zim- and 6% NaCl, enabling development of free acidity of 142 mM mermann, 1971). However, 5% NaCl, 10% moisture, and 8.5% (1.28% w/v) lactic acid and a pH value of 3.8. After 5 months brine concentration was noted as the range of non-viability of all of , olives fermented at 25◦C were judged by panelists as parasites. The process of dry natural sausage casings for being debittered and ready to eat with no off-odor development. 30 days at temperatures over 4◦C sufficiently reduces infectivity Reduction of NaCl in vegetable fermentations has been at- of zoonotic viruses that cause foot-and-mouth disease (Wijnker tempted by several researchers. Using too much NaCl or CaCl2 et al., 2007) and classical swine fever (Wijnker et al., 2008). (8%) in olive brine permitted yeast growth while inhibiting lac- Relatively high NaCl conditions in brined shrimp impacted tic acid bacteria, but concentrations of 4 and 6% permitted spoilage microflora, but inclusion of sodium benzoate was good lactic acid fermentation of olives (Tassou et al., 2007). necessary for controlling the growth of L. monocytogenes Interestingly, CaCl2 in brines at 4% provided an added bene- (Mejlholm et al., 2008). There appeared to be an interaction fit of making olive flesh stronger and stiffer. Still others have between WPS and temperature in controlling growth of L. mono- found that the addition of Lc. mesenteroides to a sauerkraut cytogenes on chum salmon roe and caviar, with 3◦C sufficiently fermentation enabled equal texture a flavor quality using 50% retarding growth regardless of NaCl level but growth occurring less sodium chloride than normally added to cabbage (Johan- at 7◦C also regardless of NaCl level (Shin and Rasco, 2007). ningsmeier et al., 2007). The use of NaCl to select for lactic Growth probabilities of L. monocytogenes on cooked salmon acid bacteria at the onset of cucumber (Cucumis sativus)fer- were affected more profoundly by NaCl and storage tempera- mentation may be eliminated by using cover liquid containing ture than by phenol content contributed by smoke application 300 ppm of added sodium metabisulfite (calculated as SO2), (Hwang, 2009). L. monocytogenes has been reported to grow in 20 mM , and HCl to give an equilibrated pH of a 6% NaCl brine solution (Hudson,1992) and in meat peptone 3.5 (McFeeters,1998). More data on NaCl and food fermenta- media containing 8% NaCl (Vasseur et al., 1999). The presence tions are reviewed in a subsequent section on Na+ replacement of relatively high levels of NaCl also played an important role in foods. in preventing the formation of biogenic amines by halophilic bacteria within the first day of drying of sardines (Sardinella Downloaded By: [[email protected]] At: 20:44 17 March 2010 gibbosa) (Lakshmanan et al., 2002). High NaCl Conditions

Drying and salting processes represent the advent of food Antimicrobial Synergies with other Food Ingredients preservation. Such processes are still widely used today for tradi- tional, specialty, and novelty foods, and it is under these circum- The synergistic effects of lactate salts and NaCl were well stances that halophilic or halotolerant pathogens and spoilage reviewed (Shelef, 1994). In conjunction with NaCl, sodium or organisms are also exposed to high-NaCl conditions in food sys- potassium lactates have been shown to inhibit lactic acid bac- tems and environments. Although somewhat arbitrary, for the teria, L. monocytogenes, and various clostridial pathogens and purposes of this review, “high” or “extreme” salt generally will spoilage bacteria. Psychrotrophic clostridia and other anaerobic be considered >5% (w/v) NaCl. sporeformers are inhibited in cooked turkey breast by combina- Death rates of E. coli, Salmonella Typhimurium, L. mono- tions of NaCl, sodium lactate, and sodium diacetate (Meyer et cytogenes, S. aureus, C. perfringens, and E. coli O157:H7 as al., 2003). Growth inhbition of various food spoilage microor- affected by NaCl levels (16.36, 23.38, 30.39, and 36.23 % w/v) ganisms and pathogens can be achieved with lower molar con- of brine solutions at 20◦C used for preservation of natural sheep centrations of sodium lacate than NaCl (Houtsma et al.,1996). casings were studied (Wijnker et al., 2006). The death rates were ThegrowthofL. sakei and Lc. mesenteroides was reportedly generally higher for Gram-negative bacteria than for Gram- controlled and the shelf-life was extended in cooked meat formu- positives, but no clear reduction in survival of C. perfringens lations with potassium lactate and sodium diacetate having up to in relation to NaCl was observed. Also, the rate of decline of a 40% reduction in the NaCl content (Devlieghere et al., 2009). 218 P. J. TAORMINA

ThegrowthrateofL. monocytogenes in RTE meats formulated Condon, 2002). When cells were challenged in tryptic soy with potassium lactate, sodium diacetate, NaCl (0.8 to 3.6%), broth (TSB) supplemented with lactic, acetic, or formic acids to and sodium nitrite has been modeled (Seman et al., 2002). RTE achieve pH 4.2, the survival rates of cells up to 135 min at 37◦C meat products used in the study were wieners, smoked-cooked was greater when the medium contained 4% (w/v) additional ham, light bologna, and cotto . Levels of potassium lac- NaCl compared to non-supplemented TSB. In TSB at pH 4.2, tate had highly significant effects on growth rate constants, as 99.99% of log phase E. coli O157:H45 cells died within 2.25 h. did sodium diacetate level and finished product moisture, but However, separate work showed that the presence of NaCl pro- interestingly, not NaCl. Others suggested a complex interaction moted the growth of E. coli O157:H7, especially under stress- between aw and product moisture in meat products containing ful conditions of low pH (Jordan and Davies, 2001). Another lactate (Shelef and Yang,1991). One possible explanation why study found that during fermentation of the NaCl did not significantly affect growth rates of L. monocyto- destruction of E. coli O157:H7 increased significantly as the pH ◦ genes in RTE meats could be that aw lowering effect of sodium decreased from 4.7 to 4.3 in the product heated from 37.7 Cto lactate may have muddled the true effect of non-plasmolysis 46.1◦C in 5.5 h regardless of NaCl concentration (Chikthimmah associated NaCl stress. In any case, the authors concluded that et al., 2001). Further, when 0 or 2.5% NaCl was used, there were finished product moisture and NaCl levels are required knowl- no differences in reductions of the pathogen. However, at the 5% edge for robust calculations with their model (Seman et al., NaCl level, lactic acid bacteria were inhibited and the degree of 2002). A follow up study investigated and modeled the growth inactivation of E. coli O157:H7 was reduced. It is likely that the / no growth boundary of L. monocytogenes at 4◦C using ob- rate of fermentation by lactic acid bacteria and lowering of pH served and predicted values in various cured and uncured meat was impeded by NaCl, lending opportunity of better survival products as affected by similar levels of NaCl, sodium diacetate, of E. coli O157:H7. These studies demonstrated that controlled , and finished product moisture (Legan et al., fermentations can be successfully carried out with reduced NaCl 2004). With growth identified as a 1-log increase in L. monocy- levels, but any changes in NaCl levels should be validated using togenes, the model predicted well for cured and uncured meats, challenge studies. but the authors suggested additional validation of uncured prod- Sodium phosphates have demonstrable synergy with NaCl ucts with low NaCl and high moisture. Their findings, that the in food systems. Approval of the addition of sodium and potas- increase in NaCl and decrease in moisture leading to reduced sium phosphates in processed meats in the 1980s in the U.S. aw reduces the growth rate and ultimately prevents the growth was based, in part, upon the fact that they may compensate of L. monocytogenes, were in agreement with others (Wijtzes for possible loss of functionality when NaCl levels are re- et al.,1993). Concentrations of 2 or 3% sodium- or potassium- duced (Terrell et al., 1983). Various phosphates were shown lactate in combination with 2% NaCl in cooked beef with 55% to inhibit growth of enteropathogenic E. coli in broth cultures moisture was inhibitory to L. monocytogenes (Chen and Shelef, supplemented also with NaCl and sodium nitrite (Hughes and 1992). Others have studied the relationship of a lower range of McDermott, 1989). Inhibition increased with concentration of NaCl (0.5 to 2.5% w/v), sodium lactate, and sodium diacetate sodium chloride/nitrite and with apparent interaction with lower in broth system with the goal of vetting the influence of aerobic temperatures and pH values. Formulation of an uncured turkey and anaerobic atmospheres (Skandamis et al., 2007). The model breast product with sodium pyrophosphate and relatively low was developed based on broth data, and fitted observations from NaCl (1.4%) as well as organic salts led to delays in C. botulinum Downloaded By: [[email protected]] At: 20:44 17 March 2010 published literature well. In the presence of 2.5% NaCl, the neurotoxin formation compared to controls (Miller et al., 1993). minimum inhibitory concentrations for sodium diacetate were Growth of C. sporogenes spores in a meat emulsion containing lower than those obtained with 0.5% NaCl, and this effect was curing agents flavorings and spice with 0.5% sodium acid py- more pronounced under anaerobic conditions. As in all studies rophosphate (SAPP) and 2.5% NaCl (4.1% brine) was slower on synergies between organic salts, sodium nitrite, and NaCl than that in emulsion with SAPP and 1.3% NaCl (2.3% brine) as inhibitors of L. monocytogenes growth in RTE meats, the (Madril and Sofos, 1986). This study concluded that SAPP could efficacy of these preservation systems are diminished at ≥10◦C. improve the antimicrobial properties of lower NaCl comminuted However, synergistic sub–lethal activity of organic salts and meat products. NaCl against L. monocytogenes may not be entirely good. The Other and food formulations may facilitate growth of L. monocytogenes in the presence of NaCl or combi- efficacy of NaCl against microorganisms. Particularly, smoke natory levels of organic salts and NaCl was shown to enhance and drying, in consort with NaCl, control pathogens. For in- the invasion of Caco-2 tissues (Garner et al., 2006). This led the stance, liquid smoke combined with NaCl inhibited C. bo- authors to hypothesize that relatively high pH and the presence tulinum in smoked fish (Eklund et al., 1982). Initial NaCl con- of NaCl in RTE turkey product formulations might enhance centrations of 1.6% w/w (WPS = 2.9%) appeared to work virulence of L. monocytogenes on such products. However, ex- together with phenolics from smoke to inhibit C. perfringens posure of cells to 2.2% NaCl also sensitized them to synthetic growth and toxin formation by S. aureus in bacon during pro- gastric fluid. cessing and cooling from 48.9 to 4.4◦Cin15h(Taormina It was discovered that NaCl could decrease the sensitiv- and Bartholomew, 2005). Air-dried fresh pork sausage ity of E. coli O157:H45 cells to organic acids (Casey and supplemented with 3.64% (w/w) NaCl limited growth of SALT REDUCTION AND FOOD SAFETY 219

