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1144

Journal of Food Protection, Vol. 63, No. 8, 2000, Pages 1144–1153


Copyright 䊚, International Association for Food Protection

Review

Microbiological Safety of Mayonnaise, Salad Dressings, and


Sauces Produced in the United States: A Review
R. B. SMITTLE*

Silliker Laboratories Group, Inc., 900 Maple Avenue, Homewood, Illinois 60430, USA

MS 99-336: Received 10 November 1999/Accepted 11 March 2000

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ABSTRACT
The literature on the death and survival of foodborne pathogens in commercial mayonnaise, dressing, and sauces was
reviewed and statistically analyzed with emphasis on Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes. The
absence of reports of foodborne illness associated directly with the consumption of commercially prepared acidic dressings
and sauces is evidence of their safety. Salmonella, E. coli O157: H7, E. coli, L. monocytogenes, Staphylococcus aureus, and
Yersinia enterocolitica die when inoculated into mayonnaise and dressings. Historically, mayonnaise and dressings have been
exempt from the acidified food regulations and have justly deserved this status due primarily to the toxic effect of acetic and
to a lesser extent lactic and citric acids. These organic acids are inimical to pathogenic bacteria and are effective natural
preservatives with acetic being the most effective in killing pathogenic bacteria at the pH values encountered in these products.
Statistical analysis on data reported in the literature shows that the most important and significant factor in destroying path-
ogenic bacteria is pH as adjusted with acetic acid followed by the concentration of acetic acid in the water phase. The reported
highest manufacturing target pH for dressings and sauces is 4.4, which is below the 4.75 pKa of acetic acid and below the
reported inhibitory pH of 4.5 for foodborne pathogens in the presence of acetic acid. The overall conclusion is that these
products are very safe. They should remain exempt from the acidified food regulations providing adequate research has been
done to validate their safety, and the predominant acid is acetic and reasonable manufacturing precautions are taken.

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

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Listeria monocytogenes 52 5.0 L. monocytogenes (2) 4.59 4.37
Staphylococcus aureus 40 4.0
a Not available.
Clostridium botulinum 37 4.6
Clostridium perfringens 44 5.0
Bacillus cereus 43 4.35
Streptococcus pyogenes 40 6.35 of pathogen growth, and the pH–organic acid relationship
Aeromonas hydrophila 71 4.0 to survivability of foodborne pathogens.
EFFECTS OF ACIDITY ON THE GROWTH AND
SURVIVAL OF MICROORGANISMS
and retailed under refrigeration are excluded from the cov-
erage of this part’’ (18). Acidity is the most important intrinsic characteristic of
This definition was promulgated to define the intrinsic mayonnaise, dressings, and sauces in determining the
food qualities necessary to prevent the growth of foodborne growth and the survival of pathogenic bacteria (68). Sec-
pathogens and define the processing necessary to eliminate ondarily, salt and sugar play minor roles, but they have an
their presence if not met. A water activity of 0.85 is the interactive effect with acetic acid in vinegar on inhibiting
upper limit for preventing the growth of Staphylococcus the growth of foodborne pathogens (25, 68). Commercially
aureus and pH 4.6 is the upper limit preventing the growth pasteurized egg whites, important in the manufacturing of
of Clostridium botulinum (40). cholesterol-free mayonnaise, have been found to be inimi-
Recently, there has been a heightened awareness cal to Listeria monocytogenes when inoculated at the
among health professionals and regulators concerning pre- 10,000/ml level and stored at refrigeration temperature (27).
vious assumptions about the safety of acid and acidified It was speculated that the antilisterial activity was due to
foods. This is largely due to the emergence of the pathogen egg white lysozyme (27). Because microorganisms need
Escherichia coli O157:H7 that is more tolerant of acidic water to grow and oil is anhydrous, the water phase milieu
conditions than other foodborne pathogens (Tables 1 and or the water–oil interface is the portion of these products
2). Outbreaks of enterohemorrhagic E. coli linked to un- that is of primary concern. However, Radford et al. (63)
pasteurized apple cider, which is a low pH product due to found that mayonnaise prepared from oils high in phenolic
malic acid (4), and the implication of mayonnaise and may- compounds, such as olive oil, can accelerate the death of
onnaise-based dressings to an E. coli O157:H7 illness (77) Salmonella Enteritidis. The acid effects on growth and sur-
have added to the confusion. Although the mayonnaise out- vival are primarily concentrated in the water phase com-
break was a result of contamination during handling after ponent.
manufacturing (77), the perception persists that mayonnaise The effects of acidity on microorganisms are deter-
and mayonnaise-based dressings are direct causes of illness. mined in three ways. They are (i) the effect of pH alone,
In light of this new knowledge about these acid-tolerant (ii) the effect of undissociated forms of a particular acid,
pathogens, there is some confusion among regulators as to and (iii) the specific effects of organic acids (66). When a
the status of mayonnaise, dressings, and sauces with regard strong acid like HCl (hydrochloric acid) is introduced into
to the CFR definitions. For example, some state regulators the water phase, it dissociates into H⫹ (hydrogen ion) and
require manufacturers producing mayonnaise, dressings, Cl⫺ (chloride ion) ions. In dilute solutions such as the water
sauces, and condiments to register their products with the phase of these products strong acids are almost completely
Food and Drug Administration as acidified foods. This is dissociated. The relationship between pH and [H⫹] (the hy-
contrary to the CFR 114.3(b) which states that ‘‘standard- drogen ion concentration) that it represents is as follows:
ized and non-standardized food dressings and condiment pH ⫽ ⫺log[H⫹] or log(1/[H⫹])
sauces’’ have always been excluded from the Food and
Drug Administration’s definition of acidified foods (18). A system at pH 7.0 is neutral, whereas a pH 6.0 is 10 times
The purpose of this review is to assess the safety of the as acidic.
acid foods, mayonnaise, dressings, sauces, and condiments In contrast to strong acids, weak lipophilic organic ac-
in light of recent microbiological research, pH limitations ids such as acetic, lactic, and citric acids are only partially
1146 SMITTLE J. Food Prot., Vol. 63, No. 8

