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Microbiological Safety of Mayonnaise Salad Dressin
Microbiological Safety of Mayonnaise Salad Dressin
Review
Silliker Laboratories Group, Inc., 900 Maple Avenue, Homewood, Illinois 60430, USA
In the United States commercially produced mayon- toxic to foodborne pathogens at or below their pKa (9, 25,
naise, salad dressings, and sauces have a remarkable food 66). Acetic is the predominant acid, which is added as var-
safety record. However, in Europe and other parts of the ious types of vinegars (68).
world where homemade mayonnaise is prepared with mild- Most food ingredients added to these products are acid-
er acid content and unpasteurized eggs, mayonnaise contin- ic. However, some ingredients are considered low acid such
ues to be a health problem from Salmonella (23, 62). In as egg and egg yolks, pH 6.0 to 7.0; garlic, pH 5.3 to 5.8;
general these products are composed of a vegetable oil or onions, pH 5.3 to 5.8; honey, pH 6.0 to 6.5; sugar, pH 6.5,
a fat-free oil substitute base and a low pH, salt-containing and egg whites, pH 9.07 (27, 40).
water phase. Vegetable oils and fat-free oil substitutes do
not contribute to the pH of these products. The predominant UNITED STATES REGULATORY INTRODUCTION
acid in the water phase is acetic and to a lesser extent,
With the exception of mayonnaise, spoonable salad
depending on the formulation, lactic or citric acid or both.
dressing, and French dressing, these products are not legally
In addition, they are flavored by acid-containing ingredients
defined. Traditionally, these foods have been classified as
such as buttermilk, sour cream, blue cheese, parmesan
cheese, and other fermented dairy products (lactic acid), acid foods with a pH below 4.6. The legal definition for
lemon juice (citric acid), pickle relishes (lactic and acetic acid foods is found in the Code of Federal Regulations
acids), and tomato solids (citric acid) just to mention a few. (CFR) 21 Part 114(1). According to the definition 114.3(b):
They are frequently implicated by uninformed people as the ‘‘Acidified foods means low-acid foods to which acid(s) or
cause of foodborne illness, especially mayonnaise. Never- acid food(s) are added. . .; They have a water activity (aw)
theless, commercially prepared products have never been greater than 0.85 and have a finished equilibrium pH of 4.6
directly identified as the cause of any foodborne illness. or below. These foods may be called, or may purport to be,
This performance is largely due to the intrinsic bactericidal ‘pickles’ or ‘pickled㛮㛮㛮.’ Carbonated beverages, jams, jel-
nature of these products. Organic acids and acid ingredients lies, preserves, acid foods (including such foods as stan-
contribute to the desirable flavor of these products and are dardized and nonstandardized food dressings and condi-
ment sauces) that contain small amounts of low-acid
* Author for correspondence. Present address: 420 Tyler Drive, Clear
food(s) and have a resultant finished equilibrium pH that
Brook, VA 22624, USA. Tel: 540-678-9991; Fax: 540-678-0399; does not significantly differ from that of the predominant
E-mail: rsmittle@visuallink.com. acid and acid food, and foods that are stored, distributed,
J. Food Prot., Vol. 63, No. 8 MICROBIOLOGICAL SAFETY OF DRESSINGS 1145
TABLE 1. The lower limits of pH allowing the initiation of TABLE 2. The inhibitory and lethal pH of acetic acid on food-
growth by some foodborne pathogens in laboratory media ad- borne pathogens in laboratory media
justed with strong acid or alkali
Inhibitory Lethal
Minimum Organism pH pH
Organism Reference pH
Salmonella Aertrycke (45) 4.9 4.5
Salmonella paratyphi 40 4.5 Staphylococcus aureus (45) 5.0 4.9
Salmonella schottmuelleri 40 4.5 Bacillus cereus (45) 4.9 4.9
Salmonella typhi 40 4.0–4.5 Salmonella Anatum, Ten-
Escherichia coli O157:H7 34 4.0 nessee, or Senftenberg
Campylobacter jejuni 72 4.9 (17) 5.4 NAa
Yersinia enterocolitica 6 4.0 Escherichia coli O157:H7
Vibrio parahaemolyticus 40 4.8 (11, 20) 4.5–5.0 (20) ⬍3.0 (11)
Plesiomonas shigelloides 42 4.0 Y. enterocolitica (7) 5.08–5.0 4.75
dissociated. When introduced into the water phase, these coli O157:H7 survived exposure in pH 3.9 acetic acid-ad-
moieties exist: justed tryptic soy broth as compared to unadapted cells ex-
posed to the same conditions (65).
HA s H⫹ ⫹ A⫺.
