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 inhibition of growth and toxin production by Clostridium botulinum in processed meats and cheeses. Other sodium salts contributing to overall sodium consumption are also very important in 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 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.

1. Implications of Sodium
Reduction on Food Safety
and Quality
Peter J. Taormina, Ph.D., RM(NRCM)
Principal Microbiologist, John Morrell Food Group
Southern California Food Industry Conference
March 6, 2013

2. P. Taormina -
March 6, 2013
Outline
 Salt and sodium reduction is now reality
 Review of antimicrobial effects of salts
 Replacement of sodium chloride with
other chloride salts
 Sodium reduction research and modeling
 Research needs

3. P. Taormina -
March 6, 2013
At Issue: Sodium Intake
 High sodium intake increases blood pressure.
 Dickinson and Havas, 2007. Arch. Intern. Med.
167:1460-1468; Karppanen and Mervaala, 2006.
Prog. Cardiovasc. Dis. 49:59-75; Cutler and Roccella,
2006. Hyptertension. 48:818-819.
 Ave. U.S. adult - 4,000 mg/day per 2,000 calories
 USDA, ARS Data Tables. 1994-96 diet and health
knowledge survey.
 Amer. Heart Assoc. recommends <2,300 mg
salt/day

4. P. Taormina -
March 6, 2013
Campaigns for “Salt” Reduction
 World Action on Salt and Health (WASH)
 Reduction in dietary salt intake of 10-15g/day
to the World Health Organization (WHO)
target of 5g/day (about 2,000 mg)
 Food Standards Agency, UK
 “No more than 6g”
 Center for Science and the Public Interest
 FDA petition to revoke GRAS status of NaCl
 Reclassify NaCl as “food additive”

5. P. Taormina -
March 6, 2013
At Issue: Sodium Intake
 Roughly 80% of daily
intake from processed
foods and restaurant
foods.
 Mattes and Donnelly,
1991. J. Am. Coll.
Nutr. 10:383-393
2010 Dietary Guidelines, USDA & USDHHS.
www.dietaryguidelines.gov

6. P. Taormina -
March 6, 2013
2010 Dietary Guidelines
 Reduce daily sodium intake to < 2,300 mg
 Further reduce intake to 1,500 mg for
about half of the U.S. population
 Children
 Majority of adults:
 51 and older
 African American
 have hypertension, diabetes, or chronic kidney
disease

7. P. Taormina -
March 6, 2013
Sodium Intake in the United States

8. P. Taormina -
March 6, 2013
A Brief History of Salt
 Most ancient known food preservative.
 Historically used to preserve meat, fish , vegetables,
fruit.
 Of crucial economic importance in ancient times.
 Served as currency in various places at various times.
 Wars have been fought over it.
 Roman soldiers received salt as part of their pay.
 “salarium argentum” → en. salary, pt. salário, es. salario
 Historical association with meat and other foods.
 Lat. sal (salt), salsus (salty), salsicus (seasoned with salt)
 en. sausage, fr. saucisse, pt. salsicha, es. salchicha
 en. salad, fr. salade, pt. salada, es. ensalada
 en. sauce, fr. sauce, pt. salsa, es. salsa
Slide courtesy of Dr. Rodrigo Tarté

9. P. Taormina -
March 6, 2013
Physiology of Salt
 Essential mineral; must be
consumed in adequate
amounts.
 Key roles
 Proper balance and acid-base
balance of body fluids.
 Regulation of movement of
fluids into and out of cells
(together with potassium).
 Regulation of blood volume
and pressure.
 Nerve function and muscle
contraction.
11
Na
Sodium (Natrium)
22.98976928
Slide courtesy of Dr. Rodrigo Tarté

10. P. Taormina -
March 6, 2013
Food Contributors to Sodium Intake
United States, 2007-2008*
* 75% of total intake; does not include sodium from salt added in the home during food preparation or at the
table, estimated at 20% of total intake
Source: What We Eat in America, NHANES 2007-2008, Day 1 dietary intake weighted.
Slide courtesy of Dr. Rodrigo Tarté

