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 food industry in a partnered approach to improve consumer public health. 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 sodium chloride 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 flavor, texture, and safety of those products. Specifically, adding sodium chloride 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 sausages. Sodium chloride also improves tenderness during cooking. The water 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 potassium 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 salt 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 nutrient 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 foods 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, Food Quality, 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 hypertension 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 salts 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 blood pressure 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 cardiovascular disease 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 Food Standards Agency, 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, food packaging, 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) •Bacon, 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- halophile,” “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 sugars. 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 sea salt, 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 metabolism 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 adenosine triphosphate (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 sausage 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 brining, olives fermented at 25◦C were judged by panelists as parasites. The process of dry salting 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 calcium chloride, 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 salami. 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 Lebanon bologna 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 potassium chloride, 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 food processing 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 (chorizo 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 taste 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 waters. 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 tastes, 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. Soy sauce, 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