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

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had been reported previously in laboratory media (39).
pH ⫽ pKa ⫹ log[A⫺]/[HA]
L. monocytogenes has also demonstrated an acid-adap-
which becomes the Henderson–Hasselbach equation with tive response to acidic conditions (29, 30, 59). In addition,
pH substituted for ⫺log[H⫹]. L. monocytogenes when exposed to mildly acidic condi-
tions results in cells capable of surviving severe acid stress
PH LIMITS OF PATHOGEN GROWTH
of pH 3.5 (59). Gahan et al. (30) showed that acid-adapted
The minimum pH values for allowing the initiation of cells are capable of surviving during milk fermentation and
growth of some common foodborne pathogens in labora- persisting in cheddar cheese for 70 days. Data by
tory media are found in Table 1. These lower limits were O’Driscoll et al. (59) suggest that low pH conditions may
determined in laboratory media using strong acids to adjust select for mutant strains of L. monocytogenes that are more
the pH. The lowest reported pH allowing growth is 4.0. virulent. Gahan et al. (30) used adapted L. monocytogenes
The pathogens that will grow at this pH are Salmonella to inoculate pH 3.0 salad dressing. They found that when
Typhi (40), E. coli O157:H7 (34), Yersinia enterocolitica inoculated at about 100/g, the adapted cells showed a max-
(6), Pleisiomonas shigelloides (42), S. aureus (40), and imum survival time of 90 min as compared to 15 min for
Aeromonas hydrophila (71). These lower limits for initia- unadapted cells.
tion of growth were determined under ideal laboratory con- All of these studies emphasize the need to assess the
ditions using laboratory media and inorganic acid. It would survival of these organisms using acid-adapted cultures in
be expected that the limits in food would be the same or order to determine the worst-case scenario. Cultures used
higher due to the interacting effects associated with the in inoculation studies with mayonnaise, dressings, and
food such as salt, sugar, inhibitory flavoring (garlic, onion), sauces presented in this paper were from the stationary
preservatives, and type of acid (40). stage of growth (Table 4).
As an added dimension to pathogen survival in acidic
EFFECT OF ORGANIC ACID ON FOODBORNE
environments, numerous researchers have reported on the
PATHOGENS
adaptive acid tolerance of Salmonella (21, 35, 46), E. coli
O157:H7 (3, 9–11, 16, 31, 47, 65, 76), E. coli (35), L. Organic acids are generally not only effective as acid-
monocytogenes (29, 30, 59), and Shigella (35). Their sur- ulents in preventing or inhibiting the growth of foodborne
vival in acidic foods and in the strong acidic environment pathogens but are inimical to bacterial pathogens, espe-
of the stomach (pH 1.5 to 3.0) are of paramount importance cially at or below their pKa (66). Antimicrobial activity is
in reducing the levels of these organisms and thus their related to the degree of undissociation (2, 9, 40). Some
infectivity (11). E. coli O157:H7 is the most acid tolerant reported inhibitory and lethal pH values for acetic acid on
of foodborne pathogens and perhaps has the lowest infec- foodborne pathogens are found in Table 2. These data
tive dose. Acid and stress tolerance in E. coli O157:H7 is clearly show that the pH where inhibition occurs is higher
controlled by the rpoS-regulated proteins that are produced than that for the minimum pH for initiation of growth
at the entrance into the stationary phase of growth (3, 16). presented in Table 1.
Buchanan and Edelson (10) have demonstrated that E. coli Organic acids have been shown to be toxic or inhibi-
O157:H7 grown in media with glucose produced catabolic tory or both to E. coli O157:H7 (1, 53, 65), L. monocyto-
acids that enhance the survival of E. coli O157:H7 when genes (13–15, 41, 70, 78), Salmonella (17, 21, 35, 45, 46,
harvested cells were introduced into brain–heart infusion 68, 78), S. aureus (68, 80), Y. enterocolitca (6–8), Bacillus
broth adjusted to pH 2.5 and 3.0. Similarly, Leyer et al. cereus (45), A. hydrophila (60), and C. botulinium (54, 74).
(47) found that E. coli O157:H7 grown in broth at pH 5.0 The growth of E. coli O157:H7, Salmonella Enteritidis,
for one or two cell generations resulted in acid-adapted Salmonella Typhimurium, Vibrio parahaemolyticus, A. hy-
cells that demonstrated enhanced resistance to lactic acid drophila, S. aureus, and B. cereus was inhibited by a 0.1%
and survival in dry salami. In a recent study, acid-adapted (wt/vol) concentration of acetic acid in vinegar, and the in-
E. coli O157:H7 was found to be more tolerant than un- hibition was increased in the presence of salt and glucose
adapted cells when exposed to reduced pH as a result of (25). Buchanan and Edelson (11) have reported on the rel-
organic acids (65). Significantly higher levels of adapted E. ative rates of E. coli O157:H7 inactivation in the presence
J. Food Prot., Vol. 63, No. 8 MICROBIOLOGICAL SAFETY OF DRESSINGS 1147