coliforms during drying at 21◦C and 60% relative humidity Bidlas and Lambert (2008) modeled the replacement of for 10 days, and as with the observations in bacon, S. aureus NaCl with KCl on time to growth of Aeromonas hydrophila, enterotoxin production but not growth was inhibited during this Cronobacter (formerly Enterobacter) sakazakii, S. flexneri, Y. process (Bang et al., 2008). enterocolitica, and three strains of S. aureus. A cultural method Functional food ingredients can also impact behavior of food- was used to assess growth and no growth conditions for each borne pathogens. Incorporation of delta-gluconolactone as a pathogen in the presence of varying concentrations of the two delayed acidulant reduced the pH of cheeses to 5.26, which humectants. It was concluded that in combination, KCl is a direct contributed to the inhibition of C. botulinum (Karahadian et 1:1 molar replacement for the antimicrobial effect of common al.,1985). All potassium emulsifiers used in the study allowed salt and in foods where salt is used to help preserve the product, toxin production suggesting that sodium and potassium ions are partial or complete replacement by KCl is possible. Challenge not equivalent in affecting inhibition of C. botulinum. Shelf- study data was used to construct an Anti-yersinial index (AI) stable fish sausage with 3.2% NaCl was formulated to aw of to represent the comparative inhibitory properties of chloride 0.97–0.92 with egg white solids and combinations of egg white salts against Y. enterocolitica in pork (Raccach and Henningsen, solids, non-fat dry milk, propylene glycol, and soy protein 1997). The index reflected that CaCl2 was most efficient against isolate (Nieto, 1989). Spores of a putrefactive anaerobic bac- serotype O:3 while the higher concentrations of KCl (1.8 and terium germinated at aw of 0.924, but growth did not occur 2.2% w/w Cl¯ ) were most efficient against serotype O:8. below aw 0.950. It was concluded that macromolecular food The antimicrobial properties of NaCl in foods may not be binders studied could be viable alternatives to high levels of solely due to Cl−, as has been proposed by some (Shelef salt. However, it should be noted that allergenicity of some and Seiter, 1993). When ionic strength equivalents of KCl and functional ingredients would preclude wide appeal as NaCl MgCl2 were compared with NaCl at 2.50 and 1.25% against Mi- replacements. crococcus, Moraxella, and Lactobacillus inoculated into ground pork, there were no significant differences between ions after ten days of storage at 5◦C (Terrell et al.,1983). However, the highest Ion Replacement and Ionic Strength Comparisons reduction of the aerobic mesophilic microflora of pork sausage was caused by CaCl2 followed by NaCl and then KCl. An- Cation replacement is the principal approach for reducing other study measured impact of complete substitution of 3.0% sodium intake in food formulations and for table salt usage, al- NaCl with KCl (3.8%) or CaCl2 (1.9%), while maintaining ionic though a survey of commercially available table salt replacement strength at 0.51, as well as CaCl2 at 2.8% to compare a higher products revealed high sodium levels in some (Ahern and Ka- ionic strength of 0.75 (Raccach and Planck, 1985). The effects ley, 1989). Non-microbial quality attributes due to replacement of salts and mixtures of salts at different molar ratios on hetero- of sodium by removal of NaCl has been studied in a variety fermentative lactic acid bacteria Pediococcus pentosaceus and of food systems including ion salted cod (Martinez-Alvarez L. plantarum in meat were indirectly measured by determining et al., 2005), frankfurters (Pappa et al., 2000), and cheese change in pH. At ionic strength equivalent of 0.51, KCl was the (Sihufe et al., 2006). Studies on the microbiological impact most inhibitory single salt to the fermentative activity of both of ion replacement are reviewed below in detail. organisms. The mixture NaCl:KCl (1:2) was most inhibitory to The salts NaCl, KCl, MgCl2, and CaCl2 or their combi- P. pentosaceus, while L. plantarum was most sensitive to the Downloaded By: [[email protected]] At: 20:44 17 March 2010 nations in pH—and aw—equalized broth and meat emulsions mixture NaCl:KCl (1:1). This study demonstrates that cation at were challenged with Brocothrix thermatospacta, Serratia liq- least influences the fermentative metabolism of these bacteria. uefaciens, and L. plantarum, and the pathogens B. cereus, Further investigations were made into whether Na+ or Salmonella, and Y. enterocolitica (Nielsen and Zeuthen,1987). Cl− ions were separately responsible for the death of E. coli In broth, pure salts CaCl2 and MgCl2 were more suppressive O157:H45 by challenging cells at pH 4.2 in TSB with similar to B. thermatospacta, L. plantarum, Salmonella Enteritidis, and aw of 0.972 to 0.982 (Casey and Condon, 2002). The decimal Salmonella Typhimurium than were NaCl or KCl singly, but reduction time for E. coli O157:H45 cells was 136 min in the this effect was less pronounced in the pork/veal meat emulsion. presence of 4% NaCl (aw 0.972), but 38.3 min in the presence of In broth, combinations of NaCl/CaCl2 and NaCl/MgCl2 were 5.1% KCl (aw 0.973), and 44.04 min in the presence of 21.6% generally more suppressive than NaCl or KCl alone, but these fructose (aw 0.974). This work was prompted by investigations effects were not as pronounced as in meat emulsion. Mixed salts of the survival of E. coli O157 in fermented meat systems (Casey NaCl/KCl/MgCl2 were not more inhibitive of Salmonella Ty- and Condon, 2000). phimurium growth than NaCl. Generally, CaCl2 was more sup- Dry and semi-dry meat products are traditionally preserved pressive than other single salts in meat emulsion. Inhibition of by the addition of NaCl and the reliance on inoculated or na- B. cereus and Y. enterocolitica was seen in meat emulsions with tive populations of lactic acid bacteria to ferment the available NaCl/MgCl2 and NaCl/CaCl2 but not NaCl/KCl combinations. carbohydrate thereby lowering the pH. The survival of lactic These researchers reported equal efficacy of KCl compared to acid bacteria and native Micrococcaceae during fermentation of NaCl in controlling these organisms in a bologna-style sausages reduced-sodium Spanish dry sausages ( de Pamplona) at the same aw. was not significantly different than the full sodium control 220 P. J. TAORMINA

product (Gimeno et al.,1999). The normal sausage formulation cess as evidenced by lowering of cabbage pH and growth of contained 2.6% NaCl, while the experimental formulation was lactic acid bacteria. Further, the final sauerkraut juice with 0.5% comprised of 1.0% NaCl, 0.55% KCl, and 0.74% CaCl2. These mineral salt was deemed to have the best by a trained findings were in agreement with others who also found partial panel. A recent study reported the individual effects of NaCl, + Na replacement in fermented sausages could result in sim- KCl, CaCl2, and MgCl2 against spoilage microorganisms as- ilar Enterobacteriaceae and lactobacilli levels during ripening sociated with table olives (Bautista-Gallego et al., 2008). All compared to normal formulations (Ibanez et al.,1995). the chloride-containing salts were significantly antimicrobial to Separately, it was reported that partial substitution of NaCl Saccharomyces cerevisiae and L. pentosus. While CaCl2 was by KCl, K-lactate and glycine had little effect on the microbi- similar in antimicrobial efficacy to NaCl, KCl and MgCl2 were ological stability of fermented sausages (Gelabert et al., 2003). less inhibitory. However, flavor and/or textural defects were detected by sensory analysis with substitution levels of 40% by KCl, 30% with K- NaCl and Survival of Microorganisms during Processing lactate, and 20% with glycine. The partial substitution (above 40%) of NaCl with different mixtures of KCl/glycine and K- The impact of NaCl on thermal resistance of microorganisms lactate/glycine showed important flavor and textural defects appears to be dependant upon a number of factors likely similar which did not permit an increase in the level of substitution to those known to influence heat resistance at physiological compared to those obtained with the individual components NaCl levels. What is not obvious is how these factors interact Research in microbiological broth media found that low to with NaCl to alter heat resistance. Table 5 demonstrates the medium NaCl concentrations (2.5–4.5% w/v) provided a pro- variability in conclusions reached on the impact of NaCl on tective effect against inhibition of L. monocytogenes by nisin susceptibility of various bacterial pathogens to heat. (Boziaris and Nychas, 2006). Further broth studies were under- Early work on NaCl and heat resistance found that 0.5 to 1% + taken with the intent to investigate the effects of Na replace- NaCl markedly increased the thermal resistance of spores of C. ment and nisin presence on L. monocytogenes in fermented botulinum, but that effect was not seen at 2% (Esty, 1922). At sausages (Boziaris et al., 2007). At pH 4.5 no growth was ob- between 2 and 8% NaCl little or no effect on heat resistance served while in the presence of nisin and/or 1 M salts of both was seen. The thermal death times were decreased above 8% NaCl or KCl, L. monocytogenes Scott A was inactivated. Equal- and up to 20% NaCl. A number of studies on the effect of so- molar concentrations of NaCl or KCl at similar aw exerted sim- lutes on heat resistance have had inconsistent results, but added ilar effects against L. monocytogenes in terms of the lag phase sucrose was generally more protective to vegetative microor- duration, growth, or the death rate. The growth boundaries of L. ganisms during heating than equal percentage concentrations ◦ monocytogenes Scott A at 5 C were also estimated by growth/no of NaCl (Corry, 1975). NaCl appeared to have a protective ef- growth turbidity data and modeled by logistic polynomial re- fect on thermal inactivation of bacterial spores in pea liquor gression. The concordance of logistic models, were 99.6 and when added at concentrations of 1 to 2.5%, while 4% NaCl 99.8% for NaCl and KCl, respectively, and growth interfaces slightly enhanced thermal destruction (Viljoen, 1926). NaCl ap- derived by both NaCl and KCl models were almost identical. peared to exert a protective effect towards micrococci when Therefore, it was concluded that NaCl can be replaced by KCl exposed to heat, but alkaline solutions of NaCl markedly reduce without risking the microbiological safety of the product.

Downloaded By: [[email protected]] At: 20:44 17 March 2010 thermal death times of spores (Jensen, 1944). When B. cereus + The potential for Na replacement in the salting process for strains were exposed to increasing concentrations of NaCl for dry-cured hams was studied by Blesa et al. (2008). Hams were 30 min and the thermotolerance was assessed at 50◦C, both salted at 2% of weight using the traditional NaCl, and two exper- strains showed enhanced thermotolerance after pre-exposure to imental formulations containing 50% NaCl and KCl, and 55% non-lethal salt stress conditions in the exponential phase (den NaCl, 25% KCl, 15% CaCl2, and 5% MgCl2. It was concluded Besten et al., 2006). However, this effect was less pronounced that hams using either reduced-sodium salt mixture, especially for the stationary phase cells. the calcium and magnesium, needed more time to reach similar Survival of Salmonella typhimurium (ATCC 13311) heated aw values than hams salted with 100% NaCl. Mesophilic mi- and recovered in media with 0, 1, 2, 3, 4, or 5% (w/w) added croorganisms, salt-tolerant flora were generally the same at days 20 and 50. By day 50, lactic acid bacteria counts were higher Table 5 Effect of added NaCl on observed heat resistance of foodborne on hams salted with 100% NaCl than on other hams. S. aureus bacteria counts were higher on hams salted with mixtures compared to Effect of Added NaCl normal, but remained below 105 CFU/g at day 80. Organism on Heat Resistance Ref. Vegetable fermentation processes have also been investigated + Escherichia coli Increased (Calhoun and Frazier,1966) for potential Na replacement. A mineral salt blend contain- Staphylococcus aureus Increased ing 28% KCl and 57% NaCl was used at 0.5% (0.3% NaCl) Pseudomonas fluorescense Decreased and compared with the use of 0.5 and 1.2% NaCl in a large- Listeria monocytogenes Increased (Juneja and Eblen,1999) scale sauerkraut fermentation process (Viander et al., 2003). The Salmonella (heat sensitive) Increased (Baird-Parker et al.,1970) mineral blend seemed to allow a very similar fermentation pro- Salmonella (heat resistant) Decreased SALT REDUCTION AND FOOD SAFETY 221