Salmonella, E. coli, and Shigella have demonstrated
At equilibrium, the ratio [H⫹][A⫺]/[HA] is a constant adaptability to acidic conditions with enhanced survival
(pKa). characteristics (12, 21, 35, 46). Leyer and Johnson (46)
found that Salmonella Typhimurium adapted to mildly
Ka ⫽ [H⫹][A⫺]/[HA]
acidic conditions (pH 5.8) demonstrated enhanced tolerance
[H⫹] ⫽ Ka[HA]/[A⫺] to heat, salt, an activated lactoperoxidase system, and the
Rewritten, this is surface-active agents crystal violet and polmyxin B. In ad-
dition, Idziak and Crossley (38) reported that the growth of
⫺log[H⫹] ⫽ ⫺log Ka ⫺ log[HA] ⫹ log[A⫺] Salmonella Typhimurium in pH 5.2 barbecue sauce at the
or early and middle log phase increased their virulence, which
TABLE 3. Summary of United States manufacturer’s maximum and target values for pH and percent total titratable acidity and target
values for percent titratable acidity as ascetic acid in the water phase and percent salt for mayonnaise, dressings, and sauces (source:
The Association for Dressings and Sauces, Atlanta, Ga.)
Titratable acidity
Total titratable as acetic
pH acidity in water phase Percent salt
Product type (n) Higha Lowb Lowb Higha Lowb Highb Lowb Highb
Pourable dressing (87)c 4.4 2.6 0.6 2.83 1.22 5.25 0.45 7.26
Pourable dressing, light
reduced calorie (35)c 4.15 2.7 1.05 2.1 1.4 5.9 0.9 5.2
Pourable dressing, fat
free (50)c 4.15 3 0.61 2.39 0.61 2.87 0.15 6.35
Real mayonnaise (6 to
of 0.5% organic acids adjusted to pH 3.0 with HCl. They (32) reported that the organic acid order of effectiveness of
found that most strains were inactivated where HCl dem- toxicity on Salmonella Typhimurium was formic ⬎ acetic
onstrated a greater inactivation rate than the organic acids ⬎ propionic ⬎ butyric ⬎ HCl but was dependent on their
citric, malic, acetic, and lactic. In a study on the growth of concentration, temperature of storage, composition of me-
E. coli O157:H7, Conner and Kotrola (20) found that when dia, and water activity. Acetic, lactic, and citric acid were
tryptic soy broth was combined with yeast extract adjusted bactericidal to Salmonella Enteritidis, Typhimurium, and
to pH values from 4.0 to 5.5 with organic acids, the order Agona in egg mass with acetic being more efficient than
of effectiveness was mandelic ⫽ acetic ⬎ citric ⬎ lactic lactic and citric being the least efficient in killing these
⬎ malic ⬎ tartaric. Ryu et al. (65) found that adapted and organisms (73). In a comparison of the effects of organic
unadapted E. coli O157:H7 did not form colonies when acids on S. aureus inhibition, Nunheimer and Fabian (58)
exposed to tryptic soy agar acidified with acetic, lactic, ma- found that acetic ⬎ lactic ⬎ citric ⬎ malic ⬎ tartaric ⬎
lic, and citric acids at pH values lower than 5.4, 4.5, 4.2, HCl. The order of effectiveness of different acids at the
and 4.2, respectively. In addition, they found that the acid- same pH on Y. enterocolitica is acetic ⬎ lactic ⬎ citric (8).
adapted cells could be recovered from the acetic acid pH The same order was confirmed in a later study with inor-
4.2-adjusted tryptic soy agar after a 48-h incubation in tryp- ganic sulfuric acid being less effective than the organic ac-
tic soy broth (65). Based on equal pH values, L. monocy- ids (49).
togenes is affected by organic acids as follows: acetic ⬎
SURVIVAL OF PATHOGENS IN MAYONNAISE,
lactic ⬎ citric ⬎ malic ⬎ HCl, but based on an equal molar
SALAD DRESSINGS, AND SAUCES
concentration the relationship is citric ⬎ malic ⬎ lactic ⬎
acetic ⬎ HCl (25 and 35⬚C) (70). Ahamad and Marth (2) A survey of mayonnaise, salad dressings, and sauces
found that acetic acid was the most detrimental to L. mon- made in the United States (Association for Dressings and
ocytogenes followed by lactic and citric acids. They also Sauces members) shows that the highest reported pH is 4.4,
found that 0.1% acetic, lactic, and citric in laboratory media which is below the pKa 4.75 for acetic acid (Table 3). The
inhibited growth and the higher the temperature the higher lowest reported percent titratable acidity as acetic in the
the degree of inhibition. Ita and Hutkins (41) reported that water phase was 0.43 for all products. Because the predom-
inhibition by undissociated organic acid species on L. mon- inant acid is acetic, these products would be expected to be
ocytogenes was a result of effects on metabolic or other toxic and destructive to the bacterial pathogens, especially
physiological activities. In a later study with E. coli by in light of their low pH and high titratable acidity as acetic.