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

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7)c 4.18 3.5 0.3 0.39 1.7 2.67 1.3 1.64
Reduced-calorie may-
onnaise (6 to 7)c 4.1 3.4 0.36 0.83 0.52 1.74 1.5 2.61
Fat-free mayonnaise
(4 to 5)c 4.1 3.1 0.28 0.6 0.43 0.8 1.85 2.3
Salad dressing (5 to 7)c 3.9 3.04 0.72 1.17 1.55 2.45 1.5 2.37
Light salad dressing,
reduced calorie (2 to
3)c 4.1 3.2 0.38 0.75 0.67 1.3 1.84 2
Fat-free salad dressing
(1 to 3)c 3 2.77 0.84 1 1.04 1.55 1.78 2
Sauces (40 to 50)c 4.2 2.86 0.46 3.2 1.33 3.8 0.88 5.68
a Maximum value (highest pH, highest total titratable acidity as acetic).
b Target value.
c Number of participants summarized for each column where data were available.

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

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as meat, seafood, and vegetables as soon as possible in and consequently producing potentially hazardous product
salad preparation (68). However, this must not be a replace- (27). Membre et al. (53) in a model development study of
ment for good sanitary practices and adequate cooling. the effects of temperature, pH, glucose, and citric acid in a
Good sanitation practices will greatly minimize the possi- reduced-calorie mayonnaise on Salmonella Typhimurium
bility of cross-contaminating all foods with foodborne path- found that all formulations and conditions showed the de-
ogens. Abdul-Raouf et al. (1) found that E. coli O157:H7 struction of this organism. The experimental parameters
can grow at pH values normally found in beef salads using were temperature (15 to 35⬚C), pH (4.5 to 6.5), glucose (1
mayonnaise, further emphasizing the need for handling pre- to 4%), and citric acid (0.05 to 0.1%) (53). Under optimum
pared salads with caution. conditions for the destruction of Salmonella at low pH and
Because these data represent varied levels of inocula, high temperature and to a lesser extent at high concentra-
storage temperatures, pH values, titratable acidities, and tions of citric acid and glucose, Salmonella Typhimurium
products, it is difficult to assess the effects of these on the can take 3 weeks to inactivate, thus allowing for a potential
survivability of foodborne pathogens. To aid in interpreting health risk (53). However, in the United States, commercial
these data, the decimal reduction times (DRT) were statis- mayonnaise, dressings, and sauces are manufactured with
tically determined by linear regression from published ta- acetic acid as the primary acidulant that rapidly kills Sal-
bles or figures from numerous studies (6, 26, 28, 30, 33, monella and Y. enterocolitica (6, 26, 33, 48, 50, 51, 56, 57,
36, 50, 57, 61, 64, 68, 75, 77, 81). The statistics of the 61, 68, 75). Therefore, it is unlikely that a safety hazard
adapted data are summarized in Table 4. The DRT values would result even using highly contaminated eggs. This is
generated from these studies were used in the analysis of providing that the predominant acid is acetic, the pH is at
variance for Salmonella, L. monocytogenes, and E. coli least 4.75, and the titratable acidity is at least 0.40% as