11. P. Taormina -
March 6, 2013
Food Contributors to Sodium Intake
Canada, 2004
Source: Sodium Reduction Strategy for Canada (2010) [Data from: CCHS 2.2 (Fischer PWF, Vigneault M, Huang R,
Arvaniti K, Roach P (2009). Sodium food sources in the Canadian diet. Appl Physiol Nutr Metab 34:884-
92)]
Slide courtesy of Dr. Rodrigo Tarté

12. P. Taormina -
March 6, 2013
Current National Recommendations
 United States, cont.
 Institute of Medicine, National Academy of Sciences
 Research Need Areas
 Understanding of how salty taste preferences develop
throughout the lifespan.
 Development of innovative methods to reduce
sodium in foods while maintaining palatability,
physical properties, and safety.
 Enhancement of current understanding of factors that
impact consumer awareness and behavior relative to
sodium reduction.
Slide courtesy of Dr. Rodrigo Tarté

13. P. Taormina -
March 6, 2013
Questions for Discussion
 Question 2. Would reducing the salt
content of food, even in a modest way,
impact the safety or quality of various
foods given the wide variety of technical
functions for which salt is used in food?
FDA; 21 CFR Part 15; Salt and Sodium: Petition to Revised the
Regulatory Status of Salt and Establish Food Labeling
Requirements Regarding Salt and Sodium Public Hearing; Request
for Comments

14. P. Taormina -
March 6, 2013
Questions for Discussion
 Question 2a. How feasible would it be
to mitigate this impact if true? Could
it be mitigated by, for example, the
addition of other ingredients?
FDA; 21 CFR Part 15; Salt and Sodium: Petition to Revised the
Regulatory Status of Salt and Establish Food Labeling
Requirements Regarding Salt and Sodium Public Hearing; Request
for Comments

15. P. Taormina -
March 6, 2013
Examples of Foods Microbiologically
Preserved
by Added Sodium Chloride
 Ready-to-eat, refrigerated
 Deli meats, bacon, hot dogs, roasts, hams, etc.
 Prepared salads and spreads
 Cottage cheese, Cheddar cheese, aged cheeses, soft
cheeses
 Ready-to-eat, shelf stable
 Dry sausages, dry cured ham, smoked fish
 Processed cheese foods and spreads
 Pre-cooked bacon
 Canned foods (soups, broths, chilies, sauces, beans,
vegetables)
 Salad dressings, condiments

16. P. Taormina -
March 6, 2013
Examples of Foods Not
Microbiologically Preserved by
Added Sodium Chloride*
 Baked breads, cereals
 Dry snack products
 Crackers, chips, popcorn, etc.
 Prepared foods (boxed)
 Rice packages, macaroni and cheese
 Frozen foods
*When foods stored properly in final packaged form

17. P. Taormina -
March 6, 2013
Examples of Foods in Which
Preservative Properties of Sodium
Chloride is Unclear
 Foods Prepared and Immediately (<1hr)
Consumed at Restaurants
 Foods Prepared but Not Immediately
Consumed at Restaurants?
 Inhibition of growth during hot holding?
 Inhibition of growth during refrigerated
storage?

18. P. Taormina -
March 6, 2013
Other Sources of Added Sodium

19. P. Taormina -
March 6, 2013
Other Sodium Preservatives
 Sodium lactate
 Sodium acetate and diacetate
 Calcium di-sodium EDTA
 Sodium hexametaphosphate
 Sodium propionate
 Sodium benzoate
 Sodium sulfite
 Sodium nitrite