NaCl was investigated (Manas et al., 2001). NaCl had a protec- by only 0.4 log after treatment for 10 min at 400 MPa (Morales tive effect in the heating medium and an inhibitory effect in the et al., 2006). On the other hand, in a 60:40 mixture of ripe Mahon recovery medium. The results showed an interaction between cheese:distilled water with aw 0.976 value, the reduction under NaCl concentration in both media on D58◦C values. Lower con- the same conditions was 3.9 log. Galactose also had a protec- centration in the heating media led to a greater effect of the tive effect on cells exposed to high-pressure processing. Others NaCl concentration in the recovery media. When the NaCl con- found that glucose, NaCl, and ethanol rendered B. stearother- centration was the same in both media, the protective effect mophilus spores more resistant to high pressure (Furukawa and exerted in the heating media dominated over its inhibitory ef- Hayakawa, 2000). fect in the recovery media. Elsewhere, a protective effect of low The effect of NaCl on virus inactivation by high pressure aw systems adjusted with glucose/fructose on Salmonella Ty- processing has also been researched, most likely due to the com- phimurium dt104 was reported, but varying effects were seen mon practice of high pressure treating shellfish and the presence with other solutes such as NaCl (Mattick et al., 2001). In a of virus in harvesting . NaCl (6%) provided a protective thorough study of the heat resistance of Salmonella serovars in effect against high pressure inactivaiton for both hepatitis A ground beef, it was concluded that increasing levels of sodium virus and feline calicivirus, a norovirus surrogate (Kingsley and pyrophosphate significantly increased heat resistance (Juneja et Chen, 2008; Kingsley and Chen, 2009). When feline calicivirus al., 2003). Further, increasing NaCl (up to 4.5%) increased the was exposed to both NaCl and sucrose, an additive effect on heat resistance for lower temperatures studied (<63.5◦C), but the barotolerance was reported (Kingsley and Chen, 2008). for higher temperatures and large lethalities, NaCl levels did not significantly affect heat resistance. The authors also found that sodium lactate did not seem to affect heat resistance of Can We Predict the Microbiological Impact of 50% Sodium Salmonella as much as the other factors (Juneja et al., 2003). Reduction in Foods? Csonka maintains that NaCl has a protective effect against heat for Salmonella Typhimurium (2009); however, D-values of S. In short, predictions of the microbial impact of salt reduction flexneri, another member of the Enterobacteriacea family, were can be accomplished using existing published data, but only for not greatly affected by NaCl (Zaika, 2002). general assessments of sodium reductions in foods. One helpful As with the impact of the cation species on the growth exercise would be to correlate typical salt level in foods at differ- of foodborne microorganisms, the impact of cation on heat- ent periods with typical shelf-life expectancies and foodborne resistance remains unclear. It may be that Cl− and not just Na+ illness data. Salt intake declined in many salt-using communi- is responsible for altering heat resistance. Whereas increasing ties between 1982 and 1988 with declines in the U.S. from 10.6 the NaCl concentration protected L. monocytogenes against the to 7.7 g NaCl/day and in the U.K. from 11.5 to 9 g NaCl/day lethal effect of heat, high SPP concentrations increased heat (Sanchez-Castillo´ et al., 2005). Assuming other factors could sensitivity (Juneja and Eblen, 1999). When spores of C. sporo- be controlled, this may prove useful towards assessing whether genes were generated in media containing CaCO2 at pH 5.0, further reductions are safe from a microbiological standpoint. the heat resistance was slightly but not significantly higher at As outlined above, the impact of formulated levels of NaCl in temperatures ranging from 113 to 121◦C than when sporulated foods and food systems on growth and inactivation of pathogens in the presence of CaCl2 (Mah et al., 2008). and spoilage organisms has been the focus or a component of Downloaded By: [[email protected]] At: 20:44 17 March 2010 The presence of NaCl can impact inactivation of microor- much research. The research clearly shows that the efficacy of ganisms by high-pressure processing. Bacterial barotolerance NaCl against growth or survival of microorganisms in food sys- appears to be related to intracellular accumulation of compati- tems is subject to many interactions with intrinsic and extrinsic ble solutes as a response to the osmotic stress (Molina-Hoppner factors. As such, reduction or replacement of NaCl lends itself et al., 2004). Lactococcus lactis treated with pressures ranging to microbial modeling, which can account for many significant from 200 to 600 MPa was protected if suspended in buffer factors and their interactions simultaneously. Several published containing 4 M NaCl and to a lesser extent 0.5 M sucrose models incorporating NaCl as a key factor are available for (Molina-Hoppner et al., 2004). Another lactic acid bacterium, B. cereus (Sutherland et al.,1996; den Besten et al., 2006), C. L. sanfranciscensis, exhibited barotolerance to 300 MPa for 30 botulinum (Fernandez et al., 2001; Graham et al.,1996), E. coli min when preincubated in NaCl (Scheyhing et al., 2004). Su- O157:H7 (Sutherland et al., 1995; Buchanan et al., 1993a), L. crose but not NaCl prevented the irreversible inactivation of L. curvatus (Wijtzes et al., 2001), L. monocytogenes (McClure lactis enzymes involved in pH homeostasis and multi-drug resis- et al., 1991; Tienungoon et al., 2000; Wijtzes et al., 1993; tance transport activity (Molina-Hoppner et al., 2004). Overall, Cheroutre-Vialette and Lebert, 2000; Cheroutre-Vialette and it was evident that disaccharides protect microorganisms against Lebert, 2002; Buchanan and Phillips, 1990), Salmonella Ty- pressure-induced inactivation of vital cellular components, and phimurium (Thayer et al., 1987), S. flexneri (Zaika et al., 1994; baroprotection with ionic solutes requires higher concentrations Zaika et al., 1998), S. aurues (Sutherland et al., 1994; Buchanan of the osmolytes than of disaccharides. In dehydrated Hispanico- et al., 1993b), and Y.enterocolitica (Bhaduri et al., 1994; Bhaduri type cheese (58.20% dry matter) in which 5% NaCl was added et al., 1995). In addition to the impact of NaCl on the growth of to achieve aw 0.904, L. monocytogenes counts were lowered foodborne pathogens, D-values of B. stearothermophilus spores 222 P. J. TAORMINA

as affected by heating medium pH, NaCl concentrations, and NaCl in human diets. However, short-term unintended conse- temperature can be modeled accurately (Tejadillos et al., 2003), quences related to the impact on microorganisms have not been as can thermal inactivation of L. monocytogenes as affected by fully explored. Regulatory action on reducing NaCl in foods pH, NaCl, and sodium pyrophosphate (Juneja and Eblen,1999). without first obtaining thorough predictions on the behavior of Primary, secondary, and tertiary models have been devel- foodborne pathogens and spoilage organisms in the food sup- oped for major foodborne bacterial pathogens in a variety of ply could lead to significant disruptions to international food food systems (Marks, 2008). The PMP 7.0 (USDA, 2003) is an commerce at best. These disruptions would be caused by mi- example of a robust and user-friendly tertiary model, and it has crobial survival, growth, and spoilage when and where pre- been used to predict the behavior of pathogens in processes as viously unexpected using processing and distribution param- affected by intrinsic and extrinsic factors of foods (Ingham et eters developed for the current amounts of sodium in foods. al., 2004b). Growth Predictor, Perfringens Predictor, and DMFit At worst, a rush to significantly reduce NaCl without research (IFR) are other examples of useful tertiary models (IFR, 2006). and careful planning could lead to significant increase in ex- The Com database draws from a vast collection of literature posure of humans to foodborne pathogens. Various research to provide useful information on predicted growth as affected groups throughout the world have capabilities for thorough by product temperature, pH, and percent NaCl (Baranyi and and detailed modeling and prediction of behavior of foodborne Tamplin, 004). While the range of NaCl is quite large (0 to pathogens in food systems as affected by intrinsic and extrin- 70%) in the Com database, the increments are in even numbers sic parameters and could address these issues with adequate restricting the flexibility in modeling within the typical range funding. Private industry resources and expertise should also be of 0.5 to 4% NaCl occurring in food products. The Optiform R included in systematic risk assessments of reduced sodium food Listeria Control Model 2007 (PURAC, the Netherlands) is a products. 7th generation tertiary model specifically designed to predict Specific research needs to be conducted on the microbio- thegrowthrateofL. monocytogenes in ready-to-eat meats as logical implications of sodium removal/reduction in prepared affected by levels of sodium or potassium lactate, sodium di- and served foods as data appear to be lacking in this area. acetate, NaCl, and moisture. Preceding iterations of the model Replacement of NaCl with antimicrobial herbs and spices, al- were developed through cooperation with industry scientists though proposed as a possible solution to sodium reduction in at Kraft Foods (Oscar Mayer), and the latest version incorpo- foods, has also not been thoroughly researched. The myriad rates their research as well as nearly 30 peer-reviewed articles sources of sodium in foods other than NaCl should be consid- and internal PURAC data. The latest version also enables pre- ered towards the goal of overall sodium reduction. Consideration diction of growth based on levels of other proprietary growth should be made to reduce sodium by targeting food ingredients inhibitors. The model enables users to enter in NaCl ranges with lesser degrees of microbiological inhibition than NaCl. of 0 to 4.3% (w/w) of finished product. However, model pre- Although cation replacement appears to be the most popular dictions in general should be interpreted with caution (Black approach to reducing sodium in processed foods, wholesale re- and Davidson, 2008), and should not replace individual product placement of NaCl by KCl or other salts is not warranted based assessments especially with substantial formulation changes. on the studies reviewed here. Successful and unsuccessful out- For instance, a tertiary model with a 95% confidence inter- comes using salt blends appear to be dependent on microbial val prediction may neglect the error in original experimental species and intrinsic properties of foods, particularly pH. Given Downloaded By: [[email protected]] At: 20:44 17 March 2010 data and the error in the primary model fit, which can actu- the apparent contradictory results in different food systems, par- ally be greater than the secondary model uncertainty (Marks, tial ion replacement using KCl or CaCl2 should be evaluated on 2008). a product by product basis with challenge studies. Generally, food products should be evaluated by challenge studies on a case by case basis until appropriate models can be constructed CONCLUSION and validated.

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Wijtzes, T., McClure, P. J., Zwietering, M. H., and Roberts, T. A. (1993). Zaika, L. L., Phillips, J. G., Fanelli, J. S., and Scullen, O. J. (1998). Revised Modelling bacterial growth of Listeria monocytogenes as a function of water model for aerobic growth of Shigella flexneri to extend the validity of pre- activity, pH and temperature. Int J Food Microbiol. 18:139–149. dictions at temperatures between 10 and 19 degrees C. Int J Food Microbiol. Wijtzes, T., Rombouts, F. M., Kant-Muermans, M. L., van Riet, K., and Zwieter- 41:9–19. ing, M. H. (2001). Development and validation of a combined temperature, Zaika, L. L. (2002). The effect of NaCl on survival of Shigella flexneri in broth water activity, pH model for bacterial growth rate of Lactobacillus curvatus. as affected by temperature and pH. J Food Prot. 65:774–779. Int J Food Microbiol. 63:57–64. Zaika, L. L. (2003). Influence of NaCl content and cooling rate on outgrowth Woods, L. F. J., and J. M. Wood (1982). The mechanism of the inhibition of Clostridium perfringens spores in cooked ham and beef. J Food Prot. of Clostridium sporogenes by sodium chloride. British Food Manufacturing 66:1599–1603. Inudstries Research Assoc., Research Report. Zaika, L. L., and Fanelli, J. S. (2003). Growth kinetics and cell morphology Zaika, L. L., Moulden, E., Weimer, L., Phillips, J. G., and Buchanan, R. L. of Listeria monocytogenes Scott A as affected by temperature, NaCl, and (1994). Model for the combined effects of temperature, initial pH, sodium EDTA. J Food Prot. 66:1208–1215. chloride and sodium nitrite concentrations on anaerobic growth of Shigella Zimmermann, W. J. (1971). Salt cure and drying-time and temperature effects flexneri. Int J Food Microbiol. 23:345–358. on viability of Trichinella spiralis in dry-cured hams. J Food Sci. 36:58–62. Downloaded By: [[email protected]] At: 20:44 17 March 2010 Sodium Reduction and Its Effect on Food Safety, Food Quality, and Human Health Marjorie Ellin Doyle and Kathleen A. Glass

ABSTRACT: Sodium is an essential nutrient with important functions in regulating extracellular fluid volume and the active transport of molecules across cell membranes. However, recent estimates from NHANES III (Third Na- tional Health and Nutrition Examination Survey) data show that over 95% of men and over 75% of women exceed the recommended daily tolerable upper intake of sodium. Since these high levels of dietary sodium are associated with a high prevalence of hypertension, prehypertension and, possibly, other adverse effects on health, many national and international health organizations recommend that sodium intake be significantly decreased. Traditionally, salt (sodium chloride) has been used as a food preservative that kills or limits the growth of foodborne pathogens and spoilage organisms by decreasing water activity. Salt also performs other important functions in foods by adding flavor and masking bitter , controlling growth of yeast and fermentative bacteria, and promoting binding of proteins and other components in foods to achieve desired textures. Many processed foods contain high levels of salt and several countries have developed national programs for significantly reducing the sodium chloride content in many processed foods and encouraging a decrease in discretionary salt use. This review considers published data on the apparent adverse health effects of excess salt intake as well as the important functions of salt in different foods and possible strategies for reducing sodium levels in processed foods while still producing safe foods that consumers find acceptable.

