635

Journal of Food Protection, Vol. 77, No. 4, 2014, Pages 635–639

doi:10.4315/0362-028X.JFP-13-408
Copyright G, International Association for Food Protection

Research Note

Survival of Salmonella during Baking of Peanut Butter Cookies

AMANDA A. LATHROP,* TIFFANY TAYLOR, AND JAMES SCHNEPF

Food Science and Nutrition Department, California Polytechnic State University, San Luis Obispo, California 93407, USA

MS 13-408: Received 27 September 2013/Accepted 18 November 2013

ABSTRACT
Peanuts and peanut-based products have been the source of recent Salmonella outbreaks worldwide. Because peanut butter
is commonly used as an ingredient in baked goods, such as cookies, the potential risk of Salmonella remaining in these products
after baking needs to be assessed. This research examines the potential hazard of Salmonella in peanut butter cookies when it is
introduced via the peanut-derived ingredient. The survival of Salmonella during the baking of peanut butter cookies was
determined. Commercial, creamy-style peanut butter was artificially inoculated with a five-strain Salmonella cocktail at a target
concentration of 108 CFU/g. The inoculated peanut butter was then used to prepare peanut butter cookie dough following a
standard recipe. Cookies were baked at 350uF (177uC) and were sampled after 10, 11, 12, 13, 14, and 15 min. Temperature
profiles of the oven and cookies were monitored during baking. The water activity and pH of the inoculated and uninoculated
peanut butter, raw dough, and baked cookies were measured. Immediately after baking, cookies were cooled, and the survival of
Salmonella was determined by direct plating or enrichment. After baking cookies for 10 min, the minimum reduction of
Salmonella observed was 4.8 log. In cookies baked for 13 and 14 min, Salmonella was only detectable by enrichment reflecting a
Salmonella reduction in the range of 5.2 to 6.2 log. Cookies baked for 15 min had no detectable Salmonella. Results of this study
showed that proper baking will reduce Salmonella in peanut butter cookies by 5 log or more.

Peanuts and peanut-based products have been the Researchers have investigated the survival and thermal
source of Salmonella outbreaks worldwide (14, 15). The tolerance of Salmonella in peanut butter (4, 13, 16, 18, 21).
most recent peanut butter outbreak in the United States Burnett et al. (4) showed that Salmonella can survive for up
occurred in 2012 and resulted in 42 illnesses (7). Reported to 24 weeks in a variety of peanut butters and spreads. Two
illnesses involving two previous outbreaks in 2008 to 2009 thermal inactivation studies using different strains showed
and 2006 to 2007 reached 529 and 628, respectively (5, 6). that to achieve a 7-log reduction of Salmonella in peanut
Not only did these outbreaks produce a staggering number butter a process of 90uC for 60 to 120 min would be needed
of illnesses, but the number of recalled products was also (16, 21). The lengthy persistence and high heat resistance of
massive. Products implicated in the 2012 and the 2008 to Salmonella in peanut butter raises concerns about its use as
2009 outbreaks supplied peanut butter as an ingredient to an ingredient, even in products that are cooked prior to sale.
numerous manufacturers, resulting not only in the recall of The presence of Salmonella in bakery products has
the contaminated peanut butter but also in the recall of been a concern for years. Outbreaks have been associated
peanut butter–containing cakes, pies, sauces, ice creams, with custards, trifles, apple pie, cakes, bread, and cake
and snack bars. These outbreaks illustrated the potential mixes (2, 3, 11, 26). Although bakery ingredients such as
enormity of an ingredient-driven outbreak. To protect flour, chocolate, peanut butter, and dairy can all be potential
consumers, the U.S. Food and Drug Administration has sources of Salmonella, the majority of outbreaks involving
issued industry guidance addressing Salmonella risk in baked goods were either associated or suspected to be
foods that contain a peanut-derived product as an ingredient associated with raw eggs and, in most cases, were the result
(23). The guidance document states that in the absence of of cross-contamination or undercooking. To address these
obtaining peanut-derived products from suppliers who have concerns, both the American Bakers Association and NSF
validated processes for Salmonella, the U.S. Food and Drug International established guidance documents for pathogen
Administration recommends manufacturers ensure that their challenge studies in baked goods (1, 17). However, neither
own manufacturing processes adequately reduce Salmonella of these guidance documents considers the potential of
by 5 log. The food industry has also issued guidance microbial contamination occurring via a low-moisture
ingredient or the effect of the baking process on the
documents that address the control of Salmonella in low-
contaminating microorganism.
moisture products (8, 9, 20).
The fate of Salmonella in bakery products when it is
introduced via a low-moisture ingredient has not been
* Author for correspondence. Tel: 805-756-6269; Fax: 805-756-1146; thoroughly examined. It has been assumed that baking will
E-mail: [email protected]. eliminate vegetative pathogens due to the temperatures that
636 LATHROP ET AL. J. Food Prot., Vol. 77, No. 4