20. P. Taormina -
March 6, 2013
Some sodium-containing preservative molecules used in processed
foods and their contribution to total sodium per serving
Sodium-Containing
Ingredient
Formula Molar Mass
(g/mole)
Molar
Ratio of
Na+
Typical Addition
Levels (g / 100g
serving)
mg Na+
/
100g
- chloride NaCl 58.44 0.3934 2.0 786.790
trisodium phosphate Na3
PO4
163.94 0.4207 1.0 420.703
disodium phosphate Na2
HPO4
141.96 0.3239 1.0 323.894
sodium tripolyphosphate Na5
P3
O10
367.86 0.3125 1.0 312.483
- lactate NaC3
H5
O3
112.06 0.2052 1.5 307.737
monosodium phosphate NaH2
PO4
119.98 0.1916 1.0 191.615
- hexametaphosphate (NaPO3
)6
611.77 0.2255 0.75 169.108
- metabisulfite Na2
S2
O5
190.11 0.2419 0.2 48.372
- citrate Na3
C6
H5
O7
258.07 0.2673 0.15 40.088
- acetate NaC2
H3
O2
136.08 0.1689 0.15 25.342
- diacetate NaC4
H7
O4
142.09 0.1618 0.15 24.270
- propionate NaC3
H5
O2
96.07 0.2393 0.025 5.983
- erythorbate NaC6
H7
O6
198.11 0.1160 0.05 5.802
- nitrite NaNO2
68.99 0.3332 0.017 5.665
- benzoate NaC6
H5
CO2
144.11 0.1595 0.025 3.988(Taormina. 2010. Crit. Rev. Food Sci. Nutr.)

21. P. Taormina -
March 6, 2013
Sodium-
Containing
Molecule
Primarily Used
as Preservative
Primarily Used for
Other Non-
Preserving
Function
Essentially Dual
Use Purpose
-Chloride Shelf stable
meats, fish
Processed meats,
cheeses
-Nitrite Processed meats
-Lactate Processed meats
-Acetate
(Diacetate)
Processed meats
-Citrate Beverages
-Polyposphates RTD beverages,
syrups, sauces
Processed meats,
Moisture enhanced
fresh meat and
poultry
-Erythorbate Processed meats
-Glutamate Various foods
-Ascorbate Various foods and
beverages

22. P. Taormina -
March 6, 2013
Sodium Chloride: Mechanism of
Action
 Lowering of aw
 Plasmolysis
 Interference with
substrate utilization
(3-7% NaCl [w/v])
 Phosphohexose
isomerase
 Isocitrate
dehydrogenase
 Aldolase
 Chloride ion

23. P. Taormina -
March 6, 2013
TEM (28,500x) of 24-h E. coli O157:H7
cultures in BHI with
NaCl at 0%, 5%, and 10%
M. Hajmeer et al. 2006. Food Microbiology 23: 446–452
0% NaCl 5% NaCl 10% NaCl

24. P. Taormina -
March 6, 2013
TEM (28,500x) of 24-h S. aureus culture
in BHI with NaCl at 0%, 5%, and 10%
M. Hajmeer et al. 2006. Food Microbiology 23: 446–452
0% NaCl 5% NaCl 10% NaCl

25. P. Taormina -
March 6, 2013
Effect of NaCl on Cells
 Extra coarse grade NaCl seemed to have
a milder effect compared to fine grade with
respect to cell damage
 24h cells were more affected than 12h
cells
M. Hajmeer et al. 2006. Food Microbiology 23: 446–452

26. P. Taormina -
March 6, 2013
Main Intrinsic Properties of
Perishable Foods That Affect
Microorganisms
 Moisture
 % Moisture
 Water activity (aw)
 Equivalent Relative Humidity
 Vapor pressure product / vapor pressure water
 Moisture:Protein ratio
 % Brine Concentration (Water-Phase Salt)
 Acidity
 pH
 Preservatives
 Salt
 Benzoate, sorbate, lactates, diacetate, nitrite, etc.
 Polyphosphates

27. P. Taormina -
March 6, 2013
Influence of Solute on Minimum
aw for Bacterial Growth
Organism Min. aw for growth in
NaCl Glucose* Glycerol
Clostridium perfringens 0.970 0.960 0.950
Clostridium botulinum type E 0.970 - 0.940
Lactobacillus helveticus 0.963 0.966 0.928
Streptococcus lactis 0.965 0.949 0.924
Pseudomonas fluorescens 0.957 - 0.940
Vibrio parahaemolyticus 0.948 0.984 0.937
Adapted from: Sperber, 1983. J. Food Prot. 46:142-150
* Glucose not sterilized separately from media; inhibitory nonenzymatic browning
products may have been present