Introduction Natural sodium levels in foods generally account for only about Traditionally, salt (sodium chloride) has been viewed as a food 10% of dietary intake. Most dietary sodium is ingested in the form preservative that enhances human health by killing or limiting of sodium chloride (table salt). In European and North American growth of foodborne pathogens and spoilage organisms. How- countries, approximately 5% to 10% of intake is due to the discre- ever, in recent decades, with increasing consumption of many tionary addition of salt at the table and during cooking, whereas different processed foods containing high levels of sodium, the processed foods and foods served in restaurants are estimated perception of dietary salt has evolved to a point where it is now to contribute over 75% of dietary sodium (Mattes and Donnelly considered, by some, to be a potential health threat. The Inst. 1991). A recent study in Denmark used lithium-tagged salt to of Medicine of the Natl. Academy of Sciences has established replace normal salt used by 87 people in the home for a 10-d adequate daily intakes (AIs) for sodium and potassium and a tol- period. Analyses of 24-h urine samples revealed that 8.7% (for erable upper intake level (UL) for sodium, based on its effects women) and 10.2% (for men) of salt consumed was added to on blood pressure (Table 1; IOM 2004). Persons with a greater foods by the subjects. Approximately, 90% of sodium chloride risk for hypertension (adults who are Black, over 40 y old, or intake came from sodium naturally present in foods or added to already have hypertension or prehypertension) have been urged processed and manufactured foods (Andersen and others 2009). to consume no more than the AI level of sodium each day (CDCP In Asian countries, salt added in home cooking and at the table 2009). accounts for an estimated 72% to 76% of dietary intake. , miso, salted vegetables, fruits, and fish contribute signifi- cantly to dietary sodium (Brown and others 2009). In addition to obviously salty foods, such as certain snacks, MS20090703 Submitted 7/22/2009, Accepted 10/2/2009. Authors are with sodium content is quite high in many packaged dinners, soups, Food Research Inst., Univ. of Wisconsin–Madison, 1550 Linden Drive, sauces, and processed meats and cheeses. Cured meats, for exam- Madison, WI 53706, U.S.A. Direct inquiries to author Doyle (E-mail: [email protected]). ple, are estimated to contribute 20.5% of the sodium in the Irish diet (Desmond 2007). Although salt levels in breads and cereals

44 COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 C 2010 Institute of Food Technologists R Sodium reduction and its effect on food safety . . .

Table 1 --- Daily sodium and potassium intakes and recommended intakes in the U.S. (IOM 2004). Sodium Sodium chloride Potassium

AI (adequate intake): 19 to 50 y 1.5 g/d (65 mmol) 3.8 g 4.7 g/d (120 mmol) AI:51to70y 1.3g/d(55mmol) 3.3g 4.7g/d(120mmol) AI: > 71 y 1.2 g/d (50 mmol) 3 g 4.7 g/d (120 mmol) UL: tolerable upper intake level 2.3 g/d (95 mmol) 5.8 g Not established Median intake (males) 4.2 g (183 mmol) 10.6 g 2.9 to 3.2 g/d (74 to 82 mmol) Median intake (females) 3.3 g (142 mmol) 8.3 g 2.1 to 2.3 g/d (54 to 59 mmol) are relatively low, people generally consume more of this food North American countries, median daily sodium intakes ranged group and therefore breads and cereals contribute an estimated from 2.3 g (100 mmol) to 4.3 g (187 mmol) (ICRG 1988). More 35% to 50% to sodium intake in some countries (Beer-Borst and than 100 publications documenting sodium intake in adults and others 2009; Brown and others 2009; Thomson 2009). children in countries around the world were recently reviewed, Some foods, for example, 8 oz of some commercial tomato including data from the 1996–1999 INTERMAP study (Brown and soups and 4 oz of some types of pizza, may contain nearly an others 2009). entire day’s adequate intake of sodium. This has led the American Approximately 98% of dietary sodium is absorbed in the in- Public Health Assn. and the American Medical Assn. to call for testine. Excess sodium is excreted mainly by the kidneys and a 50% reduction in sodium in processed and restaurant foods some is lost with perspiration. In healthy adult humans at steady- over a 10-y period. Revocation of the generally recognized as state conditions, urinary sodium excretion roughly equals intake. safe (GRAS) status of salt has also been proposed to make food Sodium is an essential nutrient, the cation mainly responsible processors justify the amount of salt added to foods (Dickinson for regulating extracellular fluid volume and plasma volume. It and Havas 2007). FDA held a hearing on this proposal and on also determines membrane potential of cells and participates in possible changes to labeling regulations in November 2007. the active transport of some molecules across cell membranes. Sodium reduction is also a topic of intense international in- Other cations, including potassium and calcium, interact with terest. WHO (World Health Organization), as part of its Global sodium and influence its physiological effects (Adrogueand´ Strategy on Diet, Physical Activity and Health, organized a forum Madias 2008). and technical meeting in 2006 to review and discuss the link Several hormones and the sympathetic nervous system enable between high salt consumption and health. Various initiatives to healthy humans to adapt to different dietary salt levels and main- reduce population-wide salt intake and the cost and effectiveness tain plasma levels of sodium within an optimal range by altering of these programs were evaluated (WHO 2007). An international the excretion of sodium in sweat and urine in response to changes organization of experts from 80 countries, WASH (World Ac- in dietary sodium intake. However, as people age or develop tion on Salt and Health), was established in 2005 to publicize certain chronic diseases, kidney function may decline thereby adverse effects of sodium chloride on health and to work with affecting homeostatic regulation of electrolytes. As the efficiency governments and industry to reduce salt levels in catered, restau- of excretion of excess sodium diminishes, plasma volume may rant, and processed foods, as well as salt added during cook- increase and stress the cardiovascular system by inducing hyper- ing and at the table (http://www.worldactiononsalt.com/). Sev- tension. Hypertension, in turn, is correlated with higher risk for eral countries, including Japan, Finland, Australia, and the U.K., coronary heart disease, , and end-stage renal disease (He have developed strategies for significantly reducing the sodium and MacGregor 2007). chloride content in many processed foods and encouraging a de- crease in discretionary salt use (Cobcroft and others 2008; He and Hypertension MacGregor 2009). Approximately two-thirds of adults in the U.S. have either hy- It is critical to note that efforts to reduce salt in processed pertension, defined as untreated systolic blood pressure (SBP) > foods must be balanced with the original purpose of salting many 139 mm or diastolic blood pressure (DBP) > 89 mm, or pre- foods—prevention of the growth of pathogenic and spoilage or- hypertension with SBP 120 to 139 mm or DBP 80 to 89 mm. ganisms. Salt- and sodium-containing ingredients also serve other Untreated hypertension is associated with increased incidences functions in foods including producing and maintaining charac- of , heart disease, stroke, and kidney disease. Therefore, teristic textures, controlling yeast growth during breadmaking, there is universal agreement that interventions that reduce or and masking bitter tastes. When salt and sodium levels in foods prevent development of high blood pressure would significantly are reduced, then other preservatives may be needed to ensure improve health (Dickinson and Havas 2007). Age, body mass food safety and flavoring agents, other additives, and different index, activity levels, and dietary sodium and potassium are all processing techniques may be required to preserve quality and known to affect blood pressure. However, some analysts ques- texture of foods. tion the importance of dietary sodium, relative to other factors, as a cause of hypertension in the general population (Hollenberg 2006). Some individuals appear to be “salt-sensitive” and experience a very significant drop in blood pressure when consuming a General low-salt diet, while others are “salt-resistant” and do not see a Humans can survive on diets with a wide range of sodium significant change. A high prevalence of salt sensitivity occurs concentrations. Results from the 1985–1987 INTERSALT study of among persons with hypertension, diabetes, chronic kidney dis- blood pressure and electrolyte excretion in 32 countries indicated ease, and metabolic syndrome as well as among persons over that median urinary excretion of sodium ranged from 0.2 mmol/d 40 and African-Americans (Dickinson and Havas 2007; He and in Yanomamo Indians in Brazil to 242 mmol/d in residents of MacGregor 2007; Chen and others 2009). U.S. Dept. of Agri- Tianjin, China. This corresponds to a range of daily intakes of culture (USDA) estimates that these at-risk individuals constitute approximately 0.0046 g to 5.6 g of sodium. In European and nearly 70% of the adult population in the U.S. (CDCP 2009). Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 45 CRFSFS: Comprehensive Reviews in Food Science and Food Safety