products typically reach during cooking (22). Previous TABLE 1. Ingredients and quantity used in the production of
research indicated that low numbers of Salmonella (10 peanut butter cookies
CFU/g) are destroyed by the baking process in pumpkin pie Ingredient Quantity
and cheesecake (12, 25). In other bakery products, this is
likely the case; however, low-moisture ingredients that are Flour 300 g
also high in fat, such as peanut butter, may not be as easily Butter 226 g
incorporated into the mix and could create a low–water Sugar 200 g
Peanut butter 180 g
activity (aw) microenvironment. Moreover, if the peanut
Brown sugar 180 g
butter is contaminated with Salmonella, cells may remain in Eggs 2 large
this high-fat, low-aw microenvironment, which could result Vanilla extract 10 ml
in increased heat resistance. Salt 2.5 g
Because of recent Salmonella outbreaks involving Baking soda 2.1 g
peanut butter, the risk of using contaminated peanut butter Baking powder 1.9 g
needs to be assessed in baked goods. This research
examines the potential hazard of Salmonella in peanut
dough last and blended for 5 min. To ensure all samples started at
butter cookies when it is introduced via the peanut-derived the same temperature, dough was weighed into 28-g portions and
ingredient. The objective was to determine the survival of held at 68uF (20uC) prior to baking.
Salmonella during the baking process.
Baking of peanut butter cookies. Samples of dough were
MATERIALS AND METHODS placed on a cookie sheet (11 by 17 in.) in one of three locations, the
Salmonella strains. Five serovars of Salmonella enterica center, the corner, or the side, and baked in an oven (OV702G,
were used in the study: Salmonella Tennessee (FSL-R8-5221, Fischer Scientific, Dubuque, IA) set to 350uF (177uC) for 10, 11,
peanut), Salmonella Tornow (FSL-R8-5222, peanut), Salmonella 12, 13, 14, or 15 min. Immediately after baking, cookies were
Hartford (FSL-R8-5223, peanut), Salmonella Agona (FSL-S5-517, placed into a Whirl-Pak bag and cooled in an ice bath. The
human), and Salmonella Typhimurium DT-104 (FSL-WI-030, temperature of the oven was recorded at the beginning and every
human) were obtained from the International Life Sciences 1 min during baking using a data logger (DI-1000-TC, DATAQ
Institute, North America (Cornell University, Ithaca, NY). All Instruments Inc., Akron, OH) with a type T thermocouple (Omega
cultures were maintained on tryptic soy agar (Oxoid, Hampshire, Scientific, Stamford, CT).
UK) containing 0.6% (wt/vol) yeast extract (Remel, Lenexa, KS) Three replicate trials of cookie temperature data were
at 4uC. Cultures were prepared by transferring a loopfull of each collected independent of the inoculated cookie trials. Cookie
organism into 10 ml of tryptic soy broth (BD, Sparks, MD) and temperature was monitored by placing a thermocouple (type K,
incubating at 35uC for 24 h. This was done for three consecutive Omega Scientific) near the center of the cookie at each location on
24-h intervals prior to being used as an inoculum. After incubation, the sheet. During baking, the initial temperature and every 1 min