28. P. Taormina -
March 6, 2013
Death Rates of Pathogens in Natural
Sheep Casings at 20ºC at Different aw
Levels
0
0.05
0.1
0.15
0.2
0.25
0.3
0.35
0.4
0.45
0.7 0.8 0.9 1
aw-levels
DeathRate(logCFU/day)
E. coli O157:H7
S. Typhimurium
L. monocytogenes
S. aureus
Adapted from Wijnker et al., 2006. Food Microbiol. 23:657

29. P. Taormina -
March 6, 2013
Clostridium perfringens Growth
During Cooling of Ham and Beef
 3% NaCl completely inhibited growth
during exponentially declining
temperatures from 54.4 to 8.5°C in 21h
 ≤ 2% NaCl permitted growth in ham
cooled in ≥18h and in beef cooled in ≥15h
Zaika, 2003. J. Food Prot. 66:1599-1603

30. P. Taormina -
March 6, 2013
aw Suppression with Binders
 Shelf stable fish sausage with 3.2% salt
was formulated to aw of 0. 97-0.92 with egg
white solids and combinations of egg
white solids, non-fat dry milk, propylene
glycol, and soy protein isolate.
 Spores of PA 3679 germinated at 0.924,
but did not grow at < 0.950
 Macromolecular food binders viable
alternative to high levels of salts
Nieto and Toledo. 1989. J. Food Sci. 54:1129-1135.

31. P. Taormina -
March 6, 2013
Firmness of Reduced Sodium Sausages with
Carrageenan
Ruusunen et al., 2003

32. P. Taormina -
March 6, 2013
Saltiness of Reduced Sodium Sausages with
Carrageenan
Ruusunen et al., 2003

33. P. Taormina -
March 6, 2013
Flavor Intensity of Reduced Sodium Sausages
with Carrageenan
Ruusunen et al., 2003

34. P. Taormina -
March 6, 2013
Reduced-Sodium Processed
Cheese Foods and Spreads
 Incorporation of delta-gluconolactone as a
delayed acidulant reduced the pH of
cheeses to 5.26, which contributed to
inhibition of C. botulinum.
 All potassium emulsifiers allowed toxin
production suggesting that sodium and
potassium ions are not equivalent in
effecting inhibition of C. botulinum.
Karahadian et al., 1984. J. Food Prot. 48:63-69

35. P. Taormina -
March 6, 2013
Ion Replacement – Spoilage Organisms
Nielsen and Zeuthen. 1987. Intl. J. Food Microbiol. 4:13-24

36. P. Taormina -
March 6, 2013
Ion Replacement – Spoilage Organisms
Nielsen and Zeuthen. 1987. Intl. J. Food Microbiol. 4:13-24

37. P. Taormina -
March 6, 2013
Ion Replacement – Spoilage Organisms
Nielsen and Zeuthen. 1987. Intl. J. Food Microbiol. 4:13-24

38. P. Taormina -
March 6, 2013
Ion Replacement - Pathogens
Nielsen and Zeuthen. 1987. Intl. J. Food Microbiol. 4:13-24

39. P. Taormina -
March 6, 2013
Ion Replacement - Pathogens
Nielsen and Zeuthen. 1987. Intl. J. Food Microbiol. 4:13-24

40. P. Taormina -
March 6, 2013
Ion Replacement - Pathogens
Nielsen and Zeuthen, 1987. Intl. J. Food Microbiol. 4:13-24

41. P. Taormina -
March 6, 2013
Ionic Strength Comparisons
 When ionic strength equivalents of KCl and
MgCl2 were compared with NaCl at 2.50 and
1.25% against Micrococcus, Moraxella, and
Lactobacillus inoculated into ground pork there
were no significant differences between ions
after ten days of storage at 5°C.
 Highest reduction of the aerobic mesophilic
microflora of pork sausage by CaCl2 followed by
NaCl>KCl.
 Terrell, R. N., M. Quintanilla, C. Vanderzant, and F. A.
Gardner. 1983. J. Food Sci. 48:122-124

42. P. Taormina -
March 6, 2013
Comparisons of Ionic Strengths
 Challenge study data was used to construct an
Anti-yersinial index (AI) to represent the
comparative inhibitory properties of chloride
salts against Yersinia enterocolitica in pork.
 The index reflected that CaCl2 was most efficient
against serotype O:3 while the higher
concentrations of KCl (1.8 and 2.2% w/w Cl¯)
were most efficient against serotype O:8.
Raccach, M., and E. C. Henningsen. 1997. Food Microbiol. 14:431-438.