Gender differences in salt sensitivity have also been reported long-term, modest decreases in dietary sodium. A recently pub- with females experiencing greater decreases in blood pressure in lished randomized crossover trial of low and high sodium diets response to dietary sodium reduction (He and others 2009b). Salt (50 and 250 mmol/d for 7 d each) reported significant reductions sensitivity may be related to changes in physiological processes of SBP and DBP of 22.7 and 9.1 mm Hg in patients with resistant during aging, body mass index, or dietary and lifestyle variables hypertension (blood pressure remains elevated despite the use of (Hoffmann and others 2008). 3 antihypertensive medications) (Pimenta and others 2009). Mechanisms by which sodium affects blood pressure and the A meta-analysis of 28 dietary interventions that lasted for at circulatory system are not completely understood. It has been least 1 mo demonstrated that reductions in dietary sodium signif- suggested that, in response to high salt intake, persons with salt- icantly decreased blood pressure in both normotensive and hy- sensitive hypertension do not excrete as much sodium in urine pertensive individuals. A weighted linear regression of the data as salt-resistant individuals. Higher serum sodium levels would indicated a significant dose response between sodium reduction be followed by an expansion of plasma volume, an increase in and blood pressure such that a reduction of 6 g salt/d resulted cardiac output, and a sustained increase in systemic vascular re- in mean decreases of 7 mm Hg in SBC for hypertensive and sistance. This may occur in some people. However, a trial with 4 mm Hg in normotensive subjects (He and MacGregor 2002). A healthy Black adults demonstrated that salt-loading induced sim- randomized double-blind crossover trial of a modest reduction of ilar serum sodium concentrations and similar increases in plasma salt (diets with 9.7 and 6.5 g salt/d) demonstrated that the lower volume and cardiac output in salt-sensitive and salt-resistant in- sodium diet was associated with significant reductions in blood dividuals. However, blood vessels of salt-resistant persons dilated pressure in white, black, and Asian subjects with mildly raised in response to high salt intake and blood pressure did not increase blood pressure in the U.K. A significant decrease in arterial stiff- significantly. This vasodilation did not occur in the salt-sensitive ness, measured by pulse wave velocity, was observed in some subjects (Schmidlin and others 2007). subjects (He and others 2009a). Data from numerous studies indicate that higher intakes of salt Other dietary constituents, including potassium, affect blood or sodium are associated with elevated blood pressure in pop- pressure. The DASH (Dietary Approaches to Stop Hypertension) ulations overall and in many individuals. The INTERSALT study diet, which provides a significant amount of potassium from fruits, found that 4 groups of people in nonindustrialized areas with very vegetables, and low-fat dairy products, has been shown to reduce low sodium intakes had low blood pressure readings that did not blood pressure (IOM 2004; Adrogue´ and Madias 2008). In a study increase with age. Data from over 45 other groups indicated comparing consumption of control “typical American” diets and that urinary sodium excretion was significantly correlated with DASH diets each containing several sodium levels (1.15 to 3.44 g blood pressure and age-related increases in blood pressure. A sodium/d), average SBP was significantly lower on the DASH diet negative association was observed between potassium excretion compared to the control diet at all salt levels. SBP also decreased and blood pressure at most centers (ICRG 1988). The INTERMAP significantly with a decrease in dietary sodium on both the “typi- study of blood pressure, dietary recall data, and urinary sodium cal” diet (–6.7 mm) and the DASH diet (–3 mm). The combination levels for over 4600 adults in the U.S., U.K., Japan, and China of the DASH diet and reduced dietary sodium appeared to have revealed that several dietary variables, including sodium, were an additive effect in reducing SBP. Greater mean reductions in correlated with blood pressure measurements (Brown and others blood pressure were observed in persons with hypertension and 2009). in African-Americans consuming the “typical” diet with the low- People living in nonindustrial societies are, of course, more est levels of sodium than in other subgroups (Sacks and others physically active, seldom overweight, and may differ genetically 2001). in some ways from more industrialized populations. However, Experimental studies with several species of animals, in which several studies of people who migrated from low-salt, isolated dietary intake can be more strictly controlled, documented in- areas to urban centers demonstrated that these people were creases in blood pressure with higher salt intakes (He and not protected by their genetics but developed hypertension as MacGregor 2007). Chimpanzees fed diets with high levels of they adapted to city life, became more sedentary, and increased potassium and high or low levels of sodium had significantly their intake of salt and consumed less dietary potassium (He and lower SBP and DBP on the lower sodium diets (Elliott and others MacGregor 2007). 2007). A review of long-term experiments on salt and hyperten- Following publication of data in the late 1960s showing that sion in animals noted that salt has 2 distinct effects: (1) a rapid Finnish men had a very high rate of coronary heart disease mor- rise in blood pressure in response to increased salt occurring over tality, Finland initiated major efforts to reduce cardiovascular days or weeks and (2) a slow, progressive increase in blood pres- disease and promote health. These included public information sure during a significant portion of the lifetime of normal individ- campaigns and collaborations with the to develop uals. In some species, this long-term increase in blood pressure lower-salt foods. Dietary salt intake among Finnish men declined appeared irreversible and may correspond to the age-related in- from 12 to 13.2 g/d in 1979 to 8.6 to 9.5 g/d in 2002. During crease in blood pressure observed in human populations (van this time, mean SBP in males declined by an average of 8 mm Vliet and Montani 2008). despite an increase in mean body mass index (Laatikainen and others 2006). Other population intervention programs involving Cardiovascular disease (CVD) thousands of people in Japan, China, and Portugal also demon- Hypertension is a recognized risk factor for CVD and is often strated decreases in population blood pressure in response to a associated with other cardiovascular risk factors, such as obesity, reduction in dietary sodium (He and MacGregor 2007). insulin resistance, and elevated blood lipids, in a condition called Numerous treatment trials have been conducted with hyper- the metabolic syndrome. A comparison of 24-h urinary sodium tensive and normotensive individuals examining the effects of excretion, in more than 700 people with and without symptoms increased/reduced dietary sodium on blood pressure. Inconsis- of the metabolic syndrome, found that higher levels of sodium tent results have been reported from studies employing acute excretion were significantly related to elevated blood pressure salt-loading or depletion for a very short term (1 wk or less). and to obesity (Hoffmann and Cubeddu 2009). Higher sodium These results have been cited by those who are skeptical of pro- intakes also impair relaxation of smooth muscles in the endothe- grams to reduce dietary sodium (Taubes 1998). However, these lium of arteries, in response to shear stress of flowing blood. This trials may not reliably predict results of currently recommended is another known risk for cardiovascular disease. Consumption 46 COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Sodium reduction and its effect on food safety . . . of a diet containing 50 mmol or 1.15 g sodium/d (slightly lower Elevated urinary calcium levels are not necessarily directly re- than the recommended intake for adults up to 50 y old) improved lated to bone mineral density or bone turnover. Persons consum- flow-mediated dilation in arteries in a group of overweight/obese ing the currently recommended amount of calcium (1200 mg/d individuals as compared to that observed in persons consuming for women past age 50) may be able to compensate for increased diets containing 150 mmol or 3.46 g sodium/d (approximately calciuria caused by an additional 2.3 g sodium/d. But with a cal- the current median intake in the U.S.). These changes were in- cium intake of 600 mg/d or less, the body most likely will not be dependent of effects on blood pressure (Dickinson and others able to increase calcium absorption enough to compensate for 2009). increased calcium excretion (Heaney 2006). A recent study with Correlations between sodium intake and cardiovascular dis- postmenopausal women found that bone calcium balance was ease and mortality are difficult to establish because this disease negative on low-calcium diets (518 mg/d) regardless of sodium develops over many years and is affected by several dietary vari- intake. On moderate calcium diets (1284 g/d), bone calcium bal- ables as well as lifestyle factors. Reviews have generally con- ance was positive when sodium levels were low (1.54 g/d), but cluded that epidemiological evidence for a positive correlation not when they were high (4.42 g/d) (Teucher and others 2008). between sodium intake and CVD is not strong (Alderman 2006; Other dietary constituents affect sodium and calcium Walker and others 2007). Results from some recently published metabolism. Consumption of the DASH diet, which contains ap- studies illustrate this. proximately 3 times the amount of calcium, magnesium, and r potassium in a “typical” American diet is associated with sig- Data from an 18-mo study on 2275 adults with prehyper- nificantly reduced markers of bone turnover in adults as com- tension found that the urinary sodium-to-potassium ratio, pared to the typical American diet (Lin and others 2003). Fruits rather than urinary sodium or urinary potassium concentra- and vegetables are not only good sources of potassium but also tions alone, was the strongest predictor of cardiovascular dis- are rich in compounds, such as citrate, that generate basic ions r ease events (Cook and others 2009). like bicarbonate during metabolism (Sebastian and others 2002). Analysis of data on a cohort from the Rotterdam Study found Sodium-loading studies demonstrated that sodium bicarbonate that there was no consistent association of urinary sodium, does not induce the same increases in urinary calcium that are potassium, or sodium/potassium ratio with CVD in 387 sub- seen with sodium chloride (Schoppen and others 2008). jects with an incident stroke or myocardial infarction com- A comparison of the net endogenous acid production of dif- pared to 1448 randomly selected subjects (Geleijnse and ferent diets revealed that typical American diets produce a low- r others 2007). grade metabolic acidosis (average of +48 mEq/d), while diets A recent analysis of data from NHANES III found an inverse of preagricultural humans were net base-producing (average of relationship between dietary sodium values, reported by 8699 –88 mEq/d). Cereal grains, the most commonly consumed foods persons, and the 754 deaths from CVD that occurred during an in modern diets, yield net acid when metabolized (Sebastian and average follow-up of 8.7 y. However, in most subgroups, this others 2002). Human clinical studies revealed that an elevated relationship was not statistically significant (Cohen and others intake of sodium chloride also results in low-grade metabolic r 2008). acidosis (Frassetto and others 2007; Frings-Meuthen and others A recent analysis of data from participants in the TOHP I and II 2008). Low-grade metabolic acidosis, caused by diets deficient in studies (Trials of Hypertension Prevention) indicated that risk fruits and vegetables and containing excess sodium chloride, may of a cardiovascular event was 25% less, during 10 to 15 y of cause increased bone resorption and calcium excretion (Morris follow-up, in the intervention groups that had received com- and others 2006). prehensive education and counseling on reduction of dietary sodium. Initially, participants in this study were prehyperten- Other health effects of salt r sive and were aged 30 to 54 y (Cook and others 2007). A follow-up study compared incidence of coronary heart dis- Some studies suggest that high dietary sodium levels are asso- ease and stroke with consumption of a DASH-style diet by ciated with other health issues including gastric cancer, kidney participants in the Nurses’ Health Study. Diet was assessed 7 stones, and severity of asthma. Data supporting these connec- times during 24 y of follow-up. Nurses who consumed diets tions are not definitive, but a high dietary intake of sodium may most similar to the DASH diet (which included lower sodium affect development or severity of some of these conditions (He levels) had a significantly lower risk for stroke and coronary and MacGregor 2009). For example, the increased urinary cal- heart disease (Fung and others 2008). Several components of cium in persons on high-salt diets may contribute to formation of the DASH diet, including lower salt and higher potassium in- calcium oxalate stones (Obligado and Goldfarb 2008). takes, may be responsible for this protective effect. Functions of Sodium Compounds in Foods Bone disease Normally the body absorbs about 27% of dietary calcium but Flavor intestinal absorption of calcium can change in response to subop- Saltiness is one of the basic tastes perceived by humans. New- timal or excess serum calcium levels and the presence of vitamin borns appear indifferent to salt, although they do react to sweet, D and other . Metabolism and intercellular transport of sour, and bitter tastes. Positive responses to salt increase during sodium and calcium are linked and, therefore, high-salt diets may the first 4 to 6 mo of life and have been associated with birth affect calcium retention and bone density. Data from several stud- weight. Lower birth weights are correlated with more positive ies have demonstrated that a higher sodium intake is correlated responses to salt during childhood and with risk for hypertension with greater urinary losses of calcium (Carbone and others 2003; later in life (Stein and others 2006; Beauchamp and Mennella Lin and others 2003; Frings-Meuthen and others 2008). For exam- 2009). ple, a diet containing 11.2 g salt/d significantly increased urinary Sodium and lithium are the only cations with a taste that calcium excretion in postmenopausal women as compared to is primarily salty. Potassium and calcium, have some compo- a diet with 3.9 g salt/d (Teucher and others 2008). Other fac- nent of saltiness to their taste but they have other flavors, some- tors, including age, gender, menopausal status, and other dietary times described as “metallic” or “bitter.” Sodium chloride is the constituents are known to affect the extent of calciuria. saltiest sodium compound. As the size of the anion associated Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 47 CRFSFS: Comprehensive Reviews in Food Science and Food Safety with sodium increases, perceived saltiness decreases. Interac- yeast growth so that dough will increase in volume slowly and tions among minerals with respect to taste are not well under- uniformly producing loaves of bread with good “grain” (Cauvain stood. Rats fed a low-potassium or low-calcium diet, consume 2007; Lynch and others 2009). more sodium chloride. It is well known that many diets in in- Salt also affects color development in baked products by in- dustrialized countries are deficient in calcium and potassium. fluencing Maillard reactions. It has been shown that salt has a However, it is not known whether this deficiency increases the plasticizing effect during heating of cereal products which im- appetite for salt in humans (McCaughey 2007). proves mobility of reactants and enhances Maillard reactions, Sodium compounds, such as sodium chloride and producing a darker colored product (Moreau and others 2009). monosodium glutamate, enhance the flavor of some other in- In cakes and quick (nonyeast) breads, salt does not have such gredients in foods. Salt affects the flavor of cheeses and appears a critical technological function and is added primarily for flavor. to have a greater impact in low-fat products (Johnson and oth- However, sodium carbonate and sodium bicarbonate, used for ers 2009; Saint-Eve and others 2009). Salt also suppresses or leavening in these products, contribute to the total sodium con- masks bitter flavors. It has been estimated that about 25% of the tent. Some published data indicate that salt concentrations are in population are nontasters (insensitive to ordinary levels of bit- the range of 1 to 1.34 g per 100 g in breads and rolls and 0.32 to ter compounds) and about 25% are supertasters (very sensitive 0.52 g/100 g in cakes (Cauvain 2007). to bitter compounds) (Kilcast and den Ridder 2007). Therefore, significantly decreasing the salt in some foods may make them Preservation and microbial safety unpalatable to as many as a fourth of consumers, while an equal Controlling growth of pathogens in foods is essential to number may not even notice the change. public health, particularly for high-risk populations including Sodium chloride levels in different natural cheeses vary from very young children, pregnant women, the elderly, and people 0.7% to 6%. Salt significantly affects growth of starter cultures whose immune systems are weakened by chronic illnesses, im- and activities of lipolytic and proteolytic enzymes that pro- munosuppressive therapy, or chemotherapy. According to the duce important characteristic flavor compounds or bitter com- website of the Centers for Disease Control and Prevention pounds during ripening of cheese (Guinee and O’Kennedy 2007; (http://www.cdc.gov; accessed in 2009), there are an estimated Johnson and others 2009). Growth and metabolic activities of 76 million cases of foodborne illnesses annually in the U.S. Al- cheese starter cultures and yeast and sourdough starters for bread though many cases involve mild to moderate gastrointestinal are stimulated or depressed depending on sodium chloride lev- symptoms, it is estimated that over 300000 people require hos- els. In addition to their other functions in foods, these microbes pitalization and approximately 5000 deaths occur annually from synthesize important flavor and aroma compounds (Man 2007). foodborne illnesses (Mead and others 1999). Microbes are also an important cause of food spoilage. USDA Texture/processing Economic Research Service estimates that billions of pounds of Sodium chloride interacts with other major components in food in the U.S. are lost annually by retailers, foodservice, and foods thereby affecting the texture of foods. For example, salt consumers (Buzby and others 2009). A significant amount of increases hydration of proteins and enhances the binding of pro- this loss is caused by microbes that alter the odor, taste, texture, teins to each other and to fat. These properties stabilize emulsions or appearance of foods causing them to be rejected for human of ground meat mixed with fat and promote development of a consumption. network of gluten proteins in yeast breads. Salt (sodium chloride) and drying have been used for thousands In meat, 1.5% to 2.5% (w/w) added salt enables proteins to of years to decrease water activity (aw) in meat, fish, vegetables, bind more water, thereby increasing tenderness and decreas- eggs, and some fruit, such as olives and dried plums, thereby pre- ing fluid loss in heat-processed products. Actin and myosin in serving these fresh foods for later consumption. Available water meat proteins swell in the presence of salt, binding water and fat is a critical factor affecting microbial growth on and in foods. and allowing formation of heat-stable emulsions of comminuted Fresh foods, process cheese, and low-salt bacon have a high aw meats, such as frankfurters. These myosin proteins bind to each (0.95 to 1), as do highly perishable foods such as fresh meat and other thereby improving the texture of processed meats (Man fish (aw > 0.99) (Christian 2000). Consequently, there is suffi- 2007; Xiong 2007) and also restructured fish products (Pedro cient water to support growth of most bacterial pathogens and and Nunes 2007). spoilage organisms if other conditions do not limit growth. Salt Solubility of proteins and the water content of cheese are also is added to meat and fish, particularly as a deterrent to growth of affected by salt. These, in turn, determine rheology, texture, and C. botulinum (Desmond 2007; Pedro and Nunes 2007). changes that occur during cooking. Low concentrations of NaCl Shelf-stable sauces, processed meats, and cheeses rely, in part, (5% to 6%, w/w, salt-in-moisture) increase the solubilization of on salt for safety and preservation. In addition to sodium chloride, casein or para-casein in natural cheeses. In pasteurized pro- other salts, sugars, proteins, and humectants in foods decrease aw. cess cheeses, emulsifying salts (sodium citrate, orthophosphates, Examples of foods with reduced aw include: hard cheeses, ham, polyphosphates) are added to aid in the hydration of para-casein, and bacon with a water activity of 0.90 to 0.95; jams and heavily emulsification of fats, and stability. Content and composition of salted fish (0.75 to 0.80); and dried fruits (0.60 to 0.75) (Christian emulsifying salts vary in different products, but a level of about 2000; Nummer and Andress 2002). Water lost during process- 1.5% is typically used (Guinee and O’Kennedy 2007; Johnson ing/cooking increases sodium concentrations on a finished prod- and others 2009). uct basis. For example, 100-g samples of fresh raw pork belly, Yeast bread and some other baked goods require some salt to raw cured bacon, and cooked bacon contain, respectively, 0.032 control growth of yeast and develop an extensible gluten net- g, 0.833 g, and 2.3 g sodium (Data from USDA Natl. Nutri- work. Salt helps control hydration of glutenin and gliadin pro- ent Database, http://www.nal.usda.gov/fnic/foodcomp/search/). teins which is critical for the development of enough gluten to Salt also inhibits spoilage microbes while allowing growth of trap small air bubbles in the dough to produce a high-quality lactic acid bacteria in fermentations producing sauerkraut and bread. Optimal salt concentrations stabilize gluten and prevent pickles. stickiness in dough. Too little salt allows excessive growth of yeast On the most basic level, salt preserves food by exerting a dry- resulting in oversized bread with poor texture. Bakers add spe- ing effect, drawing water out of cells of both the food and mi- cific amounts of salt that have been determined to allow sufficient croorganisms through the process of osmosis. Salt concentrations 48 COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Sodium reduction and its effect on food safety . . .