equal volumes of each strain were pooled to form a cocktail. The thereafter were recorded using a data logger (DI-1000-TC). Oven
cocktail was centrifuged (1,800 g | 15 min), washed twice with temperatures were also recorded, as previously described.
0.1% peptone water, and then suspended in 0.1% peptone water to
achieve the targeted population. Microbiological analysis. After cooling, baked cookies (25 g)
were diluted with 225 ml of 0.85% saline solution containing 0.1%
Inoculation of peanut butter. A commercial, creamy-style Tween 80 and blended in a stomacher for 2 min. The samples were
peanut butter purchased from a local retailer was used for the serially diluted (1:10) in 0.1% peptone water and plated in
study. Peanut butter was inoculated as described by Ma et al. (16). duplicate onto tryptic soy agar yeast extract supplemented with
Briefly, 240 g of peanut butter was aseptically weighed into a ferric ammonium citrate (0.05%) and sodium thiosulfate (0.03%).
Whirl-Pak bag (Nasco, Fort Atkinson, WI). The peanut butter was The plates were incubated at 35uC for 48 h, and Salmonella
then melted by heating to 50uC in a circulating water bath and then colonies (identified by a black precipitate in the center) were
cooled to 37uC prior to inoculation. After cooling, 2.4 ml of the counted. In anticipation of counts below the limit of detection by
Salmonella cocktail at a concentration 1010 CFU/ml was added and direct plating, sample homogenates were incubated at 35uC
mixed by hand for 5 min to evenly distribute the bacterial cells and overnight prior to streaking on xylose lysine deoxycholate agar
achieve a final population of approximately 108 CFU/g of peanut (Neogen, Lansing, MI) to determine the presence or absence of
butter. Salmonella. Samples negative by direct plating and positive by
enrichment should contain between .1 and ,10 CFU/g
Preparation of peanut butter cookie dough. All ingredients Salmonella, and for log-reduction calculations of these samples,
(Table 1) were purchased from a local retailer and kept at a range was calculated (16).
refrigeration or ambient temperature as appropriate until used.
Prior to cookie dough preparation, butter was softened at room aw and pH analysis. The aw and pH of the peanut butter
temperature (approximately 30 min). The cookie dough was before and after inoculation, the cookie dough, and the baked
prepared by creaming softened butter in a mixer (model Classic cookies were determined with a aw meter (Aqualab 4TE, Decagon
Plus, KitchenAid, St. Joseph, MI) for 2 min. Sugar and brown Devices, Pullman, WA) and a pH meter (PC510; Oakton
sugar were added and then mixed on medium speed for 5 min. Two Instruments, Vernon Hills, IL), respectively.
eggs were individually added and were mixed well after each
addition. Flour, vanilla extract, salt, baking soda, and baking Statistical analysis. For each experiment three independent
powder were then added, one at a time, with continuous mixing, trials were conducted. Average data from inoculated peanut butter,
until well blended. Inoculated peanut butter was added to the raw cookie dough, and baked cookies were averaged and converted
J. Food Prot., Vol. 77, No. 4 SALMONELLA IN PEANUT BUTTER COOKIES 637