43. P. Taormina -
March 6, 2013

44. P. Taormina -
March 6, 2013

45. P. Taormina -
March 6, 2013
Battey et al., 2002. Appl. Environ. Microbiol. 68:1901-1906
The Effects of pH and Sodium Benzoate on
Probability of Growth of a C. lipolytica, S.
cerevisiae, and Z. bailii Cocktail -
Model Bev. 100ppm Potassium Sorbate, 8wks

46. P. Taormina -
March 6, 2013
Sodium Benzoate in Beverages
 Decreasing the pH of the beverage would permit
less potassium sorbate and/or sodium benzoate
to achieve the same probability of yeast growth.
 Conversely, increasing preservative levels
provides microbial stability at increased pH
levels.
 Potassium benzoate vs. sodium benzoate
 Successful preservation in non-caloric beverages
 Offsets sodium per serving due to non-caloric
sweeteners

47. P. Taormina -
March 6, 2013
Effect of NaCl and Sucrose
Concentrations on the Growth Response
of Yeasts at Different pH Values
Praphailong and Fleet. 1997. Food Microbiol. 14:459-568.

48. P. Taormina -
March 6, 2013
NaCl and Heat Resistance
Juneja and Eblen, 1995. J. Food Prot. 58:813-816
Z values
10.08
8.82
8.47

49. P. Taormina -
March 6, 2013
NaCl and Heat Resistance
 Bacillus cereus strains exposed to
increasing concentrations of NaCl for
30min; thermotolerance assessed at 50ºC
 Both strains showed enhanced
thermotolerance after pre-exposure to non-
lethal salt stress conditions in the exponential
phase; less pronounced for stationary phase
cells.
de Besten et al., 2006. Appl. Environ. Microbiol.

50. P. Taormina -
March 6, 2013
NaCl and Heat Resistance
Organism Effect of
Added NaCl
on Heat
Resistance
Reference
Escherichia coli Increased Calhoun and Frazier,
1966
Staphylococcus aureus Increased
Pseudomonas fluorescense Decreased
Salmonella (heat sensitive) Increased Baird-Parker et al.,
1970
Salmonella (heat resistant) Decreased

51. P. Taormina -
March 6, 2013
What if?
 “A reasonable interim target is a 50%
reduction in sodium in processed foods.”
Stephen Havas, MD, MPH, MS
Barry D. Dickinson, PhD
Modena Wilson, MD, MPH
JAMA, Vol. 298, No. 12

52. P. Taormina -
March 6, 2013
What if 50% Reduction in
Sodium? – PMP 7.0 Modeling
 CSPI, 2005. Salt
Assault: Brand Name
Comparisons of
Processed Foods
 Selected food
examples
 Modeled with
reported NaCl and
50% reduced NaCl

53. P. Taormina -
March 6, 2013
What if 50% Reduction in Sodium? –
PMP 7.0 Growth Modeling
 96% Fat Free Honey Roasted and White Turkey
Breast. 1180 mg sodium / 100g
Pathogen PMP Growth
Conditions
Time to
Growth,
Regular
NaCl
Time to
Growth, 50%
Reduced NaCl
L. monocytogenes Broth culture
(aerobic);
7.2ºC; 1-log
increase
60.9 h 57.7 h
S. aureus Broth culture
(aerobic); 19ºC;
3-log increase
25.2 22.8 h

54. P. Taormina -
March 6, 2013
Inhibition of L. monocytogenes on Regular & Reduced Sodium Ham
Slices as Affected by Formulated Inhibitors and NaCl:KCl (Lite Salt)
During Vacuum-Packaged Storage at 4.4o
C (40o
F)