Table 2 --- Approximate minimum water activity values for growth of some foodborne microbes. Microbe Minimum water activity Reference

Campylobacter jejuni 0.98 Doyle and Roman (1982) Clostridium botulinum B 0.94 Ohye and Christian (1967) Clostridium botulinum E 0.97 Ohye and Christian (1967) Escherichia coli 0.95 Marshall and others (1971) Listeria monocytogenes 0.92 Tapia De Daza and others (1991) Pseudomonas fluorescens 0.97 Marshall and others (1971) Salmonella spp. 0.95 Christian (2000) Staphylococcus aureus 0.86 Scott (1953) Aspergillus flavus 0.80 Pitt and Miscamble (1995) Saccharomyces cerevisiae 0.90 Christian (2000) Zygosaccharomyces bailii 0.80 Pitt and Richardson (1973)

30 E. coli 20 Pseudomonas Brochothrix Salmonella 18 S. aureus L. monocytogenes 25 16 C. botulinum 14

20 12

10

15 8

Generation time (h) 6

Generation time (h) 10 4

2

5 0 0.5 1.5 2.5 3.5 4.5 5.5 6.5 7.5 Salt concentration (%)

0 Figure 2 --- Effect of sodium chloride on growth of food 0.5 1.5 2.5 3.5 4.5 5.5 6.5 7.5 8.5 9.5 spoilage bacteria in broth culture, pH 6, 10◦C, as esti- Salt concentration (%) mated by COMBASE (www.combase.cc/).

Figure 1 --- Effect of sodium chloride on growth of ◦ foodborne pathogens in broth culture, pH 6, 10 C, as es- nonproteolytic C. botulinum. Other microbes, including S. au- timated by Pathogen Modeling Program (www.ars.usda. reus and L. monocytogenes and the spoilage bacteria Brochothrix gov/Services/docs.htm?docid=6786) and ComBase and Pseudomonas (Figure 2), are more resistant to salt. In the ab- (www.combase.cc/). sence of salt or other preservatives, these bacteria could multiply under conditions of temperature abuse to spoil foods or cause foodborne illness. required to inhibit microbes vary with species. Campylobacters Microbes can adapt to elevated salt levels in foods. They may are highly sensitive to salt, with 0.5% NaCl being optimal for accumulate potassium, amino acids, or sugars to prevent a large growth (Doyle and Roman 1982). On the other hand, proteolytic influx of sodium and outflow of water from cells. Other strategies C. botulinum tolerate up to 10% NaCl and, when other growth include increased activity of sodium efflux systems, changes in conditions are favorable, S. aureus can grow in the presence of cell morphology and membrane fatty acids (Christian 2000; Lado > 20% NaCl. Minimum water activity levels allowing growth of and Yousef 2007), and production of specific stress proteins that some important foodborne microbes, when other growth condi- enable survival (Cheville and others 1996; Duche´ and others tions are near optimal, are listed in Table 2. At some aw levels, 2002). Microbes can also survive in very high salt concentrations bacteria are capable of growth but not toxin production. For ex- even when they cannot grow. Although Salmonella and E. coli ◦ ample, S. aureus can grow aerobically at 37 Catanaw of 0.86, require an aw of at least 0.95 for growth, both species survived for ◦ but only produces enterotoxin if aw is at least 0.90 (Baird-Parker 8to10dat20 C in natural sheep casings at an aw of 0.85 (Wijnker 1990). and others 2006). The more salt-tolerant Listeria monocytogenes, Figure 1 illustrates the inhibitory effect of salt on growth of which grows at an aw as low as 0.92, remained viable for 259 d ◦ ◦ several foodborne pathogens at 10 C (slight temperature abuse) at 4 C commercial cheese brine (23.8% NaCl, aw approximately in broth culture. While sodium chloride concentrations of 0.5% 0.80) (Larson and others 1999). and 1.5% do not significantly affect any of the pathogens, higher Other properties of foods, such as pH, temperature, oxygen, salt levels significantly increase time required for one generation fat, and other additives, affect the sensitivity of microbes to salt of growth of some pathogens including E. coli, Salmonella,and in specific foods. Table 3 demonstrates some of these effects Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 49 CRFSFS: Comprehensive Reviews in Food Science and Food Safety

Table 3 --- Influence of pH, temperature, and atmosphere on the minimal aw (maximal sodium chloride concentration) permitting growth of selected foodborne pathogens. Pathogen [NaCl] pH Temperature Atmosphere Reference ◦ Clostridium botulinum 3% 6.5 10 C10H2:90 N2 Gibson and others (2000) ◦ (B & E non-proteolytic) 3.5% 6.5 10 C10H2:85 N2:5 CO2 ◦ 0.5% 6 to 6.5 5 C 100% CO2 2.5% 5.5 to 6 10◦C 0.5% 6 5◦C Escherichia coli 6% 5.6 to 6.8 15◦C Air Gibson and Roberts (1986) (10 strains) 4% 5.6 to 6.8 10◦C Listeria monocytogenes 3% 4.5 25◦C Air McClure and others (1989) 10% 5to8 Salmonella spp. 2% 5.6 to 6.8 10◦C Air Gibson and Roberts (1986) (3 serotypes) 4% 5.6 to 6.8 15◦C 6% 6.8 15◦C 6% 5.6 to 6.2 17.5◦C for pathogens grown in laboratory media. At lower tempera- 25 tures, E. coli grows only at low salt concentrations (Gibson and 0.5% NaCl Roberts 1986). Similarly, in more acidic environments, L. mono- 3.0% NaCl cytogenes is less tolerant of salt (McClure and others 1989). Data 4.5% NaCl 20 for salmonellae demonstrate both of these effects. An atmosphere 5.5% NaCl of 100% CO2, compared to other anaerobic atmospheres, lim- its the growth of C. botulinum at higher salt levels (Gibson and Roberts 1986). 15 Large amounts of data on the effects of environmen- tal factors on growth of pathogens and spoilage organ- isms have been published and numerous predictive mod- 10 els have been developed to describe the combined effects of sodium chloride concentrations, acidity, temperature, and Generation time (h) other factors on microbial growth. Programs available on 5 the internet have integrated data from several sources to produce interactive models predicting microbial growth under different conditions. The Pathogen Modeling Program (PMP) (http://www.ars.usda.gov/Services/docs.htm?docid=6786), from 0 USDA, includes models for spoilage organisms and pathogens 0 50 100 120 150 in broth and some foods. ComBase (http://www.combase.cc/) Nitrite (ppm) is a collaborative project among the USDA, Food Standards Agency, and Inst. of Food Research in the U.K., and the Aus- Figure 3 --- Effects of combinations of sodium chloride tralian Food Safety Centre of Excellence. Its modeling toolbox and nitrite on growth of Listeria monocytogenes in broth provides a quantitative method for predicting microbial responses culture, pH 6, 10◦C, as estimated by COMBASE (www. to changes in 3 or more environmental factors. Much of the data combase.cc/). used in these models are derived from growth experiments in defined laboratory media not food. But they do provide estimates of effective concentrations and illustrate important interactions among various factors that can be tested in real foods. Foods are pounds on growth of L. monocytogenes in broth at slight temper- very complex systems and some natural and added constituents ature abuse conditions. In the absence of nitrite, 5.5% NaCl is may have unexpected effects on viability and growth of microbes required to prolong generation time to about 11 h. Combinations (van Boekel 2008). of 120 ppm nitrite plus 0.5% NaCl and of 100 ppm nitrite plus Added salt may be insufficient to completely inhibit growth of 3% NaCl have approximately the same growth inhibitory effect. pathogens, but may depress microbial growth rates and work with In a model system representative of a deli-style turkey with other preservatives, strict refrigeration (below 4◦C), or heat treat- 65% moisture and pH 6, a predictive model suggests that without ment combined with appropriate packaging, to prevent growth sodium salts, L. monocytogenes can grow within 12 d storage at and toxin production. This is multiple hurdle technology to en- 4◦C (OptiForm Listeria Control Model 2007; www.purac.com). In sure safety of foods and extend shelf life. contrast, the addition of 100 ppm sodium nitrite and 2% sodium Other sodium-containing compounds are also used for food chloride (together contributing 393 mg sodium per 50-g serving) preservation. For example, disodium phosphate is a critical com- will delay growth of the pathogen through 24 d, which provides ponent for safety of shelf-stable pasteurized process cheese prod- a significant increase in the margin of safety to the consumer ucts (Tanaka and others 1986) and sodium nitrite is important (Seman and others 2002). for preventing growth and toxin production of C. botulinum in Effective 2003, the USDA-FSIS mandated that processors in- cured meats (Davidson and Taylor 2007). Predictive models can corporate strategies, such as the use of growth inhibitors, to con- estimate effective combinations of sodium chloride and sodium trol L. monocytogenes in ready-to-eat meat and poultry products nitrite on L. monocytogenes and Salmonella (Betts and others (Anonymous 2003). In response to these regulations, many U.S. 2007). Figure 3 illustrates the combined effects of these com- manufacturers add other sodium-based inhibitors such as sodium 50 COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Sodium reduction and its effect on food safety . . .