O157:H7 (Tables 5 to 8). Each organism in Table 4 is cat- acetic acid of the water phase.
egorized by product, storage temperature, pH, DRT hours The analysis of variance of DRT (h) of studies with L.
and titratable acidity in the water phase. From these data, monocytogenes shows (Table 6) that within the narrow
it is obvious that all organisms die off, some more rapidly bounds of pH 3.3 to 4.3 there is no statistically significant
(Salmonella and Y. entercolitica) than others (E. coli O157: effect of pH on DRT at P ⬍ 0.05 (26, 30, 33). However,
H7 and L. monocytogenes). At refrigeration temperatures of there appears to be some relationship of DRT to pH (P ⫽
5 to 7⬚C, it can take as long as 448.8 h to kill 1 log of E. 0.076). There appeared to be little relationship of DRT to
coli O157:H7. On the other hand, it takes only 25.5 to 61 titratable acidity (P ⫽ 0.415).
h to kill 1 log cycle of L. monocytogenes, Salmonella, or L. monocytogenes has been isolated from high moisture
Y. entercolitica at 5 to 26.6⬚C. Some of the longer survival unripened cheeses and has resulted in illness and death
times of Salmonella and L. monocytogenes are reported on from the consumption of contaminated cheese (52). In ad-
experimental mayonnaises of as little as 0.1% titratable dition, L. monocytogenes has been isolated and shown to
acidity (acetic acid) of the water phase, which is well below grow on raw salad vegetables but not on raw whole or
the lowest U.S.-produced dressing target value of 0.43% chopped tomatoes (5). Erickson and Jenkins (27) studied
(Table 3) (33). Furthermore, it is normal to have storage or the psychrotrophic growth of L. monocytogenes in com-
shipping time of at least 72 h before presentation to con- mercially pasteurized eggs and found that they grew about
sumers, thus, allowing for dieoff of the more acid-sensitive 3 logs in 12 days at 12.8⬚C in liquid whole eggs and 5%
pathogens. It is a requirement of 21 CFR 101.100 to hold salted eggs. Although these are abusive conditions and the
acidic dressings 72 h when using unpasteurized eggs (68). eggs would probably have unacceptable sensory properties
However, commercial manufacturers use pasteurized eggs and not be used, the potential does exist that highly con-
to further ensure product safety. Analysis of variance of the taminated eggs could be used to produce mayonnaise and
Salmonella DRTs from studies where product was stored at dressings (27, 69). L. monocytogenes was shown to remain
23.9 to 26.6⬚C, which is close to the normal storage tem- viable for the entire shelf life of raw chopped tomatoes (5).
perature for these products, is found in Table 5 (26, 33, 50, Therefore, the potential exists that cheeses, vegetables, and/
57, 61, 68). This analysis shows that pH is highly signifi- or eggs added to dressings as flavorings and emulsifiers
cant and titratable acidity is not significant at the 0.05% could be contaminated with L. monocytogenes. Even at re-
J. Food Prot., Vol. 63, No. 8

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

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1150 SMITTLE J. Food Prot., Vol. 63, No. 8