55. P. Taormina -
March 6, 2013
What if 50% Reduction in Sodium? –
PMP 7.0 Growth Modeling
 Hardwood smoked bacon; 2070 mg sodium /
100g
Pathogen PMP Growth
Conditions
Time to
Growth,
Regular
NaCl
Time to
Growth, 50%
Reduced NaCl
S. aureus Broth culture
(aerobic); pH
6.0; 42ºC; 3-log
increase
10.4 h 10.1 h
C. perfringens Broth culture
(anaerobic); pH
6.0; 42ºC; 1-log
increase
5.1 h 2.9 h

56. P. Taormina -
March 6, 2013
What if 50% Reduction in Sodium? –
PMP 7.0 Growth Modeling
 Pasteurized prepared cheese product
(unrefrigerated); 1570 mg/100g
Pathogen PMP Growth
Conditions
Max.
Probability of
Growth,
Regular
NaCl
Max.
Probability of
Growth, 50%
Reduced NaCl
Proteolytic
C. botulinum
Broth culture
(anaerobic); pH
6.5; 25ºC
0.52 0.58

57. P. Taormina -
March 6, 2013
Antimicrobial Alternatives
 Plant Derived
 Glucosinolates (Isothiocyanates) – Cruciferaceae
 Lignans
 Saponins (Yucca, asparagus)
 Catechins (EGCG) – Green tea
 Hops beta-acids
 Fruit juices & extracts (acids & phytochemicals)
 Spices - essential oils & solvent extracts

58. P. Taormina -
March 6, 2013
Antimicrobial Alternatives
 Plant Derived
 Spices - Essential oils & solvent extracts
Source Antimicrobial Components
Cinnamon Cinnamic Acid, Cinnamaldehyde
Clove Eugenol
Garlic Allicin
Mustard Allyl-isothiocyanate
Oregano Carvacrol, thymol
Vanilla Vanillin
Thyme Thymol
Rosemary α- Pinene, Camphor, Verbenone, 1, 8-Cineole

59. P. Taormina -
March 6, 2013
Antimicrobial Alternatives
 Chemical
 Inorganic salts: NaCl, KCl, MgCl, CaCl2, NaNO2
 Organic salts: lactate, diacetate, citrate,
propionate
 Organic acids: lactic, acetic, citric, propionic,
malic etc.
 Fatty acid based: lauric arginate, octanoic acid
 Weak acids: benzoic, sorbic
 Phenolics: smoke fractions, synthetic phenolics
 Other: hexametaphosphate, metasilicate,
sulfite, EDTA

60. P. Taormina -
March 6, 2013
Antimicrobial Alternatives
 Microbial Derived
 Bacteriocins
 nisin, pediocin, sakacin, reuterin, leucocin
 Fermentation products (combinations of acids,
peptides & bacteriocins)
 Antimycotics
 natamycin
 “Live” microorganisms
 Lactic acid bacteria, Carnobacterium maltaromaticum
 Phage
 Virus that infects bacteria
 Listeriaphage, coliphage, etc.

61. P. Taormina -
March 6, 2013
Synergistic effect of an oregano-and-cranberry mixture
on inhibition of L. monocytogenes on beef slices, pH 6.0
Lin et al., 2004. Appl. Environ. Microbiol. 70(9):5672

62. P. Taormina -
March 6, 2013
Conclusions
 Salt (Sodium chloride) is the oldest and most
widely used inhibitory compound in foods.
 Reduction of NaCl from processed foods should
be based on results of appropriate research.
 Research on impact of salt reduction on restaurant
foods is particularly lacking.
 Hot holding
 Cooling and cold storage
 Reheating
 Replacement of NaCl with antimicrobial herbs
and spices has not been thoroughly researched.

63. P. Taormina -
March 6, 2013
Conclusions
 Other sources of sodium should be considered.
 Reduced sodium products should be validated
with challenge studies.
 For thorough reviews on Salt, Sodium and Food
Safety see:
 Doyle and Glass, 2010. Comp. Rev. Food Sci. and
Food Safety. 9:44-56.
 Taormina, 2010. Crit. Rev. Food Sci. and Nut., 50: 3,
209-227.
 Sofos, 1983. J. Food Safety. 6:45-78.
 Reddy and Marth, 1991. J. Food Prot. 54:138-150.