Sinha (67), toxicity to organic acids appears to be a result Indeed, a survey of the literature shows that this is the case.
of a failure to repair damaged DNA. Goepfert and Hicks E. coli O157:H7, L. monocytogenes, Salmonella spp., Sal-
1148 SMITTLE J. Food Prot., Vol. 63, No. 8
monella Enteritidis, S. aureus, and Y. enterocolitica died level. Figure 1 is a graphic presentation of the log DRT
off when inoculated into a variety of mayonnaises, dress- (min) of a variety of mayonnaises produced in the United
ings, and sauces (6, 19, 26, 28, 30, 33, 36, 50, 57, 61, 64, Kingdon and the United States (26, 33, 50, 51). Analysis
68, 75, 77, 81). E. coli O157:H7 demonstrated a remarkable of variance shows that the regression of pH to log DRT is
tolerance to the acidic conditions of mayonnaise and salad highly statistically significant (P ⬍ 0.001) with a linear
dressings, which has also been reported in acidified labo- regression formula of log DRT ⫽ ⫺2.89 ⫹ 1.35 pH. Whit-
ratory media (10, 16), dry salami (16), apple cider (55), ing and Buchanan (79) in the development of a quantitative
and artificial gastric juice (3). The longest survival reported risk assessment model for Salmonella Enteritidis in pas-
was 93 days in real mayonnaise at 5⬚C (36). At storage teurized liquid eggs, an essential ingredient in mayonnaise
conditions more typical of these products, the longest re- and other dressings, found that a scenario of inadequate
ported time is 40 days at 20⬚C (81). In spite of the resis- pasteurization and temperature abuse could lead to a haz-
tance of E. coli O157:H7, it is still prudent to mix may- ardous product. Y. enterocolitica has been shown to grow
onnaise and acidic dressings with high pH ingredients such in liquid whole eggs and egg whites at 2, 6.7, and 12.8⬚C
TABLE 4. Summary of storage temperatures, pH values, DRT, and titratable acidity (TA) in the water phase of some foodborne pathogens calculated from published literature on mayonnaise,
dressings, and sauces (6, 26, 28, 30, 33, 36, 50, 57, 61, 64, 68, 75, 77, 81)
Storage pH DRT (h) TA water phase
temperature
Organism Product (n) (⬚C) Minimum Mean Maximum Minimum Mean Maximum Minimum Mean Maximum
E. coli O157:H7 RMa and 20–25 3.6 3.81 4.08 7.7 58.3 174.0 0.80 1.71 2.10
RCMb (15)
RM and 5–7 3.6 3.77 4.08 174.0 267.8 448.8 0.80 1.72 2.10
RCM (11)
SDc (8) 4–5 3.6 4.27 4.51 9.36 140.4 312.0 NAf NA NA
L. monocytogenes RCM, 23.9–26.6 3.3 3.95 4.3 8.21 28.44 61.0 0.10 0.65 0.99
CFRCM,d
SS,e RCM
(9)
Salmonella spp. RCM, RM 20–26.6 2.6 3.99 4.7 0 5.15 52.7 0.10 0.65 0.99
CFRCM
(28)
Y. enterocolitica RM (3) 21 3.78 3.78 1.13 8.92 13.52 NA NA NA NA
RM (3) 5 3.78 3.78 5.41 5.81 25.5 NA NA NA NA
a Real mayonnaise.
b Reduced-calorie mayonnaise.
c Salad dressing.
d Cholesterol-free reduced-calorie mayonnaise.
e Sandwich spread.
f Not available.
MICROBIOLOGICAL SAFETY OF DRESSINGS
1149
TABLE 5. Analysis of variance of decimal reduction times (h) of TABLE 6. Analysis of variance of decimal reduction times (h) of
Salmonella spp. in real mayonnaise, reduced-calorie mayonnaise, L. monocytogenes in real mayonnaise, reduced-calorie mayon-
cholesterol-free reduced-calorie mayonnaise, and sandwich naise, cholesterol-free reduced-calorie mayonnaise, and sandwich
spread at 23.9 to 26.6⬚C, pH 3.3 to 4.3, and titratable acidity in spread at 23.9 to 26.6⬚C, pH 3.3 to 4.3, and titratable acidity in
the water phase 0.1 to 0.99% (26, 33, 50, 57, 61, 68) the water phase 0.1 to 0.99% (26, 30, 36)
Source df SS MS F value P Source df SS MS F value P
TABLE 8. Analysis of variance of decimal reduction times (h) of of mayonnaise and dressings and their continued exclusion
E. coli O157:H7 in real mayonnaise and reduced-calorie may- from the acidified foods category of 21 CFR 114.
onnaise at 20 to 25⬚C, pH 3.6 to 4.08, and titratable acidity in
water phase 0.8 to 2.1% (36, 64, 77, 81) ACKNOWLEDGMENTS
Source df SS MS F value P The author thanks the members of The Association for Dressings
and Sauces for their data on dressings and sauces produced in the United
pH 7 36,500 5,214 31.34 ⬍0.001 States. In addition, I thank the Executive Technical Board and staff of
Error 7 1,165 166 The Association for Dressings and Sauces for their review and comments
TA 6 28,686 4,781 4.26 0.032 on this manuscript. Finally, I especially thank Ms. Jeannie Milewski for
Error 8 8,980 1,122 her efforts in coordinating the review and data collection processes.
Total 14 37,665
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