Table 4 --- Amount of sodium contributed by some common sodium-containing additives as compared to that con- tributed by sodium chloride. Sodium compound Typical use % sodium in compound mg of Na/100 g food

Chloride 1.5% to 2% 39.34% 590 to 790 Benzoate 0.1% 15.95% 16 Diacetate 0.1% to 0.4% 16.18% 16 to 65 Lactate 1.5% to 3% 20.51% 310 to 620 Propionate 0.3% 23.93% 70 Sorbate 0.3% 17.14% 50 Nitrite 0.012% 33.32% 4 Acid pyrophosphate (SAPP) 0.35% 20.72% 100 Tripolyphosphate (STPP) 0.35% 31.24% 160 Pyrophosphate (TSPP) 0.35% 34.57% 170 Hexametaphosphate (SHMP) 0.35% 22.55% 110

sodium content, after sodium chloride. Formulating certain foods 20 0.5% NaCl with reduced amounts of these compounds may have a negative effect on food safety. 2.5% NaCl 3.5% NaCl 15 Strategies in Formulation of Reduced-Sodium Foods 4.5% NaCl General A comprehensive strategy to reduce salt intake to 6 g/d 10 (from around 8.6 g/d) has been undertaken in the U.K. in an effort to reduce rates of hypertension and cardiovas- cular disease. Voluntary salt reduction targets for different

Generation time (h) categories of manufactured foods were first proposed in 5 2006. Information on current target values can be found at the Food Standards Agency web site (http://www.food.gov. uk/multimedia/pdfs/consultation/consultsalttargets.pdf). Target levels were set with an eye on effects related to flavor, tex- 0 ture, and safety of foods and are periodically reconsidered 0 5000 10000 15000 20000 in light of experiences to date with these reformulations. The Lactate (ppm) overall strategy also includes a public education campaign with television commercials and an informative web site Figure 4 --- Effects of combinations of sodium chloride and (http://www.salt.gov.uk/). lactate on growth of Listeria monocytogenes in broth Food manufacturers and processors have reduced salt lev- culture, pH 6, 10◦C, as estimated by COMBASE (www. els in some foods. A comparison of sodium levels in stan- combase.cc/). dard and reduced-salt foods available in the U.S. is presented in Table 5. However, a 2009 survey by WASH (http://www. worldactiononsalt.com/) found large differences in the salt con- tent of foods produced by global companies and sold in different lactate (maximum 4.8% of formulation weight) and sodium di- countries. Kellogg’s cornflakes, for example, contains 1.75, 1.8, acetate (maximum 0.25%), in addition to sodium chloride, to or 2.8 g salt/100 g, depending on whether it is sold in Spain, Eng- deli-style meat and poultry products and frankfurters to inhibit land, or the Middle East, respectively. A KFC Fillet Burger has 3.7 g growth of this pathogen (Anonymous 2000). These compounds salt/100 g in New Zealand and only 2.4 g/100 g in Australia. Such may reduce water activity and otherwise interfere with micro- bial metabolism and transport across cell membranes (Doores 2005). Table 5 --- Sodium levels (mg/100 g) in standard and Combined effects of lactate and sodium chloride on growth of reduced-salt foods (data from http://www.nal.usda.gov/ L. monocytogenes in broth at slight temperature abuse conditions fnic/foodcomp/search/). are illustrated in Figure 4. In the absence of lactate, 4.5% NaCl is required to depress growth to a generation time of 9 to 10 h. Food Standard Reduced sodium Addition of 1% or 2% lactate permits reduced NaCl concentra- Frankfurter 1090 311 tions of 3.5% and 0.5%, respectively. All of these organic acids, Beef bologna 1080 682 1.6% lactate and 0.1% diacetate, 0.3% sorbate, 0.1% benzoate, ◦ Salami, pork, and beef 2010 623 and 0.2% propionate, can suppress growth of Listeria at 4 Cfor Bacon, cooked 2310 1030 12 wk on ham containing 2.2% NaCl and 156 ppm nitrite (Glass Ham, extra lean, roasted 1385 681 and others 2007b). Bread, commercial white 681 27 Since sodium salts of organic acids, sodium nitrite, and sodium Soup, condensed tomato (Campbell’s) 573 427 phosphate compounds are added to foods to prevent micro- Cheese, Swiss 192 14 bial growth and improve texture, sodium reduction strategies Cheese, Parmesan 1602 63 must also consider these sources of added sodium. As noted in Soy sauce 5637 3333 Table 4, sodium lactate is the largest potential contributor to Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 51 CRFSFS: Comprehensive Reviews in Food Science and Food Safety differences indicate that it is possible to reduce salt levels in many compounds that contribute to flavor. These nonsodium com- foods and still produce popular products. pounds constitute nearly 60% of some varieties of sea salt and their use may significantly reduce sodium intake (Kilcast and den Ridder 2007; Pszczola 2007). A mineral salt containing 50% Sodium chloride affects the taste of specific foods by provid- sodium chloride and 44.5% potassium chloride, along with cal- ing the flavor of saltiness, by enhancing or masking other flavors, cium and magnesium carbonates and magnesium sulfate was and by controlling growth of microbes that produce flavorful used in the formulation of several meat products. Although it sig- compounds. Small stepwise reductions, of 5% to 10%, in levels nificantly decreased sodium content, these meats were ranked of sodium chloride in foods are often not even noticed by con- lower than the standard products by a taste panel because of sumers. If this occurs over time in a number of processed foods, differences in odor, taste, and consistency (Schoene and others it may result in significantly decreased sodium intake. Successful 2009). examples include: (1) a 33% reduction in salt levels in cereals in Discovery and formulation of “bitter blockers” to reduce objec- the U.K. during a 7-y period; (2) a 33% sodium reduction in Kraft tionable flavors in salt substitutes and low-salt foods are currently processed cheese; and (3) a reformulation of Heinz products that the focus of much research. Sweeteners, such as sucrose and the resulted in an 11% to 18% decrease in sodium levels (Kilcast intensely sweet protein thaumatin, have been used to interfere and den Ridder 2007). These reductions in salt content may be with the perception of bitter compounds. Dihydroxybenzoic acid not only tolerated but even better liked than the original food and its salts have been reported to effectively counteract metallic formulation. aftertastes without affecting sweetness (McGregor 2007). A re- Enhancing saltiness of foods may be accomplished by physical view on bitter-masking molecules describes recent advances in or chemical means. Sodium chloride interacts with taste receptors the discovery and development of these compounds (Ley 2008). only when it is in solution. Therefore, physical processes that increase the solubility of salt crystals will increase the sensation Texture and other quality characteristics of saltiness for a given amount of salt. For example, finer salt Although sodium chloride performs important technological crystals could be used to coat snack foods to deliver sufficient functions during the production of many meat, fish, dairy, and saltiness with less sodium. Electrostatic coating of chips improves bakery products, some of these foods probably contain more salt adhesion of small salt particles and can give a more even coating than is necessary for high-quality characteristics. Many factors (Buck and Barringer 2007). affect the quality of processed foods, including starter cultures, Many herbs and spices add flavor to foods allowing for the moisture levels, fat content, pH, various additives, and processing reduction of sodium chloride content. Peptides from a variety conditions. Reducing sodium chloride levels may require alter- of hydrolyzed proteins and the sweeteners trehalose and thau- ations in other parameters to ensure that foods retain acceptable matin enhance the salty taste of foods and permit reduction of flavors and textures. sodium chloride levels without significantly altering taste. One Formulation of low-salt meat batters is technologically chal- recommended additive that allows reduction of sodium content lenging because a reduction in sodium chloride levels requires of foods is monosodium glutamate that provides an umami flavor other ionic compounds to replace the water-holding, protein- (Kilcast and den Ridder 2007). Salad dressings, soup, and stir-fried binding, and fat-binding functions of the salt that is eliminated. pork, produced with less salt and added naturally brewed soy Comminuted meat products containing less than 1.5% salt form sauce were judged acceptable by consumers (Kremer and others unstable emulsions with poor texture (Xiong 2007). One pro- 2009). Dried bonito (fish) enhances the saltiness and palatability posed strategy that does not involve addition of other compounds, of steamed egg custard thereby allowing a reduction in sodium is the use of different physical forms of salt. Salt companies, content (Manabe 2008). such as Morton and Cargill, produce fine flake and dendritic Odors of foods also affect perceptions of taste. A recent Euro- salts whose crystals have a larger surface area and dissolve more pean study found that salt-associated odors could enhance per- rapidly. There have been reports that such salts have the potential ception of saltiness. Panelists presented with a series of solutions to improve water and fat binding in some meat batters and emul- containing a standard, small amount of salt rated those with aro- sions at lower salt concentrations. Further research is needed to mas such as bacon, ham, peanuts, and anchovy as saltier than substantiate this claim (Desmond 2007). solutions with no added aroma or those that smelled like toma- Potassium, calcium, and magnesium and several toes. Solutions with a carrot odor were rated as less salty than polyphosphate compounds can be used to stabilize meat emul- the no-aroma solution (Lawrence and others 2009). Certain well- sions in reduced-sodium meats. KCl and NaCl, at equal ionic selected odors may effectively compensate for changes in taste strengths, interact identically with meat proteins, but calcium of low-sodium foods. and magnesium chlorides are not as effective (Gordon and Barbut Currently, there are no compounds that can effectively sub- 1992; Alino˜ and others 2009). Immersion of cod fillets in NaCl or stitute for the flavor of sodium chloride in foods. Lithium com- KCl solutions of equal molar volume had similar effects on water pounds are salty but are toxic in amounts that would be needed uptake and losses of free amino acids but the fillets in KCl had as salt substitutes. Calcium and potassium compounds have some significantly lower drip loss (Larsen and Elvevoll 2008). Potas- salty flavor but they also impart off-flavors, described as metal- sium phosphates can bind water and improve stability as well lic or bitter. Potassium chloride, for example, can replace up as their sodium counterparts, but high levels of potassium com- to about 30% of sodium chloride in many foods. Beyond that pounds may adversely alter taste. Other binding agents, such as concentration, foods become unpalatable (Charlton and others nonmeat proteins (soy, milk), starches from several plant sources, 2007; Park and others 2009). Magnesium sulfate, some ammo- and gums and alginates, increase viscosity in low-salt meat prod- nium compounds, amino acids, and dipeptides also have a salty ucts (Desmond 2007). taste but, again, it is not a “pure” salt taste so that other additives Sodium chloride controls growth of yeast and promotes the are required to mask off-flavors and bitter tastes (Kilcast and den development of gluten structure in bread. Therefore, a reduction Ridder 2007). in salt may permit more rapid yeast growth and adversely affect A wide variety of “sea salt” preparations are now sold as texture. These effects may be mitigated to some extent by de- alternatives to refined salt. Sea salts contain several calcium, creasing the amount of yeast used and by adjusting mixing and potassium, and magnesium compounds and sometimes other other mechanical processes during manufacture (Cauvain 2007). 52 COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Sodium reduction and its effect on food safety . . .