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

pH 4 2,974.27 743.57 93.23 ⬍0.001 pH 4 1,895 474 4.12 0.076


Error 5 39.88 7.98 Error 5 575 115
TA 7 2,802 400 3.76 0.226 TA 7 2,119 303 1.72 0.415
Error 2 213 106 Error 2 351 176
Total 9 3,014 Total 9 2,470

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frigeration temperatures and with adapted cells they would es, buttermilk, yogurt, sour cream, and other dairy ingre-
probably die off and not present a health hazard in well- dients (22, 24). In a simulation of postprocessing contam-
formulated products (30). This is providing the pH is 3.0 ination by E. coli O157:H7, Dineen et al. (22) found that
with the predominant acid being acetic. For those products at 1,000 CFU/ml this organism could be recovered for up
with milder pHs, that contain cheese or other dairy ingre- to 12 days in yogurt (pH 4.0), 28 days in sour cream (pH
dients or both, and that rely on refrigeration, there might 4.3), and at ⬎100 CFU/ml at 35 days in buttermilk. In
be a problem with the survival of this organism. Research addition, exposure to lactic acid, the principal acid in fer-
studies in the literature are lacking in this area. Until an- mented dairy products, has been found to induce acid tol-
swers are provided, it would be prudent for manufacturers erance in E. coli O157:H7 (31), thus improving their sur-
to screen critical ingredients or use suppliers with hazard vival characteristics for subsequent addition to dressings. E.
analysis and critical control point (HACCP) plans that ad- coli O157:H7 is remarkably acid tolerant and has been
dress the presence of L. monocytogenes and its control or shown to remain viable for extended periods of time in
both. mayonnaise and dressings (Tables 4 and 5). The organism
E. coli O157:H7 is a pathogen associated with under- gradually dies off in all of these products (DRT 448.8 h or
cooked ground beef meat (24). However, raw milk, unpas- 18.7 days) but can remain viable at refrigerated tempera-
teurized apple cider, water, and food service-contaminated tures for 93 days in real mayonnaise (36). Under normal
mayonnaise have been implicated in illness from E. coli mayonnaise and reduced-calorie mayonnaise manufacturing
O157:H7 (4, 24, 77). Dairy cattle have been shown to har- conditions and storage, E. coli O157:H7 will not survive
bor the organism and dairy cattle have been implicated as (36). Death is most rapid at 20 to 30⬚C, which is the normal
the source of beef for at least one outbreak (24). The key temperature at which these products are stored and distrib-
to controlling E coli O157:H7 successfully in dairy plants uted (36). Furthermore, commercial mayonnaise and re-
is proper pasteurization and good sanitation to prevent cross duced-calorie mayonnaise produced under good manufac-
contamination after pasteurization (22, 24). Because dairy turing practices does not represent a health risk from E. coli
products are an essential ingredient of some dressings, the O157:H7 (36). Erickson et al. (28) in a survey of mayon-
potential exists that this organism could be present in chees- naise and dressing manufacturer’s facilities and pasteurized
eggs for E. coli O157:H7 did not recover this organism in
114 environmental swabs representing 3 manufacturing fa-
cilities and in 188 lots of liquid pasteurized eggs, thus em-
phasizing the almost negligible contamination risk. The ex-
tremes of the typical manufactured dressings in the United
States are pH 4.4 to 2.6 and titratable acidity as acetic in
the water phase of 0.43 to 5.25% (Table 3). Tables 7 and
8 present the analysis of variance of DRT for E. coli O157:

TABLE 7. Analysis of variance of decimal reduction times (h) of


E. coli O157:H7 in real mayonnaise and reduced-calorie may-
onnaise at 5 to 7⬚C, pH 3.6 to 4.08, and titratable acidity in the
water phase 0.8 to 2.1% (36, 77, 81)
Source df SS MS F value P

pH 6 75,409 12,568 23.50 0.004


FIGURE 1. Relationship between pH and log DRT in minutes of
Error 4 2,139 535
Salmonella Enteritidis and various Salmonella spp. inoculated
TA 5 73,708 14,742 19.19 0.003
into real mayonnaise, reduced-calorie, garlic, lemon, and dairy
Error 5 3,840 768
substitute commercial mayonnaises produced in the United King-
Total 10 77,548
dom and the United States (26, 33, 50, 51).
J. Food Prot., Vol. 63, No. 8 MICROBIOLOGICAL SAFETY OF DRESSINGS 1151

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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