TABLE 2. pH and aw of uninoculated and inoculated peanut

butter and raw cookie dough
Sample pH aw

Uninoculated peanut
butter 6.07 ¡ 0.04 0.3930 ¡ 0.0018
Inoculated peanut butter 6.52 ¡ 0.08 0.4735 ¡ 0.0253
Uninoculated raw cookie
dough 6.73 ¡ 0.08 0.8274 ¡ 0.0044
Inoculated raw cookie
dough 6.85 ¡ 0.05 0.8223 ¡ 0.0071

to log values. Total positive enrichments by location and FIGURE 1. Temperature profiles during the baking of peanut
temperature data were compared using analysis of variance butter cookies placed at three different locations on a baking sheet.
(JMP, SAS Institute, Cary, NC) to determine significant differ-
ences at a 95% confidence interval (P , 0.05).

RESULTS AND DISCUSSION 4.4uF cooler than the average. The differences in cookie
location temperature correlate to the total number of positive
Peanut butter aw and pH values increased after enrichments at each location; the center, side, and corner
inoculation (Table 2). The pH of the cookie dough made locations had 10, 11, and 13 total positive samples,
with inoculated peanut butter was also higher than dough respectively (Table 3).
made with uninoculated peanut butter; however, the aw was The average initial Salmonella load in the inoculated
lower in cookie dough made with inoculated peanut butter. peanut butter was 8.22 log CFU/g and when this was used to
As expected, the aw of the cookies decreased over time make cookie dough, the Salmonella concentration in the
during baking from approximately 0.82 to 0.70, 0.62, 0.60, dough averaged 6.21 log CFU/g. Salmonella survived
0.53, 0.54, and 0.51 after 10, 11, 12, 13, 14, and 15 min, during the baking of peanut butter cookies when the bake
respectively. Immediately after baking, cookies were placed times were 14 min or less (Table 3). Cookies baked for 10,
into a Whirl-Pak bag and cooled in an ice bath instead of 11, or 12 min appeared underbaked, while cookies baked for
being cooled on an open rack, so this value is higher than 14 or 15 min appeared done. The 13-min bake time
typical literature values for cookies (0.40 to 0.30). Because produced cookies that could potentially be perceived as
of this, the reported values more closely reflect the aw in the underbaked or done, depending on individual preference.
oven during the time intervals tested. The 10-min bake time produced two samples with
The temperature profiles of the cookies during baking detectable populations of Salmonella by direct plating, and
are illustrated in Figure 1. Consistently monitoring cookie in the cookie with the highest count, a 4.8-log reduction was
temperature was challenging. As the cookies baked, the achieved. Less than 50% of the cookies were enrichment
thermocouples often slipped out, and it was not possible to positive for Salmonella after 13 and 14 min of baking,
determine or keep the thermocouple in the cookie’s cold resulting in a minimum observed log reduction in the range
spot. Because of this, temperature profiles were measured of 5.2 to 6.2. Salmonella was undetectable in cookies baked
independent of inoculated cookie trials, and results are an for 15 min.
estimate of the typical temperature profiles achieved during
baking. For all baking tests, the oven temperature reached
350 ¡ 2uF (177 ¡ 1uC) prior to placing cookies in the TABLE 3. Survival of Salmonella in peanut butter cookies baked
oven. Opening the oven door caused the oven temperature at 350uF when prepared with contaminated peanut butter a
to decrease nearly 50uF (28uC), and by the end of the 15 min Salmonella-positive enrichments/no. of samples tested
baking period, the average oven temperature was 347uF
(175uC). The temperature of the cookies increased from an Time (min) Center Side Corner Total (% positive)
initial average value of 69uF to a final average value of
10 3/3b 3/3c 3/3 9/9 (100)
197uF (92uC), 198uF (92uC), 217uF (103uC), 207uF (97), 11 3/3 3/3 3/3 9/9 (100)
228uF (109uC), and 229uF (109uC) after baking for 10, 11, 12 3/3 3/3c 3/3 9/9 (100)
12, 13, 14, and 15 min, respectively. Depending on the 13 1/3 1/3 2/3 4/9 (44)
location of the cookie on the cookie sheet, cookies reached a 14 0/3 1/3 2/3 3/9 (33)
temperature of 160uF (71uC) after baking between 7 to 15 0/3 0/3 0/3 0/9 (0)
8 min. The temperature of the cookie was significantly a
Peanut butter was inoculated with the bacterium at an average
different (P , 0.05), depending on the location when concentration of 8.22 log CFU/g; the average initial Salmonella
controlling for the time of baking, with the center cookie load in the cookie dough was 6.21 log CFU/g.
being 5.3uF warmer than the average, the side cookie being b
One sample had an estimated plate count of 1.4 log CFU/g.
c
0.9uF cooler than the average, and the corner cookie being One sample had an estimated plate count of 0.7 log CFU/g.
638 LATHROP ET AL. J. Food Prot., Vol. 77, No. 4

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