In a series of experiments to evaluate characteristics of wheat inary experiments with L. monocytogenes (Boziaris and others bread formulated with 0.6%, 0.3%, and 0% salt compared to the 2007) and S. aureus (Bidlas and Lambert 2008) in laboratory me- customary level of 1.2%, reduced salt levels did not significantly dia demonstrated that KCl, at the same molar ratio, could directly impact the rheological properties of the dough, baking quality, replace NaCl as an antimicrobial agent. Further challenge studies or sensory attributes. However, omission of salt completely pro- in real foods must be done to confirm that KCl can safely replace duced unpleasant flavors and a significant reduction in structural NaCl. quality of dough and bread (Lynch and others 2009). The U.K. Organic acids are used as chemical preservatives in some foods Food Standards Agency has recommended reducing salt levels in (Doores 2005). Table 4 lists concentrations of those compounds bread to a target of 0.9 g salt/100 g (Cauvain 2007). that are typically used along with the amount of sodium con- KCl has similar effects on yeast growth and rheological proper- tributed by sodium salts of these compounds. Most sodium salts ties of dough as that of NaCl but its use is limited by its metallic of organic acids contribute much less sodium than NaCl at the off-flavor (Cauvain 2007). A brown bread containing 32% less concentrations used. However, sodium lactate is used at relatively sodium and formulated with a combination of KCl, calcium car- high concentrations and can contribute a significant amount of bonate, magnesium chloride, and magnesium sulfate was judged sodium. to have acceptable baking properties, appearance, texture, and Potassium, sodium, and calcium lactates are equally effective flavor (Charlton and others 2007). in controlling growth of bacteria in meat packaged in modified Cheeses, including commercial Cheddar cheeses in the U.S., atmospheres (Devlieghere and others 2001). A combination of R vary in sodium chloride levels and it may be possible to re- potassium lactate and sodium diacetate (Purasal Opto.Form duce salt levels in some cheeses. Reducing sodium chloride in PD 4 from PURAC) in packaged cooked meats maintained sen- cheese presents many challenges as described in a recent re- sory quality and shelf life, while reducing sodium chloride levels view (Johnson and others 2009). Reductions of up to 0.5% salt by 40% (Devlieghere and others 2009). Sorbate, benzoate, pro- in Cheddar cheese and up to 35% in cottage cheese have been pionate, and diacetate inhibit L. monocytogenes in cured and judged acceptable by consumers. Partial substitution of KCl for uncured meat products (Glass and others 2007a, 2007b; Seman NaCl does not adversely affect starter culture activity or texture, and others 2008). With the exception of lactate and diacetate, although there are flavor issues with higher potassium concen- many salts of organic acids are awaiting regulatory approval for trations (Reddy and Marth 1995). Magnesium chloride and cal- use in meats in the U.S. In contrast, sorbates, propionates, and cium chloride do not appear to be good substitutes for NaCl in benzoates are approved in many other food applications and are cheeses because texture becomes crumbly, soft, or greasy. Protein widely used to inhibit yeasts and molds in baked goods, cheeses, enrichment, by addition of ultrafiltered whole milk retentate dur- and fruit products. They also effectively inhibit some impor- ing cheese-making, produces good-quality low-sodium cheeses tant pathogens such as E. coli, Salmonella,andStaphylococcus with a good texture. This may be a result of the higher calcium (Chipley 2005; Stopforth and others 2005). These preservatives and phosphate content in these cheeses (Guinee and O’Kennedy have flavors of their own which limit their use in certain products 2007). or above certain concentrations in other products. Salt levels in pasteurized process cheeses can be reduced by Natural and organic foods are becoming increasingly popu- starting with a reduced-sodium cheese and using some potassium lar and, to support this trend, there is great interest in natural emulsifying salts. Complete elimination of emulsifying salts can antimicrobials. Active components from several plants or essen- reduce sodium levels by 20% to 40%. However, the result is tial oils exhibit antimicrobial activity against molds and bacte- a gummy cheese product with separation of oil and water. A rial pathogens in numerous laboratory experiments (Burt 2004). careful blending of different cheese ingredients and optimization These include thymol, eugenol, and cinnamaldehyde, as well of processing conditions can produce a more stable product. as compounds from onion, garlic, and mustard (Benkeblia 2004; Other ingredients, such as starches and gums, can also be used Nadarajah and others 2005a, 2005b; Raybaudi-Massilia and oth- to maintain an acceptable cheese spread texture (Guinee and ers 2006). However, these compounds are generally not as effec- O’Kennedy 2007). tive in foods where fats or other food components may inactivate Salt is added to a concentration of 2% to 2.25% to cabbage in or sequester these antimicrobials (Gupta and Ravishankar 2005). making sauerkraut to suppress the growth of spoilage bacteria and In addition, many of these compounds have their own strong select for growth of fermentative lactic acid bacteria. Addition flavor profiles and may not be acceptable to consumers. of a starter culture of Leuconostoc mesenteroides to cabbage consistently produced sauerkraut with a firm texture and good flavor with salt concentrations of 0.5% or 1% (Johanningsmeier Perspectives and others 2007). Sodium chloride is an important nutrient and an essential ingre- dient in producing safe foods with acceptable sensory character- Preservation istics and structures. However, population surveys indicate that Salt reduces water activity in foods thereby acting as a crit- a great majority of people in industrialized societies consume ical hurdle to control growth of pathogens and spoilage organ- much more than the current recommended amount of sodium isms. If sodium chloride levels are decreased, it may be necessary chloride. This includes over 95% of men and over 75% of women to increase concentrations of some other preservatives or more in the U.S. according to data from NHANES III (Third National carefully control cooking, packaging, and storage temperatures Health and Nutrition Examination Survey). Reduction of sodium to ensure safe foods with a reasonable shelf life. Any changes in levels in the diet is considered to be one important strategy for re- ingredients or processes must be tested to ensure that they do not ducing prevalence of hypertension and cardiovascular diseases. render a food organoleptically unacceptable or permit growth of Other dietary and lifestyle changes, including increased exercise pathogens (Fulladosa and others 2009). and intake of fruits and vegetables with high potassium levels Substitution of potassium chloride for sodium chloride is ac- and reduced intakes of saturated fats, are also important for good ceptable to consumers for many foods as long as no more than health. 30% to 40% of the NaCl is replaced. KCl appears to affect mi- In North American and European countries, processed foods crobes in foods in a similar fashion to NaCl (Reddy and Marth and restaurant foods account for over 70% of dietary intake 1991; Askar and others 1993; Guardia and others 2006). Prelim- of sodium. Food processors face the challenge of reducing salt Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 53 CRFSFS: Comprehensive Reviews in Food Science and Food Safety content in their foods while still producing safe, palatable, and Carbone LD, Bush AJ, Barrow KD, Kang AH. 2003. The relationship of sodium intake to economical foods. It is probably not necessary, for improving calcium and sodium excretion and bone mineral density of the hip in postmenopausal African-American and Caucasian women. J Bone Miner Metab 21:415–20. health, to lower salt concentrations in every food if the overall Cauvain SP. 2007. Reduced salt in bread and other baked products. In: Kilcast D, Angus F, dietary intake is reduced. Individuals, particularly those who are editors. Reducing salt in foods. Boca Raton, Fla.: CRC Press. p 283–95. salt-sensitive, also need to control discretionary use of salt during [CDCP] Centers for Disease Control and Prevention. 2009. Application of lower sodium intake recommendations to adults—United States, 1999–2006. Morbid Mortal Weekly cooking and at meals. However, it is difficult to reduce sodium in- Rep 58:281–3. take for those who frequently eat restaurant meals and processed Charlton KE, MacGregor E, Vorster NH, Levitt NS, Steyn K. 2007. Partial replacement of NaCl can be achieved with potassium, magnesium and calcium salts in brown bread. Int J Food foods. Sci Nutr 58:508–21. In addition to processing and safety challenges involved in Chen J, Gu DF, Huang JF, Rao DC, Jaquish CE, Hixson JE, Chen CS, Chen JC, Lu FH, Hu producing low sodium foods, there is also an economic consid- DS, Rice T, Kelly TN, Hamm LL, Whelton PK, He J. 2009. Metabolic syndrome and salt sensitivity of blood pressure in non-diabetic people in China: a dietary intervention study. eration. Sodium chloride is very cheap and any substitute used Lancet 373:829–35. will increase the cost of the product. Production of foods with Cheville AM, Arnold KW, Buchrieser C, Cheng CM, Kaspar CW. 1996. rpoS regulation a reduced sodium content will require reformulation and addi- of acid, heat, and salt tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 62:1822–4. tional associated costs of consumer testing and pilot plant tests. Chipley JR. 2005. Sodium benzoate and benzoic acid. In: Davidson PM, Sofos JN, Branen This economic issue is emphasized by advocates of governmen- AL, editors. Antimicrobials in food. New York: Taylor & Francis. p 11–48. tal directives or regulations for lower-salt foods. For example, if Christian JHB. 2000. Drying and reduction of water activity. In: Lund BM, Baird-Parker TC, Gould GW, editors. The microbiological safety and quality of food. Gaithersburg, Md.: all bakers must reduce salt levels in their bread, then no one Aspen Publishers. p 146–74. company that is trying to produce a “healthier” food is at a cost Cobcroft M, Tikellis K, Busch JLHC. 2008. Salt reduction—a technical overview. Food Aus- disadvantage for using a more expensive (Purdy tralia 60:83–6. Cohen HW, Hailpern SM, Alderman MH. 2008. Sodium intake and mortality follow-up in and Armstrong 2007). the third National Health and Nutrition Examination Survey (NHANES III). J Gen Intern Several recent analyses have described the significant positive Med 23:1297–302. Cook NR, Cutler JA, Obarzanek E, Buring JE, Rexrode KM, Kumanyika SM, Appel LJ, Whel- economic benefit for society that widespread reduction in dietary ton PK. 2007. Long-term effects of dietary sodium reduction on cardiovascular disease sodium would achieve. Millions fewer people would develop hy- outcomes: observational follow-up of the trials of hypertension prevention. Brit Med J pertension and its associated diseases and this could save billions 334:885–92. Cook NR, Obarzanek E, Cutler JA, Buring JE, Rexrode KM, Kumanyika SK, Appel LJ, Whelton of dollars in health care expenditures as well as improving pro- PK. 2009. Joint effects of sodium and potassium intake on subsequent cardiovascular ductivity and quality of life (Beaglehole and others 2007; Dall disease. The Trials of Hypertension Prevention follow-up study. Arch Intern Med 169:32– and others 2009a, 2009b; Palar and Sturm 2009). 40. Dall TM, Fulgoni VL, Zhang YD, Reimers KJ, Packard PT, Astwood JD. 2009a. Potential health benefits and medical cost savings from calorie, sodium, and saturated fat reductions in the Acknowledgments American diet. Am J Health Promot 23:412–22. Dall TM, Fulgoni VL, Zhang YD, Reimers KJ, Packard PT, Astwood JD. 2009b. Potential We thank Barbara Cochrane for valuable assistance in format- national productivity implications of calorie and sodium reductions in the American diet. 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